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Label-free proteomics analysis on the envelope of budded viruses of Bombyx mori nucleopolyhedrovirus harboring differential localized GP64

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Abstract

Bombyx mori nucleopolyhedrovirus (BmNPV) GP64 is the key membrane fusion protein that mediates budded virus (BV) infection. We recently reported that BmNPV GP64’s n-region of signal peptide (SP) blocked the SP-cleavage and mediated GP64 localization on the plasma membrane (PM); n-region (SP∆nGP64) absence caused GP64 intracellular localization, however, SP∆nGP64 was still incorporated into virion to generate BVs with lower infectivity. To better understand the biogenesis of the envelope of BmNPV BV, we conducted a label-free ESI mass spectrometry analysis of the envelope of purified BVs harboring PM localized GP64 or intracellular localized SP∆nGP64. The results indicated that 31 viral proteins were identified on the envelope, among which 15 were reported in other viruses. The other 16 proteins were first reported in BmNPV BV, including the BmNPV-specific protein BRO-A and proteins associated with vesicle transportation. Six proteins with significant intensity differences were detected in virions with differential localized GP64, and five specific proteins were identified in virions with GP64. Meanwhile, we identified 81 host proteins on the envelope, and seven lipoproteins were first identified in baculovirus virion; other 74 proteins are involved in the cytoskeleton, DNA-binding, vesicle transport, etc. In the meantime, eight and five specific host proteins were, respectively, identified in GP64 and SP∆nGP64’s virions. The two virions shared 68 common host proteins, and 8 proteins were identified on their envelopes with a significant difference. This study provides new insight into the protein composition of BmNPV BV and a clue for further investigation of the budding mechanism of BmNPV.

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Data are available via ProteomeXchange with identifier PXD037503.

References

  1. Guo Y, Yue Q, Gao J, Wang Z, Chen YR, Blissard GW, Liu TX, Li Z (2017) Roles of cellular NSF protein in entry and nuclear egress of budded virions of autographa californica multiple nucleopolyhedrovirus. J Virol. https://doi.org/10.1128/JVI.01111-17

    Article  PubMed  PubMed Central  Google Scholar 

  2. 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. https://doi.org/10.1128/JVI.01636-17

    Article  PubMed  Google Scholar 

  3. Hamajima R, Saito A, Makino S, Kobayashi M, Ikeda M (2018) Antiviral immune responses of Bombyx mori cells during abortive infection with Autographa californica multiple nucleopolyhedrovirus. Virus Res 258:28–38. https://doi.org/10.1016/j.virusres.2018.09.014

    Article  CAS  PubMed  Google Scholar 

  4. 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. https://doi.org/10.1128/JVI.01742-14

    Article  CAS  PubMed  Google Scholar 

  5. Gauthier D, Thirunavukkarasu K, Faris BL, Russell DL, Weaver RF (2012) Characterization of an Autographa californica multiple nucleopolyhedrovirus dual mutant: ORF82 is required for budded virus production, and a point mutation in LEF-8 alters late and abolishes very late transcription. J Gen Virol 93:364–373. https://doi.org/10.1099/vir.0.037028-0

    Article  CAS  PubMed  Google Scholar 

  6. Nie Y, Fang M, Theilmann DA (2011) Autographa californica multiple nucleopolyhedrovirus core gene ac92 (p33) is required for efficient budded virus production. Virology 409:38–45. https://doi.org/10.1016/j.virol.2010.09.023

    Article  CAS  PubMed  Google Scholar 

  7. Rohrmann GF (2019) Baculovirus molecular biology [internet]. National Center for Biotechnology Information (US), Bethesda (MD)

  8. Xu YP, Gu LZ, Lou YH, Cheng RL, Xu HJ, Wang WB, Zhang CX (2012) A baculovirus isolated from wild silkworm encompasses the host ranges of Bombyx mori nucleopolyhedrosis virus and Autographa californica multiple nucleopolyhedrovirus in cultured cells. J Gen Virol 93:2480–2489. https://doi.org/10.1099/vir.0.043836-0

    Article  CAS  PubMed  Google Scholar 

  9. 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 

  10. Hao B, Liu L, Liu N, Sun L, Fan F, Huang J (2022) The Bombyx mori nucleopolyhedrovirus GP64 retains the transmembrane helix of signal peptide to contribute to secretion across the cytomembrane. Microbiol Spectr. https://doi.org/10.1128/spectrum.01913-22

    Article  PubMed  PubMed Central  Google Scholar 

  11. Hao B, Nan W, Xu Y, Liu L, Liu N, Huang J (2021) Two cholesterol recognition amino acid consensus motifs of GP64 with uncleaved signal peptide are required for Bombyx mori nucleopolyhedrovirus infection. Microbiol Spectr 9:e0172521. https://doi.org/10.1128/Spectrum.01725-21

