Role of Vitamin E and the Orexin System in Neuroprotection
Abstract
:1. Introduction
2. The Orexin System
3. Orexin in Microglia Activation
4. Vitamin E and Microglia Mediated Neuroprotection
5. Vitamin E in the Orexin System
6. Conclusions and Future Scenarios
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Acknowledgments
Conflicts of Interest
References
- Sessa, F.; Messina, G.; Russo, R.; Salerno, M.; Castruccio Castracani, C.; Distefano, A.; Li Volti, G.; Calogero, A.E.; Cannarella, R.; Mongioi’, L.M.; et al. Consequences on aging process and human wellness of generation of nitrogen and oxygen species during strenuous exercise. Aging Male 2020, 23, 14–22. [Google Scholar] [CrossRef]
- Ott, M.; Gogvadze, V.; Orrenius, S.; Zhivotovsky, B. Mitochondria, oxidative stress and cell death. Apoptosis 2007, 12, 913–922. [Google Scholar] [CrossRef] [PubMed]
- Calabrese, V.; Cornelius, C.; Mancuso, C.; Pennisi, G.; Calafato, S.; Bellia, F.; Bates, T.E.; Giuffrida Stella, A.M.; Schapira, T.; Dinkova Kostova, A.T.; et al. Cellular stress response: A novel target for chemoprevention and nutritional neuroprotection in aging, neurodegenerative disorders and longevity. Neurochem. Res. 2008, 33, 2444–2471. [Google Scholar] [CrossRef] [PubMed]
- Chiurchiù, V.; Orlacchio, A.; Maccarrone, M. Is Modulation of Oxidative Stress an Answer? The State of the Art of Redox Therapeutic Actions in Neurodegenerative Diseases. Oxid Med. Cell Longev. 2016, 2016, 7909380. [Google Scholar] [CrossRef]
- Zheng, M.; Storz, G. Redox sensing by prokaryotic transcription factors. BioChem. Pharmacol. 2000, 59, 1–6. [Google Scholar] [CrossRef]
- Schiavone, S.; Neri, M.; Mhillaj, E.; Pomara, C.; Trabace, L.; Turillazzi, E. The role of the NADPH oxidase derived brain oxidative stress in the cocaine-related death associated with excited delirium: A literature review. Toxicol. Lett. 2016, 258, 29–35. [Google Scholar] [CrossRef]
- Neri, M.; Riezzo, I.; Pomara, C.; Schiavone, S.; Turillazzi, E. Oxidative-Nitrosative Stress and Myocardial Dysfunctions in Sepsis: Evidence from the Literature and Postmortem Observations. Mediat. Inflamm. 2016, 2016, 3423450. [Google Scholar] [CrossRef]
- Zammit, C.; Muscat, R.; Sani, G.; Pomara, C.; Valentino, M. Cerebral white matter injuries following a hypoxic/ischemic insult during the perinatal period: Pathophysiology, prognostic factors, and future strategy of treatment approach. A minireview. Curr. Pharm. Des. 2015, 21, 1418–1425. [Google Scholar] [CrossRef] [PubMed]
- Turillazzi, E.; Neri, M.; Cerretani, D.; Cantatore, S.; Frati, P.; Moltoni, L.; Busardò, F.P.; Pomara, C.; Riezzo, I.; Fineschi, V. Lipid peroxidation and apoptotic response in rat brain areas induced by long-term administration of nandrolone: The mutual crosstalk between ROS and NF-kB. J. Cell Mol. Med. 2016, 20, 601–612. [Google Scholar] [CrossRef]
- Pawate, S.; Shen, Q.; Fan, F.; Bhat, N.R. Redox regulation of glial inflammatory response to lipopolysaccharide and interferongamma. Neurosci. Res. 2004, 77, 540–551. [Google Scholar] [CrossRef]
- Schiavone, S.; Mhillaj, E.; Neri, M.; Morgese, M.G.; Tucci, P.; Bove, M.; Valentino, M.; Di Giovanni, G.; Pomara, C.; Turillazzi, E.; et al. Early Loss of Blood-Brain Barrier Integrity Precedes NOX2 Elevation in the Prefrontal Cortex of an Animal Model of Psychosis. Mol. Neurobiol. 2017, 54, 2031–2044. [Google Scholar] [CrossRef]
- Neri, M.; Cantatore, S.; Pomara, C.; Riezzo, I.; Bello, S.; Turillazzi, E.; Fineschi, V. Immunohistochemical expression of proinflammatory cytokines IL-1β, IL-6, TNF-α and involvement of COX-2, quantitatively confirmed by Western blot analysis, in Wernicke’s encephalopathy. Pathol. Res. Pract. 2011, 207, 652–658. [Google Scholar] [CrossRef] [PubMed]
- Cerretani, D.; Bello, S.; Cantatore, S.; Fiaschi, A.I.; Montefrancesco, G.; Neri, M.; Pomara, C.; Riezzo, I.; Fiore, C.; Bonsignore, A.; et al. Acute administration of 3,4-methylenedioxymethamphetamine (MDMA) induces oxidative stress, lipoperoxidation and TNFα-mediated apoptosis in rat liver. Pharm. Res. 2011, 64, 517–527. [Google Scholar] [CrossRef] [PubMed]
- Von Arnim, C.A.; Gola, U.; Biesalski, H.K. More than the sum of its parts? Nutrition in Alzheimer’s disease. Nutrition 2010, 26, 694–700. [Google Scholar] [CrossRef]
- Hung, C.W.; Chen, Y.C.; Hsieh, W.L.; Chiou, S.H.; Kao, C.L. Ageing and neurodegenerative diseases. Ageing Res. Rev. 2010, 9, S36–S46. [Google Scholar]
