1932

Abstract

“Rotaviruses represent the most important etiological agents of acute, severe gastroenteritis in the young of many animal species, including humans.” This statement, variations of which are a common beginning in articles about rotaviruses, reflects the fact that these viruses have evolved efficient strategies for evading the innate immune response of the host and for successfully replicating in the population. In this review, we summarize what is known about the defense mechanisms that host cells employ to prevent rotavirus invasion and the countermeasures that these viruses have successfully developed to surpass cellular defenses. Rotaviruses use at least two viral multifunctional proteins to directly interact with, and prevent the activation of, the interferon system, and they use at least one other protein to halt the protein synthesis machinery and prevent the expression of most of the transcriptional antiviral program of the cell. Characterization of the confrontation between rotaviruses and their host cells has allowed us to learn about the virus–host coevolution that prevents the damaging effects of the innate immune response.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-110615-042152
2016-09-29
2024-03-28
Loading full text...

Full text loading...

/deliver/fulltext/virology/3/1/annurev-virology-110615-042152.html?itemId=/content/journals/10.1146/annurev-virology-110615-042152&mimeType=html&fmt=ahah

Literature Cited

  1. Lee LA, Franzel L, Atwell J, Datta SD, Friberg IK. 1.  et al. 2013. The estimated mortality impact of vaccinations forecast to be administered during 2011–2020 in 73 countries supported by the GAVI alliance. Vaccine 31:Suppl. 2B61–72 [Google Scholar]
  2. Tate JE, Burton AH, Boschi-Pinto C, Steele AD, Duque J. 2.  et al. 2008. Estimate of worldwide rotavirus-associated mortality in children younger than 5 years before the introduction of universal rotavirus vaccination programmes: a systematic review and meta-analysis. Lancet Infect. Dis. 12:136–41 [Google Scholar]
  3. Walker CL, Rudan I, Liu L, Nair H, Theodoratou E. 3.  et al. 2013. Global burden of childhood pneumonia and diarrhoea. Lancet 381:1405–16 [Google Scholar]
  4. Babji S, Kang G. 4.  2012. Rotavirus vaccination in developing countries. Curr. Opin. Virol. 2:443–48 [Google Scholar]
  5. Estes MK, Greenberg HB. 5.  2013. Rotaviruses and their replication. Fields Virology DN Knipe, PM Howley 1347–401 Philadelphia: Wolters Kluwer [Google Scholar]
  6. Bridger JC, Dhaliwal W, Adamson MJ, Howard CR. 6.  1998. Determinants of rotavirus host range restriction—a heterologous bovine NSP1 gene does not affect replication kinetics in the pig. Virology 245:47–52 [Google Scholar]
  7. Bridger JC, Tauscher GI, Desselberger U. 7.  1998. Viral determinants of rotavirus pathogenicity in pigs: evidence that the fourth gene of a porcine rotavirus confers diarrhea in the homologous host. J. Virol. 72:6929–31 [Google Scholar]
  8. Broome RL, Vo PT, Ward RL, Clark HF, Greenberg HB. 8.  1993. Murine rotavirus genes encoding outer capsid proteins VP4 and VP7 are not major determinants of host range restriction and virulence. J. Virol. 67:2448–55 [Google Scholar]
  9. Ciarlet M, Estes MK, Barone C, Ramig RF, Conner ME. 9.  1998. Analysis of host range restriction determinants in the rabbit model: comparison of homologous and heterologous rotavirus infections. J. Virol. 72:2341–51 [Google Scholar]
