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Analysis of the Trypanosoma cruzi cyclophilin gene family and identification of Cyclosporin A binding proteins

Published online by Cambridge University Press:  15 May 2006

M. POTENZA
Affiliation:
Instituto Nacional de Parasitología “Dr. M. Fatala Chabén”, A.N.L.I.S. Malbrán, Buenos Aires, Argentina
A. GALAT
Affiliation:
Departement d'Ingenierie et d'Etudes des Proteines, DSV/CEA, Gif-sur-Yvette Cedex, France
T. A. MINNING
Affiliation:
Department of Cellular Biology and Centre for Tropical and Emerging Global Diseases, University of Georgia, Athens, GA, USA
A. M. RUIZ
Affiliation:
Instituto Nacional de Parasitología “Dr. M. Fatala Chabén”, A.N.L.I.S. Malbrán, Buenos Aires, Argentina
R. DURAN
Affiliation:
Instituto de Investigaciones Biológicas Clemente Estable, Montevideo, Uruguay
R. L. TARLETON
Affiliation:
Department of Cellular Biology and Centre for Tropical and Emerging Global Diseases, University of Georgia, Athens, GA, USA
M. MARÍN
Affiliation:
Departamento de Bioquímica, Facultad de Ciencias, Universidad de la República, Montevideo, Uruguay
L. E. FICHERA
Affiliation:
Instituto Nacional de Parasitología “Dr. M. Fatala Chabén”, A.N.L.I.S. Malbrán, Buenos Aires, Argentina
J. BÚA
Affiliation:
Instituto Nacional de Parasitología “Dr. M. Fatala Chabén”, A.N.L.I.S. Malbrán, Buenos Aires, Argentina

Abstract

The Trypanosoma cruzi cyclophilin gene family comprises 15 paralogues whose nominal masses vary from 19 to 110 kDa, namely TcCyP19, TcCyP20, TcCyP21, TcCyP22, TcCyP24, TcCyP25, TcCyP26, TcCyP28, TcCyP29, TcCyP30, TcCyP34, TcCyP35, TcCyP40, TcCyP42 and TcCyP110. Under the conditions used, only some of the T. cruzi cyclophilin paralogue products could be isolated by affinity chromatography. The 15 paralogues were aligned with 495 cyclophilins from diverse organisms. Analyses of clusters formed by the T. cruzi cyclophilins with others encoded in various genomes revealed that 8 of them (TcCyP19, TcCyP21, TcCyP22, TcCyP24, TcCyP35, TcCyP40, TcCyP42 and TcCyP110) have orthologues in many different genomes whereas the other 7 display less-defined patterns of their sequence attributes and their classification to a specific group of cyclophilin's orthologues remains uncertain. Seven epimastigote cDNA clones encoding cyclophilin isoforms were further studied. These genes were found dispersed throughout the genome of the parasite. Amastigote and trypomastigote mRNAs encoding these 7 genes were also detected. We isolated 4 cyclosporin A-binding proteins in T. cruzi epimastigote extracts, which were identified by mass spectrometry as TcCyP19, TcCyP22, TcCyP28 and TcCyP40. Cyclosporin A-binding to these cyclophilins might be of importance to the mechanism of action of Cyclosporin A and its non-immunosuppressive analogues, whose trypanocidal effects were previously reported, and therefore, of potential interest in the chemotherapy of Chagas' disease.

