The kinase-inhibitor sorafenib inhibits multiple steps of the Hepatitis C Virus infectious cycle in vitro

Antiviral Research

Volumn 118, Issue , 2015, Pages 93-102

  Descamps, Véronique ^a   Helle, François ^a   Louandre, Christophe ^a   Martin, Elodie ^a   Brochot, Etienne ^a   Izquierdo, Laure ^a   Fournier, Carole ^a   Hoffmann, Thomas W ^a   Castelain, Sandrine ^a   Duverlie, Gilles ^a   Galmiche, Antoine ^a   François, Catherine ^a  

^a UNIVERSITÉ DE PICARDIE JULES VERNE   (France)

Author keywords

Antiviral activity; Claudin 1; Hepatitis C Virus; Sorafenib

Indexed keywords

CLAUDIN 1; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN SERINE THREONINE KINASE; SORAFENIB; VASCULOTROPIN RECEPTOR 2; ANTIVIRUS AGENT; CARBANILAMIDE DERIVATIVE; NICOTINAMIDE;

ANGIOGENESIS; ANTINEOPLASTIC ACTIVITY; ANTIVIRAL ACTIVITY; ARTICLE; CELL CYCLE; CELL PROLIFERATION; CELL VIABILITY; DRUG EFFECT; DRUG MECHANISM; ENZYME INHIBITION; FLUORESCENCE MICROSCOPY; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IN VITRO STUDY; LIVER CELL; LIVER CELL CARCINOMA; NONHUMAN; PRIORITY JOURNAL; TUMOR CELL; VIRUS ENTRY; VIRUS PARTICLE; ANALOGS AND DERIVATIVES; CELL CULTURE; DRUG EFFECTS; HEPACIVIRUS; PHYSIOLOGY; VIROLOGY; VIRUS REPLICATION;

HEPATITIS C VIRUS;

ANTIVIRAL AGENTS; CELLS, CULTURED; HEPACIVIRUS; HEPATOCYTES; HUMANS; NIACINAMIDE; PHENYLUREA COMPOUNDS; VIRUS INTERNALIZATION; VIRUS REPLICATION;

EID: 84926664291     PISSN: 01663542     EISSN: 18729096     Source Type: Journal    
DOI: 10.1016/j.antiviral.2015.03.012     Document Type: Article

References (39)

