US28 Is a Potent Activator of Phospholipase C during HCMV Infection of Clinically Relevant Target Cells

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Miller, William E ^a   Zagorski, William A ^a   Brenneman, Joanna D ^a   Avery, Diana ^a   Miller, Jeanette L C ^a   O'Connor, Christine M ^b  

^a UNIVERSITY OF CINCINNATI COLLEGE OF MEDICINE   (United States)

^b LERNER RESEARCH INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM ION; FRACTALKINE; G PROTEIN COUPLED RECEPTOR; LYSOPHOSPHATIDIC ACID; PHOSPHOLIPASE C BETA; RANTES;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CALCIUM TRANSPORT; CELL MIGRATION; CELL PROLIFERATION; CONTROLLED STUDY; CYTOMEGALOVIRUS INFECTION; ENDOTHELIUM CELL; ENZYME ACTIVATION; GENE; GLIOMA CELL; HUMAN; HUMAN CELL; IMMUNOPRECIPITATION; MOLECULAR BIOLOGY; NONHUMAN; PROTEIN EXPRESSION; SKIN FIBROBLAST; SMOOTH MUSCLE FIBER; TARGET CELL; US28 GENE; VIROGENESIS; VIRUS RECOMBINANT; VIRUS REPLICATION; WESTERN BLOTTING;

CALCIUM; CELL LINE; CELL LINE, TUMOR; CHEMOKINE CCL5; CHEMOKINE CX3CL1; CYTOMEGALOVIRUS; CYTOMEGALOVIRUS INFECTIONS; HUMANS; MYOCYTES, SMOOTH MUSCLE; RECEPTORS, CHEMOKINE; TYPE C PHOSPHOLIPASES; VIRAL PROTEINS;

CYTOMEGALOVIRUS; RODENTIA;

EID: 84870524021     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0050524     Document Type: Article

References (66)

