1932

Abstract

Reverse genetics systems for viruses, the technology used to generate gene-engineered recombinant viruses from artificial genes, enable the study of the roles of the individual nucleotides and amino acids of viral genes and proteins in infectivity, replication, and pathogenicity. The successful development of a reverse genetics system for poliovirus in 1981 accelerated the establishment of protocols for other RNA viruses important for human health. Despite multiple efforts, rotavirus (RV), which causes severe gastroenteritis in infants, was refractory to reverse genetics analysis, and the first complete reverse genetics system for RV was established in 2017. This novel technique involves use of the fusogenic protein FAST (fusion-associated small transmembrane) derived from the bat-borne Nelson Bay orthoreovirus, which induces massive syncytium formation. Co-transfection of a FAST-expressing plasmid with complementary DNAs encoding RV genes enables rescue of recombinant RV. This review focuses on methodological insights into the reverse genetics system for RV and discusses applications and potential improvements to this system.

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2021-09-29
2024-05-17
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Literature Cited

  1. 1. 
    Racaniello VR, Baltimore D. 1981. Cloned poliovirus complementary DNA is infectious in mammalian cells. Science 214:916–19
    [Google Scholar]
  2. 2. 
    Schnell MJ, Mebatsion T, Conzelmann KK. 1994. Infectious rabies viruses from cloned cDNA. EMBO J 13:4195–203
    [Google Scholar]
  3. 3. 
    Kolykhalov AA, Agapov EV, Blight KJ, Mihalik K, Feinstone SM, Rice CM. 1997. Transmission of hepatitis C by intrahepatic inoculation with transcribed RNA. Science 277:570–74
    [Google Scholar]
  4. 4. 
    Yanagi M, Purcell RH, Emerson SU, Bukh J 1997. Transcripts from a single full-length cDNA clone of hepatitis C virus are infectious when directly transfected into the liver of a chimpanzee. PNAS 94:8738–43
    [Google Scholar]
  5. 5. 
    Neumann G, Watanabe T, Ito H, Watanabe S, Goto H et al. 1999. Generation of influenza A viruses entirely from cloned cDNAs. PNAS 96:9345–50
    [Google Scholar]
  6. 6. 
    Volchkov VE, Volchkova VA, Muhlberger E, Kolesnikova LV, Weik M et al. 2001. Recovery of infectious Ebola virus from complementary DNA: RNA editing of the GP gene and viral cytotoxicity. Science 291:1965–69
    [Google Scholar]
  7. 7. 
    Furuichi Y, Morgan M, Muthukrishnan S, Shatkin AJ. 1975. Reovirus messenger RNA contains a methylated, blocked 5′-terminal structure: m-7G(5′)ppp(5′)G-MpCp. PNAS 72:362–66
    [Google Scholar]
  8. 8. 
    Joklik WK. 1981. Structure and function of the reovirus genome. Microbiol. Rev. 45:483–501
    [Google Scholar]
  9. 9. 
    Coffey MC, Strong JE, Forsyth PA, Lee PW. 1998. Reovirus therapy of tumors with activated Ras pathway. Science 282:1332–34
    [Google Scholar]
  10. 10. 
    Chua KB, Crameri G, Hyatt A, Yu M, Tompang MR et al. 2007. A previously unknown reovirus of bat origin is associated with an acute respiratory disease in humans. PNAS 104:11424–29
    [Google Scholar]
  11. 11. 
    Erasmus BJ. 1975. Bluetongue in sheep and goats. Aust. Vet. J. 51:165–70
    [Google Scholar]
  12. 12. 
    Elbers ARW, Backx A, Mintiens K, Gerbier G, Staubach C et al. 2008. Field observations during the Bluetongue serotype 8 epidemic in 2006: II. Morbidity and mortality rate, case fatality and clinical recovery in sheep and cattle in the Netherlands. Prev. Vet. Med. 87:31–40
    [Google Scholar]
  13. 13. 
    Kobayashi T, Antar AA, Boehme KW, Danthi P, Eby EA et al. 2007. A plasmid-based reverse genetics system for animal double-stranded RNA viruses. Cell Host Microbe 1:147–57
    [Google Scholar]
  14. 14. 
    Kawagishi T, Kanai Y, Tani H, Shimojima M, Saijo M et al. 2016. Reverse genetics for fusogenic bat-borne orthoreovirus associated with acute respiratory tract infections in humans: role of outer capsid protein σC in viral replication and pathogenesis. PLOS Pathog 12:e1005455
    [Google Scholar]
  15. 15. 
    Boyce M, Celma CC, Roy P. 2008. Development of reverse genetics systems for bluetongue virus: recovery of infectious virus from synthetic RNA transcripts. J. Virol. 82:8339–48
    [Google Scholar]
  16. 16. 
