Modulation of foot-and-mouth disease virus pH threshold for uncoating correlates with differential sensitivity to inhibition of cellular Rab GTPases and decreases infectivity Free

Abstract

The role of cellular Rab GTPases that govern traffic between different endosome populations was analysed on foot-and-mouth disease virus (FMDV) infection. Changes of viral receptor specificity did not alter Rab5 requirement for infection. However, a correlation between uncoating pH and requirement of Rab5 for infection was observed. A mutant FMDV with less acidic uncoating pH threshold was less sensitive to inhibition of Rab5, whereas another mutant with more acidic requirements was more sensitive to inhibition of Rab5. On the contrary, opposed correlations between uncoating pH and dependence of Rab function were observed upon expression of dominant-negative forms of Rab7 or 11. Modulation of uncoating pH also reduced FMDV virulence in suckling mice. These results are consistent with FMDV uncoating inside early endosomes and indicate that displacements from optimum pH for uncoating reduce viral fitness .

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2012-11-01
2024-03-29
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References

  1. Baranowski E., Sevilla N., Verdaguer N., Ruiz-Jarabo C. M., Beck E., Domingo E. 1998; Multiple virulence determinants of foot-and-mouth disease virus in cell culture. J Virol 72:6362–6372[PubMed]
    [Google Scholar]
  2. Baranowski E., Ruiz-Jarabo C. M., Sevilla N., Andreu D., Beck E., Domingo E. 2000; Cell recognition by foot-and-mouth disease virus that lacks the RGD integrin-binding motif: flexibility in aphthovirus receptor usage. J Virol 74:1641–1647 [View Article][PubMed]
    [Google Scholar]
  3. Baranowski E., Molina N., Núñez J. I., Sobrino F., Sáiz M. 2003; Recovery of infectious foot-and-mouth disease virus from suckling mice after direct inoculation with in vitro-transcribed RNA. J Virol 77:11290–11295 [View Article][PubMed]
    [Google Scholar]
  4. Berryman S., Clark S., Monaghan P., Jackson T. 2005; Early events in integrin αvβ6-mediated cell entry of foot-and-mouth disease virus. J Virol 79:8519–8534 [View Article][PubMed]
    [Google Scholar]
  5. Curry S., Abrams C. C., Fry E., Crowther J. C., Belsham G. J., Stuart D. I., King A. M. 1995; Viral RNA modulates the acid sensitivity of foot-and-mouth disease virus capsids. J Virol 69:430–438[PubMed]
    [Google Scholar]
  6. Di Simone C., Buchmeier M. J. 1995; Kinetics and pH dependence of acid-induced structural changes in the lymphocytic choriomeningitis virus glycoprotein complex. Virology 209:3–9 [View Article][PubMed]
    [Google Scholar]
  7. Gerges N. Z., Brown T. C., Correia S. S., Esteban J. A. 2005; Analysis of Rab protein function in neurotransmitter receptor trafficking at hippocampal synapses. Methods Enzymol 403:153–166 [View Article][PubMed]
    [Google Scholar]
  8. Grubman M. J., Baxt B. 2004; Foot-and-mouth disease. Clin Microbiol Rev 17:465–493 [View Article][PubMed]
    [Google Scholar]
  9. Gutiérrez-Rivas M., Pulido M. R., Baranowski E., Sobrino F., Sáiz M. 2008; Tolerance to mutations in the foot-and-mouth disease virus integrin-binding RGD region is different in cultured cells and in vivo and depends on the capsid sequence context. J Gen Virol 89:2531–2539 [View Article][PubMed]
    [Google Scholar]
  10. Huotari J., Helenius A. 2011; Endosome maturation. EMBO J 30:3481–3500 [View Article][PubMed]
    [Google Scholar]
  11. Jackson T., Ellard F. M., Ghazaleh R. A., Brookes S. M., Blakemore W. E., Corteyn A. H., Stuart D. I., Newman J. W., King A. M. 1996; Efficient infection of cells in culture by type O foot-and-mouth disease virus requires binding to cell surface heparan sulfate. J Virol 70:5282–5287[PubMed]
    [Google Scholar]
  12. Johns H. L., Berryman S., Monaghan P., Belsham G. J., Jackson T. 2009; A dominant-negative mutant of rab5 inhibits infection of cells by foot-and-mouth disease virus: implications for virus entry. J Virol 83:6247–6256 [View Article][PubMed]
    [Google Scholar]
  13. Jovic M., Sharma M., Rahajeng J., Caplan S. 2010; The early endosome: a busy sorting station for proteins at the crossroads. Histol Histopathol 25:99–112[PubMed]
    [Google Scholar]
  14. Knipe T., Rieder E., Baxt B., Ward G., Mason P. W. 1997; Characterization of synthetic foot-and-mouth disease virus provirions separates acid-mediated disassembly from infectivity. J Virol 71:2851–2856[PubMed]
    [Google Scholar]
