1887

Abstract

Human astrovirus non-structural protein nsP1a/4, located at the C-terminal end of nsP1a, is thought to be involved in regulating RNA replication. Here, we show that host protein CD63 interacts with the nsP1a protein. Further research showed that the large loop (LEL) domain of CD63 also interacts with nsP1a/4. Confocal microscopy showed that nsP1a/4 protein and CD63 co-localized in the cytoplasm of co-transfected cells. Co-localization of nsP1a/4 and CD63 was also observed in HAstV-1-infected cells. Overexpression of CD63 promoted replication of HAstV-1, whereas knockdown of CD63 reduced production of HAstV-1 viral progeny. These results suggest that CD63 plays a critical role in HAstV-1 replication, and provide an avenue to further understanding the interactions between host and virus proteins during replication and pathogenesis of HAstV.

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2019-02-06
2019-10-21
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References

  1. Méndez EA, Arias CF, In Knipe DM, Howley PM, Cohen JI et al. Fields virology, 6th ed.vol. 1 Philadelphia, PA, Astroviruses: Lippincott Williams &Wilkins; 2013; pp.609–628
    [Google Scholar]
  2. Kjeldsberg E. Serotyping of human astrovirus strains by immunogold staining electron microscopy. J Virol Methods 1994;50:137–144 [CrossRef][PubMed]
    [Google Scholar]
  3. Finkbeiner SR, Le BM, Holtz LR, Storch GA, Wang D. Detection of newly described astrovirus MLB1 in stool samples from children. Emerg Infect Dis 2009;15:441–444 [CrossRef][PubMed]
    [Google Scholar]
  4. Finkbeiner SR, Holtz LR, Jiang Y, Rajendran P, Franz CJ et al. Human stool contains a previously unrecognized diversity of novel astroviruses. Virol J 2009;6:161 [CrossRef][PubMed]
    [Google Scholar]
  5. Finkbeiner SR, Li Y, Ruone S, Conrardy C, Gregoricus N et al. Identification of a novel astrovirus (astrovirus VA1) associated with an outbreak of acute gastroenteritis. J Virol 2009;83:10836–10839 [CrossRef][PubMed]
    [Google Scholar]
  6. Kapoor A, Li L, Victoria J, Oderinde B, Mason C et al. Multiple novel astrovirus species in human stool. J Gen Virol 2009;90:2965–2972 [CrossRef][PubMed]
    [Google Scholar]
  7. Jiang H, Holtz LR, Bauer I, Franz CJ, Zhao G et al. Comparison of novel MLB-clade, VA-clade and classic human astroviruses highlights constrained evolution of the classic human astrovirus nonstructural genes. Virology 2013;436:8–14 [CrossRef][PubMed]
    [Google Scholar]
  8. Meyer CT, Bauer IK, Antonio M, Adeyemi M, Saha D et al. Prevalence of classic, MLB-clade and VA-clade Astroviruses in Kenya and The Gambia. Virol J 2015;12:78 [CrossRef][PubMed]
    [Google Scholar]
  9. Finkbeiner SR, Allred AF, Tarr PI, Klein EJ, Kirkwood CD et al. Metagenomic analysis of human diarrhea: viral detection and discovery. PLoS Pathog 2008;4:e1000011 [CrossRef][PubMed]
    [Google Scholar]
  10. Gallimore CI, Taylor C, Gennery AR, Cant AJ, Galloway A et al. Use of a heminested reverse transcriptase PCR assay for detection of astrovirus in environmental swabs from an outbreak of gastroenteritis in a pediatric primary immunodeficiency unit. J Clin Microbiol 2005;43:3890–3894 [CrossRef][PubMed]
    [Google Scholar]
  11. Wunderli W, Meerbach A, Güngör T, Guengoer T, Berger C et al. Astrovirus infection in hospitalized infants with severe combined immunodeficiency after allogeneic hematopoietic stem cell transplantation. PLoS One 2011;6:e27483 [CrossRef][PubMed]
    [Google Scholar]
  12. Silva RC, Benati FJ, Pena GP, Santos N. Molecular characterization of viruses associated with gastrointestinal infection in HIV-positive patients. Braz J Infect Dis 2010;14:549–552[PubMed]
    [Google Scholar]
  13. de Benedictis P, Schultz-Cherry S, Burnham A, Cattoli G. Astrovirus infections in humans and animals - molecular biology, genetic diversity, and interspecies transmissions. Infect Genet Evol 2011;11:1529–1544 [CrossRef][PubMed]
