For best viewing of the website please use Mozilla Firefox or Google Chrome.
Citation: Xingang Chen, Xiaoqin Yang, Chengfeng Lei, Fujun Qin, Xiulian Sun, Jia Hu. Autographa Californica Multiple Nucleopolyhedrovirus orf13 Is Required for Efficient Nuclear Egress of Nucleocapsids [J].VIROLOGICA SINICA.  http://dx.doi.org/10.1007/s12250-021-00353-3

Autographa Californica Multiple Nucleopolyhedrovirus orf13 Is Required for Efficient Nuclear Egress of Nucleocapsids

  • Corresponding author: Xiulian Sun, sunxl@wh.iov.cn
    Jia Hu, hujia@wh.iov.cn
  • Received Date: 20 October 2020
    Accepted Date: 18 December 2020
    Published Date: 15 March 2021
  • Autographa californica multiple nucleopolyhedrovirus (AcMNPV) orf13 (ac13) is a conserved gene in all sequenced alphabaculoviruses. However, its function in the viral life cycle remains unknown. In this study, we found that ac13 was a late gene and that the encoded protein, bearing a putative nuclear localization signal motif, colocalized with the nuclear lamina. Deletion of ac13 did not affect viral genome replication, nucleocapsid assembly or occlusion body (OB) formation, but reduced virion budding from infected cells by approximately 400-fold compared with the wild-type virus. Deletion of ac13 substantially impaired the egress of nucleocapsids from the nucleus to the cytoplasm, while the OB morphogenesis was unaffected. Taken together, our results indicated that ac13 was required for efficient nuclear egress of nucleocapsids during virion budding, but was dispensable for OB formation.

  • 加载中
  • s12250-021-00353-3-ESM.pdf
    1. Biswas S, Willis LG, Fang M, Nie Y, Theilmann DA (2017) Autographa californica nucleopolyhedrovirus ac141 (exon0), a potential e3 ubiquitin ligase, interacts with viral ubiquitin and ac66 to facilitate nucleocapsid egress. J Virol 92:e01713-01717

    2. Blissard GW, Theilmann DA (2018) Baculovirus entry and egress from insect cells. Annu Rev Virol 5:113–139

    3. Chen YR, Zhong S, Fei Z, Hashimoto Y, Xiang JZ, Zhang S, Blissard GW (2013) The transcriptome of the baculovirus autographa californica multiple nucleopolyhedrovirus in trichoplusia ni cells. J Virol 87:6391–6405

    4. Datsenko KA, Wanner BL (2000) One-step inactivation of chromosomal genes in escherichia coli k-12 using pcr products. Proc Natl Acad Sci U S A 97:6640–6645

    5. Fang M, Dai D, Theilmann DA (2007) Autographa californica multiple nucleopolyhedrovirus exon0 (orf141) is required for efficient egress of nucleocapsids from the nucleus. J Virol 81:9859–9869

    6. Feng G, Krell PJ (2014) Autographa californica multiple nucleopolyhedrovirus DNA polymerase c terminus is required for nuclear localization and viral DNA replication. J Virol 88:10918–10933

    7. Fraser MJ (1986) Ultrastructural observations of virion maturation in autographa californica nuclear polyhedrosis virus infected spodoptera frugiperda cell cultures. J Ultrastruct Mol Struct Res 95:189–195

    8. Gross CH, Russell RL, Rohrmann GF (1994) Orgyia pseudotsugata baculovirus p10 and polyhedron envelope protein genes: Analysis of their relative expression levels and role in polyhedron structure. J Gen Virol 75:1115–1123

    9. Guo Y, Yue Q, Gao J, Wang Z, Chen Y, Blissard GW, Liu T, Li Z (2017a) Roles of cellular nsf protein in entry and nuclear egress of budded virions of autographa californica multiple nucleopolyhedrovirus. J Virol 91:e01111-01117

    10. Guo YJ, Fu SH, Li LL (2017b) Autographa californica multiple nucleopolyhedrovirus ac75 is required for egress of nucleocapsids from the nucleus and formation of de novo intranuclear membrane microvesicles. PLoS ONE 12:e0185630

    11. Hellberg T, Passvogel L, Schulz KS, Klupp BG, Mettenleiter TC (2016) Nuclear egress of herpesviruses: The prototypic vesicular nucleocytoplasmic transport. Adv Virus Res 94:81–140

    12. 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

    13. Huang Z, Pan M, Zhu S, Zhang H, Wu W, Yuan M, Yang K (2017) The autographa californica multiple nucleopolyhedrovirus ac83 gene contains a cis-acting element that is essential for nucleocapsid assembly. J Virol 91:e02110-02116

