The US27 gene product of human cytomegalovirus enhances signaling of host chemokine receptor CXCR4

Virology

Volumn 439, Issue 2, 2013, Pages 122-131

  Arnolds, Kathleen L ^a   Lares, Angela P ^a   Spencer, Juliet V ^a  

^a UNIVERSITY OF SAN FRANCISCO   (United States)

Author keywords

Chemokine receptors; Chemokines; Cytomegalovirus; Immune modulation

Indexed keywords

CHEMOKINE RECEPTOR CXCR4; MESSENGER RNA; STROMAL CELL DERIVED FACTOR 1; STROMAL CELL DERIVED FACTOR 1ALPHA; VIRUS PROTEIN;

ARTICLE; CALCIUM MOBILIZATION; CALCIUM SIGNALING; CHEMOKINE RECEPTOR CXCR4 GENE; CHEMOTAXIS; CONTROLLED STUDY; CYTOMEGALOVIRUS; EMBRYO; FLOW CYTOMETRY; GENE EXPRESSION REGULATION; GENE PRODUCT; HUMAN; HUMAN CELL; IMMUNE RESPONSE GENE; IMMUNOFLUORESCENCE MICROSCOPY; IMMUNOMODULATION; LATENT VIRUS INFECTION; LIGAND BINDING; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; QUANTITATIVE ANALYSIS; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; US27 GENE; VIRUS GENE; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL LINE; CYTOMEGALOVIRUS; FLOW CYTOMETRY; GENE EXPRESSION PROFILING; HUMANS; MICROSCOPY, FLUORESCENCE; REAL-TIME POLYMERASE CHAIN REACTION; RECEPTORS, CHEMOKINE; RECEPTORS, CXCR4; SIGNAL TRANSDUCTION; VIRAL PROTEINS; VIRULENCE FACTORS;

CYTOMEGALOVIRUS; HERPESVIRIDAE; HUMAN HERPESVIRUS 5;

EID: 84875803599     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.02.006     Document Type: Article

References (54)

