1887

Abstract

The allocation of liver grafts from hepatitis C virus (HCV)-positive donors in HCV-infected liver transplant (LT) recipients leads to infection with two different viral populations. In a previous study, we examined quasispecies dynamics during reinfection by clonal sequencing, which did not allow an accurate characterization of coexistence and competition events. To overcome this limitation, here we used deep-sequencing analysis of a fragment of the HCV NS5B gene in six HCV-infected LT recipients who received HCV-infected grafts. Successive expansions and contractions of quasispecies complexity were observed, evolving in all cases towards a more homogeneous population. The population that became dominant was the one displaying the highest mutant spectrum complexity. In four patients, coexistence of minority mutants, derived from the donor or the recipient, were detected. In conclusion, our study shows that, during reinfection with a different HCV strain in LT recipients, the viral population with the highest diversity always becomes dominant.

Loading

Article metrics loading...

/content/journal/jgv/10.1099/jgv.0.000289
2015-12-01
2024-04-19
Loading full text...

Full text loading...

/deliver/fulltext/jgv/96/12/3493.html?itemId=/content/journal/jgv/10.1099/jgv.0.000289&mimeType=html&fmt=ahah

References

  1. Bartels D. J., Zhou Y., Zhang E. Z., Marcial M., Byrn R. A., Pfeiffer T., Tigges A. M., Adiwijaya B. S., Lin C., other authors. 2008; Natural prevalence of hepatitis C virus variants with decreased sensitivity to NS3.4A protease inhibitors in treatment-naive subjects. J Infect Dis 198:800–807 [View Article][PubMed]
    [Google Scholar]
  2. Bartels D. J., Sullivan J. C., Zhang E. Z., Tigges A. M., Dorrian J. L., De Meyer S., Takemoto D., Dondero E., Kwong A. D., other authors. 2013; Hepatitis C virus variants with decreased sensitivity to direct-acting antivirals (DAAs) were rarely observed in DAA-naive patients prior to treatment. J Virol 87:1544–1553 [View Article][PubMed]
    [Google Scholar]
  3. Briones C., Domingo E. 2008; Minority report: hidden memory genomes in HIV-1 quasispecies and possible clinical implications. AIDS Rev 10:93–109[PubMed]
    [Google Scholar]
  4. Clarke D. K., Duarte E. A., Elena S. F., Moya A., Domingo E., Holland J. 1994; The red queen reigns in the kingdom of RNA viruses. Proc Natl Acad Sci U S A 91:4821–4824 [View Article][PubMed]
    [Google Scholar]
  5. Domingo E., Escarmís C., Sevilla N., Moya A., Elena S. F., Quer J., Novella I. S., Holland J. J. 1996; Basic concepts in RNA virus evolution. FASEB J 10:859–864[PubMed]
    [Google Scholar]
  6. Domingo E., Sheldon J., Perales C. 2012; Viral quasispecies evolution. Microbiol Mol Biol Rev 76:159–216 [View Article][PubMed]
    [Google Scholar]
  7. Eyster M. E., Sherman K. E., Goedert J. J., Katsoulidou A., Hatzakis A. 1999; Prevalence and changes in hepatitis C virus genotypes among multitransfused persons with hemophilia. The Multicenter Hemophilia Cohort Study. J Infect Dis 179:1062–1069 [View Article][PubMed]
    [Google Scholar]
  8. Fan X., Lang D. M., Xu Y., Lyra A. C., Yusim K., Everhart J. E., Korber B. T. M., Perelson A. S., Di Bisceglie A. M. 2003; Liver transplantation with hepatitis C virus-infected graft: interaction between donor and recipient viral strains. Hepatology 38:25–33 [View Article][PubMed]
    [Google Scholar]
  9. Farci P. 2011; New insights into the HCV quasispecies and compartmentalization. Semin Liver Dis 31:356–374 [View Article][PubMed]
    [Google Scholar]
  10. Feliu A., Gay E., García-Retortillo M., Saiz J. C., Forns X. 2004; Evolution of hepatitis C virus quasispecies immediately following liver transplantation. Liver Transpl 10:1131–1139 [View Article][PubMed]
    [Google Scholar]
