Molecular features in arsenic-induced lung tumors

Molecular Cancer

Volumn 12, Issue 1, 2013, Pages

  Hubaux, Roland ^a   Becker Santos, Daiana D ^a   Enfield, Katey S S ^a   Rowbotham, David ^a   Lam, Stephen ^a   Lam, Wan L ^a   Martinez, Victor D ^a  

^a BRITISH COLUMBIA CANCER RESEARCH CENTRE   (Canada)

Author keywords

Arsenic; Arsenite; Epidermal growth factor receptor; Epigenetic; Lung cancer; NFE2 related factor 2; Phosphatidylinositol 3 kinases; Reactive oxygen species

Indexed keywords

ARSENIC; ARSENIC TRIOXIDE; CYCLIN DEPENDENT KINASE INHIBITOR 2A; DRINKING WATER; EPIDERMAL GROWTH FACTOR RECEPTOR; KELCH LIKE ECH ASSOCIATED PROTEIN 1; MICRORNA; MICRORNA 124; MICRORNA 125B; MICRORNA 181B; MICRORNA 9; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN C JUN; PROTEIN KINASE B; PROTEIN P53; PROTEIN TYROSINE KINASE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; S ADENOSYLMETHIONINE; STAT3 PROTEIN; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG;

CANADA; CHROMOSOMAL INSTABILITY; CPG ISLAND; DEAMINATION; DNA ALKYLATION; DNA DAMAGE; DNA REPAIR; DOUBLE STRANDED DNA BREAK; ENZYME ACTIVATION; EPIGENETICS; GENOMIC INSTABILITY; HUMAN; LUNG CANCER; LUNG CARCINOGENESIS; NONHUMAN; REVIEW; SIGNAL TRANSDUCTION; UNITED STATES;

ANIMALS; ARSENIC; DNA DAMAGE; EPIGENESIS, GENETIC; GENOMIC INSTABILITY; HUMANS; LUNG NEOPLASMS; MUTAGENS; SIGNAL TRANSDUCTION; WATER POLLUTANTS, CHEMICAL;

EID: 84875048855     PISSN: None     EISSN: 14764598     Source Type: Journal    
DOI: 10.1186/1476-4598-12-20     Document Type: Review

References (122)

1. IARC Some drinking-water disinfectants and contaminants, including arsenic. Monographs on chloramine, chloral and chloral hydrate, dichloroacetic acid, trichloroacetic acid and 3-chloro-4-(dichloromethyl)-5-hydroxy-2(5H)-furanone. IARC Monogr Eval Carcinog Risks Hum 2004, 84:269-477. IARC.
2. Smedley PL, Kinniburgh DG. A review of the source, behaviour and distribution of arsenic in natural waters. Appl Geochem 2002, 17:517-568.
3. Smith AH, Lingas EO, Mahfuzar R. Contamination of drinking-water by arsenic in bangladesh: a public health emergency. Bull World Health Organ 2000, 78:1093-1103. 2560840, 11019458.
4. Putila JJ, Guo NL. Association of arsenic exposure with lung cancer incidence rates in the united states. PLoS One 2011, 6:e25886. 10.1371/journal.pone.0025886, 3189216, 22003413.
5. U. S. Environmental Protection Agency National primary drinking water regulations; arsenic and clarifications to compliance and New source contaminants monitoring; final rule. Book national primary drinking water regulations; arsenic and clarifications to compliance and New source contaminants monitoring; final rule vol. 66 2001, 6975. U. S. Environmental Protection Agency.
6. Kumar A, Adak P, Gurian PL, Lockwood JR. Arsenic exposure in US public and domestic drinking water supplies: a comparative risk assessment. J Expo Sci Environ Epidemiol 2010, 20:245-254. 10.1038/jes.2009.24, 19401722.
7. Nieder AM, MacKinnon JA, Fleming LE, Kearney G, Hu JJ, Sherman RL, Huang Y, Lee DJ. Bladder cancer clusters in florida: identifying populations at risk. J Urol 2009, 182:46-50. discussion 51, 10.1016/j.juro.2009.02.149, 19450849.
8. Iland HJ, Seymour JF. Role of arsenic trioxide in acute promyelocytic leukemia. Curr Treat Options Oncol 2013, [Epub ahead of print].
9. Mi J. Current treatment strategy of acute promyelocytic leukemia. Frontiers of medicine 2011, 5:341-347. 10.1007/s11684-011-0169-z, 22198746.
