Archives of Virology

, Volume 113, Issue 3–4, pp 165–176 | Cite as

Implication of mitochondria in the replication of Nodamura virus in larvae of the Lepidoptera,Galleria mellonella (L.) and in suckling mice

  • S. Garzon
  • H. Strykowski
  • G. Charpentier
Original Papers


The replication of Nodamura virus, type species of the familyNodaviridae, takes place principally into the interfibrillar spaces of the sarcoplasm in close association with mitochondria in the infected muscles of bothG. mellonella and suckling mice. The most striking event in infection ofG. mellonella muscle cells was the aggregation and shape modification of numerous mitochondria (elongation, interdigitation, and vesiculation) at an early stage of infection. These clusters of mitochondria were cemented by a thick electrondense material at the periphery of which viral particles undergo maturation process. In a later stage, degenerated and dilated mitochondria showed a clear assembling of virus particles on their outer membrane and occasionally on some inner membranes. These facts and the localization of RNA by RNase-gold technique in the assembling sites of viruses around and inside the mitochondria allowed us to postulate a role for the mitochondria as supports and/or energy suppliers for viral RNA synthesis and translation.


Muscle Cell Infectious Disease Outer Membrane Viral Particle Type Species 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.


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  1. 1.
    Bailey L, Newman JFE, Porterfield JS (1975) The multiplication of Nodamura virus in insect and mammalian cell cultures. J Gen Virol 26: 15–20Google Scholar
  2. 2.
    Bailey L, Scott HA (1973) The pathogenicity of Nodamura virus for insects. Nature 241: 545Google Scholar
  3. 3.
    Bashiruddin JB, Cross GF (1987) Boolarra virus: ultrastructure of intracytoplasmic virus formation in cultured Drosophila cells. J Invertebr Pathol 49: 303–315Google Scholar
  4. 4.
    Bendayan M (1984) Enzyme-gold electron microscopic cytochemistry: a new affinity approach for the ultrastructural localization of macromolecules. J Electron Microsc Tech 1: 349–372Google Scholar
  5. 5.
    Bienz K, Egger D, Pasamontes L (1987) Association of polioviral proteins of the P2 genomic region with the viral replication complex and virus-induced membrane synthesis as visualized by electron microscopic immunocytochemistry and autoradiography. Virology 160: 220–226Google Scholar
  6. 6.
    Bienz K, Egger D, Rasser Y, Bossart W (1983) Intracellular distribution of poliovirus proteins and the induction of virus-specific cytoplasmic structures. Virology 131: 39–48Google Scholar
  7. 7.
    Bienz K, Bienz-Isler G, Egger D, Weiss M, Loeffler H (1970) Coxsackievirus infection in skeletal muscles of mice. An electron microscopy study. II. Appearance and fate of virus progeny. Arch Ges Virusforsch 31: 257–265Google Scholar
  8. 8.
    Binnington KC (1987) Structural transformation of blowfly mitochondria by a putative virus: similarities with virus-induced changes in plant mitochondria. J Gen Virol 68: 201–206Google Scholar
  9. 9.
    Binnington KC, Lockie E, Hines E, van Gerwen ACM (1987) Fine structure and distribution of three types of virus-like particles in the sheep blowfly,Lucilia cuprina and associated cytopathic effects. J Invertebr Pathol 49: 175–187Google Scholar
  10. 10.
    Borges ML, David-Ferreira JF (1968) Comparative study of cell structures inDatura metel L. healthy and infected with potato virus X or virus Y. Revista Biol (Lisbon) 6: 421–427Google Scholar
  11. 11.
    Caliguiri L, Tamm I (1970) Characterization of poliovirus specific structures associated with cytoplasmic membranes. Virology 42: 112–122Google Scholar
  12. 12.
    Clerx CM, Bol JF (1978) Properties of solubilized RNA-dependent RNA polymerase from alfalfa mosaic virus-infected and healthy tobacco plants. Virology 91: 453–463Google Scholar
  13. 13.
    Di Franco A, Russo M, Martelli GP (1984) Ultrastructure and origin of cytoplasmic multivesicular bodies induced by carnation Italian ringspot virus. J Gen Virol 65: 1233–1237Google Scholar
  14. 14.
    Esau K (1979) Beet yellow stunt virus in cells ofSonchus oleraceus L. and its relation to host mitochondria. Virology 98: 1–8Google Scholar
  15. 15.
    Frens G (1973) Controlled nucleation for the regulation of particle size in monodisperse gold suspension. Nature Phys Sci 241, 20–30Google Scholar
  16. 16.
    Garzon S, Charpentier G (1990) Nodaviridae. In: Adams JR, Bonami J (eds) Atlas of invertebrate viruses. CRC Press, Boca Raton (in press)Google Scholar
