Evidence for Novel Hepaciviruses in Rodents

PLoS Pathogens

Volumn 9, Issue 6, 2013, Pages

  Drexler, Jan Felix ^a   Corman, Victor Max ^a   Müller, Marcel Alexander ^a   Lukashev, Alexander N ^b   Gmyl, Anatoly ^b,c   Coutard, Bruno ^d   Adam, Alexander ^e   Ritz, Daniel ^a   Leijten, Lonneke M ^f   van Riel, Debby ^f   Kallies, Rene ^a   Klose, Stefan M ^g   Gloza Rausch, Florian ^a,h   Binger, Tabea ^a   Annan, Augustina ⁱ   Adu Sarkodie, Yaw ^j   Oppong, Samuel ^j   Bourgarel, Mathieu ^k   Rupp, Daniel ^l   Hoffmann, Bernd ^m   Schlegel, Mathias ^m   Kümmerer, Beate M ^a   Krüger, Detlev H ⁿ   Schmidt Chanasit, Jonas ^o   Setién, Alvaro Aguilar ^p   Cottontail, Veronika M ^g   Hemachudha, Thiravat ^q   Wacharapluesadee, Supaporn ^q   Osterrieder, Klaus ^r   Bartenschlager, Ralf ^l   Matthee, Sonja ^s   Beer, Martin ^m   Kuiken, Thijs ^f   Reusken, Chantal ^t   Leroy, Eric M ^u,v   Ulrich, Rainer G ^m   Drosten, Christian ^a   more..

^a UNIVERSITY OF BONN   (Germany)

^b CHUMAKOV INSTITUTE OF POLIOMYELITIS AND VIRAL ENCEPHALITIDES   (Russian Federation)

^c MOSCOW STATE UNIVERSITY   (Russian Federation)

^d AIX MARSEILLE UNIVERSITY   (France)

^e UNIVERSITY HOSPITAL OF COLOGNE   (Germany)

^f ERASMUS MEDICAL CENTER   (Netherlands)

^g UNIVERSITY OF ULM   (Germany)

^h Noctalis   (Germany)

ⁱ KUMASI CENTRE FOR COLLABORATIVE RESEARCH IN TROPICAL MEDICINE   (Ghana)

^j KWAME NKRUMAH UNIVERSITY OF SCIENCE AND TECHNOLOGY   (Ghana)

^k CIRAD   (France)

^l UNIVERSITY OF HEIDELBERG   (Germany)

^m FEDERAL RESEARCH INSTITUTE FOR ANIMAL HEALTH   (Germany)

ⁿ CHARITÉ UNIVERSITÄTSMEDIZIN BERLIN   (Germany)

^o BERNHARD NOCHT INSTITUTE FOR TROPICAL MEDICINE   (Germany)

^p HOSPITAL DE PEDIATRÍA   (Mexico)

^q CHULALONGKORN UNIVERSITY   (Thailand)

^r FREIE UNIVERSITÄT BERLIN   (Germany)

^s STELLENBOSCH UNIVERSITY   (South Africa)

^t Netherlands Center for Infectious Disease Control   (Netherlands)

^u CENTRE INTERNATIONAL DE RECHERCHES MÉDICALES DE FRANCEVILLE   (Gabon)

^v CNRS   (France)

more..

Author keywords

[No Author keywords available]

Indexed keywords

VIRUS RNA;

ANIMAL TISSUE; ARTICLE; BAT; CONFOCAL LASER MICROSCOPY; CONTROLLED STUDY; HEPATITIS C; HEPATITIS C VIRUS; HISTOPATHOLOGY; HORSE; IMMUNOBLOTTING; IMMUNOFLUORESCENCE TEST; IN SITU HYBRIDIZATION; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PHYLOGENY; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA PURIFICATION; RODENT; SEROLOGY; SEROPREVALENCE; VIRUS DETECTION; VIRUS GENOME; VOLE; WESTERN BLOTTING;

ANIMALS; BASE SEQUENCE; CATS; DOGS; EVOLUTION, MOLECULAR; GENOME, VIRAL; HEPACIVIRUS; HEPATITIS C; HEPATITIS C ANTIBODIES; HEPATITIS, ANIMAL; HORSES; MOLECULAR SEQUENCE DATA; RNA, VIRAL; RODENTIA;

