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Endocrine, Metabolic & Immune Disorders - Drug Targets

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ISSN (Print): 1871-5303
ISSN (Online): 2212-3873

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Review Article

Molecular Mechanisms of Nickel-Induced Carcinogenesis

Author(s): Young-Ok Son*

Volume 20, Issue 7, 2020

Page: [1015 - 1023] Pages: 9

DOI: 10.2174/1871530319666191125112728

Price: $65

Abstract

Background: The increased use of heavy metal nickel in modern industries results in increased environmental impact. Occupational and environmental exposure to nickel is closely linked to an increased risk of human lung cancer and nasal cancer.

Objective: Unlike other heavy metal carcinogens, nickel has weak mutagenic activity. Carcinogenesis caused by nickel is intensively studied, but the precise mechanism of action is not yet known.

Results: Epigenetic changes, activation of hypoxia signaling pathways, and generation of reactive oxygen species (ROS) are considered to be the major molecular mechanisms involved in nickelinduced carcinogenesis.

Conclusion: This review provides insights into current research on nickel-induced carcinogenesis and suggests possible effective therapeutic strategies for nickel-induced carcinogenesis.

Keywords: Apoptosis, autophagy, carcinogenesis, nickel, reactive oxygen species, transformed cells.

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[1]
Oller, A.R.; Costa, M.; Oberdörster, G. Carcinogenicity assessment of selected nickel compounds. Toxicol. Appl. Pharmacol., 1997, 143(1), 152-166.
[http://dx.doi.org/10.1006/taap.1996.8075] [PMID: 9073603]
[2]
IARC; working group on the evaluation of carcinogenic risk to humans. Arsenic, metals, fibres and dusts. lyon (FR) International Agency for Research on Cancer,, 2012.No. 100C (IARC Monographs on the Evaluation of Carcinogenic Risks to Humans).
[3]
Grimsrud, T.K.; Peto, J. Persisting risk of nickel related lung cancer and nasal cancer among Clydach refiners. Occup. Environ. Med., 2006, 63(5), 365-366.
[http://dx.doi.org/10.1136/oem.2005.026336] [PMID: 16621856]
[4]
IARC. International agency for research on cancer: Nickel and nickel compounds. Summ. Eval., 1990, 49, 257.
[5]
Ohshima, S. Induction of genetic instability and chromosomal instability by nickel sulfate in V79 Chinese hamster cells. Mutagenesis, 2003, 18(2), 133-137.
[http://dx.doi.org/10.1093/mutage/18.2.133] [PMID: 12621068]
[6]
Davidson, T.L.; Chen, H.; Di Toro, D.M.; D’Angelo, G.; Costa, M. Soluble nickel inhibits HIF-prolyl-hydroxylases creating persistent hypoxic signaling in A549 cells. Mol. Carcinog., 2006, 45(7), 479-489.
[http://dx.doi.org/10.1002/mc.20176] [PMID: 16649251]
[7]
Kawanishi, S.; Oikawa, S.; Inoue, S.; Nishino, K. Distinct mechanisms of oxidative DNA damage induced by carcinogenic nickel subsulfide and nickel oxides. Environ. Health Perspect., 2002, 110(Suppl. 5), 789-791.
[http://dx.doi.org/10.1289/ehp.02110s5789] [PMID: 12426132]
[8]
Arita, A.; Costa, M. Epigenetics in metal carcinogenesis: Nickel, arsenic, chromium and cadmium. Metallomics : Integrated biometal science, 2009, 1(3), 222-8.
[http://dx.doi.org/10.1039/b903049b]
[9]
Kasprzak, K.S.; Sunderman, F.W., Jr; Salnikow, K. Nickel carcinogenesis. Mutat. Res., 2003, 533(1-2), 67-97.
[http://dx.doi.org/10.1016/j.mrfmmm.2003.08.021] [PMID: 14643413]
[10]
Dunnick, J.K.; Elwell, M.R.; Radovsky, A.E.; Benson, J.M.; Hahn, F.F.; Nikula, K.J.; Barr, E.B.; Hobbs, C.H. Comparative carcinogenic effects of nickel subsulfide, nickel oxide, or nickel sulfate hexahydrate chronic exposures in the lung. Cancer Res., 1995, 55(22), 5251-5256.
[PMID: 7585584]
[11]
Grimsrud, T.K.; Berge, S.R.; Martinsen, J.I.; Andersen, A. Lung cancer incidence among Norwegian nickel-refinery workers 1953-2000. J. Environ. Monit., 2003, 5(2), 190-197.
[http://dx.doi.org/10.1039/b211722n] [PMID: 12729252]
[12]
Lu, H.; Shi, X.; Costa, M.; Huang, C. Carcinogenic effect of nickel compounds. Mol. Cell. Biochem., 2005, 279(1-2), 45-67.
