Skip to main content
Log in

Expression and localization of Bombyx mori nucleopolyhedrovirus GP37

  • Original Paper
  • Published:
Virus Genes Aims and scope Submit manuscript

Abstract

Mitochondria play an essential role in intracellular energy metabolism. This study described the involvement of Bombyx mori nucleopolyhedrovirus (BmNPV) GP37 (BmGP37) in host mitochondria. Herein, the proteins associated with host mitochondria isolated from BmNPV-infected or mock-infected cells by two-dimensional gel electrophoresis were compared. One mitochondria-associated protein in virus-infected cells was identified as BmGP37 by liquid chromatography-mass spectrometry analysis. Furthermore, the BmGP37 antibodies were generated, which could react specifically with BmGP37 in the BmNPV-infected BmN cells. Western blot experiments showed that BmGP37 was expressed at 18 h post-infection and was verified as a mitochondria-associated protein. Immunofluorescence analysis demonstrated that BmGP37 localized to the host mitochondria during BmNPV infection. Furthermore, western blot analysis revealed that BmGP37 is a novel component protein of the occlusion-derived virus (ODV) of BmNPV. The present results indicated that BmGP37 is one of the ODV-associated proteins and may have important roles in host mitochondria during BmNPV infection.

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.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

Data availability

The datasets generated during and/or analysed during the current study are available from the corresponding author on reasonable request.

References

  1. Jehle JA, Blissard GW, Bonning BC, Cory JS, Herniou EA, Rohrmann GF, Theilmann DA, Vlak JM (2006) On the classification and nomenclature of baculoviruses: a proposal for revision. Arch Virol 151:1257–1266. https://doi.org/10.1007/s00705-006-0763-6

    Article  CAS  PubMed  Google Scholar 

  2. Herniou EA, Luque T, Chen X, Vlak JM, Winstanley D, Cory JS, O’Reilly DR (2001) Use of whole genome sequence data to infer baculovirus phylogeny. J Virol 75:8117–8126. https://doi.org/10.1128/jvi.75.17.8117-8126.2001

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  3. Rohrmann GF (2013) Baculovirus Molecular Biology, 4th ed; National Center for Biotechnology Information: Bethesda (MD), USA, 2019, Available from: https://www.ncbi.nlm.nih.gov/books/NBK543458/

  4. Clem RJ (2005) The role of apoptosis in defense against baculovirus infection in insects. Curr Top Microbiol Immunol 289:113–129. https://doi.org/10.1007/3-540-27320-4_5

    Article  CAS  PubMed  Google Scholar 

  5. Ikeda M, Kobayashi M (1999) Cell-cycle perturbation in Sf9 cells infected with Autographa californica nucleopolyhedrovirus. Virology 258:176–188. https://doi.org/10.1006/viro.1999.9706

    Article  CAS  PubMed  Google Scholar 

  6. Iwanaga M, Shimada T, Kobayashi M, Kang W (2007) Identification of differentially expressed host genes in Bombyx mori nucleopolyhedrovirus infected cells by using subtractive hybridization. Appl Entomol Zool 42:151–159. https://doi.org/10.1303/aez.2007.151

    Article  CAS  Google Scholar 

  7. Nobiron I, O’Reilly DR, Olszewski JA (2003) Autographa californica nucleopolyhedrovirus infection of Spodoptera frugiperda cells: a global analysis of host gene regulation during infection, using a differential display approach. J Gen Virol 84:3029–3039. https://doi.org/10.1099/vir.0.19270-0

    Article  CAS  PubMed  Google Scholar 

  8. Xue J, Qiao N, Zhang W, Cheng RL, Zhang XQ, Bao YY, Xu YP, Gu LZ, Han JJ, Zhang CX (2012) Dynamic interactions between Bombyx mori nucleopolyhedrovirus and its host cells revealed by transcriptome analysis. J Virol 86:7345–7359. https://doi.org/10.1128/JVI.07217-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  9. Cha HJ, Dalal NG, Pham MQ, Kramer SF, Vakharia VN, Bentley WE (2002) Monitoring foreign protein expression under baculovirus p10 and polh promoters in insect larvae. Biotechniques 32(5):986–992. https://doi.org/10.2144/02325bm02

