Soluble nickel inhibits HIF-prolyl-hydroxylases creating persistent hypoxic signaling in A549 cells

Molecular Carcinogenesis

Volumn 45, Issue 7, 2006, Pages 479-489

  Davidson, Todd L ^a   Chen, Haobin ^a   Di Toro, Dominic M ^b   D'Angelo, Gisela ^c   Costa, Max ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF DELAWARE   (United States)

^c INSERM   (France)

Author keywords

Hypoxia inducible factor; Iron; Metals; Von Hippel Lindau

Indexed keywords

ASCORBIC ACID; HYPOXIA INDUCIBLE FACTOR 1ALPHA; IRON; METAL; NICKEL; NICKEL CHLORIDE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE;

ARTICLE; CANCER CELL CULTURE; CANCER THERAPY; CARCINOGENESIS; CARCINOGENIC ACTIVITY; CELL HYPOXIA; CELL STRAIN; CELL STRAIN A549; CONTROLLED STUDY; CULTURE MEDIUM; ENZYME INHIBITION; ENZYME STABILITY; ENZYME SUBUNIT; HUMAN; HUMAN CELL; IN VITRO STUDY; IRON DEPLETION; ISCHEMIA; LUNG NON SMALL CELL CANCER; MOLECULAR DYNAMICS; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY;

CELL HYPOXIA; CELL LINE, TUMOR; DIOXYGENASES; ENZYME INHIBITORS; HUMANS; LUNG NEOPLASMS; NICKEL; SIGNAL TRANSDUCTION;

EID: 33745728248     PISSN: 08991987     EISSN: 10982744     Source Type: Journal    
DOI: 10.1002/mc.20176     Document Type: Article

References (63)

