Dynamic changes in viral population structure and compartmentalization during chronic hepatitis C virus infection in children

Virology

Volumn 447, Issue 1-2, 2013, Pages 187-196

  Gismondi, María Inés ^a   Díaz Carrasco, Juan María ^a   Valva, Pamela ^a   Becker, Pablo Daniel ^c   Guzmán, Carlos Alberto ^c   Campos, Rodolfo Héctor ^b   Preciado, María Victoria ^a  

^a HOSPITAL DE NIÑOS RICARDO GUTIÉRREZ   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

Author keywords

Compartmentalization; Evolution; Hepatitis C virus; PBMC; Pediatric infection; Population structure

Indexed keywords

ALANINE AMINOTRANSFERASE; ALPHA INTERFERON; VIRUS RNA;

ADOLESCENT; ALANINE AMINOTRANSFERASE BLOOD LEVEL; ARTICLE; BAYES THEOREM; CELL COMPARTMENTALIZATION; CHILD; CLINICAL ARTICLE; CLINICAL FEATURE; COEVOLUTION; CONTROLLED STUDY; FEMALE; GENETIC VARIABILITY; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; LIVER BIOPSY; MALE; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PERIPHERAL BLOOD MONONUCLEAR CELL; PHYLOGENY; POPULATION STRUCTURE; PRESCHOOL CHILD; PRIORITY JOURNAL; RETROSPECTIVE STUDY; SCHOOL CHILD; SEQUENCE ANALYSIS;

COMPARTMENTALIZATION; EVOLUTION; HEPATITIS C VIRUS; PBMC; PEDIATRIC INFECTION; POPULATION STRUCTURE;

ADOLESCENT; BIOTA; CHILD; CHILD, PRESCHOOL; CLUSTER ANALYSIS; FEMALE; GENETIC VARIATION; HEPACIVIRUS; HEPATITIS C, CHRONIC; HUMANS; LEUKOCYTES, MONONUCLEAR; MALE; MOLECULAR SEQUENCE DATA; PHYLOGENY; PLASMA; RETROSPECTIVE STUDIES; RNA, VIRAL; SEQUENCE ANALYSIS, DNA;

EID: 84884954835     PISSN: 00426822     EISSN: 10960341     Source Type: Journal    
DOI: 10.1016/j.virol.2013.09.002     Document Type: Article

References (67)