    Article  CAS  PubMed  Google Scholar 

  10. Bernal V, Carinhas N, Yokomizo AY, Carrondo MJT, Alves PM (2009) Cell density effect in the baculovirus-insect cells system: A quantitative analysis of energetic metabolism. Biotechnol Bioeng 104:162–180. https://doi.org/10.1002/bit.22364

    Article  CAS  PubMed  Google Scholar 

  11. Lin YH, Tai CC, Brož V, Tang CK, Chen P, Wu CP, Li CH, Wu YL (2020) Adenosine receptor modulates permissiveness of baculovirus (budded virus) infection via regulation of energy metabolism in Bombyx mori. Front Immunol 11:763. https://doi.org/10.3389/fimmu.2020.00763

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  12. Iwanaga M, Kurihara M, Kobayashi M, Kang W (2002) Characterization of Bombyx mori nucleopolyhedrovirus orf68 gene that encodes a novel structural protein of budded virus. Virology 297:39–47. https://doi.org/10.1006/viro.2002.1443

    Article  CAS  PubMed  Google Scholar 

  13. Gomi S, Majima K, Maeda S (1999) Sequence analysis of the genome of Bombyx mori nucleopolyhedrovirus. J Gen Virol 80:1323–1337. https://doi.org/10.1099/0022-1317-80-5-1323

    Article  CAS  PubMed  Google Scholar 

  14. Iwanaga M, Takaya K, Katsuma S, Ote M, Tanaka S, Kamita SG, Kang W, Shimada T, Kobayashi M (2004) Expression profiling of baculovirus genes in permissive and nonpermissive cell lines. Biochem Biophys Res Commun 323:599–614. https://doi.org/10.1016/j.bbrc.2004.08.114

    Article  CAS  PubMed  Google Scholar 

  15. Ogata M, Kameshima Y, Hattori T, Michishita K, Suzuki T, Kawagishi H, Totani K, Hiratake J, Usui T (2010) Lactosylamidine-based affinity purification for cellulolytic enzymes EG I and CBH I from Hypocrea jecorina and their properties. Carbohydr Res 345:2623–2629. https://doi.org/10.1016/j.carres.2010.10.015

    Article  CAS  PubMed  Google Scholar 

  16. Tanaka Y, Suzuki T, Nakamura L, Nakamura M, Ebihara S, Kurokura T, Iigo M, Dohra H, Habu N, Konno N (2019) A GH family 28 endo-polygalacturonase from the brown-rot fungus Fomitopsis palustris: Purification, gene cloning, enzymatic characterization and effects of oxalate. Int J Biol Macromol 123:108–116. https://doi.org/10.1016/j.ijbiomac.2018.11.004

    Article  CAS  PubMed  Google Scholar 

  17. Iwanaga M, Shibano Y, Ohsawa T, Fujita T, Katsuma S, Kawasaki H (2014) Involvement of HSC70-4 and other inducible HSPs in Bombyx mori nucleopolyhedrovirus infection. Virus Res 179:113–118. https://doi.org/10.1016/j.virusres.2013.10.028

    Article  CAS  PubMed  Google Scholar 

  18. Katou Y, Ikeda M, Kobayashi M (2006) Abortive replication of Bombyx mori nucleopolyhedrovirus in Sf9 and High Five cells: Defective nuclear transport of the virions. Virology 347:455–465. https://doi.org/10.1016/j.virol.2005.11.043

    Article  CAS  PubMed  Google Scholar 

  19. Gross CH, Wolgamot GM, Russell RL, Pearson MN, Rohrmann GF (1993) A 37-kilodalton glycoprotein from a baculovirus of Orgyia pseudotsugata is localized to cytoplasmic inclusion bodies. J Virol 67:469–475. https://doi.org/10.1128/JVI.67.1.469-475.1993

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  20. Phanis CG, Miller DP, Cassar SC, Tristem M, Thiem SM, O’Reilly DR (1999) Identification and expression of two baculovirus gp37 genes. J Gen Virol 80:1823–1831. https://doi.org/10.1099/0022-1317-80-7-1823