[http://dx.doi.org/10.1007/s11010-005-8215-2] [PMID: 16283514]
[13]
Nickel compounds and metallic nickel. Rep. Carcinog., 2011, 12, 280-283.
[14]
Campbell, J.A. Lung tumours in mice and man. BMJ, 1943, 1(4284), 179-183.
[http://dx.doi.org/10.1136/bmj.1.4284.179] [PMID: 20784681]
[15]
Cangul, H.; Broday, L.; Salnikow, K.; Sutherland, J.; Peng, W.; Zhang, Q.; Poltaratsky, V.; Yee, H.; Zoroddu, M.A.; Costa, M. Molecular mechanisms of nickel carcinogenesis. Toxicol. Lett., 2002, 127(1-3), 69-75.
[http://dx.doi.org/10.1016/S0378-4274(01)00485-4] [PMID: 12052643]
[16]
Ke, Q.; Davidson, T.; Kluz, T.; Oller, A.; Costa, M. Fluorescent tracking of nickel ions in human cultured cells. Toxicol. Appl. Pharmacol., 2007, 219(1), 18-23.
[http://dx.doi.org/10.1016/j.taap.2006.08.013] [PMID: 17239912]
[17]
Li, Y.; Zamble, D.B. Nickel homeostasis and nickel regulation: An overview. Chem. Rev., 2009, 109(10), 4617-4643.
[http://dx.doi.org/10.1021/cr900010n] [PMID: 19711977]
[18]
Lee, Y.W.; Klein, C.B.; Kargacin, B.; Salnikow, K.; Kitahara, J.; Dowjat, K.; Zhitkovich, A.; Christie, N.T.; Costa, M. Carcinogenic nickel silences gene expression by chromatin condensation and DNA methylation: A new model for epigenetic carcinogens. Mol. Cell. Biol., 1995, 15(5), 2547-2557.
[http://dx.doi.org/10.1128/MCB.15.5.2547] [PMID: 7537850]
[19]
Govindarajan, B.; Klafter, R.; Miller, M.S.; Mansur, C.; Mizesko, M.; Bai, X.; LaMontagne, K., Jr; Arbiser, J.L. Reactive oxygen-induced carcinogenesis causes hypermethylation of p16(Ink4a) and activation of MAP kinase. Mol. Med., 2002, 8(1), 1-8.
[http://dx.doi.org/10.1007/BF03401997] [PMID: 11984000]
[20]
Zhang, J.; Zhang, J.; Li, M.; Wu, Y.; Fan, Y.; Zhou, Y.; Tan, L.; Shao, Z.; Shi, H. Methylation of RAR-β2, RASSF1A, and CDKN2A genes induced by nickel subsulfide and nickel-carcinogenesis in rats. Biomed. Environ. Sci., 2011, 24(2), 163-171.
[PMID: 21565688]
[21]
Ji, W.; Yang, L.; Yu, L.; Yuan, J.; Hu, D.; Zhang, W.; Yang, J.; Pang, Y.; Li, W.; Lu, J.; Fu, J.; Chen, J.; Lin, Z.; Chen, W.; Zhuang, Z. Epigenetic silencing of O6-methylguanine DNA methyl transferase gene in NiS-transformed cells. Carcinogenesis, 2008, 29(6), 1267-1275.
[http://dx.doi.org/10.1093/carcin/bgn012] [PMID: 18204074]
[22]
Broday, L.; Peng, W.; Kuo, M.H.; Salnikow, K.; Zoroddu, M.; Costa, M. Nickel compounds are novel inhibitors of histone H4 acetylation. Cancer Res., 2000, 60(2), 238-241.
[PMID: 10667566]
[23]
Chen, H.; Ke, Q.; Kluz, T.; Yan, Y.; Costa, M. Nickel ions increase histone H3 lysine 9 dimethylation and induce transgene silencing. Mol. Cell. Biol., 2006, 26(10), 3728-3737.
[http://dx.doi.org/10.1128/MCB.26.10.3728-3737.2006] [PMID: 16648469]
[24]
Golebiowski, F.; Kasprzak, K.S. Inhibition of core histones acetylation by carcinogenic nickel(II). Mol. Cell. Biochem., 2005, 279(1-2), 133-139.
[http://dx.doi.org/10.1007/s11010-005-8285-1] [PMID: 16283522]
[25]
Karaczyn, A.A.; Golebiowski, F.; Kasprzak, K.S. Truncation, deamidation, and oxidation of histone H2B in cells cultured with nickel(II). Chem. Res. Toxicol., 2005, 18(12), 1934-1942.
[http://dx.doi.org/10.1021/tx050122a] [PMID: 16359184]
[26]
Klein, C.B.; Costa, M. DNA methylation, heterochromatin and epigenetic carcinogens. Mutat. Res., 1997, 386(2), 163-180.
[http://dx.doi.org/10.1016/S1383-5742(96)00052-X] [PMID: 9113117]
[27]
Doll, R.; Morgan, L.G.; Speizer, F.E. Cancers of the lung and nasal sinuses in nickel workers. Br. J. Cancer, 1970, 24(4), 623-632.
[http://dx.doi.org/10.1038/bjc.1970.76] [PMID: 5503591]
[28]
Doll, R.; Mathews, J.D.; Morgan, L.G. Cancers of the lung and nasal sinuses in nickel workers: A reassessment of the period of risk. Br. J. Ind. Med., 1977, 34(2), 102-105.
[http://dx.doi.org/10.1136/oem.34.2.102] [PMID: 871439]
[29]
Zhou, C.; Huang, C.; Wang, J.; Huang, H.; Li, J.; Xie, Q.; Liu, Y.; Zhu, J.; Li, Y.; Zhang, D.; Zhu, Q.; Huang, C. LncRNA MEG3 downregulation mediated by DNMT3b contributes to nickel malignant transformation of human bronchial epithelial cells via modulating PHLPP1 transcription and HIF-1α translation. Oncogene, 2017, 36(27), 3878-3889.
