The pivotal role of phosphatidylinositol 3-kinase-Akt signal transduction in virus survival

Journal of General Virology

Volumn 85, Issue 5, 2004, Pages 1065-1076

  Cooray, Samantha ^a,b  

^a PUBLIC HEALTH ENGLAND   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B;

APOPTOSIS; CARCINOGENESIS; CELL SURVIVAL; CELL TRANSFORMATION; CELL TYPE; COXSACKIE VIRUS B3; CYTOMEGALOVIRUS; GENE EXPRESSION; HUMAN IMMUNODEFICIENCY VIRUS 1; MODULATION; NONHUMAN; ONCOGENE; PRIORITY JOURNAL; RESPIRATORY SYNCYTIAL PNEUMOVIRUS; REVIEW; SIGNAL TRANSDUCTION; UPREGULATION; VIRION; VIRUS CELL INTERACTION; VIRUS INFECTION; VIRUS REPLICATION; VIRUS SURVIVAL;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; APOPTOSIS; PROTEIN-SERINE-THREONINE KINASES; PROTEIN-TYROSINE KINASES; PROTO-ONCOGENE PROTEINS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; VIRAL PHYSIOLOGY; VIRUS DISEASES; VIRUS LATENCY; VIRUS REPLICATION;

EID: 2442686585     PISSN: 00221317     EISSN: None     Source Type: Journal    
DOI: 10.1099/vir.0.19771-0     Document Type: Review

References (118)

1. Albini, A., Benelli, R., Presta, M., Rusnati, M., Ziche, M., Rubartelli, A., Paglialunga, P., Bussolino, F. & Noonan, D. (1996). HIV-tat protein is a heparin-binding angiogenic growth factor. Oncogene 12, 289-297.
2. Antman, K. & Chang, Y. (2000). Kaposi's sarcoma. N Engl J Med 342, 1027-1038.
3. Arora, V. K., Fredericksen, B. L. & Garcia, J. V. (2002). Nef: agent of cell subversion. Microbes Infect 4, 189-199.
4. Bais, C., Santomasso, B., Coso, O. & 8 other authors (1998). G-protein-coupled receptor of Kaposi's sarcoma-associated herpesvirus is a viral oncogene and angiogenesis activator. Nature 391, 86-89.
5. Baur, A. S., Sass, G., Laffert, B., Willbold, D., Cheng-Mayer, C. & Peterlin, B. M. (1997). The N-terminus of Nef from HIV-1/SIV associates with a protein complex containing Lck and a serine kinase. Immunity 6, 283-291.
6. Bellacosa, A., Testa, J. R., Staal, S. P. & Tsichlis, P. N. (1991). A retroviral oncogene, akt, encoding a serine-threonine kinase containing an SH2-like region. Science 254, 274-277.
7. Benn, J. & Schneider, R. J. (1994). Hepatitis B virus HBx protein activates Ras-GTP complex formation and establishes a Ras, Raf, MAP kinase signaling cascade. Proc Natl Acad Sci U S A 91, 10350-10354.
8. Benn, J., Su, F., Doria, M. & Schneider, R. J. (1996). Hepatitis B virus HBx protein induces transcription factor AP-1 by activation of extracellular signal-regulated and c-Jun N-terminal mitogen-activated protein kinases. J Virol 70, 4978-4985.
9. Bitko, V., Velazquez, A., Yang, L., Yang, Y. C. & Barik, S. (1997). Transcriptional induction of multiple cytokines by human respiratory syncytial virus requires activation of NF-κB and is inhibited by sodium salicylate and aspirin. Virology 232, 369-378.
10. Bottomley, M. J., Salim, K. & Panayotou, G. (1998). Phospholipid-binding protein domains. Biochim Biophys Acta 1436, 165-183.
11. Bresnahan, W. A., Thompson, E. A. & Albrecht, T. (1997). Human cytomegalovirus infection results in altered Cdk2 subcellular localization. J Gen Virol 78, 1993-1997.