10. McGuigan CF, Hamula CLA, Huang S, Gabos S, Le XC. A review on arsenic concentrations in canadian drinking water. Environmental Reviews 2010, 18:291-307.
11. Ryker SJ. Mapping arsenic in groundwater. Geotimes 2001, 46:34-36.
12. Nordstrom DK. Public health. Worldwide occurrences of arsenic in ground water. Science 2002, 296:2143-2145. 10.1126/science.1072375, 12077387.
13. Smith AH, Hopenhayn-Rich C, Bates MN, Goeden HM, Hertz-Picciotto I, Duggan HM, Wood R, Kosnett MJ, Smith MT. Cancer risks from arsenic in drinking water. Environ Health Perspect 1992, 97:259-267. 1519547, 1396465.
14. Mead MN. Arsenic: in search of an antidote to a global poison. Environ Health Perspect 2005, 113:A378-386. 10.1289/ehp.113-a378, 1257621, 15929879.
15. Guo HR, Wang NS, Hu H, Monson RR. Cell type specificity of lung cancer associated with arsenic ingestion. Cancer epidemiology, biomarkers & prevention: a publication of the American Association for Cancer Research, cosponsored by the American Society of Preventive Oncology 2004, 13:638-643. 3616171, 23569499.
16. Barrett JC, Lamb PW, Wiseman RW. Multiple mechanisms for the carcinogenic effects of asbestos and other mineral fibers. Environ Health Perspect 1989, 81:81-89. 1567531, 2667990.
17. Ebert F, Weiss A, Bultemeyer M, Hamann I, Hartwig A, Schwerdtle T. Arsenicals affect base excision repair by several mechanisms. Mutat Res 2011, 715:32-41. 10.1016/j.mrfmmm.2011.07.004, 21782832.
18. Pomroy C, Charbonneau SM, McCullough RS, Tam GK. Human retention studies with 74As. Toxicol Appl Pharmacol 1980, 53:550-556. 10.1016/0041-008X(80)90368-3, 7385250.
19. Wang Y, Fang J, Leonard SS, Rao KM. Cadmium inhibits the electron transfer chain and induces reactive oxygen species. Free Radic Biol Med 2004, 36:1434-1443. 10.1016/j.freeradbiomed.2004.03.010, 15135180.
20. Dilda PJ, Hogg PJ. Arsenical-based cancer drugs. Cancer Treat Rev 2007, 33:542-564. 10.1016/j.ctrv.2007.05.001, 17624680.
21. Nemeti B, Regonesi ME, Tortora P, Gregus Z. Polynucleotide phosphorylase and mitochondrial ATP synthase mediate reduction of arsenate to the more toxic arsenite by forming arsenylated analogues of ADP and ATP. Toxicological sciences: an official journal of the Society of Toxicology 2010, 117:270-281.
22. Kala SV, Neely MW, Kala G, Prater CI, Atwood DW, Rice JS, Lieberman MW. The MRP2/cMOAT transporter and arsenic-glutathione complex formation are required for biliary excretion of arsenic. J Biol Chem 2000, 275:33404-33408. 10.1074/jbc.M007030200, 10938093.
23. Cullen WR, Reimer KJ. Arsenic speciation in the environment. Chem Rev 1989, 89:713.
24. Styblo M, Drobna Z, Jaspers I, Lin S, Thomas DJ. The role of biomethyl-ation in toxicity and carcinogenicity of arsenic: a research update. Environ Health Persp 2002, 110:767.
25. Thomas DJ, Styblo M, Lin S. The cellular metabolism and systemic toxicity of arsenic. Toxicol Appl Pharmacol 2001, 176:127-144. 10.1006/taap.2001.9258, 11601889.
26. Klein CB, Leszczynska J, Hickey C, Rossman TG. Further evidence against a direct genotoxic mode of action for arsenic-induced cancer. Toxicol Appl Pharmacol 2007, 222:289-297. 10.1016/j.taap.2006.12.033, 1986829, 17316729.
27. Kligerman AD, Doerr CL, Tennant AH, Harrington-Brock K, Allen JW, Winkfield E, Poorman-Allen P, Kundu B, Funasaka K, Roop BC. Methylated trivalent arsenicals as candidate ultimate genotoxic forms of arsenic: induction of chromosomal mutations but not gene mutations. Environ Mol Mutagen 2003, 42:192-205. 10.1002/em.10192, 14556226.
