publication . Article . 2016

Hepatitis C virus double‐stranded RNA is the predominant form in human liver and in interferon‐treated cells

Klepper, Arielle; Eng, Francis J.; Doyle, Erin H.; El‐Shamy, Ahmed; Rahman, Adeeb H.; Fiel, M. Isabel; Avino, Gonzalo Carrasco; Lee, Moonju; Ye, Fei; Roayaie, Sasan; ...
Open Access English
  • Published: 01 Nov 2016 Journal: Hepatology (Baltimore, Md.), volume 66, issue 2, pages 357-370 (issn: 0270-9139, eissn: 1527-3350, Copyright policy)
  • Publisher: John Wiley and Sons Inc.
Abstract
Hepatitis C virus (HCV) is unique among RNA viruses in its ability to establish chronic infection in the majority of exposed adults. HCV persists in the liver despite interferon (IFN)‐stimulated gene (ISG) induction; robust induction actually predicts treatment failure and viral persistence. It is unclear which forms of HCV RNA are associated with ISG induction and IFN resistance during natural infections. To thoroughly delineate HCV RNA populations, we developed conditions that fully separate the strands of long double‐stranded RNA (dsRNA) and allow the released RNAs to be quantified in reverse transcription/polymerase chain reaction assays. These methods revea...
Subjects
Medical Subject Headings: virus diseasesdigestive system diseasesviruses
free text keywords: Hepatitis C, Treatment, Original Article, Original Articles, Viral Hepatitis
Funded by
NIH| Optimizing Vitamin D Treatment in HIV/AIDS: An RCT
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01DA031095-04
  • Funding stream: NATIONAL INSTITUTE ON DRUG ABUSE
,
NIH| HCV Strain Variation and HCC
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R21CA152514-02
  • Funding stream: NATIONAL CANCER INSTITUTE
,
NIH| A Novel Cultue System for Hepatitis C Virus
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5F31AI081530-02
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
,
NIH| Postbaccalaureate Research Education Program (PREP)
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2R25GM064118-14
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Clinical Outcomes and the HCV Core Gene
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01DK090317-04
  • Funding stream: NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES
46 references, page 1 of 4

1 Bichoupan K, Martel‐Laferriere V, Sachs D, Ng M, Schonfeld EA, Pappas A, et al. Costs of telaprevir‐based triple therapy for hepatitis C: $189,000 per sustained virological response. Hepatology 2014;60:1187–1195. 25065814 [OpenAIRE] [PubMed]

2 Simmons B, Saleem J, Hill A, Riley RD, Cooke GS. Risk of late relapse or reinfection with hepatitis C virus after achieving a sustained virological response: a systematic review and meta‐analysis. Clin Infect Dis 2016; doi: 10.1093/cid/civ948.

3 Thomas E, Gonzalez VD, Li Q, Modi AA, Chen W, Noureddin M, et al. HCV infection induces a unique hepatic innate immune response associated with robust production of type III interferons. Gastroenterology 2012;142:978–988. 22248663 [OpenAIRE] [PubMed]

4 Chen L, Borozan I, Feld J, Sun J, Tannis LL, Coltescu C, et al. Hepatic gene expression discriminates responders and nonresponders in treatment of chronic hepatitis C viral infection. Gastroenterology 2005;128:1437–1444. 15887125 [PubMed]

5 Feld JJ, Nanda S, Huang Y, Chen W, Cam M, Pusek SN, et al. Hepatic gene expression during treatment with peginterferon and ribavirin: identifying molecular pathways for treatment response. Hepatology 2007;46:1548–1563. 17929300 [OpenAIRE] [PubMed]

6 Sarasin‐Filipowicz M, Oakeley EJ, Duong FH, Christen V, Terracciano L, Filipowicz W, et al. Interferon signaling and treatment outcome in chronic hepatitis C. Proc Natl Acad Sci U S A 2008;105:7034–7039. 18467494 [OpenAIRE] [PubMed]

