Differential activation and antagonistic function of HIF-α isoforms in macrophages are essential for NO homeostasis

Genes and Development

Volumn 24, Issue 5, 2010, Pages 491-501

  Takeda, Norihiko ^a   O'Dea, Ellen L ^a   Doedens, Andrew ^a   Kim, Jung Whan ^a   Weidemann, Alexander ^a   Stockmann, Christian ^a   Asagiri, Masataka ^a   Simon, M Celeste ^b   Hoffmann, Alexander ^a   Johnson, Randall S ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

Arginase; HIF; Hypoxia; Macrophage polarization; Nitric oxide

Indexed keywords

ARGINASE 1; CINTREDEKIN BESUDOTOX; ENDOTOXIN; GAMMA INTERFERON; HYPOXIA INDUCIBLE FACTOR 1ALPHA; HYPOXIA INDUCIBLE FACTOR 2ALPHA; INDUCIBLE NITRIC OXIDE SYNTHASE; INTERLEUKIN 4; NITRIC OXIDE;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; COMPUTER MODEL; CONTROLLED STUDY; ENZYME ACTIVATION; GENE EXPRESSION; HOMEOSTASIS; MACROPHAGE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN PROCESSING; PROTEIN SYNTHESIS; TH1 CELL;

ANIMALS; ARGINASE; BASIC HELIX-LOOP-HELIX TRANSCRIPTION FACTORS; COMPUTER SIMULATION; CYTOKINES; GENE EXPRESSION REGULATION; HOMEOSTASIS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; MACROPHAGES; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MODELS, BIOLOGICAL; NITRIC OXIDE SYNTHASE TYPE II; NITROUS OXIDE; PROTEIN ISOFORMS; TH1 CELLS; TH2 CELLS;

EID: 77649177217     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.1881410     Document Type: Article

References (61)