    Article  CAS  PubMed  Google Scholar 

  21. Copeland DE, Dalton AJ (1959) An association between mitochondria and the endoplasmic reticulum in cells of the pseudobranch gland of a teleost. J Biophys Biochem Cytol 25:393–396. https://doi.org/10.1083/jcb.5.3.393

    Article  Google Scholar 

  22. Friedman JR, Lackner LL, West M, DiBenedetto JR, Nunnari J, Voeltz GK (2011) ER tubules mark sites of mitochondrial division. Science 334:358–362. https://doi.org/10.1126/science.1207385

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  23. Zhou R, Yazdi AS, Menu P, Tschopp J (2011) A role for mitochondria in NLRP3 inflammasome activation. Nature 469:221–225. https://doi.org/10.1038/nature09663

    Article  CAS  PubMed  Google Scholar 

  24. Hamasaki M, Furuta N, Matsuda A, Nezu A, Yamamoto A, Fujita N, Oomori H, Noda T, Haraguchi T, Hiraoka Y, Amano A, Yoshimori T (2013) Autophagosomes form at ER-mitochondria contact sites. Nature 495:389–393. https://doi.org/10.1038/nature11910

    Article  CAS  PubMed  Google Scholar 

  25. Booth DM, Enyedi B, Geiszt M, Várnai P, Hajnóczky G (2016) Redox nanodomains are induced by and control calcium signaling at the ER-mitochondrial interface. Mol Cell 63:240–248. https://doi.org/10.1016/j.molcel.2016.05.040

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Cheng XW, Krell PJ, Arif BM (2001) P34.8 (GP37) is not essential for baculovirus replication. J Gen Virol 82:299–305. https://doi.org/10.1099/0022-1317-82-2-299

    Article  CAS  PubMed  Google Scholar 

  27. Zhang SZ, Zhu LB, Yu D, You LL, Wang J, Cao HH, Liu YX, Wang YL, Kong X, Toufeeq S, Xu JP (2020) Identification and functional analysis of BmNPV-interacting proteins from Bombyx mori (Lepidoptera) larval midgut based on subcellular protein levels. Front Microbiol 30:1481. https://doi.org/10.3389/fmicb.2020.01481

    Article  Google Scholar 

  28. Chacinska A, Koehler CM, Milenkovic D, Lithgow T, Pfanner N (2009) Importing mitochondrial proteins: machineries and mechanisms. Cell 138:628–644. https://doi.org/10.1016/j.cell.2009.08.005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  29. Abe Y, Shodai T, Muto T, Mihara K, Torii H, Nishikawa S, Endo T, Kohda D (2000) Structural basis of presequence recognition by the mitochondrial protein import receptor Tom20. Cell 100:551–560. https://doi.org/10.1016/s0092-8674(00)80691-1

    Article  CAS  PubMed  Google Scholar 

  30. Yamano K, Yatsukawa Y, Esaki M, Hobbs AE, Jensen RE, Endo T (2008) Tom20 and Tom22 share the common signal recognition pathway in mitochondrial protein import. J Biol Chem 283:3799–3807. https://doi.org/10.1074/jbc.M708339200

    Article  CAS  PubMed  Google Scholar 

  31. Fukasawa Y, Tsuji J, Fu SC, Tomii K, Horton P, Imai K (2015) MitoFates: improved prediction of mitochondrial targeting sequences and their cleavage sites. Mol Cell Proteomics 14:1113–1126. https://doi.org/10.1074/mcp.M114.043083

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Vialard JE, Yuen L, Richardson CD (1990) Identification and characterization of a baculovirus occlusion body glycoprotein which resembles spheroidin, an entomopoxvirus protein. J Virol 64:5804–5811. https://doi.org/10.1128/JVI.64.12.5804-5811.1990

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  33. Mitsuhashi W, Sato M, Hirai Y (2000) Involvement of spindles of an entomopoxvirus (EPV) in infectivity of the EPVs to their host insect. Arch Virol 145:1465–1471. https://doi.org/10.1007/s007050070103