- Mandel, S.; Grünblatt, E.; Riederer, P.; Gerlach, M.; Levites, Y.; Youdim, M.B. Neuroprotective strategies in Parkinson’s disease: An update on progress. CNS Drugs 2003, 17, 729–762. [Google Scholar] [CrossRef]
- Yu, Y.C.; Kuo, C.L.; Cheng, W.L.; Liu, C.S.; Hsieh, M. Decreased antioxidant enzyme activity and increased mitochondrial DNA damage in cellular models of Machado-Joseph disease. J. Neurosci. Res. 2009, 87, 1884–1891. [Google Scholar] [CrossRef] [PubMed]
- Selkoe, D.J. Alzheimer’s disease results from the cerebral accumulation and cytotoxicity of amyloid beta-protein. J. Alzheimers Dis. 2001, 3, 75–80. [Google Scholar] [CrossRef] [PubMed]
- Mattson, M.P. Pathways towards and away from Alzheimer’s disease. Nature 2004, 430, 631–639. [Google Scholar] [CrossRef]
- Dias, V.; Junn, E.; Mouradian, M.M. The role of oxidative stress in Parkinson’s disease. J. Parkinsons 2013, 3, 461–491. [Google Scholar] [CrossRef] [PubMed]
- Bosco, D.A.; Fowler, D.M.; Zhang, Q.; Nieva, J.; Powers, E.T.; Wentworth, P., Jr.; Lerner, R.A.; Kelly, J.W. Elevated levels of oxidized cholesterol metabolites in Lewy body disease brains accelerate alpha-synuclein fibrilization. Nat. Chem. Biol. 2006, 2, 249–253. [Google Scholar] [CrossRef]
- Nakabeppu, Y.; Tsuchimoto, D.; Yamaguchi, H.; Sakumi, K. Oxidative damage in nucleic acids and Parkinson’s disease. J. Neurosci. Res. 2007, 85, 919–934. [Google Scholar] [CrossRef]
- Zeevalk, G.D.; Razmpour, R.; Bernard, L.P. Glutathione and Parkinson’s disease: Is this the elephant in the room? Biomed. Pharmacother. 2008, 62, 236–249. [Google Scholar] [CrossRef]
- Puspita, L.; Chung, S.Y.; Shim, J.W. Oxidative stress and cellular pathologies in Parkinson’s disease. Mol. Brain. 2017, 10, 53. [Google Scholar] [CrossRef] [PubMed]
- Singh, A.; Kukreti, R.; Saso, S.; Kukreti, S. Oxidative Stress: A Key Modulator in Neurodegenerative Diseases. Molecules 2019, 24, 1583. [Google Scholar] [CrossRef] [PubMed]
- Polito, R.; Monda, V.; Nigro, E.; Messina, A.; Di Maio, G.; Giuliano, M.T.; Orrù, S.; Imperlini, E.; Calcagno, G.; Mosca, L.; et al. The Important Role of Adiponectin and Orexin-A, Two Key Proteins Improving Healthy Status: Focus on Physical Activity. Front. Physiol. 2020, 11, 356. [Google Scholar] [CrossRef]
- Polito, R.; Nigro, E.; Messina, A.; Monaco, M.L.; Monda, V.; Scudiero, O.; Cibelli, G.; Valenzano, A.; Picciocchi, E.; Zammit, C.; et al. Adiponectin and orexin-A as a potential immunity link between Adipose tissue and central nervous system. Front. Physiol. 2018, 9, 982. [Google Scholar] [CrossRef]
- Dong, X.S.; Ma, S.F.; Cao, C.W.; Li, J.; An, P.; Zhao, L.; Liu, N.Y.; Yan, H.; Hu, Q.T.; Mignot, E.; et al. Hypocretin (orexin) neuropeptide precursor gene, HCRT, polymorphisms in early-onset narcolepsy with cataplexy. Sleep Med. 2013, 14, 482–487. [Google Scholar] [CrossRef] [PubMed]
- Sperandeo, R.; Maldonato, M.N.; Messina, A.; Cozzolino, P.; Monda, M.; Cerroni, F.; Romano, P.; Salerno, M.; Maltese, A.; Roccella, M.; et al. Orexin system: Network multi-tasking Acta. Med. Mediterr. 2018, 34, 349–356. [Google Scholar]
- Chieffi, S.; Carotenuto, M.; Monda, V.; Valenzano, A.; Villano, I.; Precenzano, F.; Tafuri, D.; Salerno, M.; Filippi, N.; Nuccio, F.; et al. Orexin system: The key for a healthy life. Front. Neurol. 2017, 8, 357. [Google Scholar] [CrossRef] [PubMed]
- El-Bachá, R.S.; De-Lima-Filho, J.L.; Guedes, R.C. Dietary Antioxidant Deficiency Facilitates Cortical Spreading Depression Induced by Photoactivated Riboflavin. Nutr. Neurosci. 1998, 1, 205–212. [Google Scholar] [CrossRef] [PubMed]
- Oliveira, L.M.; Henrique, E.; Bustelli, I.B.; Netto, N.F.C.; Moreira, T.S.; Takakura, A.C.; Caetano, A.L. Depletion of hypothalamic hypocretin/orexin neurons correlates with impaired memory in a Parkinson’s disease animal model. Exp. Neurol. 2020, 323, 113110. [Google Scholar] [CrossRef]
- Mayo, M.C.; Deng, J.C.; Albores, J.; Zeidler, M.; Harper, R.M.; Avidan, A.Y. Hypocretin Deficiency Associated with Narcolepsy Type 1 and Central Hypoventilation Syndrome in Neurosarcoidosis of the Hypothalamus. J. Clin. Sleep Med. JCSM Off. Publ. Am. Acad. Sleep Med. 2015, 11, 1063–1065. [Google Scholar] [CrossRef] [PubMed]
- Mehr, J.B.; Mitchison, D.; Bowrey, H.E.; James, M.H. Sleep dysregulation in binge eating disorder and “food addiction”: The orexin (hypocretin) system as a potential neurobiological link. Neuropsychopharmacology 2021, 1–11. [Google Scholar] [CrossRef]
