1887

Abstract

A long-standing paradigm in virology was that non-enveloped viruses induce cell lysis to release progeny virions. However, emerging evidence indicates that some non-enveloped viruses exit cells without inducing cell lysis, while others engage both lytic and non-lytic egress mechanisms. Enteric viruses are transmitted via the faecal–oral route and are important causes of a wide range of human infections, both gastrointestinal and extra-intestinal. Virus cellular egress, when fully understood, may be a relevant target for antiviral therapies, which could minimize the public health impact of these infections. In this review, we outline lytic and non-lytic cell egress mechanisms of non-enveloped enteric RNA viruses belonging to five families: , , , and . We discuss factors that contribute to egress mechanisms and the relevance of these mechanisms to virion stability, infectivity and transmission. Since most data were obtained in traditional two-dimensional cell cultures, we will further attempt to place them into the context of polarized cultures and pathogenesis. Throughout the review, we highlight numerous knowledge gaps to stimulate future research into the egress mechanisms of these highly prevalent but largely understudied viruses.

Funding
This study was supported by the:
  • ChristianeE. Wobus , University of Michigan Biological Sciences Scholars Program
  • IreneA. Owusu , Michigan Infectious Disease International Scholars fellowship
  • IreneA. Owusu , University of Ghana-Carnegie BaNGA-Africa Project fellowship
  • IreneA. Owusu , DELTAS Africa grant , (Award DEL-15-007)
  • ChristianeE. Wobus , National Institutes of Health , (Award AI130328)
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2021-02-09
2021-02-26
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References

  1. Ma Y, Zhang Y, Liang X, Lou F, Oglesbee M et al. Origin, evolution, and virulence of porcine deltacoronaviruses in the United States. mBio 2015; 6: 1 13 [CrossRef] [PubMed]
    [Google Scholar]
  2. Zhu L, Mou C, Yang X, Lin J, Yang Q. Mitophagy in TGEV infection counteracts oxidative stress and apoptosis. Oncotarget 2016; 7: 27122 27141 [CrossRef] [PubMed]
    [Google Scholar]
  3. Blank CA, Anderson DA, Beard M, Lemon SM. Infection of polarized cultures of human intestinal epithelial cells with hepatitis A virus: vectorial release of progeny virions through apical cellular membranes. J Virol 2000; 74: 6476 6484 [CrossRef] [PubMed]
    [Google Scholar]
  4. Evans GL, Caller LG, Foster V, Crump CM. Anion homeostasis is important for non-lytic release of BK polyomavirus from infected cells. Open Biol 2015; 5: [CrossRef] [PubMed]
    [Google Scholar]
  5. González-López O, Rivera-Serrano EE, Hu F, Hensley L, McKnight KL et al. Redundant late domain functions of tandem VP2 YPX 3 L motifs in nonlytic cellular egress of Quasi-enveloped hepatitis A virus. J Virol 2018; 92: 1 16
    [Google Scholar]
  6. McKnight KL, Xie L, González-López O, Rivera-Serrano EE, Chen X et al. Protein composition of the hepatitis A virus quasi-envelope. Proc Natl Acad Sci U S A 2017; 114: 6587 6592 [CrossRef] [PubMed]
    [Google Scholar]
  7. Feng Z, Hirai-Yuki A, McKnight KL, Lemon SM. Naked Viruses That Aren't Always Naked: Quasi-Enveloped Agents of Acute Hepatitis. Annu Rev Virol 2014; 1: 539 560 [CrossRef] [PubMed]
    [Google Scholar]
  8. Mao L, Wu J, Shen L, Yang J, Chen J et al. Enterovirus 71 transmission by exosomes establishes a productive infection in human neuroblastoma cells. Virus Genes 2016; 52: 189 194 [CrossRef] [PubMed]
    [Google Scholar]
  9. Chapuy-Regaud S, Dubois M, Plisson-Chastang C, Bonnefois T, Lhomme S et al. Characterization of the lipid envelope of exosome encapsulated HEV particles protected from the immune response. Biochimie 2017; 141: 70 79 [CrossRef] [PubMed]
    [Google Scholar]
  10. Santiana M, Ghosh S, Ho BA, Rajasekaran V, Du W-L et al. Vesicle-Cloaked virus clusters are optimal units for Inter-organismal viral transmission. Cell Host Microbe 2018; 24: 208 220 [CrossRef] [PubMed]
    [Google Scholar]
  11. Ahmed SM, Hall AJ, Robinson AE, Verhoef L, Premkumar P et al. Global prevalence of norovirus in cases of gastroenteritis: a systematic review and meta-analysis. Lancet Infect Dis 2014; 14: 725 730 [CrossRef] [PubMed]
    [Google Scholar]
  12. Centers for Disease Control and Prevention Viral Meningitis [Internet]. cdc.gov. 2019
  13. Centers for Disease Control and Prevention Non-Polio Enterovirus: Enterovirus 71 [Internet]. cdc.gov. 2018
  14. Logan SAE, MacMahon E. Viral meningitis. BMJ 2008; 336: 36 40 [CrossRef] [PubMed]
    [Google Scholar]