  10. Feng N, Sen A, Wolf M, Vo P, Hoshino Y, Greenberg HB. 10.  2011. Roles of VP4 and NSP1 in determining the distinctive replication capacities of simian rotavirus RRV and bovine rotavirus UK in the mouse biliary tract. J. Virol. 85:2686–94 [Google Scholar]
  11. Feng N, Yasukawa LL, Sen A, Greenberg HB. 11.  2013. Permissive replication of homologous murine rotavirus in the mouse intestine is primarily regulated by VP4 and NSP1. J. Virol. 87:8307–16 [Google Scholar]
  12. Hoshino Y, Saif LJ, Kang SY, Sereno MM, Chen WK, Kapikian AZ. 12.  1995. Identification of group A rotavirus genes associated with virulence of a porcine rotavirus and host range restriction of a human rotavirus in the gnotobiotic piglet model. Virology 209:274–80 [Google Scholar]
  13. Offit PA, Blavat G, Greenberg HB, Clark HF. 13.  1986. Molecular basis of rotavirus virulence: role of gene segment 4. J. Virol. 57:46–49 [Google Scholar]
  14. Wang W, Donnelly B, Bondoc A, Mohanty SK, McNeal M. 14.  et al. 2011. The rhesus rotavirus gene encoding VP4 is a major determinant in the pathogenesis of biliary atresia in newborn mice. J. Virol. 85:9069–77 [Google Scholar]
  15. Arias CF, Silva-Ayala D, Lopez S. 15.  2015. Rotavirus entry: a deep journey into the cell with several exits. J. Virol. 89:890–93 [Google Scholar]
  16. Baker M, Prasad BV. 16.  2010. Rotavirus cell entry. Curr. Top. Microbiol. Immunol. 343:121–48 [Google Scholar]
  17. Lopez S, Arias CF. 17.  2004. Multistep entry of rotavirus into cells: a Versaillesque dance. Trends Microbiol 12:271–78 [Google Scholar]
  18. Lopez S, Arias CF. 18.  2006. Early steps in rotavirus cell entry. Curr. Top. Microbiol. Immunol. 309:39–66 [Google Scholar]
  19. Heaton PM, Goveia MG, Miller JM, Offit P, Clark HF. 19.  2005. Development of a pentavalent rotavirus vaccine against prevalent serotypes of rotavirus gastroenteritis. J. Infect. Dis. 192:Suppl. 1S17–21 [Google Scholar]
  20. Kato H, Takeuchi O, Sato S, Yoneyama M, Yamamoto M. 20.  et al. 2006. Differential roles of MDA5 and RIG-I helicases in the recognition of RNA viruses. Nature 441:101–5 [Google Scholar]
  21. Takeuchi O, Akira S. 21.  2009. Innate immunity to virus infection. Immunol. Rev. 227:75–86 [Google Scholar]
  22. Kawasaki T, Kawai T, Akira S. 22.  2011. Recognition of nucleic acids by pattern-recognition receptors and its relevance in autoimmunity. Immunol. Rev. 243:61–73 [Google Scholar]
  23. O'Neill LA, Bowie AG. 23.  2007. The family of five: TIR-domain-containing adaptors in Toll-like receptor signalling. Nat. Rev. Immunol. 7:353–64 [Google Scholar]
  24. Kawai T, Takahashi K, Sato S, Coban C, Kumar H. 24.  et al. 2005. IPS-1, an adaptor triggering RIG-I- and Mda5-mediated type I interferon induction. Nat. Immunol. 6:981–88 [Google Scholar]
  25. Seth RB, Sun L, Ea CK, Chen ZJ. 25.  2005. Identification and characterization of MAVS, a mitochondrial antiviral signaling protein that activates NF-κB and IRF 3. Cell 122:669–82 [Google Scholar]
  26. Xu LG, Wang YY, Han KJ, Li LY, Zhai Z, Shu HB. 26.  2005. VISA is an adapter protein required for virus-triggered IFN-β signaling. Mol. Cell 19:727–40 [Google Scholar]
  27. Ishikawa H, Ma Z, Barber GN. 27.  2009. STING regulates intracellular DNA-mediated, type I interferon-dependent innate immunity. Nature 461:788–92 [Google Scholar]
