1887

Abstract

The purpose of this study was to identify protein–protein interactions among the components of the occlusion-derived virus (ODV) of nucleopolyhedrovirus (HearNPV), a group II alphabaculovirus in the family . To achieve this, 39 selected genes of potential ODV structural proteins were cloned and expressed in the Gal4 yeast two-hybrid (Y2H) system. The direct-cross Y2H assays identified 22 interactions comprising 13 binary interactions [HA9–ODV-EC43, ODV-E56–38K, ODV-E56–PIF3, LEF3–helicase, LEF3–alkaline nuclease (AN), GP41–38K, GP41–HA90, 38K–PIF3, 38K–PIF2, VP80–HA100, ODV-E66–PIF3, ODV-E66–PIF2 and PIF3–PIF2] and nine self-associations (IE1, HA44, LEF3, HA66, GP41, CG30, 38K, PIF3 and P24). Five of these interactions – LEF3–helicase and LEF3–AN, and the self-associations of IE1, LEF3 and 38K – have been reported previously in multiple nucleopolyhedrovirus. As HA44 and HA100 were two newly identified ODV proteins of group II viruses, their interactions were further confirmed. The self-association of HA44 was verified with a His pull-down assay and the interaction of VP80–HA100 was confirmed by a co-immunoprecipitation assay. A summary of the protein–protein interactions of baculoviruses reported so far, comprising 68 interactions with 45 viral proteins and five host proteins, is presented, which will facilitate our understanding of the molecular mechanisms of baculovirus infection.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/vir.0.017103-0
2010-03-01
2024-12-07
Loading full text...

Full text loading...

/deliver/fulltext/jgv/91/3/659.html?itemId=/content/journal/jgv/10.1099/vir.0.017103-0&mimeType=html&fmt=ahah

References

  1. Belyavskyi M., Braunagel S. C., Summers M. D. 1998; The structural protein ODV-EC27 of Autographa californica nucleopolyhedrovirus is a multifunctional viral cyclin. Proc Natl Acad Sci U S A 95:11205–11210 [CrossRef]
    [Google Scholar]
  2. Beniya H., Braunagel S. C., Summers M. D. 1998; Autographa californica nuclear polyhedrosis virus: subcellular localization and protein trafficking of BV/ODV-E26 to intranuclear membranes and viral envelopes. Virology 240:64–75 [CrossRef]
    [Google Scholar]
  3. Braunagel S. C., Summers M. D. 1994; Autographa californica nuclear polyhedrosis virus, PDV, and ECV viral envelopes and nucleocapsids: structural proteins, antigens, lipid and fatty acid profiles. Virology 202:315–328 [CrossRef]
    [Google Scholar]
  4. Braunagel S. C., Summers M. D. 2007; Molecular biology of the baculovirus occlusion-derived virus envelope. Curr Drug Targets 8:1084–1095 [CrossRef]
    [Google Scholar]
  5. Braunagel S. C., Burks J. K., Rosas-Acosta G., Harrison R. L., Ma H., Summers M. D. 1999; Mutations within the Autographa californica nucleopolyhedrovirus FP25K gene decrease the accumulation of ODV-E66 and alter its intranuclear transport. J Virol 73:8559–8570
    [Google Scholar]
  6. Braunagel S. C., Guidry P. A., Rosas-Acosta G., Engelking L., Summers M. D. 2001; Identification of BV/ODV-C42, an Autographa californica nucleopolyhedrovirus orf101-encoded structural protein detected in infected-cell complexes with ODV-EC27 and p78/83. J Virol 75:12331–12338 [CrossRef]
    [Google Scholar]
  7. Braunagel S. C., Russell W. K., Rosas-Acosta G., Russell D. H., Summers M. D. 2003; Determination of the protein composition of the occlusion-derived virus of Autographa californica nucleopolyhedrovirus. Proc Natl Acad Sci U S A 100:9797–9802 [CrossRef]
    [Google Scholar]
  8. Braunagel S. C., Cox V., Summers M. D. 2009; Baculovirus data suggest a common but multifaceted pathway for sorting proteins to the inner nuclear membrane. J Virol 83:1280–1288 [CrossRef]
    [Google Scholar]
  9. Burroughs A. M., Allen K. N., Dunaway-Mariano D., Aravind L. 2006; Evolutionary genomics of the HAD superfamily: understanding the structural adaptations and catalytic diversity in a superfamily of phosphoesterases and allied enzymes. J Mol Biol 361:1003–1034 [CrossRef]