  15. Edinger AL, Thompson CB. Death by design: apoptosis, necrosis and autophagy. Curr Opin Cell Biol 2004; 16: 663 669 [CrossRef] [PubMed]
    [Google Scholar]
  16. Lemasters JJ. Molecular mechanisms of cell death. In: Molecular Pathology: The Molecular Basis of Human Disease 2018
    [Google Scholar]
  17. D'Arcy MS, D’Arcy MS. Cell death: a review of the major forms of apoptosis, necrosis and autophagy. Cell Biol Int 2019; 43: 582 592 [CrossRef] [PubMed]
    [Google Scholar]
  18. Zong WX, Thompson CB. Necrotic death as a cell fate. Genes Dev 2006; 20: 1 15 [CrossRef] [PubMed]
    [Google Scholar]
  19. Bird SW, Maynard ND, Covert MW, Kirkegaard K. Nonlytic viral spread enhanced by autophagy components. Proc Natl Acad Sci U S A 2014; 111: 13081 13086 [CrossRef] [PubMed]
    [Google Scholar]
  20. Taylor MP, Jackson WT. Viruses and arrested autophagosome development. Autophagy 2009; 5: 870 871 [CrossRef] [PubMed]
    [Google Scholar]
  21. Jackson WT, Giddings TH, Taylor MP, Mulinyawe S, Rabinovitch M, Kopito RR et al. Subversion of cellular autophagosomal machinery by RNA viruses. PLoS Biol 2005; 3: e156 [CrossRef] [PubMed]
    [Google Scholar]
  22. Wong HH, Sanyal S. Manipulation of autophagy by (+) RNA viruses. Semin Cell Dev Biol 2020; 101: 3 11 [CrossRef] [PubMed]
    [Google Scholar]
  23. Cregan SP, Dawson VL, Slack RS. Role of AIF in caspase-dependent and caspase-independent cell death. Oncogene 2004; 23: 2785 2796 [CrossRef] [PubMed]
    [Google Scholar]
  24. Cong H, Du N, Yang Y, Song L, Zhang W et al. Enterovirus 71 2B induces cell apoptosis by directly inducing the conformational activation of the proapoptotic protein Bax. J Virol 2016; 90: 9862 9878 [CrossRef] [PubMed]
    [Google Scholar]
  25. van Kuppeveld FJ, Hoenderop JG, Smeets RL, Willems PH, Dijkman HB et al. Coxsackievirus protein 2B modifies endoplasmic reticulum membrane and plasma membrane permeability and facilitates virus release. Embo J 1997; 16: 3519 3532 [CrossRef] [PubMed]
    [Google Scholar]
  26. Barco A, Feduchi E, Carrasco L. Poliovirus protease 3C(pro) kills cells by apoptosis. Virology 2000; 266: 352 360 [CrossRef] [PubMed]
    [Google Scholar]
  27. Chau DHW, Yuan J, Zhang H, Cheung P, Lim T et al. Coxsackievirus B3 proteases 2A and 3C induce apoptotic cell death through mitochondrial injury and cleavage of eIF4GI but not DAP5/p97/NAT1. Apoptosis 2007; 12: 513 524 [CrossRef] [PubMed]
    [Google Scholar]
  28. Li M-L, Hsu T-A, Chen T-C, Chang S-C, Lee J-C et al. The 3C protease activity of enterovirus 71 induces human neural cell apoptosis. Virology 2002; 293: 386 395 [CrossRef] [PubMed]
    [Google Scholar]
  29. Li X, Li Z, Zhou W, Xing X, Huang L et al. Overexpression of 4EBP1, p70S6K, Akt1 or Akt2 differentially promotes coxsackievirus B3-induced apoptosis in HeLa cells. Cell Death Dis 2013; 4: 1 15 [CrossRef] [PubMed]
    [Google Scholar]
  30. Xin L, Xiao Z, Ma X, He F, Yao H et al. Coxsackievirus B3 induces crosstalk between autophagy and apoptosis to benefit its release after replicating in autophagosomes through a mechanism involving caspase cleavage of autophagy-related proteins. Infect Genet Evol 2014; 26: 95 102 [CrossRef] [PubMed]
    [Google Scholar]
  31. Lai Y, Zeng N, Wang M, Cheng A, Yang Q et al. The VP3 protein of duck hepatitis A virus mediates host cell adsorption and apoptosis. Sci Rep 2019; 9: 1 12 [CrossRef] [PubMed]
    [Google Scholar]
  32. López-Guerrero JA, Alonso M, Martín-Belmonte F, Carrasco L. Poliovirus induces apoptosis in the human U937 promonocytic cell line. Virology 2000; 272: 250 256 [CrossRef] [PubMed]
    [Google Scholar]
  33. Liang CC, Sun MJ, Lei HY, Chen SH, Yu C-K et al. Human endothelial cell activation and apoptosis induced by enterovirus 71 infection. J Med Virol 2004; 74: 597 603 [CrossRef] [PubMed]
    [Google Scholar]
  34. Goswami BB, Kulka M, Ngo D, Cebula TA. Apoptosis induced by a cytopathic hepatitis A virus is dependent on caspase activation following ribosomal RNA degradation but occurs in the absence of 2'-5' oligoadenylate synthetase. Antiviral Res 2004; 63: 153 166 [CrossRef] [PubMed]
    [Google Scholar]
  35. Girard S, Couderc T, Destombes J, Thiesson D, Delpeyroux F et al. Poliovirus induces apoptosis in the mouse central nervous system. J Virol 1999; 73: 6066 6072 [CrossRef] [PubMed]
    [Google Scholar]
  36. Choudhary A, Sharma S, Sankhyan N, Gulati S, Kalra V et al. Midbrain and spinal cord magnetic resonance imaging (MRI) changes in poliomyelitis. J Child Neurol 2010; 25: 497 499 [CrossRef] [PubMed]
    [Google Scholar]
