Skip to main content
SpringerLink
Log in

Per os infectivity factors: a complicated and evolutionarily conserved entry machinery of baculovirus

  • Review
  • THEMATIC ISSUE: Biotic information and pest control
  • Published:
Science China Life Sciences Aims and scope Submit manuscript

Abstract

Baculoviruses are a family of arthropod-specific large DNA viruses that infect insect species belonging to the orders Lepidoptera, Hymenoptera and Diptera. In nature, occlusion-derived viruses (ODVs) initiate baculovirus primary infection in the midgut epithelium of insect hosts, and this process is largely dependent on a number of ODV envelope proteins designated as per os infectivity factors (PIFs). Interestingly, PIF homologs are also present in other invertebrate large DNA viruses, which is indicative that per os infection is an ancient and phylogenetically conserved entry mechanism shared by these viruses. Here, we review the advances in the knowledge of the functions of individual PIFs and recent discoveries about the PIF complex, and discuss the evolutionary implications of PIF homologs in invertebrate DNA viruses. Furthermore, future research highlights on the per os infection mechanism are also prospected.

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

Access this article

Log in via an institution

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

Instant access to the full article PDF.

Institutional subscriptions

Similar content being viewed by others

References

  • Alfonso, V., López, M.G., Carrillo, E., and Taboga, O. (2012). Surface display of AcMNPV occlusion-derived P74 does not enhance oral infectivity of budded viruses. Intervirology 55, 247–251.

    Article  CAS  PubMed  Google Scholar 

  • Bézier, A., Annaheim, M., Herbinière, J., Wetterwald, C., Gyapay, G., Bernard-Samain, S., Wincker, P., Roditi, I., Heller, M., Belghazi, M., Pfister-Wilhem, R., Periquet, G., Dupuy, C., Huguet, E., Volkoff, A.N., Lanzrein, B., and Drezen, J.M. (2009). Polydnaviruses of braconid wasps derive from an ancestral nudivirus. Science 323, 926–930.

    Article  PubMed  Google Scholar 

  • Bézier, A., Thézé, J., Gavory, F., Gaillard, J., Poulain, J., Drezen, J.M., and Herniou, E.A. (2015). The genome of the nucleopolyhedrosis-causing virus from Tipula oleracea sheds new light on the Nudiviridae family. J Virol 89, 3008–3025.

    Article  PubMed  Google Scholar 

  • Braunagel, S.C., Elton, D.M., Ma, H., and Summers, M.D. (1996). Identification and analysis of an autographa californica nuclear polyhedrosis virus structural protein of the occlusion-derived virus envelope: ODVE56. Virology 217, 97–110.

    Article  CAS  PubMed  Google Scholar 

  • Braunagel, S.C., Russell, W.K., Rosas-Acosta, G., Russell, D.H., and Summers, M.D. (2003). Determination of the protein composition of the occlusion-derived virus of Autographa californica nucleopolyhedrovirus. Proc Natl Acad Sci USA 100, 9797–9802.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Braunagel, S., and Summers, M. (2007). Molecular biology of the baculovirus occlusion-derived virus envelope. Curr Drug Targets 8, 1084–1095.

    Article  CAS  PubMed  Google Scholar 

  • Braunagel, S.C., Williamson, S.T., Saksena, S., Zhong, Z., Russell, W.K., Russell, D.H., and Summers, M.D. (2004). Trafficking of ODV-E66 is mediated via a sorting motif and other viral proteins: facilitated trafficking to the inner nuclear membrane. Proc Natl Acad Sci USA 101, 8372–8377.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Burke, G.R., and Strand, M.R. (2012). Polydnaviruses of parasitic wasps: domestication of viruses to act as gene delivery vectors. Insects 3, 91–119.

    Article  PubMed  PubMed Central  Google Scholar 

  • Campadelli-Fiume, G., Menotti, L., Avitabile, E., and Gianni, T. (2012). Viral and cellular contributions to herpes simplex virus entry into the cell. Curr Opin Virol 2, 28–36.