12. Briand, G., Barbeau, B. & Tremblay, M. (1997). Binding of HIV-1 to its receptor induces tyrosine phosphorylation of several CD4-associated proteins, including the phosphatidylinositol 3-kinase. Virology 228, 171-179.
13. Brunet, A., Bonni, A., Zigmond, M. J., Lin, M. Z., Juo, P., Hu, L. S., Anderson, M. J., Arden, K. C., Blenis, J. & Greenberg, M. E. (1999). Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96, 857-868.
14. Burgering, B. M. & Medema, R. H. (2003). Decisions on life and death: FOXO Forkhead transcription factors are in command when PKB/Akt is off duty. J Leukoc Biol 73, 689-701.
15. Campbell, K. S., Ogris, E., Burke, B., Su, W., Auger, K. R., Druker, B. J., Schaffhausen, B. S., Roberts, T. M. & Pallas, D. C. (1994). Polyoma middle tumor antigen interacts with SHC via the NPTY (Asn-Pro-Thr-Tyr) motif in middle tumor antigen. Proc Natl Acad Sci U S A 91, 6344-6348.
16. Cantaluppi, V., Biancone, L., Boccellino, M., Doublier, S., Benelli, R., Carlone, S., Albini, A. & Camussi, G. (2001). HIV type 1 Tat protein is a survival factor for Kaposi's sarcoma and endothelial cells. AIDS Res Hum Retrovir 17, 965-976.
17. Cantrell, D. A. (2001). Phosphoinositide 3-kinase signalling pathways. J Cell Sci 114, 1439-1445.
18. Cardone, M. H., Roy, N., Stennicke, H. R., Salvesen, G. S., Franke, T. F., Stanbridge, E., Frisch, S. & Reed, J. C. (1998). Regulation of cell death protease caspase-9 by phosphorylation. Science 282, 1318-1321.
19. Carthy, C. M., Granville, D. J., Watson, K. A., Anderson, D. R., Wilson, J. E., Yang, D., Hunt, D. W. & McManus, B. M. (1998). Caspase activation and specific cleavage of substrates after coxsackievirus B3-induced cytopathic effect in HeLa cells. J Virol 72, 7669-7675.
20. Chan, T. O., Rittenhouse, S. E. & Tsichlis, P. N. (1999). AKT/PKB and other D3 phosphoinositide-regulated kinases: kinase activation by phosphoinositide-dependent phosphorylation. Annu Rev Biochem 68, 965-1014.
21. Chang, F., Lee, J. T., Navalonic, P. M., Steelman, L. S., Shelton, J. G., Blalock, W. L., Franklin, R. A. & McCubrey, J. A. (2003). Involvement of PI3K/Akt pathway in cell cycle progression, apoptosis, and neoplastic transformation: a target for cancer chemotherapy. Leukemia 17, 590-603.
22. Chang, Y. & Moore, P. S. (1996). Kaposi's sarcoma (KS)-associated herpesvirus and its role in KS. Infect Agents Dis 5, 215-222.
23. Chen, R. H., Su, Y. H., Chuang, R. L. & Chang, T. Y. (1998). Suppression of transforming growth factor-β-induced apoptosis through a phosphatidylinositol 3-kinase/Akt-dependent pathway. Oncogene 17, 1959-1968.
24. Cheng, E. H., Nicholas, J., Bellows, D. S., Hayward, G. S., Guo, H. G., Reitz, M. S. & Hardwick, J. M. (1997). A Bcl-2 homolog encoded by Kaposi's sarcoma-associated virus, human herpesvirus 8, inhibits apoptosis but does not heterodimerize with Bax or Bak. Proc Natl Acad Sci U S A 94, 690-694.
25. Choe, H., Farzan, M., Sun, Y. & 10 other authors (1996). The β-chemokine receptors CCR3 and CCR5 facilitate infection by primary HIV-1 isolates. Cell 85, 1135-1148.
26. Coffer, P. J. & Woodgett, J. R. (1991). Molecular cloning and characterisation of a novel putative protein-serine kinase related to the cAMP-dependent and protein kinase C families. Eur J Biochem 201, 475-481.