  37. Hogue B, Mcallister R, Greene AE. The effect of poliomyelit is virus on human brain cells in tissue culture (From the Departments of Anatomy and Pediatrics, School o / Medicine Philaddphia University of Pennsylvania. 1955
  38. Madan V, Castelló A, Carrasco L. Viroporins from RNA viruses induce caspase-dependent apoptosis. Cell Microbiol 2008; 10: 437 451 [CrossRef] [PubMed]
    [Google Scholar]
  39. Clarke P, Meintzer SM, Wang Y, Moffitt LA, Richardson-Burns SM et al. Jnk regulates the release of proapoptotic mitochondrial factors in reovirus-infected cells. J Virol 2004; 78: 13132 13138 [CrossRef] [PubMed]
    [Google Scholar]
  40. Kominsky DJ, Bickel RJ, Tyler KL. Reovirus-Induced apoptosis requires both death receptor- and mitochondrial-mediated caspase-dependent pathways of cell death. Cell Death Differ 2002; 9: 926 933 [CrossRef] [PubMed]
    [Google Scholar]
  41. Kominsky DJ, Bickel RJ, Tyler KL. Reovirus-Induced apoptosis requires mitochondrial release of Smac/DIABLO and involves reduction of cellular inhibitor of apoptosis protein levels. J Virol 2002; 76: 11414 11424 [CrossRef] [PubMed]
    [Google Scholar]
  42. Connolly JL, Rodgers SE, Clarke P, Ballard DW, Kerr LD et al. Reovirus-Induced apoptosis requires activation of transcription factor NF-κB. J Virol 2000; 74: 2981 2989 [CrossRef]
    [Google Scholar]
  43. Donnell SMO, Hansberger MW, Connolly JL, Chappell JD, Watson MJ et al. Organ-Specific roles for transcription factor NF- κ B in reovirus-induced apoptosis and disease. 2005; 115 2341 2350
  44. Hansberger MW, Campbell JA, Danthi P, Arrate P, Pennington KN et al. Iκb kinase subunits α and γ are required for activation of NF-κB and induction of apoptosis by mammalian reovirus. J Virol 2007; 81: 1360 1371 [CrossRef]
    [Google Scholar]
  45. Smakman N, van den Wollenberg DJM, Borel Rinkes IHM, Hoeben RC, Kranenburg O. Sensitization to apoptosis underlies KrasD12-dependent oncolysis of murine C26 colorectal carcinoma cells by reovirus T3D. J Virol 2005; 79: 14981 14985 [CrossRef] [PubMed]
    [Google Scholar]
  46. Smakman N, van den Wollenberg DJM, Elias SG, Sasazuki T, Shirasawa S et al. KRAS(D13) Promotes apoptosis of human colorectal tumor cells by ReovirusT3D and oxaliplatin but not by tumor necrosis factor-related apoptosis-inducing ligand. Cancer Res 2006; 66: 5403 5408 [CrossRef] [PubMed]
    [Google Scholar]
  47. Strong JE, Coffey MC, Tang D, Sabinin P, Lee PW. The molecular basis of viral oncolysis: usurpation of the Ras signaling pathway by reovirus. Embo J 1998; 17: 3351 3362 [CrossRef] [PubMed]
    [Google Scholar]
  48. Garant KA, Shmulevitz M, Pan L, Daigle RM, Ahn DG et al. Oncolytic reovirus induces intracellular redistribution of Ras to promote apoptosis and progeny virus release. Oncogene 2016; 35: 771 782 [CrossRef] [PubMed]
    [Google Scholar]
  49. Clarke P, Goody R, Hoyt CC, Tyler KL. Mechanisms of reovirus-induced cell death and tissue host-cell signaling and transcription factor activation. Viral Immunol 2005; 18: 89 115
    [Google Scholar]
  50. Hoyt CC, Richardson-Burns SM, Goody RJ, Robinson BA, Debiasi RL et al. Nonstructural protein sigma1s is a determinant of reovirus virulence and influences the kinetics and severity of apoptosis induction in the heart and central nervous system. J Virol 2005; 79: 2743 2753 [CrossRef] [PubMed]
    [Google Scholar]
  51. Hoyt CC, Bouchard RJ, Tyler KL. Novel nuclear herniations induced by nuclear localization of a viral protein. J Virol 2004; 78: 6360 6369 [CrossRef] [PubMed]
    [Google Scholar]
  52. Lammerding J, Stewart CL, Lee RT, Lammerding J, Schulze PC et al. Lamin A / C deficiency causes defective nuclear mechanics and mechanotransduction Find the latest version : Lamin A / C deficiency causes defective nuclear mechanics. J Clin Invest 2004; 113: 370 378
    [Google Scholar]
  53. Poggioli GJ, Dermody TS, Tyler KL. Reovirus-induced sigma1s-dependent G(2)/M phase cell cycle arrest is associated with inhibition of p34(cdc2). J Virol 2001; 75: 7429 7434 [CrossRef] [PubMed]
    [Google Scholar]
  54. Boehme KW, Hammer K, Tollefson WC, Konopka-Anstadt JL, Kobayashi T et al. Nonstructural protein σ1s mediates reovirus-induced cell cycle arrest and apoptosis. J Virol 2013; 87: 12967 12979 [CrossRef] [PubMed]
    [Google Scholar]
  55. Becker EBE, Bonni A. Cell cycle regulation of neuronal apoptosis in development and disease. Prog Neurobiol 2004; 72: 1 25 [CrossRef] [PubMed]
    [Google Scholar]
  56. Brown JJ, Short SP, Stencel-Baerenwald J, Urbanek K, Pruijssers AJ et al. Reovirus-Induced apoptosis in the intestine limits establishment of enteric infection. J Virol 2018; 92: 1 17 [CrossRef] [PubMed]
    [Google Scholar]