28. Rossman TG, Klein CB. Genetic and epigenetic effects of environmental arsenicals. Metallomics: integrated biometal science 2011, 3:1135-1141.
29. Rossman TG, Uddin AN, Burns FJ. Evidence that arsenite acts as a cocarcinogen in skin cancer. Toxicol Appl Pharmacol 2004, 198:394-404. 10.1016/j.taap.2003.10.016, 15276419.
30. Hartwig A, Groblinghoff UD, Beyersmann D, Natarajan AT, Filon R, Mullenders LH. Interaction of arsenic(III) with nucleotide excision repair in UV-irradiated human fibroblasts. Carcinogenesis 1997, 18:399-405. 10.1093/carcin/18.2.399, 9054635.
31. Jha AN, Noditi M, Nilsson R, Natarajan AT. Genotoxic effects of sodium arsenite on human cells. Mutat Res 1992, 284:215-221. 10.1016/0027-5107(92)90005-M, 1281272.
32. Wiencke JK, Yager JW. Specificity of arsenite in potentiating cytogenetic damage induced by the DNA crosslinking agent diepoxybutane. Environ Mol Mutagen 1992, 19:195-200. 10.1002/em.2850190303, 1572342.
33. Li JH, Rossman TG. Mechanism of comutagenesis of sodium arsenite with n-methyl-n-nitrosourea. Biol Trace Elem Res 1989, 21:373-381. 10.1007/BF02917278, 2484616.
34. Lee TC, Huang RY, Jan KY. Sodium arsenite enhances the cytotoxicity, clastogenicity, and 6-thioguanine-resistant mutagenicity of ultraviolet light in chinese hamster ovary cells. Mutat Res 1985, 148:83-89. 10.1016/0027-5107(85)90210-6, 3969080.
35. Flora SJ. Arsenic-induced oxidative stress and its reversibility. Free Radic Biol Med 2011, 51:257-281. 10.1016/j.freeradbiomed.2011.04.008, 21554949.
36. Rossman TG. Mechanism of arsenic carcinogenesis: an integrated approach. Mutat Res 2003, 533:37-65. 10.1016/j.mrfmmm.2003.07.009, 14643412.
37. Naranmandura H, Xu S, Sawata T, Hao WH, Liu H, Bu N, Ogra Y, Lou YJ, Suzuki N. Mitochondria are the main target organelle for trivalent monomethylarsonous acid (MMA(III))-induced cytotoxicity. Chem Res Toxicol 2011, 24:1094-1103. 10.1021/tx200156k, 21648415.
38. Turrens JF. Superoxide production by the mitochondrial respiratory chain. Biosci Rep 1997, 17:3-8. 10.1023/A:1027374931887, 9171915.
39. Kitchin KT, Wallace K. Evidence against the nuclear in situ binding of arsenicals-oxidative stress theory of arsenic carcinogenesis. Toxicol Appl Pharmacol 2008, 232:252-257. 10.1016/j.taap.2008.06.021, 18671993.
40. Halliwell B. Oxidative stress and cancer: have we moved forward?. Biochem J 2007, 401:1-11.
41. Martinez VD, Vucic EA, Becker-Santos DD, Gil L, Lam WL. Arsenic exposure and the induction of human cancers. J Toxicol 2011, 2011:431287. 3235889, 22174709.
42. Gurr J-R, Yih L-H, Samikkannu T, Bau D-T, Lin S-Y, Jan K-Y. Nitric oxide production by arsenite. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 2003, 533:173-182.
43. Wink DA, Kasprzak KS, Maragos CM, Elespuru RK, Misra M, Dunams TM, Cebula TA, Koch WH, Andrews AW, Allen JS. DNA deaminating ability and genotoxicity of nitric oxide and its progenitors. Science 1991, 254:1001-1003. 10.1126/science.1948068, 1948068.
44. Radi R, Beckman JS, Bush KM, Freeman BA. Peroxynitrite oxidation of sulfhydryls. The cytotoxic potential of superoxide and nitric oxide. The Journal of biological chemistry 1991, 266:4244-4250.
45. Leaf CD, Wishnok JS, Tannenbaum SR. Endogenous incorporation of nitric oxide from L-arginine into N-nitrosomorpholine stimulated by escherichia coli lipopolysaccharide in the rat. Carcinogenesis 1991, 12:537-539. 10.1093/carcin/12.3.537, 1849054.
46. Tsuda M, Kurashima Y. Tobacco smoking, chewing, and snuff dipping: factors contributing to the endogenous formation of N-nitroso compounds. Crit Rev Toxicol 1991, 21:243-253. 10.3109/10408449109017912, 2069710.
