Deep sequencing identifies two genotypes and high viral genetic diversity of human pegivirus (GB virus C) in rural Ugandan patients

Journal of General Virology

Volumn 94, Issue PART 12, 2013, Pages 2670-2678

  Ghai, Ria R ^a   Sibley, Samuel D ^b   Lauck, Michael ^c   Dinis, Jorge M ^b   Bailey, Adam L ^c   Chapman, Colin A ^d,e   Omeja, Patrick ^f   Friedrich, Thomas C ^b,g   O'Connor, David H ^c   Goldberg, Tony L ^b,f,g  

^a MCGILL UNIVERSITY   (Canada)

^b UNIVERSITY OF WISCONSIN MADISON   (United States)

^c UNIVERSITY OF WISCONSIN SCHOOL OF MEDICINE AND PUBLIC HEALTH   (United States)

^d MCGILL UNIVERSITY   (Canada)

^e WILDLIFE CONSERVATION SOCIETY   (United States)

^f MAKERERE UNIVERSITY   (Uganda)

^g UNIVERSITY OF WISCONSIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADOLESCENT; ADULT; ARTICLE; CLINICAL ARTICLE; FEMALE; GENE FREQUENCY; GENE SEQUENCE; GENETIC VARIABILITY; GENOTYPE; HEPATITIS C VIRUS; HEPATITIS G VIRUS; HUMAN; MALE; NUCLEOTIDE SEQUENCE; PHYLOGENETIC TREE; PRIORITY JOURNAL; RURAL AREA; SINGLE NUCLEOTIDE POLYMORPHISM; UGANDA; VIRAL GENETICS; VIRUS GENOME;

ADOLESCENT; ADULT; ANIMALS; FEMALE; FLAVIVIRIDAE INFECTIONS; GB VIRUS C; GENETIC VARIATION; GENOME, VIRAL; GENOTYPE; HEPATITIS, VIRAL, HUMAN; HIGH-THROUGHPUT NUCLEOTIDE SEQUENCING; HIV INFECTIONS; HUMANS; MALE; MIDDLE AGED; MOLECULAR SEQUENCE DATA; RURAL POPULATION; SEQUENCE ANALYSIS, DNA; UGANDA; YOUNG ADULT;

EID: 84887540310     PISSN: 00221317     EISSN: 14652099     Source Type: Journal    
DOI: 10.1099/vir.0.055509-0     Document Type: Article

References (74)

