1887

Journal of General Virology header logo

Volume 104, Issue 9

A Coxsackievirus B1-mediated nonlytic Extracellular Vesicle-to-cell mechanism of virus transmission and its possible control through modulation of EV release No Access

Abstract

Like most non-enveloped viruses, CVB1 mainly uses cell lysis to spread. Details of a nonlytic virus transmission remain unclear. Extracellular Vesicles (EVs) transfer biomolecules between cells. We show that CVB1 entry into HeLa cells results in apoptosis and release of CVB1-induced ‘medium-sized’ EVs (CVB1-mEVs). These mEVs (100–300 nm) harbour CVB1 as shown by immunoblotting with anti-CVB1-antibody; viral capsids were detected by transmission electron microscopy and RT-PCR revealed CVB1 RNA. The percentage of mEVs released from CVB1-infected HeLa cells harbouring virus was estimated from TEM at 34 %. Inhibition of CVB1-mEV production, with calpeptin or siRNA knockdown of in HeLa cells limited spread of CVB1 suggesting these vesicles disseminate CVB1 virions to new host cells by a nonlytic EV-to-cell mechanism. This was confirmed by detecting CVB1 virions inside HeLa cells after co-culture with CVB1-mEVs; EV release may also prevent apoptosis of infected cells whilst spreading apoptosis to secondary sites of infection.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): coxsackievirus B1 , extracellular vesicles and nonlytic transmission
Funding
This study was supported by the:
  • Research Executive Agency (Award 612224)
    • Principle Award Recipient: JameelMalhador Inal
© 2023 The Authors
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/content/journal/jgv/10.1099/jgv.0.001884
2023-09-04
2024-05-10
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References

  1. Tracy S, Gauntt C. Group B coxsackievirus virulence. Curr Top Microbiol Immunol 2008; 323:49–63 [View Article] [PubMed]
     [Google Scholar]
  2. Romero JR, Selvarangan R. The human Parechoviruses: an overview. Adv Pediatr 2011; 58:65–85 [View Article] [PubMed]
     [Google Scholar]
  3. Bozym RA, Morosky SA, Kim KS, Cherry S, Coyne CB. Release of intracellular calcium stores facilitates coxsackievirus entry into polarized endothelial cells. PLoS Pathog 2010; 6:e1001135 [View Article] [PubMed]
     [Google Scholar]
  4. Patel KP, Coyne CB, Bergelson JM. Dynamin- and lipid raft-dependent entry of decay-accelerating factor (DAF)-binding and non-DAF-binding coxsackieviruses into nonpolarized cells. J Virol 2009; 83:11064–11077 [View Article] [PubMed]
     [Google Scholar]
  5. Chung S-K, Kim J-Y, Kim I-B, Park S-I, Paek K-H et al. Internalization and trafficking mechanisms of coxsackievirus B3 in HeLa cells. Virology 2005; 333:31–40 [View Article] [PubMed]
     [Google Scholar]
  6. Salako MA, Carter MJ, Kass GEN. Coxsackievirus protein 2BC blocks host cell apoptosis by inhibiting caspase-3. J Biol Chem 2006; 281:16296–16304 [View Article] [PubMed]
     [Google Scholar]
  7. Carthy CM, Yanagawa B, Luo H, Granville DJ, Yang D et al. Bcl-2 and Bcl-xL overexpression inhibits cytochrome c release, activation of multiple caspases, and virus release following coxsackievirus B3 infection. Virology 2003; 313:147–157 [View Article] [PubMed]
     [Google Scholar]
  8. Vuorinen T, Peri P, Vainionpää R. Measles virus induces apoptosis in uninfected bystander T cells and leads to granzyme B and caspase activation in peripheral blood mononuclear cell cultures. Eur J Clin Invest 2003; 33:434–442 [View Article] [PubMed]
     [Google Scholar]
  9. Cheeran M-J, Lokensgard JR, Schleiss MR. Neuropathogenesis of congenital cytomegalovirus infection: disease mechanisms and prospects for intervention. Clin Microbiol Rev 2009; 22:99–126 [View Article] [PubMed]
     [Google Scholar]
  10. Mena I, Perry CM, Harkins S, Rodriguez F, Gebhard J et al. The role of B lymphocytes in coxsackievirus B3 infection. Am J Pathol 1999; 155:1205–1215 [View Article] [PubMed]
