1887

Abstract

Baculoviruses encode inhibitors of apoptosis (IAPs), which are classified into five groups, IAP1–5, based on their sequence homology. Most of the baculovirus IAPs with anti-apoptotic functions belong to the IAP3 group, with certain exceptions. The functional roles of IAPs from other groups during virus infection have not been well established. We have previously shown that multiple nucleopolyhedrovirus (HycuMNPV) encodes three genes, , and , and that only Hycu-IAP3 has anti-apoptotic activity against actinomycin D-induced apoptosis of 9 cells. In the present study, we demonstrate that transient expression of Hycu-IAP1 is capable of inducing apoptosis and/or stimulating caspase-3-like protease activity in various lepidopteran and dipteran cell lines. Transient-expression assay analysis also demonstrates that not only Hycu-IAP1 but also IAP1s from MNPV, NPV and MNPV (OpMNPV) are capable of inducing apoptosis, and that apoptosis induced by Hycu-IAP1 is precluded by the functional anti-apoptotic baculovirus protein Hycu-IAP3. In HycuMNPV-infected (SpIm) cells and OpMNPV-infected 652Y cells, caspase-3-like protease activity is markedly stimulated during the late stages of infection, and the caspase-3-like protease activity stimulated in HycuMNPV-infected SpIm cells is repressed by RNA interference-mediated silencing of . In addition, initiator caspase Bm-Dronc, the homologue of Dronc, is cleaved upon transfection of BM-N cells with a plasmid expressing Hycu-IAP1. These results provide the first evidence that baculovirus IAP1s act to induce caspase-dependent apoptosis, possibly by replacing the cellular IAP1 that prevents Dronc activation.

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2011-11-01
2024-03-28
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References

  1. Birnbaum M. J., Clem R. J., Miller L. K. 1994; An apoptosis-inhibiting gene from a nuclear polyhedrosis virus encoding a polypeptide with Cys/His sequence motifs. J Virol 68:2521–2528[PubMed]
    [Google Scholar]
  2. Blissard G. W., Rohrmann G. F. 1990; Baculovirus diversity and molecular biology. Annu Rev Entomol 35:127–155 [View Article][PubMed]
    [Google Scholar]
  3. Carpes M. P., de Castro M. E. B., Soares E. F., Villela A. G., Pinedo F. J. R., Ribeiro B. M. 2005; The inhibitor of apoptosis gene (iap-3) of Anticarsia gemmatalis multicapsid nucleopolyhedrovirus (AgMNPV) encodes a functional IAP. Arch Virol 150:1549–1562 [View Article][PubMed]
    [Google Scholar]
  4. Clem R. J. 2005; The role of apoptosis in defense against baculovirus infection in insects. Curr Top Microbiol Immunol 289:113–129 [View Article][PubMed]
    [Google Scholar]
  5. Clem R. J. 2007; Baculoviruses and apoptosis: a diversity of genes and responses. Curr Drug Targets 8:1069–1074 [View Article][PubMed]
    [Google Scholar]
  6. Clem R. J., Miller L. K. 1994; Control of programmed cell death by the baculovirus genes p35 and iap. . Mol Cell Biol 14:5212–5222[PubMed]
    [Google Scholar]
  7. Crook N. E., Clem R. J., Miller L. K. 1993; An apoptosis-inhibiting baculovirus gene with a zinc finger-like motif. J Virol 67:2168–2174[PubMed]
    [Google Scholar]
  8. Dorstyn L., Kumar S. 2008; A biochemical analysis of the activation of the Drosophila caspase DRONC. Cell Death Differ 15:461–470 [View Article][PubMed]
    [Google Scholar]
  9. Duckett C. S., Nava V. E., Gedrich R. W., Clem R. J., Van Dongen J. L., Gilfillan M. C., Shiels H., Hardwick J. M., Thompson C. B. 1996; A conserved family of cellular genes related to the baculovirus iap gene and encoding apoptosis inhibitors. EMBO J 15:2685–2694[PubMed]
    [Google Scholar]
  10. Felipe Alves C. A., Ishikawa H., Ikeda M., Kobayashi M. 2009; hycu-hr6, A large homologous region of the Hyphantria cunea nucleopolyhedrovirus genome, as a powerful and versatile enhancer in insect expression systems. Virus Genes 39:403–408 [View Article][PubMed]