    Shmulevitz M, Duncan R. 2000. A new class of fusion-associated small transmembrane (FAST) proteins encoded by the non-enveloped fusogenic reoviruses. EMBO J 19:902–12
    [Google Scholar]
  17. 17. 
    Tate JE, Burton AH, Boschi-Pinto C, Parashar UD. 2016. Global, regional, and national estimates of rotavirus mortality in children <5 years of age, 2000–2013. Clin. Infect. Dis. 62:Suppl. 2S96–105
    [Google Scholar]
  18. 18. 
    Matthijnssens J, Otto PH, Ciarlet M, Desselberger U, Van Ranst M, Johne R. 2012. VP6-sequence-based cutoff values as a criterion for rotavirus species demarcation. Arch. Virol. 157:1177–82
    [Google Scholar]
  19. 19. 
    Saiada F, Rahman HNA, Moni S, Karim MM, Pourkarim MR et al. 2011. Clinical presentation and molecular characterization of group B rotaviruses in diarrhoea patients in Bangladesh. J. Med. Microbiol. 60:529–36
    [Google Scholar]
  20. 20. 
    Alam MM, Pun SB, Gauchan P, Yokoo M, Doan YH et al. 2013. The first identification of rotavirus B from children and adults with acute diarrhoea in Kathmandu, Nepal. Trop. Med. Health 41:129–34
    [Google Scholar]
  21. 21. 
    Chen CM, Hung T, Bridger JC, McCrae MA. 1985. Chinese adult rotavirus is a group B rotavirus. Lancet 2:1123–24
    [Google Scholar]
  22. 22. 
    Caul EO, Ashley CR, Darville JM, Bridger JC. 1990. Group C rotavirus associated with fatal enteritis in a family outbreak. J. Med. Virol. 30:201–5
    [Google Scholar]
  23. 23. 
    Phan TG, Nishimura S, Okame M, Nguyen TA, Khamrin P et al. 2004. Virus diversity and an outbreak of group C rotavirus among infants and children with diarrhea in Maizuru city, Japan during 2002–2003. J. Med. Virol. 74:173–79
    [Google Scholar]
  24. 24. 
    Sanekata T, Ahmed MU, Kader A, Taniguchi K, Kobayashi N. 2003. Human group B rotavirus infections cause severe diarrhea in children and adults in Bangladesh. J. Clin. Microbiol. 41:2187–90
    [Google Scholar]
  25. 25. 
    Matthijnssens J, Ciarlet M, Rahman M, Attoui H, Banyai K et al. 2008. Recommendations for the classification of group A rotaviruses using all 11 genomic RNA segments. Arch. Virol. 153:1621–29
    [Google Scholar]
  26. 26. 
    Imai M, Akatani K, Ikegami N, Furuichi Y. 1983. Capped and conserved terminal structures in human rotavirus genome double-stranded RNA segments. J. Virol. 47:125–36
    [Google Scholar]
  27. 27. 
    McCrae MA, McCorquodale JG. 1983. Molecular biology of rotaviruses. V. Terminal structure of viral RNA species. Virology 126:204–12
    [Google Scholar]
  28. 28. 
    Chizhikov V, Patton JT. 2000. A four-nucleotide translation enhancer in the 3′-terminal consensus sequence of the nonpolyadenylated mRNAs of rotavirus. RNA 6:814–25
    [Google Scholar]
  29. 29. 
    Vende P, Piron M, Castagne N, Poncet D. 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]
  30. 30. 
    Yang AD, Barro M, Gorziglia MI, Patton JT. 2004. Translation enhancer in the 3′-untranslated region of rotavirus gene 6 mRNA promotes expression of the major capsid protein VP6. Arch. Virol. 149:303–21
    [Google Scholar]
  31. 31. 
    Ludert JE, Krishnaney AA, Burns JW, Vo PT, Greenberg HB. 1996. Cleavage of rotavirus VP4 in vivo. J. Gen. Virol. 77:3391–95
    [Google Scholar]
  32. 32. 
    Clark SM, Roth JR, Clark ML, Barnett BB, Spendlove RS. 1981. Trypsin enhancement of rotavirus infectivity: mechanism of enhancement. J. Virol. 39:816–22
    [Google Scholar]
  33. 33. 
    Babiuk LA, Mohammed K, Spence L, Fauvel M, Petro R. 1977. Rotavirus isolation and cultivation in the presence of trypsin. J. Clin. Microbiol. 6:610–17
    [Google Scholar]
  34. 34. 
    Espejo RT, Lopez S, Arias C. 1981. Structural polypeptides of simian rotavirus Sa11 and the effect of trypsin. J. Virol. 37:156–60
    [Google Scholar]
  35. 35. 
