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Invertebrate Iridovirus modulation of apoptosis

Virologica Sinica volume 24, pages 295–304 (2009)Cite this article

Abstract

Programmed cell death (apoptosis) is a key host response to virus infection. Viruses that can modulate host apoptotic responses are likely to gain important opportunities for transmission. Here we review recent studies that demonstrate that particles of Invertebrate iridescent virus 6 (IIV-6) (Iridoviridae, genus Iridovirus), or an IIV-6 virion protein extract, are capable of inducing apoptosis in lepidopteran and coleopteran cells, at concentrations 1000-fold lower than that required to shut-off host macromolecular synthesis. Induction of apoptosis depends on endocytosis of one or more heat-sensitive virion component(s). Studies with a JNK inhibitor (SP600125) indicated that the JNK signaling pathway is significantly involved in apoptosis in IIV-6 infections of Choristoneura fumiferana cells. The genome of IIV-6 codes for an inhibitor of apoptosis iap gene (193R) that encodes a protein of 208 aa with 15% identity and 28% similarity in its amino acid sequence to IAP-3 from Cydia pomonella ganulovirus (CpGV). Transcription of IIV-6 iap did not require prior DNA or protein synthesis, indicating that it is an immediate-early class gene. Transient expression and gene knockdown studies have confirmed the functional nature of the IIV-6 iap gene. We present a tentative model for IIV-6 induction and inhibition of apoptosis in insect cells and discuss the potential applications of these findings in insect pest control.

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References

  1. Balange-Orange N, Devauchelle G. 1982. Lipid composition of an iridescent virus type 6 (CIV). Arch Virol, 73: 363–367.

    Article  PubMed  CAS  Google Scholar 

  2. Bilimoria S L. 2001. Use of viral proteins for controlling the cotton boll weevil and other insect pests. United States Patent, No. 6200561 B1.

  3. 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  CAS  Google Scholar 

  4. Brennecke J, Hipfner D R, Stark A,et al. 2003. bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the pro-apoptotic gene hid in Drosophila. Cell, 113: 25–36.

    Article  PubMed  CAS  Google Scholar 

  5. Chen C H, Guo M, Hay B A. 2006. Identifying microRNA regulators of cell death in Drosophila. In: Methods in Molecular Biology: MicroRNA Protocols (Ying S Y ed.), Totowa, NJ: Humana Press. p. 229–240.

    Google Scholar 

  6. Chinchar V G, Bryan L, Wang J,et al. 2003. Induction of apoptosis in frog virus 3-infected cells. Virology, 306: 303–312.

    Article  PubMed  CAS  Google Scholar 

  7. Chinchar V G, Dholakia J N. 1989. Frog virus 3-induced translational shut-off: activation of an eIF2 kinase in virus-infected cells. Virus Res, 14: 207–224.

    Article  PubMed  CAS  Google Scholar 

  8. Chinchar V G, Essbauer S, He J G,et al. 2005. Iridoviridae. In Virus Taxonomy: VIII Report of the International Committee on the Taxonomy of Viruses (C. M. Fauquet, M. A. Mayo, J. Maniloff,et al. Eds.), London: Elsevier. p. 145–162.

    Google Scholar 

  9. Chinchar V G, Hyatt A, Miyazaki T,et al. 2009. Iridoviridae: poor viral relations no longer. Curr Top Microbiol Immunol, 328: 123–170.

    Article  PubMed  CAS  Google Scholar 

  10. Chitnis N S, D’Costa S M, Paul E R,et al. 2008. Modulation of iridovirus-induced apoptosis by endocytosis, early expression, JNK, and apical caspase. Virology, 370: 333–342.

    Article  PubMed  CAS  Google Scholar 

  11. Cullen B R. 2006. Viruses and microRNAs. Nat Genet, 38Suppl: 25–30.

    Article  Google Scholar 

  12. Constantino M, Christian P, Marina C F,et al. 2001. A comparison of techniques for detecting Invertebrate iridescent virus 6. J Virol Meth, 98: 109–118.

    Article  CAS  Google Scholar 

  13. 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  CAS  Google Scholar 

  14. Delhon G, Tulman E R, Afonso C L,et al. 2006. Genome of invertebrate iridescent virus type 3 (mosquito iridescent virus). J Virol, 80: 8439–8449.

