The Epstein-Barr virus latent membrane protein 2A PY motif recruits WW domain-containing ubiquitin-protein ligases

Virology

Volumn 268, Issue 1, 2000, Pages 178-191

  Ikeda, Masato ^a   Ikeda, Akiko ^a   Longan, Luz C ^a   Longnecker, Richard ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LATENT MEMBRANE PROTEIN 2A; PROLINE; PROTEIN TYROSINE KINASE; UBIQUITIN PROTEIN LIGASE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; ARTICLE; B LYMPHOCYTE; BINDING AFFINITY; BINDING SITE; CONTROLLED STUDY; ENZYME BINDING; EPSTEIN BARR VIRUS; HUMAN; HUMAN CELL; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SEQUENCE ANALYSIS; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; VIRUS LATENCY;

ANIMALIA; DNA VIRUSES; HUMAN HERPESVIRUS 4;

EID: 0034007009     PISSN: 00426822     EISSN: None     Source Type: Journal    
DOI: 10.1006/viro.1999.0166     Document Type: Article

References (67)

1. Ambinder R. F., Mann R. B. Detection and characterization of Epstein-Barr virus in clinical specimens. Am. J. Pathol. 145:1994;239-252.
2. Bonifacino J. S., Weissman A. M. Ubiquitin and the control of protein fate in the secretory and endocytic pathways. Ann. Rev. Cell. Dev. Biol. 14:1998;19-57.
3. Bork P., Sudol M. The WW domain: A signalling site in dystrophin. Trends Biochem. Sci. 19:1994;531-553.
4. Burkhardt A. L., Brunswick M., Bolen J. B., Mond J. J. Anti-immunoglobulin stimulation of B lymphocytes activates src-related protein-tyrosine kinases. Proc. Natl. Acad. Sci. USA. 88:1991;7410-7414.
5. Busson P., Edwards R. H., Tursz T., Raab-Traub N. Sequence polymorphism in the Epstein-Barr virus latent membrane protein (LMP)-2 gene. J. Gen. Virol. 76:1995;139-145.
6. Caldwell R. G., Wilson J. B., Anderson S. J., Longnecker R. Epstein-Barr virus LMP2A drives B cell development and survival in the absence of normal B cell receptor signals. Immunity. 9:1998;405-411.
7. Cambier J. C., Pleiman C. M., Clark M. R. Signal transduction by the B cell antigen receptor and its coreceptors. Annu. Rev. Immunol. 12:1994;457-486.
8. Cenciarelli C., Wilhelm K. G. Jr., Guo A., Weissman A. M. T cell antigen receptor ubiquitination is a consequence of receptor- mediated tyrosine kinase activation. J. Biol. Chem. 271:1996;8709-8713.
9. Chen F., Zou J. Z., di Renzo L., Winberg G., Hu L. F., Klein E., Klein G., Ernberg I. A subpopulation of normal B cells latently infected with Epstein-Barr virus resembles Burkitt lymphoma cells in expressing EBNA-1 but not EBNA-2 or LMP1. J. Virol. 69:1995;3752-3758.
10. Chen H., Smith P., Ambinder R. F., Hayward S. D. Expression of Epstein-Barr virus BamHI-A rightward transcripts in latently infected B cells from peripheral blood. Blood. 93:1999;3026-3032.
11. Chen H. I., Sudol M. The WW domain of Yes-associated protein binds a proline-rich ligand that differs from the consensus established for Src homology 3-binding modules. Proc. Natl. Acad. Sci. USA. 92:1995;7819-7823.
12. Ciechanover A. The ubiquitin-proteasome proteolytic pathway. Cell. 79:1994;13-21.
13. DeFranco A. L. Structure and function of the B cell antigen receptor. Ann. Rev. Cell Dev. Biol. 9:1993;377-410.
14. Einbond A., Sudol M. Towards prediction of cognate complexes between the WW domain and proline-rich ligands. FEBS Lett. 384:1996;1-8.
15. Feng S., Chen J. K., Yu H., Simon J. A., Schreiber S. L. Two binding orientations for peptides to the Src SH3 domain: Development of a general model for SH3-ligand interactions. Science. 266:1994;1241-1247.
