Redox Control of the Dormant Cancer Cell Life Cycle
Abstract
:1. Introduction
2. Dormancy Entrance in Redox Perspective
2.1. Balance between Dormancy and Proliferation
2.2. Reforming the Related Microenvironment
3. Redox-Mediated Long-Term Dormancy
3.1. Redox Sustaining Cancer Cell Quiescence
3.2. Redox Managing Dormant Microenvironment
4. Redox Mechanisms Control the Metastatic Relapse of Dormant Cancer Cells
4.1. Redox Regulates Metabolism-Related Reactivation of Dormant Cancer Cells
4.2. Redox Related Cell-Extrinsic Environmental Changes
5. Targeting Dormant Cancer Cell Life Cycle by the Redox-Mediated Mechanism
5.1. Sleep or Reactivation in Dormant Cancer Cells
5.2. Killing Dormant Cancer Cells in a Redox Way
6. Conclusions
Author Contributions
Funding
Institutional Review Board Statement
Informed Consent Statement
Data Availability Statement
Conflicts of Interest
References
- Siegel, R.L.; Miller, K.D.; Fuchs, H.E.; Jemal, A. Cancer Statistics, 2021. CA Cancer J. Clin. 2021, 71, 7–33. [Google Scholar] [CrossRef]
- Sung, H.; Ferlay, J.; Siegel, R.L.; Laversanne, M.; Soerjomataram, I.; Jemal, A.; Bray, F. Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J. Clin. 2021, 71, 209–249. [Google Scholar] [CrossRef]
- Tian, H.; Zhang, J.; Zhang, H.; Jiang, Y.; Song, A.; Luan, Y. Low side-effect and heat-shock protein-inhibited chemo-phototherapy nanoplatform via co-assembling strategy of biotin-tailored IR780 and quercetin. Chem. Eng. J. 2020, 382, 123043. [Google Scholar] [CrossRef]
- Tian, H.; Zhao, S.; Nice, E.C.; Huang, C.; He, W.; Zou, B.; Lin, J. A cascaded copper-based nanocatalyst by modulating glutathione and cyclooxygenase-2 for hepatocellular carcinoma therapy. J. Colloid. Interf. Sci. 2021, 607, 1516–1526. [Google Scholar] [CrossRef]
- Marx, V. How to pull the blanket off dormant cancer cells. Nat. Methods 2018, 15, 249–252. [Google Scholar] [CrossRef]
- Aguirre-Ghiso, J.A. How dormant cancer persists and reawakens. Science 2018, 361, 1314–1315. [Google Scholar] [CrossRef] [PubMed]
- Nicolini, A.; Rossi, G.; Ferrari, P.; Carpi, A. Minimal residual disease in advanced or metastatic solid cancers: The G0-G1 state and immunotherapy are key to unwinding cancer complexity. Semin. Cancer Biol. 2020. [Google Scholar] [CrossRef] [PubMed]
- Hosseini, H.; Obradović, M.M.S.; Hoffmann, M.; Harper, K.L.; Sosa, M.S.; Werner-Klein, M.; Nanduri, L.K.; Werno, C.; Ehrl, C.; Maneck, M.; et al. Early dissemination seeds metastasis in breast cancer. Nature 2016, 540, 552–558. [Google Scholar] [CrossRef] [Green Version]
- Goddard, E.T.; Bozic, I.; Riddell, S.R.; Ghajar, C.M. Dormant tumour cells, their niches and the influence of immunity. Nat. Cell Biol. 2018, 20, 1240–1249. [Google Scholar] [CrossRef]
- Hu, Z.; Ding, J.; Ma, Z.; Sun, R.; Seoane, J.A.; Scott Shaffer, J.; Suarez, C.J.; Berghoff, A.S.; Cremolini, C.; Falcone, A.; et al. Quantitative evidence for early metastatic seeding in colorectal cancer. Nat. Genet. 2019, 51, 1113–1122. [Google Scholar] [CrossRef] [PubMed]
- Dobson, S.M.; García-Prat, L.; Vanner, R.J.; Wintersinger, J.; Waanders, E.; Gu, Z.; McLeod, J.; Gan, O.I.; Grandal, I.; Payne-Turner, D.; et al. Relapse-Fated Latent Diagnosis Subclones in Acute B Lineage Leukemia Are Drug Tolerant and Possess Distinct Metabolic Programs. Cancer Discov. 2020, 10, 568–587. [Google Scholar] [CrossRef] [Green Version]
- Pan, H.; Gray, R.; Braybrooke, J.; Davies, C.; Taylor, C.; McGale, P.; Peto, R.; Pritchard, K.I.; Bergh, J.; Dowsett, M.; et al. 20-Year Risks of Breast-Cancer Recurrence after Stopping Endocrine Therapy at 5 Years. N. Engl. J. Med. 2017, 377, 1836–1846. [Google Scholar] [CrossRef] [Green Version]
- Senft, D.; Ronai, Z.E. Adaptive Stress Responses During Tumor Metastasis and Dormancy. Trends Cancer 2016, 2, 429–442. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Mahvi, D.A.; Liu, R.; Grinstaff, M.W.; Colson, Y.L.; Raut, C.P. Local Cancer Recurrence: The Realities, Challenges, and Opportunities for New Therapies. CA Cancer J. Clin. 2018, 68, 488–505. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Vallette, F.M.; Olivier, C.; Lézot, F.; Oliver, L.; Cochonneau, D.; Lalier, L.; Cartron, P.F.; Heymann, D. Dormant, quiescent, tolerant and persister cells: Four synonyms for the same target in cancer. Biochem. Pharmacol. 2019, 162, 169–176. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Li, B.; Jiang, J.; Assaraf, Y.G.; Xiao, H.; Chen, Z.S.; Huang, C. Surmounting cancer drug resistance: New insights from the perspective of N(6)-methyladenosine RNA modification. Drug Resist. Updates 2020, 53, 100720. [Google Scholar] [CrossRef] [PubMed]
- Hen, O.; Barkan, D. Dormant disseminated tumor cells and cancer stem/progenitor-like cells: Similarities and opportunities. Semin. Cancer Biol. 2020, 60, 157–165. [Google Scholar] [CrossRef] [PubMed]
- Ferrer, A.I.; Trinidad, J.R.; Sandiford, O.; Etchegaray, J.P.; Rameshwar, P. Epigenetic dynamics in cancer stem cell dormancy. Cancer Metastasis Rev. 2020, 39, 721–738. [Google Scholar] [CrossRef]
- Phan, T.G.; Croucher, P.I. The dormant cancer cell life cycle. Nat. Rev. Cancer 2020, 20, 398–411. [Google Scholar] [CrossRef]
