Structural, Biochemical, and in Vivo Characterization of the First Virally Encoded Cyclophilin from the Mimivirus

Journal of Molecular Biology

Volumn 378, Issue 1, 2008, Pages 71-86

  Thai, Vu ^b   Renesto, Patricia ^c   Fowler, C Andrew ^d   Brown, Darin J ^a   Davis, Tara ^e   Gu, Wanjun ^a   Pollock, David D ^a   Kern, Dorothee ^b   Raoult, Didier ^c   Eisenmesser, Elan Z ^a  

^a UNIVERSITY OF COLORADO   (United States)

^b BRANDEIS UNIVERSITY   (United States)

^c AIX MARSEILLE UNIVERSITY   (France)

^d UNIVERSITY OF COLORADO   (United States)

^e UNIVERSITY OF TORONTO   (Canada)

Author keywords

cyclophilin; Mimivirus; peptidyl prolyl isomerase; pneumonia; virus

Indexed keywords

CYCLOPHILIN; PEPTIDYLPROLYL ISOMERASE;

ARTICLE; CHEMICAL ANALYSIS; CONTROLLED STUDY; ENZYME ACTIVITY; HOST CELL; HUMAN IMMUNODEFICIENCY VIRUS 1; IMMUNOFLUORESCENCE TEST; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN STRUCTURE; SEVERE ACUTE RESPIRATORY SYNDROME; VIRION;

HUMAN IMMUNODEFICIENCY VIRUS 1; MIMIVIRUS;

EID: 41249093659     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2007.08.051     Document Type: Article

References (68)

