Interaction of the human cytomegalovirus particle with the host cell induces hypoxia-inducible factor 1 alpha

Virology

Volumn 414, Issue 1, 2011, Pages 83-90

  McFarlane, Steven ^a   Nicholl, Mary Jane ^a   Sutherland, Jane S ^a   Preston, Chris M ^a  

^a MRC UNIVERSITY OF GLASGOW CENTRE FOR VIRUS RESEARCH   (United Kingdom)

Author keywords

Akt; ATM kinase; Cell signaling pathways; Human cytomegalovirus; Hypoxia inducible factor

Indexed keywords

GENE PRODUCT; HYPOXIA INDUCIBLE FACTOR 1ALPHA; PROTEIN KINASE B; RNA;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYME PHOSPHORYLATION; FETUS; GENE EXPRESSION REGULATION; HUMAN; HUMAN CELL; HUMAN CYTOMEGALOVIRUS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN FUNCTION; PROTEIN INDUCTION; SIGNAL TRANSDUCTION; SKIN FIBROBLAST; TRANSCRIPTION INITIATION; ULTRAVIOLET IRRADIATION; VIRION; VIRUS CELL INTERACTION; VIRUS GENE; VIRUS PARTICLE;

CELLS, CULTURED; CYTOMEGALOVIRUS; FIBROBLASTS; HOST-PATHOGEN INTERACTIONS; HUMANS; HYPOXIA-INDUCIBLE FACTOR 1, ALPHA SUBUNIT; RNA, MESSENGER; TRANSCRIPTIONAL ACTIVATION; VIRUS ATTACHMENT;

HUMAN HERPESVIRUS 5;

EID: 79955541111     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2011.03.005     Document Type: Article

References (81)