[http://dx.doi.org/10.1038/onc.2017.14] [PMID: 28263966]
[30]
Zhang, J.; Zhou, Y.; Ma, L.; Huang, S.; Wang, R.; Gao, R.; Wu, Y.; Shi, H.; Zhang, J. The alteration of miR-222 and its target genes in nickel-induced tumor. Biol. Trace Elem. Res., 2013, 152(2), 267-274.
[http://dx.doi.org/10.1007/s12011-013-9619-6] [PMID: 23447020]
[31]
Scanlon, S.E.; Scanlon, C.D.; Hegan, D.C.; Sulkowski, P.L.; Glazer, P.M. Nickel induces transcriptional down-regulation of DNA repair pathways in tumorigenic and non-tumorigenic lung cells. Carcinogenesis, 2017, 38(6), 627-637.
[http://dx.doi.org/10.1093/carcin/bgx038] [PMID: 28472268]
[32]
Salnikow, K.; Zhitkovich, A. Genetic and epigenetic mechanisms in metal carcinogenesis and cocarcinogenesis: Nickel, arsenic, and chromium. Chem. Res. Toxicol., 2008, 21(1), 28-44.
[http://dx.doi.org/10.1021/tx700198a] [PMID: 17970581]
[33]
Chervona, Y.; Arita, A.; Costa, M. Carcinogenic metals and the epigenome: Understanding the effect of nickel, arsenic, and chromium. Metallomics, 2012, 4(7), 619-627.
[http://dx.doi.org/10.1039/c2mt20033c]
[34]
Chervona, Y.; Costa, M. The control of histone methylation and gene expression by oxidative stress, hypoxia, and metals. Free Radic. Biol. Med., 2012, 53(5), 1041-1047.
[http://dx.doi.org/10.1016/j.freeradbiomed.2012.07.020] [PMID: 22841757]
[35]
Chen, H.; Costa, M. Iron- and 2-oxoglutarate-dependent dioxygenases: An emerging group of molecular targets for nickel toxicity and carcinogenicity. Biometals, 2009, 22(1), 191-196.
[36]
Salnikow, K.; Davidson, T.; Kluz, T.; Chen, H.; Zhou, D.; Costa, M. GeneChip analysis of signaling pathways effected by nickel. J. Environ. Monit., 2003, 5(2), 206-209.
[http://dx.doi.org/10.1039/b210262p] [PMID: 12729255]
[37]
Salnikow, K.; Blagosklonny, M.V.; Ryan, H.; Johnson, R.; Costa, M. Carcinogenic nickel induces genes involved with hypoxic stress. Cancer Res., 2000, 60(1), 38-41.
[PMID: 10646848]
[38]
Ke, Q.; Davidson, T.; Chen, H.; Kluz, T.; Costa, M. Alterations of histone modifications and transgene silencing by nickel chloride. Carcinogenesis, 2006, 27(7), 1481-1488.
[http://dx.doi.org/10.1093/carcin/bgl004] [PMID: 16522665]
[39]
Zhou, X.; Li, Q.; Arita, A.; Sun, H.; Costa, M. Effects of nickel, chromate, and arsenite on histone 3 lysine methylation. Toxicol. Appl. Pharmacol., 2009, 236(1), 78-84.
[http://dx.doi.org/10.1016/j.taap.2009.01.009] [PMID: 19371620]
[40]
Arita, A.; Niu, J.; Qu, Q.; Zhao, N.; Ruan, Y.; Nadas, A.; Chervona, Y.; Wu, F.; Sun, H.; Hayes, R.B.; Costa, M. Global levels of histone modifications in peripheral blood mononuclear cells of subjects with exposure to nickel. Environ. Health Perspect., 2012, 120(2), 198-203.
[http://dx.doi.org/10.1289/ehp.1104140] [PMID: 22024396]
[41]
Arita, A.; Shamy, M.Y.; Chervona, Y.; Clancy, H.A.; Sun, H.; Hall, M.N.; Qu, Q.; Gamble, M.V.; Costa, M. The effect of exposure to carcinogenic metals on histone tail modifications and gene expression in human subjects. J. Trace Elem. Med. Biol., 2012, 26(2-3), 174-178.
[http://dx.doi.org/10.1016/j.jtemb.2012.03.012]
[42]
Ma, L.; Bai, Y.; Pu, H.; Gou, F.; Dai, M.; Wang, H.; He, J.; Zheng, T.; Cheng, N. Histone methylation in nickel-smelting industrial workers. PLoS One, 2015, 10(10) e0140339
[http://dx.doi.org/10.1371/journal.pone.0140339] [PMID: 26474320]
[43]
Chen, H.; Kluz, T.; Zhang, R.; Costa, M. Hypoxia and nickel inhibit histone demethylase JMJD1A and repress Spry2 expression in human bronchial epithelial BEAS-2B cells. Carcinogenesis, 2010, 31(12), 2136-2144.
[http://dx.doi.org/10.1093/carcin/bgq197] [PMID: 20881000]
[44]
Johnson, A.B.; Denko, N.; Barton, M.C. Hypoxia induces a novel signature of chromatin modifications and global repression of transcription. Mutat. Res., 2008, 640(1-2), 174-179.
[http://dx.doi.org/10.1016/j.mrfmmm.2008.01.001] [PMID: 18294659]
[45]
Tausendschön, M.; Dehne, N.; Brüne, B. Hypoxia causes epigenetic gene regulation in macrophages by attenuating Jumonji histone demethylase activity. Cytokine, 2011, 53(2), 256-262.
