Wilson’s Disease—Crossroads of Genetics, Inflammation and Immunity/Autoimmunity: Clinical and Molecular Issues
Abstract
:1. Introduction
2. Wilson’s Disease—Clinical Presentations
2.1. Liver Disease
2.2. Central Nervous System (CNS) Disease
2.3. Other Symptoms
3. Mechanisms of Tissue Damage in WD
3.1. Oxidative Stress, Cuproptosis and Ferroptosis
- The effectiveness of antioxidant mechanisms is greatly reduced due to copper overload;
- Treatment that reduces the burden of copper improves the antioxidant status of patients but does not resolve it;
- The effectiveness of antioxidant protection increases after treatment;
3.2. Inflammation
3.2.1. Copper-Associated Inflammation and Liver Pathology in WD
3.2.2. Copper-Associated Inflammation and CNS Pathology in WD
3.3. Pro- and Anti-Inflammatory Cytokine Gene Polymorphisms and the Phenotype of WD
4. Cuproptosis, Ferroptosis, and Impaired Immune Reactivity in WD
5. WD—Autoimmunity
5.1. Autoimmune Events and Autoantibodies during Anti-Copper Treatment
- Boudin G, Pépin B, Godeau P, Vernant JC, Gouerou H. Lupus érythémateux induit par la pénicillamine au cours d’une maladie de Wilson [Lupus erythematosus due to penicillamine associated with Wilson’s disease]. Ann Med Interne (Paris). 1971 Feb;122(2):269-73. French. [171]
- Kalina P, Procházková L, Hauftová D. Syndróm podobný systémovému lupus erythematosus vyvolaný penicilamínom u pacienta s Wilsonovou chorobou [A syndrome similar to systemic lupus erythematosus caused by penicillamine in patients with Wilson’s disease]. Bratisl Lek Listy. 1985 Sep;84(3):336-40. Slovak. [172]
- López-Guerra N, Alvarez Lario B, García-Moncó C, Peña Sagredo JL. Lupus eritematoso sistémico inducido por d-penicilamina en enfermedad de Wilson: a propósito de un caso [Systemic lupus erythematosus induced by d-penicillamine in Wilson’s disease: apropos of a case]. Med Clin (Barc). 1987 Apr 4;88(13):552-4. Spanish. [173]
- Jan V, Callens A, Machet L, Machet MC, Lorette G, Vaillant L. Pemphigus, polymyosite et myasthénie induits par la D-pénicillamine [D-penicillamine-induced pemphigus, polymyositis and myasthenia]. Ann Dermatol Venereol. 1999 Feb;126(2):153-6. French. [174]
5.2. Autoimmune Autoantibodies Not Related to Treatment of WD
5.3. WD and Autoimmune Diseases
Age, Sex | Clinical Characteristics | Reference |
---|---|---|
15 years old, F | Acute hepatitis, Wilson disease diagnosed, no satisfying response to anti-copper drugs; ANAs 1:40, ASMAs 1:40, IgG 15.4 g/L, glucosteroids added to treatment regimen with good response | [230] |
24 years old, F | Chronic hepatitis, ASMAs 1:60, ANAs 1:40, IgG 24.6 g/L. Liver biopsy: cirrhosis with moderate, periseptal inflammatory activity (interface hepatitis). Deposits of copper in the periseptal regions. Deteriorated on steroids within 3 years, treated with liver transplantation, copper content in explanted liver 965 mg/g | [215] |
22 years old, F | Acute liver failure, ANAs 1:400, ASMA-positive, ceruloplasmin 11.2 mg/L, urine copper excretion 187.5 µg/21 (normal range 10–60 µg/24 h), Kayer–Fleischer ring present.; the patient died | [222] |
30 years old, F | Chronic hepatitis, IgG elevated, ANA-positive, liver biopsy piecemeal necrosis, interface hepatitis, AIH diagnosed, on steroids 3 years with improvement, thereafter neurological symptoms appeared. The serum ceruloplasmin was decreased normal 24 h urinary copper excretion. Kayser–Fleischer present. ATP7B mutation confirmed. Head MRI showed the hyperintensity in bilateral basal ganglia. DPA was introduced with improvement. | [231] |
10 years old, M | Acute hepatitis, ANAs 1:160, AMAs 1:160, ASMAs 1:80, Anti-LKM1 1:20, Kayser–Fleischer ring present, liver biopsy interface hepatitis, copper in dry liver tissue, 20 times the upper limit, steroids and DPA introduced, full recovery | [197] |
15 years old, F | Acute hepatitis, ANA-, ASMA-, and AMA-positive, IgG 2870mg/dL, ATP7B c.2532delA and c.3061-1 G->A, Serum ceruloplasmin: 13.7 mg/dL, Liver copper content: 388 mg Cu/g dry tissue. Failed on steroids and DPA, finally treated with liver transplantation | [232] |
5.4. Possible Patomechanisms of Autoimmunity in WD
Can Autoimmune Processes in WD Be Directly Caused by Copper?
5.5. Steroids in WD Treatment
6. Limitations, Summary, Conclusions and Future Perspectives
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Walshe, J.M. History of Wilson’s disease: 1912 to 2000. Mov. Disord. 2006, 21, 142–147. [Google Scholar] [CrossRef]
- Wu, F.; Wang, J.; Pu, C.; Qiao, L.; Jiang, C. Wilson’s disease: A comprehensive review of the molecular mechanisms. Int. J. Mol. Sci. 2015, 16, 6419–6431. [Google Scholar] [CrossRef] [PubMed]
- Roberts, E.A.; Schilsky, M.L. Current and Emerging Issues in Wilson’s Disease. N. Engl. J. Med. 2023, 389, 922–938. [Google Scholar] [CrossRef] [PubMed]
- Ovchinnikova, E.V.; Garbuz, M.M.; Ovchinnikova, A.A.; Kumeiko, V.V. Epidemiology of Wilson’s Disease and Pathogenic Variants of the ATP7B Gene Leading to Diversified Protein Disfunctions. Int. J. Mol. Sci. 2024, 25, 2402. [Google Scholar] [CrossRef] [PubMed]
- Abuduxikuer, K.; Li, L.T.; Qiu, Y.L.; Wang, N.L.; Wang, J.S. Wilson disease with hepatic presentation in an eight-month-old boy. World J. Gastroenterol. 2015, 21, 8981–8984. [Google Scholar] [CrossRef]
- Ferenci, P.; Członkowska, A.; Merle, U.; Ferenc, S.; Gromadzka, G.; Yurdaydin, C.; Vogel, W.; Bruha, R.; Schmidt, H.T.; Stremmel, W. Late-onset Wilson’s disease. Gastroenterology 2007, 132, 1294–1298. [Google Scholar] [CrossRef]
- Członkowska, A.; Rodo, M.; Gromadzka, G. Late onset Wilson’s disease: Therapeutic implications. Mov. Disord. 2008, 23, 896–898. [Google Scholar] [CrossRef]
- Członkowska, A.; Milewski, B. Immunological observations on patients with Wilson’s disease. J. Neurol. Sci. 1976, 29, 411–421. [Google Scholar] [CrossRef]
- Boga, S.; Ala, A.; Schilsky, M.L. Hepatic features of Wilson disease. Handb. Clin. Neurol. 2017, 142, 91–99. [Google Scholar]
- Członkowska, A.; Gromadzka, G.; Büttner, J.; Chabik, G. Clinical features of hemolysis, elevated liver enzymes, and low platelet count syndrome in undiagnosed Wilson disease: Report of two cases. Arch. Gynecol. Obstet. 2010, 281, 129–134. [Google Scholar] [CrossRef]
- Zischka, H.; Einer, C. Mitochondrial copper homeostasis and its derailment in Wilson disease. Int. J. Biochem. Cell Biol. 2018, 102, 71–75. [Google Scholar] [CrossRef] [PubMed]
- Szeligowska, J.; Ilczuk, T.; Nehring, P.; Górnicka, B.; Litwin, T.; Członkowska, A.; Przybyłkowski, A. Liver injury in Wilson’s disease: An immunohistochemical study. Adv. Med. Sci. 2022, 67, 203–207. [Google Scholar] [CrossRef] [PubMed]
- Fanni, D.; Guido, M.; Gerosa, C.; Vallascas, V.; Moi, M.; Coni, P.; Vallebona, E.; Van Eyken, P.; Barcellona, D.; Scano, A.; et al. Liver changes in Wilson’s disease: The full spectrum. A report of 127 biopsies from 43 patients. Eur. Rev. Med. Pharmacol. Sci. 2021, 25, 4336–4344. [Google Scholar] [PubMed]
- Stromeyer, F.W.; Ishak, K.G. Histology of the liver in Wilson’s disease: A study of 34 cases. Am. J. Clin. Pathol. 1980, 73, 12–24. [Google Scholar] [CrossRef] [PubMed]
- Deguti, M.M.; Araujo, F.C.; Terrabuio, D.R.B.; Araujo, T.F.; Barbosa, E.R.; Porta, G.; Cançado, E.L.R. Wilson disease: The diagnostic challenge and treatment outcomes in a series of 262 cases. Arq. Neuropsiquiatr. 2024, 82, s00441786855. [Google Scholar] [CrossRef]
- Dusek, P.; Litwin, T.; Członkowska, A. Neurologic impairment in Wilson disease. Ann. Transl. Med. 2019, 7, S64. [Google Scholar] [CrossRef] [PubMed]
- Jopowicz, A.; Tarnacka, B. Neurological Wilson’s Disease Signs-Hepatic Encephalopathy or Copper Toxicosis? Diagnostics 2023, 13, 893. [Google Scholar] [CrossRef]
- Rędzia-Ogrodnik, B.; Członkowska, A.; Bembenek, J.; Antos, A.; Kurkowska-Jastrzębska, I.; Skowrońska, M.; Smoliński, Ł.; Litwin, T. Brain magnetic resonance imaging and severity of neurological disease in Wilson’s disease-the neuroradiological correlations. Neurol. Sci. 2022, 43, 4405–4412. [Google Scholar] [CrossRef] [PubMed]
- Bertrand, E.; Lewandowska, E.; Szpak, G.M.; Hoogenraad, T.; Blaauwgeers, H.G.; Członkowska, A.; Dymecki, J. Neuropathological analysis of pathological forms of astroglia in Wilson’s disease. Folia. Neuropathol. 2001, 39, 73–79. [Google Scholar]
- Wierzba-Bobrowicz, T.; Gwiazda, E.; Kosno-Kruszewska, E.; Lewandowska, E.; Lechowicz, W.; Bertrand, E.; Szpak, G.M.; Schmidt-Sidor, B. Morphological analysis of active microglia--rod and ramified microglia in human brains affected by some neurological diseases (SSPE, Alzheimer’s disease and Wilson’s disease). Folia. Neuropathol. 2002, 40, 125–131. [Google Scholar] [PubMed]
- Tsvetkov, P.; Coy, S.; Petrova, B.; Dreishpoon, M.; Verma, A.; Abdusamad, M.; Rossen, J.; Joesch-Cohen, L.; Humeidi, R.; Spangler, R.D.; et al. Copper induces cell death by targeting lipoylated TCA cycle proteins. Science 2022, 375, 1254–1261. [Google Scholar] [CrossRef] [PubMed]