1. Abascal, F., Zardoya, R. & Telford, M. J. (2010). TranslatorX: multiple alignment of nucleotide sequences guided by amino acid translations. Nucleic Acids Res 38 (Web Server issue), W7-13.
2. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. (1990). Basic local alignment search tool. J Mol Biol 215, 403-410.
3. Bagasra, O., Sheraz, M. & Pace, D. G. (2012). Hepatitis G virus or GBV-C: a natural anti-HIV interfering virus. In Viruses: Essential Agents of Life, pp. 363-388. Edited by G. Witzany. New York, NY: Springer.
4. Berzsenyi, M. D., Bowden, D. S. & Roberts, S. K. (2005). GB virus C: insights into co-infection. J Clin Virol 33, 257-266.
5. Bhattarai, N. & Stapleton, J. T. (2012). GB virus C: the good boy virus? Trends Microbiol 20, 124-130.
6. Birkenmeyer, L. G., Desai, S. M., Muerhoff, A. S., Leary, T. P., Simons, J. N., Montes, C. C. & Mushahwar, I. K. (1998). Isolation of a GB virus-related genome from a chimpanzee. J Med Virol 56, 44-51.
7. Castresana, J. (2000). Selection of conserved blocks from multiple alignments for their use in phylogenetic analysis. Mol Biol Evol 17, 540-552.
8. Chandriani, S., Skewes-Cox, P., Weidong, Z., Ganem, D. E. & Divers, T. J. (2013). Identification of a previously undescribed divergent virus from the Flaviviridae family in an outbreak of equine serum hepatitis. Proceedings of the National Academy of Science. USA 110, 5733-5734.
9. Cuceanu, N. M., Tuplin, A. & Simmonds, P. (2001). Evolutionarily conserved RNA secondary structures in coding and non-coding sequences at the 39 end of the hepatitis G virus/GB-virus C genome. J Gen Virol 82, 713-722.
10. Drexler, J. F., Corman, V. M., Mü ller, M. A., Lukashev, A. N., Gmyl, A., Coutard, B., Adam, A., Ritz, D., Leijten, L. M. & other authors (2013). Evidence for novel hepaciviruses in rodents. PLoS Pathog 9, e1003438.
11. Erker, J. C., Simons, J. N., Muerhoff, A. S., Leary, T. P., Chalmers, M. L., Desai, S. M. & Mushahwar, I. K. (1996). Molecular cloning and characterization of a GB virus C isolate from a patient with non-A-E hepatitis. J Gen Virol 77, 2713-2720.
12. Feng, Y., Zhao, W., Feng, Y., Dai, J., Li, Z., Zhang, X., Liu, L., Bai, J., Zhang, H. & other authors (2011). A novel genotype of GB virus C: its identification and predominance among injecting drug users in Yunnan, China. PLoS ONE 6, e21151.
13. Fogeda, M., López-Alcorocho, J. M., Bartolomé, J., Arocena, C., Martín, M. A. & Carreñ o, V. (2000). Existence of distinct GB virus C/hepatitis G virus variants with different tropism. J Virol 74, 7936-7942.
14. Gasteiger, E., Hoogland, C., Gattiker, A., Duvaud, S., Wilkins, M. R., Appel, R. D. & Bairoch, A. (2005). Protein identification and analysis tools on the ExPASy server. In The Proteomics Protocols Handbook, pp. 571-607. Edited by J. M. Walker. Totowa, NJ: Humana Press.
15. George, S. L., Varmaz, D. & Stapleton, J. T. (2006). GB virus C replicates in primary T and B lymphocytes. J Infect Dis 193, 451-454.
16. George, S. L., Varmaz, D., Tavis, J. E. & Chowdhury, A. (2012). The GB virus C (GBV-C) NS3 serine protease inhibits HIV-1 replication in a CD4+ T lymphocyte cell line without decreasing HIV receptor expression. PLoS ONE 7, e30653.
17. Gretch, D. (2012). Editorial commentary: advocating the concept of GB virus C biotherapy against AIDS. Clin Infect Dis 55, 1020-1021.
18. Heringlake, S., Ockenga, J., Tillmann, H. L., Trautwein, C., Meissner, D., Stoll, M., Hunt, J., Jou, C., Solomon, N. & other authors (1998a). GB virus C/hepatitis G virus infection: a favorable prognostic factor in human immunodeficiency virus-infected patients? J Infect Dis 177, 1723-1726.
19. Heringlake, S., Ockenga, J., Tillmann, H. L., Trautwein, C., Meissner, D., Stoll, M., Hunt, J., Jou, C., Solomon, N. & other authors (1998b). GB virus C/hepatitis G virus infection: a favorable prognostic factor in human immunodeficiency virus-infected patients? J Infect Dis 177, 1723-1726.
