Interdependence of hypoxic and innate immune responses

Nature Reviews Immunology

Volumn 9, Issue 9, 2009, Pages 609-617

  Nizet, Victor ^a,b   Johnson, Randall S ^a,c  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CATHELICIDIN; CRE RECOMBINASE; HYPOXIA INDUCIBLE FACTOR; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; NATURAL RESISTANCE ASSOCIATED MACROPHAGE PROTEIN 1; SIDEROPHORE; TOLL LIKE RECEPTOR; UBIQUITIN PROTEIN LIGASE; HYPOXIA INDUCIBLE FACTOR 1; INTEGRIN; PROCOLLAGEN PROLINE 2 OXOGLUTARATE 4 DIOXYGENASE;

BACTERICIDAL ACTIVITY; BACTERIUM; BONE MARROW CELL; DENDRITIC CELL; DRUG TARGETING; EPITHELIUM CELL; GENE EXPRESSION; HOST PATHOGEN INTERACTION; HUMAN; HUMAN PAPILLOMAVIRUS TYPE 16; HYPOXIA; INFECTION; INFECTION SENSITIVITY; INFLAMMATION; INNATE IMMUNITY; ISCHEMIA; MACROPHAGE; MAST CELL; MICROENVIRONMENT; NEUTROPHIL; NONHUMAN; PARASITE; PATHOGENESIS; PHAGOCYTE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; RECEPTOR UPREGULATION; REPERFUSION INJURY; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; REVIEW; SEPSIS; TISSUE INJURY; VESICULAR STOMATITIS VIRUS; VIRUS; ANIMAL; CELL HYPOXIA; IMMUNOLOGY; METABOLISM;

ANIMALS; CELL HYPOXIA; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1; IMMUNITY, INNATE; INFECTION; INFLAMMATION; INTEGRINS; MYELOID CELLS; NF-KAPPA B; PROCOLLAGEN-PROLINE DIOXYGENASE; SEPSIS;

EID: 70249099576     PISSN: 14741733     EISSN: None     Source Type: Journal    
DOI: 10.1038/nri2607     Document Type: Review

References (88)

1. Saadi, S., Wrenshall, L. E. & Platt, J. L. Regional manifestations and control of the immune system. FASEB J. 16, 849-856 (2002).
2. Schor, H., Vaday, G. G. & Lider, O. Modulation of leukocyte behavior by an inflamed extracellular matrix. Dev. Immunol. 7, 227-238 (2000).
3. Vogelberg, K. H. & Konig, M. Hypoxia of diabetic feet with abnormal arterial blood flow. Clin. Invest. 71, 466-470 (1993).
4. Arnold, F. , West, D. & Kumar, s. Wound healing: the effect of macrophage and tumour derived angiogenesis factors on skin graft vascularization. Br. J. Exp. Pathol. 68, 569-574 (1987).
5. Negus, R. P. , stamp, G. W., Hadley, J. & Balkwill, F. R. Quantitative assessment of the leukocyte infiltrate in ovarian cancer and its relationship to the expression of C-C chemokines. Am. J. Pathol. 150, 1723-1734 (1997).
6. Semenza, G. L. & Wang, G. L. A nuclear factor induced by hypoxia via de novo protein synthesis binds to the human erythropoietin gene enhancer at a site required for transcriptional activation. Mol. Cell. Biol. 12, 5447-5454 (1992).
7. Wang, G. L., Jiang, B. H., Rue, E. A. & semenza, G. L. Hypoxia-inducible factor 1 is a basic-helix-loop- helix-PAs heterodimer regulated by cellular O2 tension. Proc. Natl Acad. Sci. USA 92, 5510-5514 (1995).
8. Weidemann, A. & Johnson, R. s. Biology of HIF-1α. Cell Death Differ. 15, 621-627 (2008).
9. Maxwell, P. H. The HIF pathway in cancer. Semin. Cell Dev. Biol. 16, 523-530 (2005).
10. Bruick, R. K. & McKnight, s. L. A conserved family of prolyl-4-hydroxylases that modify HIF. Science 294, 1337-1340 (2001).
11. Jaakkola, P. et al. Targeting of HIF-1α to the von Hippel-Lindau ubiquitylation complex by O2-regulated prolyl hydroxylation. Science 292, 468-472 (2001).