    Article  PubMed  Google Scholar 

  12. Huang J, Liu N, Xu F, Ayepa E, Amanze C, Sun L, Shen Y, Yang M, Yang S, Shen X, Hao B (2019) Efficient expression and processing of ebola virus glycoprotein induces morphological changes in BmN cells but cannot rescue deficiency of Bombyx mori nucleopolyhedrovirus GP64. Viruses. https://doi.org/10.3390/v11111067

    Article  PubMed  PubMed Central  Google Scholar 

  13. Sun L, Yao C, Amanze C, Yin B, Huang J, Hao B (2022) The cytoplasmic tail substitution increases the assembly efficiency of Ebola virus glycoprotein on the budded virus of Bombyx mori nucleopolyhedrovirus. Protein Expr Purif 200:106156. https://doi.org/10.1016/j.pep.2022.106156

    Article  CAS  PubMed  Google Scholar 

  14. Wang M, Tuladhar E, Shen S, Wang H, van Oers MM, Vlak JM, Westenberg M (2010) Specificity of baculovirus P6.9 basic DNA-binding proteins and critical role of the C terminus in virion formation. J Virol 84:8821–8828. https://doi.org/10.1128/JVI.00072-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  15. Hou D, Zhang L, Deng F, Fang W, Wang R, Liu X, Guo L, Rayner S, Chen X, Wang H, Hu Z (2013) Comparative proteomics reveal fundamental structural and functional differences between the two progeny phenotypes of a baculovirus. J Virol 87:829–839. https://doi.org/10.1128/JVI.02329-12

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  16. Wisniewski JR, Zougman A, Nagaraj N, Mann M (2009) Universal sample preparation method for proteome analysis. Nat Methods 6:359–362. https://doi.org/10.1038/nmeth.1322

    Article  CAS  PubMed  Google Scholar 

  17. Luber CA, Cox J, Lauterbach H, Fancke B, Selbach M, Tschopp J, Akira S, Wiegand M, Hochrein H, O’Keeffe M, Mann M (2010) Quantitative proteomics reveals subset-specific viral recognition in dendritic cells. Immunity 32:279–289. https://doi.org/10.1016/j.immuni.2010.01.013

    Article  CAS  PubMed  Google Scholar 

  18. Wang R, Deng F, Hou D, Zhao Y, Guo L, Wang H, Hu Z (2010) Proteomics of the Autographa californica nucleopolyhedrovirus budded virions. J Virol 84:7233–7242. https://doi.org/10.1128/JVI.00040-10

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  19. Wang Y, Jin F, Wang R, Li F, Wu Y, Kitazato K, Wang Y (2017) HSP90: a promising broad-spectrum antiviral drug target. Arch Virol 162:3269–3282. https://doi.org/10.1007/s00705-017-3511-1

    Article  CAS  PubMed  Google Scholar 

  20. Huang J, Li C, Tang X, Liu L, Nan W, Shen X, Hao B (2019) Transport via macropinocytic vesicles is crucial for productive infection with Bombyx mori nucleopolyhedrovirus. Viruses. https://doi.org/10.3390/v11070668

    Article  PubMed  PubMed Central  Google Scholar 

  21. Huang J, Hao B, Cheng C, Liang F, Shen X, Cheng X (2014) Entry of Bombyx mori nucleopolyhedrovirus into BmN cells by cholesterol-dependent macropinocytic endocytosis. Biochem Biophys Res Commun 453:166–171. https://doi.org/10.1016/j.bbrc.2014.09.073

    Article  CAS  PubMed  Google Scholar 

  22. 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. https://doi.org/10.1016/j.virusres.2012.02.016

    Article  CAS  PubMed  Google Scholar 

  23. Kang WK, Imai N, Suzuki M, Iwanaga M, Matsumoto S, Zemskov EA (2003) Interaction of Bombyx mori nucleopolyhedrovirus BRO-A and host cell protein laminin. Arch Virol 148:99–113. https://doi.org/10.1007/s00705-002-0902-7

    Article  CAS  PubMed  Google Scholar 

  24. Shen H, Chen K, Yao Q, Zhou Y (2009) Characterization of the Bm61 of the Bombyx mori nucleopolyhedrovirus. Curr Microbiol 59:65–70. https://doi.org/10.1007/s00284-009-9399-6