1. G.K. Abou-Alfa, L. Schwartz, S. Ricci, D. Amadori, A. Santoro, A. Figer, J. De Greve, J.Y. Douillard, C. Lathia, B. Schwartz, I. Taylor, M. Moscovici, and L.B. Saltz Phase II study of sorafenib in patients with advanced hepatocellular carcinoma J. Clin. Oncol. 24 2006 4293 4300
2. H. Barth, E.K. Schnober, F. Zhang, R.J. Linhardt, E. Depla, B. Boson, F.L. Cosset, A.H. Patel, H.E. Blum, and T.F. Baumert Viral and cellular determinants of the hepatitis C virus envelope-heparan sulfate interaction J. Virol. 80 2006 10579 10590
3. B. Bartosch, J. Dubuisson, and F.L. Cosset Infectious hepatitis C virus pseudo-particles containing functional E1-E2 envelope protein complexes J. Exp. Med. 197 2003 633 642
4. E. Blanchard, S. Belouzard, L. Goueslain, T. Wakita, J. Dubuisson, C. Wychowski, and Y. Rouille Hepatitis C virus entry depends on clathrin-mediated endocytosis J. Virol. 80 2006 6964 6972
5. R.S. Brown Hepatitis C and liver transplantation Nature 436 2005 973 978
6. T. Burckstummer, M. Kriegs, J. Lupberger, E.K. Pauli, S. Schmittel, and E. Hildt Raf-1 kinase associates with Hepatitis C virus NS5A and regulates viral replication FEBS Lett. 580 2006 575 580
7. R. Cabrera, A.R. Limaye, P. Horne, R. Mills, C. Soldevila-Pico, V. Clark, G. Morelli, R. Firpi, and D.R. Nelson The anti-viral effect of sorafenib in hepatitis C-related hepatocellular carcinoma Aliment Pharmacol. Ther. 37 2013 91 97
8. M.J. Evans, T. von Hahn, D.M. Tscherne, A.J. Syder, M. Panis, B. Wolk, T. Hatziioannou, J.A. McKeating, P.D. Bieniasz, and C.M. Rice Claudin-1 is a hepatitis C virus co-receptor required for a late step in entry Nature 446 2007 801 805
9. C. Fournier, F. Helle, V. Descamps, V. Morel, C. Francois, S. Dedeurwaerder, C. Wychowski, G. Duverlie, and S. Castelain Natural selection of adaptive mutations in non-structural genes increases trans-encapsidation of hepatitis C virus replicons lacking envelope protein genes J. Gen. Virol. 94 2013 996 1008
10. A. Galmiche, J. Fueller, A. Santel, G. Krohne, I. Wittig, A. Doye, M. Rolando, G. Flatau, E. Lemichez, and U.R. Rapp Isoform-specific interaction of C-RAF with mitochondria J. Biol. Chem. 283 2008 14857 14866
11. F. Helle, E. Brochot, C. Fournier, V. Descamps, L. Izquierdo, T.W. Hoffmann, V. Morel, Y.E. Herpe, A. Bengrine, S. Belouzard, C. Wychowski, J. Dubuisson, C. Francois, J.M. Regimbeau, S. Castelain, and G. Duverlie Permissivity of primary human hepatocytes and different hepatoma cell lines to cell culture adapted hepatitis C virus PLoS One 8 2013 e70809
12. K. Himmelsbach, and E. Hildt The kinase inhibitor Sorafenib impairs the antiviral effect of interferon alpha on hepatitis C virus replication Eur. J. Cell. Biol. 92 2013 12 20
13. K. Himmelsbach, D. Sauter, T.F. Baumert, L. Ludwig, H.E. Blum, and E. Hildt New aspects of an anti-tumour drug: sorafenib efficiently inhibits HCV replication Gut 58 2009 1644 1653
14. F. Ji, and Z. Li Letter: the antiviral activity of sorafenib in patients with hepatitis C-related hepatocellular carcinoma Aliment Pharmacol. Ther. 37 2013 372 373
15. C.T. Jones, M.T. Catanese, L.M. Law, S.R. Khetani, A.J. Syder, A. Ploss, T.S. Oh, J.W. Schoggins, M.R. MacDonald, S.N. Bhatia, and C.M. Rice Real-time imaging of hepatitis C virus infection using a fluorescent cell-based reporter system Nat. Biotechnol. 28 2010 167 171
16. T. Kato, T. Date, M. Miyamoto, A. Furusaka, K. Tokushige, M. Mizokami, and T. Wakita Efficient replication of the genotype 2a hepatitis C virus subgenomic replicon Gastroenterology 125 2003 1808 1817
17. G. Krause, L. Winkler, S.L. Mueller, R.F. Haseloff, J. Piontek, and I.E. Blasig Structure and function of claudins Biochim. Biophys. Acta 1778 2008 631 645
18. C. Louandre, Z. Ezzoukhry, C. Godin, J.C. Barbare, J.C. Maziere, B. Chauffert, and A. Galmiche Iron-dependent cell death of hepatocellular carcinoma cells exposed to sorafenib Int. J. Cancer 2013
19. J. Lupberger, M.B. Zeisel, F. Xiao, C. Thumann, I. Fofana, L. Zona, C. Davis, C.J. Mee, M. Turek, S. Gorke, C. Royer, B. Fischer, M.N. Zahid, D. Lavillette, J. Fresquet, F.L. Cosset, S.M. Rothenberg, T. Pietschmann, A.H. Patel, P. Pessaux, M. Doffoel, W. Raffelsberger, O. Poch, J.A. McKeating, L. Brino, and T.F. Baumert EGFR and EphA2 are host factors for hepatitis C virus entry and possible targets for antiviral therapy Nat. Med. 17 2011 589 595
