Browse > Article

A Cyclophilin from Griffithsia japonica Has Thermoprotective Activity and Is Affected by CsA  

Cho, Eun Kyung (Institute of Molecular Biology and Genetics, Seoul National University)
Lee, Yoo Kyung (Polar BioCenter, Korea Polar Research Institute, Korea Ocean Research and Development Institute)
Hong, Choo Bong (Institute of Molecular Biology and Genetics, Seoul National University)
Publication Information
Molecules and Cells / v.20, no.1, 2005 , pp. 142-150 More about this Journal
Abstract
Members of the multifunctional Cyp family have been isolated from a wide range of organisms. However, few functional studies have been performed on the role of these proteins as chaperones in red alga. For studying the function of cDNA GjCyp-1 isolated from the red alga (Griffithsia japonica), we expressed and purified a recombinant GjCyp-1 containing a hexahistidine tag at the amino-terminus in Escherichia coli. An expressed fusion protein, $H_6GjCyp-1$ maintained the stability of E. coli proteins up to $50^{\circ}C$. For a functional bioassay for recombinant $H_6GjCyp-1$, the viability of E. coli cells overexpressing $H_6GjCyp-1$ was compared with that of cells not expressing $H_6GjCyp-1$ at $50^{\circ}C$. After high temperature treatment for 1 h, E. coli overexpressing $H_6GjCyp-1$ survived about three times longer than E. coli lacking $H_6GjCyp-1$. Measurement of the light scattering of luciferase (luc) showed that GjCyp-1 prevents the aggregation of luc during mild heat stress and that the thermoprotective activity of GjCyp-1 is blocked by cyclosporin A (CsA), an inhibitor of Cyps. Furthermore, the Cyp-CsA complex inhibited the growth of E. coli under normal conditions. The results of the GjCyp-1 bioassays as well as in vitro studies strongly suggest that Cyp confers thermotolerance to E. coli.
Keywords
Cyclophilin; Escherichia coli; Griffithsia japonica; In Vivo and In Vitro Function; Thermotolerance;
Citations & Related Records
Times Cited By KSCI : 4  (Citation Analysis)
Times Cited By Web Of Science : 9  (Related Records In Web of Science)
연도 인용수 순위
1 Dolinski, K. J., Cardenas, M. E., and Heitman, J. (1998) CNS1 encodes an essential p60/Sti1 homolog in Saccharomyces cerevisiae that suppresses cyclophilin 40 mutations and interacts with Hsp90. Mol. Cell. Biol. 18, 7344-7352
2 Freskgard, P. O., Bergenhem, N., Jonsson, B. H., Svensson, M., and Carlson, U. (1992) Isomerase and chaperone activity of prolyl isomerase in the folding of carbonic anhydrase. Science 258, 466-468   DOI
3 Kim, K. P., Joe, M. K., and Hong, C. B. (2004) Tobacco small heat-shock protein, NtHSP18.2, has broad substrate range as a molecular chaperone. Plant Sci. 167, 1017-1025   DOI   ScienceOn
4 Luan, S., Lane, W. S., and Schreiber, S. L. (1994) pCyP B: a chloroplast-localized, heat shock-responsive cyclophilin from fava bean. Plant Cell 6, 885-892   DOI   ScienceOn
5 Matheos, D. P., Kingsbury, T. J., Ahsan, U. S., and Cunningham, K. W. (1997) Tcn1p/Crzlp, a calcineurin-dependent transcription factor that differentially regulates gene expression in Saccharomyces cerevisiae. Genes Dev. 11, 3445-3458   DOI   ScienceOn
6 Ratajczak, T. and Carrello, A. (1996) Cyclophilin 40 (CyP-40), mapping of its hsp90 binding domain and evidence that FKBP52 competes with CyP-40 for hsp90 binding. J. Biol. Chem. 271, 2961-2965   DOI
7 Rutherford, S. L. and Zuker, C. S. (1994) Protein folding and the regulation of signaling pathways. Cell 79, 1129-1132   DOI   ScienceOn