1. Abate D., Watanabe S., Mocarski E.S. Major human cytomegalovirus structural protein pp65 (ppUL830) prevents interferon response factor 3 activation in the interferon response. J. Virol. 2004, 78:10995-11006.
2. Alessi D.R., Cohen P. Mechanism of activation and function of protein kinase B. Currrent Opin. Genet. Dev. 1998, 8:55-62.
3. Bahaskar P.T., Hay N. The two TORCS and Akt. Dev. Cell 2007, 12:487-502.
4. Bai X., Jiang Y. Key factors in mTOR regulation. Cell. Mol. Life Sci. 2010, 67:239-253.
5. Bentz G.L., Yurochko A.D. Human CMV infection of endothelial cells induces an angiogenic response through viral binding to EGF receptor and β1 and β2 integrins. Proc. Natl Acad. Sci. U.S.A. 2008, 105:5531-5536.
6. Boehme K.A., Kulikov R., Blattner C. p53 stabilization in response to DNA damage requires Akt/PKB αand DNA-PK. Proc. Natl Acad. Sci. U.S.A. 2008, 105:7785-7790.
7. Boehme K.W., Guerrero M., Compton T. Human cytomegalovirus envelope glycoproteins B and H are necessary for TLR2 activation in permissive cells. J. Immunol. 2006, 177:7094-7102.
8. Boehme K.W., Singh J., Perry S.T., Compton T. Human cytomegalovirus elicits a coordinated cellular antiviral response via envelope glycoprotein B. J. Virol. 2004, 78:1201-1211.
9. Bozulic L., Hemmings B.A. PIKKing on PKB α regulation of PKB αactivity by phosphorylation. Curr. Opin. Cell Biol. 2009, 21:256-261.
10. Bozulic L., Surucu B., Hynx D., Hemmings B.A. PKB α/Akt1 acts downstream of DNA-PK in the DNA double-strand break response and promotes survival. Mol. Cell 2008, 30:203-213.
11. Bresnahan W.A., Shenk T. A subset of viral transcripts packaged within human cytomegalovirus particles. Science 2000, 288:2373-2376.
12. Browne E.P., Wing B., Coleman D., Shenk T. Altered cellular mRNA levels in human cytomegalovirus-infected fibroblasts: viral block to the accumulation of antiviral mRNAs. J. Virol. 2001, 75:12319-12330.
13. Bruick R.K. Oxygen sensing in the hypoxic response pathway: regulation of the hypoxia-inducible factor. Genes Dev. 2008, 17:2614-2623.
14. Cai Q., Lan k., Verma S.C., Si H., Lin D., Robertson E.S. 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. 2006, 80:7965-7975.
15. Caposio P., Dreano M., Garotta G., Gribaudo G., Landolfo S. Human cytomegalovirus stimulates cellular IKK2 activity and requires the enzyme for productive infection. J. Virol. 2004, 78:3190-3195.
16. Chan G., Bivins-Smith E.R., Smith M.S., Smith P.M., Yurochko A.D. Transcriptome analysis reveals human cytomegalovirus reprograms monocyte differentiation toward an M1 macrophage. J. Immunol. 2008, 181:698-711.
17. Chan G., Nogalski M.T., Bentz G.L., Smith M.S., Parmater A., Yurochko A.D. PI3K-dependent upregulation of Mcl-1 by human cytomegalovirus is mediated by epidermal growth factor receptor and inhibits apoptosis in short-lived monocytes. J. Immunol. 2010, 184:3213-3222.
18. Chen B.P.C., Uematsu N., Kobayashi J., Lerenthal Y., Krempler A., Yajima H., Lobrich M., Shiloh Y., Chen D.J. Ataxia telangiectasia mutated (ATM) is essential for DNA-PKcs phosphorylation at the Thr-2609 cluster upon DNA double strand break. J. Biol. Chem. 2007, 282:6582-6587.
19. DeFilippis V.R., Alvarado D., Sali T., Rothenburg S., Fruh K.J. Human cytomegalovirus induces the interferon response via the DNA sensor ZBP. J. Virol. 2010, 84:585-598.
20. DeMeritt I.B., Milford L.E., Yurochko A.D. Activation of the NF-κ B pathway in human cytomegalovirus-infected cells is necessary for efficient transactivation of the major immediate-early promoter. J. Virol. 2004, 78:4498-4507.
21. Dery M.C., Michaud M.D., Richard D.E. Hypoxia-inducible factor 1: regulation by hypoxic and non-hypoxic activators. Int. J. Biochem. Cell Biol. 2005, 37:535-540.
22. Deshmane S.L., Mukerjee R., Fan S., Valle L.D., Michiels C., Sweet T., Rom I., Khalili K., Rappaport J., Amini S., Sawaya B.E. Activation of the oxidative stress pathway by HIV-1 Vpr leads to induction of hypoxia-inducible factor 1α expression. J. Biol. Chem. 2009, 284:11364-11373.
