1932

Abstract

Hepaciviruses and pegiviruses constitute two closely related sister genera of the family . In the past five years, the known phylogenetic diversity of the hepacivirus genera has absolutely exploded. What was once an isolated infection in humans (and possibly other primates) has now expanded to include horses, rodents, bats, colobus monkeys, cows, and, most recently, catsharks, shedding new light on the genetic diversity and host range of hepaciviruses. Interestingly, despite the identification of these many animal and primate hepaciviruses, the equine hepaciviruses remain the closest genetic relatives of the human hepaciviruses, providing an intriguing clue to the zoonotic source of hepatitis C virus. This review summarizes the significance of these studies and discusses current thinking about the origin and evolution of the animal hepaciviruses as well as their potential usage as surrogate models for the study of hepatitis C virus.

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2016-09-29
2024-04-13
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Literature Cited

  1. Choo QL, Kuo G, Weiner AJ, Overby LR, Bradley DW, Houghton M. 1.  1989. Isolation of a cDNA clone derived from a blood-borne non-A, non-B viral hepatitis genome. Science 244:359–62 [Google Scholar]
  2. Simmonds PB, Becher P, Collett MS, Gould EA, Heinz FX. 2.  et al. 2012. Flaviviridae. Virus Taxonomy: Ninth Report of the International Committee on Taxonomy of Viruses AMQ King, MJ Adams, EB Carstens, EJ Lefkowitz 1003–20 London: Elsevier [Google Scholar]
  3. Hoofnagle JH. 3.  2002. Course and outcome of hepatitis C. Hepatology 36:S21–29 [Google Scholar]
  4. Yamane D, McGivern DR, Masaki T, Lemon SM. 4.  2013. Liver injury and disease pathogenesis in chronic hepatitis C. Curr. Top. Microbiol. Immunol. 369:263–88 [Google Scholar]
  5. Lavanchy D. 5.  2011. Evolving epidemiology of hepatitis C virus. Clin. Microbiol. Infect. 17:107–15 [Google Scholar]
  6. Jones KE, Patel NG, Levy MA, Storeygard A, Balk D. 6.  et al. 2008. Global trends in emerging infectious diseases. Nature 451:990–93 [Google Scholar]
  7. Mackenzie JS, Jeggo M. 7.  2013. Reservoirs and vectors of emerging viruses. Curr. Opin. Virol. 3:170–79 [Google Scholar]
  8. Parrish CR, Holmes EC, Morens DM, Park EC, Burke DS. 8.  et al. 2008. Cross-species virus transmission and the emergence of new epidemic diseases. Microbiol. Mol. Biol. Rev. 72:457–70 [Google Scholar]
  9. Sharp PM, Hahn BH. 9.  2011. Origins of HIV and the AIDS pandemic. Cold Spring Harb. Perspect. Med. 1:a006841 [Google Scholar]
  10. Flanagan ML, Parrish CR, Cobey S, Glass GE, Bush RM, Leighton TJ. 10.  2012. Anticipating the species jump: surveillance for emerging viral threats. Zoonoses Public Health 59:155–63 [Google Scholar]
  11. Morse SS, Mazet JA, Woolhouse M, Parrish CR, Carroll D. 11.  et al. 2012. Prediction and prevention of the next pandemic zoonosis. Lancet 380:1956–65 [Google Scholar]
  12. Pfaender S, Brown RJ, Pietschmann T, Steinmann E. 12.  2014. Natural reservoirs for homologs of hepatitis C virus. Emerg. Microbes Infect. 3:e21 [Google Scholar]
  13. Pfaender S, Cavalleri JM, Walter S, Doerrbecker J, Campana B. 13.  et al. 2014. Clinical course of infection and viral tissue tropism of hepatitis C virus-like non-primate hepaciviruses. Hepatology 61:447–59 [Google Scholar]
