Delayed temporal increase of hepatic Hsp70 in ApoE knockout mice after prenatal arsenic exposure

Toxicological Sciences

Volumn 131, Issue 1, 2013, Pages 225-233

  Ngalame, Ntube N O ^a,c   Micciche, Andrew F ^a   Feil, Marilyn E ^a   States, J Christopher ^a,b  

^a University of Louisville School of Medicine   (United States)

^b UNIVERSITY OF LOUISVILLE   (United States)

^c NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

Arsenic; DNA methylation; Hsp70; Liver; MicroRNA; Prenatal exposure; Stress response

Indexed keywords

APOLIPOPROTEIN E; ARSENIC; DRINKING WATER; HEAT SHOCK PROTEIN 70; MESSENGER RNA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARSENIC POISONING; ARTICLE; ATHEROSCLEROSIS; CONTROLLED STUDY; DNA METHYLATION; FEMALE; LIVER TOXICITY; MICROARRAY ANALYSIS; MOUSE; NONHUMAN; POSTNATAL DEVELOPMENT; PREGNANCY; PRENATAL EXPOSURE; PROMOTER REGION; PROTEIN EXPRESSION; WESTERN BLOTTING;

ANIMALS; APOLIPOPROTEINS E; ARSENITES; ATHEROSCLEROSIS; BLOTTING, WESTERN; CPG ISLANDS; DNA METHYLATION; DNA-BINDING PROTEINS; EPIGENESIS, GENETIC; FEMALE; HSP70 HEAT-SHOCK PROTEINS; LIVER; MICE; MICE, KNOCKOUT; NF-E2-RELATED FACTOR 2; PREGNANCY; PRENATAL EXPOSURE DELAYED EFFECTS; PROMOTER REGIONS, GENETIC; PROTEIN TRANSPORT; SODIUM COMPOUNDS; TRANSCRIPTION FACTORS; WATER POLLUTANTS, CHEMICAL;

MUS;

EID: 84872412175     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfs264     Document Type: Article

References (40)