1. 2 tension. Proc Natl Acad Sci USA 1995; 92:5510-5514.
2. Pugh CW, Ratcliffe PJ. Regulation of angiogenesis by hypoxia: Role of the HIF system. Nat Med 2003;9:677-684.
3. Semenza GL. HIF-1 and human disease: One highly involved factor. Genes Dev 1983;14:1983-1991.
4. Semenza GL. Hypoxia-inducible factor 1: Oxygen homeostasis and disease pathophysiology. Trends Mol Med 2001; 7:345-350.
5. Semenza GL. Targeting HIF-1 for cancer therapy. Nat Rev Cancer 2003;3:721-732.
6. Aalinkeel R, Nair MP, Sufrin G, et al. Gene expression of angiogenic factors correlates with metastatic potential of prostate cancer cells. Cancer Res 2004;64:5311-5321.
7. Dachs GU, Tozer GM. Hypoxia modulated gene expression: Angiogenesis, metastasis and therapeutic exploitation. Eur J Cancer 2000;36:1649-1660.
8. Hopfl G, Ogunshola O, Gassmann M. HIFs and tumors-causes and consequences. Am J Physiol Regul Integr Comp Physiol 2004;286:R608-R623.
9. Paul SA, Simons JW, Mabjeesh NJ. HIF at the crossroads between ischemia and carcinogenesis. J Cell Physiol 2004; 200:20-30.
10. Brown JM. Tumor microenvironment and the response to anticancer therapy. Cancer Biol Ther 2002;1:453-458.
11. Semenza GL. Hypoxia, clonal selection, and the role of HIF-1 in tumor progression. Crit Rev Biochem Mol Biol 2000; 35:71-103.
12. Carmeliet P, Dor Y, Herbert JM, et al. Role of HIF-1 alpha in hypoxia-mediated apoptosis, cell proliferation and tumour angiogenesis. [erratum appears in Nature 1998 Oct 1; 395(6701):525 Note: Keshet E [corrected to Keshert E]]. Nature 1998;394:485-490.
13. Kung AL, Wang S, Klco JM, Kaelin WG, Livingston DM. Suppression of tumor growth through disruption of hypoxia-inducible transcription. Nat Med 2000;6:1335-1340.
14. Epstein AC, Gleadle JM, McNeill LA, et al. C elegans EGL-9 and mammalian homologs define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 2001;107: 43-54.
15. 2-regulated prolyl hydroxylation. Science 2001;292:468-472.
16. Bruick RK. Oxygen sensing in the hypoxic response pathway: Regulation of the hypoxia-inducible transcription factor. Genes Dev 2003;17:2614-2623.
17. Biedermann KA, Landolph JR. Induction of anchorage independence in human diploid foreskin fibroblasts by carcinogenic metal salts. Cancer Res 1987;47:3815-3823.
18. Conway K, Costa M. Nonrandom chromosomal alterations in nickel-transformed Chinese hamster embryo cells. Cancer Res 1989;49:6032-6038.
19. Doll R. Cancer of the nose and lung in nickel workers. Br J Ind Med 1958;15:217-223.
20. Grimsrud TK, Berge SR, Haldorsen T, Andersen A. Exposure to different forms of nickel and risk of lung cancer. Am J Epidemiol 2002;156:1123-1132.
21. Grimsrud TK, Berge SR, Martinsen JI, Andersen A. Lung cancer incidence among Norwegian nickel-refinery workers 1953-2000. J Environmen Monit 2003;5:190-197.
22. International Agency for Research on Cancer I. Monographs on the evaluation of carcinogenic risks to humans: Chromium nickel and welding. Lyon, France: IARC; Vol. 49.1990.
23. Lin X, Dowjat WK, Costa M. Nickel-induced transformation of human cells causes loss of the phosphorylation of the retinoblastoma protein. Cancer Res 1994;54:2751-2754.
24. Maenza RM, Pradhan AM, Sunderman FW, Jr. Rapid induction of sarcomas in rats by combination of nickel sulfide and 3,4-benzpyrene. Cancer Res 1971;31:2067-2071.
25. McEwan JC. Cytological monitoring of nickel sinter plant workers. Ann N Y Acad Sci 1976;271:365-369.
26. Chen H, Davidson T, Singleton S, Garrick MD, Costa M. Nickel decreases cellular iron level and converts cytosolic aconitase to iron-regulatory protein 1 in A549 cells. Toxicol Appl Pharmacol 2005;206:275-287.
27. Davidson T, Salnikow K, Costa M. Hypoxia inducible factor-1 alpha-independent suppression of aryl hydrocarbon receptor-regulated genes by nickel. Mol Pharmacol 2003; 64:1485-1493.
28. Salnikow K, Davidson T, Zhang Q, Chen LC, Su W, Costa M. The involvement of hypoxia-inducible transcription factor-1-dependent pathway in nickel carcinogenesis. Cancer Res 2003;63:3524-3530.
29. Li J, Davidson G, Huang Y, et al. Nickel compounds act through phosphatidylinositol-3-kinase/Akt-dependent, p70(S6k)-independent pathway to induce hypoxia inducible factor transactivation and Cap43 expression in mouse epidermal CI41 cells. Cancer Res 2004;64:94-101.
30. Salnikow K, Donald SP, Bruick RK, Zhitkovich A, Phang JM, Kasprzak KS. Depletion of intracellular ascorbate by the carcinogenic metals nickel and cobalt results in the induction of hypoxic stress. J Biol Chem 2004;279:40337-40344.
31. D'Angelo G, Duplan E, Boyer N, Vigne P, Frelin C. Hypoxia upregulates prolyl hydroxylase activity: A feedback mechanism that limits HIF-1 responses during reoxygenation. J Biol Chem 2003;278:38183-38187.
32. Rothenberger S, Mullner EW, Kuhn LC. The mRNA-binding protein which controls ferritin and transferrin receptor expression is conserved during evolution. Nucleic Acids Res 1990;18:1175-1179.