20. ICTV (2012). ICTV Master Species List 2012 v1, February 14, 2013 edn. Leuven, Belgium: Internation Committee on Taxonomy of Viruses.
21. Jung, S., Eichenmü ller, M., Donhauser, N., Neipel, F., Engel, A. M., Hess, G., Fleckenstein, B. & Reil, H. (2007). HIV entry inhibition by the envelope 2 glycoprotein of GB virus C. AIDS 21, 645-647.
22. Kapoor, A., Simmonds, P., Cullen, J. M., Scheel, T. K. H., Medina, J. L., Giannitti, F., Nishiuchi, E., Brock, K. V., Burbelo, P. D. & other authors (2013a). Identification of a pegivirus (GB virus-like virus) that infects horses. J Virol 87, 7185-7190.
23. Kapoor, A., Simmonds, P., Scheel, T. K. H., Hjelle, B., Cullen, J. M., Burbelo, P. D., Chauhan, L. V., Duraisamy, R., Sanchez Leon, M. & other authors (2013b). Identification of rodent homologs of hepatitis C virus and pegiviruses. MBio 4, e00216-e13.
24. Koedel, Y., Eissmann, K., Wend, H., Fleckenstein, B. & Reil, H. (2011). Peptides derived from a distinct region of GB virus C glycoprotein E2 mediate strain-specific HIV-1 entry inhibition. J Virol 85, 7037-7047.
25. Kofler, R., Orozco-terWengel, P., De Maio, N., Pandey, R. V., Nolte, V., Futschik, A., Kosiol, C. & Schlö tterer, C. (2011). PoPoolation: a toolbox for population genetic analysis of next generation sequencing data from pooled individuals. PLoS ONE 6, e15925.
26. Lauck, M., Hyeroba, D., Tumukunde, A., Weny, G., Lank, S. M., Chapman, C. A., O'Connor, D. H., Friedrich, T. C. & Goldberg, T. L. (2011). Novel, divergent simian hemorrhagic fever viruses in a wild Ugandan red colobus monkey discovered using direct pyrosequencing. PLoS ONE 6, e19056.
27. Lauck, M., Alvarado-Mora, M. V., Becker, E. A., Bhattacharya, D., Striker, R., Hughes, A. L., Carrilho, F. J., O'Connor, D. H. & Pinho, J. R. (2012a). Analysis of hepatitis C virus intrahost diversity across the coding region by ultradeep pyrosequencing. J Virol 86, 3952-3960.
28. Lauck, M., Sibley, S. D., Hyeroba, D., Tumukunde, A., Weny, G., Chapman, C. A., Ting, N., Switzer, W. M., Kuhn, J. H. & other authors (2013). Exceptional simian hemorrhagic fever virus diversity in a wild African primate community. J Virol 87, 688-691.
29. Lauring, A. S. & Andino, R. (2010). Quasispecies theory and the behavior of RNA viruses. PLoS Pathog 6, e1001005.
30. Leary, T. P., Muerhoff, A. S., Simons, J. N., Pilot-Matias, T. J., Erker, J. C., Chalmers, M. L., Schlauder, G. G., Dawson, G. J., Desai, S. M. & Mushahwar, I. K. (1996). Sequence and genomic organization of GBV-C: a novel member of the flaviviridae associated with human non-A-E hepatitis. J Med Virol 48, 60-67.
31. Linnen, J., Wages, J., Jr, Zhang-Keck, Z.-Y., Fry, K. E., Krawczynski, K. Z., Alter, H., Koonin, E., Gallagher, M., Alter, M. & other authors (1996a). Molecular cloning and disease association of hepatitis G virus: a transfusion-transmissible agent. Science 271, 505-508.
32. Linnen, J., Wages, J., Jr, Zhang-Keck, Z. Y., Fry, K. E., Krawczynski, K. Z., Alter, H., Koonin, E., Gallagher, M., Alter, M. & other authors (1996b). Molecular cloning and disease association of hepatitis G virus: a transfusion-transmissible agent. Science 271, 505-508.
33. Martin, D. P., Lemey, P., Lott, M., Moulton, V., Posada, D. & Lefeuvre, P. (2010). RDP3: a flexible and fast computer program for analyzing recombination. Bioinformatics 26, 2462-2463.
34. Moaven, L. D., Hyland, C. A., Young, I. F., Bowden, D. S., McCaw, R., Mison, L. & Locarnini, S. A. (1996). Prevalence of hepatitis G virus in Queensland blood donors. Med J Aust 165, 369-371.
35. Mohr, E. L. & Stapleton, J. T. (2009). GB virus type C interactions with HIV: the role of envelope glycoproteins. J Viral Hepat 16, 757-768.
36. Muerhoff, A. S., Simons, J. N., Leary, T. P., Erker, J. C., Chalmers, M. L., Pilot-Matias, T. J., Dawson, G. J., Desai, S. M. & Mushahwar, I. K. (1996). Sequence heterogeneity within the 59-terminal region of the hepatitis GB virus C genome and evidence for genotypes. J Hepatol 25, 379-384.
