Autophagy in arsenic carcinogenesis

Experimental and Toxicologic Pathology

Volumn 66, Issue 4, 2014, Pages 163-168

  Qi, Yuanlin ^a,b   Li, Hui ^a   Zhang, Mingfang ^a,b   Zhang, Tao ^b   Frank, Jacqueline ^a   Chen, Gang ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

^b FUJIAN MEDICAL UNIVERSITY   (China)

Author keywords

Arsenic; Autophagy; Carcinogenesis; Oxidative stress

Indexed keywords

ARSENIC;

AUTOPHAGY; CARCINOGENESIS; CELL DEATH; CHROMOSOME ABERRATION; DNA MODIFICATION; EPIGENETICS; EXPOSURE; HUMAN; MITOCHONDRIAL RESPIRATION; NONHUMAN; OXIDATIVE STRESS; REVIEW; SIGNAL TRANSDUCTION;

ARSENIC; AUTOPHAGY; CARCINOGENESIS; OXIDATIVE STRESS;

ARSENIC; AUTOPHAGY; CHROMOSOME ABERRATIONS; HUMANS; NEOPLASMS; OXIDATIVE STRESS; SIGNAL TRANSDUCTION; WATER POLLUTANTS, CHEMICAL;

EID: 84896726142     PISSN: 09402993     EISSN: 16181433     Source Type: Journal    
DOI: 10.1016/j.etp.2014.01.004     Document Type: Review

References (88)