  14. Makuwa M, Souquiere S, Telfer P, Leroy E, Bourry O. 14.  et al. 2003. Occurrence of hepatitis viruses in wild-born non-human primates: a 3 year (1998–2001) epidemiological survey in Gabon. J. Med. Primatol. 32:307–14 [Google Scholar]
  15. Makuwa M, Souquiere S, Telfer P, Bourry O, Rouquet P. 15.  et al. 2006. Hepatitis viruses in non-human primates. J. Med. Primatol. 35:384–87 [Google Scholar]
  16. Burbelo PD, Dubovi EJ, Simmonds P, Medina JL, Henriquez JA. 16.  et al. 2012. Serology-enabled discovery of genetically diverse hepaciviruses in a new host. J. Virol. 86:6171–78 [Google Scholar]
  17. Deinhardt F, Holmes AW, Capps RB, Popper H. 17.  1967. Studies on the transmission of human viral hepatitis to marmoset monkeys. I. Transmission of disease, serial passages, and description of liver lesions. J. Exp. Med. 125:673–88 [Google Scholar]
  18. Simons JN, Pilot-Matias TJ, Leary TP, Dawson GJ, Desai SM. 18.  et al. 1995. Identification of two flavivirus-like genomes in the GB hepatitis agent. PNAS 92:3401–5 [Google Scholar]
  19. Stapleton JT, Foung S, Muerhoff AS, Bukh J, Simmonds P. 19.  2011. The GB viruses: a review and proposed classification of GBV-A, GBV-C (HGV), and GBV-D in genus Pegivirus within the family Flaviviridae. J. Gen. Virol. 92:233–46 [Google Scholar]
  20. Alter MJ, Gallagher M, Morris TT, Moyer LA, Meeks EL. 20.  et al. (Sentin. Cties. Viral Hepat. Study Team.) 1997. Acute non-A–E hepatitis in the United States and the role of hepatitis G virus infection. N. Engl. J. Med. 336:741–46 [Google Scholar]
  21. Schlauder GG, Pilot-Matias TJ, Gabriel GS, Simons JN, Muerhoff AS. 21.  et al. 1995. Origin of GB-hepatitis viruses. Lancet 346:447–48 [Google Scholar]
  22. Kim JP, Fry KE. 22.  1997. Molecular characterization of the hepatitis G virus. J. Viral Hepat. 4:77–79 [Google Scholar]
  23. Leary TP, Muerhoff AS, Simons JN, Pilot-Matias TJ, Erker JC. 23.  et al. 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 [Google Scholar]
  24. Xiang J, Klinzman D, McLinden J, Schmidt WN, LaBrecque DR. 24.  et al. 1998. Characterization of hepatitis G virus (GB-C virus) particles: evidence for a nucleocapsid and expression of sequences upstream of the E1 protein. J. Virol. 72:2738–44 [Google Scholar]
  25. Epstein JH, Quan PL, Briese T, Street C, Jabado O. 25.  et al. 2010. Identification of GBV-D, a novel GB-like flavivirus from old world frugivorous bats (Pteropus giganteus) in Bangladesh. PLOS Pathog. 6:e1000972 [Google Scholar]
  26. Chandriani S, Skewes-Cox P, Zhong W, Ganem DE, Divers TJ. 26.  et al. 2013. Identification of a previously undescribed divergent virus from the Flaviviridae family in an outbreak of equine serum hepatitis. PNAS 110:E1407–15 [Google Scholar]
  27. Drexler JF, Corman VM, Muller MA, Lukashev AN, Gmyl A. 27.  et al. 2013. Evidence for novel hepaciviruses in rodents. PLOS Pathog. 9:e1003438 [Google Scholar]
  28. Firth C, Bhat M, Firth MA, Williams SH, Frye MJ. 28.  et al. 2014. Detection of zoonotic pathogens and characterization of novel viruses carried by commensal Rattus norvegicus in New York City. mBio 5:e01933–14 [Google Scholar]
  29. Kapoor A, Simmonds P, Cullen JM, Scheel TK, Medina JL. 29.  et al. 2013. Identification of a pegivirus (GB virus-like virus) that infects horses. J. Virol. 87:7185–90 [Google Scholar]
