Functional analysis of the yeast 40 kDa cyclophilin Cyp40 and its role for viability and steroid receptor regulation

Biological Chemistry

Volumn 378, Issue 5, 1997, Pages 381-391

  Warth, Rainer ^a   Briand, Pierre André ^a   Picard, Didier ^a  

^a UNIVERSITY OF GENEVA   (Switzerland)

Author keywords

Cpr6; Cpr7; Cyclosporin A; Heat shock protein; Prolyl isomerase; Saccharomyces cerevisiae

Indexed keywords

CHAPERONE; CYCLOPHILIN; CYCLOSPORIN A; CYTOPLASM PROTEIN; HEAT SHOCK PROTEIN; HEAT SHOCK PROTEIN 90; IMMUNOPHILIN; ISOMERASE; POLYCLONAL ANTIBODY; RECOMBINANT PROTEIN; STEROID RECEPTOR;

AMINO ACID SEQUENCE; ARTICLE; CELL VIABILITY; CONTROLLED STUDY; ENZYME ACTIVITY; GENE EXPRESSION REGULATION; GENE INDUCTION; HEAT SHOCK; IMMUNOBLOTTING; MOLECULAR CLONING; NONHUMAN; PRIORITY JOURNAL; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; SACCHAROMYCES CEREVISIAE; YEAST CELL;

FELIS CATUS; SACCHAROMYCES CEREVISIAE; SACCHAROMYCETALES; VERTEBRATA;

EID: 0030919428     PISSN: 14316730     EISSN: None     Source Type: Journal    
DOI: 10.1515/bchm.1997.378.5.381     Document Type: Article

References (70)