    [Google Scholar]
  14. Al-Mutairy B, Walter JE, Pothen A, Mitchell DK. Genome prediction of putative genome-linked viral protein (VPg) of astroviruses. Virus Genes 2005;31:21–30 [CrossRef][PubMed]
    [Google Scholar]
  15. Guix S, Bosch A, Ribes E, Dora Martínez L, Pintó RM. Apoptosis in astrovirus-infected CaCo-2 cells. Virology 2004;319:249–261 [CrossRef][PubMed]
    [Google Scholar]
  16. Jiang B, Monroe SS, Koonin EV, Stine SE, Glass RI. RNA sequence of astrovirus: distinctive genomic organization and a putative retrovirus-like ribosomal frameshifting signal that directs the viral replicase synthesis. Proc Natl Acad Sci USA 1993;90:10539–10543 [CrossRef][PubMed]
    [Google Scholar]
  17. Méndez-Toss M, Romero-Guido P, Munguía ME, Méndez E, Arias CF. Molecular analysis of a serotype 8 human astrovirus genome. J Gen Virol 2000;81:2891–2897 [CrossRef][PubMed]
    [Google Scholar]
  18. Willcocks MM, Boxall AS, Carter MJ. Processing and intracellular location of human astrovirus non-structural proteins. J Gen Virol 1999;80:2607–2611 [CrossRef][PubMed]
    [Google Scholar]
  19. Méndez E, Salas-Ocampo MP, Munguía ME, Arias CF. Protein products of the open reading frames encoding nonstructural proteins of human astrovirus serotype 8. J Virol 2003;77:11378–11384 [CrossRef][PubMed]
    [Google Scholar]
  20. Guix S, Caballero S, Bosch A, Pintó RM. Human astrovirus C-terminal nsP1a protein is involved in RNA replication. Virology 2005;333:124–131 [CrossRef][PubMed]
    [Google Scholar]
  21. Fuentes C, Guix S, Bosch A, Pintó RM. The C-terminal nsP1a protein of human astrovirus is a phosphoprotein that interacts with the viral polymerase. J Virol 2011;85:4470–4479 [CrossRef][PubMed]
    [Google Scholar]
  22. Pols MS, Klumperman J. Trafficking and function of the tetraspanin CD63. Exp Cell Res 2009;315:1584–1592 [CrossRef][PubMed]
    [Google Scholar]
  23. Hassuna N, Monk PN, Moseley GW, Partridge LJ. Strategies for targeting tetraspanin proteins: potential therapeutic applications in microbial infections. BioDrugs 2009;23:341–359 [CrossRef][PubMed]
    [Google Scholar]
  24. van Spriel AB, Figdor CG. The role of tetraspanins in the pathogenesis of infectious diseases. Microbes Infect 2010;12:106–112 [CrossRef][PubMed]
    [Google Scholar]
  25. Monk PN, Partridge LJ. Tetraspanins: gateways for infection. Infect Disord Drug Targets 2012;12:4–17 [CrossRef][PubMed]
    [Google Scholar]
  26. Florin L, Lang T. Tetraspanin assemblies in virus infection. Front Immunol 2018;9:1140 [CrossRef][PubMed]
    [Google Scholar]
  27. Hochdorfer D, Florin L, Sinzger C, Lieber D. Tetraspanin CD151 promotes initial events in human cytomegalovirus Infection. J Virol 2016;90:6430–6442 [CrossRef][PubMed]
    [Google Scholar]
  28. Pileri P, Uematsu Y, Campagnoli S, Galli G, Falugi F et al. Binding of hepatitis C virus to CD81. Science 1998;282:938–941 [CrossRef][PubMed]
    [Google Scholar]
  29. Fast LA, Lieber D, Lang T, Florin L. Tetraspanins in infections by human cytomegalo- and papillomaviruses. Biochem Soc Trans 2017;45:489–497 [CrossRef][PubMed]
    [Google Scholar]
  30. Rocha-Perugini V, Suárez H, Álvarez S, López-Martín S, Lenzi GM et al. CD81 association with SAMHD1 enhances HIV-1 reverse transcription by increasing dNTP levels. Nat Microbiol 2017;2:1513–1522 [CrossRef][PubMed]
    [Google Scholar]
  31. Yu G, Bing Y, Li W, Xia L, Liu Z. Hepatitis B virus inhibits the expression of CD82 through hypermethylation of its promoter in hepatoma cells. Mol Med Rep 2014;10:2580–2586 [CrossRef][PubMed]
    [Google Scholar]
  32. Earnest JT, Hantak MP, Li K, Mccray PB, Perlman S et al. The tetraspanin CD9 facilitates MERS-coronavirus entry by scaffolding host cell receptors and proteases. PLoS Pathog 2017;13:e1006546 [CrossRef][PubMed]
    [Google Scholar]