- Hayes, J.D.; Dinkova-Kostova, A.T.; Tew, K.D. Oxidative Stress in Cancer. Cancer Cell 2020, 38, 167–197. [Google Scholar] [CrossRef]
- Harris, I.S.; DeNicola, G.M. The Complex Interplay between Antioxidants and ROS in Cancer. Trends Cell Biol. 2020, 30, 440–451. [Google Scholar] [CrossRef] [PubMed]
- Yamamoto, M.; Kensler, T.W.; Motohashi, H. The KEAP1-NRF2 System: A Thiol-Based Sensor-Effector Apparatus for Maintaining Redox Homeostasis. Physiol. Rev. 2018, 98, 1169–1203. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Srinivas, U.S.; Tan, B.W.Q.; Vellayappan, B.A.; Jeyasekharan, A.D. ROS and the DNA damage response in cancer. Redox Biol. 2019, 25, 101084. [Google Scholar] [CrossRef] [PubMed]
- Moloney, J.N.; Cotter, T.G. ROS signalling in the biology of cancer. Semin. Cell Dev. Biol. 2018, 80, 50–64. [Google Scholar] [CrossRef] [PubMed]
- Paulsen, C.E.; Carroll, K.S. Cysteine-mediated redox signaling: Chemistry, biology, and tools for discovery. Chem. Rev. 2013, 113, 4633–4679. [Google Scholar] [CrossRef] [PubMed]
- Alcock, L.J.; Perkins, M.V.; Chalker, J.M. Chemical methods for mapping cysteine oxidation. Chem. Soc. Rev. 2018, 47, 231–268. [Google Scholar] [CrossRef] [Green Version]
- Forman, H.J.; Zhang, H. Targeting oxidative stress in disease: Promise and limitations of antioxidant therapy. Nat. Rev. Drug Discov. 2021, 20, 689–709. [Google Scholar] [CrossRef]
- Hegedűs, C.; Kovács, K.; Polgár, Z.; Regdon, Z.; Szabó, É.; Robaszkiewicz, A.; Forman, H.J.; Martner, A.; Virág, L. Redox control of cancer cell destruction. Redox Biol. 2018, 16, 59–74. [Google Scholar] [CrossRef]
- Vaccaro, A.; Kaplan Dor, Y.; Nambara, K.; Pollina, E.A.; Lin, C.; Greenberg, M.E.; Rogulja, D. Sleep Loss Can Cause Death through Accumulation of Reactive Oxygen Species in the Gut. Cell 2020, 181, 1307–1328.e1315. [Google Scholar] [CrossRef]
- Huang, H.; Zhang, S.; Li, Y.; Liu, Z.; Mi, L.; Cai, Y.; Wang, X.; Chen, L.; Ran, H.; Xiao, D.; et al. Suppression of mitochondrial ROS by prohibitin drives glioblastoma progression and therapeutic resistance. Nat. Commun. 2021, 12, 3720. [Google Scholar] [CrossRef]
- de la Vega, M.R.; Chapman, E.; Zhang, D.D. NRF2 and the Hallmarks of Cancer. Cancer Cell 2018, 34, 21–43. [Google Scholar] [CrossRef]
- Fox, D.B.; Garcia, N.M.G.; McKinney, B.J.; Lupo, R.; Noteware, L.C.; Newcomb, R.; Liu, J.; Locasale, J.W.; Hirschey, M.D.; Alvarez, J.V. NRF2 activation promotes the recurrence of dormant tumour cells through regulation of redox and nucleotide metabolism. Nat. Metab. 2020, 2, 318–334. [Google Scholar] [CrossRef] [PubMed]
- Ghajar, C.M. Metastasis prevention by targeting the dormant niche. Nat. Rev. Cancer 2015, 15, 238–247. [Google Scholar] [CrossRef]
- Price, T.T.; Burness, M.L.; Sivan, A.; Warner, M.J.; Cheng, R.; Lee, C.H.; Olivere, L.; Comatas, K.; Magnani, J.; Kim Lyerly, H.; et al. Dormant breast cancer micrometastases reside in specific bone marrow niches that regulate their transit to and from bone. Sci. Transl. Med. 2016, 8, 340ra373. [Google Scholar] [CrossRef]
- Yates, L.R.; Knappskog, S.; Wedge, D.; Farmery, J.H.R.; Gonzalez, S.; Martincorena, I.; Alexandrov, L.B.; Van Loo, P.; Haugland, H.K.; Lilleng, P.K.; et al. Genomic Evolution of Breast Cancer Metastasis and Relapse. Cancer Cell 2017, 32, 169–184.e167. [Google Scholar] [CrossRef] [Green Version]
- Ming, H.; Li, B.; Zhou, L.; Goel, A.; Huang, C. Long non-coding RNAs and cancer metastasis: Molecular basis and therapeutic implications. Biochim. Biophys. Acta Rev. Cancer 2021, 1875, 188519. [Google Scholar] [CrossRef]
- Lu, Z.; Zou, J.; Li, S.; Topper, M.J.; Tao, Y.; Zhang, H.; Jiao, X.; Xie, W.; Kong, X.; Vaz, M.; et al. Epigenetic therapy inhibits metastases by disrupting premetastatic niches. Nature 2020, 579, 284–290. [Google Scholar] [CrossRef] [PubMed]
- Sosa, M.S.; Avivar-Valderas, A.; Bragado, P.; Wen, H.C.; Aguirre-Ghiso, J.A. ERK1/2 and p38α/β signaling in tumor cell quiescence: Opportunities to control dormant residual disease. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2011, 17, 5850–5857. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Kim, J.E.; Roh, E.; Lee, M.H.; Yu, D.H.; Kim, D.J.; Lim, T.G.; Jung, S.K.; Peng, C.; Cho, Y.Y.; Dickinson, S.; et al. Fyn is a redox sensor involved in solar ultraviolet light-induced signal transduction in skin carcinogenesis. Oncogene 2016, 35, 4091–4101. [Google Scholar] [CrossRef] [Green Version]
- Meng, J.; Fu, L.; Liu, K.; Tian, C.; Wu, Z.; Jung, Y.; Ferreira, R.B.; Carroll, K.S.; Blackwell, T.K.; Yang, J. Global profiling of distinct cysteine redox forms reveals wide-ranging redox regulation in C. elegans. Nat. Commun. 2021, 12, 1415. [Google Scholar] [CrossRef]
- Bassi, R.; Burgoyne, J.R.; DeNicola, G.F.; Rudyk, O.; DeSantis, V.; Charles, R.L.; Eaton, P.; Marber, M.S. Redox-dependent dimerization of p38α mitogen-activated protein kinase with mitogen-activated protein kinase kinase 3. J. Biol. Chem. 2017, 292, 16161–16173. [Google Scholar] [CrossRef] [Green Version]
- Lee, J.; Song, C.H. Effect of Reactive Oxygen Species on the Endoplasmic Reticulum and Mitochondria during Intracellular Pathogen Infection of Mammalian Cells. Antioxidants 2021, 10, 872. [Google Scholar] [CrossRef] [PubMed]