7 Honda M, Sakai A, Yamashita T, Nakamoto Y, Mizukoshi E, Sakai Y, et al. Hepatic ISG expression is associated with genetic variation in interleukin 28B and the outcome of IFN therapy for chronic hepatitis C. Gastroenterology 2010;139:499–509. 20434452 [OpenAIRE] [PubMed]

8 Thomas DL, Thio CL, Martin MP, Qi Y, Ge D, O'Huigin C, et al. Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature 2009;461:798–801. 19759533 [OpenAIRE] [PubMed]

9 Tillmann HL, Thompson AJ, Patel K, Wiese M, Tenckhoff H, Nischalke HD, et al. A polymorphism near IL28B is associated with spontaneous clearance of acute hepatitis C virus and jaundice. Gastroenterology 2010;139:1586–1592. 20637200 [OpenAIRE] [PubMed]

10 Ge D, Fellay J, Thompson AJ, Simon JS, Shianna KV, Urban TJ, et al. Genetic variation in IL28B predicts hepatitis C treatment‐induced viral clearance. Nature 2009;461:399–401. 19684573 [PubMed]

11 Odorizzi PM, Wherry EJ. Immunology. An interferon paradox. Science 2013;340:155–156. 23580520 [OpenAIRE] [PubMed]

12 Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, Bartenschlager R, et al. Cardif is an adaptor protein in the RIG‐I antiviral pathway and is targeted by hepatitis C virus. Nature 2005;437:1167–1172. 16177806 [OpenAIRE] [PubMed]

13 Li K, Foy E, Ferreon JC, Nakamura M, Ferreon AC, Ikeda M, et al. 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 2005;102:2992–2997. 15710891 [OpenAIRE] [PubMed]

14 Wieland S, Makowska Z, Campana B, Calabrese D, Dill MT, Chung J, et al. Simultaneous detection of hepatitis C virus and interferon stimulated gene expression in infected human liver. Hepatology 2014;59:2121–2130. 24122862 [OpenAIRE] [PubMed]

15 Koonin EV. The phylogeny of RNA‐dependent RNA polymerases of positive‐strand RNA viruses. J Gen Virol 1991;72:2197–2206. 1895057 [OpenAIRE] [PubMed]

46 references, page 1 of 4
Abstract
Hepatitis C virus (HCV) is unique among RNA viruses in its ability to establish chronic infection in the majority of exposed adults. HCV persists in the liver despite interferon (IFN)‐stimulated gene (ISG) induction; robust induction actually predicts treatment failure and viral persistence. It is unclear which forms of HCV RNA are associated with ISG induction and IFN resistance during natural infections. To thoroughly delineate HCV RNA populations, we developed conditions that fully separate the strands of long double‐stranded RNA (dsRNA) and allow the released RNAs to be quantified in reverse transcription/polymerase chain reaction assays. These methods revea...
Subjects
Medical Subject Headings: virus diseasesdigestive system diseasesviruses
free text keywords: Hepatitis C, Treatment, Original Article, Original Articles, Viral Hepatitis
Funded by
NIH| Optimizing Vitamin D Treatment in HIV/AIDS: An RCT
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01DA031095-04
  • Funding stream: NATIONAL INSTITUTE ON DRUG ABUSE
,
NIH| HCV Strain Variation and HCC
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R21CA152514-02
  • Funding stream: NATIONAL CANCER INSTITUTE
,
NIH| A Novel Cultue System for Hepatitis C Virus
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5F31AI081530-02
  • Funding stream: NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES
,
NIH| Postbaccalaureate Research Education Program (PREP)
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 2R25GM064118-14
  • Funding stream: NATIONAL INSTITUTE OF GENERAL MEDICAL SCIENCES
,
NIH| Clinical Outcomes and the HCV Core Gene
Project
  • Funder: National Institutes of Health (NIH)
  • Project Code: 5R01DK090317-04
  • Funding stream: NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES
46 references, page 1 of 4

1 Bichoupan K, Martel‐Laferriere V, Sachs D, Ng M, Schonfeld EA, Pappas A, et al. Costs of telaprevir‐based triple therapy for hepatitis C: $189,000 per sustained virological response. Hepatology 2014;60:1187–1195. 25065814 [OpenAIRE] [PubMed]

2 Simmons B, Saleem J, Hill A, Riley RD, Cooke GS. Risk of late relapse or reinfection with hepatitis C virus after achieving a sustained virological response: a systematic review and meta‐analysis. Clin Infect Dis 2016; doi: 10.1093/cid/civ948.

