The TORrid affairs of viruses: Effects of mammalian DNA viruses on the PI3K-Akt-mTOR signalling pathway

Nature Reviews Microbiology

Volumn 6, Issue 4, 2008, Pages 265-275

  Buchkovich, Nicholas J ^a   Yu, Yongjun ^a   Zampieri, Carisa A ^a   Alwine, James C ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; DNA; FK 506 BINDING PROTEIN; GUANOSINE TRIPHOSPHATE; HAMARTIN; INITIATION FACTOR 4F; MAMMALIAN TARGET OF RAPAMYCIN; PHOSPHATIDYLINOSITOL 3 KINASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; PHOSPHOPROTEIN PHOSPHATASE 2A; PROTEIN KINASE (CALCIUM,CALMODULIN) II; PROTEIN KINASE B; RHEB PROTEIN; RNA; STRUCTURAL PROTEIN; TUBERIN; VIRUS LARGE T ANTIGEN; PROTEIN KINASE; PROTEIN SERINE THREONINE KINASE; VIRUS DNA;

ADENOVIRUS; CALCIUM HOMEOSTASIS; CALCIUM SIGNALING; CARCINOGENESIS; CELL GROWTH; CELL MEMBRANE; CELL METABOLISM; CELL SURVIVAL; CELLULAR STRESS RESPONSE; DNA VIRUS; ENZYME ACTIVATION; ENZYME INHIBITION; HERPES VIRUS; HUMAN; INTERNAL RIBOSOME ENTRY SITE; MACROMOLECULE; MAMMAL; NONHUMAN; PATHOGENESIS; POLYOMA VIRUS; POXVIRUS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN PHOSPHORYLATION; REVIEW; RNA TRANSLATION; SIGNAL TRANSDUCTION; UTERINE CERVIX CANCER; VIRUS CELL INTERACTION; VIRUS INFECTION; VIRUS REPLICATION; WART VIRUS; ANIMAL; DRUG EFFECT; METABOLISM; PHYSIOLOGY;

DNA VIRUSES; MAMMALIA;

1-PHOSPHATIDYLINOSITOL 3-KINASE; ANIMALS; DNA VIRUSES; DNA, VIRAL; PROTEIN KINASES; PROTEIN-SERINE-THREONINE KINASES; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION; VIRUS REPLICATION;

EID: 40949116686     PISSN: 17401526     EISSN: None     Source Type: Journal    
DOI: 10.1038/nrmicro1855     Document Type: Review

References (122)

1. Cooray, S. The pivotal role of phosphatidylinositol-3-kinase-Akt signal transduction in virus survival. J. Gen. Virol. 85, 1065-1076 (2004).
2. Arsham, A. M., Howell, J. J. & Simon, M. C. A novel hypoxia-inducible factor-independent hypoxic response regulating mammalian target of rapamycin and its targets. J. Biol. Chem. 278, 29655-29660 (2003).
3. Kaufman, R. J. et al. The unfolded protein response in nutrient sensing and differentiation. Nature Rev. Mol. Cell Biol. 3, 411-421 (2002).
4. Wek, R. C., Jiang, H. Y. & Anthony, T G. Coping with stress: ElF2 kinases and translational control. Biochem. Soc. Trans. 34, 7-11 (2006).
5. Wouters, B. G et al. Control of the hypoxic response through regulation of mRNA translation. Sem. Cell Dev. Biol. 16, 487-501 (2005).
6. Holcik, M. & Sonenberg, N. Translational control in stress and apoptosis. Nature Rev. Mol. Cell Biol. 6, 318-327 (2005).
7. Beilacosa, A., Testa. J. R, Staal, S. P. & Tsichlis, P. N. A retroviral oncogene, akt. encoding a serine threonine kinase containing an SH2-like region. Science 254, 274-277 (1991).
8. Datta, S. R., Brunet, A. & Greenberg, M. E. Cellular survival: A play in three Akts. Genes Dev. 13, 2905-2927 (1999).
9. Sarbassov, D. D., Guertin, D. A., Ali, S. M. & Sabatini, D. M. Phosphorylation and regulation of Akt/PKB by the rictor-mTOR complex. Science. 307, 1098-1101 (2005).
10. Plas, D. R. & Thompson, C. B. Akt-dependent transformation: There is more to growth than just surviving. Oncogene 24, 7435-7442 (2005).
