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01-12-2020 | Dengue Virus | Review

Oxygen: viral friend or foe?

Authors: Esther Shuyi Gan, Eng Eong Ooi

Published in: Virology Journal | Issue 1/2020

Abstract

The oxygen levels organ and tissue microenvironments vary depending on the distance of their vasculature from the left ventricle of the heart. For instance, the oxygen levels of lymph nodes and the spleen are significantly lower than that in atmospheric air. Cellular detection of oxygen and their response to low oxygen levels can exert a significant impact on virus infection. Generally, viruses that naturally infect well-oxygenated organs are less able to infect cells under hypoxic conditions. Conversely, viruses that infect organs under lower oxygen tensions thrive under hypoxic conditions. This suggests that in vitro experiments performed exclusively under atmospheric conditions ignores oxygen-induced modifications in both host and viral responses. Here, we review the mechanisms of how cells adapt to low oxygen tensions and its impact on viral infections. With growing evidence supporting the role of oxygen microenvironments in viral infections, this review highlights the importance of factoring oxygen concentrations into in vitro assay conditions. Bridging the gap between in vitro and in vivo oxygen tensions would allow for more physiologically representative insights into viral pathogenesis.

Abrantes JL, Alves CM, Costa J, Almeida FCL, Sola-Penna M, Fontes CFL, Souza TML. Herpes simplex type 1 activates glycolysis through engagement of the enzyme 6-phosphofructo-1-kinase (PFK-1). Biochim Biophys Acta. 2012;1822:1198–206. https://doi.org/10.1016/j.bbadis.2012.04.011.CrossRefPubMed

Aghi MK, Liu T-C, Rabkin S, Martuza RL. Hypoxia enhances the replication of oncolytic herpes simplex virus. Mol Ther. 2009;17:51–6. https://doi.org/10.1038/mt.2008.232.CrossRefPubMed

Aprelikova O, Wood M, Tackett S, Chandramouli GVR, Barrett JC. Role of ETS transcription factors in the hypoxia-inducible factor-2 target gene selection. Cancer Res. 2006;66:5641–7. https://doi.org/10.1158/0008-5472.CAN-05-3345.CrossRefPubMed

Assad F, Schultheiss R, Leniger-Follert E, Wüllenweber R. Measurement of local oxygen partial pressure (PO2) of the brain cortex in cases of brain tumors. In: CNS metastases neurosurgery in the aged, advances in neurosurgery. Berlin, Heidelberg: Springer Berlin Heidelberg; 1984. p. 263–70.CrossRef

Ayala-Nunez NV, Hoornweg TE, van de Pol DPI, Sjollema KA, Flipse J, van der Schaar HM, Smit JM. How antibodies alter the cell entry pathway of dengue virus particles in macrophages. Sci Rep. 2016;6:28768. https://doi.org/10.1038/srep28768.CrossRefPubMedPubMedCentral

Beppu K, Nakamura K, Linehan WM, Rapisarda A, Thiele CJ. Topotecan blocks hypoxia-inducible factor-1alpha and vascular endothelial growth factor expression induced by insulin-like growth factor-I in neuroblastoma cells. Cancer Res. 2005;65:4775–81. https://doi.org/10.1158/0008-5472.CAN-04-3332.CrossRefPubMed

Bilz NC, Jahn K, Lorenz M, Lüdtke A, Hübschen JM, Geyer H, Mankertz A, Hübner D, Liebert UG, Claus C. Rubella viruses shift cellular bioenergetics to a more oxidative and glycolytic phenotype with a strain-specific requirement for glutamine. J Virol. 2018;92:13. https://doi.org/10.1128/JVI.00934-18.CrossRef

Boekstegers P, Riessen R, Seyde W. Oxygen partial pressure distribution within skeletal muscle: Indicator of whole body oxygen delivery in patients? In: Oxygen transport to tissue XII, advances in experimental medicine and biology. Boston: Springer; 1990. p. 507–14. https://doi.org/10.1007/978-1-4684-8181-5_57.CrossRef

Bollinger T, Bollinger A, Gies S, Feldhoff L, Solbach W, Rupp J. Transcription regulates HIF-1|[alpha]| expression in CD4|[plus]| T cells. Immunol Cell Biol. 2016;94:109–13. https://doi.org/10.1038/icb.2015.64.CrossRefPubMed

10.

Boonnak K, Slike BM, Donofrio GC, Marovich MA. Human FcγRII cytoplasmic domains differentially influence antibody-mediated dengue virus infection. J Immunol. 2013;190:5659–65. https://doi.org/10.4049/jimmunol.1203052.CrossRefPubMedPubMedCentral

11.

Bosco MC, Pierobon D, Blengio F, Raggi F, Vanni C, Gattorno M, Eva A, Novelli F, Cappello P, Giovarelli M, Varesio L. Hypoxia modulates the gene expression profile of immunoregulatory receptors in human mDCs: identification of TREM-1 as a novel hypoxic marker in vitro and in vivo. Blood. 2010;117, blood–2010–06–292136–2639. https://doi.org/10.1182/blood-2010-06-292136.

12.

Bosco MC, Puppo M, Santangelo C, Anfosso L, Pfeffer U, Fardin P, Battaglia F, Varesio L. Hypoxia modifies the transcriptome of primary human monocytes: modulation of novel immune-related genes and identification of CC-chemokine ligand 20 as a new hypoxia-inducible gene. J Immunol. 2006;177:1941–55.CrossRefPubMed

13.

Brooks AJ, Eastwood J, Beckingham IJ, Girling KJ. Liver tissue partial pressure of oxygen and carbon dioxide during partial hepatectomy. Br J Anaesth. 2004;92:735–7. https://doi.org/10.1093/bja/aeh112.CrossRefPubMed

14.

Cai QL, Knight JS, Verma SC, PLoS PZ. EC5S ubiquitin complex is recruited by KSHV latent antigen LANA for degradation of the VHL and p53 tumor suppressors; 2006.CrossRef

15.

Caillet-Fauquet P, Draps M-L, Di Giambattista M, de Launoit Y, Laub R. Hypoxia enables B19 erythrovirus to yield abundant infectious progeny in a pluripotent erythroid cell line. J Virol Methods. 2004;121:145–53. https://doi.org/10.1016/j.jviromet.2004.06.010.CrossRefPubMed

16.

Caldwell CC, Kojima H, Lukashev D, Armstrong J, Farber M, Apasov SG, Sitkovsky MV. Differential effects of physiologically relevant hypoxic conditions on T lymphocyte development and effector functions. J Immunol. 2001;167:6140–9.CrossRefPubMed

17.

Carreau A, Hafny Rahbi BE, Matejuk A, Grillon C, Kieda C. Why is the partial oxygen pressure of human tissues a crucial parameter? Small molecules and hypoxia. J Cell Mol Med. 2011;15:1239–53. https://doi.org/10.1111/j.1582-4934.2011.01258.x.CrossRefPubMedPubMedCentral

18.

