Cyclophilins as modulators of viral replication

Viruses

Volumn 5, Issue 7, 2013, Pages 1684-1701

  Frausto, Stephen D ^a   Lee, Emily ^a   Tang, Hengli ^a  

^a FLORIDA STATE UNIVERSITY   (United States)

Author keywords

Cyclophilin; Cyclosporin; HCV; HIV

Indexed keywords

ALISPORIVIR; ALPHA INTERFERON; BINDING PROTEIN; CYCLOPHILIN; CYCLOPHILIN A; CYCLOPHILIN B; CYCLOPHILIN INHIBITOR; CYCLOSPORIN A; GAG PROTEIN; NONSTRUCTURAL PROTEIN 5A; PEPTIDYLPROLYL ISOMERASE; RAN BINDING PROTEIN 2; TACROLIMUS; TRIPARTITE MOTIF PROTEIN 5; UNCLASSIFIED DRUG; VIRUS PROTEIN;

ARTERIVIRUS; BK VIRUS; CLINICAL TRIAL (TOPIC); CORONAVIRUS; DISEASE PREDISPOSITION; DISEASE SEVERITY; DRUG TARGETING; GENETIC ASSOCIATION; HEPATITIS B VIRUS; HEPATITIS C; HEPATITIS C VIRUS; HUMAN; HUMAN CYTOMEGALOVIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; HUMAN IMMUNODEFICIENCY VIRUS 1 INFECTION; INFLUENZA VIRUS; MEASLES VIRUS; NONHUMAN; NUCLEOTIDE SEQUENCE; PATHOGENESIS; PROTEIN EXPRESSION; PROTEIN FOLDING; PROTEIN FUNCTION; REVIEW; ROTAVIRUS; SINGLE NUCLEOTIDE POLYMORPHISM; TOMBUSVIRUS; VACCINIA VIRUS; VESICULAR STOMATITIS VIRUS; VIRION; VIRUS CELL INTERACTION; VIRUS REPLICATION; WART VIRUS; WEST NILE FLAVIVIRUS;

ANTIVIRAL AGENTS; CYCLOPHILINS; ENZYME INHIBITORS; HOST-PATHOGEN INTERACTIONS; HUMANS; PROTEIN FOLDING; VIRAL PROTEINS; VIRUS PHYSIOLOGICAL PHENOMENA; VIRUS REPLICATION;

EID: 84880392016     PISSN: 19994915     EISSN: None     Source Type: Journal    
DOI: 10.3390/v5071684     Document Type: Review

References (150)

1. Fischer, G.; Bang, H.; Mech, C. Determination of enzymatic catalysis for the cis-transisomerization of peptide binding in proline-containing peptides. Biomed. Biochim. Acta 1984, 43, 1101-1111
2. Fischer, G.; Bang, H. The refolding of urea-denatured ribonuclease A is catalyzed by peptidyl-prolyl cis-trans isomerase. Biochim. Biophys. Acta 1985, 828, 39-42.
3. Handschumacher, R.E.; Harding, M.W.; Rice, J.; Drugge, R.J.; Speicher, D.W. Cyclophilin: A specific cytosolic binding protein for cyclosporin A. Science 1984, 226, 544-547.
4. Fischer, G.; Wittmann-Liebold, B.; Lang, K.; Kiefhaber, T.; Schmid, F.X. Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature 1989, 337, 476-478.
5. Takahashi, N.; Hayano, T.; Suzuki, M. Peptidyl-prolyl cis-trans isomerase is the cyclosporin A-binding protein cyclophilin. Nature 1989, 337, 473-475.
6. Liu, J.; Farmer, J.D., Jr.; Lane, W.S.; Friedman, J.; Weissman, I.; Schreiber, S.L. Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 1991, 66, 807-815.
7. Thai, V.; Renesto, P.; Fowler, C.A.; Brown, D.J.; Davis, T.; Gu, W.; Pollock, D.D.; Kern, D.; Raoult, D.; Eisenmesser, E.Z. Structural, biochemical, and in vivo characterization of the first virally encoded cyclophilin from the Mimivirus. J. Mol. Biol. 2008, 378, 71-86.
8. Raoult, D.; Audic, S.; Robert, C.; Abergel, C.; Renesto, P.; Ogata, H.; La Scola, B.; Suzan, M.; Claverie, J.M. The 1.2-megabase genome sequence of Mimivirus. Science 2004, 306, 1344-1350.
9. Davis, T.L.; Walker, J.R.; Campagna-Slater, V.; Finerty, P.J.; Paramanathan, R.; Bernstein, G.; MacKenzie, F.; Tempel, W.; Ouyang, H.; Lee, W.H. et al. Structural and biochemical characterization of the human cyclophilin family of peptidyl-prolyl isomerases. PLoS Biol. 2010, 8, e1000439.
10. Siekierka, J.J.; Hung, S.H.; Poe, M.; Lin, C.S.; Sigal, N.H. A cytosolic binding protein for the immunosuppressant FK506 has peptidyl-prolyl isomerase activity but is distinct from cyclophilin. Nature 1989, 341, 755-757.
11. Harding, M.W.; Galat, A.; Uehling, D.E.; Schreiber, S.L. A receptor for the immunosuppressant FK506 is a cis-trans peptidyl-prolyl isomerase. Nature 1989, 341, 758-760.
12. Brown, E.J.; Albers, M.W.; Shin, T.B.; Ichikawa, K.; Keith, C.T.; Lane, W.S.; Schreiber, S.L. A mammalian protein targeted by G1-arresting rapamycin-receptor complex. Nature 1994, 369, 756-758.
13. Sabatini, D.M.; Erdjument-Bromage, H.; Lui, M.; Tempst, P.; Snyder, S.H. RAFT1: A mammalian protein that binds to FKBP12 in a rapamycin-dependent fashion and is homologous to yeast TORs. Cell 1994, 78, 35-43.
