The cyclophilin inhibitor alisporivir prevents hepatitis C virus-mediated mitochondrial dysfunction

Hepatology

Volumn 55, Issue 5, 2012, Pages 1333-1343

  Quarato, Giovanni ^a   D'Aprile, Annamaria ^a   Gavillet, Bruno ^b   Vuagniaux, Grégoire ^b   Moradpour, Darius ^c   Capitanio, Nazzareno ^a   Piccoli, Claudia ^a  

^a UNIVERSITY OF FOGGIA   (Italy)

^b DEBIOPHARM SA   (Switzerland)

^c LAUSANNE UNIVERSITY HOSPITAL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

ALISPORIVIR; CASPASE 3; CITRATE SYNTHASE; CYTOCHROME C; MITOCHONDRIAL PERMEABILITY TRANSITION PORE; POLYPROTEIN; REACTIVE OXYGEN METABOLITE;

ANTIVIRAL ACTIVITY; APOPTOSIS; ARTICLE; BIOENERGY; CELL DAMAGE; CELL RESPIRATION; DRUG EFFECT; ENZYME ACTIVATION; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; LIVER DISEASE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRION; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN EXPRESSION; VIRUS REPLICATION;

ANTIVIRAL AGENTS; APOPTOSIS; CALCIUM; CELL RESPIRATION; CELLS, CULTURED; CYCLOPHILINS; CYCLOSPORINE; HEPACIVIRUS; HUMANS; IMMUNOHISTOCHEMISTRY; MEMBRANE POTENTIALS; MITOCHONDRIA, LIVER; REACTIVE OXYGEN SPECIES; SENSITIVITY AND SPECIFICITY; VIRUS REPLICATION;

EID: 84859995274     PISSN: 02709139     EISSN: 15273350     Source Type: Journal    
DOI: 10.1002/hep.25514     Document Type: Article

References (44)