12. Lando, D. et al. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 16, 1466-1471 (2002).
13. Peet, D. & Linke, s. Regulation of HIF: asparaginyl hydroxylation. Novartis Found. Symp. 272, 37-49 (2006).
14. Fukuda, R. et al. HIF-1 regulates cytochrome oxidase subunits to optimize efficiency of respiration in hypoxic cells. Cell 129, 111-122 (2007).
15. Semenza, G. L., Roth, P. H., Fang, H. M. & Wang, G. L. Transcriptional regulation of genes encoding glycolytic enzymes by hypoxia-inducible factor 1. J. Biol. Chem. 269, 23757-23763 (1994).
16. Shimoda, L. A., Fallon, M., Pisarcik, s., Wang, J. & semenza, G. L. HIF-1 regulates hypoxic induction of NHE1 expression and alkalinization of intracellular pH in pulmonary arterial myocytes. Am. J. Physiol. Lung Cell. Mol. Physiol. 291, L941-L949 (2006).
17. Iyer, N. V. et al. Cellular and developmental control of O2 homeostasis by hypoxia-inducible factor 1α. Genes Dev. 12, 149-162 (1998).
18. Ryan, H. E., Lo, J. & Johnson, R. s. HIF-1α is required for solid tumor formation and embryonic vascularization. EMBo J. 17, 3005-3015 (1998).
19. Kotch, L. E., Iyer, N. V., Laughner, E. & semenza, G. L. Defective vascularization of HIF-1α-null embryos is not associated with VEGF deficiency but with mesenchymal cell death. Dev. Biol. 209, 254-267 (1999).
20. Cramer, T. et al. HIF-1α is essential for myeloid cell- mediated inflammation. Cell 11 2 , 645-657 (2003). Myeloid-specific gene targeting identifies an essential role for HIF1α in regulating the inflammatory functions of neutrophils and macrophages.
21. Hollander, A. P., Corke, K. P., Freemont, A. J. & Lewis, C. E. Expression of hypoxia-inducible factor 1α by macrophages in the rheumatoid synovium: implications for targeting of therapeutic genes to the inflamed joint. Arthritis Rheum. 44, 1540-1544 (2001).
22. Westra, J. et al. Regulation of cytokine-induced HIF-1α expression in rheumatoid synovial fibroblasts. Ann. NY Acad. Sci. 11 0 8 , 340-348 (2007).
23. Konttinen, Y. T. et al. Disease-associated increased HIF-1, αvβ3 integrin, and Flt-1 do not suffice to compensate the damage-inducing loss of blood vessels in inflammatory myopathies. Rheumatol. Int. 24, 333-339 (2004).
24. Clancy, R. M. et al. Role of hypoxia and cAMP in the transdifferentiation of human fetal cardiac fibroblasts: implications for progression to scarring in autoimmune-associated congenital heart block. Arthritis Rheum. 56, 4120-4131 (2007).
25. Vink, A. et al. HIF-1a expression is associated with an atheromatous inflammatory plaque phenotype and upregulated in activated macrophages. Atherosclerosis 195, e69-e75 (2007).
26. Peyssonnaux, C. et al. HIF-1 a expression regulates the bactericidal capacity of phagocytes. J. Clin. Invest. 115, 1806-1815 (2005).
27. Kong, T., Eltzschig, H. K., Karhausen, J., Colgan, s. P. & shelley, C. s. Leukocyte adhesion during hypoxia is mediated by HIF-1-dependent induction of (32 integrin gene expression. Proc. Natl Acad. Sci. USA 101, 10440-10445 (2004).
28. Walmsley, s. R. et al. Hypoxia-induced neutrophil survival is mediated by HIF-1a-dependent NF-KB activity. J. Exp. Med 201, 105-115 (2005).
29. Walmsley, s. R. et al. Neutrophils from patients with heterozygous germline mutations in the von Hippel Lindau protein (pVHL) display delayed apoptosis and enhanced bacterial phagocytosis. Blood 108, 3176-3178 (2006).
30. Oda, T. et al. Activation of hypoxia-inducible factor 1 during macrophage differentiation. Am. J. Physiol. Cell Physiol. 291, C1 04-C113 (2006).
