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Integrin beta and receptor for activated protein kinase C are involved in the cell entry of Bombyx mori cypovirus

  • Applied genetics and molecular biotechnology
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Abstract

Receptor-mediated endocytosis using a β1 integrin-dependent internalization was considered as the primary mechanism for the initiation of mammalian reovirus infection. Bombyx mori cypovirus (BmCPV) is a member of Reoviridae family which mainly infects the midgut epithelium of silkworm; the cell entry of BmCPV is poorly explored. In this study, co-immunoprecipitation (Co-IP), virus overlay protein binding assay (VOPBA), and BmCPV-protein interaction on the polyvinylidene difluoride membrane (BmCPV-PI-PVDF) methods were employed to screen the interacting proteins of BmCPV, and several proteins including integrin beta and receptor for activated protein kinase C (RACK1) were identified as the candidate interacting proteins for establishing the infection of BmCPV. The infectivity of BmCPV was investigated in vivo and in vitro by RNA interference (RNAi) and antibody blocking methods, and the results showed that the infectivity of BmCPV was significantly reduced by either small interfering RNA-mediated silencing of integrin beta and RACK1 or antibody blocking of integrin beta and RACK1. The expression level of integrin beta or RACK1 is not the highest in the silkworm midgut which is a principal target tissue of BmCPV, suggesting that the molecules other than integrin beta or RACK1 might play a key role in determining the tissue tropism of BmCPV infection. The establishment of BmCPV infection depends on other factors, and these factors interacted with integrin beta and RACK1 to form receptor complex for the cell entry of BmCPV.

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References

  • Arias CF, Silva-Ayala D, López S (2015) Rotavirus entry: a deep journey into the cell with several exits. J Virol 89:890–893

    Article  PubMed  Google Scholar 

  • Barton ES, Forrest JC, Connolly JL, Chappell JD, Liu Y, Schnell FJ, Nusrat A, Parkos CA, Dermody TS (2001) Junction adhesion molecule is a receptor for reovirus. Cell 104:441–451

    Article  CAS  PubMed  Google Scholar 

  • Belozerov VE, Ratkovic S, McNeill H, Hilliker AJ, McDermott JC (2014) In vivo interaction proteomics reveal a novel p38 mitogen-activated protein kinase/RACK1 pathway regulating proteostasis in Drosophila muscle. Mol Cell Biol 34:474–484

    Article  PubMed  PubMed Central  Google Scholar 

  • Besson A, Wilson TL, Yong VW (2002) The anchoring protein RACK1 links protein kinase C epsilon to integrin β chains. Requirements for adhesion and motility J Biol Chem 277:22073–22084

    CAS  PubMed  Google Scholar 

  • Boll W, Rapoport I, Brunner C, Modis Y, Prehn S, Kirchhausen T (2002) The mu2 subunit of the clathrin adaptor AP-2 binds to FDNPVY and YppØ sorting signals at distinct sites. Traffic 3:590–600

    Article  CAS  PubMed  Google Scholar 

  • Borsa J, Morash BD, Sargent MD, Copps TP, Lievaart PA, Szekely JG (1979) Two modes of entry of reovirus particles into L cells. J Gen Virol 45:161–170

    Article  CAS  PubMed  Google Scholar 

  • Buensuceso CS, Woodside D, Huff JL, Plopper GE, O’Toole TE (2001) The WD protein RACK1 mediates protein kinase C and integrin-dependent cell migration. J Cell Sci 114:1691–1698

    CAS  PubMed  Google Scholar 

  • Calderwood DA, Zent R, Grant R, Rees DJ, Hynes RO, Ginsberg MH (1999) The Talin head domain binds to integrin beta subunit cytoplasmic tails and regulates integrin activation. J Biol Chem 274:28071–28074

    Article  CAS  PubMed  Google Scholar 

  • Calderwood DA (2004) Talin controls integrin activation. Biochem Soc Trans 32:434–437