- Gromadzka, G.; Wierzbicka, D.W.; Przybyłkowski, A.; Litwin, T. Effect of homeostatic iron regulator protein gene mutation on Wilson’s disease clinical manifestation: Original data and literature review. Int. J. Neurosci. 2022, 132, 894–900. [Google Scholar] [CrossRef] [PubMed]
- Gromadzka, G.; Wierzbicka, D.; Litwin, T.; Przybyłkowski, A. Iron metabolism is disturbed and anti-copper treatment improves but does not normalize iron metabolism in Wilson’s disease. Biometals 2021, 34, 407–414. [Google Scholar] [CrossRef] [PubMed]
- Gromadzka, G.; Wierzbicka, D.; Litwin, T.; Przybyłkowski, A. Difference in iron metabolism may partly explain sex-related variability in the manifestation of Wilson’s disease. J. Trace Elem. Med. Biol. 2020, 62, 126637. [Google Scholar] [CrossRef] [PubMed]
- Litwin, T.; Gromadzka, G.; Szpak, G.M.; Jabłonka-Salach, K.; Bulska, E.; Członkowska, A. Brain metal accumulation in Wilson’s disease. J. Neurol. Sci. 2013, 329, 55–58. [Google Scholar] [CrossRef] [PubMed]
- Koppenol, W.H.; Bounds, P.L. Redox-active metals: Iron and copper. In Principles of Free Radical Biomedicine; Pantopoulos, G., Schipper, H.M., Eds.; NOYA Science Publishers: Hauppauge, NY, USA, 2011; Volume 1, pp. 91–111. [Google Scholar]
- Kang, M.A.; So, E.Y.; Simons, A.L.; Spitz, D.R.; Ouchi, T. DNA damage induces reactive oxygen species generation through the H2AX-Nox1/Rac1 pathway. Cell Death Dis. 2012, 12, e249. [Google Scholar] [CrossRef] [PubMed]
- Kowalczyk, P.; Sulejczak, D.; Kleczkowska, P.; Bukowska-Ośko, I.; Kucia, M.; Popiel, M.; Wietrak, E.; Kramkowski, K.; Wrzosek, K.; Kaczyńska, K. Mitochondrial Oxidative Stress-A Causative Factor and Therapeutic Target in Many Diseases. Int. J. Mol. Sci. 2021, 22, 13384. [Google Scholar] [CrossRef] [PubMed]
- Zischka, H.; Lichtmannegger, J. Pathological mitochondrial copper overload in livers of Wilson’s disease patients and related animal models. Ann. N. Y. Acad. Sci. 2014, 1315, 6–15. [Google Scholar] [CrossRef] [PubMed]
- Zischka, H.; Lichtmannegger, J.; Schmitt, S.; Jägemann, N.; Schulz, S.; Wartini, D.; Jennen, L.; Rust, C.; Larochette, N.; Galluzzi, L.; et al. Liver mitochondrial membrane crosslinking and destruction in a rat model of Wilson disease. J. Clin. Investig. 2011, 121, 1508–1518. [Google Scholar] [CrossRef] [PubMed]
- Su, L.J.; Zhang, J.H.; Gomez, H.; Murugan, R.; Hong, X.; Xu, D.; Jiang, F.; Peng, Z.Y. Reactive Oxygen Species-Induced Lipid Peroxidation in Apoptosis, Autophagy, and Ferroptosis. Oxid. Med. Cell. Longev. 2019, 2019, 5080843. [Google Scholar] [CrossRef] [PubMed]
- Gromadzka, G.; Przybyłkowski, A.; Litwin, T.; Karpińska, A. Antioxidant Capacity Is Decreased in Wilson’s Disease and Correlates to Liver Function. Biol. Trace Elem. Res. 2023, 201, 1582–1587. [Google Scholar] [CrossRef] [PubMed]
- Gromadzka, G.; Kruszyńska, M.; Wierzbicka, D.; Litwin, T.; Dzieżyc, K.; Wierzchowska-Ciok, A.; Chabik, G.; Członkowska, A. Gene variants encoding proteins involved in antioxidant defense system and the clinical expression of Wilson disease. Liver Int. 2015, 35, 215–222. [Google Scholar] [CrossRef]
- Gromadzka, G.; Karpińska, A.; Przybyłkowski, A.; Litwin, T.; Wierzchowska-Ciok, A.; Dzieżyc, K.; Chabik, G.; Członkowska, A. Treatment with D-penicillamine or zinc sulphate affects copper metabolism and improves but not normalizes antioxidant capacity parameters in Wilson disease. Biometals 2014, 27, 207–215. [Google Scholar] [CrossRef] [PubMed]
- Wang, D.; Tian, Z.; Zhang, P.; Zhen, L.; Meng, Q.; Sun, B.; Xu, X.; Jia, T.; Li, S. The molecular mechanisms of cuproptosis and its relevance to cardiovascular disease. Biomed. Pharmacother. 2023, 163, 114830. [Google Scholar] [CrossRef] [PubMed]
- Cobine, P.A.; Brady, D.C. Cuproptosis: Cellular and molecular mechanisms underlying copper-induced cell death. Mol. Cell. 2022, 82, 1786–1787. [Google Scholar] [CrossRef] [PubMed]
- Rowland, E.A.; Snowden, C.K.; Cristea, I.M. Protein lipoylation: An evolutionarily conserved metabolic regulator of health and disease. Curr. Opin. Chem. Biol. 2018, 42, 76–85. [Google Scholar] [CrossRef] [PubMed]
- Kang, W.; Suzuki, M.; Saito, T.; Miyado, K. Emerging Role of TCA Cycle-Related Enzymes in Human Diseases. Int. J. Mol. Sci. 2021, 22, 13057. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.; Min, J.; Wang, F. Copper homeostasis and cuproptosis in health and disease. Signal Transduct. Target Ther. 2022, 7, 378. [Google Scholar] [CrossRef] [PubMed]
- Ban, X.X.; Wan, H.; Wan, X.X.; Tan, Y.T.; Hu, X.M.; Ban, H.X.; Chen, X.Y.; Huang, K.; Zhang, Q.; Xiong, K. Copper Metabolism and Cuproptosis: Molecular Mechanisms and Therapeutic Perspectives in Neurodegenerative Diseases. Curr. Med. Sci. 2024, 44, 28–50. [Google Scholar] [CrossRef] [PubMed]
- Duan, W.J.; He, R.R. Cuproptosis: Copper-induced regulated cell death. Sci. China Life Sci. 2022, 65, 1680–1682. [Google Scholar] [CrossRef] [PubMed]
- Tsui, K.H.; Hsiao, J.H.; Lin, L.T.; Tsang, Y.L.; Shao, A.N.; Kuo, C.H.; Chang, R.; Wen, Z.H.; Li, C.J. The Cross-Communication of Cuproptosis and Regulated Cell Death in Human Pathophysiology. Int. J. Biol. Sci. 2024, 20, 218–230. [Google Scholar] [CrossRef] [PubMed]
- Xie, J.; Yang, Y.; Gao, Y.; He, J. Cuproptosis: Mechanisms and links with cancers. Mol. Cancer 2023, 22, 46. [Google Scholar] [CrossRef] [PubMed]
- Albrecht, J.; Sonnewald, U.; Waagepetersen, H.S.; Schousboe, A. Glutamine in the central nervous system: Function and dysfunction. Front. Biosci. 2007, 12, 332–343. [Google Scholar] [CrossRef] [PubMed]
- Sidoryk-Wegrzynowicz, M. Impairment of glutamine/glutamate-γ-aminobutyric acid cycle in manganese toxicity in the central nervous system. Folia Neuropathol. 2014, 52, 377–382. [Google Scholar] [CrossRef]
- Konradi, C.; Heckers, S. Molecular aspects of glutamate dysregulation: Implications for schizophrenia and its treatment. Pharmacol. Ther. 2003, 97, 153–179. [Google Scholar] [CrossRef]
- Günther, V.; Lindert, U.; Schaffner, W. The taste of heavy metals: Gene regulation by MTF-1. Biochim. Biophys. Acta 2012, 1823, 1416–1425. [Google Scholar] [CrossRef]
- Pan, Z.; Huang, L.; Gan, Y.; Xia, Y.; Yu, W. The Molecular Mechanisms of Cuproptosis and Small-Molecule Drug Design in Diabetes Mellitus. Molecules 2024, 29, 2852. [Google Scholar] [CrossRef]
- Jiang, X.; Stockwell, B.R.; Conrad, M. Ferroptosis: Mechanisms, biology and role in disease. Nat. Rev. Mol. Cell Biol. 2021, 22, 266–282. [Google Scholar] [CrossRef] [PubMed]
- Dixon, S.J.; Lemberg, K.M.; Lamprecht, M.R.; Skouta, R.; Zaitsev, E.M.; Gleason, C.E.; Patel, D.N.; Bauer, A.J.; Cantley, A.M.; Yang, W.S.; et al. Ferroptosis: An iron-dependent form of nonapoptotic cell death. Cell 2012, 149, 1060–1072. [Google Scholar] [CrossRef]
- Feng, S.; Tang, D.; Wang, Y.; Li, X.; Bao, H.; Tang, C.; Dong, X.; Li, X.; Yang, Q.; Yan, Y.; et al. The mechanism of ferroptosis and its related diseases. Mol. Biomed. 2023, 4, 33. [Google Scholar]
- Li, D.; Li, Y. The interaction between ferroptosis and lipid metabolism in cancer. Signal Transduct. Target. Ther. 2020, 5, 108. [Google Scholar] [CrossRef] [PubMed]
- Berndt, C.; Alborzinia, H.; Amen, V.S.; Ayton, S.; Barayeu, U.; Bartelt, A.; Bayir, H.; Bebber, C.M.; Birsoy, K.; Böttcher, J.P.; et al. Ferroptosis in health and disease. Redox Biol. 2024, 75, 103211. [Google Scholar] [CrossRef] [PubMed]
- Wang, Y.; Yan, D.; Liu, J.; Tang, D.; Chen, X. Protein modification and degradation in ferroptosis. Redox Biol. 2024, 75, 103259. [Google Scholar] [CrossRef] [PubMed]
- Wu, H.; Wang, F.; Ta, N.; Zhang, T.; Gao, W. The Multifaceted Regulation of Mitochondria in Ferroptosis. Life 2021, 11, 222. [Google Scholar] [CrossRef] [PubMed]
- Li, Y.; Wang, X.; Huang, Z.; Zhou, Y.; Xia, J.; Hu, W.; Wang, X.; Du, J.; Tong, X.; Wang, Y. CISD3 inhibition drives cystine-deprivation induced ferroptosis. Cell Death Dis. 2021, 12, 839. [Google Scholar] [CrossRef] [PubMed]
- Jiang, H.; Fang, Y.; Wang, Y.; Li, T.; Lin, H.; Lin, J.; Pan, T.; Liu, Q.; Lv, J.; Chen, D.; et al. FGF4 improves hepatocytes ferroptosis in autoimmune hepatitis mice via activation of CISD3. Int. Immunopharmacol. 2023, 116, 109762. [Google Scholar] [CrossRef] [PubMed]
- Gao, M.; Yi, J.; Zhu, J.; Minikes, A.M.; Monian, P.; Thompson, C.B.; Jiang, X. Role of Mitochondria in Ferroptosis. Mol. Cell. 2019, 73, 354–363. [Google Scholar] [CrossRef] [PubMed]
- Tang, D.; Chen, X.; Kroemer, G. Cuproptosis: A copper-triggered modality of mitochondrial cell death. Cell. Res. 2022, 32, 417–418. [Google Scholar] [CrossRef] [PubMed]
- Fan, H.; Wang, K.; Zhao, X.; Song, B.; Yao, T.; Liu, T.; Gao, G.; Lu, W.; Liu, C. Emerging insights into cuproptosis and copper metabolism: Implications for age-related diseases and potential therapeutic strategies. Front. Aging Neurosci. 2024, 16, 1335122. [Google Scholar] [CrossRef]
- Feng, Y.; Yang, Z.; Wang, J.; Zhao, H. Cuproptosis: Unveiling a new frontier in cancer biology and therapeutics. Cell. Commun. Signal 2024, 22, 249. [Google Scholar] [CrossRef]