    [Google Scholar]
  11. Fraser A. G., James C., Evan G. I., Hengartner M. O. 1999; Caenorhabditis elegans inhibitor of apoptosis protein (IAP) homologue BIR-1 plays a conserved role in cytokinesis. Curr Biol 9:292–302 [View Article][PubMed]
    [Google Scholar]
  12. Galluzzi L., Brenner C., Morselli E., Touat Z., Kroemer G. 2008; Viral control of mitochondrial apoptosis. PLoS Pathog 4:e1000018 [View Article][PubMed]
    [Google Scholar]
  13. Goodwin R. H., Tompkins G. J., McCawley P. 1978; Gypsy moth cell lines divergent in viral susceptibility. I. Culture and identification. In Vitro 14:485–494 [View Article][PubMed]
    [Google Scholar]
  14. Green M. C., Monser K. P., Clem R. J. 2004; Ubiquitin protein ligase activity of the anti-apoptotic baculovirus protein Op-IAP3. Virus Res 105:89–96 [View Article][PubMed]
    [Google Scholar]
  15. Griffiths C. M., Barnett A. L., Ayres M. D., Windass J., King L. A., Possee R. D. 1999; In vitro host range of Autographa californica nucleopolyhedrovirus recombinants lacking functional p35, iap1 or iap2. . J Gen Virol 80:1055–1066[PubMed]
    [Google Scholar]
  16. Harvey A. J., Soliman H., Kaiser W. J., Miller L. K. 1997; Anti- and pro-apoptotic activities of baculovirus and Drosophila IAPs in an insect cell line. Cell Death Differ 4:733–744 [View Article][PubMed]
    [Google Scholar]
  17. Hay S., Kannourakis G. 2002; A time to kill: viral manipulation of the cell death program. J Gen Virol 83:1547–1564[PubMed]
    [Google Scholar]
  18. Hebert C. G., Valdes J. J., Bentley W. E. 2009; Investigating apoptosis: characterization and analysis of Trichoplusia ni-caspase-1 through overexpression and RNAi mediated silencing. Insect Biochem Mol Biol 39:113–124 [View Article][PubMed]
    [Google Scholar]
  19. Hozak R. R., Manji G. A., Friesen P. D. 2000; The BIR motifs mediate dominant interference and oligomerization of inhibitor of apoptosis Op-IAP. Mol Cell Biol 20:1877–1885 [View Article][PubMed]
    [Google Scholar]
  20. Hughes P. R., Wood H. A. 1996; In vivo production, stabilization, and infectivity of baculovirus preoccluded virions. Appl Environ Microbiol 62:105–108[PubMed]
    [Google Scholar]
  21. Igaki T., Yamamoto-Goto Y., Tokushige N., Kanda H., Miura M. 2002; Down-regulation of DIAP1 triggers a novel Drosophila cell death pathway mediated by Dark and DRONC. J Biol Chem 277:23103–23106 [View Article][PubMed]
    [Google Scholar]
  22. Ikeda M., Yanagimoto K., Kobayashi M. 2004; Identification and functional analysis of Hyphantria cunea nucleopolyhedrovirus iap genes. Virology 321:359–371 [View Article][PubMed]
    [Google Scholar]
  23. Ikeda M., Shikata M., Shirata N., Chaeychomsri S., Kobayashi M. 2006; Gene organization and complete sequence of the Hyphantria cunea nucleopolyhedrovirus genome. J Gen Virol 87:2549–2562 [View Article][PubMed]
    [Google Scholar]
  24. Imai N., Matsuda N., Tanaka K., Nakano A., Matsumoto S., Kang W. 2003; Ubiquitin ligase activities of Bombyx mori nucleopolyhedrovirus RING finger proteins. J Virol 77:923–930 [View Article][PubMed]
    [Google Scholar]
  25. Ishikawa H., Ikeda M., Yanagimoto K., Alves C. A., Katou Y., Laviña-Caoili B. A., Kobayashi M. 2003; Induction of apoptosis in an insect cell line, IPLB-Ld652Y, infected with nucleopolyhedroviruses. J Gen Virol 84:705–714 [View Article][PubMed]
    [Google Scholar]
  26. Kamiya K., Okimoto N., Ikeda M., Kunimi Y., Kobayashi M., Kawamura S. 2003; Genotypic variation of a wild isolate of Hyphantria cunea nucleopolyhedrovirus. J Insect Biotechnol Sericology 72:57–64
    [Google Scholar]
  27. Katou Y., Ikeda M., Kobayashi M. 2001; Characterization of Bombyx mori nucleopolyhedrovirus infection of Spodoptera frugiperda cells. J Insect Biotechnol Sericology 70:137–147
    [Google Scholar]
