The accumulations of HIF-1α and HIF-2α by JNK and ERK are involved in biphasic effects induced by different levels of arsenite in human bronchial epithelial cells

Toxicology and Applied Pharmacology

Volumn 266, Issue 2, 2013, Pages 187-197

  Xu, Yuan ^a,b   Li, Yuan ^a,b   Li, Huiqiao ^c   Pang, Ying ^a,b   Zhao, Yue ^a,b   Jiang, Rongrong ^a,b   Shen, Lu ^a,b   Zhou, Jianwei ^b   Wang, Xinru ^b   Liu, Qizhan ^a,b  

^a NANJING MEDICAL UNIVERSITY   (China)

^b Nanjing Medical University   (China)

^c Qujing Center for Disease Control and Prevention   (China)

Author keywords

Arsenite; Biphasic effects; C Jun N terminal kinases (JNK); Extracellular signal regulated kinases (ERK); Hypoxia inducible factor 1 ; Hypoxia inducible factor 2

Indexed keywords

ARSENIC TRIOXIDE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; MITOGEN ACTIVATED PROTEIN KINASE; STRESS ACTIVATED PROTEIN KINASE; UBIQUITINATED PROTEIN;

APOPTOSIS; ARTICLE; BIOACCUMULATION; BRONCHUS MUCOSA; CARCINOGENESIS; CELL ASSAY; CELL PROLIFERATION; CONTROLLED STUDY; DNA DAMAGE; DOSE RESPONSE; DOWN REGULATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; EPITHELIUM CELL; HORMESIS; HUMAN; HUMAN CELL; IMMUNOCYTOCHEMISTRY; PROTEIN DEGRADATION; REAL TIME POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

APOPTOSIS; ARSENITES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRONCHI; CELL PROLIFERATION; CELLS, CULTURED; DNA DAMAGE; DOSE-RESPONSE RELATIONSHIP, DRUG; DOWN-REGULATION; EPITHELIAL CELLS; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; JNK MITOGEN-ACTIVATED PROTEIN KINASES; SIGNAL TRANSDUCTION; SODIUM COMPOUNDS;

EID: 84870788011     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2012.11.014     Document Type: Article

References (46)