    Article  CAS  PubMed  Google Scholar 

  25. Chen L, Shen Y, Yang R, Wu X, Hu W, Shen G (2015) Bombyx mori nucleopolyhedrovirus (BmNPV) Bm64 is required for BV production and per os infection. Virol J 12:173. https://doi.org/10.1186/s12985-015-0399-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  26. Shen H, Chen K (2012) BM61 of Bombyx mori nucleopolyhedrovirus: its involvement in the egress of nucleocapsids from the nucleus. FEBS Lett 586:990–995. https://doi.org/10.1016/j.febslet.2011.12.040

    Article  CAS  PubMed  Google Scholar 

  27. Nagamine T, Inaba T, Sako Y (2019) A nuclear envelop-associated baculovirus protein promotes intranuclear lipid accumulation during infection. Virology 532:108–117. https://doi.org/10.1016/j.virol.2019.04.006

    Article  CAS  PubMed  Google Scholar 

  28. Ge JQ, Gao GH, Xu YP, Zhang CX (2011) Characterization of a late gene, ORF75 from Bombyx mori nucleopolyhedrovirus. Mol Biol Rep 38:2141–2149. https://doi.org/10.1007/s11033-010-0341-6

    Article  CAS  PubMed  Google Scholar 

  29. Obeng E, Lei J, Ngowo J, Mao F, Yan H, Zhu Y, Yu W (2021) Acetylation of nucleopolyhedrovirus P35 is crucial for its anti-apoptotic activity in silkworm. Bombyx mori Acta Virol 65:264–272. https://doi.org/10.4149/av_2021_303

    Article  CAS  PubMed  Google Scholar 

  30. Shen H, Wang R, Han Q, Zhang W, Nin B, Zhou Y, Shao S, Yao Q, Chen K, Liu X (2013) Characterization of Bombyx mori nucleopolyhedrovirus Bm17. J Basic Microbiol 53:808–814. https://doi.org/10.1002/jobm.201200165

    Article  CAS  PubMed  Google Scholar 

  31. Guo YJ, Fu SH, Li LL (2017) 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. https://doi.org/10.1371/journal.pone.0185630

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  32. Patmanidi AL, Possee RD, King LA (2003) Formation of P10 tubular structures during AcMNPV infection depends on the integrity of host-cell microtubules. Virology 317:308–320. https://doi.org/10.1016/j.virol.2003.08.035

    Article  CAS  PubMed  Google Scholar 

  33. Raza F, McGouran JF, Kessler BM, Possee RD, King LA (2017) Phosphorylation induces structural changes in the Autographa californica nucleopolyhedrovirus P10 protein. J Virol. https://doi.org/10.1128/JVI.00002-17

    Article  PubMed  PubMed Central  Google Scholar 

  34. Katsuma S, Shimada T (2015) The killing speed of egt-inactivated Bombyx mori nucleopolyhedrovirus depends on the developmental stage of B. mori larvae. J Invertebr Pathol 126:64–70. https://doi.org/10.1016/j.jip.2015.01.012

    Article  PubMed  Google Scholar 

  35. Shen H, Chen K, Yao Q, Yu W, Pan Y, Huo J, Xia H, Huang G (2009) Characterization of Bombyx mori nucleopolyhedrovirus orf74, a novel gene involved in virulence of virus. Virus Genes 38:487–494. https://doi.org/10.1007/s11262-009-0350-5

    Article  CAS  PubMed  Google Scholar 

  36. Braunagel SC, He H, Ramamurthy P, Summers MD (1996) Transcription, translation, and cellular localization of three Autographa californica nuclear polyhedrosis virus structural proteins: ODV-E18, ODV-E35, and ODV-EC27. Virology 222:100–114. https://doi.org/10.1006/viro.1996.0401

    Article  CAS  PubMed  Google Scholar 

  37. McCarthy CB, Theilmann DA (2008) AcMNPV ac143 (odv-e18) is essential for mediating budded virus production and is the 30th baculovirus core gene. Virology 375:277–291. https://doi.org/10.1016/j.virol.2008.01.039

    Article  CAS  PubMed  Google Scholar 

  38. Yan H, Shobahah J, Wei M, Obeng E, Xue S, Hu D, Quan Y, Yu W (2019) Phosphorylation of nucleopolyhedrovirus 39K is essential for the regulation of viral gene transcription in silkworm cells. Acta Virol 63:469. https://doi.org/10.4149/av_2019_414

    Article  CAS  PubMed  Google Scholar 

  39. Shen Y, Feng M, Wu X (2018) Bombyx mori nucleopolyhedrovirus ORF40 is essential for budded virus production and occlusion-derived virus envelopment. J Gen Virol 99:837–850. https://doi.org/10.1099/jgv.0.001066