Carrero P, Okamoto K, Coumailleau P, O'Brien S, Tanaka H, Poellinger L. Redox-regulated recruitment of the transcriptional coactivators CREB-binding protein and SRC-1 to hypoxia-inducible factor 1alpha. Mol Cell Biol. 2000;20:402–15. https://doi.org/10.1128/MCB.20.1.402-415.2000.CrossRefPubMedPubMedCentral

19.

Chabi S, Uzan B, Naguibneva I, Rucci J, Fahy L, Calvo J, Arcangeli M-L, Mazurier F, Pflumio F, Haddad R. Hypoxia regulates lymphoid development of human hematopoietic progenitors. Cell Rep. 2019;29:2307–2320.e6. https://doi.org/10.1016/j.celrep.2019.10.050.CrossRefPubMed

20.

Chan CYY, Low JZH, Gan ES, Ong EZ, Zhang SL-X, Tan HC, Chai X, Ghosh S, Ooi EE, Chan KR. Antibody-Dependent Dengue Virus Entry Modulates Cell Intrinsic Responses for Enhanced Infection. mSphere. 2019;4:504. https://doi.org/10.1128/mSphere.00528-19.CrossRef

21.

Chan KR, Ong EZ, Tan HC, Zhang SL-X, Zhang Q, Tang KF, Kaliaperumal N, Lim APC, Hibberd ML, Chan SH, Connolly JE, Krishnan MN, Lok SM, Hanson BJ, Lin C-N, Ooi EE. Leukocyte immunoglobulin-like receptor B1 is critical for antibody-dependent dengue. Proc Natl Acad Sci U S A. 2014;111:2722–7. https://doi.org/10.1073/pnas.1317454111.CrossRefPubMedPubMedCentral

22.

Chawla T, Chan KR, Zhang SL, Tan HC, Lim APC, Hanson BJ, Ooi EE. Dengue virus neutralization in cells expressing fc gamma receptors. PLoS One. 2013;8:e65231. https://doi.org/10.1371/journal.pone.0065231.CrossRefPubMedPubMedCentral

23.

Chen AY, Guan W, Lou S, Liu Z, Kleiboeker S, Qiu J. Role of erythropoietin receptor signaling in parvovirus B19 replication in human erythroid progenitor cells. J Virol. 2010;84:12385–96. https://doi.org/10.1128/JVI.01229-10.CrossRefPubMedPubMedCentral

24.

Chen AY, Kleiboeker S, Qiu J. Productive parvovirus B19 infection of primary human erythroid progenitor cells at hypoxia is regulated by STAT5A and MEK signaling but not HIFα. PLoS Pathog. 2011;7:e1002088. https://doi.org/10.1371/journal.ppat.1002088.CrossRefPubMedPubMedCentral

25.

Cho IR et al. Oncotropic H-1 parvovirus infection degrades HIF-1α protein in human pancreatic cancer cells independently of VHL and RACK1. Int J Oncol. 2015;46(5):2076–082.

26.

Chotiwan N, Roehrig JT, Schlesinger JJ, Blair CD, Huang CY-H. Molecular determinants of dengue virus 2 envelope protein important for virus entry in FcγRIIA-mediated antibody-dependent enhancement of infection. Virology. 2014;456-457:238–46. https://doi.org/10.1016/j.virol.2014.03.031.CrossRefPubMed

27.

Connor JH, Naczki C, Koumenis C, Lyles DS. Replication and cytopathic effect of oncolytic vesicular stomatitis virus in hypoxic tumor cells in vitro and in vivo. J Virol. 2004;78:8960–70. https://doi.org/10.1128/JVI.78.17.8960-8970.2004.CrossRefPubMedPubMedCentral

28.

Corcoran SE, O'Neill LAJ. HIF1α and metabolic reprogramming in inflammation. J Clin Invest. 2016;126:3699–707. https://doi.org/10.1172/JCI84431.CrossRefPubMedPubMedCentral

29.

Cramer T, Yamanishi Y, Clausen BE, Förster I, Pawlinski R, Mackman N, Haase VH, Jaenisch R, Corr M, Nizet V, Firestein GS, Gerber HP, Ferrara N, Johnson RS. HIF-1α is essential for myeloid cell-mediated inflammation. Cell. 2003;112:645–57. https://doi.org/10.1016/S0092-8674(03)00154-5.CrossRefPubMedPubMedCentral

30.

Dames SA, Martinez-Yamout M, De Guzman RN, Dyson HJ, Wright PE. Structural basis for Hif-1 alpha /CBP recognition in the cellular hypoxic response. PNAS. 2002;99:5271–6. https://doi.org/10.1073/pnas.082121399.CrossRefPubMedPubMedCentral

31.

Davis DA, Rinderknecht AS, Zoeteweij JP, Aoki Y, Read-Connole EL, Tosato G, Blauvelt A, Yarchoan R. Hypoxia induces lytic replication of Kaposi sarcoma-associated herpesvirus. Blood. 2001;97:3244–50. https://doi.org/10.1182/blood.v97.10.3244.CrossRefPubMed

32.

Dayan F, Roux D, Brahimi-Horn MC, Pouyssegur J, Mazure NM. The oxygen sensor factor-inhibiting hypoxia-inducible factor-1 controls expression of distinct genes through the bifunctional transcriptional character of hypoxia-inducible factor-1α. Cancer Res. 2006;66:3688–98. https://doi.org/10.1158/0008-5472.CAN-05-4564.CrossRefPubMed

33.

Dejnirattisai W, Jumnainsong A, Onsirisakul N, Fitton P, Vasanawathana S, Limpitikul W, Puttikhunt C, Edwards C, Duangchinda T, Supasa S, Chawansuntati K, Malasit P, Mongkolsapaya J, Screaton G. Cross-reacting antibodies enhance dengue virus infection in humans. Science. 2010;328:745–8. https://doi.org/10.1126/science.1185181.CrossRefPubMed

34.

Del Bufalo D. et al. Antiangiogenic Potential of the Mammalian Target of Rapamycin Inhibitor Temsirolimus. Cancer Res. 2006;66(11):5549–54.

35.

Depping R, Steinhoff A, Schindler SG, Friedrich B, Fagerlund R, Metzen E, Hartmann E, Köhler M. Nuclear translocation of hypoxia-inducible factors (HIFs): involvement of the classical importin α/β pathway. Biochimica et Biophysica Acta (BBA) - Mol Cell Res. 2008;1783:394–404.CrossRef

36.

Dominguez O, Rojo P, Las Heras d S, Folgueira D, Contreras JR. Clinical presentation and characteristics of pharyngeal adenovirus infections. Pediatr Infect Dis J. 2005;24:733–4. https://doi.org/10.1097/01.inf.0000172942.96436.2d.CrossRefPubMed

37.