- Li, H.; Lu, J.; Li, S.; Huang, B.; Shi, G.; Mou, T.; Xu, Y. Increased Hypocretin (Orexin) Plasma Level in Depression, Bipolar Disorder Patients. Front. Psychiatry 2021, 31, 676336. [Google Scholar] [CrossRef]
- Sun, M.; Wang, W.; Li, Q.; Yuan, T.; Weng, W. Orexin A may suppress inflammatory response in fibroblast-like synoviocytes. Minghui Biomed. Pharmacother. 2018, 107, 763–768. [Google Scholar] [CrossRef]
- Zhan, S.; Che, P.; Zhao, X.; Li, N.; Ding, Y.; Liu, J.; Li, S.; Ding, K.; Han, L.; Huang, Z.; et al. The molecular mechanism of tumor necrosis factor alpha regulates the expression, sleep and behavior of hypocretin (orexin). J. Cell Mol. Med. 2019, 23, 6822–6834. [Google Scholar]
- Harada, S.; Fujita-Hamabe, W.; Tokuyama, S. Effect of orexin-A on post-ischemic glucose intolerance and neuronal damage. J. Pharmacol. Sci. 2011, 115, 155–163. [Google Scholar] [CrossRef] [PubMed]
- Couvineau, A.; Voisin, T.; Nicole, P.; Gratio, V.; Abad, C.; Tan, Y.V. Orexins as new therapeutic targets in inflammatory and neurodegenerative diseases. Front. Endocrinol. 2019, 10, 709. [Google Scholar] [CrossRef]
- Butterick, T.A.; Nixon, J.P.; Billington, C.J.; Kotz, C.M. Orexin A decreases lipid peroxidation and apoptosis in a novel hypothalamic cell model. Neurosci. Lett. 2012, 524, 30–34. [Google Scholar] [CrossRef] [PubMed]
- Duffy, C.M.; Nixon, J.P.; Butterick, T.A. Orexin A attenuates palmitic acid-induced hypothalamic cell death. Mol. Cell Neurosci. 2016, 7, 93–100. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; He, T.; Wan, B.; Wang, X.; Zhang, L. Orexin A ameliorates HBV X protein-induced cytotoxicity and inflammatory response in human hepatocytes. Artif. Cells Nanomed. Biotechnol. 2019, 47, 2003–2009. [Google Scholar] [CrossRef]
- Wang, C.M.; Yang, C.Q.; Cheng, B.H.; Chen, J.; Bai, B. Orexin-A protects SH-SY5Y cells from H2O2-induced oxidative damage via the PI3K/MEK1/2/ERK½. Int. J. Immunopathol. Pharm. 2018, 32, 2058738418785739. [Google Scholar] [CrossRef] [PubMed]
- Iloki-Assanga, S.B.; Lewis-Luján, L.M.; Fernández-Angulo, D.; Gil-Salido, A.A.; Lara-Espinoza, C.L.; Rubio-Pino, J.L. Bucida buceras retino-protective effect against H2O2-induced oxidative stress in the human retinal pigment epithelial cell line. BMC Complement. Altern. Med. 2015, 15, 254. [Google Scholar] [CrossRef]
- Bihamta, M.; Hosseini, A.; Ghorbani, A.; Boroushaki, M.T. Protective effect of pomegranate seed oil against oxidative stress induced by H2O2 in cardiomyocytes. Avicenna J. Phytomed. 2017, 7, 46–53. [Google Scholar]
- Hah, Y.S.; Lee, Y.R.; Jun, J.S.; Lim, H.S.; Kim, H.O.; Jeong, Y.G.; Hur, G.M.; Lee, S.Y.; Chung, M.J.; Park, J.W.; et al. A20 suppresses inflammatory responses and bone destruction in human fibroblast-like synoviocytes and in mice with collagen-induced arthritis. Arthritis Rheum. 2010, 62, 2313–2321. [Google Scholar] [CrossRef]
- Dickson, D.W.; Lee, S.C.; Mattiace, L.A.; Yen, S.H.; Brosnan, C. Microglia and cytokines in neurological disease, with special reference to AIDS and Alzheimer’s disease. Glia 1993, 7, 75. [Google Scholar] [CrossRef]
- Kettenmann, H.; Hanisch, U.K.; Noda, M.; Verkhratsky, A. Physiology of microglia. Physiol. Rev. 2011, 91, 461–553. [Google Scholar] [CrossRef] [PubMed]
- Kettenmann, H.; Kirchhoff, F.; Verkhratsky, A. Microglia: New roles for the synaptic stripper. Neuron 2013, 77, 10–18. [Google Scholar] [CrossRef]
- Soulet, D.; Rivest, S. Microglia. Curr. Biol. 2008, 18, 506–508. [Google Scholar] [CrossRef]
- Lee, J.Y.; Jhun, B.S.; Oh, Y.T.; Lee, J.H.; Choe, W.; Baik, H.H.; Ha, J.; Yoon, K.S.; Kim, S.S.; Kang, I. Activation of adenosine A3 receptor suppresses lipopolysaccharide-induced TNF-a production through inhibition of PI 3- kinase/Akt and NF-jB activation in murine BV2 microglial cells. Neurosci. Lett. 2006, 396, 1–6. [Google Scholar] [CrossRef]
- Cherry, J.D.; Olschowka, J.A.; O’Banion, M.K. Neuroinflammation and M2 microglia: The good, the bad, and the inflamed. J. Neuroinflammation 2014, 11, 98. [Google Scholar] [CrossRef]
- Nagy, E.E.; Frigy, A.; Szász, J.A.; Horváth, E. Neuroinflammation and microglia/macrophage phenotype modulate the molecular background of post-stroke depression: A literature review. Exp. Med. 2020, 20, 2510–2523. [Google Scholar] [CrossRef] [PubMed]
