Targeting a host-cell entry factor barricades antiviral-resistant HCV variants from on-therapy breakthrough in human-liver mice

Gut

Volumn 65, Issue 12, 2016, Pages 2029-2034

  Vercauteren, Koen ^a   Brown, Richard J P ^b   Mesalam, Ahmed Atef ^a   Doerrbecker, Juliane ^b   Bhuju, Sabin ^c   Geffers, Robert ^c   Van Den Eede, Naomi ^a   McClure, C Patrick ^d   Troise, Fulvia ^e   Verhoye, Lieven ^a   Baumert, Thomas ^f,g   Farhoudi, Ali ^a   Cortese, Riccardo ^e   Ball, Jonathan K ^d   Leroux Roels, Geert ^a   Pietschmann, Thomas ^b,h   Nicosia, Alfredo ^e,i   Meuleman, Philip ^a  

^a GHENT UNIVERSITY HOSPITAL   (Belgium)

^b INSTITUTE OF INFECTION IMMUNOLOGY   (Germany)

^c HELMHOLTZ CENTRE FOR INFECTION RESEARCH   (Germany)

^d UNIVERSITY OF NOTTINGHAM   (United Kingdom)

^e CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^f INSERM   (France)

^g UNIVERSITÉ DE STRASBOURG   (France)

^h German Centre for Infection Research (DZIF) Partner Site Hannover Braunschweig   (Germany)

ⁱ UNIVERSITY OF NAPLES FEDERICO II   (Italy)

Author keywords

ANTIVIRAL THERAPY; CHRONIC VIRAL HEPATITIS; HCV; HEPATITIS C; LIVER

Indexed keywords

CILUPREVIR; MONOCLONAL ANTIBODY 1671; NONSTRUCTURAL PROTEIN 3; SCAVENGER RECEPTOR BI; UNCLASSIFIED DRUG; VIRUS FUSION INHIBITOR; VIRUS RNA; ANTIVIRUS AGENT; NS-5 PROTEIN, HEPATITIS C VIRUS; PROTEINASE INHIBITOR; VIRAL PROTEIN;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTIVIRAL RESISTANCE; ARTICLE; CHRONIC HEPATITIS C; COMBINATION DRUG THERAPY; CONTROLLED STUDY; HEPATITIS C VIRUS SUBTYPE 1B; MONOTHERAPY; MOUSE; NEXT GENERATION SEQUENCING; NONHUMAN; PRIORITY JOURNAL; PROTEASE DOMAIN; PROTEIN DOMAIN; REBOUND; VIREMIA; VIRUS LOAD; AMINO ACID SUBSTITUTION; ANIMAL; DISEASE MODEL; DRUG EFFECTS; GENETICS; GENOTYPE; HEPACIVIRUS; HEPATITIS C, CHRONIC; LIVER; MISSENSE MUTATION;

AMINO ACID SUBSTITUTION; ANIMALS; ANTIVIRAL AGENTS; DISEASE MODELS, ANIMAL; DRUG RESISTANCE, VIRAL; GENOTYPE; HEPACIVIRUS; HEPATITIS C, CHRONIC; LIVER; MICE; MUTATION, MISSENSE; PROTEASE INHIBITORS; VIRAL NONSTRUCTURAL PROTEINS;

EID: 84940069500     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2014-309045     Document Type: Article

References (39)

