Baculovirus IAP1 induces caspase-dependent apoptosis in insect cells

Journal of General Virology

Volumn 92, Issue 11, 2011, Pages 2654-2663

  Ikeda, Motoko ^a   Yamada, Hayato ^a   Ito, Hiroyuki ^a   Kobayashi, Michihiro ^a  

^a NAGOYA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

BOMBYX MORI DRONC CASPASE; CASPASE 3; INHIBITOR OF APOPTOSIS PROTEIN 1; INHIBITOR OF APOPTOSIS PROTEIN 3; INITIATOR CASPASE; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ANIMAL CELL; APOPTOSIS; ARTICLE; AUTOGRAPHA CALIFORNICA MULTIPLE NUCLEAR POLYHEDROSIS VIRUS; BACULOVIRUS; BOMBYX MORI NUCLEAR POLYHEDROSIS VIRUS; CELL STRUCTURE; CONTROLLED STUDY; ENZYME ACTIVITY; FLY; HYPHANTRIA CUNEA MULTIPLE NUCLEAR POLYHEDROSIS VIRUS; INSECT CELL; LEPIDOPTERA; NONHUMAN; ORGYIA PSEUDOTSUGATA MULTIPLE NUCLEAR POLYHEDROSIS VIRUS; PLASMID; PRIORITY JOURNAL; PROTEIN CLEAVAGE; PROTEIN EXPRESSION; SPILOSOMA IMPARILIS;

ANIMALS; APOPTOSIS; CASPASE 3; CELL LINE; HOST-PATHOGEN INTERACTIONS; INHIBITOR OF APOPTOSIS PROTEINS; LEPIDOPTERA; NUCLEOPOLYHEDROVIRUS; VIRAL PROTEINS;

AUTOGRAPHA CALIFORNICA MNPV; BOMBYX MORI NPV; DIPTERA; HEXAPODA; HYPHANTRIA CUNEA; INTRACISTERNAL A-PARTICLES; NUCLEOPOLYHEDROVIRUS; ORGYIA PSEUDOTSUGATA MNPV; SPILOSOMA; SPODOPTERA FRUGIPERDA;

EID: 80053133557     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.033332-0     Document Type: Article

References (64)

1. Birnbaum, M. J., Clem, R. J. & Miller, L. K. (1994). An apoptosisinhibiting gene from a nuclear polyhedrosis virus encoding a polypeptide with Cys/His sequence motifs. J Virol 68, 2521-2528.
2. Blissard, G. W. & Rohrmann, G. F. (1990). Baculovirus diversity and molecular biology. Annu Rev Entomol 35, 127-155.
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.
4. Clem, R. J. (2005). The role of apoptosis in defense against baculovirus infection in insects. Curr Top Microbiol Immunol 289, 113-129.
5. Clem, R. J. (2007). Baculoviruses and apoptosis: a diversity of genes and responses. Curr Drug Targets 8, 1069-1074.
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.
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.
8. Dorstyn, L. & Kumar, S. (2008). A biochemical analysis of the activation of the Drosophila caspase DRONC. Cell Death Differ 15, 461-470.
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.
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.
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.
12. Galluzzi, L., Brenner, C., Morselli, E., Touat, Z. & Kroemer, G. (2008). Viral control of mitochondrial apoptosis. PLoS Pathog 4, e1000018.
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.
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.
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.
16. Harvey, A. J., Soliman, H., Kaiser, W. J. & Miller, L. K. (1997). Antiand pro-apoptotic activities of baculovirus and Drosophila IAPs in an insect cell line. Cell Death Differ 4, 733-744.
17. Hay, S. & Kannourakis, G. (2002). A time to kill: viral manipulation of the cell death program. J Gen Virol 83, 1547-1564.
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.
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.
20. Hughes, P. R. & Wood, H. A. (1996). In vivo production, stabilization, and infectivity of baculovirus preoccluded virions. Appl Environ Microbiol 62, 105-108.
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.
22. Ikeda, M., Yanagimoto, K. & Kobayashi, M. (2004). Identification and functional analysis of Hyphantria cunea nucleopolyhedrovirus iap genes. Virology 321, 359-371.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
40. Mitsuhashi, J. & Maramorosch, K. (1964). Leafhopper tissue culture: embryonic, nymphal, and imaginal tissues from aseptic insects. Contrib Boyce Thompson Inst 22, 435-460.
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.
42. Muro, I., Monser, K. & Clem, R. J. (2004). Mechanism of Dronc activation in Drosophila cells. J Cell Sci 117, 5035-5041.
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.
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.
45. Orme, M. & Meier, P. (2009). Inhibitor of apoptosis proteins in Drosophila: gatekeepers of death. Apoptosis 14, 950-960.
46. Rohrmann, G. F. (2011). Baculovirus Molecular Biology, 2nd edn (Internet). Bethesda, MD: National Library of Medicine (US), National Center for Biotechnology Information.
47. Roulston, A., Marcellus, R. C. & Branton, P. E. (1999). Viruses and apoptosis. Annu Rev Microbiol 53, 577-628.
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.
49. Schneider, I. (1972). Cell lines derived from late embryonic stages of Drosophila melanogaster. J Embryol Exp Morphol 27, 353-365.
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.
51. Smith, G. E. & Summers, M. D. (1978). Analysis of baculovirus genomes with restriction endonucleases. Virology 89, 517-527.
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.
53. Srinivasula, S. M. & Ashwell, J. D. (2008). IAPs: what's in a name? Mol Cell 30, 123-135.
54. Teodoro, J. G. & Branton, P. E. (1997). Regulation of apoptosis by viral gene products. J Virol 71, 1739-1746.
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.
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.
57. Vaux, D. L. & Silke, J. (2005). IAPs, RINGs and ubiquitylation. Nat Rev Mol Cell Biol 6, 287-297.
58. Vilaplana, L. & O'Reilly, D. R. (2003). Functional interaction between Cydia pomonella granulovirus IAP proteins. Virus Res 92, 107-111.
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.
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.
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.
62. Williams, G. V. & Faulkner, P. (1997). Cytological changes and viral morphogenesis during baculovirus infection. In The Baculoviruses, pp. 61-107. Edited by L. K. Miller. New York: Plenum Press
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.
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.