1932

Abstract

Historically, viruses were considered to be either enveloped or nonenveloped. However, recent work on hepatitis A virus and hepatitis E virus challenges this long-held tenet. Whereas these human pathogens are shed in feces as naked nonenveloped virions, recent studies indicate that both circulate in the blood completely masked in membranes during acute infection. These membrane-wrapped virions are as infectious as their naked counterparts, although they do not express a virally encoded protein on their surface, thus distinguishing them from conventional enveloped viruses. The absence of a viral fusion protein implies that these quasi-enveloped virions have unique mechanisms for entry into cells. Like true enveloped viruses, however, these phylogenetically distinct viruses usurp components of the host ESCRT system to hijack host cell membranes and noncytolytically exit infected cells. The membrane protects these viruses from neutralizing antibodies, facilitating dissemination within the host, whereas nonenveloped virions shed in feces are stable in the environment, allowing for epidemic transmission.

Loading

Article metrics loading...

/content/journals/10.1146/annurev-virology-031413-085359
2014-09-29
2024-04-18
Loading full text...

Full text loading...

/deliver/fulltext/virology/1/1/annurev-virology-031413-085359.html?itemId=/content/journals/10.1146/annurev-virology-031413-085359&mimeType=html&fmt=ahah

Literature Cited

  1. Remlinger P. 1.  1919. Action de l'ether sur le virus rabique. Ann. Inst. Pasteur 33:616–33 [Google Scholar]
  2. Taylor E, Amoss HL. 2.  1917. Carriage of the virus of poliomyelitis, with subsequent development of the infection. J. Exp. Med. 26:746–54 [Google Scholar]
  3. Sulkin SE, Zarafonetis C. 3.  1947. Influence of anesthesia on experimental neurotropic virus infections. II. In vitro studies with the viruses of Western and Eastern equine encephalomyelitis, St. Louis encephalitis, poliomyelitis (Lansing) and rabies. J. Exp. Med. 85:559–69 [Google Scholar]
  4. Andrewes CH, Horstmann DM. 4.  1947. The susceptibility of viruses to ethyl ether. J. Gen. Microbiol. 3:290–97 [Google Scholar]
  5. Smith W. 5.  1939. The action of bile salts on viruses. J. Pathol. Bacteriol. 48:557–71 [Google Scholar]
  6. Putz MM, Midgley CM, Law M, Smith GL. 6.  2006. Quantification of antibody responses against multiple antigens of the two infectious forms of vaccinia virus provides a benchmark for smallpox vaccination. Nat. Med. 12:1310–15 [Google Scholar]
  7. Wei X, Decker JM, Wang S, Hui H, Kappes JC. 7.  et al. 2003. Antibody neutralization and escape by HIV-1. Nature 422:307–12 [Google Scholar]
  8. Lemon SM. 8.  1985. Type A viral hepatitis: new developments in an old disease. N. Engl. J. Med. 313:1059–67 [Google Scholar]
  9. Purcell RH, Emerson SU. 9.  2008. Hepatitis E: an emerging awareness of an old disease. J. Hepatol. 48:494–503 [Google Scholar]
  10. Sreenivasan MA, Arankalle VA, Sehgal A, Pavri KM. 10.  1984. Non-A, non-B epidemic hepatitis: visualization of virus-like particles in the stool by immune electron microscopy. J. Gen. Virol. 65:1005–7 [Google Scholar]
  11. Feinstone SM, Kapikian AZ, Purcell RH. 11.  1973. Hepatitis A: detection by immune electron microscopy of a viruslike antigen associated with acute illness. Science 182:1026–28 [Google Scholar]
