Role of herpes simplex virus VP11/12 tyrosine-based motifs in binding and activation of the src family kinase lck and recruitment of p85, Grb2, and Shc

Journal of Virology

Volumn 87, Issue 20, 2013, Pages 11276-11286

  Strunk, Ulrike ^a   Saffran, Holly A ^a   Wu, Frederick W ^a   Smiley, James R ^a  

^a UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

GROWTH FACTOR RECEPTOR BOUND PROTEIN 2; PROTEIN KINASE LCK; PROTEIN P85; PROTEIN SHC; UNCLASSIFIED DRUG; VIRUS PROTEIN; VP11 PROTEIN; VP12 PROTEIN;

ARTICLE; HERPES SIMPLEX VIRUS 1; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; PROTEIN MOTIF; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; T LYMPHOCYTE; VIRUS GENOME;

ANIMALS; ANTIGENS, VIRAL; DNA MUTATIONAL ANALYSIS; GRB2 ADAPTOR PROTEIN; HERPESVIRUS 1, HUMAN; HOST-PATHOGEN INTERACTIONS; LYMPHOCYTE SPECIFIC PROTEIN TYROSINE KINASE P56(LCK); PROTEIN BINDING; PROTEIN INTERACTION DOMAINS AND MOTIFS; VIRAL PROTEINS;

EID: 84886919028     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.01702-13     Document Type: Article

References (51)

