Hypoxia-induced neutrophil survival is mediated by HIF-1α-dependent NF-κB activity

Journal of Experimental Medicine

Volumn 201, Issue 1, 2005, Pages 105-115

  Walmsley, Sarah R ^a   Print, Cristin ^b   Farahi, Neda ^a   Peyssonnaux, Carole ^c   Johnson, Randall S ^c   Cramer, Thorsten ^c   Sobolewski, Anastasia ^a   Condliffe, Alison M ^a   Cowburn, Andrew S ^a   Johnson, Nicola ^b   Chilvers, Edwin R ^a  

^a UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^b UNIVERSITY OF CAMBRIDGE   (United Kingdom)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GLIOTOXIN; GLUCOSE; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 1BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; OLIGONUCLEOTIDE; OXYGEN; OXYGENASE; PARTHENOLIDE; REDUCING AGENT; TAQ POLYMERASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; APOPTOSIS; ARTICLE; BONE MARROW CELL; CELL CULTURE; CELL FUNCTION; CELL MIGRATION; CELL SURVIVAL; COMPETITIVE INHIBITION; CONTROLLED STUDY; DNA MICROARRAY; EFFECTOR CELL; ENZYME INHIBITION; HUMAN; HUMAN CELL; HYPOXIA; INFLAMMATION; INNATE IMMUNITY; LONGEVITY; MICROENVIRONMENT; MOUSE; NEUTROPHIL; NEUTROPHIL CHEMOTAXIS; NONHUMAN; OXYGEN TENSION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; REGULATORY MECHANISM; WESTERN BLOTTING;

ANIMALS; ANOXIA; APOPTOSIS; BLOTTING, WESTERN; CELL SURVIVAL; CYTOKINES; DNA PRIMERS; DNA-BINDING PROTEINS; ENZYME-LINKED IMMUNOSORBENT ASSAY; GLIOTOXIN; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MACROPHAGE INFLAMMATORY PROTEIN-1; MICE; MICE, KNOCKOUT; NEUTROPHILS; NF-KAPPA B P50 SUBUNIT; NUCLEAR PROTEINS; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; OLIGONUCLEOTIDES; POLYMERASE CHAIN REACTION; PROTEIN BINDING; REPRESSOR PROTEINS; SESQUITERPENES; TRANSCRIPTION FACTORS;

EID: 19944432390     PISSN: 00221007     EISSN: None     Source Type: Journal    
DOI: 10.1084/jem.20040624     Document Type: Article

References (52)