Type
Research Article
Copyright
2006 Cambridge University Press

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References

REFERENCES

Adams, M. D., Celniker, S. E., Holt, R. A., Evans, C. A., Gocayne, J. D., Amanatides, P. G., Scherer, S. E., Li, P. W., Hoskins, R. A., Galle, R. F., George, R. A., Lewis, S. E., Richards, S., Ashburner, M., Henderson, S. N., Sutton, G. G., Wortman, J. R., Yandell, M. D., Zhang, Q., Chen, L. X., Brandon, R. C., Rogers, Y. H., Blazej, R. G., Champe, M., Pfeiffer, B. D., Wan, K. H., Doyle, C., Baxter, E. G., Helt, G., Nelson, C. R., Gabor, G. L., Abril, J. F., Agbayani, A., An, H. J., Andrews-Pfannkoch, C., Baldwin, D., Ballew, R. M., Basu, A., Baxendale, J., Bayraktaroglu, L., Beasley, E. M., Beeson, K. Y., Benos, P. V., Berman, B. P., Bhandari, D., Bolshakov, S., Borkova, D., Botchan, M. R., Bouck, J., Brokstein, P., Brottier, P., Burtis, K. C., Busam, D. A., Butler, H., Cadieu, E., Center, A., Chandra, I., Cherry, J. M., Cawley, S., Dahlke, C., Davenport, L. B., Davies, P., De Pablos, B., Delcher, A., Deng, Z., Mays, A. D., Dew, I., Dietz, S. M., Dodson, K., Doup, L. E., Downes, M., Dugan-Rocha, S., Dunkov, B. C., Dunn, P., Durbin, K. J., Evangelista, C. C., Ferraz, C., Ferriera, S., Fleischmann, W., Fosler, C., Gabrielian, A. E., Garg, N. S., Gelbart, W. M., Glasser, K., Glodek, A., Gong, F., Gorrell, J. H., Gu, Z., Guan, P., Harris, M., Harris, N. L., Harvey, D., Heiman, T. J., Hernandez, J. R., Houck, J., Hostin, D., Houston, K. A., Howland, T. J., Wei, M. H., Ibegwam, C., Jalali, M., Kalush, F., Karpen, G. H., Ke, Z., Kennison, J. A., Ketchum, K. A., Kimmel, B. E., Kodira, C. D., Kraft, C., Kravitz, S., Kulp, D., Lai, Z., Lasko, P., Lei, Y., Levitsky, A. A., Li, J., Li, Z., Liang, Y., Lin, X., Liu, X., Mattei, B., McIntosh, T. C., McLeod, M. P., McPherson, D., Merkulov, G., Milshina, N. V., Mobarry, C., Morris, J., Moshrefi, A., Mount, S. M., Moy, M., Murphy, B., Murphy, L., Muzny, D. M., Nelson, D. L., Nelson, D. R., Nelson, K. A., Nixon, K., Nusskern, D. R., Pacleb, J. M., Palazzolo, M., Pittman, G. S., Pan, S., Pollard, J., Puri, V., Reese, M. G., Reinert, K., Remington, K., Saunders, R. D., Scheeler, F., Shen, H., Shue, B. C., Siden-Kiamos, I., Simpson, M., Skupski, M. P., Smith, T., Spier, E., Spradling, A. C., Stapleton, M., Strong, R., Sun, E., Svirskas, R., Tector, C., Turner, R., Venter, E., Wang, A. H., Wang, X., Wang, Z. Y., Wassarman, D. A., Weinstock, G. M., Weissenbach, J., Williams, S. M., Woodaget, T., Worley, K. C., Wu, D., Yang, S., Yao, Q. A., Ye, J., Yeh, R. F., Zaveri, J. S., Zhan, M., Zhang, G., Zhao, Q., Zheng, L., Zheng, X. H., Zhong, F. N., Zhong, W., Zhou, X., Zhu, S., Zhu, X., Smith, H. O., Gibbs, R. A., Myers, E. W., Rubin, G. M. and Venter, J. C. ( 2000). The genome sequence of Drosophila melanogaster. Science 287, 21852195.Google Scholar
Agüero, F., Abdellah, K. B., Tekiel, V., Sanchez, D. O. and Gonzalez, A. ( 2004). Generation and analysis of expressed sequence tags from Trypanosoma cruzi trypomastigote and amastigote cDNA libraries. Molecular and Biochemical Parasitology 136, 221225.CrossRefGoogle Scholar
Altschul, S. F., Gish, W., Miller, W., Myers, E. W. and Lipman, D. J. ( 1990). Basic local alignment search tool. The Journal of Molecular Biology 215, 403410.CrossRefGoogle Scholar
Anderson, S. K., Gallinger, S., Roder, J., Frey, J., Young, H. A. and Ortaldo, J. R. ( 1993). A cyclophilin-related protein involved in the function of natural killer cells. Proceedings of the National Academy of Sciences USA 90, 542546.CrossRefGoogle Scholar
Atwood, J. A. I., Weatherly, D. B., Minning, T. A., Bundy, B., Cavola, C., Opperdoes, F. R., Orlando, R. and Tarleton, R. L. ( 2005). The Trypanosoma cruzi Proteome. Science 309, 473476.CrossRefGoogle Scholar