- Tadokoro, T.; Ikeda, M.; Ide, T.; Deguchi, H.; Ikeda, S.; Okabe, K.; Ishikita, A.; Matsushima, S.; Koumura, T.; Yamada, K.I.; et al. Mitochondria-dependent ferroptosis plays a pivotal role in doxorubicin cardiotoxicity. JCI Insight 2023, 8, e169756. [Google Scholar] [CrossRef] [PubMed]
- Tang, D.; Chen, X.; Kang, R.; Kroemer, G. Ferroptosis: Molecular mechanisms and health implications. Cell Res. 2021, 31, 107–125. [Google Scholar] [CrossRef] [PubMed]
- Battaglia, A.M.; Chirillo, R.; Aversa, I.; Sacco, A.; Costanzo, F.; Biamonte, F. Ferroptosis and Cancer: Mitochondria Meet the “Iron Maiden” Cell Death. Cells 2020, 9, 1505. [Google Scholar] [CrossRef] [PubMed]
- Liu, N.; Chen, M. Crosstalk between ferroptosis and cuproptosis: From mechanism to potential clinical application. Biomed. Pharmacother. 2024, 171, 116115. [Google Scholar] [CrossRef] [PubMed]
- Bonekamp, N.A.; Peter, B.; Hillen, H.S.; Felser, A.; Bergbrede, T.; Choidas, A.; Horn, M.; Unger, A.; Di Lucrezia, R.; Atanassov, I.; et al. Small-molecule inhibitors of human mitochondrial DNA transcription. Nature 2020, 588, 712–716. [Google Scholar] [CrossRef] [PubMed]
- Lewerenz, J.; Ates, G.; Methner, A.; Conrad, M.; Maher, P. Oxytosis/ferroptosis-(Re-) emerging roles for oxidative stress-dependent non-apoptotic cell death in diseases of the central nervous system. Front. Neurosci. 2018, 12, 214. [Google Scholar] [CrossRef] [PubMed]
- Neitemeier, S.; Jelinek, A.; Laino, V.; Hoffmann, L.; Eisenbach, I.; Eying, R.; Ganjam, G.K.; Dolga, A.M.; Oppermann, S.; Culmsee, C. BID links ferroptosis to mitochondrial cell death pathways. Redox Biol. 2017, 12, 558–570. [Google Scholar] [CrossRef] [PubMed]
- Shen, Y.; Li, D.; Liang, Q.; Yang, M.; Pan, Y.; Li, H. Cross-talk between cuproptosis and ferroptosis regulators defines the tumor microenvironment for the prediction of prognosis and therapies in lung adenocarcinoma. Front. Immunol. 2023, 13, 1029092. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Kuang, F.; Kroemer, G.; Klionsky, D.J.; Kang, R.; Tang, D. Autophagy-Dependent Ferroptosis: Machinery and Regulation. Cell Chem. Biol. 2020, 27, 420–435. [Google Scholar] [CrossRef] [PubMed]
- Yang, M.; Chen, P.; Liu, J.; Zhu, S.; Kroemer, G.; Klionsky, D.J.; Lotze, M.T.; Zeh, H.J.; Kang, R.; Tang, D. Clockophagy is a novel selective autophagy process favoring ferroptosis. Sci. Adv. 2019, 5, eaaw2238. [Google Scholar] [CrossRef] [PubMed]
- Gao, M.; Monian, P.; Pan, Q.; Zhang, W.; Xiang, J.; Jiang, X. Ferroptosis is an autophagic cell death process. Cell. Res. 2016, 26, 1021–1032. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Kang, R.; Tang, D. Signaling pathways and defense mechanisms of ferroptosis. FEBS J. 2022, 289, 7038–7050. [Google Scholar] [CrossRef]
- Park, E.; Chung, S.W. ROS-mediated autophagy increases intracellular iron levels and ferroptosis by ferritin and transferrin receptor regulation. Cell Death Dis. 2019, 10, 822. [Google Scholar] [CrossRef]
- Ferrero-Miliani, L.; Nielsen, O.H.; Andersen, P.S.; Girardin, S.E. Chronic inflammation: Importance of NOD2 and NALP3 in interleukin-1beta generation. Clin. Exp. Immunol. 2007, 147, 227–235. [Google Scholar] [CrossRef]
- Nathan, C.; Ding, A. Nonresolving inflammation. Cell. 2010, 140, 871–882. [Google Scholar] [CrossRef] [PubMed]
- Chen, L.; Deng, H.; Cui, H.; Fang, J.; Zuo, Z.; Deng, J.; Li, Y.; Wang, X.; Zhao, L. Inflammatory responses and inflammation-associated diseases in organs. Oncotarget 2017, 9, 7204–7218. [Google Scholar] [CrossRef]
- Jian, Z.; Guo, H.; Liu, H.; Cui, H.; Fang, J.; Zuo, Z.; Deng, J.; Li, Y.; Wang, X.; Zhao, L. Oxidative stress, apoptosis and inflammatory responses involved in copper-induced pulmonary toxicity in mice. Aging 2020, 12, 16867–16886. [Google Scholar] [CrossRef] [PubMed]
- Checa, J.; Aran, J.M. Reactive Oxygen Species: Drivers of Physiological and Pathological Processes. J. Inflamm. Res. 2020, 13, 1057–1073. [Google Scholar]
- Fischer, R.; Maier, O. Interrelation of oxidative stress and inflammation in neurodegenerative disease: Role of TNF. Oxid. Med. Cell. Longev. 2015, 2015, 610813. [Google Scholar]
- Bartuzi, P.; Hofker, M.H.; van de Sluis, B. Tuning NF-κB activity. A touch of COMMD proteins. Biochim. Biophys. Acta 2013, 1832, 2315–2321. [Google Scholar] [CrossRef]
- Gromadzka, G.; Tarnacka, B.; Flaga, A.; Adamczyk, A. Copper dyshomeostasis in Neurodegenerative Diseases-Therapeutic Implications. Int. J. Mol. Sci. 2020, 21, 9259. [Google Scholar] [CrossRef] [PubMed]
- Spisni, E.; Valerii, M.; Manerba, M.; Strillacci, A.; Polazzi, E.; Mattia, T.; Griffoni, C.; Tomasi, V. Effect of copper on extracellular levels of key pro-inflammatory molecules in hypothalamic GN11 and primary neurons. NeuroToxicology 2009, 30, 605–612. [Google Scholar] [CrossRef] [PubMed]
- Schmalz, G.; Schuster, U.; Schweikl, H. Influence of metals on IL-6 release in vitro. Biomaterials 1998, 19, 1689–1694. [Google Scholar] [CrossRef] [PubMed]
- Medici, V.; Shibata, N.M.; Kharbanda, K.K.; LaSalle, J.M.; Woods, R.; Liu, S.; Engelberg, J.A.; Devaraj, S.; Török, N.J.; Jiang, J.X.; et al. Wilson’s disease. Changes in methionine metabolism and inflammation affect global DNA methylation in early liver disease. Hepatology 2013, 57, 555–565. [Google Scholar] [CrossRef] [PubMed]
- Biempica, L.; Rauch, H.; Quintana, N.; Sternlieb, I. Morphologic and chemical studies on a murine mutation (Toxic Milk Mice) resulting in hepatic copper toxicosis. Lab. Investig. 1988, 59, 500–508. [Google Scholar] [PubMed]
- Togashi, Y.; Li, Y.; Kang, J.H.; Takeichi, N.; Fujioka, Y.; Nagashima, K.; Kobayashi, H. D-penicillamine prevents the development of hepatitis in Long-Evans Cinnamon rats with abnormal copper metabolism. Hepatology 1992, 15, 82–87. [Google Scholar] [CrossRef] [PubMed]
- Medici, V.; Trevisan, C.P.; D’Incŕ, R.; Barollo, M.; Zancan, L.; Fagiuoli, S.; Martines, D.; Paola, I.; Giacomo, C.S. Diagnosis and management of Wilson’s disease: Results of a single center experience. J. Clin. Gastroenterol. 2006, 40, 936–941. [Google Scholar] [CrossRef] [PubMed]
- Schroeder, S.M.; Matsukuma, K.E.; Medici, V. Wilson disease and the differential diagnosis of its hepatic manifestations: A narrative review of clinical, laboratory, and liver histological features. Ann. Transl. Med. 2021, 9, 1394. [Google Scholar] [CrossRef] [PubMed]
- Wu, P.; Dong, J.; Cheng, N.; Yang, R.; Han, Y.; Han, Y. Inflammatory cytokines expression in Wilson’s disease. Neurol. Sci. 2019, 40, 1059–1066. [Google Scholar] [CrossRef] [PubMed]
- Persichini, T.; Percario, Z.; Mazzon, E.; Colasanti, M.; Cuzzocrea, S.; Musci, G. Copper activates the NF-kappaB pathway in vivo. Antioxid. Redox Signal. 2006, 8, 1897–1904. [Google Scholar] [CrossRef]
- Sandoval, C.; Ríos, G.; Sepúlveda, N.; Salvo, J.; Souza-Mello, V.; Farías, J. Effectiveness of Copper Nanoparticles in Wound Healing Process Using In Vivo and In Vitro Studies: A Sys-tematic Review. Pharmaceutics 2022, 14, 1838. [Google Scholar] [CrossRef] [PubMed]
- Zhao, D.; Wu, L.; Fang, X.; Wang, L.; Liu, Q.; Jiang, P.; Ji, Z.; Zhang, N.; Yin, M.; Han, H. Copper exposure induces inflammation and PANoptosis through the TLR4/NF-κB signaling pathway, leading to testicular damage and impaired spermatogenesis in Wilson disease. Chem. Biol. Interact. 2024, 396, 111060. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Zhang, Z.; Mo, Y.; Zhang, Y.; Yuan, J.; Zhang, Q. MMP-3 mediates copper oxide nanoparticle-induced pulmonary inflammation and fibrosis. J. Nanobiotechnol. 2024, 22, 428. [Google Scholar] [CrossRef] [PubMed]
- Gu, T.; Kong, M.; Duan, M.; Chen, L.; Tian, Y.; Xu, W.; Zeng, T.; Lu, L. Cu exposure induces liver inflammation via regulating gut microbiota/LPS/liver TLR4 signaling axis. Ecotoxicol. Environ. Saf. 2024, 15, 116430. [Google Scholar] [CrossRef] [PubMed]
- Ho, W.I.; Hu, Y.; Cheng, C.W.; Wei, R.; Yang, J.; Li, N.; Au, K.W.; Tse, Y.L.; Wang, Q.; Ng, K.M.; et al. Liposome-encapsulated curcumin attenuates HMGB1-mediated hepatic inflammation and fibrosis in a murine model of Wilson’s disease. Biomed. Pharmacother. 2022, 152, 113197. [Google Scholar] [CrossRef] [PubMed]
- Bethin, K.E.; Cimato, T.R.; Ettinger, M.J. Copper binding to mouse liver S-adenosylhomocysteine hydrolase and the effects of copper on its levels. J. Biol. Chem. 1995, 270, 20703–20711. [Google Scholar] [CrossRef] [PubMed]
- Delgado, M.; Perez- Miguelsanz, J.; Garrido, F.; Rodriguez-Tarduchy, G.; Perez-Sala, D.; Pajares, M.A. Early effects of copper accumulation on methionine metabolism. Cell. Mol. Life Sci. 2008, 65, 2080–2090. [Google Scholar] [CrossRef] [PubMed]
- Esfandiari, F.; Medici, V.; Wong, D.H.; Jose, S.; Dolatshahi, M.; Quinlivan, E.; Dayal, S.; Lentz, R.R.; Tsukamoto, H.; Zhan, J.H.; et al. Epigenetic regulation of hepatic endoplasmic reticulum stress in the ethanol-fed cystathionine beta synthase-deficient mouse. Hepatology 2010, 51, 932–941. [Google Scholar] [CrossRef] [PubMed]