1. An J., Yin L., Shang Y., Zhong Y., Zhang X., Wu M., Yu Z., Sheng G., Fu J., Huang Y. The combined effects of BDE47 and BaP on oxidatively generated DNA damage in L02 cells and the possible molecular mechanism. Mutat. Res. 2011, 721:192-198.
2. Antoniou X., Sclip A., Ploia C., Colombo A., Moroy G., Borsello T. JNK contributes to Hif-1alpha regulation in hypoxic neurons. Molecules 2010, 15:114-127.
3. Bagla P., Kaiser J. India's spreading health crisis draws global arsenic experts. Science 1996, 274:174-175.
4. Bode A.M., Dong Z. The paradox of arsenic: molecular mechanisms of cell transformation and chemotherapeutic effects. Crit. Rev. Oncol. Hematol. 2002, 42:5-24.
5. Broich G., Lavezzi A.M., Biondo B., Pignataro L.D. PCNA-a cell proliferation marker in vocal cord cancer. Part II: recurrence in malignant laryngeal lesions. In Vivo 1996, 10:175-178.
6. Calabrese E. Hormesis, non-linearity, and risk communication. Hum. Exp. Toxicol. 2009, 28:5-6.
7. Chung J., Lee H.S., Chung H.Y., Yoon T.R., Kim H.K. Salicylideneamino-2-thiophenol inhibits inflammatory mediator genes (RANTES, MCP-1, IL-8 and HIF-1alpha) expression induced by tert-butyl hydroperoxide via MAPK pathways in rat peritoneal macrophages. Biotechnol. Lett. 2008, 30:1553-1558.
8. Comerford K.M., Cummins E.P., Taylor C.T. c-Jun NH2-terminal kinase activation contributes to hypoxia-inducible factor 1alpha-dependent P-glycoprotein expression in hypoxia. Cancer Res. 2004, 64:9057-9061.
9. Conrad P.W., Freeman T.L., Beitner-Johnson D., Millhorn D.E. EPAS1 trans-activation during hypoxia requires p42/p44 MAPK. J. Biol. Chem. 1999, 274:33709-33713.
10. Covello K.L., Kehler J., Yu H., Gordan J.D., Arsham A.M., Hu C.J., Labosky P.A., Simon M.C., Keith B. HIF-2alpha regulates Oct-4: effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes Dev. 2006, 20:557-570.
11. Danaee H., Nelson H.H., Liber H., Little J.B., Kelsey K.T. Low dose exposure to sodium arsenite synergistically interacts with UV radiation to induce mutations and alter DNA repair in human cells. Mutagenesis 2004, 19:143-148.
12. Dong Z. The molecular mechanisms of arsenic-induced cell transformation and apoptosis. Environ. Health Perspect. 2002, 110(Suppl. 5):757-759.
13. Duyndam M.C., Hulscher S.T., van der Wall E., Pinedo H.M., Boven E. Evidence for a role of p38 kinase in hypoxia-inducible factor 1-independent induction of vascular endothelial growth factor expression by sodium arsenite. J. Biol. Chem. 2003, 278:6885-6895.
14. 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.
15. Fernandez-Capetillo O., Lee A., Nussenzweig M., Nussenzweig A. H2AX: the histone guardian of the genome. DNA Repair 2004, 3:959-967.
16. Florczyk U., Czauderna S., Stachurska A., Tertil M., Nowak W., Kozakowska M., Poellinger L., Jozkowicz A., Loboda A., Dulak J. Opposite effects of HIF-1alpha and HIF-2alpha on the regulation of IL-8 expression in endothelial cells. Free Radic. Biol. Med. 2011, 51:1882-1892.
17. Franovic A., Lee S. HIF-2alpha: many cancers, one engine?. Cell Cycle 2010, 9:859-860.
18. Gao F., Brant K.A., Ward R.M., Cattley R.T., Barchowsky A., Fabisiak J.P. Multiple protein kinase pathways mediate amplified IL-6 release by human lung fibroblasts co-exposed to nickel and TLR-2 agonist, MALP-2. Toxicol. Appl. Pharmacol. 2010, 247:146-157.
19. Gordan J.D., Bertout J.A., Hu C.J., Diehl J.A., Simon M.C. HIF-2alpha promotes hypoxic cell proliferation by enhancing c-myc transcriptional activity. Cancer Cell 2007, 11:335-347.
20. Grimberg B.T., Erickson J.J., Sramkoski R.M., Jacobberger J.W., Zimmerman P.A. Monitoring Plasmodium falciparum growth and development by UV flow cytometry using an optimized Hoechst-thiazole orange staining strategy. Cytometry A 2008, 73:546-554.
21. Guo W., Yang Z., Xia Q., Liu J., Yu Y., Li J., Zuo Z., Zhang D., Li X., Shi X., Huang C. Arsenite stabilizes HIF-1alpha protein through p85alpha-mediated up-regulation of inducible Hsp70 protein expression. Cell. Mol. Life Sci. 2010, 68:475-488.
22. He X.Q., Chen R., Yang P., Li A.P., Zhou J.W., Liu Q.Z. Biphasic effect of arsenite on cell proliferation and apoptosis is associated with the activation of JNK and ERK1/2 in human embryo lung fibroblast cells. Toxicol. Appl. Pharmacol. 2007, 220:18-24.
23. Huang Y., Zhang J., McHenry K.T., Kim M.M., Zeng W., Lopez-Pajares V., Dibble C.C., Mizgerd J.P., Yuan Z.M. 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.
24. 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.
25. Kaltreider R.C., Pesce C.A., Ihnat M.A., Lariviere J.P., Hamilton J.W. Differential effects of arsenic(III) and chromium(VI) on nuclear transcription factor binding. Mol. Carcinog. 1999, 25:219-229.