- Kim, H.S.; Kim, Y.; Lim, M.J.; Park, Y.G.; Park, S.I.; Sohn, J. The p38-activated ER stress-ATF6α axis mediates cellular senescence. FASEB J. 2019, 33, 2422–2434. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Hetz, C.; Zhang, K.; Kaufman, R.J. Mechanisms, regulation and functions of the unfolded protein response. Nat. Rev. Mol. Cell Biol. 2020, 21, 421–438. [Google Scholar] [CrossRef] [PubMed]
- Chen, X.; Cubillos-Ruiz, J.R. Endoplasmic reticulum stress signals in the tumour and its microenvironment. Nat. Rev. Cancer 2021, 21, 71–88. [Google Scholar] [CrossRef] [PubMed]
- Wei, P.C.; Hsieh, Y.H.; Su, M.I.; Jiang, X.; Hsu, P.H.; Lo, W.T.; Weng, J.Y.; Jeng, Y.M.; Wang, J.M.; Chen, P.L.; et al. Loss of the oxidative stress sensor NPGPx compromises GRP78 chaperone activity and induces systemic disease. Mol. Cell 2012, 48, 747–759. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lee, D.; Hokinson, D.; Park, S.; Elvira, R.; Kusuma, F.; Lee, J.M.; Yun, M.; Lee, S.G.; Han, J. ER Stress Induces Cell Cycle Arrest at the G2/M Phase Through eIF2α Phosphorylation and GADD45α. Int. J. Mol. Sci. 2019, 20, 6309. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Zhang, Z.; Zhang, L.; Zhou, L.; Lei, Y.; Zhang, Y.; Huang, C. Redox signaling and unfolded protein response coordinate cell fate decisions under ER stress. Redox Biol. 2019, 25, 101047. [Google Scholar] [CrossRef]
- Sosa, M.S.; Parikh, F.; Maia, A.G.; Estrada, Y.; Bosch, A.; Bragado, P.; Ekpin, E.; George, A.; Zheng, Y.; Lam, H.M.; et al. NR2F1 controls tumour cell dormancy via SOX9- and RARβ-driven quiescence programmes. Nat. Commun. 2015, 6, 6170. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Engeland, K. Cell cycle arrest through indirect transcriptional repression by p53: I have a DREAM. Cell Death Differ. 2018, 25, 114–132. [Google Scholar] [CrossRef] [Green Version]
- Laplane, L.; Duluc, D.; Larmonier, N.; Pradeu, T.; Bikfalvi, A. The Multiple Layers of the Tumor Environment. Trends Cancer 2018, 4, 802–809. [Google Scholar] [CrossRef]
- Wu, P.; Gao, W.; Su, M.; Nice, E.C.; Zhang, W.; Lin, J.; Xie, N. Adaptive Mechanisms of Tumor Therapy Resistance Driven by Tumor Microenvironment. Front. Cell Dev. Biol. 2021, 9, 357. [Google Scholar] [CrossRef]
- Butturini, E.; Carcereri de Prati, A.; Boriero, D.; Mariotto, S. Tumor Dormancy and Interplay with Hypoxic Tumor Microenvironment. Int. J. Mol. Sci. 2019, 20, 4305. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ferrer, A.; Roser, C.T.; El-Far, M.H.; Savanur, V.H.; Eljarrah, A.; Gergues, M.; Kra, J.A.; Etchegaray, J.P.; Rameshwar, P. Hypoxia-mediated changes in bone marrow microenvironment in breast cancer dormancy. Cancer Lett. 2020, 488, 9–17. [Google Scholar] [CrossRef]
- Lee, H.R.; Leslie, F.; Azarin, S.M. A facile in vitro platform to study cancer cell dormancy under hypoxic microenvironments using CoCl(2). J. Biol. Eng. 2018, 12, 12. [Google Scholar] [CrossRef] [PubMed]
- Li, A.; Zhang, Y.; Wang, Z.; Dong, H.; Fu, N.; Han, X. The roles and signaling pathways of prolyl-4-hydroxylase 2 in the tumor microenvironment. Chem. Biol. Interact. 2019, 303, 40–49. [Google Scholar] [CrossRef] [PubMed]
- Chen, T.; Ren, Z.; Ye, L.C.; Zhou, P.H.; Xu, J.M.; Shi, Q.; Yao, L.Q.; Zhong, Y.S. Factor inhibiting HIF1α (FIH-1) functions as a tumor suppressor in human colorectal cancer by repressing HIF1α pathway. Cancer Biol. Ther. 2015, 16, 244–252. [Google Scholar] [CrossRef] [Green Version]
- Ju, S.; Wang, F.; Wang, Y.; Ju, S. CSN8 is a key regulator in hypoxia-induced epithelial-mesenchymal transition and dormancy of colorectal cancer cells. Mol. Cancer 2020, 19, 168. [Google Scholar] [CrossRef]
- Prunier, C.; Baker, D.; Ten Dijke, P.; Ritsma, L. TGF-β Family Signaling Pathways in Cellular Dormancy. Trends Cancer 2019, 5, 66–78. [Google Scholar] [CrossRef]
- Barkan, D.; Chambers, A.F. β1-integrin: A potential therapeutic target in the battle against cancer recurrence. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2011, 17, 7219–7223. [Google Scholar] [CrossRef] [Green Version]
- Eble, J.A.; de Rezende, F.F. Redox-relevant aspects of the extracellular matrix and its cellular contacts via integrins. Antioxid Redox Signal. 2014, 20, 1977–1993. [Google Scholar] [CrossRef] [Green Version]
- Rosenberg, N.; Mor-Cohen, R.; Sheptovitsky, V.H.; Romanenco, O.; Hess, O.; Lahav, J. Integrin-mediated cell adhesion requires extracellular disulfide exchange regulated by protein disulfide isomerase. Exp. Cell Res. 2019, 381, 77–85. [Google Scholar] [CrossRef]
- Yeh, A.C.; Ramaswamy, S. Mechanisms of Cancer Cell Dormancy--Another Hallmark of Cancer? Cancer Res. 2015, 75, 5014–5022. [Google Scholar] [CrossRef] [Green Version]
- Kechagia, J.; Ivaska, J.; Roca-Cusachs, P. Integrins as biomechanical sensors of the microenvironment. Nat. Rev. Mol. Cell Biol. 2019, 20, 457–473. [Google Scholar] [CrossRef] [PubMed]
- Bui, A.T.; Laurent, F.; Havard, M.; Dautry, F.; Tchénio, T. SMAD signaling and redox imbalance cooperate to induce prostate cancer cell dormancy. Cell Cycle 2015, 14, 1218–1231. [Google Scholar] [CrossRef] [Green Version]