3 Thomas E, Gonzalez VD, Li Q, Modi AA, Chen W, Noureddin M, et al. HCV infection induces a unique hepatic innate immune response associated with robust production of type III interferons. Gastroenterology 2012;142:978–988. 22248663 [OpenAIRE] [PubMed]

4 Chen L, Borozan I, Feld J, Sun J, Tannis LL, Coltescu C, et al. Hepatic gene expression discriminates responders and nonresponders in treatment of chronic hepatitis C viral infection. Gastroenterology 2005;128:1437–1444. 15887125 [PubMed]

5 Feld JJ, Nanda S, Huang Y, Chen W, Cam M, Pusek SN, et al. Hepatic gene expression during treatment with peginterferon and ribavirin: identifying molecular pathways for treatment response. Hepatology 2007;46:1548–1563. 17929300 [OpenAIRE] [PubMed]

6 Sarasin‐Filipowicz M, Oakeley EJ, Duong FH, Christen V, Terracciano L, Filipowicz W, et al. Interferon signaling and treatment outcome in chronic hepatitis C. Proc Natl Acad Sci U S A 2008;105:7034–7039. 18467494 [OpenAIRE] [PubMed]

7 Honda M, Sakai A, Yamashita T, Nakamoto Y, Mizukoshi E, Sakai Y, et al. Hepatic ISG expression is associated with genetic variation in interleukin 28B and the outcome of IFN therapy for chronic hepatitis C. Gastroenterology 2010;139:499–509. 20434452 [OpenAIRE] [PubMed]

8 Thomas DL, Thio CL, Martin MP, Qi Y, Ge D, O'Huigin C, et al. Genetic variation in IL28B and spontaneous clearance of hepatitis C virus. Nature 2009;461:798–801. 19759533 [OpenAIRE] [PubMed]

9 Tillmann HL, Thompson AJ, Patel K, Wiese M, Tenckhoff H, Nischalke HD, et al. A polymorphism near IL28B is associated with spontaneous clearance of acute hepatitis C virus and jaundice. Gastroenterology 2010;139:1586–1592. 20637200 [OpenAIRE] [PubMed]

10 Ge D, Fellay J, Thompson AJ, Simon JS, Shianna KV, Urban TJ, et al. Genetic variation in IL28B predicts hepatitis C treatment‐induced viral clearance. Nature 2009;461:399–401. 19684573 [PubMed]

11 Odorizzi PM, Wherry EJ. Immunology. An interferon paradox. Science 2013;340:155–156. 23580520 [OpenAIRE] [PubMed]

12 Meylan E, Curran J, Hofmann K, Moradpour D, Binder M, Bartenschlager R, et al. Cardif is an adaptor protein in the RIG‐I antiviral pathway and is targeted by hepatitis C virus. Nature 2005;437:1167–1172. 16177806 [OpenAIRE] [PubMed]

13 Li K, Foy E, Ferreon JC, Nakamura M, Ferreon AC, Ikeda M, et al. 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 2005;102:2992–2997. 15710891 [OpenAIRE] [PubMed]

14 Wieland S, Makowska Z, Campana B, Calabrese D, Dill MT, Chung J, et al. Simultaneous detection of hepatitis C virus and interferon stimulated gene expression in infected human liver. Hepatology 2014;59:2121–2130. 24122862 [OpenAIRE] [PubMed]

15 Koonin EV. The phylogeny of RNA‐dependent RNA polymerases of positive‐strand RNA viruses. J Gen Virol 1991;72:2197–2206. 1895057 [OpenAIRE] [PubMed]

46 references, page 1 of 4
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