  28. Randall RE, Goodbourn S. 28.  2008. Interferons and viruses: an interplay between induction, signalling, antiviral responses and virus countermeasures. J. Gen. Virol. 89:1–47 [Google Scholar]
  29. O'Neill LA, Bowie AG. 29.  2010. Sensing and signaling in antiviral innate immunity. Curr. Biol. 20:R328–33 [Google Scholar]
  30. Takeuchi O, Akira S. 30.  2010. Pattern recognition receptors and inflammation. Cell 140:805–20 [Google Scholar]
  31. Donnelly RP, Kotenko SV. 31.  2010. Interferon-λ: a new addition to an old family. J. Interferon Cytokine Res. 30:555–64 [Google Scholar]
  32. Kotenko SV, Gallagher G, Baurin VV, Lewis-Antes A, Shen M. 32.  et al. 2003. IFN-λs mediate antiviral protection through a distinct class II cytokine receptor complex. Nat. Immunol. 4:69–77 [Google Scholar]
  33. Pestka S. 33.  2007. The interferons: 50 years after their discovery, there is much more to learn. J. Biol. Chem. 282:20047–51 [Google Scholar]
  34. Wack A, Terczynska-Dyla E, Hartmann R. 34.  2015. Guarding the frontiers: the biology of type III interferons. Nat. Immunol. 16:802–9 [Google Scholar]
  35. Uze G, Schreiber G, Piehler J, Pellegrini S. 35.  2007. The receptor of the type I interferon family. Curr. Top. Microbiol. Immunol. 316:71–95 [Google Scholar]
  36. Sheppard P, Kindsvogel W, Xu W, Henderson K, Schlutsmeyer S. 36.  et al. 2003. IL-28, IL-29 and their class II cytokine receptor IL-28R. Nat. Immunol. 4:63–68 [Google Scholar]
  37. Dumoutier L, Tounsi A, Michiels T, Sommereyns C, Kotenko SV, Renauld JC. 37.  2004. Role of the interleukin (IL)-28 receptor tyrosine residues for antiviral and antiproliferative activity of IL-29/interferon-λ1: similarities with type I interferon signaling. J. Biol. Chem. 279:32269–74 [Google Scholar]
  38. Kotenko SV. 38.  2011. IFN-λs. Curr. Opin. Immunol. 23:583–90 [Google Scholar]
  39. Schoggins JW. 39.  2014. Interferon-stimulated genes: roles in viral pathogenesis. Curr. Opin. Virol. 6:40–46 [Google Scholar]
  40. Durbin RK, Kotenko SV, Durbin JE. 40.  2013. Interferon induction and function at the mucosal surface. Immunol. Rev. 255:25–39 [Google Scholar]
  41. Hermant P, Michiels T. 41.  2014. Interferon-λ in the context of viral infections: production, response and therapeutic implications. J. Innate Immun. 6:563–74 [Google Scholar]
  42. Mahlakoiv T, Hernandez P, Gronke K, Diefenbach A, Staeheli P. 42.  2015. Leukocyte-derived IFN-α/β and epithelial IFN-λ constitute a compartmentalized mucosal defense system that restricts enteric virus infections. PLOS Pathog 11:e1004782 [Google Scholar]
  43. Broquet AH, Hirata Y, McAllister CS, Kagnoff MF. 43.  2011. RIG-I/MDA5/MAVS are required to signal a protective IFN response in rotavirus-infected intestinal epithelium. J. Immunol. 186:1618–26 [Google Scholar]
  44. Hirata Y, Broquet AH, Menchen L, Kagnoff MF. 44.  2007. Activation of innate immune defense mechanisms by signaling through RIG-I/IPS-1 in intestinal epithelial cells. J. Immunol. 179:5425–32 [Google Scholar]
  45. Sen A, Pruijssers AJ, Dermody TS, Garcia-Sastre A, Greenberg HB. 45.  2011. The early interferon response to rotavirus is regulated by PKR and depends on MAVS/IPS-1, RIG-I, MDA-5, and IRF3. J. Virol. 85:3717–32 [Google Scholar]