    Article  CAS  PubMed  Google Scholar 

  • Dong, Z.Q., Zhang, J., Chen, X.M., He, Q., Cao, M.Y., Wang, L., Li, H.Q., Xiao, W.F., Pan, C.X., Lu, C., and Pan, M.H. (2014). Bombyx mori nucleopolyhedrovirus ORF79 is a per os infectivity factor associated with the PIF complex. Virus Res 184, 62–70.

    Article  CAS  PubMed  Google Scholar 

  • Fang, M., Nie, Y., Harris, S., Erlandson, M.A., and Theilmann, D.A. (2009). Autographa californica multiple nucleopolyhedrovirus core gene ac96 encodes a per os infectivity factor (pif-4). J Virol 83, 12569–12578.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fang, M., Nie, Y., Wang, Q., Deng, F., Wang, R., Wang, H., Wang, H., Vlak, J.M., Chen, X., and Hu, Z. (2006). Open reading frame 132 of Heliocoverpa armigera nucleopolyhedrovirus encodes a functional per os infectivity factor (PIF-2). J Gen Virol 87, 2563–2569.

    Article  CAS  PubMed  Google Scholar 

  • Faulkner, P., Kuzio, J., Williams, G.V., and Wilson, J.A. (1997). Analysis of p74, a PDV envelope protein of Autographa californica nucleopolyhedrovirus required for occlusion body infectivity in vivo. J Gen Virol 78, 3091–3100.

    Article  CAS  PubMed  Google Scholar 

  • Gao, Y. (2017). Facts of research on protein-protein interactions. Sci China Life Sci 60, 313–314.

    Article  PubMed  Google Scholar 

  • Garavaglia, M.J., Miele, S.A.B., Iserte, J.A., Belaich, M.N., and Ghiringhelli, P.D. (2012). The ac53, ac78, ac101, and ac103 genes are newly discovered core genes in the family Baculoviridae. J Virol 86, 12069–12079.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Garcia-Maruniak, A., Abd-Alla, A.M.M., Salem, T.Z., Parker, A.G., Lietze, V.U., van Oers, M.M., Maruniak, J.E., Kim, W., Burand, J.P., Cousserans, F., Robinson, A.S., Vlak, J.M., Bergoin, M., and Boucias, D.G. (2009). Two viruses that cause salivary gland hypertrophy in Glossina pallidipes and Musca domestica are related and form a distinct phylogenetic clade. J Gene Virol 90, 334–346.

    Article  CAS  Google Scholar 

  • Gauthier, L., Cornman, S., Hartmann, U., Cousserans, F., Evans, J.D., de Miranda, J.R., and Neumann, P. (2015). The Apis mellifera filamentous virus genome. Viruses 7, 3798–3815.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gutiérrez, S., Kikhno, I., and López Ferber, M. (2004). Transcription and promoter analysis of pif, an essential but low-expressed baculovirus gene. J Gene Virol 85, 331–341.

    Article  Google Scholar 

  • Haas-Stapleton, E.J., Washburn, J.O., and 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hong, T., Summers, M.D., and Braunagel, S.C. (1997). N-terminal sequences from Autographa californica nuclear polyhedrosis virus envelope proteins ODV-E66 and ODV-E25 are sufficient to direct reporter proteins to the nuclear envelope, intranuclear microvesicles and the envelope of occlusion derived virus. Proc Natl Acad Sci USA 94, 4050–4055.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Hou, D., Zhang, L., Deng, F., Fang, W., Wang, R., Liu, X., Guo, L., Rayner, S., Chen, X., Wang, H., and Hu, Z. (2013). Comparative proteomics reveal fundamental structural and functional differences between the two progeny phenotypes of a baculovirus. J Virol 87, 829–839.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang, H., Wang, M., Deng, F., Wang, H., and Hu, Z. (2012). ORF85 of HearNPV encodes the per os infectivity factor 4 (PIF4) and is essential for the formation of the PIF complex. Virology 427, 217–223.

    Article  CAS  PubMed  Google Scholar 

  • Huang, J.K., Hu, R.F., Qiao, F.B., Yin, Y.H., Liu, H.J., and Huang, Z.R. (2015). Impact of insect-resistant GM rice on pesticide use and farmers’ health in China. Sci China Life Sci 58, 466–471.