14. Rahfeld, J.U.; Rucknagel, K.P.; Schelbert, B.; Ludwig, B.; Hacker, J.; Mann, K.; Fischer, G. Confirmation of the existence of a third family among peptidyl-prolyl cis/trans isomerases. Amino acid sequence and recombinant production of parvulin. FEBS Lett. 1994, 352, 180-184.
15. Sherry, B.; Yarlett, N.; Strupp, A.; Cerami, A. Identification of cyclophilin as a proinflammatory secretory product of lipopolysaccharide-activated macrophages. Proc. Natl. Acad. Sci. USA 1992, 89, 3511-3515.
16. Arora, K.; Gwinn, W.M.; Bower, M.A.; Watson, A.; Okwumabua, I.; MacDonald, H.R.; Bukrinsky, M.I.; Constant, S.L. Extracellular cyclophilins contribute to the regulation of inflammatory responses. J. Immunol. 2005, 175, 517-522.
17. Lee, J.; Kim, S.S. Current implications of cyclophilins in human cancers. J. Exp. Clin. Cancer Res. 2010, 29, 97.
18. Pakula, R.; Melchior, A.; Denys, A.; Vanpouille, C.; Mazurier, J.; Allain, F. Syndecan-1/CD147 association is essential for cyclophilin B-induced activation of p44/42 mitogen-activated protein kinases and promotion of cell adhesion and chemotaxis. Glycobiology 2007, 17, 492-503.
19. Marcant, A.; Denys, A.; Melchior, A.; Martinez, P.; Deligny, A.; Carpentier, M.; Allain, F. Cyclophilin B attenuates the expression of TNF-alpha in lipopolysaccharide-stimulated macrophages through the induction of B cell lymphoma-3. J. Immunol. 2012, 189, 2023-2032.
20. Price, E.R.; Zydowsky, L.D.; Jin, M.J.; Baker, C.H.; McKeon, F.D.; Walsh, C.T. Human cyclophilin B: A second cyclophilin gene encodes a peptidyl-prolyl isomerase with a signal sequence. Proc. Natl. Acad. Sci. USA 1991, 88, 1903-1907.
21. Hasel, K.W.; Glass, J.R.; Godbout, M.; Sutcliffe, J.G. An endoplasmic reticulum-specific cyclophilin. Mol. Cell. Biol. 1991, 11, 3484-3491.
22. Allain, F.; Vanpouille, C.; Carpentier, M.; Slomianny, M.C.; Durieux, S.; Spik, G. Interaction with glycosaminoglycans is required for cyclophilin B to trigger integrin-mediated adhesion of peripheral blood T lymphocytes to extracellular matrix. Proc. Natl. Acad. Sci. USA 2002, 99, 2714-2719.
23. Friedman, J.; Weissman, I. Two cytoplasmic candidates for immunophilin action are revealed by affinity for a new cyclophilin: One in the presence and one in the absence of CsA. Cell 1991, 66, 799-806.
24. Obermayr, E.; Castillo-Tong, D.C.; Pils, D.; Speiser, P.; Braicu, I.; Van Gorp, T.; Mahner, S.; Sehouli, J.; Vergote, I.; Zeillinger, R. Molecular characterization of circulating tumor cells in patients with ovarian cancer improves their prognostic significance-A study of the OVCAD consortium. Gynecol. Oncol. 2013, 128, 15-21.
25. Baines, C.P.; Kaiser, R.A.; Purcell, N.H.; Blair, N.S.; Osinska, H.; Hambleton, M.A.; Brunskill, E.W.; Sayen, M.R.; Gottlieb, R.A.; Dorn, G.W. et al. Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 2005, 434, 658-662.
26. Schinzel, A.C.; Takeuchi, O.; Huang, Z.; Fisher, J.K.; Zhou, Z.; Rubens, J.; Hetz, C.; Danial, N.N.; Moskowitz, M.A.; Korsmeyer, S.J. Cyclophilin D is a component of mitochondrial permeability transition and mediates neuronal cell death after focal cerebral ischemia. Proc. Natl. Acad. Sci. USA 2005, 102, 12005-12010.
27. Jurica, M.S.; Licklider, L.J.; Gygi, S.R.; Grigorieff, N.; Moore, M.J. Purification and characterization of native spliceosomes suitable for three-dimensional structural analysis. RNA 2002, 8, 426-439.
28. Kim, J.O.; Nau, M.M.; Allikian, K.A.; Makela, T.P.; Alitalo, K.; Johnson, B.E.; Kelley, M.J. Co-amplification of a novel cyclophilin-like gene (PPIE) with L-myc in small cell lung cancer cell lines. Oncogene 1998, 17, 1019-1026.
29. Mi, H.; Kops, O.; Zimmermann, E.; Jaschke, A.; Tropschug, M. A nuclear RNA-binding cyclophilin in human T cells. FEBS Lett. 1996, 398, 201-205.
30. Wang, Y.; Han, R.; Zhang, W.; Yuan, Y.; Zhang, X.; Long, Y.; Mi, H. Human CyP33 binds specifically to mRNA and binding stimulates PPIase activity of hCyP33. FEBS Lett. 2008, 582, 835-839.
31. Dartigalongue, C.; Raina, S. A new heat-shock gene, ppiD, encodes a peptidyl-prolyl isomerase required for folding of outer membrane proteins in Escherichia coli. EMBO J. 1998, 17, 3968-3980.
32. Pirkl, F.; Buchner, J. Functional analysis of the Hsp90-associated human peptidyl prolyl cis/trans isomerases FKBP51, FKBP52 and Cyp40. J. Mol. Biol. 2001, 308, 795-806.
33. Rinfret, A.; Collins, C.; Menard, R.; Anderson, S.K. The N-terminal cyclophilin-homologous domain of a 150-kilodalton tumor recognition molecule exhibits both peptidylprolyl cis-transisomerase and chaperone activities. Biochemistry 1994, 33, 1668-1673.