ANIMALIA; CANIS FAMILIARIS; CLETHRIONOMYS GLAREOLUS; EQUIDAE; HEPACIVIRUS; HEPATITIS C VIRUS; MAMMALIA; MUS; RHABDOMYS PUMILIO; RODENTIA;

EID: 84879531467     PISSN: 15537366     EISSN: 15537374     Source Type: Journal    
DOI: 10.1371/journal.ppat.1003438     Document Type: Article

References (82)

1. Poynard T, Yuen MF, Ratziu V, Lai CL, (2003) Viral hepatitis C. Lancet 362: 2095-2100.
2. Weiss RA, McMichael AJ, (2004) Social and environmental risk factors in the emergence of infectious diseases. Nat Med 10: S70-76.
3. Perz JF, Armstrong GL, Farrington LA, Hutin YJ, Bell BP, (2006) The contributions of hepatitis B virus and hepatitis C virus infections to cirrhosis and primary liver cancer worldwide. J Hepatol 45: 529-538.
4. Brown RS, (2005) Hepatitis C and liver transplantation. Nature 436: 973-978.
5. Marcellin P, (2009) Hepatitis B and hepatitis C in 2009. Liver Int 29 (Suppl 1) (): 1-8.
6. Hanafiah KM, Groeger J, Flaxman AD, Wiersma ST, (2012) Global epidemiology of hepatitis C virus infection: New estimates of age-specific antibody to hepatitis C virus seroprevalence. Hepatology 57 (4) (): 1333-42.
7. McHutchison JG, Everson GT, Gordon SC, Jacobson IM, Sulkowski M, et al. (2009) Telaprevir with peginterferon and ribavirin for chronic HCV genotype 1 infection. N Engl J Med 360: 1827-1838.
8. Sherman KE, Flamm SL, Afdhal NH, Nelson DR, Sulkowski MS, et al. (2011) Response-guided telaprevir combination treatment for hepatitis C virus infection. N Engl J Med 365: 1014-1024.
9. Tan SL, Pause A, Shi Y, Sonenberg N, (2002) Hepatitis C therapeutics: current status and emerging strategies. Nat Rev Drug Discov 1: 867-881.
10. Lang K, Weiner DB, (2008) Immunotherapy for HCV infection: next steps. Expert Rev Vaccines 7: 915-923.
11. Biomedical CotUoCi, Research B, Council NR (2011) Chimpanzees in Biomedical and Behavioral Research: Assessing the Necessity; Bruce MA, Diane EP, Marilee KS-D, Jeffrey PK, editors: The National Academies Press.
12. Bukh J, (2012) Animal models for the study of hepatitis C virus infection and related liver disease. Gastroenterology 142: 1279-1287 e1273.
13. McGivern DR, Lemon SM, (2011) Model systems for hepatitis C research: the cup half empty? Gastroenterology 141: 806-809.
14. Long G, Hiet MS, Windisch MP, Lee JY, Lohmann V, et al. (2011) Mouse hepatic cells support assembly of infectious hepatitis C virus particles. Gastroenterology 141: 1057-1066.
15. Frentzen A, Huging K, Bitzegeio J, Friesland M, Haid S, et al. (2011) Completion of hepatitis C virus replication cycle in heterokaryons excludes dominant restrictions in human non-liver and mouse liver cell lines. PLoS Pathog 7: e1002029.
16. Ploss A, Rice CM, (2009) Towards a small animal model for hepatitis C. EMBO Rep 10: 1220-1227.
17. Dorner M, Horwitz JA, Robbins JB, Barry WT, Feng Q, et al. (2011) A genetically humanized mouse model for hepatitis C virus infection. Nature 474: 208-211.
18. Bitzegeio J, Bankwitz D, Hueging K, Haid S, Brohm C, et al. (2010) Adaptation of hepatitis C virus to mouse CD81 permits infection of mouse cells in the absence of human entry factors. PLoS Pathog 6: e1000978.
19. Wu GY, Konishi M, Walton CM, Olive D, Hayashi K, et al. (2005) A novel immunocompetent rat model of HCV infection and hepatitis. Gastroenterology 128: 1416-1423.
20. Bukh J, Apgar CL, Govindarajan S, Purcell RH, (2001) Host range studies of GB virus-B hepatitis agent, the closest relative of hepatitis C virus, in New World monkeys and chimpanzees. J Med Virol 65: 694-697.
