Involvement of HIF-2α-mediated inflammation in arsenite-induced transformation of human bronchial epithelial cells

Toxicology and Applied Pharmacology

Volumn 272, Issue 2, 2013, Pages 542-550

  Xu, Yuan ^a,b   Zhao, Yue ^a,b   Xu, Wenchao ^a,b   Luo, Fei ^a,b   Wang, Bairu ^a,b   Li, Yuan ^a,b   Pang, Ying ^a,b   Liu, Qizhan ^a,b  

^a NANJING MEDICAL UNIVERSITY   (China)

^b Nanjing Medical University   (China)

Author keywords

Arsenite; Carcinogenesis; Hypoxia inducible factor 2 (HIF 2 ); Inflammation

Indexed keywords

ARSENIC TRIOXIDE; HYPOXIA INDUCIBLE FACTOR 2ALPHA; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8;

ARTICLE; BRONCHUS MUCOSA; CELL TRANSFORMATION; EPITHELIUM CELL; GENE OVEREXPRESSION; HUMAN; HUMAN CELL; INFLAMMATION; LONG TERM EXPOSURE; LUNG CARCINOGENESIS; MALIGNANT TRANSFORMATION; PHENOTYPE;

ARSENITE; CARCINOGENESIS; HYPOXIA INDUCIBLE FACTOR-2Α (HIF-2Α); INFLAMMATION;

ARSENITES; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; BRONCHI; CELL TRANSFORMATION, NEOPLASTIC; CYTOKINES; ENZYME-LINKED IMMUNOSORBENT ASSAY; EPITHELIAL CELLS; HUMANS; REAL-TIME POLYMERASE CHAIN REACTION; SODIUM COMPOUNDS; TIME FACTORS; UP-REGULATION;

EID: 84884146830     PISSN: 0041008X     EISSN: 10960333     Source Type: Journal    
DOI: 10.1016/j.taap.2013.06.017     Document Type: Article

References (49)

