1887

Abstract

Orthotospoviruses are acquired by thrips during feeding on infected tissue. Virions travel through the foregut and enter midgut epithelial cells through the interaction between the viral glycoproteins and cellular receptors. Glycoprotein RGD motifs and N-linked glycosylation sites have been predicted to mediate receptor binding or play important roles in virus entry into host cells, yet their function needs to be validated. In this study, peptides derived from the soybean vein necrosis virus N glycoprotein were utilized to identify critical regions in virus–vector interactions. Transmission mediated by single dropped by more than 2/3 when thrips were fed on peptide NASIAAAHEVSQE or the combination of NASIRGDHEVSQE and RLTGECNITKVSLTN when compared to the controls; indicating that this strategy could significantly reduce transmission efficiency, opening new avenues in the control of diseases caused by orthotospoviruses.

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2019-11-14
2019-12-11
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References

  1. Pappu HR, Jones RAC, Jain RK. Global status of tospovirus epidemics in diverse cropping systems: successes achieved and challenges ahead. Virus Res 2009;141:219–236 [CrossRef]
    [Google Scholar]
  2. Oliver JE, Whitfield AE. The genus Tospovirus: emerging Bunyaviruses that threaten food security. Annu Rev Virol 2016;3:101–124 [CrossRef]
    [Google Scholar]
  3. Riley DG, Joseph SV, Srinivasan R, Diffie S, Stanley D. Thrips vectors of Tospoviruses. J Integr Pest Manag 2011;2:I1–I10 [CrossRef]
    [Google Scholar]
  4. Montero-Astúa M. Unveiling and blocking the interaction between Tomato spotted wilt virus and its insect vector, Frankliniella occidentalis. Kansas State University; Manhattan, U. S. Ph.D dissertation: 2012
  5. Xu Y, Gao X, Jia Z, Li W, Hu J et al. Identification of Taeniothrips eucharii (Thysanoptera: Thripidae) as a vector of hippeastrum chlorotic ringspot virus in Southern China. Plant Dis 2017;101:1597–1600 [CrossRef]
    [Google Scholar]
  6. Zhou J, Tzanetakis IE. Soybean vein necrosis virus: an emerging virus in North America. Virus Genes 2019;55:12–21 [CrossRef]
    [Google Scholar]
  7. Rotenberg D, Jacobson AL, Schneweis DJ, Whitfield AE. Thrips transmission of tospoviruses. Curr Opin Virol 2015;15:80–89 [CrossRef]
    [Google Scholar]
  8. Whitfield AE, Falk BW, Rotenberg D. Insect vector-mediated transmission of plant viruses. Virology 2015;479-480:278–289 [CrossRef]
    [Google Scholar]
  9. Ullman DE, Whitfield AE, German TL. Thrips and tospoviruses come of age: mapping determinants of insect transmission. Proc Natl Acad Sci U S A 2005;102:4931–4932 [CrossRef]
    [Google Scholar]
  10. Whitfield AE, Ullman DE, German TL. Tospovirus-Thrips interactions. Annu Rev Phytopathol 2005;43:459–489 [CrossRef]
    [Google Scholar]
  11. Montero-Astúa M, Ullman DE, Whitfield AE. Salivary gland morphology, tissue tropism and the progression of tospovirus infection in Frankliniella occidentalis. Virology 2016;493:39–51 [CrossRef]
    [Google Scholar]
  12. Widana Gamage SMK, Rotenberg D, Schneweis DJ, Tsai C-W, Dietzgen RG. Transcriptome-Wide responses of adult melon thrips (thrips palmi) associated with Capsicum chlorosis virus infection. PLoS One 2018;13:e0208538 [CrossRef]
    [Google Scholar]
  13. Marsh M, Helenius A. Virus entry: open sesame. Cell 2006;124:729–740 [CrossRef]
    [Google Scholar]
  14. Badillo-Vargas IE, Chen Y, Martin KM, Rotenberg D, Whitfield AE. Discovery of novel thrips vector proteins that bind to the plant bunyavirus, tomato spotted wilt virus. BioRxiv 2018;1–54
    [Google Scholar]