21. Bukh J, Apgar CL, Yanagi M, (1999) Toward a surrogate model for hepatitis C virus: An infectious molecular clone of the GB virus-B hepatitis agent. Virology 262: 470-478.
22. Bailey J, (2010) An assessment of the use of chimpanzees in hepatitis C research past, present and future: 1. Validity of the chimpanzee model. Altern Lab Anim 38: 387-418.
23. Kapoor A, Simmonds P, Gerold G, Qaisar N, Jain K, et al. (2011) Characterization of a canine homolog of hepatitis C virus. Proc Natl Acad Sci U S A 108: 11608-11613.
24. Burbelo PD, Dubovi EJ, Simmonds P, Medina JL, Henriquez JA, et al. (2012) Serology-enabled discovery of genetically diverse hepaciviruses in a new host. J Virol 86: 6171-6178.
25. Drexler JF, Corman VM, Muller MA, Maganga GD, Vallo P, et al. (2012) Bats host major mammalian paramyxoviruses. Nat Commun 3: 796.
26. Luis AD, Hayman DTS, O'Shea TJ, Cryan PM, Gilbert AT, et al. (2013) A comparison of bats and rodents as reservoirs of zoonotic viruses: are bats special? Proceedings of the Royal Society B: Biological Sciences 280.
27. Mickleburgh S, Waylen K, P R, (2009) Bats as bushmeat: a global review. Oryx 43: 217-234.
28. Plowright RK, Foley P, Field HE, Dobson AP, Foley JE, et al. (2011) Urban habituation, ecological connectivity and epidemic dampening: the emergence of Hendra virus from flying foxes (Pteropus spp.). Proc Biol Sci 278: 3703-3712.
29. Parrish CR, Holmes EC, Morens DM, Park EC, Burke DS, et al. (2008) Cross-species virus transmission and the emergence of new epidemic diseases. Microbiol Mol Biol Rev 72: 457-470.
30. Mills JN, (2006) Biodiversity loss and emerging infectious disease: an example from the rodent-borne hemorrhagic fevers. Biodiversity 7: 9-17.
31. Koch DE, Mohler RL, Goodin DG, (2007) Stratifying land use/land cover for spatial analysis of disease ecology and risk: an example using object-based classification techniques. Geospat Health 2: 15-28.
32. Jonsson CB, Figueiredo LTM, Vapalahti O, (2010) A global perspective on hantavirus ecology, epidemiology, and disease. Clinical microbiology reviews 23: 412-441.
33. Schipper J, Chanson JS, Chiozza F, Cox NA, Hoffmann M, et al. (2008) The status of the world's land and marine mammals: diversity, threat, and knowledge. Science 322: 225-230.
34. Bukh J, (2011) Hepatitis C homolog in dogs with respiratory illness. Proc Natl Acad Sci U S A 108: 12563-12564.
35. Drexler JF, Kupfer B, Petersen N, Grotto RM, Rodrigues SM, et al. (2009) A novel diagnostic target in the hepatitis C virus genome. PLoS Med 6: e31.
36. Ronquist F, Huelsenbeck JP, (2003) MrBayes 3: Bayesian phylogenetic inference under mixed models. Bioinformatics 19: 1572-1574.
37. Drummond AJ, Suchard MA, Xie D, Rambaut A, (2012) Bayesian phylogenetics with BEAUti and the BEAST 1.7. Mol Biol Evol 29: 1969-1973.
38. Guindon S, Dufayard JF, Lefort V, Anisimova M, Hordijk W, et al. (2010) New algorithms and methods to estimate maximum-likelihood phylogenies: assessing the performance of PhyML 3.0. Syst Biol 59: 307-321.
39. Bouckaert RR, (2010) DensiTree: making sense of sets of phylogenetic trees. Bioinformatics 26: 1372-1373.
40. Zuker M, (2003) Mfold web server for nucleic acid folding and hybridization prediction. Nucleic Acids Res 31: 3406-3415.
41. Katoh K, Misawa K, Kuma K, Miyata T, (2002) MAFFT: a novel method for rapid multiple sequence alignment based on fast Fourier transform. Nucleic Acids Research 30: 3059-3066.
42. Bendtsen JD, Nielsen H, von Heijne G, Brunak S, (2004) Improved prediction of signal peptides: SignalP 3.0. J Mol Biol 340: 783-795.