Ebbesen P, Toth FD, Villadsen JA, Nørskov-Lauritsen N. In vitro interferon and virus production at in vivo physiologic oxygen tensions. In Vivo. 1991;5:355–8.PubMed

38.

Ema M, Hirota K, Mimura J, Abe H, Yodoi J, Sogawa K, Poellinger L, Kuriyama YF. Molecular mechanisms of transcription activation by HLF and HIF1α in response to hypoxia: their stabilization and redox signal-induced interaction with CBP/p300. EMBO J. 1999;18:1905–14. https://doi.org/10.1093/emboj/18.7.1905.CrossRefPubMedPubMedCentral

39.

Ema M, Taya S, Yokotani N. 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 … , in:. Presented at the Proceedings of the …; 1997.

40.

Fleischmann E, Kurz A, Niedermayr M, Schebesta K, Kimberger O, Sessler DI, Kabon B, Prager G. Tissue oxygenation in obese and non-obese patients during laparoscopy. Obes Surg. 2005;15:813–9. https://doi.org/10.1381/0960892054222867.CrossRefPubMedPubMedCentral

41.

Fontaine KA, Sanchez EL, Camarda R, Lagunoff M. Dengue virus induces and requires glycolysis for optimal replication. J Virol. 2015;89:2358–66. https://doi.org/10.1128/JVI.02309-14.CrossRefPubMed

42.

Frakolaki E, Kaimou P, Moraiti M, Kalliampakou KI, Karampetsou K, Dotsika E, Liakos P, Vassilacopoulou D, Mavromara P, Bartenschlager R, Vassilaki N. The role of tissue oxygen tension in dengue virus replication. Cells. 2018;7:241. https://doi.org/10.3390/cells7120241.CrossRefPubMedCentral

43.

Fraser IS, Baird DT, Cockburn F. Ovarian venous blood PO 2 , PCO 2 and pH in women. J Reprod Fertil. 1973;33:11–7. https://doi.org/10.1530/jrf.0.0330011.CrossRefPubMed

44.

Freedman SJ, Sun Z-YJ, Kung AL, France DS, Wagner G, Eck MJ. Structural basis for negative regulation of hypoxia-inducible factor-1|[alpha]| by CITED2. Nat Struct Mol Biol. 2003;10:504–12. https://doi.org/10.1038/nsb936.CrossRef

45.

Galbraith MD, Allen MA, Bensard CL, Wang X, Schwinn MK, Qin B, Long HW, Daniels DL, Hahn WC, Dowell RD, Espinosa JM. HIF1A employs CDK8-mediator to stimulate RNAPII elongation in response to hypoxia. Cell. 2013;153:1327–39.CrossRefPubMedPubMedCentral

46.

Gan ES, Cheong WF, Chan KR, Ong EZ, Chai X, Tan HC, Ghosh S, Wenk MR, Ooi EE. Hypoxia enhances antibody-dependent dengue virus infection. EMBO J. 2017:e201695642. https://doi.org/10.15252/embj.201695642.

47.

Gluckman E, Broxmeyer HA, Auerbach AD, Friedman HS, Douglas GW, Devergie A, Esperou H, Thierry D, Socie G, Lehn P. Hematopoietic reconstitution in a patient with Fanconi's anemia by means of umbilical-cord blood from an HLA-identical sibling. N Engl J Med. 1989;321:1174–8. https://doi.org/10.1056/NEJM198910263211707.CrossRefPubMed

48.

Greenberger LM, Horak ID, Filpula D, Sapra P, Westergaard M, Frydenlund HF, Albæk C, Schrøder H, Ørum H. A RNA antagonist of hypoxia-inducible factor-1α, EZN-2968, inhibits tumor cell growth. Mol Cancer Ther. 2008;7:3598–608. https://doi.org/10.1158/1535-7163.MCT-08-0510.CrossRefPubMed

49.

Gu YZ et al. Molecular characterization and chromosomal localization of a third α-class hypoxia inducible factor subunit, HIF3α. Gene Expr J Liver Res. 1998;7(9):205–13.

50.

Guo X, Zhu Z, Zhang W, Meng X, Zhu Y, Han P, Zhou X, Hu Y, Wang R. Nuclear translocation of HIF-1α induced by influenza a (H1N1) infection is critical to the production of proinflammatory cytokines. Emerg Microbes Infect. 2017;6:e39–8. https://doi.org/10.1038/emi.2017.21.CrossRefPubMedPubMedCentral

51.

Guo, Y et al. Human papillomavirus 16 E6 contributes HIF-1α induced Warburg effect by attenuating the VHL-HIF-1α interaction. Cells. 2014;15:7974–86.

52.

Guzman MG, Alvarez M, Halstead SB. Secondary infection as a risk factor for dengue hemorrhagic fever/dengue shock syndrome: an historical perspective and role of antibody-dependent enhancement of infection. Arch Virol. 2013;158:1445–59. https://doi.org/10.1007/s00705-013-1645-3.CrossRefPubMed

53.

Guzman MG, Kouri G, Martínez E, Bravo J, Riverón R, Soler M, Vazquez S, Morier L. Clinical and serologic study of Cuban children with dengue hemorrhagic fever/dengue shock syndrome (DHF/DSS). Bull Pan Am Health Organ. 1987;21:270–9.PubMed

54.

Guzman MG, Kouri G, Valdes L, Bravo J, Alvarez M, Vazques S, Delgado I, Halstead SB. Epidemiologic studies on dengue in Santiago de Cuba, 1997. Am J Epidemiol. 2000;152:793–9– discussion 804. https://doi.org/10.1093/aje/152.9.793.CrossRefPubMed

55.

Habler OP, Messmer KFW. The physiology of oxygen transport. Transfus Sci. 1997;18:425–35. https://doi.org/10.1016/S0955-3886(97)00041-6.CrossRefPubMed

56.

Hagen T, Taylor CT, Lam F, Moncada S. Redistribution of intracellular oxygen in hypoxia by nitric oxide: effect on HIF1α. Science. 2003;302:1975–8. https://doi.org/10.1126/science.1088805.CrossRefPubMed

57.

Halstead SB, Nimmannitya S, Cohen SN. Observations related to pathogenesis of dengue hemorrhagic fever. IV. Relation of disease severity to antibody response and virus recovered. Yale J Biol Med. 1970;42:311–28.PubMedPubMedCentral

58.

Haque M, Davis DA, Wang V, Widmer I, Yarchoan R. Kaposi's sarcoma-associated herpesvirus (human herpesvirus 8) contains hypoxia response elements: relevance to lytic induction by hypoxia. J Virol. 2003;77:6761–8. https://doi.org/10.1128/JVI.77.12.6761-6768.2003.CrossRefPubMedPubMedCentral

59.

