1887

Abstract

Binding of echovirus 11 strain 207 (EV11-207) to Caco-2 monolayers results in rapid transfer of the virus to tight junctions prior to uptake. Using a confocal microscopy based-method, this study quantified the spatiotemporal distribution of actin during the time course of infection by EV11-207 in Caco-2 polarized cells. It was found that binding of EV11-207 to the apical surface resulted in rapid rearrangement of the actin cytoskeleton, concomitant with transport of the virus particles to tight junctions. By interfering with the actin network dynamics, the virus remained trapped at the cell surface, leading to abortion of infection. In addition, it was observed that at 4 h post-infection, concomitant with the detection of virus replication, actin filament was depolymerized and degraded. Finally, it was shown that the mechanisms leading to loss of actin were independent of viral genome synthesis, indicating a potential role for the viral protein synthesis seen in late infection. These data confirmed a previous study on the requirement for an intact actin cytoskeleton for EV11-207 to infect cells and reinforce the notion of actin cytoskeleton subversion by picornaviruses during infection in polarized epithelial cells.

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2012-03-01
2024-03-29
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References

  1. Abrami L., Leppla S. H., van der Goot F. G. 2006; Receptor palmitoylation and ubiquitination regulate anthrax toxin endocytosis. J Cell Biol 172:309–320 [View Article][PubMed]
    [Google Scholar]
  2. Abrami L., Bischofberger M., Kunz B., Groux R., van der Goot F. G. 2010; Endocytosis of the anthrax toxin is mediated by clathrin, actin and unconventional adaptors. PLoS Pathog 6:e1000792 [View Article][PubMed]
    [Google Scholar]
  3. Antecol M. H., Darveau A., Sonenberg N., Mukherjee B. B. 1986; Altered biochemical properties of actin in normal skin fibroblasts from individuals predisposed to dominantly inherited cancers. Cancer Res 46:1867–1873[PubMed]
    [Google Scholar]
  4. Arakawa Y., Cordeiro J. V., Schleich S., Newsome T. P., Way M. 2007; The release of vaccinia virus from infected cells requires RhoA-mDia modulation of cortical actin. Cell Host Microbe 1:227–240 [View Article][PubMed]
    [Google Scholar]
  5. Bella J., Rossmann M. G. 1999; Review: rhinoviruses and their ICAM receptors. J Struct Biol 128:69–74 [View Article][PubMed]
    [Google Scholar]
  6. Belnap D. M., Filman D. J., Trus B. L., Cheng N., Booy F. P., Conway J. F., Curry S., Hiremath C. N., Tsang S. K. other authors 2000a; Molecular tectonic model of virus structural transitions: the putative cell entry states of poliovirus. J Virol 74:1342–1354 [View Article][PubMed]
    [Google Scholar]
  7. Belnap D. M., McDermott B. M. Jr, Filman D. J., Cheng N., Trus B. L., Zuccola H. J., Racaniello V. R., Hogle J. M., Steven A. C. 2000b; Three-dimensional structure of poliovirus receptor bound to poliovirus. Proc Natl Acad Sci U S A 97:73–78 [View Article][PubMed]
    [Google Scholar]
  8. Burckhardt C. J., Greber U. F. 2009; Virus movements on the plasma membrane support infection and transmission between cells. PLoS Pathog 5:e1000621 [View Article][PubMed]
    [Google Scholar]
  9. Chant J., Stowers L. 1995; GTPase cascades choreographing cellular behavior: movement, morphogenesis, and more. Cell 81:1–4 [View Article][PubMed]
