Different mechanisms of hepatitis C virus RNA polymerase activation by cyclophilin A and B in vitro

Biochimica et Biophysica Acta - General Subjects

Volumn 1820, Issue 12, 2012, Pages 1886-1892

  Weng, Leiyun ^a   Tian, Xiao ^a   Gao, Yayi ^a   Watashi, Koichi ^b   Shimotohno, Kunitada ^c   Wakita, Takaji ^b   Kohara, Michinori ^d   Toyoda, Tetsuya ^a,d,e  

^a INSTITUTE PASTEUR OF SHANGHAI   (China)

^b NATIONAL INSTITUTE OF INFECTIOUS DISEASES   (Japan)

^c CHIBA INSTITUTE OF TECHNOLOGY   (Japan)

^d TOKYO METROPOLITAN INSTITUTE OF MEDICAL SCIENCE   (Japan)

^e NAGOYA CITY UNIVERSITY   (Japan)

Author keywords

Cyclophilin A; Cyclophilin B; HCV; RNA polymerase

Indexed keywords

CYCLOPHILIN A; CYCLOPHILIN B; RNA POLYMERASE;

ALLOSTERISM; ARTICLE; COLUMN CHROMATOGRAPHY; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME KINETICS; ENZYME MECHANISM; ENZYME PURIFICATION; ENZYME SPECIFICITY; GENE SILENCING; GENOTYPE; HEPATITIS C VIRUS; HUMAN; HUMAN CELL; IN VITRO STUDY; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REPLICON; VIRUS REPLICATION; VIRUS TRANSCRIPTION;

CYCLOPHILIN A; CYCLOPHILINS; CYCLOSPORINE; GENE EXPRESSION REGULATION, ENZYMOLOGIC; GENOTYPE; HEPACIVIRUS; HEPATITIS C; HUMANS; IMMUNOSUPPRESSIVE AGENTS; MUTANT PROTEINS; PLASMIDS; RNA REPLICASE; RNA, VIRAL; TRANSCRIPTION, GENETIC; VIRUS REPLICATION;

HEPATITIS C VIRUS;

EID: 84866707643     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2012.08.017     Document Type: Article

References (67)

