Completion of Hepatitis C Virus Replication Cycle in Heterokaryons Excludes Dominant Restrictions in Human Non-liver and Mouse Liver Cell Lines
Hepatitis C virus (HCV) is hepatotropic and only infects humans and chimpanzees. Consequently, an immunocompetent small animal model is lacking. The restricted tropism of HCV likely reflects specific host factor requirements. We investigated if dominant restriction factors expressed in non-liver or non-human cell lines inhibit HCV propagation thus rendering these cells non-permissive. To this end we explored if HCV completes its replication cycle in heterokaryons between human liver cell lines and non-permissive cell lines from human non-liver or mouse liver origin. Despite functional viral pattern recognition pathways and responsiveness to interferon, virus production was observed in all fused cells and was only ablated when cells were treated with exogenous interferon. These results exclude that constitutive or virus-induced expression of dominant restriction factors prevents propagation of HCV in these cell types, which has important implications for HCV tissue and species tropism. In turn, these data strongly advocate transgenic approaches of crucial human HCV cofactors to establish an immunocompetent small animal model.
Vyšlo v časopise:
Completion of Hepatitis C Virus Replication Cycle in Heterokaryons Excludes Dominant Restrictions in Human Non-liver and Mouse Liver Cell Lines. PLoS Pathog 7(4): e32767. doi:10.1371/journal.ppat.1002029
Kategorie:
Research Article
prolekare.web.journal.doi_sk:
https://doi.org/10.1371/journal.ppat.1002029
Souhrn
Hepatitis C virus (HCV) is hepatotropic and only infects humans and chimpanzees. Consequently, an immunocompetent small animal model is lacking. The restricted tropism of HCV likely reflects specific host factor requirements. We investigated if dominant restriction factors expressed in non-liver or non-human cell lines inhibit HCV propagation thus rendering these cells non-permissive. To this end we explored if HCV completes its replication cycle in heterokaryons between human liver cell lines and non-permissive cell lines from human non-liver or mouse liver origin. Despite functional viral pattern recognition pathways and responsiveness to interferon, virus production was observed in all fused cells and was only ablated when cells were treated with exogenous interferon. These results exclude that constitutive or virus-induced expression of dominant restriction factors prevents propagation of HCV in these cell types, which has important implications for HCV tissue and species tropism. In turn, these data strongly advocate transgenic approaches of crucial human HCV cofactors to establish an immunocompetent small animal model.
Zdroje
1. AlterMJ 2007 Epidemiology of hepatitis C virus infection. World J Gastroenterol 13 2436 2441
2. BartenschlagerRFreseMPietschmannT 2004 Novel insights into hepatitis C virus replication and persistence. Adv Virus Res 63 71 180
3. SimmondsPBukhJCombetCDeleageGEnomotoN 2005 Consensus proposals for a unified system of nomenclature of hepatitis C virus genotypes. Hepatology 42 962 973
4. HoofnagleJH 1997 Hepatitis C: the clinical spectrum of disease. Hepatology 26 15S 20S
5. MannsMPWedemeyerHCornbergM 2006 Treating viral hepatitis C: efficacy, side effects, and complications. Gut 55 1350 1359
6. BukhJ 2004 A critical role for the chimpanzee model in the study of hepatitis C. Hepatology 39 1469 1475
7. MercerDFSchillerDEElliottJFDouglasDNHaoC 2001 Hepatitis C virus replication in mice with chimeric human livers. Nat Med 7 927 933
8. MeulemanPLeroux-RoelsG 2008 The human liver-uPA-SCID mouse: a model for the evaluation of antiviral compounds against HBV and HCV. Antiviral Res 80 231 238
