Arsenic is cytotoxic and genotoxic to primary human lung cells

Mutation Research - Genetic Toxicology and Environmental Mutagenesis

Volumn 760, Issue , 2014, Pages 33-41

  Xie, Hong ^a   Huang, ShouPing ^a   Martin, Sarah ^a   Wise, John P ^a  

^a UNIVERSITY OF SOUTHERN MAINE   (United States)

Author keywords

Arsenic; Chromosome aberration; DNA double strand breaks; Genotoxicity; Human lung epithelial cells; Human lung fibroblasts

Indexed keywords

ARSENIC; H2AFX PROTEIN, HUMAN; HISTONE;

BRONCHUS; CELL CULTURE; CELL SURVIVAL; CHROMOSOME ABERRATION; COMET ASSAY; CYTOLOGY; DNA DAMAGE; DOSE RESPONSE; DOUBLE STRANDED DNA BREAK; DRUG EFFECTS; EPITHELIUM CELL; FIBROBLAST; FLUORESCENT ANTIBODY TECHNIQUE; HUMAN; METABOLISM; TIME;

ARSENIC; BRONCHI; CELL SURVIVAL; CELLS, CULTURED; CHROMOSOME ABERRATIONS; COMET ASSAY; DNA BREAKS, DOUBLE-STRANDED; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, DRUG; EPITHELIAL CELLS; FIBROBLASTS; FLUORESCENT ANTIBODY TECHNIQUE; HISTONES; HUMANS; TIME FACTORS;

EID: 84895066838     PISSN: 13835718     EISSN: 18793592     Source Type: Journal    
DOI: 10.1016/j.mrgentox.2013.11.001     Document Type: Article

References (71)

