Skip to main content
×
×
Home

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

  • M. POTENZA (a1), A. GALAT (a2), T. A. MINNING (a3), A. M. RUIZ (a1), R. DURAN (a4), R. L. TARLETON (a3), M. MARÍN (a5), L. E. FICHERA (a1) and J. BÚA (a1)...
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.

Copyright
Corresponding author
Instituto Nacional de Parasitología. Av. Paseo Colón 568 (1063) Buenos Aires, Argentina. Tel: +54 11 4331 4019. Fax: +54 11 4331 7142. E-mail: jacbua@yahoo.com
References
Hide All

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.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Chomczynski, P. and Sacchi, N. ( 1987). Single-step method of RNA isolation by acid guanidinium thiocyanate-phenol-chloroform extraction. Analytical Biochemistry 162, 156159.
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.
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.
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.
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.
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.
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.
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.
Galat, A. ( 2003). Peptidylprolyl cis/trans isomerases (immunophilins): biological diversity–targets–functions. Current Topics in Medicinal Chemistry 3, 13151347.
Galat, A. ( 2004). Function-dependent clustering of orthologues and paralogues of cyclophilins. PROTEINS, Structure, Function and Bioinformatics 56, 808820.
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.
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.
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.
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.
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.
Hong, X., Ma, D. and Carlow, C. K. ( 1998). Cloning, expression and characterization of a new filarial cyclophilin. Molecular and Biochemical Parasitology 91, 353358.
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.
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.
Klinkert, M. Q., Bugli, F., Cruz, J., Engels, B. and Cioli, D. ( 1996). Sequence conservation of schistosome cyclophilins. Molecular and Biochemical Parasitology 81, 239242.
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.
Laemmli, U. K. ( 1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680685.
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.
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.
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.
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.
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.
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.
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.
Otto, S. P. and Yong, P. ( 2002). The evolution of gene duplicates. Adv. Genetics 46, 451483.
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.
Page, A. P., Kumar, S. and Carlow, C. K. ( 1995). Parasite cyclophilins and antiparasite activity of cyclosporin A. Parasitology Today 11, 385388.
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.
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.
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.
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.
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.
Shevchenko, A., Wilm, M., Vorm, O. and Mann, M. ( 1996). Mass spectrometric sequencing of proteins silver-stained polyacrylamide gels. Analytical Chemistry 68, 850858.
Takahashi, N., Hayano, T. and Suzuki, M. ( 1989). Peptidyl-prolyl cis-trans isomerase is the cyclosporin A-binding protein cyclophilin. Nature, London 337, 473475.
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.
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.
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.
Urbina, J. A. and Docampo, R. ( 2003). Specific chemotherapy of Chagas disease: controversies and advances. Trends in Parasitology 19, 495501.
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.
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.
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.
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.
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.
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.
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.
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.
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.
Recommend this journal

Email your librarian or administrator to recommend adding this journal to your organisation's collection.

Parasitology
  • ISSN: 0031-1820
  • EISSN: 1469-8161
  • URL: /core/journals/parasitology
Please enter your name
Please enter a valid email address
Who would you like to send this to? *
×

Keywords:

Metrics

Full text views

Total number of HTML views: 1
Total number of PDF views: 10 *
Loading metrics...

Abstract views

Total abstract views: 90 *
Loading metrics...

* Views captured on Cambridge Core between September 2016 - 19th January 2018. This data will be updated every 24 hours.