1. Andrew, A. S., Bernardo, V., Warnke, L. A., Davey, J. C., Hampton, T., Mason, R. A., Thorpe, J. E., Ihnat, M. A., and Hamilton, J. W. (2007). Exposure to arsenic at levels found in U.S. drinking water modifies expression in the mouse lung. Toxicol. Sci. 100, 75-87.
2. Arteel, G. E., Guo, L., Schlierf, T., Beier, J. I., Kaiser, J. P., Chen, T. S., Liu, M., Conklin, D. J., Miller, H. L., von Montfort, C., et al. (2008). Subhepatotoxic exposure to arsenic enhances lipopolysaccharide-induced liver injury in mice. Toxicol. Appl. Pharmacol. 226, 128-139.
3. Asea, A. (2007). Mechanisms of HSP72 release. J. Biosci. 32, 579-584.
4. Bartel, D. P. (2009). MicroRNAs: Target recognition and regulatory functions. Cell 136, 215-233.
5. Bellentani, S., Bedogni, G., and Tiribelli, C. (2008). Liver and heart: A new link? J. Hepatol. 49, 300-302.
6. Bielecka-Dabrowa, A., Barylski, M., Mikhailidis, D. P., Rysz, J., and Banach, M. (2009). HSP 70 and atherosclerosis-protector or activator? Expert Opin. Ther. Targets 13, 307-317.
7. Bohr, V. A., Smith, C. A., Okumoto, D. S., and Hanawalt, P. C. (1985). DNA repair in an active gene: Removal of pyrimidine dimers from the DHFR gene of CHO cells is much more efficient than in the genome overall. Cell 40, 359-369.
8. Brea, A., Mosquera, D., Martín, E., Arizti, A., Cordero, J. L., and Ros, E. (2005). Nonalcoholic fatty liver disease is associated with carotid atherosclerosis: A case-control study. Arterioscler. Thromb. Vasc. Biol. 25, 1045-1050.
9. Chen, H., Li, S., Liu, J., Diwan, B. A., Barrett, J. C., and Waalkes, M. P. (2004). Chronic inorganic arsenic exposure induces hepatic global and individual gene hypomethylation: Implications for arsenic hepatocarcinogenesis. Carcinogenesis 25, 1779-1786.
10. Concha, G., Vogler, G., Lezcano, D., Nermell, B., and Vahter, M. (1998). Exposure to inorganic arsenic metabolites during early human development. Toxicol. Sci. 44, 185-190.
11. Del Razo, L. M., Quintanilla-Vega, B., Brambila-Colombres, E., Calderón-Aranda, E. S., Manno, M., and Albores, A. (2001). Stress proteins induced by arsenic. Toxicol. Appl. Pharmacol. 177, 132-148.
12. Gething, M. J., and Sambrook, J. (1992). Protein folding in the cell. Nature 355, 33-45.
13. Gorzowski, J. J., Eckerley, C. A., Halgren, R. G., Mangurten, A. B., and Phillips, B. (1995). Methylation-associated transcriptional silencing of the major histocompatibility complex-linked hsp70 genes in mouse cell lines. J. Biol. Chem. 270, 26940-26949.
14. Guha Mazumder, D. N. (2001). Arsenic and liver disease. J. Indian Med. Assoc. 99, 311, 314-315, 318.
15. Jin, Y., Xi, S., Li, X., Lu, C., Li, G., Xu, Y., Qu, C., Niu, Y., and Sun, G. (2006). Arsenic speciation transported through the placenta from mother mice to their newborn pups. Environ. Res. 101, 349-355.
16. Kato, K., Ito, H., and Okamoto, K. (1997). Modulation of the arsenite-induced expression of stress proteins by reducing agents. Cell Stress Chaperones 2, 199-209.
17. Khalil, S., Luciano, J., Chen, W., and Liu, A. Y. (2006). Dynamic regulation and involvement of the heat shock transcriptional response in arsenic carcinogenesis. J. Cell. Physiol. 207, 562-569.
18. Kiang, J. G., and Tsokos, G. C. (1998). Heat shock protein 70 kDa: Molecular biology, biochemistry, and physiology. Pharmacol. Ther. 80, 183-201.
19. Kobayashi, M. (2005). Molecular mechanisms activating the Nrf2-Keap1 pathway of antioxidant gene regulation. Antioxid. Rodox Signal. 7, 385-394.
20. Lemaire, M., Lemarié, C. A., Molina, M. F., Schiffrin, E. L., Lehoux, S., and Mann, K. K. (2011). Exposure to moderate arsenic concentrations increases atherosclerosis in ApoE-/- mouse model. Toxicol. Sci. 122, 211-221.
21. Liu, J., Kadiiska, M. B., Liu, Y., Lu, T., Qu, W., and Waalkes, M. P. (2001). Stress-related gene expression in mice treated with inorganic arsenicals. Toxicol. Sci. 61, 314-320.