    14. Jehle JA, Blissard GW, Bonning BC, Cory JS, Herniou EA, Rohrmann GF, Theilmann DA, Thiem SM, Vlak JM (2006) On the classification and nomenclature of baculoviruses: a proposal for revision. Arch Virol 151:1257–1266

    15. Johnson DC, Baines JD (2011) Herpesviruses remodel host membranes for virus egress. Nat Rev Microbiol 9:382–394

    16. Jones P, Binns D, Chang HY, Fraser M, Li W, McAnulla C, McWilliam H, Maslen J, Mitchell A, Nuka G, Pesseat S, Quinn AF, Sangrador-Vegas A, Scheremetjew M, Yong SY, Lopez R, Hunter S (2014) Interproscan 5: genome-scale protein function classification. Bioinformatics 30:1236–1240

    17. 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

    18. Klupp BG, Granzow H, Fuchs W, Keil GM, Finke S, Mettenleiter TC (2007) Vesicle formation from the nuclear membrane is induced by coexpression of two conserved herpesvirus proteins. Proc Natl Acad Sci U S A 104:7241–7246

    19. Kokusho R, Koh Y, Fujimoto M, Shimada T, Katsuma S (2016) Bombyx mori nucleopolyhedrovirus bm5 protein regulates progeny virus production and viral gene expression. Virology 498:240–249

    20. Kuang W, Zhang H, Wang M, Zhou NY, Deng F, Wang H, Gong P, Hu Z (2017) Three conserved regions in baculovirus sulfhydryl oxidase p33 are critical for enzymatic activity and function. J Virol 91:e01158-e11117

    21. Lei C, Yang J, Hu J, Sun X (2020) On the calculation of tcid50 for quantitation of virus infectivity. Virol Sin. https://doi.org/10.1007/s12250-020-00230-5.

    22. Li C, Wen A, Shen B, Lu J, Huang Y, Chang Y (2011) Fastcloning: a highly simplified, purification-free, sequence- and ligation-independent pcr cloning method. BMC Biotechnol 11:92

    23. Li J, Zhou Y, Lei C, Fang W, Sun X (2015) Improvement in the UV resistance of baculoviruses by displaying nano-zinc oxide-binding peptides on the surfaces of their occlusion bodies. Appl Microbiol Biotechnol 99:6841–6853

    24. Li Y, Shen S, Hu L, Deng F, Vlak JM, Hu Z, Wang H, Wang M (2018) The functional oligomeric state of tegument protein gp41 is essential for baculovirus bv and odv assembly. J Virol 92:e02083-e12017

    25. Marchler-Bauer A, Bo Y, Han L, He J, Lanczycki CJ, Lu S, Chitsaz F, Derbyshire MK, Geer RC, Gonzales NR, Gwadz M, Hurwitz DI, Lu F, Marchler GH, Song JS, Thanki N, Wang Z, Yamashita RA, Zhang D, Zheng C, Geer LY, Bryant SH (2017) Cdd/sparcle: functional classification of proteins via subfamily domain architectures. Nucl Acids Res 45:D200–D203

    26. McCarthy CB, Dai X, Donly C, Theilmann DA (2008) Autographa californica multiple nucleopolyhedrovirus ac142, a core gene that is essential for bv production and odv envelopment. Virology 372:325–339

    27. Ohkawa T, Welch MD (2018) Baculovirus actin-based motility drives nuclear envelope disruption and nuclear egress. Curr Biol 28:2153–2159

    28. Olson VA, Wetter JA, Friesen PD (2002) Baculovirus transregulator ie1 requires a dimeric nuclear localization element for nuclear import and promoter activation. J Virol 76:9505–9515

    29. Olszewski J, Miller LK (1997) A role for baculovirus gp41 in budded virus production. Virology 233:292–301

    30. Ono C, Kamagata T, Taka H, Sahara K, Asano S, Bando H (2012) Phenotypic grouping of 141 bmnpvs lacking viral gene sequences. Virus Res 165:197–206

    31. Pearson MN, Rohrmann GF (2002) Transfer, incorporation, and substitution of envelope fusion proteins among members of the baculoviridae, orthomyxoviridae, and metaviridae (insect retrovirus) families. J Virol 76:5301–5304

    32. Peng Y, Li K, Pei RJ, Wu CC, Liang CY, Wang Y, Chen XW (2012) The protamine-like DNA-binding protein p6.9 epigenetically up-regulates autographa californica multiple nucleopolyhedrovirus gene transcription in the late infection phase. Virol Sin 27:57–68

    33. Qin F, Xu C, Hu J, Lei C, Zheng Z, Peng K, Wang H, Sun X (2019) Dissecting the cell entry pathway of baculovirus by single-particle tracking and quantitative electron microscopic analysis. J Virol 93:e00033-e119

