Hypoxia-Inducible Factor (HIF) as a Pharmacological Target for Prevention and Treatment of Infectious Diseases

Infectious Diseases and Therapy

Volumn 3, Issue 2, 2014, Pages 159-174

  Bhandari, Tamara ^a   Nizet, Victor ^a,b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

Author keywords

Bacteria; Dendritic cells; Hypoxia inducible factor; Innate immunity; Macrophages; Neutrophils; T cells; Virus

Indexed keywords

ANTIBIOTIC AGENT; CHEMOKINE; CYTOKINE; DEFEROXAMINE; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; HYPOXIA INDUCIBLE FACTOR; HYPOXIA INDUCIBLE FACTOR 1; HYPOXIA INDUCIBLE FACTOR 2; I KAPPA B KINASE BETA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 4; INTERLEUKIN 8; MIMOSINE; SOMATOMEDIN; TOLL LIKE RECEPTOR; UNCLASSIFIED DRUG; VASCULOTROPIN; VIRUS PROTEIN;

ADAPTIVE IMMUNITY; ANTIGEN PRESENTATION; CELL FUNCTION; CELL MATURATION; CELL MIGRATION; DENDRITIC CELL; GENE CONTROL; GENE EXPRESSION; GENETIC TRANSCRIPTION; HOST PATHOGEN INTERACTION; HUMAN; HYPERTENSION; HYPOXIA; IMMUNE RESPONSE; IMMUNOCOMPETENT CELL; IMMUNOMODULATION; INFECTION; INNATE IMMUNITY; MACROPHAGE; MAJOR HISTOCOMPATIBILITY COMPLEX; NEUTROPHIL; NONHUMAN; OXYGEN TENSION; PATHOGENESIS; PROTEIN STABILITY; REGULATORY T LYMPHOCYTE; REVIEW; THROMBOSIS;

EID: 84977071153     PISSN: 21938229     EISSN: 21936382     Source Type: Journal    
DOI: 10.1007/s40121-014-0030-1     Document Type: Review

References (119)

1. Wang GL, Jiang BH, Rue EA, Semenza GL. Hypoxia-inducible factor 1 is a basic-helix–loop–helix-PAS heterodimer regulated by cellular O2 tension. Proc Natl Acad Sci USA. 1995;92:5510–4.
2. Semenza GL, Wang GL. 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. 1992;12:5447–54.
3. Nizet V, Johnson RS. Interdependence of hypoxic and innate immune responses. Nat Rev Immunol. 2009;9:609–17.
4. Heikkila M, Pasanen A, Kivirikko KI, Myllyharju J. Roles of the human hypoxia-inducible factor (HIF)-3α variants in the hypoxia response. Cell Mol Life Sci. 2011;68:3885–901.
5. Tian H, McKnight SL, Russell DW. Endothelial PAS domain protein 1 (EPAS1), a transcription factor selectively expressed in endothelial cells. Genes Dev. 1997;11:72–82.
6. Ema M, Taya S, Yokotani N, Sogawa K, Matsuda Y, Fujii-Kuriyama Y. A novel bHLH-PAS factor with close sequence similarity to hypoxia-inducible factor 1α regulates the VEGF expression and is potentially involved in lung and vascular development. Proc Natl Acad Sci USA. 1997;94:4273–8.
7. Talks KL, Turley H, Gatter KC, Maxwell PH, Pugh CW, Ratcliffe PJ, 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.
8. Ivan M, Kondo K, Yang H, Kim W, Valiando J, Ohh M, et al. HIFα targeted for VHL-mediated destruction by proline hydroxylation: implications for O2 sensing. Science. 2001;292:464–8.
9. 2-regulated prolyl hydroxylation. Science. 2001;292:468–72.
10. Ebert BL, Bunn HF. Regulation of transcription by hypoxia requires a multiprotein complex that includes hypoxia-inducible factor 1, an adjacent transcription factor, and p300/CREB binding protein. Mol Cell Biol. 1998;18:4089–96.