Belfiore, M., Pugnale, P., Saudan, Z. and Puoti, A. ( 2004). Roles of the C. elegans cyclophilin-like protein MOG-6 in MEP-1 binding and germline fates. Development 131, 29352945.Google Scholar
Bergsma, D. J., Eder, C., Gross, M., Kersten, H., Sylvester, D., Appelbaum, E., Cusimano, D., Livi, G. P., McLaughlin, M. M., Kasyan, K., Porter, T. G., Silverman, C., Dunningtong, D., Hand, A., Prichett, W. P., Bossard, M. J., Brandt, M. and Levy, M. A. ( 1991). The cyclophilin multigene family of peptidyl-prolyl isomerases. Characterization of three separate human isoforms. The Journal of Biological Chemistry 266, 2320423214.Google Scholar
Bourquin, J. P., Stagljar, I., Meier, P., Moosmann, P., Silke, J., Baechi, T., Georgiev, O. and Schaffner, W. ( 1997). A serine/arginine-rich nuclear matrix cyclophilin interacts with the C-terminal domain of RNA polymerase II. Nucleic Acids Research 25, 20552061.CrossRefGoogle Scholar
Bua, J., Aslund, L., Pereyra, N., Garcia, G. A., Bontempi, E. J. and Ruiz, A. M. ( 2001). Characterisation of a cyclophilin isoform in Trypanosoma cruzi. FEMS Microbiology Letters 200, 4347.CrossRefGoogle Scholar
Bua, J., Ruiz, A. M., Potenza, M. and Fichera, L. E. ( 2004). In vitro anti-parasitic activity of Cyclosporin A analogs on Trypanosoma cruzi. Bioorganic and Medicinal Chemistry Letters 14, 46334637.CrossRefGoogle Scholar
Chomczynski, P. and Sacchi, N. ( 1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162, 156159.CrossRefGoogle Scholar
Colley, N. J., Baker, E. K., Stamnes, M. A. and Zuker, C. S. ( 1991). The cyclophilin homolog ninaA is required in the secretory pathway. Cell 67, 255263.CrossRefGoogle Scholar
Dolinski, K., Muir, S., Cardenas, M. and Heitman, J. ( 1997). All cyclophilins and FK506 binding proteins are, individually and collectively, dispensable for viability in Saccharomyces cerevisiae. Proceedings of the National Academy of Sciences, USA 94, 1309313098.CrossRefGoogle Scholar
Edgar, K. A., Belvin, M., Parks, A. L., Whittaker, K., Mahoney, M. B., Nicoll, M., Park, C. C., Winter, C. G., Chen, F., Lickteig, K., Ahmad, F., Esengil, H., Lorenzi, M. V., Norton, A., Rupnow, B. A., Shayesteh, L., Tabios, M., Young, L. M., Carroll, P. M., Kopczynski, C., Plowman, G. D., Friedman, L. S. and Francis-Lang, H. L. ( 2005) Synthetic lethality of retinoblastoma mutant cells in the Drosophila eye by mutation of a novel peptidyl prolyl isomerase gene. Genetics 170, 161171.CrossRefGoogle Scholar
El-Sayed, N. M., Myler, P. J., Bartholomeu, D. C., Nilsson, D., Aggarwal, G., Tran, A. N., Ghedin, E., Worthey, E. A., Delcher, A. L., Blandin, G., Westenberger, S. J., Caler, E., Cerqueira, G. C., Branche, C., Haas, B., Anupama, A., Arner, E., Aslund, L., Attipoe, P., Bontempi, E., Bringaud, F., Burton, P., Cadag, E., Campbell, D. A., Carrington, M., Crabtree, J., Darban, H., Da Silveira, J. F., De Jong, P., Edwards, K., Englund, P. T., Fazelina, G., Feldblyum, T., Ferella, M., Frasch, A. C., Gull, K., Horn, D., Hou, L., Huang, Y., Kindlund, E., Klingbeil, M., Kluge, S., Koo, H., Lacerda, D., Levin, M. J., Lorenzi, H., Louie, T., Machado, C. R., McCulloch, R., McKenna, A., Mizuno, Y., Mottram, J. C. J., Nelson, S., Ochaya, S., Osoegawa, K., Pai, G., Parsons, M., Pentony, M., Pettersson, U., Pop, M., Ramirez, J. L., Rinta, J., Robertson, L., Salzberg, S. L., Sanchez, D. O., Seyler, A., Sharma, R., Shetty, J., Simpson, A. J., Sisk, E., Tammi, M. T., Tarleton, R., Teixeira, S., Van Aken, S., Vogt, C., Ward, P. N., Wickstead, B., Wortman, J., White, O., Fraser, C. M., Stuart, K. D. and Andersson, B. ( 2005). The genome sequence of Trypanosoma cruzi, etiologic agent of Chagas disease. Science 309, 409415.CrossRefGoogle Scholar