1. US Environmental Protection Agency Inorganic Arsenic, TEACH Chemical Summary 2007.
2. Environmental Protection Agency National primary drinking water regulations; arsenic and clarifications to compliance and new source contaminants monitoring; final rule. Fed. Reg. 2001, 66:6976-7066.
3. Chan P.C., Huff J. Arsenic carcinogenesis in animals and in humans: mechanistic, experimental and epidemiological evidence. Environ. Carcinog. Ecotoxicol. Rev. 1997, 15:83-122.
4. Smith A.H., Lingas E.O., Rahman M. Contamination of drinking-water by arsenic in Bangladesh: a public health emergency. Bull. World Health Organ. 2000, 78:1093-1103. (review).
5. Hughes M.F., Beck B.D., Chen Y., Lewis A.S., Thomas D.J. Arsenic exposure and toxicology: a historical perspective. Toxicol. Sci. 2011, 123:305-332.
6. Jemal A., Center M.M., DeSantis C., Ward E.M. Global patterns of cancer incidence and mortality rates and trends. Cancer Epidemiol. Biomarkers Prev. 2010, 19:1893-1907.
7. International Agency for Research on Cancer IARC Monographs on the Evaluation of the Carcinogenic Risk of Chemicals to Humans. Some Metals and Metallic Compounds 1980, vol. 23:39-141. International Agency for Research on Cancer, Lyon.
8. Martinez V.D., Becker-Santos D.D., Vucic E.A., Lam S., Lam W.L. Induction of human squamous cell-type carcinomas by arsenic. J. Skin Cancer. 2011, 454157.
9. Chen C.J., Chuang Y.C., Lin T.M., Wu H.Y. Malignant neoplasms among residents of a blackfoot disease-endemic area in Taiwan: high-arsenic artesian well water and cancers. Cancer Res. 1985, 45:5895-5899.
10. Wu M.M., Kuo T.L., Hwang Y.H., Chen C.J. Dose-response relation between arsenic concentration in well water and mortality from cancers and vascular diseases. Am. J. Epidemiol. 1989, 130:1123-1132.
11. Ferreccio C., González C., Milosavjlevic V., Marshall G., Sancha A.M., Smith A.H. Lung cancer and arsenic concentrations in drinking water in Chile. Epidemiology 2000, 11:673-679.
12. Steinmaus C.M., Ferreccio C., Acevedo Romo J., Yuan Y., Cortes S., Marshall G., Moore L.E., Balmes J.R., Liaw J., Golden T., Smith A.H. Drinking water arsenic in northern Chile: high cancer risks 40 years after exposure cessation. Cancer Epidemiol. Biomarkers Prev. 2013, 22:623-630.
13. Putila J.J., Guo N.L. Association of arsenic exposure with lung cancer incidence rates in the United States. PLoS ONE 2011, 6:e25886.
14. Wen G., Calaf G.M., Partridge M.A., Echiburú-Chau C., Zhao Y., Huang S., Chai Y., Li B., Hu B., Hei T.K. Neoplastic transformation of human small airway epithelial cells induced by arsenic. Mol. Med. 2008, 14:2-10.
15. Chang Q., Pan J., Wang X., Zhang Z., Chen F., Shi X. Reduced reactive oxygen species-generating capacity contributes to the enhanced cell growth of arsenic-transformed epithelial cells. Cancer Res. 2010, 70:5127-5135.
16. Stueckle T.A., Lu Y., Davis M.E., Wang L., Jiang B.H., Holaskova I., Schafer R., Barnett J.B., 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.
17. Kitchin K.T. Recent advances in arsenic carcinogenesis: modes of action, animal model systems, and methylated arsenic metabolites. Toxicol. Appl. Pharmacol. 2001, 172:249-261. (review).
18. Dulout F.N., Grillo C.A., Seoane A.I., Maderna C.R., Nilsson R., Vahter M., Darroudi F., Natarajan A.T. Chromosomal aberrations in peripheral blood lymphocytes from native Andean women and children from northwestern Argentina exposed to arsenic in drinking water. Mutat. Res. 1996, 370:151-158.
19. Gonsebatt M.E., Vega L., Salazar A.M., Montero R., Guzmán P., Blas J., Del Razo L.M., García-Vargas G., Albores A., Cebrián M.E., Kelsh M., Ostrosky-Wegman P. Cytogenetic effects in human exposure to arsenic. Mutat. Res. 1997, 386:219-228.