- LaSalle, J.M. A genomic point-of-view on environmental factors influencing the human brain methylome. Epigenetics 2011, 6, 829–862. [Google Scholar] [CrossRef] [PubMed]
- Gonda, T.A.; Kim, Y.I.; Salas, M.C.; Gamble, M.V.; Shibata, W.; Muthupalani, S.; Sohn, K.J.; Abrams, J.A.; Fox, J.G.; Wang, T.C.; et al. Folic Acid Increases Global DNA Methylation and Reduces Inflammation to Prevent Helicobacter-Associated Gastric Cancer in Mice. Gastroenterology 2012, 142, 824–833. [Google Scholar] [CrossRef] [PubMed]
- Bethin, K.E.; Petrovic, N.; Ettinger, M.J. Identification of a major hepatic copper binding protein as S-adenosylhomocysteine hydrolase. J. Biol. Chem. 1995, 270, 20698–20702. [Google Scholar] [CrossRef] [PubMed]
- Chen, R.; Kang, R.; Tang, D. The mechanism of HMGB1 secretion and release. Exp. Mol. Med. 2022, 54, 91–102. [Google Scholar] [CrossRef] [PubMed]
- Liu, J.; Liu, Y.; Wang, Y.; Kang, R.; Tang, D. HMGB1 is a mediator of cuproptosis-related sterile inflammation. Front. Cell Dev. Biol. 2022, 10, 996307. [Google Scholar] [CrossRef] [PubMed]
- Ye, F.; Chai, W.; Xie, M.; Yang, M.; Yu, Y.; Cao, L.; Yang, L. HMGB1 regulates erastin-induced ferroptosis via RAS-JNK/p38 signaling in HL-60/NRASQ61L cells. Am. J. Cancer Res. 2019, 9, 730–739. [Google Scholar] [PubMed]
- An, Y.; Li, S.; Huang, X.; Chen, X.; Shan, H.; Zhang, M. The Role of Copper Homeostasis in Brain Disease. Int. J. Mol. Sci. 2022, 23, 13850. [Google Scholar] [CrossRef] [PubMed]
- Stuerenburg, H.J. CSF copper concentrations, blood-brain barrier function, and ceruloplasmin synthesis during the treatment of Wilson’s disease. J. Neural. Transm. 2000, 107, 321–329. [Google Scholar] [CrossRef]
- Shribman, S.; Bocchetta, M.; Sudre, C.H.; Acosta-Cabronero, J.; Burrows, M.; Cook, P.; Thomas, D.L.; Gillett, G.T.; Tsochatzis, E.A.; Bandmann, O.; et al. Neuroimaging correlates of brain injury in Wilson’s disease: A multimodal, whole-brain MRI study. Brain 2022, 145, 263–275. [Google Scholar] [CrossRef] [PubMed]
- Wang, X.; Garrick, M.D.; Collins, J.F. Animal Models of Normal and Disturbed Iron and Copper Metabolism. J. Nutr. 2019, 149, 2085–2100. [Google Scholar] [CrossRef] [PubMed]
- Kalita, J.; Kumar, V.; Misra, U.K.; Kumar, S. Movement disorder in Wilson disease. Correlation with MRI and biomarkers of cell injury. J. Mol. Neurosci. 2020, 71, 338–346. [Google Scholar] [CrossRef]
- Gromadzka, G.; Członkowska, A. Influence of IL-1RN intron 2 variable number of tandem repeats (VNTR) polymorphism on the age at onset of neuropsychiatric symptoms in Wilson’s disease. Int. J. Neurosci. 2011, 121, 8–15. [Google Scholar] [CrossRef] [PubMed]
- Seripa, D.; Matera, M.G.; Dal Forno, G.; Gravina, C.; Masullo, C.; Daniele, A.; Binetti, G.; Bonvicini, C.; Squitti, R.; Palermo, M.T.; et al. Genotypes and haplotypes in the IL-1 gene cluster: Analysis of two genetically and diagnostically distinct groups of Alzheimer patients. Neurobiol. Aging 2005, 26, 455–464. [Google Scholar] [CrossRef] [PubMed]
- Su, F.; Bai, F.; Zhang, Z. Inflammatory Cytokines and Alzheimer’s Disease: A Review from the Perspective of Genetic Polymorphisms. Neurosci. Bull. 2016, 32, 469–480. [Google Scholar] [CrossRef] [PubMed]
- Wang, B.; Zhou, S.; Yang, Z.; Xie, Y.C.; Wang, J.; Zhang, P.; Lv, Z.; Zheng, C.; Ma, X. Genetic analysis of tumour necrosis factor-alpha (TNF-alpha) G-308A and Saitohin Q7R polymorphisms with Alzheimer’s disease. J. Neurol. Sci. 2008, 270, 148–151. [Google Scholar] [CrossRef] [PubMed]
- Watanabe, H.; Son, M. The Immune Tolerance Role of the HMGB1-RAGE Axis. Cells 2021, 10, 564. [Google Scholar] [CrossRef]
- Huber, R.; Meier, B.; Otsuka, A.; Fenini, G.; Satoh, T.; Gehrke, S.; Widmer, D.; Levesque, M.P.; Mangana, J.; Kerl, K.; et al. Tumour hypoxia promotes melanoma growth and metastasis via High Mobility Group Box-1 and M2-like macrophages. Sci. Rep. 2016, 6, 29914. [Google Scholar]
- Son, M.; Porat, A.; He, M.; Suurmond, J.; Santiago-Schwarz, F.; Andersson, U.; Coleman, T.R.; Volpe, B.T.; Tracey, K.J.; Al-Abed, Y.; et al. C1q and HMGB1 reciprocally regulate human macrophage polarization. Blood 2016, 128, 2218–2228. [Google Scholar] [CrossRef]
- Das, U.N. Arachidonic acid and lipoxin A4 as possible endogenous anti-diabetic molecules. Prostaglandins Leukot. Essent. Fat. Acids 2013, 88, 201–210. [Google Scholar] [CrossRef]
- Levy, B.D.; Clish, C.B.; Schmidt, B.; Gronert, K.; Serhan, C.N. Lipid mediator class switching during acute inflammation: Signals in resolution. Nat. Immunol. 2001, 2, 612–619. [Google Scholar] [CrossRef]
- Liu, T.; Xiang, A.; Peng, T.; Doran, A.C.; Tracey, K.J.; Barnes, B.J.; Tabas, I.; Son, M.; Diamond, B. HMGB1-C1q complexes regulate macrophage function by switching between leukotriene and specialized proresolving mediator biosynthesis. Proc. Natl. Acad. Sci. USA 2019, 116, 23254–23263. [Google Scholar] [CrossRef]
- Yang, H.; Wang, H.; Levine, Y.A.; Gunasekaran, M.K.; Wang, Y.; Addorisio, M.; Zhu, S.; Li, W.; Li, J.; de Kleijn, D.P.; et al. Identification of CD163 as an anti-inflammatory receptor for HMGB1-haptoglobin complexes. JCI Insight 2016, 1, e85375. [Google Scholar]
- Bandala-Sanchez, E.; Bediaga, N.G.; Goddard-Borger, E.D.; Ngui, K.; Naselli, G.; Stone, N.L.; Neale, A.M.; Pearce, L.A.; Wardak, A.; Czabotar, P.; et al. CD52 glycan binds the proinflammatory B box of HMGB1 to engage the Siglec-10 receptor and suppress human T cell function. Proc. Natl. Acad. Sci. USA 2018, 115, 7783–7788. [Google Scholar] [CrossRef] [PubMed]
- Wang, J.; Li, J.; Liu, J.; Chan, K.Y.; Lee, H.S.; Lin, K.N.; Wang, C.C.; Lau, T.S. Interplay of Ferroptosis and Cuproptosis in Cancer: Dissecting Metal-Driven Mechanisms for Therapeutic Potentials. Cancers 2024, 16, 512. [Google Scholar] [CrossRef] [PubMed]
- Kim, R.; Hashimoto, A.; Markosyan, N.; Tyurin, V.A.; Tyurina, Y.Y.; Kar, G.; Fu, S.; Sehgal, M.; Garcia-Gerique, L.; Kossenkov, A.; et al. Ferroptosis of tumour neutrophils causes immune suppression in cancer. Nature 2022, 612, 338–346. [Google Scholar] [CrossRef] [PubMed]
- Flemming, A. Neutrophil ferroptosis causes immunosuppression. Nat. Rev. Immunol. 2023, 23, 6. [Google Scholar] [CrossRef]
- Xu, S.; Min, J.; Wang, F. Ferroptosis: An emerging player in immune cells. Sci Bull 2021, 66, 2257–2260. [Google Scholar] [CrossRef]
- Yao, F.; Zhan, Y.; Pu, Z.; Lu, Y.; Chen, J.; Deng, J.; Wu, Z.; Chen, B.; Chen, J.; Tian, K.; et al. LncRNAs Target Ferroptosis-Related Genes and Impair Activation of CD4+ T Cell in Gastric Cancer. Front. Cell Dev. Biol. 2021, 9, 797339. [Google Scholar] [CrossRef]
- Voli, F.; Valli, E.; Lerra, L.; Kimpton, K.; Saletta, F.; Giorgi, F.M.; Mercatelli, D.; Rouaen, J.R.C.; Shen, S.; Murray, J.E.; et al. Intratumoral Copper Modulates PD-L1 Expression and Influences Tumor Immune Evasion. Cancer Res. 2020, 80, 4129–4144. [Google Scholar] [CrossRef]
- Ishida, Y.; Agata, Y.; Shibahara, K.; Honjo, T. Induced expressionof PD-1, a novel member of the immunoglobulin gene superfamily upon programmed cell death. EMBO J. 1992, 11, 3887–3895. [Google Scholar] [CrossRef]
- Keir, M.E.; Butte, M.J.; Freeman, G.J.; Sharpe, A.H. PD-1 and its ligands in tolerance and immunity. Annu. Rev. Immunol. 2008, 26, 677–704. [Google Scholar] [CrossRef]
- Gianchecchi, E.; Delfino, D.V.; Fierabracci, A. Recent insights into the role of the PD-1/PD-L1 pathway in immunological tolerance and autoimmunity. Autoimmun. Rev. 2013, 12, 1091–1100. [Google Scholar] [CrossRef]
- Agata, Y.; Kawasaki, A.; Nishimura, H.; Ishida, Y.; Tsubata, T.; Yagita, H.; Honjo, T. Expression of the PD-1 antigen on the surface of stimulated mouse T and B lymphocytes. Int. Immunol. 1996, 8, 765–772. [Google Scholar] [CrossRef]
- Freeman, G.J.; Wherry, E.J.; Ahmed, R.; Sharpe, A.H. Reinvigorating exhausted HIV-specific T cells via PD-1-PD-1 ligand blockade. J. Exp. Med. 2006, 203, 2223–2227. [Google Scholar] [CrossRef]
- Kinter, A.L.; Godbout, E.J.; McNally, J.P.; Sereti, I.; Roby, G.A.; O’Shea, M.A.; Fauci, A.S. The common g-chain cytokines IL-2, IL-7,IL-15, and IL-21 induce the expression of programmed death-1 and its ligands. J. Immunol. 2008, 181, 6738–6746. [Google Scholar] [CrossRef] [PubMed]
- Dong, H.; Strome, S.E.; Salomao, D.R.; Tamura, H.; Hirano, F.; Flies, D.B.; Roche, P.C.; Lu, J.; Zhu, G.; Tamada, K.; et al. Tumor-associated B7-H1 promotes T-cell apoptosis: A potential mechanism of immune evasion. Nat. Med. 2002, 8, 793–800. [Google Scholar] [CrossRef] [PubMed]
- Riley, J.L. PD-1 signaling in primary T cells. Immunol Rev. 2009, 229, 114–125. [Google Scholar] [CrossRef]
- Crusz, S.M.; Balkwill, F.R. Inflammation and cancer: Advances and new agents. Nat. Rev. Clin. Oncol. 2015, 12, 584–596. [Google Scholar] [CrossRef] [PubMed]
- Kahan, S.M.; Wherry, E.J.; Zajac, A.J. T cell exhaustion during persistent viral infections. Virology 2015, 479, 180–193. [Google Scholar] [CrossRef]