    Lopez S, Arias CF, Bell JR, Strauss JH, Espejo RT. 1985. Primary structure of the cleavage site associated with trypsin enhancement of rotavirus Sa11 infectivity. Virology 144:11–19
    [Google Scholar]
  36. 36. 
    Delorme C, Brussow H, Sidoti J, Roche N, Karlsson KA et al. 2001. Glycosphingolipid binding specificities of rotavirus: identification of a sialic acid-binding epitope. J. Virol. 75:2276–87
    [Google Scholar]
  37. 37. 
    Yu X, Dang VT, Fleming FE, von Itzstein M, Coulson BS, Blanchard H. 2012. Structural basis of rotavirus strain preference toward N-acetyl- or N-glycolylneuraminic acid-containing receptors. J. Virol. 86:13456–66
    [Google Scholar]
  38. 38. 
    Hu L, Crawford SE, Czako R, Cortes-Penfield NW, Smith DF et al. 2012. Cell attachment protein VP8* of a human rotavirus specifically interacts with A-type histo-blood group antigen. Nature 485:256–59
    [Google Scholar]
  39. 39. 
    Hu L, Ramani S, Czako R, Sankaran B, Yu Y et al. 2015. Structural basis of glycan specificity in neonate-specific bovine-human reassortant rotavirus. Nat. Commun. 6:8346
    [Google Scholar]
  40. 40. 
    Huang P, Xia M, Tan M, Zhong W, Wei C et al. 2012. Spike protein VP8* of human rotavirus recognizes histo-blood group antigens in a type-specific manner. J. Virol. 86:4833–43
    [Google Scholar]
  41. 41. 
    Liu Y, Huang P, Tan M, Liu Y, Biesiada J et al. 2012. Rotavirus VP8*: phylogeny, host range, and interaction with histo-blood group antigens. J. Virol. 86:9899–910
    [Google Scholar]
  42. 42. 
    Hu L, Sankaran B, Laucirica DR, Patil K, Salmen W et al. 2018. Glycan recognition in globally dominant human rotaviruses. Nat. Commun. 9:2631
    [Google Scholar]
  43. 43. 
    Gutierrez M, Isa P, Sanchez-San Martin C, Perez-Vargas J, Espinosa R et al. 2010. Different rotavirus strains enter MA104 cells through different endocytic pathways: the role of clathrin-mediated endocytosis. J. Virol. 84:9161–69
    [Google Scholar]
  44. 44. 
    Martin CSS, Lopez T, Arias CF, Lopez S. 2004. Characterization of rotavirus cell entry. J. Virol. 78:2310–18
    [Google Scholar]
  45. 45. 
    Ludert JE, Michelangeli F, Gil F, Liprandi F, Esparza J. 1987. Penetration and uncoating of rotaviruses in cultured cells. Intervirology 27:95–101
    [Google Scholar]
  46. 46. 
    Salgado EN, Garcia Rodriguez B, Narayanaswamy N, Krishnan Y, Harrison SC 2018. Visualization of calcium ion loss from rotavirus during cell entry. J. Virol. 92:24e01327-18
    [Google Scholar]
  47. 47. 
    Abdelhakim AH, Salgado EN, Fu X, Pasham M, Nicastro D et al. 2014. Structural correlates of rotavirus cell entry. PLOS Pathog 10:e1004355
    [Google Scholar]
  48. 48. 
    Patton JT, Silvestri LS, Tortorici MA, Vasquez-Del Carpio R, Taraporewala ZF. 2006. Rotavirus genome replication and morphogenesis: role of the viroplasm. Curr. Top. Microbiol. Immunol. 309:169–87
    [Google Scholar]
  49. 49. 
    Fabbretti E, Afrikanova I, Vascotto F, Burrone OR. 1999. Two non-structural rotavirus proteins, NSP2 and NSP5, form viroplasm-like structures in vivo. J. Gen. Virol. 80:2333–39
    [Google Scholar]
  50. 50. 
    Trask SD, McDonald SM, Patton JT. 2012. Structural insights into the coupling of virion assembly and rotavirus replication. Nat. Rev. Microbiol. 10:165–77
    [Google Scholar]
  51. 51. 
    Jourdan N, Maurice M, Delautier D, Quero AM, Servin AL, Trugnan G. 1997. Rotavirus is released from the apical surface of cultured human intestinal cells through nonconventional vesicular transport that bypasses the Golgi apparatus. J. Virol. 71:8268–78
    [Google Scholar]
  52. 52. 
    Trejo-Cerro O, Eichwald C, Schraner EM, Silva-Ayala D, Lopez S, Arias CF. 2018. Actin-dependent nonlytic rotavirus exit and infectious virus morphogenetic pathway in nonpolarized cells. J. Virol. 92:6e02076-17
    [Google Scholar]
  53. 53. 