- Zhang, D.; Jin, W.; Wu, R.; Li, J.; Park, S.A.; Tu, E.; Zanvit, P.; Xu, J.; Liu, O.; Cain, A.; et al. High Glucose Intake Exacerbates Autoimmunity through Reactive-Oxygen-Species-Mediated TGF-β Cytokine Activation. Immunity 2019, 51, 671–681.e675. [Google Scholar] [CrossRef]
- van Caam, A.; Madej, W.; de Vinuesa, A.G.; Goumans, M.J.; Dijke, P.T.; Davidson, E.B.; van der Kraan, P. TGFβ1-induced SMAD2/3 and SMAD1/5 phosphorylation are both ALK5-kinase-dependent in primary chondrocytes and mediated by TAK1 kinase activity. Arthritis Res. Ther. 2017, 19, 112. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Jiang, F.; Liu, G.S.; Dusting, G.J.; Chan, E.C. NADPH oxidase-dependent redox signaling in TGF-β-mediated fibrotic responses. Redox Biol. 2014, 2, 267–272. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Takahashi, N.; Cho, P.; Selfors, L.M.; Kuiken, H.J.; Kaul, R.; Fujiwara, T.; Harris, I.S.; Zhang, T.; Gygi, S.P.; Brugge, J.S. 3D Culture Models with CRISPR Screens Reveal Hyperactive NRF2 as a Prerequisite for Spheroid Formation via Regulation of Proliferation and Ferroptosis. Mol. Cell 2020, 80, 828–844.e826. [Google Scholar] [CrossRef]
- Bragado, P.; Estrada, Y.; Parikh, F.; Krause, S.; Capobianco, C.; Farina, H.G.; Schewe, D.M.; Aguirre-Ghiso, J.A. TGF-β2 dictates disseminated tumour cell fate in target organs through TGF-β-RIII and p38α/β signalling. Nat. Cell Biol. 2013, 15, 1351–1361. [Google Scholar] [CrossRef] [Green Version]
- Yu-Lee, L.Y.; Yu, G.; Lee, Y.C.; Lin, S.C.; Pan, J.; Pan, T.; Yu, K.J.; Liu, B.; Creighton, C.J.; Rodriguez-Canales, J.; et al. Osteoblast-Secreted Factors Mediate Dormancy of Metastatic Prostate Cancer in the Bone via Activation of the TGFβRIII-p38MAPK-pS249/T252RB Pathway. Cancer Res. 2018, 78, 2911–2924. [Google Scholar] [CrossRef] [Green Version]
- Ghajar, C.M.; Peinado, H.; Mori, H.; Matei, I.R.; Evason, K.J.; Brazier, H.; Almeida, D.; Koller, A.; Hajjar, K.A.; Stainier, D.Y.; et al. The perivascular niche regulates breast tumour dormancy. Nat. Cell Biol. 2013, 15, 807–817. [Google Scholar] [CrossRef]
- van Velthoven, C.T.J.; Rando, T.A. Stem Cell Quiescence: Dynamism, Restraint, and Cellular Idling. Cell Stem Cell 2019, 24, 213–225. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martin, V.; Turos-Cabal, M.; Sanchez-Sanchez, A.M.; Rodríguez, C. Metabolism-Redox Interplay in Tumor Stem Cell Signaling. In Handbook of Oxidative Stress in Cancer: Mechanistic Aspects; Springer: Berlin/Heidelberg, Germany, 2020; pp. 1–22. [Google Scholar]
- Ma, X.; Su, P.; Yin, C.; Lin, X.; Wang, X.; Gao, Y.; Patil, S.; War, A.R.; Qadir, A.; Tian, Y.; et al. The Roles of FoxO Transcription Factors in Regulation of Bone Cells Function. Int. J. Mol. Sci. 2020, 21, 692. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Eijkelenboom, A.; Burgering, B.M. FOXOs: Signalling integrators for homeostasis maintenance. Nat. Rev. Mol. Cell Biol. 2013, 14, 83–97. [Google Scholar] [CrossRef] [PubMed]
- Fu, X.; Zhu, X.; Qin, F.; Zhang, Y.; Lin, J.; Ding, Y.; Yang, Z.; Shang, Y.; Wang, L.; Zhang, Q.; et al. Linc00210 drives Wnt/β-catenin signaling activation and liver tumor progression through CTNNBIP1-dependent manner. Mol. Cancer 2018, 17, 73. [Google Scholar] [CrossRef] [Green Version]
- Collins, S.J.; Tumpach, C.; Groveman, B.R.; Drew, S.C.; Haigh, C.L. Prion protein cleavage fragments regulate adult neural stem cell quiescence through redox modulation of mitochondrial fission and SOD2 expression. Cell. Mol. Life Sci. 2018, 75, 3231–3249. [Google Scholar] [CrossRef] [Green Version]
- Tao, J.; Krutsenko, Y.; Moghe, A.; Singh, S.; Poddar, M.; Bell, A.; Oertel, M.; Singhi, A.D.; Geller, D.; Chen, X.; et al. Nuclear factor erythroid 2-related factor 2 and β-Catenin Coactivation in Hepatocellular Cancer: Biological and Therapeutic Implications. Hepatology 2021, 74, 741–759. [Google Scholar] [CrossRef]
- Wakabayashi, N.; Chartoumpekis, D.V.; Kensler, T.W. Crosstalk between Nrf2 and Notch signaling. Free. Radic. Biol. Med. 2015, 88, 158–167. [Google Scholar] [CrossRef] [Green Version]
- Kim, J.H.; Thimmulappa, R.K.; Kumar, V.; Cui, W.; Kumar, S.; Kombairaju, P.; Zhang, H.; Margolick, J.; Matsui, W.; Macvittie, T.; et al. NRF2-mediated Notch pathway activation enhances hematopoietic reconstitution following myelosuppressive radiation. J. Clin. Investig. 2014, 124, 730–741. [Google Scholar] [CrossRef] [Green Version]
- Leung, H.W.; Lau, E.Y.T.; Leung, C.O.N.; Lei, M.M.L.; Mok, E.H.K.; Ma, V.W.S.; Cho, W.C.S.; Ng, I.O.L.; Yun, J.P.; Cai, S.H.; et al. NRF2/SHH signaling cascade promotes tumor-initiating cell lineage and drug resistance in hepatocellular carcinoma. Cancer Lett. 2020, 476, 48–56. [Google Scholar] [CrossRef]
- Ren, D.; Dai, Y.; Yang, Q.; Zhang, X.; Guo, W.; Ye, L.; Huang, S.; Chen, X.; Lai, Y.; Du, H.; et al. Wnt5a induces and maintains prostate cancer cells dormancy in bone. J. Exp. Med. 2019, 216, 428–449. [Google Scholar] [CrossRef] [PubMed]
- Popova, S.A.; Buczacki, S.J.A. Itraconazole perturbs colorectal cancer dormancy through SUFU-mediated WNT inhibition. Mol. Cell. Oncol. 2018, 5, e1494950. [Google Scholar] [CrossRef] [Green Version]
