Normoxic stabilization of hypoxia-inducible factor-1α by modulation of the labile iron pool in differentiating U937 macrophages: Effect of natural resistance-associated macrophage protein 1

Cancer Research

Volumn 66, Issue 5, 2006, Pages 2600-2607

  Knowles, Helen J ^a   Mole, David R ^b   Ratcliffe, Peter J ^b   Harris, Adrian L ^a  

^a JOHN RADCLIFFE HOSPITAL   (United Kingdom)

^b UNIVERSITY OF OXFORD   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

ASCORBIC ACID; HYPOXIA INDUCIBLE FACTOR 1ALPHA; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 1; PHORBOL 13 ACETATE 12 MYRISTATE; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE; TRANSCRIPTION FACTOR;

ARTICLE; CELL DIFFERENTIATION; CELL STRAIN U937; ENZYME INDUCTION; FLUORESCENCE; HUMAN; HUMAN CELL; HYDROXYLATION; HYPOXIA; IRON METABOLISM; MACROPHAGE ACTIVATION; MACROPHAGE FUNCTION; MONOCYTE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN STABILITY; RECEPTOR DOWN REGULATION; RECEPTOR UPREGULATION; RNA INTERFERENCE;

ASCORBIC ACID; CATION TRANSPORT PROTEINS; CELL DIFFERENTIATION; CELL LINE, TUMOR; FERROUS COMPOUNDS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; IRON; MACROPHAGES; OXYGEN; TETRADECANOYLPHORBOL ACETATE; U937 CELLS; UP-REGULATION;

EID: 33645080666     PISSN: 00085472     EISSN: None     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-05-2351     Document Type: Article

References (49)