    Article  CAS  PubMed  Google Scholar 

  40. Wang D, Zhang CX (2007) Helicoverpa armigera nucleopolyhedrovirus ORF80 encodes a late, nonstructural protein. J Biochem Mol Biol 40:65–71. https://doi.org/10.5483/bmbrep.2007.40.1.065

    Article  PubMed  Google Scholar 

  41. Marek M, Merten OW, Galibert L, Vlak JM, van Oers MM (2011) Baculovirus VP80 protein and the F-actin cytoskeleton interact and connect the viral replication factory with the nuclear periphery. J Virol 85:5350–5362. https://doi.org/10.1128/JVI.00035-11

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  42. Braunagel S, Russell W, Rosas-Acosta G, Russell D, Summers M (2003) Determination of the protein composition of the occlusion-derived virus of Autographa californica nucleopolyhedrovirus. Proc Natl Acad Sci 100:9797–9802. https://doi.org/10.1073/pnas.1733972100

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  43. Pearson MN, Russell RL, Rohrmann G (2001) Characterization of a baculovirus-encoded protein that is associated with infected-cell membranes and budded virions. J Virology 291:22–31. https://doi.org/10.1006/viro.2001.1191

    Article  CAS  Google Scholar 

  44. Xu W, Kong X, Liu H, Wang H, Wu X (2020) Bombyx mori nucleopolyhedrovirus F-like protein Bm14 is a type I integral membrane protein that facilitates ODV attachment to the midgut epithelial cells. J Gen Virol 101:309–321. https://doi.org/10.1099/jgv.0.001389

    Article  CAS  PubMed  Google Scholar 

  45. Lung OY, Cruz-Alvarez M, Blissard GW (2003) Ac23, an envelope fusion protein homolog in the baculovirus Autographa californica multicapsid nucleopolyhedrovirus, is a viral pathogenicity factor. J Virol 77:328–339. https://doi.org/10.1128/jvi.77.1.328-339.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  46. Sakai M, Kakutani S, Asano SI, Sato M, Bando H (2021) Proliferation of Bombyx mori nucleopolyhedrovirus strain H4 in BmN cells is enhanced by exchange of the F gene sequence with type strain T3. Virus Res 291:198195. https://doi.org/10.1016/j.virusres.2020.198195

    Article  CAS  PubMed  Google Scholar 

  47. Kong X, Xu W, Chen N, Li Y, Shen Y, Wu X (2021) Bombyx mori nucleopolyhedrovirus F-like protein Bm14 is a factor for viral-induced cytopathic effects via regulating oxidative phosphorylation and cellular ROS levels. Virology 552:83–93. https://doi.org/10.1016/j.virol.2020.10.001

    Article  CAS  PubMed  Google Scholar 

  48. Xu W, Fan Y, Wang H, Feng M, Wu X (2019) Bombyx mori nucleopolyhedrovirus F-like protein Bm14 affects the morphogenesis and production of occlusion bodies and the embedding of ODVs. Virology 526:61–71. https://doi.org/10.1016/j.virol.2018.10.008

    Article  CAS  PubMed  Google Scholar 

  49. Xu HJ, Yang ZN, Zhao JF, Tian CH, Ge JQ, Tang XD, Bao YY, Zhang CX (2008) Bombyx mori nucleopolyhedrovirus ORF56 encodes an occlusion-derived virus protein and is not essential for budded virus production. J Gen Virol 89:1212–1219. https://doi.org/10.1099/vir.0.83633-0

    Article  CAS  PubMed  Google Scholar 

  50. Imai N, Matsuda N, Tanaka K, Nakano A, Matsumoto S, Kang W (2003) Ubiquitin ligase activities of Bombyx mori nucleopolyhedrovirus RING finger proteins. J Virol 77:923–930. https://doi.org/10.1128/jvi.77.2.923-930.2003

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  51. Katsuma S, Kawaoka S, Mita K, Shimada T (2008) Genome-wide survey for baculoviral host homologs using the Bombyx genome sequence. Insect Biochem Mol Biol 38:1080–1086. https://doi.org/10.1016/j.ibmb.2008.05.008

    Article  CAS  PubMed  Google Scholar 

  52. Loret S, Guay G, Lippé R (2008) Comprehensive characterization of extracellular herpes simplex virus type 1 virions. J Virol 82:8605–8618. https://doi.org/10.1128/JVI.00904-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  53. Chung C-S, Chen C-H, Ho M-Y, Huang C-Y, Liao C-L, Chang WJ (2006) Vaccinia virus proteome: identification of proteins in vaccinia virus intracellular mature virion particles. J Virol 80:2127–2140. https://doi.org/10.1128/JVI.80.5.2127-2140