  30. Kapoor A, Simmonds P, Scheel TK, Hjelle B, Cullen JM. 30.  et al. 2013. Identification of rodent homologs of hepatitis C virus and pegiviruses. mBio 4:e00216–13 [Google Scholar]
  31. Quan PL, Firth C, Conte JM, Williams SH, Zambrana-Torrelio CM. 31.  et al. 2013. Bats are a major natural reservoir for hepaciviruses and pegiviruses. PNAS 110:8194–99 [Google Scholar]
  32. Smith DB, Bukh J, Kuiken C, Muerhoff AS, Rice CM. 32.  et al. 2014. Expanded classification of hepatitis C virus into 7 genotypes and 67 subtypes: updated criteria and genotype assignment web resource. Hepatology 59:318–27 [Google Scholar]
  33. Neumann AU, Lam NP, Dahari H, Gretch DR, Wiley TE. 33.  et al. 1998. Hepatitis C viral dynamics in vivo and the antiviral efficacy of interferon-α therapy. Science 282:103–7 [Google Scholar]
  34. Galli A, Bukh J. 34.  2014. Comparative analysis of the molecular mechanisms of recombination in hepatitis C virus. Trends Microbiol 22:354–64 [Google Scholar]
  35. Messina JP, Humphreys I, Flaxman A, Brown A, Cooke GS. 35.  et al. 2015. Global distribution and prevalence of hepatitis C virus genotypes. Hepatology 61:77–87 [Google Scholar]
  36. Murphy DG, Willems B, Deschenes M, Hilzenrat N, Mousseau R, Sabbah S. 36.  2007. Use of sequence analysis of the NS5B region for routine genotyping of hepatitis C virus with reference to C/E1 and 5′ untranslated region sequences. J. Clin. Microbiol. 45:1102–12 [Google Scholar]
  37. Simmonds P. 37.  2013. The origin of hepatitis C virus. Curr. Top. Microbiol. Immunol. 369:1–15 [Google Scholar]
  38. Smith DB, Pathirana S, Davidson F, Lawlor E, Power J. 38.  et al. 1997. The origin of hepatitis C virus genotypes. J. Gen. Virol. 78:Pt. 2321–28 [Google Scholar]
  39. Pybus OG, Cochrane A, Holmes EC, Simmonds P. 39.  2005. The hepatitis C virus epidemic among injecting drug users. Infect. Genet. Evol. 5:131–39 [Google Scholar]
  40. Magiorkinis G, Magiorkinis E, Paraskevis D, Ho SY, Shapiro B. 40.  et al. 2009. The global spread of hepatitis C virus 1a and 1b: a phylodynamic and phylogeographic analysis. PLOS Med 6:e1000198 [Google Scholar]
  41. Gray RR, Tanaka Y, Takebe Y, Magiorkinis G, Buskell Z. 41.  et al. 2013. Evolutionary analysis of hepatitis C virus gene sequences from 1953. Philos. Trans. R. Soc. B 368:20130168 [Google Scholar]
  42. Gao F, Bailes E, Robertson DL, Chen Y, Rodenburg CM. 42.  et al. 1999. Origin of HIV-1 in the chimpanzee Pan troglodytes troglodytes. Nature 397:436–41 [Google Scholar]
  43. Kapoor A, Simmonds P, Gerold G, Qaisar N, Jain K. 43.  et al. 2011. Characterization of a canine homolog of hepatitis C virus. PNAS 108:11608–13 [Google Scholar]
  44. Bexfield NH, Watson PJ, Heaney J, Heeney JL, Tiley L. 44.  2014. Canine hepacivirus is not associated with chronic liver disease in dogs. J. Viral Hepat. 21:223–28 [Google Scholar]
  45. Lyons S, Kapoor A, Sharp C, Schneider BS, Wolfe ND. 45.  et al. 2012. Nonprimate hepaciviruses in domestic horses, United Kingdom. Emerg. Infect. Dis. 18:1976–82 [Google Scholar]
  46. Scheel TK, Kapoor A, Nishiuchi E, Brock KV, Yu Y. 46.  et al. 2015. Characterization of nonprimate hepacivirus and construction of a functional molecular clone. PNAS 112:2192–97 [Google Scholar]