11. Rius J, Guma M, Schachtrup C, Akassoglou K, Zinkernagel AS, Nizet V, et al. NF-κB links innate immunity to the hypoxic response through transcriptional regulation of HIF-1α. Nature. 2008;453:807–11.
12. Taylor CT, Cummins EP. The role of NF-kappaB in hypoxia-induced gene expression. Ann NY Acad Sci. 2009;1177:178–84.
13. Shin DH, Li SH, Yang S-W, Lee BL, Lee MK, Park J-W. Inhibitor of nuclear factor-κB alpha derepresses hypoxia-inducible factor-1 during moderate hypoxia by sequestering factor inhibiting hypoxia-inducible factor from hypoxia-inducible factor 1α. FEBS J. 2009;276:3470–80.
14. Feldser D, Agani F, Iyer NV, Pak B, Ferreira G, Semenza GL. Reciprocal positive regulation of hypoxia-inducible factor 1α and insulin-like growth factor 2. Cancer Res. 1999;59:3915–8.
15. Hellwig-Bürgel T, Rutkowski K, Metzen E, Fandrey J, Jelkmann W. Interleukin-1β and tumor necrosis factor-α stimulate DNA binding of hypoxia-inducible factor-1. Blood. 1999;94:1561–7.
16. Moon EJ, Jeong CH, Jeong JW, Kim KR, Yu DY, Murakami S, et al. Hepatitis B virus X protein induces angiogenesis by stabilizing hypoxia-inducible factor-1α. FASEB J. 2004;18:382–4.
17. Karapetsas A, Giannakakis A, Pavlaki M, Panayiotidis M, Sandaltzopoulos R, Galanis A. Biochemical and molecular analysis of the interaction between ERK2 MAP kinase and hypoxia inducible factor-1α. Int J Biochem Cell Biol. 2011;43:1582–90.
18. Frede S, Stockmann C, Freitag P, Fandrey J. Bacterial lipopolysaccharide induces HIF-1 activation in human monocytes via p44/42 MAPK and NF-kappaB. Biochem J. 2006;396:517–27.
19. Sumbayev VV. PI3 kinase and direct S-nitrosation are involved in down-regulation of apoptosis signal-regulating kinase 1 during LPS-induced Toll-like receptor 4 signalling. Immunol Lett. 2008;115:126–30.
20. Nicholas SA, Sumbayev VV. The involvement of hypoxia-inducible factor 1α in Toll-like receptor 7/8-mediated inflammatory response. Cell Res. 2009;19:973–83.
21. Gibbs BF, Yasinska IM, Pchejetski D, Wyszynski RW, Sumbayev VV. Differential control of hypoxia-inducible factor 1 activity during pro-inflammatory reactions of human haematopoietic cells of myeloid lineage. Int J Biochem Cell Biol. 2012;44:1739–49.
22. Imtiyaz HZ, Simon MC. Hypoxia-inducible factors as essential regulators of inflammation. Curr Τοp Microbiol Immunol. 2010;345:105–20.
23. Zhou J, Schmid T, Brune B. Tumor necrosis factor-α causes accumulation of a ubiquitinated form of hypoxia inducible factor-1α through a nuclear factor-κB-dependent pathway. Mol Biol Cell. 2003;14:2216–25.
24. Jung Y-J, Isaacs JS, Lee S, Trepel J, Neckers L. IL-1β-mediated up-regulation of HIF-1α via an NFκB/COX-2 pathway identifies HIF-1 as a critical link between inflammation and oncogenesis. FASEB J. 2003;17:2115–7.
25. Silver IA. Tissue PO2 changes in acute inflammation. Adv Exp Med Biol. 1977;94:769–74.
26. Hong SW, Yoo JW, Kang HS, Kim S, Lee DK. HIF-1α-dependent gene expression program during the nucleic acid-triggered antiviral innate immune responses. Mol Cells. 2009;27:243–50.