    [Google Scholar]
  10. Chen X., IJkel W. F., Tarchini R., Sun X., Sandbrink H., Wang H., Peters S., Zuidema D., Lankhorst R. K. et al. 2001; The sequence of the Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus genome. J Gen Virol 82:241–257
    [Google Scholar]
  11. Crouch E. A., Cox L. T., Morales K. G., Passarelli A. L. 2007; Inter-subunit interactions of the Autographa californica M nucleopolyhedrovirus RNA polymerase. Virology 367:265–274 [CrossRef]
    [Google Scholar]
  12. Dai X., Stewart T. M., Pathakamuri J. A., Li Q., Theilmann D. A. 2004; Autographa californica multiple nucleopolyhedrovirus exon0 ( orf141 ), which encodes a RING finger protein, is required for efficient production of budded virus. J Virol 78:9633–9644 [CrossRef]
    [Google Scholar]
  13. Deng F., Wang R., Fang M., Jiang Y., Xu X., Wang H., Chen X., Arif B. M., Guo L. et al. 2007; Proteomics analysis of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus identified two new occlusion-derived virus-associated proteins, HA44 and HA100. J Virol 81:9377–9385 [CrossRef]
    [Google Scholar]
  14. Dong C., Li D., Long G., Deng F., Wang H., Hu Z. 2005; Identification of functional domains required for HearNPV P10 filament formation. Virology 338:112–120 [CrossRef]
    [Google Scholar]
  15. Dreschers S., Roncarati R., Knebel-Morsdorf D. 2001; Actin rearrangement-inducing factor of baculoviruses is tyrosine phosphorylated and colocalizes to F-actin at the plasma membrane. J Virol 75:3771–3778 [CrossRef]
    [Google Scholar]
  16. Evans J. T., Rohrmann G. F. 1997; The baculovirus single-stranded DNA binding protein, LEF-3, forms a homotrimer in solution. J Virol 71:3574–3579
    [Google Scholar]
  17. Evans J. T., Leisy D. J., Rohrmann G. F. 1997; Characterization of the interaction between the baculovirus replication factors LEF-1 and LEF-2. J Virol 71:3114–3119
    [Google Scholar]
  18. Evans J. T., Rosenblatt G. S., Leisy D. J., Rohrmann G. F. 1999; Characterization of the interaction between the baculovirus ssDNA-binding protein (LEF-3) and putative helicase (P143).. J Gen Virol 80:493–500
    [Google Scholar]
  19. Fan X., McLachlin J. R., Weaver R. F. 1998; Identification and characterization of a protein kinase-interacting protein encoded by the Autographa californica nuclear polyhedrosis virus. Virology 240:175–182 [CrossRef]
    [Google Scholar]
  20. Fang M., Dai X., Theilmann D. A. 2007; Autographa californica multiple nucleopolyhedrovirus EXON0 (ORF141) is required for efficient egress of nucleocapsids from the nucleus. J Virol 81:9859–9869 [CrossRef]
    [Google Scholar]
  21. Fang M., Nie Y., Dai X., Theilmann D. A. 2008; Identification of AcMNPV EXON0 ( ac141 ) domains required for efficient production of budded virus, dimerization and association with BV/ODV-C42 and FP25. Virology 375:265–276 [CrossRef]
    [Google Scholar]
  22. Fang M., Nie Y., Theilmann D. A. 2009; AcMNPV EXON0 (AC141) which is required for the efficient egress of budded virus nucleocapsids interacts with β -tubulin. Virology 385:496–504 [CrossRef]
    [Google Scholar]
  23. Fields S. 2005; High-throughput two-hybrid analysis. The promise and the peril. FEBS J 272:5391–5399 [CrossRef]
    [Google Scholar]
  24. Garcia-Maruniak A., Abd-Alla A. M., Salem T. Z., Parker A. G., Lietze V. U., van Oers M. M., Maruniak J. E., Kim W., Burand J. P. et al. 2009; Two viruses that cause salivary gland hypertrophy in Glossina pallidipes and Musca domestica are related and form a distinct phylogenetic clade. J Gen Virol 90:334–346 [CrossRef]
    [Google Scholar]
  25. Gietz R. D., Woods R. A. 2002; Transformation of yeast by lithium acetate/single-stranded carrier DNA/polyethylene glycol method. Methods Enzymol 350:87–96