    Article  PubMed  Google Scholar 

  • Huang, Z., Pan, M., Zhu, S., Zhang, H., Wu, W., Yuan, M., and Yang, K. (2017). The Autographa californica multiple nucleopolyhedrovirus ac83 gene contains a cis-acting element that is essential for nucleocapsid assembly. J Virol 91, e02110–16.

    Google Scholar 

  • Javed, M.A., Biswas, S., Willis, L.G., Harris, S., Pritchard, C., van Oers, M.M., Donly, B.C., Erlandson, M.A., Hegedus, D.D., and Theilmann, D.A. (2017). Autographa californica multiple nucleopolyhedrovirus AC83 is a per os infectivity factor (PIF) protein required for occlusion- derived virus (ODV) and budded virus nucleocapsid assembly as well as assembly of the PIF complex in ODV envelopes. J Virol 91, e02115–16.

    Article  Google Scholar 

  • Jehle, J.A., Abd-Alla, A.M., and Wang, Y. (2013). Phylogeny and evolution of Hytrosaviridae. J Invertebr Pathol 112 Suppl, S62–S67.

    Article  PubMed  Google Scholar 

  • Kikhno, I., Gutiérrez, S., Croizier, L., Croizier, G., and Ferber, M.L. (2002). Characterization of pif, a gene required for the per os infectivity of Spodoptera littoralis nucleopolyhedrovirus. J Gen Virol 83, 3013–3022.

    Article  CAS  PubMed  Google Scholar 

  • Kuzio, J., Jaques, R., and Faulkner, P. (1989). Identification of p74, a gene essential for virulence of baculovirus occlusion bodies. Virology 173, 759–763.

    Article  CAS  PubMed  Google Scholar 

  • Li, G., Chen, H., Tang, Q., Huang, G., Deng, R., Wang, J., and Wang, X. (2011). Effect of ac68 knockout and lef3 leading sequence disruption on viral propagation. Curr Microbiol 62, 191–197.

    Article  CAS  PubMed  Google Scholar 

  • Li, G., Wang, J., Deng, R., and Wang, X. (2008). Characterization of AcMNPV with a deletion of ac68 gene. Virus Genes 37, 119–127.

    Article  PubMed  Google Scholar 

  • Li, X., Song, J., Jiang, T., Liang, C., and Chen, X. (2007). The N-terminal hydrophobic sequence of Autographa californica nucleopolyhedrovirus PIF-3 is essential for oral infection. Arch Virol 152, 1851–1858.

    Article  CAS  PubMed  Google Scholar 

  • Liu, J, Zhu, L., Zhang, S., Deng, Z., Huang, Z., Yuan, M., Wu, W., and Yang, K. (2016). The Autographa californica multiple nucleopolyhedrovirus ac110 gene encodes a new per os infectivity factor. Virus Res 221, 30–37.

    Article  CAS  Google Scholar 

  • Misof, B., Liu, S., Meusemann, K., Peters, R.S., Donath, A., Mayer, C., Frandsen, P.B., Ware, J., Flouri, T., Beutel, R.G., Niehuis, O., Petersen, M., Izquierdo-Carrasco, F., Wappler, T., Rust, J., Aberer, A.J., Aspock, U., Aspock, H., Bartel, D., Blanke, A., Berger, S., Bohm, A., Buckley, T.R., Calcott, B., Chen, J., Friedrich, F., Fukui, M., Fujita, M., Greve, C., Grobe, P., Gu, S., Huang, Y., Jermiin, L.S., Kawahara, A.Y., Krogmann, L., Kubiak, M., Lanfear, R., Letsch, H., Li, Y., Li, Z., Li, J., Lu, H., Machida, R., Mashimo, Y., Kapli, P., McKenna, D.D., Meng, G., Nakagaki, Y., Navarrete-Heredia, J.L., Ott, M., Ou, Y., Pass, G., Podsiadlowski, L., Pohl, H., von Reumont, B.M., Schutte, K., Sekiya, K., Shimizu, S., Slipinski, A., Stamatakis, A., Song, W., Su, X., Szucsich, N.U., Tan, M., Tan, X., Tang, M., Tang, J., Timelthaler, G., Tomizuka, S., Trautwein, M., Tong, X., Uchifune, T., Walzl, M.G., Wiegmann, B.M., Wilbrandt, J., Wipfler, B., Wong, T.K., Wu, Q., Wu, G., Xie, Y., Yang, S., Yang, Q., Yeates, D.K., Yoshizawa, K., Zhang, Q., Zhang, R., Zhang, W., Zhang, Y., Zhao, J., Zhou, C., Zhou, L., Ziesmann, T., Zou, S., Xu, X., Yang, H., Wang, J., Kjer, K.M., and Zhou, X. (2014). Phylogenomics resolves the timing and pattern of insect evolution. Science 346, 763–767.