9. PlossARiceCM 2009 Towards a small animal model for hepatitis C. EMBO Rep 10 1220 1227
10. PlossAEvansMJGaysinskayaVAPanisMYouH 2009 Human occludin is a hepatitis C virus entry factor required for infection of mouse cells. Nature 457 882 886
11. FlintMvon HahnTZhangJFarquharMJonesCT 2006 Diverse CD81 proteins support hepatitis C virus infection. J Virol 80 11331 11342
12. CataneseMTAnsuiniHGrazianiRHubyTMoreauM 2010 Role of scavenger receptor class B type I in hepatitis C virus entry: kinetics and molecular determinants. J Virol 84 34 43
13. HaidSWindischMPBartenschlagerRPietschmannT 2010 Mouse-specific residues of claudin-1 limit hepatitis C virus genotype 2a infection in a human hepatocyte cell line. J Virol 84 964 975
14. BitzegeioJBankwitzDHuegingKHaidSBrohmC 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
15. ZhuQGuoJTSeegerC 2003 Replication of hepatitis C virus subgenomes in nonhepatic epithelial and mouse hepatoma cells. J Virol 77 9204 9210
16. KatoTDateTMiyamotoMZhaoZMizokamiM 2005 Nonhepatic cell lines HeLa and 293 support efficient replication of the hepatitis C virus genotype 2a subgenomic replicon. J Virol 79 592 596
17. AliSPellerinCLamarreDKukoljG 2004 Hepatitis C virus subgenomic replicons in the human embryonic kidney 293 cell line. J Virol 78 491 501
18. DateTKatoTMiyamotoMZhaoZYasuiK 2004 Genotype 2a hepatitis C virus subgenomic replicon can replicate in HepG2 and IMY-N9 cells. J Biol Chem 279 22371 22376
19. ChangKSCaiZZhangCSenGCWilliamsBR 2006 Replication of hepatitis C virus (HCV) RNA in mouse embryonic fibroblasts: protein kinase R (PKR)-dependent and PKR-independent mechanisms for controlling HCV RNA replication and mediating interferon activities. J Virol 80 7364 7374
20. UprichardSLChungJChisariFVWakitaT 2006 Replication of a hepatitis C virus replicon clone in mouse cells. Virol J 3 89
21. StrebelKLubanJJeangKT 2009 Human cellular restriction factors that target HIV-1 replication. BMC Med 7 48
22. GoffSP 2004 Retrovirus restriction factors. Mol Cell 16 849 859
23. SheehyAMGaddisNCChoiJDMalimMH 2002 Isolation of a human gene that inhibits HIV-1 infection and is suppressed by the viral Vif protein. Nature 418 646 650
24. StremlauMOwensCMPerronMJKiesslingMAutissierP 2004 The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 427 848 853
25. NeilSJZangTBieniaszPD 2008 Tetherin inhibits retrovirus release and is antagonized by HIV-1 Vpu. Nature 451 425 430
26. Rocha-PeruginiVMontpellierCDelgrangeDWychowskiCHelleF 2008 The CD81 partner EWI-2wint inhibits hepatitis C virus entry. PLoS One 3 e1866
27. KukiharaHMoriishiKTaguwaSTaniHAbeT 2009 Human VAP-C negatively regulates hepatitis C virus propagation. J Virol 83 7959 7969
28. KoutsoudakisGKaulASteinmannEKallisSLohmannV 2006 Characterization of the early steps of hepatitis C virus infection by using luciferase reporter viruses. J Virol 80 5308 5320
29. BlightKJMcKeatingJARiceCM 2002 Highly permissive cell lines for subgenomic and genomic hepatitis C virus RNA replication. J Virol 76 13001 13014
30. WindischMPFreseMKaulATripplerMLohmannV 2005 Dissecting the interferon-induced inhibition of hepatitis C virus replication by using a novel host cell line. J Virol 79 13778 13793
31. SteinmannEBrohmCKallisSBartenschlagerRPietschmannT 2008 Efficient trans-encapsidation of hepatitis C virus RNAs into infectious virus-like particles. J Virol 82 7034 7046
32. BlakqoriGDelhayeSHabjanMBlairCDSanchez-VargasI 2007 La Crosse bunyavirus nonstructural protein NSs serves to suppress the type I interferon system of mammalian hosts. J Virol 81 4991 4999
33. SumpterRJrLooYMFoyELiKYoneyamaM 2005 Regulating intracellular antiviral defense and permissiveness to hepatitis C virus RNA replication through a cellular RNA helicase, RIG-I. J Virol 79 2689 2699