  11. Felsenstein J. 2004 Inferring Phylogenies Sunderland: Sinauer Associates;
    [Google Scholar]
  12. Gaud U., Langer B., Petropoulou T., Thomas H. C., Karayiannis P. 2003; Changes in hypervariable region 1 of the envelope 2 glycoprotein of hepatitis C virus in children and adults with humoral immune defects. J Med Virol 69:350–356 [View Article][PubMed]
    [Google Scholar]
  13. Gause G. 1932; Experimental studies on the struggle for existence I. Mixed population of two species of yeast. J Exp Biol 9:389–402
    [Google Scholar]
  14. Gregori J., Esteban J. I., Cubero M., Garcia-Cehic D., Perales C., Casillas R., Alvarez-Tejado M., Rodríguez-Frías F., Guardia J., other authors. 2013; Ultra-deep pyrosequencing (UDPS) data treatment to study amplicon HCV minor variants. PLoS One 8:e83361 [View Article][PubMed]
    [Google Scholar]
  15. Gregori J., Salicrú M., Domingo E., Sanchez A., Esteban J. I., Rodríguez-Frías F., Quer J. 2014; Inference with viral quasispecies diversity indices: clonal and NGS approaches. Bioinformatics 30:1104–1111 [View Article][PubMed]
    [Google Scholar]
  16. Hardin G. 1960; The competitive exclusion principle. Science 131:1292–1297 [View Article][PubMed]
    [Google Scholar]
  17. Herring B. L., Page-Shafer K., Tobler L. H., Delwart E. L. 2004; Frequent hepatitis C virus superinfection in injection drug users. J Infect Dis 190:1396–1403 [View Article][PubMed]
    [Google Scholar]
  18. Hughes M. G. J. Jr, Rudy C. K., Chong T. W., Smith R. L., Evans H. L., Iezzoni J. C., Sawyer R. G., Pruett T. L. 2004; E2 quasispecies specificity of hepatitis C virus association with allografts immediately after liver transplantation. Liver Transpl 10:208–216 [View Article][PubMed]
    [Google Scholar]
  19. Laskus T., Wang L. F., Rakela J., Vargas H., Pinna A. D., Tsamandas A. C., Demetris A. J., Fung J. 1996; Dynamic behavior of hepatitis C virus in chronically infected patients receiving liver graft from infected donors. Virology 220:171–176 [View Article][PubMed]
    [Google Scholar]
  20. Laskus T., Wang L. F., Radkowski M., Nowicki M., Wilkinson J., Rakela J. 2001; Exposure of hepatitis C virus-negative recipients to ≥ 2 infected blood donors. J Infect Dis 183:666–669 [View Article][PubMed]
    [Google Scholar]
  21. Le Pogam S., Seshaadri A., Kosaka A., Chiu S., Kang H., Hu S., Rajyaguru S., Symons J., Cammack N., Nájera I. 2008; Existence of hepatitis C virus NS5B variants naturally resistant to non-nucleoside, but not to nucleoside, polymerase inhibitors among untreated patients. J Antimicrob Chemother 61:1205–1216 [View Article][PubMed]
    [Google Scholar]
  22. Mao Q., Ray S. C., Laeyendecker O., Ticehurst J. R., Strathdee S. A., Vlahov D., Thomas D. L. 2001; Human immunodeficiency virus seroconversion and evolution of the hepatitis C virus quasispecies. J Virol 75:3259–3267 [View Article][PubMed]
    [Google Scholar]
  23. Mensa L., Pérez-del-Pulgar S., Crespo G., Koutsoudakis G., Fernández-Carrillo C., Coto-Llerena M., Miquel R., Allende H., Castells L., other authors. 2013; Imaging of hepatitis C virus infection in liver grafts after liver transplantation. J Hepatol 59:271–278 [View Article][PubMed]
    [Google Scholar]
  24. Nichol S. T., Rowe J. E., Fitch W. M. 1993; Punctuated equilibrium and positive Darwinian evolution in vesicular stomatitis virus. Proc Natl Acad Sci U S A 90:10424–10428 [View Article][PubMed]
    [Google Scholar]
  25. Novella I. S., Holland J. J., Elena S. F., Moya A., Domingo E. 1996; Repeated transfer of small RNA virus populations leading to balanced fitness with infrequent stochastic drift. Mol Gen Genet 252:733–738 [View Article][PubMed]
    [Google Scholar]