8 Stamnes, M. A., Shieh, B. H., Chuman, L., Harris, G. L., and Zuker, C. S. (1991) The cyclophilin homolog ninaA is a tissue- specific integral membrane protein required for the proper synthesis of a subset of Drosophila rhodopsins. Cell 65, 219-227   DOI   ScienceOn
9 Weisman, R., Creanor, J., and Fantes, P. (1996) A multicopy suppressor of a cell cycle defect in S. pombe encodes a heat shock-inducible 40 kDa cyclophilin-like protein. EMBO J. 15, 447-456
10 Lee, Y. K., Hong, C. B., Suh, Y. B., and Lee, I. K. (2002) A cDNA clone for cyclophilin from Griffithsia japonica and phylogenetic analysis of cyclophilins. Mol. Cells 13, 12-20
11 Liu, J., Farmer, J. D., Lane, W. S., Friedman, J., Weissman, I., et al. (1991) Calcineurin is a common target of cyclophilincyclosporin A and FKBP-FK506 complexes. Cell 66, 807- 815   DOI   ScienceOn
12 Wang, P., Cardenas, M. E., Cox, G. M., Perfect, J. R., and Heitman, J. (2001) Two cyclophilin A homologs with shared and distinct functions important for growth and virulence of Cryptococcus neoformans. EMBO Rep. 2, 511-518   DOI   ScienceOn
13 Fischer, G. and Schmid, F. X. (1990) The mechanism of protein folding. Implications of in vitro refolding models for de novo protein folding and translocation in the cell. Biochemistry 29, 2205-2212   DOI   ScienceOn
14 Fejzo, J., Etzkorn, F. A., Clubb, R. T., Shi, Y., Walsh, C. T., et al. (1994) The mutant Escherichia coli F112W cyclophilin binds cyclosporin A in nearly identical conformation as human cyclophilin. Biochemistry 33, 5711-5720   DOI   ScienceOn
15 Liu, X. D., Morano, K. A., and Thiele, D. J. (1999) The yeast Hsp110 family member, Sse1, is an Hsp90 cochaperone. J. Biol. Chem. 274, 26654-26660   DOI
16 Sambrook, J., Fritsch, E. F., and Maniatis, T. (1989) Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor Laboratory Press, Cold Spring Harbor, New York
17 Sykes, K., Gething, M., and Sambrook, J. (1993) Proline isomerases function during heat shock. Proc. Natl. Acad. Sci. USA 90, 5853-5857
18 Duina, A. A., Marsh, J. A., Kurtz, R. B., Chang, H. J., Lindquist, S., et al. (1998) The peptidyl-prolyl isomerase domain of the CyP-40 cyclophilin homolog Cpr7 is not required to support growth or glucocorticoid receptor activity in Saccharomyces cerevisiae. J. Biol. Chem. 273, 10819-10822   DOI   ScienceOn
19 Lee, G. J. and Vierling, E. (1998) Expression, purification and molecular chaperone activity of plant recombinant small heat shock proteins: Protein Folding: catalysts, accessory proteins, and chaperones; in Methods in Enzymology, Lorimer, G. and Baldwin, T. O. (eds.), Vol. 29, pp. 350-365
20 Dolinski, K., Muir, R. S., Cardenas, M. E., and Heitman, J. (1997) All cyclophilins and FK506 binding proteins are, individually and collectively, dispensable for viability in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 94, 13093-13098
21 Schneider, H., Charara, N., and Schmitz, R. (1994) Human cyclophilin C: primary structure, tissue distribution, and determination of binding specificity for cyclosporins. Biochemistry 33, 8218-8224   DOI   ScienceOn
22 Foor, F., Parent, S. A., Morin, N., Dahl, A. M., Ramadan, N., et al. (1992) Calcineurin mediates inhibition by FK506 and cyclosporin of recovery from $\alpha$-factor arrest in yeast. Nature 360, 682-684   DOI   ScienceOn
23 Breuder, T., Hemenway, C. S., Movva, N. R., Cardenas, M. E., and Heitman, J. (1994) Calcineurin is essential in cyclosporin A- and FK506-sensitive yeast strains. Proc. Natl. Acad. Sci. USA 91, 5372-5376
