Altered gene expression by low-dose arsenic exposure in humans and cultured cardiomyocytes: Assessment by real-time PCR arrays

International Journal of Environmental Research and Public Health

Volumn 8, Issue 6, 2011, Pages 2090-2108

  Mo, Jinyao ^a   Xia, Yajuan ^b   Wade, Timothy J ^c   DeMarini, David M ^c   Davidson, Mercy ^d   Mumford, Judy ^c  

^a UNIVERSITY OF NORTH CAROLINA SCHOOL OF MEDICINE   (United States)

^b Inner Mongolia Center for Endemic Disease Control and Research   (China)

^c U S ENVIRONMENTAL PROTECTION AGENCY   (United States)

^d Howard Hughes Medical Institute   (United States)

Author keywords

Arsenic; Cardiomycocytes; Drinking water; Low density array; Real time PCR

Indexed keywords

ARSENIC; DRINKING WATER; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; ION CHANNEL; POTASSIUM ION; WATER;

ADULT; ARTICLE; BAX GENE; BCL 2 GENE; CARDIOVASCULAR DISEASE; CHILD; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; DIABETES MELLITUS; DISEASE ASSOCIATION; DNA METHYLATION; DNA METHYLTRANSFERASE 1 GENE; DOWN REGULATION; FEMALE; GENE; GENE EXPRESSION; GENETIC ASSOCIATION; GENETIC VARIABILITY; HEART MUSCLE CELL; HUMAN; HUMAN CELL; IN VITRO STUDY; INFLAMMATION; JUN GENE; MALE; NEOPLASM; OXIDATIVE STRESS; POLB GENE; POTASSIUM CHANNEL KV1.5 GENE; QT PROLONGATION; RAD50 GENE; REAL TIME POLYMERASE CHAIN REACTION; SCHOOL CHILD; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR MAF GENE; TUMOR NECROSIS FACTOR ALPHA GENE; UPREGULATION; URINE LEVEL;

EID: 79959829513     PISSN: None     EISSN: 16604601     Source Type: Journal    
DOI: 10.3390/ijerph8062090     Document Type: Article

References (51)

