Control of viral latency in neurons by axonal mTOR signaling and the 4E-BP translation repressor

Genes and Development

Volumn 26, Issue 14, 2012, Pages 1527-1532

  Kobayashi, Mariko ^a   Wilson, Angus C ^a   Chao, Moses V ^a   Mohr, Ian ^a  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

eIF4E binding protein 4E BP1; Local translational control; mTOR signaling; Neurons; Virus latency

Indexed keywords

INITIATION FACTOR 4E; MAMMALIAN TARGET OF RAPAMYCIN COMPLEX 1;

ARTICLE; CONTROLLED STUDY; HERPES SIMPLEX VIRUS 1; NERVE CELL CULTURE; NERVE FIBER; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; TRANSLATION REGULATION; VIRUS GENOME; VIRUS INHIBITION; VIRUS LATENCY;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ANIMALS; AXONS; CELLS, CULTURED; GENOME, VIRAL; HERPES SIMPLEX; HERPESVIRUS 1, HUMAN; PROTEINS; RATS; TOR SERINE-THREONINE KINASES; VIRUS LATENCY;

HUMAN HERPESVIRUS 1; RAPTORES;

EID: 84864007849     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.190157.112     Document Type: Article

References (41)

1. Bloom DC, Giordani NV, Kwiatkowski DL. 2010. Epigenetic regulation of latent HSV-1 gene expression. Biochim Biophys Acta 1799: 246-256.
2. Brugarolas J, Lei K, Hurley RL, Manning BD, Reiling JH, Hafen E, Witters LA, Ellisen LW, Kaelin WG Jr. 2004. Regulation of mTOR function in response to hypoxia by REDD1 and the TSC1/TSC2 tumor suppressor complex. Genes Dev 18: 2893-2904.
3. Calleja V, Laguerre M, Parker PJ, Larijani B. 2009. Role of a novel PHkinase domain interface in PKB/Akt regulation: Structural mechanism for allosteric inhibition. PLoS Biol 7: e17. doi: 10.1371/journal. pbio.1000017.
4. Camarena V, KobayashiM, Kim JY, Roehm P, Perez R, Gardner J, Wilson AC, Mohr I, Chao MV. 2010. Nature and duration of growth factor signaling through receptor tyrosine kinases regulates HSV-1 latency in neurons. Cell Host Microbe 8: 320-330.
5. Chao MV. 2003. Retrograde transport redux. Neuron 39: 1-2.
6. Connolly E, Braunstein S, Formenti S, Schneider RJ. 2006. Hypoxia inhibits protein synthesis through a 4E-BP1 and elongation factor 2 kinase pathway controlled by mTOR and uncoupled in breast cancer cells. Mol Cell Biol 26: 3955-3965.
7. Cox LJ, Hengst U, Gurskaya NG, Lukyanov KA, Jaffrey SR. 2008. Intraaxonal translation and retrograde trafficking of CREB promotes neuronal survival. Nat Cell Biol 10: 149-159.
8. Cunningham AL, Diefenbach RJ, Miranda-Saksena M, Bosnjak L, Kim M, Jones C, Douglas MW. 2006. The cycle of human herpes simplex virus infection: Virus transport and immune control. J Infect Dis 194: S11-S18. doi: 10.1086/505359.
9. Cushing H. 1905. The surgical aspects of major neuralgia of the trigeminal nerve. JAMA 44: 773-779.
10. Du T, Zhou G, Roizman B. 2011. HSV-1 gene expression from reactivated ganglia is disordered and concurrent with suppression of latencyassociated transcript and miRNAs. Proc Natl Acad Sci 108: 18820-18824.
11. Feldman ME, Apsel B, Uotila A, Loewith R, Knight ZA, Ruggero D, Shokat KM. 2009. Active-site inhibitors of mTOR target rapamycinresistant outputs of mTORC1 and mTORC2. PLoS Biol 7: e38. doi: 10.1371/journal.pbio.1000038.
12. Franklin JL, Johnson EM. 1998. Control of neuronal size homeostasis by trophic factor-mediated coupling of protein degradation to protein synthesis. J Cell Biol 142: 1313-1324.
13. Gingras AC, Gygi SP, Raught B, Polakiewicz RD, Abraham RT, HoekstraMF, Aebersold R, Sonenberg N. 1999. Regulation of 4E-BP1 phosphorylation: A novel two-step mechanism. Genes Dev 13: 1422-1437.
14. Goodpasture EW. 1929. Herpetic infection with especial reference to involvement of the nervous system. Medicine 8: 223-243.
15. Herman C, Ogura T, Tomoyasu T, Hiraga S, Akiyama Y, Ito K, Thomas R, D'Ari R, Bouloc P. 1993. Cell growth and l phage development controlled by the same Escherichia coli gene, ftsH/hflB. Proc Natl Acad Sci 90: 10861-10865.
16. Hill JM, Garza HH Jr, Helmy MF, Cook SD, Osborne PA, Johnson EM Jr, Thompson HW, Green LC, O'Callaghan RJ, Gebhardt BM. 1997. Nerve growth factor antibody stimulates reactivation of ocular herpes simplex virus type 1 in latently infected rabbits. J Neurovirol 3: 206-211.