    34. Qiu J, Tang Z, Cai Y, Wu W, Yuan M, Yang K (2019) The autographa californica multiple nucleopolyhedrovirus ac51 gene is required for efficient nuclear egress of nucleocapsids and is essential for in vivo virulence. J Virol 93:e01923-e11918

    35. Rohrmann GF (2019) Baculovirus molecular biology, 4th edn. National Center for Biotechnology Information, Bethesda

    36. Shen YW, Feng M, Wu XF (2018) Bombyx mori nucleopolyhedrovirus orf40 is essential for budded virus production and occlusion-derived virus envelopment. J Gen Virol 99:837–850

    37. Shi A, Hu Z, Zuo Y, Wang Y, Wu W, Yuan M, Yang K (2017) Autographa californica multiple nucleopolyhedrovirus ac75 is required for the nuclear egress of nucleocapsids and intranuclear microvesicle formation. J Virol 92:e01509-01517

    38. Slack J, Arif BM (2006) The baculoviruses occlusion‐derived virus: virion structure and function. Adv Virus Res 69:99–165

    39. Tao XY, Choi JY, Kim WJ, Lee JH, Liu Q, Kim SE, An SB, Lee SH, Woo SD, Jin BR, Je YH (2013) The autographa californica multiple nucleopolyhedrovirus orf78 is essential for budded virus production and general occlusion body formation. J Virol 87:8441–8450

    40. Tao XY, Choi JY, Kim WJ, An SB, Liu Q, Kim SE, Lee SH, Kim JH, Woo SD, Jin BR, Je YH (2015) Autographa californica multiple nucleopolyhedrovirus orf11 is essential for budded-virus production and occlusion-derived-virus envelopment. J Virol 89:373–383

    41. PubMed Article CAS

    42. Vanarsdall AL, Okano K, Rohrmann GF (2005) Characterization of the replication of a baculovirus mutant lacking the DNA polymerase gene. Virology 331:175–180

    43. Victoria A, Mei Y, Carstens EB (2009) Characterization of a baculovirus nuclear localization signal domain in the late expression factor 3 protein. Virology 385:209–217

    44. Xu C, Wang J, Yang J, Lei C, Hu J, Sun X (2019) Nsp2 forms viroplasms during dendrolimus punctatus cypovirus infection. Virology 533:68–76

    45. Young JC, MacKinnon EA, Faulkner P (1993) The architecture of the virogenic stroma in isolated nuclei of spodoptera frugiperda cells in vitro infected by autographa californica nuclear polyhedrosis virus. J Struct Biol 110:141–153

    46. Yuan M, Huang Z, Wei D, Hu Z, Yang K, Pang Y (2011) Identification of autographa californica nucleopolyhedrovirus ac93 as a core gene and its requirement for intranuclear microvesicle formation and nuclear egress of nucleocapsids. J Virol 85:11664–11674

    47. Yuan M, Wu W, Liu C, Wang Y, Hu Z, Yang K, Pang Y (2008) A highly conserved baculovirus gene p48 (ac103) is essential for bv production and odv envelopment. Virology 379:87–96

    48. Yue Q, Yu Q, Yang Q, Xu Y, Guo Y, Blissard GW, Li Z (2018) Distinct roles of cellular escrt-i and escrt-iii proteins in efficient entry and egress of budded virions of autographa californica multiple nucleopolyhedrovirus. J Virol 92:e01636-e11617

  • 加载中

Article Metrics

Article views(2459) PDF downloads(10) Cited by()

Related
Proportional views
    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Autographa Californica Multiple Nucleopolyhedrovirus orf13 Is Required for Efficient Nuclear Egress of Nucleocapsids

      Corresponding author: Xiulian Sun, sunxl@wh.iov.cn
      Corresponding author: Jia Hu, hujia@wh.iov.cn
    • 1 Wuhan Institute of Virology, Center for Biosafety MegaScience, Chinese Academy of Sciences, Wuhan 430071, China
    • 2 University of Chinese Academy of Sciences, Beijing 100049, China

    Abstract: Autographa californica multiple nucleopolyhedrovirus (AcMNPV) orf13 (ac13) is a conserved gene in all sequenced alphabaculoviruses. However, its function in the viral life cycle remains unknown. In this study, we found that ac13 was a late gene and that the encoded protein, bearing a putative nuclear localization signal motif, colocalized with the nuclear lamina. Deletion of ac13 did not affect viral genome replication, nucleocapsid assembly or occlusion body (OB) formation, but reduced virion budding from infected cells by approximately 400-fold compared with the wild-type virus. Deletion of ac13 substantially impaired the egress of nucleocapsids from the nucleus to the cytoplasm, while the OB morphogenesis was unaffected. Taken together, our results indicated that ac13 was required for efficient nuclear egress of nucleocapsids during virion budding, but was dispensable for OB formation.

    Reference (48) Relative (20)

    目录

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return