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  54. Luftig RB, Lupo LD (1994) Viral interactions with the host-cell cytoskeleton: the role of retroviral proteases. Trends Microbiol 2:178–182. https://doi.org/10.1016/0966-842x(94)90669-6

    Article  CAS  PubMed  Google Scholar 

  55. Katsuma S, Tsuchida A, Matsuda-Imai N, Kang W, Shimada T (2011) Role of the ubiquitin-proteasome system in Bombyx mori nucleopolyhedrovirus infection. J Gen Virol 92:699–705. https://doi.org/10.1099/vir.0.027573-0

    Article  CAS  PubMed  Google Scholar 

  56. Zemskov EA, Kang W, Maeda S (2000) Evidence for nucleic acid binding ability and nucleosome association of Bombyx mori nucleopolyhedrovirus BRO proteins. J Virol 74:6784–6789. https://doi.org/10.1128/jvi.74.15.6784-6789.2000

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  57. Gupta S, Yla-Anttila P, Sandalova T, Achour A, Masucci MG (2020) Interaction with 14–3-3 correlates with inactivation of the RIG-I signalosome by herpesvirus ubiquitin deconjugases. Front Immunol 11:437. https://doi.org/10.3389/fimmu.2020.00437

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  58. Thatte J, Banks L (2017) Human papillomavirus 16 (HPV-16), HPV-18, and HPV-31 E6 override the normal phosphoregulation of E6AP enzymatic activity. J Virol. https://doi.org/10.1128/JVI.01390-17

    Article  PubMed  PubMed Central  Google Scholar 

  59. Yue Q, Li J, Guo Y, Yan F, Liu X, Blissard GW, Li Z (2020) Efficient entry of budded virions of Autographa californica multiple nucleopolyhedrovirus into Spodoptera frugiperda cells is dependent on dynamin, Rab5, and Rab11. Insect Biochem Mol Biol 123:103409. https://doi.org/10.1016/j.ibmb.2020.103409

    Article  CAS  PubMed  Google Scholar 

  60. Feng M, Zhang J, Xu W, Wang H, Kong X, Wu X (2018) Bombyx mori nucleopolyhedrovirus utilizes a clathrin and dynamin dependent endocytosis entry pathway into BmN cells. Virus Res 253:12–19. https://doi.org/10.1016/j.virusres.2018.05.020

    Article  CAS  PubMed  Google Scholar 

  61. Xie E, Guo H, Jiang L, Xia Q (2020) Identification of the Vo domain of V-ATPase in Bombyx mori silkworm. Int J Biol Macromol 163:386–392. https://doi.org/10.1016/j.ijbiomac.2020.07.003

    Article  CAS  PubMed  Google Scholar 

  62. Pavelin J, McCormick D, Chiweshe S, Ramachandran S, Lin YT, Grey F (2017) Cellular v-ATPase is required for virion assembly compartment formation in human cytomegalovirus infection. Open Biol. https://doi.org/10.1098/rsob.160298

    Article  PubMed  PubMed Central  Google Scholar 

  63. Shaw ML, Stone KL, Colangelo CM, Gulcicek EE, Palese P (2008) Cellular proteins in influenza virus particles. PLoS Pathog 4:e1000085. https://doi.org/10.1371/journal.ppat.1000085

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  64. Lussignol M, Kopp M, Molloy K, Vizcay-Barrena G, Fleck RA, Dorner M, Bell KL, Chait BT, Rice CM, Catanese MT (2016) Proteomics of HCV virions reveals an essential role for the nucleoporin Nup98 in virus morphogenesis. Proc Natl Acad Sci USA 113:2484–2489. https://doi.org/10.1073/pnas.1518934113

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  65. Chertova E, Chertov O, Coren LV, Roser JD, Trubey CM, Bess JW Jr, Sowder RC 2nd, Barsov E, Hood BL, Fisher RJ, Nagashima K, Conrads TP, Veenstra TD, Lifson JD, Ott DE (2006) Proteomic and biochemical analysis of purified human immunodeficiency virus type 1 produced from infected monocyte-derived macrophages. J Virol 80:9039–9052. https://doi.org/10.1128/JVI.01013-06

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  66. Cheng S, Zhao F, Wen L, Yang B, Wang XZ, Huang SN, Jiang X, Zeng WB, Sun JY, Zhang FK, Shen HJ, Fortunato E, Luo MH, Cheng H (2022) iTRAQ-based proteomics analysis of human cytomegalovirus latency and reactivation in T98G cells. J Virol 96:e0147621. https://doi.org/10.1128/JVI.01476-21

