Skip to main content
Log in

The long road to understanding the baculovirus P10 protein

  • Published:
Virologica Sinica

Abstract

The baculovirus P10 protein has always represented a mystery in the field of insect virology. Like the baculovirus polyhedrin protein it is expressed at high levels very late in infection. Homologues of the Autographa californica nucleopolyhedrovirus p10 gene are conserved in all Alphabaculoviruses and in other viruses of lepidopteran hosts yet is completely dispensable for virus replication and transmission. P10 is a microtubule interacting protein whose expression has been associated with the formation of a variety of complex and extensive cytoplasmic and nuclear structures. P10 has been associated with a number of roles during infection ranging from the formation of virus occlusion bodies, to affecting the rate of cellular and/or nuclear lysis during the final stages of the virus replication cycle. In this article we review recent work aimed at understanding the role of this enigmatic protein, putting them into context with recent advances in understanding of protein structure and function. We look back at a number of historical studies and observations, reanalysing their conclusions based on recent data and our own observations. The role of the P10 protein during baculovirus replication remains elusive, however, novel avenues of investigation have been identified that will, we are sure, eventually lead to an understanding of this protein.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. Adang M J, Miller L K. 1982. Molecular cloning of DNA complementary to mRNA of the baculovirus Autographa californica nuclear polyhedrosis virus: location and gene products of RNA transcripts found late in infection. J Virol, 44(3): 782–793.

    PubMed  CAS  Google Scholar 

  2. Alaoui-Ismaili M H, Richardson C D. 1996. Identification and characterization of a filament-associated protein encoded by Amsacta moorei entomopoxvirus. J Virol, 70(5): 2697–2705.

    PubMed  CAS  Google Scholar 

  3. Alaoui-Ismaili M H, Richardson C D. 1998. Insect virus proteins (FALPE and p10) self-associate to form filaments in infected cells. J Virol, 72(3): 2213–2223.

    PubMed  CAS  Google Scholar 

  4. Bonner W M. 1975. Protein migration into nuclei. I. Frog oocyte nuclei in vivo accumulate microinjected histones, allow entry to small proteins, and exclude large proteins. J Cell Biol, 64(2): 421–430.

    Article  PubMed  CAS  Google Scholar 

  5. Brown J H, Cohen C, Parry D A. 1996. Heptad breaks in alpha-helical coiled coils: stutters and stammers. Proteins, 26(2): 134–145.

    Article  PubMed  CAS  Google Scholar 

  6. Carpentier D C, Griffiths C M, King L A. 2008. The baculovirus P10 protein of Autographa californica nucleopolyhedrovirus forms two distinct cytoskeletal-like structures and associates with polyhedral occlusion bodies during infection. Virology, 371(2): 278–291.

    Article  PubMed  CAS  Google Scholar 

  7. Chaabihi H, Ogliastro M H, Martin M, et al. 1993. Competition between baculovirus polyhedrin and p10 gene expression during infection of insect cells. J Virol, 67(5): 2664–2671.

    PubMed  CAS  Google Scholar 

  8. Chang D K, Cheng S F, Trivedi V D, et al. 1999. Proline affects oligomerization of a coiled coil by inducing a kink in a long helix. J Struct Biol, 128(3): 270–279.

    Article  PubMed  CAS  Google Scholar 

  9. Cheley S, Kosik K S, Paskevich P, et al. 1992. Phosphorylated baculovirus p10 is a heat-stable microtubuleassociated protein associated with process formation in Sf9 cells. J Cell Sci, 102(Pt 4): 739–752.

    PubMed  CAS  Google Scholar 

  10. Chothia C, Levitt M, Richardson D. 1981. Helix to helix packing in proteins. J Mol Biol, 145(1): 215–250.

    Article  PubMed  CAS  Google Scholar 

  11. Chung K L, Brown M, Faulkner P. 1980. Studies on the morphogenesis of polyhedral inclusion bodies of a baculovirus autographa californica NPV. J Gen Virol, 46: 335–347.

    Article  Google Scholar 

  12. Cohen C, Parry D A. 1994. Alpha-helical coiled coils: more facts and better predictions. Science, 263(5146): 488–489.