- Zhou, Y.; Su, Y.; Zhu, H.; Wang, X.; Li, X.; Dai, C.; Xu, C.; Zheng, T.; Mao, C.; Chen, D. Interleukin-23 receptor signaling mediates cancer dormancy and radioresistance in human esophageal squamous carcinoma cells via the Wnt/Notch pathway. J. Mol. Med. 2019, 97, 177–188. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Abravanel, D.L.; Belka, G.K.; Pan, T.C.; Pant, D.K.; Collins, M.A.; Sterner, C.J.; Chodosh, L.A. Notch promotes recurrence of dormant tumor cells following HER2/neu-targeted therapy. J. Clin. Investig. 2015, 125, 2484–2496. [Google Scholar] [CrossRef] [Green Version]
- Capulli, M.; Hristova, D.; Valbret, Z.; Carys, K.; Arjan, R.; Maurizi, A.; Masedu, F.; Cappariello, A.; Rucci, N.; Teti, A. Notch2 pathway mediates breast cancer cellular dormancy and mobilisation in bone and contributes to haematopoietic stem cell mimicry. Br. J. Cancer 2019, 121, 157–171. [Google Scholar] [CrossRef] [Green Version]
- Sadarangani, A.; Pineda, G.; Lennon, K.M.; Chun, H.J.; Shih, A.; Schairer, A.E.; Court, A.C.; Goff, D.J.; Prashad, S.L.; Geron, I.; et al. GLI2 inhibition abrogates human leukemia stem cell dormancy. J. Transl. Med. 2015, 13, 98. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Ligeon, L.A.; Pena-Francesch, M.; Vanoaica, L.D.; Núñez, N.G.; Talwar, D.; Dick, T.P.; Münz, C. Oxidation inhibits autophagy protein deconjugation from phagosomes to sustain MHC class II restricted antigen presentation. Nat. Commun. 2021, 12, 1508. [Google Scholar] [CrossRef]
- Li, X.; He, S.; Ma, B. Autophagy and autophagy-related proteins in cancer. Mol. Cancer 2020, 19, 12. [Google Scholar] [CrossRef]
- Vera-Ramirez, L.; Vodnala, S.K.; Nini, R.; Hunter, K.W.; Green, J.E. Autophagy promotes the survival of dormant breast cancer cells and metastatic tumour recurrence. Nat. Commun. 2018, 9, 1944. [Google Scholar] [CrossRef] [Green Version]
- Zhao, D.; Zou, C.X.; Liu, X.M.; Jiang, Z.D.; Yu, Z.Q.; Suo, F.; Du, T.Y.; Dong, M.Q.; He, W.; Du, L.L. A UPR-Induced Soluble ER-Phagy Receptor Acts with VAPs to Confer ER Stress Resistance. Mol. Cell 2020, 79, 963–977.e963. [Google Scholar] [CrossRef]
- Qiu, Y.; Qiu, S.; Deng, L.; Nie, L.; Gong, L.; Liao, X.; Zheng, X.; Jin, K.; Li, J.; Tu, X.; et al. Biomaterial 3D collagen I gel culture model: A novel approach to investigate tumorigenesis and dormancy of bladder cancer cells induced by tumor microenvironment. Biomaterials 2020, 256, 120217. [Google Scholar] [CrossRef]
- Wang, H.; Wang, N.; Xu, D.; Ma, Q.; Chen, Y.; Xu, S.; Xia, Q.; Zhang, Y.; Prehn, J.H.M.; Wang, G.; et al. Oxidation of multiple MiT/TFE transcription factors links oxidative stress to transcriptional control of autophagy and lysosome biogenesis. Autophagy 2020, 16, 1683–1696. [Google Scholar] [CrossRef] [PubMed]
- Zheng, X.; Yang, Z.; Gu, Q.; Xia, F.; Fu, Y.; Liu, P.; Yin, X.M.; Li, M. The protease activity of human ATG4B is regulated by reversible oxidative modification. Autophagy 2020, 16, 1838–1850. [Google Scholar] [CrossRef] [PubMed]
- Frudd, K.; Burgoyne, T.; Burgoyne, J.R. Oxidation of Atg3 and Atg7 mediates inhibition of autophagy. Nat. Commun. 2018, 9, 95. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Cosin-Roger, J.; Simmen, S.; Melhem, H.; Atrott, K.; Frey-Wagner, I.; Hausmann, M.; de Vallière, C.; Spalinger, M.R.; Spielmann, P.; Wenger, R.H.; et al. Hypoxia ameliorates intestinal inflammation through NLRP3/mTOR downregulation and autophagy activation. Nat. Commun. 2017, 8, 98. [Google Scholar] [CrossRef] [Green Version]
- Tian, H.; Zhang, M.; Jin, G.; Jiang, Y.; Luan, Y. Cu-MOF chemodynamic nanoplatform via modulating glutathione and H2O2 in tumor microenvironment for amplified cancer therapy. J. Colloid Interface Sci. 2021, 587, 358–366. [Google Scholar] [CrossRef]
- Hu, W.; Zhang, L.; Dong, Y.; Tian, Z.; Chen, Y.; Dong, S. Tumour dormancy in inflammatory microenvironment: A promising therapeutic strategy for cancer-related bone metastasis. Cell Mol. Life Sci. 2020, 77, 5149–5169. [Google Scholar] [CrossRef]
- Gao, X.L.; Zheng, M.; Wang, H.F.; Dai, L.L.; Yu, X.H.; Yang, X.; Pang, X.; Li, L.; Zhang, M.; Wang, S.S.; et al. NR2F1 contributes to cancer cell dormancy, invasion and metastasis of salivary adenoid cystic carcinoma by activating CXCL12/CXCR4 pathway. BMC Cancer 2019, 19, 743. [Google Scholar] [CrossRef]
- Adamski, V.; Hattermann, K.; Kubelt, C.; Cohrs, G.; Lucius, R.; Synowitz, M.; Sebens, S.; Held-Feindt, J. Entry and exit of chemotherapeutically-promoted cellular dormancy in glioblastoma cells is differentially affected by the chemokines CXCL12, CXCL16, and CX3CL1. Oncogene 2020, 39, 4421–4435. [Google Scholar] [CrossRef]
- Decker, A.M.; Decker, J.T.; Jung, Y.; Cackowski, F.C.; Daignault-Newton, S.; Morgan, T.M.; Shea, L.D.; Taichman, R.S. Adrenergic Blockade Promotes Maintenance of Dormancy in Prostate Cancer Through Upregulation of GAS6. Transl. Oncol. 2020, 13, 100781. [Google Scholar] [CrossRef] [PubMed]
- Ottewell, P.D.; Wang, N.; Brown, H.K.; Fowles, C.A.; Croucher, P.I.; Eaton, C.L.; Holen, I. OPG-Fc inhibits ovariectomy-induced growth of disseminated breast cancer cells in bone. Int. J. Cancer 2015, 137, 968–977. [Google Scholar] [CrossRef]
