Sulfotyrosines of the Kaposi's sarcoma-associated herpesvirus G protein-coupled receptor promote tumorigenesis through autocrine activation

Journal of Virology

Volumn 84, Issue 7, 2010, Pages 3351-3361

  Feng, Hao ^a,b   Sun, Zhifeng ^a   Farzan, Michael R ^c   Feng, Pinghui ^a  

^a UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^b HUNAN NORMAL UNIVERSITY   (China)

^c HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE RECEPTOR AGONIST; G PROTEIN COUPLED RECEPTOR; GAMMA INTERFERON INDUCIBLE PROTEIN 10; GRO ALPHA; PROTEIN KINASE B; SULFOTYROSINE DERIVATIVE; TYROSINE DERIVATIVE; TYROSINE SULFATE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; AUTOCRINE EFFECT; BINDING ASSAY; CARCINOGENESIS; CONTROLLED STUDY; CYTOKINE RELEASE; DISEASE ASSOCIATION; ENZYME PHOSPHORYLATION; HERPES VIRUS; HUMAN; HUMAN CELL; KAPOSI SARCOMA; MOUSE; NONHUMAN; PRIORITY JOURNAL; TUMOR GROWTH;

ANIMALS; CHEMOKINE CXCL1; CHEMOKINE CXCL10; CYTOKINES; HERPESVIRUS 8, HUMAN; HUMANS; MICE; NIH 3T3 CELLS; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, G-PROTEIN-COUPLED; SARCOMA, KAPOSI; SIGNAL TRANSDUCTION; TYROSINE;

HUMAN HERPESVIRUS 8; MUS MUSCULUS;

EID: 77949401409     PISSN: 0022538X     EISSN: None     Source Type: Journal    
DOI: 10.1128/JVI.01939-09     Document Type: Article

References (48)

