The west nile virus capsid protein blocks apoptosis through a phosphatidylinositol 3-kinase-dependent mechanism

Journal of Virology

Volumn 87, Issue 2, 2013, Pages 872-881

  Urbanowski, Matt D ^a   Hobman, Tom C ^a,b  

^a UNIVERSITY OF ALBERTA   (Canada)

^b UNIVERSITY OF ALBERTA   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

2 MORPHOLINO 8 PHENYLCHROMONE; AMINO ACID; CAPSID PROTEIN; CASPASE 3; CASPASE 8; GENOMIC RNA; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN KINASE B; VIRUS PROTEIN;

APOPTOSIS; ARTICLE; CELL DEATH; CELL LEVEL; CELL PROTECTION; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME PHOSPHORYLATION; HOST CELL; HUMAN; HUMAN CELL; MAMMAL CELL; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN SYNTHESIS; VIRUS ASSEMBLY; VIRUS CELL INTERACTION; VIRUS REPLICATION; VIRUS SURVIVAL; WEST NILE FLAVIVIRUS;

ANIMALS; APOPTOSIS; CAPSID PROTEINS; CELL LINE; CHROMONES; ENZYME INHIBITORS; HOST-PATHOGEN INTERACTIONS; HUMANS; MORPHOLINES; PHOSPHATIDYLINOSITOL 3-KINASE; WEST NILE VIRUS;

MIRIDAE; WEST NILE VIRUS;

EID: 84871941263     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02030-12     Document Type: Article

References (55)