1. Babcock G.J., Farzan M., Sodroski J. Ligand-independent dimerization of CXCR4, a principal HIV-1 coreceptor. J. Biol. Chem. 2003, 278:3378-3385.
2. Beck S., Barrell B.G. Human cytomegalovirus encodes a glycoprotein homologous to MHC class-I antigens. Nature 1988, 331:269-272.
3. Billstrom M.A., Johnson G.L., Avdi N.J., Worthen G.S. Intracellular signaling by the chemokine receptor US28 during human cytomegalovirus infection. J. Virol. 1998, 72:5535-5544.
4. Bodaghi B., Jones T.R., Zipeto D., Vita C., Sun L., Laurent L., Arenzana-Seisdedos F., Virelizier J.L., Michelson S. Chemokine sequestration by viral chemoreceptors as a novel viral escape strategy: withdrawal of chemokines from the environment of cytomegalovirus-infected cells. J. Exp. Med. 1998, 188:855-866.
5. Burns J.M., Lewis G.K. Improved measurement of calcium mobilization by flow cytometry. Biotechniques 1997, 23(1022-1024):1026.
6. Busillo J.M., Armando S., Sengupta R., Meucci O., Bouvier M., Benovic J.L. Site-specific phosphorylation of CXCR4 is dynamically regulated by multiple kinases and results in differential modulation of CXCR4 signaling. J. Biol. Chem. 2010, 285:7805-7817.
7. Casarosa P., Bakker R.A., Verzijl D., Navis M., Timmerman H., Leurs R., Smit M.J. Constitutive signaling of the human cytomegalovirus-encoded chemokine receptor US28. J. Biol. Chem. 2001, 276:1133-1137.
8. Charo I.F., Ransohoff R.M. The many roles of chemokines and chemokine receptors in inflammation. N. Engl. J. Med. 2006, 354:610-621.
9. Chee M.S., Satchwell S.C., Preddie E., Weston K.M., Barrell B.G. Human cytomegalovirus encodes three G protein-coupled receptor homologues. Nature 1990, 344:774-777.
10. Fan G.H., Yang W., Sai J., Richmond A. Hsc/Hsp70 interacting protein (hip) associates with CXCR2 and regulates the receptor signaling and trafficking. J. Biol. Chem. 2002, 277:6590-6597.
11. Flanagan C.A. A GPCR that is not "DRY". Mol. Pharmacol. 2005, 68:1-3.
12. Fraile-Ramos A., Pelchen-Matthews A., Kledal T.N., Browne H., Schwartz T.W., Marsh M. Localization of HCMV UL33 and US27 in endocytic compartments and viral membranes. Traffic 2002, 3:218-232.
13. Frascaroli G., Varani S., Blankenhorn N., Pretsch R., Bacher M., Leng L., Bucala R., Landini M.P., Mertens T. Human cytomegalovirus paralyzes macrophage motility through down-regulation of chemokine receptors, reorganization of the cytoskeleton, and release of macrophage migration inhibitory factor. J. Immunol. 2009, 182:477-488.
14. Gao J.L., Murphy P.M. Human cytomegalovirus open reading frame US28 encodes a functional beta chemokine receptor. J. Biol. Chem. 1994, 269:28539-28542.
15. Gupta S.K., Lysko P.G., Pillarisetti K., Ohlstein E., Stadel J.M. Chemokine receptors in human endothelial cells. Functional expression of CXCR4 and its transcriptional regulation by inflammatory cytokines. J. Biol. Chem. 1998, 273:4282-4287.
16. Hendrix C.W., Collier A.C., Lederman M.M., Schols D., Pollard R.B., Brown S., Jackson J.B., Coombs R.W., Glesby M.J., Flexner C.W., Bridger G.J., Badel K., MacFarland R.T., Henson G.W., Calandra G. Safety, pharmacokinetics, and antiviral activity of AMD3100, a selective CXCR4 receptor inhibitor, in HIV-1 infection. J. Acquired Immune Defic. Syndr. 2004, 37:1253-1262.
17. Heydorn A., Sondergaard B.P., Ersboll B., Holst B., Nielsen F.C., Haft C.R., Whistler J., Schwartz T.W. A library of 7TM receptor C-terminal tails. Interactions with the proposed post-endocytic sorting proteins ERM-binding phosphoprotein 50 (EBP50), N-ethylmaleimide-sensitive factor (NSF), sorting nexin 1 (SNX1), and G protein-coupled receptor-associated sorting protein (GASP). J. Biol. Chem. 2004, 279:54291-54303.
18. Hoffmann F., Muller W., Schutz D., Penfold M.E., Wong Y.H., Schulz S., Stumm R. Rapid uptake and degradation of CXCL12 depend on CXCR7 Carboxyl-terminal serine/threonine residues. J. Biol. Chem. 2012, 287:28362-28377.