  12. Feng Z, Hensley L, McKnight KL, Hu F, Madden V. 12.  et al. 2013. A pathogenic picornavirus acquires an envelope by hijacking cellular membranes. Nature 496:367–71 [Google Scholar]
  13. Takahashi M, Tanaka T, Takahashi H, Hoshino Y, Nagashima S. 13.  et al. 2010. Hepatitis E virus (HEV) strains in serum samples can replicate efficiently in cultured cells despite the coexistence of HEV antibodies: characterization of HEV virions in blood circulation. J. Clin. Microbiol. 48:1112–25 [Google Scholar]
  14. Rossman JS, Lamb RA. 14.  2013. Viral membrane scission. Annu. Rev. Cell Dev. Biol. 29:551–69 [Google Scholar]
  15. Votteler J, Sundquist WI. 15.  2013. Virus budding and the ESCRT pathway. Cell Host Microbe 14:232–41 [Google Scholar]
  16. Jemielity S, Wang JJ, Chan YK, Ahmed AA, Li W. 16.  et al. 2013. TIM-family proteins promote infection of multiple enveloped viruses through virion-associated phosphatidylserine. PLoS Pathog. 9:e1003232 [Google Scholar]
  17. Moller-Tank S, Kondratowicz AS, Davey RA, Rennert PD, Maury W. 17.  2013. Role of the phosphatidylserine receptor TIM-1 in enveloped-virus entry. J. Virol. 87:8327–41 [Google Scholar]
  18. Bissig C, Gruenberg J. 18.  2014. ALIX and the multivesicular endosome: ALIX in Wonderland. Trends Cell Biol. 24:19–25 [Google Scholar]
  19. Hurley JH. 19.  2010. The ESCRT complexes. Crit. Rev. Biochem. Mol. Biol. 45:463–87 [Google Scholar]
  20. Rusten TE, Vaccari T, Stenmark H. 20.  2011. Shaping development with ESCRTs. Nat. Cell Biol. 14:38–45 [Google Scholar]
  21. Wollert T, Hurley JH. 21.  2010. Molecular mechanism of multivesicular body biogenesis by ESCRT complexes. Nature 464:864–69 [Google Scholar]
  22. Bobrie A, Colombo M, Raposo G, Thery C. 22.  2011. Exosome secretion: molecular mechanisms and roles in immune responses. Traffic 12:1659–68 [Google Scholar]
  23. Mathivanan S, Ji H, Simpson RJ. 23.  2010. Exosomes: extracellular organelles important in intercellular communication. J. Proteomics 73:1907–20 [Google Scholar]
  24. Engelenburg SB, Shtengel G, Sengupta P, Waki K, Jarnik M. 24.  Van et al. 2014. Distribution of ESCRT machinery at HIV assembly sites reveals virus scaffolding of ESCRT subunits. Science 343:653–56 [Google Scholar]
  25. Chen BJ, Lamb RA. 25.  2008. Mechanisms for enveloped virus budding: Can some viruses do without an ESCRT?. Virology 372:221–32 [Google Scholar]
  26. Ren X, Hurley JH. 26.  2011. Proline-rich regions and motifs in trafficking: from ESCRT interaction to viral exploitation. Traffic 12:1282–90 [Google Scholar]
  27. Schauflinger M, Fischer D, Schreiber A, Chevillotte M, Walther P. 27.  et al. 2011. The tegument protein UL71 of human cytomegalovirus is involved in late envelopment and affects multivesicular bodies. J. Virol. 85:3821–32 [Google Scholar]
  28. Das S, Pellett PE. 28.  2011. Spatial relationships between markers for secretory and endosomal machinery in human cytomegalovirus–infected cells versus those in uninfected cells. J. Virol. 85:5864–79 [Google Scholar]
  29. Morita E, Sandrin V, Chung HY, Morham SG, Gygi SP. 29.  et al. 2007. Human ESCRT and ALIX proteins interact with proteins of the midbody and function in cytokinesis. EMBO J. 26:4215–27 [Google Scholar]