1. Diamond MS. 2009. Progress on the development of therapeutics against West Nile virus. Antiviral Res. 83:214-227.
2. Smithburn KC, Hughes TP, Burke AW, Paul JH. 1940. A neurotropic virus isolated from the blood of a native of Uganda. Am. J. Trop. Med. Hyg. 20:471-492.
3. Lanciotti RS, Roehrig JT, Deubel V, Smith J, Parker M, Steele K, Crise B, Volpe KE, Crabtree MB, Scherret JH, Hall RA, MacKenzie JS, Cropp CB, Panigrahy B, Ostlund E, Schmitt B, Malkinson M, Banet C, Weissman J, Komar N, Savage HM, Stone W, McNamara T, Gubler DJ. 1999. Origin of the West Nile virus responsible for an outbreak of encephalitis in the northeastern United States. Science 286:2333-2337.
4. Brinton MA. 2002. The molecular biology of West Nile Virus: a new invader of the western hemisphere. Annu. Rev. Microbiol. 56:371-402.
5. Firth AE, Atkins JF. 2009. A conserved predicted pseudoknot in the NS2A-encoding sequence of West Nile and Japanese encephalitis flaviviruses suggests NS1' may derive from ribosomal frameshifting. Virol. J. 6:14.
6. Melian EB, Hinzman E, Nagasaki T, Firth AE, Wills NM, Nouwens AS, Blitvich BJ, Leung J, Funk A, Atkins JF, Hall R, Khromykh AA. 2010. NS1' of flaviviruses in the Japanese encephalitis virus serogroup is a product of ribosomal frameshifting and plays a role in viral neuroinvasiveness. J. Virol. 84:1641-1647.
7. Beatch MD, Everitt JC, Law LJ, Hobman TC. 2005. Interactions between rubella virus capsid and host protein p32 are important for virus replication. J. Virol. 79:10807-10820.
8. Hunt TA, Urbanowski MD, Kakani K, Law LM, Brinton MA, Hobman TC. 2007. Interactions between the West Nile virus capsid protein and the host cell-encoded phosphatase inhibitor, I2PP2A. Cell. Microbiol. 9:2756-2766.
9. Ilkow CS, Goping IS, Hobman TC. 2011. The rubella virus capsid is an anti-apoptotic protein that attenuates the pore-forming ability of Bax. PLoS Pathog. 7:e1001291. doi:10.1371/journal.ppat.1001291. 10. Ilkow CS, Mancinelli V, Beatch MD, Hobman TC. 2008. Rubella virus capsid protein interacts with poly(A)-binding protein and inhibits translation. J. Virol. 82:4284-4294.
10. Ilkow CS, Mancinelli V, Beatch MD, Hobman TC. 2008. Rubella virus capsid protein interacts with poly(A)-binding protein and inhibits translation. J. Virol. 82:4284-4294.
11. Ilkow CS, Weckbecker D, Cho WJ, Meier S, Beatch MD, Goping IS, Herrmann JM, Hobman TC. 2010. The rubella virus capsid protein inhibits mitochondrial import. J. Virol. 84:119-130.
12. Tzeng WP, Frey TK. 2005. Rubella virus capsid protein modulation of viral genomic and subgenomic RNA synthesis. Virology 337:327-334.
13. Xu Z, Anderson R, Hobman TC. 2011. The capsid-binding nucleolar helicase DDX56 is important for infectivity of West Nile virus. J. Virol. 85:5571-5580.
14. Kleinschmidt MC, Michaelis M, Ogbomo H, Doerr HW, Cinatl J, Jr. 2007. Inhibition of apoptosis prevents West Nile virus induced cell death. BMC Microbiol. 7:49. doi:10.1186/1471-2180-7-49.
15. Kobayashi S, Orba Y, Yamaguchi H, Kimura T, Sawa H. 2011. Accumulation of ubiquitinated proteins is related to West Nile virus-induced neuronal apoptosis. Neuropathology 32:398-405.
16. Medigeshi GR, Lancaster AM, Hirsch AJ, Briese T, Lipkin WI, Defilippis V, Fruh K, Mason PW, Nikolich-Zugich J, Nelson JA. 2007. West Nile virus infection activates the unfolded protein response, leading to CHOP induction and apoptosis. J. Virol. 81:10849-10860.
17. Parquet MC, Kumatori A, Hasebe F, Morita K, Igarashi A. 2001. West Nile virus-induced bax-dependent apoptosis. FEBS Lett. 500:17-24.
18. Smith JL, Grey FE, Uhrlaub JL, Nikolich-Zugich J, Hirsch AJ. 2012. Induction of the cellular microRNA, Hs_154, by West Nile virus contributes to virus-mediated apoptosis through repression of antiapoptotic factors. J. Virol. 86:5278-5287.