     [Google Scholar]
  11. DeBiasi RL, Edelstein CL, Sherry B, Tyler KL. Calpain inhibition protects against virus-induced apoptotic myocardial injury. J Virol 2001; 75:351–361 [View Article] [PubMed]
     [Google Scholar]
  12. Ponnuraj EM, John TJ, Levin MJ, Simoes EA. Cell-to-cell spread of poliovirus in the spinal cord of bonnet monkeys (Macaca radiata). J Gen Virol 1998; 79:2393–2403 [View Article] [PubMed]
     [Google Scholar]
  13. 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 [View Article] [PubMed]
     [Google Scholar]
  14. Kowal J, Arras G, Colombo M, Jouve M, Morath JP et al. Proteomic comparison defines novel markers to characterize heterogeneous populations of extracellular vesicle subtypes. Proc Natl Acad Sci U S A 2016; 113:E968–77 [View Article] [PubMed]
     [Google Scholar]
  15. Moore C, Kosgodage U, Lange S, Inal JM. The emerging role of exosome and microvesicle- (EMV-) based cancer therapeutics and immunotherapy. Int J Cancer 2017; 141:428–436 [View Article] [PubMed]
     [Google Scholar]
  16. Menck K, Sönmezer C, Worst TS, Schulz M, Dihazi GH et al. Neutral sphingomyelinases control extracellular vesicles budding from the plasma membrane. J Extracell Vesicles 2017; 6:1378056 [View Article] [PubMed]
     [Google Scholar]
  17. Stratton D, Moore C, Antwi-Baffour S, Lange S, Inal J. Microvesicles released constitutively from prostate cancer cells differ biochemically and functionally to stimulated microvesicles released through sublytic C5b-9. Biochem Biophys Res Commun 2015; 460:589–595 [View Article] [PubMed]
     [Google Scholar]
  18. Stachowiak JC, Brodsky FM, Miller EA. A cost-benefit analysis of the physical mechanisms of membrane curvature. Nat Cell Biol 2013; 15:1019–1027 [View Article] [PubMed]
     [Google Scholar]
  19. Kholia S, Jorfi S, Thompson PR, Causey CP, Nicholas AP et al. A novel role for peptidylarginine deiminases in microvesicle release reveals therapeutic potential of PAD inhibition in sensitizing prostate cancer cells to chemotherapy. J Extracell Vesicles 2015; 4:26192 [View Article] [PubMed]
     [Google Scholar]
  20. Wilson KF, Erickson JW, Antonyak MA, Cerione RA. Rho GTPases and their roles in cancer metabolism. Trends Mol Med 2013; 19:74–82 [View Article] [PubMed]
     [Google Scholar]
  21. Sedgwick AE, Clancy JW, Olivia Balmert M, D’Souza-Schorey C. Extracellular microvesicles and invadopodia mediate non-overlapping modes of tumor cell invasion. Sci Rep 2015; 5:14748 [View Article] [PubMed]
     [Google Scholar]
  22. Schlienger S, Campbell S, Claing A. ARF1 regulates the Rho/MLC pathway to control EGF-dependent breast cancer cell invasion. Mol Biol Cell 2014; 25:17–29 [View Article] [PubMed]
     [Google Scholar]
  23. Liao C-F, Lin S-H, Chen H-C, Tai C-J, Chang C-C et al. CSE1L, a novel microvesicle membrane protein, mediates Ras-triggered microvesicle generation and metastasis of tumor cells. Mol Med 2012; 18:1269–1280 [View Article] [PubMed]
     [Google Scholar]
  24. Inal JM, Ansa-Addo EA, Stratton D, Kholia S, Antwi-Baffour SS et al. Microvesicles in health and disease. Arch Immunol Ther Exp 2012; 60:107–121 [View Article] [PubMed]
     [Google Scholar]
  25. De Sousa KP, Rossi I, Abdullahi M, Ramirez MI, Stratton D et al. Isolation and characterization of extracellular vesicles and future directions in diagnosis and therapy. Wiley Interdiscip Rev Nanomed Nanobiotechnol 2023; 15:e1835 [View Article] [PubMed]
     [Google Scholar]
  26. Pegtel DM, Peferoen L, Amor S. Extracellular vesicles as modulators of cell-to-cell communication in the healthy and diseased brain. Philos Trans R Soc Lond B Biol Sci 2014; 369:20130516 [View Article] [PubMed]
     [Google Scholar]
