Novel apoptosis suppressor apsup from the baculovirus Lymantria dispar multiple nucleopolyhedrovirus precludes apoptosis by preventing proteolytic processing of initiator caspase dronc

Journal of Virology

Volumn 87, Issue 23, 2013, Pages 12925-12934

  Yamada, Hayato ^a   Kitaguchi, Koji ^a   Hamajima, Rina ^a   Kobayashi, Michihiro ^a   Ikeda, Motoko ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

APSUP; INITIATOR CASPASE; INITIATOR CASPASE DRONC; MEMBRANE PROTEIN; UNCLASSIFIED DRUG;

ANIMAL CELL; APOPTOSIS; ARTICLE; BACULOVIRUS; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; IMMUNOBLOTTING; IMMUNOPRECIPITATION; LYMANTRIA DISPAR; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEGRADATION; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROCESSING; PROTEIN PROTEIN INTERACTION; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CASPASES; CELL LINE; DOWN-REGULATION; INHIBITOR OF APOPTOSIS PROTEINS; INSECT PROTEINS; MOTHS; NUCLEOPOLYHEDROVIRUS; PROTEIN BINDING; PROTEOLYSIS; VIRAL PROTEINS;

EID: 84887206197     PISSN: 0022538X     EISSN: 10985514     Source Type: Journal    
DOI: 10.1128/JVI.02065-13     Document Type: Article

References (63)