    Article  PubMed  CAS  Google Scholar 

  15. Devauchelle G, Attias J, Monnier C,et al. 1985. Chilo iridescent virus. Curr Top Microbiol Immunol, 116, 37–48.

    PubMed  CAS  Google Scholar 

  16. Eaton H E, Metcalf J, Penny E,et al. 2007. Comparative genomic analysis of the family Iridoviridae: re-annotating and defining the core set of iridovirus genes. Virol J, 4: 11 doi: 10.1186/1743-422X-4-11

    Article  PubMed  Google Scholar 

  17. Essbauer S, Ahne W. 2002. The epizootic haematopoietic necrosis virus (Iridoviridae) induces apoptosis in vitro. J Vet Med B Infect Dis Vet Public Health, 49: 25–30.

    PubMed  CAS  Google Scholar 

  18. Federici B A. 1984. Diseases of terrestrial isopods. Symp Zool Soc Lond, 53: 233–245.

    Google Scholar 

  19. Fowler H G. 1989. An epizootic iridovirus of Orthoptera (Gryllotalpidae: Scapteriscus borellii) and its pathogenicity to termites (Isoptera: Cryptotermes). Rev Microbiol, 20: 115–120.

    Google Scholar 

  20. Fukaya M, Nasu S. 1966. A Chilo iridescent virus from the rice stem borer, Chilo supressalis Walker (Lepidoptera: Pyrallidae). Appl Entomol Zool, 1: 69–72.

    Google Scholar 

  21. Fukuda T. 1971. Per os transmission of Chilo iridescent virus to mosquitoes. J Invertebr Pathol, 18: 152–153.

    Article  PubMed  CAS  Google Scholar 

  22. Funk C J, Hunter W B, Achor D S. 2001. Replication of insect iridescent virus 6 in a whitefly cell line. J Invertebr Pathol, 77: 144–146.

    Article  PubMed  CAS  Google Scholar 

  23. Galluzzi L, Brenner C, Morselli E,et al. 2008. Viral control of mitochondrial apoptosis. PLoS Pathog, 4: e1000018.

  24. Grosholz E D. 1992. Interactions of intraspecific, interspecific and apparent competition with host-pathogen population dynamics. Ecology, 73: 507–514.

    Article  Google Scholar 

  25. Hay B A, Guo M. 2006. Caspase-dependent cell death in Drosophila. Annu Rev Cell Dev Biol, 22: 623–650.

    Article  PubMed  CAS  Google Scholar 

  26. Henderson C W, Johnson C L, Lodhi S A,et al. 2001. Replication of Chilo iridescent virus in the cotton boll weevil, Anthonomus grandis, and development of an infectivity assay. Arch Virol, 146: 767–775.

    Article  PubMed  CAS  Google Scholar 

  27. Holley C L, Olson R R, Colón-Ramos D A,et al. 2002. Reaper-mediated elimination of IAP proteins through stimulated IAP degradation and generalized translational inhibition. Nat Cell Biol, 4: 439–444.

    Article  PubMed  CAS  Google Scholar 

  28. Hu G B, Cong R S, Fan T J,et al. 2004. Induction of apoptosis in a flounder gill cell line by lymphocystis disease virus infection. J Fish Dis, 27: 657–662.

    Article  PubMed  Google Scholar 

  29. Huang X, Huang Y, Gong J,et al. 2008. Identification and characterization of a putative lipopolysaccharide-induced TNF-alpha factor (LITAF) homolog from Singapore grouper iridovirus. Biochem Biophys Res Commun, 373: 140–145.

    Article  PubMed  CAS  Google Scholar 

  30. Huang Y H, Huang X H, Gui J F,et al. 2007. Mitochondrion-mediated apoptosis induced by Rana grylio virus infection in fish cells. Apoptosis, 12: 1569–1577.

    Article  PubMed  Google Scholar 

  31. Hunter W B, Lapointe S L. 2003. Iridovirus infection of cell cultures from the Diaprepes root weevil, Diaprepes abbreviatus. J Insect Sci, 3: 37.

    PubMed  CAS  Google Scholar 

  32. Imajoh M, Sugiura H, Oshima S. 2004. Morphological changes contribute to apoptotic cell death and are affected by caspase-3 and caspase-6 inhibitors during red sea bream iridovirus permissive replication. Virology, 322: 220–230.

    Article  PubMed  CAS  Google Scholar 

  33. Ince I A, Westenberg M, Vlak J M,et al. 2008. Open reading frame 193R of Chilo iridescent virus encodes a functional inhibitor of apoptosis (IAP). Virology, 376: 124–131.

    Article  PubMed  CAS  Google Scholar 

  34. Jakob N J, Müller K, Bahr U,et al. 2001. Analysis of the first complete DNA sequence of an invertebrate iridovirus: coding strategy of the genome of Chilo iridescent virus. Virology, 286: 182–196.