  15. Whitfield AE, Ullman DE, German TL. Expression and characterization of a soluble form of Tomato spotted wilt virus glycoprotein GN. J Virol 2004;78:13197–13206 [CrossRef]
    [Google Scholar]
  16. Schwab EH, Halbig M, Glenske K, Wagner A-S, Wenisch S et al. Distinct effects of RGD-glycoproteins on integrin-mediated adhesion and osteogenic differentiation of human mesenchymal stem cells. Int J Med Sci 2013;10:1846–1859 [CrossRef]
    [Google Scholar]
  17. Badillo-Vargas IE. Dissecting the molecular interplay between Tomato spotted wilt virus and the insect vector, Frankliniella occidentalis. Manhattan, U. S. Ph.D dissertation; Kansas State University: 2014
  18. Yu Y-P, Wang Q, Liu Y-C, Xie Y. Molecular basis for the targeted binding of RGD-containing peptide to integrin αvβ3. Biomaterials 2014;35:1667–1675 [CrossRef]
    [Google Scholar]
  19. Whitfield AE. Tomato spotted wilt virus acquisition by thrips: the role of the viral glycoproteins. Madison, U. S. Ph.D dissertation; Univerisity of Wisconsin-Madison: 2004
  20. Whitfield AE, Kumar NKK, Rotenberg D, Ullman DE, Wyman EA et al. A soluble form of the Tomato spotted wilt virus (TSWV) glycoprotein G(N) (G(N)-S) inhibits transmission of TSWV by Frankliniella occidentalis. Phytopathology 2008;98:45–50 [CrossRef]
    [Google Scholar]
  21. Wild C, Oas T, McDanal C, Bolognesi D, Matthews T. A synthetic peptide inhibitor of human immunodeficiency virus replication: correlation between solution structure and viral inhibition. Proc Natl Acad Sci U S A 1992;89:10537–10541 [CrossRef]
    [Google Scholar]
  22. Dus Santos Marı́a J, Wigdorovitz A, Trono K, Rı́os RD, Franzone PM et al. A novel methodology to develop a foot and mouth disease virus (FMDV) peptide-based vaccine in transgenic plants. Vaccine 2002;20:1141–1147 [CrossRef]
    [Google Scholar]
  23. Firbas C, Jilma B, Tauber E, Buerger V, Jelovcan S et al. Immunogenicity and safety of a novel therapeutic hepatitis C virus (HCV) peptide vaccine: a randomized, placebo controlled trial for dose optimization in 128 healthy subjects. Vaccine 2006;24:4343–4353 [CrossRef]
    [Google Scholar]
  24. Borrego P, Calado R, Marcelino JM, Pereira P, Quintas A et al. An ancestral HIV-2/simian immunodeficiency virus peptide with potent HIV-1 and HIV-2 fusion inhibitor activity. AIDS 2013;27:1081–1090 [CrossRef]
    [Google Scholar]
  25. Muhamad A, KL H. Basyaruddin Abdul Rahman a, Tejo Ba, Uhrin D, Tan Ws. hepatitis B virus peptide inhibitors: solution structures and interactions with the viral capsid. Organic and Biomolecular Chemistry 2015;13:7780–7789
    [Google Scholar]
  26. Yang M, Sunderland K, Mao C. Virus-Derived peptides for clinical applications. Chem Rev 2017;117:10377–10402 [CrossRef]
    [Google Scholar]
  27. Liu S, Sivakumar S, Sparks WO, Miller WA, Bonning BC. A peptide that binds the pea aphid gut impedes entry of pea enation mosaic virus into the aphid hemocoel. Virology 2010;401:107–116 [CrossRef]
    [Google Scholar]
  28. Zhou J, Tzanetakis IE. Epidemiology of soybean vein necrosis-associated virus. Phytopathology 2013;103:966–971 [CrossRef]
    [Google Scholar]
  29. Keough S, Han J, Shuman T, Wise K, Nachappa P. Effects of soybean vein necrosis virus on life history and host preference of its vector, Neohydatothrips variabilis, and evaluation of vector status of Frankliniella tritici and Frankliniella fusca. J Econ Entomol 2016;109:1979–1987 [CrossRef]
    [Google Scholar]
  30. Han J, Nalam VJ, Yu I-C, Nachappa P. Vector competence of thrips species to transmit soybean vein necrosis virus. Front Microbiol 2019;10:431 [CrossRef]
    [Google Scholar]
  31. Chen T-C, Li J-T, Fan Y-S, Yeh Y-C, Yeh S-D et al. Molecular characterization of the full-length L and M RNAs of Tomato yellow ring virus, a member of the genus Tospovirus. Virus Genes 2013;46:487–495 [CrossRef]