19. Holst P.J., Rosenkilde M.M. Microbiological exploitation of the chemokine system. Microbes Infect. 2003, 5:179-187.
20. Jackson S.E., Mason G.M., Wills M.R. Human cytomegalovirus immunity and immune evasion. Virus Res. 2011, 157:151-160.
21. Katritch V., Cherezov V., Stevens R.C. Diversity and modularity of G protein-coupled receptor structures. Trends Pharmacol. Sci. 2012, 33:17-27.
22. Kesson A.M., Kakakios A. Immunocompromised children: conditions and infectious agents. Paediatr. Respir. Rev. 2007, 8:231-239.
23. Kumar A., Kremer K.N., Dominguez D., Tadi M., Hedin K.E. Galpha13 and Rho mediate endosomal trafficking of CXCR4 into Rab11+ vesicles upon stromal cell-derived factor-1 stimulation. J. Immunol. 2011, 186:951-958.
24. Lam L.T., Pickeral O.K., Peng A.C., Rosenwald A., Hurt E.M., Giltnane J.M., Averett L.M., Zhao H., Davis R.E., Sathyamoorthy M., Wahl L.M., Harris E.D., Mikovits J.A., Monks A.P., Hollingshead M.G., Sausville E.A., Staudt L.M. Genomic-scale measurement of mRNA turnover and the mechanisms of action of the anti-cancer drug flavopiridol. Genome Biol. 2001, 2(10):0041-1-0041-11.
25. Levoye A., Balabanian K., Baleux F., Bachelerie F., Lagane B. CXCR7 heterodimerizes with CXCR4 and regulates CXCL12-mediated G protein signaling. Blood 2009, 113:6085-6093.
26. Luo C., Pan H., Mines M., Watson K., Zhang J., Fan G.H. CXCL12 induces tyrosine phosphorylation of cortactin, which plays a role in CXC chemokine receptor 4-mediated extracellular signal-regulated kinase activation and chemotaxis. J. Biol. Chem. 2006, 281:30081-30093.
27. Margulies B.J., Gibson W. The chemokine receptor homologue encoded by US27 of human cytomegalovirus is heavily glycosylated and is present in infected human foreskin fibroblasts and enveloped virus particles. Virus Res. 2007, 123:57-71.
28. McCormick A.L. Control of apoptosis by human cytomegalovirus. Curr. Top Microbiol. Immunol. 2008, 325:281-295.
29. Moriuchi H., Moriuchi M., Fauci A.S. Cloning and analysis of the promoter region of CCR5, a coreceptor for HIV-1 entry. J. Immunol. 1997, 159:5441-5449.
30. Moriuchi M., Moriuchi H., Margolis D.M., Fauci A.S. USF/c-Myc enhances, while Yin-Yang 1 suppresses, the promoter activity of CXCR4, a coreceptor for HIV-1 entry. J. Immunol. 1999, 162:5986-5992.
31. Neote K., DiGregorio D., Mak J.Y., Horuk R., Schall T.J. Molecular cloning, functional expression, and signaling characteristics of a C-C chemokine receptor. Cell 1993, 72:415-425.
32. Nijmeijer S., Leurs R., Smit M.J., Vischer H.F. The Epstein-Barr virus-encoded G protein-coupled receptor BILF1 hetero-oligomerizes with human CXCR4, scavenges Galphai proteins, and constitutively impairs CXCR4 functioning. J. Biol. Chem. 2010, 285:29632-29641.
33. O'Connor C.M., Shenk T. Human cytomegalovirus pUS27 G protein-coupled receptor homologue is required for efficient spread by the extracellular route but not for direct cell-to-cell spread. J. Virol. 2011, 85:3700-3707.
34. Orsini M.J., Parent J.L., Mundell S.J., Marchese A., Benovic J.L. Trafficking of the HIV coreceptor CXCR4. Role of arrestins and identification of residues in the c-terminal tail that mediate receptor internalization. J. Biol. Chem. 1999, 274:31076-31086.
35. Pleskoff O., Treboute C., Alizon M. The cytomegalovirus-encoded chemokine receptor US28 can enhance cell-cell fusion mediated by different viral proteins. J. Virol. 1998, 72:6389-6397.
36. Pleskoff O., Treboute C., Brelot A., Heveker N., Seman M., Alizon M. Identification of a chemokine receptor encoded by human cytomegalovirus as a cofactor for HIV-1 entry. Science 1997, 276:1874-1878.
37. Revello M.G., Campanini G., Piralla A., Furione M., Percivalle E., Zavattoni M., Gerna G. Molecular epidemiology of primary human cytomegalovirus infection in pregnant women and their families. J. Med. Virol. 2008, 80:1415-1425.
