Overexpression, purification and assessment of cyclosporin binding of a family of cyclophilins and cyclophilin-like proteins of the human malarial parasite Plasmodium falciparum

Protein Expression and Purification

Volumn 78, Issue 2, 2011, Pages 225-234

  Marín Menéndez, Alejandro ^a   Bell, Angus ^a  

^a Moyne Institute of Preventive Medicine   (Ireland)

Author keywords

Cyclophilin; Cyclosporin; Hexahistidine tag; Malaria; Metal chelate affinity chromatography; Plasmodium falciparum; Thermal melt

Indexed keywords

CYCLOPHILIN; CYCLOSPORIN; HIS HIS HIS HIS HIS HIS; HIS-HIS-HIS-HIS-HIS-HIS; HISTIDINE; HYBRID PROTEIN; OLIGOPEPTIDE; PROTOZOAL PROTEIN;

AFFINITY CHROMATOGRAPHY; ARTICLE; BIOSYNTHESIS; CHEMISTRY; ESCHERICHIA COLI; GENETICS; HUMAN; METABOLISM; PHYLOGENY; PLASMODIUM FALCIPARUM; POLYACRYLAMIDE GEL ELECTROPHORESIS; PROTEIN BINDING; PROTEIN STABILITY; SEQUENCE ALIGNMENT; SITE DIRECTED MUTAGENESIS; TEMPERATURE;

CHROMATOGRAPHY, AFFINITY; CYCLOPHILINS; CYCLOSPORINE; ELECTROPHORESIS, POLYACRYLAMIDE GEL; ESCHERICHIA COLI; HISTIDINE; HUMANS; MUTAGENESIS, SITE-DIRECTED; OLIGOPEPTIDES; PHYLOGENY; PLASMODIUM FALCIPARUM; PROTEIN BINDING; PROTEIN STABILITY; PROTOZOAN PROTEINS; RECOMBINANT FUSION PROTEINS; SEQUENCE ALIGNMENT; TEMPERATURE;

ANIMALIA; ESCHERICHIA COLI; PLASMODIUM FALCIPARUM;

EID: 79958768895     PISSN: 10465928     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.pep.2011.04.012     Document Type: Article

References (60)