- Boyerinas, B.; Zafrir, M.; Yesilkanal, A.E.; Price, T.T.; Hyjek, E.M.; Sipkins, D.A. Adhesion to osteopontin in the bone marrow niche regulates lymphoblastic leukemia cell dormancy. Blood 2013, 121, 4821–4831. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Johnson, R.W.; Finger, E.C.; Olcina, M.M.; Vilalta, M.; Aguilera, T.; Miao, Y.; Merkel, A.R.; Johnson, J.R.; Sterling, J.A.; Wu, J.Y.; et al. Induction of LIFR confers a dormancy phenotype in breast cancer cells disseminated to the bone marrow. Nat. Cell Biol. 2016, 18, 1078–1089. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Levoye, A.; Balabanian, K.; Baleux, F.; Bachelerie, F.; Lagane, B. CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling. Blood 2009, 113, 6085–6093. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Martin, T.J.; Johnson, R.W. Multiple actions of parathyroid hormone-related protein in breast cancer bone metastasis. Br. J. Pharmacol. 2021, 178, 1923–1935. [Google Scholar] [CrossRef]
- Beekman, K.M.; Zwaagstra, M.; Veldhuis-Vlug, A.G.; van Essen, H.W.; den Heijer, M.; Maas, M.; Kerckhofs, G.; Parac-Vogt, T.N.; Bisschop, P.H.; Bravenboer, N. Ovariectomy increases RANKL protein expression in bone marrow adipocytes of C3H/HeJ mice. Am. J. Physiol. Endocrinol. Metab 2019, 317, e1050–e1054. [Google Scholar] [CrossRef]
- Abuna, R.P.; De Oliveira, F.S.; Santos Tde, S.; Guerra, T.R.; Rosa, A.L.; Beloti, M.M. Participation of TNF-α in Inhibitory Effects of Adipocytes on Osteoblast Differentiation. J. Cell. Physiol. 2016, 231, 204–214. [Google Scholar] [CrossRef]
- Delort, L.; Rossary, A.; Farges, M.C.; Vasson, M.P.; Caldefie-Chézet, F. Leptin, adipocytes and breast cancer: Focus on inflammation and anti-tumor immunity. Life Sci. 2015, 140, 37–48. [Google Scholar] [CrossRef]
- Dou, C.; Ding, N.; Zhao, C.; Hou, T.; Kang, F.; Cao, Z.; Liu, C.; Bai, Y.; Dai, Q.; Ma, Q.; et al. Estrogen Deficiency-Mediated M2 Macrophage Osteoclastogenesis Contributes to M1/M2 Ratio Alteration in Ovariectomized Osteoporotic Mice. J. Bone Miner. Res. 2018, 33, 899–908. [Google Scholar] [CrossRef] [Green Version]
- Hirata, Y.; Kakiuchi, M.; Robson, S.C.; Fujisaki, J. CD150(high) CD4 T cells and CD150(high) regulatory T cells regulate hematopoietic stem cell quiescence via CD73. Haematologica 2019, 104, 1136–1142. [Google Scholar] [CrossRef] [Green Version]
- Hirata, Y.; Furuhashi, K.; Ishii, H.; Li, H.W.; Pinho, S.; Ding, L.; Robson, S.C.; Frenette, P.S.; Fujisaki, J. CD150(high) Bone Marrow Tregs Maintain Hematopoietic Stem Cell Quiescence and Immune Privilege via Adenosine. Cell Stem Cell 2018, 22, 445–453.e445. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Luo, X.; Cheng, C.; Tan, Z.; Li, N.; Tang, M.; Yang, L.; Cao, Y. Emerging roles of lipid metabolism in cancer metastasis. Mol. Cancer 2017, 16, 76. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Pascual, G.; Avgustinova, A.; Mejetta, S.; Martín, M.; Castellanos, A.; Attolini, C.S.; Berenguer, A.; Prats, N.; Toll, A.; Hueto, J.A.; et al. Targeting metastasis-initiating cells through the fatty acid receptor CD36. Nature 2017, 541, 41–45. [Google Scholar] [CrossRef]
- Watt, M.J.; Clark, A.K.; Selth, L.A.; Haynes, V.R.; Lister, N.; Rebello, R.; Porter, L.H.; Niranjan, B.; Whitby, S.T.; Lo, J.; et al. Suppressing fatty acid uptake has therapeutic effects in preclinical models of prostate cancer. Sci. Transl. Med. 2019, 11, eaau5758. [Google Scholar] [CrossRef]
- Jay, A.G.; Chen, A.N.; Paz, M.A.; Hung, J.P.; Hamilton, J.A. CD36 binds oxidized low density lipoprotein (LDL) in a mechanism dependent upon fatty acid binding. J. Biol. Chem. 2015, 290, 4590–4603. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Wang, R.; Tao, B.; Fan, Q.; Wang, S.; Chen, L.; Zhang, J.; Hao, Y.; Dong, S.; Wang, Z.; Wang, W.; et al. Fatty-acid receptor CD36 functions as a hydrogen sulfide-targeted receptor with its Cys333-Cys272 disulfide bond serving as a specific molecular switch to accelerate gastric cancer metastasis. EBioMedicine 2019, 45, 108–123. [Google Scholar] [CrossRef] [Green Version]
- Panigrahy, D.; Edin, M.L.; Lee, C.R.; Huang, S.; Bielenberg, D.R.; Butterfield, C.E.; Barnés, C.M.; Mammoto, A.; Mammoto, T.; Luria, A.; et al. Epoxyeicosanoids stimulate multiorgan metastasis and tumor dormancy escape in mice. J. Clin. Investig. 2012, 122, 178–191. [Google Scholar] [CrossRef] [Green Version]
- Perego, M.; Tyurin, V.A.; Tyurina, Y.Y.; Yellets, J.; Nacarelli, T.; Lin, C.; Nefedova, Y.; Kossenkov, A.; Liu, Q.; Sreedhar, S.; et al. Reactivation of dormant tumor cells by modified lipids derived from stress-activated neutrophils. Sci. Transl. Med. 2020, 12, eabb5817. [Google Scholar] [CrossRef]
- McGarry, T.; Biniecka, M.; Veale, D.J.; Fearon, U. Hypoxia, oxidative stress and inflammation. Free. Radic. Biol. Med. 2018, 125, 15–24. [Google Scholar] [CrossRef]
- Liu, Y.; Li, Z.; Li, J.; Yang, S.; Zhang, Y.; Yao, B.; Song, W.; Fu, X.; Huang, S. Stiffness-mediated mesenchymal stem cell fate decision in 3D-bioprinted hydrogels. Burns. Trauma 2020, 8, tkaa029. [Google Scholar] [CrossRef] [PubMed]
