Synergy of entry inhibitors with direct-acting antivirals uncovers novel combinations for prevention and treatment of hepatitis C

Gut

Volumn 64, Issue 3, 2015, Pages 483-494

  Xiao, Fei ^a   Fofana, Isabel ^a   Thumann, Christine ^a   Mailly, Laurent ^a   Alles, Roxane ^a,b   Robinet, Eric ^a   Meyer, Nicolas ^c   Schaeffer, Mickaël ^c   Habersetzer, François ^a,c   Doffoël, Michel ^a,c   Leyssen, Pieter ^d   Neyts, Johan ^d   Zeisel, Mirjam B ^a   Baumert, Thomas F ^a,c,e  

^a UNIVERSITÉ DE STRASBOURG   (France)

^b INSERM   (France)

^c UNIVERSITY HOSPITAL OF STRASBOURG   (France)

^d REGA INSTITUTE FOR MEDICAL RESEARCH   (Belgium)

^e MASSACHUSETTS GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALISPORIVIR; ALPHA INTERFERON; ANTIVIRUS AGENT; BOCEPREVIR; CD81 ANTIGEN; CLAUDIN 1; DACLATASVIR; DANOPREVIR; DASATINIB; ERLOTINIB; MERICITABINE; RIBAVIRIN; SCAVENGER RECEPTOR B; SCAVENGER RECEPTOR BI; SIMEPREVIR; SOFOSBUVIR; TELAPREVIR;

ANIMAL EXPERIMENT; ARTICLE; CELL CULTURE; CLINICAL PRACTICE; CONTROLLED STUDY; DRUG EFFICACY; DRUG POTENTIATION; GENOTYPE; GRAFT INFECTION; HEPATITIS C; HUMAN; IC50; LIVER GRAFT; MOUSE; NONHUMAN; TREATMENT OUTCOME; VIRUS ENTRY; ANIMAL; CELL LINE; CHIMERA; COMBINATION DRUG THERAPY; DRUG EFFECTS; HEPACIVIRUS; LIVER CELL; SCID MOUSE; VIROLOGY;

ANIMALS; ANTIVIRAL AGENTS; CELL LINE; CHIMERA; DRUG SYNERGISM; DRUG THERAPY, COMBINATION; HEPACIVIRUS; HEPATITIS C; HEPATOCYTES; HUMANS; MICE; MICE, SCID; VIRUS INTERNALIZATION;

EID: 84922375496     PISSN: 00175749     EISSN: 14683288     Source Type: Journal    
DOI: 10.1136/gutjnl-2013-306155     Document Type: Article

References (54)