38. Rey M., Valenzuela-Fernandez A., Urzainqui A., Yanez-Mo M., Perez-Martinez M., Penela P., Mayor F., Sanchez-Madrid F. Myosin IIA is involved in the endocytosis of CXCR4 induced by SDF-1alpha. J. Cell Sci. 2007, 120:1126-1133.
39. See H.B., Seeber R.M., Kocan M., Eidne K.A., Pfleger K.D. Application of G protein-coupled receptor-heteromer identification technology to monitor beta-arrestin recruitment to G protein-coupled receptor heteromers. Assay Drug Dev. Technol. 2011, 9:21-30.
40. Sierra M.I., Wright M.H., Nash P.D. AMSH interacts with ESCRT-0 to regulate the stability and trafficking of CXCR4. J. Biol. Chem. 2010, 285:13990-14004.
41. Sohy D., Parmentier M., Springael J.Y. Allosteric transinhibition by specific antagonists in CCR2/CXCR4 heterodimers. J. Biol. Chem. 2007, 282:30062-30069.
42. Soroceanu L., Matlaf L., Bezrookove V., Harkins L., Martinez R., Greene M., Soteropoulos P., Cobbs C.S. Human cytomegalovirus US28 found in glioblastoma promotes an invasive and angiogenic phenotype. Cancer Res. 2011, 71:6643-6653.
43. Spencer J.V., Lockridge K.M., Barry P.A., Lin G., Tsang M., Penfold M.E., Schall T.J. Potent immunosuppressive activities of cytomegalovirus-encoded interleukin-10. J. Virol. 2002, 76:1285-1292.
44. Stapleton L.K., Arnolds K.L., Lares A.P., Devito T.M., Spencer J.V. Receptor chimeras demonstrate that the C-terminal domain of the human cytomegalovirus US27 gene product is necessary and sufficient for intracellular receptor localization. Virol. J. 2012, 9:42.
45. Streblow D.N., Soderberg-Naucler C., Vieira J., Smith P., Wakabayashi E., Ruchti F., Mattison K., Altschuler Y., Nelson J.A. The human cytomegalovirus chemokine receptor US28 mediates vascular smooth muscle cell migration. Cell 1999, 99:511-520.
46. Stropes M.P., Schneider O.D., Zagorski W.A., Miller J.L., Miller W.E. The carboxy-terminal tail of human cytomegalovirus (HCMV) US28 regulates both chemokine-independent and chemokine-dependent signaling in HCMV-infected cells. J. Virol. 2009, 83:10016-10027.
47. Tadagaki K., Tudor D., Gbahou F., Tschische P., Waldhoer M., Bomsel M., Jockers R., Kamal M. Human cytomegalovirus-encoded UL33 and UL78 heteromerize with host CCR5 and CXCR4 impairing their HIV coreceptor activity. Blood 2012, 119:4908-4918.
48. Tomasec P., Braud V.M., Rickards C., Powell M.B., McSharry B.P., Gadola S., Cerundolo V., Borysiewicz L.K., McMichael A.J., Wilkinson G.W. Surface expression of HLA-E, an inhibitor of natural killer cells, enhanced by human cytomegalovirus gpUL40. Science 2000, 287:1031.
49. Tschische P., Tadagaki K., Kamal M., Jockers R., Waldhoer M. Heteromerization of human cytomegalovirus encoded chemokine receptors. Biochem. Pharmacol. 2011, 82:610-619.
50. Vieira J., Schall T.J., Corey L., Geballe A.P. Functional analysis of the human cytomegalovirus US28 gene by insertion mutagenesis with the green fluorescent protein gene. J. Virol. 1998, 72:8158-8165.
51. Vila-Coro A.J., Rodriguez-Frade J.M., Martin De Ana A., Moreno-Ortiz M.C., Martinez A.C., Mellado M. The chemokine SDF-1alpha triggers CXCR4 receptor dimerization and activates the JAK/STAT pathway. Faseb J. 1999, 13:1699-1710.
52. Vischer H.F., Vink C., Smit M.J. A viral conspiracy: hijacking the chemokine system through virally encoded pirated chemokine receptors. Curr. Top. Microbiol. Immunol. 2006, 303:121-154.
53. Wegner S.A., Ehrenberg P.K., Chang G., Dayhoff D.E., Sleeker A.L., Michael N.L. Genomic organization and functional characterization of the chemokine receptor CXCR4, a major entry co-receptor for human immunodeficiency virus type 1. J. Biol. Chem. 1998, 273:4754-4760.
54. Zhang Y., Foudi A., Geay J.F., Berthebaud M., Buet D., Jarrier P., Jalil A., Vainchenker W., Louache F. Intracellular localization and constitutive endocytosis of CXCR4 in human CD34+ hematopoietic progenitor cells. Stem Cells 2004, 22:1015-1029.