1. Billich, A., Hammerschmid, F., Peichl, P., Wenger, R., Zenke, G., Quesniaux, V., and Rosenwirth, B. (1995). Mode of action of SDZ NIM 811, a nonimmunosuppressive cyclosporin A analog with activity against human immunodeficiency virus (HIV) type 1: interference with HIV protein-cyclophilin A interactions. J. Virol. 69, 2451-2461.
2. Bose, S., Weikl, T., Bügl, H., and Buchner, J. (1996). Chaperone function of Hsp90-associated proteins. Science 274, 1715-1717.
3. Bossard, M.J., Koser, P.L., Brandt, M., Bergsma, D.J., and Levy, M.A. (1991). A single Trp121 to Ala121 mutation in human cyclophilin alters cyclosporin A affinity and peptidyl-prolyl isomerase activity. Biochem. Biophys. Res. Commun. 176, 1142-1148.
4. 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.
5. Chang, H.C.J., and Lindquist, S.L. (1994). Conservation of Hsp90 macromolecular complexes in Saccharomyces cerevisiae. J. Biol. Chem. 269, 24983-24988.
6. Chang, H.-C.J., Nathan, D.F., and Undquist, S. (1997). In vivo analysis of the Hsp90 cochaperone Stil (p60). Mol. Cell. Biol. 17, 318-325.
7. Davis, E.S., Becker, A., Heitman, J., Hall, M.N., and Brennan, M.B. (1992). A yeast cyclophilin gene essential for lactate metabolism at high temperature. Proc. Natl. Acad. Sci. USA 89, 11169-11173.
8. Dittmar, K.D., Hutchison, K.A. Owens-Grillo, J.K., and Pratt, W.B. (1996). Reconstitution of the steroid receptor hsp90 hetero-complex assembly system of rabbit reticulocyte lysate. J. Biol. Chem. 271, 12833-12839.
9. Duina, A.A., Chang, H.-C.J., Marsh, J.A., Lindquist, S., and Gaber, R.F. (1996a). Acyclophilin function in Hsp90-dependent signal transduction. Science 274, 1713-1715.
10. Duina, A.A., Marsh, J.A., and Gaber, R.F. (1996b). Identification of two CyP-40-like cyclophilins in Saccharomyces cerevisiae, one of which is required for normal growth. Yeast 12, 943-952.
11. Ferreira, P.A., Nakayama, T.A., Pak, W.L., and Travis, G.H. (1996). Cyclophilin-related protein RanBP2 acts as chaperone for red/green opsin. Nature 383, 637-640.
12. Fischer, G., Bang, H., Berger, E., and Schellenberger, A. (1984). Conformational specificity of chymotrypsin toward proline-containing substrates. Biochim. Biophys. Acta 791, 87-97.
13. Flanagan, W.M., Corthesy, B., Bram, R.J., and Crabtree, G.R. (1991). Nuclear association of a T-cell transcription factor blocked by FK-506 and cyclosporin A. Nature 352, 803-807.
14. Franco, L., Jimenez, A., Demolder, J., Molemans, F., Fiers, W., and Contreras, R. (1991). The nucleotide sequence of a third cyclophilin-homologous gene from Saccharomyces cerevisiae. Yeast 7, 971-979.
15. Franke, E.K., Yuan, H.E.H., and Luban, J. (1994). Specific incorporation of cyclophilin A into HIV-1 virions. Nature 372, 359-362.
16. Freeman, B.C., Toft, D.O., and Morimoto, R.I. (1996). Molecular chaperone machines: chaperone activities of the cyclophilin Cyp-40 and the steroid aporeceptor-associated protein p23. Science 274, 1718-1720.
17. Freskgård, P.-O., Bergenhem, N., Jonsson, B.-H., Svensson, M., and Carlsson, U. (1992). lsomerase and chaperone activity of prolyl isomerase in the folding of carbonic anhydrase. Science 258, 466-468.
18. Frigerio, G., and Pelham, H.R.B. (1993). A Saccharomyces cerevisiae cyclophilin resident in the endoplasmic reticulum. J. Mol. Biol. 233, 183-188.
19. Fruman, D.A., Burakoff, S.J., and Bierer, B.E. (1994). Immunophilins in protein folding and immunosuppression. FASEB J. 8, 391-400.
20. Galat, A. (1993). Peptidylproline cis-trans-isomerases: immunophilins. Eur. J. Biochem. 216, 689-707.
21. Garabedian, M.J. (1993). Genetic approaches to mammalian nuclear receptor function in yeast. Companion Methods Enzymol. 5, 138-146.
22. Heitman, J., Koller, A., Cardenas, M.E., and Hall, M.N. (1993). Identification of immunosuppressive drug targets in yeast. Companion Methods Enzymol. 5, 176-187.
23. Hoffmann, K., and Handschumacher, R.E. (1995). Cyclophilin-40: evidence for a dimeric complex with hsp90. Biochem. J. 307, 5-8.
24. 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. Eur. J. Biochem. 229, 188-193.
25. Hutchison, K.A., Scherrer, L.C., Czar, M.J., Ning, Y., Sanchez, E.R., Leach, K.L., Deibel, M.R., Jr., and Pratt, W.B. (1993). FK506 binding to the 56-kilodalton immunophilin (Hsp56) in the glucocorticoid receptor heterocomplex has no effect on receptor folding or function. Biochem. 32, 3953-3957.