1. Alexander A., Cai S.L., Kim J., Nanez A., Sahin M., MacLean K.H., et al. ATM signals to TSC2 in the cytoplasm to regulate mTORC1 in response to ROS. Proc Natl Acad Sci USA 2010, 107:4153-4158.
2. Amaravadi R.K., Thompson C.B. The roles of therapy-induced autophagy and necrosis in cancer treatment. Clin Cancer Res 2007, 13:7271-7279.
3. Azad M.B., Chen Y., Gibson S.B. Regulation of autophagy by reactive oxygen species (ROS): implications for cancer progression and treatment. Antioxid Redox Signal 2009, 11:777-790.
4. Banerjee N., Banerjee M., Ganguly S., Bandyopadhyay S., Das J.K., Bandyopadhay A., et al. Arsenic-induced mitochondrial instability leading to programmed cell death in the exposed individuals. Toxicology 2008, 246:101-111.
5. Barrett J.C., Thomassen D.G., Hesterberg T.W. Role of gene and chromosomal mutations in cell transformation. Ann N Y Acad Sci 1983, 407:291-300.
6. Benbrahim-Tallaa L., Waterland R.A., Styblo M., Achanzar W.E., Webber M.M., Waalkes M.P. Molecular events associated with arsenic-induced malignant transformation of human prostatic epithelial cells: aberrant genomic DNA methylation and K-ras oncogene activation. Toxicol Appl Pharmacol 2005, 206:288-298.
7. Bhadauria S., Flora S.J. Response of arsenic-induced oxidative stress, DNA damage, and metal imbalance to combined administration of DMSA and monoisoamyl-DMSA during chronic arsenic poisoning in rats. Cell Biol Toxicol 2007, 23:91-104.
8. Bjelland S., Seeberg E. Mutagenicity, toxicity and repair of DNA base damage induced by oxidation. Mutat Res 2003, 531:37-80.
9. Bolt A.M., Byrd R.M., Klimecki W.T. Autophagy is the predominant process induced by arsenite in human lymphoblastoid cell lines. Toxicol Appl Pharmacol 2010, 244:366-373.
10. Brazy P.C., Balaban R.S., Gullans S.R., Mandel L.J., Dennis V.W. Inhibition of renal metabolism. Relative effects of arsenate on sodium, phosphate, and glucose transport by the rabbit proximal tubule. J Clin Invest 1980, 66:1211-1221.
11. Carames B., Taniguchi N., Otsuki S., Blanco F.J., Lotz M. Autophagy is a protective mechanism in normal cartilage, and its aging-related loss is linked with cell death and osteoarthritis. Arthritis Rheum 2010, 62:791-801.
12. Cavigelli M., Li W.W., Lin A., Su B., Yoshioka K., Karin M. The tumor promoter arsenite stimulates AP-1 activity by inhibiting a JNK phosphatase. EMBO J 1996, 15:6269-6279.
13. Cerda S., Weitzman S.A. Influence of oxygen radical injury on DNA methylation. Mutat Res 1997, 386:141-152.
14. Chen F., Ding M., Castranova V., Shi X. Carcinogenic metals and NF-kappaB activation. Mol Cell Biochem 2001, 222:159-171.
15. Chen H., Li S., Liu J., Diwan B.A., Barrett J.C., Waalkes M.P. Chronic inorganic arsenic exposure induces hepatic global and individual gene hypomethylation: implications for arsenic hepatocarcinogenesis. Carcinogenesis 2004, 25:1779-1786.
16. Chen Y., Gibson S.B. Is mitochondrial generation of reactive oxygen species a trigger for autophagy?. Autophagy 2008, 4:246-248.
17. Chen Y., McMillan-Ward E., Kong J., Israels S.J., Gibson S.B. Oxidative stress induces autophagic cell death independent of apoptosis in transformed and cancer cells. Cell Death Differ 2008, 15:171-182.
18. Corsini E., Asti L., Viviani B., Marinovich M., Galli C.L. Sodium arsenate induces overproduction of interleukin-1alpha in murine keratinocytes: role of mitochondria. J Invest Dermatol 1999, 113:760-765.
19. Covacci V., Torsello A., Palozza P., Sgambato A., Romano G., Boninsegna A., et al. DNA oxidative damage during differentiation of HL-60 human promyelocytic leukemia cells. Chem Res Toxicol 2001, 14:1492-1497.
20. Cuervo A.M., Bergamini E., Brunk U.T., Droge W., Ffrench M., Terman A. Autophagy and aging: the importance of maintaining "clean" cells. Autophagy 2005, 1:131-140.