22. Liu, J., Xie, Y., Ward, J. M., Diwan, B. A., and Waalkes, M. P. (2004). Toxicogenomic analysis of aberrant gene expression in liver tumors and nontumorous livers of adult mice exposed in utero to inorganic arsenic. Toxicol. Sci. 77, 249-257.
23. Lu, X., and Kakkar, V. (2010). The role of heat shock protein (HSP) in atherosclerosis: Pathophysiology and clinical opportunities. Curr. Med. Chem. 17, 957-973.
24. Nordstrom, D. K. (2002). Public health. Worldwide occurrences of arsenic in ground water. Science 296, 2143-2145.
25. Petrick, J. S., Blachere, F. M., Selmin, O., and Lantz, R. C. (2009). Inorganic arsenic as a developmental toxicant: In utero exposure and alterations in the developing rat lungs. Mol. Nutr. Food Res. 53, 583-591.
26. Reichard, J. F., and Puga, A. (2010). Effects of arsenic exposure on DNA methylation and epigenetic gene regulation. Epigenomics 2, 87-104.
27. Rinaldi Tosi, M. E., Bocanegra, V., Manucha, W., Gil Lorenzo, A., and Vallés, P. G. (2011). The Nrf2-Keap1 cellular defense pathway and heat shock protein 70 (Hsp70) response. Role in protection against oxidative stress in early neonatal unilateral ureteral obstruction (UUO). Cell Stress Chaperones 16, 57-68.
28. Rosenberg, H. G. (1973). Systemic arterial disease with myocardial infarction. Report on two infants. Circulation 47, 270-275.
29. Rosenberg, H. G. (1974). Systemic arterial disease and chronic arsenicism in infants. Arch. Pathol. 97, 360-365.
30. Santra, A., Maiti, A., Das, S., Lahiri, S., Charkaborty, S. K., and Mazumder, D. N. (2000). Hepatic damage caused by chronic arsenic toxicity in experimental animals. J. Toxicol. Clin. Toxicol. 38, 395-405.
31. Srivastava, S., D'Souza, S. E., Sen, U., and States, J. C. (2007). In utero arsenic exposure induces early onset of atherosclerosis in ApoE-/- mice. Reprod. Toxicol. 23, 449-456.
32. Srivastava, S., Vladykovskaya, E. N., Haberzettl, P., Sithu, S. D., D'Souza, S. E., and States, J. C. (2009). Arsenic exacerbates atherosclerotic lesion formation and inflammation in ApoE-/- mice. Toxicol. Appl. Pharmacol. 241, 90-100.
33. States, J. C., Singh, A. V., Knudsen, T. B., Rouchka, E. C., Ngalame, N. O., Arteel, G. E., Piao, Y., and Ko, M. S. (2012). Prenatal arsenic exposure alters gene expression in the adult liver to a proinflammatory state contributing to accelerated atherosclerosis. PLOS ONE 7, e38713.
34. States, J. C., Srivastava, S., Chen, Y., and Barchowsky, A. (2009). Arsenic and cardiovascular disease. Toxicol. Sci. 107, 312-323.
35. Vega, V. L., Rodríguez-Silva, M., Frey, T., Gehrmann, M., Diaz, J. C., Steinem, C., Multhoff, G., Arispe, N., and De Maio, A. (2008). Hsp70 translocates into the plasma membrane after stress and is released into the extracellular environment in a membrane-associated form that activates macrophages. J. Immunol. 180, 4299-4307.
36. Waalkes, M. P., Liu, J., Chen, H., Xie, Y., Achanzar, W. E., Zhou, Y. S., Cheng, M. L., and Diwan, B. A. (2004). Estrogen signaling in livers of male mice with hepatocellular carcinoma induced by exposure to arsenic in utero. J. Natl. Cancer Inst. 96, 466-474.
37. Waalkes, M. P., Ward, J. M., Liu, J., and Diwan, B. A. (2003). Transplacental carcinogenicity of inorganic arsenic in the drinking water: Induction of hepatic, ovarian, pulmonary, and adrenal tumors in mice. Toxicol. Appl. Pharmacol. 186, 7-17.
38. Wijeweera, J. B., Gandolfi, A. J., Parrish, A., and Lantz, R. C. (2001). Sodium arsenite enhances AP-1 and NFkappaB DNA binding and induces stress protein expression in precision-cut rat lung slices. Toxicol. Sci. 61, 283-294.
39. Wright, B. H., Corton, J. M., El-Nahas, A. M., Wood, R. F., and Pockley, A. G. (2000). Elevated levels of circulating heat shock protein 70 (Hsp70) in peripheral and renal vascular disease. Heart Vessels 15, 18-22.
40. Xie, Y., Liu, J., Benbrahim-Tallaa, L., Ward, J. M., Logsdon, D., Diwan, B. A., and Waalkes, M. P. (2007). Aberrant DNA methylation and gene expression in livers of newborn mice transplacentally exposed to a hepatocarcinogenic dose of inorganic arsenic. Toxicology 236, 7-15.