11. Baker, S. J. PTEN enters the nuclear age. Cell 128, 25-28 (2007).
12. Cass, L. A. et al. Protein kinase A-dependent and -independent signaling pathways contribute to cyclic AMP-stimulated proliferation. Mol. Cell. Biol. 19, 5882-5891 (1999).
13. Summers, S. A., Garza, L. A., Zhou, H. & Birnbaum, M. J. Regulation of insulin-stimulated glucose transporter GLUT4 translocation and Akt kinase activity by ceramide. Mol Cell. Biol. 18, 5457-5464 (1998).
14. Hill., M. M. et al. A role for protein kinase Bβ/Akt2 in insulin-stimulated GLUT4 translocation in adipocytes. Mol Cell. Biol. 19, 7771-7781 (1999).
15. Ueki, K. et al. Potential role of protein kinase B in insulin-induced glucose transport, glycogen synthesis, and protein synthesis. J. Biol. Chem. 273, 5315-5322 (1998).
16. Jozwiak, J. Hamartin and tuberin: Working together for tumour suppression. Int J. Cancer. 118, 1-5 (2006).
17. Krymskaya, V. P. Tumour suppressors hamartin and tuberin: Intracellular signalling. Cell. Signal. 15, 729-739 (2003).
18. Long, X., Lin, Y., Ortiz-Vega, S., Yonezawa, K. & Avruch, J. Rheb binds and regulates the mTOR kinase. Curr. Biol. 15, 702-713 (2005).
19. Long, X., Ortiz-Vega, S., Lin, Y. & Avruch, J. Rheb binding to mammalian target of rapamycin (mT0R) is regulated by amino acid sufficiency. J. Biol. Chem. 280, 23433-23436(2005).
20. Astrinidis, A. & Henske, E. P. Tuberous sclerosis complex: Linking growth and energy signaling pathways with human disease. Oncogene 24, 7475-7481 (2005).
21. Avruch, J. et al. Insulin and amino-acid regulation of mTOR signaling and kinase activity through the Rheb GTPase. Oncogene 25, 6361-6372 (2006).
22. Bai, X. et al. Rheb activates mTOR by antagonizing its endogenous inhibitor, FKBP38. Science 318, 977-980 (2007).
23. Kim, D. H. et al. mTOR interacts with raptor to form a nutrient-sensitive complex that signals to the cell growth machinery. Cell 110, 163-175 (2002).
24. Sarbassov, D. D. et al. Rictor, a novel binding partner of mTOR, defines a rapamycin-insensitive and raptor-independent pathway that regulates the cytoskeleton. Curr. Biol. 14, 1296-1302 (2004).
25. Kim, D. H. et al. GßL, a positive regulator of the rapamycin-sensitive pathway required for the nutrient-sensitive interaction between raptor and mTOR. Mol. Cell 11, 895-904 (2003).
26. Jacinto, E. et al. SIN 1/MIP 1 maintains rictor-mTOR complex integrity and regulates Akt phosphorylation and substrate specificity. Cell 127, 125-137 (2006).
27. Yang, O., Inoki, K., Ikenoue, T., Guan, K. L & Iaccheri, L. Identification of Sin I as an essential TORC2 component required for complex formation and kinase activity. Genes Dev. 20, 2820-2832 (2006).
28. Polak, P. & Hall, M. N. mTORC2 caught in a SiNful Akt. Dev. Cell 11, 433-434 (2006).
29. Sarbassov, D. D., Ali, S. M. & Sabatini, D. M. Growing roles for the mTOR pathway. Curr. Opin. Cell Biol. 17, 596-603(2005).
30. Reiling. J. H. & Sabatini, D. M. Stress and mTORture signaling. Oncogene 25, 6373-6383 (2006).
31. Mamane, Y, Petroulakis, E., LeBacquer, O. & Sonenberg, N. mTOR, translation initiation and cancer. Oncogene 25, 6416-6422 (2006).
32. Jacinto, E. et al. Mammalian TOR complex 2 controls the actin cytoskeleton and is rapamycin insensitive. Nature Cell Biol. 6 1122-1128 (2004).
33. Yang, O., Inoki, K., Kim, E. & Guan, K. L. TSC1/TSC2 and Rheb have different effects on TORC1 and.TORC2 activity. Proc. Natl Acad. Sci. USA 103, 6811-6816 (2006).
34. Brugarolas J. et al. Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev. 18, 2893-2904 (2004).
35. Arsham, A. M., Plas, D. R., Thompson, C. B. & Simon, M. C. P13-K/Akt signaling is neither required for hypoxic stabilization of HIF-1 nor sufficient for HIF-1-dependent target gene transcription. J. Biol. Chem. 277, 15162-15170 (2002).