27. Collins, P. L., Chanock, R. M. & Murphy, B. R. (2001). Respiratory syncytial virus. In Fields Virology, 4th edn, pp. 1443-1486. Edited by D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman & S. E. Straus. Philadelphia: Lippincott Williams & Wilkins.
28. Cross, D. A., Alessi, D. R., Cohen, P., Anjelkovic, M. & Hemmings, B. A. (1995). Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378, 785-789.
29. Crusius, K., Auvinen, E., Steuer, B., Gaissert, H. & Alonso, A. (1998). The human papillomavirus type 16 E5-protein modulates ligand-dependent activation of the EGF receptor family in the human epithelial cell line HaCaT. Exp Cell Res 241, 76-83.
30. Dahl, J., Jurczak, A., Cheng, L. A., Baker, D. C. & Benjamin, T. L. (1998). Evidence of a role for phosphatidylinositol 3-kinase activation in the blocking of apoptosis by polyomavirus middle T antigen. J Virol 72, 3221-3226.
31. Dalgleish, A. G., Beverley, P. C., Clapham, P. R., Crawford, D. H., Greaves, M. F. & Weiss, R. A. (1984). The CD4 (T4) antigen is an essential component of the receptor for the AIDS retrovirus. Nature 312, 763-767.
32. Darr, C. D., Mauser, A. & Kenny, S. (2001). Epstein-Barr virus immediate-early protein BRLF1 induces the lytic form of viral replication through a mechanism involving phosphatidylinositol-3 kinase activation. J Virol 75, 6135-6142.
33. Datta, S. R., Dudek, H., Tao, X., Masters, S., Fu, H., Gotoh, Y. & Greenberg, M. E. (1997). Akt phosphorylation of BAD couples survival signals to the cell-intrinsic death machinery. Cell 91, 231-241.
34. Dawson, C. W., Tramountanis, G., Eliopoulos, A. G. & Young, L. S. (2003). Epstein-Barr virus latent membrane protein 1 (LMP1) activates the phosphatidylinositol 3-kinase/Akt pathway to promote cell survival and induce actin filament remodelling. J Biol Chem 278, 3694-3704.
35. Deregibus, M. C., Cantaluppi, V., Doublier, S., Brizzi, M. F., Deambrosis, I., Albini, A. & Camussi, G. (2002). HIV-1-Tat protein activates phosphatidylinositol 3-kinase/AKT-dependent survival pathways in Kaposi's sarcoma cells. J Biol Chem 277, 25195-25202.
36. Eliopoulos, A. G. & Young, L. S. (1998). Activation of the cJun N-terminal kinase (JNK) pathway by the Epstein-Barr virus-encoded latent membrane protein 1 (LMP1). Oncogene 16, 1731-1742.
37. Enamoto, N., Sakuma, I., Asahina, Y. & 7 other authors (1996). Mutations in the nonstructural protein 5A gene and response to interferon in patients with chronic hepatitis C virus 1b infection. N Engl J Med 334, 77-81.
38. Ensoli, B., Barillari, G., Salahuddin, S. Z., Gallo, R. C. & Wong-Staal, F. (1990). Tat protein of HIV-1 stimulates growth of cells derived from Kaposi's sarcoma lesions of AIDS patients. Nature 345, 84-86.
39. Ensoli, B., Buonaguro, L., Barillari, G., Fiorelli, V., Gendelman, R., Morgan, R. A., Wingfield, P. & Gallo, R. C. (1993). Release, uptake, and effects of extracellular human immunodeficiency virus type 1 Tat protein on cell growth and viral transactivation. J Virol 67, 277-287.
40. Eves, E. M., Xiong, W., Bellacosa, A., Kennedy, S. G., Tsichlis, P. N., Rosner, M. R. & Hay, N. (1998). Akt, a target of phosphatidylinositol 3-kinase, inhibits apoptosis in a differentiating neuronal cell line. Mol Cell Biol 18, 2143-2152.