47. Beckman JS, Beckman TW, Chen J, Marshall PA, Freeman BA. Apparent hydroxyl radical production by peroxynitrite: implications for endothelial injury from nitric oxide and superoxide. Proc Natl Acad Sci USA 1990, 87:1620-1624. 10.1073/pnas.87.4.1620, 53527, 2154753.
48. Andrew AS, Karagas MR, Hamilton JW. Decreased DNA repair gene expression among individuals exposed to arsenic in united states drinking water. Int J Cancer 2003, 104:263-268. 10.1002/ijc.10968, 12569548.
49. Andrew AS, Burgess JL, Meza MM, Demidenko E, Waugh MG, Hamilton JW, Karagas MR. Arsenic exposure is associated with decreased DNA repair in vitro and in individuals exposed to drinking water arsenic. Environ Health Perspect 2006, 114:1193-1198. 10.1289/ehp.9008, 1552016, 16882524.
50. Nollen M, Ebert F, Moser J, Mullenders LH, Hartwig A, Schwerdtle T. Impact of arsenic on nucleotide excision repair: XPC function, protein level, and gene expression. Mol Nutr Food Res 2009, 53:572-582. 10.1002/mnfr.200800480, 19382146.
51. Walter I, Schwerdtle T, Thuy C, Parsons JL, Dianov GL, Hartwig A. Impact of arsenite and its methylated metabolites on PARP-1 activity, PARP-1 gene expression and poly(ADP-ribosyl)ation in cultured human cells. DNA Repair 2007, 6:61-70. 10.1016/j.dnarep.2006.08.008, 17011244.
52. Osmond MJ, Kunz BA, Snow ET. Age and exposure to arsenic alter base excision repair transcript levels in mice. Mutagenesis 2010, 25:517-522. 10.1093/mutage/geq037, 20643705.
53. Wen G, Calaf GM, Partridge MA, Echiburu-Chau C, Zhao Y, Huang S, Chai Y, Li B, Hu B, Hei TK. Neoplastic transformation of human small airway epithelial cells induced by arsenic. Mol Med 2008, 14:2-10. 2082132, 18037969.
54. Zhao Y, Toselli P, Li W. Microtubules as a critical target for arsenic toxicity in lung cells in vitro and in vivo. Int J Environ Res Public Health 2012, 9:474-495. 10.3390/ijerph9020474, 3315258, 22470304.
55. Sciandrello G, Caradonna F, Mauro M, Barbata G. Arsenic-induced DNA hypomethylation affects chromosomal instability in mammalian cells. Carcinogenesis 2004, 25:413-417.
56. Sciandrello G, Barbaro R, Caradonna F, Barbata G. Early induction of genetic instability and apoptosis by arsenic in cultured chinese hamster cells. Mutagenesis 2002, 17:99-103. 10.1093/mutage/17.2.99, 11880537.
57. Vega L, Gonsebatt ME, Ostrosky-Wegman P. Aneugenic effect of sodium arsenite on human lymphocytes in vitro: an individual susceptibility effect detected. Mutat Res 1995, 334:365-373. 10.1016/0165-1161(95)90074-8, 7753100.
58. Vogt BL, Rossman TG. Effects of arsenite on p53, p21 and cyclin D expression in normal human fibroblasts - a possible mechanism for arsenite's comutagenicity. Mutation Research/Fundamental and Molecular Mechanisms of Mutagenesis 2001, 478:159-168.
59. Tang F, Liu G, He Z, Ma WY, Bode AM, Dong Z. Arsenite inhibits p53 phosphorylation, DNA binding activity, and p53 target gene p21 expression in mouse epidermal JB6 cells. Mol Carcinog 2006, 45:861-870. 10.1002/mc.20245, 16739126.
60. Huang Y, Zhang J, McHenry KT, Kim MM, Zeng W, Lopez-Pajares V, Dibble CC, Mizgerd JP, Yuan ZM. Induction of cytoplasmic accumulation of p53: a mechanism for low levels of arsenic exposure to predispose cells for malignant transformation. Cancer Res 2008, 68:9131-9136. 10.1158/0008-5472.CAN-08-3025, 2717853, 19010883.
61. Komissarova EV, Rossman TG. Arsenite induced poly(ADP-ribosyl)ation of tumor suppressor P53 in human skin keratinocytes as a possible mechanism for carcinogenesis associated with arsenic exposure. Toxicol Appl Pharmacol 2010, 243:399-404. 10.1016/j.taap.2009.12.014, 2830301, 20036271.