    [Google Scholar]
  32. Zhou J, Aboughanem-Sabanadzovic N, Sabanadzovic S, Tzanetakis IE. First Report of Soybean Vein Necrosis Virus Infecting Kudzu (Pueraria montana) in the United States of America. Plant Dis 2018;102:1674 [CrossRef]
    [Google Scholar]
  33. Krogh A, Larsson B, von Heijne G, Sonnhammer EL. Predicting transmembrane protein topology with a hidden Markov model: application to complete genomes. J Mol Biol 2001;305:567–580 [CrossRef]
    [Google Scholar]
  34. Campanella JJ, Bitincka L, Smalley J. MatGAT: an application that generates similarity/identity matrices using protein or DNA sequences. BMC Bioinformatics 2003;4:29–4 [CrossRef]
    [Google Scholar]
  35. Julenius K, Mølgaard A, Gupta R, Brunak S, Prediction BS. Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 2005;15:153–164 [CrossRef]
    [Google Scholar]
  36. Zhou J, Kantartzi SK, Wen R-H, Newman M, Hajimorad MR et al. Molecular characterization of a new Tospovirus infecting soybean. Virus Genes 2011;43:289–295 [CrossRef]
    [Google Scholar]
  37. Dunnett CW. A multiple comparison procedure for comparing several treatments with a control. J Am Stat Assoc 1955;50:1096–1121 [CrossRef]
    [Google Scholar]
  38. Caprioli RM, Farmer TB, Gile J. Molecular imaging of biological samples: localization of peptides and proteins using MALDI-TOF MS. Anal Chem 1997;69:4751–4760 [CrossRef]
    [Google Scholar]
  39. Dams R, Huestis MA, Lambert WE, Murphy CM. Matrix effect in bio-analysis of illicit drugs with LC-MS/MS: influence of ionization type, sample preparation, and biofluid. J Am Soc Mass Spectrom 2003;14:1290–1294 [CrossRef]
    [Google Scholar]
  40. Houimel M, Dellagi K. Peptide mimotopes of rabies virus glycoprotein with immunogenic activity. Vaccine 2009;27:4648–4655 [CrossRef]
    [Google Scholar]
  41. Arosio D, Casagrande C, Manzoni L. Integrin-Mediated drug delivery in cancer and cardiovascular diseases with peptide-functionalized nanoparticles. Curr Med Chem 2012;19:3128–3151 [CrossRef]
    [Google Scholar]
  42. Gosselet F, Saint-Pol J, Candela P, Fenart L, peptides A-beta. Alzheimer’s disease and the bold-brain barrier. Current Alzheimer Research 2013;10:1015–1033 [CrossRef]
    [Google Scholar]
  43. Hipolito SG, Shitara A, Kondo H, Hirono I. Role of Marsupenaeus japonicus crustin-like peptide against Vibrio penaeicida and white spot syndrome virus infection. Dev Comp Immunol 2014;46:461–469 [CrossRef]
    [Google Scholar]
  44. Zhang Z, Pan L, Ding Y, Zhou P, Lv J et al. Efficacy of synthetic peptide candidate vaccines against serotype-A foot-and-mouth disease virus in cattle. Appl Microbiol Biotechnol 2015;99:1389–1398 [CrossRef]
    [Google Scholar]
  45. Rudolph C, Schreier PH, Uhrig JF. Peptide-Mediated broad-spectrum plant resistance to tospoviruses. Proc Natl Acad Sci U S A 2003;100:4429–4434 [CrossRef]
    [Google Scholar]
  46. Lopez-Ochoa L, Ramirez-Prado J, Hanley-Bowdoin L. Peptide aptamers that bind to a geminivirus replication protein interfere with viral replication in plant cells. J Virol 2006;80:5841–5853 [CrossRef]
    [Google Scholar]
  47. Bai M, Harfe B, Freimuth P. Mutations that alter an Arg-Gly-Asp (RGD) sequence in the adenovirus type 2 penton base protein abolish its cell-rounding activity and delay virus reproduction in flat cells. J Virol 1993;67:5198–5205
    [Google Scholar]
  48. Wei Y, Zhang Y, Cai H, Mirza AM, Iorio RM et al. Roles of the putative integrin-binding motif of the human metapneumovirus fusion (F) protein in cell-cell fusion, viral infectivity, and pathogenesis. J Virol 2014;88:4338–4352 [CrossRef]
    [Google Scholar]