36. Cai, S. L. et al. Activity of TSC2 is inhibited by AKT-mediated phosphorylation and membrane partitioning. J. Cell Biol. 173 279-289 (2006).
37. van den Beucken, T, Koritzinsky, M. & Wouters, B. G. Translational control of gene expression during hypoxia. Cancer Biol. Ther. 5 749-755 (2006).
38. Ellisen, L W. Growth control under stress: MTOR regulation through the REDD 1-TSC pathway. Cell Cycle 4, 1500-1502 (2005).
39. Schwarzer, R. et al. REDDI integrates hypoxia-mediated survival signaling downstream of phosphatidylinositol 3-kinase. Oncogene 24, 1138-1149 (2005).
40. Corradetti, M. N., Inoki, K., Bardeesy, N., DePinho, R. A, & Guan, K. L Regulation of the TSC pathway by LKB 1: Evidence of a molecular link between tuberous sclerosis complex and Peutz-Jeghers syndrome. Genes Dev. 18, 1533-1538 (2004).
41. Shaw, R. J. et al. The LKB1 tumor suppressor negatively regulates mTOR signaling. Cancer Cell 6, 91-99 (2004).
42. Kimble, S. R. Interaction between the AMP-activated protein kinase and mTOR signaling pathways. Med. Sci. Sports Exerc. 38, 1958-1964 (2006).
43. Luo, Z., Saha, A. K., Xiang, X. & Ruderman, N. B. AMPK, the metabolic syndrome and cancer. Trends Pharmocol. Sci. 26, 69-76 (2005).
44. Hardie, D.G. AMP-activated protein kinase as a drug target. Annu. Rev. Pharmacol Toxicol. 47, 185-210 2007).
45. Chami, M., Oules, B. & Paterlini-Brechot, P. Cytobiological consequences of calcium-signaling alterations induced by human viral protein. Biochim. Biophys Acta 1763, 1344-1362 (2006).
46. Avruch, J. et al. Insulin and amino-acid regulation of mTOR signaling and kinase activity through the Rheb GTPase. Oncogene 25, 6361-6372 (2006).
47. Vezina, C., Kudelski, A. & Sehgal, S. N. Rapamycin (AY-22,989), a new antifungal antibiotic. I. Taxonomy the producing streptomycete and isolation of the active principle. J. Antibiol. 28, 721-726 (1975).
48. Sarbassov, D. D. et at Prolonged rapamycin treatment inhibits mTORC2 assembly and Akt/PKB. Mol Cell 22, 159-168 (2006).
49. Zeng, Z. et al. Rapamycin derivatives reduce mTORC2 signaling and inhibit AKT activation in AMIL. Blood 109, 3509-3512(2007).
50. Gottlieb, K. A. & Villarreal, L. P. Natural biology of polyonnavirus middle T antigen. Microbiol. Mol. Biol. Rev. 65, 288-318 (2001).
51. Ichaso, N. & Dilworth, S. M. Cell transformation by the middle T-antigen of polyoma virus. Oncogene 20, 7908-7916 (2001)
52. Utermark, T, Schaffhausen, B. S., Roberts, T. M. & Zhao, J. J. The p 110α isofbrm of phosphatidylinositol 3-kinase is essential for polyomavirus middle T antigen-mediated transformation. J. Virol. 81, 7069-7076 (2007).
53. Summers, S. A., Lipfert, L. & Birnbaum, M. J. Polyoma middle T antigen activates the Ser/Thr kinase Akt in a PI3-kinase-dependent manner. Biochem. Biophys. Res. Commun. 246, 76-81 (1998).
54. Kaplan, D. R. et al. Common elements in growth factor stimulation and oncogenic transformation: 85 kd phosphoprotein and phosphatidylinositol kinase activity. Cell 50, 1021-1029 (1987).
55. Kaplan, D. R. et al. Phosphatidylinositol metabolism and polyoma-mediated transformation. Proc. Natl Acad. Sci. USA 83 3624-3628 (1986).
56. Whitman, M., Kaplan, D. R., Schaffhausen, B., Cantley, L. & Roberts, T. M. Association of phosphatidylinositol kinase activity with polyoma middle-T competent for transformation. Nature 315, 239-242 (1985).
57. Andrabi, S., Gjoerup, O. V., Kean, J. A., Roberts, T. M. & Schaffhausen, B. Protein phosphatase 2A regulates life and death decisions via Akt in a context-dependent manner. Proc. Natl Acad. Sci. USA 104, 19011-19016 (2007).