    [Google Scholar]
  10. Cooper P. D. 1964; The kinetics of the appearance of poliovirus ribonucleic acid. J Gen Microbiol 37:267–270[PubMed] [CrossRef]
    [Google Scholar]
  11. Cooper J. A. 1987; Effects of cytochalasin and phalloidin on actin. J Cell Biol 105:1473–1478 [View Article][PubMed]
    [Google Scholar]
  12. Coyne C. B., Bergelson J. M. 2006; Virus-induced Abl and Fyn kinase signals permit coxsackievirus entry through epithelial tight junctions. Cell 124:119–131 [View Article][PubMed]
    [Google Scholar]
  13. Coyne C. B., Shen L., Turner J. R., Bergelson J. M. 2007; Coxsackievirus entry across epithelial tight junctions requires occludin and the small GTPases Rab34 and Rab5. Cell Host Microbe 2:181–192 [View Article][PubMed]
    [Google Scholar]
  14. Cramer L. P., Briggs L. J., Dawe H. R. 2002; Use of fluorescently labelled deoxyribonuclease I to spatially measure G-actin levels in migrating and non-migrating cells. Cell Motil Cytoskeleton 51:27–38 [View Article][PubMed]
    [Google Scholar]
  15. Croons V., Martinet W., Herman A. G., De Meyer G. R. 2008; Differential effect of the protein synthesis inhibitors puromycin and cycloheximide on vascular smooth muscle cell viability. J Pharmacol Exp Ther 325:824–832 [View Article][PubMed]
    [Google Scholar]
  16. Cudmore S., Cossart P., Griffiths G., Way M. 1995; Actin-based motility of vaccinia virus. Nature 378:636–638 [View Article][PubMed]
    [Google Scholar]
  17. Cudmore S., Reckmann I., Way M. 1997; Viral manipulations of the actin cytoskeleton. Trends Microbiol 5:142–148 [View Article][PubMed]
    [Google Scholar]
  18. Dang Y., Schneider-Poetsch T., Eyler D. E., Jewett J. C., Bhat S., Rawal V. H., Green R., Liu J. O. 2011; Inhibition of eukaryotic translation elongation by the antitumor natural product Mycalamide B. RNA 17:1578–1588 [View Article][PubMed]
    [Google Scholar]
  19. DuBose D. A., Haugland R. 1993; Comparisons of endothelial cell G- and F-actin distribution in situ and in vitro. Biotech Histochem 68:8–16 [View Article][PubMed]
    [Google Scholar]
  20. Elton D., Simpson-Holley M., Archer K., Medcalf L., Hallam R., McCauley J., Digard P. 2001; Interaction of the influenza virus nucleoprotein with the cellular CRM1-mediated nuclear export pathway. J Virol 75:408–419 [View Article][PubMed]
    [Google Scholar]
  21. Ewers H., Smith A. E., Sbalzarini I. F., Lilie H., Koumoutsakos P., Helenius A. 2005; Single-particle tracking of murine polyoma virus-like particles on live cells and artificial membranes. Proc Natl Acad Sci U S A 102:15110–15115 [View Article][PubMed]
    [Google Scholar]
  22. Gill R. K., Shen L., Turner J. R., Saksena S., Alrefai W. A., Pant N., Esmaili A., Dwivedi A., Ramaswamy K., Dudeja P. K. 2008; Serotonin modifies cytoskeleton and brush-border membrane architecture in human intestinal epithelial cells. Am J Physiol Gastrointest Liver Physiol 295:G700–G708 [View Article][PubMed]
    [Google Scholar]
  23. Glacy S. D. 1983; Pattern and time course of rhodamine–actin incorporation in cardiac myocytes. J Cell Biol 96:1164–1167 [View Article][PubMed]
    [Google Scholar]
  24. Gottlieb T. A., Ivanov I. E., Adesnik M., Sabatini D. D. 1993; Actin microfilaments play a critical role in endocytosis at the apical but not the basolateral surface of polarized epithelial cells. J Cell Biol 120:695–710 [View Article][PubMed]