1. Reference deleted.
2. Arvanitakis, L., E. Geras-Raaka, A. Varma, M. C. Gershengorn, and E. Cesarman. 1997. Human herpesvirus KSHV encodes a constitutively active G-protein-coupled receptor linked to cell proliferation. Nature 385:347-350.
3. Bais, C., B. Santomasso, O. Coso, L. Arvanitakis, E. G. Raaka, J. S. Gutkind, A. S. Asch, E. Cesarman, M. C. Gershengorn, and E. A. Mesri. 1998. Gprotein-coupled receptor of Kaposi's sarcoma-associated herpesvirus is a viral oncogene and angiogenesis activator. Nature 391:86-89.
4. Bais, C., A. Van Geelen, P. Eroles, A. Mutlu, C. Chiozzini, S. Dias, R. L. Silverstein, S. Rafii, and E. A. Mesri. 2003. Kaposi's sarcoma associated herpesvirus G protein-coupled receptor immortalizes human endothelial cells by activation of the VEGF receptor-2/ KDR. Cancer Cell 3:131-143.
5. Cannon, M., N. J. Philpott, and E. Cesarman. 2003. The Kaposi's sarcomaassociated herpesvirus G protein-coupled receptor has broad signaling effects in primary effusion lymphoma cells. J. Virol. 77:57-67.
6. Cannon, M. L., and E. Cesarman. 2004. The KSHV G protein-coupled receptor signals via multiple pathways to induce transcription factor activation in primary effusion lymphoma cells. Oncogene 23:514-523.
7. Cesarman, E., Y. Chang, P. S. Moore, J. W. Said, and D. M. Knowles. 1995. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in AIDS-related body-cavity-based lymphomas. N. Engl. J. Med. 332:1186- 1191.
8. Cesarman, E., E. A. Mesri, and M. C. Gershengorn. 2000. Viral G proteincoupled receptor and Kaposi's sarcoma: a model of paracrine neoplasia? J. Exp. Med. 191:417-422.
9. Chang, Y., E. Cesarman, M. S. Pessin, F. Lee, J. Culpepper, D. M. Knowles, and P. S. Moore. 1994. Identification of herpesvirus-like DNA sequences in AIDS-associated Kaposi's sarcoma. Science 266:1865-1869.
10. Chiou, C. J., L. J. Poole, P. S. Kim, D. M. Ciufo, J. S. Cannon, C. M. ap Rhys, D. J. Alcendor, J. C. Zong, R. F. Ambinder, and G. S. Hayward. 2002. Patterns of gene expression and a transactivation function exhibited by the vGCR (ORF74) chemokine receptor protein of Kaposi's sarcoma-associated herpesvirus. J. Virol. 76:3421-3439.
11. Choe, H., W. Li, P. L. Wright, N. Vasilieva, M. Venturi, C. C. Huang, C. Grundner, T. Dorfman, M. B. Zwick, L. Wang, E. S. Rosenberg, P. D. Kwong, D. R. Burton, J. E. Robinson, J. G. Sodroski, and M. Farzan. 2003. Tyrosine sulfation of human antibodies contributes to recognition of the CCR5 binding region of HIV-1 gp120. Cell 114:161-170.
12. Couty, J. P., E. Geras-Raaka, B. B. Weksler, and M. C. Gershengorn. 2001. Kaposi's sarcoma-associated herpesvirus G protein-coupled receptor signals through multiple pathways in endothelial cells. J. Biol. Chem. 276:33805-33811.
13. Farzan, M., G. J. Babcock, N. Vasilieva, P. L. Wright, E. Kiprilov, T. Mirzabekov, and H. Choe. 2002. The role of post-translational modifications of the CXCR4 amino terminus in stromal-derived factor 1 alpha association and HIV-1 entry. J. Biol. Chem. 277:29484-29489.
14. Farzan, M., T. Mirzabekov, P. Kolchinsky, R. Wyatt, M. Cayabyab, N. P. Gerard, C. Gerard, J. Sodroski, and H. Choe. 1999. Tyrosine sulfation of the amino terminus of CCR5 facilitates HIV-1 entry. Cell 96:667-676.
15. Farzan, M., C. E. Schnitzler, N. Vasilieva, D. Leung, J. Kuhn, C. Gerard, N. P. Gerard, and H. Choe. 2001. Sulfated tyrosines contribute to the formation of the C5a docking site of the human C5a anaphylatoxin receptor. J. Exp. Med. 193:1059-1066.
16. Feng, H., X. Dong, A. Negaard, and P. Feng. 2008. Kaposi's sarcoma-associated herpesvirus K7 induces viral G protein-coupled receptor degradation and reduces its tumorigenicity. PLoS Pathog. 4:e1000157.