  47. Ramsay JD, Evanoff R, Wilkinson TE Jr, Divers TJ, Knowles DP, Mealey RH. 47.  2015. Experimental transmission of equine hepacivirus in horses as a model for hepatitis C virus. Hepatology 61:1533–46 [Google Scholar]
  48. Park SH, Rehermann B. 48.  2014. Immune responses to HCV and other hepatitis viruses. Immunity 40:13–24 [Google Scholar]
  49. Postel A, Cavalleri JM, Pfaender S, Walter S, Steinmann E. 49.  et al. 2016. Frequent presence of hepaci and pegiviruses in commercial equine serum pools. Vet. Microbiol. 182:8–14 [Google Scholar]
  50. Lyons S, Kapoor A, Schneider BS, Wolfe ND, Culshaw G. 50.  et al. 2014. Viraemic frequencies and seroprevalence of non-primate hepacivirus and equine pegiviruses in horses and other mammalian species. J. Gen. Virol. 95:1701–11 [Google Scholar]
  51. Theze J, Lowes S, Parker J, Pybus OG. 51.  2015. Evolutionary and phylogenetic analysis of the hepaciviruses and pegiviruses. Genome Biol. Evol. 7:2996–3008 [Google Scholar]
  52. Scheel TK, Simmonds P, Kapoor A. 52.  2015. Surveying the global virome: identification and characterization of HCV-related animal hepaciviruses. Antivir. Res. 115:83–93 [Google Scholar]
  53. Lauck M, Sibley SD, Lara J, Purdy MA, Khudyakov Y. 53.  et al. 2013. A novel hepacivirus with an unusually long and intrinsically disordered NS5A protein in a wild Old World primate. J. Virol. 87:8971–81 [Google Scholar]
  54. Corman VM, Grundhoff A, Baechlein C, Fischer N, Gmyl A. 54.  et al. 2015. Highly divergent hepaciviruses from African cattle. J. Virol. 89:5876–82 [Google Scholar]
  55. Baechlein C, Fischer N, Grundhoff A, Alawi M, Indenbirken D. 55.  et al. 2015. Identification of a novel hepacivirus in domestic cattle from Germany. J. Virol. 89:7007–15 [Google Scholar]
  56. Shi M, Lin XD, Vasilakis N, Tian JH, Li CX. 56.  et al. 2015. Divergent viruses discovered in arthropods and vertebrates revise the evolutionary history of the Flaviviridae and related viruses. J. Virol. 90:659–69 [Google Scholar]
  57. Jopling CL, Yi M, Lancaster AM, Lemon SM, Sarnow P. 57.  2005. Modulation of hepatitis C virus RNA abundance by a liver-specific microRNA. Science 309:1577–81 [Google Scholar]
  58. Sagan SM, Sarnow P, Wilson JA. 58.  2013. Modulation of GB virus B RNA abundance by microRNA-122: dependence on and escape from microRNA-122 restriction. J. Virol. 87:7338–47 [Google Scholar]
  59. Hundt J, Li Z, Liu Q. 59.  2013. Post-translational modifications of hepatitis C viral proteins and their biological significance. World J. Gastroenterol. 19:8929–39 [Google Scholar]
  60. Kapoor A, Kumar A, Simmonds P, Bhuva N, Singh Chauhan L. 60.  et al. 2015. Virome analysis of transfusion recipients reveals a novel human virus that shares genomic features with hepaciviruses and pegiviruses. mBio 6:e01466–15 [Google Scholar]
  61. Berg MG, Lee D, Coller K, Frankel M, Aronsohn A. 61.  et al. 2015. Discovery of a novel human pegivirus in blood associated with hepatitis C virus co-infection. PLOS Pathog 11:e1005325 [Google Scholar]
  62. Bonsall D, Gregory WF, Ip CL, Donfield S, Iles J. 62.  et al. 2016. Evaluation of viremia frequencies of a novel human pegivirus by using bioinformatic screening and PCR. Emerg. Infect. Dis. 22:671–78 [Google Scholar]