    Article  CAS  PubMed  Google Scholar 

  • Mora, C., Tittensor, D.P., Adl, S., Simpson, A.G., and Worm, B. (2011). How many species are there on Earth and in the ocean? PLoS Biol 9, e1001127.

  • Mu, J., van Lent, J.W.M., Smagghe, G., Wang, Y., Chen, X., Vlak, J.M., and van Oers, M.M. (2014). Live imaging of baculovirus infection of midgut epithelium cells: a functional assay of per os infectivity factors. J Gene Virol 95, 2531–2539.

    Article  Google Scholar 

  • Nie, Y., Fang, M., Erlandson, M.A., and Theilmann, D.A. (2012). Analysis of the Autographa californica multiple nucleopolyhedrovirus overlapping gene pair lef3 and ac68 reveals that AC68 is a per os infectivity factor and that LEF3 is critical, but not essential, for virus replication. J Virol 86, 3985–3994.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ohkawa, T. (1997). Identification and characterization of genes of the baculovirus Bombyx mori nucleopolyhedrovirus (BmNPV) involved in viral pathogenesis. Doctoral Dissertation. (California: University of California- Davis).

  • Ohkawa, T., Washburn, J.O., Sitapara, R., Sid, E., and 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.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng, K., van Lent, J.W.M., Boeren, S., Fang, M., Theilmann, D.A., Erlandson, M.A., Vlak, J.M., and van Oers, M.M. (2012). Characterization of novel components of the baculovirus per os infectivity factor complex. J Virol 86, 4981–4988.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng, K., van Lent, J.W.M., Vlak, J.M., Hu, Z., and van Oers, M.M. (2011). In situ cleavage of baculovirus occlusion-derived virus receptor binding protein P74 in the peroral infectivity complex. J Virol 85, 10710–10718.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng, K., van Oers, M.M., Hu, Z., van Lent, J.W.M., and Vlak, J.M. (2010a). Baculovirus per os infectivity factors form a complex on the surface of occlusion-derived virus. J Virol 84, 9497–9504.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Peng, K., Wu, M., Deng, F., Song, J., Dong, C., Wang, H., and Hu, Z. (2010b). Identification of protein-protein interactions of the occlusionderived virus-associated proteins of Helicoverpa armigera nucleopolyhedrovirus. J Gene Virol 91, 659–670.

    Article  CAS  Google Scholar 

  • Perera, O., Green, T.B., Stevens, S.M., White, S., and Becnel, J.J. (2007). Proteins associated with Culex nigripalpus nucleopolyhedrovirus occluded virions. J Virol 81, 4585–4590.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Pijlman, G.P., Pruijssers, A.J.P., and Vlak, J.M. (2003). Identification of pif-2, a third conserved baculovirus gene required for per os infection of insects. J Gene Virol 84, 2041–2049.

    Article  CAS  Google Scholar 

  • Russell, R.L.Q., and Rohrmann, G.F. (1997). Characterization of P91, a protein associated with virions of an Orgyia pseudotsugata baculovirus. Virology 233, 210–223.

    Article  CAS  PubMed  Google Scholar 

  • Saksena, S., Summers, M.D., Burks, J.K., Johnson, A.E., and Braunagel, S.C. (2006). Importin-a-16 is a translocon-associated protein involved in sorting membrane proteins to the nuclear envelope. Nat Struct Mol Biol 13, 500–508.