Hara S, Hamada J, Kobayashi C, Kondo Y, Imura N. Expression and characterization of hypoxia-inducible factor (HIF)-3alpha in human kidney: suppression of HIF-mediated gene expression by HIF-3alpha. Biochem Biophys Res Commun. 2001;287:808–13. https://doi.org/10.1006/bbrc.2001.5659.CrossRefPubMed

60.

Harrison JS, Rameshwar P, Chang V, Bandari P. Oxygen saturation in the bone marrow of healthy volunteers. Blood. 2002;99:394. https://doi.org/10.1182/blood.v99.1.394.CrossRefPubMed

61.

He B, Chou J, Liebermann DA, Hoffman B, Roizman B. The carboxyl terminus of the murine MyD116 gene substitutes for the corresponding domain of the gamma (1)34.5 gene of herpes simplex virus to preclude the premature shutoff of total protein synthesis in infected human cells. J Virol. 1996;70:84–90.CrossRefPubMedPubMedCentral

62.

Hegedus A, Kavanagh Williamson M, Huthoff H. HIV-1 pathogenicity and virion production are dependent on the metabolic phenotype of activated CD4+ T cells. Retrovirology. 2014;11:98–18. https://doi.org/10.1186/s12977-014-0098-4.CrossRefPubMedPubMedCentral

63.

Hellwig-Bürgel T, Rutkowski K, Metzen E, Fandrey J, Jelkmann W. Interleukin-1beta and tumor necrosis factor-alpha stimulate DNA binding of hypoxia-inducible factor-1. Blood. 1999;94:1561–7.CrossRefPubMed

64.

Hockel M, Vaupel P. Tumor hypoxia: definitions and current clinical, biologic, and molecular aspects. J Natl Cancer Instit. 2001;93(4):266–76.

65.

Holland SK, Kennan RP, Schaub MM, D'Angelo MJ, Gore JC. Imaging oxygen tension in liver and spleen by 19F NMR. Magn Reson Med. 1993;29:446–58. https://doi.org/10.1002/mrm.1910290405.CrossRefPubMed

66.

Hu C-J, Wang L-Y, Chodosh LA, Keith B, Simon MC. Differential roles of hypoxia-inducible factor 1alpha (HIF-1alpha) and HIF-2alpha in hypoxic gene regulation. Mol Cell Biol. 2003;23:9361–74. https://doi.org/10.1128/MCB.23.24.9361-9374.2003.CrossRefPubMedPubMedCentral

67.

Hu CJ, Sataur A, Wang L, Chen H. The N-terminal transactivation domain confers target gene specificity of hypoxia-inducible factors HIF-1α and HIF-2α. Mol Biol Cell. 2007;18:4528–42.CrossRefPubMedPubMedCentral

68.

Hu J-L, Liu L-P, Yang S-L, Fang X, Wen L, Ren Q-G, Yu C. Hepatitis B virus induces hypoxia-inducible factor-2α expression through hepatitis B virus X protein. Oncol Rep. 2016;35:1443–8. https://doi.org/10.3892/or.2015.4480.CrossRefPubMed

69.

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. https://doi.org/10.1128/JVI.01014-06.CrossRefPubMedPubMedCentral

70.

Hwang S, Nguyen AD, Jo Y, Engelking LJ, Brugarolas J, DeBose-Boyd RA. Hypoxia-inducible factor 1α activates insulin-induced gene 2 (Insig-2) transcription for degradation of 3-hydroxy-3-methylglutaryl (HMG)-CoA reductase in the liver. J Biol Chem. 2017;292:9382–93. https://doi.org/10.1074/jbc.M117.788562.CrossRefPubMedPubMedCentral

71.

Imesch P, Samartzis EP, Schneider M, Fink D, Fedier A. Inhibition of transcription, expression, and secretion of the vascular epithelial growth factor in human epithelial endometriotic cells by romidepsin. Fertil Steril. 2011;95:1579–83. https://doi.org/10.1016/j.fertnstert.2010.12.058.CrossRefPubMed

72.

Imtiyaz HZ, Williams EP, Hickey MM, Patel SA, Durham AC, Yuan L-J, Hammond R, Gimotty PA, Keith B, Simon MC. Hypoxia-inducible factor 2α regulates macrophage function in mouse models of acute and tumor inflammation. J Clin Invest. 2010;120:2699–714. https://doi.org/10.1172/JCI39506.CrossRefPubMedPubMedCentral

73.

Ingels A et al. Preclinical trial of a new dual mTOR inhibitor, MLN0128, using renal cell carcinoma tumorgrafts. Int J Cancer. 2014;134(10):2322–29.

74.

Isaacs JS et al. Hsp90 regulates a von Hippel Lindau-independent hypoxia-inducible factor-1α-degradative pathway. Journal of Biological. 2002;277:29936–44.

75.

Jantsch J, Chakravortty D, Turza N, Prechtel AT, Buchholz B, Gerlach RG, Volke M, Gläsner J, Warnecke C, Wiesener MS, Eckardt K-U, Steinkasserer A, Hensel M, Willam C. Hypoxia and hypoxia-inducible factor-1 alpha modulate lipopolysaccharide-induced dendritic cell activation and function. J Immunol. 2008;180:4697–705. https://doi.org/10.4049/jimmunol.180.7.4697.CrossRefPubMed

76.

Jauniaux E, Watson AL, Hempstock J, Bao YP, Skepper JN, Burton GJ. Onset of maternal arterial blood flow and placental oxidative stress. A possible factor in human early pregnancy failure. Am J Pathol. 2000;157:2111–22. https://doi.org/10.1016/S0002-9440(10)64849-3.CrossRefPubMedPubMedCentral

77.

Jeong J-W, Bae M-K, Ahn M-Y, Kim S-H, Sohn T-K, Bae M-H, Yoo M-A, Song EJ, Lee K-J, Kim K-W. Regulation and destabilization of HIF-1α by ARD1-mediated acetylation. Cell. 2002;111:709–20.CrossRefPubMed

78.

Jeong W, Rapisarda A, Park SR, Kinders RJ, Chen A, Melillo G, Turkbey B, Steinberg SM, Choyke P, Doroshow JH, Kummar S. Pilot trial of EZN-2968, an antisense oligonucleotide inhibitor of hypoxia-inducible factor-1 alpha (HIF-1α), in patients with refractory solid tumors. Cancer Chemother Pharmacol. 2014;73:343–8. https://doi.org/10.1007/s00280-013-2362-z.CrossRefPubMed

79.

Jones DT, Harris AL. Identification of novel small-molecule inhibitors of hypoxia-inducible factor-1 transactivation and DNA binding. Mol Cancer Ther. 2006;5:2193–202. https://doi.org/10.1158/1535-7163.MCT-05-0443.CrossRefPubMed

80.