    Bass DM, Baylor MR, Chen C, Mackow EM, Bremont M, Greenberg HB. 1992. Liposome-mediated transfection of intact viral particles reveals that plasma membrane penetration determines permissivity of tissue culture cells to rotavirus. J. Clin. Invest. 90:2313–20
    [Google Scholar]
  54. 54. 
    Furuichi Y, Muthukrishnan S, Shatkin AJ. 1975. 5′-Terminal m-7G(5′)ppp(5′)G-m-p in vivo: identification in reovirus genome RNA. PNAS 72:742–45
    [Google Scholar]
  55. 55. 
    Furuichi Y, Muthukrishnan S, Tomasz J, Shatkin AJ. 1976. Mechanism of formation of reovirus mRNA 5′-terminal blocked and methylated sequence, m7GpppGmpC. J. Biol. Chem. 251:5043–53
    [Google Scholar]
  56. 56. 
    Kozak M. 1977. Nucleotide sequences of 5′-terminal ribosome-protected initiation regions from two reovirus messages. Nature 269:391–94
    [Google Scholar]
  57. 57. 
    Kozak M, Shatkin AJ. 1976. Characterization of ribosome-protected fragments from reovirus messenger RNA. J. Biol. Chem. 251:4259–66
    [Google Scholar]
  58. 58. 
    Kozak M, Shatkin AJ. 1978. Identification of features in 5′ terminal fragments from reovirus mRNA which are important for ribosome binding. Cell 13:201–12
    [Google Scholar]
  59. 59. 
    Roner MR, Sutphin LA, Joklik WK. 1990. Reovirus RNA is infectious. Virology 179:845–52
    [Google Scholar]
  60. 60. 
    Roner MR, Joklik WK 2001. Reovirus reverse genetics: incorporation of the CAT gene into the reovirus genome. PNAS 98:8036–41
    [Google Scholar]
  61. 61. 
    Roner MR, Steele BG. 2007. Localizing the reovirus packaging signals using an engineered m1 and s2 ssRNA. Virology 358:89–97
    [Google Scholar]
  62. 62. 
    Ishii K, Ueda Y, Matsuo K, Matsuura Y, Kitamura T et al. 2002. Structural analysis of vaccinia virus DIs strain: application as a new replication-deficient viral vector. Virology 302:433–44
    [Google Scholar]
  63. 63. 
    Kobayashi T, Ooms LS, Ikizler M, Chappell JD, Dermody TS. 2010. An improved reverse genetics system for mammalian orthoreoviruses. Virology 398:194–200
    [Google Scholar]
  64. 64. 
    Boehme KW, Guglielmi KM, Dermody TS 2009. Reovirus nonstructural protein σ1s is required for establishment of viremia and systemic dissemination. PNAS 106:19986–91
    [Google Scholar]
  65. 65. 
    Demidenko AA, Blattman JN, Blattman NN, Greenberg PD, Nibert ML 2013. Engineering recombinant reoviruses with tandem repeats and a tetravirus 2A-like element for exogenous polypeptide expression. PNAS 110:E1867–76
    [Google Scholar]
  66. 66. 
    Kanai Y, Kawagishi T, Matsuura Y, Kobayashi T. 2019. In vivo live imaging of oncolytic mammalian orthoreovirus expressing NanoLuc luciferase in tumor xenograft mice. J. Virol. 93:14e00401-19
    [Google Scholar]
  67. 67. 
    Kemp V, van den Wollenberg DJM, Camps MGM, van Hall T, Kinderman P et al. 2018. Arming oncolytic reovirus with GM-CSF gene to enhance immunity. Cancer Gene Ther 26:268–81
    [Google Scholar]
  68. 68. 
    Boyce M, Roy P. 2007. Recovery of infectious bluetongue virus from RNA. J. Virol. 81:2179–86
    [Google Scholar]
  69. 69. 
    Kaname Y, Celma CCP, Kanai Y, Roy P. 2013. Recovery of African horse sickness virus from synthetic RNA. J. Gen. Virol. 94:2259–65
    [Google Scholar]
  70. 70. 
    Yang T, Zhang J, Xu Q, Sun E, Li J et al. 2015. Development of a reverse genetics system for epizootic hemorrhagic disease virus and evaluation of novel strains containing duplicative gene rearrangements. J. Gen. Virol. 96:2714–20
    [Google Scholar]
  71. 71. 
    Matsuo E, Celma CCP, Roy P 2010. A reverse genetics system of African horse sickness virus reveals existence of primary replication. FEBS Lett 584:3386–91
    [Google Scholar]
  72. 72. 