41. Fackler, O. T., Luo, W., Geyer, M., Alberts, A. S. & Peterlin, B. M. (1999). Activation of Vav by Nef induces cytoskeletal rearrangements and downstream effector functions. Mol Cell 3, 729-739.
42. Fang, Y., Broder, C. C., Kennedy, P. E. & Berger, E. A. (1996). HIV-1 entry cofactor: functional cDNA cloning of a seven-transmembrane, G protein-coupled receptor. Science 272, 872-877.
43. Flemington, E. & Speck, S. H. (1990). Epstein-Barr virus BZLF1 trans activator induces the promoter of a cellular cognate gene, c-fos. J Virol 64, 4549-4552.
44. + T lymphocytes and macrophages. J Virol 77, 2539-2549.
45. Gallo, R. C. (1998). The enigmas of Kaposi's sarcoma. Science 282, 1837-1839.
46. Geleziunas, R., Xu, W., Takeda, K., Ichijo, H. & Greene, W. C. (2001). HIV-1 Nef inhibits ASK1-dependent death signalling providing a potential mechanism for protecting the infected host cell. Nature 410, 834-838.
47. Georgopoulou, U., Caravokiri, K. & Mavromara, P. (2003). Suppression of the ERK1/2 signaling pathway from HCV NS5A protein expressed by herpes simplex recombinant viruses. Arch Virol 148, 237-251.
48. Gires, O., Zimber-Strobl, U., Gonnella, R., Ueffing, M., Marschall, G., Zeidler, R., Pich, D. & Hammerschmidt, W. (1997). Latent membrane protein 1 of Epstein-Barr virus mimics a constitutively active receptor molecule. EMBO J 16, 6131-6140.
49. Gires, O., Kohlhuber, F., Kilger, E. & 7 other authors (1999). Latent membrane protein 1 of Epstein-Barr virus interacts with JAK3 and activates STAT proteins. EMBO J 18, 3064-3073.
50. Gold, M. R., Ingham, R. J., McLeod, S. J., Christian, S. L., Scheid, M. P., Duronio, V., Santos, L. & Matsuuchi, L. (2000). Targets of B-cell antigen receptor signaling: the phosphatidylinositol 3-kinase/ Akt/glycogen synthase kinase-3 signaling pathway and the Rap1 GTPase. Immunol Rev 176, 47-68.
51. Gottlieb, K. A. & Villarreal, L. P. (2001). Natural biology of polyomavirus middle T antigen. Microbiol Mol Biol Rev 65, 288-318.
52. Haeberle, H. A., Takizawa, R., Casola, A., Brasier, A. R., Dieterich, H. J., Van Rooijen, N., Gatalica, Z. & Garofalo, R. P. (2002). Respiratory syncytial virus-induced activation of nuclear factor-κB in the lung involves alveolar macrophages and toll-like receptor 4-dependent pathways. J Infect Dis 186, 1199-1206.
53. Hatano, E. & Brenner, D. A. (2001). Akt protects mouse hepatocytes from TNF-α- and Fas-mediated apoptosis through NF-κB activation. Am J Physiol Gastrointest Liver Physiol 281, G1357-1368.
54. Hawley-Nelson, P., Vousden, K. H., Hubbert, N. L., Lowy, D. R. & Schiller, J. T. (1989). HPV16 E6 and E7 proteins cooperate to immortalize human foreskin keratinocytes. EMBO J 8, 3905-3910.
55. He, Y., Nakao, H., Tan, S. L., Polyak, S. J., Neddermann, P., Vijaysri, S., Jacobs, B. L. & Katze, M. G. (2002). Subversion of cell signaling pathways by hepatitis C virus nonstructural 5A protein via interaction with Grb2 and P85 phosphatidylinositol 3-kinase. J Virol 76, 9207-9217.
56. Hwang, E. S., Nottoli, T. & Dimaio, D. (1995). The HPV-16 E5 protein: expression, detection, and stable complex formation with transmembrane proteins in COS cells. Virology 211, 227-233.