    [Google Scholar]
  25. Grist N. R., Bell E. J., Assaad F. 1978; Enteroviruses in human disease. Prog Med Virol 24:114–157[PubMed]
    [Google Scholar]
  26. Grusche F. A., Hidalgo C., Fletcher G., Sung H. H., Sahai E., Thompson B. J. 2009; Sds22, a PP1 phosphatase regulatory subunit, regulates epithelial cell polarity and shape [Sds22 in epithelial morphology]. BMC Dev Biol 9:14 [View Article][PubMed]
    [Google Scholar]
  27. Guttman J. A., Finlay B. B. 2009; Tight junctions as targets of infectious agents. Biochim Biophys Acta 1788:832–841 [View Article][PubMed]
    [Google Scholar]
  28. Haidari M., Zhang W., Ganjehei L., Ali M., Chen Z. 2011; Inhibition of MLC phosphorylation restricts replication of influenza virus – a mechanism of action for anti-influenza agents. PLoS One 6:e21444 [View Article][PubMed]
    [Google Scholar]
  29. Ivanov A. I. 2008; Actin motors that drive formation and disassembly of epithelial apical junctions. Front Biosci 13:6662–6681 [View Article][PubMed]
    [Google Scholar]
  30. Joachims M., Harris K. S., Etchison D. 1995; Poliovirus protease 3C mediates cleavage of microtubule-associated protein 4. Virology 211:451–461 [View Article][PubMed]
    [Google Scholar]
  31. Jolly C., Mitar I., Sattentau Q. J. 2007; Requirement for an intact T-cell actin and tubulin cytoskeleton for efficient assembly and spread of human immunodeficiency virus type 1. J Virol 81:5547–5560 [View Article][PubMed]
    [Google Scholar]
  32. Kelly R. B. 1995; Ringing necks with dynamin. Nature 374:116–117 [View Article][PubMed]
    [Google Scholar]
  33. Lea S. M., Powell R. M., McKee T., Evans D. J., Brown D., Stuart D. I., van der Merwe P. A. 1998; Determination of the affinity and kinetic constants for the interaction between the human virus echovirus 11 and its cellular receptor, CD55. J Biol Chem 273:30443–30447 [View Article][PubMed]
    [Google Scholar]
  34. Lehmann M. J., Sherer N. M., Marks C. B., Pypaert M., Mothes W. 2005; Actin- and myosin-driven movement of viruses along filopodia precedes their entry into cells. J Cell Biol 170:317–325 [View Article][PubMed]
    [Google Scholar]
  35. Li E., Stupack D., Bokoch G. M., Nemerow G. R. 1998; Adenovirus endocytosis requires actin cytoskeleton reorganization mediated by Rho family GTPases. J Virol 72:8806–8812[PubMed]
    [Google Scholar]
  36. Longworth M. S., Laimins L. A. 2004; Pathogenesis of human papillomaviruses in differentiating epithelia. Microbiol Mol Biol Rev 68:362–372 [View Article][PubMed]
    [Google Scholar]
  37. Mercer J., Helenius A. 2008; Vaccinia virus uses macropinocytosis and apoptotic mimicry to enter host cells. Science 320:531–535 [View Article][PubMed]
    [Google Scholar]
  38. Miazza V., Mottet-Osman G., Startchick S., Chaponnier C., Roux L. 2011; Sendai virus induced cytoplasmic actin remodeling correlates with efficient virus particle production. Virology 410:7–16 [View Article][PubMed]
    [Google Scholar]
  39. Modlin J. F. 1986; Perinatal echovirus infection: insights from a literature review of 61 cases of serious infection and 16 outbreaks in nurseries. Rev Infect Dis 8:918–926 [View Article][PubMed]
    [Google Scholar]
  40. Moreau V., Madania A., Martin R. P., Winson B. 1996; The Saccharomyces cerevisiae actin-related protein Arp2 is involved in the actin cytoskeleton. J Cell Biol 134:117–132 [View Article][PubMed]
    [Google Scholar]