21. Dastgiri S., Mosaferi M., Fizi M.A., Olfati N., Zolali S., Pouladi N., et al. Arsenic exposure, dermatological lesions, hypertension, and chromosomal abnormalities among people in a rural community of northwest Iran. J Health Popul Nutr 2010, 28:14-22.
22. Degenhardt K., Mathew R., Beaudoin B., Bray K., Anderson D., Chen G., et al. Autophagy promotes tumor cell survival and restricts necrosis, inflammation, and tumorigenesis. Cancer Cell 2006, 10:51-64.
23. Dong J.T., Luo X.M. Arsenic-induced DNA-strand breaks associated with DNA-protein crosslinks in human fetal lung fibroblasts. Mutat Res 1993, 302:97-102.
24. Germolec D.R., Spalding J., Yu H.S., Chen G.S., Simeonova P.P., Humble M.C., et al. Arsenic enhancement of skin neoplasia by chronic stimulation of growth factors. Am J Pathol 1998, 153:1775-1785.
25. Glick D., Barth S., Macleod K.F. Autophagy: cellular and molecular mechanisms. J Pathol 2010, 221:3-12.
26. Halliwell B. Oxidative stress and cancer: have we moved forward?. Biochem J 2007, 401:1-11.
27. Hoyer-Hansen M., Jaattela M. Connecting endoplasmic reticulum stress to autophagy by unfolded protein response and calcium. Cell Death Differ 2007, 14:1576-1582.
28. Huang C., Ke Q., Costa M., Shi X. Molecular mechanisms of arsenic carcinogenesis. Mol Cell Biochem 2004, 255:57-66.
29. Jensen T.J., Novak P., Eblin K.E., Gandolfi A.J., Futscher B.W. Epigenetic remodeling during arsenical-induced malignant transformation. Carcinogenesis 2008, 29:1500-1508.
30. Jiang T., Huang Z., Chan J.Y., Zhang D.D. Nrf2 protects against As(III)-induced damage in mouse liver and bladder. Toxicol Appl Pharmacol 2009, 240:8-14.
31. Jin S. Autophagy, mitochondrial quality control, and oncogenesis. Autophagy 2006, 2:80-84.
32. Karantza-Wadsworth V., Patel S., Kravchuk O., Chen G., Mathew R., Jin S., et al. Autophagy mitigates metabolic stress and genome damage in mammary tumorigenesis. Genes Dev 2007, 21:1621-1635.
33. Karpinets T.V., Foy B.D. Tumorigenesis: the adaptation of mammalian cells to sustained stress environment by epigenetic alterations and succeeding matched mutations. Carcinogenesis 2005, 26:1323-1334.
34. Kessel M., Liu S.X., Xu A., Santella R., Hei T.K. Arsenic induces oxidative DNA damage in mammalian cells. Mol Cell Biochem 2002, 234-235:301-308.
35. Kirkland R.A., Adibhatla R.M., Hatcher J.F., Franklin J.L. Loss of cardiolipin and mitochondria during programmed neuronal death: evidence of a role for lipid peroxidation and autophagy. Neuroscience 2002, 115:587-602.
36. Kligerman A.D., Doerr C.L., Tennant A.H. Oxidation and methylation status determine the effects of arsenic on the mitotic apparatus. Mol Cell Biochem 2005, 279:113-121.
37. Klionsky D.J. Autophagy: from phenomenology to molecular understanding in less than a decade. Nat Rev Mol Cell Biol 2007, 8:931-937.
38. Klionsky D.J., Abdalla F.C., Abeliovich H., Abraham R.T., Acevedo-Arozena A., Adeli K., et al. Guidelines for the use and interpretation of assays for monitoring autophagy in higher eukaryotes. Autophagy 2008, 4:151-175.
39. Kojima C., Ramirez D.C., Tokar E.J., Himeno S., Drobna Z., Styblo M., et al. Requirement of arsenic biomethylation for oxidative DNA damage. J Natl Cancer Inst 2009, 101:1670-1681.
40. Lau A., Zheng Y., Tao S., Wang H., Whitman S.A., White E., et al. Arsenic inhibits autophagic flux activating the Nrf2-Keap1 pathway in a p62-dependent manner. Mol Cell Biol 2013.
41. Lee T.C., Ho I.C. Modulation of cellular antioxidant defense activities by sodium arsenite in human fibroblasts. Arch Toxicol 1995, 69:498-504.
42. Lengfelder E., Hofmann W.K., Nowak D. Impact of arsenic trioxide in the treatment of acute promyelocytic leukemia. Leukemia 2012, 26:433-442.
43. Liang C., Feng P., Ku B., Dotan I., Canaani D., Oh B.H., et al. Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat Cell Biol 2006, 8:688-699.