31. Anand, R. J. et al. Hypoxia causes an increase in phagocytosis by macrophages in a HIF-1 a -dependent manner. J. Leukoc. Biol. 82, 1257-1265 (2007).
32. Kuhlicke, J., Frick, J. s., Morote-Garcia, J. C, Rosenberger, P. & Eltzschig, H. K. Hypoxia inducible factor (HIF)-1 coordinates induction of Toll-like receptors TLR2 and TLR6 during hypoxia. PLoS oNE 2, e1364 (2007).
33. Jantsch, J. et al. Hypoxia and hypoxia-inducible factor-1a modulate lipopolysaccharide-induced dendritic cell activation and function. J. Immunol. 180, 4697-4705 (2008).
34. Hacker, H. & Karin, M. Regulation and function of IKK and IKK-related kinases. Sci. STKE re13 (2006).
35. Peyssonnaux, C. et al. Cutting edge: essential role of hypoxia inducible factor-1 a in development of lipopolysaccharide-induced sepsis. J. Immunol. 178, 7516-7519 (2007).
36. Cummins, E. P. et al. Prolyl hydroxylase-1 negatively regulates IKB kinase-p, giving insight into hypoxia- induced NFKB activity. Proc. Natl Acad. Sci. USA 103, 18154-18159 (2006)
37. Frede, s., stockmann, C, Freitag, P. & Fandrey, J. Bacterial lipopolysaccharide induces HIF-1 activation in human monocytes via p44/42 MAPK and NF-KB. Biochem. J. 396, 517-527 (2006).
38. Belaiba, R. s. et al. Hypoxia up-regulates hypoxia- inducible factor-1 a transcription by involving phosphatidylinositol 3-kinase and nuclear factor KB in pulmonary artery smooth muscle cells. Mol. Biol. Cell 18, 4691-4697 (2007).
39. Rius, J. et al. NF-KB links innate immunity to the hypoxic response through transcriptional regulation of HIF- 1a. Nature 453, 807-811 (2008)
40. NF-KB is shown to be essential for HIF1a upregulation at the mRNA level in response to hypoxia or infection.
41. Fang, H. Y. et al. Hypoxia inducible factors 1 and 2 are important transcriptional effectors in primary macrophages experiencing hypoxia. Blood 114, 844-859 (2009).
42. Mi, Z. et al. synergystic induction of HIF-1 a transcriptional activity by hypoxia and lipopolysaccharide in macrophages. Cell Cycle 7, 232-241 (2008).
43. Goodarzi, H., Trowbridge, J. & Gallo, R. L. Innate immunity: a cutaneous perspective. Clin. Rev. Allergy Immunol. 33, 15-26 (2007).
44. Braff, M. H., Zaiou, M., Fierer, J., Nizet, V. & Gallo, R. L Keratinocyte production of cathelicidin provides direct activity against bacterial skin pathogens. Infect. Immun. 73, 6771-6781 (2005).
45. Peyssonnaux, C. et al. Critical role of HIF-1a in keratinocyte defense against bacterial infection. J. Invest. Dermatol. 128, 1964-1968 (2008).
46. Koury, J. et al. Persistent HIF-1 a activation in gut ischemia/reperfusion injury: potential role of bacteria and lipopolysaccharide. Shock 22, 270-277 (2004).
47. Shah, Y. M. et al. Hypoxia-inducible factor augments experimental colitis through an MIF-dependent inflammatory signaling cascade. Gastroenterology 134, 2036-2048 (2008).
48. Karhausen, J. et al. Epithelial hypoxia-inducible factor-1 is protective in murine experimental colitis. J. Clin. Invest. 11 4 , 1098-1106 (2004).
49. Robinson, A. et al. Mucosal protection by hypoxia- inducible factor prolyl hydroxylase inhibition. Gastroenterology 134, 145-155 (2008).
50. Cummins, E. P. et al. The hydroxylase inhibitor dimethyloxalylglycine is protective in a murine model of colitis. Gastroenterology 134, 156-165 (2008).
51. Rao, K. N. & Brown, M. A. Mast cells: multifaceted immune cells with diverse roles in health and disease. Ann. NY Acad. Sci. 1143, 83-104 (2008).