    Matsuo E, Roy P. 2013. Minimum requirements for bluetongue virus primary replication in vivo. J. Virol. 87:882–89
    [Google Scholar]
  73. 73. 
    van Rijn PA, van de Water SG, Feenstra F, van Gennip RG. 2016. Requirements and comparative analysis of reverse genetics for bluetongue virus (BTV) and African horse sickness virus (AHSV). Virol. J. 13:119
    [Google Scholar]
  74. 74. 
    Matsuo E, Saeki K, Roy P, Kawano J 2015. Development of reverse genetics for Ibaraki virus to produce viable VP6-tagged IBAV. FEBS Open Bio 5:445–53
    [Google Scholar]
  75. 75. 
    Guo Y, Pretorius JM, Xu Q, Wu D, Bu Z et al. 2020. Development and optimization of a DNA-based reverse genetics systems for epizootic hemorrhagic disease virus. Arch. Virol. 165:1079–87
    [Google Scholar]
  76. 76. 
    Komoto S, Sasaki J, Taniguchi K 2006. Reverse genetics system for introduction of site-specific mutations into the double-stranded RNA genome of infectious rotavirus. PNAS 103:4646–51
    [Google Scholar]
  77. 77. 
    Troupin C, Dehee A, Schnuriger A, Vende P, Poncet D, Garbarg-Chenon A. 2010. Rearranged genomic RNA segments offer a new approach to the reverse genetics of rotaviruses. J. Virol. 84:6711–19
    [Google Scholar]
  78. 78. 
    Trask SD, Taraporewala ZF, Boehme KW, Dermody TS, Patton JT 2010. Dual selection mechanisms drive efficient single-gene reverse genetics for rotavirus. PNAS 107:18652–57
    [Google Scholar]
  79. 79. 
    Johne R, Reetz J, Kaufer BB, Trojnar E. 2016. Generation of an avian-mammalian rotavirus reassortant by using a helper virus-dependent reverse genetics system. J. Virol. 90:1439–43
    [Google Scholar]
  80. 80. 
    Komoto S, Kugita M, Sasaki J, Taniguchi K. 2008. Generation of recombinant rotavirus with an antigenic mosaic of cross-reactive neutralization epitopes on VP4. J. Virol. 82:6753–57
    [Google Scholar]
  81. 81. 
    Komoto S, Wakuda M, Ide T, Niimi G, Maeno Y et al. 2011. Modification of the trypsin cleavage site of rotavirus VP4 to a furin-sensitive form does not enhance replication efficiency. J. Gen. Virol. 92:2914–21
    [Google Scholar]
  82. 82. 
    Navarro A, Trask SD, Patton JT. 2013. Generation of genetically stable recombinant rotaviruses containing novel genome rearrangements and heterologous sequences by reverse genetics. J. Virol. 87:6211–20
    [Google Scholar]
  83. 83. 
    Kanai Y, Komoto S, Kawagishi T, Nouda R, Nagasawa N et al. 2017. Entirely plasmid-based reverse genetics system for rotaviruses. PNAS 114:2349–54
    [Google Scholar]
  84. 84. 
    Casais R, Thiel V, Siddell SG, Cavanagh D, Britton P. 2001. Reverse genetics system for the avian coronavirus infectious bronchitis virus. J. Virol. 75:12359–69
    [Google Scholar]
  85. 85. 
    Schneider H, Spielhofer P, Kaelin K, Dotsch C, Radecke F et al. 1997. Rescue of measles virus using a replication-deficient vaccinia-T7 vector. J. Virol. Methods 64:57–64
    [Google Scholar]
  86. 86. 
    Kato A, Sakai Y, Shioda T, Kondo T, Nakanishi M, Nagai Y. 1996. Initiation of Sendai virus multiplication from transfected cDNA or RNA with negative or positive sense. Genes Cells 1:569–79
    [Google Scholar]
  87. 87. 
    Peeters BPH, de Leeuw OS, Koch G, Gielkens ALJ. 1999. Rescue of Newcastle disease virus from cloned cDNA: evidence that cleavability of the fusion protein is a major determinant for virulence. J. Virol. 73:5001–9
    [Google Scholar]
  88. 88. 
    Ensinger MJ, Martin SA, Paoletti E, Moss B 1975. Modification of the 5′-terminus of mRNA by soluble guanylyl and methyl transferases from vaccinia virus. PNAS 72:2525–29
    [Google Scholar]
  89. 89. 
    Niles EG, Lee-Chen GJ, Shuman S, Moss B, Broyles SS. 1989. Vaccinia virus gene D12L encodes the small subunit of the viral mRNA capping enzyme. Virology 172:513–22
    [Google Scholar]
  90. 90. 
    Morgan JR, Cohen LK, Roberts BE. 1984. Identification of the DNA sequences encoding the large subunit of the mRNA-capping enzyme of vaccinia virus. J. Virol. 52:206–14
    [Google Scholar]
  91. 91. 
