Functions of FKBP12 and mitochondrial cyclophilin active site residues in vitro and in vivo in Saccharomyces cerevisiae

Molecular Biology of the Cell

Volumn 8, Issue 11, 1997, Pages 2267-2280

  Dolinski, Kara ^a   Scholz, Christian ^b   Scott Muir, R ^a   Rospert, Sabine ^c   Schmid, Franz X ^b   Cardenas, Maria E ^a   Heitman, Joseph ^a  

^a DUKE UNIVERSITY MEDICAL CENTER   (United States)

^b UNIVERSITY OF BAYREUTH   (Germany)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

[No Author keywords available]

Indexed keywords

CHYMOTRYPSIN; CYCLOPHILIN; CYCLOSPORIN A; DIHYDROFOLATE REDUCTASE; FK 506 BINDING PROTEIN; PROTEINASE; RIBONUCLEASE T1; TACROLIMUS;

ARTICLE; CONTROLLED STUDY; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME INACTIVATION; GENE; HUMAN; ISOMERISM; MITOCHONDRION; MUTATION; NONHUMAN; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN FOLDING; SACCHAROMYCES CEREVISIAE; SITE DIRECTED MUTAGENESIS;

SACCHAROMYCES CEREVISIAE;

EID: 0030731995     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.8.11.2267     Document Type: Article

References (81)