    Article  PubMed  Google Scholar 

  67. Treguier Y, Bull-Maurer A, Roingeard P (2022) Apolipoprotein E, a crucial cellular protein in the lifecycle of hepatitis viruses. Int J Mol Sci. https://doi.org/10.3390/ijms23073676

    Article  PubMed  PubMed Central  Google Scholar 

  68. Qiao L, Luo GG (1911) Functional characterization of apolipoproteins in the HCV life cycle. Methods Mol Biol 235–246:2019. https://doi.org/10.1007/978-1-4939-8976-8_16

    Article  CAS  Google Scholar 

  69. Mancone C, Steindler C, Santangelo L, Simonte G, Vlassi C, Longo MA, D’Offizi G, Di Giacomo C, Pucillo LP, Amicone L, Tripodi M, Alonzi T (2011) Hepatitis C virus production requires apolipoprotein A-I and affects its association with nascent low-density lipoproteins. Gut 60:378–386. https://doi.org/10.1136/gut.2010.211292

    Article  CAS  PubMed  Google Scholar 

  70. Cai H, Yao W, Huang J, Xiao J, Chen W, Hu L, Mai R, Liang M, Chen D, Jiang N, Zhou L, Peng T (2020) Apolipoprotein M, identified as a novel hepatitis C virus (HCV) particle associated protein, contributes to HCV assembly and interacts with E2 protein. Antiviral Res 177:104756. https://doi.org/10.1016/j.antiviral.2020.104756

    Article  CAS  PubMed  Google Scholar 

  71. Syed GH, Amako Y, Siddiqui A (2010) Hepatitis C virus hijacks host lipid metabolism. Trends Endocrinol Metab 21:33–40. https://doi.org/10.1016/j.tem.2009.07.005

    Article  CAS  PubMed  Google Scholar 

  72. Sawada H, Yamahama Y, Mase K, Hirakawa H, Iino T (2007) Molecular properties and tissue distribution of 30K proteins as ommin-binding proteins from diapause eggs of the silkworm, Bombyx mori. Compar Biochem Physiol B 146:172–179. https://doi.org/10.1016/j.cbpb.2006.10.101

    Article  CAS  Google Scholar 

  73. Pietrzyk AJ, Bujacz A, Lochynska M, Jaskolski M, Bujacz G (2014) Crystal structure of Bombyx mori lipoprotein 6: comparative structural analysis of the 30-kDa lipoprotein family. PLoS ONE 9:e108761. https://doi.org/10.1371/journal.pone.0108761

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  74. Zhou Y, Wang L, Li R, Liu M, Li X, Su H, Xu Y, Wang H (2018) Secreted glycoprotein BmApoD1 plays a critical role in anti-oxidation and anti-apoptosis in Bombyx mori. Biochem Biophys Res Commun 495:839–845. https://doi.org/10.1016/j.bbrc.2017.11.044

    Article  CAS  PubMed  Google Scholar 

  75. Wu W, Lin S, Zhao Z, Su Y, Li R, Zhang Z, Guo X (2021) Bombyx mori Apolipophorin-III inhibits Beauveria bassiana directly and through regulating expression of genes relevant to immune signaling pathways. J Invertebr Pathol 184:107647. https://doi.org/10.1016/j.jip.2021.107647

    Article  CAS  PubMed  Google Scholar 

  76. Xiao Y, Li LL, Bibi A, Zhang N, Chen T, Mo Y, Yue W, Miao Y (2020) Role of Bm30kc6 gene in cell apoptosis and the silk gland degradation signaling pathway in Bombyx mori L. Arch Insect Biochem Physiol 105:e21741. https://doi.org/10.1002/arch.21741

    Article  CAS  PubMed  Google Scholar 

  77. Dhawan R, Gupta K, Kajla M, Kakani P, Choudhury TP, Kumar S, Kumar V, Gupta L (2017) Apolipophorin-III acts as a positive regulator of plasmodium development in Anopheles stephensi. Front Physiol 8:185. https://doi.org/10.3389/fphys.2017.00185

    Article  PubMed  PubMed Central  Google Scholar 

  78. Carrique L, Fan H, Walker AP, Keown JR, Sharps J, Staller E, Barclay WS, Fodor E, Grimes JM (2020) Host ANP32A mediates the assembly of the influenza virus replicase. Nature 587:638–643. https://doi.org/10.1038/s41586-020-2927-z

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  79. Eberle CA, Zayas M, Stukalov A, Pichlmair A, Alvisi G, Muller AC, Bennett KL, Bartenschlager R, Superti-Furga G (2014) The lysine methyltransferase SMYD3 interacts with hepatitis C virus NS5A and is a negative regulator of viral particle production. Virology 462–463:34–41. https://doi.org/10.1016/j.virol.2014.05.016