1. S. Lemon, C. Walker, M. Alter, and M. Yi Hepatitis C virus D. Knipe, P. Howley, Fields Virology 2007 Lippincott-Raven Publishers Philadelphia, PA 1253 1304
2. A. Grakoui, D.W. McCourt, C. Wychowski, S.M. Feinstone, and C.M. Rice A second hepatitis C virus-encoded proteinase Proc. Natl. Acad. Sci. U. S. A. 90 1993 10583 10587
3. T.L. Tellinghuisen, and C.M. Rice Interaction between hepatitis C virus proteins and host cell factors Curr. Opin. Microbiol. 5 2002 419 427
4. T. Kashiwagi, K. Hara, M. Kohara, K. Kohara, J. Iwahashi, N. Hamada, H. Yoshino, and T. Toyoda Kinetic analysis of C-terminally truncated RNA-dependent RNA polymerase of hepatitis C virus Biochem. Biophys. Res. Commun. 290 2002 1188 1194
5. S.E. Behrens, L. Tomei, and R. De Francesco Identification and properties of the RNA-dependent RNA polymerase of hepatitis C virus EMBO J. 15 1996 12 22
6. I. Saito, T. Miyamura, A. Ohbayashi, H. Harada, T. Katayama, S. Kikuchi, Y. Watanabe, S. Koi, M. Onji, and Y. Ohta Hepatitis C virus infection is associated with the development of hepatocellular carcinoma Proc. Natl. Acad. Sci. U. S. A. 87 1990 6547 6549
7. R. Bartenschlager, M. Frese, and T. Pietschmann Novel insights into hepatitis C virus replication and persistence Adv. Virus Res. 63 2004 71 180
8. T. Poynard, M.F. Yuen, V. Ratziu, and C.L. Lai Viral hepatitis C Lancet 362 2003 2095 2100
9. M.P. Manns, J.G. McHutchison, S.C. Gordon, V.K. Rustgi, M. Shiffman, R. Reindollar, Z.D. Goodman, K. Koury, M. Ling, and J.K. Albrecht Peginterferon alfa-2b plus ribavirin compared with interferon alfa-2b plus ribavirin for initial treatment of chronic hepatitis C: a randomised trial Lancet 358 2001 958 965
10. M.W. Fried, M.L. Shiffman, K.R. Reddy, C. Smith, G. Marinos, F.L. Goncales Jr., D. Haussinger, M. Diago, G. Carosi, D. Dhumeaux, A. Craxi, A. Lin, J. Hoffman, and J. Yu Peginterferon alfa-2a plus ribavirin for chronic hepatitis C virus infection N. Engl. J. Med. 347 2002 975 982
11. I.M. Jacobson, J.G. McHutchison, G. Dusheiko, A.M. Di Bisceglie, K.R. Reddy, N.H. Bzowej, P. Marcellin, A.J. Muir, P. Ferenci, R. Flisiak, J. George, M. Rizzetto, D. Shouval, R. Sola, R.A. Terg, E.M. Yoshida, N. Adda, L. Bengtsson, A.J. Sankoh, T.L. Kieffer, S. George, R.S. Kauffman, and S. Zeuzem Telaprevir for previously untreated chronic hepatitis C virus infection N. Engl. J. Med. 364 2011 2405 2416
12. F. Poordad, J. McCone Jr., B.R. Bacon, S. Bruno, M.P. Manns, M.S. Sulkowski, I.M. Jacobson, K.R. Reddy, Z.D. Goodman, N. Boparai, M.J. DiNubile, V. Sniukiene, C.A. Brass, J.K. Albrecht, and J.P. Bronowicki Boceprevir for untreated chronic HCV genotype 1 infection N. Engl. J. Med. 364 2011 1195 1206
13. M.L. Vachon, and D.T. Dieterich The era of direct-acting antivirals has begun: the beginning of the end for HCV? Semin. Liver Dis. 31 2011 399 409
14. J. Paeshuyse, A. Kaul, E. De Clercq, B. Rosenwirth, J.M. Dumont, P. Scalfaro, R. Bartenschlager, and J. Neyts The non-immunosuppressive cyclosporin DEBIO-025 is a potent inhibitor of hepatitis C virus replication in vitro Hepatology (Baltimore, Md) 43 2006 761 770
15. S. Ma, J.E. Boerner, C. TiongYip, B. Weidmann, N.S. Ryder, M.P. Cooreman, and K. Lin NIM811, a cyclophilin inhibitor, exhibits potent in vitro activity against hepatitis C virus alone or in combination with alpha interferon Antimicrob. Agents Chemother. 50 2006 2976 2982
16. S. Hopkins, B. Scorneaux, Z. Huang, M.G. Murray, S. Wring, C. Smitley, R. Harris, F. Erdmann, G. Fischer, and Y. Ribeill SCY-635, a novel nonimmunosuppressive analog of cyclosporine that exhibits potent inhibition of hepatitis C virus RNA replication in vitro Antimicrob. Agents Chemother. 54 2010 660 672
17. D.N. Fusco, and R.T. Chung Novel therapies for hepatitis C: insights from the structure of the virus Annu. Rev. Med. 63 2011 373 387