16. Franken M., Annis B., Ali A. N., Wang F. 5′ Coding and regulatory region sequence divergence with conserved function of the Epstein-Barr virus LMP2A homolog in herpesvirus papio. J. Virol. 69:1995;8011-8019.
17. Fruehling S., Lee S. K., Herrold R., Frech B., Laux G., Kremmer E., Grasser F. A., Longnecker R. Identification of latent membrane protein 2A (LMP2A) domains essential for the LMP2A dominant-negative effect on B-lymphocyte surface immunoglobulin signal transduction. J. Virol. 70:1996;6216-6226.
18. Fruehling S., Longnecker R. The immunoreceptor tyrosine-based activation motif of Epstein-Barr virus LMP2A is essential for blocking BCR-mediated signal transduction. Virology. 235:1997;241-251.
19. Fruehling S., Swart R., Dolwick K. M., Kremmer E., Longnecker R. Tyrosine 112 of latent membrane protein 2A is essential for protein tyrosine kinase loading and regulation of Epstein-Barr virus latency. J. Virol. 72:1998;7796-7806.
20. Galan J. M., Moreau V., Andre B., Volland C., Haguenauer-Tsapis R. Ubiquitination mediated by the Npi1p/Rsp5p ubiquitin-protein ligase is required for endocytosis of the yeast uracil permease. J. Biol. Chem. 271:1996;10946-10952.
21. Garnier L., Wills J. W., Verderame M. F., Sudol M. WW domains and retrovirus budding. Nature. 381:1996;744-745.
22. Hansson J. H., Nelson-Williams C., Suzuki H., Schild L., Shimkets R., Lu Y., Canessa C., Iwasaki T., Rossier B., Lifton R. P. Hypertension caused by a truncated epithelial sodium channel gamma subunit: Genetic heterogeneity of Liddle syndrome. Nat. Genet. 11:1995a;76-82.
23. Hansson J. H., Schild L., Lu Y., Wilson T. A., Gautschi I., Shimkets R., Nelson-Williams C., Rossier B. C., Lifton R. P. A de novo missense mutation of the beta subunit of the epithelial sodium channel causes hypertension and Liddle syndrome, identifying a proline-rich segment critical for regulation of channel activity. Proc. Natl. Acad. Sci. USA. 92:1995b;11495-11499.
24. Harvey K. F., Kumar S. Nedd4-like proteins: An emerging family of ubiquitin-protein ligases implicated in diverse cellular functions. Trends Cell Biol. 9:1999;166-169.
25. Hein C., Springael J. Y., Volland C., Haguenauer-Tsapis R., Andre B. NPl1, an essential yeast gene involved in induced degradation of Gap1 and Fur4 permeases, encodes the Rsp5 ubiquitin-protein ligase. Mol. Microbiol. 18:1995;77-87.
26. Hicke L. Gettin' down with ubiquitin: Turning off cell-surface receptors, transporters and channels. Trends Cell Biol. 9:1999;107-112.
27. Hicke L., Riezman H. Ubiquitination of a yeast plasma membrane receptor signals its ligand-stimulated endocytosis. Cell. 84:1996;277-287.
28. Hochstrasser M. Protein degradation or regulation: Ub the judge. Cell. 84:1996;813-815.
29. Hofmann K., Bucher P. The rsp5-domain is shared by proteins of diverse functions. FEBS Lett. 358:1995;153-157.
30. Huibregtse J. M., Scheffner M., Beaudenon S., Howley P. M. A family of proteins structurally and functionally related to the E6-AP ubiquitin-protein ligase. Proc. Natl. Acad. Sci. USA. 92:1995;2563-2567.
31. Huibregtse J. M., Scheffner M., Howley P. M. A cellular protein mediates association of p53 with the E6 oncoprotein of human papillomavirus types 16 or 18. EMBO J. 10:1991;4129-4135.