27. Werth N, Beerlage C, Rosenberger C, Yazdi AS, Edelmann M, Amr A, et al. Activation of hypoxia inducible factor 1 is a general phenomenon in infections with human pathogens. PLoS ONE. 2010;5:e11576.
28. Zarember KA, Malech HL. HIF-1α: a master regulator of innate host defenses? J Clin Invest. 2005;115:1702–4.
29. Bosco MC, Varesio L. Dendritic cell reprogramming by the hypoxic environment. Immunobiology. 2012;217:1241–9.
30. Kong T, Eltzschig HK, Karhausen J, Colgan SP, Shelley CS. Leukocyte adhesion during hypoxia is mediated by HIF-1-dependent induction of β2 integrin gene expression. Proc Natl Acad Sci USA. 2004;101:10440–5.
31. Zhou J, Dehne N, Brüne B. Nitric oxide causes macrophage migration via the HIF-1-stimulated small GTPases Cdc42 and Rac1. Free Radic Biol Med. 2009;47:741–9.
32. Schioppa T, Uranchimeg B, Saccani A, Biswas SK, Doni A, Rapisarda A, et al. Regulation of the chemokine receptor CXCR4 by hypoxia. J Exp Med. 2003;198:1391–402.
33. Bosco MC, Reffo G, Puppo M, Varesio L. Hypoxia inhibits the expression of the CCR5 chemokine receptor in macrophages. Cell Immunol. 2004;228:1–7.
34. Walmsley SR, Cadwallader KA, Chilvers ER. The role of HIF-1α in myeloid cell inflammation. Trends Immunol. 2005;26:434–9.
35. Elks PM, van Eeden FJ, Dixon G, Wang X, Reyes-Aldasoro CC, Ingham PW, et al. Activation of hypoxia-inducible factor-1α (Hif-1α) delays inflammation resolution by reducing neutrophil apoptosis and reverse migration in a zebrafish inflammation model. Blood. 2011;118:712–22.
36. Roiniotis J, Dinh H, Masendycz P, Turner A, Elsegood CL, Scholz GM, et al. Hypoxia prolongs monocyte/macrophage survival and enhanced glycolysis is associated with their maturation under aerobic conditions. J Immunol. 2009;182:7974–81.
37. Kuhlicke J, Frick JS, Morote-Garcia JC, Rosenberger P, Eltzschig HK. Hypoxia inducible factor (HIF)-1 coordinates induction of Toll-like receptors TLR2 and TLR6 during hypoxia. PLoS ONE. 2007;2:e1364.
38. Kim SY, Choi YJ, Joung SM, Lee BH, Jung Y-S, Lee JY. Hypoxic stress up-regulates the expression of Toll-like receptor 4 in macrophages via hypoxia-inducible factor. Immunology. 2010;129:516–24.
39. Anand RJ, Gribar SC, Li J, Kohler JW, Branca MF, Dubowski T, et al. Hypoxia causes an increase in phagocytosis by macrophages in a HIF-1α-dependent manner. J Leuk Biol. 2007;82:1257–65.
40. Walmsley SR, Cowburn AS, Clatworthy MR, Morrell NW, Roper EC, Singleton V, et al. Neutrophils from patients with heterozygous germline mutations in the von Hippel Lindau protein (pVHL) display delayed apoptosis and enhanced bacterial phagocytosis. Blood. 2006;108:3176–8.
41. Peyssonnaux C, Datta V, Cramer T, Doedens A, Theodorakis EA, Gallo RL, et al. HIF-1α expression regulates the bactericidal capacity of phagocytes. J Clin Invest. 2005;115:1806–15.