  46. Di Fiore IJ, Holloway G, Coulson BS. 46.  2015. Innate immune responses to rotavirus infection in macrophages depend on MAVS but involve neither the NLRP3 inflammasome nor JNK and p38 signaling pathways. Virus Res 208:89–97 [Google Scholar]
  47. Hornung V, Ellegast J, Kim S, Brzozka K, Jung A. 47.  et al. 2006. 5′-triphosphate RNA is the ligand for RIG-I. Science 314:994–97 [Google Scholar]
  48. Pichlmair A, Schulz O, Tan CP, Naslund TI, Liljestrom P. 48.  et al. 2006. RIG-I-mediated antiviral responses to single-stranded RNA bearing 5′-phosphates. Science 314:997–1001 [Google Scholar]
  49. Kato H, Takeuchi O, Mikamo-Satoh E, Hirai R, Kawai T. 49.  et al. 2008. Length-dependent recognition of double-stranded ribonucleic acids by retinoic acid-inducible gene-I and melanoma differentiation-associated gene 5. J. Exp. Med. 205:1601–10 [Google Scholar]
  50. Silvestri LS, Taraporewala ZF, Patton JT. 50.  2004. Rotavirus replication: plus-sense templates for double-stranded RNA synthesis are made in viroplasms. J. Virol. 78:7763–74 [Google Scholar]
  51. Sanchez-Tacuba L, Rojas M, Arias CF, Lopez S. 51.  2015. Rotavirus controls activation of the 2′-5′-oligoadenylate synthetase/RNase L pathway using at least two distinct mechanisms. J. Virol. 89:12145–53 [Google Scholar]
  52. Uzri D, Greenberg HB. 52.  2013. Characterization of rotavirus RNAs that activate innate immune signaling through the RIG-I-like receptors. PLOS ONE 8:e69825 [Google Scholar]
  53. Li W, Manktelow E, von Kirchbach JC, Gog JR, Desselberger U, Lever AM. 53.  2010. Genomic analysis of codon, sequence and structural conservation with selective biochemical-structure mapping reveals highly conserved and dynamic structures in rotavirus RNAs with potential cis-acting functions. Nucleic Acids Res 38:7718–35 [Google Scholar]
  54. Rojas M, Arias CF, Lopez S. 54.  2010. Protein kinase R is responsible for the phosphorylation of eIF2α in rotavirus infection. J. Virol. 84:10457–66 [Google Scholar]
  55. Kordasti S, Istrate C, Banasaz M, Rottenberg M, Sjovall H. 55.  et al. 2006. Rotavirus infection is not associated with small intestinal fluid secretion in the adult mouse. J. Virol. 80:11355–61 [Google Scholar]
  56. Vancott JL, McNeal MM, Choi AH, Ward RL. 56.  2003. The role of interferons in rotavirus infections and protection. J. Interferon Cytokine Res. 23:163–70 [Google Scholar]
  57. Pott J, Stockinger S, Torow N, Smoczek A, Lindner C. 57.  et al. 2012. Age-dependent TLR3 expression of the intestinal epithelium contributes to rotavirus susceptibility. PLOS Pathog 8:e1002670 [Google Scholar]
  58. Deal EM, Jaimes MC, Crawford SE, Estes MK, Greenberg HB. 58.  2010. Rotavirus structural proteins and dsRNA are required for the human primary plasmacytoid dendritic cell IFNα response. PLOS Pathog 6:e1000931 [Google Scholar]
  59. Uchiyama R, Chassaing B, Zhang B, Gewirtz AT. 59.  2015. MyD88-mediated TLR signaling protects against acute rotavirus infection while inflammasome cytokines direct Ab response. Innate Immun 21:416–28 [Google Scholar]
  60. Arnold MM, Sen A, Greenberg HB, Patton JT. 60.  2013. The battle between rotavirus and its host for control of the interferon signaling pathway. PLOS Pathog 9:e1003064 [Google Scholar]
  61. Holloway G, Coulson BS. 61.  2013. Innate cellular responses to rotavirus infection. J. Gen. Virol. 94:1151–60 [Google Scholar]