1. Arora K., Gwinn W.M., Bower M.A., Watson A., Okwumabua I., MacDonald H.R., et al. Extracellular cyclophilins contribute to the regulation of inflammatory responses. J. Immun. 175 (2005) 517-522
2. Yao Q.Z., Li M., Yang H., Chai H., Fisher W., and Chen C.Y. Roles of cyclophilins in cancers and other organ systems. World J. Surg. 29 (2005) 276-280
3. Shaw P.E. Peptidyl-prolyl isomerases: a new twist to transcription. EMBO Rep. 3 (2002) 521-526
4. Breheny P.J., Laederach A., Fulton D.B., and Andreotti A.H. Ligand specificity modulated by prolyl imide bond cis/trans isomerization in the Itk SH2 domain: a quantitative NMR study. J. Am. Chem. Soc. 125 (2003) 15706-15707
5. Bose S., Mathur M., Bates P., Joshi N., and Banerjee A.K. Requirement for cyclophilin A for the replication of vesicular stomatitis virus New Jersey serotype. J. Gen. Virol. 84 (2003) 1687-1699
6. Chen Z.N., Mi L., Xu J., Yu J.Y., Wang X.H., Jiang J.L., et al. Function of HAb18G/CD147 in invasion of host cells by severe acute respiratory syndrome coronavirus. J. Infect. Dis. 191 (2005) 755-760
7. Lin T.Y., and Emerman M. Cyclophilin A interacts with diverse lentiviral capsids. Retrovirology 3 (2006) 70
8. Sorin M., and Kalpana G.V. Dynamics of virus-host interplay in HIV-1 replication. Curr. Hiv Res. 4 (2006) 117-130
9. Watashi K., Ishii N., Hijikata M., Inoue D., Murata T., Miyanari Y., and Shimotohno K. Cyclophilin B is a functional regulator of hepatitis C virus RNA polymerase. Mol. Cell 19 (2005) 111-122
10. Castro A.P.V., Carvalho T.M.U., Moussatche N., and Damaso C.R.A. Redistribution of cyclophilin A to viral factories during vaccinia virus infection and its incorporation into mature particles. J. Virol. 77 (2003) 9052-9068
11. Goff S.P. Retrovirus restriction factors. Mol. Cell 16 (2004) 849-859
12. Yurchenko V., Constant S., and Bukrinsky M. Dealing with the family: CD147 interactions with cyclophilins. Immunology 117 (2006) 301-309
13. Raoult D., Audic S., Robert C., Abergel C., Renesto P., Ogata H., et al. The 1.2-megabase genome sequence of mimivirus. Science 306 (2004) 1344-1350
14. Renesto P., Abergel C., Decloquement P., Moinier D., Azza S., Ogata H., et al. Mimivirus giant particles incorporate a large fraction of anonymous and unique gene products. J. Virol. 80 (2006) 11678-11685
15. Claverie J.M., Ogata H., Audic S., Abergel C., Suhre K., and Fournier P.E. Mimivirus and the emerging concept of "giant" virus. Virus Res. 117 (2006) 133-144
16. La Scola B., Marrie T.J., Auffray J.P., and Raoult D. Mimivirus in pneumonia patients. Emerg. Infect. Dis.s 11 (2005) 449-452
17. Raoult D., Renesto P., and Brouqui P. Laboratory infection of a technician by mimivirus. Ann. Int. Med. 144 (2006) 702-703
18. Xiao C.A., Chipman P.R., Battisti A.J., Bowman V.D., Renesto P., Raoult D., and Rossmann M.G. Cryo-electron microscopy of the giant mimivirus. J. Mol. Biol. 353 (2005) 493-496
19. Moreira D., and Lopez-Garcia P. Comment on "The 1.2-megabase genome sequence of Mimivirus". Science 308 (2005)
20. Iyer L.M., Koonin E.V., Leipe D.D., and Aravind L. Origin and evolution of the archaeo-eukaryotic primase superfamily and related palm-domain proteins: structural insights and new members. Nucl. Acids Res. 33 (2005) 3875-3896
21. Suzan-Monti M., La Scola B., and Raoult D. Genomic and evolutionary aspects of Mimivirus. Virus Res. 117 (2006) 145-155
22. Pushkarsky T., Zybarth G., Dubrovsky L., Yurchenko V., Tang H., Guo H.M., et al. CD147 facilitates HIV-1 infection by interacting with virus-associated cyclophilin A. Proc. Natl Acad. Sci. USA 98 (2001) 6360-6365
23. Saphire A.C.S., Bobardt M.D., and Gallay P.A. Cyclophilin a plays distinct roles in human immunodeficiency virus type 1 entry and postentry events, as revealed by spinoculation. J. Virol. 76 (2002) 4671-4677
24. Gamble T.R., Vajdos F.F., Yoo S.H., Worthylake D.K., Houseweart M., Sundquist W.I., and Hill C.P. Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cel 87 (1996) 1285-1294
25. Ostoa-Saloma P., Carrero J.C., Petrossian P., Herion P., Landa A., and Laclette J.P. Cloning, characterization and functional expression of a cyclophilin of Entamoeba histolytica. Mol. Biochem. Parasitol. 107 (2000) 219-225