1. Best SM. 2008. Viral subversion of apoptotic enzymes:escape from death row. Annu. Rev. Microbiol. 62:171-192.
2. Roulston A, Marcellus RC, Branton PE. 1999. Viruses and apoptosis. Annu. Rev. Microbiol. 53:577-628.
3. Clarke TE, Clem RJ. 2003. Insect defenses against virus infection:the role of apoptosis. Int. Rev. Immunol. 22:401-424.
4. Clem RJ. 2005. The role of apoptosis in defense against baculovirus infection in insects. Curr. Top. Microbiol. Immunol. 289:113-130.
5. Ikeda M, Yamada H, Hamajima R, Kobayashi M. 2013. Baculovirus genes modulating intracellular innate antiviral immunity of lepidopteran insect cells. Virology 435:1-13.
6. Thiem SM. 2009. Baculovirus genes affecting host function. In Vitro Cell. Dev. Biol. Anim. 45:111-126.
7. Ishikawa H, Ikeda M, Yanagimoto K, Felipe Alves CA, Katou Y, Laviña-Caoili BA, Kobayashi M. 2003. Induction of apoptosis in an insect cell line, IPLB-Ld652Y, infected with nucleopolyhedroviruses. J. Gen. Virol. 84:705-714.
8. Ikeda M, Yanagimoto K, Kobayashi M. 2004. Identification and functional analysis of Hyphantria cunea nucleopolyhedrovirus iap genes. Virology 321:359-371.
9. Means JC, Muro I, Clem RJ. 2003. Silencing of the baculovirus Op-iap3 gene by RNA interference reveals that it is required for prevention of apoptosis during Orgyia pseudotsugataMnucleopolyhedrovirus infection of Ld652Y cells. J. Virol. 77:4481-4488.
10. Yamada H, Shibuya M, Kobayashi M, Ikeda M. 2011. Identification of a novel apoptosis suppressor gene from the baculovirus Lymantria diaper multicapsid nucleopolyhedrovirus. J. Virol. 85:5237-5242.
11. Clem RJ. 2007. Baculoviruses and apoptosis:a diversity of genes and responses. Curr. Drug Targets 8:1069-1074.
12. Means JC, Clem RJ. 2008. Evolution and function of the p35 family of apoptosis inhibitors. Future Virol. 3:383-391.
13. Clem RJ, Fechheimer M, Miller LK. 1991. Prevention of apoptosis by a baculovirus gene during infection of insect cells. Science 254:1388-1390.
14. Bertin J, Mendrysa SM, LaCount DJ, Gaur S, Krebs JF, Armstrong RC, Tomaselli KJ, Friesen PD. 1996. Apoptotic suppression by baculovirus P35 involves cleavage by and inhibition of a virus-induced CED-3/ICElike protease. J. Virol. 70:6251-6259.
15. Bump NJ, Hackett M, Hugunin M, Seshagiri S, Brady K, Chen P, Ferenz C, Franklin S, Ghayur T, Li P, Licari P, Mankovich J, Shi L, Greenberg AH, Miller LK, Wong WW. 1995. Inhibition of ICE family proteases by baculovirus antiapoptotic protein p35. Science 269:1885-1888.
16. Eddins MJ, Lemongello D, Friesen PD, Fisher AJ. 2002. Crystallization and low-resolution structure of an effector-caspase/P35 complex:similarities and differences to an initiator-caspase/P35 complex. Acta Crystallogr. D Crystallogr. 58(Pt 2):299-302.
17. Xu G, Cirilli M, Huang Y, Rich RL, Myszka DG, Wu H. 2001. Covalent inhibition revealed by the crystal structure of the caspase-8/p35 complex. Nature 410:494-497.
18. Xue D, Horvitz HR. 1995. Inhibition of the Caenorhabditis elegans celldeath protease CED-3 by a CED-3 cleavage site in baculovirus p35 protein. Nature 377:248-251.
19. Du Q, Lehavi D, Faktor O, Qi Y, Chejanovsky N. 1999. Isolation of an apoptosissuppressor gene of the Spodoptera littoralis nucleopolyhedrovirus. J. Virol. 73:1278-1285.
20. Pei Z, Reske G, Huang Q, Hammock BD, Qi Y, Chejanovsky N. 2002. Characterization of the apoptosis suppressor protein P49 from the Spodoptera littralis nucleopolyhedrovirus. J. Biol. Chem. 277:48677-48684.
21. Kim Y-S, Xiao H-Z, Du E-Q, Cai G-S, Lu S-Y, Qi Y-P. 2007. Identification and functional analysis of LsMNPV anti-apoptosis genes. J. Biochem. Mol. Biol. 40:571-576.
22. Lin T, Yu M, Wu W, Yu Q, Weng Q, Yang K, Yuan M, Pang Y. 2010. Functional analysis of Spodoptera litura nucleopolyhedrovirus p49 gene during Autographa californica nucleopolyhedrovirus infection of SpLi-221 cells. Virus Genes 41:441-449.