20. Bau D.T., Wang T.S., Chung C.H., Wang A.S., Wang A.S., Jan K.Y. Oxidative DNA adducts and DNA-protein cross-links are the major DNA lesions induced by arsenite. Environ. Health Perspect. 2002, 110:753-756. (review).
21. Kesari V.P., Kumar A., Khan P.K. Genotoxic potential of arsenic at its reference dose. Ecotoxicol. Environ. Saf. 2012, 80:126-131.
22. 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.
23. Mourón S.A., Golijow C.D., Dulout F.N. DNA damage by cadmium and arsenic salts assessed by the single cell gel electrophoresis assay. Mutat. Res. 2001, 498:47-55.
24. Wise J.P., Wise S.S., Little J.E. The cytotoxicity and genotoxicity of particulate and soluble hexavalent chromium in human lung cells. Mutat. Res. 2002, 517:221-229.
25. Xie H., Wise S.S., Holmes A.L., Xu B., Wakeman T.P., Pelsue S.C., Singh N.P., Wise J.P. Carcinogenic lead chromate induces DNA double-strand breaks in human lung cells. Mutat. Res. 2005, 586:160-172.
26. Wise S.S., Holmes A.L., Qin Q., Xie H., Katsifis S.P., Thompson W.D., Wise J.P. Comparative genotoxicity and cytotoxicity of four hexavalent chromium compounds in human bronchial cells. Chem. Res. Toxicol. 2010, 23:365-372.
27. Wise S.S., Holmes A.L., Xie H., Thompson W.D., Wise J.P. Chronic exposure to particulate chromate induces spindle assembly checkpoint bypass in human lung cells. Chem. Res. Toxicol. 2006, 19:1492-1498.
28. Holmes A.L., Wise S.S., Pelsue S.C., Aboueissa A.M., Lingle W., Salisbury J., Gallagher J., Wise J.P. Chronic exposure to zinc chromate induces centrosome amplification and spindle assembly checkpoint bypass in human lung fibroblasts. Chem. Res. Toxicol. 2010, 23:386-395.
29. Kops G.J., Weaver B.A., Cleveland D.W. On the road to cancer: aneuploidy and the mitotic checkpoint. Nat. Rev. Cancer 2005, 5:773-785. (review).
30. van Gent D.C., Hoeijmakers J.H., Kanaar R. Chromosomal stability and the DNA double-stranded break connection. Nat. Rev. Genet. 2001, 2:196-206. (review).
31. Smith A.H., Ercumen A., Yuan Y., Steinmaus C.M. Increased lung cancer risks are similar whether arsenic is ingested or inhaled. J. Expo. Sci. Environ. Epidemiol. 2009, 19:343-348.
32. Liao W.T., Lin P., Cheng T.S., Yu H.S., Chang L.W. Arsenic promotes centrosome abnormalities and cell colony formation in p53 compromised human lung cells. Toxicol. Appl. Pharmacol. 2007, 225:162-170.
33. Andrew A.S., Mason R.A., Memoli V., Duell E.J. Arsenic activates EGFR pathway signaling in the lung. Toxicol. Sci. 2009, 109:350-357.
34. Walker A.M., Stevens J.J., Ndebele K., Tchounwou P.B. Arsenic trioxide modulates DNA synthesis and apoptosis in lung carcinoma cells. Int. J. Environ. Res. Public Health 2010, 7:1996-2007.
35. 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.
36. Miao Z.F., Chang E.E., Tsai F.Y., Yeh S.C., Wu C.F., Wu K.Y., Wang C.J., Tsou T.C. Increased aquaglyceroporin 9 expression disrupts arsenic resistance in human lung cancer cells. Toxicol. In Vitro 2009, 23:209-216.
37. Albright C.D., Jones R.T., Hudson E.A., Fontana J.A., Trump B.F., Resau J.H. Transformed human bronchial epithelial cells (BEAS-2B) alter the growth and morphology of normal human bronchial epithelial cells in vitro. Cell Biol. Toxicol. 1990, 6:379-398.
38. Willey J.C., Broussoud A., Sleemi A., Bennett W.P., Cerutti P., Harris C.C. Immortalization of normal human bronchial epithelial cells by human papillomaviruses 16 or 18. Cancer Res. 1991, 51:5370-5377.