1. Alfonso V., Mbayed V.A., Sookoian S., Campos R.H. Intra-host evolutionary dynamics of hepatitis C virus in treated patients. J. Gen. Virol. 2005, 86:2781-2786.
2. HCV Sequence Database. Available from:. http://www.hcv.lanl.gov.
3. Bandelt H.J., Forster P., Röhl A. Median-joining networks for inferring intraspecific phylogenies. Mol. Biol. Evol. 1999, 16(1):37-48.
4. Bankwitz D., Steinmann E., Bitzegeio J., Ciesek S., Friesland M., Herrmann E., et al. Hepatitis C virus hypervariable region 1 modulates receptor interactions, conceals the CD81 binding site, and protects conserved neutralizing epitopes. J. Virol. 2010, 84(11):5751-5763.
5. Bartosch B., Cosset F.L. Cell entry of hepatitis C virus. Virology 2006, 348(1):1-12.
6. Bartosch B., Bukh J., Meunier J.C., Granier C., Engle R.E., Blackwelder W.C., et al. In vitro assay for neutralizing antibody to hepatitis C virus: evidence for broadly conserved neutralization epitopes. Proc. Natl. Acad. Sci. U.S.A. 2003, 100:14199-14204.
7. Bartosch B., Verney G., Dreux M., Donot P., Morice Y., Penin F., et al. An interplay between hypervariable region 1 of the hepatitis C virus E2 glycoprotein, the scavenger receptor BI, and high-density lipoprotein promotes both enhancement of infection and protection against neutralizing antibodies. J. Virol. 2005, 79(13):8217-8229.
8. Blackard J.T., Hiasa Y., Smeaton L., Jamieson D.J., Rodriguez I., Mayer K.H., et al. Compartmentalization of hepatitis C virus (HCV) during HCV/HIV coinfection. J. Infect. Dis. 2007, 195:1765-1773.
9. Bortolotti F., Verucchi G., Camma C., Cabibbo G., Zancan L., Indolfi G., et al. Long-term course of chronic hepatitis C in children: from viral clearance to end-stage liver disease. Gastroenterology 2008, 134(7):1900-1907.
10. Corander J., Marttinen P., Sirén J., Tang J. Enhanced Bayesian modelling in BAPS software for learning genetic structures of populations. BMC Bioinf. 2008, 9:539.
11. Crooks G.E., Hon G., Chandonia J.M., Brenner S.E. WebLogo: a sequence logo generator. Genome Res. 2004, 14:1188-1190.
12. Delport W., Poon A.F., Frost S.D.W., Kosakovsky Pond S.L. Datamonkey 2010: a suite of phylogenetic analysis tools for evolutionary biology. Bioinformatics 2010, 26(19):2455-2457.
13. Drummond A.J., Rambaut A. BEAST: Bayesian evolutionary analysis by sampling trees. BMC Evol. Biol. 2007, 7:214.
14. Durand T., Di Liberto G., Colman H., Cammas A., Boni S., Marcellin P., et al. Occult infection of peripheral B cells by hepatitis C variants which have low translational efficiency in cultured hepatocytes. Gut 2010, 59(7):934-942.
15. Farci P., Shimoda A., Wong D., Cabezon T., De Gioannis D., Strazzera A., et al. Prevention of hepatitis C virus infection in chimpanzees by hyperimmune serum against the hypervariable region 1 of the envelope 2 protein. Proc. Natl. Acad. Sci. U. S. A. 1996, 93(26):15394-15399.
16. Farci P., Quinti I., Farci S., Alter H.J., Strazzera R., Palomba E., et al. Evolution of hepatitis C viral quasispecies and hepatic injury in perinatally infected children followed prospectively. Proc. Natl. Acad. Sci. 2006, 103(22):8475-8480.
17. Farci P., Wollenberg K., Diaz G., Engle R.E., Lai M.E., Klenerman P., et al. Profibrogenic chemokines and viral evolution predict rapid progression of hepatitis C to cirrhosis. Proc. Natl. Acad. Sci. U. S. A. 2012, 109(36):14562-14567.
18. Figlerowicz M., Jackowiak P., Formanowicz P., Kedziora P., Alejska M., Malinowska N., et al. Hepatitis C virus quasispecies in chronically infected children subjected to interferon-ribavirin therapy. Arch. Virol. 2010, 155(12):1977-1987.
19. Forton D.M., Karayiannis P., Mahmud N., Taylor-Robinson S., Thomas H.C. Identification of unique hepatitis C virus quasispecies in the central nervous system and comparative analysis of internal translational efficiency of brain, liver, and serum variants. J. Virol. 2004, 78(10):5170-5183.
20. Ghany M.G., Strader D.B., Thomas D.L., Seeff L.B. Diagnosis, management, and treatment of hepatitis C: an update. Hepatology 2009, 49(4):1335-1374.
21. Gismondi M.I., Turazza E.I., Grinstein S., Galoppo M.C., Preciado M.V. Hepatitis C virus infection in infants and children from Argentina. J. Clin. Microbiol. 2004, 42(3):1199-1202.
22. Gismondi M.I., Becker P.D., Díaz Carrasco J.M., Guzmán C.A., Campos R.H., Preciado M.V. Evolution of hepatitis C virus hypervariable region 1 in immunocompetent children born to HCV-infected mothers. J. Viral Hepat. 2009, 16:332-339.