1. Hajarizadeh B, Grebely J, Dore GJ. Epidemiology and natural history of HCV infection. Nat Rev Gastroenterol Hepatol 2013;10:553-62.
2. Pawlotsky JM. Treatment failure and resistance with direct-acting antiviral drugs against hepatitis C virus. Hepatology 2011;53:1742-51.
3. Chung RT, Baumert TF. Curing chronic hepatitis C-the arc of a medical triumph. N Engl J Med 2014;370:1576-8.
4. Kieffer TL, Sarrazin C, Miller JS, et al. Telaprevir and pegylated interferon-alpha-2a inhibit wild-type and resistant genotype 1 hepatitis C virus replication in patients. Hepatology 2007;46:631-9.
5. Susser S, Welsch C, Wang Y, et al. Characterization of resistance to the protease inhibitor boceprevir in hepatitis C virus-infected patients. Hepatology 2009;50:1709-18.
6. Feld JJ, Kowdley KV, Coakley E, et al. Treatment of HCV with ABT-450/r-ombitasvir and dasabuvir with ribavirin. N Engl J Med 2014;370:1594-603.
7. Scarselli E, Ansuini H, Cerino R, et al. The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus. EMBO J 2002;21:5017-25.
8. Meuleman P, Catanese MT, Verhoye L, et al. A human monoclonal antibody targeting scavenger receptor class B type I precludes hepatitis C virus infection and viral spread in vitro and in vivo. Hepatology 2012;55:364-72.
9. Lacek K, Vercauteren K, Grzyb K, et al. Novel human SR-BI antibodies prevent infection and dissemination of HCV in vitro and in humanized mice. J Hepatol 2012;57:17-23.
10. Vercauteren K, Van Den Eede N, Mesalam AA, et al. Successful anti-scavenger receptor class B type I (SR-BI) monoclonal antibody therapy in humanized mice after challenge with HCV variants with in vitro resistance to SR-BI-targeting agents. Hepatology 2014;60:1508-18.
11. Meuleman P, Libbrecht L, De Vos R, et al. Morphological and biochemical characterization of a human liver in a uPA-SCID mouse chimera. Hepatology 2005;41:847-56.
12. Mercer DF, Schiller DE, Elliott JF, et al. Hepatitis C virus replication in mice with chimeric human livers. Nat Med 2001;7:927-33.
13. Vercauteren K, de Jong YP, Meuleman P. Animal models for the study of HCV. Curr Opin Virol 2015;13:67-74.
14. Vercauteren K, de Jong YP, Meuleman P. HCV animal models and liver disease. J Hepatol 2014;61(1 Suppl):S26-33.
15. Irving WL, Rupp D, McClure CP, et al. Development of a high-throughput pyrosequencing assay for monitoring temporal evolution and resistance associated variant emergence in the Hepatitis C virus protease coding-region. Antivir Res 2014;110:52-9.
16. Verbinnen T, Van Marck H, Vandenbroucke I, et al. Tracking the evolution of multiple in vitro hepatitis C virus replicon variants under protease inhibitor selection pressure by 454 deep sequencing. J Virol 2010;84:11124-33.
17. Lenz O, Verbinnen T, Lin TI, et al. In vitro resistance profile of the hepatitis C virus NS3/4A protease inhibitor TMC435. Antimicrob Agents Chemother 2010;54:1878-87.
18. Rong LB, Dahari H, Ribeiro RM, et al. Rapid emergence of protease inhibitor resistance in hepatitis C virus. Sci Transl Med 2010;2:30ra32.
19. Mailly L, Xiao F, Lupberger J, et al. Clearance of persistent hepatitis C virus infection in humanized mice using a claudin-1-targeting monoclonal antibody. Nat Biotechnol 2015;33:549-54.
20. de Jong YP, Dorner M, Mommersteeg MC, et al. Broadly neutralizing antibodies abrogate established hepatitis C virus infection. Sci Transl Med 2014;6:254ra129.
21. Sato M, Maekawa S, Komatsu N, et al. Deep sequencing and phylogenetic analysis of variants resistant to interferon-based protease inhibitor therapy in chronic hepatitis induced by genotype 1b hepatitis C virus. J Virol 2015;89:6105-16.