1. International Agency for Research on Cancer (IARC). IARC Monographs on the Evaluation of Carcinogenic Risks to Humans. Some Drinking-Water Disinfectants and Contaminants, Including Arsenic; IARC: Lyon, France, 2004; Volume 84.
2. Tapio, S.; Grosche, B. Arsenic in the aetiology of cancer. Mutat. Res. 2006, 612, 215-246.
3. Straif, K.; Benbrahim-Tallaa, L.; Baan, R.; Grosse, Y.; Secretan, B.; El Ghissassi, F.; Bouvard, V.; Guha, N.; Freeman, C; Galichet, L.; et al. A review of human carcinogens-Part C: Metals, arsenic, dusts, and fibres. Lancet Oncol. 2009, 10, 453-454.
4. Rossman, T.G.; Uddin, A.N.; Burns, F.J. Evidence that arsenite acts as a cocarcinogen in skin cancer. Toxicol. Appl. Pharmacol. 2004, 198, 394-404.
5. Mumford, J.L.; Wu, K.; Xia, Y.; Kwok, R.; Yang, Z.; Foster, J.; Sanders, W.E. Chronic arsenic exposure and cardiac repolarization abnormalities with QT interval prolongation in a population-based study. Environ. Health Perspect. 2007, 115, 690-694.
6. Westervelt, P.; Brown, R.A.; Adkins, D.R.; Khoury, H.; Curtin, P.; Hurd, D.; Luger, S.M.; Ma, M.K.; Ley, T.J.; DiPersio, J.F. Sudden death among patients with acute promyelocytic leukemia treated with arsenic trioxide. Blood 2001, 98, 266-271.
7. Sanz, M.A.; Grimwade, D.; Tallman, M.S.; Lowenberg, B.; Fenaux, P.; Estey, E.H.; Naoe, T.; Lengfelder, E.; Buchner, T.; Dohner, H.; Burnett, A.K.; Lo-Coco, F. Management of acute promyelocytic leukemia: recommendations from an expert panel on behalf of the European LeukemiaNet. Blood 2009, 113, 1875-1891.
8. States, J.C.; Srivastava, S.; Chen, Y.; Barchowsky, A. Arsenic and cardiovascular disease. Toxicol. Sci. 2009, 107, 312-323.
9. Wade, T.J.; Xia, Y.; Wu, K.; Li, Y.; Ning, Z.; Le, X.C.; Lu, X.; Feng, Y.; He, X.; Mumford, J.L. Increased mortality associated with well-water arsenic exposure in Inner Mongolia, China. Int. J. Environ. Res. Public Health 2009, 6, 1107-1123.
10. Wang, C.H.; Chen, C.L.; Hsiao, C.K.; Chiang, F.T.; Hsu, L.I.; Chiou, H.Y.; Hsueh, Y.M.; Wu, M.M.; Chen, C.J. Increased risk of QT prolongation associated with atherosclerotic diseases in arseniasis-endemic area in southwestern coast of Taiwan. Toxicol. Appl. Pharmacol. 2009, 239, 320-324.
11. Mordukhovich, I.; Wright, R.O.; Amarasiriwardena, C.; Baja, E.; Baccarelli, A.; Suh, H.; Sparrow, D.; Vokonas, P.; Schwartz, J. Association between low-level environmental arsenic exposure and QT interval duration in a general population study. Am. J. Epidemiol. 2009, 170, 739-746.
12. Liu, J.; Kadiiska, M.B.; Liu, Y.; Lu, T.; Qu, W.; Waalkes, M.P. Stress-related gene expression in mice treated with inorganic arsenicals. Toxicol. Sci. 2001, 61, 314-320.
13. Rea, M.A.; Gregg, J.P.; Qin, Q.; Phillips, M.A.; Rice, R.H. Global alteration of gene expression in human keratinocytes by inorganic arsenic. Carcinogenesis 2003, 24, 747-756.
14. Argos, M.; Kibriya, M.G.; Parvez, F.; Jasmine, F.; Rakibuz-Zaman, M.; Ahsan, H. Gene expression profiles in peripheral lymphocytes by arsenic exposure and skin lesion status in a Bangladeshi population. Cancer Epidemiol. Biomarkers Prev. 2006, 15, 1367-1375.
15. Fry, R.C.; Navasumrit, P.; Valiathan, C.; Svensson, J.P.; Hogan, B.J.; Luo, M.; Bhattacharya, S.; Kandjanapa, K.; Soontararuks, S.; Nookabkaew, S.; et al. Activation of inflammation/NF-κB signaling in infants born to arsenic-exposed mothers. PLoS Genet. 2007, 3, e207.
16. Ghosh, P.; Banerjee, M.; Giri, A.K.; Ray, K. Toxcogenomics of arsenic: Classical ideas and recent advances. Mutat. Res. 2008, 659, 293-301.
17. Abruzzo, L.V.; Lee, K.Y.; Fuller, A.; Silverman, A.; Keating, M.J.; Medeiros, L.J.; Coombes, K.R. Validation of oligonucleotide microarray data using microfluidic low-density arrays: A new statistical method to normalize real-time RT-PCR data. Biotechniques 2005, 38, 785-792.