58. Simmons, D. T. SV40 large T antigen functions in DNA replication and transformation. Adv. Virus Res. 55, 75-134 (2000).
59. DeAngelis, T., Chen, J., Wu, A., Prisco, M. & Baserga, R. Transformation by the simian virus 40 T antigen is regulated by IGF-I receptor and IRS-1 signaling. Oncogene 25, 32-42 (2006).
60. Rundell, K. & Parakati, R. The role of the SV40 ST antigen in cell growth promotion and transformation. Semin. Cancer Biol. 11, 5-13 (2001).
61. Yang, S. I. et al. Control of protein phosphatase 2A by simian virus 40 small-t antigen. Mol. Cell. Biol. 11, 1988-1995 (1991).
62. Yang, C. S. et al. Simian virus 40 small t antigen mediates conformation-dependent transfer of protein phosphatase 2A onto the androgen receptor. Mol. Cell. Biol. 25, 1298-1308 (2005).
63. Yu, Y., Kudchodkar, S. B. & Alwine, J. C. Effects of simian virus 40 large and small tumor antigens on mammalian target of rapamycin (mTOR) signaling: Small tumor antigen mediates hypophosphorylation of eIF4E-binding protein 1 late in infection. J. Virol. 79, 6882-6889 (2005).
64. Yu, Y. & Alwine, J. C. 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 cellular kinase Akt. J. Virol. 76, 3731-3738 (2002).
65. Yuan, H., Veldman, T., Rundell, K. & Schlegel, R. Simian virus 40 small tumor antigen activates AKT and telomerase and induces anchorage-independent growth of human epithelial cells. J. Virol. 76, 10685-10691 (2002).
66. Backer, J. M. et al. Phosphatidylinositol 3′-kinase is activated by association with IRS-1 during insulin stimulation. EMBO J. 11, 3469-3479 (1992).
67. Lange-Mutschler, J., Deppert, W., Hanke, K. & Hennin, R. Detection of simian virus 40 T-antigen-related antigens by a 125I-protein A-binding assay and by immunofluorescence microscopy on the surface of SV40 transformed monolayer cells. J. Gen. Virol. 52, 301-312 (1981).
68. Lange-Mutschler, J. & Henning, R. A subclass of simian virus 40 T antigen with a high cell surface binding affinity. Virology 127 333-344 (1983).
69. Yu, Y. & Alwine, J. C. 19S late mRNAs of simian virus 40 have an internal ribosome entry site upstream of the virion structural protein 3 coding sequence. J. Virol. 80, 6553-6558 (2006).
70. Mirzamani, N., Salehian, P., Farhadi, M. & Tehran, E. A. Detection of EBV and HPV in nasopharyngeal carcinoma by in situ hybridization. Exp. Mol. Pathol. 81, 231-234 (2006).
71. Schiffman, M., Castle, P. E., Jeronimo, J., Rodriguez, A. C. & Wacholder, S. Human papillomavirus and cervical cancer. Lancet 370, 890-907 (2007).
72. Pim, D., Massimi, P., Dilworth, S. M. & Banks, L. Activation of the protein kinase B pathway by the HPV-16 E7 oncoprotein occurs through a mechanism involving interaction with PP2A. Oncogene 24, 7830-7838 (2005).
73. Menges, C. W., Baglia, L. A., Lapoint, R. & McCance, D. J. Human papillomavirus type 16 E7 up-regulates AKT activity through the retinoblastoma protein. Cancer Res. 66, 5555-5559 (2006).
74. Oh, K. J., Kalinina, A., Park, N. H. & Bagchi, S. Deregulation of e1F4E: 4E-BP1 in differentiated human papillomavirus-containing cells leads to high levels of expression of the E7 oncoprotein. J. Virol. 80 7079-7088 (2006).
75. Kim, S. H. et al. Human papillomavirus 16 E5 upregulates the expression of vascular endothelial growth factor through the activation of epidermal growth factor receptor, MEK/ERK1,2 and P13K/Akt. Cell. Mol. Life Sci. 63, 930-938 (2006).
76. Lu, Z. et al. Human papillomavirus 16 E6 oncoprotein interferences with insulin signaling pathway by binding to tuberin. J. Biol. Chem. 279, 35664-35670 (2004).
77. O'Shea, C. C., Choi, S., McCormick, F. & Stokoe, D. Adenovirus overrides cellular checkpoints for protein translation. Cell Cycle 4, 883-888 (2005).