[http://dx.doi.org/10.1016/j.cyto.2010.11.002] [PMID: 21131212]
[46]
Ge, Y.; Bruno, M.; Haykal-Coates, N.; Wallace, K.; Andrews, D.; Swank, A.; Winnik, W.; Ross, J.A. Proteomic Assessment of Biochemical Pathways That Are Critical to Nickel-Induced Toxicity Responses in Human Epithelial Cells. PLoS One, 2016, 11(9) e0162522
[http://dx.doi.org/10.1371/journal.pone.0162522] [PMID: 27626938]
[47]
Patierno, S.R.; Dirscherl, L.A.; Xu, J. Transformation of rat tracheal epithelial cells to immortal growth variants by particulate and soluble nickel compounds. Mutat. Res., 1993, 300(3-4), 179-193.
[http://dx.doi.org/10.1016/0165-1218(93)90049-J] [PMID: 7687017]
[48]
Biedermann, K.A.; Landolph, J.R. Induction of anchorage independence in human diploid foreskin fibroblasts by carcinogenic metal salts. Cancer Res., 1987, 47(14), 3815-3823.
[PMID: 3594439]
[49]
Costa, M.; Nye, J.S.; Sunderman, F.W., Jr; Allpass, P.R.; Gondos, B. Induction of sarcomas in nude mice by implantation of Syrian hamster fetal cells exposed in vitro to nickel subsulfide. Cancer Res., 1979, 39(9), 3591-3597.
[PMID: 476684]
[50]
Kerckaert, G.A.; LeBoeuf, R.A.; Isfort, R.J. Use of the Syrian hamster embryo cell transformation assay for determining the carcinogenic potential of heavy metal compounds. Fundam. Appl. Toxicol., 1996, 34(1), 67-72.
[51]
Salnikow, K.; Wang, S.; Costa, M. Induction of activating transcription factor 1 by nickel and its role as a negative regulator of thrombospondin I gene expression. Cancer Res., 1997, 57(22), 5060-5066.
[PMID: 9371503]
[52]
Salnikow, K.; Cosentino, S.; Klein, C.; Costa, M. Loss of thrombospondin transcriptional activity in nickel-transformed cells. Mol. Cell. Biol., 1994, 14(1), 851-858.
[http://dx.doi.org/10.1128/MCB.14.1.851] [PMID: 8264652]
[53]
Ke, Q.; Costa, M. Hypoxia-inducible factor-1 (HIF-1). Mol. Pharmacol., 2006, 70(5), 1469-1480.
[http://dx.doi.org/10.1124/mol.106.027029] [PMID: 16887934]
[54]
Maxwell, P.; Salnikow, K. HIF-1: An oxygen and metal responsive transcription factor. Cancer Biol. Ther., 2004, 3(1), 29-35.
[http://dx.doi.org/10.4161/cbt.3.1.547] [PMID: 14726713]
[55]
Wu, C.H.; Tang, S.C.; Wang, P.H.; Lee, H.; Ko, J.L. Nickel-induced epithelial-mesenchymal transition by reactive oxygen species generation and E-cadherin promoter hypermethylation. J. Biol. Chem., 2012, 287(30), 25292-25302.
[http://dx.doi.org/10.1074/jbc.M111.291195] [PMID: 22648416]
[56]
Goebeler, M.; Meinardus-Hager, G.; Roth, J.; Goerdt, S.; Sorg, C. Nickel chloride and cobalt chloride, two common contact sensitizers, directly induce expression of intercellular adhesion molecule-1 (ICAM-1), vascular cell adhesion molecule-1 (VCAM-1), and endothelial leukocyte adhesion molecule (ELAM-1) by endothelial cells. J. Invest. Dermatol., 1993, 100(6), 759-765.
[http://dx.doi.org/10.1111/1523-1747.ep12476328] [PMID: 7684425]
[57]
Oblak, A.; Pohar, J.; Jerala, R. MD-2 determinants of nickel and cobalt-mediated activation of human TLR4. PLoS One, 2015, 10(3) e0120583
[http://dx.doi.org/10.1371/journal.pone.0120583]] [PMID: 25803856]
[58]
Tsou, T.C.; Liou, S.H.; Yeh, S.C.; Tsai, F.Y.; Chao, H.R. Crucial role of Toll-like receptors in the zinc/nickel-induced inflammatory response in vascular endothelial cells. Toxicol. Appl. Pharmacol., 2013, 273(3), 492-499.
[http://dx.doi.org/10.1016/j.taap.2013.09.014] [PMID: 24080332]
[59]
Pestka, J.; Zhou, H. R. Toll-like receptor priming sensitizes macrophages to proinflammatory cytokine gene induction by deoxynivalenol and other toxicants. Toxicological sciences : an official journal of the Society of Toxicology, 2006, 92(2), 445-55.
[http://dx.doi.org/10.1093/toxsci/kfl012]
[60]
Kawai, T.; Akira, S. The role of pattern-recognition receptors in innate immunity: Update on Toll-like receptors. Nat. Immunol., 2010, 11(5), 373-384.
[http://dx.doi.org/10.1038/ni.1863] [PMID: 20404851]
[61]
Adams, J.M.; Cory, S. The Bcl-2 apoptotic switch in cancer development and therapy. Oncogene, 2007, 26(9), 1324-1337.
[http://dx.doi.org/10.1038/sj.onc.1210220] [PMID: 17322918]
[62]