43. Julenius K, Molgaard A, Gupta R, Brunak S, (2005) Prediction, conservation analysis, and structural characterization of mammalian mucin-type O-glycosylation sites. Glycobiology 15: 153-164.
44. Gupta R, Jung E, Brunak S (2004) Prediction of N-glycosylation sites in human proteins. http://www.cbs.dtu.dk/services/NetNGlyc. Accessed 14/05/2012.
45. Tamura K, Peterson D, Peterson N, Stecher G, Nei M, et al. (2011) MEGA5: Molecular Evolutionary Genetics Analysis using Maximum Likelihood, Evolutionary Distance, and Maximum Parsimony Methods. Mol Biol Evol 28 (10) (): 2731-9.
46. Muller MA, Paweska JT, Leman PA, Drosten C, Grywna K, et al. (2007) Coronavirus antibodies in African bat species. Emerg Infect Dis 13: 1367-1370.
47. Lantez V, Dalle K, Charrel R, Baronti C, Canard B, et al. (2011) Comparative production analysis of three phlebovirus nucleoproteins under denaturing or non-denaturing conditions for crystallographic studies. PLoS Negl Trop Dis 5: e936.
48. Epstein JH, Quan PL, Briese T, Street C, Jabado O, 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.
49. Xu Z, Choi J, Yen TS, Lu W, Strohecker A, et al. (2001) Synthesis of a novel hepatitis C virus protein by ribosomal frameshift. EMBO J 20: 3840-3848.
50. Vassilaki N, Mavromara P, (2009) The HCV ARFP/F/core+1 protein: production and functional analysis of an unconventional viral product. IUBMB Life 61: 739-752.
51. Li YP, Gottwein JM, Scheel TK, Jensen TB, Bukh J, (2011) MicroRNA-122 antagonism against hepatitis C virus genotypes 1-6 and reduced efficacy by host RNA insertion or mutations in the HCV 5′ UTR. Proc Natl Acad Sci U S A 108: 4991-4996.
52. Kozak M, (1991) An analysis of vertebrate mRNA sequences: intimations of translational control. J Cell Biol 115: 887-903.
53. Hansson L, (1990) Breeding of captive bank voles (Clethrionomys glareolus) related to dynamics of source populations. J Reprod Fertil 89: 769-772.
54. Hughes DJ, Kipar A, Leeming G, Sample JT, Stewart JP, (2012) Experimental infection of laboratory-bred bank voles (Myodes glareolus) with murid herpesvirus 4. Arch Virol 157: 2207-2212.
55. Hardestam J, Karlsson M, Falk KI, Olsson G, Klingstrom J, et al. (2008) Puumala hantavirus excretion kinetics in bank voles (Myodes glareolus). Emerg Infect Dis 14: 1209-1215.
56. Labuda M, Austyn JM, Zuffova E, Kozuch O, Fuchsberger N, et al. (1996) Importance of localized skin infection in tick-borne encephalitis virus transmission. Virology 219: 357-366.
57. Wu Z, Ren X, Yang L, Hu Y, Yang J, et al. (2012) Virome analysis for identification of novel mammalian viruses in bat species from Chinese provinces. J Virol 86: 10999-11012.
58. Kirkland PD, Frost MJ, Finlaison DS, King KR, Ridpath JF, et al. (2007) Identification of a novel virus in pigs-Bungowannah virus: a possible new species of pestivirus. Virus Res 129: 26-34.
59. de Lamballerie X, Crochu S, Billoir F, Neyts J, de Micco P, et al. (2002) Genome sequence analysis of Tamana bat virus and its relationship with the genus Flavivirus. J Gen Virol 83: 2443-2454.
60. Kapoor A, Victoria J, Simmonds P, Slikas E, Chieochansin T, et al. (2008) A highly prevalent and genetically diversified Picornaviridae genus in South Asian children. Proc Natl Acad Sci U S A 105: 20482-20487.
61. Stapleton JT, Foung S, Muerhoff AS, Bukh J, Simmonds P, (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: 233-246.
62. International Committee on Taxonomy of Viruses., King A, Adams M, Carstens EB, Lefkowitz EJ, et al. (2012) Virus taxonomy: classification and nomenclature of viruses: ninth report of the International Committee on Taxonomy of Viruses. Amsterdam; Boston: Elsevier/Academic Press. viii, 1259 p. p.