Fischer, G., Wittmann-Liebold, B., Lang, K., Kiefhaber, T. and Schmid, F. X. ( 1989). Cyclophilin and peptidyl-prolyl cis-trans isomerase are probably identical proteins. Nature, London 337, 476478.CrossRefGoogle Scholar
Galagan, J. E., Calvo, S. E., Borkovich, K. A., Selker, E. U., Read, N. D., Jaffe, D., Fitzhugh, W., Ma, L. J., Smirnov, S., Purcell, S., Rehman, B., Elkins, T., Engels, R., Wang, S., Nielsen, C. B., Butler, J., Endrizzi, M., Qui, D., Ianakiev, P., Bell-Pedersen, D., Nelson, M. A., Werner-Washburne, M., Selitrennikoff, C. P., Kinsey, J. A., Braun, E. L., Zelter, A., Schulte, U., Kothe, G. O., Jedd, G., Mewes, W., Staben, C., Marcotte, E., Greenberg, D., Roy, A., Foley, K., Naylor, J., Stange-Thomann, N., Barrett, R., Gnerre, S., Kamal, M., Kamvysselis, M., Mauceli, E., Bielke, C., Rudd, S., Frishman, D., Krystofova, S., Rasmussen, C., Metzenberg, R. L., Perkins, D. D., Kroken, S., Cogoni, C., Macino, G., Catcheside, D., Li, W., Pratt, R. J., Osmani, S. A., Desouza, C. P., Glass, L., Orbach, M. J., Berglund, J. A., Voelker, R., Yarden, O., Plamann, M., Seiler, S., Dunlap, J., Radford, A., Aramayo, R., Natvig, D. O., Alex, L. A., Mannhaupt, G., Ebbole, D. J., Freitag, M., Paulsen, I., Sachs, M. S., Lander, E. S., Nusbaum, C. and Birren, B. ( 2003). The genome sequence of the filamentous fungus Neurospora crassa. Nature 422, 859868.CrossRefGoogle Scholar
Galat, A. ( 1999). Variations of sequences and amino acid compositions of proteins that sustain their biological functions: an analysis of the cyclophilin family of proteins. Archives of Biochemistry and Biophysics 371, 149162.CrossRefGoogle Scholar
Galat, A. ( 2003). Peptidylprolyl cis/trans isomerases (immunophilins): biological diversity–targets–functions. Current Topics in Medicinal Chemistry 3, 13151347.CrossRefGoogle Scholar
Galat, A. ( 2004). Function-dependent clustering of orthologues and paralogues of cyclophilins. PROTEINS, Structure, Function and Bioinformatics 56, 808820.CrossRefGoogle Scholar
Gardner, M. J., Hall, N., Fung, E., White, O., Berriman, M., Hyman, R. W., Carlton, J. M., Pain, A., Nelson, K. E., Bowman, S., Paulsen, I. T., James, K., Eisen, J. A., Rutherford, K., Salzberg, S. L., Craig, A., Kyes, S., Chan, M. S., Nene, V., Shallom, S. J., Suh, B., Peterson, J., Angiuoli, S., Pertea, M., Allen, J., Selengut, J., Haft, D., Mather, M. W., Vaidya, A. B., Martin, D. M., Fairlamb, A. H., Fraunholz, M. J., Roos, D. S., Ralph, S. A., McFadden, G. I., Cummings, L. M., Subramanian, G. M., Mungall, C., Venter, J. C., Carucci, D. J., Hoffman, S. L., Newbold, C., Davis, R. W., Fraser, C. M. and Barrell, B. ( 2002). Genome sequence of the human malaria parasite Plasmodium falciparum. Nature, London 419, 498511.CrossRefGoogle Scholar
Handschumacher, R. E., Harding, M. W., Rice, J., Drugge, R. J. and Speicher, D. W. ( 1984). Cyclophilin: a specific cytosolic binding protein for cyclosporin A. Science 226, 544547.CrossRefGoogle Scholar
Harris, T. W., Lee, R., Schwarz, E., Bradnam, K., Lawson, D., Chen, W., Blasier, D., Kenny, E., Cunningham, F., Kishore, R., Chan, J., Muller, H. M., Petcherski, A., Thorisson, G., Day, A., Bieri, T., Rogers, A., Chen, C. K., Spieth, J., Sternberg, P., Durbin, R. and Stein, L. D. ( 2003). WormBase: a cross-species database for comparative genomics. Nucleic Acids Research 31, 133137.CrossRefGoogle Scholar
Ho, S., Clipstone, N., Timmermann, L., Northrop, J., Graef, I., Fiorentino, D., Nourse, J. and Crabtree, G. R. ( 1996). The mechanism of action of cyclosporin A and FK506. Clinical Immunology and Immunopathology 80, S40S45.CrossRefGoogle Scholar