Junttila, M.R.; Evan, G.I. p53--a Jack of all trades but master of none. Nat. Rev. Cancer, 2009, 9(11), 821-829.
[http://dx.doi.org/10.1038/nrc2728] [PMID: 19776747]
[63]
Hanahan, D.; Weinberg, R.A. Hallmarks of cancer: The next generation. Cell, 2011, 144(5), 646-674.
[http://dx.doi.org/10.1016/j.cell.2011.02.013] [PMID: 21376230]
[64]
Maehle, L.; Metcalf, R.A.; Ryberg, D.; Bennett, W.P.; Harris, C.C.; Haugen, A. Altered p53 gene structure and expression in human epithelial cells after exposure to nickel. Cancer Res., 1992, 52(1), 218-221.
[PMID: 1727381]
[65]
Maiuri, M.C.; Zalckvar, E.; Kimchi, A.; Kroemer, G. Self-eating and self-killing: crosstalk between autophagy and apoptosis. Nat. Rev. Mol. Cell Biol., 2007, 8(9), 741-752.
[http://dx.doi.org/10.1038/nrm2239] [PMID: 17717517]
[66]
Orrenius, S.; Kaminskyy, V.O.; Zhivotovsky, B. Autophagy in toxicology: cause or consequence? Annu. Rev. Pharmacol. Toxicol., 2013, 53, 275-297.
[http://dx.doi.org/10.1146/annurev-pharmtox-011112-140210] [PMID: 23072380]
[67]
Shintani, T.; Klionsky, D.J. Autophagy in health and disease: a double-edged sword. Science, 2004, 306(5698), 990-995.
[http://dx.doi.org/10.1126/science.1099993] [PMID: 15528435]
[68]
White, E.; DiPaola, R.S. The double-edged sword of autophagy modulation in cancer. Clin. Cancer Res., 2009, 15(17), 5308-5316.
[http://dx.doi.org/10.1158/1078-0432.CCR-07-5023] [PMID: 19706824]
[69]
Mathew, R.; Karp, C.M.; Beaudoin, B.; Vuong, N.; Chen, G.; Chen, H.Y.; Bray, K.; Reddy, A.; Bhanot, G.; Gelinas, C.; Dipaola, R.S.; Karantza-Wadsworth, V.; White, E. Autophagy suppresses tumorigenesis through elimination of p62. Cell, 2009, 137(6), 1062-1075.
[http://dx.doi.org/10.1016/j.cell.2009.03.048] [PMID: 19524509]
[70]
Huang, H.; Zhu, J.; Li, Y.; Zhang, L.; Gu, J.; Xie, Q.; Jin, H.; Che, X.; Li, J.; Huang, C.; Chen, L.C.; Lyu, J.; Gao, J.; Huang, C. Upregulation of SQSTM1/p62 contributes to nickel-induced malignant transformation of human bronchial epithelial cells. Autophagy, 2016, 12(10), 1687-1703.
[http://dx.doi.org/10.1080/15548627.2016.1196313] [PMID: 27467530]
[71]
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(21), 9926-9930.
[http://dx.doi.org/10.1073/pnas.91.21.9926] [PMID: 7937919]
[72]
Niture, S.K.; Jaiswal, A.K. Nrf2-induced antiapoptotic Bcl-xL protein enhances cell survival and drug resistance. Free Radic. Biol. Med., 2013, 57, 119-131.
[http://dx.doi.org/10.1016/j.freeradbiomed.2012.12.014] [PMID: 23275004]
[73]
Niture, S.K.; Jaiswal, A.K. Nrf2 protein up-regulates antiapoptotic protein Bcl-2 and prevents cellular apoptosis. J. Biol. Chem., 2012, 287(13), 9873-9886.
[http://dx.doi.org/10.1074/jbc.M111.312694] [PMID: 22275372]
[74]
Chan, K.; Han, X.D.; Kan, Y.W. An important function of Nrf2 in combating oxidative stress: detoxification of acetaminophen. Proc. Natl. Acad. Sci. USA, 2001, 98(8), 4611-4616.
[http://dx.doi.org/10.1073/pnas.081082098] [PMID: 11287661]
[75]
Singh, A.; Misra, V.; Thimmulappa, R.K.; Lee, H.; Ames, S.; Hoque, M.O.; Herman, J.G.; Baylin, S.B.; Sidransky, D.; Gabrielson, E.; Brock, M.V.; Biswal, S. Dysfunctional KEAP1-NRF2 interaction in non-small-cell lung cancer. PLoS Med., 2006, 3(10) e420
[http://dx.doi.org/10.1371/journal.pmed.0030420] [PMID: 17020408]
[76]
Stacy, D.R.; Ely, K.; Massion, P.P.; Yarbrough, W.G.; Hallahan, D.E.; Sekhar, K.R.; Freeman, M.L. Increased expression of nuclear factor E2 p45-related factor 2 (NRF2) in head and neck squamous cell carcinomas. Head Neck, 2006, 28(9), 813-818.
[http://dx.doi.org/10.1002/hed.20430] [PMID: 16637057]
[77]
Ishii, T.; Itoh, K.; Takahashi, S.; Sato, H.; Yanagawa, T.; Katoh, Y.; Bannai, S.; Yamamoto, M. Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J. Biol. Chem., 2000, 275(21), 16023-16029.
[http://dx.doi.org/10.1074/jbc.275.21.16023] [PMID: 10821856]
[78]
Edwards, M.R.; Johnson, B.; Mire, C.E.; Xu, W.; Shabman, R.S.; Speller, L.N.; Leung, D.W.; Geisbert, T.W.; Amarasinghe, G.K.; Basler, C.F. The Marburg virus VP24 protein interacts with Keap1 to activate the cytoprotective antioxidant response pathway. Cell Rep., 2014, 6(6), 1017-1025.