1. Balkwill F.R., Mantovani A. Cancer-related inflammation: common themes and therapeutic opportunities. Semin. Cancer Biol. 2012, 22:33-40.
2. Black P.C., Dinney C.P. Bladder cancer angiogenesis and metastasis - translation from murine model to clinical trial. Cancer Metastasis Rev. 2007, 26:623-634.
3. Brant K.A., Fabisiak J.P. Nickel and the microbial toxin, MALP-2, stimulate proangiogenic mediators from human lung fibroblasts via a HIF-1alpha and COX-2-mediated pathway. Toxicol. Sci. 2009, 107:227-237.
4. Brereton C.F., Sutton C.E., Lalor S.J., Lavelle E.C., Mills K.H. Inhibition of ERK MAPK suppresses IL-23- and IL-1-driven IL-17 production and attenuates autoimmune disease. J. Immunol. 2009, 183:1715-1723.
5. Bruning U., Fitzpatrick S.F., Frank T., Birtwistle M., Taylor C.T., Cheong A. NFkappaB and HIF display synergistic behaviour during hypoxic inflammation. Cell. Mol. Life Sci. 2012, 69:1319-1329.
6. Chen C.L., Hsu L.I., Chiou H.Y., Hsueh Y.M., Chen S.Y., Wu M.M., Chen C.J. Ingested arsenic, cigarette smoking, and lung cancer risk: a follow-up study in arseniasis-endemic areas in Taiwan. JAMA 2004, 292:2984-2990.
7. Chen W., Xu X., Bai L., Padilla M.T., Gott K.M., Leng S., Tellez C.S., Wilder J.A., Belinsky S.A., Scott B.R., Lin Y. Low-dose gamma-irradiation inhibits IL-6 secretion from human lung fibroblasts that promotes bronchial epithelial cell transformation by cigarette-smoke carcinogen. Carcinogenesis 2012, 33:1368-1374.
8. Cormet-Boyaka E., Jolivette K., Bonnegarde-Bernard A., Rennolds J., Hassan F., Mehta P., Tridandapani S., Webster-Marketon J., Boyaka P.N. An NF-kappaB-independent and Erk1/2-dependent mechanism controls CXCL8/IL-8 responses of airway epithelial cells to cadmium. Toxicol. Sci. 2012, 125:418-429.
9. Davies D.E., Holgate S.T. Asthma: the importance of epithelial mesenchymal communication in pathogenesis. Inflammation and the airway epithelium in asthma. Int. J. Biochem. Cell Biol. 2002, 34:1520-1526.
10. Elson D.A., Ryan H.E., Snow J.W., Johnson R., Arbeit J.M. Coordinate up-regulation of hypoxia inducible factor (HIF)-1alpha and HIF-1 target genes during multi-stage epidermal carcinogenesis and wound healing. Cancer Res. 2000, 60:6189-6195.
11. Escudero-Lourdes C., Medeiros M.K., Cardenas-Gonzalez M.C., Wnek S.M., Gandolfi J.A. Low level exposure to monomethyl arsonous acid-induced the over-production of inflammation-related cytokines and the activation of cell signals associated with tumor progression in a urothelial cell model. Toxicol. Appl. Pharmacol. 2010, 244:162-173.
12. Escudero-Lourdes C., Wu T., Camarillo J.M., Gandolfi A.J. Interleukin-8 (IL-8) over-production and autocrine cell activation are key factors in monomethylarsonous acid [MMA(III)]-induced malignant transformation of urothelial cells. Toxicol. Appl. Pharmacol. 2012, 258:10-18.
13. 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.
14. Fry R.C., Navasumrit P., Valiathan C., Svensson J.P., Hogan B.J., Luo M., Bhattacharya S., Kandjanapa K., Soontararuks S., Nookabkaew S., Mahidol C., Ruchirawat M., Samson L.D. Activation of inflammation/NF-kappaB signaling in infants born to arsenic-exposed mothers. PLoS Genet. 2007, 3:e207.
15. Han J., Lee J.S., Choi D., Lee Y., Hong S., Choi J., Han S., Ko Y., Kim J.A., Kim Y.M., Jung Y. Manganese (II) induces chemical hypoxia by inhibiting HIF-prolyl hydroxylase: implication in manganese-induced pulmonary inflammation. Toxicol. Appl. Pharmacol. 2009, 235:261-267.
16. Hollins F., Kaur D., Yang W., Cruse G., Saunders R., Sutcliffe A., Berger P., Ito A., Brightling C.E., Bradding P. Human airway smooth muscle promotes human lung mast cell survival, proliferation, and constitutive activation: cooperative roles for CADM1, stem cell factor, and IL-6. J. Immunol. 2008, 181:2772-2780.
17. 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.
18. Kaluz S., Van Meir E.G. At the crossroads of cancer and inflammation: Ras rewires an HIF-driven IL-1 autocrine loop. J. Mol. Med. (Berl.) 2011, 89:91-94.
19. Koh E., Iizasa T., Yamaji H., Sekine Y., Hiroshima K., Yoshino I., Fujisawa T. Significance of the correlation between the expression of interleukin 6 and clinical features in patients with non-small cell lung cancer. Int. J. Surg. Pathol. 2012, 20:233-239.
20. Kumagai Y., Sumi D. Arsenic: signal transduction, transcription factor, and biotransformation involved in cellular response and toxicity. Annu. Rev. Pharmacol. Toxicol. 2007, 47:243-262.
21. Kuphal S., Winklmeier A., Warnecke C., Bosserhoff A.K. Constitutive HIF-1 activity in malignant melanoma. Eur. J. Cancer 2010, 46:1159-1169.
22. Lau W.K., Chan S.C., Law A.C., Ip M.S., Mak J.C. The role of MAPK and Nrf2 pathways in ketanserin-elicited attenuation of cigarette smoke-induced IL-8 production in human bronchial epithelial cells. Toxicol. Sci. 2012, 125:569-577.