  62. Sen A, Rothenberg ME, Mukherjee G, Feng N, Kalisky T. 62.  et al. 2012. Innate immune response to homologous rotavirus infection in the small intestinal villous epithelium at single-cell resolution. PNAS 109:20667–72 [Google Scholar]
  63. De Boissieu D, Lebon P, Badoual J, Bompard Y, Dupont C. 63.  1993. Rotavirus induces α-interferon release in children with gastroenteritis. J. Pediatr. Gastroenterol. Nutr. 16:29–32 [Google Scholar]
  64. La Bonnardiere C, Cohen J, Contrepois M. 64.  1981. Interferon activity in rotavirus infected newborn calves. Ann. Rech. Vétérinaires 12:85–91 [Google Scholar]
  65. Frias AH, Vijay-Kumar M, Gentsch JR, Crawford SE, Carvalho FA. 65.  et al. 2010. Intestinal epithelia activate anti-viral signaling via intracellular sensing of rotavirus structural components. Mucosal Immunol 3:622–32 [Google Scholar]
  66. Feng N, Kim B, Fenaux M, Nguyen H, Vo P. 66.  et al. 2008. Role of interferon in homologous and heterologous rotavirus infection in the intestines and extraintestinal organs of suckling mice. J. Virol. 82:7578–90 [Google Scholar]
  67. Angel J, Franco MA, Greenberg HB, Bass D. 67.  1999. Lack of a role for type I and type II interferons in the resolution of rotavirus-induced diarrhea and infection in mice. J. Interferon Cytokine Res. 19:655–59 [Google Scholar]
  68. Pott J, Mahlakoiv T, Mordstein M, Duerr CU, Michiels T. 68.  et al. 2011. IFN-λ determines the intestinal epithelial antiviral host defense. PNAS 108:7944–49 [Google Scholar]
  69. Feng N, Sen A, Nguyen H, Vo P, Hoshino Y. 69.  et al. 2009. Variation in antagonism of the interferon response to rotavirus NSP1 results in differential infectivity in mouse embryonic fibroblasts. J. Virol. 83:6987–94 [Google Scholar]
  70. Bass DM. 70.  1997. Interferon γ and interleukin 1, but not interferon α, inhibit rotavirus entry into human intestinal cell lines. Gastroenterology 113:81–89 [Google Scholar]
  71. Egli A, Santer DM, O'Shea D, Tyrrell DL, Houghton M. 71.  2014. The impact of the interferon-λ family on the innate and adaptive immune response to viral infections. Emerg. Microbes Infect. 3:e51 [Google Scholar]
  72. Lasfar A, Zloza A, Cohen-Solal KA. 72.  2016. IFN-λ therapy: current status and future perspectives. Drug Discov. Today 21:167–71 [Google Scholar]
  73. Sommereyns C, Paul S, Staeheli P, Michiels T. 73.  2008. IFN-lambda (IFN-λ) is expressed in a tissue-dependent fashion and primarily acts on epithelial cells in vivo. PLOS Pathog 4:e1000017 [Google Scholar]
  74. Hernandez PP, Mahlakoiv T, Yang I, Schwierzeck V, Nguyen N. 74.  et al. 2015. Interferon-λ and interleukin 22 act synergistically for the induction of interferon-stimulated genes and control of rotavirus infection. Nat. Immunol. 16:698–707 [Google Scholar]
  75. Zhang B, Chassaing B, Shi Z, Uchiyama R, Zhang Z. 75.  et al. 2014. Prevention and cure of rotavirus infection via TLR5/NLRC4-mediated production of IL-22 and IL-18. Science 346:861–65 [Google Scholar]
  76. Lopez S, Arias CF. 76.  2012. Rotavirus–host cell interactions: an arms race. Curr. Opin. Virol. 2:389–98 [Google Scholar]
  77. Morelli M, Ogden KM, Patton JT. 77.  2015. Silencing the alarms: innate immune antagonism by rotavirus NSP1 and VP3. Virology 479:75–84 [Google Scholar]
  78. Dunn SJ, Cross TL, Greenberg HB. 78.  1994. Comparison of the rotavirus nonstructural protein NSP1 (NS53) from different species by sequence analysis and northern blot hybridization. Virology 203:178–83 [Google Scholar]