39. Ramirez R.D., Sheridan S., Girard L., Sato M., Kim Y., Pollack J., Peyton M., Zou Y., Kurie J.M., Dimaio J.M., Milchgrub S., Smith A.L., Souza R.F., Gilbey L., Zhang X., Gandia K., Vaughan M.B., Wright W.E., Gazdar A.F., Shay J.W., Minna J.D. Immortalization of human bronchial epithelial cells in the absence of viral oncoproteins. Cancer Res. 2004, 64:9027-9034.
40. Wise S.S., Holmes A.L., Wise J.P. Particulate and soluble hexavalent chromium are cytotoxic and genotoxic to human lung epithelial cells. Mutat. Res. 2006, 610:2-7.
41. Styblo M., Del Razo L.M., Vega L., Germolec D.R., LeCluyse E.L., Hamilton G.A., Reed W., Wang C., Cullen W.R., Thomas D.J. Comparative toxicity of trivalent and pentavalent inorganic and methylated arsenicals in rat and human cells. Arch. Toxicol. 2000, 74:289-299.
42. Park W.H., Kim S.H. Arsenic trioxide induces human pulmonary fibroblast cell death via the regulation of Bcl-2 family and caspase-8. Mol. Biol. Rep. 2012, 39:4311-4318.
43. Wang F., Shi Y., Yadav S., Wang H. p52-Bcl3 complex promotes cyclin D1 expression in BEAS-2B cells in response to low concentration arsenite. Toxicology 2010, 29:12-18.
44. Ghosh P., Basu A., Singh K.K., Giri A.K. Evaluation of cell types for assessment of cytogenetic damage in arsenic exposed population. Mol. Cancer 2008, 7. 10.1186/1476-4598-7-45.
45. Martinez V.D., Buys T.P., Adonis M., Benítez H., Gallegos I., Lam S., Lam W.L., Gil L. Arsenic-related DNA copy-number alterations in lung squamous cell carcinomas. Br. J. Cancer 2010, 103:1277-1283.
46. Larramendy M.L., Popescu N.C., Dipaolo J.A. Induction by inorganic metal salts of sister chromatid exchanges and chromosome aberrations in human and Syrian hamster cell strains. Environ. Mol. Mutagen. 2006, 3:597-606.
47. Kligerman A.D., Tennant A.H. Insights into the carcinogenic mode of action of arsenic. Toxicol. Appl. Pharmacol. 2007, 222:281-288.
48. Oya-Ohta Y., Kaise T., Ochi T. Induction of chromosomal aberrations in cultured human fibroblasts by inorganic and organic arsenic compounds and the different roles of glutathione in such induction. Mutat. Res. 1996, 357:123-129.
49. Sinha D., Bhattacharya R.K., Siddiqi M., Roy M. Amelioration of sodium arsenite-induced clastogenicity by tea extracts in Chinese hamster v79 cells. J. Environ. Pathol. Toxicol. Oncol. 2005, 24:129-140.
50. Tiwari H., Rao M.V. Curcumin supplementation protects from genotoxic effects of arsenic and fluoride. Food Chem. Toxicol. 2010, 48:1234-1238.
51. Ghosh P., Basu A., Mahata J., Basu S., Sengupta M., Das J.K., Mukherjee A., Sarkar A.K., Mondal L., Ray K., Giri A.K. Cytogenetic damage and genetic variants in the individuals susceptible to arsenic-induced cancer through drinking water. Int. J. Cancer 2006, 118:2470-2478.
52. Ramírez P., Eastmond D.A., Laclette J.P., Ostrosky-Wegman P. Disruption of microtubule assembly and spindle formation as a mechanism for the induction of aneuploid cells by sodium arsenite and vanadium pentoxide. Mutat. Res. 1997, 386:291-298.
53. Suzuki T., Miyazaki K., Kita K., Ochi T. Trivalent dimethylarsenic compound induces histone H3 phosphorylation and abnormal localization of Aurora B kinase in HepG2 cells. Toxicol. Appl. Pharmacol. 2009, 241:275-282.
54. Ditchfield C., Johnson V.L., Tighe A., Ellston R., Haworth C., Johnson T., Mortlock A., Keen N., Taylor Aurora S.S. B couples chromosome alignment with anaphase by targeting BubR1, Mad2, and Cenp-E to kinetochores. J. Cell Biol. 2003, 161:267-280.
55. Li D., Morimoto K., Takeshita T., Lu Y. Arsenic induces DNA damage via reactive oxygen species in human cells. Environ. Health Prev. Med. 2001, 6:27-32.