57. Izumi, K. M., Cahir McFarland, E. D., Ting, A. T., Riley, E. A., Seed, B. & Kieff, E. D. (1999). The Epstein-Barr virus oncoprotein latent membrane protein 1 engages the tumor necrosis factor receptor-associated proteins TRADD and receptor-interacting protein (RIP) but does not induce apoptosis or require RIP for NF-κB activation. Mol Cell Biol 19, 5759-5767.
58. Johnson, R. A., Huong, S. M. & Huang, E. S. (2000). Activation of the mitogen-activated protein kinase p38 by human cytomegalovirus infection through two distinct pathways: a novel mechanism for activation of p38. J Virol 74, 1158-1167.
59. Johnson, R. A., Ma, X. L., Yurochko, A. D. & Huang, E. S. (2001a). The role of MKK1/2 kinase activity in human cytomegalovirus infection. J Gen Virol 82, 493-497.
60. Johnson, R. A., Wang, X., Ma, X. L., Huong, S. M. & Huang, E. S. (2001b). Human cytomegalovirus up-regulates the phosphatidylinositol 3-kinase (PI3-K) pathway: inhibition of PI3-K activity inhibits viral replication and virus-induced signaling. J Virol 75, 6022-6032.
61. Jones, P. F., Jakubowicz, T., Pitossi, F. J., Maurer, F. & Hemmings, B. A. (1991). Molecular cloning and identification of a serine/ threonine protein kinase of the second-messenger subfamily. Proc Natl Acad Sci U S A 88, 4171-4175.
62. Joo, C. H., Hong, H. N., Kim, E. O. & 7 other authors (2003). Coxsackievirus B3 induces apoptosis in the early phase of murine myocarditis: a comparative analysis of cardiovirulent and non-cardiovirulent strains. Intervirology 46, 135-140.
63. Kaplan, D. R., Whitman, M., Schaffhausen, B., Raptis, L., Garcea, R. L., Pallas, D., Roberts, T. M. & Cantley, L. (1986). Phosphatidylinositol metabolism and polyoma-mediated transformation. Proc Natl Acad Sci U S A 83, 3624-3628.
64. Kaur, P., McDougall, J. K. & Cone, R. (1989). Immortalization of primary human epithelial cells by cloned cervical carcinoma DNA containing human papillomavirus type 16 E6/E7 open reading frames. J Gen Virol 70, 1261-1266.
65. Khwaja, A. (1999). Akt is more than just a Bad kinase. Nature 401, 33-34.
66. Kieff, E. & Rickinson, A. B. (2001). Epstein-Barr virus and its replication. In Fields Virology, 4th edn, pp. 2511-2574. Edited by D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman & S. E. Straus. Philadelphia: Lippincott Williams & Wilkins.
67. Kong, X., San Juan, H., Kumar, M., Behera, A. K., Mohapatra, A., Hellermann, G. R., Mane, S., Lockey, R. F. & Mohapatra, S. S. (2003). Respiratory syncytial virus infection activates STAT signaling in human epithelial cells. Biochem Biophys Res Commun 306, 616-622.
68. Kulik, G., Klippel, A. & Weber, M. J. (1997). Antiapoptotic signalling by the insulin-like growth factor I receptor, phosphatidylinositol 3-kinase, and Akt. Mol Cell Biol 17, 1595-1606.
69. Lan, K. H., Sheu, M. L., Hwang, S. J. & 8 other authors (2002). HCV NS5A interacts with p53 and inhibits p53-mediated apoptosis. Oncogene 21, 4801-4811.
70. Lee, Y. I., Kang-Park, S. & Do, S. I. (2001). The hepatitis B virus-X protein activates a phosphatidylinositol 3-kinase-dependent survival signaling cascade. J Biol Chem 276, 16969-16977.
71. Leslie, N. R., Downes, C. P., Maehama, T. & Dixon, J. E. (2002). PTEN: the down side of PI 3-kinase signalling. The tumor suppressor, PTEN/MMAC1, dephosphorylates the lipid second messenger, phosphatidylinositol 3,4,5-trisphosphate. Cell Signal 14, 285-295.