23. Goutagny N., Fatmi A., De Ledinghen V., Penin F., Couzigou P., Inchauspe G., et al., 2003. Evidence of viral replication in circulating dendritic cells during hepatitis C virus infection. J. Infect. Dis. 187(12), 1951-1958.
24. Gray R.R., Salemi M., Klenerman P., Pybus O.G. A new evolutionary model for hepatitis C virus chronic infection. PLoS Pathog. 2012, 8(5):e1002656.
25. Guan M., Wang W., Liu X., Tong Y., Liu Y., Ren H., et al. Three Different Functional Microdomains in the Hepatitis C Virus Hypervariable Region 1 (HVR1) Mediate Entry and Immune Evasion. J. Biol. Chem. 2012, 287(42):35631-35645.
26. Guindon S., Gascuel O. A simple, fast, and accurate algorithm to estimate large phylogenies by maximum likelihood. Syst. Biol. 2003, 52(5):696-704.
27. Hijikata M., Kato N., Ootsuyama Y., Nakagawa M., Ohkoshi S., Shimotohno K. Hypervariable regions in the putative glycoprotein of hepatitis C virus. Biochem. Biophys. Res. Commun. 1991, 175(1):220-228.
28. Jackowiak P., Kowala-Piaskowska A., Figlerowicz M., Alejska M., Malinowska N. Evolution of hepatitis C virus hypervariable region 1 in chronically infected children. Virus Res. 2012, 167(2):380-384.
29. Jara P., Resti M., Hierro L., Giacchino R., Barbera C., Zancan L., et al. Chronic hepatitis C virus infection in childhood: clinical patterns and evolution in 224 white children. Clin. Infect. Dis. 2003, 36(3):275-280.
30. Jonas M.M. Children with hepatitis C. Hepatology 2002, 36(5 Suppl. 1):S173-S178.
31. Jouvencel A.M., Neau D., Faure M., Neau M., Martinaud C., Legrand E., et al. Plasma and liver hepatitis C virus variability in patients coinfected with human immunodeficiency virus. J. Clin. Microl. 2006, 44(5):1877-1880.
32. Kosakovsky Pond S.L. Frost SDW. Not so different after all: a comparison of methods for detecting amino acid sites under selection. Mol. Biol. Evol. 2005, 22(5):1208-1222.
33. Lerat H., Rumin S., Habersetzer F., Berby F., Trabaud M., Trépo C., et al. In vivo tropism of hepatitis C virus genomic sequences in haematopoietic cells: influence of viral load, viral genotype, and cell phenotype. Blood 1998, 91(10):3841-3849.
34. Li H., McMahon B.J., McArdle S., Bruden D., Sullivan D.G., Shelton D., et al. Hepatitis C virus envelope glycoprotein co-evolutionary dynamics during chronic hepatitis C. Virology 2008, 375(2):80-91.
35. Martell M., Esteban J.I., Quer J., Genesca J., Weiner A., Esteban R., et al. Hepatitis C virus (HCV) circulates as a population of different but closely related genomes: quasispecies nature of HCV genome distribution. J. Virol. 1992, 66(5):3225-3229.
36. Marukian S., Jones C.T., Andrus L., Evans M.J., Ritola K.D., Charles E.D., et al. Cell culture-produced hepatitis C virus does not infect peripheral blood mononuclear cells. Hepatology 2008, 48(6):1843-1850.
37. Mohan N., González-Peralta R.P., Fujisawa T., Chang M.H., Heller S., Jara P., et al. Chronic hepatitis C virus infection in children. J. Pediatr. Gastroenterol. Nutr. 2010, 50(2):123-131.
38. Murrell B., Wertheim J.O., Moola S., Weighill T., Scheffler K., Kosakovsky Pond S.L. Detecting individual sites subject to episodic diversifying selection. PLoS Genet. 2012, 8(7):e10022764.
39. Natarajan V., Kottilil S., Hazen A., Adelsberger J., Murphy A.A., Polis M.A., et al. HCV in peripheral blood mononuclear cells are predominantly carried on the surface of cells in HIV/HCV co-infected individuals. J. Med. Virol. 2010, 82(12):2032-2037.
40. Op De Beeck A, Cocquerel L., Dubuisson J. Biogenesis of hepatitis C virus envelope glycoproteins. J. Gen. Virol. 2001, 82(Pt. 11):2589-2595.
41. Pal S., Sullivan D.G., Kim S., Lai K.K., Kae J., Cotler S.J., et al. Productive replication of HCV in perihepatic lymph nodes in vivo: implications for HCV lymphotropism. Gastroenterology 2005, 130(4):1107-1116.
42. Palmer B.A., Moreau I., Levis J., Harty C., Crosbie O., Kenny-Walsh E., et al. Insertion and recombination events at the HVR1 over 9.6 years of hepatitis C virus chronic infection. J. Gen. Virol. 2012, 93(Pt. 12):2614-2624.
43. Parker J., Rambaut A., Pybus O.G. Correlating viral phenotypes with phylogeny: accounting for phylogenetic uncertainty. Infect., Genet. Evol. 2008, 8(3):239-246.
44. Penin F., Combet C., Germanidis G., Frainais P.O., Deleage G., Pawlotsky J.M. Conservation of the conformation and positive charges of hepatitis C virus E2 envelope glycoprotein hypervariable region 1 points to a role in cell attachment. J. Virol. 2001, 75(12):703-5710.
45. Pham T.N.Q., MacParland S.A., Mulrooney P.M., Cooksley H., Naoumov N.V., Michalak T.I. Hepatitis C virus persistence after spontaneous or treatment-induced resolution of hepatitis C. J. Virol. 2004, 78(11):5867-5874.