  26. Ohtsuru S., Ueda Y., Marusawa H., Inuzuka T., Nishijima N., Nasu A., Shimizu K., Koike K., Uemoto S., Chiba T. 2013; Dynamics of defective hepatitis C virus clones in reinfected liver grafts in liver transplant recipients: ultradeep sequencing analysis. J Clin Microbiol 51:3645–3652 [View Article][PubMed]
    [Google Scholar]
  27. Ojosnegros S., Agudo R., Sierra M., Briones C., Sierra S., González-López C., Domingo E., Cristina J. 2008; Topology of evolving, mutagenized viral populations: quasispecies expansion, compression, and operation of negative selection. BMC Evol Biol 8:207 [View Article][PubMed]
    [Google Scholar]
  28. Perales C., Henry M., Domingo E., Wain-Hobson S., Vartanian J. -P. 2011; Lethal mutagenesis of foot-and-mouth disease virus involves shifts in sequence space. J Virol 85:12227–12240 [View Article][PubMed]
    [Google Scholar]
  29. Quer J., Huerta R., Novella I. S., Tsimring L., Domingo E., Holland J. J. 1996; Reproducible nonlinear population dynamics and critical points during replicative competitions of RNA virus quasispecies. J Mol Biol 264:465–471 [View Article][PubMed]
    [Google Scholar]
  30. Quer J., Gregori J., Rodríguez-Frias F., Buti M., Madejon A., Pérez-del-Pulgar S., Garcia-Cehic D., Casillas R., Blasi M., other authors. 2015; High-resolution hepatitis C virus subtyping using NS5B deep sequencing and phylogeny, an alternative to current methods. J Clin Microbiol 53:219–226 [View Article][PubMed]
    [Google Scholar]
  31. Ramírez S., Pérez-del-Pulgar S., Carrion J. A., Costa J., Gonzalez P., Massaguer A., Fondevila C., Garcia-Valdecasas J. C., Navasa M., Forns X. 2009; Hepatitis C virus compartmentalization and infection recurrence after liver transplantation. Am J Transplant 9:1591–1601 [View Article][PubMed]
    [Google Scholar]
  32. Ramírez S., Pérez-del-Pulgar S., Carrión J. A., Coto-Llerena M., Mensa L., Dragun J., García-Valdecasas J. C., Navasa M., Forns X. 2010; Hepatitis C virus superinfection of liver grafts: a detailed analysis of early exclusion of non-dominant virus strains. J Gen Virol 91:1183–1188 [View Article][PubMed]
    [Google Scholar]
  33. Rencher A. C. 2002 Methods of Multivariate Analysis, 2nd edn. New York: John Wiley & Sons; [CrossRef]
    [Google Scholar]
  34. Ruiz-Jarabo C. M., Arias A., Baranowski E., Escarmís C., Domingo E. 2000; Memory in viral quasispecies. J Virol 74:3543–3547 [View Article][PubMed]
    [Google Scholar]
  35. Schvoerer E., Soulier E., Royer C., Renaudin A. -C., Thumann C., Fafi-Kremer S., Brignon N., Doridot S., Meyer N., other authors. 2007; Early evolution of hepatitis C virus (HCV) quasispecies after liver transplant for HCV-related disease. J Infect Dis 196:528–536 [View Article][PubMed]
    [Google Scholar]
  36. Vargas H. E., Laskus T., Wang L. F., Lee R., Radkowski M., Dodson F., Fung J. J., Rakela J. 1999; Outcome of liver transplantation in hepatitis C virus-infected patients who received hepatitis C virus-infected grafts. Gastroenterology 117:149–153 [View Article][PubMed]
    [Google Scholar]
  37. Wieland S., Makowska Z., Campana B., Calabrese D., Dill M. T., Chung J., Chisari F. V., Heim M. H. 2014; Simultaneous detection of hepatitis C virus and interferon stimulated gene expression in infected human liver. Hepatology 59:2121–2130 [View Article][PubMed]
    [Google Scholar]
  38. Zuckerkandl E., Pauling L. B. 1962; Molecular disease, evolution, and genetic heterogeneity. In Horizons in Biochemistry pp. 189–225 Edited by Kasha M., Pullman B. New York: Academic Press;
    [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/jgv/10.1099/jgv.0.000289
Loading
/content/journal/jgv/10.1099/jgv.0.000289
Loading

Data & Media loading...

Supplements

Supplementary Data

PDF
This is a required field
Please enter a valid email address
Approval was a Success
Invalid data
An Error Occurred
Approval was partially successful, following selected items could not be processed due to error