Jung G-S, Jeon J-H, Choi Y-K, Jang SY, Park SY, Kim S-W, Byun J-K, Kim M-K, Lee S, Shin E-C, Lee I-K, Kang YN, Park K-G. Pyruvate dehydrogenase kinase regulates hepatitis C virus replication. Sci Rep. 2016;6:30846–13. https://doi.org/10.1038/srep30846.CrossRefPubMedPubMedCentral

81.

Kang F-W, Que L, Wu M, Wang Z-L, Sun J. Effects of trichostatin a on HIF-1α and VEGF expression in human tongue squamous cell carcinoma cells in vitro. Oncol Rep. 2012;28:193–9. https://doi.org/10.3892/or.2012.1784.CrossRefPubMed

82.

Kenneth NS, Mudie S, van Uden P, Rocha S. SWI/SNF regulates the cellular response to hypoxia. J Biol Chem. 2009;284:4123–31. https://doi.org/10.1074/jbc.M808491200.CrossRefPubMed

83.

Kessler J, Hahnel A, Wichmann H, Rot S, Kappler M, Bache M, Vordermark D. HIF-1α inhibition by siRNA or chetomin in human malignant glioma cells: effects on hypoxic radioresistance and monitoring via CA9 expression. BMC Cancer 2008. 2010;10:605. https://doi.org/10.1186/1471-2407-10-605.CrossRefPubMedPubMedCentral

84.

Kilani MM, Mohammed KA, Nasreen N, Tepper RS, Antony VB. RSV causes HIF-1α stabilization via NO release in primary bronchial epithelial cells. Inflammation. 2004;28:245–51.CrossRefPubMed

85.

Kim BS, Lee K, Jung HJ, Bhattarai D, Kwon HJ. HIF-1α suppressing small molecule, LW6, inhibits cancer cell growth by binding to calcineurin b homologous protein 1. Biochem Biophys Res Commun. 2015;458:14–20. https://doi.org/10.1016/j.bbrc.2015.01.031.CrossRefPubMed

86.

Kimura H, Weisz A, Kurashima Y, Hashimoto K, Ogura T, D'Acquisto F, Addeo R, Makuuchi M, Esumi H. Hypoxia response element of the human vascular endothelial growth factor gene mediates transcriptional regulation by nitric oxide: control of hypoxia-inducible factor-1 activity by nitric oxide. Blood. 2000;95:189–97.CrossRefPubMed

87.

Kimura H, Weisz A, Ogura T, Hitomi Y, Kurashima Y, Hashimoto K, D'Acquisto F, Makuuchi M, Esumi H. Identification of hypoxia-inducible factor 1 ancillary sequence and its function in vascular endothelial growth factor gene induction by hypoxia and nitric oxide. J Biol Chem. 2001;276:2292–8. https://doi.org/10.1074/jbc.M008398200.CrossRefPubMed

88.

Koh MY, Spivak-Kroizman T, Venturini S, Welsh S, Williams RR, Kirkpatrick DL, Powis G. Molecular mechanisms for the activity of PX-478, an antitumor inhibitor of the hypoxia-inducible factor-1alpha. Mol Cancer Ther. 2008;7:90–100. https://doi.org/10.1158/1535-7163.MCT-07-0463.CrossRefPubMed

89.

Kondo S, Seo SY, Yoshizaki T, Wakisaka N, Furukawa M, Joab I, Jang KL, Pagano JS. EBV latent membrane protein 1 up-regulates hypoxia-inducible factor 1alpha through Siah1-mediated down-regulation of prolyl hydroxylases 1 and 3 in nasopharyngeal epithelial cells. Cancer Res. 2006;66:9870–7. https://doi.org/10.1158/0008-5472.CAN-06-1679.CrossRefPubMed

90.

Kraus RJ, Yu X, Cordes B-LA, Sathiamoorthi S, Iempridee T, Nawandar DM, Ma S, Romero-Masters JC, McChesney KG, Lin Z, Makielski KR, Lee DL, Lambert PF, Johannsen EC, Kenney SC, Mertz JE. Hypoxia-inducible factor-1α plays roles in Epstein-Barr virus's natural life cycle and tumorigenesis by inducing lytic infection through direct binding to the immediate-early BZLF1 gene promoter. PLoS Pathog. 2017;13:e1006404. https://doi.org/10.1371/journal.ppat.1006404.CrossRefPubMedPubMedCentral

91.

Lando D, Peet DJ, Gorman JJ, Whelan DA, Whitelaw ML, Bruick RK. FIH-1 is an asparaginyl hydroxylase enzyme that regulates the transcriptional activity of hypoxia-inducible factor. Genes Dev. 2002;16:1466–71. https://doi.org/10.1101/gad.991402.CrossRefPubMedPubMedCentral

92.

Law, R., Bukwirwa, H., 1999. The physiology of oxygen delivery. Update Anaesthesia.

93.

Le Q-T, Chen E, Salim A, Cao H, Kong CS, Whyte R, Donington J, Cannon W, Wakelee H, Tibshirani R, Mitchell JD, Richardson D, O'Byrne KJ, Koong AC, Giaccia AJ. An evaluation of tumor oxygenation and gene expression in patients with early stage non–small cell lung cancers. Clin Cancer Res. 2006;12:1507–14. https://doi.org/10.1158/1078-0432.CCR-05-2049.CrossRefPubMed

94.

Leary TS, Klinck JR, Hayman G, Friend P, Jamieson NV, Gupta AK. Measurement of liver tissue oxygenation after orthotopic liver transplantation using a multiparameter sensor. Anaesthesia. 2002;57:1128–33. https://doi.org/10.1046/j.1365-2044.2002.02782_5.x.CrossRefPubMed

95.

Lee JS, Kim Y, Bhin J, Shin H-JR, Nam HJ, Lee SH, Yoon J-B, Binda O, Gozani O, Hwang D, Baek SH. Hypoxia-induced methylation of a pontin chromatin remodeling factor. Proc Natl Acad Sci U S A. 2011;108:13510–5. https://doi.org/10.1073/pnas.1106106108.CrossRefPubMedPubMedCentral

96.

Liu L-P, Hu B-G, Ye C, Ho RLK, Chen GG, Lai PBS. HBx mutants differentially affect the activation of hypoxia-inducible factor-1α in hepatocellular carcinoma. Br J Cancer. 2014;110:1066–73. https://doi.org/10.1038/bjc.2013.787.CrossRefPubMed

97.

Luo W, Hu H, Chang R, Zhong J, Knabel M, O'Meally R, Cole RN, Pandey A, Semenza GL. Pyruvate kinase M2 is a PHD3-stimulated coactivator for hypoxia-inducible factor 1. Cell. 2011;145:732–44.CrossRefPubMedPubMedCentral

98.

Makino Y, Kanopka A, Wilson WJ, Tanaka H, Poellinger L. Inhibitory PAS domain protein (IPAS) is a hypoxia-inducible splicing variant of the hypoxia-inducible factor-3alpha locus. J Biol Chem. 2002;277:32405–8. https://doi.org/10.1074/jbc.C200328200.CrossRefPubMed

99.