  27. Lange S, Gallagher M, Kholia S, Kosgodage US, Hristova M et al. Peptidylarginine deiminases-roles in cancer and neurodegeneration and possible avenues for therapeutic intervention via modulation of exosome and microvesicle (EMV) release?. Int J Mol Sci 2017; 18:1196 [View Article] [PubMed]
     [Google Scholar]
  28. Jorfi S, Ansa-Addo EA, Kholia S, Stratton D, Valley S et al. Inhibition of microvesiculation sensitizes prostate cancer cells to chemotherapy and reduces docetaxel dose required to limit tumor growth in vivo. Sci Rep 2015; 5:13006 [View Article] [PubMed]
     [Google Scholar]
  29. Muralidharan-Chari V, Kohan HG, Asimakopoulos AG, Sudha T, Sell S et al. Microvesicle removal of anticancer drugs contributes to drug resistance in human pancreatic cancer cells. Oncotarget 2016; 7:50365–50379 [View Article] [PubMed]
     [Google Scholar]
  30. Aubertin K, Silva AKA, Luciani N, Espinosa A, Djemat A et al. Massive release of extracellular vesicles from cancer cells after photodynamic treatment or chemotherapy. Sci Rep 2016; 6:35376 [View Article] [PubMed]
     [Google Scholar]
  31. Antwi-Baffour S, Kholia S, Aryee Y-D, Ansa-Addo EA, Stratton D et al. Human plasma membrane-derived vesicles inhibit the phagocytosis of apoptotic cells--possible role in SLE. Biochem Biophys Res Commun 2010; 398:278–283 [View Article] [PubMed]
     [Google Scholar]
  32. Shao W-H, Cohen PL. Disturbances of apoptotic cell clearance in systemic lupus erythematosus. Arthritis Res Ther 2011; 13:202 [View Article] [PubMed]
     [Google Scholar]
  33. Valenti R, Huber V, Iero M, Filipazzi P, Parmiani G et al. Tumor-released microvesicles as vehicles of immunosuppression. Cancer Res 2007; 67:2912–2915 [View Article] [PubMed]
     [Google Scholar]
  34. Becker A, Thakur BK, Weiss JM, Kim HS, Peinado H et al. Extracellular vesicles in cancer: cell-to-cell mediators of metastasis. Cancer Cell 2016; 30:836–848 [View Article] [PubMed]
     [Google Scholar]
  35. Peinado H, Zhang H, Matei IR, Costa-Silva B, Hoshino A et al. Pre-metastatic niches: organ-specific homes for metastases. Nat Rev Cancer 2017; 17:302–317 [View Article] [PubMed]
     [Google Scholar]
  36. Jorfi S, Inal JM. The role of microvesicles in cancer progression and drug resistance. Biochem Soc Trans 2013; 41:293–298 [View Article] [PubMed]
     [Google Scholar]
  37. Robbins PD, Dorronsoro A, Booker CN. Regulation of chronic inflammatory and immune processes by extracellular vesicles. J Clin Invest 2016; 126:1173–1180 [View Article] [PubMed]
     [Google Scholar]
  38. Sarkar A, Mitra S, Mehta S, Raices R, Wewers MD. Monocyte derived microvesicles deliver a cell death message via encapsulated caspase-1. PLoS One 2009; 4:e7140 [View Article] [PubMed]
     [Google Scholar]
  39. Ansa-Addo EA, Lange S, Stratton D, Antwi-Baffour S, Cestari I et al. Human plasma membrane-derived vesicles halt proliferation and induce differentiation of THP-1 acute monocytic leukemia cells. J Immunol 2010; 185:5236–5246 [View Article] [PubMed]
     [Google Scholar]
  40. Ismail N, Wang Y, Dakhlallah D, Moldovan L, Agarwal K et al. Macrophage microvesicles induce macrophage differentiation and miR-223 transfer. Blood 2013; 121:984–995 [View Article] [PubMed]
     [Google Scholar]
  41. Coakley G, Maizels RM, Buck AH. Exosomes and other extracellular vesicles: the new communicators in parasite infections. Trends Parasitol 2015; 31:477–489 [View Article] [PubMed]
     [Google Scholar]
  42. Cestari I, Ansa-Addo E, Deolindo P, Inal JM, Ramirez MI. Trypanosoma cruzi immune evasion mediated by host cell-derived microvesicles. J Immunol 2012; 188:1942–1952 [View Article] [PubMed]
     [Google Scholar]
  43. Antwi-Baffour S, Malibha-Pinchbeck M, Stratton D, Jorfi S, Lange S et al. Plasma mEV levels in Ghanain malaria patients with low parasitaemia are higher than those of healthy controls, raising the potential for parasite markers in mEVs as diagnostic targets. J Extracell Vesicles 2020; 9:1697124 [View Article] [PubMed]