    Article  CAS  PubMed  Google Scholar 

  • Campbell JA, Schelling P, Wetzel JD, Johnson EM, Forrest JC, Wilson GAR, Aurrand-Lions M, Imhof BA, Stehle T, Dermody TS (2005) Junctional adhesion molecule-A serves as a receptor for prototype and field-isolate strains of mammalian reovirus. J Virol 79:7967–7978

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Cao GL, Meng XK, Xue RY, Zhu YX, Zhang X, Pan ZH, Zheng XJ, Gong CL (2012) Characterization of the complete genome segments from BmCPV-SZ, a novel Bombyx mori cypovirus 1 isolate. Can J Microbiol 58:872–883

    Article  CAS  PubMed  Google Scholar 

  • Cayrol C, Bertrand C, Kowalski-Chauvel A, Daulhac L, Cohen-Jonathan-Moyal E, Ferrand A, Seva C (2011) Alphav integrin: a new gastrin target in human pancreatic cancer cells. World J Gastroenterol 17:4488–4495

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chang BY, Chiang M, Cartwright CA (2001) The interaction of Src and RACK1 is enhanced by activation of protein kinase C and tyrosine phosphorylation of RACK1. J Biol Chem 276:20346–20356

    Article  CAS  PubMed  Google Scholar 

  • Chen WJ, Goldstein JL, Brown MS (1990) NPXY, a sequence often found in cytoplasmic tails, is required for coated pit-mediated internalization of the low density lipoprotein receptor. J Biol Chem 265:3116–3123

    CAS  PubMed  Google Scholar 

  • Cheng Y, Wang XY, Hu H, Killiny N, Xu JP (2014) A hypothetical model of crossing Bombyx mori nucleopolyhedrovirus through its host midgut physical barrier. PLoS One 9:e115032–e115032

    Article  PubMed  PubMed Central  Google Scholar 

  • Chiu CY, Mathias P, Nemerow GR, Stewart PL (1999) Structure of adenovirus complexed with its internalization receptor, alphavbeta5 integrin. J Virol 73:6759–6768

    CAS  PubMed  PubMed Central  Google Scholar 

  • Cox EA, Bennin D, Doan AT, O’Toole T, Huttenlocher A (2003) RACK1 regulates integrin-mediated adhesion, protrusion, and chemotactic cell migration via its Src-binding site. Mol Biol Cell 14:658–669

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Coyle SM, Gilbert WV, Doudna JA (2009) Direct link between RACK1 function and localization at the ribosome in vivo. Mol Cell Biol 29:1626–1634

    Article  CAS  PubMed  Google Scholar 

  • Davis CG, Lehrman MA, Russell DW, Anderson RG, Brown MS, Goldstein JL (1986) The J. D. mutation in familial hypercholesterolemia: amino acid substitution in cytoplasmic domain impedes internalization of LDL receptors. Cell 45:15–24

    Article  CAS  PubMed  Google Scholar 

  • Dedhar S, Hannigan GE (1996) Integrin cytoplasmic interactions and bidirectional transmembrane signalling. Curr Opin Cell Biol Curr Opin Cell Biol 8:657–669

    Article  CAS  PubMed  Google Scholar 

  • Ehrlich M, Boll W, Van Oijen A, Hariharan R, Chandran K, Nibert ML, Kirchhausen T (2004) Endocytosis by random initiation and stabilization of clathrin-coated pits. Cell 118:591–605

    Article  CAS  PubMed  Google Scholar 

  • Forrest JC, Campbell JA, Schelling P, Stehle T, Dermody TS (2003) Structure-function analysis of reovirus binding to junctional adhesion molecule 1. Implications for the mechanism of reovirus attachment J Biol Chem 278:48434–48444

    CAS  PubMed  Google Scholar 

  • Gallina A, Rossi F, Milanesi G (2001) RACK1 binds HIV-1 Nef and can act as a Nef–protein kinase C adaptor. Virology 283:7–18

    Article  CAS  PubMed  Google Scholar 

  • Gavrilovskaya IN, Shepley M, Shaw R, Ginsberg MH, Mackow ER (1998) β 3 integrins mediate the cellular entry of hantaviruses that cause respiratory failure. Proc Natl Acad Sci U S A 95:7074–7079