62. Qin XJ, Liu W, Li YN, Sun X, Hai CX, Hudson LG, Liu KJ. Poly(ADP-ribose) polymerase-1 inhibition by arsenite promotes the survival of cells with unrepaired DNA lesions induced by UV exposure. Toxicological sciences: an official journal of the Society of Toxicology 2012, 127:120-129.
63. Martinez VD, Buys TP, Adonis M, Benitez H, Gallegos I, Lam S, Lam WL, Gil L. Arsenic-related DNA copy-number alterations in lung squamous cell carcinomas. Br J Cancer 2010, 103:1277-1283. 10.1038/sj.bjc.6605879, 2967055, 20842114.
64. Tonon G, Wong KK, Maulik G, Brennan C, Feng B, Zhang Y, Khatry DB, Protopopov A, You MJ, Aguirre AJ. High-resolution genomic profiles of human lung cancer. Proc Natl Acad Sci USA 2005, 102:9625-9630. 10.1073/pnas.0504126102, 1160520, 15983384.
65. Venkatesan RN, Treuting PM, Fuller ED, Goldsby RE, Norwood TH, Gooley TA, Ladiges WC, Preston BD, Loeb LA. Mutation at the polymerase active site of mouse DNA polymerase delta increases genomic instability and accelerates tumorigenesis. Mol Cell Biol 2007, 27:7669-7682. 10.1128/MCB.00002-07, 2169052, 17785453.
66. Parsons JL, Preston BD, O'Connor TR, Dianov GL. DNA polymerase delta-dependent repair of DNA single strand breaks containing 3'-end proximal lesions. Nucleic Acids Res 2007, 35:1054-1063. 10.1093/nar/gkl1115, 1851633, 17264132.
67. Goldsby RE, Hays LE, Chen X, Olmsted EA, Slayton WB, Spangrude GJ, Preston BD. High incidence of epithelial cancers in mice deficient for DNA polymerase delta proofreading. Proc Natl Acad Sci USA 2002, 99:15560-15565. 10.1073/pnas.232340999, 137756, 12429860.
68. Simeonova PP, Luster MI. Mechanisms of arsenic carcinogenicity: genetic or epigenetic mechanisms?. J Environ Pathol Toxicol Oncol 2000, 19:281-286.
69. Mazumder DN. Effect of chronic intake of arsenic-contaminated water on liver. Toxicol Appl Pharmacol 2005, 206:169-175. 10.1016/j.taap.2004.08.025, 15967205.
70. Tseng CH, Chong CK, Chen CJ, Tai TY. Dose-response relationship between peripheral vascular disease and ingested inorganic arsenic among residents in blackfoot disease endemic villages in taiwan. Atherosclerosis 1996, 120:125-133. 10.1016/0021-9150(95)05693-9, 8645353.
71. Engel RR, Hopenhayn-Rich C, Receveur O, Smith AH. Vascular effects of chronic arsenic exposure: a review. Epidemiol Rev 1994, 16:184-209.
72. Intarasunanont P, Navasumrit P, Woraprasit S, Chaisatra K, Suk WA, Mahidol C, Ruchirawat M. Effects of arsenic exposure on DNA methylation in cord blood samples from newborn babies and in a human lymphoblast cell line. Environmental health: a global access science source 2012, 11:31.
73. Jensen TJ, Wozniak RJ, Eblin KE, Wnek SM, Gandolfi AJ, Futscher BW. Epigenetic mediated transcriptional activation of WNT5A participates in arsenical-associated malignant transformation. Toxicol Appl Pharmacol 2009, 235:39-46. 10.1016/j.taap.2008.10.013, 19061910.
74. Reichard JF, Puga A. Effects of arsenic exposure on DNA methylation and epigenetic gene regulation. Epigenomics 2010, 2:87-104. 10.2217/epi.09.45, 2877392, 20514360.
75. Cui X, Wakai T, Shirai Y, Hatakeyama K, Hirano S. Chronic oral exposure to inorganic arsenate interferes with methylation status of p16INK4a and RASSF1A and induces lung cancer in a/J mice. Toxicological sciences: an official journal of the Society of Toxicology 2006, 91:372-381.
76. Marsit CJ, Eddy K, Kelsey KT. MicroRNA responses to cellular stress. Cancer Res 2006, 66:10843-10848. 10.1158/0008-5472.CAN-06-1894, 17108120.