     [Google Scholar]
  44. Lee Y, El Andaloussi S, Wood MJA. Exosomes and microvesicles: extracellular vesicles for genetic information transfer and gene therapy. Hum Mol Genet 2012; 21:R125–R134 [View Article] [PubMed]
     [Google Scholar]
  45. Stratton D, Moore C, Zheng L, Lange S, Inal J. Prostate cancer cells stimulated by calcium-mediated activation of protein kinase C undergo a refractory period before re-releasing calcium-bearing microvesicles. Biochem Biophys Res Commun 2015; 460:511–517 [View Article] [PubMed]
     [Google Scholar]
  46. Inal JM, Ansa-Addo EA, Lange S. Interplay of host-pathogen microvesicles and their role in infectious disease. Biochem Soc Trans 2013; 41:258–262 [View Article] [PubMed]
     [Google Scholar]
  47. Rossi IV, Nunes MAF, Sabatke B, Ribas HT, Winnischofer SMB et al. An induced population of Trypanosoma cruzi epimastigotes more resistant to complement lysis promotes a phenotype with greater differentiation, invasiveness, and release of extracellular vesicles. Front Cell Infect Microbiol 2022; 12:1046681 [View Article] [PubMed]
     [Google Scholar]
  48. Evans-Osses I, Mojoli A, Monguió-Tortajada M, Marcilla A, Aran V et al. Microvesicles released from Giardia intestinalis disturb host-pathogen response in vitro. Eur J Cell Biol 2017; 96:131–142 [View Article] [PubMed]
     [Google Scholar]
  49. Badorff C, Berkely N, Mehrotra S, Talhouk JW, Rhoads RE et al. Enteroviral protease 2A directly cleaves dystrophin and is inhibited by a dystrophin-based substrate analogue. J Biol Chem 2000; 275:11191–11197 [View Article] [PubMed]
     [Google Scholar]
  50. Seipelt J, Liebig HD, Sommergruber W, Gerner C, Kuechler E. 2A proteinase of human rhinovirus cleaves cytokeratin 8 in infected HeLa cells. J Biol Chem 2000; 275:20084–20089 [View Article] [PubMed]
     [Google Scholar]
  51. Xiong D, Lee G-H, Badorff C, Dorner A, Lee S et al. Dystrophin deficiency markedly increases enterovirus-induced cardiomyopathy: a genetic predisposition to viral heart disease. Nat Med 2002; 8:872–877 [View Article] [PubMed]
     [Google Scholar]
  52. Fox JE, Austin CD, Boyles JK, Steffen PK. Role of the membrane skeleton in preventing the shedding of procoagulant-rich microvesicles from the platelet plasma membrane. J Cell Biol 1990; 111:483–493 [View Article] [PubMed]
     [Google Scholar]
  53. 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 [View Article] [PubMed]
     [Google Scholar]
  54. Masi G, Mercati D, Vannuccini E, Paccagnini E, Riparbelli MG et al. p66Shc regulates vesicle-mediated secretion in mast cells by affecting F-actin dynamics. J Leukoc Biol 2014; 95:285–292 [View Article] [PubMed]
     [Google Scholar]
  55. Huber V, Fais S, Iero M, Lugini L, Canese P et al. Human colorectal cancer cells induce T-cell death through release of proapoptotic microvesicles: role in immune escape. Gastroenterology 2005; 128:1796–1804 [View Article] [PubMed]
     [Google Scholar]
  56. Andreola G, Rivoltini L, Castelli C, Huber V, Perego P et al. Induction of lymphocyte apoptosis by tumor cell secretion of FasL-bearing microvesicles. J Exp Med 2002; 195:1303–1316 [View Article] [PubMed]
     [Google Scholar]
  57. Jorfi S, Ansa-Addo E, Inal JM. Coxsackie virus entry and spread in HeLa cells is aided by microvesicle release (170.22). J Immunol 2012; 188:170 [View Article]
     [Google Scholar]
  58. Jorfi S, Ansa-Addo E, Inal JM. Plasma membrane-derived vesicles (Pmvs) released from infected Hela cells by Coxsackie virus B1 induce apoptosis in recipient viable cells. Immunology 2010222 [View Article]
     [Google Scholar]
  59. Inal JM, Jorfi S. Coxsackievirus B transmission and possible new roles for extracellular vesicles. Biochem Soc Trans 2013; 41:299–302 [View Article] [PubMed]
     [Google Scholar]