Hoffmann, K., Kakalis, L. T., Anderson, K. S., Armitage, I. M. and Handschumacher, R. E. ( 1995). Expression of human cyclophilin-40 and the effect of the His141–>Trp mutation on catalysis and cyclosporin A binding. European Journal of Biochemistry 229, 188193.CrossRefGoogle Scholar
Hong, X., Ma, D. and Carlow, C. K. ( 1998). Cloning, expression and characterization of a new filarial cyclophilin. Molecular and Biochemical Parasitology 91, 353358.CrossRefGoogle Scholar
Ke, H. ( 1992). Similarities and differences between human cyclophilin A and other beta-barrel structures. Structural refinement at 1·63 A resolution. The Journal of Molecular Biology 228, 539550.Google Scholar
Kieffer, L. J., Seng, T. W., Li, W., Osterman, D. G., Handschumacher, R. E. and Bayney, R. M. ( 1993). Cyclophilin-40, a protein with homology to the P59 component of the steroid receptor complex. Cloning of the cDNA and further characterization. The Journal of Biological Chemistry 268, 1230312310.Google Scholar
Klinkert, M. Q., Bugli, F., Cruz, J., Engels, B. and Cioli, D. ( 1996). Sequence conservation of schistosome cyclophilins. Molecular and Biochemical Parasitology 81, 239242.CrossRefGoogle Scholar
Kyte, J. and Doolittle, R. F. ( 1982). A simple method for displaying the hydropathic character of a protein. The Journal of Molecular Biology 157, 105132.CrossRefGoogle Scholar
Laemmli, U. K. ( 1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680685.CrossRefGoogle Scholar
Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., Fitzhugh, W., Funke, R., Gage, D., Harris, K., Heaford, A., Howland, J., Kann, L., Lehoczky, J., Levine, R., McEwan, P., McKernan, K., Meldrim, J., Mesirov, J. P., Miranda, C., Morris, W., Naylor, J., Raymond, C., Rosetti, M., Santos, R., Sheridan, A., Sougnez, C., Stange-Thomann, N., Stojanovic, N., Subramanian, A., Wyman, D., Rogers, J., Sulston, J., Ainscough, R., Beck, S., Bentley, D., Burton, J., Clee, C., Carter, N., Coulson, A., Deadman, R., Deloukas, P., Dunham, A., Dunham, I., Durbin, R., French, L., Grafham, D., Gregory, S., Hubbard, T., Humphray, S., Hunt, A., Jones, M., Lloyd, C., McMurray, A., Matthews, L., Mercer, S., Milne, S., Mullikin, J. C., Mungall, A., Plumb, R., Ross, M., Shownkeen, R., Sims, S., Waterston, R. H., Wilson, R. K., Hillier, L. W., McPherson, J. D., Marra, M. A., Mardis, E. R., Fulton, L. A., Chinwalla, A. T., Pepin, K. H., Gish, W. R., Chissoe, S. L., Wendl, M. C., Delehaunty, K. D., Miner, T. L., Delehaunty, A., Kramer, J. B., Cook, L. L., Fulton, R. S., Johnson, D. L., Minx, P. J., Clifton, S. W., Hawkins, T., Branscomb, E., Predki, P., Richardson, P., Wenning, S., Slezak, T., Doggett, N., Cheng, J. F., Olsen, A., Lucas, S., Elkin, C., Uberbacher, E., Frazier, M., Gibbs, R. A., Muzny, D. M., Scherer, S. E., Bouck, J. B., Sodergren, E. J., Worley, K. C., Rives, C. M., Gorrell, J. H., Metzker, M. L., Naylor, S. L., Kucherlapati, R. S., Nelson, D. L., Weinstock, G. M., Sakaki, Y., Fujiyama, A., Hattori, M., Yada, T., Toyoda, A., Itoh, T., Kawagoe, C., Watanabe, H., Totoki, Y., Taylor, T., Weissenbach, J., Heilig, R., Saurin, W., Artiguenave, F., Brottier, P., Bruls, T., Pelletier, E., Robert, C., Wincker, P., Smith, D. R., Doucette-Stamm, L., Rubenfield, M., Weinstock, K., Lee, H. M., Dubois, J., Rosenthal, A., Platzer, M., Nyakatura, G., Taudien, S., Rump, A., Yang, H., Yu, J., Wang, J., Huang, G., Gu, J., Hood, L., Rowen, L., Madan, A., Qin, S., Davis, R. W., Federspiel, N. A., Abola, A. P., Proctor, M. J., Myers, R. M., Schmutz, J., Dickson, M., Grimwood, J., Cox, D. R., Olson, M. V., Kaul, R., Raymond, C., Shimizu, N., Kawasaki, K., Minoshima, S., Evans, G. A., Athanasiou, M., Schultz, R., Roe, B. A., Chen, F., Pan, H., Ramser, J., Lehrach, H., Reinhardt, R., McCombie, W. R., De La