46. Pham T.N.Q., King D., MacParland S.A., McGrath J.S., Reddy S.B., Bursey F.R., et al. Hepatitis C virus replicates in the same immune subsets in chronic hepatitis C and occult infection. Gastroenterology 2008, 13:812-822.
47. Posada D. jModelTest: phylogenetic model averaging. Mol. Biol. Evol. 2008, 25:1253-1256.
48. Qin H., Shire N.J., Keenan E.D., Rouster S.D., Eyster M.E., Goedert J.J., et al. HCV quasispecies evolution: association with progression to end-stage liver disease in hemophiliacs infected with HCV or HCV/HIV. Blood 2005, 105(2):533-541.
49. Quesnel-Vallieres M., Lemay M., Lapointe N., Martin S.R., Soudeyns H. HCV quasispecies evolution during treatment with interferon alfa-2b and ribavirin in two children coinfected with HCV and HIV-1. J. Clin. Virol. 2008, 43(2):236-240.
50. Radkowski M., Wilkinson J., Nowicki M., Adair D., Vargas H., Ingui C., et al. Search for hepatitis C virus negative-strand RNA sequences and analysis of viral sequences in the central nervous system: evidence of replication. J. Virol. 2002, 76(2):600-608.
51. Ramachandran S., Campo D.S., Dimitrova Z.E., Xia G.L., Purdy M.A., Khudyakov Y.E. Temporal variations in the hepatitis C virus intrahost population during chronic infection. J. Virol. 2011, 85(13):6369-6380.
52. Ramírez S., Pérez-del-Pulgar S., Carrión J.A., Costa J., González P., Massaguer A., et al. Hepatitis C virus compartmentalization and infection recurrence after liver transplantation. Am. J. Transplant. 2009, 9(7):1591-1601.
53. Rehermann B. Hepatitis C virus versus innate and adaptive immune responses: a tale of coevolution and coexistence. J. Clin. Invest. 2009, 119(7):1745-1754.
54. Roccasecca R.M., Ansuini H., Vitelli A., Meola A., Scarselli E., Acali S., et al. Binding of the hepatitis C virus E2 glycoprotein to CD81 is strain specific and is modulated by a complex interplay between hypervariable regions 1 and 2. J. Virol. 2003, 77(3):1856-1867.
55. Roque-Afonso A.M., Ducoulombier D., Di Liberto G., Kara R., Gigou M., Dussaix E., et al. Compartmentalization of hepatitis C virus genotypes between plasma and peripheral blood mononuclear cells. J. Virol. 2005, 79(10):6349-6357.
56. Sambrook J., Russell D. Molecular Cloning: A Laboratory Manual 2001, Cold Spring Harbor Laboratory Press, New York. third ed.
57. Schramm F., Soulier E., Royer C., Weitten T., Fafi-Kremer S., Brignon N., et al. Frequent compartmentalization of hepatitis C virus with leukocyte-related amino acids in the setting of liver transplantation. J. Infect. Dis. 2008, 198(11):1656-1666.
58. Shimizu Y.K., Igarashi H., Kiyohara T., Cabezon T., Farci P., Purcell R.H., et al. A hyperimmune serum against a synthetic peptide corresponding to the hypervariable region 1 of hepatitis C virus can prevent viral infection in cell cultures. Virology 1996, 223(2):409-412.
59. Slatkin M., Maddison W.P. A cladistic measure of gene flow inferred from the phylogenies of alleles. Genetics 1989, 123(3):603-613.
60. Smith D. Evolution of the hypervariable region of hepatitis C virus. J. Viral Hepat. 1999, 6(1):41-46.
61. Stumpf M.P.H., Pybus O.G. Genetic diversity and models of viral evolution for the hepatitis C virus. FEMS Microbiol. Lett. 2002, 2002(214):143-152.
62. Sullivan D.G., Bruden D., Deubner H., McArdle S., Chung M., Christensen C., et al. Hepatitis C virus dynamics during natural infection are associated with long-term histological outcome of chronic hepatitis C disease. J. Infect. Dis. 2007, 196(2):239-248.
63. Theise N., Bordenheimer H., Ferrel L. Acute and chronic viral hepatitis. MacSweens Pathology of the liver 2007, cap 8:418-419. Churchill-Livingstone, London. 5th ed.
64. Thompson J.D., Gibson T.J., Plewniak F., Jeanmougin F., Higgins D.G. The ClustalX windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 24:4876-4882.
65. Vera-Otarola J., Barría M.I., León U., Marsac D., Carvallo P., Soza A., et al. Hepatitis C virus quasispecies in plasma and peripheral blood mononuclear cells of treatment naïve chronically infected patients. J. Viral Hepat. 2009, 16(9):633-643.
66. Wilkinson J., Radkowski M., Laskus T. Hepatitis C virus neuroinvasion: identification of infected cells. J. Virol. 2009, 83(3):1312-1319.
67. Zehender G., Meroni L., De Maddalena C., Varchetta S., Monti G., Galli M. Detection of hepatitis C virus RNA in CD19 peripheral blood mononuclear cells of chronically infected patients. J. Infect. Dis. 1997, 176:1209-1214.