18. L. Coelmont, X. Hanoulle, U. Chatterji, C. Berger, J. Snoeck, M. Bobardt, P. Lim, I. Vliegen, J. Paeshuyse, G. Vuagniaux, A.M. Vandamme, R. Bartenschlager, P. Gallay, G. Lippens, and J. Neyts DEB025 (Alisporivir) inhibits hepatitis C virus replication by preventing a cyclophilin A induced cis-trans isomerisation in domain II of NS5A PLoS One 5 2010 e13687
19. R.E. Handschumacher, M.W. Harding, J. Rice, R.J. Drugge, and D.W. Speicher Cyclophilin: a specific cytosolic binding protein for cyclosporin A Science (New York, N.Y.) 226 1984 544 547
20. G. Fischer, T. Tradler, and T. Zarnt The mode of action of peptidyl prolyl cis/trans isomerases in vivo: binding vs. catalysis FEBS Lett. 426 1998 17 20
21. G.J. Towers, T. Hatziioannou, S. Cowan, S.P. Goff, J. Luban, and P.D. Bieniasz Cyclophilin A modulates the sensitivity of HIV-1 to host restriction factors Nat. Med. 9 2003 1138 1143
22. E.K. Franke, H.E. Yuan, and J. Luban Specific incorporation of cyclophilin A into HIV-1 virions Nature 372 1994 359 362
23. K. Inoue, K. Sekiyama, M. Yamada, T. Watanabe, H. Yasuda, and M. Yoshiba Combined interferon alpha2b and cyclosporin A in the treatment of chronic hepatitis C: controlled trial J. Gastroenterol. 38 2003 567 572
24. M. Nakagawa, N. Sakamoto, N. Enomoto, Y. Tanabe, N. Kanazawa, T. Koyama, M. Kurosaki, S. Maekawa, T. Yamashiro, C.H. Chen, Y. Itsui, S. Kakinuma, and M. Watanabe Specific inhibition of hepatitis C virus replication by cyclosporin A Biochem. Biophys. Res. Commun. 313 2004 42 47
25. H. Akiyama, H. Yoshinaga, T. Tanaka, K. Hiruma, S. Tanikawa, H. Sakamaki, Y. Onozawa, T. Wakita, and M. Kohara Effects of cyclosporin A on hepatitis C virus infection in bone marrow transplant patients. Bone Marrow Transplantation Team Bone Marrow Transplant. 20 1997 993 995
26. K. Watashi, M. Hijikata, M. Hosaka, M. Yamaji, and K. Shimotohno Cyclosporin A suppresses replication of hepatitis C virus genome in cultured hepatocytes Hepatology (Baltimore, Md) 38 2003 1282 1288
27. F. Fernandes, D.S. Poole, S. Hoover, R. Middleton, A.C. Andrei, J. Gerstner, and R. Striker Sensitivity of hepatitis C virus to cyclosporine A depends on nonstructural proteins NS5A and NS5B Hepatology (Baltimore, Md) 46 2007 1026 1033
28. J.M. Robida, H.B. Nelson, Z. Liu, and H. Tang Characterization of hepatitis C virus subgenomic replicon resistance to cyclosporine in vitro J. Virol. 81 2007 5829 5840
29. K. Watashi, N. Ishii, M. Hijikata, D. Inoue, T. Murata, Y. Miyanari, and K. Shimotohno Cyclophilin B is a functional regulator of hepatitis C virus RNA polymerase Mol. Cell 19 2005 111 122
30. F. Yang, J.M. Robotham, H.B. Nelson, A. Irsigler, R. Kenworthy, and H. Tang Cyclophilin A is an essential cofactor for hepatitis C virus infection and the principal mediator of cyclosporine resistance in vitro J. Virol. 82 2008 5269 5278
31. K. Goto, K. Watashi, D. Inoue, M. Hijikata, and K. Shimotohno Identification of cellular and viral factors related to anti-hepatitis C virus activity of cyclophilin inhibitor Cancer Sci. 100 2009 1943 1950
32. U. Chatterji, M. Bobardt, S. Selvarajah, F. Yang, H. Tang, N. Sakamoto, G. Vuagniaux, T. Parkinson, and P. Gallay The isomerase active site of cyclophilin a is critical for hepatitis C virus replication J. Biol. Chem. 284 2009 16998 17005
33. F. Fernandes, I.U. Ansari, and R. Striker cyclosporine inhibits a direct interaction between cyclophilins and hepatitis C NS5A PLoS One 5 2010 e9815
34. A. Kaul, S. Stauffer, C. Berger, T. Pertel, J. Schmitt, S. Kallis, M.Z. Lopez, V. Lohmann, J. Luban, and R. Bartenschlager Essential role of cyclophilin A for hepatitis C virus replication and virus production and possible link to polyprotein cleavage kinetics PLoS Pathog. 5 2009 e1000546
35. D. Verdegem, A. Badillo, J.M. Wieruszeski, I. Landrieu, A. Leroy, R. Bartenschlager, F. Penin, G. Lippens, and X. Hanoulle Domain 3 of NS5A protein from the hepatitis C virus has intrinsic {alpha}-helical propensity and is a substrate of cyclophilin A J. Biol. Chem. 286 2011 20441 20454