    Article  PubMed  CAS  Google Scholar 

  13. Crick F H C. 1952. Is alpha-keratin a coiled coil? Nature, 170(4334): 882–883.

    Article  PubMed  CAS  Google Scholar 

  14. Crick F H C. 1953. The packing of alpha-helices: Simple coiled-coils. Acta Crystallogr, 6: 689–697.

    Article  CAS  Google Scholar 

  15. Croizier G, Gonnet P, Devauchelle G. 1987. Localisation cytologique de la proteine non structurale p10 du baculovirus de la polyedrose nucleaire do Lepidoptere Galleria mellonella. L CR Acad Sci Paris, 305: 677–681.

    CAS  Google Scholar 

  16. Crook N. 1991. Baculoviridae: subgroup B: Comparative aspects of granulosis viruses. In: Viruses of Invertebrates (Kurstak E, ed.), New York: Marcel Dekker. p73–110.

    Google Scholar 

  17. Dong C, Deng F, Li D, et al. 2007. The heptad repeats region is essential for AcMNPV P10 filament formation and not the proline-rich or the C-terminus basic regions. Virology, 365(2): 390–397

    Article  PubMed  CAS  Google Scholar 

  18. Dong C, Li D, Long G, et al. 2005. Identification of functional domains required for HearNPV P10 filament formation. Virology, 338(1): 112–120.

    Article  PubMed  CAS  Google Scholar 

  19. Fong J H, Keating A E, Singh M. 2004. Predicting specificity in bZIP coiled-coil protein interactions. Genome Biol, 5(2): R11.

    Article  PubMed  Google Scholar 

  20. Fuxa J R, Matter M M, Abdel-Rahman A, et al. 2001. Persistence and Distribution of Wild-Type and Recombinant Nucleopolyhedroviruses in Soil. Microb Ecol, 41(3): 222–231.

    PubMed  Google Scholar 

  21. Garcia M L, Cleveland D W. 2001. Going new places using an old MAP: tau, microtubules and human neurodegenerative disease. Curr Opin Cell Biol, 13(1): 41–48.

    Article  PubMed  CAS  Google Scholar 

  22. Ghose R, Shekhtman A, Goger M J, et al. 2001. A novel, specific interaction involving the Csk SH3 domain and its natural ligand. Nat Struct Biol, 8(11): 998–1004.

    Article  PubMed  CAS  Google Scholar 

  23. Goenka S, Weaver R F. The p26 gene of the Autographa californica nucleopolyhedrovirus: timing of transcription, and cellular localization and dimerization of product. Virus Res. 2008 Feb;131(2): 136–44.

    Article  PubMed  CAS  Google Scholar 

  24. Gruber M, Soding J, Lupas A N. 2006. Comparative analysis of coiled-coil prediction methods. J Struct Biol, 155(2): 140–145.

    Article  PubMed  CAS  Google Scholar 

  25. Herniou E A, Olszewski J A, O’Reilly D R, et al. 2004. Ancient coevolution of baculoviruses and their insect hosts. J Virol, 78(7): 3244–3251.

    Article  PubMed  CAS  Google Scholar 

  26. Hess R T, Falcon L A. 1978. Electron microscope observations of the membrane surrounding polyhedral inclusion bodies of insects. Arch Virol, 56(1–2): 169–176.

    Article  PubMed  CAS  Google Scholar 

  27. Holt M R, Koffer A. 2001. Cell motility: proline-rich proteins promote protrusions. Trends Cell Biol, 11(1): 38–46.

    Article  PubMed  CAS  Google Scholar 

  28. Jarvis D L, Bohlmeyer D A, Jr. Garcia A. 1991. Requirements for nuclear localization and supramolecular assembly of a baculovirus polyhedrin protein. Virology, 185(2): 795–810.

    Article  PubMed  CAS  Google Scholar 

  29. Jehle J A, Lange M, Wang H, et al. 2006. Molecular identification and phylogenetic analysis of baculoviruses from Lepidoptera. Virology, 346(1): 180–193.

    Article  PubMed  CAS  Google Scholar 

  30. Katsuki M, Tokuraku K, Murofushi H, et al. 1999. Functional analysis of microtubule-binding domain of bovine MAP4. Cell Struct Funct, 24(5): 337–344.

    Article  PubMed  CAS  Google Scholar 

  31. Kim Y, Chang S. 2006. Ever-expanding network of dynamininteracting proteins. Mol Neurobiol, 34(2): 129–136.

    Article  PubMed  CAS  Google Scholar 

  32. Knudson D L, Harrap K A. 1975. Replication of nuclear polyhedrosis virus in a continuous cell culture of Spodoptera frugiperda: microscopy study of the sequence of events of the virus infection. J Virol, 17(1): 254–268.