52. Jeong, H. J. et al. Expression of proinflammatory cytokines via HIF-1α and NF-κB activation on desferrioxamine-stimulated HMC-1 cells. Biochem. Biophys. Res. Commun. 306, 805-811 (2003).
53. Lee, K. s. et al. Mast cells can mediate vascular permeability through regulation of the PI3K-HIF-1α- VEGF axis. Am. J. Respir. Crit. Care Med. 178, 787-797 (2008).
54. Jeong, H. J. et al. Activation of hypoxia-inducible factor-1 regulates human histidine decarboxylase expression. Cell. Mol. Life Sci. 66, 1309-1319 (2009).
55. Lukashev, D. et al. Cutting edge: hypoxia-inducible factor 1α and its activation-inducible short isoform I.1 negatively regulate functions of CD4+ and CD8+ T lymphocytes. J. Immunol. 177, 4962-4965 (2006).
56. Thiel, M. et al. Targeted deletion of HIF-1α gene in T cells prevents their inhibition in hypoxic inflamed tissues and improves septic mice survival. PLoS oNE 2, e853 (2007).
57. Lukashev, D. & sitkovsky, M. Preferential expression of the novel alternative isoform I.3 of hypoxia- inducible factor 1α in activated human T lymphocytes. Hum. Immunol. 69, 421-425 (2008).
58. Biju, M. P. et al. Vhlh gene deletion induces HIF-1-mediated cell death in thymocytes. Mol. Cell. Biol. 24, 9038-9047 (2004).
59. Kilani, M. M., Mohammed, K. A., Nasreen, N., Tepper, R. s. & Antony, V. B. RsV causes HIF-1α stabilization via NO release in primary bronchial epithelial cells. Inflammation 28, 245-251 (2004).
60. Hwang, II, Watson, I. R., Der, s. D. & Ohh, M. Loss of VHL confers hypoxia-inducible factor (HIF)-dependent resistance to vesicular stomatitis virus: role of HIF in antiviral response. J. Virol. 80, 10712-10723 (2006).
61. Yoo, Y. G. et al. Hepatitis B virus X protein enhances transcriptional activity of hypoxia-inducible factor-1α through activation of mitogen-activated protein kinase pathway. J. Biol. Chem. 278, 39076-39084 (2003).
62. Moon, E. J. et al. Hepatitis B virus X protein induces angiogenesis by stabilizing hypoxia-inducible factor-1α. FASEB J. 18, 382-384 (2004).
63. Nasimuzzaman, M., Waris, G., Mikolon, D., stupack, D. G. & siddiqui, A. Hepatitis C virus stabilizes hypoxia-inducible factor 1α and stimulates the synthesis of vascular endothelial growth factor. J. Virol. 81, 10249-10257 (2007).
64. Tang, X. et al. Overexpression of human papillomavirus type 16 oncoproteins enhances hypoxia-inducible factor 1α protein accumulation and vascular endothelial growth factor expression in human cervical carcinoma cells. Clin. Cancer Res. 13, 2568-2576 (2007).
65. Lu, Z. H., Wright, J. D., Belt, B., Cardiff, R. D. & Arbeit, J. M. Hypoxia-inducible factor-1 facilitates cervical cancer progression in human papillomavirus type 16 transgenic mice. Am. J. Pathol. 171, 667-681 (2007).
66. Birner, P. et al. Overexpression of hypoxia-inducible factor 1α is a marker for an unfavorable prognosis in early-stage invasive cervical cancer. Cancer Res. 60, 4693-4696 (2000).
67. Tomita, M. et al. Activation of hypoxia-inducible factor 1 in human T-cell leukaemia virus type 1-infected cell lines and primary adult T-cell leukaemia cells. Biochem. J. 406, 317-323 (2007).
68. Wakisaka, N. et al. Epstein-Barr virus latent membrane protein 1 induces synthesis of hypoxia-inducible factor 1α. Mol. Cell. Biol. 24, 5223-5234 (2004)
69. Kondo, s. et al. EBV latent membrane protein 1 up-regulates hypoxia-inducible factor 1α through siah1-mediated down-regulation of prolyl hydroxylases 1 and 3 in nasopharyngeal epithelial cells. Cancer Res. 66, 9870-9877 (2006).