34. Anderson, S.K.; Gallinger, S.; Roder, J.; Frey, J.; Young, H.A.; Ortaldo, J.R. A cyclophilinrelated protein involved in the function of natural killer cells. Proc. Natl. Acad. Sci. USA 1993, 90, 542-546.
35. Nestel, F.P.; Colwill, K.; Harper, S.; Pawson, T.; Anderson, S.K. RS cyclophilins: Identification of an NK-TR1-related cyclophilin. Gene 1996, 180, 151-155.
36. Bourquin, J.P.; Stagljar, I.; Meier, P.; Moosmann, P.; Silke, J.; Baechi, T.; Georgiev, O.; Schaffner, W. A serine/arginine-rich nuclear matrix cyclophilin interacts with the C-terminal domain of RNA polymerase II. Nucleic Acids Res. 1997, 25, 2055-2061.
37. Horowitz, D.S.; Kobayashi, R.; Krainer, A.R. A new cyclophilin and the human homologues of yeast Prp3 and Prp4 form a complex associated with U4/U6 snRNPs. RNA 1997, 3, 1374-1387.
38. Teigelkamp, S.; Achsel, T.; Mundt, C.; Gothel, S.F.; Cronshagen, U.; Lane, W.S.; Marahiel, M.; Luhrmann, R. The 20kD protein of human [U4/U6.U5] tri-snRNPs is a novel cyclophilin that forms a complex with the U4/U6-specific 60kD and 90kD proteins. RNA 1998, 4, 127-141.
39. Horowitz, D.S.; Lee, E.J.; Mabon, S.A.; Misteli, T. A cyclophilin functions in pre-mRNA splicing. EMBO J. 2002, 21, 470-480.
40. Ozaki, K.; Fujiwara, T.; Kawai, A.; Shimizu, F.; Takami, S.; Okuno, S.; Takeda, S.; Shimada, Y.; Nagata, M.; Watanabe, T. et al. Cloning, expression and chromosomal mapping of a novel cyclophilin-related gene (PPIL1) from human fetal brain. Cytogenet. Cell Genet. 1996, 72, 242-245.
41. Jurica, M.S.; Moore, M.J. Pre-mRNA splicing: Awash in a sea of proteins. Mol. Cell 2003, 12, 5-14.
42. Xu, C.; Zhang, J.; Huang, X.; Sun, J.; Xu, Y.; Tang, Y.; Wu, J.; Shi, Y.; Huang, Q.; Zhang, Q. Solution structure of human peptidyl prolyl isomerase-like protein 1 and insights into its interaction with SKIP. J. Biol. Chem. 2006, 281, 15900-15908.
43. Pushkarsky, T.; Yurchenko, V.; Vanpouille, C.; Brichacek, B.; Vaisman, I.; Hatakeyama, S.; Nakayama, K.I.; Sherry, B.; Bukrinsky, M.I. Cell surface expression of CD147/EMMPRIN is regulated by cyclophilin 60. J. Biol. Chem. 2005, 280, 27866-27871.
44. Wang, B.B.; Hayenga, K.J.; Payan, D.G.; Fisher, J.M. Identification of a nuclear-specific cyclophilin which interacts with the proteinase inhibitor eglin c. Biochem. J. 1996, 314, 313-319.
45. Zhou, Z.; Ying, K.; Dai, J.; Tang, R.; Wang, W.; Huang, Y.; Zhao, W.; Xie, Y.; Mao, Y. Molecular cloning and characterization of a novel peptidylprolyl isomerase (cyclophilin)-like gene (PPIL3) from human fetal brain. Cytogenet. Cell Genet. 2001, 92, 231-236.
46. Mesa, A.; Somarelli, J.A.; Herrera, R.J. Spliceosomal immunophilins. FEBS Lett. 2008, 582, 2345-2351.
47. Zeng, L.; Zhou, Z.; Xu, J.; Zhao, W.; Wang, W.; Huang, Y.; Cheng, C.; Xu, M.; Xie, Y.; Mao, Y. Molecular cloning, structure and expression of a novel nuclear RNA-binding cyclophilin-like gene (PPIL4) from human fetal brain. Cytogenet. Cell Genet. 2001, 95, 43-47.
48. Beddow, A.L.; Richards, S.A.; Orem, N.R.; Macara, I.G. The Ran/TC4 GTPase-binding domain: Identification by expression cloning and characterization of a conserved sequence motif. Proc. Natl. Acad. Sci. USA 1995, 92, 3328-3332.
49. Wu, J.; Matunis, M.J.; Kraemer, D.; Blobel, G.; Coutavas, E. Nup358, a cytoplasmically exposed nucleoporin with peptide repeats, Ran-GTP binding sites, zinc fingers, a cyclophilin A homologous domain, and a leucine-rich region. J. Biol. Chem. 1995, 270, 14209-14213.
50. Davis, T.L.; Walker, J.R.; Ouyang, H.; MacKenzie, F.; Butler-Cole, C.; Newman, E.M.; Eisenmesser, E.Z.; Dhe-Paganon, S. The crystal structure of human WD40 repeat-containing peptidylprolyl isomerase (PPWD1). FEBS J. 2008, 275, 2283-2295.
51. Sutherland, H.G.; Mumford, G.K.; Newton, K.; Ford, L.V.; Farrall, R.; Dellaire, G.; Caceres, J.F.; Bickmore, W.A. Large-scale identification of mammalian proteins localized to nuclear sub-compartments. Hum. Mol. Genet. 2001, 10, 1995-2011.
52. Luban, J.; Bossolt, K.L.; Franke, E.K.; Kalpana, G.V.; Goff, S.P. Human immunodeficiency virus type 1 Gag protein binds to cyclophilins A and B. Cell 1993, 73, 1067-1078.