    [Google Scholar]
  26. Goenka S., Weaver R. F. 2008; The p26 gene of the Autographa californica nucleopolyhedrovirus: timing of transcription, and cellular localization and dimerization of product. Virus Res 131:136–144 [CrossRef]
    [Google Scholar]
  27. Goley E. D., Ohkawa T., Mancuso J., Woodruff J. B., D'Alessio J. A., Cande W. Z., Volkman L. E., Welch M. D. 2006; Dynamic nuclear actin assembly by Arp2/3 complex and a baculovirus WASP-like protein. Science 314:464–467 [CrossRef]
    [Google Scholar]
  28. Guarino L. A., Xu B., Jin J., Dong W. 1998; A virus-encoded RNA polymerase purified from baculovirus-infected cells. J Virol 72:7985–7991
    [Google Scholar]
  29. Haas-Stapleton E. J., Washburn J. O., Volkman L. E. 2004; P74 mediates specific binding of Autographa californica M nucleopolyhedrovirus occlusion-derived virus to primary cellular targets in the midgut epithelia of Heliothis virescens larvae. J Virol 78:6786–6791 [CrossRef]
    [Google Scholar]
  30. Harwood S. H., Li L., Ho P. S., Preston A. K., Rohrmann G. F. 1998; AcMNPV late expression factor-5 interacts with itself and contains a zinc ribbon domain that is required for maximal late transcription activity and is homologous to elongation factor TFIIS. Virology 250:118–134 [CrossRef]
    [Google Scholar]
  31. Hefferon K. L. 2003a; Characterization of HCF-1, a determinant of Autographa californica multiple nucleopolyhedrovirus host specificity. Insect Mol Biol 12:651–658 [CrossRef]
    [Google Scholar]
  32. Hefferon K. L. 2003b; ORF98 of Autographa californica nucleopolyhedrosisvirus is an auxiliary factor in late gene expression. Can J Microbiol 49:157–163 [CrossRef]
    [Google Scholar]
  33. Herniou E. A., Luque T., Chen X., Vlak J. M., Winstanley D., Cory J. S., O'Reilly D. R. 2001; Use of whole genome sequence data to infer baculovirus phylogeny. J Virol 75:8117–8126 [CrossRef]
    [Google Scholar]
  34. Herniou E. A., Olszewski J. A., Cory J. S., O'Reilly D. R. 2003; The genome sequence and evolution of baculoviruses. Annu Rev Entomol 48:211–234 [CrossRef]
    [Google Scholar]
  35. Imai N., Kang W., Iwabuchi K., Sato K., Maeda S. 2000; Analysis of interaction between molecules of Bombyx mori nucleopolyhedrovirus IE-2 using a yeast two-hybrid system. Acta Virol 44:199–202
    [Google Scholar]
  36. Jehle J. A., Blissard G. W., Bonning B. C., Cory J. S., Herniou E. A., Rohrmann G. F., Theilmann D. A., Thiem S. M., Vlak J. M. 2006; On the classification and nomenclature of baculoviruses: a proposal for revision. Arch Virol 151:1257–1266 [CrossRef]
    [Google Scholar]
  37. Kang W., Imai N., Kawasaki Y., Nagamine T., Matsumoto S. 2005; IE1 and hr facilitate the localization of Bombyx mori nucleopolyhedrovirus ORF8 to specific nuclear sites. J Gen Virol 86:3031–3038 [CrossRef]
    [Google Scholar]
  38. Katsuma S., Daimon T., Mita K., Shimada T. 2006; Lepidopteran ortholog of Drosophila breathless is a receptor for the baculovirus fibroblast growth factor. J Virol 80:5474–5481 [CrossRef]
    [Google Scholar]
  39. Ke J., Wang J., Deng R., Wang X. 2008; Autographa californica multiple nucleopolyhedrovirus ac66 is required for the efficient egress of nucleocapsids from the nucleus, general synthesis of preoccluded virions and occlusion body formation. Virology 374:421–431 [CrossRef]
    [Google Scholar]
  40. Lanier L. M., Volkman L. E. 1998; Actin binding and nucleation by Autographa californica M nucleopolyhedrovirus. Virology 243:167–177 [CrossRef]
    [Google Scholar]
  41. Li Z., Blissard G. W. 2009; The Autographa californica multicapsid nucleopolyhedrovirus GP64 protein: analysis of transmembrane domain length and sequence requirements. J Virol 83:4447–4461 [CrossRef]
    [Google Scholar]