- Albrengues, J.; Shields, M.A.; Ng, D.; Park, C.G.; Ambrico, A.; Poindexter, M.E.; Upadhyay, P.; Uyeminami, D.L.; Pommier, A.; Küttner, V.; et al. Neutrophil extracellular traps produced during inflammation awaken dormant cancer cells in mice. Science 2018, 361, eaao4227. [Google Scholar] [CrossRef] [Green Version]
- El-Shennawy, L.; Dubrovskyi, O.; Kastrati, I.; Danes, J.M.; Zhang, Y.; Whiteley, H.E.; Creighton, C.J.; Frasor, J. Coactivation of Estrogen Receptor and IKKβ Induces a Dormant Metastatic Phenotype in ER-Positive Breast Cancer. Cancer Res. 2018, 78, 974–984. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Maiti, S.; Nazmeen, A. Impaired redox regulation of estrogen metabolizing proteins is important determinant of human breast cancers. Cancer Cell Int. 2019, 19, 111. [Google Scholar] [CrossRef] [PubMed]
- Lawson, M.A.; McDonald, M.M.; Kovacic, N.; Hua Khoo, W.; Terry, R.L.; Down, J.; Kaplan, W.; Paton-Hough, J.; Fellows, C.; Pettitt, J.A.; et al. Osteoclasts control reactivation of dormant myeloma cells by remodelling the endosteal niche. Nat. Commun. 2015, 6, 8983. [Google Scholar] [CrossRef] [Green Version]
- Cabezas-Wallscheid, N.; Buettner, F.; Sommerkamp, P.; Klimmeck, D.; Ladel, L.; Thalheimer, F.B.; Pastor-Flores, D.; Roma, L.P.; Renders, S.; Zeisberger, P.; et al. Vitamin A-Retinoic Acid Signaling Regulates Hematopoietic Stem Cell Dormancy. Cell 2017, 169, 807–823.e819. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Price, D.K. Efficacy of androgen deprivation therapy and the role of oxidative stress. Ann. Oncol. 2017, 28, 451–453. [Google Scholar] [CrossRef]
- Havas, K.M.; Milchevskaya, V.; Radic, K.; Alladin, A.; Kafkia, E.; Garcia, M.; Stolte, J.; Klaus, B.; Rotmensz, N.; Gibson, T.J.; et al. Metabolic shifts in residual breast cancer drive tumor recurrence. J. Clin. Investig. 2017, 127, 2091–2105. [Google Scholar] [CrossRef] [Green Version]
- El Touny, L.H.; Vieira, A.; Mendoza, A.; Khanna, C.; Hoenerhoff, M.J.; Green, J.E. Combined SFK/MEK inhibition prevents metastatic outgrowth of dormant tumor cells. J. Clin. Investig. 2014, 124, 156–168. [Google Scholar] [CrossRef] [Green Version]
- Abderrahman, B.; Jordan, V.C. Rethinking Extended Adjuvant Antiestrogen Therapy to Increase Survivorship in Breast Cancer. JAMA Oncol. 2018, 4, 15–16. [Google Scholar] [CrossRef]
- O’Leary, B.; Finn, R.S.; Turner, N.C. Treating cancer with selective CDK4/6 inhibitors. Nat. Rev. Clin. Oncol. 2016, 13, 417–430. [Google Scholar] [CrossRef]
- Nakayama, T.; Sano, T.; Oshimo, Y.; Kawada, C.; Kasai, M.; Yamamoto, S.; Fukuhara, H.; Inoue, K.; Ogura, S.I. Enhanced lipid metabolism induces the sensitivity of dormant cancer cells to 5-aminolevulinic acid-based photodynamic therapy. Sci. Rep. 2021, 11, 7290. [Google Scholar] [CrossRef] [PubMed]
- Nicolini, F.E.; Etienne, G.; Huguet, F.; Guerci-Bresler, A.; Charbonnier, A.; Escoffre-Barbe, M.; Dubruille, V.; Johnson-Ansah, H.; Legros, L.; Coiteux, V. The Combination of Nilotinib+ Pegylated IFN Alpha 2a Provides Somewhat Higher Cumulative Incidence Rates of MR4. 5 at M36 Versus Nilotinib Alone in Newly Diagnosed CP CML Patients. In Updated Results of the Petals Phase III National Study; American Society of Hematology Washington: Washington, DC, USA, 2019. [Google Scholar]
- Pietras, E.M.; Lakshminarasimhan, R.; Techner, J.M.; Fong, S.; Flach, J.; Binnewies, M.; Passegué, E. Re-entry into quiescence protects hematopoietic stem cells from the killing effect of chronic exposure to type I interferons. J. Exp. Med. 2014, 211, 245–262. [Google Scholar] [CrossRef]
- Tasdogan, A.; Kumar, S.; Allies, G.; Bausinger, J.; Beckel, F.; Hofemeister, H.; Mulaw, M.; Madan, V.; Scharffetter-Kochanek, K.; Feuring-Buske, M.; et al. DNA Damage-Induced HSPC Malfunction Depends on ROS Accumulation Downstream of IFN-1 Signaling and Bid Mobilization. Cell Stem Cell 2016, 19, 752–767. [Google Scholar] [CrossRef]
- Singh, S.; Jakubison, B.; Keller, J.R. Protection of hematopoietic stem cells from stress-induced exhaustion and aging. Curr. Opin. Hematol. 2020, 27, 225–231. [Google Scholar] [CrossRef]
- Hampsch, R.A.; Wells, J.D.; Traphagen, N.A.; McCleery, C.F.; Fields, J.L.; Shee, K.; Dillon, L.M.; Pooler, D.B.; Lewis, L.D.; Demidenko, E.; et al. AMPK Activation by Metformin Promotes Survival of Dormant ER(+) Breast Cancer Cells. Clin. Cancer Res. Off. J. Am. Assoc. Cancer Res. 2020, 26, 3707–3719. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Viale, A.; Pettazzoni, P.; Lyssiotis, C.A.; Ying, H.; Sánchez, N.; Marchesini, M.; Carugo, A.; Green, T.; Seth, S.; Giuliani, V.; et al. Oncogene ablation-resistant pancreatic cancer cells depend on mitochondrial function. Nature 2014, 514, 628–632. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Lagadinou, E.D.; Sach, A.; Callahan, K.; Rossi, R.M.; Neering, S.J.; Minhajuddin, M.; Ashton, J.M.; Pei, S.; Grose, V.; O’Dwyer, K.M.; et al. BCL-2 inhibition targets oxidative phosphorylation and selectively eradicates quiescent human leukemia stem cells. Cell Stem Cell 2013, 12, 329–341. [Google Scholar] [CrossRef] [Green Version]