42. Berger EA, McClellan SA, Vistisen KS, Hazlett LD. HIF-1α is essential for effective PMN bacterial killing, antimicrobial peptide production and apoptosis in Pseudomonas aeruginosa keratitis. PLoS Pathog. 2013;9:e1003457.
43. Zinkernagel AS, Peyssonnaux C, Johnson RS, Nizet V. Pharmacologic augmentation of hypoxia-inducible factor-1α with mimosine boosts the bactericidal capacity of phagocytes. J Infect Dis. 2008;197:214–7.
44. Okumura CYM, Hollands A, Tran DN, Olson J, Dahesh S, Köckritz-Blickwede MV, et al. A new pharmacological agent (AKB-4924) stabilizes hypoxia inducible factor-1 (HIF-1) and increases skin innate defenses against bacterial infection. J Mol Med. 2012;90:1079–89.
45. Mecklenburgh KI, Walmsley SR, Cowburn AS, Wiesener M, Reed BJ, Upton PD, et al. Involvement of a ferroprotein sensor in hypoxia-mediated inhibition of neutrophil apoptosis. Blood. 2002;100:3008–16.
46. McInturff AM, Cody MJ, Elliott EA, Glenn JW, Rowley JW, Rondina MT, et al. Mammalian target of rapamycin regulates neutrophil extracellular trap formation via induction of hypoxia-inducible factor 1α. Blood. 2012;120:3118–25.
47. Branitzki-Heinemann K, Okumura CY, Völlger L, Kawakami Y, Kawakami T, Naim HY, et al. A novel role for the transcription factor HIF-1α in the formation of mast cell extracellular traps. Biochem J. 2012;446:159–63.
48. McLellan AD, Kämpgen E. Functions of myeloid and lymphoid dendritic cells. Immunol Lett. 2000;72:101–5.
49. Randolph GJ, Inaba K, Robbiani DF, Steinman RM, Muller WA. Differentiation of phagocytic monocytes into lymph node dendritic cells in vivo. Immunity. 1999;11:753–61.
50. Shortman K, Naik SH. Steady-state and inflammatory dendritic-cell development. Nat Rev Immunol. 2007;7:19–30.
51. Rama I, Bruene B, Torras J, Koehl R, Cruzado JM, Bestard O, et al. Hypoxia stimulus: an adaptive immune response during dendritic cell maturation. Kidney Int. 2008;2008(73):816–25.
52. Goth SR, Chu RA, Pessah IN. Oxygen tension regulates the in vitro maturation of GM-CSF expanded murine bone marrow dendritic cells by modulating class II MHC expression. J Immunol Methods. 2006;308:179–91.
53. Jantsch J, Chakravortty D, Turza N, Prechtel AT, Buchholz B, Gerlach RG, et al. Hypoxia and hypoxia-inducible factor-1α modulate lipopolysaccharide-induced dendritic cell activation and function. J Immunol. 2008;180:4697–705.
54. Spirig R, Djafarzadeh S, Regueira T, Shaw SG, von Garnier C, Takala J, et al. Effects of TLR Agonists on the hypoxia-regulated transcription factor HIF-1α and dendritic cell maturation under normoxic conditions. PLoS ONE. 2010;5:e10983.
55. Yang M, Ma C, Liu S, Sun J, Shao Q, Gao W, et al. Hypoxia skews dendritic cells to a T helper type 2-stimulating phenotype and promotes tumour cell migration by dendritic cell-derived osteopontin. Immunology. 2009;128:e237–49.
56. Ogino T, Onishi H, Suzuki H, Morisaki T, Tanaka M, Katano M. Inclusive estimation of complex antigen presentation functions of monocyte-derived dendritic cells differentiated under normoxia and hypoxia conditions. Cancer Immunol Immunother. 2012;61:409–24.
57. Elia AR, Cappello P, Puppo M, Fraone T, Vanni C, Eva A, et al. Human dendritic cells differentiated in hypoxia down-modulate antigen uptake and change their chemokine expression profile. J Leuk Biol. 2008;84:1472–82.