1. Harris AL. Hypoxia - a key regulatory factor in tumor growth. Nat Rev 2002;2:38-47.
2. Epstein ACR, Gleadle JM, McNeill LA, et al. C. elegans EGL-9 and mammalian homologues define a family of dioxygenases that regulate HIF by prolyl hydroxylation. Cell 2001;107:42-54.
3. Bruick RK, McKnight SL. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 2001;294:1337-40.
4. Knowles HJ, Raval RR, Harris AL, Ratcliffe PJ. Effect of ascorbate on the activity of hypoxia-inducible factor in cancer cells. Cancer Res 2003;63:1764-8.
5. Zhong H, De Marzo AM, Laughner E, et al. Overexpression of hypoxia-inducible factor 1 α in common human cancers and their metastases. Cancer Res 1999; 59:5830-5.
6. Talks KL, Turley H, Gatter KC, et al. The expression and distribution of the hypoxia-inducible factors HIF-1α and HIF-2α in normal human tissues, cancers and tumor-associated macrophages. Am J Pathol 2000;157:411-21.
7. Bingle L, Brown NJ, Lewis CE. The role of tumor-associated macrophages in tumor progression: implications for new anticancer therapies. J Pathol 2002;196:254-65.
8. Leek RD, Lewis CE, Whitehouse R, Greenall M, Clarke J, Harris AL. Association of macrophage infiltration with angiogenesis and prognosis in invasive breast carcinoma. Cancer Res 1996;56:4625-9.
9. Burke B, Tang N, Corke KP, et al. Expression of HIF-1α by human macrophages: implications for the use of macrophages in hypoxia-regulated cancer therapy. J Pathol 2002;196:204-12.
10. Leek RD, Talks KL, Pezzella F, et al. Relation of hypoxia-inducible factor-2 α (HIF-2 α) expression in tumor-infiltrative macrophages to tumor angiogenesis and the oxidative thymidine phosphorylase pathway in human breast cancer. Cancer Res 2002;62:1326-9.
11. Onita T, Ji PG, Xuan JW, et al. Hypoxia-induced, perinecrotic expression of endothelial Per-ARNT-Sim domain protein-1/hypoxia-inducible factor-2α correlates with tumor progression, vascularisation and focal macrophage infiltration in bladder cancer. Clin Cancer Res 2002;8:471-80.
12. Cramer T, Yamanishi Y, Clausen BE, et al. HIF-1α is essential for myeloid cell-mediated inflammation. Cell 2003;112:645-57.
13. Shatrov VA, Sumbayev VV, Zhou J, Brune B. Oxidised low-density lipoprotein (oxLDL) triggers hypoxia-inducible factor-1α (HIF-1α) accumulation via redox-dependent mechanisms. Blood 2003;101:4847-9.
14. Blouin CC, Page EL, Soucy GM, Richard DE. Hypoxic gene activation by lipopolysaccharide in macrophages: implication of hypoxia-inducible factor 1α. Blood 2004; 103:1124-30.
15. Li J, Post M, Volk R, et al. PR39, a peptide regulator of angiogenesis. Nat Med 2000;6:49-55.
16. Tuckerman JR, Zhao Y, Hewitson KS, et al. Determination and comparison of specific activity of the HIF-prolyl hydroxylases. FEBS Lett 2004;576:145-50.
17. Epsztejn S, Kakhlon O, Glickstein H, Breuer W, Cabantchik I. Fluorescence analysis of the labile iron pool in mammalian cells. Anal Biochem 1997; 248:31-40.
18. Ponka P, Borova J, Neuwirt J, Fuchs O, Necas E. A study of intracellular iron metabolism using pyridoxal isonicotinoyl hydrazone and other synthetic chelating agents. Biochim Biophys Acta 1979;586:278-97.
19. O-Rourke JF, Tian Y-M, Ratcliffe PJ, Pugh CW. Oxygen-regulated and transactivating domains in endothelial PAS protein 1: comparison with hypoxia-inducible factor-1α. J Biol Chem 1999;274:2060-71.
20. Canonne-Hergaux F, Calafat J, Richer E, et al. Expression and subcellular localisation of NRAMP1 in human neutrophil granules. Blood 2002;100:268-75.
21. Sowter HM, Raval RR, Moore JW, Ratcliffe PJ, Harris AL. Predominant role of hypoxia-inducible transcription factor (HIF)-1α versus HIF-2α in regulation of the transcriptional response to hypoxia. Cancer Res 2003;63:6130-4.
22. Drakesmith H, Sweetland E, Schimanski L, et al. The hemochromatosis protein HFE inhibits iron export from macrophages. Proc Natl Acad Sci U S A 2002;99:15602-7.
23. Teichmann R, Stremmel W. Iron uptake by human upper small intestine microvillous membrane vesicles: indication for a facilitated transport mechanism mediated by a membrane iron-binding protein. J Clin Invest 1990;86:2145-53.
