Flock House Virus: A Model System for Understanding Non-Enveloped Virus Entry and Membrane Penetration

Chapter
Part of the Current Topics in Microbiology and Immunology book series (CT MICROBIOLOGY, volume 343)

Abstract

The means by which non-enveloped viruses penetrate cellular membranes during cell entry remain poorly defined. Recent findings indicate that several members of this group share a common mechanism of membrane penetration in which the virus particle undergoes programmed conformational changes, leading to capsid disassembly and release of small membrane-interacting peptides. Flock House Virus (FHV), a member of the nodaviridae family, offers some unique advantages for studying non-enveloped virus entry. The simplicity of the FHV capsid, coupled with a robust reverse genetics system for virus expression and an abundance of structural and biochemical data, make FHV an ideal model system for such studies. Here, we review the FHV atomic structure and examine how these molecular details provide insight into the mechanism of FHV entry. In addition, recent studies of FHV entry are discussed and a current model of FHV entry and membrane penetration is presented. A complete understanding of host cell entry by this minimal system will help elucidate the mechanisms of non-enveloped virus membrane penetration in general.

References

  1. Ball LA, Amann JM et al (1992) Replication of nodamura virus after transfection of viral RNA into mammalian cells in culture. J Virol 66(4):2326–2334PubMedGoogle Scholar
  2. Banerjee M, Johnson JE (2008) Activation, exposure and penetration of virally encoded, membrane-active polypeptides during non-enveloped virus entry. Curr Protein Pept Sci 9(1):16–27PubMedCrossRefGoogle Scholar
  3. Banerjee M, Khayat R et al (2009) Dissecting the functional domains of a non-enveloped virus membrane penetration peptide. J Virol 83(13):6929–6933PubMedCrossRefGoogle Scholar
  4. Banerjee M, Speir JA et al (2010) Structure and function of a genetically engineered mimic of a non-enveloped virus entry intermediate. J of Virology 2010, Feb 17 [Epub ahead of print]Google Scholar
  5. Bong DT, Steinem C et al (1999) A highly membrane-active peptide in Flock House virus: implications for the mechanism of nodavirus infection. Chem Biol 6(7):473–481PubMedCrossRefGoogle Scholar
  6. Bong DT, Janshoff A et al (2000) Membrane partitioning of the cleavage peptide in Flock House virus. Biophys J 78(2):839–845PubMedCrossRefGoogle Scholar
  7. Bothner B, Dong XF et al (1998) Evidence of viral capsid dynamics using limited proteolysis and mass spectrometry. J Biol Chem 273(2):673–676PubMedCrossRefGoogle Scholar
  8. Bothner B, Schneemann A et al (1999) Crystallographically identical virus capsids display different properties in solution. Nat Struct Biol 6(2):114–116PubMedCrossRefGoogle Scholar
  9. Chandran K, Nibert ML (2003) Animal cell invasion by a large nonenveloped virus: reovirus delivers the goods. Trends Microbiol 11(8):374–382PubMedCrossRefGoogle Scholar
  10. Chao JA, Lee JH et al (2005) Dual modes of RNA-silencing suppression by Flock House virus protein B2. Nat Struct Mol Biol 12(11):952–957PubMedGoogle Scholar
  11. Cheng RH, Reddy VS et al (1994) Functional implications of quasi-equivalence in a T = 3 icosahedral animal virus established by cryo-electron microscopy and X-ray crystallography. Structure 2(4):271–282PubMedCrossRefGoogle Scholar
  12. Dearing SC, Scotti PD et al (1980) A small RNA virus isolated from the grass grub, Costelytra zealandica (Coleoptera: Scarabaeidae). N Z J Zool 7:267–269CrossRefGoogle Scholar
  13. Farr GA, Zhang LG et al (2005) Parvoviral virions deploy a capsid-tethered lipolytic enzyme to breach the endosomal membrane during cell entry. Proc Natl Acad Sci U S A 102(47): 17148–17153PubMedCrossRefGoogle Scholar
  14. Fisher AJ, Johnson JE (1993) Ordered duplex RNA controls capsid architecture in an icosahedral animal virus. Nature 361(6408):176–179PubMedCrossRefGoogle Scholar
  15. Fisher AJ, McKinney BR et al (1993) Crystallization of viruslike particles assembled from Flock House virus coat protein expressed in a baculovirus system. J Virol 67(5):2950–2953PubMedGoogle Scholar
  16. Friesen PD, Rueckert RR (1981) Synthesis of black beetle virus proteins in cultured drosophila cells: differential expression of RNAs 1 and 2. J Virol 37(3):876–886PubMedGoogle Scholar
  17. Gallagher TM, Rueckert RR (1988) Assembly-dependent maturation cleavage in provirions of a small icosahedral insect ribovirus. J Virol 62(9):3399–3406PubMedGoogle Scholar
  18. Guarino LA, Ghosh A et al (1984) Sequence of the black beetle virus subgenomic RNA and its location in the viral genome. Virology 139(1):199–203PubMedCrossRefGoogle Scholar