26. Johnson, J.L., and Toft, D.O. (1994). A novel chaperone complex for steroid receptors involving heat shock proteins, immunophilins, and p23. J. Biol. Chem. 269, 24989-24993.
27. Kern, G., Kern, D., Schmid, F.X., and Fischer, G. (1995). A kinetic analysis of the folding of human carbonic anhydrase II and its catalysis by cyclophilin. J. Biol. Chem. 270, 740-745.
28. Kieffer, L.J., Thalhammer, T., and Handschumacher, R.E. (1992). Isolation and characterization of a 40-kDa cyclophilin-related protein. J. Biol. Chem. 267, 5503-5507.
29. 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. J. Biol. Chem. 268, 12303-12310.
30. Kofron, J.L., Kuzmic, P., Kishore, V., Colón-Bonilla, E., and Rich, D.H. (1991). Determination of kinetic constants for peptidyl prolyl cis-trans isomerases by an improved spectrophotometric assay. Biochem. 30, 6127-6134.
31. Koser, P.L., Bergsma, D.J., Cafferkey, R., Eng, W.-K., McLaughlin, M.M., Ferrara, A., Silverman, C., Kasyan, K., Bossard, M.J., Johnson, R.K., Porter, T.G., Levy, M.A., and Livi, G.P. (1991). Gene 108, 73-80.
32. Kunz, J., and Hall, M.N. (1993). Cyclosporin A, FK506 and rapamycin: more than just immunosuppression. Trends Biochem. Sci. 18, 334-338.
33. Liu, J., Chen, C.M., and Walsh, C.T. (1991). Human and Escherichia coli cyclophilins: sensitivity to inhibition by the immunosuppressant cyclosporin A correlates with a specific tryptophan residue. Biochem. 30, 2306-2310.
34. Louvion, J.-F., Warth, R., and Picard, D. (1996). Two eukaryote-specific regions of Hsp82 are dispensable for its viability and signal transduction functions in yeast. Proc. Natl. Acad. Sci. USA 93, 13937-13942.
35. Luban, J. (1996). Absconding with the chaperone: essential cyclophilin-Gag interaction in HIV-1 virions. Cell 87, 1157-1159.
36. Marks, A. (1996). Cellular functions of immunophilins. Physiol. Rev. 76, 631-649.
37. Matouschek, A., Rospert, S., Schmid, K., Glick, B.S., and Schatz, G. (1995). Cyclophilin catalyzes protein folding in yeast mitochondria. Proc. Natl. Acad. Sci. USA 92, 6319-6323.
38. Milad, M., Sullivan, W., Diehl, E., Altmann, M., Nordeen, S., Edwards, D.P., and Toft, D.O. (1995). Interaction of the progesterone receptor with binding proteins for FK506 and cyclosporin A. MoI. Endocrinol. 9, 838-847.
39. Ning, Y.-M., and Sanchez, E.R. (1993). Potentiation of glucocorticoid receptor-mediated gene expression by the immunophilin ligands and rapamycin. J. Biol. Chem. 268, 6073-6076.
40. Owens-Grillo, J.K., Hoffmann, K., Hutchison, K.A., Yem, A.W., Deibel, M.R., Handschumacher, R.E., and Pratt, W.B. (1995). The cyclosporin A-binding immunophilin CyP-40 and the FK506-binding immunophilin hsp56 bind to a common site on hsp90 and exist in independent cytosolic heterocomplexes with the untransformed glucocorticoid receptor. J. Biol. Chem. 270, 20479-20484.
41. Owens-Grillo, J.K., Czar, M.J., Hutchison, K.A., Hoffman, K., Perdew, G.H., and Pratt, W.B. (1996). A model of protein targeting mediated by immunophilins and other proteins that bind to hsp90 via tetratricopeptide repeat domains. J. Biol. Chem. 271,13468-13475.
42. Palmer, G., Louvion, J.-F., Tibbetts, R.S., Engman, D.M., and Picard, D. (1995). Trypanosoma cruzi heat-shock protein 90 can functionally complement yeast. Mol. Biochem. Parasitol. 70, 199-202.
43. Perisic, O., Xiao, H., and Lis, J.T. (1989). Stable binding of Drosophila heat shock factor to head-to-head and tail-to-tail repeats of a conserved 5 bp recognition unit. Cell 59, 797-806.
44. Picard, D., Khursheed, B., Garabedian, M.J., Fortin, M.G., Lindquist, S., and Yamamoto, K.R. (1990). Reduced levels of hsp90 compromise steroid receptor action in vivo. Nature 348, 166-168.
45. Pratt, W.B. (1993). The role of heat shock proteins in regulating the function, folding, and trafficking of the glucocorticoid receptor. J. Biol. Chem. 268, 21455-21458.
46. Pratt, W.B., and Toft, D.O. (1997). Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocr. Rev., in press.
47. Radanyi, C., Chambraud, B., and Baulieu, E.-E. (1994). The ability of the immunophilin FKBP59-HBI to interact with the 90-kDa heat shock protein is encoced by its tetratricopeptide repeat domain. Proc. Natl. Acad. Sci. USA 91, 11197-11201.