34. WitteveldtJEvansMJBitzegeioJKoutsoudakisGOwsiankaAM 2009 CD81 is dispensable for hepatitis C virus cell-to-cell transmission in hepatoma cells. J Gen Virol 90 48 58
35. EvansMJvon HahnTTscherneDMSyderAJPanisM 2007 Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry. Nature 446 801 805
36. SkelleyAMKirakOSuhHJaenischRVoldmanJ 2009 Microfluidic control of cell pairing and fusion. Nat Methods 6 147 152
37. LindemannDGoepfertPA 2003 The foamy virus envelope glycoproteins. Curr Top Microbiol Immunol 277 111 129
38. PietschmannTKaulAKoutsoudakisGShavinskayaAKallisS 2006 Construction and characterization of infectious intragenotypic and intergenotypic hepatitis C virus chimeras. Proc Natl Acad Sci U S A 103 7408 7413
39. JoplingCLYiMLancasterAMLemonSMSarnowP 2005 Modulation of hepatitis C virus RNA abundance by a liver-specific MicroRNA. Science 309 1577 1581
40. ChangJGuoJTJiangDGuoHTaylorJM 2008 Liver-specific microRNA miR-122 enhances the replication of hepatitis C virus in nonhepatic cells. J Virol 82 8215 8223
41. LinLTNoyceRSPhamTNWilsonJASissonGR 2010 Replication of subgenomic hepatitis C virus replicons in mouse fibroblasts is facilitated by deletion of interferon regulatory factor 3 and expression of liver-specific microRNA 122. J Virol 84 9170 9180
42. FriewYNBoykoVHuWSPathakVK 2009 Intracellular interactions between APOBEC3G, RNA, and HIV-1 Gag: APOBEC3G multimerization is dependent on its association with RNA. Retrovirology 6 56
43. VarthakaviVSmithRMBourSPStrebelKSpearmanP 2003 Viral protein U counteracts a human host cell restriction that inhibits HIV-1 particle production. Proc Natl Acad Sci U S A 100 15154 15159
44. YuXYuYLiuBLuoKKongW 2003 Induction of APOBEC3G ubiquitination and degradation by an HIV-1 Vif-Cul5-SCF complex. Science 302 1056 1060
45. GoffinetCAllespachIHomannSTervoHMHabermannA 2009 HIV-1 antagonism of CD317 is species specific and involves Vpu-mediated proteasomal degradation of the restriction factor. Cell Host Microbe 5 285 297
46. McNattMWZangTHatziioannouTBartlettMFofanaIB 2009 Species-specific activity of HIV-1 Vpu and positive selection of tetherin transmembrane domain variants. PLoS Pathog 5 e1000300
47. MarianiRChenDSchrofelbauerBNavarroFKonigR 2003 Species-specific exclusion of APOBEC3G from HIV-1 virions by Vif. Cell 114 21 31
48. BishopKNHolmesRKSheehyAMMalimMH 2004 APOBEC-mediated editing of viral RNA. Science 305 645
49. KirchhoffF 2010 Immune evasion and counteraction of restriction factors by HIV-1 and other primate lentiviruses. Cell Host Microbe 8 55 67
50. TurelliPMangeatBJostSVianinSTronoD 2004 Inhibition of hepatitis B virus replication by APOBEC3G. Science 303 1829
51. JouvenetNNeilSJZhadinaMZangTKratovacZ 2009 Broad-spectrum inhibition of retroviral and filoviral particle release by tetherin. J Virol 83 1837 1844
52. KaletskyRLFrancicaJRAgrawal-GamseCBatesP 2009 Tetherin-mediated restriction of filovirus budding is antagonized by the Ebola glycoprotein. Proc Natl Acad Sci U S A 106 2886 2891
53. SakumaTNodaTUrataSKawaokaYYasudaJ 2009 Inhibition of Lassa and Marburg virus production by tetherin. J Virol 83 2382 2385
54. PardieuCViganRWilsonSJCalviAZangT 2010 The RING-CH ligase K5 antagonizes restriction of KSHV and HIV-1 particle release by mediating ubiquitin-dependent endosomal degradation of tetherin. PLoS Pathog 6 e1000843
55. MeylanECurranJHofmannKMoradpourDBinderM 2005 Cardif is an adaptor protein in the RIG-I antiviral pathway and is targeted by hepatitis C virus. Nature 437 1167 1172
56. SaitoTOwenDMJiangFMarcotrigianoJGaleMJr 2008 Innate immunity induced by composition-dependent RIG-I recognition of hepatitis C virus RNA. Nature 454 523 527