    Article  CAS  PubMed  Google Scholar 

  • Senkevich, T.G., Ojeda, S., Townsley, A., Nelson, G.E., and Moss, B. (2005). Poxvirus multiprotein entry-fusion complex. Proc Natl Acad Sci USA 102, 18572–18577.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Simón, O., Palma, L., Williams, T., López-Ferber, M., and Caballero, P. (2012). Analysis of a naturally-occurring deletion mutant of Spodoptera frugiperda multiple nucleopolyhedrovirus reveals sf58 as a new per os infectivity factor of lepidopteran-infecting baculoviruses. J Invertebr Pathol 109, 117–126.

    Article  PubMed  Google Scholar 

  • Simón, O., Williams, T., Cerutti, M., Caballero, P., and López-Ferber, M. (2013). Expression of a peroral infection factor determines pathogenicity and population structure in an insect virus. PLoS ONE 8, e78834.

    Article  Google Scholar 

  • Slack, J., and Arif, B.M. (2006). The baculoviruses occlusion-derived virus: virion structure and function. Adv Virus Res 69, 99–165.

    Article  Google Scholar 

  • Slack, J.M., Lawrence, S.D., Krell, P.J., and Arif, B.M. (2008). Trypsin cleavage of the baculovirus occlusion-derived virus attachment protein P74 is prerequisite in per os infection. J Gene Virol 89, 2388–2397.

    Article  CAS  Google Scholar 

  • Slack, J.M., Lawrence, S.D., Krell, P.J., and Arif, B.M. (2010). A soluble form of P74 can act as a per os infectivity factor to the Autographa californica multiple nucleopolyhedrovirus. J Gene Virol 91, 915–918.

    Article  CAS  Google Scholar 

  • Song, J., Wang, M., Huang, H., Luo, X., Deng, F., Wang, H., and Hu, Z. (2012). Functional studies of per os infectivity factor 3 of Helicoverpa armigera nucleopolyhedrovirus. J Gene Virol 93, 374–382.

    Article  CAS  Google Scholar 

  • Song, J., Wang, R., Deng, F., Wang, H., and Hu, Z. (2008). Functional studies of per os infectivity factors of Helicoverpa armigera single nucleocapsid nucleopolyhedrovirus. J Gene Virol 89, 2331–2338.

    Article  CAS  Google Scholar 

  • Song, J., Wang, X., Hou, D., Huang, H., Liu, X., Deng, F., Wang, H., Arif, B.M., Hu, Z., and Wang, M. (2016). The host specificities of baculovirus per os infectivity factors. PLoS ONE 11, e0159862.

    Google Scholar 

  • Sparks, W.O., Harrison, R.L., and Bonning, B.C. (2011). Autographa californica multiple nucleopolyhedrovirus ODV-E56 is a per os infectivity factor, but is not essential for binding and fusion of occlusion-derived virus to the host midgut. Virology 409, 69–76.

    Article  CAS  PubMed  Google Scholar 

  • Tang, Q., Li, G., Yao, Q., Chen, L., Lv, P., Lian, C., and Chen, K. (2013). Bm91 is an envelope component of ODV but is dispensable for the propagation of Bombyx mori nucleopolyhedrovirus. J Invertebr Pathol 113, 70–77.

    Article  CAS  PubMed  Google Scholar 

  • Thézé, J., Bézier, A., Periquet, G., Drezen, J.M., and Herniou, E.A. (2011). Paleozoic origin of insect large dsDNA viruses. Proc Natl Acad Sci USA 108, 15931–15935.

    Article  PubMed  PubMed Central  Google Scholar 

  • Wang, D., and Shenk, T. (2005). Human cytomegalovirus virion protein complex required for epithelial and endothelial cell tropism. Proc Natl Acad Sci USA 102, 18153–18158.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Wang, Y., Bininda-Emonds, O.R.P., van Oers, M.M., Vlak, J.M., and Jehle, J.A. (2011). The genome of Oryctes rhinoceros nudivirus provides novel insight into the evolution of nuclear arthropod-specific large circular double-stranded DNA viruses. Virus Genes 42, 444–456.

    Article  CAS  PubMed  Google Scholar 

  • Wei, D., Wang, Y., Zhang, X., Hu, Z., Yuan, M., and Yang, K. (2014). Autographa californica nucleopolyhedrovirus Ac76: a dimeric type II integral membrane protein that contains an inner nuclear membrane-sorting motif. J Virol 88, 1090–1103.