  30. Martin A, Lemon SM. 30.  2006. Hepatitis A virus: from discovery to vaccines. Hepatology 43:S164–72 [Google Scholar]
  31. Martin A, Lemon SM. 31.  2002. The molecular biology of hepatitis A virus. Hepatitis Viruses J Ou 23–50 Norwell, MA: Kluwer Acad. [Google Scholar]
  32. Feng Z, Lemon SM. 32.  2010. Hepatitis A virus. The Picornaviruses E Ehrenfeld, E Domingo, RP Roos 383–96 Washington, DC: ASM [Google Scholar]
  33. Chow M, Newman JFE, Filman DJ, Hogle JM, Rowlands DJ, Brown F. 33.  1987. Myristylation of picornavirus capsid protein VP4 and its structural significance. Nature 327:482–86 [Google Scholar]
  34. Ansardi DC, Porter DC, Morrow CD. 34.  1992. Myristylation of poliovirus capsid precursor P1 is required for assembly of subviral particles. J. Virol. 66:4556–63 [Google Scholar]
  35. Anderson DA, Ross BC. 35.  1990. Morphogenesis of hepatitis A virus: isolation and characterization of subviral particles. J. Virol. 64:5284–89 [Google Scholar]
  36. Probst C, Jecht M, Gauss-Muller V. 36.  1999. Intrinsic signals for the assembly of hepatitis A virus particles: role of structural proteins VP4 and 2A. J. Biol. Chem. 274:4527–31 [Google Scholar]
  37. Cohen L, Benichou D, Martin A. 37.  2002. Analysis of deletion mutants indicates that the 2A polypeptide of hepatitis A virus participates in virion morphogenesis. J. Virol. 76:7495–505 [Google Scholar]
  38. Graff J, Richards OC, Swiderek KM, Davis MT, Rusnak F. 38.  et al. 1999. Hepatitis A virus capsid protein VP1 has a heterogeneous C terminus. J. Virol. 73:6015–23 [Google Scholar]
  39. Martin A, Benichou D, Chao SF, Cohen LM, Lemon SM. 39.  1999. Maturation of the hepatitis A virus capsid protein VP1 is not dependent on processing by the 3Cpro proteinase. J. Virol. 73:6220–27 [Google Scholar]
  40. Morace G, Kusov Y, Dzagurov G, Beneduce F, Gauss-Muller V. 40.  2008. The unique role of domain 2A of the hepatitis A virus precursor polypeptide P1-2A in viral morphogenesis. BMB Rep. 41:678–83 [Google Scholar]
  41. Binn LN, Lemon SM, Marchwicki RH, Redfield RR, Gates NL, Bancroft WH. 41.  1984. Primary isolation and serial passage of hepatitis A virus strains in primate cell cultures. J. Clin. Microbiol. 20:28–33 [Google Scholar]
  42. Emerson SU, Huang YK, Purcell RH. 42.  1993. 2B and 2C mutations are essential but mutations throughout the genome of HAV contribute to adaptation to cell culture. Virology 194:475–80 [Google Scholar]
  43. Funkhouser AW, Schultz DE, Lemon SM, Purcell RH, Emerson SU. 43.  1999. Hepatitis A virus translation is rate-limiting for virus replication in MRC-5 cells. Virology 254:268–78 [Google Scholar]
  44. Gosert R, Egger D, Bienz K. 44.  2000. A cytopathic and a cell culture adapted hepatitis A virus strain differ in cell killing but not in intracellular membrane rearrangements. Virology 266:157–69 [Google Scholar]
  45. Kulka M, Chen A, Ngo D, Bhattacharya SS, Cebula TA, Goswami BB. 45.  2003. The cytopathic 18f strain of hepatitis A virus induces RNA degradation in FrhK4 cells. Arch. Virol. 148:1275–300 [Google Scholar]
  46. Lanford RE, Feng Z, Chavez D, Guerra B, Brasky KM. 46.  et al. 2011. Acute hepatitis A virus infection is associated with a limited type I interferon response and persistence of intrahepatic viral RNA. Proc. Natl. Acad. Sci. USA 108:11223–28 [Google Scholar]