  57. Chaïbi C, Cotte-Laffitte J, Sandré C, Esclatine A, Servin AL et al. Rotavirus induces apoptosis in fully differentiated human intestinal Caco-2 cells. Virology 2005; 332: 480 490 [CrossRef] [PubMed]
    [Google Scholar]
  58. Superti F, Ammendolia MG, Tinari A, Bucci B, Giammarioli AM et al. Induction of apoptosis in HT-29 cells infected with SA-11 rotavirus. 1996; 334 325 334
  59. Halasz P, Holloway G, Coulson BS. Death mechanisms in epithelial cells following rotavirus infection, exposure to inactivated rotavirus or genome transfection. J Gen Virol 2010; 91: 2007 2018 [CrossRef] [PubMed]
    [Google Scholar]
  60. Martin-Latil S, Mousson L, Autret A, Colbère-Garapin F, Blondel B. Bax is activated during rotavirus-induced apoptosis through the mitochondrial pathway. J Virol 2007; 81: 4457 4464 [CrossRef] [PubMed]
    [Google Scholar]
  61. Bautista D, Rodríguez LS, Franco MA, Angel J, Barreto A. Caco-2 cells infected with rotavirus release extracellular vesicles that express markers of apoptotic bodies and exosomes. Cell Stress Chaperones 2015; 20: 697 708 [CrossRef] [PubMed]
    [Google Scholar]
  62. Bhowmick R, Halder UC, Chattopadhyay S, Chanda S, Nandi S et al. Rotaviral enterotoxin nonstructural protein 4 targets mitochondria for activation of apoptosis during infection. J Biol Chem 2012; 287: 35004 35020 [CrossRef] [PubMed]
    [Google Scholar]
  63. Chang-Graham AL, Perry JL, Strtak AC, Ramachandran NK, Criglar JM et al. Rotavirus calcium dysregulation manifests as dynamic calcium signaling in the cytoplasm and endoplasmic reticulum. Sci Rep 2019; 9: 1 20 [CrossRef] [PubMed]
    [Google Scholar]
  64. Boshuizen JA, Reimerink JHJ, Korteland-van Male AM, van Ham VJJ, Koopmans MPG et al. Changes in small intestinal homeostasis, morphology, and gene expression during rotavirus infection of infant mice. J Virol 2003; 77: 13005 13016 [CrossRef] [PubMed]
    [Google Scholar]
  65. Wobus CE, Karst SM, Thackray LB, Chang KO, Sosnovtsev SV et al. Replication of norovirus in cell culture reveals a tropism for dendritic cells and macrophages. PLoS Biol 2004; 2: e432 [CrossRef] [PubMed]
    [Google Scholar]
  66. Jones MK, Watanabe M, Zhu S, Graves CL, Keyes LR et al. Enteric bacteria promote human and mouse norovirus infection of B cells. Science 2014; 346: 755 759 [CrossRef] [PubMed]
    [Google Scholar]
  67. Bok K, Prikhodko VG, Green KY, Sosnovtsev SV. Apoptosis in murine norovirus-infected RAW264.7 cells is associated with downregulation of survivin. J Virol 2009; 83: 3647 3656 [CrossRef] [PubMed]
    [Google Scholar]
  68. Furman LM, Maaty WS, Petersen LK, Ettayebi K, Hardy ME et al. Cysteine protease activation and apoptosis in murine norovirus infection. Virol J 2009; 6: 1 11
    [Google Scholar]
  69. McFadden N, Bailey D, Carrara G, Benson A, Chaudhry Y et al. Norovirus regulation of the innate immune response and apoptosis occurs via the product of the alternative open reading frame 4. PLoS Pathog 2011; 7: e1002413 [CrossRef] [PubMed]
    [Google Scholar]
  70. Herod MR, Salim O, Skilton RJ, Prince CA, Ward VK et al. Expression of the murine norovirus (MNV) ORF1 polyprotein is sufficient to induce apoptosis in a virus-free cell model. PLoS One 2014; 9: 3 11
    [Google Scholar]
  71. Barrera-Vázquez OS, Cancio-Lonches C, Hernández-González O, Chávez-Munguia B, Villegas-Sepúlveda N et al. The feline calicivirus leader of the capsid protein causes survivin and XIAP downregulation and apoptosis. Virology 2019; 527: 146 158 [CrossRef] [PubMed]
    [Google Scholar]
  72. Robinson BA, Van Winkle JA, McCune BT, Peters AM, Nice TJ. Caspase-Mediated cleavage of murine norovirus nS1/2 potentiates apoptosis and is required for persistent infection of intestinal epithelial cells. PLoS Pathog 2019; 15: 1 29 [CrossRef] [PubMed]
    [Google Scholar]
  73. Lee S, Liu H, Wilen CB, Sychev ZE, Desai C et al. A secreted viral nonstructural protein determines intestinal norovirus pathogenesis. Cell Host Microbe 2019; 25: 845 857 [CrossRef] [PubMed]
    [Google Scholar]
  74. Troeger H, Loddenkemper C, Schneider T, Schreier E, Epple HJ et al. Structural and functional changes of the duodenum in human norovirus infection. Gut 2009; 58: 1070 1077 [CrossRef] [PubMed]
    [Google Scholar]
  75. Ettayebi K, Crawford SE, Murakami K, Broughman JR, Karandikar U et al. Replication of human noroviruses in stem cell-derived human enteroids. Science 2016; 353: 1387 1393 [CrossRef] [PubMed]
    [Google Scholar]
  76. Yang Y, Shi R, Soomro MH, Hu F, Du F et al. Hepatitis E virus induces hepatocyte apoptosis via mitochondrial pathway in Mongolian gerbils. Front Microbiol 2018; 9: 460 [CrossRef] [PubMed]
    [Google Scholar]