  60. Kosgodage US, Trindade RP, Thompson PR, Inal JM, Lange S. Chloramidine/Bisindolylmaleimide-I-Mediated inhibition of exosome and microvesicle release and enhanced efficacy of cancer chemotherapy. Int J Mol Sci 2017; 18:1007 [View Article] [PubMed]
     [Google Scholar]
  61. Théry C, Witwer KW, Aikawa E, Alcaraz MJ, Anderson JD et al. Minimal information for studies of extracellular vesicles 2018 (MISEV2018): a position statement of the International Society for Extracellular Vesicles and update of the MISEV2014 guidelines. J Extracell Vesicles 2018; 7:1535750 [View Article] [PubMed]
     [Google Scholar]
  62. Kosgodage US, Uysal-Onganer P, MacLatchy A, Mould R, Nunn AV et al. Cannabidiol affects extracellular vesicle release, miR21 and miR126, and reduces prohibitin protein in Glioblastoma Multiforme cells. Transl Oncol 2019; 12:513–522 [View Article] [PubMed]
     [Google Scholar]
  63. Hui K-M, Orriss GL, Schirmer T, Magnadóttir B, Schifferli JA et al. Expression of functional recombinant von Willebrand factor-A domain from human complement C2: A potential binding site for C4 and CRIT. Biochem J 2005; 389:863–868 [View Article] [PubMed]
     [Google Scholar]
  64. Schindelin J, Arganda-Carreras I, Frise E, Kaynig V, Longair M et al. Fiji: an open-source platform for biological-image analysis. Nat Methods 2012; 9:676–682 [View Article] [PubMed]
     [Google Scholar]
  65. Commisso C, Flinn RJ, Bar-Sagi D. Determining the macropinocytic index of cells through a quantitative image-based assay. Nat Protoc 2014; 9:182–192 [View Article] [PubMed]
     [Google Scholar]
  66. Wang JTH, Teasdale RD, Liebl D. Macropinosome quantitation assay. MethodsX 2014; 1:36–41 [View Article] [PubMed]
     [Google Scholar]
  67. Manders EM, Stap J, Brakenhoff GJ, van Driel R, Aten JA. Dynamics of three-dimensional replication patterns during the S-phase, analysed by double labelling of DNA and confocal microscopy. J Cell Sci 1992; 103:857–862 [View Article] [PubMed]
     [Google Scholar]
  68. Bolte S, Cordelières FP. A guided tour into subcellular colocalization analysis in light microscopy. J Microsc 2006; 224:213–232 [View Article] [PubMed]
     [Google Scholar]
  69. Stratton D, Lange S, Inal JM. Pulsed extremely low-frequency magnetic fields stimulate microvesicle release from human monocytic leukaemia cells. Biochem Biophys Res Commun 2013; 430:470–475 [View Article] [PubMed]
     [Google Scholar]
  70. Evans-Osses I, Mojoli A, Monguió-Tortajada M, Marcilla A, Aran V et al. Microvesicles released from Giardia intestinalis disturb host-pathogen response in vitro. Eur J Cell Biol 2017; 96:131–142 [View Article] [PubMed]
     [Google Scholar]
  71. O’Neill CP, Gilligan KE, Dwyer RM. Role of Extracellular Vesicles (EVs) in cell stress response and resistance to cancer therapy. Cancers 2019; 11:136 [View Article] [PubMed]
     [Google Scholar]
  72. Bernimoulin M, Waters EK, Foy M, Steele BM, Sullivan M et al. Differential stimulation of monocytic cells results in distinct populations of microparticles. J Thromb Haemost 2009; 7:1019–1028 [View Article] [PubMed]
     [Google Scholar]
  73. Durcin M, Fleury A, Taillebois E, Hilairet G, Krupova Z et al. Characterisation of adipocyte-derived extracellular vesicle subtypes identifies distinct protein and lipid signatures for large and small extracellular vesicles. J Extracell Vesicles 2017; 6:1305677 [View Article] [PubMed]
     [Google Scholar]
  74. Xiao X, Yu S, Li S, Wu J, Ma R et al. Exosomes: decreased sensitivity of lung cancer A549 cells to cisplatin. PLoS One 2014; 9:e89534 [View Article] [PubMed]
     [Google Scholar]
  75. Le M, Fernandez-Palomo C, McNeill FE, Seymour CB, Rainbow AJ et al. Exosomes are released by bystander cells exposed to radiation-induced biophoton signals: reconciling the mechanisms mediating the bystander effect. PLoS One 2017; 12:e0173685 [View Article] [PubMed]
     [Google Scholar]