  28. Katou Y., Ikeda M., Kobayashi M. 2006; Abortive replication of Bombyx mori nucleopolyhedrovirus in Sf9 and High Five cells: defective nuclear transport of the virions. Virology 347:455–465 [View Article][PubMed]
    [Google Scholar]
  29. Kawarabata T. 1974; Highly infectious free virions in the hemolymph of the silkworm (Bombyx mori) infected with a nuclear polyhedrosis virus. J Invertebr Pathol 24:196–200 [View Article][PubMed]
    [Google Scholar]
  30. Kawarabata T., Aratake Y. 1978; Functional differences between occluded and nonoccluded viruses of a nuclear polyhedrosis of the silkworm, Bombyx mori. . J Invertebr Pathol 31:329–336 [View Article][PubMed]
    [Google Scholar]
  31. Keddie B. A., Volkman L. E. 1985; Infectivity difference between the two phenotypes of Autographa californica nuclear polyhedrosis virus: importance of the 64K envelope glycoprotein. J Gen Virol 66:1195–1200 [View Article]
    [Google Scholar]
  32. Leisy D. J., Rohrmann G. F., Nesson M., Beaudreau G. S. 1986; Nucleotide sequencing and transcriptional mapping of the Orgyia pseudotsugata multicapsid nuclear polyhedrosis virus p10 gene. Virology 153:157–167 [View Article][PubMed]
    [Google Scholar]
  33. Liu Q., Clem R. J. 2011; Defining the core apoptosis pathway in the mosquito disease vector Aedes aegypti: the roles of iap1, ark, dronc, and effector caspases. Apoptosis 16:105–113 [View Article][PubMed]
    [Google Scholar]
  34. Liu Q., Qi Y., Chejanovsky N. 2003; Identification and classification of the Spodoptera littoralis nucleopolyhedrovirus inhibitor of apoptosis gene. Virus Genes 26:143–149 [View Article][PubMed]
    [Google Scholar]
  35. Luque T., Finch R., Crook N., O’Reilly D. R., Winstanley D. 2001; The complete sequence of the Cydia pomonella granulovirus genome. J Gen Virol 82:2531–2547[PubMed]
    [Google Scholar]
  36. Mace P. D., Shirley S., Day C. L. 2010; Assembling the building blocks: structure and function of inhibitor of apoptosis proteins. Cell Death Differ 17:46–53 [View Article][PubMed]
    [Google Scholar]
  37. Maguire T., Harrison P., Hyink O., Kalmakoff J., Ward V. K. 2000; The inhibitors of apoptosis of Epiphyas postvittana nucleopolyhedrovirus. J Gen Virol 81:2803–2811[PubMed]
    [Google Scholar]
  38. McLachlin J. R., Escobar J. C., Harrelson J. A., Clem R. J., Miller L. K. 2001; Deletions in the Ac-iap1 gene of the baculovirus AcMNPV occur spontaneously during serial passage and confer a cell line-specific replication advantage. Virus Res 81:77–91 [View Article][PubMed]
    [Google Scholar]
  39. Mitsuhashi J., Inoue H. 1988; Obtainment of a continuous cell line from the larval fat bodies of the mulberry tiger moth, Spilosoma imparilis (Lepidoptera: Arctiidae). Appl Entomol Zool (Jpn) 23:488–490
    [Google Scholar]
  40. Mitsuhashi J., Maramorosch K. 1964; Leafhopper tissue culture: embryonic, nymphal, and imaginal tissues from aseptic insects. Contrib Boyce Thompson Inst 22:435–460
    [Google Scholar]
  41. Muro I., Hay B. A., Clem R. J. 2002; The Drosophila DIAP1 protein is required to prevent accumulation of a continuously generated, processed form of the apical caspase DRONC. J Biol Chem 277:49644–49650 [View Article][PubMed]
    [Google Scholar]
  42. Muro I., Monser K., Clem R. J. 2004; Mechanism of Dronc activation in Drosophila cells. J Cell Sci 117:5035–5041 [View Article][PubMed]
    [Google Scholar]
  43. Nagamine T., Shimomura M., Sugimori H., Kobayashi M. 1989; Titration of Bombyx mori (Lepidoptera: Bombycidae) nuclear polyhedrosis virus in a Bombyx mori cell line. Appl Entomol Zool (Jpn) 24:235–237
    [Google Scholar]
  44. O’Riordan M. X. D., Bauler L. D., Scott F. L., Duckett C. S. 2008; Inhibitor of apoptosis proteins in eukaryotic evolution and development: a model of thematic conservation. Dev Cell 15:497–508 [View Article][PubMed]
    [Google Scholar]
  45. Orme M., Meier P. 2009; Inhibitor of apoptosis proteins in Drosophila: gatekeepers of death. Apoptosis 14:950–960 [View Article][PubMed]