    Article  PubMed  CAS  Google Scholar 

  35. Jensen D D, Hukuhara T, Tanada Y. 1972. Lethality of Chilo iridescent virus to Colladonus montana leafhoppers. J Invertebr Pathol, 19: 276–278.

    Article  Google Scholar 

  36. Just F T, Essbauer S S. 2001. Characterization of an iridescent virus isolated from Gryllus bimaculatus (Orthoptera: Gryllidae). J Invertebr Pathol, 77: 51–61.

    Article  PubMed  CAS  Google Scholar 

  37. Kelly D C, Robertson J S. 1973. Icosahedral cytoplasmic deoxyriboviruses. J Gen Virol, 20: 17–41 (suppl).

    Article  PubMed  Google Scholar 

  38. Kleespies R G, Tidona C A, Darai G. 1999. Characterization of a new iridovirus isolated from crickets and investigations on the host range. J Invertebr Pathol, 73: 84–90.

    Article  PubMed  Google Scholar 

  39. Lai Y S, Chiou P P, Chen W J,et al. 2008. Characterization of apoptosis induced by grouper iridovirus in two newly established cell lines from barramundi, Lates calcarifer (Bloch). J Fish Dis, 31: 825–834.

    Article  PubMed  CAS  Google Scholar 

  40. Lannan E, Vandergaast R, Friesen P D. 2007. Baculovirus caspase inhibitors P49 and P35 block virus-induced apoptosis downstream of effector caspase DrICE activation in Drosophila melanogaster cells. J Virol, 81: 9319–9330.

    Article  PubMed  CAS  Google Scholar 

  41. Lin P W, Huang Y J, John J A,et al. 2008. Iridovirus Bcl-2 protein inhibits apoptosis in the early stage of viral infection. Apoptosis, 13: 165–176.

    Article  PubMed  Google Scholar 

  42. Lockshin R A, Zakeri Z, Tilly J L. 1998. When Cells Die: A Comprehensive Evaluation of Apoptosis and Programmed Cell Death, New York: Wiley-Liss, p528.

    Google Scholar 

  43. López M, Rojas J C, Vandame R,et al. 2002. Parasitoid-mediated transmission of an iridescent virus. J Invertebr Pathol, 80: 160–170.

    Article  PubMed  Google Scholar 

  44. Marina C F, Arredondo-Jiménez J I, Castillo A,et al. 1999. Sublethal effects of iridovirus disease in a mosquito. Oecologia, 119: 383–388.

    Article  Google Scholar 

  45. Marina C F, Ibarra J E, Arredondo-Jiménez J I,et al. 2003. Adverse effects of covert iridovirus infection on life history and demographic parameters of Aedes aegypti. Entomol Exp Appl, 106: 53–61.

    Article  Google Scholar 

  46. McIntosh A H, Kimura M. 1974. Replication of the Chilo iridescent virus (CIV) in a poikilothermic vertebrate cell line. Intervirol, 4: 257–267.

    CAS  Google Scholar 

  47. McLaughlin R E, Scott H A, Bell M R. 1972. Infection of the boll weevil by Chilo iridescent virus. J Invertebr Pathol, 19: 285–290.

    Article  Google Scholar 

  48. Miller L K. 1997. Baculovirus interaction with host apoptotic pathways. J Cell Physiol, 173: 178–182.

    Article  PubMed  CAS  Google Scholar 

  49. Mitsuhashi J. 1967. Infection of the green rice hopper, Nephotetix cincticeps by Chilo iridescent virus. J Invertebr Pathol, 9: 432–436.

    Article  Google Scholar 

  50. Mullens B A, Velten R K, Federici B A. 1999. Iridescent virus infection in Culicoides variipennis sonorensis and interactions with the mermithid parasite Heleidomermis magnapapula. J Invertebr Pathol, 73: 231–233.

    Article  PubMed  CAS  Google Scholar 

  51. Nalcacioglu R, Ince I A, Demirbag Z. 2009. The biology of Chilo iridescent virus (Iridoviridae). Virol Sinica, 24(4): 285–294.

    Article  CAS  Google Scholar 

  52. Oberst A, Bender C, Green D R. 2008. Living with death: the evolution of the mitochondrial pathway of apoptosis in animals. Cell Death Differ, 15: 1149–1136.

    Article  Google Scholar 

  53. Ohba M. 1975. Studies on the parthogenesis of Chilo iridescent virus 3. Multiplication of CIV in the silkworm Bombyx mori L. and field insects. Sci Bull Fac Agr Kyushu Univ, 30: 71–81. (in Japanese)

    Google Scholar 

  54. Ohba M, Aizawa K. 1979. Multiplication of Chilo iridescent virus in noninsect arthropods. J Invertebr Pathol, 33: 278–283.