  41. Morgan M. R., Humphries M. J., Bass M. D. 2007; Synergistic control of cell adhesion by integrins and syndecans. Nat Rev Mol Cell Biol 8:957–969 [View Article][PubMed]
    [Google Scholar]
  42. Mulholland J., Preuss D., Moon A., Wong A., Drubin D., Botstein D. 1994; Ultrastructure of the yeast actin cytoskeleton and its association with the plasma membrane. J Cell Biol 125:381–391 [View Article][PubMed]
    [Google Scholar]
  43. Patel J. R., Daniel J., Mathan V. I. 1985; An epidemic of acute diarrhoea in rural southern India associated with echovirus type 11 infection. J Hyg (Lond) 95:483–492 [View Article][PubMed]
    [Google Scholar]
  44. Patel K. P., Coyne C. B., Bergelson J. M. 2009; Dynamin- and lipid raft-dependent entry of decay-accelerating factor (DAF)-binding and non-DAF-binding coxsackieviruses into nonpolarized cells. J Virol 83:11064–11077 [View Article][PubMed]
    [Google Scholar]
  45. Pelkmans L. 2005; Viruses as probes for systems analysis of cellular signalling, cytoskeleton reorganization and endocytosis. Curr Opin Microbiol 8:331–337 [View Article][PubMed]
    [Google Scholar]
  46. Powell R. M., Ward T., Evans D. J., Almond J. W. 1997; Interaction between echovirus 7 and its receptor, decay-accelerating factor (CD55): evidence for a secondary cellular factor in A-particle formation. J Virol 71:9306–9312[PubMed]
    [Google Scholar]
  47. Rhoades R. E., Tabor-Godwin J. M., Tsueng G., Feuer R. 2011; Enterovirus infections of the central nervous system. Virology 411:288–305 [View Article][PubMed]
    [Google Scholar]
  48. Rubinstein N., Chi J., Holtzer H. 1976; Coordinated synthesis and degradation of actin and myosin in a variety of myogenic and non-myogenic cells. Exp Cell Res 97:387–393 [View Article][PubMed]
    [Google Scholar]
  49. Samarin S., Nusrat A. 2009; Regulation of epithelial apical junctional complex by Rho family GTPases. Front Biosci 14:1129–1142 [View Article][PubMed]
    [Google Scholar]
  50. Schelhaas M., Ewers H., Rajamäki M. L., Day P. M., Schiller J. T., Helenius A. 2008; Human papillomavirus type 16 entry: retrograde cell surface transport along actin-rich protrusions. PLoS Pathog 4:e1000148 [View Article][PubMed]
    [Google Scholar]
  51. Selinka H. C., Giroglou T., Sapp M. 2002; Analysis of the infectious entry pathway of human papillomavirus type 33 pseudovirions. Virology 299:279–287 [View Article][PubMed]
    [Google Scholar]
  52. Shafti-Keramat S., Handisurya A., Kriehuber E., Meneguzzi G., Slupetzky K., Kirnbauer R. 2003; Different heparan sulfate proteoglycans serve as cellular receptors for human papillomaviruses. J Virol 77:13125–13135 [View Article][PubMed]
    [Google Scholar]
  53. Sherer N. M., Lehmann M. J., Jimenez-Soto L. F., Horensavitz C., Pypaert M., Mothes W. 2007; Retroviruses can establish filopodial bridges for efficient cell-to-cell transmission. Nat Cell Biol 9:310–315 [View Article][PubMed]
    [Google Scholar]
  54. Shurety W., Stewart N. L., Stow J. L. 1998; Fluid-phase markers in the basolateral endocytic pathway accumulate in response to the actin assembly-promoting drug Jasplakinolide. Mol Biol Cell 9:957–975[PubMed] [CrossRef]
    [Google Scholar]
  55. Sobo K., Rubbia-Brandt L., Brown T. D., Stuart A. D., McKee T. A. 2011; Decay-accelerating factor binding determines the entry route of echovirus 11 in polarized epithelial cells. J Virol 85:12376–12386 [View Article][PubMed]