1. Shepard CW, Finelli L, Alter MJ. Global epidemiology of hepatitis C virus infection. Lancet Infect Dis 2005; 5: 558-567.
2. Pawlotsky JM. Therapy of hepatitis C: from empiricism to eradication. Hepatology 2006; 43: S207-S220.
3. Gallay PA. Cyclophilin inhibitors. Clin Liver Dis 2009; 13: 403-417.
4. Paeshuyse J, Kaul A, De Clercq E, Rosenwirth B, Dumont JM, Scalfaro P, et al. The non-immunosuppressive cyclosporin DEBIO-025 is a potent inhibitor of hepatitis C virus replication in vitro. Hepatology 2006; 43: 761-770.
5. Crabbé R, Vuagniaux G, Dumont JM, Nicolas-Métral V, Marfurt J, Novaroli L. An evaluation of the cyclophilin inhibitor Debio 025 and its potential as a treatment for chronic hepatitis C. Expert Opin Investig Drugs 2009; 18: 211-220.
6. Coelmont L, Kaptein S, Paeshuyse J, Vliegen I, Dumont JM, Vuagniaux G, et al. Debio 025, a cyclophilin binding molecule, is highly efficient in clearing hepatitis C virus (HCV) replicon-containing cells when used alone or in combination with specifically targeted antiviral therapy for HCV (STAT-C) inhibitors. Antimicrob Agents Chemother 2009; 53: 967-976.
7. Landrieu I, Hanoulle X, Bonachera F, Hamel A, Sibille N, Yin Y, et al. Structural basis for the non-immunosuppressive character of the cyclosporin A analogue Debio 025. Biochemistry 2010; 49: 4679-4686.
8. Gaither LA, Borawski J, Anderson LJ, Balabanis KA, Devay P, Joberty G, et al. Multiple cyclophilins involved in different cellular pathways mediate HCV replication. Virology 2010; 397: 43-55.
9. Liu Z, Yang F, Robotham JM, Tang H. Critical role of cyclophilin A and its prolyl-peptidyl isomerase activity in the structure and function of the hepatitis C virus replication complex. J Virol 2009; 83: 6554-6565.
10. Coelmont L, Hanoulle X, Chatterji U, Berger C, Snoeck J, Bobardt M, et al. DEB025 (Alisporivir) inhibits hepatitis C virus replication by preventing a cyclophilin A induced cis-trans isomerisation in domain II of NS5A. PLoS One 2010; 5: e13687.
11. Giorgio V, Soriano ME, Basso E, Bisetto E, Lippe G, Forte MA, et al. Cyclophilin D in mitochondrial pathophysiology. Biochim Biophys Acta 2010; 1797: 1113-1118.
12. Kroemer G, Galluzzi L, Brenner C. Mitochondrial membrane permeabilization in cell death. Physiol Rev 2007; 87: 99-163.
13. Rasola A, Sciacovelli M, Pantic B, Bernardi P. Signal transduction to the permeability transition pore. FEBS Lett 2010; 584: 1989-1996.
14. Rasola A, Bernardi P. The mitochondrial permeability transition pore and its involvement in cell death and in disease pathogenesis. Apoptosis 2007; 12: 815-833.
15. Lemasters JJ, Theruvath TP, Zhong Z, Nieminen AL. Mitochondrial calcium and the permeability transition in cell death. Biochim Biophys Acta 2009; 1787: 1395-1401.
16. Millar DP, Sargent MA, Osinska H, Baines CP, Barton ER, Vuagniaux G, et al. Genetic and pharmacologic inhibition of mitochondrial-dependent necrosis attenuates muscular dystrophy. Nat Med 2008; 14: 442-447.
17. Merlini L, Angelin A, Tiepolo T, Braghetta P, Sabatelli P, Zamparelli A, et al. Cyclosporin A corrects mitochondrial dysfunction and muscle apoptosis in patients with collagen VI myopathies. Proc Natl Acad Sci U S A 2008; 105: 5225-5229.
18. Gomez L, Thibault H, Gharib A, Dumont JM, Vuagniaux G, Scalfaro P, et al. Inhibition of mitochondrial permeability transition improves functional recovery and reduces mortality following acute myocardial infarction in mice. Am J Physiol Heart Circ Physiol 2007; 293: H1654-H661.
19. Piccoli C, Scrima R, Quarato G, D'Aprile A, Ripoli M, Lecce L, et al. Hepatitis C virus protein expression causes calcium-mediated mitochondrial bioenergetic dysfunction and nitro-oxidative stress. Hepatology 2007; 46: 58-65.
20. Piccoli C, Quarato G, Ripoli M, D'Aprile A, Scrima R, Cela O, et al. HCV infection induces mitochondrial bioenergetic unbalance: causes and effects. Biochim Biophys Acta 2009; 1787: 539-546.
21. Moradpour D, Kary P, Rice CM, Blum HE. Continuous human cell lines inducibly expressing hepatitis C virus structural and nonstructural proteins. Hepatology 1998; 28: 192-201.
22. Barrientos A. In vivo and in organello assessment of OXPHOS activities. Methods 2002; 26: 307-316.