  49. Gutiérrez-Rivas M, Pulido MR, Baranowski E, Sobrino F, Sáiz M. Tolerance to mutations in the foot-and-mouth disease virus integrin-binding RGD region is different in cultured cells and in vivo and depends on the capsid sequence context. J Gen Virol 2008;89:2531–2539 [CrossRef]
    [Google Scholar]
  50. Spizz G, Blackshear PJ. Overexpression of the myristoylated alanine-rich C-kinase substrate inhibits cell adhesion to extracellular matrix components. J Biol Chem 2001;276:32264–32273 [CrossRef]
    [Google Scholar]
  51. Pierschbacher MD, Ruoslahti E. Cell attachment activity of fibronectin can be duplicated by small synthetic fragments of the molecule. Nature 1984;309:30–33 [CrossRef]
    [Google Scholar]
  52. Bellis SL. Advantages of RGD peptides for directing cell association with biomaterials. Biomaterials 2011;32:4205–4210 [CrossRef]
    [Google Scholar]
  53. Schwab EH, Halbig M, Glenske K, Wagner A-S, Wenisch S et al. Distinct effects of RGD-glycoproteins on integrin-mediated adhesion and osteogenic differentiation of human mesenchymal stem cells. Int J Med Sci 2013;10:1846–1859 [CrossRef]
    [Google Scholar]
  54. Akiyama SK, Johnson MD. Fibronectin in evolution: presence in invertebrates and isolation from Microciona prolifera. Comparative Biochemistry and Physiology Part B: Comparative Biochemistry 1983;76:687–694 [CrossRef]
    [Google Scholar]
  55. Pradel G, Hayton K, Aravind L, Iyer LM, Abrahamsen MS et al. A multidomain adhesion protein family expressed in Plasmodium falciparum is essential for transmission to the mosquito. J Exp Med 2004;199:1533–1544 [CrossRef]
    [Google Scholar]
  56. Hanington PC, Zhang S-M. The primary role of fibrinogen-related proteins in invertebrates is defense, not coagulation. J Innate Immun 2011;3:17–27 [CrossRef]
    [Google Scholar]
  57. Woods A, Couchman JR, Johansson S, Höök M. Adhesion and cytoskeletal organisation of fibroblasts in response to fibronectin fragments. Embo J 1986;5:665–670 [CrossRef]
    [Google Scholar]
  58. Aota S, Nagai T, Yamada KM. Characterization of regions of fibronectin besides the arginine-glycine-aspartic acid sequence required for adhesive function of the cell-binding domain using site-directed mutagenesis. The Journal Biological Chemistry 1991;266:15938–15943
    [Google Scholar]
  59. Bisson MMA, Kessenbrock M, Müller L, Hofmann A, Schmitz F et al. Peptides interfering with protein-protein interactions in the ethylene signaling pathway delay tomato fruit ripening. Sci Rep 2016;6:30634 [CrossRef]
    [Google Scholar]
  60. Pierschbacher MD, Ruoslahti E. Influence of stereochemistry of the sequence Arg-Gly-Asp-Xaa on binding specificity in cell adhesion. The Journal Biological Chemistry 1987;262:17294–17298
    [Google Scholar]
  61. Plow EF, Pierschbacher MD, Ruoslahti E, Marguerie G, Ginsberg MH. Arginyl-Glycyl-Aspartic acid sequences and fibrinogen binding to platelets. Blood 1987;70:110–115 [CrossRef]
    [Google Scholar]
  62. Lin HB, Sun W, Mosher DF, García-Echeverría C, Schaufelberger K et al. Synthesis, surface, and cell-adhesion properties of polyurethanes containing covalently grafted RGD-peptides. J Biomed Mater Res 1994;28:329–342 [CrossRef]
    [Google Scholar]
  63. Haubner R, Gratias R, Diefenbach B, Goodman SL, Jonczyk A et al. Structural and functional aspects of RGD-containing cyclic pentapeptides as highly potent and selective integrin alphavbeta3 Antagonists. J Am Chem Soc 1996;118:7461–7472 [CrossRef]
    [Google Scholar]
  64. Hersel U, Dahmen C, Kessler H. Rgd modified polymers: biomaterials for stimulated cell adhesion and beyond. Biomaterials 2003;24:4385–4415 [CrossRef]
    [Google Scholar]
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