Bastide, M., Dedhia, N., Blocker, H., Hornischer, K., Nordsiek, G., Agarwala, R., Aravind, L., Bailey, J. A., Bateman, A., Batzoglou, S., Birney, E., Bork, P., Brown, D. G., Burge, C. B., Cerutti, L., Chen, H. C., Church, D., Clamp, M., Copley, R. R., Doerks, T., Eddy, S. R., Eichler, E. E., Furey, T. S., Galagan, J., Gilbert, J. G., Harmon, C., Hayashizaki, Y., Haussler, D., Hermjakob, H., Hokamp, K., Jang, W., Johnson, L. S., Jones, T. A., Kasif, S., Kaspryzk, A., Kennedy, S., Kent, W. J., Kitts, P., Koonin, E. V., Korf, I., Kulp, D., Lancet, D., Lowe, T. M., McLysaght, A., Mikkelsen, T., Moran, J. V., Mulder, N., Pollara, V. J., Ponting, C. P., Schuler, G., Schultz, J., Slater, G., Smit, A. F., Stupka, E., Szustakowski, J., Thierry-Mieg, D., Thierry-Mieg, J., Wagner, L., Wallis, J., Wheeler, R., Williams, A., Wolf, Y. I., Wolfe, K. H., Yang, S. P., Yeh, R. F., Collins, F., Guyer, M. S., Peterson, J., Felsenfeld, A., Wetterstrand, K. A., Patrinos, A., Morgan, M. J., De Jong, P., Catanese, J. J., Osoegawa, K., Shizuya, H., Choi, S. and Chen, Y. J. ( 2001). Initial sequencing and analysis of the human genome. Nature 409, 860921.Google Scholar
Liu, J., Farmer, J. D. Jr, Lane, W. S., Friedman, J., Weissman, I. and Schreiber, S. L. ( 1991). Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66, 807815.CrossRefGoogle Scholar
Ma, D., Hong, X., Raghavan, N., Scott, A. L., McCarthy, J. S., Nutman, T. B., Williams, S. A. and Carlow, C. K. ( 1996). A Cyclosporin A-sensitive small molecular weight cyclophilin of filarial parasites. Molecular and Biochemical Parasitology 79, 235241.CrossRefGoogle Scholar
McCabe, R. E., Remington, J. S. and Araujo, F. G. ( 1985). In vivo and in vitro effects of cyclosporin A on Trypanosoma cruzi. The American Journal of Tropical Medicine & Hygiene 34, 861865.CrossRefGoogle Scholar
Mi, H., Kops, O., Zimmermann, E., Jaschke, A. and Tropschug, M. ( 1996). A nuclear RNA-binding cyclophilin in human T cells. FEBS Letters 398, 201205.CrossRefGoogle Scholar
Minning, T. A., Bua, J., Garcia, G. A., McGraw, R. A. and Tarleton, R. L. ( 2003). Microarray profiling of gene expression during trypomastigote to amastigote transition in Trypanosoma cruzi. Molecular and Biochemical Parasitology 131, 5564.CrossRefGoogle Scholar
Nestel, F. P., Colwill, K., Harper, S., Pawson, T. and Anderson, S. K. ( 1996). RS cyclophilins: identification of an NK-TR1-related cyclophilin. Gene 180, 151155.CrossRefGoogle Scholar
Otto, S. P. and Yong, P. ( 2002). The evolution of gene duplicates. Adv. Genetics 46, 451483.CrossRefGoogle Scholar
Ozaki, K., Fujiwara, T., Kawai, A., Shimizu, F., Takami, S., Okuno, S., Takeda, S., Shimada, Y., Nagata, M., Watanabe, T., Takaichi, A., Takahashi, E., Nakamura, Y. and Shin, S. ( 1996). Cloning, expression and chromosomal mapping of a novel cyclophilin-related gene (PPIL1) from human fetal brain. Cytogenetics and Cell Genetics 72, 242245.CrossRefGoogle Scholar
Page, A. P., Kumar, S. and Carlow, C. K. ( 1995). Parasite cyclophilins and antiparasite activity of cyclosporin A. Parasitology Today 11, 385388.CrossRefGoogle Scholar
Page, A. P. and Winter, A. D. ( 1998). A divergent multi-domain cyclophilin is highly conserved between parasitic and free-living nematode species and is important in larval muscle development Molecular and Biochemical Parasitology 95, 215227.Google Scholar
Piras, R., Piras, M. M. and Henriquez, D. ( 1982). The effect of inhibitors of macromolecular biosynthesis on the in vitro infectivity and morphology of Trypanosoma cruzi trypomastigotes. Molecular and Biochemical Parasitology 6, 8392.CrossRefGoogle Scholar