1. Mocarski ES, Courcelle CT (2001) Cytomegaloviruses and their replication. In: Knipe DM, Howley PM, editors. Fields Virology. Philadelpha, PA: Lippinscott Williams & Williams. 2629-2973.
2. Pass RF (2001) Cytomegaloviruses. In: Knipe DM, Howley PM, editors. Fields Virology. Philadelpha, PA: Lippinscott Williams & Williams. 2675-2706.
3. Khanna R, Diamond DJ, (2006) Human cytomegalovirus vaccine: time to look for alternative options. Trends Mol Med 12: 26-33.
4. Stagno S, Pass RF, Dworsky ME, Henderson RE, Moore EG, et al. (1982) Congenital cytomegalovirus infection: The relative importance of primary and recurrent maternal infection. N Engl J Med 306: 945-949.
5. Boppana SB, Pass RF, Britt WJ, Stagno S, Alford CA, (1992) Symptomatic congenital cytomegalovirus infection: neonatal morbidity and mortality. Pediatr Infect Dis J 11: 93-99.
6. Ljungman P, Griffiths P, Paya C, (2002) Definitions of cytomegalovirus infection and disease in transplant recipients. Clin Infect Dis 34: 1094-1097.
7. Hebart H, Einsele H, (1998) Diagnosis and treatment of cytomegalovirus infection. Curr Opin Hematol 5: 483-487.
8. Ahuja SK, Murphy PM, (1993) Molecular piracy of mammalian interleukin-8 receptor type B by herpesvirus saimiri. J Biol Chem 268: 20691-20694.
9. Cesarman E, Nador RG, Bai F, Bohenzky RA, Russo JJ, et al. (1996) Kaposi's sarcoma-associated herpesvirus contains G protein-coupled receptor and cyclin D homologs which are expressed in Kaposi's sarcoma and malignant lymphoma. J Virol 70: 8218-8223.
10. Isegawa Y, Ping Z, Nakano K, Sugimoto N, Yamanishi K, (1998) Human herpesvirus 6 open reading frame U12 encodes a functional beta-chemokine receptor. J Virol 72: 6104-6112.
11. Margulies BJ, Browne H, Gibson W, (1996) Identification of the human cytomegalovirus G protein-coupled receptor homologue encoded by UL33 in infected cells and enveloped virus particles. Virology 225: 111-125.
12. Milne RS, Mattick C, Nicholson L, Devaraj P, Alcami A, et al. (2000) RANTES binding and down-regulation by a novel human herpesvirus-6 beta chemokine receptor. J Immunol 164: 2396-2404.
13. Neote K, DiGregorio D, Mak JY, Horuk R, Schall TJ, (1993) Molecular cloning, functional expression, and signaling characteristics of a C-C chemokine receptor. Cell 72: 415-425.
14. Gao JL, Murphy PM, (1994) Human cytomegalovirus open reading frame US28 encodes a functional beta chemokine receptor. J Biol Chem 269: 28539-28542.
15. Casarosa P, Bakker RA, Verzijl D, Navis M, Timmerman H, et al. (2001) Constitutive signaling of the human cytomegalovirus-encoded chemokine receptor US28. J Biol Chem 276: 1133-1137.
16. Miller WE, Houtz DA, Nelson CD, Kolattukudy PE, Lefkowitz RJ, (2003) G-protein-coupled Receptor (GPCR) Kinase Phosphorylation and {beta}-Arrestin Recruitment Regulate the Constitutive Signaling Activity of the Human Cytomegalovirus US28 GPCR. J Biol Chem 278: 21663-21671.
17. Billstrom MA, Johnson GL, Avdi NJ, Worthen GS, (1998) Intracellular signaling by the chemokine receptor US28 during human cytomegalovirus infection. J Virol 72: 5535-5544.
18. Waldhoer M, Kledal TN, Farrell H, Schwartz TW, (2002) Murine cytomegalovirus (CMV) M33 and human CMV US28 receptors exhibit similar constitutive signaling activities. J Virol 76: 8161-8168.
19. Maussang D, Verzijl D, van Walsum M, Leurs R, Holl J, et al. (2006) Human cytomegalovirus-encoded chemokine receptor US28 promotes tumorigenesis. Proc Natl Acad Sci U S A 103: 13068-13073.
20. Streblow DN, Soderberg-Naucler C, Vieira J, Smith P, Wakabayashi E, et al. (1999) The human cytomegalovirus chemokine receptor US28 mediates vascular smooth muscle cell migration. Cell 99: 511-520.
21. Vieira J, Schall TJ, Corey L, Geballe AP, (1998) Functional analysis of the human cytomegalovirus US28 gene by insertion mutagenesis with the green fluorescent protein gene. J Virol 72: 8158-8165.
22. Bodaghi B, Jones TR, Zipeto D, Vita C, Sun L, et al. (1998) Chemokine sequestration by viral chemoreceptors as a novel viral escape strategy: withdrawal of chemokines from the environment of cytomegalovirus-infected cells. J Exp Med 188: 855-866.
23. Melnychuk RM, Streblow DN, Smith PP, Hirsch AJ, Pancheva D, et al. (2004) Human cytomegalovirus-encoded G protein-coupled receptor US28 mediates smooth muscle cell migration through Galpha12. J Virol 78: 8382-8391.