  79. Graff JW, Ewen J, Ettayebi K, Hardy ME. 79.  2007. Zinc-binding domain of rotavirus NSP1 is required for proteasome-dependent degradation of IRF3 and autoregulatory NSP1 stability. J. Gen. Virol. 88:613–20 [Google Scholar]
  80. Morelli M, Dennis AF, Patton JT. 80.  2015. Putative E3 ubiquitin ligase of human rotavirus inhibits NF-κB activation by using molecular mimicry to target β-TrCP. mBio 6:e02490 [Google Scholar]
  81. Graff JW, Mitzel DN, Weisend CM, Flenniken ML, Hardy ME. 81.  2002. Interferon regulatory factor 3 is a cellular partner of rotavirus NSP1. J. Virol. 76:9545–50 [Google Scholar]
  82. Arnold MM, Barro M, Patton JT. 82.  2013. Rotavirus NSP1 mediates degradation of interferon regulatory factors through targeting of the dimerization domain. J. Virol. 87:9813–21 [Google Scholar]
  83. Barro M, Patton JT. 83.  2005. Rotavirus nonstructural protein 1 subverts innate immune response by inducing degradation of IFN regulatory factor 3. PNAS 102:4114–19 [Google Scholar]
  84. Barro M, Patton JT. 84.  2007. Rotavirus NSP1 inhibits expression of type I interferon by antagonizing the function of interferon regulatory factors IRF3, IRF5, and IRF7. J. Virol. 81:4473–81 [Google Scholar]
  85. Yanai H, Negishi H, Taniguchi T. 85.  2012. The IRF family of transcription factors: inception, impact and implications in oncogenesis. Oncoimmunology 1:1376–86 [Google Scholar]
  86. Graff JW, Ettayebi K, Hardy ME. 86.  2009. Rotavirus NSP1 inhibits NFκB activation by inducing proteasome-dependent degradation of β-TrCP: a novel mechanism of IFN antagonism. PLOS Pathog 5:e1000280 [Google Scholar]
  87. Hinz M, Arslan SC, Scheidereit C. 87.  2012. It takes two to tango: IκBs, the multifunctional partners of NF-κB. Immunol. Rev. 246:59–76 [Google Scholar]
  88. Kanarek N, Ben-Neriah Y. 88.  2012. Regulation of NF-κB by ubiquitination and degradation of the IκBs. Immunol. Rev. 246:77–94 [Google Scholar]
  89. Hayden MS, Ghosh S. 89.  2012. NF-κB, the first quarter-century: remarkable progress and outstanding questions. Genes Dev 26:203–34 [Google Scholar]
  90. Bour S, Perrin C, Akari H, Strebel K. 90.  2001. The human immunodeficiency virus type 1 Vpu protein inhibits NF-κB activation by interfering with βTrCP-mediated degradation of IκB. J. Biol. Chem. 276:15920–28 [Google Scholar]
  91. Mangeat B, Gers-Huber G, Lehmann M, Zufferey M, Luban J, Piguet V. 91.  2009. HIV-1 Vpu neutralizes the antiviral factor Tetherin/BST-2 by binding it and directing its β-TrCP2-dependent degradation. PLOS Pathog 5:e1000574 [Google Scholar]
  92. Mansur DS, Maluquer de Motes C, Unterholzner L, Sumner RP, Ferguson BJ. 92.  et al. 2013. Poxvirus targeting of E3 ligase β-TrCP by molecular mimicry: a mechanism to inhibit NF-κB activation and promote immune evasion and virulence. PLOS Pathog 9:e1003183 [Google Scholar]
  93. Margottin F, Bour SP, Durand H, Selig L, Benichou S. 93.  et al. 1998. A novel human WD protein, h-βTrCP, that interacts with HIV-1 Vpu connects CD4 to the ER degradation pathway through an F-box motif. Mol. Cell 1:565–74 [Google Scholar]
  94. Tang W, Pavlish OA, Spiegelman VS, Parkhitko AA, Fuchs SY. 94.  2003. Interaction of Epstein-Barr virus latent membrane protein 1 with SCFHOS/β-TrCP E3 ubiquitin ligase regulates extent of NF-κB activation. J. Biol. Chem. 278:48942–49 [Google Scholar]