17. Jeanneteau F, Deinhardt K, Miyoshi G, Bennett AM, Chao MV. 2010. The MAP kinase phosphatase MKP-1 regulates BDNF-induced axon branching. Nat Neurosci 13: 1373-1379.
18. Kim JY, Mandarino A, Chao M, Mohr I, Wilson AC. 2012. Transient reversal of episome silencing precedes VP16-dependent transcription during reactivation of latent HSV-1 in neurons. PLoS Pathog 8: e1002540. doi: 10.1371/journal.ppat.1002540.
19. +T cell inhibition of HSV-1 reactivation from neuronal latency. Science 322: 268-271.
20. Knipe DM, Cliffe A. 2008. Chromatin control of herpes simplex virus lytic and latent infection. Nat Rev Microbiol 6: 211-221.
21. Kobayashi M, Kim JY, Camarena V, Roehm PC, Chao MV, Wilson AC, Mohr I. 2012. A primary neuron culture system for the study of herpes simplex virus latency and reactivation. J Vis Exp 62: e3823. doi: 10.3791/3823.
22. Li Y, Inoki K, Guan KL. 2004. Biochemical and functional characterizations of small GTPase Rheb and TSC2 GAP activity. Mol Cell Biol 24: 7965-7975.
23. Lin AC, Holt CE. 2008. Function and regulation of local axonal translation. Curr Opin Neurobiol 18: 60-68.
24. Long X, Lin Y, Ortiz-Vega S, Yonezawa K, Avruch J. 2005. Rheb binds and regulates the mTOR kinase. Curr Biol 15: 702-713.
25. Ma XM, Blenis J. 2009. Molecular mechanisms of mTOR-mediated translational control. Nat Rev Mol Cell Biol 10: 307-318.
26. Magnuson B, Ekim B, Fingar DC. 2012. Regulation and function of ribosomal protein S6 kinase (S6K) within mTOR signalling networks. Biochem J 441: 1-21.
27. Martin DP, Schmidt RE, DiStefano PS, Lowry OH, Carter JG, Johnson EM Jr. 1988. Inhibitors of protein synthesis and RNA synthesis prevent neuronal death caused by nerve growth factor deprivation. J Cell Biol 106: 829-844.
28. Martin DP, Ito A, Horigome K, Lampe PA, Johnson EM Jr. 1992. Biochemical characterization of programmed cell death in NGFdeprived sympathetic neurons. J Neurobiol 23: 1205-1220.
29. Richter JD, Klann E. 2009. Making synaptic plasticity and memory last: Mechanisms of translational regulation. Genes Dev 23: 1-11.
30. Roizman B, Knipe DM, Whitley R. 2007. Herpes simplex viruses. In Fields' virology, 5th ed. (ed. DM Knipe, PM Howley), pp. 2501-2602. Lippincott, Williams & Wilkins, Philadelphia.
31. Sengupta S, Peterson TR, Sabatini DM. 2010. Regulation of the mTOR complex 1 pathway by nutrients, growth factors, and stress. Mol Cell 40: 310-322.
32. Taylor AM, Blurton-Jones M, Rhee SW, Cribbs DH, Cotman CW, Jeon NL. 2005. A microfluidic culture platform for CNS axonal injury, regeneration and transport. Nat Methods 2: 599-605.
33. Thompson RL, Preston CM, Sawtell NM. 2009. De novo synthesis of VP16 coordinates the exit from HSV latency in vivo. PLoS Pathog 5: e1000352. doi: 10.1371/journal.ppat.1000352
34. Thoreen CC, Kang SA, Chang JW, Liu Q, Zhang J, Gao Y, Reichling LJ, Sim T, Sabatini DM, Gray NS. 2009. An ATP-competitive mammalian target of rapamycin inhibitor reveals rapamycin-resistant functions of mTORC1. J Biol Chem 284: 8023-8032.
35. Umbach JL, Kramer MF, Jurak I, Karnowski HW, Coen DM, Cullen BR. 2008. MicroRNAs expressed by herpes simplex virus 1 during latent infection regulate viral mRNAs. Nature 454: 780-783.
36. Wagner EK, Bloom DC. 1997. Experimental investigation of herpes simplex virus latency. Clin Microbiol Rev 10: 419-443.
37. Walsh D, Mohr I. 2011. Viral subversion of the host protein synthesis machinery. Nat Rev Microbiol 9: 860-875.
38. Wilcox CL, Johnson EM Jr. 1987. Nerve growth factor deprivation results in the reactivation of latent herpes simplex virus in vitro. J Virol 61: 2311-2315.
39. Wilcox CL, Smith RL, Freed CR, Johnson EM Jr. 1990. Nerve growth factor-dependence of herpes simplex virus latency in peripheral sympathetic and sensory neurons in vitro. J Neurosci 10: 1268-1275.
40. Willis DE, Twiss JL. 2006. The evolving roles of axonally synthesized proteins in regeneration. Curr Opin Neurobiol 16: 111-118.
41. Zheng JQ, Kelly TK, Chang B, Ryazantsev S, Rajasekaran AK, Martin KC, Twill JL. 2001. A functional role for intra-axonal protein synthesis during axonal regeneration from adult sensory neurons. J Neurosci 21: 9291-9303.