32. Huibregtse J. M., Scheffner M., Howley P. M. Cloning and expression of the cDNA for E6-AP, a protein that mediates the interaction of the human papillomavirus E6 oncoprotein with p53. Mol. Cell. Biol. 13:1993a;775-784.
33. Huibregtse J. M., Scheffner M., Howley P. M. Localization of the E6-AP regions that direct human papillomavirus E6 binding, association with p53, and ubiquitination of associated proteins. Mol. Cell. Biol. 13:1993b;4918-4927.
34. Hustad C. M., Perry W. L., Siracusa L. D., Rasberry C., Cobb L., Cattanach B. M., Kovatch R., Copeland N. G., Jenkins N. A. Molecular genetic characterization of six recessive viable alleles of the mouse agouti locus. Genetics. 140:1995;255-265.
35. Jeffers M., Taylor G. A., Weidner K. M., Omura S., Vande Woude G. F. Degradation of the Met tyrosine kinase receptor by the ubiquitin- proteasome pathway. Mol. Cell. Biol. 17:1997;799-808.
36. Kieff E. Epstein-Barr virus and its replication. Fields B. N., Knipe D. M., Howley P. M. Fields Virology. 1996;1109-1162 Lippincott-Raven, Philadelphia.
37. Kinsella T. M., Nolan G. P. Episomal vectors rapidly and stably produce high-titer recombinant retrovirus. Hum. Gene Ther. 7:1996;1405-1413.
38. Kozak M. Point mutations define a sequence flanking the AUG initiator codon that modulates translation by eukaryotic ribosomes. Cell. 44:1986;283-292.
39. Lim W. A., Richards F. M., Fox R. O. Structural determinants of peptide-binding orientation and of sequence specificity in SH3 domains. Nature. 372:1994;375-379.
40. Longnecker R. Molecular biology of Epstein-Barr virus. McCance D. Humor Tumor Viruses. 1998;133-172 American Society for Microbiology, Washington.
41. Longnecker R., Druker B., Roberts T. M., Kieff E. An Epstein-Barr virus protein associated with cell growth transformation interacts with a tyrosine kinase. J. Virol. 65:1991;3681-3692.
42. Longnecker R., Kieff E. A second Epstein-Barr virus membrane protein (LMP2) is expressed in latent infection and colocalizes with LMP1. J. Virol. 64:1990;2319-2326.
43. Miller C. L., Burkhardt A. L., Lee J. H., Stealey B., Longnecker R., Bolen J. B., Kieff E. Integral membrane protein 2 of Epstein-Barr virus regulates reactivation from latency through dominant negative effects on protein-tyrosine kinases. Immunity. 2:1995;155-166.
44. Miller C. L., Lee J. H., Kieff E., Burkhardt A. L., Bolen J. B., Longnecker R. Epstein-Barr virus protein LMP2A regulates reactivation from latency by negatively regulating tyrosine kinases involved in sIg-mediated signal transduction. Infect. Agents Dis. 3:1994a;128-136.
45. Miller C. L., Lee J. H., Kieff E., Longnecker R. An integral membrane protein (LMP2) blocks reactivation of Epstein-Barr virus from latency following surface immunoglobulin crosslinking. Proc. Natl. Acad. Sci. USA. 91:1994b;772-776.
46. Miller C. L., Longnecker R., Kieff E. Epstein-Barr virus latent membrane protein 2A blocks calcium mobilization in B lymphocytes. J. Virol. 67:1993;3087-3094.
47. Miyashita E. M., Yang B., Babcock G. J., Thorley-Lawson D. A. Identification of the site of Epstein-Barr virus persistence in vivo as a resting B cell. J. Virol. 71:1997;4882-4891.
48. Miyashita E. M., Yang B., Lam K. M., Crawford D. H., Thorley-Lawson D. A. A novel form of Epstein-Barr virus latency in normal B cells in vivo. Cell. 80:1995;593-601.
49. Nakano H., Yamazaki T., Ikeda M., Masai H., Miyatake S., Saito T. Purification of glutathione S-transferase fusion proteins as a non-degraded form by using a protease-negative E. coli strain, AD202. Nucleic Acids Res. 22:1994;543-544.