77. Zhao CQ, Young MR, Diwan BA, Coogan TP, Waalkes MP. Association of arsenic-induced malignant transformation with DNA hypomethylation and aberrant gene expression. Proc Natl Acad Sci USA 1997, 94:10907-10912. 10.1073/pnas.94.20.10907, 23527, 9380733.
78. Mass MJ, Wang L. Arsenic alters cytosine methylation patterns of the promoter of the tumor suppressor gene p53 in human lung cells: a model for a mechanism of carcinogenesis. Mutat Res 1997, 386:263-277. 10.1016/S1383-5742(97)00008-2, 9219564.
79. Chiang PK, Gordon RK, Tal J, Zeng GC, Doctor BP, Pardhasaradhi K, McCann PP. S-adenosylmethionine and methylation. FASEB journal: official publication of the Federation of American Societies for Experimental Biology 1996, 10:471-480.
80. Jensen TJ, Novak P, Eblin KE, Gandolfi AJ, Futscher BW. Epigenetic remodeling during arsenical-induced malignant transformation. Carcinogenesis 2008, 29:1500-1508. 10.1093/carcin/bgn102, 2516486, 18448484.
81. Ren X, McHale CM, Skibola CF, Smith AH, Smith MT, Zhang L. An emerging role for epigenetic dysregulation in arsenic toxicity and carcinogenesis. Environ Health Perspect 2011, 119:11-19. 3018488, 20682481.
82. Salnikow K, Zhitkovich A. Genetic and epigenetic mechanisms in metal carcinogenesis and cocarcinogenesis: nickel, arsenic, and chromium. Chem Res Toxicol 2008, 21:28-44. 10.1021/tx700198a, 2602826, 17970581.
83. Loenen WA. S-adenosylmethionine: jack of all trades and master of everything?. Biochem Soc Trans 2006, 34:330-333.
84. Chen WT, Hung WC, Kang WY, Huang YC, Chai CY. Urothelial carcinomas arising in arsenic-contaminated areas are associated with hypermethylation of the gene promoter of the death-associated protein kinase. Histopathology 2007, 51:785-792. 10.1111/j.1365-2559.2007.02871.x, 17953697.
85. Chai CY, Huang YC, Hung WC, Kang WY, Chen WT. Arsenic salts induced autophagic cell death and hypermethylation of DAPK promoter in SV-40 immortalized human uroepithelial cells. Toxicol Lett 2007, 173:48-56. 10.1016/j.toxlet.2007.06.006, 17683884.
86. Vogt BL, Rossman TG. Effects of arsenite on p53, p21 and cyclin D expression in normal human fibroblasts - a possible mechanism for arsenite's comutagenicity. Mutat Res 2001, 478:159-168. 10.1016/S0027-5107(01)00137-3, 11406180.
87. Ziech D, Franco R, Pappa A, Panayiotidis MI. Reactive oxygen species (ROS)-induced genetic and epigenetic alterations in human carcinogenesis. Mutat Res 2011, 711:167-173. 10.1016/j.mrfmmm.2011.02.015, 21419141.
88. Chanda S, Dasgupta UB, Guhamazumder D, Gupta M, Chaudhuri U, Lahiri S, Das S, Ghosh N, Chatterjee D. DNA hypermethylation of promoter of gene p53 and p16 in arsenic-exposed people with and without malignancy. Toxicological sciences: an official journal of the Society of Toxicology 2006, 89:431-437.
89. Jo WJ, Ren X, Chu F, Aleshin M, Wintz H, Burlingame A, Smith MT, Vulpe CD, Zhang L. Acetylated H4K16 by MYST1 protects UROtsa cells from arsenic toxicity and is decreased following chronic arsenic exposure. Toxicol Appl Pharmacol 2009, 241:294-302. 10.1016/j.taap.2009.08.027, 2784148, 19732783.
90. Zhou X, Sun H, Ellen TP, Chen H, Costa M. Arsenite alters global histone H3 methylation. Carcinogenesis 2008, 29:1831-1836. 10.1093/carcin/bgn063, 2722848, 18321869.
91. Wang Z, Zhao Y, Smith E, Goodall GJ, Drew PA, Brabletz T, Yang C. Reversal and prevention of arsenic-induced human bronchial epithelial cell malignant transformation by microRNA-200b. Toxicological sciences: an official journal of the Society of Toxicology 2011, 121:110-122.