1. WHO, Annual Report 2010, World Health Organization, Geneva, 2010.
2. S.I. Hay, C.A. Guerra, P.W. Gething, A.P. Patil, A.J. Tatem, A.M. Noor, C.W. Kabaria, B.H. Manh, I.R. Elyazar, S. Brooker, D.L. Smith, R.A. Moyeed, R.W. Snow, A world malaria map: Plasmodium falciparum endemicity in 2007, PLoS Med. 6 (2009) e1000048.
3. L. Tilley, T.M.E. Davis, P.G. Bray, Prospects for the treatment of drug-resistant malaria parasites, Future Microbiol. 1 (2006) 127-141.
4. I. Yeh, R.B. Altman, Drug targets for Plasmodium falciparum: a post-genomic review/survey, Mini Rev. Med. Chem. 6 (2006) 177-202.
5. L.M. Birkholtz, G. Blatch, T.L. Coetzer, H.C. Hoppe, E. Human, E.J. Morris, Z. Ngcete, L. Oldfield, R. Roth, A. Shonhai, L. Stephens, A.I. Louw, Heterologous expression of plasmodial proteins for structural studies, functional annotation, Malar. J. 7 (2008) 179.
6. E.A. Gowda, E.A. Davidson, Protein glycosylation in the malaria parasite, Parasitol. Today 15 (2009) 147-152.
7. L. Aravind, L.M. Iyer, T.E. Wellems, L.H. Miller, Plasmodium biology: genomic gleanings, Cell 115 (2003) 771-785. (Pubitemid 38058491)
8. S. Buratowski, Transcription. Gene expression - where to start?, Science 19 (2008) 1804-1805
9. C. Mehlin, E. Boni, F.S. Buckner, L. Engel, T. Feist, M.H. Gelb, L. Haji, D. Kim, C. Liu, N. Mueller, P.J. Myler, J.T. Reddy, J.N. Sampson, E. Subramanian, W.C. Van Voorhis, E. Worthey, F. Zucker, W.G. Hol, Heterologous expression of proteins from Plasmodium falciparum: results from 1000 genes, Mol. Biochem. Parasitol. 148 (2006) 144-160. (Pubitemid 43964865)
10. M. Uhlen, G. Forsberg, T. Moks, M. Hartmanis, B. Nilsson, Fusion proteins in biotechnology, Curr. Opin. Biotechnol. 3 (1992) 363-369.
11. J. Porath, Immobilized metal ion affinity chromatography, Protein Expr. Purif. 3 (1992) 263-281.
12. M. Carson, D.H. Johnson, H. McDonald, C. Brouillette, L.J. Delucas, His-tag impact on structure, Acta Crystallogr. D: Biol. Crystallogr. 63 (2007) 295-301. (Pubitemid 46438522)
13. G.A. Cole, S.P. Nickell, F. Mokhtarian, L.W. Scheibel, Effects of cyclosporin on experimental infections, Transplant. Proc. 15 (1983) 3013-3018.
14. A. Bell, H.C. Roberts, L.H. Chappell, The antiparasite effects of cyclosporin A: possible drug targets and clinical applications, Gen. Pharmacol. 27 (1996) 963-971.
15. A. Bell, Antimalarial peptides: the long and the short of it, Curr. Pharm. Des., in press.
16. A. Bell, B. Wernli, R.M. Franklin, Roles of peptidyl-prolyl cis-trans isomerase and calcineurin in the mechanisms of antimalarial action of cyclosporin A, FK506, and rapamycin, Biochem. Pharmacol. 48 (1994) 495-503. (Pubitemid 24257012)
17. P.S. Mattila, The actions of cyclosporin A and FK506 on T-lymphocyte activation, Biochem. Soc. Trans. 24 (1996) 45-49. (Pubitemid 26052287)
18. A. Galat, Function-dependent clustering of orthologues and paralogues of cyclophilins, Proteins 56 (2004) 808-820. (Pubitemid 39063322)
19. C.S. Gavigan, S.P. Kiely, J. Hirtzlin, A. Bell, Cyclosporin-binding proteins of Plasmodium falciparum, Int. J. Parasitol. 33 (2003) 987-996.
20. A. Bell, P. Monaghan, A.P. Page, 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. (Pubitemid 43376108)
21. J. Hirtzlin, P.M. Farber, R.M. Franklin, A. Bell, Molecular and biochemical characterization of a Plasmodium falciparum cyclophilin containing a cleavable signal sequence, Eur. J. Biochem. 232 (1995) 765-772.
22. M. Berriman, A.H. Fairlamb, Detailed characterization of a cyclophilin from the human malaria parasite Plasmodium falciparum, Biochem. J. 334 (1998) 437-445. (Pubitemid 28448588)
23. W. Trager, J.B. Jensen, Human malaria parasites in continuous culture, Science 193 (1976) 673-675.
24. A. Zuckerman, D. Spira, J. Hamburger, A procedure for the harvesting of mammalian plasmodia, Bull. World Health Organ. 37 (1967) 431-436.