1. Nunn, J.F. 1993. Nunn's Applied Respiratory Physiology. Cambridge University Press, Cambridge, UK. 658 pp.
2. Ellis, G.A., S.E. Edmonds, K. Gaffney, R.B. Williams, and D. Blake. 1994. Synovial tissue oxygenation profile in inflamed and non-inflamed knee joints. Br. J. Rheumatol. 33:172.
3. Niinikoski, J., T.K. Hunt, and J. Englebert Dunphy. 1972. Oxygen supply in healing tissue. Ant. J. Surg. 123:247-252.
4. Levene, P.A., and G.M. Meyer. 1912. The action of leucocytes on glucose. J. Biol. Chem. 11:361-370.
5. Masson, N., C. William, P. Maxwell, C.W. Pugh, and P.J. Ratcliffe. 2001. Independent function of two destruction domains in hypoxia-inducible factor-α chains activated by prolyl hydroxylation. EMBO J. 20:5197-5206.
6. 2 sensing. Science. 292:464-468.
7. 2 regulated prolyl hydroxylation. Science. 292:468-472.
8. Yu, F., S.B. White, Q. Zhao, and F.S. Lee. 2001. Dynamic, site-specific interaction of hypoxia-inducible factor-1α with the von Hippel-Lindau tumour suppressor protein. Cancer Res. 61:4136-4142.
9. Mahon, P.C., K. Hirota, and G.L. Semenza. 2001. FIH-1: a novel protein that interacts with HIF-1α and VHL to mediate repression of HIF-1 transcriptional activity. Genes Dev. 15:2675-2686.
10. Lando, D., D.J. Peet, D.A. Whelan, J.J. Gorman, and M.L. Whitelaw. 2002. Asparagine hydroxylation of the HIF transactivation domain: a hypoxic switch. Science. 295:858-861.
11. Sang, N., J. Fang, V. Srinivas, I. Leshchinsky, and J. Caro. 2002. Carboxyl-terminal transactivation activity of hypoxia-inducible factor 1α is governed by a von Hippel-Lindau protein-independent, hydroxylation-regulated association with p300/CBP. Mol. Cell. Biol. 22:2984-2992.
12. 2 homeostasis by hypoxia-inducible factor 1. Annu. Rev. Cell Dev. Biol. 15:551-578.
13. Cormier-Regard, S., S.V. Nguyen, and W.C. Claycomb. 1998. Adrenomedullin gene expression is developmentally regulated and induced by hypoxia in rat ventricular cardiac myocytes. J. Biol. Chem. 273:17787-17792.
14. Metzen, E., U. Berchner-Pfannschmidt, P. Stengel, J.H. Marxsen, I. Stolze, M. Klinger, W.Q. Huang, C. Wotzlaw, T. Hellwig-Burgel, W. Jelkmann, et al. 2003. Intracellular localisation of human HIF-1 alpha hydroxylases: implications for oxygen sensing. J. Cell Sci. 116:1319-1326.
15. 2 regulated gene expression. FASEB J. 16:1151-1162.
16. Kotch, L.E., N.V. Iyer, E. Laughner, and G.L. Semenza. 1999. Defective vascularisation of HIF-1α-null embryos is not associated with VEGF deficiency but with mesenchymal cell death. Dev. Biol. 209:254-267.
17. 2 homeostasis by hypoxia-inducible factor 1α. Genes Dev. 12:149-162.
18. Cramer, T., Y. Yamanishi, B.E. Clausen, I. Forster, R. Pawlinski, N. Mackman, V.H. Haase, R. Jaenisch, M. Corr, V. Nizet, et al. 2003. HIF-1α is essential for myeloid cell-mediated inflammation. Cell. 112:645-657.
19. Haslett, C. 1992. Resolution of acute inflammation and the role of apoptosis in the tissue fate of granulocytes. Clin. Sci. 83:639-648.
20. Savill, J.S., A.H. Wyllie, J.E. Henson, M.J. Walport, P.M. Henson, and C. Haslett. 1989. Macrophage phagocytosis of ageing neutrophils in inflammation: programmed cell death in the neutrophil leads to recognition by macrophages. J. Clin. Invest. 83:865-875.
21. Brown, S., I. Heinisch, E. Ross, K. Shaw, C.D. Buckley, and J. Savill. 2002. Apoptosis disables CD31-mediated cell detachment from phagocytes promoting binding and engulfment. Nature. 418:200-203.