56. Dopp E., von Recklinghausen U., Hartmann L.M., Stueckradt I., Pollok I., Rabieh S., Hao L., Nussler A., Katier C., Hirner A.V., Rettenmeier A.W. Subcellular distribution of inorganic and methylated arsenic compounds in human urothelial cells and human hepatocytes. Drug Metab. Dispos. 2008, 36:971-979.
57. Qin X.J., Hudson L.G., Liu W., Ding W., Cooper K.L., Liu K.J. Dual actions involved in arsenite-induced oxidative DNA damage. Chem. Res. Toxicol. 2008, 21:1806-1813.
58. Khanna K.K., Jackson S.P. DNA double-strand breaks: signaling, repair and the cancer connection. Nat. Genet. 2001, 27:247-254. (review).
59. Ying S., Myers K., Bottomley S., Helleday T., Bryant H.E. BRCA2-dependent homologous recombination is required for repair of arsenite-induced replication lesions in mammalian cells. Nucleic Acids Res. 2009, 37:5105-5113.
60. Yih L.H., Hsueh S.W., Luu W.S., Chiu T.H., Lee T.C. Arsenite induces prominent mitotic arrest via inhibition of G2 checkpoint activation in CGL-2 cells. Carcinogenesis 2005, 26:53-63.
61. Chai C.Y., Huang Y.C., Hung W.C., Kang W.Y., Chen W.T. Arsenic salt-induced DNA damage and expression of mutant p53 and COX-2 proteins in SV-40 immortalized human uroepithelial cells. Mutagenesis 2007, 22:403-408.
62. Drobná Z., Waters S.B., Devesa V., Harmon A.W., Thomas D.J., Stýblo M. Metabolism and toxicity of arsenic in human urothelial cells expressing rat arsenic (+3 oxidation state)-methyltransferase. Toxicol. Appl. Pharmacol. 2005, 207:147-159.
63. Zhao R., Hou Y., Zhang Q., Woods C.G., Xue P., Fu J., Yarborough K., Guan D., Andersen M.E., Pi J. Cross-regulations among NRFs and KEAP1 and effects of their silencing on arsenic-induced antioxidant response and cytotoxicity in human keratinocytes. Environ. Health Perspect. 2012, 120:583-589.
64. Sandoval M., Morales M., Tapia R., del Carmen Alarcón L., Sordo M., Ostrosky-Wegman P., Ortega A., López-Bayghen E. p53 response to arsenic exposure in epithelial cells: protein kinase B/Akt involvement. Toxicol. Sci. 2007, 99:126-140.
65. Bredfeldt T.G., Kopplin M.J., Gandolfi A.J. Effects of arsenite on UROtsa cells: low-level arsenite causes accumulation of ubiquitinated proteins that is enhanced by reduction in cellular glutathione levels. Toxicol. Appl. Pharmacol. 2004, 198:412-418.
66. Wang T.C., Jan K.Y., Wang A.S., Gurr J.R. Trivalent arsenicals induce lipid peroxidation, protein carbonylation, and oxidative DNA damage in human urothelial cells. Mutat. Res. 2007, 615(February (1-2)):75-86.
67. Moore L.E., Smith A.H., Hopenhayn-Rich C., Biggs M.L., Kalman D.A., Smith M.T. Micronuclei in exfoliated bladder cells among individuals chronically exposed to arsenic in drinking water. Cancer Epidemiol. Biomarkers Prev. 1997, 6:31-36.
68. Li Y., Ling M., Xu Y., Wang S., Li Z., Zhou J., Wang X., Liu Q. The repressive effect of NF-kappaB on p53 by mot-2 is involved in human keratinocyte transformation induced by low levels of arsenite. Toxicol. Sci. 2010, 116:174-182.
69. Dopp E., von Recklinghausen U., Diaz-Bone R., Hirner A.V., Rettenmeier A.W. Cellular uptake, subcellular distribution and toxicity of arsenic compounds in methylating and non-methylating cells. Environ. Res. 2010, 110:435-442.
70. Lee T.C., Ho I.C., Lu W.J., Huang J.D. Enhanced expression of multidrug resistance-associated protein 2 and reduced expression of aquaglyceroporin 3 in an arsenic-resistant human cell line. J. Biol. Chem. 2006, 281:18401-18407.
71. Tatum F.M., Hood R.D. Arsenite uptake and metabolism by rat hepatocyte primary cultures in comparison with kidney- and hepatocyte-derived rat cell lines. Toxicol. Sci. 1999, 52:20-25.