25. K. Moll, I. Ljungström, H. Perlmann, A. Scherf, M. Wahlgren, Methods in Malaria Research, fifth ed., 2008.
26. U.K. Laemmli, Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227 (1970) 680-685.
27. M.W. Pantoliano, E.C. Petrella, J.D. Kwasnoski, V.S. Lobanov, J. Myslik, E. Graf, T. Carver, E. Asel, B.A. Springer, P. Lane, F.R. Salemme, High-density miniaturized thermal shift assays as a general strategy for drug discovery, J. Biomol. Screen. 6 (2001) 429-440.
28. A. Galat, Peptidylprolyl cis/trans isomerases (immunophilins): biological diversity-targets-functions, Curr. Top. Med. Chem. 3 (2003) 1315-1347.
29. PlasmoDB version 7.1. (December 2010).
30. National Center for Biotechnology Information. (December 2010).
31. G.R. Reddy, Cloning and characterization of a Plasmodium falciparum cyclophilin gene that is stage-specifically expressed, Mol. Biochem. Parasitol. 73 (1995) 111-121.
32. L.A. Kelley, M.J. Sternberg, Protein structure prediction on the Web: a case study using the Phyre server, Nat. Protoc. 4 (2009) 363-371.
33. A. Wu, A. Craig, Comparative proteomic analysis of metabolically labelled proteins from Plasmodium falciparum isolates with different adhesion properties, Malar. J. 5 (2006) 67.
34. A.B. Vaidya, M.W. Mather, Mitochondrial evolution and functions in malaria parasites, Annu. Rev. Microbiol. 63 (2009) 249-267.
35. M.G. Claros, P. Vincens, Computational method to predict mitochondrially imported proteins and their targeting sequences, Eur. J. Biochem. 241 (1996) 779-786.
36. A. Bender, G.G. Van Dooren, S.A. Ralph, G.I. McFadden, G. Schneider, Properties and prediction of mitochondrial transit peptides from Plasmodium falciparum, Mol. Biochem. Parasitol. 132 (2003) 59-66. (Pubitemid 37352901)
37. R. Verma, G.C. Varshney, G.P. Raghava, Prediction of mitochondrial proteins of malaria parasite using split amino acid composition and PSSM profile, Amino Acids 39 (2010) 101-110.
38. B.J. Foth, S.A. Ralph, C.J. Tonkin, N.S. Struck, M. Fraunholz, D.S. Roos, A.F. Cowman, G.I. McFadden, Dissecting apicoplast targeting in the malaria parasite Plasmodium falciparum, Science 299 (2003) 705-708. (Pubitemid 36159484)
39. M. Rashid, S. Saha, G.P. Raghava, Support Vector Machine-based method for predicting subcellular localization of mycobacterial proteins using evolutionary information and motifs, BMC Bioinf. 8 (2007) 337.
40. M. Marti, R.T. Good, M. Rug, E. Knuepfer, A.F. Cowman, Targeting malaria virulence and remodeling proteins to the host erythrocyte, Science 306 (2004) 1930-1933. (Pubitemid 39627856)
41. R. Vincentelli, C. Bignon, A. Gruez, S. Canaan, G. Sulzenbacher, M. Tegoni, V. Campanacci, C. Cambillau, Medium-scale structural genomics: strategies for protein expression and crystallization, Acc. Chem. Res. 36 (2003) 165-172.
42. G.J. Crowther, P. He, P.P. Rodenbough, A.P. Thomas, K.V. Kovzun, D.J. Leibly, J. Bhandari, L.J. Castaneda, W.G. Hol, M.H. Gelb, A.J. Napuli, W.C. Van Voorhis, Use of thermal melt curves to assess the quality of enzyme preparations, Anal. Biochem. 399 (2010) 268-275.
43. J.R. Lakowicz, S. Keating, Binding of an indole derivative to micelles as quantified by phase-sensitive detection of fluorescence, J. Biol. Chem. 258 (1983) 5519-5524.
44. M.J. Bossard, P.L. Koser, M. Brandt, D.J. Bergsma, M. Levy, A single Trp121 to Ala121 mutation in human cyclophilin alters cyclosporin A affinity and peptidyl-prolyl isomerase activity, Biochem. Biophys. Res. Commun. 176 (1991) 1142-1148.
45. T.J. Pemberton, Identification and comparative analysis of sixteen fungal peptidyl-prolyl cis/trans isomerase repertoires, BMC Genom. 7 (2006) 244.