  47. Jansen RW, Newbold JE, Lemon SM. 47.  1988. Complete nucleotide sequence of a cell culture–adapted variant of hepatitis A virus: comparison with wild-type virus with restricted capacity for in vitro replication. Virology 163:299–307 [Google Scholar]
  48. Lemon SM, Binn LN. 48.  1985. Incomplete neutralization of hepatitis A virus in vitro due to lipid-associated virions. J. Gen. Virol. 66:2501–5 [Google Scholar]
  49. Provost PJ, Wolanski BS, Miller WJ, Ittensohn OL, McAleer WJ, Hilleman MR. 49.  1975. Physical, chemical and morphologic dimensions of human hepatitis A virus strain CR326 (38578). Proc. Soc. Exp. Biol. Med. 148:532–39 [Google Scholar]
  50. Zhadina M, Bieniasz PD. 50.  2010. Functional interchangeability of late domains, late domain cofactors and ubiquitin in viral budding. PLoS Pathog. 6:e1001153 [Google Scholar]
  51. Dores MR, Chen B, Lin H, Soh UJ, Paing MM. 51.  et al. 2012. ALIX binds a YPX3L motif of the GPCR PAR1 and mediates ubiquitin-independent ESCRT-III/MVB sorting. J. Cell Biol. 197:407–19 [Google Scholar]
  52. Fujii K, Hurley JH, Freed EO. 52.  2007. Beyond Tsg101: the role of Alix in “ESCRTing” HIV-1. Nat. Rev. Microbiol. 5:912–16 [Google Scholar]
  53. Sette P, Mu R, Dussupt V, Jiang J, Snyder G. 53.  et al. 2011. The Phe105 loop of Alix Bro1 domain plays a key role in HIV-1 release. Structure 19:1485–95 [Google Scholar]
  54. Taylor MP, Burgon TB, Kirkegaard K, Jackson WT. 54.  2009. Role of microtubules in extracellular release of poliovirus. J. Virol. 83:6599–609 [Google Scholar]
  55. Asher LVS, Binn LN, Mensing TL, Marchwicki RH, Vassell RA, Young GD. 55.  1995. Pathogenesis of hepatitis A in orally inoculated owl monkeys (Aotus trivergatus). J. Med. Virol. 47:260–68 [Google Scholar]
  56. Schulman AN, Dienstag JL, Jackson DR, Hoofnagle JH, Gerety RJ. 56.  et al. 1976. Hepatitis A antigen particles in liver, bile, and stool of chimpanzees. J. Infect. Dis. 134:80–84 [Google Scholar]
  57. Mercer DF, Schiller DE, Elliott JF, Douglas DN, Hao C. 57.  et al. 2001. Hepatitis C virus replication in mice with chimeric human livers. Nat. Med. 7:927–33 [Google Scholar]
  58. Treyer A, Musch A. 58.  2013. Hepatocyte polarity. Compr. Physiol. 3:243–87 [Google Scholar]
  59. Crawford JM. 59.  1996. Role of vesicle-mediated transport pathways in hepatocellular bile secretion. Semin. Liver Dis. 16:169–89 [Google Scholar]
  60. Boyer JL. 60.  2013. Bile formation and secretion. Compr. Physiol. 3:1035–78 [Google Scholar]
  61. Lemon SM, Binn LN, Marchwicki R, Murphy PC, Ping LH. 61.  et al. 1990. In vivo replication and reversion to wild-type of a neutralization-resistant variant of hepatitis A virus. J. Infect. Dis. 161:7–13 [Google Scholar]
  62. Kaplan G, Totsuka A, Thompson P, Akatsuka T, Moritsugu Y, Feinstone SM. 62.  1996. Identification of a surface glycoprotein on African green monkey kidney cells as a receptor for hepatitis A virus. EMBO J. 15:4282–96 [Google Scholar]
  63. Balasubramanian S, Kota SK, Kuchroo VK, Humphreys BD, Strom TB. 63.  2012. TIM family proteins promote the lysosomal degradation of the nuclear receptor NUR77. Sci. Signal. 5:ra90 [Google Scholar]
  64. Kolter T, Sandhoff K. 64.  2010. Lysosomal degradation of membrane lipids. FEBS Lett. 584:1700–12 [Google Scholar]
  65. Emerson SU, Purcell RH. 65.  2003. Hepatitis E virus. Rev. Med. Virol. 13:145–54 [Google Scholar]