18. Goulter, A.B.; Harmer, D.W.; Clark, K.L.O. Evaluation of low density array technology for quantitative parallel measurement of multiple genes in human tissue. BMC Genomics 2006, 7, 34.
19. Ma, H.Z.; Xia, Y.J.; Wu, K.G.; Sun, T.Z.; Mumford, J.L. Human exposure to arsenic and health effects in Bayingnormen, Inner Mongolia. In Arsenic Exposure and Health Effects; Abernathy, W.R., Calderon, C.O., Chappell, R., Eds.; Elsevier: Amsterdam, The Netherlands, 1999; pp. 127-131.
20. Mo, J.; Xia, Y.; Wade, T.J.; Schmitt, M.; Le, X.C.; Dang, R.; Mumford, J.L. Chronic arsenic exposure and oxidative stress: OGG1 expression and arsenic exposure, nail selenium, and skin hyperkeratosis in Inner Mongolia. Environ. Health Perspect. 2006, 114, 835-841.
21. World Medical Association. Declaration of Helsinki, 1989.Available online: http://www.wma.net/e/policy/pdf/17c.pdf (accessed on 23 March 2011).
22. Gong, Z.; Lu, X.; Watt, C.; Wen, B.; He, B.; Mumford, J.; Ning, Z.; Xia, Y.; Le, X.C. Speciation analysis of arsenic in groundwater from Inner Mongolia with an emphasis on acid-leachable particulate arsenic. Anal. Chim. Acta 2006, 555, 181-187.
23. Schmitt, M.T.; Schreinemachers, D.; Wu, K.; Ning, Z.; Zhao, B.; Le, X.C.; Mumford, J.L. Human nails as a biomarker of arsenic exposure from well water in Inner Mongolia: Comparing atomic fluorescence spectrometry and neutron activation analysis. Biomarkers 2005, 10, 95-104.
24. Heydorn, K. Neutron Activation Analysis for Clinical Trace Element Research; CRC Press: Boca Raton, FL, USA, 1984; Volumes 1 and 2.
25. Otto, D.; Xia, Y.; Li, Y.; Wu, K.; He, L.; Telech, J.; Hundell, H.; Prah, J.; Mumford, J.; Wade, T. Neurosensory effects of chronic human exposure to arsenic associated with body burden and environmental measures. Hum. Exp. Toxicol. 2007, 26, 169-177.
26. Royston, P.; Ambler, G.; Sauerbrei, W. The use of fractional polynomials to model continuous risk variables in epidemiology. Int. J. Epidemiol. 1999, 28, 964-974.
27. Watanabe, C.; Inaoka, T.; Kadono, T.; Nagano, M.; Nakamura, S.; Ushijima, K.; Murayama, N.; Miyazaki, K.; Ohtsuka, R. Males in rural Bangladeshi communities are more susceptible to chronic arsenic poisoning than females: Analyses based on urinary arsenic. Environ. Health Perspect. 2001, 109, 1265-1270.
28. Ahsan, H.; Perrin, M.; Rahman, A.; Parvez, F.; Stute, M.; Zheng, Y.; Milton, A.H.; Brandt-Rauf, P.; van Geen, A.; Graziano, J. Associations between drinking water and urinary arsenic levels and skin lesions in Bangladesh. J. Occup. Environ. Med. 2000, 42, 1195-1201.
29. Maki-Paakkanen, J.; Kurttio, P.; Paldy, A.; Pekkanen, J. Association between the clastogenic effect in peripheral lymphocytes and human exposure to arsenic through drinking water. Environ. Mol. Mutagen. 1998, 32, 301-313.
30. Bevnova, E.E.; Platoshyn, O.; Zhang, S.; Yuan, J.X. Overexpression of human KCNA5 increases IK V and enhances apoptosis. Am. J. Physiol. Cell Physiol. 2004, 287, C715-C722.
31. Nattel, S.; Bourne, G.; Talajic, M. Insights into mechanisms of antiarrythmic drug action from experimental models of atrial fibrillation. J. Cardiovasc. Electrophysiol. 1997, 8, 469-480.
32. Fountain, S.J.; Cheong, A.; Li, J.; Dondas, N.Y.; Zeng, F.; Wood, I.C.; Beech, D.J. K9v1.5 potassium channel gene regulation by Sp1 transcription factor and oxidative stress. Am. J. Physiol. Heart Circ. Physiol. 2007, 293, H2719-H2725.
33. Germolec, D.R.; Spalding, J.; Boorman, G.A.; Wilmer, J.L.; Yoshida, T.; Simeonova, P.P.; Bruccoleri, A.; Kayama, F.; Gaido, K.; Tennant, R.; et al. Arsenic can mediate skin neoplasia by chronic stimulation of keratinocyte-derived growth factors. Mutat. Res. 1997, 386, 209-218.
34. Yih, L.H.; Peck, K.; Lee, T.C. Changes in gene expression profiles of human fibroblasts in response to sodium arsenite treatment. Carcinogenesis 2002, 23, 867-876.