Maynard MA, Qi H, Chung J, Lee EHL, Kondo Y, Hara S, Conaway RC, Conaway JW, Ohh M. Multiple splice variants of the human HIF-3 alpha locus are targets of the von Hippel-Lindau E3 ubiquitin ligase complex. J Biol Chem. 2003;278:11032–40. https://doi.org/10.1074/jbc.M208681200.CrossRefPubMed

100.

Mazzon M, Peters NE, Loenarz C, Krysztofinska EM, Ember SWJ, Ferguson BJ, Smith GL. A mechanism for induction of a hypoxic response by vaccinia virus. Proc Natl Acad Sci U S A. 2013;110:12444–9. https://doi.org/10.1073/pnas.1302140110.CrossRefPubMedPubMedCentral

101.

McNamee EN, Johnson DK, Homann D, Clambey ET. Hypoxia and hypoxia-inducible factors as regulators of T cell development, differentiation, and function. Immunol Res. 2013;55:58–70. https://doi.org/10.1007/s12026-012-8349-8.CrossRefPubMedPubMedCentral

102.

Meixensberger J, Dings J, Kuhnigk H, Roosen K. Studies of tissue PO2 in normal and pathological human brain cortex. Acta Neurochir Suppl (Wien). 1993;59:58–63. https://doi.org/10.1007/978-3-7091-9302-0_10.CrossRef

103.

Mills EL, Kelly B, Logan A, Costa ASH, Varma M, Bryant CE, Tourlomousis P, Däbritz JHM, Gottlieb E, Latorre I, Corr SC, McManus G, Ryan D, Jacobs HT, Szibor M, Xavier RJ, Braun T, Frezza C, Murphy MP, O'Neill LA. Succinate dehydrogenase supports metabolic repurposing of mitochondria to drive inflammatory macrophages. Cell. 2016;167:457–470.e13. https://doi.org/10.1016/j.cell.2016.08.064.CrossRefPubMedPubMedCentral

104.

Mimouna S, Gonçalvès D, Barnich N, Darfeuille-Michaud A, Hofman P, Vouret-Craviari V. Crohn disease-associated Escherichia coli promote gastrointestinal inflammatory disorders by activation of HIF-dependent responses. Gut Microbes. 2011;2:335–46. https://doi.org/10.4161/gmic.18771.CrossRefPubMed

105.

Mole DR, Blancher C, Copley RR, Pollard PJ, Gleadle JM, Ragoussis J, Ratcliffe PJ. Genome-wide association of hypoxia-inducible factor (HIF)-1alpha and HIF-2alpha DNA binding with expression profiling of hypoxia-inducible transcripts. J Biol Chem. 2009;284:16767–75. https://doi.org/10.1074/jbc.M901790200.CrossRefPubMedPubMedCentral

106.

Moon E-J, Jeong C-H, Jeong J-W, Kim KR, Yu D-Y, Murakami S, Kim CW, Kim K-W. Hepatitis B virus X protein induces angiogenesis by stabilizing hypoxia-inducible factor-1alpha. FASEB J. 2004;18:382–4. https://doi.org/10.1096/fj.03-0153fje.CrossRefPubMed

107.

Mottet D, Dumont V, Deccache Y, Demazy C, Ninane N, Raes M, Michiels C. Regulation of hypoxia-inducible factor-1alpha protein level during hypoxic conditions by the phosphatidylinositol 3-kinase/Akt/glycogen synthase kinase 3beta pathway in HepG2 cells. J Biol Chem. 2003;278:31277–85.CrossRefPubMed

108.

Muller M, Schück R, Erkens U, Sticher J, Haase C, Hempelmann G. Effects of lumbar peridural anesthesia on tissue pO2 of the large intestine in man. Anasthesiol Intensivmed Notfallmed Schmerzther. 1995;30:108–10. https://doi.org/10.1055/s-2007-996457.CrossRefPubMed

109.

Nasimuzzaman M et al. Hepatitis C virus stabilizes hypoxia-inducible factor 1α and stimulates the synthesis of vascular endothelial growth factor. J Virol. 2007;81(19):10249–57.

110.

Neckers L. Using natural product inhibitors to validate Hsp90 as a molecular target in cancer. Curr Top Med Chem. 2006;6:1163–71.CrossRefPubMed

111.

O'Neill LAJ, Kishton RJ, Rathmell J. A guide to immunometabolism for immunologists. Nat Rev Immunol. 2016;16:553–65. https://doi.org/10.1038/nri.2016.70.CrossRefPubMedPubMedCentral

112.

Onnis B, Rapisarda A, Melillo G. Development of HIF-1 inhibitors for cancer therapy. J Cell Mol Med. 2009;13:2780–6. https://doi.org/10.1111/j.1582-4934.2009.00876.x.CrossRefPubMedPubMedCentral

113.

Palazon A, Goldrath AW, Nizet V, Johnson RS. HIF transcription factors, inflammation, and immunity. Immunity. 2014;41:518–28. https://doi.org/10.1016/j.immuni.2014.09.008.CrossRefPubMedPubMedCentral

114.

Parmar K, Mauch P, Vergilio J-A, Sackstein R, Down JD. Distribution of hematopoietic stem cells in the bone marrow according to regional hypoxia. PNAS. 2007;104:5431–6. https://doi.org/10.1073/pnas.0701152104.CrossRefPubMedPubMedCentral

115.

Pasanen A, Heikkilä M, Rautavuoma K, Hirsilä M, Kivirikko KI, Myllyharju J. Hypoxia-inducible factor (HIF)-3α is subject to extensive alternative splicing in human tissues and cancer cells and is regulated by HIF-1 but not HIF-2. Int J Biochem Cell Biol. 2010;42:1189–200. https://doi.org/10.1016/j.biocel.2010.04.008.CrossRefPubMed

116.

Passalacqua KD, Lu J, Goodfellow I, Kolawole AO, Arche JR, Maddox RJ, Carnahan KE, O'Riordan MXD, Wobus CE. Glycolysis is an intrinsic factor for optimal replication of a Norovirus. MBio. 2019;10:609. https://doi.org/10.1128/mBio.02175-18.CrossRef

117.

Patnaik, A., Chiorean, E.G., Tolcher, A., Papadopoulos, K., Beeram, M., Kee, D., Waddell, M., Gilles, E., Buchbinder, A., 2009. EZN-2968, a novel hypoxia-inducible factor-1{alpha} (HIF-1{alpha}) messenger ribonucleic acid (mRNA) antagonist: results of a phase I, pharmacokinetic (PK), dose-escalation study of daily administration in patients (pts) with advanced malignancies. ASCO Meeting Abstracts 27, 2564.

118.