  42. Li X., Pang A., Lauzon H. A., Sohi S. S., Arif B. M. 1997; The gene encoding the capsid protein P82 of the Choristoneura fumiferana multicapsid nucleopolyhedrovirus: sequencing, transcription and characterization by immunoblot analysis. J Gen Virol 78:2665–2673
    [Google Scholar]
  43. Li Z., Li C., Pan L., Yu M., Yang K., Pang Y. 2005; Characterization of p24 gene of Spodoptera litura multicapsid nucleopolyhedrovirus. Virus Genes 30:349–356 [CrossRef]
    [Google Scholar]
  44. Lin G., Blissard G. W. 2002; Analysis of an Autographa californica nucleopolyhedrovirus lef-11 knockout: LEF-11 is essential for viral DNA replication. J Virol 76:2770–2779 [CrossRef]
    [Google Scholar]
  45. Liu X., Chen K., Cai K., Yao Q. 2008; Determination of protein composition and host-derived proteins of Bombyx mori nucleopolyhedrovirus by 2-dimensional electrophoresis and mass spectrometry. Intervirology 51:369–376
    [Google Scholar]
  46. Long G., Chen X., Peters D., Vlak J. M., Hu Z. 2003; Open reading frame 122 of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus encodes a novel structural protein of occlusion-derived virions. J Gen Virol 84:115–121 [CrossRef]
    [Google Scholar]
  47. Lu A., Miller L. K. 1995; The roles of eighteen baculovirus late expression factor genes in transcription and DNA replication. J Virol 69:975–982
    [Google Scholar]
  48. Mainz D., Quadt I., Knebel-Morsdorf D. 2002; Nuclear IE2 structures are related to viral DNA replication sites during baculovirus infection. J Virol 76:5198–5207 [CrossRef]
    [Google Scholar]
  49. McIntosh A. H., Ignoffo C. M. 1983; Characterization of five cell lines established from species of Heliothis . Appl Entomol Zool (Jpn) 18:262–269
    [Google Scholar]
  50. Mikhailov V. S., Mikhailova A. L., Iwanaga M., Gomi S., Maeda S. 1998; Bombyx mori nucleopolyhedrovirus encodes a DNA-binding protein capable of destabilizing duplex DNA. J Virol 72:3107–3116
    [Google Scholar]
  51. Mikhailov V. S., Okano K., Rohrmann G. F. 2003; Baculovirus alkaline nuclease possesses a 5′→3′ exonuclease activity and associates with the DNA-binding protein LEF-3. J Virol 77:2436–2444 [CrossRef]
    [Google Scholar]
  52. Mikhailov V. S., Vanarsdall A. L., Rohrmann G. F. 2008; Isolation and characterization of the DNA-binding protein (DBP) of the Autographa californica multiple nucleopolyhedrovirus. Virology 370:415–429 [CrossRef]
    [Google Scholar]
  53. Miller L. K. 1997 The Baculoviruses New York: Plenum Press;
  54. Murges D., Quadt I., Schroer J., Knebel-Morsdorf D. 2001; Dynamic nuclear localization of the baculovirus proteins IE2 and PE38 during the infection cycle: the promyelocytic leukemia protein colocalizes with IE2. Exp Cell Res 264:219–232 [CrossRef]
    [Google Scholar]
  55. Nie Y., Fang M., Theilmann D. A. 2009; AcMNPV AC16 (DA26, BV/ODV-E26) regulates the levels of IE0 and IE1 and binds to both proteins via a domain located within the acidic transcriptional activation domain. Virology 385:484–495 [CrossRef]
    [Google Scholar]
  56. Ohkawa T., Washburn J. O., Sitapara R., Sid E., Volkman L. E. 2005; Specific binding of Autographa californica M nucleopolyhedrovirus occlusion-derived virus to midgut cells of Heliothis virescens larvae is mediated by products of pif genes Ac119 and Ac022 but not by Ac115 . J Virol 79:15258–15264 [CrossRef]
    [Google Scholar]
  57. Olson V. A., Wetter J. A., Friesen P. D. 2001; Oligomerization mediated by a helix–loop–helix-like domain of baculovirus IE1 is required for early promoter transactivation. J Virol 75:6042–6051 [CrossRef]
    [Google Scholar]
  58. Olson V. A., Wetter J. A., Friesen P. D. 2002; Baculovirus transregulator IE1 requires a dimeric nuclear localization element for nuclear import and promoter activation. J Virol 76:9505–9515 [CrossRef]
    [Google Scholar]
  59. Oomens A. G., Blissard G. W. 1999; Requirement for GP64 to drive efficient budding of Autographa californica multicapsid nucleopolyhedrovirus. Virology 254:297–314 [CrossRef]