58. Ricciardi A, Elia AR, Cappello P, Puppo M, Vanni C, Fardin P, et al. Transcriptome of hypoxic immature dendritic cells: modulation of chemokine/receptor expression. Mol Cancer Res. 2008;6:175–85.
59. Pierobon D, Bosco MC, Blengio F, Raggi F, Eva A, Filippi M, et al. Chronic hypoxia reprograms human immature dendritic cells by inducing a proinflammatory phenotype and TREM-1 expression. Eur J Immunol. 2013;43:949–66.
60. Mancino A, Schioppa T, Larghi P, Pasqualini F, Nebuloni M, Chen IH, et al. Divergent effects of hypoxia on dendritic cell functions. Blood. 2008;112:3723–34.
61. Zhao W, Darmanin S, Fu Q, Chen J, Cui H, Wang J, et al. Hypoxia suppresses the production of matrix metalloproteinases and the migration of human monocyte-derived dendritic cells. Eur J Immunol. 2005;35:3468–77.
62. Qu X, Yang M-X, Kong B-H, Qi L, Lam QLK, Yan S, et al. Hypoxia inhibits the migratory capacity of human monocyte-derived dendritic cells. Immunol Cell Biol. 2005;83:668–73.
63. Rahat MA, Marom B, Bitterman H, Weiss-Cerem L, Kinarty A, Lahat N. Hypoxia reduces the output of matrix metalloproteinase-9 (MMP-9) in monocytes by inhibiting its secretion and elevating membranal association. J Leuk Biol. 2006;79:706–18.
64. Bosseto MC, Palma PVB, Covas DT, Giorgio S. Hypoxia modulates phenotype, inflammatory response, and leishmanial infection of human dendritic cells. APMIS. 2010;2010(118):108–14.
65. Lahat N, Rahat MA, Ballan M, Weiss-Cerem L, Engelmayer M, Bitterman H. Hypoxia reduces CD80 expression on monocytes but enhances their LPS-stimulated TNF-α secretion. J Leuk Biol. 2003;74:197–205.
66. Acosta-Iborra B, Elorza A, Olazabal IM, Martín-Cofreces NB, Martin-Puig S, Miró M, et al. Macrophage oxygen sensing modulates antigen presentation and phagocytic functions involving IFN-γ production through the HIF-1α transcription tactor. J Immunol. 2009;182:3155–64.
67. Werno C, Menrad H, Weigert A, Dehne N, Goerdt S, Schledzewski K, et al. Knockout of HIF-1α in tumor-associated macrophages enhances M2 polarization and attenuates their pro-angiogenic responses. Carcinogenesis. 2010;31:1863–72.
68. Blengio F, Raggi F, Pierobon D, Cappello P, Eva A, Giovarelli M, et al. The hypoxic environment reprograms the cytokine/chemokine expression profile of human mature dendritic cells. Immunobiology. 2013;218:76–89.
69. Murata Y, Ohteki T, Koyasu S, Hamuro J. IFN-γ and pro-inflammatory cytokine production by antigen-presenting cells is dictated by intracellular thiol redox status regulated by oxygen tension. Eur J Immunol. 2002;32:2866–73.
70. Wobben R, Huesecken Y, Lodewick C, Gibbert K, Fandrey J, Winning S. Role of hypoxia inducible factor-1α for interferon synthesis in mouse dendritic cells. Biol Chem. 2013;394:495–505.
71. Longhi MP, Trumpfheller C, Idoyaga J, Caskey M, Matos I, Kluger C, et al. Dendritic cells require a systemic type I interferon response to mature and induce CD4+ Th1 immunity with poly IC as adjuvant. J Exp Med. 2009;206:1589–602.
72. Doedens AL, Stockmann C, Rubinstein MP, Liao D, Zhang N, DeNardo DG, et al. Macrophage expression of hypoxia-inducible factor-1 alpha suppresses T-cell function and promotes tumor progression. Cancer Res. 2010;70:7465–75.