44. Liang X.H., Jackson S., Seaman M., Brown K., Kempkes B., Hibshoosh H., et al. Induction of autophagy and inhibition of tumorigenesis by beclin 1. Nature 1999, 402:672-676.
45. Liu Z., Lenardo M.J. Reactive oxygen species regulate autophagy through redox-sensitive proteases. Dev Cell 2007, 12:484-485.
46. Ma B., Liang L.Z., Liao G.Q., Liang Y.J., Liu H.C., Zheng G.S., et al. Inhibition of autophagy enhances cisplatin cytotoxicity in human adenoid cystic carcinoma cells of salivary glands. J Oral Pathol Med 2013.
47. Marsit C.J., Eddy K., Kelsey K.T. MicroRNA responses to cellular stress. Cancer Res 2006, 66:10843-10848.
48. Mass M.J., Tennant A., Roop B.C., Cullen W.R., Styblo M., Thomas D.J., et al. Methylated trivalent arsenic species are genotoxic. Chem Res Toxicol 2001, 14:355-361.
49. Mass M.J., 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.
50. Mathew R., Karantza-Wadsworth V., White E. Role of autophagy in cancer. Nat Rev Cancer 2007, 7:961-967.
51. Mathew R., Karantza-Wadsworth V., White E. Assessing metabolic stress and autophagy status in epithelial tumors. Methods Enzymol 2009, 453:53-81.
52. Mathew R., Karp C.M., Beaudoin B., Vuong N., Chen G., Chen H.Y., et al. Autophagy suppresses tumorigenesis through elimination of p62. Cell 2009, 137:1062-1075.
53. Mathew R., Kongara S., Beaudoin B., Karp C.M., Bray K., Degenhardt K., et al. Autophagy suppresses tumor progression by limiting chromosomal instability. Genes Dev 2007, 21:1367-1381.
54. Mathew R., White E. Why sick cells produce tumors: the protective role of autophagy. Autophagy 2007, 3:502-505.
55. Mizushima N., Yoshimori T. How to interpret LC3 immunoblotting. Autophagy 2007, 3:542-545.
56. Ochi T., Mogi M., Watanabe M., Ohsawa M. Induction of chromosomal aberrations in cultured Chinese hamster cells by short-term treatment with cadmium chloride. Mutat Res 1984, 137:103-109.
57. Pucer A., Castino R., Mirkovic B., Falnoga I., Slejkovec Z., Isidoro C., et al. Differential role of cathepsins B and L in autophagy-associated cell death induced by arsenic trioxide in U87 human glioblastoma cells. Biol Chem 2010.
58. Qian W., Liu J., Jin J., Ni W., Xu W. Arsenic trioxide induces not only apoptosis but also autophagic cell death in leukemia cell lines via up-regulation of Beclin-1. Leuk Res 2007, 31:329-339.
59. Qu X., Yu J., Bhagat G., Furuya N., Hibshoosh H., Troxel A., et al. Promotion of tumorigenesis by heterozygous disruption of the beclin 1 autophagy gene. J Clin Invest 2003, 112:1809-1820.
60. Ramirez P., Del Razo L.M., Gutierrez-Ruiz M.C., Gonsebatt M.E. Arsenite induces DNA-protein crosslinks and cytokeratin expression in the WRL-68 human hepatic cell line. Carcinogenesis 2000, 21:701-706.
61. Rossman T.G., Klein C.B. Genetic and epigenetic effects of environmental arsenicals. Metallomics 2011, 3:1135-1141.
62. Ruiz-Ramos R., Lopez-Carrillo L., Rios-Perez A.D., De Vizcaya-Ruiz A., Cebrian M.E. Sodium arsenite induces ROS generation, DNA oxidative damage, HO-1 and c-Myc proteins, NF-kappaB activation and cell proliferation in human breast cancer MCF-7 cells. Mutat Res 2009, 674:109-115.
63. Salazar A.M., Ostrosky-Wegman P., Menendez D., Miranda E., Garcia-Carranca A., Rojas E. Induction of p53 protein expression by sodium arsenite. Mutat Res 1997, 381:259-265.
64. Scherz-Shouval R., Elazar Z. ROS, mitochondria and the regulation of autophagy. Trends Cell Biol 2007, 17:422-427.
65. Scherz-Shouval R., Shvets E., Elazar Z. Oxidation as a post-translational modification that regulates autophagy. Autophagy 2007, 3:371-373.
66. Scherz-Shouval R., Shvets E., Fass E., Shorer H., Gil L., Elazar Z. Reactive oxygen species are essential for autophagy and specifically regulate the activity of Atg4. EMBO J 2007, 26:1749-1760.