36. F. Yang, J.M. Robotham, H. Grise, S. Frausto, V. Madan, M. Zayas, R. Bartenschlager, M. Robinson, A.E. Greenstein, A. Nag, T.M. Logan, E. Bienkiewicz, and H. Tang A major determinant of cyclophilin dependence and cyclosporine susceptibility of hepatitis C virus identified by a genetic approach PLoS Pathog. 6 2010
37. L. Weng, J. Du, J. Zhou, J. Ding, T. Wakita, M. Kohara, and T. Toyoda Modification of hepatitis C virus 1b RNA polymerase to make a highly active JFH1-type polymerase by mutation of the thumb domain Arch. Virol. 154 2009 765 773
38. L. Weng, Y. Hirata, M. Arai, M. Kohara, T. Wakita, K. Watashi, K. Shimotohno, Y. He, J. Zhong, and T. Toyoda Sphingomyelin activates hepatitis C virus RNA polymerase in a genotype-specific manner J. Virol. 84 2010 11761 11770
39. A. Murayama, L. Weng, T. Date, D. Akazawa, X. Tian, T. Suzuki, T. Kato, Y. Tanaka, M. Mizokami, T. Wakita, and T. Toyoda RNA polymerase activity and specific RNA structure are required for efficient HCV replication in cultured cells PLoS Pathog. 6 2010 e1000885
40. L. Weng, M. Kohara, T. Wakita, K. Shimotohno, and T. Toyoda Detergent-induced activation of the hepatitis C virus genotype 1b RNA polymerase Gene 496 2012 79 87
41. N. Ishii, K. Watashi, T. Hishiki, K. Goto, D. Inoue, M. Hijikata, T. Wakita, N. Kato, and K. Shimotohno Diverse effects of cyclosporine on hepatitis C virus strain replication J. Virol. 80 2006 4510 4520
42. H. Grise, S. Frausto, T. Logan, and H. Tang A conserved tandem cyclophilin-binding site in hepatitis C virus nonstructural protein 5A regulates alisporivir susceptibility J. Virol. 86 2012 4811 4822
43. U. Chatterji, P. Lim, M.D. Bobardt, S. Wieland, D.G. Cordek, G. Vuagniaux, F. Chisari, C.E. Cameron, P. Targett-Adams, T. Parkinson, and P.A. Gallay HCV resistance to cyclosporin A does not correlate with a resistance of the NS5A-cyclophilin A interaction to cyclophilin inhibitors J. Hepatol. 53 2010 50 56
44. T.L. Foster, P. Gallay, N.J. Stonehouse, and M. Harris Cyclophilin A interacts with domain II of hepatitis C virus NS5A and stimulates RNA binding in an isomerase-dependent manner J. Virol. 85 2011 7460 7464
45. Z. Liu, J.M. Robida, S. Chinnaswamy, G. Yi, J.M. Robotham, H.B. Nelson, A. Irsigler, C.C. Kao, and H. Tang Mutations in the hepatitis C virus polymerase that increase RNA binding can confer resistance to cyclosporine A Hepatology (Baltimore, Md) 50 2009 25 33
46. R. Flisiak, A. Horban, P. Gallay, M. Bobardt, S. Selvarajah, A. Wiercinska-Drapalo, E. Siwak, I. Cielniak, J. Higersberger, J. Kierkus, C. Aeschlimann, P. Grosgurin, V. Nicolas-Metral, J.M. Dumont, H. Porchet, R. Crabbe, and P. Scalfaro The cyclophilin inhibitor Debio-025 shows potent anti-hepatitis C effect in patients coinfected with hepatitis C and human immunodeficiency virus Hepatology (Baltimore, Md) 47 2008 817 826
47. M. Nakagawa, N. Sakamoto, Y. Tanabe, T. Koyama, Y. Itsui, Y. Takeda, C.H. Chen, S. Kakinuma, S. Oooka, S. Maekawa, N. Enomoto, and M. Watanabe Suppression of hepatitis C virus replication by cyclosporin a is mediated by blockade of cyclophilins Gastroenterology 129 2005 1031 1041
48. L. Jin, and S.C. Harrison Crystal structure of human calcineurin complexed with cyclosporin A and human cyclophilin Proc. Natl. Acad. Sci. U. S. A. 99 2002 13522 13526
49. V. Mikol, J. Kallen, G. Pflugl, and M.D. Walkinshaw X-ray structure of a monomeric cyclophilin A-cyclosporin A crystal complex at 2.1 A resolution J. Mol. Biol. 234 1993 1119 1130
50. G. Pflugl, J. Kallen, T. Schirmer, J.N. Jansonius, M.G. Zurini, and M.D. Walkinshaw X-ray structure of a decameric cyclophilin-cyclosporin crystal complex Nature 361 1993 91 94
51. X. Puyang, D.L. Poulin, J.E. Mathy, L.J. Anderson, S. Ma, Z. Fang, S. Zhu, K. Lin, R. Fujimoto, T. Compton, and B. Wiedmann Mechanism of resistance of hepatitis C virus replicons to structurally distinct cyclophilin inhibitors Antimicrob. Agents Chemother. 54 2010 1981 1987