33. Oehme F, Jonghaus W, Narouz-Ott L, Huetter J, Flamme I. A nonradioactive 96-well plate assay for the detection of hypoxia-inducible factor prolyl hydroxylase activity. Anal Biochem 2004;330:74-80.
34. Martell AE, Smith RM, Motekaitis RJ. NIST critically selected stability constants of metal complexes. NIST standard reference database 46 Version 6.0. Gaithersburg, MD: US Dept. of Commerce National Institute of Standards Technology; 2001.
35. Davidson T, Chen H, Garrick MD, D'Angelo G, Costa M. Soluble nickel interferes with iron homeostasis. Mol Cell Biochem 2005;279:157-162.
36. Grimsrud TK, Berge SR, Haldorsen T, Andersen A. Can lung cancer risk among nickel refinery workers be explained by occupational exposures other than nickel? Epidemiology 2005;16:146-154.
37. Costa M. Molecular mechanisms of nickel carcinogenesis. Ann Annu Rev Pharmacol Toxicol 1991;31:321-337.
38. Costa M. Model for the epigenetic mechanism of action of nongenotoxic carcinogens. Am J Clin Nutr 1995;61:666S-669S.
39. Salnikow K, Costa M. Epigenetic mechanisms of nickel carcinogenesis. J Environ Pathol Toxicol Oncol 2000;19: 307-318.
40. Kasprzak KS, Sunderman FW, Jr., Salnikow K. Nickel carcinogenesis. Mutat Res 2003;533:67-97.
41. Maxwell PH, Ratcliffe PJ. Oxygen sensors and angiogenesis. Semin Cell Dev Biol 2002;13:29-37.
42. Erez N, Milyavsky M, Eilam R, Shats I, Goldfinger N, Rotter V. Expression of prolyl-hydroxylase-1 (PHD1/EGLN2)suppresses hypoxia inducible factor-1 alpha activation and inhibits tumor growth. Cancer Res 2003;63:8777-8783.
43. Salnikow K, An WG, Melillo G, Blagosklonny MV, Costa M. Nickel-induced transformation shifts the balance between HIF-1 and p53 transcription factors. Carcinogenesis 1999; 20:1819-1823.
44. Salnikow K, Davidson T, Costa M. The role of hypoxia-inducible signaling pathway in nickel carcinogenesis. Environ Health Perspect 2002;110:831-834.
45. Gao N, Jiang BH, Leonard SS, et al. p38 Signaling-mediated hypoxia-inducible factor 1alpha and vascular endothelial growth factor induction by Cr(VI)in DU145 human prostate carcinoma cells. J Biol Chem 2002;277:45041-45048.
46. Majamaa K, Kuutti-Savolainen ER, Tuderman L, Kivirikko KI. Turnover of prolyl hydroxylase tetramers and the monomersize protein in chick-embryo cartilaginous bone and lung in vivo. Biochem J 1979;178:313-322.
47. Knowles HJ, Raval RR, Harris AL, Ratcliffe PJ. Effect of ascorbate on the activity of hypoxia-inducible factor in cancer cells. Cancer Res 2003;63:1764-1768.
48. Bridges KR, Hoffman KE. The effects of ascorbic acid on the intracellular metabolism of iron and ferritin. J Biol Chem 1986;261:14273-14277.
49. Kivirikko KI, Myllyharju J. Prolyl 4-hydroxylases and their protein disulfide isomerase subunit. Matrix Biol 1998;16: 357-368.
50. Kivirikko KI, Pihlajaniemi T. Collagen hydroxylases and the protein disulfide isomerase subunit of prolyl 4-hydroxylases. Adv Enzymol Relat Areas Mol Biol 1998;72:325-398.
51. Rapaka RS, Sorensen KR, Lee SD, Bhatnagar RS. Inhibition of hydroxyproline synthesis by palladium ions. Biochim Biophys Acta 1976;429:63-71.
52. Tuderman L, Myllyla R, Kivirikko KI. Mechanism of the prolyl hydroxylase reaction 1. Role of co-substrates. Eur J Biochem 1977;80:341-348.
53. Batie CJ, Ballou DP. Phthalate dioxygenase. Methods Enzymol 1990;188:61-70.
54. Batie CJ, LaHaie E, Ballou DP. Purification and characterization of phthalate oxygenase and phthalate oxygenase reductase from Pseudomonas cepacia. J Biol Chem 1987; 262:1510-1518.
55. Ming LJ, Que L, Jr., Kriauciunas A, Frolik CA, Chen VJ. NMR studies of the active site of isopenicillin N synthase, a non-heme iron(II) enzyme. Biochemistry 1991;30:11653-11659.
56. Schofield CJ, Ratcliffe PJ. Oxygen sensing by HIF hydroxylases. Nat Rev Mol Cell Biol 2004;5:343-354.
57. Elkins JM, Hewitson KS, McNeill LA, et al. Structure of factor-inhibiting hypoxia-inducible factor (HIF) reveals mechanism of oxidative modification of HIF-1 alpha. J Biol Chem 2003;278:1802-1806.
58. Maxwell P, Salnikow K. HIF-1: An oxygen and metal responsive transcription factor. Cancer Biol Ther 2004; 3:29-35.
59. Yuan Y, Hilliard G, Ferguson T, Millhorn DE. Cobalt inhibits the interaction between hypoxia-inducible factor-alpha and von Hippel-Lindau protein by direct binding to hypoxia-inducible factor-alpha. J Biol Chem 2003;278:15911-15916.
60. Martin F, Linden T, Katschinski DM, et al. Copper-dependent activation of hypoxia-inducible factor (HIF)-1: Implications for ceruloplasmin regulation. Blood 2005;105:4613-4619.
61. Kagi JH, Kojima Y. Chemistry and biochemistry of metallothionein. Experientia Supplementum 1987;52:25-61.
62. Nath R, Kambadur R, Gulati S, Paliwal VK, Sharma M. Molecular aspects, physiological function, and clinical significance of metallothioneins. Crit Rev Food Sci Nutr 1988;27:41-85.
63. Hirsila M, Koivunen P, Xu L, Seeley T, Kivirikko KI, Myllyharju J. Effect of desferrioxamine and metals on the hydroxylases in the oxygen sensing pathway. FASEB J 2005;19:1308-1310.