1. Roizman B, Knipe DM, Whitley RJ. 2007. Herpes simplex viruses, p 2501-2601. In Knipe DM, Howley PM (ed), Fields virology, 5th ed. Lippincott, Williams and Wilkins, Philadelphia, PA.
2. Corey L, Wald A, Celum CL, Quinn TC. 2004. The effects of herpes simplex virus-2 on HIV-1 acquisition and transmission: a review of two overlapping epidemics. J. Acquir. Immune Defic. Syndr. 35:435-445.
3. Wald A, Schacker T, Corey L. 1997. HSV-2 and HIV: consequences of an endemic opportunistic infection. STEP Perspect. 9:2-4.
4. Manning BD, Cantley LC. 2007. AKT/PKB signaling: navigating downstream. Cell 129:1261-1274.
5. Kelly JD, Haldeman BA, Grant FJ, Murray MJ, Seifert RA, Bowen-Pope DF, Cooper JA, Kazlauskas A. 1991. Platelet-derived growth factor (PDGF) stimulates PDGF receptor subunit dimerization and intersubunit trans-phosphorylation. J. Biol. Chem. 266:8987-8992.
6. Wu H, Windmiller DA, Wang L, Backer JM. 2003. YXXM motifs in the PDGF-beta receptor serve dual roles as phosphoinositide 3-kinase binding motifs and tyrosine-based endocytic sorting signals. J. Biol. Chem. 278:40425-40428.
7. Liu P, Cheng H, Roberts TM, Zhao JJ. 2009. Targeting the phosphoinositide 3-kinase pathway in cancer. Nat. Rev. Drug Discov. 8:627-644.
8. Alessi DR, James SR, Downes CP, Holmes AB, Gaffney PR, Reese CB, Cohen P. 1997. Characterization of a 3-phosphoinositide-dependent protein kinase which phosphorylates and activates protein kinase Bα. Curr. Biol. 7:261-269.
9. Sarbassov DD, Guertin DA, Ali SM, Sabatini DM. 2005. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science 307:1098-1101.
10. Andjelkovic M, Alessi DR, Meier R, Fernandez A, Lamb NJ, Frech M, Cron P, Cohen P, Lucocq JM, Hemmings BA. 1997. Role of translocation in the activation and function of protein kinase B. J. Biol. Chem. 272:31515-31524.
11. Stambolic V, Suzuki A, de la Pompa JL, Brothers GM, Mirtsos C, Sasaki T, Ruland J, Penninger JM, Siderovski DP, Mak TW. 1998. Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN. Cell 95:29-39.
12. Maehama T, Dixon JE. 1998. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. J. Biol. Chem. 273:13375-13378.
13. Carracedo A, PandolfiPP. 2008. The PTEN-PI3K pathway: of feedbacks and cross-talks. Oncogene 27:5527-5541.
14. Shin YK, Liu Q, Tikoo SK, Babiuk LA, Zhou Y. 2007. Influenza A virus NS1 protein activates the phosphatidylinositol 3-kinase (PI3K)/Akt pathway by direct interaction with the p85 subunit of PI3K. J. Gen. Virol. 88:13-18.
15. Johnson RA, Wang X, Ma XL, Huong SM, Huang ES. 2001. Human cytomegalovirus up-regulates the phosphatidylinositol 3-kinase (PI3-K) pathway: inhibition of PI3-K activity inhibits viral replication and virusinduced signaling. J. Virol. 75:6022-6032.
16. Mannova P, Beretta L. 2005. Activation of the N-Ras-PI3K-Akt-mTOR pathway by hepatitis C virus: control of cell survival and viral replication. J. Virol. 79:8742-8749.
17. Street A, Macdonald A, McCormick C, Harris M. 2005. Hepatitis C virus NS5A-mediated activation of phosphoinositide 3-kinase results in stabilization of cellular beta-catenin and stimulation of beta-cateninresponsive transcription. J. Virol. 79:5006-5016.
18. Portis T, Longnecker R. 2004. Epstein-Barr virus (EBV) LMP2A mediates B-lymphocyte survival through constitutive activation of the Ras/PI3K/Akt pathway. Oncogene 23:8619-8628.
19. Montaner S, Sodhi A, Pece S, Mesri EA, Gutkind JS. 2001. The Kaposi's sarcoma-associated herpesvirusGprotein-coupled receptor promotes endothelial cell survival through the activation of Akt/protein kinase B. Cancer Res. 61:2641-2648.
20. Tomlinson CC, Damania B. 2004. The K1 protein of Kaposi's sarcomaassociated herpesvirus activates the Akt signaling pathway. J. Virol. 78: 1918-1927.
21. Liu X, Cohen JI. 2013. Varicella-zoster virus ORF12 protein activates the phosphatidylinositol 3-kinase/Akt pathway to regulate cell cycle progression. J. Virol. 87:1842-1848.
22. Benetti L, Roizman B. 2006. Protein kinase B/Akt is present in activated form throughout the entire replicative cycle of δU(S)3 mutant virus but only at early times after infection with wild-type herpes simplex virus 1. J. Virol. 80:3341-3348.
23. Chuluunbaatar U, Roller R, Feldman ME, Brown S, Shokat KM, Mohr I. 2010. Constitutive mTORC1 activation by a herpesvirus Akt surrogate stimulates mRNA translation and viral replication. Genes Dev. 24:2627-2639.
24. Wagner MJ, Smiley JR. 2009. Herpes simplex virus requires VP11/12 to induce phosphorylation of the activation loop tyrosine (Y394) of the Src family kinase Lck in T lymphocytes. J. Virol. 83:12452-12461.
25. Wagner MJ, Smiley JR. 2011. Herpes simplex virus requires VP11/12 to activate Src family kinase-phosphoinositide 3-kinase-Akt signaling. J. Virol. 85:2803-2812.