92. Cui Y, Han Z, Hu Y, Song G, Hao C, Xia H, Ma X. MicroRNA-181b and microRNA-9 mediate arsenic-induced angiogenesis via NRP1. J Cell Physiol 2012, 227:772-783. 10.1002/jcp.22789, 21503876.
93. Yarden Y, Sliwkowski MX. Untangling the ErbB signalling network. Nat Rev Mol Cell Biol 2001, 2:127-137. 10.1038/35052073, 11252954.
94. Andrew AS, Mason RA, Memoli V, Duell EJ. Arsenic activates EGFR pathway signaling in the lung. Toxicological sciences: an official journal of the Society of Toxicology 2009, 109:350-357.
95. Sung TI, Wang YJ, Chen CY, Hung TL, Guo HR. Increased serum level of epidermal growth factor receptor in liver cancer patients and its association with exposure to arsenic. Sci Total Environ 2012, 424:74-78.
96. Biscardi JS, Maa MC, Tice DA, Cox ME, Leu TH, Parsons SJ. c-Src-mediated phosphorylation of the epidermal growth factor receptor on Tyr845 and Tyr1101 is associated with modulation of receptor function. J Biol Chem 1999, 274:8335-8343. 10.1074/jbc.274.12.8335, 10075741.
97. Tice DA, Biscardi JS, Nickles AL, Parsons SJ. Mechanism of biological synergy between cellular Src and epidermal growth factor receptor. Proc Natl Acad Sci USA 1999, 96:1415-1420. 10.1073/pnas.96.4.1415, 15477, 9990038.
98. Simeonova PP, Luster MI. Arsenic carcinogenicity: relevance of c-Src activation. Mol Cell Biochem 2002, 234-235:277-282. 2899892, 19444596.
99. Li G, Lee LS, Li M, Tsao SW, Chiu JF. Molecular changes during arsenic-induced cell transformation. J Cell Physiol 2011, 226:3225-3232. 10.1002/jcp.22683, 21344382.
100. Liu LZ, Jiang Y, Carpenter RL, Jing Y, Peiper SC, Jiang BH. Role and mechanism of arsenic in regulating angiogenesis. PLoS One 2011, 6:e20858. 10.1371/journal.pone.0020858, 3110823, 21687637.
101. Cheng HY, Li P, David M, Smithgall TE, Feng L, Lieberman MW. Arsenic inhibition of the JAK-STAT pathway. Oncogene 2004, 23:3603-3612. 10.1038/sj.onc.1207466, 15116095.
102. Liu J, Chen B, Lu Y, Guan Y, Chen F. JNK-dependent Stat3 phosphorylation contributes to Akt activation in response to arsenic exposure. Toxicological sciences: an official journal of the Society of Toxicology 2012, 129:363-371.
103. Herbert KJ, Snow ET. Modulation of arsenic-induced epidermal growth factor receptor pathway signalling by resveratrol. Chem Biol Interact 2012, 198:38-48. 10.1016/j.cbi.2012.05.004, 22634503.
104. Verma A, Mohindru M, Deb DK, Sassano A, Kambhampati S, Ravandi F, Minucci S, Kalvakolanu DV, Platanias LC. Activation of Rac1 and the p38 mitogen-activated protein kinase pathway in response to arsenic trioxide. J Biol Chem 2002, 277:44988-44995. 10.1074/jbc.M207176200, 12239215.
105. Cheng L, Alexander RE, Maclennan GT, Cummings OW, Montironi R, Lopez-Beltran A, Cramer HM, Davidson DD, Zhang S. Molecular pathology of lung cancer: key to personalized medicine. Modern pathology: an official journal of the United States and Canadian Academy of Pathology, Inc 2012, 25:347-369.
106. Papadimitrakopoulou V. Development of PI3K/AKT/mTOR pathway inhibitors and their application in personalized therapy for non-small-cell lung cancer. Journal of thoracic oncology: official publication of the International Association for the Study of Lung Cancer 2012, 7:1315-1326.
107. Stueckle TA, Lu Y, Davis ME, Wang L, Jiang BH, Holaskova I, Schafer R, Barnett JB, Rojanasakul Y. Chronic occupational exposure to arsenic induces carcinogenic gene signaling networks and neoplastic transformation in human lung epithelial cells. Toxicol Appl Pharmacol 2012, 261:204-216. 10.1016/j.taap.2012.04.003, 22521957.