23. Ripoli M, D'Aprile A, Quarato G, Sarasin-Filipowicz M, Gouttenoire J, Scrima R, et al. Hepatitis C virus-linked mitochondrial dysfunction promotes hypoxia-inducible factor 1 alpha-mediated glycolytic adaptation. J Virol 2010; 84: 647-660.
24. Di Lisa F, Menabò R, Canton M, Barile M, Bernardi P. Opening of the mitochondrial permeability transition pore causes depletion of mitochondrial and cytosolic NAD+ and is a causative event in the death of myocytes in postischemic reperfusion of the heart. J Biol Chem 2001 26; 276: 2571-2575.
25. Giorgio V, Bisetto E, Soriano ME, Dabbeni-Sala F, Basso E, Petronilli V, et al. Cyclophilin D modulates mitochondrial F0F1-ATP synthase by interacting with the lateral stalk of the complex. J Biol Chem 2009; 284: 33982-33988.
26. Brookes PS, Yoon Y, Robotham JL, Anders MW, Sheu SS. Calcium, ATP, and ROS: a mitochondrial love-hate triangle. Am J Physiol Cell Physiol 2004; 287: C817-C833.
27. Wang W, Fang H, Groom L, et al. Superoxide flashes in single mitochondria. Cell 2008; 134: 279-290.
28. Petronilli V, Penzo D, Scorrano L, Bernardi P, Di Lisa F. The mitochondrial permeability transition, release of cytochrome c and cell death. Correlation with the duration of pore openings in situ. J Biol Chem 2001; 276: 12030-12034.
29. 2+ uniporter activity. FASEB J 2007; 21: 2474-2485.
30. Dionisio N, Garcia-Mediavilla MV, Sanchez-Campos S, Majano PL, Benedicto I, Rosado JA, et al. Hepatitis C virus NS5A and core proteins induce oxidative stress mediated calcium signalling alterations in hepatocytes. J Hepatol 2009; 50: 872-882.
31. Waris G, Tardif KD, Siddiqui A. Endoplasmic reticulum (ER) stress: hepatitis C virus induces an ER-nucleus signal transduction pathway and activates NF-kappaB and STAT-3. Biochem Pharmacol 2002; 64: 1425-1430.
32. Williamson CD, Colberg-Poley AM. Access of viral proteins to mitochondria via mitochondria-associated membranes. Rev Med Virol 2009; 19: 147-164.
33. Huser J, Blatter LA. Fluctuation in mitochondrial membrane potential caused by repetitive gating of the permeability transition pore. Biochem J 1999; 343: 311-317.
34. Rimessi A, Giorgi C, Pinton P, Rizzuto R. The versatility of mitochondrial calcium signals: from stimulation of cell metabolism to induction of cell death. Biochim Biophys Acta 2008; 1777: 808-816.
35. Fischer R, Baumert T, Blum HE. Hepatitis C virus infection and apoptosis. World J Gastroenterol 2007; 13: 4865-4872.
36. Galluzzi L, Brenner C, Morselli E, Touat Z, Kroemer G. Viral control of mitochondrial apoptosis. PLoS Pathog 2008; 4: e1000018.
37. Masuoka HC, Guicciardi ME, Gores GJ. Caspase inhibitors for the treatment of hepatitis C. Clin Liver Dis 2009; 13: 467-475.
38. Nelson DR, Ghalib RH, Sulkowski M, Schiff E, Rustgi V, Pockros PJ, et al. Efficacy and safety of the cyclophilin inhibitor Debio 025 in combination with pegylated interferon alpha-2a and ribavirin in previously null-responder genotype 1 HCV patients. J Hepatol 2009; 50( Suppl. 1): S40.
39. Ghibelli L, Coppola S, Fanelli C, Rotilio G, Civitareale P, Scovassi AI, et al. Glutathione depletion causes cytochrome c release even in the absence of cell commitment to apoptosis. FASEB J 1999; 13: 2031-2036.
40. Castro L, Eiserich JP, Sweeney S, Radi R, Freeman BA. Cytochrome c: a catalyst and target of nitrite-hydrogen peroxide-dependent protein nitration. Arch Biochem Biophys 2004; 421: 99-107.
41. Diamond DL, Syder AJ, Jacobs JM, Sorensen CM, Walters KA, Proll SC, et al. Temporal proteome and lipidome profiles reveal hepatitis C virus-associated reprogramming of hepatocellular metabolism and bioenergetics. PLoS Pathog 2010; 6: e1000719.
42. Nasimuzzaman M, Waris G, Mikolon D, Stupack DG, Siddiqui A. Hepatitis C virus stabilizes hypoxia-inducible factor 1alpha and stimulates the synthesis of vascular endothelial growth factor. J Virol 2007; 81: 10249-10257.
43. Lerat H, Kammoun HL, Hainault I, Mérour E, Higgs MR, Callens C, et al. Hepatitis C virus proteins induce lipogenesis and defective triglyceride secretion in transgenic mice. J Biol Chem 2009; 284: 33466-33474.
44. Fukasawa M. Cellular lipid droplets and hepatitis C virus life cycle. Biol Pharm Bull 2010; 33: 355-359.