    [Google Scholar]
  56. Spector I., Shochet N. R., Kashman Y., Groweiss A. 1983; Latrunculins: novel marine toxins that disrupt microfilament organization in cultured cells. Science 219:493–495 [View Article][PubMed]
    [Google Scholar]
  57. Stuart A. D., Eustace H. E., McKee T. A., Brown T. D. 2002a; A novel cell entry pathway for a DAF-using human enterovirus is dependent on lipid rafts. J Virol 76:9307–9322 [View Article][PubMed]
    [Google Scholar]
  58. Stuart A. D., McKee T. A., Williams P. A., Harley C., Shen S., Stuart D. I., Brown T. D., Lea S. M. 2002b; Determination of the structure of a decay accelerating factor-binding clinical isolate of echovirus 11 allows mapping of mutants with altered receptor requirements for infection. J Virol 76:7694–7704 [View Article][PubMed]
    [Google Scholar]
  59. Sun X., Whittaker G. R. 2007; Role of the actin cytoskeleton during influenza virus internalization into polarized epithelial cells. Cell Microbiol 9:1672–1682 [View Article][PubMed]
    [Google Scholar]
  60. Taylor M. P., Koyuncu O. O., Enquist L. W. 2011; Subversion of the actin cytoskeleton during viral infection. Nat Rev Microbiol 9:427–439 [View Article][PubMed]
    [Google Scholar]
  61. Tsukita S., Furuse M., Itoh M. 2001; Multifunctional strands in tight junctions. Nat Rev Mol Cell Biol 2:285–293 [View Article][PubMed]
    [Google Scholar]
  62. Urzainqui A., Carrasco L. 1989; Degradation of cellular proteins during poliovirus infection: studies by two-dimensional gel electrophoresis. J Virol 63:4729–4735[PubMed]
    [Google Scholar]
  63. Ventura K. C., Hawkins H., Smith M. B., Walker D. H. 2001; Fatal neonatal echovirus 6 infection: autopsy case report and review of the literature. Mod Pathol 14:85–90 [View Article][PubMed]
    [Google Scholar]
  64. Wells C. L., van de Westerlo E. M., Jechorek R. P., Haines H. M., Erlandsen S. L. 1998; Cytochalasin-induced actin disruption of polarized enterocytes can augment internalization of bacteria. Infect Immun 66:2410–2419[PubMed]
    [Google Scholar]
  65. Wien M. W., Chow M., Hogle J. M. 1996; Poliovirus: new insights from an old paradigm. Structure 4:763–767 [View Article][PubMed]
    [Google Scholar]
  66. Winder S. J., Ayscough K. R. 2005; Actin-binding proteins. J Cell Sci 118:651–654 [View Article][PubMed]
    [Google Scholar]
  67. Xing L., Tjarnlund K., Lindqvist B., Kaplan G. G., Feigelstock D., Cheng R. H., Casasnovas J. M. 2000; Distinct cellular receptor interactions in poliovirus and rhinoviruses. EMBO J 19:1207–1216 [View Article][PubMed]
    [Google Scholar]
  68. Yarmola E. G., Somasundaram T., Boring T. A., Spector I., Bubb M. R. 2000; Actin–latrunculin A structure and function. Differential modulation of actin-binding protein function by latrunculin A. J Biol Chem 275:28120–28127[PubMed]
    [Google Scholar]
  69. Yu K., Cheevers W. P. 1976; DNA synthesis in polyoma virus infection. V. Kinetic evidence for two requirements for protein synthesis during viral DNA replication. J Virol 17:415–421[PubMed]
    [Google Scholar]
  70. Zinchuk V., Zinchuk O., Okada T. 2007; Quantitative colocalization analysis of multicolor confocal immunofluorescence microscopy images: pushing pixels to explore biological phenomena. Acta Histochem Cytochem 40:101–111 [View Article][PubMed]
    [Google Scholar]
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