46. P. Monaghan, A. Bell, A Plasmodium falciparum FK506-binding protein (FKBP) with peptidyl-prolyl cis-trans isomerase and chaperone activities, Mol. Biochem. Parasitol. 139 (2005) 185-195. (Pubitemid 40128214)
47. R. Kumar, B. Adams, A. Musiyenko, O. Shulyayeva, S. Barik, The FK506-binding protein of the malaria parasite, Plasmodium falciparum, is a FK506-sensitive chaperone with FK506-independent calcineurin-inhibitory activity, Mol. Biochem. Parasitol. 141 (2005) 163-173.
48. J. Krucken, G. Greif, G. Von Samson-Himmelstjerna, In silico analysis of the cyclophilin repertoire of apicomplexan parasites, Parasit. Vectors 2 (2009) 27.
49. D. Christendat, A. Yee, A. Dharamsi, Y. Kluger, M. Gerstein, C.H. Arrowsmith, A.M. Edwards, Structural proteomics: prospects for high throughput sample preparation, Prog. Biophys. Mol. Biol. 73 (2000) 339-345.
50. E. Dobrovetsky, M.L. Lu, R. Andorn-Broza, G. Khutoreskaya, J.E. Bray, A. Savchenko, C.H. Arrowsmith, A.M. Edwards, C.M. Koth, High-throughput production of prokaryotic membrane proteins, J. Struct. Funct. Genom. 6 (2005) 33-50. (Pubitemid 40898074)
51. J.R. Sayers, H.P. Price, P.G. Fallon, M.J. Doenhoff, AGA/AGG codon usage in parasites: implications for gene expression in Escherichia coli, Parasitol. Today 11 (1995) 345-346.
52. X. Wu, H. Jornvall, K.D. Berndt, U. Oppermann, Codon optimization reveals critical factors for high level expression of two rare codon genes in Escherichia coli: RNA stability and secondary structure but not tRNA abundance, Biochem. Biophys. Res. Commun. 313 (2004) 89-96. (Pubitemid 37524029)
53. J.C. Aguiar, J. Labaer, P.L. Blair, V.Y. Shamailova, M. Koundinya, J.A. Russell, F. Huang, W. Mar, R.M. Anthony, A. Witney, S.R. Caruana, L. Brizuela, J.B. Sacci, S.L. Hoffman, D.J. Carucci, High-throughput generation of P. falciparum functional molecules by recombinational cloning, Genome Res. 14 (2004) 2076-2082. (Pubitemid 39440189)
54. G.J. Crowther, A.J. Napuli, A.P. Thomas, D.J. Chung, K.V. Kovzun, D.J. Leibly, L.J. Castaneda, J. Bhandari, C.J. Damman, R. Hui, W.G. Hol, F.S. Buckner, C.L. Verlinde, Z. Zhang, E. Fan, W.C. Van Voorhis, Buffer optimization of thermal melt assays of Plasmodium proteins for detection of small-molecule ligands, J. Biomol. Screen. 14 (2009) 700-707.
55. M. Vedadi, F.H. Niesen, A. Allali-Hassani, O.Y. Fedorov, P.J.J.R. Finerty, G.A. Wasney, R. Yeung, C. Arrowsmith, L.J. Ball, H. Berglund, R. Hui, B.D. Marsden, P. Nordlund, M. Sundstrom, J. Weigelt, A.M. Edwards, Chemical screening methods to identify ligands that promote protein stability, protein crystallization, and structure determination, Proc. Natl. Acad. Sci. USA 103 (2006) 15835-15840.
56. W.A. Guiguemde, A.A. Shelat, D. Bouck, S. Duffy, G.J. Crowther, P.H. Davis, D.C. Smithson, M. Connelly, J. Clark, F. Zhu, M.B. Jiménez- Díaz, M.S. Martinez, E.B. Wilson, A.K. Tripathi, J. Gut, E.R. Sharlow, I. Bathurst, F.E. Mazouni, J.W. Fowble, I. Forquer, P.L. McGinley, S. Castro, I. Angulo-Barturen, S. Ferrer, P.J. Rosenthal, J.L. DeRisi, D.J. Sullivan, J.S. Lazo, D.S. Roos, M.K. Riscoe, M.A. Phillips, P.K. Rathod, W.C. Van Voorhis, V.M. Avery, R.K. Guy, Chemical genetics of Plasmodium falciparum, Nature 465 (2010) 311-315.
57. S. Barik, Immunophilins: for the love of proteins, Cell. Mol. Life Sci. 63 (2006) 2889-2900. (Pubitemid 46072296)
58. P. Acharya, R. Kumar, U. Tatu, Chaperoning a cellular upheaval in malaria: heat shock proteins in Plasmodium falciparum, Mol. Biochem. Parasitol. 153 (2007) 85-94. (Pubitemid 46654240)
59. N. Saitou, M. Nei, The neighbor-joining method: a new method for reconstructing phylogenetic trees, Mol. Biol. Evol. 4 (1987) 406-425.
60. K. Tamura, J. Dudley, M. Nei, S. Kumar, MEGA4: Molecular Evolutionary Genetics Analysis (MEGA) software version 4.0, Mol. Biol. Evol. 24 (2007) 1596-1599. (Pubitemid 47236692)