73. Jantsch J, Wiese M, Schödel J, Castiglione K, Gläsner J, Kolbe S, et al. Toll-like receptor activation and hypoxia use distinct signaling pathways to stabilize hypoxia-inducible factor 1α (HIF1α) and result in differential HIF1α-dependent gene expression. J Leuk Biol. 2011;90:551–62.
74. Sun J, Zhang Y, Yang M, Xie Q, Li Z, Dong Z, et al. Hypoxia induces T-cell apoptosis by inhibiting chemokine C receptor 7 expression: the role of adenosine receptor A(2). Cell Mol Immunol. 2010;7:77–82.
75. Larbi A, Cabreiro F, Zelba H, Marthandan S, Combet E, Friguet B, et al. Reduced oxygen tension results in reduced human T cell proliferation and increased intracellular oxidative damage and susceptibility to apoptosis upon activation. Free Radic Biol Med. 2010;48:26–34.
76. Conforti L, Petrovic M, Mohammad D, Lee S, Ma Q, Barone S, et al. Hypoxia regulates expression and activity of Kv1.3 channels in T lymphocytes: a possible role in T cell proliferation. J Immunol. 2003;170:695–702.
77. 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. 2008;69:421–5.
78. Georgiev P, Belikoff BB, Hatfield S, Ohta A, Sitkovsky MV, Lukashev D. Genetic deletion of the HIF-1α isoform I.1 in T cells enhances anti-bacterial immunity and improves survival in a murine peritonitis model. Eur J Immunol. 2013;43:655–66.
79. Lukashev D, Klebanov B, Kojima H, Grinberg A, Ohta A, Berenfeld L, 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. 2006;177:4962–5.
80. Fontenot JD, Gavin MA, Rudensky AY. Foxp3 programs the development and function of CD4 + CD25 + regulatory T cells. Nat Immunol. 2003;4:330–6.
81. Ivanov II, McKenzie BS, Zhou L, Tadokoro CE, Lepelley A, Lafaille JJ, et al. The orphan nuclear receptor RORγt directs the differentiation program of proinflammatory IL-17+ T helper cells. Cell. 2006;126:1121–33.
82. Clambey ET, McNamee EN, Westrich JA, Glover LE, Campbell EL, Jedlicka P, et al. Hypoxia-inducible factor-1α-dependent induction of FoxP3 drives regulatory T-cell abundance and function during inflammatory hypoxia of the mucosa. Proc Natl Acad Sci USA. 2012;109:E2784–93.
83. Ben-Shoshan J, Maysel-Auslender S, Mor A, Keren G, George J. Hypoxia controls CD4+ CD25+ regulatory T-cell homeostasis via hypoxia-inducible factor-1α. Eur J Immunol. 2008;38:2412–8.
84. Higashiyama M, Hokari R, Hozumi H, Kurihara C, Ueda T, Watanabe C, et al. HIF-1 in T cells ameliorated dextran sodium sulfate-induced murine colitis. J Leuk Biol. 2012;91:901–9.
85. Ikejiri A, Nagai S, Goda N, Kurebayashi Y, Osada-Oka M, Takubo K, et al. Dynamic regulation of Th17 differentiation by oxygen concentrations. Int Immunol. 2012;24:137–46.
86. Dang EV, Barbi J, Yang H-Y, Jinasena D, Yu H, Zheng Y, et al. Control of TH17/Treg balance by hypoxia-inducible factor 1. Cell. 2011;146:772–84.
87. Shi LZ, Wang R, Huang G, Vogel P, Neale G, Green DR, et al. HIF1α-dependent glycolytic pathway orchestrates a metabolic checkpoint for the differentiation of TH17 and Treg cells. J Exp Med. 2011;208:1367–76.