- Ha, S.J.; West, E.E.; Koichi, A.; Smith, K.A.; Ahmed, R. Manipulating both the inhibitory and stimulatory immune system towards the success of therapeutic vaccination against chronic viral infections. Immunol. Rev. 2008, 223, 317–333. [Google Scholar] [CrossRef]
- Albillos, A.; Lario, M.; Álvarez-Mon, M. Cirrhosis-associated immune dysfunction: Distinctive features and clinical relevance. J. Hepatol. 2014, 61, 1385–1396. [Google Scholar] [CrossRef]
- Helmy, K.Y.; Katschke, K.J., Jr.; Gorgani, N.N.; Kljavin, N.M.; Elliott, J.M.; Diehl, L.; Scales, S.J.; Ghilardi, N.; van Lookeren Campagne, M. CRIg: A macrophage complement receptor required for phagocytosis of circulating pathogens. Cell 2006, 124, 915–927. [Google Scholar] [CrossRef]
- Rimola, A.; Soto, R.; Bory, F.; Arroyo, V.; Piera, C.; Rodes, J. Reticuloendothelial system phagocytic activity in cirrhosis and its relation to bacterial infections and prognosis. Hepatology 1984, 4, 53–58. [Google Scholar] [CrossRef]
- Rajkovic, I.A.; Williams, R. Abnormalities of neutrophil phagocytosis, intracellular killing and metabolic activity in alcoholic cirrhosis and hepatitis. Hepatology 1986, 6, 252–262. [Google Scholar] [CrossRef]
- Fiuza, C.; Salcedo, M.; Clemente, G.; Tellado, J.M. In vivo neutrophil dysfunction in cirrhotic patients with advanced liver disease. J. Infect. Dis. 2000, 182, 526–533. [Google Scholar] [CrossRef] [PubMed]
- Tritto, G.; Bechlis, Z.; Stadlbauer, V.; Davies, N.; Frances, R.; Shah, N.; Mookerjee, R.P.; Such, J.; Jalan, R. Evidence of neutrophil functional defect despite inflammation in stable cirrhosis. J. Hepatol. 2011, 55, 574–581. [Google Scholar] [CrossRef] [PubMed]
- Ono, Y.; Watanabe, T.; Matsumoto, K.; Ito, T.; Kunii, O.; Goldstein, E. Opsonophagocytic dysfunction in patients with liver cirrhosis and low responses to tumor necrosis factor-a and lipopolysaccharide in patients’ blood. J. Infect. Chemother. 2004, 10, 200–207. [Google Scholar] [CrossRef] [PubMed]
- Albillos, A.; de la Hera, A.; Reyes, E.; Monserrat, J.; Muñoz, L.; Nieto, M.; Prieto, A.; Sanz, E.; Alvarez-Mon, M. Tumour necrosis factor-alpha expression by activated monocytes and altered T-cell homeostasis in ascitic alcoholic cirrhosis: Amelioration with norfloxacin. J. Hepatol. 2004, 40, 624–631. [Google Scholar] [CrossRef]
- Perrin, D.; Bignon, J.D.; Beaujard, E.; Cheneau, M.L. Populations of circulating T lymphocytes in patients with alcoholic cirrhosis. Gastroenterol. Clin. Biol. 1984, 8, 907–910. [Google Scholar]
- Morita, K.; Fukuda, Y.; Nakano, I.; Katano, Y.; Hayakawa, T. Peripheral lymphocyte subsets vary with stage of hepatitis C virus-associated liver disease. Hepatogastroenterology 2005, 52, 1803–1808. [Google Scholar]
- McGovern, B.H.; Golan, Y.; Lopez, M.; Pratt, D.; Lawton, A.; Moore, G.; Epstein, M.; Knox, T.A. The impact of cirrhosis on CD4+ T cell counts in HIV-seronegative patients. Clin. Infect. Dis. 2007, 44, 431–437. [Google Scholar] [CrossRef]
- Lario, M.; Munoz, L.; Ubeda, M.; Borrero, M.J.; Martinez, J.; Monserrat, J.; Díaz, D.; Álvarez-Mon, M.; Albillos, A. Defective thymopoiesis and poor peripheral homeostatic replenishment of T-helper cells cause T-cell lymphopenia in cirrhosis. J. Hepatol. 2013, 59, 723–730. [Google Scholar] [CrossRef]
- Deviere, J.; Denys, C.; Schandene, L.; Romasco, F.; Adler, M.; Wybran, J.; Dupont, E. Decreased proliferative activity associated with activation markers in patients with alcoholic liver cirrhosis. Clin. Exp. Immunol. 1988, 72, 377–382. [Google Scholar]
- Giron-Gonzalez, J.A.; Alvarez-Mon, M.; Menendez-Caro, J.L.; Manzano, L.; Abreu, L.; Yebra, M.; Durántez-Martínez, A. T lymphocytes from alcoholic cirrhotic patients show normal interleukin-2 production but a defective proliferative response to polyclonal mitogens. Am. J. Gastroenterol. 1994, 89, 767–773. [Google Scholar]
- Morishima, C.; Di Bisceglie, A.M.; Rothman, A.L.; Bonkovsky, H.L.; Lindsay, K.L.; Lee, W.M.; Koziel, M.J.; Fontana, R.J.; Kim, H.Y.; Wright, E.C.; et al. Antigen-specific T lymphocyte proliferation decreases over time in advanced chronic hepatitis C. J. Viral. Hepat. 2012, 19, 404–413. [Google Scholar] [CrossRef]
- Laso, F.J.; Madruga, J.I.; Giron, J.A.; Lopez, A.; Ciudad, J.; San Miguel, J.F.; Alvarez-Mon, M.; Orfao, A. Decreased natural killer cytotoxic activity in chronic alcoholism is associated with alcohol liver disease but not active ethanol consumption. Hepatology 1997, 25, 1096–1100. [Google Scholar] [CrossRef]
- Członkowska, A.; Niewada, M.; Litwin, T.; Kraiński, Ł.; Skowrońska, M.; Piechal, A.; Antos, A.; Misztal, M.; Khanna, I.; Kurkowska-Jastrzębska, I. Seven decades of clinical experience with Wilson’s disease: Report from the national reference centre in Poland. Eur. J. Neurol. 2022. [Google Scholar] [CrossRef]
- Socha, P.; Czlonkowska, A.; Janczyk, W.; Litwin, T. Wilson’s disease- management and long term outcomes. Best Pract. Res. Clin. Gastroenterol. 2022, 56, 101768. [Google Scholar] [CrossRef]
- Członkowska, A.; Litwin, T.; Dusek, P.; Ferenci, P.; Lutsenko, S.; Medici, V.; Rybakowski, J.K.; Weiss, K.H.; Schilsky, M.L. Wilson disease. Nat. Rev. Dis. Primers 2018, 4, 21. [Google Scholar] [CrossRef]
- Czlonkowska, A.; Litwin, T. Wilson disease—Currently used anticopper therapy. Handb. Clin. Neurol. 2017, 142, 181–191. [Google Scholar]
- Litwin, T.; Członkowska, A.; Socha, P. Oral Chelator Treatment of Wilson Disease: D-Penicillamine. In Clinical and Translational Perspectives on WILSON DISEASE; Kerkar, N., Roberts, E.A., Eds.; Academic Press: Cambridge, MA, USA, 2019; Chapter 34; pp. 357–364. [Google Scholar]
- Meyer, O. D-pénicillamine: Mécanisme d’action cellulaire et maladies auto-immunes induites [D-penicillamine: Mechanism of cellular action and induced autoimmune diseases]. Rev. Rhum. Mal. Osteoartic. 1986, 53, 15–20. [Google Scholar]
- Li, J.; Uetrecht, J.P. D-penicillamine-induced autoimmunity: Relationship to macrophage activation. Chem. Res. Toxicol. 2009, 22, 1526–1533. [Google Scholar] [CrossRef]
- Enzenauer, R.J.; West, S.G.; Rubin, R.L. D-penicillamine-induced lupus erythematosus. Arthritis Rheum. 1990, 33, 1582–1585. [Google Scholar] [CrossRef] [PubMed]
- Kang, S.; Cho, M.H.; Hyun, H.; Kim, J.H.; Ko, J.S.; Kang, H.G.; Cheong, H., II; Kim, W.S.; Moon, K.C.; Ha, I.S. A pediatric case of a D-Penicillamine induced ANCA-associated vasculitis manifesting a pulmonary-renal syndrome. J. Korean Med. Sci. 2019, 34, e173. [Google Scholar] [CrossRef]
- Poulas, K.; Koutsouraki, E.; Kordas, G.; Kokla, A.; Tzartos, S.J. Anti- MuSK- and anti-AChR-positive myasthenia gravis induced by d-penicillamine. J. Neuroimmunol. 2012, 250, 94–98. [Google Scholar] [CrossRef] [PubMed]
- Harpey, J.P.; Caille, B.; Moulias, R.; Goust, J.M. Lupus-like syndrome induced by D-penicillamine in Wilson’s disease. Lancet 1971, 1, 292. [Google Scholar] [CrossRef] [PubMed]
- Walshe, J.M. Penicillamine and the SLE syndrome. J. Rheumatol. Suppl. 1981, 7, 155–160. [Google Scholar]
- Barthel, H.R.; Wallace, D.J.; Klinenberg, J.R. Liver transplantation in patients with systemic lupus erythematosus. Lupus 1995, 4, 15–17. [Google Scholar] [CrossRef] [PubMed]
- Dell’era, L.; Boati, E.; Nebbia, G.; Corona, F. Wilson’s disease treated with penicillamine and lupus erythematosus: Related or distinct entities? Minerva Pediatr. 2012, 64, 55–57. [Google Scholar] [PubMed]
- Seessle, J.; Gotthardt, D.N.; Schäfer, M.; Gohdes, A.; Pfeiffenberger, J.; Ferenci, P.; Stremmel, W.; Weiss, K.H. Concomitant immune-related events in Wilson disease: Implications for monitoring chelator therapy. J. Inherit. Metab. Dis. 2016, 39, 125–130. [Google Scholar] [CrossRef] [PubMed]
- Boudin, G.; Pépin, B.; Godeau, P.; Vernant, J.C.; Gouerou, H. Lupus érythémateux induit par la pénicillamine au cours d’une maladie de Wilson [Lupus erythematosus due to penicillamine associated with Wilson’s disease]. Ann. Med. Interne 1971, 122, 269–273. [Google Scholar]
- Kalina, P.; Procházková, L.; Hauftová, D. Syndróm podobný systémovému lupus erythematosus vyvolaný penicilamínom u pacienta s Wilsonovou chorobou [A syndrome similar to systemic lupus erythematosus caused by penicillamine in patients with Wilson’s disease]. Bratisl. Lek. Listy 1985, 84, 336–340. [Google Scholar] [PubMed]
- López-Guerra, N.; Alvarez Lario, B.; García-Moncó, C.; Peña Sagredo, J.L. Lupus eritematoso sistémico inducido por d-penicilamina en enfermedad de Wilson: A propósito de un caso [Systemic lupus erythematosus induced by d-penicillamine in Wilson’s disease: Apropos of a case]. Med. Clin. 1987, 88, 552–554. [Google Scholar]
- Jan, V.; Callens, A.; Machet, L.; Machet, M.C.; Lorette, G.; Vaillant, L. Pemphigus, polymyosite et myasthénie induits par la D-pénicillamine [D-penicillamine-induced pemphigus, polymyositis and myasthenia]. Ann. Dermatol. Venereol. 1999, 126, 153–156. [Google Scholar]
- Electronic Medicines Compendium. D-penicillamine Summary of Product Characteristic. Available online: https://www.medicines.org.uk/emc (accessed on 3 July 2024).