19. Gadaleta P, Perfetti X, Mersich S, Coulombie F. 2005. Early activation of the mitochondrial apoptotic pathway in vesicular stomatitis virusinfected cells. Virus Res. 109:65-69.
20. Lopez-Herrera A, Ruiz-Saenz J, Goez YP, Zapata W, Velilla PA, Arango AE, Urcuqui-Inchima S. 2009. Apoptosis as pathogenic mechanism of infection with vesicular stomatitis virus. Evidence in primary bovine fibroblast cultures. Biocell 33:121-132.
21. Pearce AF, Lyles DS. 2009. Vesicular stomatitis virus induces apoptosis primarily through Bak rather than Bax by inactivating Mcl-1 and Bcl-XL. J. Virol. 83:9102-9112.
22. Bhuvanakantham R, Cheong YK, Ng ML. 2010. West Nile virus capsid protein interaction with importin and HDM2 protein is regulated by protein kinase C-mediated phosphorylation. Microbes Infect. 12:615-625.
23. Oh W, Yang MR, Lee EW, Park KM, Pyo S, Yang JS, Lee HW, Song J. 2006. Jab1 mediates cytoplasmic localization and degradation of West Nile virus capsid protein. J. Biol. Chem. 281:30166-30174.
24. Yang JS, Ramanathan MP, Muthumani K, Choo AY, Jin SH, Yu QC, Hwang DS, Choo DK, Lee MD, Dang K, Tang W, Kim JJ, Weiner DB. 2002. Induction of inflammation by West Nile virus capsid through the caspase-9 apoptotic pathway. Emerg. Infect. Dis. 8:1379-1384.
25. Yang MR, Lee SR, Oh W, Lee EW, Yeh JY, Nah JJ, Joo YS, Shin J, Lee HW, Pyo S, Song J. 2008. West Nile virus capsid protein induces p53- mediated apoptosis via the sequestration of HDM2 to the nucleolus. Cell. Microbiol. 10:165-176.
26. Das S, Chakraborty S, Basu A. 2010. Critical role of lipid rafts in virus entry and activation of phosphoinositide 3' kinase/Akt signaling during early stages of Japanese encephalitis virus infection in neural stem/ progenitor cells. J. Neurochem. 115:537-549.
27. Lee CJ, Liao CL, Lin YL. 2005. Flavivirus activates phosphatidylinositol 3-kinase signaling to block caspase-dependent apoptotic cell death at the early stage of virus infection. J. Virol. 79:8388-8399.
28. + influx extends survival of West Nile virus-infected cells. J. Virol. 84:8721-8731.
29. Shrestha B, Diamond MS. 2007. Fas ligand interactions contribute to CD8+ T-cell-mediated control of West Nile virus infection in the central nervous system. J. Virol. 81:11749-11757.
30. Wang T, Town T, Alexopoulou L, Anderson JF, Fikrig E, Flavell RA. 2004. Toll-like receptor 3 mediates West Nile virus entry into the brain causing lethal encephalitis. Nat. Med. 10:1366-1373.
31. O'Donnell D, Milligan RL, Stark JM. 1999. Induction of CD95 (Fas) and apoptosis in respiratory epithelial cell cultures following respiratory syncytial virus infection. Virology 257:198-207.
32. Medigeshi GR, Hirsch AJ, Brien JD, Uhrlaub JL, Mason PW, Wiley C, Nikolich-Zugich J, Nelson JA. 2009. West Nile virus capsid degradation of claudin proteins disrupts epithelial barrier function. J. Virol. 83:6125-6134.
33. Amberg SM, Rice CM. 1999. Mutagenesis of the NS2B-NS3-mediated cleavage site in the flavivirus capsid protein demonstrates a requirement for coordinated processing. J. Virol. 73:8083-8094.
34. Lobigs M, Lee E, Ng ML, Pavy M, Lobigs P. 2010. A flavivirus signal peptide balances the catalytic activity of two proteases and thereby facilitates virus morphogenesis. Virology 401:80-89.
35. Stocks CE, Lobigs M. 1998. Signal peptidase cleavage at the flavivirus C-prM junction: dependence on the viral NS2B-3 protease for efficient processing requires determinants in C, the signal peptide, and prM. J. Virol. 72:2141-2149.
36. Megyeri K, Berencsi K, Halazonetis TD, Prendergast GC, Gri G, Plotkin SA, Rovera G, Gonczol E. 1999. Involvement of a p53-dependent pathway in rubella virus-induced apoptosis. Virology 259:74-84.