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gibson TJ (2012) RACK1 research-ships passing in the night? FEBS Lett 586:2787–2789

    Article  CAS  PubMed  Google Scholar 

  • Grace TD (1967) Establishment of a line of cells from the silkworm Bombyx mori. Nature 216:613

    Article  CAS  PubMed  Google Scholar 

  • Guo R, Wang SM, Xue RY, Cao GL, Hu XL, Huang ML, Zhang YQ, Lu YH, Zhu LY, Chen F, Liang Z, Kuang SL, Gong CL (2015) The gene expression profile of resistant and susceptible Bombyx mori, strains reveals cypovirus-associated variations in host gene transcript levels. Appl Microbiol Biot 99:5175–5187

    Article  CAS  Google Scholar 

  • Hannigan GE, Leung-Hagesteijn C, Fitz-Gibbon L, Coppolino MG, Radeva G, Filmus J, Bell JC, Dedhar S (1996) Regulation of cell adhesion and anchorage-dependent growth by a new β1-integrin-linked protein kinase. Nature 379:91–96

    Article  CAS  PubMed  Google Scholar 

  • Hill CL, Booth TF, Stuart DI, Mertens PP (1999) Lipofectin increases the specific activity of cypovirus particles for cultured insect cells. J Virol Methods 78:177–189

    Article  CAS  PubMed  Google Scholar 

  • Horwitz A, Duggan K, Buck C (1986) Interaction of plasma membrane fibronectin receptor with talin-a transmembrane linkage. Nature 320:531–533

    Article  CAS  PubMed  Google Scholar 

  • Huang DH, Qin F, Shi L, Tong XQ, Chen ZQ, Wang ZH, Yao WQ (2012) Causes and countermeasures of control of silkworm virus disease in summer and autumn. China Sericulture 33:63–66

    Google Scholar 

  • Hynes RO (1992) Integrins: versatility, modulation, and signaling in cell adhesion. Cell 69:11–25

    Article  CAS  PubMed  Google Scholar 

  • Hynes RO (2002) Integrins: bidirectional, allosteric signaling machines. Cell 110:673–687

    Article  CAS  PubMed  Google Scholar 

  • Inoue H, Taniai k, Kobayashi J (1990) Establishment and characterization of substrate-depending cell lines of Bombyx mori. Bull Natl Inst Seric Entomol Sci 1:13–25

    Google Scholar 

  • Jannot G, Bajan S, Giguère NJ, Bouasker S, Banville IH, Piquet S, Hutvagner G, Simard MJ (2011) The ribosomal protein RACK1 is required for microRNA function in both C. elegans and humans. EMBO Rep 12:581–586

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Kirchhausen T, Bonifacino JS, Riezman H (1997) Linking cargo to vesicle formation: receptor tail interactions with coat proteins. Curr Opin Cell Biol 9:488–495

    Article  CAS  PubMed  Google Scholar 

  • Laflamme SE, Thomas LA, Yamada SS, Yamada KM (1994) Single subunit chimeric integrins as mimics and inhibitors of endogenous integrin functions in receptor localization, cell spreading and migration, and matrix assembly. J Cell Biol 126:1287–1298

    Article  CAS  PubMed  Google Scholar 

  • Li E, Brown SL, Stupack DG, Puente XS, Cheresh DA, Nemerow GR (2001) Integrin alpha (v) beta1 is an adenovirus coreceptor. J Virol 75:5405–5409

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Liliental J, Chang DD (1998) RACK1, a receptor for activated protein kinase C, interacts with integrin β subunit. J Biol Chem 273:2379–2383

    Article  CAS  PubMed  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2-ΔΔCT method. Methods 25:402–408

    Article  CAS  PubMed  Google Scholar 

  • Long LY, Deng YZ, Yao F, Guan DX, Feng YY, Jiang H, Li XB, Hu PT, Lu XC, Wang H, Li JJ, Gao X, Xie D (2014) Recruitment of phosphatase PP2A by RACK1 adaptor protein deactivates transcription factor IRF3 and limits type I interferon signaling. Immunity 40:515–529