26. Eisenmesser E.Z., Bosco D.A., Akke M., and Kern D. Enzyme dynamics during catalysis. Science 295 (2002) 1520-1523
27. Zhao Y., and Ke H. Crystal structure implies that cyclophilin predominantly catalyzes the trans to cis isomerization. Biochemistry 35 (1996) 7356-7361
28. Zydowsky L.D., Etzkorn F.A., Chang H.Y., Ferguson S.B., Stolz L.A., Ho S.I., and Walsh C.T. Active site mutants of human cyclophilin A separate peptidyl-prolyl isomerase activity from cyclosporin A binding and calcineurin inhibition. Protein Sci. 1 (1992) 1092-1099
29. Ke H.M., and Huai Q. Crystal structures of cyclophilin and its partners. Front. Biosci. 9 (2004) 2285-2296
30. Taylor P., Dornan J., Carrello A., Minchin R.F., Ratajczak T., and Walkinshaw M.D. Two structures of cyclophilin 40: folding and fidelity in the TPR domains. Structure 9 (2001) 431-438
31. Manteca A., Kamphausen T., Fanghanel J., Fischer G., and Sanchez J. Cloning and characterization of a Streptomyces antibioticus ATCC11891 cyclophilin related to Gram negative bacteria cyclophilins. FEBS Letters 572 (2004) 19-26
32. Manteca A., Pelaez A.I., Zardoya R., and Sanchez J. Actinobacteria cyclophilins: Phylogenetic relationships and description of new class- and order-specific paralogues. J. Mol. Evol. 63 (2006) 719-732
33. Rinfret A., Collins C., Menard R., and Anderson S.K. The N-terminal cyclophilin-homologous domain of a 150-kilodalton tumor recognition molecule exhibits both peptidylprolyl cis-trans-isomerase and chaperone activities. Biochemistry 33 (1994) 1668-1673
34. Eisenmesser E.Z., Millet O., Labeikovsky W., Korzhnev D.M., Wolf-Watz M., Bosco D.A., et al. Intrinsic dynamics of an enzyme underlies catalysis. Nature 438 (2005) 117-121
35. Fejzo J., Etzkorn F.A., Clubb R.T., Shi Y.A., Walsh C.T., and Wagner G. The mutant Escherichia coli F112W cyclophilin binds cyclosporin A in nearly identical conformation as human cyclophilin. Biochemistry 33 (1994) 5711-5720
36. Ottiger M., Zerbe O., Guntert P., and Wuthrich K. The NMR solution conformation of unligated human cyclophilin A. J. Mol. Biol. 272 (1997) 64-81
37. Wilmot C.M., and Thornton J.M. Analysis and prediction of the different types of beta-turn in proteins. J. Mol. Biol. 203 (1988) 221-232
38. Reidt U., Wahl M.C., Fasshauer D., Horowitz D.S., Luhrmann R., and Ficner R. Crystal structure of a complex between human spliceosomal cyclophilin H and a U4/U6 snRNP-60K peptide. J. Mol. Biol. 331 (2003) 45-56
39. Limacher A., Kloer D.P., Fluckiger S., Folkers G., Crameri R., and Scapozza L. The crystal structure of Aspergillus fumigatus cyclophilin reveals 3D domain swapping of a central element. Structure 14 (2006) 185-195
40. Abdurahman S., Hoglund S., Hoglund A., and Vahlne A. Mutation in the loop C-terminal to the cyclophilin A binding site of HIV-1 capsid protein disrupts proper virus assembly and infectivity. Retrovirology 4 (2007) 4-19
41. Zhao Y.D., and Ke H.M. Mechanistic implication of crystal structures of the cyclophilin-dipeptide complexes. Biochemistry 35 (1996) 7362-7368
42. Piotukh K., Gu W., Kofler M., Labudde D., Helms V., and Freund C. Cyclophilin a binds to linear peptide motifs containing a consensus that is present in many human proteins. J. Biol. Chem. 280 (2005) 23668-23674
43. Fischer G., Bang H., and Mech C. Determination of enzymatic catalysis for the cis-trans-isomerization of peptide binding in proline-containing peptides. Biomed. Biochim. Acta 43 (1984) 1101-1111
44. Liu J., Chen C.M., and Walsh C.T. Human and Escherichia-coli cyclophilins - sensitivity to inhibition by the immunosuppressant cyclosporine-a correlates with a specific tryptophan residue. Biochemistry 30 (1991) 2306-2310
45. Kern D., Drakenberg T., Wikstrom M., Forsen S., Bang H., and Fischer G. The cis/trans interconversion of the calcium regulating hormone calcitonin is catalyzed by cyclophilin. FEBS Leters 323 (1993) 198-202
46. Suzan-Monti M., La Scola B., Barrassi L., Espinosa L., and Raoult D. Ultrastructural characterization of the giant volcano-like virus factory of Acanthamoeba polyphaga Mimivirus. PLoS 2 (2007) 1-11