- Han, L.; Cavazos, A.; Baran, N.; Zhang, Q.; Kuruvilla, V.M.; Gay, J.P.; Feng, N.; Battula, V.L.; Kantarjian, H.M.; Daver, N.G. Mitochondrial OxPhos as Survival Mechanism of Minimal Residual AML Cells after Induction Chemotherapy: Survival Benefit by Complex. I Inhibition with IACS-010759; American Society of Hematology Washington: Washington, DC, USA, 2019. [Google Scholar]
- Han, L.; Cavazos, A.; Baran, N.; Zhang, Q.; Kuruvilla, V.M.; Gay, J.P.; Feng, N.; Battula, V.L.; Andreeff, M.; Kantarjian, H.M. Targeting residual chemotherapy-resistant acute myeloid leukemia cells by a novel OXPHOS inhibitor IACS010759. Blood 2017, 130, 2623. [Google Scholar]
- Dower, C.M.; Wills, C.A.; Frisch, S.M.; Wang, H.G. Mechanisms and context underlying the role of autophagy in cancer metastasis. Autophagy 2018, 14, 1110–1128. [Google Scholar] [CrossRef] [Green Version]
- Sandoval, M.V.; Fluegen, G.; Staschke, K.A.; Calvo-Vidal, V.; Aguirre-Ghiso, J.A. Abstract A45: PERK-Inhibition as a possible therapy for hypoxia-induced solitary dormant tumor cells. AACR 2016, 76, A45. [Google Scholar]
- Chen, X.; Kang, R.; Kroemer, G.; Tang, D. Broadening horizons: The role of ferroptosis in cancer. Nat. Rev. Clin. Oncol. 2021, 18, 280–296. [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]
- Recasens, A.; Munoz, L. Targeting Cancer Cell Dormancy. Trends Pharmacol. Sci. 2019, 40, 128–141. [Google Scholar] [CrossRef]
- Hangauer, M.J.; Viswanathan, V.S.; Ryan, M.J.; Bole, D.; Eaton, J.K.; Matov, A.; Galeas, J.; Dhruv, H.D.; Berens, M.E.; Schreiber, S.L.; et al. Drug-tolerant persister cancer cells are vulnerable to GPX4 inhibition. Nature 2017, 551, 247–250. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Barrera, G.; Pizzimenti, S.; Daga, M.; Dianzani, C.; Arcaro, A.; Cetrangolo, G.P.; Giordano, G.; Cucci, M.A.; Graf, M.; Gentile, F. Lipid Peroxidation-Derived Aldehydes, 4-Hydroxynonenal and Malondialdehyde in Aging-Related Disorders. Antioxidants 2018, 7, 102. [Google Scholar] [CrossRef] [PubMed] [Green Version]
- Raha, D.; Wilson, T.R.; Peng, J.; Peterson, D.; Yue, P.; Evangelista, M.; Wilson, C.; Merchant, M.; Settleman, J. The cancer stem cell marker aldehyde dehydrogenase is required to maintain a drug-tolerant tumor cell subpopulation. Cancer Res. 2014, 74, 3579–3590. [Google Scholar] [CrossRef] [PubMed] [Green Version]
Strategy | Title Name | Drug Name | Tumor | Phase | NCT Number |
---|---|---|---|---|---|
Keeping dormant cells asleep | Defined green tea catechin extract for treating women with hormone receptor-negative stage I-III breast cancer | Green tea catechin extract | Hormone receptor negative stage I–III breast cancer | I | NCT00516243 |
Effects of muscadine grape extract in men with prostate cancer on androgen deprivation therapy | Muscadine Grape Extract, androgen deprivation therapy | Recurrent prostate cancer | II | NCT03496805 | |
A pilot study of 5-AZA and ATRA for prostate cancer with PSA-only recurrence after local treatment | 5-Azacitidine, retinoic acid, Lupron | Prostate cancer | II | NCT03572387 | |
Awaking dormant cells | Nilotinib Plus Pegylated Interferon-α2b in CML | Pegylated interferon α-2b, nilotinib | Chronic myeloid leukemia | II | NCT01866553 |
Killing dormant cells | IACS-010759 in advanced cancers | Oxidative Phosphorylation Inhibitor IACS-010759 | Advanced cancers | I | NCT03291938 |
Oxidative Phosphorylation Inhibitor IACS-010759 for treating patients with relapsed or refractory Acute Myeloid Leukemia | Oxidative Phosphorylation Inhibitor IACS-010759 | Relapsed or refractory acute myeloid leukemia | I | NCT02882321 | |
Gedatolisib, Hydroxychloroquine, or the combination for prevention of recurrent breast cancer (“GLACIER”) | Hydroxychloroqui-ne, Gedatolisib | Breast cancer | I/II | NCT03400254 | |
CLEVER Pilot Trial: A phase II pilot trial of HydroxyChLoroquine, EVErolimus, or the combination for prevention of recurrent breast cancer | Hydroxychloroqui-ne, Everolimus | Breast cancer and harbored bone marrow disseminated tumor cells. | II | NCT03032406 | |
Avelumab or Hydroxychloroquine with or without Palbociclib to eliminate dormant breast cancer (PALAVY) | Hydroxychloroqui-ne, Avelumab, Palbociclib | Dormant breast cancer | II | NCT04841148 | |
Altretamine and Etoposide for treating patients with HIV-related cancer | Altretamine (GPX4 inhibitor), etoposide | HIV-related cancer | I | NCT00002936 | |
Ashwagandha for cognitive dysfunction | Ashwagandha (GPX4 inhibitor) | Breast cancer | II | NCT04092647 |
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Li, B.; Huang, Y.; Ming, H.; Nice, E.C.; Xuan, R.; Huang, C. Redox Control of the Dormant Cancer Cell Life Cycle. Cells 2021, 10, 2707. https://doi.org/10.3390/cells10102707
Li B, Huang Y, Ming H, Nice EC, Xuan R, Huang C. Redox Control of the Dormant Cancer Cell Life Cycle. Cells. 2021; 10(10):2707. https://doi.org/10.3390/cells10102707
Chicago/Turabian StyleLi, Bowen, Yichun Huang, Hui Ming, Edouard C. Nice, Rongrong Xuan, and Canhua Huang. 2021. "Redox Control of the Dormant Cancer Cell Life Cycle" Cells 10, no. 10: 2707. https://doi.org/10.3390/cells10102707
APA StyleLi, B., Huang, Y., Ming, H., Nice, E. C., Xuan, R., & Huang, C. (2021). Redox Control of the Dormant Cancer Cell Life Cycle. Cells, 10(10), 2707. https://doi.org/10.3390/cells10102707