23. Yu M, Li Z, Yang K, Lin T, Gong Y, Pan L, Pang Y. 2005. Identification of the apoptosis inhibitor gene p49 of Spodoptera litura multicapsid nucleopolyhedrovirus. Virus Genes 31:145-151.
24. Yu Q, Lin T, Feng G, Yang K, Pang Y. 2008. Functional analysis of the putative antiapoptotic genes, p49, and iap4, of Spodoptera litura nucleopolyhedrovirus with RNAi. J. Gen. Virol. 89:1873-1880.
25. Jabbour AM, Ekert PG, Coulson EJ, Knight MJ, Ashley DM, Hawkins CJ. 2002. The p35 relative, p49, inhibits mammalian and Drosophila caspases including DRONC and protects against apoptosis. Cell Death Differ. 9:1311-1320.
26. Zoog SJ, Schiller JJ, Wetter JA, Chejanovsky N, Friesen PD. 2002. Baculovirus apoptotic suppressor P49 is a substrate inhibitor of initiator caspases resistant to P35 in vivo. EMBO J. 21:5130-5140.
27. Birnbaum MJ, Clem RJ, Miller LK. 1994. An apoptosis-inhibiting gene from a nuclear polyhedrosis virus encoding a polypeptide with Cys/His sequence motifs. J. Virol. 68:2521-2528.
28. Crook NE, Clem RJ, Miller LK. 1993. An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J. Virol. 67:2168-2174.
29. Luque T, Finch R, Crook N, O'Reilly DR, Winstanley D. 2001. The complete sequence of the Cydia pomonella granulovirus genome. J. Gen. Virol. 82:2531-2547.
30. Uren AG, Coulson EJ, Vaux DL. 1998. Conservation of baculovirus inhibitor of apoptosis repeat proteins (BIRPs) in viruses, nematodes, vertebrates and yeast. Trends Biochem. Sci. 23:159-162.
31. Verhagen AM, Coulson EJ, Vaux DL. 2001. Inhibitor of apoptosis proteins and their relatives:IAPs and other BIRPs. Genome Biol. 2:reviews3009-reviews3009.10. doi:10.1186/gb-2001-2-7-reviews3009.
32. Dubrez-Daloz L, Dupoux A, Cartier J. 2008. IAPs:more than just inhibitors of apoptotic proteins. Cell Cycle 7:1036-1046.
33. Gyrd-Hansen M, Meier P. 2010. IAPs:from caspase inhibitors to modulators of NF-kB, inflammation and cancer. Nat. Rev. Cancer 10:561-574.
34. Mace PD, Shirley S, Day CL. 2010. Assembling the building blocks: structure and function of inhibitor of apoptosis proteins. Cell Death Differ. 17:46-53.
35. Srinivasula SM, Ashwell JD. 2008. IAPs:what's in a name? Mol. Cell 30:123-135.
36. Goodwin RH, Tompkins GJ, McCawley P. 1978. Gypsy moth cell lines divergent in viral susceptibility. I. Culture and identification. In Vitro 14:485-494.
37. Luckow VE, Summers MD. 1988. Signals important for high-level expression of foreign genes in Autographa californica nuclear polyhedrosis virus expression vectors. Virology 167:56-71.
38. Schneider I. 1972. Cell lines derived from late embryonic stage of Drosophila melanogaster. J. Embryol. Exp. Morphol. 27:353-365.
39. Smith GE, Summers MD. 1978. Analysis of baculovirus genomes with restriction endonucleases. Virology 89:517-527.
40. Slavicek JM, Mercer MJ, Kelly ME, Hayes-Plazolles N. 1996. Isolation of a baculovirus variant that exhibits enhanced polyhedra production stability during serial passage in cell culture. J. Invertebr. Pathol. 67:153-160.
41. Clarke TE, Clem RJ. 2003. In vivo induction of apoptosis correlating with reduced infectivity during baculovirus infection. J. Virol. 77:2227-2232.
42. Du X, Thiem SM. 1997. Responses of insect cells to baculovirus infection: protein synthesis shutdown and apoptosis. J. Virol. 71:7866-7872.
43. Du X, Thiem SM. 1997. Characterization of host range factor 1 (hrf-1) expression in Lymantria dispar M nucleopolyhedrovirus-and recombinant Autographa californica M nucleopolyhedrovirus-infected IPLBLd652Y cells. Virology 227:420-430.
44. Shirata N, Ikeda M, Kobayashi M. 2010. Identification of a Hyphantria cunea nucleopolyhedrovirus (NPV) gene that is involved in global protein synthesis shutdown and restricted Bombyx mori NPV multiplication in a B. mori cell line. Virology 398:149-157.
45. Suganuma I, Ushiyama T, Yamada H, Iwamoto A, Kobayashi M, Ikeda M. 2011. Cloning and characterization of a dronc homologue in the silkworm, Bombyx mori. Insect Biochem. Mol. Biol. 41:909-921.