37. Muerhoff, A. S., Leary, T. P., Sathar, M. A., Dawson, G. J. & Desai, S. M. (2005). African origin of GB virus C determined by phylogenetic analysis of a complete genotype 5 genome from South Africa. J Gen Virol 86, 1729-1735.
38. Muerhoff, A. S., Dawson, G. J. & Desai, S. M. (2006). A previously unrecognized sixth genotype of GB virus C revealed by analysis of 59-untranslated region sequences. J Med Virol 78, 105-111.
39. Naito, H., Win, K. M. & Abe, K. (1999). Identification of a novel genotype of hepatitis G virus in Southeast Asia. J Clin Microbiol 37, 1217-1220.
40. Nielsen, H., Engelbrecht, J., Brunak, S. & von Heijne, G. (1997). Identification of prokaryotic and eukaryotic signal peptides and prediction of their cleavage sites. Protein Eng 10, 1-6.
41. Parreira, R., Branco, C., Piedade, J. & Esteves, A. (2012). GB virus C (GBV-C) evolutionary patterns revealed by analyses of reference genomes, E2 and NS5B sequences amplified from viral strains circulating in the Lisbon area (Portugal). Infect Genet Evol 12, 86-93.
42. Pavesi, A. (2001). Origin and evolution of GBV-C/hepatitis G virus and relationships with ancient human migrations. J Mol Evol 53, 104-113.
43. Petersen, T. N., Brunak, S., von Heijne, G. & Nielsen, H. (2011). SignalP 4.0: discriminating signal peptides from transmembrane regions. Nat Methods 8, 785-786.
44. Polgreen, P. M., Xiang, J., Chang, Q. & Stapleton, J. T. (2003). GB virus type C/hepatitis G virus: a non-pathogenic flavivirus associated with prolonged survival in HIV-infected individuals. Microbes Infect 5, 1255-1261.
45. Posada, D. (2008). jModelTest: PhylogeneticModel Averaging. Mol Biol Evol 25, 1253-1256.
46. Quan, P.-L., Firth, C., Conte, J. M., Williams, S. H., Zambrana-Torrelio, C. M., Anthony, S. J., Ellison, J. A., Gilbert, A. T., Kuzmin, I. V. & other authors (2013). Bats are a major natural reservoir for hepaciviruses and pegiviruses. Proc Natl Acad Sci U S A 110, 8194-8199.
47. Romano, C. M., Zanotto, P. M. & Holmes, E. C. (2008). Bayesian coalescent analysis reveals a high rate of molecular evolution in GB virus C. J Mol Evol 66, 292-297.
48. Ronquist, F. & Huelsenbeck, J. P. (2003). MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19, 1572-1574.
49. Rubaihayo, J., Surat, A., Ezekiel, M. & Andrew, A. (2010). High HIV prevalence and associated factors in a remote community in the Rwenzori region of Western Uganda. Infectious Disease Reports 2, e13.
50. Ruiz, V., Giordano, M., Rivero, C. W., Minassian, M. L., Cuestas, M. L., Trinks, J., Mathet, V. L. & Oubiñ a, J. R. (2010). GB virus C quasispecies detected in plasma and lymphocyte subsets in a natural human infection. J Gen Virol 91, 1687-1692.
51. Saito, T., Shiino, T., Arakawa, Y., Hayashi, S. & Abe, K. (1998). Geographical characterization of hepatitis G virus genome: Evidence for HGV genotypes based on phylogenetic analysis. Hepatol Res 10, 121-130.
52. Saito, T., Ishikawa, K.-i., Osei-Kwasi, M., Kaneko, T., Brandful, J. A. M., Nuvor, V., Aidoo, S., Ampofo, W., Apeagyei, F. A. & other authors (1999). Prevalence of hepatitis G virus and characterization of viral genome in Ghana. Hepatol Res 13, 221-231.
53. Sathar, M. A. & York, D. F. (2001). Group 5: GBV-C/HGV isolates from South Africa. J Med Virol 65, 121-122.
54. Sathar, M. A., Soni, P. N., Naicker, S., Conradie, J., Lockhat, F. & Gouws, E. (1999). GB virus C/hepatitis G virus infection in KwaZulu Natal, South Africa. J Med Virol 59, 38-44.
55. Simons, J. N., Leary, T. P., Dawson, G. J., Pilot-Matias, T. J., Muerhoff, A. S., Schlauder, G. G., Desai, S. M. & Mushahwar, I. K. (1995). Isolation of novel virus-like sequences associated with human hepatitis. Nat Med 1, 564-569.
56. Simons, J. N., Desai, S. M., Schultz, D. E., Lemon, S. M. & Mushahwar, I. K. (1996). Translation initiation in GB viruses A and C: evidence for internal ribosome entry and implications for genome organization. J Virol 70, 6126-6135.