  63. Kubo Y, Takeuchi K, Boonmar S, Katayama T, Choo QL. 63.  et al. 1989. A cDNA fragment of hepatitis C virus isolated from an implicated donor of post-transfusion non-A, non-B hepatitis in Japan. Nucleic Acids Res 17:10367–72 [Google Scholar]
  64. Pybus OG, Gray RR. 64.  2013. The virus whose family expanded. Nature 498:310–11 [Google Scholar]
  65. Pybus OG, Theze J. 65.  2016. Hepacivirus cross-species transmission and the origins of the hepatitis C virus. Curr. Opin. Virol. 16:1–7 [Google Scholar]
  66. Krey T, d'Alayer J, Kikuti CM, Saulnier A, Damier-Piolle L. 66.  et al. 2010. The disulfide bonds in glycoprotein E2 of hepatitis C virus reveal the tertiary organization of the molecule. PLOS Pathog 6:e1000762 [Google Scholar]
  67. Parera M, Martrus G, Franco S, Clotet B, Martinez MA. 67.  2012. Canine hepacivirus NS3 serine protease can cleave the human adaptor proteins MAVS and TRIF. PLOS ONE 7:e42481 [Google Scholar]
  68. Patel MR, Loo YM, Horner SM, Gale M Jr, Malik HS. 68.  2012. Convergent evolution of escape from hepaciviral antagonism in primates. PLOS Biol. 10:e1001282 [Google Scholar]
  69. Tanaka T, Kasai H, Yamashita A, Okuyama-Dobashi K, Yasumoto J. 69.  et al. 2014. Hallmarks of hepatitis C virus in equine hepacivirus. J. Virol. 88:13352–66 [Google Scholar]
  70. Worobey M, Telfer P, Souquiere S, Hunter M, Coleman CA. 70.  et al. 2010. Island biogeography reveals the deep history of SIV. Science 329:1487 [Google Scholar]
  71. Katzourakis A, Gifford RJ. 71.  2010. Endogenous viral elements in animal genomes. PLOS Genet 6:e1001191 [Google Scholar]
  72. Kapoor A, Simmonds P, Lipkin WI. 72.  2010. Discovery and characterization of mammalian endogenous parvoviruses. J. Virol. 84:12628–35 [Google Scholar]
  73. Kapoor A, Simmonds P, Dubovi EJ, Qaisar N, Henriquez JA. 73.  et al. 2011. Characterization of a canine homolog of human Aichivirus. J. Virol. 85:11520–25 [Google Scholar]
  74. Gravitz L. 74.  2011. Introduction: a smouldering public-health crisis. Nature 474:S2–4 [Google Scholar]
  75. Verstrepen BE, Boonstra A, Koopman G. 75.  2015. Immune mechanisms of vaccine induced protection against chronic hepatitis C virus infection in chimpanzees. World J. Hepatol. 7:53–69 [Google Scholar]
  76. Lavanchy D. 76.  2009. The global burden of hepatitis C. Liver Int 29:Suppl. 174–81 [Google Scholar]
  77. Hagan LM, Wolpe PR, Schinazi RF. 77.  2013. Treatment as prevention and cure towards global eradication of hepatitis C virus. Trends Microbiol 21:625–33 [Google Scholar]
  78. Lindenbach BD, Rice CM. 78.  2013. The ins and outs of hepatitis C virus entry and assembly. Nat. Rev. Microbiol. 11:688–700 [Google Scholar]
  79. Scheel TK, Rice CM. 79.  2013. Understanding the hepatitis C virus life cycle paves the way for highly effective therapies. Nat. Med. 19:837–49 [Google Scholar]
  80. Walker CM, Grakoui A. 80.  2015. Hepatitis C virus: Why do we need a vaccine to prevent a curable persistent infection?. Curr. Opin. Immunol. 35:137–43 [Google Scholar]
  81. Raghuraman S, Park H, Osburn WO, Winkelstein E, Edlin BR, Rehermann B. 81.  2012. Spontaneous clearance of chronic hepatitis C virus infection is associated with appearance of neutralizing antibodies and reversal of T-cell exhaustion. J. Infect. Dis. 205:763–71 [Google Scholar]