17. Feng, P., D. N. Everly, Jr., and G. S. Read. 2001. mRNA decay during herpesvirus infections: interaction between a putative viral nuclease and a cellular translation factor. J. Virol. 75:10272-10280.
18. Feng, P., C. Liang, Y. C. Shin, E. Xiaofei, W. Zhang, R. Gravel, T. T. Wu, R. Sun, E. Usherwood, and J. U. Jung. 2007. A novel inhibitory mechanism of mitochondrion-dependent apoptosis by a herpesviral protein. PLoS Pathog. 3:e174.
19. Feng, P., C. W. Scott, N. H. Cho, H. Nakamura, Y. H. Chung, M. J. Monteiro, and J. U. Jung. 2004. Kaposi's sarcoma-associated herpesvirus K7 protein targets a ubiquitin-like/ubiquitin-associated domain-containing protein to promote protein degradation. Mol. Cell. Biol. 24:3938-3948.
20. Geras-Raaka, E., A. Varma, I. Clark-Lewis, and M. C. Gershengorn. 1998. Kaposi's sarcoma-associated herpesvirus (KSHV) chemokine vMIP-II and human SDF-1α inhibit signaling by KSHV G protein-coupled receptor. Biochem. Biophys. Res. Commun. 253:725-727.
21. Geras-Raaka, E., A. Varma, H. Ho, I. Clark-Lewis, and M. C. Gershengorn. 1998. Human interferon-gamma-inducible protein 10 (IP-10) inhibits constitutive signaling of Kaposi's sarcoma-associated herpesvirus G proteincoupled receptor. J. Exp. Med. 188:405-408.
22. Gershengorn, M. C., E. Geras-Raaka, A. Varma, and I. Clark-Lewis. 1998. Chemokines activate Kaposi's sarcoma-associated herpesvirus G proteincoupled receptor in mammalian cells in culture. J. Clin. Invest. 102:1469-1472.
23. Hayward, G. S. 2003. Initiation of angiogenic Kaposi's sarcoma lesions. Cancer Cell 3:1-3.
24. Ho, H. H., D. Du, and M. C. Gershengorn. 1999. The N terminus of Kaposi's sarcoma-associated herpesvirus G protein-coupled receptor is necessary for high affinity chemokine binding but not for constitutive activity. J. Biol. Chem. 274:31327-31332.
25. Holst, P. J., M. M. Rosenkilde, D. Manfra, S. C. Chen, M. T. Wiekowski, B. Holst, F. Cifire, M. Lipp, T. W. Schwartz, and S. A. Lira. 2001. Tumorigenesis induced by the HHV8-encoded chemokine receptor requires ligand modulation of high constitutive activity. J. Clin. Invest. 108:1789-1796.
26. Kirshner, J. R., K. Staskus, A. Haase, M. Lagunoff, and D. Ganem. 1999. Expression of the open reading frame 74 (G-protein-coupled receptor) gene of Kaposi's sarcoma (KS)-associated herpesvirus: implications for KS pathogenesis. J. Virol. 73:6006-6014.
27. Kledal, T. N., M. M. Rosenkilde, F. Coulin, G. Simmons, A. H. Johnsen, S. Alouani, C. A. Power, H. R. Luttichau, J. Gerstoft, P. R. Clapham, I. Clark-Lewis, T. N. Wells, and T. W. Schwartz. 1997. A broad-spectrum chemokine antagonist encoded by Kaposi's sarcoma-associated herpesvirus. Science 277:1656-1659.
28. Lane, B. R., J. Liu, P. J. Bock, D. Schols, M. J. Coffey, R. M. Strieter, P. J. Polverini, and D. M. Markovitz. 2002. Interleukin-8 and growth-regulated oncogene alpha mediate angiogenesis in Kaposi's sarcoma. J. Virol. 76: 11570-11583.
29. Lane, B. R., R. M. Strieter, M. J. Coffey, and D. M. Markovitz. 2001. Human immunodeficiency virus type 1 (HIV-1)-induced GRO-alpha production stimulates HIV-1 replication in macrophages and T lymphocytes. J. Virol. 75:5812-5822.
30. Liang, C., P. Feng, B. Ku, I. Dotan, D. Canaani, B. H. Oh, and J. U. Jung. 2006. Autophagic and tumour suppressor activity of a novel Beclin1-binding protein UVRAG. Nat. Cell Biol. 8:688-699.
31. Liu, C., G. Sandford, G. Fei, and J. Nicholas. 2004. Galpha protein selectivity determinant specified by a viral chemokine receptor-conserved region in the C tail of the human herpesvirus 8 G protein-coupled receptor. J. Virol. 78:2460-2471.
32. Maussang, D., D. Verzijl, M. van Walsum, R. Leurs, J. Holl, O. Pleskoff, D. Michel, G. A. van Dongen, and M. J. Smit. 2006. Human cytomegalovirusencoded chemokine receptor US28 promotes tumorigenesis. Proc. Natl. Acad. Sci. U. S. A. 103:13068-13073.