22. Cox, G., J. Gauldie, and M. Jordaria. 1992. Bronchial, epithelial cell-derived cytokines (G-CSF and GM-CSF) promote the survival of peripheral blood neutrophils in vitro. Am. J. Respir. Cell Mol. Biol. 7:507-513.
23. Ward, C., E.R. Chilvers, M.F. Lawson, J.G. Pryde, S. Fujihara, S.N. Farrow, C. Haslett, and A.G. Rossi. 1999. NF-κB activation is a critical regulator of human granulocyte apoptosis in vitro. J. Biol. Chem. 274:4309-4318.
24. Mecklenburgh, K.I., S.R. Walmsley, A.S. Cowburn, M. Wiesener, B.J. Reed, P.D. Upton, J. Deighton, A.P. Greening, and E.R. Chilvers. 2002. Involvement of a ferroprotein sensor in hypoxia-mediated inhibition of neutrophil apoptosis. Blood. 100:3008-3016.
25. Haslett, C., L.A. Guthrie, M.M. Kopamiak, R.B. Johnson, and P.M. Henson. 1985. Modulation of multiple neutrophil functions by preparative methods or trace concentrations of bacterial lipopolysaccharide. Am. J. Pathol. 119:101-110.
26. Klein, J.B., M.J. Rane, J.A. Scherzer, P.Y. Coxon, R. Kettritz, J.M. Mathiesen, A. Buridi, and K.R. McLeish. 2000. Granulocyte-macrophage colony-stimulating factor delays neutrophil constitutive apoptosis through phosphoinositide 3-kinase and extracellular signal-regulated kinase pathways. J. Immunol. 164:4286-4299.
27. Cowburn, A.S., K. Cadwallader, B. Reed, N. Farahi, and E.R. Chilvers. 2002. Role of PI3-kinase-dependent Bad phosphorylation and altered transcription in cytokine-mediated neutrophil survival. Blood. 100:2607-2616.
28. Hanson, E.S., M.L. Rawlins, and E.A. Leibold. 2003. Oxygen and iron regulation of iron regulatory protein 2. J. Biol. Chem. 278:40337-40342.
29. Mole, D.R., I. Schlemminger, L.A. McNeill, K.S. Hewitson, C.W. Pugh, P.J. RatclifFe, and C.J. Schofield. 2003. 2-oxoglutarate analogue inhibitors of HIF prolyl hydroxylase. Bioorg. Med. Chem. Lett. 13:2677-2680.
30. Villunger, A., C. Scott, P. Bouillet, and A. Strasser. 2003. Essential role for the BH3-only protein BIM but redundant roles for Bax, Bcl-2, and Bcl-w in the control of granulocyte survival. Blood. 101:2393-2400.
31. Evans, A.L., A.S. Sharkey, S.A. Saidi, C.G. Print, R.D. Catalano, S.K. Smith, and D.S. Charnock-Jones. 2003. Generation and use of a tailored gene array to investigate vascular biology. Angiogenesis. 6:93-104.
32. Graven, K.K., R.F. Troxler, H. Kornfield, M.V. Panchenko, and H.W. Farber. 1994. Regulation of endothelial cell glyceraldehydes-3-phosphate dehydrogenase expression by hypoxia. J. Biol. Chem. 269:24446-24453.
33. Graven, K.K., Q. Yu, D. Pan, J.S. Roncarati, and H.W. Farber. 1999. Identification of an oxygen responsive enhancer element in the glycer-aldehydes-3-phosphate dehydrogenase gene. Biochim. Biophys. Acta. 1447:208-218.
34. Lu, S., X. Gu, S. Hoestje, and D.E. Epner. 2002. Identification of an additional hypoxia responsive element in glyceraldehydes-3-phosphate dehydrogenase gene promoter. Biochim. Biophys. Acta. 1574:152-156.
35. Walmsley, S.R., A.S. Cowburn, A. Sobolewski, J. Murray, N. Farahi, I. Sabroe, and E.R. Chilvers. 2004. Characterisation of the survival effect of tumour necrosis factor-α in human neutrophils. Biodiem. Soc. Trans. 32:456-460.
36. Leek, R.D., K.L. Talks, F. Pezzella, H. Turley, L. Campo, N.S. Brown, R. Bicknell, M. Taylor, K.C. Gatter, and A.L. Harris. 2002. Relation of hypoxia-inducible factor-2 alpha (HIF-2 alpha) expression in tumour-infiltrative macrophages to tumour angiogenesis and the oxidative thymidine phosphorylase pathway in human breast cancer. Cancer Res. 62:1326-1329.