53. Franke, E.K.; Yuan, H.E.; Luban, J. Specific incorporation of cyclophilin A into HIV-1 virions. Nature 1994, 372, 359-362.
54. Thali, M.; Bukovsky, A.; Kondo, E.; Rosenwirth, B.; Walsh, C.T.; Sodroski, J.; Gottlinger, H.G. Functional association of cyclophilin A with HIV-1 virions. Nature 1994, 372, 363-365.
55. Gamble, T.R.; Vajdos, F.F.; Yoo, S.; Worthylake, D.K.; Houseweart, M.; Sundquist, W.I.; Hill, C.P. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell 1996, 87, 1285-1294.
56. Braaten, D.; Ansari, H.; Luban, J. The hydrophobic pocket of cyclophilin is the binding site for the human immunodeficiency virus type 1 Gag polyprotein. J. Virol. 1997, 71, 2107-2113.
57. Braaten, D.; Aberham, C.; Franke, E.K.; Yin, L.; Phares, W.; Luban, J. Cyclosporine A-resistant human immunodeficiency virus type 1 mutants demonstrate that Gag encodes the functional target of cyclophilin A. J. Virol. 1996, 70, 5170-5176.
58. Braaten, D.; Luban, J. Cyclophilin A regulates HIV-1 infectivity, as demonstrated by gene targeting in human T cells. EMBO J. 2001, 20, 1300-1309.
59. Towers, G.J.; Hatziioannou, T.; Cowan, S.; Goff, S.P.; Luban, J.; Bieniasz, P.D. Cyclophilin A modulates the sensitivity of HIV-1 to host restriction factors. Nat. Med. 2003, 9, 1138-1143.
60. Sokolskaja, E.; Sayah, D.M.; Luban, J. Target cell cyclophilin A modulates human immunodeficiency virus type 1 infectivity. J. Virol. 2004, 78, 12800-12808.
61. Hatziioannou, T.; Perez-Caballero, D.; Cowan, S.; Bieniasz, P.D. Cyclophilin interactions with incoming human immunodeficiency virus type 1 capsids with opposing effects on infectivity in human cells. J. Virol. 2005, 79, 176-183.
62. Li, Y.; Kar, A.K.; Sodroski, J. Target cell type-dependent modulation of human immunodeficiency virus type 1 capsid disassembly by cyclophilin A. J. Virol. 2009, 83, 10951-10962.
63. Shah, V.B.; Shi, J.; Hout, D.R.; Oztop, I.; Krishnan, L.; Ahn, J.; Shotwell, M.S.; Engelman, A.; Aiken, C. The host proteins transportin SR2/TNPO3 and cyclophilin A exert opposing effects on HIV-1 uncoating. J. Virol. 2013, 87, 422-432.
64. Shibata, R.; Sakai, H.; Kawamura, M.; Tokunaga, K.; Adachi, A. Early replication block of human immunodeficiency virus type 1 in monkey cells. J. Gen. Virol. 1995, 76, 2723-2730.
65. Himathongkham, S.; Luciw, P.A. Restriction of HIV-1 (subtype B) replication at the entry step in rhesus macaque cells. Virology 1996, 219, 485-488.
66. Munk, C.; Brandt, S.M.; Lucero, G.; Landau, N.R. A dominant block to HIV-1 replication at reverse transcription in simian cells. Proc. Natl. Acad. Sci. USA 2002, 99, 13843-13848.
67. Besnier, C.; Takeuchi, Y.; Towers, G. Restriction of lentivirus in monkeys. Proc. Natl. Acad. Sci. USA 2002, 99, 11920-11925.
68. Kootstra, N.A.; Munk, C.; Tonnu, N.; Landau, N.R.; Verma, I.M. Abrogation of postentry restriction of HIV-1-based lentiviral vector transduction in simian cells. Proc. Natl. Acad. Sci. USA 2003, 100, 1298-1303.
69. Hofmann, W.; Schubert, D.; LaBonte, J.; Munson, L.; Gibson, S.; Scammell, J.; Ferrigno, P.; Sodroski, J. Species-specific, postentry barriers to primate immunodeficiency virus infection. J. Virol. 1999, 73, 10020-10028.
70. Stremlau, M.; Owens, C.M.; Perron, M.J.; Kiessling, M.; Autissier, P.; Sodroski, J. The cytoplasmic body component TRIM5alpha restricts HIV-1 infection in Old World monkeys. Nature 2004, 427, 848-853.
71. Sayah, D.M.; Sokolskaja, E.; Berthoux, L.; Luban, J. Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 2004, 430, 569-573.
72. Nisole, S.; Lynch, C.; Stoye, J.P.; Yap, M.W. A Trim5-cyclophilin A fusion protein found in owl monkey kidney cells can restrict HIV-1. Proc. Natl. Acad. Sci. USA 2004, 101, 13324-13328.
73. Wilson, S.J.; Webb, B.L.; Ylinen, L.M.; Verschoor, E.; Heeney, J.L.; Towers, G.J. Independent evolution of an antiviral TRIMCyp in rhesus macaques. Proc. Natl. Acad. Sci. USA 2008, 105, 3557-3562.
74. Brennan, G.; Kozyrev, Y.; Hu, S.L. TRIMCyp expression in Old World primates Macaca nemestrina and Macaca fascicularis. Proc. Natl. Acad. Sci. USA 2008, 105, 3569-3574.
75. Newman, R.M.; Hall, L.; Kirmaier, A.; Pozzi, L.A.; Pery, E.; Farzan, M.; O'Neil, S.P.; Johnson, W. Evolution of a TRIM5-CypA splice isoform in old world monkeys. PLoS Pathog. 2008, 4, e1000003.
76. Virgen, C.A.; Kratovac, Z.; Bieniasz, P.D.; Hatziioannou, T. Independent genesis of chimeric TRIM5-cyclophilin proteins in two primate species. Proc. Natl. Acad. Sci. USA 2008, 105, 3563-3568.