    Article  CAS  PubMed  Google Scholar 

  • Maginnis MS, Forrest JC, Kopecky-Bromberg SA, Dickeson SK, Santoro SA, Zutter MM, Nemerow GR, Bergelson JM, Dermody TS (2006) Beta1 integrin mediates internalization of mammalian reovirus. J Virol 80:2760–2770

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Maginnis MS, Mainou BA, Derdowski A, Johnson EM, Zent R, Dermody TS (2008) NPXY motifs in the beta1 integrin cytoplasmic tail are required for functional reovirus entry. J Virol 82:3181–3191

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Magnoler A (1974) Effects of a cytoplasmic polyhedrosis on larval and postlarval stages of the gypsy moth, Porthetria dispar. J Invertebr Pathol 23:263–274

    Article  CAS  PubMed  Google Scholar 

  • Mainou BA, Dermody TS (2011) Src kinase mediates productive endocytic sorting of reovirus during cell entry. J Virol 85:3203–3213

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Majzoub K, Hafirassou ML, Meignin C, Goto A, Marzi S, Fedorova A, Verdier Y, Vinh J, Hoffmann JA, Martin F, Baumert FT, Catherine S, Imler J-L (2014) RACK1 controls IRES-mediated translation of viruses. Cell 159:1086–1095

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Monazahian M, Böhme I, Bonk S, Koch A, Scholz C, Grethe S (1999) Thomssen R. Low density lipoprotein receptor as a candidate receptor for hepatitis C virus J Med Virol 57:223–229

    CAS  PubMed  Google Scholar 

  • Nermut MV, Green NM, Eason P, Yamada SS, Yamada KM (1989) Electron microscopy and structural model of human fibronectin receptor. EMBO J 7:4093–4099

    Google Scholar 

  • Nilsson J, Sengupta J, Frank J, Nissen P (2004) Regulation of eukaryotic translation by the RACK1 protein: a platform for signalling molecules on the ribosome. EMBO Rep 5:1137–1141

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Oleinikov AV, Zhao J, Makker SP (2000) Cytosolic adaptor protein Dab2 is an intracellular ligand of endocytic receptor gp600/megalin. Biochem J 347:613–621

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Omura T, Mertens PPC (2005) Phytoreovirus. In: Fauquet CM, Mayo MA, Maniloff J, Desselberger U, Ball AL (eds) Virus taxonomy: 8th report of the International Committee on Taxonomy of Viruses. Academic Press, London, pp 543–549

    Google Scholar 

  • Otey CA, Pavalko FM, Burridge K (1990) An interaction between α-actinin and the beta 1 integrin subunit in vitro. J Cell Biol 111:721–729

    Article  CAS  PubMed  Google Scholar 

  • Otey CA, Vasquez GB, Burridge K, Erickson BW (1993) Mapping of the alpha-actinin binding site within the beta 1 integrin cytoplasmic domain. J Cell Biol 268:21193–21197

    CAS  Google Scholar 

  • Parry C, Bell S, Minson T, Browne H (2005) Herpes simplex virus type 1 glycoprotein H binds to alphavbeta3 integrins. J Gen Virol 86:7–10

    Article  CAS  PubMed  Google Scholar 

  • Pearse BM (1988) Receptors compete for adaptors found in plasma membrane coated pits. EMBO J 7:3331–3336

    CAS  PubMed  PubMed Central  Google Scholar 

  • Pfaff M, Liu S, Erle DJ, Ginsberg MH (1998) Integrin β cytoplasmic domains differentially bind to cytoskeletal proteins. J Biol Chem 273:6104–6109

    Article  CAS  PubMed  Google Scholar 

  • Ron D, Chen CH, Caldwell J, Jamieson L, Orr E, Mochly-Rosen D (1994) Cloning of an intracellular receptor for protein kinase C: a homolog of the β-subunit of G proteins. Proc Natl Acad Sci U S A 91:839–843

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ron D, Jiang Z, Yao L, Vagts A, Diamond I, Gordon A (1999) Coordinated movement of RACK1 with activated βIIPKC. J Biol Chem 274:27039–27046