57. Smith, D. B., Cuceanu, N., Davidson, F., Jarvis, L. M., Mokili, J. L., Hamid, S., Ludlam, C. A. & Simmonds, P. (1997). Discrimination of hepatitis G virus/GBV-C geographical variants by analysis of the 5' non-coding region. J Gen Virol 78, 1533-1542.
58. Smith, D. B., Basaras, M., Frost, S., Haydon, D., Cuceanu, N., Prescott, L., Kamenka, C., Millband, D., Sathar, M. A. & Simmonds, P. (2000). Phylogenetic analysis of GBV-C/hepatitis G virus. J Gen Virol 81, 769-780.
59. Stapleton, J. T. (2003). GB virus type C/Hepatitis G virus. Semin Liver Dis 23, 137-148.
60. Stapleton, J. T., Williams, C. F. & Xiang, J. (2004). GB virus type C: a beneficial infection? J Clin Microbiol 42, 3915-3919.
61. Stapleton, J. T., Foung, S., Muerhoff, A. S., Bukh, J. & Simmonds, P. (2011). The GB viruses: a review and proposed classification of GBVA, GBV-C (HGV), and GBV-D in genus Pegivirus within the family Flaviviridae. J Gen Virol 92, 233-246.
62. Suzuki, Y., Katayama, K., Fukushi, S., Kageyama, T., Oya, A., Okamura, H., Tanaka, Y., Mizokami, M. & Gojobori, T. (1999). Slow evolutionary rate of GB virus C/hepatitis G virus. J Mol Evol 48, 383-389.
63. Tamura, K., Peterson, D., Peterson, N., Stecher, G., Nei, M. & Kumar, S. (2011). MEGA5: molecular evolutionary genetics analysis using maximum likelihood, evolutionary distance, and maximum parsimony methods. Mol Biol Evol 28, 2731-2739.
64. Tanaka, Y., Mizokami, M., Orito, E., Ohba, K.-i., Kato, T., Kondo, Y., Mboudjeka, I., Zekeng, L., Kaptue, L. & other authors (1998). African origin of GB virus C/hepatitis G virus. FEBS Lett 423, 143-148.
65. Tillmann, H. L., Heiken, H., Knapik-Botor, A., Heringlake, S., Ockenga, J., Wilber, J. C., Goergen, B., Detmer, J., McMorrow, M. & other authors (2001). Infection with GB virus C and reduced mortality among HIV-infected patients. N Engl J Med 345, 715-724.
66. Timmons, C. L., Shao, Q., Wang, C., Liu, L., Liu, H., Dong, X. & Liu, B. (2013). GB virus type C E2 protein inhibits human immunodeficiency virus type 1 assembly through interference with HIV-1 gag plasma membrane targeting. J Infect Dis 207, 1171-1180.
67. Tucker, T. J. & Smuts, H. E. (2000). GBV-C/HGV genotypes: proposed nomenclature for genotypes 1-5. J Med Virol 62, 82-83.
68. Tucker, T. J., Smuts, H., Eickhaus, P., Robson, S. C. & Kirsch, R. E. (1999). Molecular characterization of the 59 non-coding region of South African GBV-C/HGV isolates: major deletion and evidence for a fourth genotype. J Med Virol 59, 52-59.
69. Williams, C. F., Klinzman, D., Yamashita, T. E., Xiang, J., Polgreen, P. M., Rinaldo, C., Liu, C., Phair, J., Margolick, J. B. & other authors (2004). Persistent GB virus C infection and survival in HIV-infected men. N Engl J Med 350, 981-990.
70. Wu, H., Padhi, A., Xu, J., Gong, X. & Tien, P. (2012). Intra-host diversity and emergence of unique GBV-C viral lineages in HIV infected subjects in central China. PLoS ONE 7, e48417.
71. Xiang, J., Wü nschmann, S., Schmidt, W., Shao, J. & Stapleton, J. T. (2000). Full-length GB virus C (Hepatitis G virus) RNA transcripts are infectious in primary CD4-positive T cells. J Virol 74, 9125-9133.
72. Xiang, J., Wü nschmann, S., Diekema, D. J., Klinzman, D., Patrick, K. D., George, S. L. & Stapleton, J. T. (2001). Effect of coinfection with GB virus C on survival among patients with HIV infection. N Engl J Med 345, 707-714.
73. Xiang, J., McLinden, J. H., Chang, Q., Kaufman, T. M. & Stapleton, J. T. (2006). An 85-aa segment of the GB virus type C NS5A phosphoprotein inhibits HIV-1 replication in CD4+ Jurkat T cells. Proc Natl Acad Sci U S A 103, 15570-15575.
74. Xiang, J., McLinden, J. H., Chang, Q., Jordan, E. L. & Stapleton, J. T. (2008). Characterization of a peptide domain within the GB virus C NS5A phosphoprotein that inhibits HIV replication. PLoS ONE 3, e2580.