  15. Lea S., Hernández J., Blakemore W., Brocchi E., Curry S., Domingo E., Fry E., Abu-Ghazaleh R., King A.other authors 1994; The structure and antigenicity of a type C foot-and-mouth disease virus. Structure 2:123–139 [View Article][PubMed]
    [Google Scholar]
  16. Martín V., Grande-Pérez A., Domingo E. 2008; No evidence of selection for mutational robustness during lethal mutagenesis of lymphocytic choriomeningitis virus. Virology 378:185–192 [View Article][PubMed]
    [Google Scholar]
  17. Martín-Acebes M. A., González-Magaldi M., Sandvig K., Sobrino F., Armas-Portela R. 2007; Productive entry of type C foot-and-mouth disease virus into susceptible cultured cells requires clathrin and is dependent on the presence of plasma membrane cholesterol. Virology 369:105–118 [View Article][PubMed]
    [Google Scholar]
  18. Martín-Acebes M. A., González-Magaldi M., Rosas M. F., Borrego B., Brocchi E., Armas-Portela R., Sobrino F. 2008; Subcellular distribution of swine vesicular disease virus proteins and alterations induced in infected cells: a comparative study with foot-and-mouth disease virus and vesicular stomatitis virus. Virology 374:432–443 [View Article][PubMed]
    [Google Scholar]
  19. Martín-Acebes M. A., González-Magaldi M., Vázquez-Calvo A., Armas-Portela R., Sobrino F. 2009; Internalization of swine vesicular disease virus into cultured cells: a comparative study with foot-and-mouth disease virus. J Virol 83:4216–4226 [View Article][PubMed]
    [Google Scholar]
  20. Martín-Acebes M. A., Rincón V., Armas-Portela R., Mateu M. G., Sobrino F. 2010; A single amino acid substitution in the capsid of foot-and-mouth disease virus can increase acid lability and confer resistance to acid-dependent uncoating inhibition. J Virol 84:2902–2912 [View Article][PubMed]
    [Google Scholar]
  21. Martín-Acebes M. A., Vázquez-Calvo A., Rincón V., Mateu M. G., Sobrino F. 2011; A single amino acid substitution in the capsid of foot-and-mouth disease virus can increase acid resistance. J Virol 85:2733–2740 [View Article][PubMed]
    [Google Scholar]
  22. Muench R. L. J. H. 1935; A simple method of estimating fifty percent endpoints. Am J Hyg 27:493–497
    [Google Scholar]
  23. Núñez J. I., Molina N., Baranowski E., Domingo E., Clark S., Burman A., Berryman S., Jackson T., Sobrino F. 2007; Guinea pig-adapted foot-and-mouth disease virus with altered receptor recognition can productively infect a natural host. J Virol 81:8497–8506 [View Article][PubMed]
    [Google Scholar]
  24. O’Donnell V., LaRocco M., Duque H., Baxt B. 2005; Analysis of foot-and-mouth disease virus internalization events in cultured cells. J Virol 79:8506–8518 [View Article][PubMed]
    [Google Scholar]
  25. O’Donnell V., Larocco M., Baxt B. 2008; Heparan sulfate-binding foot-and-mouth disease virus enters cells via caveola-mediated endocytosis. J Virol 82:9075–9085 [View Article][PubMed]
    [Google Scholar]
  26. Poteryaev D., Datta S., Ackema K., Zerial M., Spang A. 2010; Identification of the switch in early-to-late endosome transition. Cell 141:497–508 [View Article][PubMed]
    [Google Scholar]
  27. Quirin K., Eschli B., Scheu I., Poort L., Kartenbeck J., Helenius A. 2008; Lymphocytic choriomeningitis virus uses a novel endocytic pathway for infectious entry via late endosomes. Virology 378:21–33 [View Article][PubMed]
    [Google Scholar]
  28. Ruiz-Sáenz J., Goez Y., Tabares W., López-Herrera A. 2009; Cellular receptors for foot and mouth disease virus. Intervirology 52:201–212 [View Article][PubMed]
    [Google Scholar]
  29. Sáiz M., Núñez J. I., Jimenez-Clavero M. A., Baranowski E., Sobrino F. 2002; Foot-and-mouth disease virus: biology and prospects for disease control. Microbes Infect 4:1183–1192 [View Article][PubMed]
    [Google Scholar]
  30. Schwartz S. L., Cao C., Pylypenko O., Rak A., Wandinger-Ness A. 2007; Rab GTPases at a glance. J Cell Sci 120:3905–3910 [View Article][PubMed]
    [Google Scholar]
  31. Sobrino F., Dávila M., Ortín J., Domingo E. 1983; Multiple genetic variants arise in the course of replication of foot-and-mouth disease virus in cell culture. Virology 128:310–318 [View Article][PubMed]
    [Google Scholar]
  32. Urata S., Yun N., Pasquato A., Paessler S., Kunz S., de la Torre J. C. 2011; Antiviral activity of a small-molecule inhibitor of arenavirus glycoprotein processing by the cellular site 1 protease. J Virol 85:795–803 [View Article][PubMed]
    [Google Scholar]
  33. Vázquez-Calvo A., Saiz J. C., McCullough K. C., Sobrino F., Martín-Acebes M. A. 2012; Acid-dependent viral entry. Virus Res 167:125–137 [View Article][PubMed]
    [Google Scholar]
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