  95. Kumar KG, Krolewski JJ, Fuchs SY. 95.  2004. Phosphorylation and specific ubiquitin acceptor sites are required for ubiquitination and degradation of the IFNAR1 subunit of type I interferon receptor. J. Biol. Chem. 279:46614–20 [Google Scholar]
  96. Cui W, Xiao N, Xiao H, Zhou H, Yu M. 96.  et al. 2012. β-TrCP-mediated IRAK1 degradation releases TAK1–TRAF6 from the membrane to the cytosol for TAK1-dependent NF-κB activation. Mol. Cell. Biol. 32:3990–4000 [Google Scholar]
  97. Bagchi P, Bhowmick R, Nandi S, Kant Nayak M, Chawla-Sarkar M. 97.  2013. Rotavirus NSP1 inhibits interferon induced non-canonical NFκB activation by interacting with TNF receptor associated factor 2. Virology 444:41–44 [Google Scholar]
  98. Xie P. 98.  2013. TRAF molecules in cell signaling and in human diseases. J. Mol. Signal. 8:7 [Google Scholar]
  99. Bhowmick R, Halder UC, Chattopadhyay S, Nayak MK, Chawla-Sarkar M. 99.  2013. Rotavirus-encoded nonstructural protein 1 modulates cellular apoptotic machinery by targeting tumor suppressor protein p53. J. Virol. 87:6840–50 [Google Scholar]
  100. Sen A, Feng N, Ettayebi K, Hardy ME, Greenberg HB. 100.  2009. IRF3 inhibition by rotavirus NSP1 is host cell and virus strain dependent but independent of NSP1 proteasomal degradation. J. Virol. 83:10322–35 [Google Scholar]
  101. Qin L, Ren L, Zhou Z, Lei X, Chen L. 101.  et al. 2011. Rotavirus nonstructural protein 1 antagonizes innate immune response by interacting with retinoic acid inducible gene I. Virol. J. 8:526 [Google Scholar]
  102. Nandi S, Chanda S, Bagchi P, Nayak MK, Bhowmick R, Chawla-Sarkar M. 102.  2014. MAVS protein is attenuated by rotavirus nonstructural protein 1. PLOS ONE 9:e92126 [Google Scholar]
  103. Stark GR, Darnell JE Jr. 103.  2012. The JAK–STAT pathway at twenty. Immunity 36:503–14 [Google Scholar]
  104. Holloway G, Truong TT, Coulson BS. 104.  2009. Rotavirus antagonizes cellular antiviral responses by inhibiting the nuclear accumulation of STAT1, STAT2, and NF-κB. J. Virol. 83:4942–51 [Google Scholar]
  105. Holloway G, Dang VT, Jans DA, Coulson BS. 105.  2014. Rotavirus inhibits IFN-induced STAT nuclear translocation by a mechanism that acts after STAT binding to importin-α. J. Gen. Virol. 95:1723–33 [Google Scholar]
  106. Sen A, Rott L, Phan N, Mukherjee G, Greenberg HB. 106.  2014. Rotavirus NSP1 protein inhibits interferon-mediated STAT1 activation. J. Virol. 88:41–53 [Google Scholar]
  107. Desselberger U. 107.  2014. Rotaviruses. Virus Res. 190:75–96 [Google Scholar]
  108. Ogden KM, Snyder MJ, Dennis AF, Patton JT. 108.  2014. Predicted structure and domain organization of rotavirus capping enzyme and innate immune antagonist VP3. J. Virol. 88:9072–85 [Google Scholar]
  109. Chen D, Luongo CL, Nibert ML, Patton JT. 109.  1999. Rotavirus open cores catalyze 5′-capping and methylation of exogenous RNA: evidence that VP3 is a methyltransferase. Virology 265:120–30 [Google Scholar]
  110. Spencer E, Garcia BI. 110.  1984. Effect of S-adenosylmethionine on human rotavirus RNA synthesis. J. Virol. 52:188–97 [Google Scholar]
  111. Imai M, Akatani K, Ikegami N, Furuichi Y. 111.  1983. Capped and conserved terminal structures in human rotavirus genome double-stranded RNA segments. J. Virol. 47:125–36 [Google Scholar]