  33. Hurwitz SN, Nkosi D, Conlon MM, York SB, Liu X et al. CD63 regulates epstein-barr virus LMP1 exosomal packaging, enhancement of vesicle production, and noncanonical NF-κB signaling. J Virol 2017;91:e02251-16 [CrossRef][PubMed]
    [Google Scholar]
  34. Raaben M, Jae LT, Herbert AS, Kuehne AI, Stubbs SH et al. NRP2 and CD63 are host factors for Lujo virus cell entry. Cell Host Microbe 2017;22:688–696 [CrossRef][PubMed]
    [Google Scholar]
  35. Chapellier B, Tange S, Tasaki H, Yoshida K, Zhou Y et al. Examination of a plasmid-based reverse genetics system for human astrovirus. Microbiol Immunol 2015;59:586–596 [CrossRef][PubMed]
    [Google Scholar]
  36. Méndez E, Fernández-Luna T, López S, Méndez-Toss M, Arias CF. Proteolytic processing of a serotype 8 human astrovirus ORF2 polyprotein. J Virol 2002;76:7996–8002 [CrossRef][PubMed]
    [Google Scholar]
  37. Liu C, Liu WH, Kan LL, Li X, Li YG et al. Production of polyclonal antibody to a recombinant non-structural protein Nsp1a of human astrovirus. J Virol Methods 2014;209:82–85 [CrossRef][PubMed]
    [Google Scholar]
  38. Zhao W, Li X, Liu WH, Zhao J, Jin YM et al. Construction of high-quality Caco-2 three-frame cDNA library and its application to yeast two-hybrid for the human astrovirus protein-protein interaction. J Virol Methods 2014;205:104–109 [CrossRef][PubMed]
    [Google Scholar]
  39. Zinchuk V, Zinchuk O, Okada T. Quantitative colocalization analysis of multicolor confocal immunofluorescence microscopy images: pushing pixels to explore biological phenomena. Acta Histochem Cytochem 2007;40:101–111 [CrossRef][PubMed]
    [Google Scholar]
  40. Ahlquist P, Noueiry AO, Lee WM, Kushner DB, Dye BT. Host factors in positive-strand RNA virus genome replication. J Virol 2003;77:8181–8186 [CrossRef][PubMed]
    [Google Scholar]
  41. Murillo A, vera-Estrella R, Barkla BJ, Méndez E, Arias CF. Identification of host cell factors associated with astrovirus replication in caco-2 cells. J Virol 2015;89:10359–10370 [CrossRef][PubMed]
    [Google Scholar]
  42. Berditchevski F. Complexes of tetraspanins with integrins: more than meets the eye. J Cell Sci 2001;114:4143–4151[PubMed]
    [Google Scholar]
  43. Bassani S, Cingolani LA. Tetraspanins: Interactions and interplay with integrins. Int J Biochem Cell Biol 2012;44:703–708 [CrossRef][PubMed]
    [Google Scholar]
  44. Radford KJ, Thorne RF, Hersey P. CD63 associates with transmembrane 4 superfamily members, CD9 and CD81, and with beta 1 integrins in human melanoma. Biochem Biophys Res Commun 1996;222:13–18 [CrossRef][PubMed]
    [Google Scholar]
  45. Berditchevski F, Odintsova E. Tetraspanins as regulators of protein trafficking. Traffic 2007;8:89–96 [CrossRef][PubMed]
    [Google Scholar]
  46. Yoshida T, Kawano Y, Sato K, Ando Y, Aoki J et al. A CD63 mutant inhibits T-cell tropic human immunodeficiency virus type 1 entry by disrupting CXCR4 trafficking to the plasma membrane. Traffic 2008;9:540–558 [CrossRef][PubMed]
    [Google Scholar]
  47. Latysheva N, Muratov G, Rajesh S, Padgett M, Hotchin NA et al. Syntenin-1 is a new component of tetraspanin-enriched microdomains: mechanisms and consequences of the interaction of syntenin-1 with CD63. Mol Cell Biol 2006;26:7707–7718 [CrossRef][PubMed]
    [Google Scholar]
  48. von Lindern JJ, Rojo D, Grovit-Ferbas K, Yeramian C, Deng C et al. Potential role for CD63 in CCR5-mediated human immunodeficiency virus type 1 infection of macrophages. J Virol 2003;77:3624–3633 [CrossRef][PubMed]
    [Google Scholar]
  49. Li G, Dziuba N, Friedrich B, Murray JL, Ferguson MR. A post-entry role for CD63 in early HIV-1 replication. Virology 2011;412:315–324 [CrossRef][PubMed]
    [Google Scholar]
  50. Chen H, Dziuba N, Friedrich B, von Lindern J, Murray JL et al. A critical role for CD63 in HIV replication and infection of macrophages and cell lines. Virology 2008;379:191–196 [CrossRef][PubMed]
    [Google Scholar]