47. Braaten D., Franke E.K., and Luban J. Cyclophilin A is required for the replication of group M human immunodeficiency virus type 1 (HIV-1) and simian immunodeficiency virus SIV(CPZ)GAB but not group O HIV-1 or other primate immunodeficiency viruses. J. Virol. 70 (1996) 4220-4227
48. Franke E.K., and Luban J. Inhibition of HIV-1 replication by cyclosporine A or related compounds correlates with the ability to disrupt the Gag-cyclophilin A interaction. Virology 222 (1996) 279-282
49. Sherry B., Zybarth G., Alfano M., Dubrovsky L., Mitchell R., Rich D., et al. Role of cyclophilin A in the uptake of HIV-1 by macrophages and T lymphocytes. Proc. Natl Acad. Sci. USA 95 (1998) 1758-1763
50. Bell A., Monaghan P., and Page A.P. Peptidyl-prolyl cis-trans isomerases (immunophilins) and their roles in parasite biochemistry, host-parasite interaction and antiparasitic drug action. Int. J. Parasitol. 36 (2006) 261-276
51. Pemberton T.J. Identification and comparative analysis of sixteen fungal peptidyl-prolyl cis/trans isomerase repertoires. BMC Genom. 7 (2006) 244
52. Dietrich L., Ehrlich L.S., LaGrassa T.J., Ebbets-Reed D., and Carter C. Structural consequences of cyclophilin a binding on maturational refolding in human immunodeficiency virus type 1 capsid protein. J. Virol. 75 (2001) 4721-4733
53. Bosco D.A., Eisenmesser E.Z., Pochapsky S., Sundquist W.I., and Kern D. Catalysis of cis/trans isomerization in native HIV-1 capsid by human cyclophilin A. Proc. Natl Acad. Sci. USA 99 (2002) 5247-5252
54. Howard B.R., Vajdos F.F., Li S., Sundquist W.I., and Hill C.P. Structural insights into the catalytic mechanism of cyclophilin A. Nature Struct. Biol. 10 (2003) 475-481
55. Zeng L., Zhou Z., Xu J., Zhao W., Wang W., Huang Y., et al. Molecular cloning, structure and expression of a novel nuclear RNA-binding cyclophilin-like gene (PPIL4) from human fetal brain. Cytogenet. Cell Genet. 95 (2001) 43-47
56. Cantin R., Methot S., and Tremblay M.J. Plunder and stowaways: Incorporation of cellular proteins by enveloped viruses. J. Virol. 79 (2005) 6577-6587
57. Hatziioannou T., Perez-Caballero D., Cowan S., and Bieniasz P.D. Cyclophilin interactions with incoming human immunodeficiency virus type 1 capsids with opposing effects on infectivity in human cells. J. Virol. 79 (2005) 176-183
58. Khan M., La Scola B., Lepidi H., and Raoult D. Pneumonia in mice inoculated experimentally with Acanthamoeba polyphaga mimivirus. Microb. Pathogen. 42 (2007) 56-61
59. Sayah D.M., Sokolskaja E., Berthoux L., and Luban J. Cyclophilin A retrotransposition into TRIM5 explains owl monkey resistance to HIV-1. Nature 430 (2004) 569-573
60. Muchmore D.C., McIntosh L.P., Russell C.B., Anderson D.E., and Dahlquist F.W. Expression and N-15 labeling of proteins for proton and N-15 nuclear-magnetic-resonance. Methods Enzymol. 177 (1989) 44-73
61. Otwinowski Z., and Minor W. Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276 (2001) 307-326
62. Read R.J. Pushing the boundaries of molecular replacement with maximum likelihood. Acta Crystallog. sect. D 57 (2001) 1373-1382
63. Murshudov G.N., Vagin A.A., and Dodson E.J. Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallog. sect. D 53 (1997) 240-255
64. Emsley P., and Cowtan K. Coot: model-building tools for molecular graphics. Acta Crystallog. sect. D 60 (2004) 2126-2132
65. Cohen S.X., Morris R.J., Fernandez F.J., Ben Jelloul M., Kakaris M., Parthasarathy V., et al. Towards complete validated models in the next generation of ARP/wARP. Acta Crystallog. sect. D 60 (2004) 2222-2229
66. Laskowski R.A., Macarthur M.W., Moss D.S., and Thornton J.M. Procheck - a program to check the stereochemical quality of protein structures. J. Appl. Crystallog. 26 (1993) 283-291
67. Delaglio F., Grzesiek S., Vuister G.W., Zhu G., Pfeifer J., and Bax A. Nmrpipe - a multidimensional spectral processing system based on Unix Pipes. J. Biomol. NMR 6 (1995) 277-293
68. Vranken W.F., Boucher W., Stevens T.J., Fogh R.H., Pajon A., Llinas P., et al. The CCPN data model for NMR spectroscopy: development of a software pipeline. Proteins:Struct. Funct. Bioinformat. 59 (2005) 687-696