20. C.J. Mee, M.J. Farquhar, H.J. Harris, K. Hu, W. Ramma, A. Ahmed, P. Maurel, R. Bicknell, P. Balfe, and J.A. McKeating Hepatitis C virus infection reduces hepatocellular polarity in a vascular endothelial growth factor-dependent manner Gastroenterology 138 2010 1134 1142
21. L. Meertens, C. Bertaux, and T. Dragic Hepatitis C virus entry requires a critical postinternalization step and delivery to early endosomes via clathrin-coated vesicles J. Virol. 80 2006 11571 11578
22. N. Menzel, W. Fischl, K. Hueging, D. Bankwitz, A. Frentzen, S. Haid, J. Gentzsch, L. Kaderali, R. Bartenschlager, and T. Pietschmann MAP-kinase regulated cytosolic phospholipase A2 activity is essential for production of infectious hepatitis C virus particles PLoS Pathog. 8 2012 e1002829
23. D. Moradpour, F. Penin, and C.M. Rice Replication of hepatitis C virus Nat. Rev. Microbiol. 5 2007 453 463
24. C.L. Murray, and C.M. Rice Turning hepatitis C into a real virus Annu. Rev. Microbiol. 65 2011 307 327
25. H. Nakabayashi, K. Taketa, K. Miyano, T. Yamane, and J. Sato Growth of human hepatoma cells lines with differentiated functions in chemically defined medium Cancer Res. 42 1982 3858 3863
26. A. Op De Beeck, C. Voisset, B. Bartosch, Y. Ciczora, L. Cocquerel, Z. Keck, S. Foung, F.L. Cosset, and J. Dubuisson Characterization of functional hepatitis C virus envelope glycoproteins J. Virol. 78 2004 2994 3002
27. J.M. Pawlotsky Treatment failure and resistance with direct-acting antiviral drugs against hepatitis C virus Hepatology 53 2011 1742 1751
28. P. Pileri, Y. Uematsu, S. Campagnoli, G. Galli, F. Falugi, R. Petracca, A.J. Weiner, M. Houghton, D. Rosa, G. Grandi, and S. Abrignani Binding of hepatitis C virus to CD81 Science 282 1998 938 941
29. A. Ploss, M.J. Evans, V.A. Gaysinskaya, M. Panis, H. You, Y.P. de Jong, and C.M. Rice Human occludin is a hepatitis C virus entry factor required for infection of mouse cells Nature 457 2009 882 886
30. C.I. Popescu, and J. Dubuisson Role of lipid metabolism in hepatitis C virus assembly and entry Biol. Cell 102 2010 63 74
31. V. Rocha-Perugini, M. Lavie, D. Delgrange, J. Canton, A. Pillez, J. Potel, C. Lecoeur, E. Rubinstein, J. Dubuisson, C. Wychowski, and L. Cocquerel The association of CD81 with tetraspanin-enriched microdomains is not essential for hepatitis C virus entry BMC Microbiol. 9 2009 111
32. B. Sainz Jr., N. Barretto, D.N. Martin, N. Hiraga, M. Imamura, S. Hussain, K.A. Marsh, X. Yu, K. Chayama, W.A. Alrefai, and S.L. Uprichard Identification of the Niemann-Pick C1-like 1 cholesterol absorption receptor as a new hepatitis C virus entry factor Nat. Med. 18 2012 281 285
33. B. Sainz Jr., N. Barretto, and S.L. Uprichard Hepatitis C virus infection in phenotypically distinct Huh7 cell lines PLoS One 4 2009 e6561
34. E. Scarselli, H. Ansuini, R. Cerino, R.M. Roccasecca, S. Acali, G. Filocamo, C. Traboni, A. Nicosia, R. Cortese, and A. Vitelli The human scavenger receptor class B type I is a novel candidate receptor for the hepatitis C virus EMBO J. 21 2002 5017 5025
35. J.M. Timpe, Z. Stamataki, A. Jennings, K. Hu, M.J. Farquhar, H.J. Harris, A. Schwarz, I. Desombere, G.L. Roels, P. Balfe, and J.A. McKeating Hepatitis C virus cell-cell transmission in hepatoma cells in the presence of neutralizing antibodies Hepatology 47 2008 17 24
36. T. Wakita, T. Pietschmann, T. Kato, T. Date, M. Miyamoto, Z. Zhao, K. Murthy, A. Habermann, H.G. Krausslich, M. Mizokami, R. Bartenschlager, and T.J. Liang Production of infectious hepatitis C virus in tissue culture from a cloned viral genome Nat. Med. 11 2005 791 796
37. S. Wilhelm, C. Carter, M. Lynch, T. Lowinger, J. Dumas, R.A. Smith, B. Schwartz, R. Simantov, and S. Kelley Discovery and development of sorafenib: a multikinase inhibitor for treating cancer Nat. Rev. Drug Discov. 5 2006 835 844
38. J. Witteveldt, M.J. Evans, J. Bitzegeio, G. Koutsoudakis, A.M. Owsianka, A.G. Angus, Z.Y. Keck, S.K. Foung, T. Pietschmann, C.M. Rice, and A.H. Patel CD81 is dispensable for hepatitis C virus cell-to-cell transmission in hepatoma cells J. Gen. Virol. 90 2009 48 58
39. L. Zona, J. Lupberger, N. Sidahmed-Adrar, C. Thumann, H.J. Harris, A. Barnes, J. Florentin, R.G. Tawar, F. Xiao, M. Turek, S.C. Durand, F.H. Duong, M.H. Heim, F.L. Cosset, I. Hirsch, D. Samuel, L. Brino, M.B. Zeisel, F. Le Naour, J.A. McKeating, and T.F. Baumert HRas signal transduction promotes hepatitis C virus cell entry by triggering assembly of the host tetraspanin receptor complex Cell Host Microbe 13 2013 302 313