The Shb signalling scaffold binds to and regulates constitutive signals from the Epstein-Barr virus LMP2A membrane protein

Oncogene

Volumn 26, Issue 34, 2007, Pages 4908-4917

  Matskova, L V ^a,e   Helmstetter, C ^a   Ingham, R J ^b   Gish, G ^c   Lindholm, C K ^d   Ernberg, I ^a   Pawson, T ^c   Winberg, G ^a  

^a KAROLINSKA INSTITUTE   (Sweden)

^b UNIVERSITY OF VICTORIA   (Canada)

^c MOUNT SINAI HOSPITAL   (Canada)

^d UNIVERSITY OF LAUSANNE   (Switzerland)

^e KAROLINSKA INSTITUTE   (Sweden)

Author keywords

AIP4; Akt; Epstein Barr virus; Latency associated membrane protein 2A (LMP2A); Shb; Syk

Indexed keywords

MEMBRANE PROTEIN; PROTEIN; PROTEIN KINASE B; PROTEIN KINASE SYK; PROTEIN LMP2A; PROTEIN PTB; PROTEIN SH2; PROTEIN SHB; SCAFFOLD PROTEIN; SHORT HAIRPIN RNA; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ARTICLE; B LYMPHOCYTE; CONTROLLED STUDY; DOWN REGULATION; EMBRYO; ENZYME ACTIVATION; EPSTEIN BARR VIRUS; GENE MUTATION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; REGULATORY MECHANISM; SIGNAL TRANSDUCTION;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; B-LYMPHOCYTES; BINDING SITES; CELL LINE; CELL LINE, TRANSFORMED; HERPESVIRUS 4, HUMAN; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; PHOSPHORYLATION; PROTEIN STRUCTURE, TERTIARY; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; REPRESSOR PROTEINS; SIGNAL TRANSDUCTION; TYROSINE; UBIQUITIN-PROTEIN LIGASES; VIRAL MATRIX PROTEINS;

HUMAN HERPESVIRUS 4;

EID: 34547455781     PISSN: 09509232     EISSN: 14765594     Source Type: Journal    
DOI: 10.1038/sj.onc.1210298     Document Type: Article

References (47)