52. U. Chatterji, M.D. Bobardt, P. Lim, and P.A. Gallay Cyclophilin A-independent recruitment of NS5A and NS5B into hepatitis C virus replication complexes J. Gen. Virol. 91 2010 1189 1193
53. Z. Liu, F. Yang, J.M. Robotham, and H. Tang 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. 83 2009 6554 6565
54. J.A. Heck, X. Meng, and D.N. Frick Cyclophilin B stimulates RNA synthesis by the HCV RNA dependent RNA polymerase Biochem. Pharmacol. 77 2009 1173 1180
55. R. Crabbe, G. Vuagniaux, J.M. Dumont, V. Nicolas-Metral, J. Marfurt, and L. Novaroli An evaluation of the cyclophilin inhibitor Debio 025 and its potential as a treatment for chronic hepatitis C Expert Opin. Investig. Drugs 18 2009 211 220
56. A. Romani Regulation of magnesium homeostasis and transport in mammalian cells Arch. Biochem. Biophys. 458 2007 90 102
57. M. Morello, A. Canini, P. Mattioli, R.P. Sorge, A. Alimonti, B. Bocca, G. Forte, A. Martorana, G. Bernardi, and G. Sancesario Sub-cellular localization of manganese in the basal ganglia of normal and manganese-treated rats. An electron spectroscopy imaging and electron energy-loss spectroscopy study Neurotoxicology 29 2008 60 72
58. K. Kalia, W. Jiang, and W. Zheng Manganese accumulates primarily in nuclei of cultured brain cells Neurotoxicology 29 2008 466 470
59. H. Gatanaga, D. Das, Y. Suzuki, D.D. Yeh, K.A. Hussain, A.K. Ghosh, and H. Mitsuya Altered HIV-1 Gag protein interactions with cyclophilin A (CypA) on the acquisition of H219Q and H219P substitutions in the CypA binding loop J. Biol. Chem. 281 2006 1241 1250
60. E.R. Price, M. Jin, D. Lim, S. Pati, C.T. Walsh, and F.D. McKeon Cyclophilin B trafficking through the secretory pathway is altered by binding of cyclosporin A Proc. Natl. Acad. Sci. U. S. A. 91 1994 3931 3935
61. E.R. Price, L.D. Zydowsky, M.J. Jin, C.H. Baker, F.D. McKeon, and C.T. Walsh Human cyclophilin B: a second cyclophilin gene encodes a peptidyl-prolyl isomerase with a signal sequence Proc. Natl. Acad. Sci. U. S. A. 88 1991 1903 1907
62. Y. Liu, W.W. Jiang, J. Pratt, T. Rockway, K. Harris, S. Vasavanonda, R. Tripathi, R. Pithawalla, and W.M. Kati Mechanistic study of HCV polymerase inhibitors at individual steps of the polymerization reaction Biochemistry 45 2006 11312 11323
63. S.S. Carroll, V. Sardana, Z. Yang, A.R. Jacobs, C. Mizenko, D. Hall, L. Hill, J. Zugay-Murphy, and L.C. Kuo Only a small fraction of purified hepatitis C RNA-dependent RNA polymerase is catalytically competent: implications for viral replication and in vitro assays Biochemistry 39 2000 8243 8249
64. D.L. Thomas, C.L. Thio, M.P. Martin, Y. Qi, D. Ge, C. O'Huigin, J. Kidd, K. Kidd, S.I. Khakoo, G. Alexander, J.J. Goedert, G.D. Kirk, S.M. Donfield, H.R. Rosen, L.H. Tobler, M.P. Busch, J.G. McHutchison, D.B. Goldstein, and M. Carrington Genetic variation in IL28B and spontaneous clearance of hepatitis C virus Nature 461 2009 798 801
65. D. Ge, J. Fellay, A.J. Thompson, J.S. Simon, K.V. Shianna, T.J. Urban, E.L. Heinzen, P. Qiu, A.H. Bertelsen, A.J. Muir, M. Sulkowski, J.G. McHutchison, and D.B. Goldstein Genetic variation in IL28B predicts hepatitis C treatment-induced viral clearance Nature 461 2009 399 401
66. Y. Tanaka, N. Nishida, M. Sugiyama, M. Kurosaki, K. Matsuura, N. Sakamoto, M. Nakagawa, M. Korenaga, K. Hino, S. Hige, Y. Ito, E. Mita, E. Tanaka, S. Mochida, Y. Murawaki, M. Honda, A. Sakai, Y. Hiasa, S. Nishiguchi, A. Koike, I. Sakaida, M. Imamura, K. Ito, K. Yano, N. Masaki, F. Sugauchi, N. Izumi, K. Tokunaga, and M. Mizokami Genome-wide association of IL28B with response to pegylated interferon-alpha and ribavirin therapy for chronic hepatitis C Nat. Genet. 41 2009 1105 1109
67. M. Gao, R.E. Nettles, M. Belema, L.B. Snyder, V.N. Nguyen, R.A. Fridell, M.H. Serrano-Wu, D.R. Langley, J.H. Sun, D.R. O'Boyle II, J.A. Lemm, C. Wang, J.O. Knipe, C. Chien, R.J. Colonno, D.M. Grasela, N.A. Meanwell, and L.G. Hamann Chemical genetics strategy identifies an HCV NS5A inhibitor with a potent clinical effect Nature 465 2010 96 100