77. Berthoux, L.; Sebastian, S.; Sokolskaja, E.; Luban, J. Cyclophilin A is required for TRIM5{alpha}-mediated resistance to HIV-1 in Old World monkey cells. Proc. Natl. Acad. Sci. USA 2005, 102, 14849-14853.
78. Stremlau, M.; Song, B.; Javanbakht, H.; Perron, M.; Sodroski, J. Cyclophilin A: An auxiliary but not necessary cofactor for TRIM5alpha restriction of HIV-1. Virology 2006, 351, 112-120.
79. Keckesova, Z.; Ylinen, L.M.; Towers, G.J. Cyclophilin A renders human immunodeficiency virus type 1 sensitive to Old World monkey but not human TRIM5 alpha antiviral activity. J. Virol. 2006, 80, 4683-4690.
80. Rits, M.A.; van Dort, K.A.; Kootstra, N.A. Polymorphisms in the regulatory region of the Cyclophilin A gene influence the susceptibility for HIV-1 infection. PLoS One 2008, 3, e3975.
81. Bleiber, G.; May, M.; Martinez, R.; Meylan, P.; Ott, J.; Beckmann, J.S.; Telenti, A. Use of a combined ex vivo/in vivo population approach for screening of human genes involved in the human immunodeficiency virus type 1 life cycle for variants influencing disease progression. J. Virol. 2005, 79, 12674-12680.
82. An, P.; Wang, L.H.; Hutcheson-Dilks, H.; Nelson, G.; Donfield, S.; Goedert, J.J.; Rinaldo, C.R.; Buchbinder, S.; Kirk, G.D.; O'Brien, S.J.; et al. Regulatory polymorphisms in the cyclophilin A gene, PPIA, accelerate progression to AIDS. PLoS Pathog. 2007, 3, e88.
83. Zander, K.; Sherman, M.P.; Tessmer, U.; Bruns, K.; Wray, V.; Prechtel, A.T.; Schubert, E.; Henklein, P.; Luban, J.; Neidleman, J. et al. Cyclophilin A interacts with HIV-1 Vpr and is required for its functional expression. J. Biol. Chem. 2003, 278, 43202-43213.
84. Solbak, S.M.; Reksten, T.R.; Roder, R.; Wray, V.; Horvli, O.; Raae, A.J.; Henklein, P.; Fossen, T. HIV-1 p6-Another viral interaction partner to the host cellular protein cyclophilin A. Biochim. Biophys. Acta 2012, 1824, 667-678.
85. Solbak, S.M.; Wray, V.; Horvli, O.; Raae, A.J.; Flydal, M.I.; Henklein, P.; Nimtz, M.; Schubert, U.; Fossen, T. The host-pathogen interaction of human cyclophilin A and HIV-1 Vpr requires specific N-terminal and novel C-terminal domains. BMC Struct. Biol. 2011, 11, 49.
86. Demange, L.; Moutiez, M.; Vaudry, K.; Dugave, C. Interaction of human cyclophilin hCyp-18 with short peptides suggests the existence of two functionally independent subsites. FEBS Lett. 2001, 505, 191-195.
87. Ardon, O.; Zimmerman, E.S.; Andersen, J.L.; DeHart, J.L.; Blackett, J.; Planelles, V. Induction of G2 arrest and binding to cyclophilin A are independent phenotypes of human immunodeficiency virus type 1 Vpr. J. Virol. 2006, 80, 3694-3700.
88. Brass, A.L.; Dykxhoorn, D.M.; Benita, Y.; Yan, N.; Engelman, A.; Xavier, R.J.; Lieberman, J.; Elledge, S.J. Identification of host proteins required for HIV infection through a functional genomic screen. Science 2008, 319, 921-926.
89. Konig, R.; Zhou, Y.; Elleder, D.; Diamond, T.L.; Bonamy, G.M.; Irelan, J.T.; Chiang, C.Y.; Tu, B.P.; de Jesus, P.D.; Lilley, C.E. et al. Global analysis of host-pathogen interactions that regulate early-stage HIV-1 replication. Cell 2008, 135, 49-60.
90. Schaller, T.; Ocwieja, K.E.; Rasaiyaah, J.; Price, A.J.; Brady, T.L.; Roth, S.L.; Hue, S.; Fletcher, A.J.; Lee, K.; KewalRamani, V.N. et al. HIV-1 capsid-cyclophilin interactions determine nuclear import pathway, integration targeting and replication efficiency. PLoS Pathog. 2011, 7, e1002439.
91. Ocwieja, K.E.; Brady, T.L.; Ronen, K.; Huegel, A.; Roth, S.L.; Schaller, T.; James, L.C.; Towers, G.J.; Young, J.A.; Chanda, S.K. et al. HIV integration targeting: A pathway involving Transportin-3 and the nuclear pore protein RanBP2. PLoS Pathog. 2011, 7, e1001313.
92. Ansari, H.; Greco, G.; Luban, J. Cyclophilin A peptidyl-prolyl isomerase activity promotes ZPR1 nuclear export. Mol. Cell. Biol. 2002, 22, 6993-7003.
93. Zhu, C.; Wang, X.; Deinum, J.; Huang, Z.; Gao, J.; Modjtahedi, N.; Neagu, M.R.; Nilsson, M.; Eriksson, P.S.; Hagberg, H. et al. Cyclophilin A participates in the nuclear translocation of apoptosis-inducing factor in neurons after cerebral hypoxia-ischemia. J. Exp. Med. 2007, 204, 1741-1748.
94. Pan, H.; Luo, C.; Li, R.; Qiao, A.; Zhang, L.; Mines, M.; Nyanda, A.M.; Zhang, J.; Fan, G.H. Cyclophilin A is required for CXCR4-mediated nuclear export of heterogeneous nuclear ribonucleoprotein A2, activation and nuclear translocation of ERK1/2, and chemotactic cell migration. J. Biol. Chem. 2008, 283, 623-637.