    Article  CAS  PubMed  Google Scholar 

  34. Takemoto Y, Mitsuhashi W, Murakami R, Konishi H, Miyamoto K (2008) The N-terminal region of an entomopoxvirus fusolin is essential for the enhancement of peroral infection, whereas the C-terminal region is eliminated in digestive juice. J Virol 82:12406–12415. https://doi.org/10.1128/JVI.01605-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  35. Wijonarko A, Hukuhara T (1998) Detection of a virus enhancing factor in the spheroid, spindle, and virion of an entomopoxvirus. J Invertebr Pathol 72:82–86. https://doi.org/10.1006/jipa.1998.4756

    Article  CAS  PubMed  Google Scholar 

  36. Li Z, Li C, Yang K, Wang L, Yin C, Gong Y, Pang Y (2003) Characterization of a chitin-binding protein GP37 of Spodoptera litura multicapsid nucleopolyhedrovirus. Virus Res 96:113–122. https://doi.org/10.1016/s0168-1702(03)00179-5

    Article  CAS  PubMed  Google Scholar 

  37. Wang P, Granados RR (1997) An intestinal mucin is the target substrate for a baculovirus enhancin. Proc Natl Acad Sci USA 94:6977–6982. https://doi.org/10.1073/pnas.94.13.6977

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  38. Liu X, Fang W, Fan R, Zhang L, Lei C, Zhang J, Nian W, Dou T, An S, Zhou L, Sun X (2019) Granulovirus GP37 facilitated ODVs cross insect peritrophic membranes and fuse with epithelia. Toxins (Basel) 11:145. https://doi.org/10.3390/toxins11030145

    Article  CAS  PubMed  Google Scholar 

  39. Liu X, Ma X, Lei C, Xiao Y, Zhang Z, Sun X (2011) Synergistic effects of Cydia pomonella granulovirus GP37 on the infectivity of nucleopolyhedroviruses and the lethality of Bacillus thuringiensis. Arch Virol 156:1707–1715. https://doi.org/10.1007/s00705-011-1039-3

    Article  CAS  PubMed  Google Scholar 

  40. Li X, Barrett J, Pang A, Klose RJ, Krell PJ, Arif BM (2000) Characterization of an overexpressed spindle protein during a baculovirus infection. Virology 268:56–67. https://doi.org/10.1006/viro.1999.0138

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgements

This work was supported by grants from JSPS KAKENHI (grant no. 20K06069) to MI. The authors are grateful to Dr. Ikeda for the kind gift of anti-VP39 antibody. The authors would like to thank Enago (www.enago.jp) for the English language review.

Author information

Authors and Affiliations

Authors

Contributions

All authors contributed to the study conception and design. The experiments were conceived and designed by SF and MI. The experiments were performed by SF, KF, TS, SK, and MI. The paper was written by MI and SK.

Corresponding author

Correspondence to Masashi Iwanaga.

Ethics declarations

Conflicts of interest

The authors declare that they have no conflict of interest.

Ethical approval

This study was performed in accordance with institutional committee protocols of Utsunomiya University.

Informed consent

There were no human participants in this study.

Research involving human and animal participants

This article does not contain any studies with human participants or animals performed by any of the authors.

Additional information

Edited by Sassan Asgari.

Publisher's Note

Springer Nature remains neutral with regard to jurisdictional claims in published maps and institutional affiliations.

Rights and permissions

Springer Nature or its licensor (e.g. a society or other partner) holds exclusive rights to this article under a publishing agreement with the author(s) or other rightsholder(s); author self-archiving of the accepted manuscript version of this article is solely governed by the terms of such publishing agreement and applicable law.

Reprints and permissions

About this article

Check for updates. Verify currency and authenticity via CrossMark

Cite this article

Fujimoto, S., Fujimaki, K., Suzuki, T. et al. Expression and localization of Bombyx mori nucleopolyhedrovirus GP37. Virus Genes 59, 457–463 (2023). https://doi.org/10.1007/s11262-023-01983-3

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s11262-023-01983-3

Keywords

Navigation