72. Linnemann, T., Zheng, Y. H., Mandic, R. & Peterlin, B. M. (2002). Interaction between Nef and phosphatidylinositol-3-kinase leads to activation of p21-activated kinase and increased production of HIV. Virology 294, 246-255.
73. Longnecker, R., Miller, C. L., Miao, X. Q., Marchini, A. & Kieff, E. (1992). The only domain which distinguishes Epstein-Barr virus latent membrane protein 2A (LMP2A) from LMP2B is dispensable for lymphocyte infection and growth transformation in vitro; LMP2A is therefore nonessential. J Virol 66, 6461-6469.
74. Maehama, T. & Dixon, J. E. (1999). PTEN: a tumour suppressor that functions as a phospholipid phosphatase. Trends Cell Biol 9, 125-128.
75. Miller, C. L., Lee, J. H., Kieff, E. & Longnecker, R. (1994). An integral membrane protein (LMP2) blocks reactivation of Epstein-Barr virus from latency following surface immunoglobulin crosslinking. Proc Natl Acad Sci U S A 91, 772-776.
76. Moore, P. S., Boshoff, C., Weiss, R. A. & Chang, Y. (1996). Molecular mimicry of human cytokine and cytokine response pathway genes by KSHV. Science 274, 1739-1744.
77. Mosialos, G., Birkenbach, M., Yalamanchili, R., VanArsdale, T., Ware, C. & Kieff, E. (1995). The Epstein-Barr virus transforming protein LMP1 engages signaling proteins for the tumor necrosis factor receptor family. Cell 80, 389-399.
78. Munger, K., Phelps, W. C., Bubb, V., Howley, P. M. & Schlegl, R. (1989). The E6 and E7 genes of the human papillomavirus type 16 together are necessary and sufficient for transformation of primary human keratinocytes. J Virol 63, 4417-4421.
79. Murakami, S. (1999). Hepatitis B virus X protein: structure, function and biology. Intervirology 42, 81-99.
80. Ozes, O. N., Mayo, L. D., Gustin, J. A., Pfeffer, S. R., Pfeffer, L. M. & Donner, D. B. (1999). NF-κB activation by tumour necrosis factor requires the Akt serine-threonine kinase. Nature 401, 82-85.
81. Pap, M. & Cooper, G. M. (1998). Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway. J Biol Chem 273, 19929-19932.
82. Pass, R. F. (2001). Cytomeglovirus. In Fields Virology, 4th edn, pp. 2675-2706. Edited by D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman & S. E. Straus. Philadelphia: Lippincott Williams & Wilkins.
83. Qadri, I., Iwahashi, M. & Simon, F. (2002). Hepatitis C virus NS5A protein binds TBP and p53, inhibiting their DNA binding and p53 interactions with TBP and ERCC3. Biochim Biophys Acta 1592, 193-204.
84. Rena, G., Guo, S., Cichy, S. C., Unterman, T. G. & Cohen, P. (1999). Phosphorylation of the transcription factor forkhead family member FKHR by protein kinase B. J Biol Chem 274, 17179-17183.
85. Rickinson, A. B. & Kieff, E. (2001). Epstein-Barr virus. In Fields Virology, 4th edn, pp. 2575-2628. Edited by D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman & S. E. Straus. Philadelphia: Lippincott Williams & Wilkins.
86. Roberts, M. L. & Cooper, N. R. (1998). Activation of a ras-MAPK-dependent pathway by Epstein-Barr virus latent membrane protein 1 is essential for cellular transformation. Virology 240, 93-99.
87. Romashkova, J. A. & Makarov, S. S. (1999). NF-κB is a target of Akt in anti-apoptotic PDGF signalling. Nature 401, 86-90.
88. Roulston, A., Marcellus, R. C. & Branton, P. E. (1999). Viruses and apoptosis. Annu Rev Microbiol 53, 577-628.
89. Scheid, M. P. & Woodgett, J. R. (2003). Unraveling the activation mechanism of protein kinase B/Akt. FEBS Letters 546, 108-112.