26. Zahariadis G, Wagner MJ, Doepker RC, Maciejko JM, Crider CM, Jerome KR, Smiley JR. 2008. Cell-type-specific tyrosine phosphorylation of the herpes simplex virus tegument protein VP11/12 encoded by gene UL46. J. Virol. 82:6098-6108.
27. Zhang Y, McKnight JL. 1993. Herpes simplex virus type 1 UL46 and UL47 deletion mutants lack VP11 and VP12 or VP13 and VP14, respectively, and exhibit altered viral thymidine kinase expression. J. Virol. 67:1482-1492.
28. Zhang Y, Sirko DA, McKnight JL. 1991. Role of herpes simplex virus type 1 UL46 and UL47 in alpha TIF-mediated transcriptional induction: characterization of three viral deletion mutants. J. Virol. 65:829-841.
29. Murphy MA, Bucks MA, O'Regan KJ, Courtney RJ. 2008. The HSV-1 tegument protein pUL46 associates with cellular membranes and viral capsids. Virology 376:279-289.
30. Kato K, Daikoku T, Goshima F, Kume H, Yamaki K, Nishiyama Y. 2000. Synthesis, subcellular localization and VP16 interaction of the herpes simplex virus type 2 UL46 gene product. Arch. Virol. 145:2149-2162.
31. McKnight JL, Pellett PE, Jenkins FJ, Roizman B. 1987. Characterization and nucleotide sequence of two herpes simplex virus 1 genes whose products modulate alpha-trans-inducing factor-dependent activation of alpha genes. J. Virol. 61:992-1001.
32. Vittone V, Diefenbach E, Triffett D, Douglas MW, Cunningham AL, Diefenbach RJ. 2005. Determination of interactions between tegument proteins of herpes simplex virus type 1. J. Virol. 79:9566-9571.
33. Songyang Z, Shoelson SE, Chaudhuri M, Gish G, Pawson T, Haser WG, King F, Roberts T, Ratnofsky S, Lechleider RJ. 1993. SH2 domains recognize specific phosphopeptide sequences. Cell 72:767-778.
34. Minaker RL, Mossman KL, Smiley JR. 2005. Functional inaccessibility of quiescent herpes simplex virus genomes. Virol. J. 2:85.
35. Gierasch WW, Zimmerman DL, Ward SL, Vanheyningen TK, Romine JD, Leib DA. 2006. Construction and characterization of bacterial artificial chromosomes containing HSV-1 strains 17 and KOS. J. Virol. Methods 135:197-206.
36. Tischer BK, Smith GA, Osterrieder N. 2010. En passant mutagenesis: a two step markerless red recombination system. Methods Mol. Biol. 634: 421-430.
37. Willard M. 2002. Rapid directional translocations in virus replication. J. Virol. 76:5220-5232.
38. Dunant NM, Messerschmitt AS, Ballmer-Hofer K. 1997. Functional interaction between the SH2 domain of Fyn and tyrosine 324 of hamster polyomavirus middle-T antigen. J. Virol. 71:199-206.
39. Isakov N. 1997. Immunoreceptor tyrosine-based activation motif (ITAM), a unique module linking antigen and Fc receptors to their signaling cascades. J. Leukoc. Biol. 61:6-16.
40. Fruehling S, Longnecker R. 1997. The immunoreceptor tyrosine-based activation motif of Epstein-Barr virus LMP2A is essential for blocking BCR-mediated signal transduction. Virology 235:241-251.
41. Lee H, Guo J, Li M, Choi JK, DeMaria M, Rosenzweig M, Jung JU. 1998. Identification of an immunoreceptor tyrosine-based activation motif of K1 transforming protein of Kaposi's sarcoma-associated herpesvirus. Mol. Cell. Biol. 18:5219-5228.
42. Inubushi S, Nagano-Fujii M, Kitayama K, Tanaka M, An C, Yokozaki H, Yamamura H, Nuriya H, Kohara M, Sada K, Hotta H. 2008. Hepatitis C virus NS5A protein interacts with and negatively regulates the non-receptor protein tyrosine kinase Syk. J. Gen. Virol. 89:1231-1242.
43. Jang IK, Zhang J, Gu H. 2009. Grb2, a simple adapter with complex roles in lymphocyte development, function, and signaling. Immunol. Rev. 232: 150-159.
44. Tari AM, Lopez-Berestein G. 2001. GRB2: a pivotal protein in signal transduction. Semin. Oncol. 28:142-147.
45. Wills MK, Jones N. 2012. Teaching an old dogma new tricks: twenty years of Shc adaptor signalling. Biochem. J. 447:1-16.
46. Liu X, Li Q, Dowdell K, Fischer ER, Cohen JI. 2012. Varicella-zoster virus ORF12 protein triggers phosphorylation of ERK1/2 and inhibits apoptosis. J. Virol. 86:3143-3151.
47. McLean TI, Bachenheimer SL. 1999. Activation of cJUN N-terminal kinase by herpes simplex virus type 1 enhances viral replication. J. Virol. 73:8415-8426.
48. Sloan DD, Han JY, Sandifer TK, Stewart M, Hinz AJ, Yoon M, Johnson DC, Spear PG, Jerome KR. 2006. Inhibition of TCR signaling by herpes simplex virus. J. Immunol. 176:1825-1833.
49. Chuluunbaatar U, Roller R, Mohr I. 2012. Suppression of extracellular signal-regulated kinase activity in herpes simplex virus 1-infected cells by the Us3 protein kinase. J. Virol. 86:7771-7776.
50. Talbert-Slagle K, DiMaio D. 2009. The bovine papillomavirus E5 protein and the PDGF beta receptor: it takes two to tango. Virology 384:345-351.
51. Schaffhausen BS, Roberts TM. 2009. Lessons from polyoma middle T antigen on signaling and transformation: A DNA tumor virus contribution to the war on cancer. Virology 384:304-316.