- Rutschman, R.; Lang, R.; Hesse, M.; Ihle, J.N.; Wynn, T.A.; Murray, P.J. Cutting edge: STAT6-dependent substrate depletion regulates nitric oxide production. J. Immunol. 2001, 166, 2173–2177. [Google Scholar] [CrossRef]
- Gordon, S. Alternative activation of macrophages. Nat. Rev. Immunol. 2003, 3, 23–35. [Google Scholar] [CrossRef]
- Lawrence, T.; Natoli, G. Transcriptional regulation of macrophage polarization: Enabling diversity with identity. Nat. Rev. Immunol. 2011, 11, 750–761. [Google Scholar] [CrossRef]
- Mills, C.D. M1and M2 macrophages: Oracles of health and disease. Crit. Rev. Immunol. 2012, 32, 463–488. [Google Scholar] [CrossRef] [PubMed]
- Wynn, T.A.; Chawla, A.; Pollard, J.W. Macrophage biology in development, homeostasis and disease. Nature 2013, 496, 445–455. [Google Scholar] [CrossRef] [PubMed]
- Gordon, S.; Martinez, F.O. Alternative activation of macrophages: Mechanism and functions. Immunity 2010, 32, 593–604. [Google Scholar] [CrossRef] [PubMed]
- Ortega-Gómez, A.; Perretti, M.; Soehnlein, O. Resolution of inflammation: An integrated view. EMBO Mol. Med. 2013, 5, 661–674. [Google Scholar] [CrossRef]
- Manich, G.; Recasens, M.; Valente, T.; Almolda, B.; González, B.; Castellano, B. Role of the CD200-CD200R Axis During Homeostasis and Neuroinflammation. Neuroscience 2019, 405, 118–136. [Google Scholar] [CrossRef]
- Wang, W.Y.; Tan, M.S.; Yu, J.; Tan, L. Role of proinflammatory cytokines released from microglia in Alzheimer’s disease. Ann. Transl. Med. 2015, 3, 136. [Google Scholar] [PubMed]
- Chen, W.W.; Zhang, X.; Huang, W.J. Role of neuroinflammation in neurodegenerative diseases. Mol. Med. Rep. 2016, 13, 3391–3396. [Google Scholar] [CrossRef] [PubMed]
- Aloisi, F. Immune function of microglia. Glia 2001, 36, 165–179. [Google Scholar] [CrossRef]
- Block, M.L.; Zecca, L.; Hong, J.S. Microglia-mediated neurotoxicity: Uncovering the molecular mechanisms. Nat. Rev. Neurosci. 2007, 8, 57–69. [Google Scholar] [CrossRef] [PubMed]
- Li, T.; Xu, W.; Ouyang, J.; Lu, X.; Sherchan, P.; Lenahan, C.; Irio, G.; Zhang, J.H.; Zhao, J.; Zhang, Y.; et al. Orexin A alleviates neuroinflammation via OXR2/CaMKKβ/AMPK signaling pathway after ICH in mice. J. Neuroinflammation 2020, 17, 1–15. [Google Scholar] [CrossRef] [PubMed]
- Sun, H.; He, X.; Tao, X.; Hou, T.; Chen, M.; He, M.; Liao, H. The CD200/CD200R signaling pathway contributes to spontaneous functional recovery by enhancing synaptic plasticity after stroke. J. Neuroinflammation 2020, 17, 1–15. [Google Scholar] [CrossRef]
- Wang, L.; Yu, C.C.; Liu, X.Y.; Deng, X.N.; Tian, Q.; Du, Y.J. Epigenetic Modulation of Microglia Function and Phenotypes in Neurodegenerative Diseases. Neural Plast. 2021, 2021, 9912686. [Google Scholar] [CrossRef]
- Yuan, L.B.; Dong, H.L.; Zhang, H.P.; Zhao, R.N.; Gong, G.; Chen, X.M.; Zhang, L.N.; Xiong, L. Neuroprotective Effect of Orexin-A Is Mediated by an Increase of Hypoxia-inducible Factor-1 Activity in Rat. Anesthesiology 2011, 114, 340–354. [Google Scholar] [CrossRef]
- Becquet, L.; Abad, C.; Leclercq, M.; Miel, C.; Jean, L.; Riou, G.; Couvineau, A.; Boyer, O.; Tan, Y.V. Systemic administration of orexin A ameliorates established experimental autoimmune encephalomyelitis by diminishing neuroinflammation. J. Neuroinflammation 2019, 16, 1–12. [Google Scholar] [CrossRef]
- Sokolowska, P.; Urbańska, A.; Biegańska, K.; Wagner, W.; Ciszewski, W.; Namiecińska, M.; Zawilska, J.B. Orexins protect neuronal cell cultures against hypoxic stress: An involvement of Akt signaling. J. Mol. Neurosci. 2014, 52, 48–55. [Google Scholar] [CrossRef]
- Synchikova, A.P.; Horiuchi, H.; Nabekura, J. The effect of orexin A application on the reaction of microglia cells body size stimulated by LPS injection. Med. Acad. J. 2019, 9, 232–233. [Google Scholar] [CrossRef]
- Xiong, X.; White, R.E.; Xu, L.; Yang, L.; Sun, X.; Zou, B.; Pascual, C.; Sakurai, T.; Giffard, R.C.; Xie, X.S. Mitigation of murine focal cerebral ischemia by the hypocretin/orexin system is associated with reduced inflammation. Stroke 2013, 44, 764–770. [Google Scholar] [CrossRef]
- Duffy, C.M.; Yuan, C.; Wisdorf, L.E.; Billington, C.J.; Kotz, C.M.; Nixon, J.P.; Butterick, T.A. Role of orexin A signaling in dietary palmitic acid-activated microglial cells. Neurosci. Lett. 2015, 606, 140–144. [Google Scholar] [CrossRef]