57. LiKFoyEFerreonJCNakamuraMFerreonAC 2005 Immune evasion by hepatitis C virus NS3/4A protease-mediated cleavage of the Toll-like receptor 3 adaptor protein TRIF. Proc Natl Acad Sci U S A 102 2992 2997
58. AhlenGDerkEWeilandMJiaoJRahbinN 2009 Cleavage of the IPS-1/Cardif/MAVS/VISA does not inhibit T cell-mediated elimination of hepatitis C virus non-structural 3/4A-expressing hepatocytes. Gut 58 560 569
59. LindenbachBDEvansMJSyderAJWolkBTellinghuisenTL 2005 Complete replication of hepatitis C virus in cell culture. Science 309 623 626
60. ZhongJGastaminzaPChengGKapadiaSKatoT 2005 Robust hepatitis C virus infection in vitro. Proc Natl Acad Sci U S A 102 9294 9299
61. WakitaTPietschmannTKatoTDateTMiyamotoM 2005 Production of infectious hepatitis C virus in tissue culture from a cloned viral genome. Nat Med 11 791 796
62. BurgelBFrieslandMKochAMannsMPWedemeyerH 2010 Hepatitis C virus enters human peripheral neuroblastoma cells - evidence for extra-hepatic cells sustaining hepatitis C virus penetration. J Viral Hepat doi:10.1111/j.1365-2893.2010.01339.x
63. LindemannDPietschmannTPicard-MaureauMBergAHeinkeleinM 2001 A particle-associated glycoprotein signal peptide essential for virus maturation and infectivity. J Virol 75 5762 5771
64. HanikaALarischBSteinmannESchwegmann-WesselsCHerrlerG 2005 Use of influenza C virus glycoprotein HEF for generation of vesicular stomatitis virus pseudotypes. J Gen Virol 86 1455 1465
65. SahaiAMalladiPMelin-AldanaHGreenRMWhitingtonPF 2004 Upregulation of osteopontin expression is involved in the development of nonalcoholic steatohepatitis in a dietary murine model. Am J Physiol Gastrointest Liver Physiol 287 G264 273
66. DullTZuffereyRKellyMMandelRJNguyenM 1998 A third-generation lentivirus vector with a conditional packaging system. J Virol 72 8463 8471
67. KalajzicIStoverMLLiuPKalajzicZRoweDW 2001 Use of VSV-G pseudotyped retroviral vectors to target murine osteoprogenitor cells. Virology 284 37 45
68. SpearmanC 1908 The method of “right and wrong cases” (“constant stimuli”) without Gauss's formulae. British Journal of Psychology 2 227 242
69. KärberG 1931 Beitrag zur kollektiven Behandlung pharmakologischer Reihenversuche. Archiv für experimentelle Pathologie und Pharmakologie 162 480 487
70. KeckZYLiSHXiaJvon HahnTBalfeP 2009 Mutations in hepatitis C virus E2 located outside the CD81 binding sites lead to escape from broadly neutralizing antibodies but compromise virus infectivity. J Virol 83 6149 6160
71. OwsiankaAClaytonRFLoomis-PriceLDMcKeatingJAPatelAH 2001 Functional analysis of hepatitis C virus E2 glycoproteins and virus-like particles reveals structural dissimilarities between different forms of E2. J Gen Virol 82 1877 1883
72. LivakKJSchmittgenTD 2001 Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25 402 408
73. JornsCHolzingerDThimmeRSpangenbergHCWeidmannM 2006 Rapid and simple detection of IFN-neutralizing antibodies in chronic hepatitis C non-responsive to IFN-alpha. J Med Virol 78 74 82
Štítky
Hygiena a epidemiológia Infekčné lekárstvo LaboratóriumČlánok vyšiel v časopise
PLOS Pathogens
2011 Číslo 4
- Parazitičtí červi v terapii Crohnovy choroby a dalších zánětlivých autoimunitních onemocnění
- Koronavirus hýbe světem: Víte jak se chránit a jak postupovat v případě podezření?
- Očkování proti virové hemoragické horečce Ebola experimentální vakcínou rVSVDG-ZEBOV-GP
Najčítanejšie v tomto čísle
- NF-κB Hyper-Activation by HTLV-1 Tax Induces Cellular Senescence, but Can Be Alleviated by the Viral Anti-Sense Protein HBZ
- Bacterial and Host Determinants of MAL Activation upon EPEC Infection: The Roles of Tir, ABRA, and FLRT3
- Innate Immune Sensing of DNA
- Structure-Function Analysis of the LRIM1/APL1C Complex and its Interaction with Complement C3-Like Protein TEP1