[http://dx.doi.org/10.1016/j.celrep.2014.01.043] [PMID: 24630991]
[79]
Wang, X.J.; Sun, Z.; Villeneuve, N.F.; Zhang, S.; Zhao, F.; Li, Y.; Chen, W.; Yi, X.; Zheng, W.; Wondrak, G.T.; Wong, P.K.; Zhang, D.D. Nrf2 enhances resistance of cancer cells to chemotherapeutic drugs, the dark side of Nrf2. Carcinogenesis, 2008, 29(6), 1235-1243.
[http://dx.doi.org/10.1093/carcin/bgn095] [PMID: 18413364]
[80]
Ohta, T.; Iijima, K.; Miyamoto, M.; Nakahara, I.; Tanaka, H.; Ohtsuji, M.; Suzuki, T.; Kobayashi, A.; Yokota, J.; Sakiyama, T.; Shibata, T.; Yamamoto, M.; Hirohashi, S. Loss of Keap1 function activates Nrf2 and provides advantages for lung cancer cell growth. Cancer Res., 2008, 68(5), 1303-1309.
[http://dx.doi.org/10.1158/0008-5472.CAN-07-5003] [PMID: 18316592]
[81]
Tong, K.I.; Katoh, Y.; Kusunoki, H.; Itoh, K.; Tanaka, T.; Yamamoto, M. Keap1 recruits Neh2 through binding to ETGE and DLG motifs: Characterization of the two-site molecular recognition model. Mol. Cell. Biol., 2006, 26(8), 2887-2900.
[http://dx.doi.org/10.1128/MCB.26.8.2887-2900.2006] [PMID: 16581765]
[82]
McMahon, M.; Thomas, N.; Itoh, K.; Yamamoto, M.; Hayes, J.D. Dimerization of substrate adaptors can facilitate cullin-mediated ubiquitylation of proteins by a “tethering” mechanism: a two-site interaction model for the Nrf2-Keap1 complex. J. Biol. Chem., 2006, 281(34), 24756-24768.
[http://dx.doi.org/10.1074/jbc.M601119200] [PMID: 16790436]
[83]
Sporn, M.B.; Liby, K.T. NRF2 and cancer: The good, the bad and the importance of context. Nat. Rev. Cancer, 2012, 12(8), 564-571.
[http://dx.doi.org/10.1038/nrc3278] [PMID: 22810811]
[84]
Zhang, P.; Singh, A.; Yegnasubramanian, S.; Esopi, D.; Kombairaju, P.; Bodas, M.; Wu, H.; Bova, S.G.; Biswal, S. Loss of Kelch-like ECH-associated protein 1 function in prostate cancer cells causes chemoresistance and radioresistance and promotes tumor growth. Mol. Cancer Ther., 2010, 9(2), 336-346.
[http://dx.doi.org/10.1158/1535-7163.MCT-09-0589] [PMID: 20124447]
[85]
Jiang, T.; Chen, N.; Zhao, F.; Wang, X.J.; Kong, B.; Zheng, W.; Zhang, D.D. High levels of Nrf2 determine chemoresistance in type II endometrial cancer. Cancer Res., 2010, 70(13), 5486-5496.
[http://dx.doi.org/10.1158/0008-5472.CAN-10-0713] [PMID: 20530669]
[86]
Komatsu, M. Potential role of p62 in tumor development. Autophagy, 2011, 7(9), 1088-1090.
[http://dx.doi.org/10.4161/auto.7.9.16474] [PMID: 21617386]
[87]
Kim, H.L.; Seo, Y.R. Molecular and genomic approach for understanding the gene-environment interaction between Nrf2 deficiency and carcinogenic nickel-induced DNA damage. Oncol. Rep., 2012, 28(6), 1959-1967.
[http://dx.doi.org/10.3892/or.2012.2057] [PMID: 23023193]
[88]
Scanlon, S.E.; Glazer, P.M. Multifaceted control of DNA repair pathways by the hypoxic tumor microenvironment. DNA Repair (Amst.), 2015, 32, 180-189.
[http://dx.doi.org/10.1016/j.dnarep.2015.04.030] [PMID: 25956861]
[89]
Bindra, R.S.; Gibson, S.L.; Meng, A.; Westermark, U.; Jasin, M.; Pierce, A.J.; Bristow, R.G.; Classon, M.K.; Glazer, P.M. Hypoxia-induced down-regulation of BRCA1 expression by E2Fs. Cancer Res., 2005, 65(24), 11597-11604.
[http://dx.doi.org/10.1158/0008-5472.CAN-05-2119] [PMID: 16357170]
[90]
Bindra, R.S.; Glazer, P.M. Co-repression of mismatch repair gene expression by hypoxia in cancer cells: role of the Myc/Max network. Cancer Lett., 2007, 252(1), 93-103.
[http://dx.doi.org/10.1016/j.canlet.2006.12.011] [PMID: 17275176]
[91]
Bindra, R.S.; Glazer, P.M. Repression of RAD51 gene expression by E2F4/p130 complexes in hypoxia. Oncogene, 2007, 26(14), 2048-2057.
[http://dx.doi.org/10.1038/sj.onc.1210001] [PMID: 17001309]
[92]
Lu, Y.; Chu, A.; Turker, M.S.; Glazer, P.M. Hypoxia-induced epigenetic regulation and silencing of the BRCA1 promoter. Mol. Cell. Biol., 2011, 31(16), 3339-3350.
[http://dx.doi.org/10.1128/MCB.01121-10] [PMID: 21670155]
[93]
Lu, Y.; Wajapeyee, N.; Turker, M.S.; Glazer, P.M. Silencing of the DNA mismatch repair gene MLH1 induced by hypoxic stress in a pathway dependent on the histone demethylase LSD1. Cell Rep., 2014, 8(2), 501-513.