  76. Angeloni NL, McMahon KM, Swaminathan S, Plebanek MP, Osman I et al. Pathways for modulating exosome lipids identified by high-density lipoprotein-like nanoparticle binding to scavenger receptor type B-1. Sci Rep 2016; 6:22915 [View Article] [PubMed]
     [Google Scholar]
  77. Debiasi RL, Squier MK, Pike B, Wynes M, Dermody TS et al. Reovirus-induced apoptosis is preceded by increased cellular calpain activity and is blocked by calpain inhibitors. J Virol 1999; 73:695–701 [View Article] [PubMed]
     [Google Scholar]
  78. Bozym RA, Patel K, White C, Cheung K-H, 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 [View Article] [PubMed]
     [Google Scholar]
  79. Kim D-K, Lee J, Kim SR, Choi D-S, Yoon YJ et al. EVpedia: a community web portal for extracellular vesicles research. Bioinformatics 2015; 31:933–939 [View Article] [PubMed]
     [Google Scholar]
  80. Elstein KH, Zucker RM. Comparison of cellular and nuclear flow cytometric techniques for discriminating apoptotic subpopulations. Exp Cell Res 1994; 211:322–331 [View Article] [PubMed]
     [Google Scholar]
  81. Tisdale EJ, Shisheva A, Artalejo CR. Overexpression of atypical protein kinase C in HeLa cells facilitates macropinocytosis via Src activation. Cell Signal 2014; 26:1235–1242 [View Article] [PubMed]
     [Google Scholar]
  82. Grimmer S, van Deurs B, Sandvig K. Membrane ruffling and macropinocytosis in A431 cells require cholesterol. J Cell Sci 2002; 115:2953–2962 [View Article] [PubMed]
     [Google Scholar]
  83. Cao H, Chen J, Awoniyi M, Henley JR, McNiven MA. Dynamin 2 mediates fluid-phase micropinocytosis in epithelial cells. J Cell Sci 2007; 120:4167–4177 [View Article] [PubMed]
     [Google Scholar]
  84. Preta G, Cronin JG, Sheldon IM. Dynasore - not just a dynamin inhibitor. Cell Commun Signal 2015; 13:24 [View Article] [PubMed]
     [Google Scholar]
  85. Coyne CB, Bergelson JM. Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions. Cell 2006; 124:119–131 [View Article] [PubMed]
     [Google Scholar]
  86. Coyne CB, Kim KS, Bergelson JM. Poliovirus entry into human brain microvascular cells requires receptor-induced activation of SHP-2. EMBO J 2007; 26:4016–4028 [View Article] [PubMed]
     [Google Scholar]
  87. Mi J, Li ZY, Ni S, Steinwaerder D, Lieber A. Induced apoptosis supports spread of adenovirus vectors in tumors. Hum Gene Ther 2001; 12:1343–1352 [View Article] [PubMed]
     [Google Scholar]
  88. Inal JM, Kosgodage U, Azam S, Stratton D, Antwi-Baffour S et al. Blood/plasma secretome and microvesicles. Biochim Biophys Acta 2013; 1834:2317–2325 [View Article] [PubMed]
     [Google Scholar]
  89. Arenaccio C, Federico M. The multifaceted functions of exosomes in health and disease: an overview. Adv Exp Med Biol 2017; 998:3–19 [View Article] [PubMed]
     [Google Scholar]
  90. Prada I, Meldolesi J. Binding and fusion of extracellular vesicles to the plasma membrane of their cell targets. Int J Mol Sci 2016; 17:1296 [View Article] [PubMed]
     [Google Scholar]
  91. Raposo G, Stoorvogel W. Extracellular vesicles: exosomes, microvesicles, and friends. J Cell Biol 2013; 200:373–383 [View Article] [PubMed]
     [Google Scholar]
  92. Taylor DD, Gercel-Taylor C. The origin, function, and diagnostic potential of RNA within extracellular vesicles present in human biological fluids. Front Genet 2013; 4:142 [View Article] [PubMed]
     [Google Scholar]
  93. 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 [View Article] [PubMed]
     [Google Scholar]
  94. Faille D, El-Assaad F, Mitchell AJ, Alessi M-C, Chimini G et al. Endocytosis and intracellular processing of platelet microparticles by brain endothelial cells. J Cell Mol Med 2012; 16:1731–1738 [View Article] [PubMed]
     [Google Scholar]
  95. Kanada M, Bachmann MH, Hardy JW, Frimannson DO, Bronsart L et al. Differential fates of biomolecules delivered to target cells via extracellular vesicles. Proc Natl Acad Sci U S A 2015; 112:E1433–42 [View Article] [PubMed]