  17. 17.
    Garzon S, Charpentier G, Kurstak E (1978) Morphogenesis of the Nodamura virus in the larvae of the lepidopteranGalleria mellonella (L.). Arch Virol 56, 61–76Google Scholar
  18. 18.
    Godman GC (1973) Picornaviruses. In: Dalton AJ, Haguenau F (eds) Ultrastructure of animal viruses and bacteriophages: an atlas. Academic Press, New York, pp 133–153 (Ultrastructure in biological systems, vol 5)Google Scholar
  19. 19.
    Guarino LA, Kaesberg P (1981) Isolation and characterization of an RNA-dependent RNA polymerase from black beetle virus-infectedDrosophila melanogaster cells. J Virol 40: 379–386Google Scholar
  20. 20.
    Harrison BD, Stefanac Z, Roberts IM (1970) Role of mitochondria in the formation of X-bodies in cells ofNicotiana clevelandii infected by tabacco rattle viruses. J Gen Virol 6: 127–140Google Scholar
  21. 21.
    Hatta T, Nakamoto T, Takagi Y, Ushiyama R (1971) Cytological abnormalities of mitochondria induced by infection with cucumber green mottle mosaic virus. Virology 45: 292–297Google Scholar
  22. 22.
    Kitajima EW, Lovisolo O (1972) Mitochondrial aggregates inDatura leaf cells infected with Henbane mosaic virus. J Gen Virol 16: 265–271Google Scholar
  23. 23.
    Larsen WJ (1970) Genesis of mitochondria in insect fat body. J Cell Biol 47: 373–383Google Scholar
  24. 24.
    Lesemann DE (1977) Virus group-specific and virus-specific cytological alterations induced by members of the tymovirus group. Phytopathol Z 90: 315–336Google Scholar
  25. 25.
    Murphy FA, Scherer WF, Harrison AK, Dunne HW, Gary Jr GM (1970) Characterization of Nodamura virus, an arthropod transmissible picornavirus. Virology 40: 1008–1021Google Scholar
  26. 26.
    Newman JFE, Brown F (1973) Evidence for a divided genome in Nodamura virus, an arthropod-borne picornavirus. J Gen Virol 21: 371–384Google Scholar
  27. 27.
    Newman JFE, Matthews T, Omilianowski DR, Salerno T, Kaesberg P Rueckert R (1978) In vitro translation of the two RNAs of Nodamura virus, a novel mammalian virus with a divided genome. J Virol 25: 78–85Google Scholar
  28. 28.
    Perry RP, Thorell B, Akerman L, Chance F (1959) Localization and assay of respiratory enzymes in single living cells. Absorbancy measurements on the “nebenkern”. Nature 184: 929–931Google Scholar
  29. 29.
    Pratt SA (1968) An electron microscope study of nebenkern formation and differentiation in spermatids ofMurgantia histrionica (Heminoptera, Pentatomidae). J Morphol 126: 31–36Google Scholar
  30. 30.
    Reinganum C, Bashiruddin JB, Cross GF (1985) Boolara virus: a member of the Nodaviridae isolated fromOncopera intricoides (Lepidoptera: Hepialidae). Intervirology 20: 10–17Google Scholar
  31. 31.
    Reynolds ES (1963) The use of lead citrate at high pH as an electron opaque stain in electron microscopy. J Cell Biol 17: 208–212Google Scholar
  32. 32.
    Russo M, Di Franco A, Martelli GP (1987) Cytopathology in the identification and classification of tombusviruses. Intervirology 28: 134–143Google Scholar
  33. 33.
    Scherer WF, Verna JE, Richter GW (1968) Nodamura virus, an ether and chloroform-resistant arbovirus from Japan. Am J Epidemiol 86: 120–128Google Scholar
  34. 34.
    Scherer WF, Hurlbut HS (1967) Nodamura virus from Japan: a new and unusual arbovirus resistant to diethyl ether and chloroform. Am J Epidemiol 86: 271–285Google Scholar
  35. 35.
    Takeda N, Kuhn RJ, Yang CF, Takegami T, Wimmer E (1986) Initiation of poliovirus plus-strand RNA synthesis in a membrane complex of infected HeLa cells. J Virol 60: 43–53Google Scholar
  36. 36.
    Tesh RB (1980) Infectivity and pathogenicity of Nodamura virus for mosquitoes. J Gen Virol 48: 177–182Google Scholar
  37. 37.
    Traub A, Diskin B, Rosenberg H, Kalmar E (1976) Isolation and properties of the replicase of encephalomyocarditis virus. J Virol 18: 375–382Google Scholar
  38. 38.
    Yin FH (1977) Involvement of viral procapsid in the RNA synthesis and maturation of poliovirus. Virology 82: 299–307Google Scholar
  39. 39.
    Zabel PH, Weenen-Swaans H, van Kammen A (1974) In vitro replication of cowpea mosaic virus RNA. I. Isolation and properties of the membrane-bound replicase. J Virol 14: 1049–1055Google Scholar

Copyright information

© Springer-Verlag 1990

Authors and Affiliations

  • S. Garzon
    • 1
  • H. Strykowski
    • 1
  • G. Charpentier
    • 2
  1. 1.Département de Microbiologie et d'Immunologie, Faculté de MédecineUniversité de MontréalMontréalCanada
  2. 2.Departement de Chimie-BiologieUniversité du Québec à Trois-RivièresTrois-RivièresCanada

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