33. McLean, K. A., P. J. Holst, L. Martini, T. W. Schwartz, and M. M. Rosenkilde. 2004. Similar activation of signal transduction pathways by the herpesvirus-encoded chemokine receptors US28 and ORF74. Virology 325:241-251.
34. Montaner, S., A. Sodhi, A. Molinolo, T. H. Bugge, E. T. Sawai, Y. He, Y. Li, P. E. Ray, and J. S. Gutkind. 2003. Endothelial infection with KSHV genes in vivo reveals that vGPCR initiates Kaposi's sarcomagenesis and can promote the tumorigenic potential of viral latent genes. Cancer Cell 3:23-36.
35. Moore, K. L. 2003. The biology and enzymology of protein tyrosine Osulfation. J. Biol. Chem. 278:24243-24246.
36. Nador, R. G., E. Cesarman, D. M. Knowles, and J. W. Said. 1995. Herpeslike DNA sequences in a body-cavity-based lymphoma in an HIV-negative patient. N. Engl. J. Med. 333:943.
37. Nador, R. G., L. L. Milligan, O. Flore, X. Wang, L. Arvanitakis, D. M. Knowles, and E. Cesarman. 2001. Expression of Kaposi's sarcoma-associated herpesvirus G protein-coupled receptor monocistronic and bicistronic transcripts in primary effusion lymphomas. Virology 287:62-70.
38. Pati, S., M. Cavrois, H. G. Guo, J. S. Foulke, Jr., J. Kim, R. A. Feldman, and M. Reitz. 2001. Activation of NF-κB by the human herpesvirus 8 chemokine receptor ORF74: evidence for a paracrine model of Kaposi's sarcoma pathogenesis. J. Virol. 75:8660-8673.
39. Polson, A. G., D. Wang, J. DeRisi, and D. Ganem. 2002. Modulation of host gene expression by the constitutively active G protein-coupled receptor of Kaposi's sarcoma-associated herpesvirus. Cancer Res. 62:4525-4530.
40. Rosenkilde, M. M., T. N. Kledal, H. Brauner-Osborne, and T. W. Schwartz. 1999. Agonists and inverse agonists for the herpesvirus 8-encoded constitutively active seven-transmembrane oncogene product, ORF-74. J. Biol. Chem. 274:956-961.
41. Russo, J. J., R. A. Bohenzky, M. C. Chien, J. Chen, M. Yan, D. Maddalena, J. P. Parry, D. Peruzzi, I. S. Edelman, Y. Chang, and P. S. Moore. 1996. Nucleotide sequence of the Kaposi sarcoma-associated herpesvirus (HHV8). Proc. Natl. Acad. Sci. U. S. A. 93:14862-14867.
42. i and phospholipase C-dependent signaling pathways. J. Virol. 76:1744-1752.
43. Sodhi, A., R. Chaisuparat, J. Hu, A. K. Ramsdell, B. D. Manning, E. A. Sausville, E. T. Sawai, A. Molinolo, J. S. Gutkind, and S. Montaner. 2006. The TSC2/mTOR pathway drives endothelial cell transformation induced by the Kaposi's sarcoma-associated herpesvirus G protein-coupled receptor. Cancer Cell 10:133-143.
44. Sodhi, A., S. Montaner, V. Patel, J. J. Gomez-Roman, Y. Li, E. A. Sausville, E. T. Sawai, and J. S. Gutkind. 2004. Akt plays a central role in sarcomagenesis induced by Kaposi's sarcoma herpesvirus-encoded G protein-coupled receptor. Proc. Natl. Acad. Sci. U. S. A. 101:4821-4826.
45. Soulier, J., L. Grollet, E. Oksenhendler, P. Cacoub, D. Cazals-Hatem, P. Babinet, M. F. d'Agay, J. P. Clauvel, M. Raphael, L. Degos, et al. 1995. Kaposi's sarcoma-associated herpesvirus-like DNA sequences in multicentric Castleman's disease. Blood 86:1276-1280.
46. Veldkamp, C. T., C. Seibert, F. C. Peterson, T. P. Sakmar, and B. F. Volkman. 2006. Recognition of a CXCR4 sulfotyrosine by the chemokine stromal cell-derived factor-1α (SDF-1α/CXCL12). J. Mol. Biol. 359:1400-1409.
47. Virgin, H. W., IV, P. Latreille, P. Wamsley, K. Hallsworth, K. E. Weck, A. J. Dal Canto, and S. H. Speck. 1997. Complete sequence and genomic analysis of murine gammaherpesvirus 68. J. Virol. 71:5894-5904.
48. Yang, T. Y., S. C. Chen, M. W. Leach, D. Manfra, B. Homey, M. Wiekowski, L. Sullivan, C. H. Jenh, S. K. Narula, S. W. Chensue, and S. A. Lira. 2000. Transgenic expression of the chemokine receptor encoded by human herpesvirus 8 induces an angioproliferative disease resembling Kaposi's sarcoma. J. Exp. Med. 191:445-454.