  77. Tian J, Shi R, Xiao P, Liu T, She R et al. Hepatitis E virus induces brain injury probably associated with mitochondrial apoptosis. Front Cell Infect Microbiol 2019; 9: 1 11
    [Google Scholar]
  78. Ripellino P, Pasi E, Melli G, Staedler C, Fraga M et al. Neurologic complications of acute hepatitis E virus infection. Neurol Neuroimmunol Neuroinflamm 2020; 7: [CrossRef] [PubMed]
    [Google Scholar]
  79. Kamar N, Bendall RP, Peron JM, Cintas P, Prudhomme L et al. Hepatitis E virus and neurologic disorders. Emerg Infect Dis 2011; 17: 173 179 [CrossRef] [PubMed]
    [Google Scholar]
  80. Lee TJ, Kim EJ, Kim S, Jung EM, Park JW et al. Caspase-Dependent and caspase-independent apoptosis induced by evodiamine in human leukemic U937 cells. Mol Cancer Ther 2006; 5: 2398 2407 [CrossRef] [PubMed]
    [Google Scholar]
  81. Wu M, Xu L-G, Li X, Zhai Z, Shu H-B. Amid, an apoptosis-inducing factor-homologous mitochondrion-associated protein, induces caspase-independent apoptosis. J Biol Chem 2002; 277: 25617 25623 [CrossRef] [PubMed]
    [Google Scholar]
  82. Tait SWG, Green DR. Caspase-Independent cell death: leaving the set without the final cut. Oncogene 2008; 27: 6452 6461 [CrossRef] [PubMed]
    [Google Scholar]
  83. Berg CP, Schlosser SF, Neukirchen DK, Papadakis C, Gregor M et al. Hepatitis C virus core protein induces apoptosis-like caspase independent cell death. Virol J 2009; 6: 1 13
    [Google Scholar]
  84. Kim Y, Lee C. Porcine epidemic diarrhea virus induces caspase-independent apoptosis through activation of mitochondrial apoptosis-inducing factor. Virology 2014; 460-461: 180 193 [CrossRef] [PubMed]
    [Google Scholar]
  85. Agol VI, Belov GA, Bienz K, Egger D, Kolesnikova MS et al. Two types of death of poliovirus-infected cells: caspase involvement in the apoptosis but not cytopathic effect. Virology 1998; 252: 343 353 [CrossRef] [PubMed]
    [Google Scholar]
  86. Yuan JP, Zhao W, Wang HT, Wu KY, Li T et al. Coxsackievirus B3-induced apoptosis and caspase-3. Cell Res 2003; 13: 203 209 [CrossRef] [PubMed]
    [Google Scholar]
  87. Proskuryakov SY, Gabai VL, Konoplyannikov AG. Necrosis is an active and controlled form of programmed cell death. Biochemistry 2002; 67: 387 408 [CrossRef] [PubMed]
    [Google Scholar]
  88. Bozym RA, Patel K, White C, Cheung KH, Bergelson JM et al. Calcium signals and calpain-dependent necrosis are essential for release of coxsackievirus B from polarized intestinal epithelial cells. Mol Biol Cell 2011; 22: 3010 3021 [CrossRef] [PubMed]
    [Google Scholar]
  89. Carocci M, Cordonnier N, Huet H, Romey A, Relmy A et al. Encephalomyocarditis virus 2A protein is required for viral pathogenesis and inhibition of apoptosis. J Virol 2011; 85: 10741 10754 [CrossRef] [PubMed]
    [Google Scholar]
  90. Romanova LI, Lidsky PV, Kolesnikova MS, Fominykh KV, Gmyl AP et al. Antiapoptotic activity of the cardiovirus leader protein, a viral "security" protein. J Virol 2009; 83: 7273 7284 [CrossRef] [PubMed]
    [Google Scholar]
  91. Castilho JG, Botelho MVJ, Lauretti F, Taniwaki N, Linhares REC et al. The in vitro cytopathology of a porcine and the simian (SA-11) strains of rotavirus. Mem Inst Oswaldo Cruz 2004; 99: 313 317 [CrossRef] [PubMed]
    [Google Scholar]
  92. Berger AK, Danthi P. Reovirus activates a caspase-independent cell death pathway. mBio 2013; 4: 1 10 [CrossRef] [PubMed]
    [Google Scholar]
  93. Tkach M, Théry C. Communication by extracellular vesicles: where we are and where we need to go. Cell 2016; 164: 1226 1232 [CrossRef] [PubMed]
    [Google Scholar]
  94. Colombo M, Raposo G, Théry C, Biogenesis TC. Biogenesis, secretion, and intercellular interactions of exosomes and other extracellular vesicles. Annu Rev Cell Dev Biol 2014; 30: 255 289 [CrossRef] [PubMed]
    [Google Scholar]
  95. Altan-Bonnet N, Perales C, Domingo E. Extracellular vesicles: vehicles of en bloc viral transmission. Virus Res 2019; 265: 143 149 [CrossRef] [PubMed]
    [Google Scholar]
  96. Muralidharan-Chari V, Clancy JW, Sedgwick A, D'Souza-Schorey C. Microvesicles: mediators of extracellular communication during cancer progression. J Cell Sci 2010; 123: 1603 1611 [CrossRef] [PubMed]
    [Google Scholar]
  97. Mutsafi Y, Altan-Bonnet N. Enterovirus transmission by secretory autophagy. Viruses 2018; 10: 1 8 [CrossRef] [PubMed]
    [Google Scholar]
  98. Ponpuak M, Mandell MA, Kimura T, Chauhan S, Cleyrat C et al. Secretory autophagy. Curr Opin Cell Biol 2015; 35: 106 116 [CrossRef] [PubMed]
    [Google Scholar]
  99. Barski G, Robineaux R, Endo M. Phase contrast cinematography of cellular lesion produced by poliomyelitis virus in vitro. Proc Soc Exp Biol Med 1955; 88: 57 59 [CrossRef] [PubMed]