- Perry, V.H.; Holmes, C. Microglial priming in neurodegenerative disease. Nat. Rev. Neurol. 2014, 10, 217–224. [Google Scholar] [CrossRef] [PubMed]
- Xu, Y.; Xu, Y.; Wang, Y.; Wang, Y.; He, L.; Jiang, Z.; Huang, Z.; Liao, H.; Li, J.; Saavedra, J.M.; et al. Telmisartan prevention of LPS-induced microglia activation involves M2 microglia polarization via CaMKKβ-dependent AMPK activation. Brain Behav. Immun. 2015, 50, 298–313. [Google Scholar] [CrossRef] [PubMed]
- Zhou, X.; Cao, Y.; Ao, G.; Hu, L.; Liu, H.; Wu, J.; Wang, X.; Jin, M.; Zheng, S.; Zhen, X.; et al. CaMKKβ-dependent activation of AMP-activated protein kinase is critical to suppressive effects of hydrogen sulfide on neuroinflammation. Antioxid Redox Signal. 2014, 21, 1741–1758. [Google Scholar] [CrossRef] [PubMed]
- Wu, W.N.; Wu, P.F.; Zhou, J.; Guan, X.L.; Zhang, Z.; Yang, Y.J.; Long, L.H.; Xie, N.; Chen, J.G.; Wang, F. Orexin-A activates hypothalamic AMP-activated protein kinase signaling through a Ca2+-dependent mechanism involving voltage-gated L-type calcium channel. Mol. Pharmacol. 2013, 84, 876–887. [Google Scholar] [CrossRef] [PubMed]
- Wang, L.; Liu, Y.; Yan, S.; Du, T.; Fu, X.; Gong, X.; Zhou, X.; Zhang, T.; Wang, X. Disease Progression-Dependent Expression of CD200R1 and CX3CR1 in Mouse Models of Parkinson’s Disease. Aging Dis. 2020, 11, 254–268. [Google Scholar] [CrossRef] [PubMed]
- Miyazawa, T.; Burdeos, G.C.; Itaya, M.; Nakagawa, K.; Miyazawa, T. Vitamin E: Regulatory Redox Interactions. IUBMB Life 2019, 71, 430–441. [Google Scholar] [CrossRef] [PubMed]
- Mustacich, D.J.; Bruno, R.S.; Traber, M.G. Vitamin E. Vitam. Horm. 2007, 76, 1–21. [Google Scholar] [PubMed]
- Wu, J.H.; Croft, K.D. Vitamin E metabolism. Mol. Aspects Med. 2007, 28, 437–452. [Google Scholar] [CrossRef] [PubMed]
- Kamal-Eldin, A.; Appelqvist, L.A. The chemistry and antioxidant properties of tocopherols and tocotrienols. Lipids 1996, 31, 671–701. [Google Scholar] [CrossRef]
- Sen, C.K.; Khanna, S.; Roy, S. Tocotrienols: Vitamin E beyond tocopherols. Life Sci. 2006, 27, 2088–2098. [Google Scholar] [CrossRef] [PubMed]
- Floyd, R.A.; West, M.; Hensley, K. Oxidative biochemical markers: Clues to understanding aging in long-lived species. Exp. Gerontol. 2001, 36, 619–640. [Google Scholar] [CrossRef]
- Ambrogini, P.; Betti, M.; Galati, C.; Di Palma, M.; Lattanzi, D.; Savelli, D.; Galli, F.; Cuppini, R.; Minelli, A. Alpha-Tocopherol and Hippocampal Neural Plasticity in Physiological and Pathological Conditions. Int. J. Mol. Sci. 2016, 17, 2107. [Google Scholar] [CrossRef]
- Lohr, J.B.; Kuczenski, R.; Niculescu, A. Oxidative mechanisms and tardive dyskinesia. CNS Drugs 2003, 17, 47–62. [Google Scholar] [CrossRef] [PubMed]
- Altavilla, D.; Deodato, B.; Campo, G.M.; Arlotta, M.; Miano, M.; Squadrito, G.; Saitta, A.; Cucinotta, D.; Ceccarelli, S.; Ferlito, M.; et al. A novel dual vitamin E-like antioxidant, inhibits activation of nuclear factor-kappaB and reduces the inflammatory response in myo cardial ischemia-reperfusion injury. Cardiovasc. Res. 2000, 47, 515–528. [Google Scholar] [CrossRef]
- Behl, C. Vitamin E protects neurons against oxidative cell death in vitro more effectively than 17-beta estradiol and induces the activity of the transcription factor NF-kappaB. J. Neural. Transm. 2000, 107, 393–407. [Google Scholar] [CrossRef]
- Vatassery, G.T. Vitamin E and other endogenous antioxidants in the central nervous system. Geriatrics 1998, 53 (Suppl. S1), 25–27. [Google Scholar]
- Wolf, R.; Wolf, D.; Ruocco, V. Vitamin E: The radical protector. J. Eur. Acad. Derm. Venereol. 1998, 10, 103–117. [Google Scholar] [CrossRef]
- Martin, A.; Youdim, K.; Szprengiel, A. Roles of Vitamins E and C on Neurodegenerative Diseases and Cognitive Performance. Nutr. Rev. 2002, 60, 308–326. [Google Scholar] [CrossRef]
- Delanty, N.; Dichter, M.A. Antioxidant therapy in neurologic disease. Arch. Neurol. 2000, 57, 1265–1270. [Google Scholar] [CrossRef]
- Grundman, M. Vitamin E and Alzheimer disease: The basis for additional clinical trials. Am. J. Clin. Nutr. 2000, 71, 630–636. [Google Scholar] [CrossRef]
- Takahashi, T.; Nakaso, K.; Horikoshi, Y.; Hanaki, T.; Yamakawa, M.; Nakasone, M.; Kitagawa, Y.; Koike, T.; Matsura, T. Rice Bran Dietary Supplementation Improves Neurological Symptoms and Loss of Purkinje Cells in Vitamin E-Deficient Mice. Yonago Acta Med. 2016, 59, 188–195. [Google Scholar] [PubMed]