    Scholz J, Bachlein C, Gadicherla AK, Falkenhagen A, Tausch SH, Johne R. 2020. Establishment of a plasmid-based reverse genetics system for the cell culture-adapted hepatitis E virus genotype 3c strain 47832c. Pathogens 9:3157
    [Google Scholar]
  92. 92. 
    Eaton HE, Kobayashi T, Dermody TS, Johnston RN, Jais PH, Shmulevitz M. 2017. African swine fever virus NP868R capping enzyme promotes reovirus rescue during reverse genetics by promoting reovirus protein expression, virion assembly, and RNA incorporation into infectious virions. J. Virol. 91:11e02416-16
    [Google Scholar]
  93. 93. 
    Kanai Y, Kawagishi T, Sakai Y, Nouda R, Shimojima M et al. 2019. Cell-cell fusion induced by reovirus FAST proteins enhances replication and pathogenicity of non-enveloped dsRNA viruses. PLOS Pathog 15:e1007675
    [Google Scholar]
  94. 94. 
    Ciechonska M, Duncan R. 2014. Reovirus FAST proteins: virus-encoded cellular fusogens. Trends Microbiol 22:715–24
    [Google Scholar]
  95. 95. 
    Yang Y, Gaspard G, McMullen N, Duncan R. 2020. Polycistronic genome segment evolution and gain and loss of FAST protein function during fusogenic orthoreovirus speciation. Viruses 12:7702
    [Google Scholar]
  96. 96. 
    Diller JR, Parrington HM, Patton JT, Ogden KM. 2019. Rotavirus species B encodes a functional fusion-associated small transmembrane protein. J. Virol. 93:20e00813-19
    [Google Scholar]
  97. 97. 
    Corcoran JA, Duncan R. 2004. Reptilian reovirus utilizes a small type III protein with an external myristylated amino terminus to mediate cell-cell fusion. J. Virol. 78:4342–51
    [Google Scholar]
  98. 98. 
    Dawe S, Corcoran JA, Clancy EK, Salsman J, Duncan R. 2005. Unusual topological arrangement of structural motifs in the baboon reovirus fusion-associated small transmembrane protein. J. Virol. 79:6216–26
    [Google Scholar]
  99. 99. 
    Corcoran JA, Syvitski R, Top D, Epand RM, Epand RF et al. 2004. Myristoylation, a protruding loop, and structural plasticity are essential features of a nonenveloped virus fusion peptide motif. J. Biol. Chem. 279:51386–94
    [Google Scholar]
  100. 100. 
    Shmulevitz M, Salsman J, Duncan R. 2003. Palmitoylation, membrane-proximal basic residues, and transmembrane glycine residues in the reovirus p10 protein are essential for syncytium formation. J. Virol. 77:9769–79
    [Google Scholar]
  101. 101. 
    Read J, Clancy EK, Sarker M, de Antueno R, Langelaan DN et al. 2015. Reovirus FAST proteins drive pore formation and syncytiogenesis using a novel helix-loop-helix fusion-inducing lipid packing sensor. PLOS Pathog 11:e1004962
    [Google Scholar]
  102. 102. 
    Boutilier J, Duncan R. 2011. The reovirus fusion-associated small transmembrane (FAST) proteins: virus-encoded cellular fusogens. Curr. Top. Membr. 68:107–40
    [Google Scholar]
  103. 103. 
    Top D, Barry C, Racine T, Ellis CL, Duncan R. 2009. Enhanced fusion pore expansion mediated by the trans-acting endodomain of the reovirus FAST proteins. PLOS Pathog 5:e1000331
    [Google Scholar]
  104. 104. 
    Barry C, Duncan R. 2009. Multifaceted sequence-dependent and -independent roles for reovirus FAST protein cytoplasmic tails in fusion pore formation and syncytiogenesis. J. Virol. 83:12185–95
    [Google Scholar]
  105. 105. 
    Corcoran JA, Clancy EK, Duncan R. 2011. Homomultimerization of the reovirus p14 fusion-associated small transmembrane protein during transit through the ER-Golgi complex secretory pathway. J. Gen. Virol. 92:162–66
    [Google Scholar]
  106. 106. 
    Corcoran JA, Salsman J, de Antueno R, Touhami A, Jericho MH et al. 2006. The p14 fusion-associated small transmembrane (FAST) protein effects membrane fusion from a subset of membrane microdomains. J. Biol. Chem. 281:31778–89
    [Google Scholar]
  107. 107. 
    Key T, Duncan R. 2014. A compact, multifunctional fusion module directs cholesterol-dependent homomultimerization and syncytiogenic efficiency of reovirus p10 FAST proteins. PLOS Pathog 10:e1004023
    [Google Scholar]
  108. 108. 