48. 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.
49. Ratajczak, T., Carrello, A., Mark, P.J., Warner, B.J., Simpson, R.J., Moritz, R.L., and House, A.K. (1993). The cyclophilin component of the unactivated estrogen receptor contains a tetratrico-peptide repeat domain and shares identity with p59 (FKBP59). J. Biol. Chem. 268, 13187-13192.
50. Ratajczak, T., Carrello, A., and Minchin, R.F. (1995). Biochemical and calmodulin binding properties of estrogen receptor binding cyclophilin expressed in Escherichia coli. Biochem. Biophys. Res. Commun. 209, 177-125.
51. Ratajczak, T., Mark, P.J., Martin, R.L., and Minchin, R.F. (1996). Cyclosporin A potentiates estradiol-induced expression of the cathepsin D gene in MCF7 breast cancer cells. Biochem. Biophys. Res. Commun. 220, 208-212.
52. Renoir, J.-M., Bihan, S.L., Mercier-Bodard, C., Gold, A., Arjomandi, M., Radanyi, C., and Baulieu, E.-E. (1994). Effects of immunosuppressants FK506 and rapamycin on the heterooligomeric form of the progesterone receptor. J. Steroid Biochem. Molec. Biol. 48, 101-110.
53. Renoir, J.-M., Mercier-Bodard, C., Hoffmann, K., Bihan, S.L., Ning, Y.-M., Sanchez, E.R., Handschumacher, R.E., and Baulieu, E.-E. (1995). Cyclosporin A potentiates the dexamethasone induced mouse mammary tumor viruschloramphenicol acetyltransferase activity in LMCAT cells: A possible role for different heat shock protein-binding immunophilin in glucocorticoid receptor-mediated gene expression. Proc. Natl. Acad. Sci. USA 92, 4977-4981.
54. Schena, M., Picard, D., and Yamamoto, K.R. (1991). Vectors for constitutive and inducible gene expression in yeast. Methods Enzymol. 194, 389-398.
55. Schena, M., and Yamamoto, K.R. (1988). Mammalian glucocorticoid receptor derivatives enhance transcription in yeast. Science 241, 965-967.
56. Schmid, F.X. (1995). Prolyl isomerases join the fold. Curr. Biol. 5, 993-994.
57. Scholz, C., Stoller, G., Zarnt, T, Fischer, G., and Schmid, F.X. (1997). Cooperation of enzymatic and chaperone functions of trigger factor in the catalysis of protein folding. EMBO J. 16, 54-58.
58. Sigal, N.H., and Dumont, F.J. (1992). Cyclosporin A, FK-506, and rapamycin: pharmacological probes of lymphocyte signal transduction. Annu. Rev. Immunol. 10, 519-560.
59. Sikorski, R.S., and Hieter, P. (1989). A system of shuttle vectors and yeast host strains designed for efficient manipulation of DNA in Saccharomyces cerevisiae. Genetics 122, 19-27.
60. Smith, D.F. (1993). Dynamics of heat shock protein 90-progesterone receptor binding and the disactivation loop model for steroid receptor complexes. Mol. Endocrinol. 7, 1418-1429.
61. Smith, D.F., and Toft, D.O. (1993). Steroid receptors and their associated proteins. Mol. Endocrinol. 7, 4-11.
62. Smith, D.F., Whitesell, L., Nair, S.C., Chen, S., Prapapanich, V., and Rimerman, R.A. (1995). Progesterone receptor structure and function altered by geldanamycin, an hsp90-binding agent. Mol. Cell. Biol. 15, 6804-6812.
63. Stamnes, M.A., Rutherford, S.L., and Zuker, C.S. (1992a). Cyclophilins: a new family of proteins involved in intracellular folding. Trends Cell Biol. 2, 272-276.
64. Stamnes, M.A., Shieh, B.-H., Chuman, L., Harris, G.L., and Zuker, C.S. (1992b). 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.
65. Sykes, K., Gething, M.-J., and Sambrook, J. (1993). Proline isomerase function during heat shock. Proc. Natl. Acad. Sci. USA 90, 5853-5857.
66. Tai, P.-K., Albers, M.W., McDonnell, D.P., Chang, H., Schreiber, S.L., and Faber, L.E. (1994). Potentiation of progesterone receptor-mediated transcription by the immunosuppressant FK506. Biochem. 33, 10666-10671.
67. Thali, M., Bukovsky, A., Kondo, E., Rosenwirth, B., Walsh, C.T., Sodroski, J., and Gottlinger, H.G. (1994). Functional association of cyclophilin A with HIV-1 virions. Nature 372, 363-365.
68. Timmerman, L.A., Clipstone, N.A., Ho, S.N., Northrop, J.P., and Crabtree, G.R. (1996). Rapid shuttling of NF-AT in discrimination of Ca2+ signals and immunosuppression. Nature 383, 837-840.
69. 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.
70. Yocum, R.R., Hanley, S., West, R.W., Jr., and Ptashne, M. (1984). Use of lacZ fusions to delimit regulatory elements of the inducible divergent GAL1-GAL10 promoter in Saccharomyces cerevisiae. Mol. Cell. Biol. 4, 1985-1998.