    [Google Scholar]
  46. Rohrmann G. F. 2011 Baculovirus Molecular Biology, 2nd edn (Internet). Bethesda, MD: National Library of Medicine (US), National Center for Biotechnology Information;
    [Google Scholar]
  47. Roulston A., Marcellus R. C., Branton P. E. 1999; Viruses and apoptosis. Annu Rev Microbiol 53:577–628 [View Article][PubMed]
    [Google Scholar]
  48. Salvesen G. S., Duckett C. S. 2002; IAP proteins: blocking the road to death’s door. Nat Rev Mol Cell Biol 3:401–410 [View Article][PubMed]
    [Google Scholar]
  49. Schneider I. 1972; Cell lines derived from late embryonic stages of Drosophila melanogaster. . J Embryol Exp Morphol 27:353–365[PubMed]
    [Google Scholar]
  50. Seshagiri S., Miller L. K. 1997; Baculovirus inhibitors of apoptosis (IAPs) block activation of Sf-caspase-1. Proc Natl Acad Sci U S A 94:13606–13611 [View Article][PubMed]
    [Google Scholar]
  51. Smith G. E., Summers M. D. 1978; Analysis of baculovirus genomes with restriction endonucleases. Virology 89:517–527 [View Article][PubMed]
    [Google Scholar]
  52. Snipas S. J., Drag M., Stennicke H. R., Salvesen G. S. 2008; Activation mechanism and substrate specificity of the Drosophila initiator caspase DRONC. Cell Death Differ 15:938–945 [View Article][PubMed]
    [Google Scholar]
  53. Srinivasula S. M., Ashwell J. D. 2008; IAPs: what’s in a name?. Mol Cell 30:123–135 [View Article][PubMed]
    [Google Scholar]
  54. Teodoro J. G., Branton P. E. 1997; Regulation of apoptosis by viral gene products. J Virol 71:1739–1746[PubMed]
    [Google Scholar]
  55. Uren A. G., Coulson E. J., Vaux D. L. 1998; Conservation of baculovirus inhibitor of apoptosis repeat proteins (BIRPs) in viruses, nematodes, vertebrates and yeasts. Trends Biochem Sci 23:159–162 [View Article][PubMed]
    [Google Scholar]
  56. Uren A. G., Beilharz T., O’Connell M. J., Bugg S. J., van Driel R., Vaux D. L., Lithgow T. 1999; Role for yeast inhibitor of apoptosis (IAP)-like proteins in cell division. Proc Natl Acad Sci U S A 96:10170–10175 [View Article][PubMed]
    [Google Scholar]
  57. Vaux D. L., Silke J. 2005; IAPs, RINGs and ubiquitylation. Nat Rev Mol Cell Biol 6:287–297 [View Article][PubMed]
    [Google Scholar]
  58. Vilaplana L., O’Reilly D. R. 2003; Functional interaction between Cydia pomonella granulovirus IAP proteins. Virus Res 92:107–111 [View Article][PubMed]
    [Google Scholar]
  59. Volkman L. E., Goldsmith P. A. 1982; Generalized immunoassay for Autographa californica nuclear polyhedrosis virus infectivity in vitro . Appl Environ Microbiol 44:227–233[PubMed]
    [Google Scholar]
  60. Volkman L. E., Summers M. D. 1977; Autographa californica nuclear polyhedrosis virus: comparative infectivity of the occluded, alkali-liberated, and nonoccluded forms. J Invertebr Pathol 30:102–103 [View Article][PubMed]
    [Google Scholar]
  61. Volkman L. E., Summers M. D., Hsieh C.-H. 1976; Occluded and nonoccluded nuclear polyhedrosis virus grown in Trichoplusia ni: comparative neutralization comparative infectivity, and in vitro growth studies. J Virol 19:820–832[PubMed]
    [Google Scholar]
  62. Williams G. V., Faulkner P. 1997; Cytological changes and viral morphogenesis during baculovirus infection. In The Baculoviruses pp. 61–107 Edited by Miller L. K. New York: Plenum Press; [CrossRef]
    [Google Scholar]
  63. Yan N., Huh J. R., Schirf V., Demeler B., Hay B. A., Shi Y. 2006; Structure and activation mechanism of the Drosophila initiator caspase Dronc. J Biol Chem 281:8667–8674 [View Article][PubMed]
    [Google Scholar]
  64. Yan F., Deng X., Yan J., Wang J., Yao L., Lv S., Qi Y., Xu H. 2010; Functional analysis of the inhibitor of apoptosis genes in Antheraea pernyi nucleopolyhedrovirus. J Microbiol 48:199–205 [View Article][PubMed]
    [Google Scholar]
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