1. Dabbouseh NM, Jensen DM. Future therapies for chronic hepatitis C. Nat Rev Gastroenterol Hepatol 2013; 10:268-76.
2. Liang TJ, Ghany MG. Current and future therapies for hepatitis C virus infection. N Engl J Med 2013; 368:1907-17.
3. Sarrazin C, Hezode C, Zeuzem S., et al. Antiviral strategies in hepatitis C virus infection. J Hepatol 2012; 56(SUPPL. 1):S88-100.
4. Chung RT, Baumert TF. Curing chronic hepatitis C-the arc of a medical triumph. N Engl J Med 2014; 370:1576-8.
5. Crespo G, Marino Z, Navasa M., et al. Viral hepatitis in liver transplantation. Gastroenterology 2012; 142:1373-83 e1.
6. Garg V, van Heeswijk R, Lee JE, et al. Effect of telaprevir on the pharmacokinetics of cyclosporine and tacrolimus. Hepatology 2011; 54:20-7.
7. Charlton M. Telaprevir, boceprevir, cytochrome P450 and immunosuppressive agents-a potentially lethal cocktail. Hepatology 2011; 54:3-5.
8. Zeisel MB, Lupberger J, Fofana I., et al. Host-targeting agents for prevention and treatment of chronic hepatitis C-perspectives and challenges. J Hepatol 2013; 58:375-84.
9. 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.
10. Fofana I, Fafi-Kremer S, Carolla P., et al. Mutations that alter use of hepatitis C virus cell entry factors mediate escape from neutralizing antibodies. Gastroenterology 2012; 143:223-33 e9.
11. Zona L, Lupberger J, Sidahmed-Adrar N, et al. HRas signal transduction promotes hepatitis C virus cell entry by triggering assembly of the host tetraspanin receptor complex. Cell Host Microbe 2013; 13:302-13.
12. Sainz B Jr, Barretto N., Martin DN, et al. Identification of the Niemann-Pick C1-like 1 cholesterol absorption receptor as a new hepatitis C virus entry factor. Nat Med 2012; 18:281-5.
13. Lupberger J, Zeisel MB, Xiao F, et al. EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy. Nat Med 2011; 17:589-95.
14. Zahid MN, Turek M, Xiao F., et al. The postbinding activity of scavenger receptor class B type I mediates initiation of hepatitis C virus infection and viral dissemination. Hepatology 2013; 57:492-504.
15. 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.
16. Fofana I, Xiao F, Thumann C., et al. A novel monoclonal anti-CD81 antibody produced by genetic immunization efficiently inhibits Hepatitis C virus cell-cell transmission. PLoS One 2013; 8:e64221.
17. Meuleman P, Hesselgesser J, Paulson M., et al. Anti-CD81 antibodies can prevent a hepatitis C virus infection in vivo. Hepatology 2008; 48:1761-8.
18. Syder AJ, Lee H, Zeisel M.B., et al. Small molecule scavenger receptor BI antagonists are potent HCV entry inhibitors. J Hepatol 2011; 54:48-55.
19. Haid S, Novodomska A, Gentzsch J., et al. A plant-derived flavonoid inhibits entry of all HCV genotypes into human hepatocytes. Gastroenterology 2012; 143:213-22.e5.
20. Calland N, Albecka A, Belouzard S., et al. (-)-Epigallocatechin-3-gallate is a new inhibitor of hepatitis C virus entry. Hepatology 2012; 55:720-9.
21. Meuleman P, Albecka A, Belouzard S., et al. Griffithsin has antiviral activity against hepatitis C virus. Antimicrob Agents Chemother 2011; 55:5159-67.
22. Fofana I, Krieger SE, Grunert F, et al. Monoclonal anti-claudin 1 antibodies prevent hepatitis C virus infection of primary human hepatocytes. Gastroenterology 2010; 139:953-64, 64 e1-4.
23. Lupberger J, Duong FH, Fofana I, et al. Epidermal growth factor receptor signaling impairs the antiviral activity of interferon-alpha. Hepatology 2013; 58:1225-35.
24. Zhao L, Wientjes MG, Au JL. Evaluation of combination chemotherapy: integration of nonlinear regression, curve shift, isobologram, and combination index analyses. Clin Cancer Res 2004; 10:7994-8004.
25. Prichard MN, Shipman C Jr. A three-dimensional model to analyze drug-drug interactions. Antiviral Res 1990; 14:181-205.
26. Bauhofer O, Ruggieri A, Schmid B., et al. Persistence of HCV in quiescent hepatic cells under conditions of an interferon-induced antiviral response. Gastroenterology 2012; 143:429-38 e8.
27. Pietschmann T, Zayas M, Meuleman P., et al. Production of infectious genotype 1b virus particles in cell culture and impairment by replication enhancing mutations. PLoS Pathog 2009; 5:e1000475.
28. Mercer DF, Schiller DE, Elliott J.F., et al. Hepatitis C virus replication in mice with chimeric human livers. Nat Med 2001; 7:927-33.
29. Wyles DL, Kaihara KA, Vaida F, et al. Synergy of small molecular inhibitors of hepatitis C virus replication directed at multiple viral targets. J Virol 2007; 81:3005-8.