26. Koh M.Y., Lemos R., Liu X., Powis G. The hypoxia-associated factor switches cells from HIF-1alpha- to HIF-2alpha-dependent signaling promoting stem cell characteristics, aggressive tumor growth and invasion. Cancer Res. 2011, 71:4015-4027.
27. Kumareswaran R., Ludkovski O., Meng A., Sykes J., Pintilie M., Bristow R.G. Chronic hypoxia compromises repair of DNA double-strand breaks to drive genetic instability. J. Cell Sci. 2011, 125:189-199.
28. Li Y., Jiang R., Zhao Y., Xu Y., Ling M., Pang Y., Shen L., Zhou Y., Zhang J., Zhou J., Wang X., Liu Q. Opposed arsenite-mediated regulation of p53-survivin is involved in neoplastic transformation, DNA damage, or apoptosis in human keratinocytes. Toxicology 2012, 300:121-131.
29. Mattson M.P. Hormesis defined. Ageing Res. Rev. 2008, 7:1-7.
30. Menrad H., Werno C., Schmid T., Copanaki E., Deller T., Dehne N., Brune B. Roles of hypoxia-inducible factor-1alpha (HIF-1alpha) versus HIF-2alpha in the survival of hepatocellular tumor spheroids. Hepatology 2010, 51:2183-2192.
31. Mottet D., Michel G., Renard P., Ninane N., Raes M., Michiels C. Role of ERK and calcium in the hypoxia-induced activation of HIF-1. J. Cell. Physiol. 2003, 194:30-44.
32. Ohh M., Park C.W., Ivan M., Hoffman M.A., Kim T.Y., Huang L.E., Pavletich N., Chau V., Kaelin W.G. Ubiquitination of hypoxia-inducible factor requires direct binding to the beta-domain of the von Hippel-Lindau protein. Nat. Cell Biol. 2000, 2:423-427.
33. Reddel R.R., Ke Y., Gerwin B.I., McMenamin M.G., Lechner J.F., Su R.T., Brash D.E., Park J.B., Rhim J.S., Harris C.C. Transformation of human bronchial epithelial cells by infection with SV40 or adenovirus-12 SV40 hybrid virus, or transfection via strontium phosphate coprecipitation with a plasmid containing SV40 early region genes. Cancer Res. 1988, 48:1904-1909.
34. Sakon S., Xue X., Takekawa M., Sasazuki T., Okazaki T., Kojima Y., Piao J.H., Yagita H., Okumura K., Doi T., Nakano H. NF-kappaB inhibits TNF-induced accumulation of ROS that mediate prolonged MAPK activation and necrotic cell death. EMBO J. 2003, 22:3898-3909.
35. Schults M.A., Timmermans L., Godschalk R.W., Theys J., Wouters B.G., van Schooten F.J., Chiu R.K. Diminished carcinogen detoxification is a novel mechanism for hypoxia-inducible factor 1-mediated genetic instability. J. Biol. Chem. 2010, 285:14558-14564.
36. Shen S., Lee J., Weinfeld M., Le X.C. Attenuation of DNA damage-induced p53 expression by arsenic: a possible mechanism for arsenic co-carcinogenesis. Mol. Carcinog. 2008, 47:508-518.
37. Shin H.J., Choi M.S., Ryoo N.H., Nam K.Y., Park G.Y., Bae J.H., Suh S.I., Baek W.K., Park J.W., Jang B.C. Manganese-mediated up-regulation of HIF-1alpha protein in Hep2 human laryngeal epithelial cells via activation of the family of MAPKs. Toxicol. In Vitro 2010, 24:1208-1214.
38. Song L., Li J., Zhang D., Liu Z.G., Ye J., Zhan Q., Shen H.M., Whiteman M., Huang C. IKKbeta programs to turn on the GADD45alpha-MKK4-JNK apoptotic cascade specifically via p50 NF-kappaB in arsenite response. J. Cell Biol. 2006, 175:607-617.
39. Soucy N.V., Klei L.R., Mayka D.D., Barchowsky A. Signaling pathways for arsenic-stimulated vascular endothelial growth factor-a expression in primary vascular smooth muscle cells. Chem. Res. Toxicol. 2004, 17:555-563.
40. Thayer K.A., Melnick R., Burns K., Davis D., Huff J. Fundamental flaws of hormesis for public health decisions. Environ. Health Perspect. 2005, 113:1271-1276.
41. Uchida T., Rossignol F., Matthay M.A., Mounier R., Couette S., Clottes E., Clerici C. Prolonged hypoxia differentially regulates hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha expression in lung epithelial cells: implication of natural antisense HIF-1alpha. J. Biol. Chem. 2004, 279:14871-14878.
42. Warnecke C., Zaborowska Z., Kurreck J., Erdmann V.A., Frei U., Wiesener M., Eckardt K.U. Differentiating the functional role of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha (EPAS-1) by the use of RNA interference: erythropoietin is a HIF-2alpha target gene in Hep3B and Kelly cells. FASEB J. 2004, 18:1462-1464.
43. Wen G., Calaf G.M., Partridge M.A., Echiburu-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.
44. Wirthner R., Wrann S., Balamurugan K., Wenger R.H., Stiehl D.P. Impaired DNA double-strand break repair contributes to chemoresistance in HIF-1 alpha-deficient mouse embryonic fibroblasts. Carcinogenesis 2008, 29:2306-2316.
45. Xu Y., Li Y., Pang Y., Ling M., Shen L., Jiang R., Zhao Y., Zhou J., Wang X., Liu Q. Blockade of p53 by HIF-2alpha, but not HIF-1alpha, is involved in arsenite-induced malignant transformation of human bronchial epithelial cells. Arch. Toxicol. 2012, 86:947-959.
46. 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.