    [Google Scholar]
  100. Dunnebacke TH, Levinthal JD, Williams RC. Entry and release of poliovirus as observed by electron microscopy of cultured cells. J Virol 1969; 4: 505 513 [CrossRef] [PubMed]
    [Google Scholar]
  101. Schlegel A, Giddings TH, Ladinsky MS, Kirkegaard K. Cellular origin and ultrastructure of membranes induced during poliovirus infection. J Virol 1996; 70: 6576 6588 [CrossRef] [PubMed]
    [Google Scholar]
  102. Chen YH, Du W, Hagemeijer MC, Takvorian PM, Pau C et al. Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses. Cell 2015; 160: 619 630 [CrossRef] [PubMed]
    [Google Scholar]
  103. Suhy DA, Giddings TH, Kirkegaard K. Remodeling the endoplasmic reticulum by poliovirus infection and by individual viral proteins: an autophagy-like origin for virus-induced vesicles. J Virol 2000; 74: 8953 8965 [CrossRef]
    [Google Scholar]
  104. Taylor MP, Burgon TB, Kirkegaard K, Jackson WT. Role of microtubules in extracellular release of poliovirus. J Virol 2009; 83: 6599 6609 [CrossRef] [PubMed]
    [Google Scholar]
  105. Richards AL, Jackson WT. Intracellular vesicle acidification promotes maturation of infectious poliovirus particles. PLoS Pathog 2012; 8: e1003046 [CrossRef] [PubMed]
    [Google Scholar]
  106. Sin J, Mcintyre L, Stotland A, Feuer R, Gottlieb A. Coxsackievirus B escapes the infected cell in ejected Mitophagosomes Jon. 2017; 91 1 16
  107. Robinson SM, Tsueng G, Sin J, Mangale V, Rahawi S et al. Coxsackievirus B exits the host cell in shed microvesicles displaying autophagosomal markers. PLoS Pathog 2014; 10: e1004045 [CrossRef] [PubMed]
    [Google Scholar]
  108. Kemball CC, Alirezaei M, Flynn CT, Wood MR, Harkins S et al. Coxsackievirus infection induces autophagy-like vesicles and megaphagosomes in pancreatic acinar cells in vivo. J Virol 2010; 84: 12110 12124 [CrossRef] [PubMed]
    [Google Scholar]
  109. Wong J, Zhang J, Si X, Gao G, Mao I et al. Autophagosome supports coxsackievirus B3 replication in host cells. J Virol 2008; 82: 9143 9153 [CrossRef] [PubMed]
    [Google Scholar]
  110. Johnstone RM, Adam M, Hammond JR, Orr L, Turbide C. Vesicle formation during reticulocyte maturation. Association of plasma membrane activities with released vesicles (exosomes). J Biol Chem 1987; 262: 9412 9420 [PubMed]
    [Google Scholar]
  111. Skotland T, Sandvig K, Llorente A. Lipids in exosomes: current knowledge and the way forward. Prog Lipid Res 2017; 66: 30 41 [CrossRef] [PubMed]
    [Google Scholar]
  112. Kowal J, Tkach M, Théry C. Biogenesis and secretion of exosomes. Curr Opin Cell Biol 2014; 29: 116 125 [CrossRef] [PubMed]
    [Google Scholar]
  113. IHK T, Yeo H, Sessions OM, Yan B, Libau EA et al. Enterovirus 71 infection of motor neuron-like NSC-34 cells undergoes a non-lytic exit pathway. Sci Rep 2016; 6: 1 16
    [Google Scholar]
  114. Feng Z, Hensley L, McKnight KL, Hu F, Madden V et al. A pathogenic picornavirus acquires an envelope by hijacking cellular membranes. Nature 2013; 496: 367 371 [CrossRef] [PubMed]
    [Google Scholar]
  115. Hirai-Yuki A, Hensley L, Whitmire JK, Lemon SM. Biliary secretion of quasi-enveloped human hepatitis A virus. mBio 2016; 7: 1 11 [CrossRef] [PubMed]
    [Google Scholar]
  116. Rivera-Serrano EE, González-López O, Das A, Lemon SM. Cellular entry and uncoating of naked and quasi-enveloped human hepatoviruses. Elife 2019; 8: 1 24 [CrossRef] [PubMed]
    [Google Scholar]
  117. Wang Y, Zhang S, Song W, Zhang W, Li J et al. Exosomes from EV71-infected oral epithelial cells can transfer miR-30a to promote EV71 infection. 2019; 2020 1 11
  118. Gu J, Wu J, Fang D, Qiu Y, Zou X et al. Exosomes cloak the virion to transmit enterovirus 71 non-lytically. Virulence 2020; 11: 32 38 [CrossRef] [PubMed]
    [Google Scholar]
  119. van der Grein SG, Defourny KAY, Rabouw HH, Galiveti CR, Langereis MA et al. Picornavirus infection induces temporal release of multiple extracellular vesicle subsets that differ in molecular composition and infectious potential. PLoS Pathog 2019; 15: 1 22 [CrossRef] [PubMed]
    [Google Scholar]
  120. Khushman Moh'd, Bhardwaj A, Patel GK, Laurini JA, Roveda K et al. Exosomal markers (CD63 and CD9) expression pattern using immunohistochemistry in resected malignant and nonmalignant pancreatic specimens. Pancreas 2017; 46: 782 788 [CrossRef] [PubMed]
    [Google Scholar]
  121. Laulagnier K, Motta C, Hamdi S, Roy S, Fauvelle F et al. Mast cell- and dendritic cell-derived exosomes display a specific lipid composition and an unusual membrane organization. Biochem J 2004; 380: 161 171 [CrossRef] [PubMed]
    [Google Scholar]