- Antos, A.J.; Litwin, T.; Przybyłkowski, A.; Skowrońska, M.; Kurkowska-Jastrzębska, I.; Członkowska, A. D-penicillamine-induced lupus erythematosus as an adverse reaction of treatment of Wilson’s Disease. Neurol. Neurochir. Pol. 2021, 55, 595–597. [Google Scholar] [CrossRef]
- Antos, A.; Członkowska, A.; Bembenek, J.; Kurkowska-Jastrzębska, I.; Litwin, T. D-Penicillamine-Induced Myasthenia Gravis-A Probable Complication of Wilson’s Disease Treatment-A Case Report and Systematic Review of the Literature. Life 2023, 13, 1715. [Google Scholar] [CrossRef]
- Thapa, L.; Thapa, M.; Bhattarai, S.; Shrestha, A.M.; Sharma, N.; Rai, N.; Pokharel, M.; Paudel, R. D-penicillamine induced myasthenia gravis in Wilson’s disease: A case report. JNMA J. Nepal Med. Assoc. 2022, 60, 644–647. [Google Scholar] [CrossRef]
- Reuner, U.; Stremmel, W.; Weiskirchen, R. The interesting case-orphan diseases-double trouble. Ann. Transl. Med. 2019, 7, S7. [Google Scholar] [CrossRef]
- Tan, S.S.; Latif, S.A.; Poh, W.Y. Concurrent massive breast enlargement, myasthenia gravis and dermopathy as manifestations of penicillamine toxicity in a Wilson’s disease patient. Med. J. Malaysia 2012, 67, 323–325. [Google Scholar]
- Varghese, T.; Ahmed, R.; Sankaran, J.D.; Al-Khusaiby, S.M. D-Penicillamine induced myasthenia gravis. Neurosciences 2002, 7, 293–295. [Google Scholar]
- Masters, C.L.; Dawkins, R.L.; Zilko, P.J.; Simpson, J.A.; Leedman, R.J. Penicillamine-associated myasthenia gravis, antiacetylcholine receptor and antistriational antibodies. Am. J. Med. 1977, 63, 689–694. [Google Scholar] [CrossRef]
- Czlonkowska, A. Myasthenia syndrome during penicillamine treatment. Br. Med. J. 1975, 28, 726–727. [Google Scholar] [CrossRef]
- Mao, Z.; Hu, X.; Lu, Z.; Hackett, M.L. Prognostic factors of remission in myasthenia gravis after thymectomy. Eur. J. Cardiothorac. Surg. 2015, 48, 18–24. [Google Scholar] [CrossRef]
- Hill, M.; Moss, P.; Wordsworth, P.; Newsom-Davis, J.; Willcox, N. T cell responses to D-penicillamine in drug-induced myasthenia gravis: Recognition of modified DR1:peptide complexes. J. Neuroimmunol. 1999, 97, 146–153. [Google Scholar] [CrossRef] [PubMed]
- Essigman, W.K. Multiple side effects of penicillamine therapy in one patient with rheumatoid arthritis. Ann. Rheum. Dis. 1982, 41, 617–620. [Google Scholar] [CrossRef]
- Kimbrough, R.L.; Mewis, L.; Stewart, R.H. D-penicillamine and the ocular myasthenic syndrome. Ann. Ophthalmol. 1981, 13, 1171–1172. [Google Scholar]
- Rodolico, C.; Bonanno, C.; Toscano, A.; Vita, G. Mu-SK-associated myasthenia gravis: Clinical features and management. Front. Neurol. 2020, 11, 660. [Google Scholar] [CrossRef]
- Marchiori, P.E.; Scaff, M.; Cossermelli, W.; De Assis, J.L. Myasthenia gravis induced by D-penicillamine in a patient with progressive systemic sclerosis. Arq. Neuropsiquiatr. 1984, 42, 380–383. [Google Scholar] [CrossRef] [PubMed]
- Członkowska, A. The influence of prolonged treatment with D-penicillamine on the immune response in Wilson’s disease. Eur. J. Clin. Pharmacol. 1977, 12, 265–271. [Google Scholar] [CrossRef] [PubMed]
- Komal Kumar, R.N.; Patil, S.A.; Taly, A.B.; Nirmala, M.; Sinha, S.; Arunodaya, G.R. Effect of D-penicillamine on neuromuscular junction in patients with Wilson disease. Neurology 2004, 63, 935–936. [Google Scholar] [CrossRef]
- Antczak-Kowalska, M.; Członkowska, A.; Eyileten, C.; Palejko, A.; Cudna, A.; Wolska, M.; Piechal, A.; Litwin, T. Autoantibodies in Wilson disease: Impact on clinical course. JIMD Rep. 2022, 63, 508–517. [Google Scholar] [CrossRef]
- Giannoccaro, M.P.; Gastaldi, M.; Rizzo, G.; Jacobson, L.; Vacchiano, V.; Perini, G.; Capellari, S.; Franciotta, D.; Costa, A.; Liguori, R.; et al. Antibodies to neuronal surface antigens in patients with a clinical diagnosis of neurodegenerative disorder. Brain Behav. Immun. 2021, 96, 106–112. [Google Scholar] [CrossRef]
- Giannoccaro, M.P.; Verde, F.; Morelli, L.; Rizzo, G.; Ricciardiello, F.; Liguori, R. Neural Surface Antibodies and Neurodegeneration: Clinical Commonalities and Pathophysiological Relationships. Biomedicines 2023, 11, 666. [Google Scholar] [CrossRef] [PubMed]
- Gromadzka, G.; Karlińska, A.G.; Łysiak, Z.; Błażejewska-Hyżorek, B.; Litwin, T.; Członkowska, A. Positivity of serum “classical” onconeural antibodies in a series of 2063 consecutive patients with suspicion of paraneoplastic neurological syndrome. J. Neuroimmunol. 2013, 259, 75–80. [Google Scholar] [CrossRef] [PubMed]
- Jańczyk, W.; Bierła, J.B.; Trojanowska, I.; Wierzbicka-Rucińska, A.; Cukrowska, B.; Socha, P. Prevalence and Significance of Autoantibody Seropositivity in Children with Wilson’s Disease. Diagnostics 2023, 13, 768. [Google Scholar] [CrossRef] [PubMed]
- Dara, N.; Imanzadeh, F.; Sayyari, A.A.; Nasri, P.; Hosseini, A.H. Simultaneous Presentation of Wilson’s Disease and Autoimmune Hepatitis; A Case Report and Review of Literature. Hepat. Mon. 2015, 15, e29043. [Google Scholar] [CrossRef] [PubMed]
- Robinson, M.W.; Harmon, C.; O’Farrelly, C. Liver immunology and its role in inflammation and homeostasis. Cell. Mol. Immunol. 2016, 13, 267–276. [Google Scholar] [CrossRef] [PubMed]
- Heymann, F.; Tacke, F. Immunology in the liver—From homeostasis to disease. Nat. Rev. Gastroenterol. Hepatol. 2016, 13, 88–110. [Google Scholar] [CrossRef] [PubMed]
- Shi, W.; Huang, X.; Zhang, S.; Jiao, Y. Co-occurring Wilson’s disease and non-penicillamine-induced systematic lupus erythematosus: A case report and literature review. Clin. Rheumatol. 2020, 6, 2485–2490. [Google Scholar] [CrossRef] [PubMed]
- Kim, T.Y.; Lee, S.H.; Kim, T.J.; Cho, K.R.; Cho, S.C.; Han, S.H.; Yang, S.Y.; Chung, Y.W.; Sohn, J.H.; Baik, S.H.; et al. A case of fulminant hepatic failure in Wilson’s disease combined with systemic lupus erythematosus. Taehan Kan Hakhoe Chi= Korean J. Hepatol. 2002, 8, 100–104. [Google Scholar]
- Santhakumar, R.; Gayathri, K.; Ramalingam, P.K.; Manjunath, B.V.; Karuppusamy, N.; Vetriveeran, B.; Selvamani, S.; Vishnuram, P.; Muruganathan, A.; Natarajan, K. Wilson’s Disease with Systemic Lupus Erythematosus. J. Assoc. Physicians India 2016, 64, 81–82. [Google Scholar] [PubMed]
- Pradhan, S.; Krishnamurthy, S.; Jagadisan, B.; Rajesh, N.G.; Kaliaperumal, S.; Ramasamy, S.; Subramanian, N. Wilson disease and lupus nephritis: Is it coincidence or a true association? Paediatr. Int. Child Health 2018, 39, 146–149. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Wang, D.; Wei, W.; Zeng, X. Wilson’s disease combined with systemic lupus erythematosus: A case report and literature review. BMC Neurol. 2018, 18, 85. [Google Scholar] [CrossRef] [PubMed]
- Xu, L.; Liu, B.; Liu, Z.; Tang, N.; She, C.; Wang, J.; Zang, B.; Yang, Y. Co-occurrence of Wilson’s disease and systemic lupus erythematosus: A case report and literature review. BMC Gastroenterol. 2021, 2, 229. [Google Scholar] [CrossRef] [PubMed]
- Yang, Z.; Su, Y.; Liu, M.; Sun, L.; Zhang, F.; Lin, W. A rare concomitance of Wilson’s disease and systemic lupus erythematosus in a teenage girl: A case report and literature review. Front. Pediatr. 2024, 11, 1296426. [Google Scholar] [CrossRef] [PubMed]
- Hadef, D.; Slimani, S.; Lahouel, F.; Benlahcen, B.; Bouchair, N. Concomitance of primary systemic lupus erythematosus and Wilson’s disease in a male child: A case report. Rheumatology 2022, 61 (Suppl. S2), keac496-079. [Google Scholar] [CrossRef]
- Mageed, S.A.; Rawla, P.; Mahmoud, M.A.; Shahba, A. Systemic lupus erythematosus, hypoparathyroidism, and hemolytic anemia in a patient with Wilson’s disease. Reumatologia 2019, 57, 239–242. [Google Scholar] [CrossRef] [PubMed]
- Yang, Z.; Li, Q.; Liu, S.; Zong, Z.; Yu, L.; Sun, S. Systemic lupus erythematosus combined with Wilson’s disease: A case report and literature review. BMC Pediatr. 2024, 24, 253. [Google Scholar] [CrossRef] [PubMed]
- González-Regueiro, J.A.; Cruz-Contreras, M.; Merayo-Chalico, J.; Barrera-Vargas, A.; Ruiz-Margáin, A.; Campos-Murguía, A.; Espin-Nasser, M.; Martínez-Benítez, B.; Méndez-Cano, V.H.; Macías-Rodríguez, R.U. Hepatic manifestations in systemic lupus erythematosus. Lupus 2020, 29, 813–824. [Google Scholar] [CrossRef] [PubMed]
- Zheng, R.H.; Wang, J.H.; Wang, S.B.; Chen, J.; Guan, W.M.; Chen, M.H. Clinical and immunopathological features of patients with lupus hepatitis. Chin. Med. J. 2013, 126, 260–266. [Google Scholar] [CrossRef] [PubMed]
- Matsumoto, T.; Kobayashi, S.; Shimizu, H.; Nakajima, M.; Watanabe, S.; Kitami, N.; Sato, N.; Abe, H.; Aoki, Y.; Hoshi, T.; et al. The liver in collagen diseases: Pathologic study of 160 cases with particular reference to hepatic arteritis, primary biliary cirrhosis, autoimmune hepatitis and nodular regenerative hyperplasia of the liver. Liver 2000, 20, 366–373. [Google Scholar] [CrossRef] [PubMed]
- Matsumoto, T.; Yoshimine, T.; Shimouchi, K.; Shiotu, H.; Kuwabara, N.; Fukuda, Y.; Hoshi, T. The liver in systemic lupus erythematosus: Pathologic analysis of 52 cases and review of Japanese Autopsy Registry Data. Hum. Pathol. 1992, 23, 1151–1158. [Google Scholar] [CrossRef] [PubMed]
- Santos, B.C.; Guedes, L.R.; Faria, L.C.; Couto, C.A. Wilson’s disease presentation resembling autoimmune hepatitis. BMJ Case Rep. 2019, 12, e230721. [Google Scholar] [CrossRef]
- Milkiewicz, P.; Saksena, S.; Hubscher, S.G.; Elias, E. Wilson’s disease with superimposed autoimmune features: Report of two cases and review. J. Gastroenterol. Hepatol. 2000, 15, 570–574. [Google Scholar] [CrossRef]
- Alvarez, F.; Berg, P.A.; Bianchi, F.B.; Bianchi, L.; Burroughs, A.K.; Cancado, E.L.; Chapman, R.W.; Cooksley, W.G.; Czaja, A.J.; Desmet, V.J.; et al. International Autoimmune Hepatitis Group report: Review of criteria for diagnosis of autoimmune hepatitis. J. Hepatol. 1999, 31, 929. [Google Scholar] [CrossRef] [PubMed]
- Manns, M.P.; Czaja, A.J.; Gorham, J.D.; Krawitt, E.L.; Mieli-Vergani, G.; Vergani, D.; Vierling, J.M. Diagnosis and management of autoimmune hepatitis. Hepatology 2010, 51, 2193–2213. [Google Scholar] [PubMed]