90. Scholle, F., Bendt, K. M. & Raab-Traub, N. (2000). Epstein-Barr virus LMP2A transforms epithelial cells, inhibits cell differentiation, and activates Akt. J Virol 74, 10681-10689.
91. Shih, W. L., Kuo, M. L., Chuang, S. E., Cheng, A. L. & Doong, S. L. (2000). Hepatitis B virus X protein inhibits transforming growth factor-β-induced apoptosis through the activation of phosphatidylinositol 3-kinase pathway. J Biol Chem 275, 25858-25864.
92. Shih, W. L., Kuo, M. L., Chuang, S. E., Cheng, A. L. & Doong, S. L. (2003). Hepatitis B virus X protein activates a survival signaling by linking SRC to phosphatidylinositol 3-kinase. J Biol Chem 278, 31807-31813.
93. Simmons, A., Aluvihare, V. & McMichael, A. (2001). Nef triggers a transcriptional program in T cells imitating single-signal T cell activation and inducing HIV virulence mediators. Immunity 14, 763-777.
94. Speck, P., Kline, K. A., Cheresh, P. & Longnecker, R. (1999). Epstein-Barr virus lacking latent membrane protein 2 immortalizes B cells with efficiency indistinguishable from that of wild-type virus. J Gen Virol 80, 2193-2203.
95. Staal, S. P., Hartley, J. W. & Rowe, W. P. (1977). Isolation of transforming murine leukemia viruses from mice with a high incidence of spontaneous lymphoma. Proc Natl Acad Sci U S A 74, 3065-3067.
96. Su, W., Liu, W., Schaffhausen, B. S. & Roberts, T. M. (1995). Association of Polyomavirus middle tumor antigen with phospholipase C-γ1. J Biol Chem 270, 12331-12334.
97. Summers, S. A., Lipfert, L. & Birnbaum, M. J. (1998). Polyoma middle T antigen activates the Ser/Thr kinase Akt in a PI3-kinase-dependent manner. Biochem Biophys Res Commun 246, 76-81.
98. Swart, R., Ruf, I. K., Sample, J. & Longnecker, R. (2000). Latent membrane protein 2A-mediated effects on the phosphatidylinositol 3-kinase/Akt pathway. J Virol 74, 10838-10845.
99. Tan, S. L., Nakao, H., He, Y., Vijaysri, S., Neddermann, P., Jacobs, B. L., Mayer, B. J. & Katze, M. G. (1999). NS5A, a nonstructural protein of hepatitis C virus, binds growth factor receptor-bound protein 2 adaptor protein in a Src homology 3 domain/ligand-dependent manner and perturbs mitogenic signaling. Proc Natl Acad Sci U S A 96, 5533-5538.
100. Thomas, K. W., Monick, M. M., Staber, J. M., Yarovinsky, T., Carter, A. B. & Hunninghake, G. W. (2002). Respiratory syncytial virus inhibits apoptosis and induces NF-κB activity through a phosphatidylinositol. 3-kinase-dependent pathway. J Biol Chem 277, 492-501.
101. Tyler, K. L. & Nathanson, N. (2001). Pathogenesis of viral infections. In Fields Virology, 4th edn, pp. 199-244. Edited by D. M. Knipe, P. M. Howley, D. E. Griffin, R. A. Lamb, M. A. Martin, B. Roizman & S. E. Straus. Philadelphia: Lippincott Williams & Wilkins.
102. Vanhaesebroeck, B. & Alessi, D. R. (2000). The PI3K-PDK1 connection: more than just a road to PKB. Biochem J 346, 561-576.
103. Vanhaesebroeck, B. & Waterfield, M. D. (1999). Signaling by distinct classes of phosphoinositide 3-kinases. Exp Cell Res 253, 239-254.
104. Vanhaesebroeck, B., Leevers, S. J., Ahmadi, K., Timms, J., Katso, R., Driscoll, P. C., Woscholski, R., Parker, P. J. & Waterfield, M. D. (2001). Synthesis and function of 3-phosphorylated inositol lipids. Annu Rev Biochem 70, 535-602.