24 Stathopoulos, A. M. and Cyert, M. S. (1997) Calcineurin acts through the CRZ1/TCN1-encoded transcription factor to regulate gene expression in yeast. Genes Dev. 11, 3432-3444   DOI   ScienceOn
25 Ondek, B., Hardy, R. W., Baker, E. K., Stamnes, M. A., Shieh, B. H., et al. (1992) Genetic dissection of cyclophilin function. Saturation mutagenesis of the Drosophila cyclophilin homolog ninaA. J. Biol. Chem. 267, 16460-16466
26 Stamnes, M. A., Rutherford, S. L., and Zuker, C. S. (1992) Cyclophilins: a new family of proteins involved in intracellular folding. Trends Cell Biol. 2, 272-276   DOI   ScienceOn
27 Hartl, F. U. and Hayer-Hartl, M. (2002) Molecular chaperones in the cytosol: from nascent chain to folded protein. Science 295, 1852-1858   DOI   ScienceOn
28 Stathopoulos-Gerontides, A., Guo, J. J., and Cyert, M. S. (1999) Yeast calcineurin regulates nuclear localization of the Crz1p transcription factor through dephosphorylation. Genes Dev. 13, 798-803   DOI
29 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, 544-547   DOI
30 Clubb, R. T., Ferguson, S. B., Walsh, C. T., and Wagner, G. (1994) Three-dimensional solution structure of Escherichia coli periplasmic cyclophilin. Biochem. 33, 2761-2772   DOI   ScienceOn
31 Zander, K., Sherman, M. P., Tessmer, U., Bruns, K., Wray, V., et al. (2003) Cyclophilin A interacts with HIV-1 Vpr and is required for its functional expression. J. Biol. Chem. 278, 43202-43213   DOI   ScienceOn
32 Tai, P.-K. K., Albers, M. W., Chang, H., Faber, L. E., and Schreiber, S. L. (1992) Association of a 59-kilodalton immunophilin with the glucocorticoid receptor complex. Science 256, 1315-1318   DOI
33 Crabtree, G. R. (2001) Calcium, calcineurin and the control of transcription. J. Biol. Chem. 276, 2313-2316   DOI   ScienceOn
34 Galat, A. (1993) Peptidylproline cis-trans-isomerases: immunophilins. Eur. J. Biochem. 216, 689-707   DOI   ScienceOn
35 Groenendyk, J., Lynch, J., and Michalak, M. (2004) Calreticulin, $Ca^{2+}$, and calcineurin-signaling from the endoplasmic reticulum. Mol. Cells 17, 383-389
36 Kimura, Y., Yahara, I., and Lindquist, S. (1995) Role of the protein chaperone YDJ1 in establishing Hsp90-mediated signal transduction pathways. Science 268, 1362-1365   DOI
37 Mayer, M. P., Brehmer, D., Gassler, C. S., and Bukau, B. (2001) Protein folding in the cell; in Advances in Protein Chemistry, Horwich, A. (ed.), pp. 1-44, Academic Press, San Diego
38 Chang, H. C. and Lindquist, S. (1994) Conservation of Hsp90 macromolecular complexes in Saccharomyces cerevisiae. J. Biol. Chem. 269, 24983-24988
39 Edvardsson, A., Eshaghi, S., Vener, A. V., and Andersson, B. (2003) The major peptidyl-prolyl isomerase activity in thylakoid lumen of plant chloroplasts belongs to a novel cyclophilin TLP20. FEBS Lett. 542, 137-141   DOI   ScienceOn
40 Tesic, M., Marsh, J. A., Cullinan, S. B., and Gaber, R. F. (2003) Functional interactions between Hsp90 and co-chaperones Cns1 and Cpr7 in Saccharomyces cerevisiae. J. Biol. Chem. 278, 32692-32701   DOI   ScienceOn
41 Yu, H. S., Kong, H. H., and Chung, D. I. (2002) Cloning and characterization of Giardia intestinalis cyclophilin. Korean J. Parasit. 40, 131-138   DOI   ScienceOn
42 Kern, G., Kern, D., Schimid, F. X., and Fischer, G. (1994) Reassessment of the putative chaperone function of prolylcis/ trans-isomerase. FEBS Lett. 348, 145-148   DOI   ScienceOn
43 Steinmann, B., Bruckner, P., and Superti-Furga, A. (1991) Cyclosporin A slows collagen triple-helix formation in vivo: indirect evidence for a physiologic role of peptidyl-prolyl cistrans isomerase. J. Biol. Chem. 266, 1299-1303