- European Association for the Study of the Liver. EASL clinical practice guidelines: Autoimmune hepatitis. J. Hepatol. 2015, 63, 971–1004. [Google Scholar]
- Scheinberg, I.H.; Sternlieb, I. Wilson’s Disease; Saunders: Philadelphia, PA, USA, 1984. [Google Scholar]
- European Association for Study of Liver. EASL Clinical Practice Guidelines: Wilson’s disease. J. Hepatol. 2012, 56, 671–685. [Google Scholar]
- Stremmel, W.; Meyerrose, K.W.; Niederau, C.; Hefter, H.; Kreuzpaintner, G.; Strohmeyer, G. Wilson disease: Clinical presentation, treatment, and survival. Ann. Intern. Med. 1991, 115, 720–726. [Google Scholar] [CrossRef]
- Yener, S.; Akarsu, M.; Karacanci, C.; Sengul, B.; Topalak, O.; Biberoglu, K.; Akpinar, H. Wilson’s disease with coexisting autoimmune hepatitis. J. Gastroenterol. Hepatol. 2004, 19, 114–116. [Google Scholar] [PubMed]
- Santos, R.G.; Alissa, F.; Reyes, J.; Teot, L.; Ameen, N. Fulminant hepatic failure: Wilson’s disease or autoimmune hepatitis? Implications for transplantation. Pediatr. Transplant. 2005, 9, 112–116. [Google Scholar] [CrossRef]
- Nasri, P.; Hosseini-Kordkhyli, S.E.; Jafari-Koulaee, A.; Hovsepian, S.; Saneian, H.; Khademian, M.; Famouri, F. Simultaneous Presentation of Autoimmune Hepatitis and Wilson’s Disease: A Systematic Review Study. J. Pediatr. Rev. 2021, 9, 277–292. [Google Scholar] [CrossRef]
- Dziezyc, K.; Litwin, T.; Czlonkowska, A. Multiple sclerosis in two patients with coexisting Wilson’s disease. Mult. Scler. Relat. Disord. 2014, 3, 387–390. [Google Scholar] [CrossRef] [PubMed]
- Despotov, K.; Klivenyi, P.; Nagy, I.; Palvolgyi, A.; Vecsei, L.; Rajda, V. Rare co-occurrence of multiple sclerosis and Wilson’s disease -case report. BMC Neurol. 2022, 22, 178. [Google Scholar] [CrossRef]
- Yetkin, M.F.; Miraz, M.; Gursoy, S. Multiple sclerosis and Wilson disease; a rare coincidence. Clin. Neurol. Neurosurg. 2019, 186, 105507. [Google Scholar] [CrossRef]
- Ghazavi, A.; Kianbakht, T.; Hasami, K.; Mosayebi, G. High copper and low zinc serum levels in Iranian patients with multiple sclerosis. Clin. Lab. 2012, 58, 161–164. [Google Scholar]
- Ascherio, A.; Munger, K. Environmental risk factors for multiple sclerosis. Part II: Noninfectious factors. Ann. Neurol. 2007, 61, 504–513. [Google Scholar] [CrossRef] [PubMed]
- Naorniakowska, M.; Woźniak, M.; Pronicki, M.; Grajkowska, W.; Kamińska, D.; Jańczyk, W.; Dądalski, M.; Cukrowska, B.; Socha, P. Autoimmune hepatitis, Wilson’s disease, or both? An analysis of challenging cases. Pediatr. Pol. J. Paediatr. 2020, 95, 18–24. [Google Scholar] [CrossRef]
- Gromny, I.; Kukulska, M.; Poniewierka, E.; Hałoń, A. Unusual case of Wilson’s disease and coexisting autoimmune hepatitis. Biomed. J. Sci. Tech. Res. 2019, 13, 10114–10115. [Google Scholar] [CrossRef]
- Loudianos, G.; Zappu, A.; Lepori, M.B.; Dessì, V.; Mameli, E.; Orrù, S.; Podda, R.A.; De Virgiliis, S. Acute liver failure because of Wilson disease with overlapping autoimmune hepatitis features: The coexistence of two diseases? J. Pediatr. Gastroenterol. Nutr. 2016, 63, e23–e24. [Google Scholar] [CrossRef] [PubMed]
- Bjørklund, G.; Dadar, M.; Chirumbolo, S.; Aaseth, J.; Peana, M. Metals, autoimmunity, and neuroendocrinology: Is there a connection? Environ. Res. 2020, 187, 109541. [Google Scholar] [CrossRef]
- Rosenblum, M.D.; Remedios, K.A.; Abbas, A.K. Mechanisms of human autoimmunity. J. Clin. Investig. 2015, 125, 2228–2233. [Google Scholar] [CrossRef]
- Duan, L.; Rao, X.; Sigdel, K.R. Regulation of Inflammation in Autoimmune Disease. J. Immunol. Res. 2019, 2019, 7403796. [Google Scholar] [CrossRef]
- Chen, Z.; Bozec, A.; Ramming, A.; Schett, G. Anti-inflammatory and immune-regulatory cytokines in rheumatoid arthritis. Nat. Rev. Rheumatol. 2019, 15, 9–17. [Google Scholar] [CrossRef]
- Nikoopour, E.; Schwartz, J.; Singh, B. Therapeutic benefits of regulating inflammation in autoimmunity. Inflamm. Allergy Drug Targets 2008, 7, 203–210. [Google Scholar] [CrossRef]
- Shen, H.H.; Yang, Y.X.; Meng, X.; Luo, X.Y.; Li, X.M.; Shuai, Z.W.; Ye, D.Q.; Pan, H.F. NLRP3: A promising therapeutic target for autoimmune diseases. Autoimmun. Rev. 2018, 17, 694–702. [Google Scholar] [CrossRef]
- Shlomchik, M.J.; Craft, J.E.; Mamula, M.J. From T to B and back again: Positive feedback in systemic autoimmune disease. Nat. Rev. Immunol. 2001, 1, 147–153. [Google Scholar] [CrossRef]
- Mauri, C.; Bosma, A. Immune regulatory function of B cells. Ann. Rev Immunol. 2012, 30, 221–241. [Google Scholar] [CrossRef] [PubMed]
- Berthelot, J.M.; Jamin, C.; Amrouche, K.; Le Goff, B.; Maugars, Y.; Youinou, P. Regulatory B cells play a key role in immune system balance. Jt. Bone Spine 2013, 80, 18–22. [Google Scholar] [CrossRef] [PubMed]
- Kuzuya, M.; Yamada, K.; Hayashi, T.; Funaki, C.; Naito, M.; Asai, K.; Kuzuya, F. Role of lipoprotein-copper complex in copper catalyzed- peroxidation of low-density lipoprotein. Biochim. Biophys. Acta 1992, 1123, 334–341. [Google Scholar] [CrossRef] [PubMed]
- Rubino, J.T.; Chenkin, M.P.; Keller, M.; Riggs-Gelasco, P.; Franz, K.J. A comparison of methionine, histidine and cysteine in copper(I)-binding peptides reveals differences relevant to copper uptake by organisms in diverse environments. Metallomics 2011, 3, 61–73. [Google Scholar] [CrossRef]
- Zhang, Y.; Wang, X.P.; Perner, S.; Bankfalvi, A.; Schlücker, S. Effect of antigen retrieval methods on nonspecific binding of antibody–metal nanoparticle conjugates on formalin-fixed paraffin-embedded tissue. Anal. Chem. 2017, 90, 760–768. [Google Scholar] [CrossRef]
- Abou-Donia, M.B.; Lieberman, A.; Curtis, L. Neural autoantibodies in patients with neurological symptoms and histories of chemical/mold exposures. Toxicol. Ind. Health. 2018, 34, 44–53. [Google Scholar] [CrossRef] [PubMed]
- De Wall, S.L.; Painter, C.; Stone, J.D.; Bandaranayake, R.; Wiley, D.C.; Mitchison, T.J.; Stern, L.J.; DeDecker, B.S. Noble metals strip peptides from class II MHC proteins. Nat. Chem. Biol. 2006, 2, 197. [Google Scholar] [CrossRef] [PubMed]
- Zelikoff, J.T. Trace metals and the immune system. In Encyclopedia of Immunotoxicology; Vohr, H.W., Ed.; Springer: Berlin/Heidelberg, Germany, 2016; pp. 907–911. [Google Scholar]
- Falcão, P.L.; Campos, T.P.R. The role of regulatory T cells, interleukin-10 and in vivo scintigraphy in autoimmune and idiopathic diseases-therapeutic perspectives and prognosis. Rev. Assoc. Med. Bras. 2017, 63, 1090–1099. [Google Scholar] [CrossRef] [PubMed]
- Zhang, Y.; Lawrence, D.A. Metals and autoimmune disease. In Encyclopedia of Immunotoxicology; Vohr, H.W., Ed.; Springer: Berlin/Heidelberg, Germany, 2016; pp. 603–609. [Google Scholar]
- Zhu, M.; Liang, Z.; Wang, T.; Chen, R.; Wang, G.; Ji, Y. Th1/Th2/Th17 cells imbalance in patients with asthma with and without psychological symptoms. Allergy Asthma Proc. 2016, 37, 148–156. [Google Scholar] [CrossRef] [PubMed]
- Magna, M.; Pisetsky, D.S. The role of HMGB1 in the pathogenesis of inflammatory and autoimmune diseases. Mol. Med. 2014, 20, 138–146. [Google Scholar] [CrossRef] [PubMed]
- Venereau, E.; Casalgrandi, M.; Schiraldi, M.; Antoine, D.J.; Cattaneo, A.; De Marchis, F.; Liu, J.; Antonelli, A.; Preti, A.; Raeli, L. Mutually exclusive redox forms of HMGB1 promote cell recruitment or proinflammatory cytokine release. J. Exp. Med. 2012, 209, 1519–1528. [Google Scholar] [CrossRef] [PubMed]
- Yang, H.; Lundbäck, P.; Ottosson, L.; Erlandsson-Harris, H.; Venereau, E.; Bianchi, M.E.; Al-Abed, Y.; Andersson, U.; Tracey, K.J.; Antoine, D.J. Expression of Concern to: Redox modification of cysteine residues regulates the cytokine activity of high mobility group box-1 (HMGB1). Mol. Med. 2020, 26, 18. [Google Scholar] [CrossRef] [PubMed]
- Park, J.S.; Svetkauskaite, D.; He, Q.; Kim, J.Y.; Strassheim, D.; Ishizaka, A.; Abraham, E. Involvement of toll-like receptors 2 and 4 in cellular activation by high mobility group box 1 protein. J. Biol. Chem. 2004, 279, 7370–7377. [Google Scholar] [CrossRef] [PubMed]
- Park, J.S.; Gamboni-Robertson, F.; He, Q.; Svetkauskaite, D.; Kim, J.Y.; Strassheim, D.; Sohn, J.W.; Yamada, S.; Maruyama, I.; Banerjee, A.; et al. High mobility group box 1 protein interacts with multiple toll-like receptors. Am. J. Physiol. Cell Physiol. 2006, 290, C917–C924. [Google Scholar] [CrossRef]
- Bianchi, M.E. HMGB1 loves company. J. Leukoc. Biol. 2009, 86, 573–576. [Google Scholar] [CrossRef] [PubMed]
- Reau, S.N.; Lammert, C.C.; Weiberg, E.M. Autoimmune hepatitis: Current and future therapies. Hepatol. Commun. 2024, 8, e0458. [Google Scholar] [CrossRef] [PubMed]
- Czaja, A.J. Drug choices in autoimmune hepatitis: Part A—Steroids. Expert Rev. Gastroenterol. Hepatol. 2012, 6, 603–615. [Google Scholar] [CrossRef] [PubMed]
- Pitman, S.K.; Huynh, T.; Bjarnason, T.A.; An, J.; Malkhaysan, K.A. A case report and focused literature review of d-penicillamine and severe neutropenia; a serious toxicity from seldom-used drug. Clin. Case Rep. 2019, 7, 990–994. [Google Scholar] [CrossRef] [PubMed]
- Stremmel, W.; Longerich, T.; Liere, R.; Vacata, V.; von Helden, J.; Weiskirchen, R. Wilson disease—The impact of hyperimmunity on disease activity: A case report. World J. Clin. Cases 2021, 9, 1386–1393. [Google Scholar] [CrossRef] [PubMed]
- Hsu, H.L.; Huang, F.C.; Ni, Y.H.; Chang, M.H. Steroids used to desensitize penicillamine allergy in Wilson disease. Acta Paediatr. Taiwan. 1999, 40, 448–450. [Google Scholar] [PubMed]
- Zheng, Z.W.; Dong, Y.; Wu, Z.Y. Latest innovations in the treatment of Wilson’s disease. iLiver 2022, 1, 181–186. [Google Scholar] [CrossRef]
- Ferenci, P.; Caca, K.; Loudianos, G.; Mieli-Vergani, G.; Tanner, S.; Sternlieb, I.; Schilsky, M.; Cox, D.; Berr, F. Diagnosis and phenotypic classification of Wilson disease. Liver Int. 2003, 23, 139–142. [Google Scholar] [CrossRef] [PubMed]