67. 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.
68. Sciandrello G., Caradonna F., Mauro M., Barbata G. Arsenic-induced DNA, hypomethylation affects chromosomal instability in mammalian cells. Carcinogenesis 2004, 25:413-417.
69. Selvakumaran M., Amaravadi R., Vasilevskaya I.A., O'Dwyer P.J. Autophagy inhibition sensitizes colon cancer cells to anti-angiogenic and cytotoxic therapy. Clin Cancer Res 2013.
70. Shen H.M., Codogno P. Autophagic cell death: Loch Ness monster or endangered species?. Autophagy 2011, 7:457-465.
71. Shi H., Hudson L.G., Ding W., Wang S., Cooper K.L., Liu S., et al. Arsenite causes DNA damage in keratinocytes via generation of hydroxyl radicals. Chem Res Toxicol 2004, 17:871-878.
72. Sinha D., Biswas J., Bishayee A. Nrf2-mediated redox signaling in arsenic carcinogenesis: a review. Arch Toxicol 2013, 87:383-396.
73. Stipanuk M.H. Macroautophagy and its role in nutrient homeostasis. Nutr Rev 2009, 67:677-689.
74. Takahashi M., Barrett J.C., Tsutsui T. Transformation by inorganic arsenic compounds of normal Syrian hamster embryo cells into a neoplastic state in which they become anchorage-independent and cause tumors in newborn hamsters. Int J Cancer 2002, 99:629-634.
75. Tsujimoto Y., Shimizu S. Another way to die: autophagic programmed cell death. Cell Death Differ 2005, 12(Suppl. 2):1528-1534.
76. Valko M., Morris H., Cronin M.T. Metals, toxicity and oxidative stress. Curr Med Chem 2005, 12:1161-1208.
77. Wang X.J., Sun Z., Chen W., Li Y., Villeneuve N.F., Zhang D.D. Activation of Nrf2 by arsenite and monomethylarsonous acid is independent of Keap1-C151: enhanced Keap1-Cul3 interaction. Toxicol Appl Pharmacol 2008, 230:383-389.
78. Wen G., Calaf G.M., Partridge M.A., Echiburu-Chau C., Zhao Y., Huang S., et al. Neoplastic transformation of human small airway epithelial cells induced by arsenic. Mol Med 2008, 14:2-10.
79. White E., Karp C., Strohecker A.M., Guo Y., Mathew R. Role of autophagy in suppression of inflammation and cancer. Curr Opin Cell Biol 2010, 22:212-217.
80. Wikstrom J.D., Twig G., Shirihai O.S. What can mitochondrial heterogeneity tell us about mitochondrial dynamics and autophagy?. Int J Biochem Cell Biol 2009, 41:1914-1927.
81. Wu Y.T., Tan H.L., Huang Q., Ong C.N., Shen H.M. Activation of the PI3K-Akt-mTOR signaling pathway promotes necrotic cell death via suppression of autophagy. Autophagy 2009, 5:824-834.
82. Wu Y.T., Tan H.L., Shui G., Bauvy C., Huang Q., Wenk M.R., et al. Dual role of 3-methyladenine in modulation of autophagy via different temporal patterns of inhibition on class I and III phosphoinositide 3-kinase. J Biol Chem 2010, 285:10850-10861.
83. Yang Y.P., Liang Z.Q., Gao B., Jia Y.L., Qin Z.H. Dynamic effects of autophagy on arsenic trioxide-induced death of human leukemia cell line HL60 cells. Acta Pharmacol Sin 2008, 29:123-134.
84. Yue Z., Jin S., Yang C., Levine A.J., Heintz N. Beclin 1, an autophagy gene essential for early embryonic development, is a haploinsufficient tumor suppressor. Proc Natl Acad Sci USA 2003, 100:15077-15082.
85. Zhang D., Li J., Gao J., Huang C. c-Jun/AP-1 pathway-mediated cyclin D1 expression participates in low dose arsenite-induced transformation in mouse epidermal JB6 Cl41 cells. Toxicol Appl Pharmacol 2009, 235:18-24.
86. Zhang T., Qi Y., Liao M., Xu M., Bower K.A., Frank J.A., et al. Autophagy is a cell self-protective mechanism against arsenic-induced cell transformation. Toxicol Sci 2012, 130:298-308.
87. Zhang Y., Qi H., Taylor R., Xu W., Liu L.F., Jin S. The role of autophagy in mitochondria maintenance: characterization of mitochondrial functions in autophagy-deficient S. cerevisiae strains. Autophagy 2007, 3:337-346.
88. Zhou X., Sun H., Ellen T.P., Chen H., Costa M. Arsenite alters global histone H3 methylation. Carcinogenesis 2008, 29:1831-1836.