  122. Nagashima S, Takahashi M, Jirintai S, Kobayashi T et al. 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 2014; 159: 979 991 [CrossRef] [PubMed]
    [Google Scholar]
  123. Nagashima S, Takahashi M, Kobayashi T, Nishizawa T et al. Characterization of the Quasi-Enveloped hepatitis E virus particles released by the cellular exosomal pathway. J Virol 2017; 91: 1 16 [CrossRef] [PubMed]
    [Google Scholar]
  124. Nagashima S, Jirintai S, Takahashi M, Kobayashi T, Tanggis NT. Hepatitis E virus egress depends on the exosomal pathway, with secretory exosomes derived from multivesicular bodies. J Gen Virol 2014; 95: 2166 2175 [CrossRef] [PubMed]
    [Google Scholar]
  125. Montpellier C, Wychowski C, Sayed IM, Meunier JC, Saliou JM et al. Hepatitis E virus lifecycle and identification of 3 forms of the ORF2 capsid protein. Gastroenterology 2018; 154: 211 223 [CrossRef] [PubMed]
    [Google Scholar]
  126. Nagashima S, Takahashi M, Jirintai S, Tanaka T, Nishizawa T et al. Tumour susceptibility gene 101 and the vacuolar protein sorting pathway are required for the release of hepatitis E virions. J Gen Virol 2011; 92: 2838 2848 [CrossRef] [PubMed]
    [Google Scholar]
  127. Yamada K, Takahashi M, Hoshino Y, Takahashi H, Ichiyama K et al. Orf3 protein of hepatitis E virus is essential for virion release from infected cells. J Gen Virol 2009; 90: 1880 1891 [CrossRef] [PubMed]
    [Google Scholar]
  128. Nagashima S, Takahashi M, Tanaka T, Yamada K, Nishizawa T. A PSAP motif in the ORF3 protein of hepatitis E virus is necessary for virion release from infected cells. J Gen Virol 2011; 92: 269 278 [CrossRef] [PubMed]
    [Google Scholar]
  129. Takahashi M, Yamada K, Hoshino Y, Takahashi H, Ichiyama K et al. 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 1703; 2008: 153
    [Google Scholar]
  130. Emerson SU, Nguyen HT, Torian U, Burke D, Engle R et al. Release of genotype 1 hepatitis E virus from cultured hepatoma and polarized intestinal cells depends on open reading frame 3 protein and requires an intact PXXP motif. J Virol 2010; 84: 9059 9069 [CrossRef] [PubMed]
    [Google Scholar]
  131. Takahashi M, Tanaka T, Takahashi H, Hoshino Y, Nagashima S et al. 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 2010; 48: 1112 1125 [CrossRef] [PubMed]
    [Google Scholar]
  132. Yin X, Ambardekar C, Lu Y, Feng Z. Distinct entry mechanisms for nonenveloped and Quasi-Enveloped hepatitis E viruses. J Virol 2016; 90: 4232 4242 [CrossRef] [PubMed]
    [Google Scholar]
  133. Jansens RJJ, Tishchenko A, Favoreel HW. crossm nanotubes. 2020 1 14
  134. Paloheimo O, Ihalainen TO, Tauriainen S, Välilehto O, Kirjavainen S et al. Coxsackievirus B3-induced cellular protrusions: structural characteristics and functional competence. J Virol 2011; 85: 6714 6724 [CrossRef] [PubMed]
    [Google Scholar]
  135. Arias CF, DuBois RM. The astrovirus capsid: a review. Viruses 2017; 9: 1 13 [CrossRef] [PubMed]
    [Google Scholar]
  136. Méndez E, Salas-Ocampo E, Arias CF. Caspases mediate processing of the capsid precursor and cell release of human astroviruses. J Virol 2004; 78: 8601 8608 [CrossRef] [PubMed]
    [Google Scholar]
  137. 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]
  138. Banos-Lara MdelR, Méndez E. Role of individual caspases induced by astrovirus on the processing of its structural protein and its release from the cell through a non-lytic mechanism. Virology 2010; 401: 322 332 [CrossRef] [PubMed]
    [Google Scholar]
  139. Janowski AB, Bauer IK, Holtz LR, Wang D. Propagation of astrovirus Va1, a neurotropic human astrovirus, in cell culture. J Virol 2017; 91: 1 13 [CrossRef] [PubMed]
    [Google Scholar]
  140. Kuranaga E, Miura M. Nonapoptotic functions of caspases: caspases as regulatory molecules for immunity and cell-fate determination. Trends Cell Biol 2007; 17: 135 144 [CrossRef] [PubMed]
    [Google Scholar]
  141. Sommerville RG, McIntosh EG, Carson HG. The growth cycle of echo viruses in tissue culture. I. maturation and release of echo virus types 1,2,7 and 11, from monolayer cultures of monkey kidney cells. Br J Exp Pathol 1958; 39: 589 58996 [PubMed]
    [Google Scholar]
  142. Kramer M, Schulte BM, Toonen LWJ, de Bruijni MAM, Galama JMD et al. Echovirus infection causes rapid loss-of-function and cell death in human dendritic cells. Cell Microbiol 2007; 9: 1507 1518 [CrossRef] [PubMed]
    [Google Scholar]
  143. Hudson RW, Herrmann JE, Blacklow NR. Plaque quantitation and virus neutralization assays for human astroviruses. Arch Virol 1989; 108: 33 38 [CrossRef] [PubMed]
    [Google Scholar]