24. Berra E, Benizri E, Ginouves A, Volmat V, Roux D, Pouyssegur J. HIF prolyl-hydroxyase 2 is the key oxygen sensor setting low steady-state levels of HIF-1 α in normoxia. EMBO J 2003;22:4082-90.
25. Lando D, Peet DJ, Gorman JJ, Whelan DA, Whitelaw ML, Bruick RK. FIH-1 is an asparagunyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev 2002;16:1466-71.
26. Cellier M, Shustik C, Dalton W, et al. Expression of the human NRAMP1 gene in professional primary phagocytes: studies in blood cells and in HL-60 promyelocytic leukaemia. J Leukoc Biol 1997;61:96-105.
27. Barton CH, Biggs TE, Baker ST, Bowen H, Atkinson PG. Nramp1: a link between intracellular iron transport and innate resistance to intracellular pathogens. J Leukoc Biol 1999;66:757-62.
28. G169 in RAW264.7 cell transfectants: analysis of intracellular iron transport. Immunology 1999;96:656-62.
29. Pietrangelo A. The ferroportin disease. Blood Cells Mol Dis 2004;32:131-8.
30. Sarkar J, Seshadri V, Tripoulas NA, Ketterer ME, Fox PL. Role of ceruloplasmin in macrophage iron efflux during hypoxia. J Biol Chem 2003;278:44018-24.
31. Bridges KR, Hoffman KE. The effects of ascorbic acid on the intracellular metabolism of iron and ferritin. J Biol Chem 1986;261:14273-7.
32. May JM, Qu Z, Mandiratta S. Role of ascorbic acid in transferrin- independent reduction and uptake of iron by U937 cells. Biochem Pharmacol 1999;57:1275-82.
33. Minta JO, Pambrun L. In vitro induction of cytologic and functional differentiation of the immature human monocyte-like cell line U937 with phorbol myristate acetate. Am J Pathol 1985;119:111-26.
34. Asseffa A, Dickson LA, Mohla S, Bremner TA. Phorbol myristate acetate-differentiated THP1 cells display increased levels of MHC class I and class II mRNA and interferon-γ-inducible tumoricidal activity. Oncol Res 1993;5:11-8.
35. Appelhoff RJ, Tian YM, Raval RR, et al. Differential regulation of the prolyl hydroxylases PHD1, PHD2 and PHD3 in the regulation of hypoxia-inducible factor. J Biol Chem 2004;279:38458-65.
36. 2-regulated prolyl hydroxylation. Science 2001;292:468-72.
37. Kakhlon O, Cabantchik ZI. The labile iron pool: characterisation, measurement and participation in cellular processes. Free Radic Biol Med 2002;33:1037-46.
38. Wyllie S, Seu P, Goss JA. The natural resistance-associated macrophage protein 1 Slc11a1 (formerly Nramp1) and iron metabolism in macrophages. Microbes Infect 2002;4:351-9.
39. +-coupled metal-ion transporters Nramp1 and DMT1. Pflugers Arch 2004;447:571-9.
40. Gruenheid S, Pinner E, Desjardins M, Gros P. Natural resistance to infection with intracellular pathogens: the Nramp1 protein is recruited to the membrane of the phagosome. J Exp Med 1997;185:717-30.
41. Forbes JR, Gros P. Iron, manganese, and cobalt transport by Nramp1 (Slc11a1) and Nramp2 (Slc11a2) expressed at the plasma membrane. Blood 2003;102:1884-92.
42. Zwilling BS, Kuhn DE, Wikoff L, Brown D, Lafuse W. Role of iron in Nramp1-mediated inhibition of mycobacterial growth. Infect Immun 1999;67:1386-92.
43. Tenopoulou M, Doulias PT, Barbouti A, Brunk U, Galaris D. Role of compartmentalised redox-active iron in hydrogen peroxide-induced DNA damage and apoptosis. Biochem J 2005;387:703-10.
44. Atkinson PGP, Barton H. Ectopic expression of Nramp1 in COS-1 cells modulates iron accumulation. FEBS Lett 1998;425:239-42.
45. Baker ST, Barton CH, Biggs TE. A negative autoregulatory link between Nramp1 function and expression. J Leukoc Biol 2000;67:501-7.
46. Gerald D, Berra E, Frapart YM, et al. JunD reduces tumor angiogenesis by protecting cells from oxidative stress. Cell 2004;118:781-94.
47. Evans RM, Currie L, Campbell A. The distribution of ascorbic acid between various cellular components of blood in normal individuals and its relation to the plasma concentration. Br J Nutr 1982;47:473-82.
48. Ramaswamy G, Krishnamoorthy L. Serum carotene, vitamin A and vitamin C levels in breast cancer and cancer of the uterine cervix. Nutr Cancer 1996; 25:173-7.
49. Tarng DC, Wei YH, Huang TP, Kuo BI, Yang WC. Intravenous ascorbic acid as an adjuvant therapy for recombinant erythropoietin in haemodialysis patients with hyperferritinaemia. Kidney Int 1999;55:2477-86.