     [Google Scholar]
  96. French KC, Antonyak MA, Cerione RA. Extracellular vesicle docking at the cellular port: extracellular vesicle binding and uptake. Semin Cell Dev Biol 2017; 67:48–55 [View Article] [PubMed]
     [Google Scholar]
  97. Too IHK, 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; 6:36983 [View Article] [PubMed]
     [Google Scholar]
  98. 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:e1007594 [View Article] [PubMed]
     [Google Scholar]
  99. 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 [View Article] [PubMed]
     [Google Scholar]
  100. Chen Y-H, Du W, Hagemeijer MC, Takvorian PM, Pau C et al. Phosphatidylserine vesicles enable efficient en bloc transmission of enteroviruses. Cell 2015; 160:619–630 [View Article] [PubMed]
     [Google Scholar]
  101. 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 [View Article] [PubMed]
     [Google Scholar]
  102. Kalra H, Drummen GPC, Mathivanan S. Focus on extracellular vesicles: introducing the next small big thing. Int J Mol Sci 2016; 17:170 [View Article] [PubMed]
     [Google Scholar]
  103. Muralidharan-Chari V, Clancy J, Plou C, Romao M, Chavrier P et al. ARF6-regulated shedding of tumor cell-derived plasma membrane microvesicles. Curr Biol 2009; 19:1875–1885 [View Article] [PubMed]
     [Google Scholar]
  104. Spiller OB, Goodfellow IG, Evans DJ, Hinchliffe SJ, Morgan BP. Coxsackie B viruses that use human DAF as a receptor infect pig cells via pig CAR and do not use pig DAF. J Gen Virol 2002; 83:45–52 [View Article] [PubMed]
     [Google Scholar]
  105. Pan J, Zhang L, Organtini LJ, Hafenstein S, Bergelson JM. Specificity of coxsackievirus B3 interaction with human, but not murine, decay-accelerating factor: replacement of a single residue within short consensus repeat 2 prevents virus attachment. J Virol 2015; 89:1324–1328 [View Article] [PubMed]
     [Google Scholar]
  106. Pan J, Narayanan B, Shah S, Yoder JD, Cifuente JO et al. Single amino acid changes in the virus capsid permit coxsackievirus B3 to bind decay-accelerating factor. J Virol 2011; 85:7436–7443 [View Article] [PubMed]
     [Google Scholar]
  107. Böing AN, Stap J, Hau CM, Afink GB, Ris-Stalpers C et al. Active caspase-3 is removed from cells by release of caspase-3-enriched vesicles. Biochim Biophys Acta 2013; 1833:1844–1852 [View Article] [PubMed]
     [Google Scholar]
  108. Li H, Pauza CD. Rapamycin increases the yield and effector function of human γδ T cells stimulated in vitro. Cancer Immunol Immunother 2011; 60:361–370 [View Article] [PubMed]
     [Google Scholar]
  109. Coyne CB, Shen L, Turner JR, Bergelson JM. Coxsackievirus entry across epithelial tight junctions requires occludin and the small GTPases Rab34 and Rab5. Cell Host Microbe 2007; 2:181–192 [View Article] [PubMed]
     [Google Scholar]
  110. Korns D, Frasch SC, Fernandez-Boyanapalli R, Henson PM, Bratton DL. Modulation of macrophage efferocytosis in inflammation. Front Immunol 2011; 2:57 [View Article] [PubMed]
     [Google Scholar]
  111. Ogden CA, deCathelineau A, Hoffmann PR, Bratton D, Ghebrehiwet B et al. C1q and mannose binding lectin engagement of cell surface calreticulin and CD91 initiates macropinocytosis and uptake of apoptotic cells. J Exp Med 2001; 194:781–795 [View Article] [PubMed]
     [Google Scholar]
  112. Hoffmann PR, deCathelineau AM, Ogden CA, Leverrier Y, Bratton DL et al. Phosphatidylserine (PS) induces PS receptor-mediated macropinocytosis and promotes clearance of apoptotic cells. J Cell Biol 2001; 155:649–659 [View Article] [PubMed]
     [Google Scholar]
  113. de Vries E, Tscherne DM, Wienholts MJ, Cobos-Jiménez V, Scholte F et al. Dissection of the influenza A virus endocytic routes reveals macropinocytosis as an alternative entry pathway. PLoS Pathog 2011; 7:e1001329 [View Article] [PubMed]