1. Abdallah B, Hassan A, Benoist C, Goula D, Behr JP, Demeneix BA. (1996). A powerful nonviral vector for in vivo gene transfer into the adult mammalian brain: polyethylenimine. Hum Gene Ther 7: 1947-1954.
2. Beaufils P, Choquet D, Mamoun RZ, Malissen B. (1993). The (YXXL/I)2 signalling motif found in the cytoplasmic segments of the bovine leukaemia virus envelope protein and Epstein-Barr virus latent membrane protein 2A can elicit early and late lymphocyte activation events. EMBO J 12: 5105-5112.
3. Caldwell RG, Wilson JB, Anderson SJ, Longnecker R. (1998). Epstein-Barr virus LMP2A drives B cell development and survival in the absence of normal B cell receptor signals. Immunity 9: 405-411.
4. Casola S, Otipoby KL, Alimzhanov M, Humme S, Uyttersprot N, Kutok JL et al. (2004). B cell receptor signal strength determines B cell fate. Nat Immunol 5: 317-327.
5. Coligan JE, Dunn BM, Ploegh HL, Speicher DW, Wingfield PT. (2001). Current Protocols in Protein Science. John Wiley & Sons, Inc.: New York.
6. Coopman PJ, Do MT, Barth M, Bowden ET, Hayes AJ, Basyuk E et al. (2000). The Syk tyrosine kinase suppresses malignant growth of human breast cancer cells. Nature 406: 742-747.
7. Courbard JR, Fiore F, Adelaide J, Borg JP, Birnbaum D, Ollendorff V. (2002). Interaction between two ubiquitin-protein isopeptide ligases of different classes, CBLC and AIP4/ITCH. J Biol Chem 277: 45267-45275.
8. Dianzani U, Funaro A, DiFranco D, Garbarino G, Bragardo M, Redoglia V et al. (1994). Interaction between endothelium and CD4+CD45RA+ lymphocytes. Role of the human CD38 molecule. J Immunol 153: 952-959.
9. Engels N, Merchant M, Pappu R, Chan AC, Longnecker R, Wienands J. (2001). Epstein-Barr virus latent membrane protein 2A (LMP2A) employs the SLP-65 signaling module. J Exp Med 194: 255-264.
10. Ettenberg SA, Magnifico A, Cuello M, Nau MM, Rubinstein YR, Yarden Y et al. (2001). Cbl-b-dependent coordinated degradation of the epidermal growth factor receptor signaling complex. J Biol Chem 276: 27677-27684.
11. Fodor S, Jakus Z, Mócsai A. (2006). ITAM-based signaling beyond the adaptive immune response. Immunology Lett 104: 29-37.
12. Franke TF, Yang SI, Chan TO, Datta K, Kazlauskas A, Morrison DK et al. (1995). The protein kinase encoded by the Akt proto-oncogene is a target of the PDGF-activated phosphatidylinositol 3-kinase. Cell 81: 727-736.
13. Fruehling S, Lee SK, Herrold R, Frech B, Laux G, Kremmer E et al. (1996). Identification of latent membrane protein 2A (LMP2A) domains essential for the dominant-negative effect on B-lymphocyte surface immunoglobulin signal transduction. J Virol 70: 6216-6226.
14. Grande SM, Ross SR, Monroe JG. (2006). Viral immunoreceptor-associated tyrosine-based activation motifs: potential players in oncogenesis. Future Oncol 2: 301-310.
15. Graham FL, Smiley J, Russell WC, Nairn R. (1977). Characteristics of a human cell line transformed by DNA from human adenovirus type 5. J Gen Virol 36: 59-74.
16. Harlowe E, Lane D. (1988). Antibodies, A Laboratory Manual. Cold Spring Harbor Laboratory Press: Cold Spring Harbor, New York.
17. Holmqvist K, Cross MJ, Rolny C, Hagerkvist R, Rahimi N, Matsumoto T et al. (2004). The adaptor protein Shb binds to tyrosine 1175 in vascular endothelial growth factor (VEGF) receptor-2 and regulates VEGF-dependent cellular migration. J Biol Chem 279: 22267-22275.
18. Ikeda M, Ikeda A, Longan LC, Longnecker R. (2000). The Epstein-Barr virus latent membrane protein 2A PY motif recruits WW domain-containing ubiquitin-protein ligases. Virology 268: 178-191.
19. Ikeda M, Ikeda A, Longnecker R. (2002). Lysine-independent ubiquitination of Epstein-Barr virus LMP2A. Virology 300: 153-159.
20. Ingham RJ, Raaijmakers J, Lim CS, Mbamalu G, Gish G, Chen F et al. (2005). The Epstein-Barr virus protein, latent membrane protein 2A, co-opts tyrosine kinases used by the T cell receptor. J Biol Chem 280: 34133-34142.
21. Karlsson T, Songyang Z, Landgren E, Lavergne C, Di Fiore PP, Ana. M et al. (1995). Molecular interactions of the Src homology 2 domain protein Shb with phosphotyrosine residues, tyrosine kinase receptors and Src homology 3 domain proteins. Oncogene 10: 1475-1483.
22. Katz E, Lareef MH, Rassa JC, Grande SM, King LB, Russo J et al. (2005). MMTV Env encodes an ITAM responsible for transformation of mammary epithelial cells in three-dimensional culture. J Exp Med 201: 431-439.
23. Koretzky GA, Abtahian F, Silverman MA. (2006). SLP76 and SLP65: complex regulation of signalling in lymphocytes and beyond. Nat Revs Immunol 6: 67-78.
24. Kunath T, Gish G, Lickert H, Jones N, Pawson T, Rossant J. (2003). Transgenic RNA interference in ES cell-derived embryos recapitulates a genetic null phenotype. Nat Biotechnol 21: 559-561.