    Podbilewicz B. 2014. Virus and cell fusion mechanisms. Annu. Rev. Cell Dev. Biol. 30:111–39
    [Google Scholar]
  109. 109. 
    Duncan R. 2019. Fusogenic reoviruses and their fusion-associated small transmembrane (FAST) proteins. Annu. Rev. Virol. 6:341–63
    [Google Scholar]
  110. 110. 
    Salsman J, Top D, Barry C, Duncan R. 2008. A virus-encoded cell-cell fusion machine dependent on surrogate adhesins. PLOS Pathog 4:e1000016
    [Google Scholar]
  111. 111. 
    Rosenberger JK, Sterner FJ, Botts S, Lee KP, Margolin A. 1989. In vitro and in vivo characterization of avian reoviruses. I. Pathogenicity and antigenic relatedness of several avian reovirus isolates. Avian Dis. 33:535–44
    [Google Scholar]
  112. 112. 
    Duncan R, Murphy FA, Mirkovic RR. 1995. Characterization of a novel syncytium-inducing baboon reovirus. Virology 212:752–56
    [Google Scholar]
  113. 113. 
    Leland MM, Hubbard GB, Sentmore HT, Soike KF, Hilliard JK 2000. Outbreak of orthoreovirus-induced meningoencephalomyelitis in baboons. Comp. Med. 50:199–205
    [Google Scholar]
  114. 114. 
    Chua KB, Voon K, Crameri G, Tan HS, Rosli J et al. 2008. Identification and characterization of a new orthoreovirus from patients with acute respiratory infections. PLOS ONE 3:e3803
    [Google Scholar]
  115. 115. 
    Chua KB, Voon K, Yu M, Keniscope C, Abdul Rasid K, Wang LF 2011. Investigation of a potential zoonotic transmission of orthoreovirus associated with acute influenza-like illness in an adult patient. PLOS ONE 6:e25434
    [Google Scholar]
  116. 116. 
    Voon K, Tan YF, Leong PP, Teng CL, Gunnasekaran R et al. 2015. Pteropine orthoreovirus infection among out-patients with acute upper respiratory tract infection in Malaysia. J. Med. Virol. 87:2149–53
    [Google Scholar]
  117. 117. 
    Ahne W, Thomsen I, Winton J. 1987. Isolation of a reovirus from the snake, Python regius. Brief report. Arch. Virol. 94:135–39
    [Google Scholar]
  118. 118. 
    Lamirande EW, Nichols DK, Owens JW, Gaskin JM, Jacobson ER. 1999. Isolation and experimental transmission of a reovirus pathogenic in ratsnakes (Elaphe species). Virus Res 63:135–41
    [Google Scholar]
  119. 119. 
    Vieler E, Baumgartner W, Herbst W, Kohler G. 1994. Characterization of a reovirus isolate from a rattle snake, Crotalus viridis, with neurological dysfunction. Arch. Virol. 138:341–44
    [Google Scholar]
  120. 120. 
    Blahak S, Ott I, Vieler E. 1995. Comparison of 6 different reoviruses of various reptiles. Vet. Res. 26:470–76
    [Google Scholar]
  121. 121. 
    Duncan R, Chen Z, Walsh S, Wu S. 1996. Avian reovirus-induced syncytium formation is independent of infectious progeny virus production and enhances the rate, but is not essential, for virus-induced cytopathology and virus egress. Virology 224:453–64
    [Google Scholar]
  122. 122. 
    Duncan R, Sullivan K. 1998. Characterization of two avian reoviruses that exhibit strain-specific quantitative differences in their syncytium-inducing and pathogenic capabilities. Virology 250:263–72
    [Google Scholar]
  123. 123. 
    Kanai Y, Kawagishi T, Okamoto M, Sakai Y, Matsuura Y, Kobayashi T. 2018. Lethal murine infection model for human respiratory disease-associated Pteropine orthoreovirus. Virology 514:57–65
    [Google Scholar]
  124. 124. 
    Le Boeuf F, Gebremeskel S, McMullen N, He H, Greenshields AL et al. 2017. Reovirus FAST protein enhances vesicular stomatitis virus oncolytic virotherapy in primary and metastatic tumor models. Mol. Ther.-Oncolyt. 6:80–89
    [Google Scholar]
  125. 125. 
    Huang CP, Liu WJ, Xu W, Jin T, Zhao YZ et al. 2016. A bat-derived putative cross-family recombinant coronavirus with a reovirus gene. PLOS Pathog 12:9e1005883
    [Google Scholar]
  126. 126. 
    Sattentau Q. 2008. Avoiding the void: cell-to-cell spread of human viruses. Nat. Rev. Microbiol. 6:815–26
    [Google Scholar]
  127. 127. 
    Stacy-Phipps S, Patton JT. 1987. Synthesis of plus- and minus-strand RNA in rotavirus-infected cells. J. Virol. 61:3479–84
    [Google Scholar]
  128. 128. 