23. Dolan A., Cunningham C., Hector R.D., Hassan-Walker A.F., Lee L., Addison C., Dargan D.J., McGeoch D.J., Gatherer D., Emery V.C., Griffiths P.D., Sinzger C., McSharry B.P., Wilkinson G.W.G., Davison A.J. Genetic content of wild-type human cytomegalovirus. J. Gen. Virol. 2004, 85:1301-1312.
24. Engelman J.A., Luo J., Cantley L.C. The evolution of phosphatidylinositol 3-kinases as regulators of growth and metabolism. Nat. Rev. Genet. 2006, 7:606-619.
25. Feng J., Park J., Cron P., Hess D., Hemmings B.A. Identification of a PKB αAkt hydrophobic motif Ser-473 kinase as DNA-dependent protein kinase. J. Biol. Chem. 2004, 279:41189-41196.
26. Fortunato E.A., Dell'Aquila M.L., Spector D.H. Specific chromosome 1 breaks induced by human cytomegalovirus. Proc. Natl Acad. Sci. U.S.A. 2000, 97:853-858.
27. Frede S., Stockmann C., Freitag P., Fandrey J. Bacterial lipopolysaccharide induces HIF-1αactivation in human monocytes via p44/42 MAPK and NF-κ B. Biochem. J. 2006, 396:517-527.
28. Fukuda R., Hirota K., Fan F., Jung Y.D., Ellis L.M., Semenza G.L. Insulin-like growth factor 1 induces hypoxia-inducible factor 1-mediated vascular endothelial growth factor expression, which is dependent on MAP kinase and phosphatidylinositol 3-kinase signaling in colon cancer cells. J. Biol. Chem. 2002, 277:38205-38211.
29. Greijer A.E., Dekkers C.A.J., Middledrop J.M. Human cytomegalovirus virions differentially incorporate viral and host cell RNA during the assembly process. J. Virol. 2000, 74:9078-9082.
30. Hellwig-Burgel T., Stiehl D.P., Wagner A.E., Metzen E., Jelkmann W. Hypoxia-inducible factor-1 (HIF): a novel transcription factor in immune reactions. J. Interferon Cytokine Res. 2005, 25:297-310.
31. Hertel L., Mocarski E.S. Global analysis of host cell gene expression late during cytomegalovirus infection reveals extensive dysregulation of cell cycle gene expression and induction of pseudomitosis independent of US28 function. J. Virol. 2004, 78:11988-12011.
32. Hickson I., Zhao Y., Richardson C.J., Green S.J., Martin N.M.B., Orr A.I., Reaper P.M., Jackson S.P., Curtin N.J., Smith G.C.M. Identification and characterization of a novel and specific inhibitor of the ataxia-telangiectasia mutated kinase ATM. Cancer Res. 2004, 64:9152-9159.
33. Hotamisligil G.S., Erbay E. Nutrient sensing and inflammation in metabolic diseases. Nat. Rev. Immunol. 2008, 8:923-934.
34. Johnson R.A., Wang X., Ma X.L., Huong S.M., Huang E.S. Human cytomegalovirus up-regulates the phosphatidylinositol 3-kinase (PI3-K) pathway: inhibition of PI3-K activity inhibits viral replication and virus-induced signaling. J. Virol. 2001, 75:6022-6032.
35. Juckem L.K., Boehme K.W., Feire A.L., Compton T. Differential initiation of innate immune responses induced by human cytomegalovirus entry into fibroblast cells. J. Immunol. 2008, 180:4965-4977.
36. Kenzelmann M., Muhlemann K. Transcriptome analysis of fibroblast cells immediate-early after human cytomegalovirus infection. J. Mol. Biol. 2000, 304:741-751.
37. Kilani M.M., Mohammad K.A., Nasreen N., Tepper R.S., Antony V.B. RSV causes HIF1α stabilization via NO release in primary bronchial epithelial cells. Inflammation 2004, 28:245-251.
38. Knight Z.A., Gonzalez B., Feldman M.E., Zunder E.R., Goldenberg D.D., Williams O., Loweith R., Stokoe D., Balla A., Toth B., Balla T., Weiss W.A., Williams R.L., Shokat K.M. A pharmacological map of the PI3-K family defines a role for p110α in insulin signaling. Cell. Mol. Life Sci. 2006, 125:733-747.
39. Kowalik T.F., Wing B., Haskill J.S., Baldwin A.S., Huang E.S. Multiple mechanisms are implicated in the regulation of NF-κ B activity during human cytomegalovirus infection. Proc. Natl Acad. Sci. U.S.A. 1993, 90:1107-1111.
40. Kudchodkar S.B., Yu Y., Maguire T.G., Alwine J.C. Human cytomegalovirus infection induces rapamycin-insensitive phosphorylation of downstream effectors of mTOR kinase. J. Virol. 2004, 78:11030-11039.
41. Kudchodkar S.B., Yu Y., Maguire T.G., Alwine J.C. Human cytomegalovirus infection alters the substrate specificities and rapamycin sensitivities of raptor- and rictor-containing complexes. Proc. Natl Acad. Sci. U.S.A. 2006, 103:14182-14187.