- Li, Y.; Liu, L.; Barger, S.W. Vitamin E Suppression of Microglial Activation Is Neuroprotective. J. Neurosci. Res. 2001, 66, 163–170. [Google Scholar] [CrossRef] [PubMed]
- Bialowas-McGoey, L.A.; Lesicka, A.; Whitaker-Azmitia, P.M. Vitamin E increases S100B-mediated microglial activation in an S100B-overexpressing mouse model of pathological aging. Glia 2008, 56, 1780–1790. [Google Scholar] [CrossRef] [PubMed]
- Barger, S.W.; Goodwin, M.E.; Porter, M.M.; Beggs, M.L. Glutamate release from activated microglia requires the oxidative burst and lipid peroxidation. J. Neurochem. 2007, 101, 1205–1213. [Google Scholar] [CrossRef] [PubMed]
- Annaházi, A.; Mracskó, E.; Süle, Z.; Karg, E.; Penke, B.; Bari, F.; Farkas, E. Pre-treatment and post-treatment with alpha-tocopherol attenuates hippocampal neuronal damage in experimental cerebral hypoperfusion. Eur. J. Pharmacol. 2007, 571, 120–128. [Google Scholar] [CrossRef]
- Stolzing, A.; Widmer, R.; Jung, T. Tocopherol-mediated modulation of age-related changes in microglial cells: Turnover of extracellular oxidized protein material. Free Radic. Biol. Med. 2006, 40, 2126–2135. [Google Scholar] [CrossRef]
- Godbout, J.P.; Berg, B.M.; Kelley, K.W. A-Tocopherol reduces lipopolysaccharide-induced peroxide radicalformation and interleukin-6 secretion in primary murine microglia and in brain. J. Neuroimmunol. 2004, 149, 101–109. [Google Scholar] [CrossRef] [PubMed]
- Sen, C.K.; Khanna, S.; Roy, S.; Packer, L. Molecular basis of vitamin E action. Tocotrienol potently inhibits glutamate-induced pp60(c-Src) kinase activation and death of HT4 neuronal cells. J. Biol. Chem. 2000, 275, 13049–13055. [Google Scholar] [CrossRef]
- Tan, S.W.; Ali, D.A.; Khaza’ai, H.; Wong, J.W.; Vidyadaran, S. Cellular uptake and anti-inflammatory effects of palm oil-derived delta (δ)- tocotrienol in microglia. Cell. Immunol. 2020, 357, 104–200. [Google Scholar] [CrossRef] [PubMed]
- Tan, S.W.; Ramasamy, R.; Abdullah, M. Inhibitory effects of palm a-, c- and d-tocotrienol on lipopolisaccaride- induced nitric oxide production in BV2 microglia. Cell Immunol. 2011, 271, 205–209. [Google Scholar] [CrossRef] [PubMed]
- Egger, T.; Schuligoi, R.; Wintersperger, A.; Amann, R.; Malle, E.; Sattler, W. Vitamin E (alpha-tocopherol) attenuates cyclo-oxygenase 2 transcription and synthesis in immortalized murine BV-2 microglia. Biochem. J. 2003, 370, 459–467. [Google Scholar] [CrossRef]
- Jiang, Q.; Elson-Schwab, I.; Courtemance, C.; Ames, B.N. Gammatocopherol and its major metabolite, in contrast to alpha-tocopherol, inhibit cyclooxygenase activity in macrophages and epithelial cells. Proc. Natl. Acad. Sci. USA 2000, 97, 11494–11499. [Google Scholar] [CrossRef]
- Behl, C. Vitamin E and other antioxidants in neuroprotection. Int. J. Vitam. Nutr. Res. 1999, 69, 213–219. [Google Scholar] [CrossRef]
- Goodman, Y.; Mattson, M.P. Secreted forms of β-amyloid precursor protein protect hippocampal neurons against amyloid β-peptide-induced oxidative injury. Exp. Neurol. 1994, 128, 1–12. [Google Scholar] [CrossRef] [PubMed]
- Halks-Miller, M.; Henderson, M.; Eng, L.F. α-Tocopherol decreases lipid peroxidation, neuronal necrosis, and reactive gliosis in reaggregate cultures of fetal rat brain. J. Neuropathol. Exp. Neurol. 1986, 45, 471–484. [Google Scholar] [CrossRef]
- The HOPE and HOPE-TOO Trial Investigators. Effects of long-term vitamin E supplementation on cardiovascular events and cancer: A randomised controlled trial. JAMA 2005, 293, 1338–1347. [Google Scholar] [CrossRef] [PubMed]
- Yadav, A.; Kumari, R.; Yadav, A.; Mishra, J.P.; Srivatva, S.; Prabha, S. Antioxidants and its functions in human body—A Review. Res. Environ. Life Sci. 2016, 9, 1328–1331. [Google Scholar]
- Heppner, F.L.; Roth, K.; Nitsch, R.; Hailer, N.P. Vitamin E induces ramification and downregulation of adhesion molecole in cultures microglial cells. Glia 1998, 22, 180–188. [Google Scholar] [CrossRef]
- Grundmann, M.; Grundman, M.; Delaney, P. Antioxidant strategies for Alzheimer’s disease. Proc. Nutr. Soc. 2002, 61, 191–202. [Google Scholar] [CrossRef]
- Azzi, A.; Ricciarelli, R.; Zingg, J.M. Non-antioxidant molecular functions of α-tocopherol (vitamin E). FEBS Lett. 2002, 519, 8–10. [Google Scholar] [CrossRef]