50. Nefsky B., Beach D. Pub1 acts as an E6-AP-like protein ubiquitiin ligase in the degradation of cdc25. EMBO J. 15:1996;1301-1312.
51. Ohno S., Kawasaki H., Imajoh S., Suzuki K., Inagaki M., Yokokura H., Sakoh T., Hidaka H. Tissue-specific expression of three distinct types of rabbit protein kinase C. Nature. 325:1987;161-166.
52. Perry W. L., Hustad C. M., Swing D. A., O'Sullivan T. N., Jenkins N. A., Copeland N. G. The itchy locus encodes a novel ubiquitin protein ligase that is disrupted in a18H mice. Nat. Genet. 18:1998;143-146.
53. Pirozzi G., McConnell S. J., Uveges A. J., Carter J. M., Sparks A. B., Kay B. K., Fowlkes D. M. Identification of novel human WW domain-containing proteins by cloning of ligand targets. J. Biol. Chem. 272:1997;14611-14616.
54. Qu L., Rowe D. T. Epstein-Barr virus latent gene expression in uncultured peripheral blood lymphocytes. J. Virol. 66:1992;3715-3724.
55. Rajewsky K. Clonal selection and learning in the antibody system. Nature. 381:1996;751-758.
56. Rickinson A. B., Kieff E. Epstein-Barr virus. Fields B. N., Knipe D. M., Howley P. M. Fields Virology. 1996;2397-2446 Lippincott-Raven, Philadelphia.
57. Rossier B. C., Palmer L. G. Mechanisms of aldosterone action on sodium and potassium transport. Seldin D. W., Giebisch G. The Kidney: Physiology and Pathophysiology. 1992;1373-1409 Raven Press, New York.
58. Rotin D. WW (WWP) domains: From structure to function. Curr. Top. Microbiol. Immunol. 228:1998;115-133.
59. Scheffner M., Huibregtse J. M., Vierstra R. D., Howley P. M. The HPV-16 E6 and E6-AP complex functions as a ubiquitin-protein ligase in the ubiquitination of p53. Cell. 75:1993;495-505.
60. Shimkets R. A., Warnock D. G., Bositis C. M., Nelson-Williams C., Hansson J. H., Schambelan M., Gill J. R. Jr., Ulick S., Milora R. V., Findling J. W., Milora R. V., Findling J. W. Liddle's syndrome: Heritable human hypertension caused by mutations in the beta subunit of the epithelial sodium channel. Cell. 79:1994;407-414.
61. Staub O., Dho S., Henry P., Correa J., Ishikawa T., McGlade J., Rotin D. WW domains of Nedd4 bind to the proline-rich PY motifs in the epithelial Na+ channel deleted in Liddle's syndrome. EMBO J. 15:1996;2371-2380.
62. Staub O., Gautschi I., Ishikawa T., Breitschopf K., Ciechanover A., Schild L., Rotin D. Regulation of stability and function of the epithelial Na+ channel (ENaC) by ubiquitination. EMBO J. 16:1997;6325-6336.
63. Sudol M. Structure and function of the WW domain. Prog. Biophys. Mol. Biol. 65:1996;113-132.
64. Tamura H., Schild L., Enomoto N., Matsui N., Marumo F., Rossier B. C. Liddle disease caused by a missense mutation of beta subunit of the epithelial sodium channel gene. J. Clin. Invest. 97:1996;1780-1784.
65. Thorley-Lawson D. A., Miyashita E. M., Khan G. Epstein-Barr virus and the B cell: That's all it takes. Trends Microbiol. 4:1996;204-208.
66. Tierney R. J., Steven N., Young L. S., Rickinson A. B. Epstein-Barr virus latency in blood mononuclear cells: Analysis of viral gene transcription during primary infection and in the carrier state. J. Virol. 68:1994;7374-7385.
67. Wood J. D., Yuan J., Margolis R. L., Colomer V., Duan K., Kushi J., Kaminsky Z., Kleiderlein J. J., Sharp A. H., Ross C. A. Atrophin-1, the DRPLA gene product, interacts with two families of WW domain-containing proteins. Mol. Cell. Neurosci. 11:1998;149-160.