35. Simeonova, P.P.; Luster, M.I. Mechanisms of arsenic carcinogenicity: Genetic or epigenetic mechanisms? J. Environ. Pathol. Toxicol. Oncol. 2000, 19, 281-286.
36. Schoen, A.; Beck, B.; Sharma, R.; Dube, E. Arsenic toxicity at low doses: Epidemiological and mode of action considerations. Toxicol. Appl. Pharmacol. 2004, 198, 253-267.
37. Itoh, K.; Chiba, T.; Takahashi, S.; Ishii, T.; Igarashi, K.; Katoh, Y.; Oyake, T.; Hayashi, N.; Satoh, K.; Hatayama, I.; et al. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem. Biophys. Res. Commun. 1997, 236, 313-322.
38. Komissarova, E.V.; Li, P.; Uddin, A.N.; Chen, X.; Nadas, A.; Rossman, T.G. Gene expression levels in normal human lymphoblasts with variable sensitivities to arsenite: Identification of GGT1 and NFKBIE expression levels as possible biomarkers of susceptibility. Toxicol. Appl. Pharmacol. 2008, 226, 199-205.
39. Hu, Y.; Jin, X.; Snow, E.T. Effect of arsenic on transcription factor AP-1 and NF-kappaB DNA binding activity and related gene expression. Toxicol. Lett. 2002, 133, 33-45.
40. Liu, Q.; Zhang, H.; Smeester, L.; Zou, F.; Kesic, M.; Jaspers, I.; Pi, J.; Fry, R.C. The NRF2-mediated oxidative stress response pathway is associated with tumor cell resistance to arsenic trioxide across the NCI-60 panel. BMC Med. Genomics 2010, 3, 37.
41. Navas-Acien, A.; Sharrett, A.R.; Silbergeld, E.K.; Schwartz, B.S.; Nachman, K.E.; Burke, T.A.; Guallar, E. Arsenic exposure and cardiovascular disease: A systematic review of the epidemiologic evidence. Am. J. Epidemiol. 2005, 162, 1037-1049.
42. Kligerman, A.D.; Doerr, C.L.; Tennant, A.H.; Harrington-Brock, K.; Allen, J.W.; Winkfield, E.; Poorman-Allen, P.; Kundu, B.; Funasaka, K.; Roop, B.C.; Mass, M.J.; DeMarini, D.M. 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.
43. Wang, C.H.; Hsiao, C.K.; Chen, C.L.; Hsu, L.I.; Chiou, H.Y.; Chen, S.Y.; Hsueh, Y.M.; Wu, M.M.; Chen, C.J. A review of the epidemiologic literature on the role of environmental arsenic exposure and cardiovascular diseases. Toxicol. Appl. Pharmacol. 2007, 222, 315-326.
44. Sykora, P.; Snow, E.T. Modulation of DNA polymerase beta-dependent base excision repair in cultured human cells after low dose exposure to arsenite. Toxicol. Appl. Pharmacol. 2008, 228, 385-394.
45. Zhang, T.C.; Schmitt, M.T.; Mumford, J.L. Effects of arsenic on telomerase and telomeres in relation to cell proliferation and apoptosis in human keratinocytes and leukemia cells in vitro. Carcinogenesis 2003, 24, 1811-1817.
46. Pi, J.; Yamauchi, H.; Kumagai, Y.; Sun, G.; Yoshida, T.; Aikawa, H.; Hopenhayn-Rich, C.; Shimojo, N. Evidence for induction of oxidative stress caused by chronic exposure of Chinese residents to arsenic contained in drinking water. Environ. Health Perspect. 2002, 110, 331-336.
47. Dixon, J.E.; McKinnon, D. Quantitative analysis of potassium channel mRNA expression in atrial and ventricular muscle of rats. Circ. Res. 1994, 75, 252-260.
48. Wan, X.; Dennis, A.T.; Obejero-Paz, C.; Overholt, J.L.; Heredia-Moya, J.; Kirk, K.L.; Ficker, E. Oxidative inactivation of the lipid phosphatase phosphatase and tensin homolog on chromosome ten (PTEN) as a novel mechanism of acquired long QT syndrome. J. Biol. Chem. 2011, 286, 2843-2852.
49. Diaz-Villaseñor, A.; Burns, A.L.; Hiriart, M.; Cebrián, M.E.; Ostrosky-Wegman, P. Arsenic-induced alteration in the expression of genes related to type 2 diabetes mellitus. Toxicol. Appl. Pharmacol. 2007, 225, 123-133.
50. Diaz-Villaseñor, A.; Hiriart, M.; Cebrián, M.E.; Zacarías-Castillo, R.; Ostrosky-Wegman, P. The activity of calpains in lymphocytes is glucose-dependent and is decreased in diabetic patients. Blood Cells Mol. Dis. 2008, 40, 414-419.
51. Smeester, L.; Rager, J.E.; Bailey, K.A.; Guan, X.; Smith, N.; García-Vargas, G.; Del Razo, L.M.; Drobná, Z.; Kelkar, H.; Stýblo, M.; Fry, R.C. Epigenetic changes in individuals with arsenicosis. Chem. Res. Toxicol. 2011, 24, 165-167.