22. Flores MV, Corbau RG, Guionaud S. Pharmacokinetics and safety in cynomolgus monkeys of a monoclonal antibody targeting human scavenger receptor class B type-1 for hepatitis C treatment. Antivir Ther 2013;18:775-84.
23. Masson D, Koseki M, Ishibashi M, et al. Increased HDL cholesterol and apoA-I in humans and mice treated with a novel SR-BI inhibitor. Arterioscler Thromb Vasc Biol 2009;29:2054-60.
24. Wong-Staal F, Syder AJ, McKelvy JF. Targeting HCV entry for development of therapeutics. Viruses 2010;2:1718-33.
25. Haqqani AA, Tilton JC. Entry inhibitors and their use in the treatment of HIV-1 infection. Antiviral Res 2013;98:158-70.
26. Xiao F, Fofana I, Thumann C, et al. Synergy of entry inhibitors with direct-acting antivirals uncovers novel combinations for prevention and treatment of hepatitis C. Gut 2015;64:483-94.
27. Uprichard SL, Sainz B. Inhibition of hepatitis C entry: too soon to dismiss while many are still being denied treatment. Gut 2015;64:6901.
28. Xiao F, Fofana I, Heydmann L, et al. Hepatitis C virus cell-cell transmission and resistance to direct-acting antiviral agents. PLoS Pathog 2014;10:e1004128.
29. Zhu H, Wong-Staal F, Lee H, et al. Evaluation of ITX 5061, a scavenger receptor B1 antagonist: resistance selection and activity in combination with other hepatitis C virus antivirals. J Infect Di 2012;205:656-62.
30. Forns X, Gordon SC, Zuckerman E, et al. Grazoprevir/elbasvir plus ribavirin for chronic HCV genotype-1 infection after failure of combination therapy containing a direct-acting antiviral agent. J Hepatol Published Online First: 18 Apr 2015. doi:10.1016/j.jhep.2015.04.009
31. Lawitz E, Flamm S, Yang JC, et al. Retreatment of patients who failed 8 or 12 weeks of ledipasvir/sofosbuvir-based regimens with ledipasvir/sofosbuvir for 24 weeks. J Hepatol 2015;62:S192. abstract # O005.
32. Poordad F, Lawitz E, Gutierrez JA, et al. C-swift: grazoprevir/elbasvir+sofosbuvir in cirrhotic and noncirrhotic, treatment-naive patients with hepatitis c virus genotype 1 infection, for durations of 4, 6 or 8 weeks and genotype 3 infection for durations of 8 or 12 weeks. J Hepatol 2015;62:S192. abstract # O006.
33. Poordad F, Schiff ER, Vierling JM, et al. Daclatasvir, Sofosbuvir, and Ribavirin combination for hcv patients with advanced cirrhosis or posttransplant recurrence: phase 3 ally-1 study. 2015;62(Suppl 2):S261. abstract #LO8.
34. Dvory-Sobol H, Wyles D, Ouyang W, et al. Long-term persistence of HCV ns5a variants after treatment with ns5a inhibitor ledipasvir. J Hepatol 2015;62:S221. abstract O059.
35. Petersen J, Dandri M, Mier W, et al. Prevention of hepatitis B virus infection in vivo by entry inhibitors derived from the large envelope protein. Nat Biotechnol 2008;26:335-41.
36. Meuleman P, Vanlandschoot P, Leroux-Roels G. A simple and rapid method to determine the zygosity of uPA-transgenic SCID mice. Biochem Biophys Res Commun 2003;308:375-8.
37. Vanwolleghem T, Libbrecht L, Hansen BE, et al. Factors determining successful engraftment of hepatocytes and susceptibility to hepatitis B and C virus infection in uPA-SCID mice. J Hepatol 2010;53:468-76.
38. Catanese MT, Graziani R, von Hahn T, et al. High-avidity monoclonal antibodies against the human scavenger class B type I receptor efficiently block hepatitis C virus infection in the presence of high-density lipoprotein. J Virol 2007; 81:8063-71.
39. Fafi-Kremer S, Fofana I, Soulier E, et al. Viral entry and escape from antibody-mediated neutralization influence hepatitis C virus reinfection in liver transplantation. J Exp Med 2010;207:2019-31.