Porcel, B. M., Tran, A. N., Tammi, M., Nyarady, Z., Rydaker, M., Urmenyi, T. P., Rondinelli, E., Pettersson, U., Andersson, B. and Aslund, L. ( 2000). Gene survey of the pathogenic protozoan Trypanosoma cruzi. Genome Research 10, 11031107.CrossRefGoogle Scholar
Roberts, H. C., Sternberg, J. M. and Chappell, L. H. ( 1995). Hymenolepis diminuta and H. microstoma: uptake of cyclosporin A and drug binding to parasite cyclophilins. Parasitology 111, 591597.Google Scholar
Schneider, H., Charara, N., Schmitz, R., Wehrli, S., Mikol, V., Zurini, M. G., Quesniaux, V. F. and Movva, N. R. ( 1994). Human cyclophilin C: primary structure, tissue distribution, and determination of binding specificity for cyclosporins. Biochemistry 33, 82188224.CrossRefGoogle Scholar
Shevchenko, A., Wilm, M., Vorm, O. and Mann, M. ( 1996). Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Analytical Chemistry 68, 850858.CrossRefGoogle Scholar
Takahashi, N., Hayano, T. and Suzuki, M. ( 1989). Peptidyl-prolyl cis-trans isomerase is the cyclosporin A-binding protein cyclophilin. Nature, London 337, 473475.CrossRefGoogle Scholar
Teigelkamp, S., Achsel, T., Mundt, C., Gothel, S. F., Cronshagen, U., Lane, W. S., Marahiel, M. and Luhrmann, R. ( 1998). The 20 kD protein of human [U4/U6.U5] tri-snRNPs is a novel cyclophilin that forms a complex with the U4/U6-specific 60 kD and 90 kD proteins. RNA 4, 127141.Google Scholar
Thompson, J. D., Higgins, D. G. and Gibson, T. J. ( 1994). CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Research 22, 46734680.CrossRefGoogle Scholar
Tomlinson, S., Vandekerckhove, F., Frevert, U. and Nussenzweig, V. ( 1995). The induction of Trypanosoma cruzi trypomastigote to amastigote transformation by low pH. Parasitology 110, 547554.CrossRefGoogle Scholar
Urbina, J. A. and Docampo, R. ( 2003). Specific chemotherapy of Chagas disease: controversies and advances. Trends in Parasitology 19, 495501.CrossRefGoogle Scholar
Urmenyi, T. P., Bonaldo, M. F., Soares, M. B. and Rondinelli, E. ( 1999). Construction of a normalized cDNA library for the Trypanosoma cruzi genome project. The Journal of Eukaryotic Microbiology 46, 542544.CrossRefGoogle Scholar
Venter, J. C., Adams, M. D., Myers, E. W., Li, P. W., Mural, R. J., Sutton, G. G., Smith, H. O., Yandell, M., Evans, C. A., Holt, R. A., Gocayne, J. D., Amanatides, P., Ballew, R. M., Huson, D. H., Wortman, J. R., Zhang, Q., Kodira, C. D., Zheng, X. H., Chen, L., Skupski, M., Subramanian, G., Thomas, P. D., Zhang, J., Gabor Miklos, G. L., Nelson, C., Broder, S., Clark, A. G., Nadeau, J., McKusick, V. A., Zinder, N., Levine, A. J., Roberts, R. J., Simon, M., Slayman, C., Hunkapiller, M., Bolanos, R., Delcher, A., Dew, I., Fasulo, D., Flanigan, M., Florea, L., Halpern, A., Hannenhalli, S., Kravitz, S., Levy, S., Mobarry, C., Reinert, K., Remington, K., Abu-Threideh, J., Beasley, E., Biddick, K., Bonazzi, V., Brandon, R., Cargill, M., Chandramouliswaran, I., Charlab, R., Chaturvedi, K., Deng, Z., Di Francesco, V., Dunn, P., Eilbeck, K., Evangelista, C., Gabrielian, A. E., Gan, W., Ge, W., Gong, F., Gu, Z., Guan, P., Heiman, T. J., Higgins, M. E., Ji, R. R., Ke, Z., Ketchum, K. A., Lai, Z., Lei, Y., Li, Z., Li, J., Liang, Y., Lin, X., Lu, F., Merkulov, G. V., Milshina, N., Moore, H. M., Naik, A. K., Narayan, V. A., Neelam, B., Nusskern, D., Rusch, D. B., Salzberg, S., Shao, W., Shue, B., Sun, J., Wang, Z., Wang, A., Wang, X., Wang, J., Wei, M., Wides, R., Xiao, C., Yan, C., Yao, A., Ye, J., Zhan, M., Zhang, W., Zhang, H., Zhao, Q., Zheng, L., Zhong, F., Zhong, W., Zhu, S., Zhao, S., Gilbert, D., Baumhueter, S., Spier, G., Carter, C., Cravchik, A., Woodage, T., Ali, F., An, H., Awe, A., Baldwin, D., Baden, H., Barnstead, M., Barrow, I., Beeson, K., Busam, D., Carver, A., Center, A., Cheng, M. L., Curry, L., Danaher, S., Davenport, L., Desilets