  66. Dalton HR, Bendall R, Ijaz S, Banks M. 66.  2008. Hepatitis E: an emerging infection in developed countries. Lancet Infect. Dis. 8:698–709 [Google Scholar]
  67. Mansuy JM, Peron JM, Abravanel F, Poirson H, Dubois M. 67.  et al. 2004. Hepatitis E in the south west of France in individuals who have never visited an endemic area. J. Med. Virol. 74:419–24 [Google Scholar]
  68. Ijaz S, Arnold E, Banks M, Bendall RP, Cramp ME. 68.  et al. 2005. Non-travel-associated hepatitis E in England and Wales: demographic, clinical, and molecular epidemiological characteristics. J. Infect. Dis. 192:1166–72 [Google Scholar]
  69. Purcell RH, Emerson SU. 69.  2008. Hepatitis E: an emerging awareness of an old disease. J. Hepatol. 48:494–503 [Google Scholar]
  70. Dalton HR, Bendall RP, Keane FE, Tedder RS, Ijaz S. 70.  2009. Persistent carriage of hepatitis E virus in patients with HIV infection. N. Engl. J. Med. 361:1025–27 [Google Scholar]
  71. Tam AW, Smith MM, Guerra ME, Huang CC, Bradley DW. 71.  et al. 1991. Hepatitis E virus (HEV): molecular cloning and sequencing of the full-length viral genome. Virology 185:120–31 [Google Scholar]
  72. Yamada K, Takahashi M, Hoshino Y, Takahashi H, Ichiyama K. 72.  et al. 2009. ORF3 protein of hepatitis E virus is essential for virion release from infected cells. J. Gen. Virol. 90:1880–91 [Google Scholar]
  73. Bradley D, Andjaparidze A, Cook EH Jr, McCaustland K, Balayan M. 73.  et al. 1988. Aetiological agent of enterically transmitted non-A, non-B hepatitis. J. Gen. Virol. 69:731–38 [Google Scholar]
  74. Koonin EV, Dolja VV. 74.  1993. Evolution and taxonomy of positive-strand RNA viruses: implications of comparative analysis of amino acid sequences. Crit. Rev. Biochem. Mol. Biol. 28:375–430 [Google Scholar]
  75. Yamashita T, Mori Y, Miyazaki N, Cheng RH, Yoshimura M. 75.  et al. 2009. Biological and immunological characteristics of hepatitis E virus-like particles based on the crystal structure. Proc. Natl. Acad. Sci. USA 106:12986–91 [Google Scholar]
  76. Graff J, Zhou YH, Torian U, Nguyen H, St Claire M. 76.  et al. 2008. Mutations within potential glycosylation sites in the capsid protein of hepatitis E virus prevent the formation of infectious virus particles. J. Virol. 82:1185–94 [Google Scholar]
  77. Takahashi M, Yamada K, Hoshino Y, Takahashi H, Ichiyama K. 77.  et al. 2008. Monoclonal antibodies raised against the ORF3 protein of hepatitis E virus (HEV) can capture HEV particles in culture supernatant and serum but not those in feces. Arch. Virol. 153:1703–13 [Google Scholar]
  78. Okamoto H. 78.  2013. Culture systems for hepatitis E virus. J. Gastroenterol. 48:147–58 [Google Scholar]
  79. Takahashi M, Hoshino Y, Tanaka T, Takahashi H, Nishizawa T, Okamoto H. 79.  2008. Production of monoclonal antibodies against hepatitis E virus capsid protein and evaluation of their neutralizing activity in a cell culture system. Arch. Virol. 153:657–66 [Google Scholar]
  80. Tyagi S, Korkaya H, Zafrullah M, Jameel S, Lal SK. 80.  2002. The phosphorylated form of the ORF3 protein of hepatitis E virus interacts with its non-glycosylated form of the major capsid protein, ORF2. J. Biol. Chem. 277:22759–67 [Google Scholar]