Pillet S, Le Guyader N, Hofer T, NguyenKhac F, Koken M, Aubin J-T, Fichelson S, Gassmann M, Morinet F. Hypoxia enhances human B19 erythrovirus gene expression in primary erythroid cells. Virology. 2004;327:1–7. https://doi.org/10.1016/j.virol.2004.06.020.CrossRefPubMed

119.

Pipiya T, Sauthoff H, Huang YQ, Chang B, Cheng J, Heitner S, Chen S, Rom WN, Hay JG. Hypoxia reduces adenoviral replication in cancer cells by downregulation of viral protein expression. Gene Ther. 2005;12:911–7. https://doi.org/10.1038/sj.gt.3302459.CrossRefPubMed

120.

Pittman RN. Regulation of tissue oxygenation. In: Colloquium Series on Integrated Systems Physiology: From Molecule to Function, vol. 3; 2011a. p. 1–100. https://doi.org/10.4199/C00029ED1V01Y201103ISP017.CrossRef

121.

Pittman RN. Oxygen gradients in the microcirculation. Acta Physiol (Oxf). 2011b;202:311–22. https://doi.org/10.1111/j.1748-1716.2010.02232.x.CrossRef

122.

Rathmell WK, Chmielecki C, Van Dyke T, Simon MC. Models of Von Hippel-Lindau tumor suppressor disease specific activity. J Clin Oncol. 2004;22:9553.CrossRef

123.

Ren L, Zhang W, Han P, Zhang J, Zhu Y, Meng X, Zhang J, Hu Y, Yi Z, Wang R. Influenza a virus (H1N1) triggers a hypoxic response by stabilizing hypoxia-inducible factor-1α via inhibition of proteasome. Virology. 2019;530:51–8. https://doi.org/10.1016/j.virol.2019.02.010.CrossRefPubMed

124.

Riedinger HJ, van Betteraey M, Probst H. Hypoxia blocks in vivo initiation of simian virus 40 replication at a stage preceding origin unwinding. J Virol. 1999;73:2243–52.CrossRefPubMedPubMedCentral

125.

Salceda S, Caro J. Hypoxia-inducible factor 1α (HIF-1α) protein is rapidly degraded by the ubiquitin-proteasome system under normoxic conditions its stabilization by hypoxia depends on redox-induced changes. J Biol Chem. 1997;272:22642–7. https://doi.org/10.1074/jbc.272.36.22642.CrossRefPubMed

126.

Santos SAD, de Andrade DR. HIF-1alpha and infectious diseases: a new frontier for the development of new therapies. Rev Inst Med Trop Sao Paulo. 2017;59:e92. https://doi.org/10.1590/S1678-9946201759092.CrossRefPubMedPubMedCentral

127.

Sapra P, Kraft P, Pastorino F, Ribatti D, Dumble M, Mehlig M, Wang M, Ponzoni M, Greenberger LM, Horak ID. Potent and sustained inhibition of HIF-1α and downstream genes by a polyethyleneglycol-SN38 conjugate, EZN-2208, results in anti-angiogenic effects. Angiogenesis. 2011;14:245–53. https://doi.org/10.1007/s10456-011-9209-1.CrossRefPubMedPubMedCentral

128.

Schödel J, Oikonomopoulos S, Ragoussis J, Pugh CW, Ratcliffe PJ, Mole DR. High-resolution genome-wide mapping of HIF-binding sites by ChIP-seq. Blood. 2011;117:e207–17. https://doi.org/10.1182/blood-2010-10-314427.CrossRefPubMedPubMedCentral

129.

Schurek HJ, Jost U, Baumgärtl H, Bertram H, Heckmann U. Evidence for a preglomerular oxygen diffusion shunt in rat renal cortex. Am J Phys. 1990;259:F910–5. https://doi.org/10.1152/ajprenal.1990.259.6.F910.CrossRef

130.

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. https://doi.org/10.1128/MCB.12.12.5447.CrossRefPubMedPubMedCentral

131.

Shalova IN, Lim JY, Chittezhath M, Zinkernagel AS, Beasley F, Hernández-Jiménez E, Toledano V, Cubillos-Zapata C, Rapisarda A, Chen J, Duan K, Yang H, Poidinger M, Melillo G, Nizet V, Arnalich F, López-Collazo E, Biswas SK. Human monocytes undergo functional re-programming during sepsis mediated by hypoxia-inducible factor-1α. Immunity. 2015;42:484–98. https://doi.org/10.1016/j.immuni.2015.02.001.CrossRefPubMed

132.

Shen BH, Hermiston TW. Effect of hypoxia on Ad5 infection, transgene expression and replication. Gene Ther. 2005;12:902–10. https://doi.org/10.1038/sj.gt.3302448.CrossRefPubMed

133.

Smallwood HS, Duan S, Morfouace M, Rezinciuc S, Shulkin BL, Shelat A, Zink EE, Milasta S, Bajracharya R, Oluwaseum AJ, Roussel MF, Green DR, Pasa-Tolic L, Thomas PG. Targeting metabolic reprogramming by influenza infection for therapeutic intervention. Cell Rep. 2017;19:1640–53. https://doi.org/10.1016/j.celrep.2017.04.039.CrossRefPubMedPubMedCentral

134.

Thaker SK, Ch'ng J, Christofk HR. Viral hijacking of cellular metabolism. BMC Biol. 2019;17:59. https://doi.org/10.1186/s12915-019-0678-9.CrossRefPubMedPubMedCentral

135.

Thompson AAR, Dickinson RS, Murphy F, Thomson JP, Marriott HM, Tavares A, Willson J, Williams L, Lewis A, Mirchandani A, Coelho S, Dos P, Doherty C, Ryan E, Watts E, Morton NM, Forbes S, Stimson RH, Hameed AG, Arnold N, Preston JA, Lawrie A, Finisguerra V, Mazzone M, Sadiku P, Goveia J, Taverna F, Carmeliet P, Foster SJ, Chilvers ER, Cowburn AS, Dockrell DH, Johnson RS, Meehan RR, Whyte MKB, Walmsley SR. Hypoxia determines survival outcomes of bacterial infection through HIF-1alpha dependent re-programming of leukocyte metabolism. Sci Immunol. 2017;2:eaal2861. https://doi.org/10.1126/sciimmunol.aal2861.CrossRefPubMedPubMedCentral

136.

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. https://doi.org/10.1101/gad.11.1.72.CrossRefPubMed

137.

Torre C, Perret C, Colnot S. Molecular determinants of liver zonation. Prog Mol Biol Transl Sci. 2010;97:127–50. https://doi.org/10.1016/B978-0-12-385233-5.00005-2.CrossRefPubMed

138.

Vandamme T et al. Long-term acquired everolimus resistance in pancreatic neuroendocrine tumours can be overcome with novel PI3K-AKT-mTOR inhibitors. Br J Cancer. 2016;114(6):650–58.

139.