42. Laughner E., Taghavi P., Chiles K., Mahon P.C., Semenza G.L. HER2 (neu) signaling increases the rate of hypoxia-inducible factor 1β (HIF-1α) synthesis: novel mechanism for HIF-1αmediated vascular endothelial growth factor expression. Mol. Cell. Biol. 2001, 21:3995-4004.
43. Li Y., Inoki K., Vacratsis P., Guan K.L. The p38 and MK2 kinase cascade phosphorylates tuberin, the tuberous sclerosis 2 gene product, and enhances its interaction with 14-3-3. J. Biol. Chem. 2003, 278:13663-13671.
44. Lukashchuk V., McFarlane S., Everett R.D., Preston C.M. Human cytomegalovirus protein pp71 displaces the chromatin-associated factor ATRX from nuclear domain 10 at early stages of infection. J. Virol. 2008, 82:12543-12554.
45. Luo M.H., Rosenke K., Czornak K., Fortunato E.A. Human cytomegalovirus disrupts both ataxia telangiectasia mutated protein (ATM) and ATM-Rad3-related kinase-mediated DNA damage response during lytic infection. J. Virol. 2007, 81:1934-1950.
46. Marshall K.R., Rowley K.V., Rinaldi A., Nicholson I.P., Ishov A.M., Maul G.G., Preston C.M. Activity and intracellular localization of the human cytomegalovirus protein pp71. J. Gen. Virol. 2002, 83:1601-1612.
47. Moin S.M., Chandra V., Arya R., Jameel S. The hepatitis E virus ORF3 protein stabilizes HIF-1α and enhances HIF-mediated transcriptional activity through p300/CBP. Cell. Microbiol. 2009, 11:1409-1421.
48. Moorman N.J., Cristea I.M., Terhune S.S., Rout M.P., Chait B.T., Shenk T. Human cytomegalovirus protein UL38 inhibits host cell stress responses by antagonizing the tuberous sclerosis protein complex. Cell Host Microbe 2008, 3:253-262.
49. Moorman N.J., Shenk T. Rapamycin-resistant mTORC1 kinase activity is required for herpesvirus replication. J. Virol. 2010, 84:5260-5269.
50. Nasimuzzaman M., Waris G., Mikolon D., Stupack D.G., Siddiqui A. Hepatitis C virus stabilizes hypoxia-inducible factor 1a and stimulates the synthesis of vascular endothelial growth factor. J. Virol. 2007, 81:10249-10257.
51. Navarro L., Mowen K., Rodems S., Weaver B., Reich N., Spector D., David M. Cytomegalovirus activates interferon immediate-early response gene expression and an interferon regulatory factor 3-containing interferon response element-binding complex. Mol. Cell. Biol. 1998, 18:3796-3802.
52. Netterwald J.R., Jones T.R., Britt W.J., Yang S.J., McCrone I.P., Zhu H. Postattachment events associated with viral entry are necessary for induction of interferon-stimulated genes by human cytomegalovirus. J. Virol. 2004, 78:6688-6691.
53. Noyce R.S., Collins S.E., Mossman K.L. Differential modification of interferon regulatory factor 3 following virus particle entry. J. Virol. 2009, 83:4013-4022.
54. Page E.L., Robitaille G.A., Pouyssegur J., Richard D.E. Induction of hypoxia-inducible factor-1α by transcriptional and translational mechanisms. J. Biol. Chem. 2002, 277:48403-48409.
55. Paladino P., Cummings D.T., Noyce R.S., Mossman K.L. The IFN-independent response to virus particle entry provides a first line of antiviral defense that is independent of TLRs and retinoic acid-inducible gene I. J. Immunol. 2006, 177:8008-8016.
56. Preston C.M., Harman A.N., Nicholl M.J. Activation of interferon response factor-3 in human cells infected with herpes simplex virus type 1 or human cytomegalovirus. J. Virol. 2001, 75:8909-8916.
57. Qutub A.A., Popel A.S. Reactive oxygen species regulate hypoxia-inducible factor 1α differentially in cancer and ischemia. Mol. Cell. Biol. 2008, 28:5106-5119.
58. Reiling J.H., Sabatini D.M. Stress and mTORture signaling. Oncogene 2006, 25:6373-6383.
59. Ripoli M., D'Aprile A.D., Quarato G., Sarasin-Filipwicz M., Gouttenoure J., Scrima R., Cela O., Boffoli D., Heim M.H., Moradpour D., Capitanio N., Piccoli C. Hepatitis C virus-linked mitochondrial dysfunction promotes hypoxia-inducible factor 1α-mediated glycolytic adaptation. J. Virol. 2010, 84:647-660.
60. Rius J., Guma M., Schachtrup C., Akassoglou K., Zinkernagel A.S., Nizet V., Johnson R.S., Haddad G.G., Karin M. NF-κ B links innate immunity to the hypoxic response through transcriptional regulation of HIF-1α. Nature 2008, 453:807-811.