1. Albina JE, Mills CD, Henry WL Jr, Caldwell MD. 1990. Temporal expression of different pathways of 1-arginine metabolism in healing wounds. J Immunol 144: 3877-3880.
2. Bansal V, Ochoa JB. 2003. Arginine availability, arginase, and the immune response. Curr Opin Clin Nutr Metab Care 6: 223-228.
3. Benoit M, Desnues B, Mege JL. 2008. Macrophage polarization in bacterial infections. J Immunol 181: 3733-3739.
4. Bermudez LE, Young LS. 1988. Tumor necrosis factor, alone or in combination with IL-2, but not IFN-γ, is associated with macrophage killing of Mycobacterium avium complex. J Immunol 140: 3006-3013.
5. Bertout JA, Majmundar AJ, Gordan JD, Lam JC, Ditsworth D, Keith B, Brown EJ, Nathanson KL, Simon MC. 2009. HIF2α inhibition promotes p53 pathway activity, tumor cell death, and radiation responses. Proc Natl Acad Sci 106: 14391-14396.
6. Bonecini-Almeida MG, Chitale S, Boutsikakis I, Geng J, Doo H, He S, Ho JL. 1998. Induction of in vitro human macrophage anti-Mycobacterium tuberculosis activity: Requirement for IFN-g and primed lymphocytes. J Immunol 160: 4490-4499.
7. Bronte V, Zanovello P. 2005. Regulation of immune responses by L-arginine metabolism. Nat Rev Immunol 5: 641-654.
8. Bronte V, Serafini P, Mazzoni A, Segal DM, Zanovello P. 2003. L-arginine metabolism in myeloid cells controls T-lymphocyte functions. Trends Immunol 24: 302-306.
9. Chatila TA. 2004. Interleukin-4 receptor signaling pathways in asthma pathogenesis. Trends Mol Med 10: 493-499.
10. Clausen BE, Burkhardt C, ReithW, Renkawitz R, Forster I. 1999. Conditional gene targeting in macrophages and granulocytes using LysMcre mice. Transgenic Res 8: 265-277.
11. Covello KL, Kehler J, Yu H, Gordan JD, Arsham AM, Hu CJ, Labosky PA, Simon MC, Keith B. 2006. HIF-2α regulates Oct-4: Effects of hypoxia on stem cell function, embryonic development, and tumor growth. Genes & Dev 20: 557-570.
12. Cramer T, Yamanishi Y, Clausen BE, Forster I, Pawlinski R, Mackman N, Haase VH, Jaenisch R, Corr M, Nizet V, et al. 2003. HIF-1α is essential for myeloid cell-mediated inflammation. Cell 112: 645-657.
13. Dickensheets HL, Venkataraman C, Schindler U, Donnelly RP. 1999. Interferons inhibit activation of STAT6 by interleukin 4 in human monocytes by inducing SOCS-1 gene expression. Proc Natl Acad Sci 96: 10800-10805.
14. Durante W, Johnson FK, Johnson RA. 2007. Arginase: A critical regulator of nitric oxide synthesis and vascular function. Clin Exp Pharmacol Physiol 34: 906-911.
15. El Kasmi KC, Qualls JE, Pesce JT, Smith AM, Thompson RW, Henao-Tamayo M, Basaraba RJ, Konig T, Schleicher U, Koo MS, et al. 2008. Toll-like receptor-induced arginase 1 in macrophages thwarts effective immunity against intracellular pathogens. Nat Immunol 9: 1399-1406.
16. Frede S, Stockmann C, Freitag P, Fandrey J. 2006. Bacterial lipopolysaccharide induces HIF-1 activation in human monocytes via p44/42 MAPK and NF-κB. Biochem J 396: 517-527.
17. Frede S, Berchner-Pfannschmidt U, Fandrey J. 2007. Regulation of hypoxia-inducible factors during inflammation. Methods Enzymol 435: 405-419.
18. Gordan JD, Thompson CB, Simon MC. 2007. HIF and c-Myc: Sibling rivals for control of cancer cell metabolism and proliferation. Cancer Cell 12: 108-113.
19. Gordon S. 2003. Alternative activation of macrophages. Nat Rev Immunol 3: 23-35.
20. Gruber M, Hu CJ, Johnson RS, Brown EJ, Keith B, Simon MC. 2007. Acute postnatal ablation of Hif-2a results in anemia. Proc Natl Acad Sci 104: 2301-2306.
21. Haase VH, Glickman JN, Socolovsky M, Jaenisch R. 2001. Vascular tumors in livers with targeted inactivation of the von Hippel-Lindau tumor suppressor. Proc Natl Acad Sci 98: 1583-1588.
22. Hoffmann A, Levchenko A, Scott ML, Baltimore D. 2002. The IκB-NF-κB signaling module: Temporal control and selective gene activation. Science 298: 1241-1245.