    Article  CAS  PubMed  Google Scholar 

  • Rubin DH, Weiner DB, Dworkin C, Greene MI, Maul GG, Williams WV (1992) Receptor utilization by reovirus type 3: distinct binding sites on thymoma and fibroblast cell lines result in differential compartmentalization of virions. Microb Pathog 12:351–365

    Article  CAS  PubMed  Google Scholar 

  • Rubinstein R, Harley EH, Losman M, Lutton D (1976) The nucleic acids of viruses infecting Heliothis armigera. Virology 69:323–326

    Article  CAS  PubMed  Google Scholar 

  • Scarselli E, Ansuini H, Cerino R, Roccasecca RM, Acali S, Filocamo G, Traboni C, Nicosia A, Cortese R, Vitelli A (2002) The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J 21:5017–5025

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Schaller MD, Otey CA, Hildebrand JD, Parsons JT (1995) Focal adhesion kinase and paxillin bind to peptides mimicking beta integrin cytoplasmic domains. J Biol Chem 130:1181–1187

    CAS  Google Scholar 

  • Schols D (2006) HIV co-receptor inhibitors as novel class of anti-HIV drugs. Antivir Res 71:216–226

    Article  CAS  PubMed  Google Scholar 

  • Schweneker M, Bachmann AS, Moelling K (2004) The HIV-1 co-receptor CCR5 binds to α-catenin, a component of the cellular cytoskeleton. Biochem Biophys Res Commun 325:751–757

    Article  CAS  PubMed  Google Scholar 

  • Sengupta J, Nilsson J, Gursky R, Spahn CM, Nissen P, Frank J (2004) Identification of the versatile scaffold protein RACK1 on the eukaryotic ribosome by cryo-EM. Nat Struct Mol Biol 11:957–962

    Article  CAS  PubMed  Google Scholar 

  • Sharma CP, Ezzell RM, Arnaout MA (1995) Direct interaction of filamin (ABP-280) with the beta 2-integrin subunit CD18. J Immunol 154:3461–3470

    CAS  PubMed  Google Scholar 

  • Shevchenko A, Tomas H, Havlis J, Olsen JV, Mann M (2006) In-gel digestion for mass spectrometric characterization of proteins and proteomes. Nat Protoc 1:2856–2860

    Article  CAS  PubMed  Google Scholar 

  • Siljamäki E, Rintanen N, Kirsi M, Upla P, Wang W, Karjalainen M, Ikonen E, Marjomäki V (2013) Cholesterol dependence of collagen and echovirus 1 trafficking along the novel α2β1 integrin internalization pathway. PLoS One 8:e55465

    Article  PubMed  PubMed Central  Google Scholar 

  • Song JW, Song KJ, Baek LJ, Frost B, Poncz M, Park K (2005) In vivo characterization of the integrin beta3 as a receptor for Hantaan virus cellular entry. Exp MolL Med 37:121–127

    Article  CAS  Google Scholar 

  • Spear PG, Longnecker R (2003) Herpesvirus entry: an update. J Virol 77:10179–10185

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Stergiou L, Bauer M, Mair W, Bausch-Fluck D, Drayman N, Wollscheid B, Oppenheim A, Pelkmans L (2013) Integrin-mediated signaling induced by simian virus 40 leads to transient uncoupling of cortical actin and the plasma membrane. PLoS One 8:e55799

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sturzenbecker LJ, Nibert M, Furlong D, Fields BN (1987) Intracellular digestion of reovirus particles requires a low pH and is an essential step in the viral infectious cycle. J Virol 61:2351–2361

    CAS  PubMed  PubMed Central  Google Scholar 

  • Tan YR, Sun JC, Lu XY, Su DM, Zhang JQ (2003) Entry of Bombyx mori cypovirus 1 into midgut cells in vivo. J Electron Microsc 52:485

    Article  Google Scholar 

  • Taylor SL, Frias-Staheli N, García-Sastre A, Schmaljohn CS (2009) Hantaan virus nucleocapsid protein binds to importin α proteins and inhibits tumor necrosis factor alpha-induced activation of nuclear factor kappa B. J Virol 83:1271–1279