  19. Janshoff A, Bong DT et al (1999) An animal virus-derived peptide switches membrane morphology: possible relevance to nodaviral transfection processes. Biochemistry 38(17):5328–5336PubMedCrossRefGoogle Scholar
  20. Li H, Li WX et al (2002) Induction and suppression of RNA silencing by an animal virus. Science 296(5571):1319–1321PubMedCrossRefGoogle Scholar
  21. Maia LF, Soares MR et al (2006) Structure of a membrane-binding domain from a non-enveloped animal virus: insights into the mechanism of membrane permeability and cellular entry. J Biol Chem 281(39):29278–29286PubMedCrossRefGoogle Scholar
  22. Marshall D, Schneemann A (2001) Specific packaging of nodaviral RNA2 requires the N-terminus of the capsid protein. Virology 285(1):165–175PubMedCrossRefGoogle Scholar
  23. Mellman I, Fuchs R et al (1986) Acidification of the endocytic and exocytic pathways. Annu Rev Biochem 55:663–700PubMedCrossRefGoogle Scholar
  24. Odegard AL, Kwan MH et al (2009) Low endocytic pH and capsid protein autocleavage are critical components of Flock House virus cell entry. J Virol 83:8628–8637Google Scholar
  25. Odegard AL, Chandran K et al (2004) Putative autocleavage of outer capsid protein micro1, allowing release of myristoylated peptide micro1N during particle uncoating, is critical for cell entry by reovirus. J Virol 78(16):8732–8745PubMedCrossRefGoogle Scholar
  26. Oliveira AC, Gomes AM et al (2000) Virus maturation targets the protein capsid to concerted disassembly and unfolding. J Biol Chem 275(21):16037–16043PubMedCrossRefGoogle Scholar
  27. Rossmann MG, Johnson JE (1989) Icosahedral RNA virus structure. Annu Rev Biochem 58:533–573PubMedCrossRefGoogle Scholar
  28. Schneemann A, Marshall D (1998) Specific encapsidation of nodavirus RNAs is mediated through the C terminus of capsid precursor protein alpha. J Virol 72(11):8738–8746PubMedGoogle Scholar
  29. Schneemann A, Zhong W et al (1992) Maturation cleavage required for infectivity of a nodavirus. J Virol 66(11):6728–6734PubMedGoogle Scholar
  30. Schneemann A, Dasgupta R et al (1993) Use of recombinant baculoviruses in synthesis of morphologically distinct viruslike particles of Flock House virus, a nodavirus. J Virol 67(5):2756–2763PubMedGoogle Scholar
  31. Schneemann A, Gallagher TM et al (1994) Reconstitution of Flock House provirions: a model system for studying structure and assembly. J Virol 68(7):4547–4556PubMedGoogle Scholar
  32. Scotti PD, Dearing S et al (1983) Flock House virus: a nodavirus isolated from Costelytra zealandica (White) (Coleoptera: Scarabaeidae). Arch Virol 75(3):181–189PubMedCrossRefGoogle Scholar
  33. Speir JA, Munshi S et al (1995) Structures of the native and swollen forms of cowpea chlorotic mottle virus determined by X-ray crystallography and cryo-electron microscopy. Structure 3(1):63–78PubMedCrossRefGoogle Scholar
  34. Speir JA, Bothner B et al (2006) Enhanced local symmetry interactions globally stabilize a mutant virus capsid that maintains infectivity and capsid dynamics. J Virol 80(7):3582–3591PubMedCrossRefGoogle Scholar
  35. Tang L, Johnson KN et al (2001) The structure of pariacoto virus reveals a dodecahedral cage of duplex RNA. Nat Struct Biol 8(1):77–83PubMedCrossRefGoogle Scholar
  36. Tihova M, Dryden KA et al (2004) Nodavirus coat protein imposes dodecahedral RNA structure independent of nucleotide sequence and length. J Virol 78(6):2897–2905PubMedCrossRefGoogle Scholar
  37. Tsai B (2007) Penetration of nonenveloped viruses into the cytoplasm. Annu Rev Cell Dev Biol 23:23–43PubMedCrossRefGoogle Scholar
  38. Walukiewicz HE, Johnson JE et al (2006) Morphological changes in the T = 3 capsid of Flock House virus during cell entry. J Virol 80(2):615–622PubMedCrossRefGoogle Scholar
  39. Walukiewicz HE, Banerjee M et al (2008) Rescue of maturation-defective flock house virus infectivity with noninfectious, mature, viruslike particles. J Virol 82(4):2025–2027PubMedCrossRefGoogle Scholar
  40. Yamashiro DJ, Maxfield FR (1984) Acidification of endocytic compartments and the intracellular pathways of ligands and receptors. J Cell Biochem 26(4):231–246PubMedCrossRefGoogle Scholar
  41. Zlotnick A, Reddy VS et al (1994) Capsid assembly in a family of animal viruses primes an autoproteolytic maturation that depends on a single aspartic acid residue. J Biol Chem 269(18):13680–13684PubMedGoogle Scholar

Copyright information

© Springer-Verlag Berlin Heidelberg 2010

Authors and Affiliations

  • Amy Odegard
    • 1
  • Manidipa Banerjee
    • 2
  • John E. Johnson
    • 3
  1. 1.Department of ChemistryUniversity of Puget SoundTacomaUSA
  2. 2.School of Biological SciencesIIT-DelhiNew DelhiIndia
  3. 3.Department of Molecular BiologyThe Scripps Research InstituteLa JollaUSA

Personalised recommendations