Vassilaki N, Kalliampakou KI, Kotta-Loizou I, Befani C, Liakos P, Simos G, Mentis AF, Kalliaropoulos A, Doumba PP, Smirlis D, Foka P, Bauhofer O, Poenisch M, Windisch MP, Lee ME, Koskinas J, Bartenschlager R, Mavromara P. Low oxygen tension enhances hepatitis C virus replication. J Virol. 2013;87:2935–48. https://doi.org/10.1128/JVI.02534-12.CrossRefPubMedPubMedCentral

140.

Veeranna RP, Haque M, Davis DA, Yang M, Yarchoan R. Kaposi's sarcoma-associated herpesvirus latency-associated nuclear antigen induction by hypoxia and hypoxia-inducible factors. J Virol. 2012;86:1097–108. https://doi.org/10.1128/JVI.05167-11.CrossRefPubMedPubMedCentral

141.

Wakisaka N, Kondo S, Yoshizaki T, Murono S, Furukawa M, Pagano JS. Epstein-Barr virus latent membrane protein 1 induces synthesis of hypoxia-inducible factor 1 alpha. Mol Cell Biol. 2004;24:5223–34. https://doi.org/10.1128/MCB.24.12.5223-5234.2004.CrossRefPubMedPubMedCentral

142.

Walmsley SR, Print C, Farahi N, Peyssonnaux C, Johnson RS, Cramer T, Sobolewski A, Condliffe AM, Cowburn AS, Johnson N, Chilvers ER. Hypoxia-induced neutrophil survival is mediated by HIF-1α–dependent NF-κB activity. J Exp Med. 2005;201:105–15. https://doi.org/10.1084/jem.20040624.CrossRefPubMedPubMedCentral

143.

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. PNAS. 1995;92:5510–4.CrossRefPubMedPubMedCentral

144.

Wang GL, Semenza GL. Purification and characterization of hypoxia-inducible factor 1. J Biol Chem. 1995;270:1230–7. https://doi.org/10.1074/jbc.270.3.1230.CrossRefPubMed

145.

Wang GL, Semenza GL. General involvement of hypoxia-inducible factor 1 in transcriptional response to hypoxia. PNAS. 1993;90:4304–8. https://doi.org/10.1073/pnas.90.9.4304.CrossRefPubMedPubMedCentral

146.

Wang TT, Sewatanon J, Memoli MJ, Wrammert J, Bournazos S, Bhaumik SK, Pinsky BA, Chokephaibulkit K, Onlamoon N, Pattanapanyasat K, Taubenberger JK, Ahmed R, Ravetch JV. IgG antibodies to dengue enhanced for FcγRIIIA binding determine disease severity. Science. 2017;355:395–8. https://doi.org/10.1126/science.aai8128.CrossRefPubMedPubMedCentral

147.

Wang W, Winlove CP, Michel CC. Oxygen partial pressure in outer layers of skin of human finger nail folds. J Physiol Lond. 2003;549:855–63. https://doi.org/10.1113/jphysiol.2002.037994.CrossRefPubMedPubMedCentral

148.

Xia X, Kung AL. Preferential binding of HIF-1 to transcriptionally active loci determines cell-type specific response to hypoxia. Genome Biol. 2009;10:R113. https://doi.org/10.1186/gb-2009-10-10-r113.CrossRefPubMedPubMedCentral

149.

Xu D, Yao Y, Lu L, Costa M, Dai W. Plk3 functions as an essential component of the hypoxia regulatory pathway by direct phosphorylation of HIF-1alpha. J Biol Chem. 2010;285:38944–50. https://doi.org/10.1074/jbc.M110.160325.CrossRefPubMedPubMedCentral

150.

Yamamoto M, Curiel DT. Current issues and future directions of oncolytic adenoviruses. Mol Ther. 2010;18:243–50. https://doi.org/10.1038/mt.2009.266.CrossRefPubMed

151.

Yasinska IM, Sumbayev VV. S-nitrosation of Cys-800 of HIF-1α protein activates its interaction with p300 and stimulates its transcriptional activity. FEBS Lett. 2003;549:105–9. https://doi.org/10.1016/S0014-5793(03)00807-X.CrossRefPubMed

152.

Yogev O, Lagos D, Enver T, Boshoff C. Kaposi's sarcoma herpesvirus microRNAs induce metabolic transformation of infected cells. PLoS Pathog. 2014;10(9):e1004400. https://doi.org/10.1371/journal.ppat.1004400.

153.

Yoo Y-G, Oh SH, Park ES, Cho H, Lee N, Park H, Kim DK, Yu D-Y, Seong JK, Lee M-O. Hepatitis B virus X protein enhances transcriptional activity of hypoxia-inducible factor-1alpha through activation of mitogen-activated protein kinase pathway. J Biol Chem. 2003;278:39076–84. https://doi.org/10.1074/jbc.M305101200.CrossRefPubMed

154.

Young RM, Wang SJ, Gordan JD, Ji X, Liebhaber SA, Simon MC. Hypoxia-mediated selective mRNA translation by an internal ribosome entry site-independent mechanism. J Biol Chem. 2008;283:16309–19. https://doi.org/10.1074/jbc.M710079200.CrossRefPubMedPubMedCentral

155.

Zeng L, Zhou H-Y, Tang N-N, Zhang W-F, He G-J, Hao B, Feng Y-D, Zhu H. Wortmannin influences hypoxia-inducible factor-1 alpha expression and glycolysis in esophageal carcinoma cells. World J Gastroenterol. 2016;22:4868–80. https://doi.org/10.3748/wjg.v22.i20.4868.CrossRefPubMedPubMedCentral

156.

Zhang H, Qian DZ, Tan YS, Lee K, Gao P, Ren YR, Rey S, Hammers H, Chang D, Pili R, Dang CV, Liu JO, Semenza GL. Digoxin and other cardiac glycosides inhibit HIF-1alpha synthesis and block tumor growth. Proc Natl Acad Sci U S A. 2008;105:19579–86. https://doi.org/10.1073/pnas.0809763105.CrossRefPubMedPubMedCentral

157.

Zhou X, Chen J, Yi G, Deng M, Liu H, Liang M, Shi B, Fu X, Chen Y, Chen L, He Z, Wang J, Liu J. Metformin suppresses hypoxia-induced stabilization of HIF-1α through reprogramming of oxygen metabolism in hepatocellular carcinoma. Oncotarget. 2016;7:873–84. https://doi.org/10.18632/oncotarget.6418.CrossRefPubMed

Title: Oxygen: viral friend or foe?
Authors: Esther Shuyi Gan
Eng Eong Ooi
Publication date: 01-12-2020
Publisher: BioMed Central
Keywords: Dengue Virus
Kaposi's Sarcoma-Associated Herpesvirus
Published in: Virology Journal / Issue 1/2020
Electronic ISSN: 1743-422X
DOI: https://doi.org/10.1186/s12985-020-01374-2

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