25. Laux G, Perricaudet M, Farrell PJ. (1988). A spliced Epstein-Barr virus gene expressed in immortalized lymphocytes is by circularization of the linear viral genome. EMBO J 7: 769-774.
26. Lindholm CK, Henriksson ML, Hallberg B, Welsh M. (2002). Shb links SLP-76 and Vav with the CD3 complex in Jurkat T cells. Eur J Biochem 269: 3279-3288.
27. Longnecker R, Druker B, Roberts TM, Kieff E. (1991). An Epstein-Barr virus protein associated with cell growth transformation interacts with a tyrosine kinase. J Virol 65: 3681-3692.
28. Lu J, Lin WH, Chen SY, Longnecker R, Tsai SC, Chen CL et al. (2006). Syk tyrosine kinase mediates Epstein-Barr virus latent membrane protein 2A-induced cell migration in epithelial cells. J Biol Chem 281: 8806-8814.
29. Lupher Jr ML, Rao N, Lill NL, Andoniou CE, Miyake S, Clark EA et al. (1998). Cbl-mediated negative regulation of the Syk tyrosine kinase. A critical role for Cbl phosphotyrosine-binding domain binding to Syk phosphotyrosine 323. J Biol Chem 273: 35273-35281.
30. Magnifico A, Ettenberg S, Yang C, Mariano J, Tiwari S, Fang S et al. (2003). WW domain HECT E3s target Cbl RING finger E3s for proteasomal degradation. J Biol Chem 278: 43169-43177.
31. Matskova L, Ernberg I, Pawson T, Winberg G. (2001). C-terminal domain of the Epstein-Barr virus LMP2A membrane protein contains a clustering signal. J Virol 75: 10941-10949.
32. Merchant M, Caldwell RG, Longnecker R. (2000). The LMP2A ITAM is essential for providing B cells with development and survival signals in vivo. J Virol 74: 9115-9124.
33. Morrison JA, Raab-Traub N. (2005). Roles of the ITAM and PY motifs of Epstein-Barr virus latent membrane protein 2A in the inhibition of epithelial cell differentiation and activation of beta-catenin signaling. J Virol 79: 2375-2382.
34. Ota S, Hazeki K, Rao N, Lupher Jr ML, Andoniou CE, Drukeri B et al. (2000). The RING finger domain of Cbl is essential for negative regulation of the Syk tyrosine kinase. J Biol Chem 275: 414-422.
35. Rao N, Ghosh AK, Ota S, Zhou P, Reddi AL, Hakezi K et al. (2001). The non-receptor tyrosine kinase Syk is a target of Cbl-mediated ubiquitylation upon B-cell receptor stimulation. EMBO J 20: 7085-7095.
36. Scholle F, Bendt KM, Raab-Traub N. (2000). Epstein Barr virus LMP2A transforms epithelial cells, inhibits cell differentiation, and activates Akt. J Virol 74: 10681-10689.
37. Scholle F, Longnecker R, Raab-Traub N. (2001). Analysis of the phosphorylation status of Epstein-Barr virus LMP2A in epithelial cells. Virology 291: 208-214.
38. Shaw G, Morse S, Ararat M, Graham FL. (2002). Preferential transformation of human neuronal cells by human adenoviruses and the origin of HEK 293 cells. FASEB J 16: 869-871.
39. Silvennoinen O, Nishigaki H, Kitanaka A, Kumagai M, Ito C, Malavasi F et al. (1996). CD38 signal transduction in human B cell precursors. Rapid induction of tyrosine phosphorylation, activation of syk tyrosine kinase, and phosphorylation of phospholipase C-gamma and phosphatidylinositol 3-kinase. J Immunol 156: 100-107.
40. Swart R, Fruehling S, Longnecker R. (1998). Tyrosines 60, 64 and 101 of Epstein-Barr virus LMP2A are not essential for blocking B cell signal transduction. Virology 263: 485-495.
41. Swart R, Ruf IK, Sample J, Longnecker R. (2000). Latent membrane protein 2A-mediated effects on the phosphatidylinositol 3-Kinase/Akt pathway. J Virol 74: 10838-10845.
42. Tomlinson CC, Damania B. (2004). The K1 protein of Kaposi's sarcoma-associated herpesvirus activates the Akt signaling pathway. J Virol 78: 1918-1927.
43. Welsh M, Mares J, Karlsson T, Lavergne C, Bréant B, Claesson-Welsh L. (1994). Shb is a ubiquitously expressed Src homology 2 protein. Oncogene 9: 19-27.
44. Welsh M, Songyang Z, Frantz JD, Trub T, Reedquist KA, Karlsson T et al. (1998). Stimulation through the T cell receptor leads to interactions between SHB and several signaling proteins. Oncogene 16: 891-901.
45. Welsh N, Makeeva N, Welsh M. (2002). Overexpression of the Shb SH2 domain-protein in insulin-producing cells leads to altered signaling through the IRS-1 and IRS-2 proteins. Mol Med 8: 695-704.
46. Winberg G, Matskova L, Chen F, Plant P, Rotin D, Gish G et al. (2000). Latent membrane protein 2A of Epstein-Barr virus binds WW domain E3 protein-ubiquitin ligases that ubiquitinate B cell tyrosine kinases. Mol Cell Biol 20: 8526-8535.
47. Zubiaur M, Izquierdo M, Terhorst C, Malavasi F, Sancho J. (1997). CD38 ligation results in activation of the Raf-1/mitogen-activated protein kinase and the CD3-zeta/zeta-associated protein-70 signaling pathways in Jurkat T lymphocytes. J Immunol 159: 193-205.