[http://dx.doi.org/10.1016/j.celrep.2014.06.035] [PMID: 25043185]
[94]
Scanlon, S.E.; Glazer, P.M. Hypoxic stress facilitates acute activation and chronic downregulation of fanconi anemia proteins. Mol. Cancer Res., 2014, 12(7), 1016-1028.
[http://dx.doi.org/10.1158/1541-7786.MCR-13-0628] [PMID: 24688021]
[95]
Kim, Y.J.; Lee, Y.J.; Kim, H.J.; Kim, H.S.; Kang, M.S.; Lee, S.K.; Park, M.K.; Murata, K.; Kim, H.L.; Seo, Y.R. A molecular mechanism of nickel (II): reduction of nucleotide excision repair activity by structural and functional disruption of p53. Carcinogenesis, 2018, 39(9), 1157-1164.
[http://dx.doi.org/10.1093/carcin/bgy070] [PMID: 29931256]
[96]
Rezvani, H.R.; Mahfouf, W.; Ali, N.; Chemin, C.; Ged, C.; Kim, A.L.; de Verneuil, H.; Taïeb, A.; Bickers, D.R.; Mazurier, F. Hypoxia-inducible factor-1alpha regulates the expression of nucleotide excision repair proteins in keratinocytes. Nucleic Acids Res., 2010, 38(3), 797-809.
[http://dx.doi.org/10.1093/nar/gkp1072] [PMID: 19934262]
[97]
Chan, N.; Ali, M.; McCallum, G.P.; Kumareswaran, R.; Koritzinsky, M.; Wouters, B.G.; Wells, P.G.; Gallinger, S.; Bristow, R.G. Hypoxia provokes base excision repair changes and a repair-deficient, mutator phenotype in colorectal cancer cells. Mol. Cancer Res., 2014, 12(10), 1407-1415.
[http://dx.doi.org/10.1158/1541-7786.MCR-14-0246] [PMID: 25030372]
[98]
Leonard, S.S.; Harris, G.K.; Shi, X. Metal-induced oxidative stress and signal transduction. Free Radic. Biol. Med., 2004, 37(12), 1921-1942.
[http://dx.doi.org/10.1016/j.freeradbiomed.2004.09.010] [PMID: 15544913]
[99]
Koedrith, P.; Seo, Y.R. Advances in carcinogenic metal toxicity and potential molecular markers. Int. J. Mol. Sci., 2011, 12(12), 9576-9595.
[http://dx.doi.org/10.3390/ijms12129576] [PMID: 22272150]
[100]
Joshi, S.; Husain, M.M.; Chandra, R.; Hasan, S.K.; Srivastava, R.C. Hydroxyl radical formation resulting from the interaction of nickel complexes of L-histidine, glutathione or L-cysteine and hydrogen peroxide. Hum. Exp. Toxicol., 2005, 24(1), 13-17.
[http://dx.doi.org/10.1191/0960327105ht493oa] [PMID: 15727051]
[101]
Zarei, M.H.; Hosseini Shirazi, S.F.; Aghvami, M.; Salimi, A.; Pourahmad, J. Analysis of cytotoxic effects of nickel on human blood lymphocytes. Toxicol. Mech. Methods, 2018, 28(2), 79-86.
[http://dx.doi.org/10.1080/15376516.2017.1364314] [PMID: 28774209]
[102]
Stinson, T.J.; Jaw, S.; Jeffery, E.H.; Plewa, M.J. The relationship between nickel chloride-induced peroxidation and DNA strand breakage in rat liver. Toxicol. Appl. Pharmacol., 1992, 117(1), 98-103.
[http://dx.doi.org/10.1016/0041-008X(92)90222-E] [PMID: 1440619]
[103]
Huang, X.; Frenkel, K.; Klein, C.B.; Costa, M. Nickel induces increased oxidants in intact cultured mammalian cells as detected by dichlorofluorescein fluorescence. Toxicol. Appl. Pharmacol., 1993, 120(1), 29-36.
[http://dx.doi.org/10.1006/taap.1993.1083] [PMID: 8511780]
[104]
Wang, Y.F.; Shyu, H.W.; Chang, Y.C.; Tseng, W.C.; Huang, Y.L.; Lin, K.H.; Chou, M.C.; Liu, H.L.; Chen, C.Y. Nickel (II)-induced cytotoxicity and apoptosis in human proximal tubule cells through a ROS- and mitochondria-mediated pathway. Toxicol. Appl. Pharmacol., 2012, 259(2), 177-186.
[http://dx.doi.org/10.1016/j.taap.2011.12.022] [PMID: 22245127]
[105]
Lee, Y.J.; Lim, S.S.; Baek, B.J.; An, J.M.; Nam, H.S.; Woo, K.M.; Cho, M.K.; Kim, S.H.; Lee, S.H. Nickel(II)-induced nasal epithelial toxicity and oxidative mitochondrial damage. Environ. Toxicol. Pharmacol., 2016, 42, 76-84.
[http://dx.doi.org/10.1016/j.etap.2016.01.005] [PMID: 26809061]
[106]
Park, J.; Lee, J.; Choi, C. Mitochondrial network determines intracellular ROS dynamics and sensitivity to oxidative stress through switching inter-mitochondrial messengers. PLoS One, 2011, 6(8) e23211
[http://dx.doi.org/10.1371/journal.pone.0023211] [PMID: 21829717]
[107]
Otera, H.; Mihara, K. Molecular mechanisms and physiologic functions of mitochondrial dynamics. J. Biochem., 2011, 149(3), 241-251.
[http://dx.doi.org/10.1093/jb/mvr002] [PMID: 21233142]
[108]