78. Helt, A. M. & Galloway, D. A. Mechanims by which DNA tumor virus oncoproteins target the Rb family of pocket proteins. Carcinogenesis 24, 159-169 (2003).
79. Ouerido, E. et al. Degradation of p53 by adenovirus E4orf6 and E1 B55K proteins occurs via a novel mechanism involving a Cullin-containing complex. Genes Dev. 15, 3104-3117 (2001).
80. Querido, E. et al. Regulation of p53 levels by the E1B 55-kilodalton protein and E4orf6 in adenovirus-infected cells. J. Virol. 71, 3788-3798 (1997).
81. O'Shea, C. et al. Adenoviral proteins mimic nutrient/growth signals to activate the mTOR pathway for viral replication. EMBO J. 24, 1211-1221 (2005).
82. Gingras, A. C. & Sonenburg, N. Adenovirus infection inactivates the translational inhibitors 4E-BP1 and 4E-PB2. Virology 237, 182-186 (1997).
83. de Groot, R. P. et al. Induction of the mitogen-activated p70 S6 kinase by adenovirus E1A. Oncogene 10, 543-548 (1995).
84. Boyer, J. & Ketner, G. Manipulation of early region 4. Methods Mol. Med. 130, 1-17 (2007).
85. Frese, K. K. et al. Selective PDZ protein-dependent stimulation of phosphatidylinositol 3-kinase by the adenovirus E4-ORF1 oncoprotein. Oncogene 22, 710-721 (2003).
86. Kudchodkar, S., Yu, Y., Maguire, T. & Alwine, J. C. Human cytomegalovirus infection induces rapamycin insensitive phosphorylation of downstream effectors of mTOR kinase. J. Virol. 78, 11030-11039 (2004).
87. Kudchodkar, S. B., Del Prete, G. Q., Maguire, T. G. & Alwine, J. C. AMPK-mediated inhibition of mTOR kinase is circumvented during immediate-eady times of human cytomegalovirus infection. J. Virol. 81, 3649-3651 (2007).
88. Kudchodkar, S. B., Yu, Y., Maguire, T. G. & Nwine, J. C. Human cytomegalovirus infection alters the substrate specificities and rapamycin sensitivities of raptor- and rictor-containing complexes. Proc. Natl Acad. Sci. USA 103, 14182-14187 (2006).
89. Isler, J. A., Skalet, A. H. & Alwine, J. C. Human cytomegalovirus infection activates and regulates the unfolded protein response. J. Virol. 79, 6890-6899 (2005).
90. Isler, J. A., Maguire, T. G. & Alwine, J. C. Production of infectious HCMV virions is inhibited by drugs that disrupt calcium homeostasis in the endoplasmic reticulum. J. Virol. 79, 15338-15397 (2005).
91. Alwine, J. C. in Current Topics in Microbiology and Immunology Vol. 325 (eds Shenk, T. E. & Stinski, M. F.) 263-279 (Springer, New York, 2008).
92. Hakki, M. & Geballe, A. P. Double-stranded RNA binding by human cytomegalovirus pTRS1. J. Virol. 79, 7311-7318 (2005).
93. Walsh, D., Perez, C., Notary, J. & Mohr, I. Regulation of the translation initiation factor eIF4F by multiple mechanisms in human cytomegalovirus-infected cells. J. Virol. 79, 8057-8064 (2005).
94. Buchkovich, N. J. et al. Human cytomegalovirus specifically controls the levels of the endoplasmic reticulum chaperone BiP/GRP78, which is required for virion assembly. J. Virol. 82, 31-39 (2008).
95. Johnson, R. A., Wang, X., Ma, X. L., Huang, S. M. & Huang, E. S. Human cytomegalovirus up-regulates the phosphatidylinositol 3-kinase [P13-K) pathway: Inhibition of P13-K activity inhibits viral replication and virus-induced signaling. J. Virol. 75, 6022-6032 (2001).
96. Shen, Y. H. et al. Human cytomegalovirus inhibits Akt-mediated eNOS activation through upregulating PTEN (phosphatase and tensin homolog deleted on chromosome 10). Cardiovosc. Res. 69, 502-511 (2006).
97. Smith, C. C. The herpes simplex virus type 2 protein ICP10PK: A master of versatility. Front. Biosci. 10, 2820-2831 (2005).
98. Langelier, Y. et al. The R1 subunit of herpes simplex virus ribonucleotide reductase is a good substrate for host cell protein kinases but is not itself a protein kinase. J. Biol. Chem. 273 1435-1443 (1998).