88. Kominsky DJ, Campbell EL, Colgan SP. Metabolic shifts in immunity and inflammation. J Immunol. 2010;184:4062–8.
89. Haeberle HA, Dürrstein C, Rosenberger P, Hosakote YM, Kuhlicke J, Kempf VAJ, et al. Oxygen-independent stabilization of hypoxia inducible factor (HIF)-1 during RSV Infection. PLoS ONE. 2008;3:e3352.
90. Hwang IIL, Watson IR, Der SD, Ohh M. Loss of VHL confers hypoxia-inducible factor (HIF)-dependent resistance to vesicular stomatitis virus: role of HIF in antiviral response. J Virol. 2006;80:10712–23.
91. Cho IR, Koh SS, Min HJ, Park EH, Ratakorn S, Jhun BH, et al. Down-regulation of HIF-1α by oncolytic reovirus infection independently of VHL and p53. Cancer Gene Ther. 2010;17:365–72.
92. Lungu GF, Stoica G, Wong PKY. Down-regulation of Jab1, HIF-1α, and VEGF by Moloney murine leukemia virus-ts1 infection: a possible cause of neurodegeneration. J Neurovirol. 2008;14:239–51.
93. Rupp J, Gieffers J, Klinger M, Van Zandbergen G, Wrase R, Maass M, et al. Chlamydia pneumoniae directly interferes with HIF-1α stabilization in human host cells. Cell Microbiol. 2007;9:2181–91.
94. Legendre C, Reen FJ, Mooij MJ, McGlacken GP, Adams C, O’Gara F. Pseudomonas aeruginosa alkyl quinolones repress hypoxia-inducible factor 1 (HIF-1) signaling through HIF-1α degradation. Infect Immun. 2012;80:3985–92.
95. Yoo YG, Oh SH, Park ES, Cho H, Lee N, Park H, 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. 2003;278:39076–84.
96. Cai QL, Knight JS, Verma SC, Zald P, Robertson ES. EC5S ubiquitin complex is recruited by KSHV latent antigen LANA for degradation of the VHL and p53 tumor suppressors. PLoS Pathog. 2006;2:e116.
97. Kondo S, Seo SY, Yoshizaki T, Wakisaka N, Furukawa M, Joab I, 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. 2006;66:9870–7.
98. Deshmane SL, Mukerjee R, Fan S, Del Valle L, Michiels C, Sweet T, et al. Activation of the oxidative stress pathway by HIV-1 Vpr leads to induction of hypoxia-inducible factor 1α expression. J Biol Chem. 2009;284(17):11364–73.
99. Piña-Oviedo S, Khalili K, Del Valle L. Hypoxia inducible factor-1α activation of the JCV promoter: role in the pathogenesis of progressive multifocal leukoencephalopathy. Acta Neuropathol. 2009;118:235–47.
100. Polcicova K, Hrabovska Z, Mistrikova J, Tomaskova J, Pastorek J, Pastorekova S, et al. Up-regulation of Murid herpesvirus 4 ORF50 by hypoxia: possible implication for virus reactivation from latency. Virus Res. 2008;132:257–62.
101. Jiang J-H, Wang N, Li A, Liao W-T, Pan Z-G, Mai S-J, et al. Hypoxia can contribute to the induction of the Epstein–Barr virus (EBV) lytic cycle. J Clin Virol. 2006;37:98–103.
102. Keely S, Glover LE, Weissmueller T, MacManus CF, Fillon S, Fennimore B, et al. Hypoxia-inducible factor-dependent regulation of platelet-activating factor receptor as a route for Gram-positive bacterial translocation across epithelia. Mol Biol Cell. 2010;21:538–46.
103. Spear W, Chan D, Coppens I, Johnson RS, Giaccia A, Blader IJ. The host cell transcription factor hypoxia-inducible factor 1 is required for Toxoplasma gondii growth and survival at physiological oxygen levels. Cell Microbiol. 2006;8:339–52.