46. Kitaguchi K, Hamajima R, Yamada H, Kobayashi M, Ikeda M. 2013. Cloning and functional characterization of the Lymantria dispar initiator caspase dronc. Biochem. Biophys. Res. Commun. 436:331-337.
47. Yamada H, Okamoto K, Kobayashi M, Ikeda M. 2012. Cloning and characterization of an effector caspase, Ld-caspase-1, from the Lymantria dispar Ld652Y cells. J. Insect Biotechnol. Sericol. 81:75-83.
48. Yamada H, Shibuya M, Kobayashi M, Ikeda M. 2012. Baculovirus Lymantria dispar multiple nucleopolyhedrovirus IAP2 and IAP3 do not suppress apoptosis, but trigger apoptosis of insect cells in a transient expression assay. Virus Genes 45:370-379.
49. Kobayashi M, Kotake M, Sugimori H, Nagamine T, Kajiura Z. 1990. Identification of virus-specific polypeptides and translatable mRNAs in the isolated pupal abdomens of the silkworm, Bombyx mori, infected with nuclear polyhedrosis virus. J. Invertebr. Pathol. 55:52-60.
50. Sugimori H, Nagamine T, Kobayashi M. 1990. Analysis of structural polypeptides of Bombyx mori (Lepidoptera:Bombycidae) nuclear polyhedrosis virus. Appl. Entomol. Zool. 25:67-77.
51. Ikeda M, Yamada H, Ito H, Kobayashi M. 2011. Baculovirus IAP1 induces caspase-dependent apoptosis in insect cells. J. Gen. Virol. 92: 2654-2663.
52. Kitaguchi K, Hamajima R, Yamada H, Kobayashi M, Ikeda M. Transient expression assay reveals kinetic difference in the proteolytic processing between Dronc proteins from the gypsy moth Lymantria dispar and the silkworm Bombyx mori. J. Insect Biotechnol. Sericol., in press.
53. Hebert CG, Valdes JJ, Bentley WE. 2009. Investigating apoptosis:characterization and analysis of Trichplusia ni-caspase-1 through overexpression and RNAi mediated silencing. Insect Biochem. Mol. Biol. 39:113-124.
54. Schultz KLW, Friesen PD. 2009. Baculovirus DNA replication-specific expression factors trigger apoptosis and shutoff of host protein synthesis during infection. J. Virol. 83:11123-11132.
55. Salem TZ, Zhang F, Xie Y, Thiem SM. 2011. Comprehensive analysis of host gene expression in Autographa californica nucleopolyhedrovirusinfected Spodoptera frugiperda cells. Virology 412:167-178.
56. Xue J, Qiao N, Zhang W, Cheng R-L, Zhang X-Q, Bao Y-Y, Xu Y-P, Gu L-Z, Han J-DJ, Zhang C-X. 2012. Dynamic interactions between Bombyx mori nucleopolyhedrovirus and its host cells revealed by transcriptome analysis. J. Virol. 86:7345-7359.
57. Huang Q, Deveraux QL, Maeda S, Salvesen GS, Stennicke HR, Hammock BD, Reed JC. 2000. Evolutionary conservation of apoptosis mechanisms: lepidopteran and baculoviral inhibitor of apoptosis proteins are inhibitors of mammalian caspase-9. Proc. Natl. Acad. Sci. U.S.A. 97: 1427-1432.
58. Ahmad M, Srinivasule SM, Wang L, Litwack G, Fernandes-Alnemri T, Alnemri ES. 1997. Spodoptera frugiperda caspase-1, a novel insect death protease that cleaves the nuclear immunophilin FKBP46, is the target of the baculovirus antiapoptotic protein p35. J. Biol. Chem. 272:1421-1424.
59. Seshagiri S, Miller LK. 1997. Baculovirus inhibitors of apoptosis (IAPs) block activation of Sf-caspase-1. Proc. Natl. Acad. Sci. U.S.A. 94:13606-13611.
60. LaCount DJ, Hanson SF, Schneider CL, Friesen PD. 2000. Caspase inhibitor P35 and inhibitor of apoptosis Op-IAP block in vivo proteolytic activation of an effector caspase at different steps. J. Biol. Chem. 275: 15657-15664.
61. Manji GA, Hozak RR, LaCount DJ, Friesen PD. 1997. Baculovirus inhibitor of apoptosis functions at or upstream of the apoptotic suppressor P35 to prevent programmed cell death. J. Virol. 71:4509-4516.
62. Wright CW, Means JC, Penabaz T, Clem RJ. 2005. The baculovirus anti-apoptotic protein Op-IAP does not inhibit Drosophila caspases or apoptosis in Drosophila S2 cells and instead sensitizes S2 cells to virusinduced apoptosis. Virology 335:61-71.
63. Courtiade J, Pauchet Y, Vogel H, Heckel DG. 2011. A comprehensive characterization of the caspase gene family in insects from the order Lepidoptera. BMC Genomics 12:357. doi:10.1186/1471-2164-12-357.