95. Watashi, K.; Hijikata, M.; Hosaka, M.; Yamaji, M.; Shimotohno, K. Cyclosporin A suppresses replication of hepatitis C virus genome in cultured hepatocytes. Hepatology 2003, 38, 1282-1288.
96. Nakagawa, M.; Sakamoto, N.; Enomoto, N.; Tanabe, Y.; Kanazawa, N.; Koyama, T.; Kurosaki, M.; Maekawa, S.; Yamashiro, T.; Chen, C.H. et al. Specific inhibition of hepatitis C virus replication by cyclosporin A. Biochem. Biophys. Res. Commun. 2004, 313, 42-47.
97. Watashi, K.; Ishii, N.; Hijikata, M.; Inoue, D.; Murata, T.; Miyanari, Y.; Shimotohno, K. Cyclophilin B is a functional regulator of hepatitis C virus RNA polymerase. Mol. Cell 2005, 19, 111-122.
98. Nakagawa, M.; Sakamoto, N.; Tanabe, Y.; Koyama, T.; Itsui, Y.; Takeda, Y.; Chen, C.H.; Kakinuma, S.; Oooka, S.; Maekawa, S. et al. Suppression of hepatitis C virus replication by cyclosporin a is mediated by blockade of cyclophilins. Gastroenterology 2005, 129, 1031-1041.
99. Robida, J.M.; Nelson, H.B.; Liu, Z.; Tang, H. Characterization of hepatitis C virus subgenomic replicon resistance to cyclosporine in vitro. J. Virol. 2007, 81, 5829-5840.
100. Yang, F.; Robotham, J.M.; Nelson, H.B.; Irsigler, A.; Kenworthy, R.; Tang, H. Cyclophilin a is an essential cofactor for hepatitis C virus infection and the principal mediator of cyclosporine resistance in vitro. J. Virol. 2008, 82, 5269-5278.
101. Kaul, A.; Stauffer, S.; Berger, C.; Pertel, T.; Schmitt, J.; Kallis, S.; Zayas, M.; Lohmann, V.; Luban, J.; Bartenschlager, R. Essential role of cyclophilin A for hepatitis C virus replication and virus production and possible link to polyprotein cleavage kinetics. PLoS Pathog. 2009, 5, e1000546.
102. Chatterji, U.; Bobardt, M.; Selvarajah, S.; Yang, F.; Tang, H.; Sakamoto, N.; Vuagniaux, G.; Parkinson, T.; Gallay, P. The isomerase active site of cyclophilin A is critical for hepatitis C virus replication. J. Biol. Chem. 2009, 284, 16998-17005.
103. Liu, Z.; Yang, F.; Robotham, J.M.; 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.
104. Ciesek, S.; Steinmann, E.; Wedemeyer, H.; Manns, M.P.; Neyts, J.; Tautz, N.; Madan, V.; Bartenschlager, R.; von Hahn, T.; Pietschmann, T. Cyclosporine A inhibits hepatitis C virus nonstructural protein 2 through cyclophilin A. Hepatology 2009, 50, 1638-1645.
105. Von Hahn, T.; Schiene-Fischer, C.; van, N.D.; Pfaender, S.; Karavul, B.; Steinmann, E.; Potthoff, A.; Strassburg, C.; Hamdi, N.; Abdelaziz, A.I. et al. Hepatocytes that express variants of cyclophilin A are resistant to HCV infection and replication. Gastroenterology 2012, 143, 439-447.
106. Foster, T.L.; Gallay, P.; Stonehouse, N.J.; Harris, M. Cyclophilin A interacts with domain II of hepatitis C virus NS5A and stimulates RNA binding in an isomerase-dependent manner. J. Virol. 2011, 85, 7460-7464.
107. Nag, A.; Robotham, J.M.; Tang, H. Suppression of viral RNA binding and the assembly of infectious hepatitis C virus particles in vitro by cyclophilin inhibitors. J. Virol. 2012, 86, 12616-12624.
108. Bobardt, M.; Hopkins, S.; Baugh, J.; Chatterji, U.; Hernandez, F.; Hiscott, J.; Sluder, A.; Lin, K.; Gallay, P.A. HCV NS5A and IRF9 compete for CypA binding. J. Hepatol. 2013, 58, 16-23.
109. Fernandes, F.; Poole, D.S.; Hoover, S.; Middleton, R.; Andrei, A.C.; Gerstner, J.; Striker, R. Sensitivity of hepatitis C virus to cyclosporine A depends on nonstructural proteins NS5A and NS5B. Hepatology 2007, 46, 1026-1033.
110. Hanoulle, X.; Badillo, A.; Wieruszeski, J.M.; Verdegem, D.; Landrieu, I.; Bartenschlager, R.; Penin, F.; Lippens, G. Hepatitis C virus NS5A protein is a substrate for the peptidyl-prolyl cis/trans isomerase activity of cyclophilins A and B. J. Biol. Chem. 2009, 284, 13589-13601.
111. Yang, F.; Robotham, J.M.; Grise, H.; Frausto, S.; Madan, V.; Zayas, M.; Bartenschlager, R.; Robinson, M.; Greenstein, A.E.; Nag, A. et al. A major determinant of cyclophilin dependence and cyclosporine susceptibility of hepatitis C virus identified by a genetic approach. PLoS Pathog. 2010, 6, e1001118.
112. Chatterji, U.; Lim, P.; Bobardt, M.D.; Wieland, S.; Cordek, D.G.; Vuagniaux, G.; Chisari, F.; Cameron, C.E.; Targett-Adams, P.; Parkinson, T. et al. HCV resistance to cyclosporin A does not correlate with a resistance of the NS5A-cyclophilin A interaction to cyclophilin inhibitors. J. Hepatol. 2010, 53, 50-56.