  112. Silverman RH. 112.  2007. Viral encounters with 2′,5′-oligoadenylate synthetase and RNase L during the interferon antiviral response. J. Virol. 81:12720–29 [Google Scholar]
  113. Chakrabarti A, Jha BK, Silverman RH. 113.  2011. New insights into the role of RNase L in innate immunity. J. Interferon Cytokine Res. 31:49–57 [Google Scholar]
  114. Silverman RH, Weiss SR. 114.  2014. Viral phosphodiesterases that antagonize double-stranded RNA signaling to RNase L by degrading 2-5A. J. Interferon Cytokine Res. 34:455–63 [Google Scholar]
  115. Zhang R, Jha BK, Ogden KM, Dong B, Zhao L. 115.  et al. 2013. Homologous 2′,5′-phosphodiesterases from disparate RNA viruses antagonize antiviral innate immunity. PNAS 110:13114–19 [Google Scholar]
  116. Ogden KM, Hu L, Jha BK, Sankaran B, Weiss SR. 116.  et al. 2015. Structural basis for 2′-5′-oligoadenylate binding and enzyme activity of a viral RNase L antagonist. J. Virol. 89:6633–45 [Google Scholar]
  117. Dever TE. 117.  2002. Gene-specific regulation by general translation factors. Cell 108:545–56 [Google Scholar]
  118. Walsh D, Mohr I. 118.  2011. Viral subversion of the host protein synthesis machinery. Nat. Rev. Microbiol. 9:860–75 [Google Scholar]
  119. Poncet D, Aponte C, Cohen J. 119.  1993. Rotavirus protein NSP3 (NS34) is bound to the 3′ end consensus sequence of viral mRNAs in infected cells. J. Virol. 67:3159–65 [Google Scholar]
  120. Groft CM, Burley SK. 120.  2002. Recognition of eIF4G by rotavirus NSP3 reveals a basis for mRNA circularization. Mol. Cell 9:1273–83 [Google Scholar]
  121. Piron M, Vende P, Cohen J, Poncet D. 121.  1998. Rotavirus RNA-binding protein NSP3 interacts with eIF4GI and evicts the poly(A) binding protein from eIF4F. EMBO J 17:5811–21 [Google Scholar]
  122. Vende P, Piron M, Castagne N, Poncet D. 122.  2000. Efficient translation of rotavirus mRNA requires simultaneous interaction of NSP3 with the eukaryotic translation initiation factor eIF4G and the mRNA 3′ end. J. Virol. 74:7064–71 [Google Scholar]
  123. Montero H, Arias CF, Lopez S. 123.  2006. Rotavirus nonstructural protein NSP3 is not required for viral protein synthesis. J. Virol. 80:9031–38 [Google Scholar]
  124. Harb M, Becker MM, Vitour D, Baron CH, Vende P. 124.  et al. 2008. Nuclear localization of cytoplasmic poly(A)-binding protein upon rotavirus infection involves the interaction of NSP3 with eIF4G and RoXaN. J. Virol. 82:11283–93 [Google Scholar]
  125. Montero H, Rojas M, Arias CF, Lopez S. 125.  2008. Rotavirus infection induces the phosphorylation of eIF2α but prevents the formation of stress granules. J. Virol. 82:1496–504 [Google Scholar]
  126. Rubio RM, Mora SI, Romero P, Arias CF, Lopez S. 126.  2013. Rotavirus prevents the expression of host responses by blocking the nucleocytoplasmic transport of polyadenylated mRNAs. J. Virol. 87:6336–45 [Google Scholar]
  127. Vijay-Kumar M, Gentsch JR, Kaiser WJ, Borregaard N, Offermann MK. 127.  et al. 2005. Protein kinase R mediates intestinal epithelial gene remodeling in response to double-stranded RNA and live rotavirus. J. Immunol. 174:6322–31 [Google Scholar]
/content/journals/10.1146/annurev-virology-110615-042152
Loading
/content/journals/10.1146/annurev-virology-110615-042152
Loading

Data & Media loading...

  • Article Type: Review Article
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error