70. Carroll, P. A., Kenerson, H. L., Yeung, R. s. & Lagunoff, M. Latent Kaposi's sarcoma-associated herpesvirus infection of endothelial cells activates hypoxia-induced factors. J. Virol. 80, 10802-10812 (2006).
71. Cai, Q. et al. Kaposi's sarcoma-associated herpesvirus latent protein LANA interacts with HIF-1α to upregulate RTA expression during hypoxia: latency control under low oxygen conditions. J. Virol. 80, 7965-7975 (2006).
72. Bayele, H. K. et al. HIF-1 regulates heritable variation and allele expression phenotypes of the macrophage immune response gene SLC11A1 from a Z-DNA forming microsatellite. Blood 11 0 , 3039-3048 (2007).
73. Hartmann, H. et al. Hypoxia-independent activation of HIF-1 by enterobacteriaceae and their siderophores. Gastroenterology 134, 756-767 (2008).
74. Kempf, V. A. et al. Activation of hypoxia-inducible factor-1 in bacillary angiomatosis: evidence for a role of hypoxia-inducible factor-1 in bacterial infections. Circulation 111 , 1054-1062 (2005).
75. Rupp, J. et al. Chlamydia pneumoniae directly interferes with HIF-1α stabilization in human host cells. Cell. Microbiol. 9, 2181-2191 (2007).
76. Spear, W. et al. The host cell transcription factor hypoxia-inducible factor 1 is required for Toxoplasma gondii growth and survival at physiological oxygen levels. Cell. Microbiol. 8, 339-352 (2006).
77. Blader, I. J., Manger, I. D. & Boothroyd, J. C. Microarray analysis reveals previously unknown changes in Toxoplasma gondii-infected human cells. J. Biol. Chem. 276, 24223-24231 (2001).
78. Arrais-silva, W. W., Paffaro, V. A., Yamada, A. T. & Giorgio, s. Expression of hypoxia-inducible factor-1α in the cutaneous lesions of BALB/c mice infected with Leishmania amazonensis. Exp. Mol. Pathol. 78, 49-54 (2005).
79. Mohamed, H. s. et al. SLC11A1 (formerly NRAMP1) and susceptibility to visceral leishmaniasis in The sudan. Eur. J. Hum. Genet. 12, 66-74 (2004).
80. Li, H. T. , Zhang, T. T. , Zhou, Y. Q., Huang, Q. H. & Huang, J. SLC11A1 (formerly NRAMP1) gene polymorphisms and tuberculosis susceptibility: a meta- analysis. Int. J. Tuberc. Lung Dis. 10, 3-12 (2006).
81. Runstadler, J. A. et al. Association of SLC11A1 (NRAMP1) with persistent oligoarticular and polyarticular rheumatoid factor-negative juvenile idiopathic arthritis in Finnish patients: haplotype analysis in Finnish families. Arthritis Rheum. 52, 247-256 (2005).
82. Takahashi, K. et al. Promoter polymorphism of SLC11A1 (formerly NRAMP1) confers susceptibility to autoimmune type 1 diabetes mellitus in Japanese. Tissue Antigens 63, 231-236 (2004).
83. Strieter, R. M. Mastering innate immunity. Nature Med. 9, 512-513 (2003).
84. Zarember, K. A. & Malech, H. L. HIF-1α: a master regulator of innate host defenses? J. Clin. Invest. 11 5 , 1702-1704 (2005)
85. Zinkernagel, A. s., Peyssonnaux, C., Johnson, R. s. & Nizet, V. Pharmacologic augmentation of hypoxia- inducible factor-1α with mimosine boosts the bactericidal capacity of phagocytes. J. Infect. Dis. 197, 214-217 (2008).
86. Nizet, V. Understanding how leading bacterial pathogens subvert innate immunity to reveal novel therapeutic targets. J. Allergy Clin. Immunol. 120, 13-22 (2007).
87. Hsieh, M. M. et al. HIF prolyl hydroxylase inhibition results in endogenous erythropoietin induction, erythrocytosis, and modest fetal hemoglobin expression in rhesus macaques. Blood 11 0 , 2140-2147 (2007).
88. Botusan, I. R. et al. stabilization of HIF-1α is critical to improve wound healing in diabetic mice. Proc. Natl Acad. Sci. USA 105, 19426-19431 (2008).