    Article  CAS  PubMed  Google Scholar 

  • Trerotola M, Li J, Alberti S, Languino LR (2012) Trop-2 inhibits prostate cancer cell adhesion to fibronectin through the β1 integrin-RACK1 axis. J Cell Physiol 227:3670–3677

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Triantafilou K, Triantafilou M (2003) Lipid raft microdomains: key sites for Coxsackievirus A9 infectious cycle. Virology 317:128–135

    Article  CAS  PubMed  Google Scholar 

  • Wang GX, Wang YH, Shang YJ, Zhang ZD, Liu XT (2015) How foot-and-mouth disease virus receptor mediates foot-and-mouth disease virus infection. Virol J 12:1–7

    Article  Google Scholar 

  • Wei T, Chen H, Ichiki-Uehara T, Hibino H, Omura T (2007) Entry of rice dwarf virus into cultured cells of its insect vector involves clathrin-mediated endocytosis. J Virol 81:7811–7815

  • Whitton JL, Cornell CT, Feuer R (2005) Host and virus determinants of picornavirus pathogenesis and tropism. Nat Rev Microbiol 3:765–776

    Article  CAS  PubMed  Google Scholar 

  • Zhang XL, Guo R, Kumar D, Ma HY, Liu JB, Hu XL, Cao GL, Xue RY, Gong CL (2016) Identification, gene expression and immune function of the novel Bm-STAT gene in virus-infected Bombyx mori. Gene 577:82–88

    Article  CAS  PubMed  Google Scholar 

  • Zhang YL, Xue RY, Cao GL, Meng XK, Zhu YX, Pan ZH, Gong CL (2014) Nonvirus encoded proteins could be embedded into Bombyx mori cypovirus polyhedra. Mol Biol Rep 41:2657–2666

    Article  CAS  PubMed  Google Scholar 

  • Zhou TX (2008) Prevention measures for the happening and prevalence of Bombyx mori cypovirus. Yunnan Nongye Keji S2:66–68

    Google Scholar 

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Acknowledgments

The authors are very grateful to the National Natural Science Foundation of China (31272500), National Basic Research Program of China (973 Program, 2012CB114600), and Priority Academic Program of Development of Jiangsu Higher Education Institutions for their financial and moral support.

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Author notes

  1. Yiling Zhang

    Present address: Suzhou Municipal Key Laboratory of Molecular Diagnostics and Therapeutics, Suzhou Institute of Biomedical Engineering and Technology, Chinese Academy of Sciences, Suzhou, 215163, People’s Republic of China

  2. Simei Wang

    Present address: Department of Hematology, The First Affiliated Hospital of Gannan Medical College, Ganzhou, 341000, Jiangxi, People’s Republic of China

Authors and Affiliations

  1. School of Biology and Basic Medical Sciences, Soochow University, Suzhou, 215123, Jiangsu, People’s Republic of China

    Yiling Zhang, Guangli Cao, Liyuan Zhu, Fei Chen, Mian Sahib Zar, Simei Wang, Xiaolong Hu, Yuhong Wei, Renyu Xue & Chengliang Gong

  2. National Engineering Laboratory for Modern Silk, Soochow University, Postal address: No. 199 Ren’ai Road, Suzhou Industrial Park, Suzhou, 215123, Jiangsu, People’s Republic of China

    Guangli Cao, Xiaolong Hu, Renyu Xue & Chengliang Gong

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All procedures on the animals, including mice and silkworms, were approved by the Ethic Committee of Experimental Animals of Soochow University and were carried out in accordance with the Guide of the Care and Use of Laboratory Animals.

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Yiling Zhang and Guangli Cao contributed equally to this work.

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Zhang, Y., Cao, G., Zhu, L. et al. Integrin beta and receptor for activated protein kinase C are involved in the cell entry of Bombyx mori cypovirus. Appl Microbiol Biotechnol 101, 3703–3716 (2017). https://doi.org/10.1007/s00253-017-8158-z

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