113. Fernandes, F.; Ansari, I.U.; Striker, R. cyclosporine inhibits a direct interaction between cyclophilins and hepatitis C NS5A. PLoS One 2010, 5, e9815.
114. Grise, H.; Frausto, S.; Logan, T.; Tang, H. A conserved tandem cyclophilin-binding site in hepatitis C virus nonstructural protein 5A regulates Alisporivir susceptibility. J. Virol. 2012, 86, 4811-4822.
115. Verdegem, D.; Badillo, A.; Wieruszeski, J.M.; Landrieu, I.; Leroy, A.; Bartenschlager, R.; Penin, F.; Lippens, G.; Hanoulle, X. 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. 2011, 286, 20441-20454.
116. Liang, Y.; Ye, H.; Kang, C.B.; Yoon, H.S. Domain 2 of nonstructural protein 5A (NS5A) of hepatitis C virus is natively unfolded. Biochemistry 2007, 46, 11550-11558.
117. Hanoulle, X.; Verdegem, D.; Badillo, A.; Wieruszeski, J.M.; Penin, F.; Lippens, G. Domain 3 of non-structural protein 5A from hepatitis C virus is natively unfolded. Biochem. Biophys. Res. Commun. 2009, 381, 634-638.
118. Hilgard, P.; Kahraman, A.; Lehmann, N.; Seltmann, C.; Beckebaum, S.; Ross, R.S.; Baba, H.A.; Malago, M.; Broelsch, C.E.; Gerken, G. Cyclosporine versus tacrolimus in patients with HCV infection after liver transplantation: Effects on virus replication and recurrent hepatitis. World J. Gastroenterol. 2006, 12, 697-702.
119. Martin, P.; Busuttil, R.W.; Goldstein, R.M.; Crippin, J.S.; Klintmalm, G.B.; Fitzsimmons, W.E.; Uleman, C. Impact of tacrolimus versus cyclosporine in hepatitis C virus-infected liver transplant recipients on recurrent hepatitis: A prospective, randomized trial. Liver Transpl. 2004, 10, 1258-1262.
120. Guitard, J.; Sandres-Saune, K.; Kamar, N.; Ribes, D.; Faguer, S.; Esposito, L.; Lavit, M.; Muscari, F.; Peron, J.M.; Lavayssiere, L. et al. Hepatitis C virus viral load after conversion from tacrolimus to cyclosporine in liver transplant patients: A pilot study. Transplant. Proc. 2007, 39, 2603-2605.
121. Rayhill, S.C.; Barbeito, R.; Katz, D.; Voigt, M.; Labrecque, D.; Kirby, P.; Miller, R.; Stolpen, A.; Wu, Y.; Schmidt, W. A cyclosporine-based immunosuppressive regimen may be better than tacrolimus for long-term liver allograft survival in recipients transplanted for hepatitis C. Transplant. Proc. 2006, 38, 3625-3628.
122. Inoue, K.; Sekiyama, K.; Yamada, M.; Watanabe, T.; Yasuda, H.; Yoshiba, M. Combined interferon alpha2b and cyclosporin A in the treatment of chronic hepatitis C: Controlled trial. J. Gastroenterol. 2003, 38, 567-572.
123. Inoue, K.; Yoshiba, M. Interferon combined with cyclosporine treatment as an effective countermeasure against hepatitis C virus recurrence in liver transplant patients with end-stage hepatitis C virus related disease. Transplant. Proc. 2005, 37, 1233-1234.
124. Flisiak, R.; Jaroszewicz, J.; Flisiak, I.; Lapinski, T. Update on alisporivir in treatment of viral hepatitis C. Expert Opin. Investig. Drugs 2012, 21, 375-382.
125. Hopkins, S.; Dimassimo, B.; Rusnak, P.; Heuman, D.; Lalezari, J.; Sluder, A.; Scorneaux, B.; Mosier, S.; Kowalczyk, P.; Ribeill, Y. et al. The cyclophilin inhibitor SCY-635 suppresses viral replication and induces endogenous interferons in patients with chronic HCV genotype 1 infection. J. Hepatol. 2012, 57, 47-54.
126. Gregory, M.A.; Bobardt, M.; Obeid, S.; Chatterji, U.; Coates, N.J.; Foster, T.; Gallay, P.; Leyssen, P.; Moss, S.J.; Neyts, J. et al. Preclinical characterization of naturally occurring polyketide cyclophilin inhibitors from the sanglifehrin family. Antimicrob. Agents Chemother. 2011, 55, 1975-1981.
127. Goto, K.; Watashi, K.; Inoue, D.; Hijikata, M.; Shimotohno, K. Identification of cellular and viral factors related to anti-hepatitis C virus activity of cyclophilin inhibitor. Cancer Sci. 2009, 100, 1943-1950.
128. Puyang, X.; Poulin, D.L.; Mathy, J.E.; Anderson, L.J.; Ma, S.; Fang, Z.; Zhu, S.; Lin, K.; Fujimoto, R.; Compton, T. et al. Mechanism of resistance of hepatitis C virus replicons to structurally distinct cyclophilin inhibitors. Antimicrob. Agents Chemother. 2010, 54, 1981-1987.
129. Delang, L.; Vliegen, I.; Froeyen, M.; Neyts, J. Comparative study of the genetic barriers and pathways towards resistance of selective inhibitors of hepatitis C virus replication. Antimicrob. Agents Chemother. 2011, 55, 4103-4113.
130. Colgan, J.; Asmal, M.; Neagu, M.; Yu, B.; Schneidkraut, J.; Lee, Y.; Sokolskaja, E.; Andreotti, A.; Luban, J. Cyclophilin A regulates TCR signal strength in CD4+ T cells via a proline-directed conformational switch in Itk. Immunity 2004, 21, 189-201.