37. Talks, K.L., H. Turley, K.C. Gatter, P.H. Maxwell, C.W. Pugh, P.J. Ratcliffe, and A.L. Harris. 2000. The expression and distribution of the hypoxia-inducible factors HIF-1α and HIF-2α in normal human tissues, cancers, and tumour-associated macrophages. Am. J. Pathol. 157:411-421.
38. Rosenbaum, D.M., M. Michaelson, D.K. Batter, P. Doshi, and J.A. Kessler. 1994. Evidence for hypoxia-mduced, programmed cell death of cultured neurons. Ann. Neurol. 36:864-870.
39. Graeber, T.G., C. Osmanian, T. Jacks, D.E. Housman, C.J. Koch, S.W. Lowe, and A.J. Giaccia. 1996. Hypoxia-mediated selection of cells with diminished apoptotic potential in solid tumours. Nature. 379:88-91.
40. Borregaard, N., and T. Herlin. 1982. Energy metabolism of human neutrophils during phagocytosis. J. Clin. Invest. 70:550-557.
41. Chandel, N.S., W.C. Trzyna, D.S. McClintock, and P.T. Schumacker. 2000. Role of oxidants in NF-κB activation and TNF-α gene transcription induced by hypoxia and endotoxin. J. Immunol. 165:1013-1021.
42. Lukiw, W.J., A. Ottlecz, G. Lambrou, M. Grueninger, J. Finley, H.W. Thompson, and N.G. Bazan. 2003. Coordinate activation of HIF-1 and NF-κB DNA binding and COX-2 and VEGF expression in retinal cells by hypoxia. Invest. Ophthalmol. Vis. Sci. 44:4163-4170.
43. Digicaylioglu, M., and S.A. Lipton. 2001. Eythropoietin-mediated neuroprotection involves cross-talk between Jak2 and NF-κB signalling cascades. Nature. 412:641-647.
44. Zhou, J., T. Schmid, and B. Brune. 2003. Tumour necrosis factor-α causes accumulation of a ubiquitinated form of hypoxia inducible factor-1α through a nuclear factor-κB-dependent pathway. Mol. Biol. Cell. 14:2216-2225.
45. Yamamoto, Y., U.N. Verma, S. Prajapati, Y.-T. Kwak, and R.B. Gaynor. 2003. Histone H3 phosphorylation by IKK-α is critical for cytokine-induced gene expression. Nature. 423:655-659.
46. Vancurova, I., V. Miskolci, and D. Davidson. 2001. NF-κB activation in tumour necrosis factor α-stimulated neutrophils is mediated by protein kinase Cδ. J. Biol. Chem. 276:19746-19752.
47. Choi, M., S. Rolle, M. Wellner, M.C. Cardoso, C. Scheidereit, F.C. Luft, and R. Kettritz. 2003. Inhibition of NF-κB by a TAT-NEMO-binding domain peptide accelerates constitutive apoptosis and abrogates LPS-delayed neutrophil apoptosis. Blood. 102:2259-2267.
48. Castro-Alcaraz, S., V. Miskolci, B. Kalasapudi, D. Davidson, and I. Vancurova. 2002. NF-κB regulation in human neutrophils by nuclear IκBα: correlation to apoptosis. J. Immunol. 169:3947-3953.
49. Suttmann, H., N. Lehan, A. Bohle, and S. Brandau. 2003. Stimulation of neutrophil granulocytes with Mycobacterium bovis bacillus Calmette-Guerin induces changes in phenotype and gene expression and inhibits spontaneous apoptosis. Infect. Immun. 71:4647-4656.
50. VanOtteren, G.M., T.J. Standiford, S.L. Kunkel, J.M. Danforth, and R. Streiter. 1995. Alterations of ambient oxygen tension modulate the expression of tumour necrosis factor and macrophage inflammatory protein alpha from murine alveolar macrophages. Am. J. Respir. Cell Mol. Biol. 13:399-409.
51. Baumann, R., C. Casaulta, S. Dagmar, S. Conus, S. Yousefi, and S. Hans-Uwe. 2003. Macrophage migration inhibitory factor delays apoptosis in neutrophils by inhibiting the mitochondria-dependent death pathway. FASEB J. 17:2221-2230.
52. Bacher, M., J. Schrader, N. Thompson, K. Kuschela, D. Gemsa, G. Weaber, and J. Schlegel. 2003. Up regulation of macrophage migration inhibitory factor gene and protein expression in glial tumour cells during hypoxic and hypoglycaemic stress indicates a critical role for angiogenesis in glioglastoma multiforme. Am. J. Pathol. 162:11-17.