105. Webster, M. A., Hutchinson, J. N., Rauh, M. J., Muthuswamy, S. K., Anton, M., Tortorice, C. G., Cardiff, R. D., Graham, F. L., Hassell, J. A. & Muller, W. J. (1998). Requirement for both Shc and phosphatidylinositol 3′ kinase signaling pathways in polyomavirus middle T-mediated mammary tumorigenesis. Mol Cell Biol 18, 2344-2359.
106. Whitman, M., Kaplan, D. R., Schaffhausen, B., Cantley, L. & Roberts, T. M. (1985). Association of phosphatidylinositol kinase activity with polyoma middle-T competent for transformation. Nature 315, 239-242.
107. Wolf, D., Witte, V., Laffert, B., Blume, K., Stromer, E., Trapp, S., d'Aloja, P., Schurmann, A. & Baur, A. S. (2001). HIV-1 Nef associated PAK and PI3-kinases stimulate Akt-independent Bad phosphorylation to induce anti-apoptotic signals. Nat Med 11, 1217-1224.
108. Yang, D., Yu, J., Luo, Z., Carthy, C. M., Wilson, J. E., Liu, Z. & McManus, B. M. (1999). Viral myocarditis: identification of five differentially expressed genes in coxsackievirus B3-infected mouse heart. Circ Res 84, 704-712.
109. Yang, C. H., Murti, A., Pfeffer, S. R., Kim, J. G., Donner, D. B. & Pfeffer, L. M. (2001). Interferon α/β promotes cell survival by activating nuclear factor κB through phosphatidylinositol 3-kinase and Akt. J Biol Chem 276, 13756-13761.
110. Yu, Y. & Alwine, J. C. (2002). Human cytomegalovirus major immediate-early proteins and simian virus 40 large T antigen can inhibit apoptosis through activation of the phosphatidylinositide 3′-OH kinase pathway and the cellular kinase Akt. J Virol 76, 3731-3738.
111. Yurochko, A. D., Mayo, M. W., Poma, E. E., Baldwin, A. S., Jr & Huang, E. S. (1997a). Induction of the transcription factor Sp1 during human cytomegalovirus infection mediates upregulation of the p65 and p105/p50 NF-κB promoters. J Virol 71, 4638-4648.
112. Yurochko, A. D., Hwang, E. S., Rasmussen, L., Keay, S., Pereira, L. & Huang, E. S. (1997b). The human cytomegalovirus UL55 (gB) and UL75 (gH) glycoprotein ligands initiate the rapid activation of Sp1 and NF-κB during infection. J Virol 71, 5051-5059.
113. Zalani, S., Holley-Guthrie, E. & Kenney, S. (1996). Epstein-Barr viral latency is disrupted by the immediate-early BRLF1 protein through a cell-specific mechanism. Proc Natl Acad Sci U S A 93, 9194-9199.
114. Zhang, B., Spandau, D. F. & Roman, A. (2002). E5 protein of human papillomavirus type 16 protects human foreskin keratinocyes from UV B-irradiation-induced apoptosis. J Virol 76, 220-231.
115. Zhang, H. M., Yuan, J., Cheung, P. & 9 other authors (2003). Overexpression of interferon-γ-inducible GTPase inhibits coxsackie-virus B3-induced apoptosis through the activation of the phosphatidylinositol 3-kinase/Akt pathway and inhibition of viral replication. J Biol Chem 278, 33011-33019.
116. Zhu, H., Shen, Y. & Shenk, T. (1995). Human cytomegalovirus IE1 and IE2 proteins block apoptosis. J Virol 69, 7960-7970.
117. zur Hausen, H. (2002). Papillomaviruses and cancer: from basic studies to clinical application. Nat Rev Cancer 2, 342-350.
118. zur Hausen, H. & de Villiers, E. M. (1994). Human papillomaviruses. Annu Rev Microbiol 48, 427-447.