     [Google Scholar]
  114. Monks J, Rosner D, Geske FJ, Lehman L, Hanson L et al. Epithelial cells as phagocytes: apoptotic epithelial cells are engulfed by mammary alveolar epithelial cells and repress inflammatory mediator release. Cell Death Differ 2005; 12:107–114 [View Article] [PubMed]
     [Google Scholar]
  115. Taja-Chayeb L, Chavez-Blanco A, Martínez-Tlahuel J, González-Fierro A, Candelaria M et al. Expression of platelet derived growth factor family members and the potential role of imatinib mesylate for cervical cancer. Cancer Cell Int 2006; 6:22 [View Article] [PubMed]
     [Google Scholar]
  116. Dharmawardhane S, Schürmann A, Sells MA, Chernoff J, Schmid SL et al. Regulation of macropinocytosis by p21-activated kinase-1. Mol Biol Cell 2000; 11:3341–3352 [View Article] [PubMed]
     [Google Scholar]
  117. Liang C-C, Sun M-J, Lei H-Y, Chen S-H, Yu C-K et al. Human endothelial cell activation and apoptosis induced by enterovirus 71 infection. J Med Virol 2004; 74:597–603 [View Article] [PubMed]
     [Google Scholar]
  118. Ekström J-O, Tolf C, Fahlgren C, Johansson ES, Arbrandt G et al. Replication of Ljungan virus in cell culture: the genomic 5’-end, infectious cDNA clones and host cell response to viral infections. Virus Res 2007; 130:129–139 [View Article] [PubMed]
     [Google Scholar]
  119. Wei T, Kikuchi A, Moriyasu Y, Suzuki N, Shimizu T et al. The spread of rice dwarf virus among cells of its insect vector exploits virus-induced tubular structures. J Virol 2006; 80:8593–8602 [View Article] [PubMed]
     [Google Scholar]
  120. Wei T, Shimizu T, Omura T. Endomembranes and myosin mediate assembly into tubules of Pns10 of rice dwarf virus and intercellular spreading of the virus in cultured insect vector cells. Virology 2008; 372:349–356 [View Article] [PubMed]
     [Google Scholar]
  121. Wei T, Uehara-Ichiki T, Miyazaki N, Hibino H, Iwasaki K et al. Association of rice gall dwarf virus with microtubules is necessary for viral release from cultured insect vector cells. J Virol 2009; 83:10830–10835 [View Article] [PubMed]
     [Google Scholar]
  122. Fu Y, Xiong S, Kuhn RJ. Exosomes mediate Coxsackievirus B3 transmission and expand the viral tropism. PLoS Pathog 2023; 19:e1011090 [View Article] [PubMed]
     [Google Scholar]
  123. Roseblade A, Luk F, Rawling T, Ung A, Grau GER et al. Cell-derived microparticles: new targets in the therapeutic management of disease. J Pharm Pharm Sci 2013; 16:238–253 [View Article] [PubMed]
     [Google Scholar]
  124. Mediouni S, Mou H, Otsuka Y, Jablonski JA, Adcock RS et al. Identification of potent small molecule inhibitors of SARS-CoV-2 entry. SLAS Discovery: Advancing Life Sciences R & D 2022; 278–19 [View Article] [PubMed]
     [Google Scholar]
  125. Günther S, Reinke PYA, Fernández-García Y, Lieske J, Lane TJ et al. X-ray screening identifies active site and allosteric inhibitors of SARS-CoV-2 main protease. Science 2021; 372:642–646 [View Article] [PubMed]
     [Google Scholar]
  126. Inal J, Paizuldaeva A, Terziu E. Therapeutic use of calpeptin in COVID-19 infection. Clin Sci 2022; 136:1439–1447 [View Article] [PubMed]
     [Google Scholar]
  127. Sisa C, Kholia S, Naylor J, Herrera Sanchez MB, Bruno S et al. Mesenchymal stromal cell derived extracellular vesicles reduce hypoxia-ischaemia induced perinatal brain injury. Front Physiol 2019; 10:282 [View Article] [PubMed]
     [Google Scholar]
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A Coxsackievirus B1-mediated nonlytic Extracellular Vesicle-to-cell mechanism of virus transmission and its possible control through modulation of EV release
J. Gen. Virol. 104, 001884 (2023); https://doi.org/10.1099/jgv.0.001884
/content/journal/jgv/10.1099/jgv.0.001884
/content/journal/jgv/10.1099/jgv.0.001884
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