23. Holmquist-Mengelbier L, Fredlund E, Lofstedt T, Noguera R, Navarro S, Nilsson H, Pietras A, Vallon-Christersson J, Borg A, Gradin K, et al. 2006. Recruitment of HIF-1α and HIF-2α to common target genes is differentially regulated in neuroblastoma: HIF-2α promotes an aggressive phenotype. Cancer Cell 10: 413-423.
24. Hopper KE. 1986. Kinetics of macrophage recruitment and turnover in peritoneal inflammatory exudates induced by Salmonella or thioglycollate broth. J Leukoc Biol 39: 435-446.
25. Jurgensen JS, Rosenberger C, Wiesener MS, Warnecke C, Horstrup JH, Grafe M, Philipp S, Griethe W, Maxwell PH, Frei U, et al. 2004. Persistent induction of HIF-1α and -2α in cardiomyocytes and stromal cells of ischemic myocardium. FASEB J 18: 1415-1417.
26. Kamada Y, Nagaretani H, Tamura S, Ohama T, Maruyama T, Hiraoka H, Yamashita S, Yamada A, Kiso S, Inui Y, et al. 2001. Vascular endothelial dysfunction resulting from L-arginine deficiency in a patient with lysinuric protein intolerance. J Clin Invest 108: 717-724.
27. Kisanuki YY, Hammer RE, Miyazaki J, Williams SC, Richardson JA, Yanagisawa M. 2001. Tie2-Cre transgenic mice: A new model for endothelial cell-lineage analysis in vivo. Dev Biol 230: 230-242.
28. Kong X, Alvarez-Castelao B, Lin Z, Castano JG, Caro J. 2007. Constitutive/hypoxic degradation of HIF-α proteins by the proteasome is independent of von Hippel Lindau protein ubiquitylation and the transactivation activity of the protein. J Biol Chem 282: 15498-15505.
29. Krieg M, Haas R, Brauch H, Acker T, Flamme I, Plate KH. 2000. Up-regulation of hypoxia-inducible factors HIF-1α and HIF-2α under normoxic conditions in renal carcinoma cells by von Hippel-Lindau tumor suppressor gene loss of function. Oncogene 19: 5435-5443.
30. Losman JA, Chen XP, Hilton D, Rothman P. 1999. Cutting edge: SOCS-1 is a potent inhibitor of IL-4 signal transduction. J Immunol 162: 3770-3774.
31. Louis CA, Reichner JS, Henry WL Jr, Mastrofrancesco B, Gotoh T, Mori M, Albina JE. 1998. Distinct arginase isoforms expressed in primary and transformed macrophages: Regulation by oxygen tension. Am J Physiol 274: R775-R782.
32. MacNaul KL, Hutchinson NI. 1993. Differential expression of iNOS and cNOS mRNA in human vascular smooth muscle cells and endothelial cells under normal and inflammatory conditions. Biochem Biophys Res Commun 196: 1330-1334.
33. Mantovani A, Sozzani S, Locati M, Allavena P, Sica A. 2002. Macrophage polarization: Tumor-associated macrophages as a paradigm for polarized M2 mononuclear phagocytes. Trends Immunol 23: 549-555.
34. Mantovani A, Sica A, Sozzani S, Allavena P, Vecchi A, Locati M. 2004. The chemokine system in diverse forms of macrophage activation and polarization. Trends Immunol 25: 677-686.
35. Martinez FO, Helming L, Gordon S. 2009. Alternative activation of macrophages: An immunologic functional perspective. Annu Rev Immunol 27: 451-483.
36. Maxwell PH, Wiesener MS, Chang GW, Clifford SC, Vaux EC, Cockman ME, Wykoff CC, Pugh CW, Maher ER, Ratcliffe PJ. 1999. The tumour suppressor protein VHL targets hypoxiainducible factors for oxygen-dependent proteolysis. Nature 399: 271-275.
37. Melillo G, Musso T, Sica A, Taylor LS, Cox GW, Varesio L. 1995. A hypoxia-responsive element mediates a novel pathway of activation of the inducible nitric oxide synthase promoter. J Exp Med 182: 1683-1693.
38. Michl J, Pieczonka MM, Unkeless JC, Silverstein SC. 1979. Effects of immobilized immune complexes on Fc- and complement-receptor function in resident and thioglycollateelicited mouse peritoneal macrophages. J Exp Med 150: 607-621.
39. Mosser DM, Edwards JP. 2008. Exploring the full spectrum of macrophage activation. Nat Rev Immunol 8: 958-969.