    Ayala-Breton C, Arias M, Espinosa R, Romero P, Arias CF, Lopez S. 2009. Analysis of the kinetics of transcription and replication of the rotavirus genome by RNA interference. J. Virol. 83:8819–31
    [Google Scholar]
  129. 129. 
    Papa G, Venditti L, Braga L, Schneider E, Giacca M et al. 2020. CRISPR-Csy4-mediated editing of rotavirus double-stranded RNA genome. Cell Rep 32:108205
    [Google Scholar]
  130. 130. 
    Kanai Y, Kawagishi T, Nouda R, Onishi M, Pannacha P et al. 2019. Development of stable rotavirus reporter expression systems. J. Virol. 93:e01774-18
    [Google Scholar]
  131. 131. 
    Komoto S, Fukuda S, Ide T, Ito N, Sugiyama M et al. 2018. Generation of recombinant rotaviruses expressing fluorescent proteins by using an optimized reverse genetics system. J. Virol. 92:13e00588-18
    [Google Scholar]
  132. 132. 
    Borodavka A, Dykeman EC, Schrimpf W, Lamb DC 2017. Protein-mediated RNA folding governs sequence-specific interactions between rotavirus genome segments. eLife 6:e27453
    [Google Scholar]
  133. 133. 
    Matsuo E, Roy P. 2009. Bluetongue virus VP6 acts early in the replication cycle and can form the basis of chimeric virus formation. J. Virol. 83:8842–48
    [Google Scholar]
  134. 134. 
    Boyce M, Celma CC, Roy P. 2012. Bluetongue virus non-structural protein 1 is a positive regulator of viral protein synthesis. Virol. J. 9:178
    [Google Scholar]
  135. 135. 
    Johnson MA, McCrae MA. 1989. Molecular biology of rotaviruses. VIII. Quantitative analysis of regulation of gene expression during virus replication. J. Virol. 63:2048–55
    [Google Scholar]
  136. 136. 
    Mitzel DN, Weisend CM, White MW, Hardy ME. 2003. Translational regulation of rotavirus gene expression. J. Gen. Virol. 84:383–91
    [Google Scholar]
  137. 137. 
    Precious BL, Carlos TS, Goodbourn S, Randall RE. 2007. Catalytic turnover of STAT1 allows PIV5 to dismantle the interferon-induced anti-viral state of cells. Virology 368:114–21
    [Google Scholar]
  138. 138. 
    Didcock L, Young DF, Goodbourn S, Randall RE. 1999. The V protein of simian virus 5 inhibits interferon signalling by targeting STAT1 for proteasome-mediated degradation. J. Virol. 73:9928–33
    [Google Scholar]
  139. 139. 
    Chen Z, Rijnbrand R, Jangra RK, Devaraj SG, Qu L et al. 2007. Ubiquitination and proteasomal degradation of interferon regulatory factor-3 induced by Npro from a cytopathic bovine viral diarrhea virus. Virology 366:277–92
    [Google Scholar]
  140. 140. 
    Hilton L, Moganeradj K, Zhang G, Chen YH, Randall RE et al. 2006. The NPro product of bovine viral diarrhea virus inhibits DNA binding by interferon regulatory factor 3 and targets it for proteasomal degradation. J. Virol. 80:11723–32
    [Google Scholar]
  141. 141. 
    Sanchez-Tacuba L, Feng N, Meade NJ, Mellits KH, Jais PH et al. 2020. An optimized reverse genetics system suitable for efficient recovery of simian, human and murine-like rotaviruses. J. Virol. 94:18e01294-20
    [Google Scholar]
  142. 142. 
    Komoto S, Fukuda S, Kugita M, Hatazawa R, Koyama C et al. 2019. Generation of infectious recombinant human rotaviruses from just 11 cloned cDNAs encoding the rotavirus genome. J. Virol. 93:e02207-18
    [Google Scholar]
  143. 143. 
    Kawagishi T, Nurdin JA, Onishi M, Nouda R, Kanai Y et al. 2020. Reverse genetics system for a human group A rotavirus. J. Virol. 94:2e00963-19
    [Google Scholar]
  144. 144. 
    McDonald SM, Matthijnssens J, McAllen JK, Hine E, Overton L et al. 2009. Evolutionary dynamics of human rotaviruses: balancing reassortment with preferred genome constellations. PLOS Pathog 5:e1000634
    [Google Scholar]
  145. 145. 
    Philip AA, Perry JL, Eaton HE, Shmulevitz M, Hyser JM et al. 2019. Generation of recombinant rotavirus expressing NSP3-UnaG fusion protein by a simplified reverse genetics system. J. Virol. 93:24e01616-19
    [Google Scholar]
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