104. Wiley M, Sweeney KR, Chan DA, Brown KM, McMurtrey C, Howard EW, et al. Toxoplasma gondii activates hypoxia-inducible factor (HIF) by stabilizing the HIF-1α subunit via type I activin-like receptor kinase receptor signaling. J Biol Chem. 2010;285:26852–60.
105. Degrossoli A, Bosetto MC, Lima CBC, Giorgio S. Expression of hypoxia-inducible factor 1α in mononuclear phagocytes infected with Leishmania amazonensis. Immunol Lett. 2007;114:119–25.
106. Singh AK, Mukhopadhyay C, Biswas S, Singh VK, Mukhopadhyay CK. Intracellular pathogen Leishmania donovani activates hypoxia inducible factor-1 by dual mechanism for survival advantage within macrophage. PLoS ONE. 2012;7:e38489.
107. Zhao S, Wu J. Hypoxia inducible factor stabilization as a novel strategy to treat anemia. Curr Med Chem. 2013;20:2697–711.
108. Peyssonnaux C, Cejudo-Martin P, Doedens A, Zinkernagel AS, Johnson RS, Nizet V. Cutting edge: essential role of hypoxia inducible factor-1α in development of lipopolysaccharide-induced sepsis. J Immunol. 2007;178:7516–9.
109. Thiel M, Caldwell CC, Kreth S, Kuboki S, Chen P, Smith P, 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. 2007;2:e853.
110. Schafer ST, Frede S, Winning S, Bick A, Roshangar P, Fandrey J, et al. Hypoxia-inducible factor and target gene expression are decreased in patients with sepsis: prospective observational clinical and cellular studies. Anesthesiology. 2013;118:1426–36.
111. Keely S, Campbell EL, Baird AW, Hansbro PM, Shalwitz RA, Kotsakis A, et al. Contribution of epithelial innate immunity to systemic protection afforded by prolyl hydroxylase inhibition in murine colitis. Mucosal Immunol. 2014;7:114–23.
112. Campbell EL, Bruyninckx WJ, Kelly CJ, Glover LE, McNamee EN, Bowers BE, et al. Transmigrating neutrophils shape the mucosal microenvironment through localized oxygen depletion to influence resolution of inflammation. Immunity. 2014;40:66–77.
113. Weigert A, Weichand B, Sekar D, Sha W, Hahn C, Mora J, et al. HIF-1α is a negative regulator of plasmacytoid DC development in vitro and in vivo. Blood. 2012;120:3001–6.
114. Bhandari T, Olson J, Johnson RS, Nizet V. HIF-1alpha influences myeloid cell antigen presentation and response to subcutaneous OVA vaccination. J Mol Med (Berlin). 2013;91:1199–205.
115. Loboda A, Jozkowicz A, Dulak J. HIF-1 and HIF-2 transcription factors—similar but not identical. Mol Cells. 2010;29:435–42.
116. Loboda A, Jozkowicz A, Dulak J. HIF-1 versus HIF-2—is one more important than the other? Vascul Pharmacol. 2012;56:245–51.
117. Florczyk U, Czauderna S, Stachurska A, Tertil M, Nowak W, Kozakowska M, et al. Opposite effects of HIF-1α and HIF-2α on the regulation of IL-8 expression in endothelial cells. Free Radic Biol Med. 2011;51:1882–92.
118. Fang H-Y, Hughes R, Murdoch C, Coffelt SB, Biswas SK, Harris AL, et al. Hypoxia-inducible factors 1 and 2 are important transcriptional effectors in primary macrophages experiencing hypoxia. Blood. 2009;114:844–59.
119. Loboda A, Stachurska A, Florczyk U, Rudnicka D, Jazwa A, Wegrzyn J, et al. HIF-1 induction attenuates Nrf2-dependent IL-8 expression in human endothelial cells. Antioxid Redox Signal. 2009;11:1501–17.