    [Google Scholar]
  60. Oomens A. G., Monsma S. A., Blissard G. W. 1995; The baculovirus GP64 envelope fusion protein: synthesis, oligomerization, and processing. Virology 209:592–603 [CrossRef]
    [Google Scholar]
  61. Pan X., Long G., Wang R., Hou S., Wang H., Zheng Y., Sun X., Westenberg M., Deng F. et al. 2007; Deletion of a Helicoverpa armigera nucleopolyhedrovirus gene encoding a virion structural protein (ORF107) increases the budded virion titre and reduces in vivo infectivity. J Gen Virol 88:3307–3316 [CrossRef]
    [Google Scholar]
  62. Passarelli A. L., Guarino L. A. 2007; Baculovirus late and very late gene regulation. Curr Drug Targets 8:1103–1115 [CrossRef]
    [Google Scholar]
  63. 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 317:308–320 [CrossRef]
    [Google Scholar]
  64. Perera O., Green T. B., Stevens S. M. Jr, White S., Becnel J. J. 2007; Proteins associated with Culex nigripalpus nucleopolyhedrovirus occluded virions. J Virol 81:4585–4590 [CrossRef]
    [Google Scholar]
  65. Rodems S. M., Friesen P. D. 1995; Transcriptional enhancer activity of hr5 requires dual-palindrome half sites that mediate binding of a dimeric form of the baculovirus transregulator IE1. J Virol 69:5368–5375
    [Google Scholar]
  66. Rosas-Acosta G., Braunagel S. C., Summers M. D. 2001; Effects of deletion and overexpression of the Autographa californica nuclear polyhedrosis virus FP25K gene on synthesis of two occlusion-derived virus envelope proteins and their transport into virus-induced intranuclear membranes. J Virol 75:10829–10842 [CrossRef]
    [Google Scholar]
  67. Russell R. L., Funk C. J., Rohrmann G. F. 1997; Association of a baculovirus-encoded protein with the capsid basal region. Virology 227:142–152 [CrossRef]
    [Google Scholar]
  68. Slack J., Arif B. M. 2007; The baculoviruses occlusion-derived virus: virion structure and function. Adv Virus Res 69:99–165
    [Google Scholar]
  69. Song J., Wang R., Deng F., Wang H., Hu Z. 2008; Functional studies of per os infectivity factors of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus. J Gen Virol 89:2331–2338 [CrossRef]
    [Google Scholar]
  70. Vigdorovich V., Miller A. D., Strong R. K. 2007; Ability of hyaluronidase 2 to degrade extracellular hyaluronan is not required for its function as a receptor for jaagsiekte sheep retrovirus. J Virol 81:3124–3129 [CrossRef]
    [Google Scholar]
  71. Wang Y., Jehle J. A. 2009; Nudiviruses and other large, double-stranded circular DNA viruses of invertebrates: new insights on an old topic. J Invertebr Pathol 101:187–193 [CrossRef]
    [Google Scholar]
  72. Wang Y., Wang Q., Liang C., Song J., Li N., Shi H., Chen X. 2008; Autographa californica : multiple nucleopolyhedrovirus nucleocapsid protein BV/ODV-C42 mediates the nuclear entry of P78/83. J Virol 82:4554–4561 [CrossRef]
    [Google Scholar]
  73. Wu D., Deng F., Sun X., Wang H., Yuan L., Vlak J. M., Hu Z. 2005; Functional analysis of FP25K of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus. J Gen Virol 86:2439–2444 [CrossRef]
    [Google Scholar]
  74. Wu W., Lin T., Pan L., Yu M., Li Z., Pang Y., Yang K. 2006; Autographa californica multiple nucleopolyhedrovirus nucleocapsid assembly is interrupted upon deletion of the 38K gene. J Virol 80:11475–11485 [CrossRef]
    [Google Scholar]
  75. Wu W., Liang H., Kan J., Liu C., Yuan M., Liang C., Yang K., Pang Y. 2008; Autographa californica multiple nucleopolyhedrovirus 38K is a novel nucleocapsid protein that interacts with VP1054, VP39, VP80, and itself. J Virol 82:12356–12364 [CrossRef]
    [Google Scholar]
/content/journal/jgv/10.1099/vir.0.017103-0
Loading
/content/journal/jgv/10.1099/vir.0.017103-0
Loading

Data & Media loading...

This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error