    Article  PubMed  PubMed Central  Google Scholar 

  • Xiang, X., Chen, L., Guo, A., Yu, S., Yang, R., and Wu, X. (2011). The Bombyx mori nucleopolyhedrovirus (BmNPV) ODV-E56 envelope protein is also a per os infectivity factor. Virus Res 155, 69–75.

    Article  CAS  PubMed  Google Scholar 

  • Xiang, X., Shen, Y., Yang, R., Chen, L., Hu, X., and Wu, X. (2013). Bombyx mori nucleopolyhedrovirus BmP95 plays an essential role in budded virus production and nucleocapsid assembly. J Gene Virol 94, 1669–1679.

    Article  CAS  Google Scholar 

  • Xu, H.J., Yang, Z.N., Zhao, J.F., Tian, C.H., Ge, J.Q., Tang, X.D., Bao, Y.Y., and Zhang, C.X. (2008). Bombyx mori nucleopolyhedrovirus ORF56 encodes an occlusion-derived virus protein and is not essential for budded virus production. J Gene Virol 89, 1212–1219.

    Article  CAS  Google Scholar 

  • Yao, L., Zhou, W., Xu, H., Zheng, Y., and Qi, Y. (2004). The Heliothis armigera single nucleocapsid nucleopolyhedrovirus envelope protein P74 is required for infection of the host midgut. Virus Res 104, 111–121.

    Article  CAS  PubMed  Google Scholar 

  • Zhang, J., Shen, Y., and Wu, X. (2014). A minireview on per os infectivity factors of insect baculovirus. Sci Sericult 40, 0730–0736.

    CAS  Google Scholar 

  • Zheng, Q., Shen, Y., Kon, X., Zhang, J., Feng, M., and Wu, X. (2017). Protein-protein interactions of the baculovirus per os infectivity factors (PIFs) in the PIF complex. J Gen Virol in press doi: 10.1099/jgv.0.000730.

    Google Scholar 

  • Zhou, W., Yao, L., Xu, H., Yan, F., and Qi, Y. (2005). The function of envelope protein P74 from Autographa californica multiple nucleopolyhedrovirus in primary infection to host. Virus Genes 30, 139–150.

    Article  CAS  PubMed  Google Scholar 

  • Zhu, S., Wang, W., Wang, Y., Yuan, M., and Yang, K. (2013). The baculovirus core gene ac83 is required for nucleocapsid assembly and per os infectivity of Autographa californica nucleopolyhedrovirus. J Virol 87, 10573–10586.

    Article  CAS  PubMed  PubMed Central  Google Scholar 

Download references

Acknowledgements

This work was supported by the Strategic Priority Research Program of the Chinese Academy of Sciences (XDB11030400), the National Natural Science Foundation of China (31130058,31621061), the Key Research Program of Frontier Sciences of the Chinese Academy of Sciences (QYZDJ-SSW-SMC021), and the Virology Key Frontier Science Program of the State Key Laboratory of Virology (klv-2016-03).

Author information

Authors and Affiliations

  1. State Key Laboratory of Virology, Wuhan Institute of Virology, Chinese Academy of Sciences, Wuhan, 430071, China

    Xi Wang, Xiaoping Liu, George Alliwa Makalliwa, Jiang Li, Hualin Wang, Zhihong Hu & Manli Wang

  2. University of Chinese Academy of Sciences, Beijing, 100049, China

    Xi Wang, Xiaoping Liu & George Alliwa Makalliwa

Authors
  1. Xi Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Xiaoping Liu
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. George Alliwa Makalliwa
    View author publications

    You can also search for this author in PubMed Google Scholar

  4. Jiang Li
    View author publications

    You can also search for this author in PubMed Google Scholar

  5. Hualin Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

  6. Zhihong Hu
    View author publications

    You can also search for this author in PubMed Google Scholar

  7. Manli Wang
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Manli Wang.

Rights and permissions

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Wang, X., Liu, X., Makalliwa, G.A. et al. Per os infectivity factors: a complicated and evolutionarily conserved entry machinery of baculovirus. Sci. China Life Sci. 60, 806–815 (2017). https://doi.org/10.1007/s11427-017-9127-1

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11427-017-9127-1

Keywords

Search

Navigation