  144. van Dongen HM, Masoumi N, Witwer KW, Pegtel DM. Extracellular vesicles exploit viral entry routes for cargo delivery. Microbiol Mol Biol Rev 2016; 80: 369 386 [CrossRef] [PubMed]
    [Google Scholar]
  145. Vicente-Manzanares M, Sánchez-Madrid F. Cell polarization: a comparative cell biology and immunological view. Dev Immunol 2000; 7: 51 65 [CrossRef] [PubMed]
    [Google Scholar]
  146. Rodriguez-Boulan E, Macara IG. Organization and execution of the epithelial polarity programme. Nat Rev Mol Cell Biol 2014; 15: 225 242 [CrossRef] [PubMed]
    [Google Scholar]
  147. Garcia-Castillo MD, Chinnapen DJF, Lencer WI. Membrane transport across polarized epithelia. Cold Spring Harb Perspect Biol 2017; 9: 1 16 [CrossRef] [PubMed]
    [Google Scholar]
  148. Tucker SP, Thornton CL, Wimmer E, Compans RW. Vectorial release of poliovirus from polarized human intestinal epithelial cells. 1993; 67 4274 4282
  149. Snooks MJ, Bhat P, Mackenzie J, Counihan NA, Vaughan N et al. Vectorial entry and release of hepatitis A virus in polarized human hepatocytes. J Virol 2008; 82: 8733 8742 [CrossRef] [PubMed]
    [Google Scholar]
  150. Seggewiß N, Paulmann D, Dotzauer A. Lysosomes serve as a platform for hepatitis A virus particle maturation and nonlytic release. Arch Virol 2016; 161: 43 52 [CrossRef] [PubMed]
    [Google Scholar]
  151. Yotsuyanagi H, Iino S, Koike K, Yasuda K, Hino K et al. Duration of viremia in human hepatitis a viral infection as determined by polymerase chain reaction I. 1993; 38 35 38
  152. Bower WA, Nainan OV, Han X, Margolis HS. Duration of viremia in hepatitis A virus infection. J Infect Dis 2000; 182: 12 17 [CrossRef] [PubMed]
    [Google Scholar]
  153. Schulman AN, Dienstag JL, Jackson DR, Hoofnagle JH, Gerety RJ et al. Hepatitis A antigen particles in liver, bile, and stool of chimpanzees. J Infect Dis 1976; 134: 80 84 [CrossRef]
    [Google Scholar]
  154. Capelli N, Marion O, Dubois M, Allart S, Bertrand-Michel J et al. Vectorial release of hepatitis E virus in polarized human hepatocytes. J Virol 2019; 93: 1207 1218 [CrossRef] [PubMed]
    [Google Scholar]
  155. Treyer A, Müsch A. Hepatocyte polarity. Compr Physiol 2013; 3: 243 287 [CrossRef] [PubMed]
    [Google Scholar]
  156. Marks MS, Heijnen HFG, Raposo G. Lysosome-Related organelles: unusual compartments become mainstream. Curr Opin Cell Biol 2013; 25: 495 505 [CrossRef] [PubMed]
    [Google Scholar]
  157. Excoffon K, Guglielmi KM, Wetzel JD, Gansemer ND, Campbell JA et al. Reovirus preferentially infects the basolateral surface and is released from the apical surface of polarized human respiratory epithelial cells. J Infect Dis 2008; 197: 1189 1197 [CrossRef] [PubMed]
    [Google Scholar]
  158. Rosenblatt J, Raff MC, Cramer LP. An epithelial cell destined for apoptosis signals its neighbors to extrude it by an actin- and myosin-dependent mechanism. Curr Biol 2001; 11: 1847 1857 [CrossRef] [PubMed]
    [Google Scholar]
  159. Lai CM, Mainou BA, Kim KS, Dermody TS. Directional release of reovirus from the apical surface of polarized endothelial cells. mBio 2013; 4: 1 9 [CrossRef] [PubMed]
    [Google Scholar]
  160. Cevallos Porta D, López S, Arias CF, Isa P. Polarized rotavirus entry and release from differentiated small intestinal cells. Virology 2016; 499: 65 71 [CrossRef] [PubMed]
    [Google Scholar]
  161. Svensson L, Finlay BB, Bass D, von Bonsdorff CH, Greenberg HB. Symmetric infection of rotavirus on polarized human intestinal epithelial (Caco-2) cells. J Virol 1991; 65: 4190 4197 [CrossRef] [PubMed]
    [Google Scholar]
  162. Jourdan N, Maurice M, Delautier D, Quero AM, Servin AL et al. Rotavirus is released from the apical surface of cultured human intestinal cells through nonconventional vesicular transport that bypasses the Golgi apparatus. J Virol 1997; 71: 8268 8278 [CrossRef] [PubMed]
    [Google Scholar]
  163. Blutt SE, Matson DO, Crawford SE, Staat MA, Azimi P et al. Rotavirus antigenemia in children is associated with viremia. PLoS Med 2007; 4: 660 668 [CrossRef] [PubMed]
    [Google Scholar]
  164. Blutt SE, Conner ME. Rotavirus: to the gut and beyond!. Curr Opin Gastroenterol 2007; 23: 39 43 [CrossRef] [PubMed]
    [Google Scholar]
  165. Alfajaro MM, Cho KO. Evidences and consequences of extra-intestinal spread of rotaviruses in humans and animals. Virusdisease 2014; 25: 186 194 [CrossRef] [PubMed]
    [Google Scholar]
  166. Medici MC, Abelli LA, Guerra P, Dodi I, Dettori G et al. Case report: detection of rotavirus RNA in the cerebrospinal fluid of a child with rotavirus gastroenteritis and meningism. J Med Virol 2011; 83: 1637 1640 [CrossRef] [PubMed]
    [Google Scholar]
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