99. Conner, J. The unique N terminus of herpes simplex virus type 1 ribonucleotide reductase large subunit is phosphorylated by casein kinase 2, which may have a homologue in Escherichia coli. J. Gen. Virol. 80, 1471-1476 (1999).
100. s3 mutant virus but only at early times after infection with wild-type herpes simplex virus 1. J. Virol. 80, 3341-3348 (2006).
101. Walsh, D. & Mohr, I. Phosphorylation of eIF4E by Mnk- 1 enhances HSV- 1 translation and replication in quiescent cells. Genes Dev. 18 660-672 (2004).
102. Walsh, D. & Mohr, I. Assembly of an active translation initiation factor complex by a viral protein. Genes Dev. 20, 461-472 (2006).
103. Rahaus, M., Desloges, N. & Wolff, M. H. Varicellazoster virus requires a functional P13K/Akt/GSK-3 signaling cascade for efficient replication. Cell. Signal. 19, 312-318 (2007).
104. Moody, C. A. et al. Modulation of the cell growth regulator mTOR by Epstein-Barr virus-encoded LMP2A. J. Virol. 79, 5499-5506 (2005).
105. Scholle, F., Bendt, K. M. & Raab-Traub, N. Epstein-Barr virus LMP2A transforms epithelial cells, inhibits cell differentiation, and activates Akt. J. Virol. 74, 10681-10689 (2000).
106. Swart, R., Ruf, I. K., Sample, J. & Longnecker, R. Latent membrane protein 2A-mediated effects on the phosphatidyiinositol 3-kinase/Akt pathway. J. Virol. 74, 10838-10845 (2000).
107. Sodhi, A. et al. 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 (2006).
108. Moss, B. in Field's Virology (eds Knipe, D. M. et al.) 2849-2883 (Lippincott Williams & Wilkins, Philadelphia, 2007).
109. Condit, R. C., Moussatche, N. & Traktman, P. In a nutshell: Structure and assembly of the vaccinia virion. Adv. Virus Res. 66, 31-124 (2006).
110. Venkatesan, S., Gershowitz, A. & Moss, B. Modification of the 5′ end of mRNA: Association of RNA triphosphatase with the RNA guanylyl-transferase-RNA (guanine-7) methyltransferase complex from vaccinia virus. J. Biol. Chem. 255, 903-908 (1980).
111. Walsh, D. et al. eIF4F architectural alterations accompany cellular translation initiation factor redistribution in poxvirus-infected cells. Mol. Cell. Biol. 4 Feb 2008 (doi: 10.1128/MCB.01631-07).
112. Kerr, P. & McFadden, G. Immune responses to myxoma virus. Viral Immunol. 15, 229-246 (2002).
113. Fenner, F. Adventures with poxviruses of vertebrates. FEMS Microbiol. Rev. 24, 123-133 (2000).
114. Jackson, E. W., Dorn, C. R., Saito, J. K. & McKercher, D. G. Absence of serological evidence of myxoma virus infection in humans exposed during an outbreak of myxomatosis. Nature 211, 313-314 (1966).
115. McFadden, C. Poxvirus tropism. Nature Rev. Microbiol. 3, 201-213 (2005).
116. Sypula, J., Wang, F., Ma, Y., Bell, J. C. & McFadden, G. Myxoma virus tropism in human tumor cells. Gene Ther. Mol. Biol. 8, 108-114 (2004).
117. Wang, G. et al. Infection of human cancer cells with myxoma virus requires Akt activation via interaction with a viral ankyrin-repeat host range factor. Proc. Natl Acad. Sci. USA 103, 4640-4645 (2006).
118. Schneider, R. J. & Mohr, I. Translation initiation and viral tricks. Trends Biochem. Sci. 28, 130-136 (2003).
119. Ryabova, L. A., Pooggin, M. M. & Hohn, T. Viral strategies of translation initiation: Ribosomal shunt and reinitiation. Prog. Nucleic Acid Res. Mol. Biol. 72, 1-39 (2002).
120. Hellen, C. U. T. & Sarnow, P. Internal ribosome entry sites in eukaryotic mRNA molecules. Genes Dev. 15, 1593-1612 (2001).
121. Flint, S. J., Enquist, L. W., Krug, R. M., Racaniello, V. R. & Skalka, A. M. (eds) Principles of Virology (American Society for Microbiology, Washington D. C., 2004).
122. Knipe, D. M. et al. (eds) Field's Virology (Lippincott Williams & Wilkins, Philadelphia, 2006).