63. Thurner C, Witwer C, Hofacker IL, Stadler PF, (2004) Conserved RNA secondary structures in Flaviviridae genomes. J Gen Virol 85: 1113-1124.
64. Hellen CU, de Breyne S, (2007) A distinct group of hepacivirus/pestivirus-like internal ribosomal entry sites in members of diverse picornavirus genera: evidence for modular exchange of functional noncoding RNA elements by recombination. J Virol 81: 5850-5863.
65. Willcocks MM, Locker N, Gomwalk Z, Royall E, Bakhshesh M, et al. (2011) Structural features of the Seneca Valley virus internal ribosome entry site (IRES) element: a picornavirus with a pestivirus-like IRES. J Virol 85: 4452-4461.
66. Agol VI, Gmyl AP, (2010) Viral security proteins: counteracting host defences. Nat Rev Microbiol 8: 867-878.
67. Simmonds P, Bukh J, Combet C, Deleage G, Enomoto N, et al. (2005) Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 42: 962-973.
68. Bukh J, Apgar CL, (1997) Five new or recently discovered (GBV-A) virus species are indigenous to New World monkeys and may constitute a separate genus of the Flaviviridae. Virology 229: 429-436.
69. Lyons S, Kapoor A, Sharp C, Schneider B, Wolfe N, et al. (2012) Nonprimate hepaciviruses in domestic horses, United Kingdom. Emerg Infect Dis [Internet] Dec [08 Nov 2012]: http://dx.doi.org/10.3201/eid1812.120498.
70. Calisher CH, Childs JE, Field HE, Holmes KV, Schountz T, (2006) Bats: important reservoir hosts of emerging viruses. Clin Microbiol Rev 19: 531-545.
71. Wu S, Wu W, Zhang F, Ye J, Ni X, et al. (2012) Molecular and paleontological evidence for a post-Cretaceous origin of rodents. PLoS ONE 7: e46445.
72. Spitzenberger F (1999) Clethrionomys glareolus. In: Mitchell-Jones AJ, editor. The atlas of European mammals. London: T & AD Poyser. pp. xi, 484 p.
73. Michalopoulos GK, (2007) Liver regeneration. J Cell Physiol 213: 286-300.
74. Ratterree MS, Gutierrez RA, Travassos da Rosa AP, Dille BJ, Beasley DW, et al. (2004) Experimental infection of rhesus macaques with West Nile virus: level and duration of viremia and kinetics of the antibody response after infection. J Infect Dis 189: 669-676.
75. Sandvik T, Fredriksen B, Loken T, (1997) Level of viral antigen in blood leucocytes from cattle acutely infected with bovine viral diarrhoea virus. Zentralbl Veterinarmed B 44: 583-590.
76. Bininda-Emonds OR, Cardillo M, Jones KE, MacPhee RD, Beck RM, et al. (2007) The delayed rise of present-day mammals. Nature 446: 507-512.
77. Friebe P, Bartenschlager R, (2002) Genetic analysis of sequences in the 3′ nontranslated region of hepatitis C virus that are important for RNA replication. J Virol 76: 5326-5338.
78. Rijnbrand R, Abell G, Lemon SM, (2000) Mutational analysis of the GB virus B internal ribosome entry site. J Virol 74: 773-783.
79. Imberti L, Cariani E, Bettinardi A, Zonaro A, Albertini A, et al. (1991) An immunoassay for specific amplified HCV sequences. J Virol Methods 34: 233-243.
80. Laperche S, Lunel F, Izopet J, Alain S, Deny P, et al. (2005) Comparison of hepatitis C virus NS5b and 5′ noncoding gene sequencing methods in a multicenter study. J Clin Microbiol 43: 733-739.
81. Murphy DG, Willems B, Deschenes M, Hilzenrat N, Mousseau R, et al. (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: 1102-1112.
82. Moureau G, Temmam S, Gonzalez JP, Charrel RN, Grard G, et al. (2007) A real-time RT-PCR method for the universal detection and identification of flaviviruses. Vector Borne Zoonotic Dis 7: 467-477.