108. Gao N, Shen L, Zhang Z, Leonard SS, He H, Zhang XG, Shi X, Jiang BH. Arsenite induces HIF-1alpha and VEGF through PI3K, Akt and reactive oxygen species in DU145 human prostate carcinoma cells. Mol Cell Biochem 2004, 255:33-45.
109. Dong Z. The molecular mechanisms of arsenic-induced cell transformation and apoptosis. Environ Health Perspect 2002, 110 Suppl 5:757-759. 1241240, 12426127.
110. Chen B, Liu J, Chang Q, Beezhold K, Lu Y, Chen F. JNK and STAT3 signaling pathways converge on Akt-mediated phosphorylation of EZH2 in bronchial epithelial cells induced by arsenic. Cell Cycle 2012, 12.
111. Beezhold K, Liu J, Kan H, Meighan T, Castranova V, Shi X, Chen F. miR-190-mediated downregulation of PHLPP contributes to arsenic-induced Akt activation and carcinogenesis. Toxicological sciences: an official journal of the Society of Toxicology 2011, 123:411-420.
112. Wang Z, Yang J, Fisher T, Xiao H, Jiang Y, Yang C. Akt activation is responsible for enhanced migratory and invasive behavior of arsenic-transformed human bronchial epithelial cells. Environ Health Perspect 2012, 120:92-97. 3261952, 21954225.
113. Zhang Y, Bhatia D, Xia H, Castranova V, Shi X, Chen F. Nucleolin links to arsenic-induced stabilization of GADD45alpha mRNA. Nucleic Acids Res 2006, 34:485-495. 10.1093/nar/gkj459, 1342039, 16421274.
114. Tokar EJ, Diwan BA, Waalkes MP. Arsenic exposure transforms human epithelial stem/progenitor cells into a cancer stem-like phenotype. Environ Health Perspect 2010, 118:108-115. 2831952, 20056578.
115. Ling M, Li Y, Xu Y, Pang Y, Shen L, Jiang R, Zhao Y, Yang X, Zhang J, Zhou J. Regulation of miRNA-21 by reactive oxygen species-activated ERK/NF-kappaB in arsenite-induced cell transformation. Free Radic Biol Med 2012, 52:1508-1518. 10.1016/j.freeradbiomed.2012.02.020, 22387281.
116. Zhang DD. Mechanistic studies of the Nrf2-Keap1 signaling pathway. Drug Metab Rev 2006, 38:769-789. 10.1080/03602530600971974, 17145701.
117. Thu KL, Pikor LA, Chari R, Wilson IM, Macaulay CE, English JC, Tsao MS, Gazdar AF, Lam S, Lam WL, Lockwood WW. Genetic disruption of KEAP1/CUL3 E3 ubiquitin ligase complex components is a key mechanism of NF-kappaB pathway activation in lung cancer. Journal of thoracic oncology: official publication of the International Association for the Study of Lung Cancer 2011, 6:1521-1529.
118. Wang XJ, Sun Z, Chen W, Eblin KE, Gandolfi JA, Zhang DD. Nrf2 Protects human bladder urothelial cells from arsenite and monomethylarsonous acid toxicity. Toxicol Appl Pharmacol 2007, 225:206-213. 10.1016/j.taap.2007.07.016, 2610476, 17765279.
119. Zheng Y, Tao S, Lian F, Chau BT, Chen J, Sun G, Fang D, Lantz RC, Zhang DD. Sulforaphane prevents pulmonary damage in response to inhaled arsenic by activating the Nrf2-defense response. Toxicol Appl Pharmacol 2012, 265:292-299. 10.1016/j.taap.2012.08.028, 22975029.
120. Andujar P, Wang J, Descatha A, Galateau-Salle F, Abd-Alsamad I, Billon-Galland MA, Blons H, Clin B, Danel C, Housset B. p16INK4A Inactivation mechanisms in non-small-cell lung cancer patients occupationally exposed to asbestos. Lung Cancer 2010, 67:23-30. 10.1016/j.lungcan.2009.03.018, 19375815.
121. Wang XJ, Sun Z, Chen W, Li Y, Villeneuve NF, Zhang DD. Activation of Nrf2 by arsenite and monomethylarsonous acid is independent of Keap1-C151: enhanced Keap1-Cul3 interaction. Toxicol Appl Pharmacol 2008, 230:383-389. 10.1016/j.taap.2008.03.003, 2610481, 18417180.
122. American Cancer Society Cancer facts & figures 2012. Book cancer facts & figures 2012 2012, Atlanta: American Cancer Society, American Cancer Society.