  81. Nagashima S, Takahashi M, Jirintai, Tanaka T, Yamada K. 81.  et al. 2011. A PSAP motif in the ORF3 protein of hepatitis E virus is necessary for virion release from infected cells. J. Gen. Virol. 92:269–78 [Google Scholar]
  82. Nagashima S, Takahashi M, Jirintai S, Tanaka T, Nishizawa T. 82.  et al. 2011. Tumour susceptibility gene 101 and the vacuolar protein sorting pathway are required for the release of hepatitis E virions. J. Gen. Virol. 92:2838–48 [Google Scholar]
  83. Nagashima S, Takahashi M, Jirintai S, Tanggis, Kobayashi T. 83.  et al. 2013. The membrane on the surface of hepatitis E virus particles is derived from the intracellular membrane and contains trans-Golgi network protein 2. Arch. Virol. 159:979–91 [Google Scholar]
  84. Zafrullah M, Ozdener MH, Kumar R, Panda SK, Jameel S. 84.  1999. Mutational analysis of glycosylation, membrane translocation, and cell surface expression of the hepatitis E virus ORF2 protein. J. Virol. 73:4074–82 [Google Scholar]
  85. Lemon SM, Murphy PC, Provost PJ, Chalikonda I, Davide JP. 85.  et al. 1997. Immunoprecipitation and virus neutralization assays demonstrate qualitative differences between protective antibody responses to inactivated hepatitis A vaccine and passive immunization with immune globulin. J. Infect. Dis. 176:9–19 [Google Scholar]
  86. Victor JC, Monto AS, Surdina TY, Suleimenova SZ, Vaughan G. 86.  et al. 2007. Hepatitis A vaccine versus immune globulin for postexposure prophylaxis. N. Engl. J. Med. 357:1685–94 [Google Scholar]
  87. Kosugi I, Muro H, Shirasawa H, Ito I. 87.  1992. Endocytosis of soluble IgG immune complex and its transport to lysosomes in hepatic sinusoidal endothelial cells. J. Hepatol. 16:106–14 [Google Scholar]
  88. Tans C, Dubois F, Zhong ZD, Jadot M, Wattiaux R, Wattiaux-De Coninck S. 88.  1994. Uptake by rat liver of bovine growth hormone free or bound to a monoclonal antibody. Biol. Cell 82:45–49 [Google Scholar]
  89. Schilling R, Ijaz S, Davidoff M, Lee JY, Locarnini S. 89.  et al. 2003. Endocytosis of hepatitis B immune globulin into hepatocytes inhibits the secretion of hepatitis B virus surface antigen and virions. J. Virol. 77:8882–92 [Google Scholar]
  90. Junghans RP, Anderson CL. 90.  1996. The protection receptor for IgG catabolism is the β2-microglobulin-containing neonatal intestinal transport receptor. Proc. Natl. Acad. Sci. USA 93:5512–16 [Google Scholar]
  91. Tomana M, Kulhavy R, Mestecky J. 91.  1988. Receptor-mediated binding and uptake of immunoglobulin A by human liver. Gastroenterology 94:762–70 [Google Scholar]
  92. Bai Y, Ye L, Tesar DB, Song H, Zhao D. 92.  et al. 2011. Intracellular neutralization of viral infection in polarized epithelial cells by neonatal Fc receptor (FcRn)-mediated IgG transport. Proc. Natl. Acad. Sci. USA 108:18406–11 [Google Scholar]
  93. Mitrenga D, Arnold W, Muller O, Mayersbach HV. 93.  1975. The fate of injected human IgG in the mouse liver: uptake, immunological inactivation, and lysosomal reactions. Cell Tissue Res. 156:359–76 [Google Scholar]
  94. Mallery DL, McEwan WA, Bidgood SR, Towers GJ, Johnson CM, James LC. 94.  2010. Antibodies mediate intracellular immunity through tripartite motif–containing 21 (TRIM21). Proc. Natl. Acad. Sci. USA 107:19985–90 [Google Scholar]
  95. Strauss M, Levy H, Bostina M, Filman DJ, Hogle JM. 95.  2013. RNA transfer from poliovirus 135S particles across membranes is mediated by long umbilical connectors. J. Virol. 87:3903–14 [Google Scholar]