Li, Y.; Lu, X.; Qi, H.; Li, X.; Xiao, X.; Gao, J. Ursolic acid induces apoptosis through mitochondrial intrinsic pathway and suppression of ERK1/2 MAPK in HeLa cells. J. Pharmacol. Sci., 2014, 125(2), 202-210.
[http://dx.doi.org/10.1254/jphs.14017FP] [PMID: 24881958]
[109]
Lee, J.W.; Kim, W.H.; Lim, J.H.; Song, E.H.; Song, J.; Choi, K.Y.; Jung, M.H. Mitochondrial dysfunction: Glucokinase downregulation lowers interaction of glucokinase with mitochondria, resulting in apoptosis of pancreatic beta-cells. Cell. Signal., 2009, 21(1), 69-78.
[http://dx.doi.org/10.1016/j.cellsig.2008.09.015] [PMID: 18940247]
[110]
Shackelford, R.E.; Kaufmann, W.K.; Paules, R.S. Oxidative stress and cell cycle checkpoint function. Free Radic. Biol. Med., 2000, 28(9), 1387-1404.
[http://dx.doi.org/10.1016/S0891-5849(00)00224-0] [PMID: 10924858]
[111]
Zhong, W.; Oberley, L.W.; Oberley, T.D.; St Clair, D.K. Suppression of the malignant phenotype of human glioma cells by overexpression of manganese superoxide dismutase. Oncogene, 1997, 14(4), 481-490.
[http://dx.doi.org/10.1038/sj.onc.1200852] [PMID: 9053845]
[112]
Long, D.J., II; Waikel, R.L.; Wang, X.J.; Perlaky, L.; Roop, D.R.; Jaiswal, A.K. NAD(P)H:quinone oxidoreductase 1 deficiency increases susceptibility to benzo(a)pyrene-induced mouse skin carcinogenesis. Cancer Res., 2000, 60(21), 5913-5915.
[PMID: 11085502]
[113]
Li, J.J.; Oberley, L.W.; Fan, M.; Colburn, N.H. Inhibition of AP-1 and NF-kappaB by manganese-containing superoxide dismutase in human breast cancer cells. FASEB J., 1998, 12(15), 1713-1723.
[http://dx.doi.org/10.1096/fasebj.12.15.1713] [PMID: 9837861]
[114]
Sen, C.K.; Packer, L. Antioxidant and redox regulation of gene transcription. FASEB J., 1996, 10(7), 709-720.
[http://dx.doi.org/10.1096/fasebj.10.7.8635688] [PMID: 8635688]
[115]
Lander, H.M. An essential role for free radicals and derived species in signal transduction. FASEB J., 1997, 11(2), 118-124.
[http://dx.doi.org/10.1096/fasebj.11.2.9039953] [PMID: 9039953]
[116]
Wiseman, H.; Halliwell, B. Damage to DNA by reactive oxygen and nitrogen species: role in inflammatory disease and progression to cancer. Biochem. J., 1996, 313(Pt. 1), 17-29.
[http://dx.doi.org/10.1042/bj3130017] [PMID: 8546679]
[117]
Costa, M. Molecular mechanisms of nickel carcinogenesis. Annu. Rev. Pharmacol. Toxicol., 1991, 31, 321-337.
[http://dx.doi.org/10.1146/annurev.pa.31.040191.001541] [PMID: 2064378]
[118]
Ellen, T.P.; Kluz, T.; Harder, M.E.; Xiong, J.; Costa, M. Heterochromatinization as a potential mechanism of nickel-induced carcinogenesis. Biochemistry, 2009, 48(21), 4626-4632.
[http://dx.doi.org/10.1021/bi900246h] [PMID: 19338343]
[119]
Costa, M.; Davidson, T.L.; Chen, H.; Ke, Q.; Zhang, P.; Yan, Y.; Huang, C.; Kluz, T. Nickel carcinogenesis: epigenetics and hypoxia signaling. Mutat. Res., 2005, 592(1-2), 79-88.
[http://dx.doi.org/10.1016/j.mrfmmm.2005.06.008] [PMID: 16009382]
[120]
M’Bemba-Meka, P.; Lemieux, N.; Chakrabarti, S.K. Nickel compound-induced DNA single-strand breaks in chromosomal and nuclear chromatin in human blood lymphocytes in vitro: role of oxidative stress and intracellular calcium. Mutat. Res., 2005, 586(2), 124-137.
[http://dx.doi.org/10.1016/j.mrgentox.2005.06.001] [PMID: 16099703]
[121]
Latvala, S.; Hedberg, J.; Di Bucchianico, S.; Möller, L.; Odnevall Wallinder, I.; Elihn, K.; Karlsson, H.L. Nickel Release, ROS Generation and Toxicity of Ni and NiO Micro- and Nanoparticles. PLoS One, 2016, 11(7) e0159684
[http://dx.doi.org/10.1371/journal.pone.0159684] [PMID: 27434640]
[122]
Schwerdtle, T.; Seidel, A.; Hartwig, A. Effect of soluble and particulate nickel compounds on the formation and repair of stable benzo[a]pyrene DNA adducts in human lung cells. Carcinogenesis, 2002, 23(1), 47-53.
[http://dx.doi.org/10.1093/carcin/23.1.47] [PMID: 11756222]
[123]
Chen, Q.Y.; DesMarais, T.; Costa, M. Metals and Mechanisms of Carcinogenesis. Annu. Rev. Pharmacol. Toxicol., 2019, 59, 537-554.
[http://dx.doi.org/10.1146/annurev-pharmtox-010818-021031] [PMID: 30625284]

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