61. Rodriguez J.E., Loepfe T.R., Swack N.S. Beta interferon production in primed and unprimed cells infected with human cytomegalovirus. Arch. Virol. 1987, 94:177-189.
62. Sambucetti L.C., Cherrington J.M., Wilkinson G.W.G., Mocarski E.S. NF-Kappa-B activation of the cytomegalo-virus enhancer is mediated by a viral transactivator and by T-cell stimulation. EMBO J. 1989, 8:4251-4258.
63. Semenza G.L. Hypoxia-inducible factor 1: master regulator of O2 homeostasis. Curr. Opin. Genet. Dev. 1998, 8:588-594.
64. Semenza G.L. Hypoxia-inducible factor 1: oxygen homeostasis and disease pathophysiology. Trends Mol. Med. 2001, 7:345-350.
65. Shaw R.J., Cantley L.C. Ras, PI(3)K and mTOR signaling controls tumor cell growth. Nat. Immunol. 2006, 441:424-430.
66. Shin Y.C., Joo C.H., Gack M.U., Lee H.R., Jung J.U. Kaposi's sarcoma-associated herpesvirus viral IFN regulatory factor 3 stabilizes hypoxia-inducible factor-1α to induce vascular endothelial growth factor expression. Cancer Res. 2008, 68:1751-1759.
67. Stanton R.J., McSharry B.P., Rickards C.R., Wang E.C.Y., Tomasec P., Wilkinson G.W.G. Cytomegalovirus destruction of focal adhesions revealed in a high-throughput western blot analysis of cellular protein expression. J. Virol. 2007, 81:7860-7872.
68. Talbot P., Almeida J.D. Human cytomegalovirus: purification of enveloped virions and dense bodies. J. Gen. Virol. 1977, 36:345-349.
69. Taylor R.T., Bresnahan W.A. Human cytomegalovirus immediate-early 2 gene expression blocks virus-induced beta interferon production. J. Virol. 2005, 79:3873-3877.
70. van Uden l.P., Kenneth N.S., Rocha S. Regulation of hypoxia-inducible factor-1α by NF-κ B. Biochem. J. 2008, 412:477-484.
71. Varnum S.M., Streblow D.N., Monroe M.E., Smith P., Auberry K.J., Pasa-Tolic L., Wang D., Camp D.G., Rodland K., Wiley S., Britt W., Shenk T., Smith R.D., Nelson J.A. Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J. Virol. 2004, 78:10960-10966.
72. Wakisaka N., Kondo S., Yoshizaki T., Murono S., Furukawa M., Pagano J.S. Epstein-Barr virus latent membrane protein 1 induces synthesis of hypoxia-inducible factor 1α. Mol. Cell. Biol. 2004, 24:5223-5234.
73. Walmsley S.R., McGovern N.N., Whyte M.K.B., Chilvers E.R. The HIF/VHL pathway. Am. J. Respir. Cell Mol. Biol. 2007, 38:251-255.
74. Walsh D., Perez C., Notary J., Mohr I. Regulation of the translational initiation factor eIF4F by multiple mechanisms in human cytomegalovirus-infected cells. J. Virol. 2005, 79:8057-8064.
75. Wathen M.W., Stinski M.F. Temporal patterns of human cytomegalovirus transcription: mapping of the viral RNAs synthesized at immediate early, early, and late times after infection. J. Virol. 1982, 41:462-477.
76. Werth N., Beerlage C., Rosenberger C., Yazdi A.S., Edelmann M., Amr A., Bernhardt W., von Eiff C., Becker K., Schafer A., Peschel A., Kempf V.A.J. Activation of hypoxia inducible factor 1 is a general phenomenon in infections with human pathogens. PLoS ONE 2010, 5:e11576.
77. Yoo Y.G., Oh S.H., Park E.S., Cho H., Lee N., Park H., Kim D.K., Yu D.Y., Seong J.K., Lee M.O. 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, 278:39076-39084.
78. Yurochko A.D., Kowalik T.F., Huong S.M., Huang E.S. Human cytomegalovirus upregulates NF-κ B activity by transactivating the NF-κ B p105/p50 and p65 promoters. J. Virol. 1995, 69:5391-5400.
79. Zhu H., Cong J.P., Mamtora T., Gingeras T., Shenk T. Cellular gene expression altered by human cytomegalovirus: global monitoring with oligonucleotide arrays. Proc. Natl Acad. Sci. U.S.A. 1998, 95:14470-14475.
80. Zhu H., Cong J.P., Shenk T. Use of differential display analysis to assess the effect of human cytomegalovirus infection on the accumulation of cellular RNAs: induction of interferon-responsive RNAs. Proc. Natl Acad. Sci. U.S.A. 1997, 94:13985-13990.
81. Zinkernagel A.S., Johnson R.S., Nizet V. Hypoxia inducible factor (HIF) function in innate immunity and infection. J. Mol. Med. 2007, 85:1339-1346.