  96. Icenogle J, Shiwen H, Duke G, Gilbert S, Rueckert R, Anderegg J. 96.  1983. Neutralization of poliovirus by a monoclonal antibody: kinetics and stoichiometry. Virology 127:412–25 [Google Scholar]
  97. Schotte L, Strauss M, Thys B, Halewyck H, Filman DJ. 97.  et al. 2014. Mechanism of action and capsid stabilizing properties of VHHs with an in vitro anti-polioviral activity. J. Virol. 884403–13
  98. Zhou Y, Callendret B, Xu D, Brasky KM, Feng Z. 98.  et al. 2012. Dominance of the CD4+ T helper cell response during acute resolving hepatitis A virus infection. J. Exp. Med. 209:1481–92 [Google Scholar]
  99. Clayson ET, Jones-Brando LV, Compans RW. 99.  1989. Release of simian virus 40 virions from epithelial cells is polarized and occurs without cell lysis. J. Virol. 63:2278–88 [Google Scholar]
  100. Bar S, Rommelaere J, Nuesch JP. 100.  2013. Vesicular transport of progeny parvovirus particles through ER and Golgi regulates maturation and cytolysis. PLoS Pathog. 9:e1003605 [Google Scholar]
  101. King AMQ, Adams MJ, Carstens EB, Lefkowitz EJ. 101.  2012. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses Oxford, UK: Academic
  102. Marvil P, Knowles NJ, Mockett AP, Britton P, Brown TD, Cavanagh D. 102.  1999. Avian encephalomyelitis virus is a picornavirus and is most closely related to hepatitis A virus. J. Gen. Virol. 80:653–62 [Google Scholar]
  103. Tannock GA, Shafren DR. 103.  1994. Avian encephalomyelitis: a review. Avian Pathol. 23:603–20 [Google Scholar]
  104. Kapsenberg JG, Ras A, Korte J. 104.  1979. Improvement of enterovirus neutralization by treatment with sodium deoxycholate or chloroform. Intervirology 12:329–34 [Google Scholar]
  105. Blackwell JH, Wool S, Kosikowski FV. 105.  1981. Vesicular exocytosis of foot-and-mouth disease virus from mammary gland secretory epithelium of infected cows. J. Gen. Virol. 56:207–12 [Google Scholar]
  106. Inal JM, Jorfi S. 106.  2013. Coxsackievirus B transmission and possible new roles for extracellular vesicles. Biochem. Soc. Trans. 41:299–302 [Google Scholar]
  107. Patel A, Roy P. 107.  2013. The molecular biology of bluetongue virus replication. Virus. Res. 182:5–20 [Google Scholar]
  108. Hyatt AD, Eaton BT, Brookes SM. 108.  1989. The release of bluetongue virus from infected cells and their superinfection by progeny virus. Virology 173:21–34 [Google Scholar]
  109. Wirblich C, Bhattacharya B, Roy P. 109.  2006. Nonstructural protein 3 of bluetongue virus assists virus release by recruiting ESCRT-I protein Tsg101. J. Virol. 80:460–73 [Google Scholar]
  110. Celma CC, Roy P. 110.  2009. A viral nonstructural protein regulates bluetongue virus trafficking and release. J. Virol. 83:6806–16 [Google Scholar]
  111. Bhattacharya B, Roy P. 111.  2013. Cellular phosphoinositides and the maturation of bluetongue virus, a non-enveloped capsid virus. Virol. J. 10:73 [Google Scholar]
  112. Stoltz D, Makkay A. 112.  2000. Co-replication of a reovirus and a polydnavirus in the ichneumonid parasitoid Hyposoter exiguae. Virology 278:266–75 [Google Scholar]
/content/journals/10.1146/annurev-virology-031413-085359
Loading
/content/journals/10.1146/annurev-virology-031413-085359
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