  51. Grigorov B, Molle J, Rubinstein E, Zoulim F, Bartosch B. CD81 large extracellular loop-containing fusion proteins with a dominant negative effect on HCV cell spread and replication. J Gen Virol 2017;98:1646–1657 [CrossRef][PubMed]
    [Google Scholar]
  52. Ramanathan A, Gusarova V, Stahl N, Gurnett-Bander A, Kyratsous CA. Alirocumab, a therapeutic human antibody to PCSK9, does not affect CD81 levels or hepatitis C virus entry and replication into hepatocytes. PLoS One 2016;11:e0154498 [CrossRef][PubMed]
    [Google Scholar]
  53. Gräßel L, Fast LA, Scheffer KD, Boukhallouk F, Spoden GA et al. The CD63-Syntenin-1 complex controls post-endocytic trafficking of oncogenic human papilloma viruses. Sci Rep 2016;6:32337 [CrossRef][PubMed]
    [Google Scholar]
  54. Scheffer KD, Gawlitza A, Spoden GA, Zhang XA, Lambert C et al. Tetraspanin CD151 mediates papillomavirus type 16 endocytosis. J Virol 2013;87:3435–3446 [CrossRef][PubMed]
    [Google Scholar]
  55. Mazurov D, Heidecker G, Derse D. HTLV-1 Gag protein associates with CD82 tetraspanin microdomains at the plasma membrane. Virology 2006;346:194–204 [CrossRef][PubMed]
    [Google Scholar]
  56. Shanmukhappa K, Kim JK, Kapil S. Role of CD151, A tetraspanin, in porcine reproductive and respiratory syndrome virus infection. Virol J 2007;4:62 [CrossRef][PubMed]
    [Google Scholar]
  57. Stipp CS, Kolesnikova TV, Hemler ME. Functional domains in tetraspanin proteins. Trends Biochem Sci 2003;28:106–112 [CrossRef][PubMed]
    [Google Scholar]
  58. Kitadokoro K, Bordo D, Galli G, Petracca R, Falugi F et al. CD81 extracellular domain 3D structure: insight into the tetraspanin superfamily structural motifs. Embo J 2001;20:12–18 [CrossRef][PubMed]
    [Google Scholar]
  59. Barreto A, Rodríguez LS, Rojas OL, Wolf M, Greenberg HB et al. Membrane vesicles released by intestinal epithelial cells infected with rotavirus inhibit T-cell function. Viral Immunol 2010;23:595–608 [CrossRef][PubMed]
    [Google Scholar]
  60. Halasz P, Fleming FE, Coulson BS. Evaluation of specificity and effects of monoclonal antibodies submitted to the Eighth Human Leucocyte Differentiation Antigen Workshop on rotavirus-cell attachment and entry. Cell Immunol 2005;236:179–187 [CrossRef][PubMed]
    [Google Scholar]
  61. Ivanusic D. HIV-1 cell-to-cell spread: CD63-gp41 interaction at the virological synapse. AIDS Res Hum Retroviruses 2014;30:844–845 [CrossRef][PubMed]
    [Google Scholar]
  62. Toricelli M, Melo FH, Peres GB, Silva DC, Jasiulionis MG. Timp1 interacts with beta-1 integrin and CD63 along melanoma genesis and confers anoikis resistance by activating PI3-K signaling pathway independently of Akt phosphorylation. Mol Cancer 2013;12:22 [CrossRef][PubMed]
    [Google Scholar]
  63. Moser LA, Schultz-Cherry S. Suppression of astrovirus replication by an ERK1/2 inhibitor. J Virol 2008;82:7475–7482 [CrossRef][PubMed]
    [Google Scholar]
  64. Tange S, Zhou Y, Nagakui-Noguchi Y, Imai T, Nakanishi A. Initiation of human astrovirus type 1 infection was blocked by inhibitors of phosphoinositide 3-kinase. Virol J 2013;10:153 [CrossRef][PubMed]
    [Google Scholar]
  65. Yauch RL, Hemler ME. Specific interactions among transmembrane 4 superfamily (TM4SF) proteins and phosphoinositide 4-kinase. Biochem J 2000;351 Pt 3:629–637[PubMed]
    [Google Scholar]
  66. Jang HI, Lee H. A decrease in the expression of CD63 tetraspanin protein elevates invasive potential of human melanoma cells. Exp Mol Med 2003;35:317–323 [CrossRef][PubMed]
    [Google Scholar]
  67. Humphries MJ. Integrin structure. Biochem Soc Trans 2000;28:311–340 [CrossRef][PubMed]
    [Google Scholar]
  68. Méndez E, Muñoz-Yañez C, Sánchez-San Martín C, Aguirre-Crespo G, Baños-Lara MR et al. Characterization of human astrovirus cell entry. J Virol 2014;88:2452–2460 [CrossRef][PubMed]
    [Google Scholar]
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