131. Liu, X.; Zhao, Z.; Liu, W. Insights into the roles of cyclophilin A during influenza virus infection. Viruses 2013, 5, 182-191.
132. Mendu, V.; Chiu, M.; Barajas, D.; Li, Z.; Nagy, P.D. Cpr1 cyclophilin and Ess1 parvulin prolyl isomerases interact with the tombusvirus replication protein and inhibit viral replication in yeast model host. Virology 2010, 406, 342-351.
133. Qing, M.; Yang, F.; Zhang, B.; Zou, G.; Robida, J.M.; Yuan, Z.; Tang, H.; Shi, P.Y. Cyclosporine inhibits flavivirus replication through blocking the interaction between host cyclophilins and viral NS5 protein. Antimicrob. Agents Chemother. 2009, 53, 3226-3235.
134. Li, Y.J.; Wu, H.H.; Weng, C.H.; Chen, Y.C.; Hung, C.C.; Yang, C.W.; Wang, R.Y.; Sakamoto, N.; Tian, Y.C. Cyclophilin A and nuclear factor of activated T cells are essential in cyclosporinemediated suppression of polyomavirus BK replication. Am. J. Transplant. 2012, 12, 2348-2362.
135. De Wilde, A.H.; Li, Y.; van der Meer, Y.; Vuagniaux, G.; Lysek, R.; Fang, Y.; Snijder, E.J.; van Hemert, M.J. Cyclophilin inhibitors block arterivirus replication by interfering with viral RNA synthesis. J. Virol. 2013, 87, 1454-1464.
136. He, H.; Zhou, D.; Fan, W.; Fu, X.; Zhang, J.; Shen, Z.; Li, J.; Wu, Y. Cyclophilin A inhibits rotavirus replication by facilitating host IFN-I production. Biochem. Biophys. Res. Commun. 2012, 422, 664-669.
137. Keyes, L.R.; Bego, M.G.; Soland, M.; St Jeor, S. Cyclophilin A is required for efficient human cytomegalovirus DNA replication and reactivation. J. Gen. Virol. 2012, 93, 722-732.
138. Bose, S.; Mathur, M.; Bates, P.; Joshi, N.; Banerjee, A.K. Requirement for cyclophilin A for the replication of vesicular stomatitis virus New Jersey serotype. J. Gen. Virol. 2003, 84, 1687-1699.
139. Castro, A.P.; Carvalho, T.M.; Moussatche, N.; Damaso, C.R. Redistribution of cyclophilin A to viral factories during vaccinia virus infection and its incorporation into mature particles. J. Virol. 2003, 77, 9052-9068.
140. Chung, C.S.; Chen, C.H.; Ho, M.Y.; Huang, C.Y.; Liao, C.L.; Chang, W. Vaccinia virus proteome: Identification of proteins in vaccinia virus intracellular mature virion particles. J. Virol. 2006, 80, 2127-2140.
141. Watanabe, A.; Yoneda, M.; Ikeda, F.; Terao-Muto, Y.; Sato, H.; Kai, C. CD147/EMMPRIN acts as a functional entry receptor for measles virus on epithelial cells. J. Virol. 2010, 84, 4183-4193.
142. Bienkowska-Haba, M.; Patel, H.D.; Sapp, M. Target cell cyclophilins facilitate human papillomavirus type 16 infection. PLoS Pathog. 2009, 5, e1000524.
143. Bienkowska-Haba, M.; Williams, C.; Kim, S.M.; Garcea, R.L.; Sapp, M. Cyclophilins facilitate dissociation of the human papillomavirus type 16 capsid protein L1 from the L2/DNA complex following virus entry. J. Virol. 2012, 86, 9875-9887.
144. De Wilde, A.H.; Zevenhoven-Dobbe, J.C.; van der Meer, Y.; Thiel, V.; Narayanan, K.; Makino, S.; Snijder, E.J.; van Hemert, M.J. Cyclosporin A inhibits the replication of diverse coronaviruses. J. Gen. Virol. 2011, 92, 2542-2548.
145. Pfefferle, S.; Schopf, J.; Kogl, M.; Friedel, C.C.; Muller, M.A.; Carbajo-Lozoya, J.; Stellberger, T.; von Dall'Armi, E.; Herzog, P.; Kallies, S. et al. The SARS-coronavirus-host interactome: Identification of cyclophilins as target for pan-coronavirus inhibitors. PLoS Pathog. 2011, 7, e1002331.
146. Favreau, D.J.; Meessen-Pinard, M.; Desforges, M.; Talbot, P.J. Human coronavirus-induced neuronal programmed cell death is cyclophilin d dependent and potentially caspase dispensable. J. Virol. 2012, 86, 81-93.
147. Xia, W.L.; Shen, Y.; Zheng, S.S. Inhibitory effect of cyclosporine A on hepatitis B virus replication in vitro and its possible mechanisms. Hepatobiliary Pancreat. Dis. Int. 2005, 4, 18-22.
148. Zhao, C.; Fang, C.Y.; Tian, X.C.; Wang, L.; Yang, P.Y.; Wen, Y.M. Proteomic analysis of hepatitis B surface antigen positive transgenic mouse liver and decrease of cyclophilin A. J. Med. Virol. 2007, 79, 1478-1484.
149. Tian, X.; Zhao, C.; Zhu, H.; She, W.; Zhang, J.; Liu, J.; Li, L.; Zheng, S.; Wen, Y.M.; Xie, Y. Hepatitis B virus (HBV) surface antigen interacts with and promotes cyclophilin a secretion: Possible link to pathogenesis of HBV infection. J. Virol. 2010, 84, 3373-3381.
150. Ansari, I.; Allen, T; Berical, A; Stock, P.; Barin, B.; Striker, R. Phenotypic analysis of NS5A variant from liver transplant patient with increased cyclosporine susceptibility. Virology 2013, 436, 268-273