  82. Rehermann B. 82.  2009. Hepatitis C virus versus innate and adaptive immune responses: a tale of coevolution and coexistence. J. Clin. Investig. 119:1745–54 [Google Scholar]
  83. Lindenbach BD, Evans MJ, Syder AJ, Wolk B, Tellinghuisen TL. 83.  et al. 2005. Complete replication of hepatitis C virus in cell culture. Science 309:623–26 [Google Scholar]
  84. Pietschmann T, Lohmann V, Kaul A, Krieger N, Rinck G. 84.  et al. 2002. Persistent and transient replication of full-length hepatitis C virus genomes in cell culture. J. Virol. 76:4008–21 [Google Scholar]
  85. Wakita T, Pietschmann T, Kato T, Date T, Miyamoto M. 85.  et al. 2005. Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat. Med. 11:791–96 [Google Scholar]
  86. Dolgin E. 86.  2011. Research technique: the murine candidate. Nature 474:S14–15 [Google Scholar]
  87. Barth H, Robinet E, Liang TJ, Baumert TF. 87.  2008. Mouse models for the study of HCV infection and virus-host interactions. J. Hepatol. 49:134–42 [Google Scholar]
  88. Beames B, Chavez D, Lanford RE. 88.  2001. GB virus B as a model for hepatitis C virus. ILAR J 42:152–60 [Google Scholar]
  89. Billerbeck E, de Jong Y, Dorner M, de la Fuente C, Ploss A. 89.  2013. Animal models for hepatitis C. Curr. Top. Microbiol. Immunol. 369:49–86 [Google Scholar]
  90. Hoebe K, Janssen E, Beutler B. 90.  2004. The interface between innate and adaptive immunity. Nat. Immunol. 5:971–74 [Google Scholar]
  91. Lanford RE, Bigger C, Bassett S, Klimpel G. 91.  2001. The chimpanzee model of hepatitis C virus infections. ILAR J 42:117–26 [Google Scholar]
  92. Lanford RE, Evans MJ, Lohmann V, Lindenbach B, Gale M Jr. 92. et al. 2009. The accelerating pace of HCV research: a summary of the 15th International Symposium on Hepatitis C Virus and Related Viruses. Gastroenterology 1369–16
  93. Liu L, Fisher BE, Thomas DL, Cox AL, Ray SC. 93.  2012. Spontaneous clearance of primary acute hepatitis C virus infection correlated with high initial viral RNA level and rapid HVR1 evolution. Hepatology 55:1684–91 [Google Scholar]
  94. Scull MA, Shi C, de Jong YP, Gerold G, Ries M. 94.  et al. 2015. Hepatitis C virus infects rhesus macaque hepatocytes and simianized mice. Hepatology 62:57–67 [Google Scholar]
  95. von Schaewen M, Ploss A. 95.  2014. Murine models of hepatitis C: What can we look forward to?. Antivir. Res. 104:15–22 [Google Scholar]
  96. Li K, Lemon SM. 96.  2013. Innate immune responses in hepatitis C virus infection. Semin. Immunopathol. 35:53–72 [Google Scholar]
  97. Bukh J. 97.  2012. Animal models for the study of hepatitis C virus infection and related liver disease. Gastroenterology 142:1279–87 [Google Scholar]
  98. Vercauteren K, de Jong YP, Meuleman P. 98.  2014. HCV animal models and liver disease. J. Hepatol. 61:S26–33 [Google Scholar]
  99. Dorner M, Rice CM, Ploss A. 99.  2013. Study of hepatitis C virus entry in genetically humanized mice. Methods 59:249–57 [Google Scholar]
  100. Chen J, Zhao Y, Zhang C, Chen H, Feng J. 100.  et al. 2014. Persistent hepatitis C virus infections and hepatopathological manifestations in immune-competent humanized mice. Cell Res 24:1050–66 [Google Scholar]
  101. Karst SM, Wobus CE. 101.  2015. Viruses in rodent colonies: lessons learned from murine noroviruses. Annu. Rev. Virol. 2:525–48 [Google Scholar]