    Article  CAS  PubMed  Google Scholar 

  80. Ye L, Zhang Y, Dong Z, Guo P, Zhao D, Li H, Hu H, Zhou X, Chen H, Zhao P (2021) Five silkworm 30K proteins are involved in the cellular immunity against fungi. Insects. https://doi.org/10.3390/insects12020107

    Article  PubMed  PubMed Central  Google Scholar 

  81. Blissard GW, Theilmann DA (2018) Baculovirus entry and egress from insect cells. Annu Rev Virol 5:113–139. https://doi.org/10.1146/annurev-virology-092917-043356

    Article  CAS  PubMed  Google Scholar 

  82. Arii J, Watanabe M, Maeda F, Tokai-Nishizumi N, Chihara T, Miura M, Maruzuru Y, Koyanagi N, Kato A, Kawaguchi Y (2018) ESCRT-III mediates budding across the inner nuclear membrane and regulates its integrity. Nat Commun 9:3379. https://doi.org/10.1038/s41467-018-05889-9

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  83. Willan J, Cleasby AJ, Flores-Rodriguez N, Stefani F, Rinaldo C, Pisciottani A, Grant E, Woodman P, Bryant HE, Ciani B (2019) ESCRT-III is necessary for the integrity of the nuclear envelope in micronuclei but is aberrant at ruptured micronuclear envelopes generating damage. Oncogenesis 8:29. https://doi.org/10.1038/s41389-019-0136-0

    Article  PubMed  PubMed Central  Google Scholar 

  84. Johnson DS, Bleck M, Simon SM (2018) Timing of ESCRT-III protein recruitment and membrane scission during HIV-1 assembly. Elife. https://doi.org/10.7554/eLife.36221

    Article  PubMed  PubMed Central  Google Scholar 

  85. Guo ZJ, Zhu YM, Li GH, Chen KP, Zhang CX (2011) Ubiquitins of Bombyx mori nucleopolyhedrovirus and Helicoverpa armigera nucleopolyhedrovirus show distinct subcellular localization in infected cells. Acta Virol 55:101–106. https://doi.org/10.4149/av_2011_02_101

    Article  CAS  PubMed  Google Scholar 

  86. Gomi S, Zhou CE, Yih W, Majima K, Maeda S (1997) Deletion analysis of four of eighteen late gene expression factor gene homologues of the baculovirus. BmNPV Virol 230:35–47. https://doi.org/10.1006/viro.1997.8457

    Article  CAS  Google Scholar 

  87. Hou Y, Xia Q, Yuan YA (2012) Crystal structure of Bombyx mori nucleopolyhedrovirus ORF75 reveals a pseudo-dimer of thiol oxidase domains with a putative substrate-binding pocket. J Gen Virol 93:2142–2151. https://doi.org/10.1099/vir.0.042747-0

    Article  CAS  PubMed  Google Scholar 

  88. Daimon T, Katsuma S, Kang W, Shimada T (2006) Comparative studies of Bombyx mori nucleopolyhedrovirus chitinase and its host ortholog. BmChi-h Biochem Biophys Res Commun 345:825–833. https://doi.org/10.1016/j.bbrc.2006.04.112

    Article  CAS  PubMed  Google Scholar 

  89. Xiang X, Chen L, Guo A, Yu S, Yang R, Wu X (2011) The Bombyx mori nucleopolyhedrovirus (BmNPV) ODV-E56 envelope protein is also a per os infectivity factor. Virus Res 155:69–75. https://doi.org/10.1016/j.virusres.2010.08.024

    Article  CAS  PubMed  Google Scholar 

  90. Kamita SG, Nagasaka K, Chua JW, Shimada T, Mita K, Kobayashi M, Maeda S, Hammock BD (2005) A baculovirus-encoded protein tyrosine phosphatase gene induces enhanced locomotory activity in a lepidopteran host. Proc Natl Acad Sci USA 102:2584–2589. https://doi.org/10.1073/pnas.0409457102

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  91. Dry I, Haig D, Inglis N, Imrie L, Stewart J, Russell GJJ (2008) Proteomic analysis of pathogenic and attenuated alcelaphine herpesvirus 1. J Virol 82:5390–5397. https://doi.org/10.1128/jvi.00094-08

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  92. Johannsen E, Luftig M, Chase M, Weicksel S, Cahir-McFarland E, Illanes D, Sarracino D et al (2004) Proteins of purified Epstein-Barr virus. Proc Natl Acad Sci 101:16286–16291. https://doi.org/10.1073/pnas.0407320101