- Tasinato, A.; Boscoboinik, D.; Bartoli, G.M.; Maroni, P.; Azzi, A. d-Alpha-tocopherol inhibition of vascular smooth muscle cell proliferation occurs at physiological concentrations, correlates with protein kinase C inhibition, and is independent of its antioxidant properties. Proc. Natl. Acad. Sci. USA 1995, 92, 12190–12194. [Google Scholar] [CrossRef] [PubMed]
- Cachia, O.; Benna, J.E.; Pedruzzi, E.; Descomps, B.; Gougerot-Pocidalo, M.A.; Leger, C.L. Alpha-tocopherol inhibits the respiratory burst in human monocytes. Attenuation of p47(phox) membrane translocation and phosphorylation. J. Biol. Chem. 1998, 273, 32801–32805. [Google Scholar] [CrossRef]
- Kamat, J.P.; Devasagayam, T.P. Tocotrienols from palm oil as potent inhibitors of lipid peroxidation and protein oxidation in rat brain mitochondria. Neurosci. Lett. 1995, 11, 179–182. [Google Scholar] [CrossRef]
- Lively, S.; Schlichter, L.C. Microglia Responses to Pro-inflammatory Stimuli (LPS, IFNγ+TNFα) and Reprogramming by Resolving Cytokines (IL-4, IL-10). Front. Cell Neurosci. 2018, 12, 215. [Google Scholar] [CrossRef]
- Lee, G.Y.; Han, S.N. The Role of Vitamin E in Immunity. Nutrients 2018, 10, 1614. [Google Scholar] [CrossRef]
- Jiang, Q.; Lykkesfeldt, J.; Shigenaga, M.K.; Shigeno, E.T.; Christen, S.; Ames, B.N. Gamma-tocopherol supplementation inhibits protein nitration and ascorbate oxidation in rats with inflammation. Free Rad. Biol. Med. 2002, 33, 1534–1542. [Google Scholar] [CrossRef]
- Funk, C.D. Prostaglandins and leukotrienes: Advances in eicosanoid biology. Science 2001, 294, 1871–1875. [Google Scholar] [CrossRef] [PubMed]
- Wang, S.W.; Yang, S.G.; Liu, W.; Zhang, Y.X.; Xu, P.X.; Wang, T.; Ling, T.J.; Liu, R.T. Alpha-tocopherol quinine ameliorates spatial memory deficits by reducing beta-amyloid oligomers, neuroinflammation and oxidative stress in transgenic mice with Alzheimer’s disease. Behav. Brain Res. 2016, 296, 109. [Google Scholar] [CrossRef] [PubMed]
- De Rijk, M.C.; Breteler, M.M.; den Breeijen, J.H.; Launer, L.J.; Grobbee, D.E.; van der Meche, F.G. Dietary antioxidants and Parkinson disease. The Rotterdam study. Arch. Neurol. 1997, 54, 762–765. [Google Scholar] [CrossRef]
- Sano, M.; Ernesto, C.; Thomas, R.G.; Klauber, M.R.; Schafer, K.; Grundman, M.; Woodbury, P.; Growdon, J.; Cotman, C.W.; Pfeiffer, E.; et al. A controlled trial of selegiline, α-tocopherol, or both as treatment for Alzheimer’s disease. The Alzheimer’s disease cooperative study. N. Engl. J. Med. 1997, 336, 1216–1222. [Google Scholar] [CrossRef]
- Ascherio, A.; Weisskopf, M.G.; O’Reilly, E.J.; Jacobs, E.J.; McCullough, M.L.; Calle, E.E.; Cudkowicz, M.; Thun, M.J. Vitamin E intake and risk of amyotrophic lateral sclerosis. Ann. Neurol. 2005, 57, 104–110. [Google Scholar] [CrossRef] [PubMed]
- Bowry, V.; Stocker, R. Tocopherol-mediated peroxidation: The prooxidant effect of vitamin E on the radical-initiated effect oxidation of human low-density lipoprotein. J. Am. Chem. Soc. 1993, 115, 6029–6044. [Google Scholar] [CrossRef]
- Pearson, P.J.; Lewis, S.A.; Britton, J.; Fogarty, A. Vitamin E supplementation in the treatment of asthma: A randomised controlled trial. Thorax 2004, 59, 652–656. [Google Scholar] [CrossRef]
- Miller, E.R.; Pastor-Barriuso, R.; Dalal, D.; Riemersma, R.A.; Appel, L.J.; Guallar, E. Meta-analysis: High dose vitamin E supplementation may increase all-cause mortality. Ann. Intern. Med. 2005, 142, 1–11. [Google Scholar] [CrossRef]
- DeLong, J.; Prange, R.K.; Hodges, D.M.; Forney, C.F.; Bishop, M.C.; Quilliam, M. Using a modified ferrous-oxidationxyelnol orange (FOX) assay for detection of lipid hydrperoxides in plant tissue. J. Agric. Food Chem. 2002, 50, 248–254. [Google Scholar] [CrossRef]
- Balluz, L.; Kieszak, S.; Philen, R.M.; Mulinare, J. Vitamin and mineral supplement use in the United States. Arch. Fam. Med. 2000, 9, 258–262. [Google Scholar] [CrossRef]
- Tafazoli, S.; Wright, J.S.; O’Brien, P.J. Prooxidant and Antioxidant Activity of Vitamin E Analogues and Troglitazone. Chem. Res. Toxicol. 2005, 18, 1567–1574. [Google Scholar] [CrossRef] [PubMed]
- Institute of Science. Dietary Reference Intakes for Vitamin C, Vitamin E, Selenium and Carotenoids; National Academies Press: Washington, DC, USA, 2000. [Google Scholar]
- Masoudi, S.; Ploen, D.; Kunz, K.; Hildt, E. The adjuvant component α-tocopherol triggers the expression and turnover of hypocretin in vitro and its implications in the development of narcolepsy through the modulation of Nrf2. Vaccine 2014, 32, 2980–2988. [Google Scholar] [CrossRef]