37. Borisevich V, Seregin A, Nistler R, Mutabazi D, Yamshchikov V. 2006. Biological properties of chimeric West Nile viruses. Virology 349:371-381.
38. Schoggins JW, Wilson SJ, Panis M, Murphy MY, Jones CT, Bieniasz P, Rice CM. 2011. A diverse range of gene products are effectors of the type I interferon antiviral response. Nature 472:481-485.
39. Chu JJ, Ng ML. 2003. The mechanism of cell death during West Nile virus infection is dependent on initial infectious dose. J. Gen. Virol. 84:3305-3314.
40. Samuel MA, Morrey JD, Diamond MS. 2007. Caspase 3-dependent cell death of neurons contributes to the pathogenesis of West Nile virus encephalitis. J. Virol. 81:2614-2623.
41. Sharif-Askari E, Nakhaei P, Oliere S, Tumilasci V, Hernandez E, Wilkinson P, Lin R, Bell J, Hiscott J. 2007. Bax-dependent mitochondrial membrane permeabilization enhances IRF3-mediated innate immune response during VSV infection. Virology 365:20-33.
42. Keckler MS. 2007. Dodging the CTL response: viral evasion of Fas and granzyme induced apoptosis. Front. Biosci. 12:725-732.
43. Ly JD, Grubb DR, Lawen A. 2003. The mitochondrial membrane potential (deltapsi(m)) in apoptosis; an update. Apoptosis 8:115-128.
44. Romanova LI, Lidsky PV, Kolesnikova MS, Fominykh KV, Gmyl AP, Sheval EV, Hato SV, van Kuppeveld FJ, Agol VI. 2009. Antiapoptotic activity of the cardiovirus leader protein, a viral "security" protein. J. Virol. 83:7273-7284.
45. Salako MA, Carter MJ, Kass GE. 2006. Coxsackievirus protein 2BC blocks host cell apoptosis by inhibiting caspase-3. J. Biol. Chem. 281: 16296-16304.
46. Diez H, Garrido JJ, Wandosell F. 2012. Specific roles of Akt iso forms in apoptosis and axon growth regulation in neurons. PLoS One 7:e32715. doi:10.1371/journal.pone.0032715.
47. Franke TF, Hornik CP, Segev L, Shostak GA, Sugimoto C. 2003. PI3K/Akt and apoptosis: size matters. Oncogene 22:8983-8998.
48. Kapoor V, Zaharieva MM, Das SN, Berger MR. 2012. Erufosine simultaneously induces apoptosis and autophagy by modulating the AktmTOR signaling pathway in oral squamous cell carcinoma. Cancer Lett. 319:39-48.
49. Yang CM, Lin CC, Lee IT, Lin YH, Chen WJ, Jou MJ, Hsiao LD. 2012. Japanese encephalitis virus induces matrix metalloproteinase-9 expression via a ROS/c-Src/PDGFR/PI3K/Akt/MAPKs-dependent AP-1 pathway in rat brain astrocytes. J. Neuroinflammation 9:12. doi:10.1186/1742-2094-9-12.
50. Lucas M, Mashimo T, Frenkiel MP, Simon-Chazottes D, Montagutelli X, Ceccaldi PE, Guenet JL, Despres P. 2003. Infection of mouse neurones by West Nile virus is modulated by the interferon-inducible 2'-5' oligoadenylate synthetase 1b protein. Immunol. Cell Biol. 81:230-236.
51. Brunet A, Bonni A, Zigmond MJ, Lin MZ, Juo P, Hu LS, Anderson MJ, Arden KC, Blenis J, Greenberg ME. 1999. Akt promotes cell survival by phosphorylating and inhibiting a Forkhead transcription factor. Cell 96: 857-868.
52. Hausler P, Papoff G, Eramo A, Reif K, Cantrell DA, Ruberti G. 1998. Protection of CD95-mediated apoptosis by activation of phosphatidylinositide 3-kinase and protein kinase B. Eur. J. Immunol. 28:57-69.
53. Shahbazian D, Roux PP, Mieulet V, Cohen MS, Raught B, Taunton J, Hershey JW, Blenis J, Pende M, Sonenberg N. 2006. The mTOR/PI3K and MAPK pathways converge on eIF4B to control its phosphorylation and activity. EMBO J. 25:2781-2791.
54. Fang M, Shen Z, Huang S, Zhao L, Chen S, Mak TW, Wang X. 2010. The ER UDPase ENTPD5 promotes protein N-glycosylation, the Warburg effect, and proliferation in the PTEN pathway. Cell 143:711-724.
55. Shen Z, Huang S, Fang M, Wang X. 2011. ENTPD5, an endoplasmic reticulum UDPase, alleviates ER stress induced by protein overloading in AKT-activated cancer cells. Cold Spring Harbor Symp. Quant. Biol. 76: 217-223.