  102. Herbst MM, Prescott J, Palmer AD, Schountz T. 102.  2002. Sequence and expression analysis of deer mouse interferon-γ, interleukin-10, tumor necrosis factor, and lymphotoxin-α. Cytokine 17:203–13 [Google Scholar]
  103. Oko L, Aduddell-Swope B, Willis D, Hamor R, Coons TA. 103.  et al. 2006. Profiling helper T cell subset gene expression in deer mice. BMC Immunol 7:18 [Google Scholar]
  104. Root JJ, Black WC III, Calisher CH, Wilson KR, Mackie RS. 104.  et al. 2003. Analyses of gene flow among populations of deer mice (Peromyscus maniculatus) at sites near hantavirus pulmonary syndrome case-patient residences. J. Wildl. Dis. 39:287–98 [Google Scholar]
  105. Schountz T, Acuna-Retamar M, Feinstein S, Prescott J, Torres-Perez F. 105.  et al. 2012. Kinetics of immune responses in deer mice experimentally infected with Sin Nombre virus. J. Virol. 86:10015–27 [Google Scholar]
  106. Schountz T, Green R, Davenport B, Buniger A, Richens T. 106.  et al. 2004. Cloning and characterization of deer mouse (Peromyscus maniculatus) cytokine and chemokine cDNAs. BMC Immunol 5:1 [Google Scholar]
  107. Schountz T, Quackenbush S, Rovnak J, Haddock E, Black WC IV. 107.  et al. 2014. Differential lymphocyte and antibody responses in deer mice infected with Sin Nombre or Andes hantaviruses. J. Virol. 88:8319–31 [Google Scholar]
  108. Schountz T, Shaw TI, Glenn TC, Feldmann H, Prescott J. 108.  2013. Expression profiling of lymph node cells from deer mice infected with Andes virus. BMC Immunol 14:18 [Google Scholar]
  109. Spada E, Mele A, Berton A, Ruggeri L, Ferrigno L. 109.  et al. 2004. Multispecific T cell response and negative HCV RNA tests during acute HCV infection are early prognostic factors of spontaneous clearance. Gut 53:1673–81 [Google Scholar]
  110. von Hahn T, Yoon JC, Alter H, Rice CM, Rehermann B. 110.  et al. 2007. Hepatitis C virus continuously escapes from neutralizing antibody and T-cell responses during chronic infection in vivo. Gastroenterology 132:667–78 [Google Scholar]
  111. Dahari H, Feinstone SM, Major ME. 111.  2010. Meta-analysis of hepatitis C virus vaccine efficacy in chimpanzees indicates an importance for structural proteins. Gastroenterology 139:965–74 [Google Scholar]
  112. Le SQ, Gascuel O. 112.  2008. An improved general amino acid replacement matrix. Mol. Biol. Evol. 25:1307–20 [Google Scholar]
  113. Kumar S, Stecher G, Tamura K. 113.  2016. MEGA7: Molecular Evolutionary Genetics Analysis version 7.0 for bigger datasets. Mol. Biol. Evol. 331870–74
  114. Mohr EL, Stapleton JT. 114.  2009. GB virus type C interactions with HIV: the role of envelope glycoproteins. J. Viral Hepat. 16:757–68 [Google Scholar]
  115. Lyons S, Kapoor A, Schneider BS, Wolfe ND, Culshaw G. 115.  et al. 2014. Viraemic frequencies and seroprevalence of non-primate hepacivirus and equine pegiviruses in horses and other mammalian species. J. Gen. Virol. 95:1701–11 [Google Scholar]
  116. Drexler JF, Corman VM, Muller MA, Lukashev AN, Gmyl A. 116.  et al. 2013. Evidence for novel hepaciviruses in rodents. PLOS Pathog 9:e1003438 [Google Scholar]
  117. Takikawa S, Engle RE, Emerson SU, Purcell RH St, Claire M, Bukh J. 117.  2006. Functional analyses of GB virus B p13 protein: development of a recombinant GB virus B hepatitis virus with a p7 protein. PNAS 103:3345–50 [Google Scholar]
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