40. Murdoch C, Muthana M, Lewis CE. 2005. Hypoxia regulates macrophage functions in inflammation. J Immunol 175: 6257-6263.
41. Nathan CF, Murray HW, Wiebe ME, Rubin BY. 1983. Identification of interferon-g as the lymphokine that activates human macrophage oxidative metabolism and antimicrobial activity. J Exp Med 158: 670-689.
42. Nizet V, Johnson RS. 2009. Interdependence of hypoxic and innate immune responses. Nat Rev Immunol 9: 609-617.
43. Norton JM, Munck A. 1980. Glucose transport in murine macrophages: In vitro characterization of the monosaccharide transport system of the thioglycollate-elicited mouse peritoneal macrophage. J Immunol 125: 252-258.
44. Odegaard JI, Ricardo-Gonzalez RR, Goforth MH, Morel CR, Subramanian V, Mukundan L, Red Eagle A, Vats D, Brombacher F, Ferrante AW, et al. 2007. Macrophage-specific PPARg controls alternative activation and improves insulin resistance. Nature 447: 1116-1120.
45. Peyssonnaux C, Datta V, Cramer T, Doedens A, Theodorakis EA, Gallo RL, Hurtado-Ziola N, Nizet V, Johnson RS. 2005. HIF-1α expression regulates the bactericidal capacity of phagocytes. J Clin Invest 115: 1806-1815.
46. Rankin EB, Biju MP, Liu Q, Unger TL, Rha J, Johnson RS, Simon MC, Keith B, Haase VH. 2007. Hypoxia-inducible factor-2 (HIF-2) regulates hepatic erythropoietin in vivo. J Clin Invest 117: 1068-1077.
47. Rius J, Guma M, Schachtrup C, Akassoglou K, Zinkernagel AS, Nizet V, Johnson RS, Haddad GG, Karin M. 2008. NF-κB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1α. Nature 453: 807-811.
48. Ryan HE, Lo J, Johnson RS. 1998. HIF-1α is required for solid tumor formation and embryonic vascularization. EMBO J 17: 3005-3015.
49. Sandau KB, Fandrey J, Brune B. 2001. Accumulation of HIF-1α under the influence of nitric oxide. Blood 97: 1009-1015.
50. Stein M, Keshav S, Harris N, Gordon S. 1992. Interleukin 4 potently enhances murine macrophage mannose receptor activity: A marker of alternative immunologic macrophage activation. J Exp Med 176: 287-292.
51. Suh H, Peresleni T, Wadhwa N, McNurlan M, Garlick P, Goligorsky MS. 1997. Amino acid profile and nitric oxide pathway in patients on continuous ambulatory peritoneal dialysis: L-arginine depletion in acute peritonitis. Am J Kidney Dis 29: 712-719.
52. Summersgill JT, Powell LA, Buster BL, Miller RD, Ramirez JA. 1992. Killing of Legionella pneumophila by nitric oxide in γ-interferon- activated macrophages. J Leukoc Biol 52: 625-629.
53. Takeda N, Maemura K, Horie S, Oishi K, Imai Y, Harada T, Saito T, Shiga T, Amiya E, Manabe I, et al. 2007. Thrombomodulin is a clock-controlled gene in vascular endothelial cells. J Biol Chem 282: 32561-32567.
54. Talks KL, Turley H, Gatter KC, Maxwell PH, Pugh CW, Ratcliffe PJ, Harris AL. 2000. 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 157: 411-421.
55. Tian H, McKnight SL, Russell DW. 1997. Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes & Dev 11: 72-82.
56. van Uden P, Kenneth NS, Rocha S. 2008. Regulation of hypoxiainducible factor-1α by NF-κB. Biochem J 412: 477-484.
57. Wang GL, Semenza GL. 1993. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. Proc Natl Acad Sci 90: 4304-4308.
58. Weidemann A, Johnson RS. 2008. Biology of HIF-1α. Cell Death Differ 15: 621-627.
59. Werner SL, Barken D, Hoffmann A. 2005. Stimulus specificity of gene expression programs determined by temporal control of IKK activity. Science 309: 1857-1861.
60. Wu G, Morris SM Jr. 1998. Arginine metabolism: Nitric oxide and beyond. Biochem J 336: 1-17.
61. Zhou J, Fandrey J, Schumann J, Tiegs G, Brune B. 2003. NO and TNF-α released from activated macrophages stabilize HIF-1α in resting tubular LLC-PK1 cells. Am J Physiol Cell Physiol 284: C439-C446. doi: 10.1152/ajpcell.00294.2002.