- Nagral, A.; Sarma, M.S.; Matthai, J.; Kukkle, P.L.; Devarbhavi, H.; Sinha, S.; Alam, S.; Bavdekar, A.; Dhiman, R.K.; Eapen, C.E.; et al. Wilson’s disease: Clinical Practice Guidelines of the Indian National Association for Study of the Liver, the Indian Society of Pediatric Gastroenterology, Hepatology and Nutrition, and the Movement Disorders Society of India. J. Clin. Exp. Hepatol. 2019, 9, 74–98, Erratum in J. Clin. Exp. Hepatol. 2020, 10, 99. [Google Scholar] [CrossRef]
Patient Description Sex, Age at WD Diagnosis | WD Form | Age at AID Diagnosis | Time of Treatment before AID Onset (Years) | AID | ANA | Treatment Decision after SLE Diagnosis | Did SLE Symptoms Disappear after Discontinuing DPA? | Reference |
---|---|---|---|---|---|---|---|---|
Female 22 | P | 23 y | 1 year | SLE symptoms (polyarthralgia, pericarditis, pleurisy, fever) and aortic regurgitation | ANA (1/500) and antinucleoprotein antibodies | Discontinuation DPA, corticosteroids | Yes, after 6 months | [166] |
Sex * 8 | * | * | * | SLE | “serologic changes of SLE” | In 4 discontinuation of DPA treatment | * | [167] |
Female 19 | P | 22 y | 3 y | arthritis | ANA of 1:640 (homogeneous), C3 35 mg/dl and anti-DNA 85% lupus anticoagulant was detected, anti-DNA of 1:2560 | tetraethylene tetramine dihydrochloride was substituted for DPA, steroids; liver transplantaion | Yes (after liver transplantation) | [168] |
Female 5 | ? | 7 y | 2 y | SLE | arthritis, malar rash and laboratory findings suggestive for lupus erythematosus | zinc acetate was substituted for penicillamine | * | [169] |
Male 9 | M | 22 y | 11 y | SLE seronegative polyarthritis | elevated ANA titers (>1:160) | Zinc | * | [170] |
Male 23 | NP | 1 y | SLE fever with arthralgia of the shoulders, hips, knees, feet, and thoracic spine | lupus anticoagulant and antinuclear antibodies (ANAs); anti-dsDNA, c-and p-ANCA, CCP antibodies (-) | Zinc sulphate, steroids | Yes, over 7 weeks | [176] |
Patient Description Sex, Age at WD Diagnosis | WD Manifestation | Age at AID Diagnosis | Time of Treatment before AID Onset (Years) | ANA | Treatment Decision after SLE Diagnosis | Did SLE Symptoms Disappear after Discontinuing DPA? | Reference |
---|---|---|---|---|---|---|---|
Male 56 y | H | 58 y | 15 months | AChR-Abs (+) MuSKAbs (+) | Withdrawal of DPA zinc sulphate pyridostigmine | At the follow-up visit after 6 months the patient did not present MG symptoms | [177] |
Male 9 y | NP | 15 y | 6 years | AChR-Abs (+) MuSK-Abs (-) | Withdrawal of DPA Pyridostigmine | Remarkable improvement within 2 months | [178] |
Female 11 y | H | 17 y | 6 years | AChR-Abs (+) MuSK-Abs not tested | DPA Pyridostigmine | Remarkable improvement | [179] |
Female 15 y | P | 16 y | 4 months | AChR-Abs and MuSK-Abs not tested | Trientine instead of DPA clobetasone butyrate for skin lesions (indication dermopathy) | One month later disappearance of the visual and skin complaints At follow-up at 7 months, complete resolution of all DPA-associated side effects | [180] |
Female 8 y | H | 12 y | 4 years | AChR-Abs (+) MuSK-Abs not tested | Withdrawal of DPA trientine | Remarkable improvement within 3 months | [181] |
Female 10 y | H | 18 | 8 years | AChR-Abs (+) MuSK-Abs not tested | DPA pyridostigmine and neostigmine | Increased serum AChR-Abs were observed during follow-up | [182] |
Male 13 y | P | 14 y | 13 months | AChR-Abs (+) MuSK-Abs not tested | Withdrawal of DPA Neostigmine | Remarkable improvement with cessation of all symptoms within 6 weeks | [183] |
Patient Description Sex, Age at WD Diagnosis | WD Form | Age at AID Diagnosis | Time of Treatment before AID Onset (Years) | AID | ANA Elevation | WD Treatment Decision |
---|---|---|---|---|---|---|
Female 27 | N | 38 y | 11 y | Ulcerative colitis | At diagnosis (−) Following second-line therapy (+) | Zinc |
Male 23 | M | 24 y | 1 y | SLE | At diagnosis (−) Following second-line therapy (+) | Zinc |
Female 17 | H | 39 y | 22 y | MS | At diagnosis (−) Following second-line therapy (−) | Zinc |
Female 16 | H | 28 y | 12 y | Morbus Werlhof | At diagnosis (−) Following second-line therapy (−) | Trientine |
Male 9 | H | 20 y | 11 y | Polyarthritis (seronegative) | At diagnosis (−) Following second-line therapy (+) | Zinc + trientine |
Female 8 | P | 32 y | 24 y | Psoriasis with psoriatic arthritis | At diagnosis (−) Following second-line therapy (+) | Trientine |
Patient’s Sex | WD Manifestation | Age at WD/AID Diagnosis | Disease Sequence | Main Symptoms | Immune/Autoimmune Laboratory Tests Results | Reference |
---|---|---|---|---|---|---|
Female | H | 18/18 | SLE/WD simultaneous | rashes on face and trunk together with icterus, pruritis, and fatigue; mild anemia and thrombocytopenia; elevated liver enzymes, hypoalbuminemia, and bilrubinemia; erythematous and slightly scaly macular papules on both cheeks and the neck and upper back, hepatomegaly, splenomegaly, and KF rings in both eyes. Decreased serum ceruloplasmin and copper, elevated urinary copper. Cirrhosis and splenomegaly | hypocomplementemia, ANA, anti-dsDNA antibodies, and anti-β2GP1 antibodies (+); Coombs test (−), bone marrow smear showed marked hyperplasia and defective megakaryocyte maturation consistent with immune thrombocytopenia. | [200] |
Female | FH | 12/10.5 | WD after 1.5 years of SLE | nephritis, pleurisy, hemolytic anemia; fulminant hepatic failure; decreased serum ceruloplasmin level and the presence of KF ring | ANA, anti-dsDNA, Coombs test (+) | [201] |
Female | H | 12/12 | SLE/WD simultaneous | abnormal LFT; abnormal copper metabolism; Kayser–Fleischer rings; nephritis | complement C3 decreased; ANA, anti-dsDNA, LA | [203] |
Female | NP | 18/18 | simultaneous WD/SLE/secondary Sjögren syndrome with aPL antibodies. | abnormal limb movements and slurred speech; dysdipsia, unsteady gait, dyskinesia, significantly increased involuntary movements of limbs; KF ring in both eyes; nephritis, fever, oral ulceration, xerostomia, keratoconjunctivitis sicca; Sjögren syndrome | elevated ESR, C-reactive protein, IgG, and IgM, and hypocomplementemia; ANA, anti-SSA antibody, anti-rRNP antibodies; anti-ACL antbodies, LA and anti-β2GP1 antibodies (+) | [204] |
Female | H | 32/29 | simultaneous | recurrent fever and multi-joint pain; liver cirrhosis, liver fibrosis, K–F ring | Leucopenia, anemia, multiple auto-antibodies, ANA anti-dsDNAanti-SSA anti-Smith antibody, anti-Ro52 antibody and anti-rRNP antibody, low levels of serum complement components (C3, C4). | [205] |
Female | NP | ?/24 | SLE with antiphospholipid syndrome, next WD | fever, neuropsychiatric symptoms, abnormal copper metabolismsm, KF rings; | ? | [202] * |
Female | H | 17/17 | Simultaneous WD/ SLE with APLA syndrome | facial and limb edema, abdominal distension, ascites, and splenomegaly. Abnormal LFT, low platelets; liver cirrhosis with splenomegaly. | Increased IgG, IgM; positive tests for antibodies against Sjögren’s syndrome A antigen (SSA), lupus anticoagulant (LA), and APLAs, including anti-domain I β2GPI antibodies, anti-vimentin antibodies, and anti-annexin A2 antibodies. The anti-dsDNA (−). Decreased complement 3 and C4. ANA (+), LA (+); AIH-related autoantibodies, such as ASMAs and LKM1 antibodies (−) | [206] |
Male | H | 12 | SLE Simultaneous | hepatic cytolysis, and hepato-cellular insufficiency; impaired liver function, hemolytic anaemia, and normal alkaline phosphatase levels; abnormal copper metabolism; nephrotic syndrome and the presence of inflammatory syndrome; the kidney biopsy histopathology revealed nephritis lupus class II | native anti-DNA and anti-PCNA antibodies (+) | [207] |
Female | N/M | 19/16 | SLE then WD | slurred speech, mild difficulty with deglutition, and an abnormally hyperextended right big toe; symmetrical basal ganglia abnormal signal intensity; severe acute hemolytic anemia; arthralgia of both knees, oral ulcers, photosensitivity, and proteinuria; thrombotic microangiopathy joint pain; abnormal LFT, | Smooth muscle antibody (SMA) and liver kidney microsomal type 1 (anti-LKM-1) antibodies (−) ANA (+), anti-dsDNA equivocal, and APLA (−) | [208] |
Female | H | 9/9 | Simultaneous | red-colored urine, thrombocytopenia, anemia, abnormal LFT, SLE and lupus nephritis (LN) Under light microscopy 2 focal segmental sclerosis with balloon adhesions and one case of cell-fibrous neoplasm formation in 26 glomeruli. Diffuse light-moderate proliferation was present in the mesangial zone. Podocyte swelling, swelling of epithelial cells, and focal fibrosis of the renal interstitium. | ANA (+), anti-dsDNA (+), A kidney biopsy was performed to determine the renal pathology. We detected IgA(+), IgG(+), C3(+), F+(−), IgM(++), and C1q(++) | [209] |
WD | Feature | SLE |
---|---|---|
- | Photosensitivity and malar rash | + |
+ (after DPA) | Oral ulcers | + |
+ (after DPA) | Proteinuria | + |
Rare, may be the initial manifestation | Hemolytic anemia | + |
+ (extrapyramidal) | Neuropsychiatric symptoms (CNS involvement) | + (lupus cerebritis, TTP) |
Rare | Arthralgia | + |
+ (pathognomic) | Kayser–Fleischer ring | - |
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Gromadzka, G.; Czerwińska, J.; Krzemińska, E.; Przybyłkowski, A.; Litwin, T. Wilson’s Disease—Crossroads of Genetics, Inflammation and Immunity/Autoimmunity: Clinical and Molecular Issues. Int. J. Mol. Sci. 2024, 25, 9034. https://doi.org/10.3390/ijms25169034
Gromadzka G, Czerwińska J, Krzemińska E, Przybyłkowski A, Litwin T. Wilson’s Disease—Crossroads of Genetics, Inflammation and Immunity/Autoimmunity: Clinical and Molecular Issues. International Journal of Molecular Sciences. 2024; 25(16):9034. https://doi.org/10.3390/ijms25169034
Chicago/Turabian StyleGromadzka, Grażyna, Julia Czerwińska, Elżbieta Krzemińska, Adam Przybyłkowski, and Tomasz Litwin. 2024. "Wilson’s Disease—Crossroads of Genetics, Inflammation and Immunity/Autoimmunity: Clinical and Molecular Issues" International Journal of Molecular Sciences 25, no. 16: 9034. https://doi.org/10.3390/ijms25169034