30. Jacobson IM, McHutchison JG, Dusheiko G, et al. Telaprevir for previously untreated chronic hepatitis C virus infection. N Engl J Med 2011; 364:2405-16.
31. Zeuzem S, Andreone P, Pol S., et al. Telaprevir for retreatment of HCV infection. N Engl J Med 2011; 364:2417-28.
32. Bacon BR, Gordon SC, Lawitz E, et al. Boceprevir for previously treated chronic HCV genotype 1 infection. N Engl J Med 2011; 364:1207-17.
33. Poordad F, McCone J Jr, Bacon BR, et al. Boceprevir for untreated chronic HCV genotype 1 infection. N Engl J Med 2011; 364:1195-206.
34. Reesink HW, Fanning GC, Farha K.A., et al. Rapid HCV-RNA decline with once daily TMC435: a phase I study in healthy volunteers and hepatitis C patients. Gastroenterology 2010; 138:913-21.
35. Gane EJ, Roberts SK, Stedman C.A., et al. Oral combination therapy with a nucleoside polymerase inhibitor (RG7128) and danoprevir for chronic hepatitis C genotype 1 infection (INFORM-1): a randomised, double-blind, placebo-controlled, dose-escalation trial. Lancet 2010; 376:1467-75.
36. Gao M, Nettles RE, Belema M, et al. Chemical genetics strategy identifies an HCV NS5A inhibitor with a potent clinical effect. Nature 2010; 465:96-100.
37. Lok AS, Gardiner DF, Lawitz E, et al. Preliminary study of two antiviral agents for hepatitis C genotype 1. N Engl J Med 2012; 366:216-24.
38. Chayama K, Takahashi S, Toyota J., et al. Dual therapy with the nonstructural protein 5A inhibitor, daclatasvir, and the nonstructural protein 3 protease inhibitor, asunaprevir, in hepatitis C virus genotype 1b-infected null responders. Hepatology 2012; 55:742-8.
39. Gane EJ, Stedman CA, Hyland R.H., et al. Nucleotide polymerase inhibitor sofosbuvir plus ribavirin for hepatitis C. N Engl J Med 2013; 368:34-44.
40. Lawitz E, Mangia A, Wyles D., et al. Sofosbuvir for previously untreated chronic hepatitis C infection. N Engl J Med 2013; 368:1878-87.
41. Jacobson IM, Gordon SC, Kowdley K.V., et al. Sofosbuvir for hepatitis C genotype 2 or 3 in patients without treatment options. N Engl J Med 2013; 368:1867-77.
42. Flisiak R, Feinman SV, Jablkowski M, et al. The cyclophilin inhibitor Debio 025 combined with PEG IFNalpha2a significantly reduces viral load in treatment-naive hepatitis C patients. Hepatology 2009; 49:1460-8.
43. Himmelsbach K, Hildt E. The kinase inhibitor Sorafenib impairs the antiviral effect of interferon alpha on hepatitis C virus replication. Eur J Cell Biol 2013; 92:12-20.
44. Shi N, Hiraga N, Imamura M., et al. Combination therapies with NS5A, NS3 and NS5B inhibitors on different genotypes of hepatitis C virus in human hepatocyte chimeric mice. Gut 2013; 62:1055-61.
45. Lawitz E, Lalezari JP, Hassanein T, et al. Sofosbuvir in combination with peginterferon alfa-2a and ribavirin for non-cirrhotic, treatment-naive patients with genotypes 1, 2, and 3 hepatitis C infection: a randomised, double-blind, phase 2 trial. Lancet Infect Dis 2013; 13:401-8.
46. Kowdley KV, Lawitz E, Crespo I., et al. Sofosbuvir with pegylated interferon alfa-2a and ribavirin for treatment-naive patients with hepatitis C genotype-1 infection (ATOMIC): an open-label, randomised, multicentre phase 2 trial. Lancet 2013; 381:2100-7.
47. Tong X, Le Pogam S, Li L, et al. In vivo emergence of a novel mutant L159F/L320F in the NS5B polymerase confers low-level resistance to the HCV polymerase inhibitors mericitabine and sofosbuvir. J Infect Dis 2014; 209:668-75.
48. Henrich TJ, Kuritzkes DR. HIV-1 entry inhibitors: recent development and clinical use. Curr Opin Virol 2013; 3:51-7.
49. Shepherd FA, Rodrigues Pereira J, Ciuleanu T, et al. Erlotinib in previously treated non-small-cell lung cancer. N Engl J Med 2005; 353:123-32.
50. Matsumura T, Hu Z, Kato T., et al. Amphipathic DNA polymers inhibit hepatitis C virus infection by blocking viral entry. Gastroenterology 2009; 137:673-81.
51. Wagoner J, Negash A, Kane O.J., et al. Multiple effects of silymarin on the hepatitis C virus lifecycle. Hepatology 2010; 51:1912-21.
52. Marino Z, Crespo G, D'Amato M, et al. Intravenous silibinin monotherapy shows significant antiviral activity in HCV-infected patients in the peri-transplantation period. J Hepatol 2013; 58:415-20.
53. Chung RT, Gordon FD, Curry M.P., et al. Human monoclonal antibody MBL-HCV1 delays HCV viral rebound following liver transplantation: a randomized controlled study. Am J Transplant 2013; 13:1047-54.
54. Cataldo VD, Gibbons DL, Perez-Soler R, et al. Treatment of non-small-cell lung cancer with erlotinib or gefitinib. N Engl J Med 2011; 364:947-55.