24. Streblow DN, Vomaske J, Smith P, Melnychuk R, Hall L, et al. (2003) Human cytomegalovirus chemokine receptor US28-induced smooth muscle cell migration is mediated by focal adhesion kinase and Src. J Biol Chem 278: 50456-50465.
25. Maussang D, Langemeijer E, Fitzsimons CP, Stigter-van Walsum M, Dijkman R, et al. (2009) The human cytomegalovirus-encoded chemokine receptor US28 promotes angiogenesis and tumor formation via cyclooxygenase-2. Cancer Res 69: 2861-2869.
26. Slinger E, Maussang D, Schreiber A, Siderius M, Rahbar A, et al. (2010) HCMV-encoded chemokine receptor US28 mediates proliferative signaling through the IL-6-STAT3 axis. Sci Signal 3: ra58.
27. Bongers G, Maussang D, Muniz LR, Noriega VM, Fraile-Ramos A, et al. (2010) The cytomegalovirus-encoded chemokine receptor US28 promotes intestinal neoplasia in transgenic mice. J Clin Invest 120: 3969-3978.
28. Davis-Poynter NJ, Lynch DM, Vally H, Shellam GR, Rawlinson WD, et al. (1997) Identification and characterization of a G protein-coupled receptor homolog encoded by murine cytomegalovirus. J Virol 71: 1521-1529.
29. Case R, Sharp E, Benned-Jensen T, Rosenkilde MM, Davis-Poynter N, et al. (2008) Functional analysis of the murine cytomegalovirus chemokine receptor homologue M33: ablation of constitutive signaling is associated with an attenuated phenotype in vivo. J Virol 82: 1884-1898.
30. Kledal TN, Rosenkilde MM, Schwartz TW, (1998) Selective recognition of the membrane-bound CX3C chemokine, fractalkine, by the human cytomegalovirus-encoded broad-spectrum receptor US28. FEBS Lett 441: 209-214.
31. Kuhn DE, Beall CJ, Kolattukudy PE, (1995) The cytomegalovirus US28 protein binds multiple CC chemokines with high affinity. Biochem Biophys Res Commun 211: 325-330.
32. Casarosa P, Menge WM, Minisini R, Otto C, van Heteren J, et al. (2003) Identification of the first nonpeptidergic inverse agonist for a constitutively active viral-encoded G protein-coupled receptor. J Biol Chem 278: 5172-5178.
33. Casarosa P, Waldhoer M, LiWang PJ, Vischer HF, Kledal T, et al. (2005) CC and CX3C chemokines differentially interact with the N terminus of the human cytomegalovirus-encoded US28 receptor. J Biol Chem 280: 3275-3285.
34. Fraile-Ramos A, Kledal TN, Pelchen-Matthews A, Bowers K, Schwartz TW, et al. (2001) The human cytomegalovirus US28 protein is located in endocytic vesicles and undergoes constitutive endocytosis and recycling. Mol Biol Cell 12: 1737-1749.
35. Minisini R, Tulone C, Luske A, Michel D, Mertens T, et al. (2003) Constitutive inositol phosphate formation in cytomegalovirus-infected human fibroblasts is due to expression of the chemokine receptor homologue pUS28. J Virol 77: 4489-4501.
36. McLean KA, Holst PJ, Martini L, Schwartz TW, Rosenkilde MM, (2004) Similar activation of signal transduction pathways by the herpesvirus-encoded chemokine receptors US28 and ORF74. Virology 325: 241-251.
37. Pleskoff O, Casarosa P, Verneuil L, Ainoun F, Beisser P, et al. (2005) The human cytomegalovirus-encoded chemokine receptor US28 induces caspase-dependent apoptosis. Febs J 272: 4163-4177.
38. Stropes MP, Schneider OD, Zagorski WA, Miller JL, Miller WE, (2009) The carboxy-terminal tail of human cytomegalovirus (HCMV) US28 regulates both chemokine-independent and chemokine-dependent signaling in HCMV-infected cells. J Virol 83: 10016-10027.
39. Vomaske J, Melnychuk RM, Smith PP, Powell J, Hall L, et al. (2009) Differential ligand binding to a human cytomegalovirus chemokine receptor determines cell type-specific motility. PLoS Pathog 5: e1000304.
40. Vomaske J, Streblow DN (2009) Human Cytomegalovirus US28: A Functionally Selective Chemokine Binding Receptor. Infect Disord Drug Targets.
41. Wing BA, Johnson RA, Huang ES, (1998) Identification of positive and negative regulatory regions involved in regulating expression of the human cytomegalovirus UL94 late promoter: role of IE2-86 and cellular p53 in mediating negative regulatory function. J Virol 72: 1814-1825.
42. Hahn G, Khan H, Baldanti F, Koszinowski UH, Revello MG, et al. (2002) The human cytomegalovirus ribonucleotide reductase homolog UL45 is dispensable for growth in endothelial cells, as determined by a BAC-cloned clinical isolate of human cytomegalovirus with preserved wild-type characteristics. J Virol 76: 9551-9555.