- Moi, P.; Chan, K.; Asunis, I.; Cao, A.; Kan, Y.W. Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region. Proc. Natl. Acad. Sci. USA 1994, 91, 9926–9930. [Google Scholar] [CrossRef]
- Johnson, J.A.; Johnson, D.A.; Kraft, A.D.; Calkins, M.J.; Jakel, R.J.; Vargas, M.R.; Chen, P. The Nrf2-ARE pathway: An indicator and modulator of oxidative stress in neurodegeneration. Ann. N. Y. Acad. Sci. 2008, 1147, 61–69. [Google Scholar] [CrossRef] [PubMed]
- Masoudi, S.; Ploen, D.; Hildt, E. Is there an association between pandemic influenza H1N1 vaccination and the manifestation of narcolepsy? J. Vaccines Vaccin. 2015, 6, 3. [Google Scholar]
- Matsuki, K.; Grumet, F.C.; Lin, X.; Gelb, M.; Guilleminault, C.; Dement, W.C.; Mignot, E. DQ (rather than DR) gene marks susceptibility to narcolepsy. Lancet 1992, 339, 1052. [Google Scholar] [CrossRef]
- Nishino, S.; Mignot, E. Pharmacological aspects of human and canine narcolepsy. Prog. Neurobiol. 1997, 52, 27–78. [Google Scholar] [CrossRef]
- Nishino, S.; Okuro, M.; Kotorii, N.; Anegawa, E.; Ishimaru, Y.; Matsumura, M.; Kanbayashi, T. Hypocretin/orexin and narcolepsy: New basic and clinical insights. Acta Physiol. 2010, 198, 209–222. [Google Scholar] [CrossRef] [PubMed]
- Mahlios, J.; De la Herrán-Arita, A.K.; Mignot, E. The autoimmune basis of narcolepsy. Curr. Opin. Neurobiol. 2013, 23, 767–773. [Google Scholar] [CrossRef] [PubMed]
- De la Herrán-Arita, A.K.; García-García, F. Narcolepsy as an immune-mediated disease. Sleep Disord. 2014, 2014, 792687. [Google Scholar] [CrossRef] [PubMed]
- LAKEMEDELSVERKET. Available online: http://www.lakemedelsverket.se/upload/nyheter/2011/Fallinventeringsrport_pandermrix_110630.pdf (accessed on 20 July 2021).
- Sessa, F.; Maglietta, F.; Bertozzi, G.; Salerno, M.; Di Mizio, G.; Messina, G.; Montana, A.; Ricci, P.; Pomara, C. Human brain injury and mirnas: An experimental study. Int. J. Mol. Sci. 2019, 20, 1546. [Google Scholar] [CrossRef] [PubMed]
Type of Vitamin E | Biological Activity | Study Model | References |
---|---|---|---|
α-tocopherol | Reduces astrocytosis and microglia activation | Cell rat hippocampus | Ambrogini et al. [86] |
α-tocopherol | Inhibits Microglia Activation | Pheochromocytoma cell line: PC12 cells | Li et al. [96] |
α-tocopheryl acetate | Increases microglial activation and RAGE expression | Astroglial cell of mice | Bialowas-McGoey et al. 2008 [97] |
α-tocopherol | Blocks glutamate release | Sprague Dawley rats | Barger et al. 2007 [98] |
α-tocopherol | Attenuates expression of COX-2 and the production of proinflammatory cytokines | Cell rat hippocampus | Annàhazi et al. 2007 [99] |
α-tocopherol | Reduces proinflammatory cytokines and production of ROS | Primary glial cultures | Stolzing et al. [100] |
α-tocopherol | Decreases lipid peroxidation and IL-6 secretion | BALB/c mice | Godbout et al., 2004 [101] |
Tocotrienols | Prevents death of HT4 cells treated with glutamate | HT4 hippocampal neuronal cells | Sen et al., 2000 [102] |
δ-tocotrienol | Reduces NO production and IL-1β expression, inhibits PGE2 expression | BV2 microglia cells | Tan et al., 2020 [103] |
α-, γ- and δ-tocotrienol | Reduce NO release | BV2 microglia cells | Tan et al., 2011 [104] |
α-tocopherol | Attenuates COX-2 protein synthesis | BV2 microglia cells | Egger et al. [105] |
γ-Tocopherol | Inhibits cyclooxygenase activity and nitrite accumulation | Murine RAW264.7 macrophages | Jiang Q et al., 2000 [106] |
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La Torre, M.E.; Villano, I.; Monda, M.; Messina, A.; Cibelli, G.; Valenzano, A.; Pisanelli, D.; Panaro, M.A.; Tartaglia, N.; Ambrosi, A.; et al. Role of Vitamin E and the Orexin System in Neuroprotection. Brain Sci. 2021, 11, 1098. https://doi.org/10.3390/brainsci11081098
La Torre ME, Villano I, Monda M, Messina A, Cibelli G, Valenzano A, Pisanelli D, Panaro MA, Tartaglia N, Ambrosi A, et al. Role of Vitamin E and the Orexin System in Neuroprotection. Brain Sciences. 2021; 11(8):1098. https://doi.org/10.3390/brainsci11081098
Chicago/Turabian StyleLa Torre, Maria Ester, Ines Villano, Marcellino Monda, Antonietta Messina, Giuseppe Cibelli, Anna Valenzano, Daniela Pisanelli, Maria Antonietta Panaro, Nicola Tartaglia, Antonio Ambrosi, and et al. 2021. "Role of Vitamin E and the Orexin System in Neuroprotection" Brain Sciences 11, no. 8: 1098. https://doi.org/10.3390/brainsci11081098