    PubMed  CAS  Google Scholar 

  33. Kuzio J, Rohel D Z, Curry C J, et al. 1984. Nucleotide sequence of the p10 polypeptide gene of Autographa californica nuclear polyhedrosis virus. Virology, 139: 414–418.

    Article  PubMed  CAS  Google Scholar 

  34. Lee G, Cowan N, Kirschner M. 1988. The primary structure and heterogeneity of tau protein from mouse brain. Science, 239(4837): 285–288.

    Article  PubMed  CAS  Google Scholar 

  35. Lee S Y, Poloumienko A, Belfry S, et al. 1996. A common pathway for p10 and calyx proteins in progressive stages of polyhedron envelope assembly in AcMNPV-infected Spodoptera frugiperda larvae. Arch Virol, 141(7): 1247–1258.

    Article  PubMed  CAS  Google Scholar 

  36. Lewis S A, Wang D H, Cowan N J. 1988. Microtubule-associated protein MAP2 shares a microtubule binding motif with tau protein. Science, 242(4880): 936–939.

    Article  PubMed  CAS  Google Scholar 

  37. Li S S. 2005. Specificity and versatility of SH3 and other proline-recognition domains: structural basis and implications for cellular signal transduction. Biochem J, 390(Pt 3): 641–653.

    PubMed  CAS  Google Scholar 

  38. Li Y, Miller L K. 1995. Properties of a baculovirus mutant defective in the protein phosphatase gene. J Virol, 69(7): 4533–4537.

    PubMed  CAS  Google Scholar 

  39. Lupas A N, Gruber M. 2005. The structure of alphahelical coiled coils. Adv Protein Chem, 70: 37–78.

    Article  PubMed  CAS  Google Scholar 

  40. Lupas A, Van Dyke M, Stock J. 1991. Predicting coiled coils from protein sequences. Science, 252(5010): 1162–1164.

    Article  CAS  Google Scholar 

  41. MacKinnon E A, Henderson J F, Stoltz D B, et al. 1974. Morphogenesis of nuclear polyhedrosis virus under conditions of prolonged passage in vitro. J Ultrastruct Res, 49(3): 419–435.

    Article  PubMed  CAS  Google Scholar 

  42. Meggio F, Pinna L A. 2003. One-thousand-and-one substrates of protein kinase CK2? Faseb J, 17(3): 349–368.

    Article  PubMed  CAS  Google Scholar 

  43. Melki R, Kerjan P, Waller J P, et al. 1991. Interaction of microtubule-associated proteins with microtubules: yeast lysyl-and valyl-tRNA synthetases and tau 218-235 synthetic peptide as model systems. Biochemistry, 30(49): 11536–11545.

    Article  PubMed  CAS  Google Scholar 

  44. Nguyen M, Fasold H. 1991. A strongly basic protein of the MAP2 family copolymerizes with tubulin and induces polymerization. J Protein Chem, 10(5): 511–516.

    Article  PubMed  CAS  Google Scholar 

  45. Offer G, Hicks M R, Woolfson D N. 2002. Generalized Crick equations for modeling noncanonical coiled coils. J Struct Biol, 137(1–2): 41–53.

    Article  PubMed  CAS  Google Scholar 

  46. Patmanidi A L, Possee R D, King L A. 2003. Formation of P10 tubular structures during AcMNPV infection depends on the integrity of host-cell microtubules. Virology, 317(2): 308–320.

    Article  PubMed  CAS  Google Scholar 

  47. Preuss U, Biernat J, Mandelkow E M, et al. 1997. The’ jaws’ model of tau-microtubule interaction examined in CHO cells. J Cell Sci, 110(Pt 6): 789–800.

    PubMed  CAS  Google Scholar 

  48. Quant-Russell R L, Pearson M N, Rohrmann G F, et al. 1987. Characterization of baculovirus p10 synthesis using monoclonal antibodies. Virology, 160(1): 9–19.

    Article  PubMed  CAS  Google Scholar 

  49. Rogers S, Wells R, Rechsteiner M. 1986. Amino acid sequences common to rapidly degraded proteins: the PEST hypothesis. Science, 234(4774): 364–368.

    Article  PubMed  CAS  Google Scholar 

  50. Rohel D Z, Cochran M A, Faulkner P. 1983. Characterization of two abundant mRNAs of Autographa californica nuclear polyhedrosis virus present late in infection. Virology, 124(2): 357–365.