43. Stropes MP, Miller WE, (2008) Functional analysis of human cytomegalovirus pUS28 mutants in infected cells. J Gen Virol 89: 97-105.
44. O'Connor CM, Shenk T, (2011) 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. Journal of virology 85: 3700-3707.
45. Lee EC, Yu D, Martinez de Velasco J, Tessarollo L, Swing DA, et al. (2001) A highly efficient Escherichia coli-based chromosome engineering system adapted for recombinogenic targeting and subcloning of BAC DNA. Genomics 73: 56-65.
46. Warming S, Costantino N, Court DL, Jenkins NA, Copeland NG, (2005) Simple and highly efficient BAC recombineering using galK selection. Nucleic Acids Res 33: e36.
47. Zhu H, Shen Y, Shenk T, (1995) Human cytomegalovirus IE1 and IE2 proteins block apoptosis. J Virol 69: 7960-7970.
48. Terhune S, Torigoi E, Moorman N, Silva M, Qian Z, et al. (2007) Human cytomegalovirus UL38 protein blocks apoptosis. J Virol 81: 3109-3123.
49. Sharon-Friling R, Goodhouse J, Colberg-Poley AM, Shenk T, (2006) Human cytomegalovirus pUL37x1 induces the release of endoplasmic reticulum calcium stores. Proc Natl Acad Sci U S A 103: 19117-19122.
50. Bakker RA, Casarosa P, Timmerman H, Smit MJ, Leurs R, (2004) Constitutively active Gq/11-coupled receptors enable signaling by co-expressed G(i/o)-coupled receptors. The Journal of biological chemistry 279: 5152-5161.
51. Schober A, Siess W (2012) Lysophosphatidic acid in atherosclerotic diseases. Br J Pharmacol.
52. Zhang C, Baker DL, Yasuda S, Makarova N, Balazs L, et al. (2004) Lysophosphatidic acid induces neointima formation through PPARgamma activation. J Exp Med 199: 763-774.
53. Yoshida K, Nishida W, Hayashi K, Ohkawa Y, Ogawa A, et al. (2003) Vascular remodeling induced by naturally occurring unsaturated lysophosphatidic acid in vivo. Circulation 108: 1746-1752.
54. Subramanian P, Karshovska E, Reinhard P, Megens RT, Zhou Z, et al. (2010) Lysophosphatidic acid receptors LPA1 and LPA3 promote CXCL12-mediated smooth muscle progenitor cell recruitment in neointima formation. Circ Res 107: 96-105.
55. Mokros T, Rehm A, Droese J, Oppermann M, Lipp M, et al. (2002) Surface expression and endocytosis of the human cytomegalovirus-encoded chemokine receptor US28 is regulated by agonist-independent phosphorylation. J Biol Chem 277: 45122-45128.
56. Geballe AP, Leach FS, Mocarski ES, (1986) Regulation of cytomegalovirus late gene expression: gamma genes are controlled by posttranscriptional events. J Virol 57: 864-874.
57. Gibson W, (1983) Protein counterparts of human and simian cytomegaloviruses. Virology 128: 391-406.
58. Stinski MF, (1978) Sequence of protein synthesis in cells infected by human cytomegalovirus: early and late virus-induced polypeptides. J Virol 26: 686-701.
59. Sinzger C, Hahn G, Digel M, Katona R, Sampaio KL, et al. (2008) Cloning and sequencing of a highly productive, endotheliotropic virus strain derived from human cytomegalovirus TB40/E. The Journal of general virology 89: 359-368.
60. O'Connor CM, Shenk T (2012) Human Cytomegalovirus pUL78 G Protein-coupled Receptor Homologue Is Required for Timely Cell Entry in Epithelial Cells but not Fibroblasts. J Virol.
61. O'Connor CM, Murphy EA, (2012) A myeloid progenitor cell line capable of supporting human cytomegalovirus latency and reactivation, resulting in infectious progeny. J Virol 86: 9854-9865.
62. Magri G, Muntasell A, Romo N, Saez-Borderias A, Pende D, et al. (2011) NKp46 and DNAM-1 NK-cell receptors drive the response to human cytomegalovirus-infected myeloid dendritic cells overcoming viral immune evasion strategies. Blood 117: 848-856.
63. Schempp S, Topp M, Kessler T, Sampaio KL, Dennehy KM, et al. (2011) Deletion mutant of human cytomegalovirus lacking US2-US6 and US11 maintains MHC class I expression and antigen presentation by infected dendritic cells. Virus Res 155: 446-454.
64. Maussang D, Vischer HF, Schreiber A, Michel D, Smit MJ, (2009) Pharmacological and biochemical characterization of human cytomegalovirus-encoded G protein-coupled receptors. Methods in enzymology 460: 151-171.
65. Vischer HF, Leurs R, Smit MJ (2005) HCMV-encoded G-protein-coupled receptors as constitutively active modulators of cellular signaling networks. Trends Pharmacol Sci.
66. Soroceanu L, Matlaf L, Bezrookove V, Harkins L, Martinez R, et al. (2011) Human Cytomegalovirus US28 Found in Glioblastoma Promotes an Invasive and Angiogenic Phenotype. Cancer Res.