23. Li Y., Xu Y., Ling M., Yang Y., Wang S., Li Z., Zhou J., Wang X., Liu Q. mot-2-Mediated cross talk between nuclear factor-B and p53 is involved in arsenite-induced tumorigenesis of human embryo lung fibroblast cells. Environ. Heal. Perspect. 2010, 118:936-942.
24. 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.
25. Lin W.W., Karin M. A cytokine-mediated link between innate immunity, inflammation, and cancer. J. Clin. Invest. 2007, 117:1175-1183.
26. Mantovani A., Allavena P., Sica A., Balkwill F. Cancer-related inflammation. Nature 2008, 454:436-444.
27. Mumm J.B., Oft M. Cytokine-based transformation of immune surveillance into tumor-promoting inflammation. Oncogene 2008, 27:5913-5919.
28. Noreault-Conti T.L., Fellows A., Jacobs J.M., Trask H.W., Strom S.C., Evans R.M., Wrighton S.A., Sinclair P.R., Sinclair J.F., Nichols R.C. Arsenic decreases RXRalpha-dependent transcription of CYP3A and suppresses immune regulators in hepatocytes. Int. Immunopharmacol. 2012, 12:651-656.
29. O'Callaghan D.S., O'Donnell D., O'Connell F., O'Byrne K.J. The role of inflammation in the pathogenesis of non-small cell lung cancer. J. Thorac. Oncol. 2010, 5:2024-2036.
30. Pratheeshkumar P., Kuttan G. Vernolide-A inhibits radiation-induced hypoxia-mediated tumor angiogenesis by regulating HIF-1alpha, MMP-2, MMP-9, and VEGF. J. Environ. Pathol. Toxicol. Oncol. 2011, 30:139-151.
31. Rose-John S., Schooltink H. Cytokines are a therapeutic target for the prevention of inflammation-induced cancers. Recent Results Cancer Res. 2007, 174:57-66.
32. Ryu J.H., Yang S., Shin Y., Rhee J., Chun C.H., Chun J.S. Interleukin-6 plays an essential role in hypoxia-inducible factor 2alpha-induced experimental osteoarthritic cartilage destruction in mice. Arthritis Rheum. 2011, 63:2732-2743.
33. Saini Y., Greenwood K.K., Merrill C., Kim K.Y., Patial S., Parameswaran N., Harkema J.R., LaPres J.J. Acute cobalt-induced lung injury and the role of hypoxia-inducible factor 1alpha in modulating inflammation. Toxicol. Sci. 2010, 116:673-681.
34. Simeonova P.P., Hulderman T., Harki D., Luster M.I. Arsenic exposure accelerates atherogenesis in apolipoprotein E(-/-) mice. Environ. Heal. Perspect. 2003, 111:1744-1748.
35. Simpson J.L., Phipps S., Gibson P.G. Inflammatory mechanisms and treatment of obstructive airway diseases with neutrophilic bronchitis. Pharmacol. Ther. 2009, 124:86-95.
36. Singh N., Kumar D., Lal K., Raisuddin S., Sahu A.P. Adverse health effects due to arsenic exposure: modification by dietary supplementation of jaggery in mice. Toxicol. Appl. Pharmacol. 2010, 242:247-255.
37. Stasinopoulos I., O'Brien D.R., Bhujwalla Z.M. Inflammation, but not hypoxia, mediated HIF-1alpha activation depends on COX-2. Cancer Biol. Ther. 2009, 8:31-35.
38. 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.
39. Tapio S., Grosche B. Arsenic in the aetiology of cancer. Mutat. Res. 2006, 612:215-246.
40. Torii S., Kurihara A., Li X.Y., Yasumoto K., Sogawa K. Inhibitory effect of extracellular histidine on cobalt-induced HIF-1alpha expression. J. Biochem. 2011, 149:171-176.
41. Walmsley S.R., Print C., Farahi N., Peyssonnaux C., Johnson R.S., Cramer T., Sobolewski A., Condliffe A.M., Cowburn A.S., Johnson N., Chilvers E.R. Hypoxia-induced neutrophil survival is mediated by HIF-1alpha-dependent NF-kappaB activity. J. Exp. Med. 2005, 201:105-115.
42. Wang L., Yi T., Zhang W., Pardoll D.M., Yu H. IL-17 enhances tumor development in carcinogen-induced skin cancer. Cancer Res. 2010, 70:10112-10120.
43. Wang Y., Li L., Guo X., Jin X., Sun W., Zhang X., Xu R.C. Interleukin-6 signaling regulates anchorage-independent growth, proliferation, adhesion and invasion in human ovarian cancer cells. Cytokine 2012, 59:228-236.
44. Wang Y., Xu R.C., Zhang X.L., Niu X.L., Qu Y., Li L.Z., Meng X.Y. Interleukin-8 secretion by ovarian cancer cells increases anchorage-independent growth, proliferation, angiogenic potential, adhesion and invasion. Cytokine 2012, 59:145-155.
45. 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.
46. Wu J., Liu J., Waalkes M.P., Cheng M.L., Li L., Li C.X., Yang Q. High dietary fat exacerbates arsenic-induced liver fibrosis in mice. Exp. Biol. Med. (Maywood) 2008, 233:377-384.
47. Xu Y., Li Y., Li H., Pang Y., Zhao Y., Jiang R., Shen L., Zhou J., Wang X., Liu Q. The accumulations of HIF-1alpha and HIF-2alpha by JNK and ERK are involved in biphasic effects induced by different levels of arsenite in human bronchial epithelial cells. Toxicol. Appl. Pharmacol. 2012, 266:187-197.
48. 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.
49. 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.