    Article  Google Scholar 

  55. Paul E R, Chitnis N S, Henderson C W,et al. 2007. Induction of apoptosis by iridovirus virion protein extract. Arch Virol, 152: 1353–1364.

    Article  PubMed  CAS  Google Scholar 

  56. Pomar N, Berlanga J J, Campuzano S,et al. 2003. Functional characterization of Drosophila melanogaster PERK eukaryotic initiation factor 2α (eIF2α) kinase. FEBS J, 270: 293–306

    CAS  Google Scholar 

  57. Seshagiri S, Miller L K. 1997. Baculovirus inhibitors of apoptosis (IAPs) black activation of Sf-caspase-1. Proc Natl Acad Sci USA, 94: 13606–13611.

    Article  PubMed  CAS  Google Scholar 

  58. Shiozaki E N, Chai J, Rigotti D J,et al. 2003. Mechanism of XIAP-mediated inhibition of caspase-9. Mol Cell, 11: 519–527.

    Article  PubMed  CAS  Google Scholar 

  59. Song W, Lin Q, Joshi S B,et al. 2006. Proteomic studies of the Singapore grouper iridovirus. Mol Cell Prot, 5.2: 256–264.

    Google Scholar 

  60. Stark A, Brennecke J, Russell R B,et al. 2003 Identification of Drosophila MicroRNA targets. PLoS Biol, 1: e60, doi: 10.1371/journal.pbio.0000060

    Article  PubMed  Google Scholar 

  61. Tidona C A, Darai G 1997. The complete DNA sequence of lymphocystis disease virus. Virology, 230: 207–216.

    Article  PubMed  CAS  Google Scholar 

  62. Tonka T, Weiser J. 2000. Iridovirus infection in mayfly larvae. J Invertebr Pathol, 76: 229–231.

    Article  PubMed  CAS  Google Scholar 

  63. Vaux D L, Silke J. 2005. IAPs, RINGs and ubiquitylation. Nat Rev Mol Cell Biol, 6: 287–297.

    Article  PubMed  CAS  Google Scholar 

  64. Williams T. 1993. Covert iridovirus infection of blackfly larvae. Proc R Soc B Biol Sci, 251: 225–230.

    Article  Google Scholar 

  65. Williams T. 2008 Natural invertebrate hosts to iridoviruses (Iridoviridae). Neotrop Entomol, 37: 615–632.

    Article  PubMed  Google Scholar 

  66. Williams T, Barbosa-Solomieu V, Chinchar V G. 2005. A decade of advances in iridovirus research. Adv Virus Res, 65: 173–248.

    Article  PubMed  CAS  Google Scholar 

  67. Williams T, Hernández O. 2006. Costs of cannibalism in the presence of an iridovirus pathogen of Spodoptera frugiperda. Ecol Entomol, 31: 106–113.

    Article  Google Scholar 

  68. Yu J Y, Silke J, Ekert P G. 2006. Inhibitor of apoptosis proteins and caspases. In: Apoptosis, Cell Signaling, and Human Diseases: Molecular Mechanisms (Srivastava R. ed.), Volume 2. Totowa, NJ: Humana Press. p. 313–334.

    Google Scholar 

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Authors and Affiliations

  1. Instituto de Ecología AC, Xalapa, Ver, 91070, Mexico

    Trevor Williams

  2. Abramson Cancer Center and Department of Cancer Biology, University of Pennsylvania, Philadelphia, PA, 19104, USA

    Nilesh S. Chitnis

  3. Department of Biological Sciences, The Center for Biotechnology and Genomics, Texas Tech University, Lubbock, TX, 79409-3131, USA

    Shän L. Bilimoria

Authors
  1. Trevor Williams
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  2. Nilesh S. Chitnis
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  3. Shän L. Bilimoria
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Corresponding author

Correspondence to Trevor Williams.

Additional information

Foundation items: SLB was supported in part by Research Enhancement Funds and Research Development Funds from the Office of the Vice-President for Research, Texas Tech University and the Texas Higher Education Coordinating Board. Support was also provided by the Department of Biological Sciences at Texas Tech University.

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Williams, T., Chitnis, N.S. & Bilimoria, S.L. Invertebrate Iridovirus modulation of apoptosis. Virol. Sin. 24, 295–304 (2009). https://doi.org/10.1007/s12250-009-3060-1

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  • DOI: https://doi.org/10.1007/s12250-009-3060-1

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Key words

  • Apoptosis
  • Invertebrate iridescent virus 6
  • Induction by endocytosis
  • Inhibition of apoptosis (iap) gene
  • Iridoviridae
  • JNK pathway involvement