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  93. Saphire A, Gallay P, Bark SJJOPR (2006) Proteomic analysis of human immunodeficiency virus using liquid chromatography/tandem mass spectrometry effectively distinguishes specific incorporated host proteins. J Proteome Res 5:530–538. https://doi.org/10.1021/pr050276b

    Article  CAS  PubMed  Google Scholar 

  94. Varnum S, Streblow D, Monroe M, Smith P, Auberry K, Pasa-Tolic L, Wang D, Camp D, Rodland K, Wiley S, Britt W, Shenk T, Smith R, Nelson JJJOV (2004) Identification of proteins in human cytomegalovirus (HCMV) particles: the HCMV proteome. J Virol 78:10960–10966. https://doi.org/10.1128/jvi.78.20.10960-10966.2004

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  95. Zhu F, Chong J, Wu L, Yuan YJJOV (2005) Virion proteins of Kaposi’s sarcoma-associated herpesvirus. J Virol 79:800–811. https://doi.org/10.1128/jvi.79.2.800-811.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  96. Bechtel J, Winant R, Ganem DJJOV (2005) Host and viral proteins in the virion of Kaposi’s sarcoma-associated herpesvirus. J Virol 79:4952–4964. https://doi.org/10.1128/jvi.79.8.4952-4964.2005

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  97. Segura M, Garnier A, Di Falco M, Whissell G, Meneses-Acosta A, Arcand N, Kamen AJJ (2008) Identification of host proteins associated with retroviral vector particles by proteomic analysis of highly purified vector preparations. J Virol 82:1107–1117. https://doi.org/10.1128/jvi.01909-07

    Article  CAS  PubMed  Google Scholar 

  98. Manes N, Estep R, Mottaz H, Moore R, Clauss T, Monroe M, Du X, Adkins J, Wong S, Smith RJ (2008) Comparative proteomics of human monkeypox and vaccinia intracellular mature and extracellular enveloped virions. J Proteome Res 7:960–968

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  99. Radhakrishnan A, Yeo D, Brown G, Myaing M, Iyer L, Fleck R, Tan B, Aitken J, Sanmun D, Tang K, Yarwood A, Brink J, Sugrue RJM et al (2010) Protein analysis of purified respiratory syncytial virus particles reveals an important role for heat shock protein 90 in virus particle assembly. Mol Cell Protomics 9:1829–1848. https://doi.org/10.1074/mcp.M110.001651

    Article  CAS  Google Scholar 

  100. Resch W, Hixson K, Moore R, Lipton M, Moss BJV (2007) Protein composition of the vaccinia virus mature virion. Virology 358:233–247. https://doi.org/10.1016/j.virol.2006.08.025

    Article  CAS  PubMed  Google Scholar 

  101. McKnight K, Xie L, González-López O, Rivera-Serrano E, Chen X et al (2017) Protein composition of the hepatitis A virus quasi-envelope. Proc Natl Acad Sci 114:6587–6592. https://doi.org/10.1073/pnas.1619519114

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  102. Zhang Y, Wang Y, Feng Y, Tu Z, Lou Z, Tu C (2020) Proteomic profiling of purified rabies virus particles. Virol Sin 35:143–155. https://doi.org/10.1007/s12250-019-00157-6

    Article  CAS  PubMed  Google Scholar 

  103. Kramer T, Greco T, Enquist L, Cristea IJJOV (2011) Proteomic characterization of pseudorabies virus extracellular virions. J Virol 85:6427–6441

    Article  CAS  PubMed  PubMed Central  Google Scholar 

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Acknowledgements

This work was supported by the National Natural Science Foundation of China (32172796 and 31670152) and the National Science Foundation of the Jiangsu Higher Education Institute of China (2020210558). We thank Prof. Manli Wang of Wuhan Institute of Virology, CAS for providing the polyclonal antibodies. We also thank Katherine Huang for the manuscript revising.

Funding

Funding was provided by National Social Science Fund of China (Grant Numbers 32172796 and 31670152), National Science Foundation of the Jiangsu Higher Education Institute of China (Grant Number 2020210558).

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BH, JH: Conceptualization, JH: Methodology, JL, CS, JH: Formal analysis and investigation, BH, JH: Writing—original draft preparation, BH, JH: Writing—reviewing and editing, BH, JH: Funding acquisition, JH: Supervision.

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Correspondence to Jinshan Huang.

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Hao, B., Li, J., Sun, C. et al. Label-free proteomics analysis on the envelope of budded viruses of Bombyx mori nucleopolyhedrovirus harboring differential localized GP64. Virus Genes 59, 260–275 (2023). https://doi.org/10.1007/s11262-022-01961-1

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