    Article  PubMed  CAS  Google Scholar 

  51. Rohel D Z, Faulkner P. 1984. Time Course Analysis and Mapping of Autographa californica Nuclear Polyhedrosis Virus Transcripts. J Virol, 50(3): 739–747.

    PubMed  CAS  Google Scholar 

  52. Smith G E, Fraser M J, Summers M D. 1983. Molecular Engineering of the Autographa californica Nuclear Polyhedrosis Virus Genome: Deletion Mutations Within the Polyhedrin Gene. J Virol, 46(2):584–593.

    PubMed  CAS  Google Scholar 

  53. Sparks A B, Rider J E, Kay B K. 1998. Mapping the specificity of SH3 domains with phage-displayed randompeptide libraries. Methods Mol Biol, 84: 87–103.

    PubMed  CAS  Google Scholar 

  54. Summers M D, Arnott H J. 1969. Ultrastructural studies on inclusion formation and virus occlusion in nuclear polyhedrosis and granulosis virus-infected cells of Trichoplusia ni (Hubner). J Ultrastruct Res, 28(5): 462–480.

    Article  PubMed  CAS  Google Scholar 

  55. Van der Wilk F, Van Lent J W M, Vlak J M. 1987. Immunogold detection of polyhedrin, p10 and virion antigens in Autographa californica nuclear polyhedrosis virus-infected Spodoptera frugiperda cells. J Gen Virol, 68: 2615–2623.

    Article  Google Scholar 

  56. Van Oers M M, Flipsen J T, Reusken C B, et al. 1993. Functional domains of the p10 protein of Autographa californica nuclear polyhedrosis virus. J Gen Virol, 74(Pt 4): 563–574.

    Article  PubMed  Google Scholar 

  57. Van Oers M M, Flipsen J T, Reusken CB, et al. 1994. Specificity of baculovirus p10 functions. Virology, 200(2): 513–23.

    Article  PubMed  Google Scholar 

  58. Van Oers M M, Vlak J M. 1997. The baculovirus 10-kDa protein. J Invertebr Pathol, 70(1): 1–17.

    Article  PubMed  Google Scholar 

  59. Vlak J M, Klinkenberg F A, Zaal K J, et al. 1988. Functional studies on the p10 gene of Autographa californica nuclear polyhedrosis virus using a recombinant expressing a p10-beta-galactosidase fusion gene. J Gen Virol, 69(Pt 4): 765–776.

    Article  PubMed  CAS  Google Scholar 

  60. Vlak J M, Smith G E, Summers M D. 1981. Hybridization Selection and In Vitro Translation of Autographa californica Nuclear Polyhedrosis Virus mRNA. J Virol, 40(3): 762–771.

    PubMed  CAS  Google Scholar 

  61. Volkman L E, Zaal K J. 1990. Autographa californica M nuclear polyhedrosis virus: microtubules and replication. Virology, 175(1): 292–302.

    Article  PubMed  CAS  Google Scholar 

  62. Walshaw J, Woolfson D N. 2001. Open-and-shut cases in coiled-coil assembly: alpha-sheets and alpha-cylinders. Protein Sci, 10(3): 668–673.

    Article  PubMed  CAS  Google Scholar 

  63. Williams G V, Rohel D Z, Kuzio J, et al. 1989. A cytopathological investigation of Autographa californica nuclear polyhedrosis virus p10 gene function using insertion/deletion mutants. J Gen Virol, 70(Pt 1): 187–202.

    Article  PubMed  CAS  Google Scholar 

  64. Wilson J A, Hill J E, Kuzio J, et al. 1995. Characterization of the baculovirus Choristoneura fumiferana multicapsid nuclear polyhedrosis virus p10 gene indicates that the polypeptide contains a coiled-coil domain. J Gen Virol, 76(Pt 12): 2923–2932.

    Article  PubMed  CAS  Google Scholar 

  65. Zanotto P M, Kessing B D, Maruniak J E. 1993. Phylogenetic interrelationships among baculoviruses: evolutionary rates and host associations. J Invertebr Pathol, 62(2): 147–164.

    Article  PubMed  CAS  Google Scholar 

  66. Zetina C R. 2001. A conserved helix-unfolding motif in the naturally unfolded proteins. Proteins, 44(4): 479–483.

    Article  PubMed  CAS  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Linda A. King.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Carpentier, D.C.J., King, L.A. The long road to understanding the baculovirus P10 protein. Virol. Sin. 24, 227–242 (2009). https://doi.org/10.1007/s12250-009-3045-0

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s12250-009-3045-0

Key words

CLC number

Navigation