, R., Dietz, S., Dodson, K., Doup, L., Ferriera, S., Garg, N., Gluecksmann, A., Hart, B., Haynes, J., Haynes, C., Heiner, C., Hladun, S., Hostin, D., Houck, J., Howland, T., Ibegwam, C., Johnson, J., Kalush, F., Kline, L., Koduru, S., Love, A., Mann, F., May, D., McCawley, S., McIntosh, T., McMullen, I., Moy, M., Moy, L., Murphy, B., Nelson, K., Pfannkoch, C., Pratts, E., Puri, V., Qureshi, H., Reardon, M., Rodriguez, R., Rogers, Y. H., Romblad, D., Ruhfel, B., Scott, R., Sitter, C., Smallwood, M., Stewart, E., Strong, R., Suh, E., Thomas, R., Tint, N. N., Tse, S., Vech, C., Wang, G., Wetter, J., Williams, S., Williams, M., Windsor, S., Winn-Deen, E., Wolfe, K., Zaveri, J., Zaveri, K., Abril, J. F., Guigo, R., Campbell, M. J., Sjolander, K. V., Karlak, B., Kejariwal, A., Mi, H., Lazareva, B., Hatton, T., Narechania, A., Diemer, K., Muruganujan, A., Guo, N., Sato, S., Bafna, V., Istrail, S., Lippert, R., Schwartz, R., Walenz, B., Yooseph, S., Allen, D., Basu, A., Baxendale, J., Blick, L., Caminha, M., Carnes-Stine, J., Caulk, P., Chiang, Y. H., Coyne, M., Dahlke, C., Mays, A., Dombroski, M., Donnelly, M., Ely, D., Esparham, S., Fosler, C., Gire, H., Glanowski, S., Glasser, K., Glodek, A., Gorokhov, M., Graham, K., Gropman, B., Harris, M., Heil, J., Henderson, S., Hoover, J., Jennings, D., Jordan, C., Jordan, J., Kasha, J., Kagan, L., Kraft, C., Levitsky, A., Lewis, M., Liu, X., Lopez, J., Ma, D., Majoros, W., McDaniel, J., Murphy, S., Newman, M., Nguyen, T., Nguyen, N., Nodell, M., Pan, S., Peck, J., Peterson, M., Rowe, W., Sanders, R., Scott, J., Simpson, M., Smith, T., Sprague, A., Stockwell, T., Turner, R., Venter, E., Wang, M., Wen, M., Wu, D., Wu, M., Xia, A., Zandieh, A. and Zhu, X. ( 2001). The sequence of the human genome. Science 291, 13041351.Google Scholar
Verdun, R. E., Di Paolo, N., Urmenyi, T. P., Rondinelli, E., Frasch, A. C. and Sanchez, D. O. ( 1998). Gene discovery through expressed sequence Tag sequencing in Trypanosoma cruzi. Infection and Immunity 66, 53935398.Google Scholar
Wang, B. B., Hayenga, K. J., Payan, D. G. and Fisher, J. M. ( 1996). Identification of a nuclear-specific cyclophilin which interacts with the proteinase inhibitor eglin c. Biochemistry Journal 314, 313319.CrossRefGoogle Scholar
Wheeler, D. L., Church, D. M., Edgar, R., Federhen, S., Helmberg, W., Madden, T. L., Pontius, J. U., Schuler, G. D., Schriml, L. M., Sequeira, E., Suzek, T. O., Tatusova, T. A. and Wagner, L. ( 2004). Database resources of the National Center for Biotechnology Information: update. Nucleic Acids Research 32, D3540.CrossRefGoogle Scholar
Wu, C. H., Yeh, L. S., Huan, G. H., Arminski, L., Castro-Alvear, J., Chen, Y., Hu, Z., Kourtesis, P., Ledley, R. S., Suzek, B. E., Vinayaka, C. R., Zhang, J. and Barker, W. C. ( 2003). The Protein Information Resource. Nucleic Acids Research 31, 345347.CrossRefGoogle Scholar
Yokoyama, N., Hayashi, N., Seki, T., Pante, N., Ohba, T., Nishii, K., Kuma, K., Hayashida, T., Miyata, T., Aebi, U., Fukui, M. and Nishimoto, T. ( 1995). A giant nucleopore protein that binds Ran/TC4. Nature, London 376, 184188.CrossRefGoogle Scholar
Zhou, Z., Ying, K., Dai, J., Tang, R., Wang, W., Huang, Y., Zhao, W., Xie, Y. and Mao, Y. ( 2001). Molecular cloning and characterization of a novel peptidylprolyl isomerase (cyclophilin)-like gene (PPIL3) from human fetal brain. Cytogenetics and Cell Genetics 92, 231236.CrossRefGoogle Scholar
Zydowsky, L. D., Etzkorn, F. A., Chang, H. Y., Ferguson, S. B., Stolz, L. A., Ho, S. I. and Walsh, C. T. ( 1992). Active site mutants of human cyclophilin A separate peptidyl-prolyl isomerase activity from cyclosporin A binding and calcineurin inhibition. Protein Science 1, 10921099.CrossRefGoogle Scholar