1. Aberham, C., Weber, S., and Phares, W. (1996). Spontaneous mutations in the human immunodeficiency virus type 1 gag gene that affect viral replication in the presence of cyclosporins. J. Virol. 70, 3536-3544.
2. Aldape, R.A., Futer, O., DeCenzo, M.T., Jarrett, B.P., Murcko, M.A., and Livingston, D.J. (1992). Charged surface residues of FKBP12 participate in formation of the FKBP12-FK506-calcineurin complex. J. Biol. Chem. 267, 16029-16032.
3. Anfinsen, C.B. (1973). Principles that govern the folding of protein chains. Science 181, 223-230.
4. Baker, E.K., Colley, N.J., and Zuker, C.S. (1994). The cyclophilin homolog NinaA functions as a chaperone, forming a stable complex in vivo with its protein target rhodopsin. EMBO J. 13, 4886-4895.
5. Braaten, D., Aberham, C., Franke, E.K., Yin, L., Phares, W., and Luban, J. (1996a). Cyclosporin A-resistant human immunodeficiency virus type 1 mutants demonstrate that Gag encodes the functional target of cyclophilin A. J. Virol. 70, 5170-5176.
6. Braaten, D., Ansari, H., and Luban, J. (1997). The hydrophobic pocket of cyclophilin is the binding site for the human immunodeficiency virus type I gag protein. J. Virol. 71, 2107-2113.
7. Braaten, D., Franke, E.K., and Luban, J. (1996b). Cyclophilin A is required for an early step in the life cycle of human immunodeficiency virus type 1 before the initiation of reverse transcription. J. Virol. 70, 3551-3560.
8. 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.
9. Brillantes, A.-M.B., Ondrias, K., Scott, A., Kobrinsky, E., Ondriasova, E., Moschella, M.C., Jayaraman, T., Landers, M., Ehrlich, B.E., and Marks, A.R. (1994). Stabilization of calcium release channel (ryanodine receptor) function by FK506-binding protein. Cell 77, 513-523.
10. 2+ flux. Cell 83, 463-472.
11. Cardenas, M.E., Hemenway, C., Muir, R.S., Ye, R., Fiorentino, D., and Heitman, J. (1994). Immunophilins interact with calcineurin in the absence of exogenous immunosuppressive ligands. EMBO J. 13, 5944-5957.
12. Cardenas, M., Muir, R.S., Breuder, T., and Heitman, J. (1995). Targets of immunophilin-immunosuppressant complexes are distinct highly conserved regions of calcineurin A. EMBO J. 14, 2772-2783.
13. 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, 255-263.
14. Cullin, C., and Minvielle-Sebastia, L. (1994). Multipurpose vectors designed for the fast generation of N- or C-terminal epitope-tagged proteins. Yeast 10, 105-112.
15. 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.
16. DeCenzo, M.T., Park, ST., Jarrett, B.P., Aldape, R.A., Futer, O., Murcko, M.A., and Livingston, D.J. (1996). FK506-binding protein mutational analysis: defining the active-site residue contributions to catalysis and the stability of ligand complexes. Protein Eng. 9, 173-180.
17. Dolinski, K., and Heitman, J. (1997). Peptidyl-prolyl isomerases (PPIases). In: Molecular Chaperones and Protein Folding Catalysts, ed. S. Tooze, London: Oxford University Press (in press).
18. Eberhardt, E.S., Loh, S.N., Hinck, A.P., and Raines, R.T. (1992). Solvent effects on the energetics of prolyl peptide bond isomerization. J. Am. Chem. Soc. 114, 5437-5439.
19. 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.
20. Fischer, G. (1994). Peptidyl-prolyl cis/trans isomerases and their effectors. Angew. Chem. Int. Ed. Engl. 33, 1415-1436.
21. Fischer, G., Bang, H., and Mech, C. (1984). Nachweis einer enzymkatalyse die cis-trans-isomerisierung der peptidbindung in prolin-haltigen petiden. Biomed. Biochim. Acta 43, 1101-1111.
22. Fischer, S., Michnick, S., and Karplus, M. (1993). A mechanism for rotamase catalysis by the FK506 binding protein (FKBP). Biochemistry 32, 13830-13837.
23. Franke, E.K., Yuan, H.E.H., and Luban, J. (1994). Specific incorporation of cyclophilin A into HIV-1 virions. Nature 372, 359-362.
24. Freskgard, P.-O., Bergenham, N., Jonsson, B.-H., Svensson, M., and Carlsson, U. (1992). Isomerase and chaperone activity of prolyl isomerase in the folding of carbonic anhydrase. Science 258, 466-468.
25. Frigerio, G., and Pelham, H.R.B. (1993). A Saccharomyces cerevisiae cyclophilin resident in the endoplasmic reticulum. J. Mol. Biol. 233, 183-188.
26. Gamble, T.R., Vajdos, F.F., Yoo, S., Worthylake, D.K., Houseweart, M., Sundquist, W.I., and Hill, C.P. (1996). Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell 87, 1285-1294.
27. Gething, M.-J., and Sambrook, J. (1992). Protein folding in the cell. Nature 355, 33-45.
28. Gietz, R.D., and Sugino, A. (1988). New yeast-Escherichia coli shuttle vectors constructed with in vitro mutagenized yeast genes lacking six-base pair restriction sites. Gene 74, 527-534.
29. Glick, B.S., and Pon, L.A. (1995). Isolation of highly purified mitochondria from Saccharomyces cerevisiae. Methods Enzymol. 260, 213-223.
30. Heitman, J., Koller, A., Cardenas, M.E., and Hall, M.N. (1993). Identification of immunosuppressive drug targets in yeast. Methods 5, 176-187.
31. Heitman, J., Mowa, N.R., and Hall, M.N. (1991a). Targets for cell cycle arrest by the immunosuppressant rapamycin in yeast. Science 253, 905-909.
32. Heitman, J., Movva, N.K., and Hall, M.N. (1992). Proline isomerases at the crossroads of protein folding, signal transduction, and immunosuppression. New Biol. 4, 448-460.
33. Heitman, J., Movva, N.R., Hiestand, P.C., and Hall, M.N. (1991b). FK506-binding protein proline rotamase is a target for the immunosuppressive agent FK506 in Saccharomyces cerevisiae. Proc. Natl. Acad. Sci. USA 88, 1948-1952.
34. +-ATPase assembly. Genetics 141, 833-844.
35. Hemenway, C.S., and Heitman, J. (1996). Immunosuppressant target protein FKBP12 is required for P-glycoprotein function in yeast. J. Biol. Chem. 271, 18527-18534.
36. Ho, S.N., Hunt, H.D., Horton, R.M., Pullen, J.K., and Pease, L.R. (1989). Site-directed mutagenesis by overlap extension using the polymerase chain reaction. Gene 77, 51-59.
37. Kallen, J., and Walkinshaw, M.D. (1992). The x-ray structure of a tetrapeptide bound to the active site of human cyclophilin A. FEBS Lett. 300, 286-290.
38. Ke, H., Mayrose, D., and Cao, W. (1993). Crystal structure of cyclophilin A complexed with substrate ala-pro suggests a solvent-assisted mechanism of cis-trans isomerization. Proc. Natl. Acad. Sci. USA 90, 3324-3328.
39. Kern, G., Kern, D., Schmid, F.X., and Fischer, G. (1994). Reassessment of the putative chaperone function of prolyl-cis/trans-isomerases. FEBS Lett. 348, 145-148.
40. Kiefhaber, T., Grunert, H.-P., Hahn, U., and Schmid, F.X. (1990a). Replacement of a cis proline simplifies the mechanism of ribonuclease T1 folding. Biochemistry 29, 6475-6480.
41. Kiefhaber, T., Quaas, R., Hahn, U., and Schmid, F.X. (1990b). Folding of ribonuclease T1.2. Kinetic models for the folding and unfolding reactions. Biochemistry 29, 3061-3070.
42. Lodish, H.F., and Kong, N. (1991). Cyclosporin A inhibits an initial step in folding of transferrin within the endoplasmic reticulum. J. Biol. Chem. 266, 14835-14838.
43. Lorenz, M.C., and Heitman, J. (1995). TOR mutations confer rapamycin resistance by preventing interaction with FKBP12-rapamycin. J. Biol. Chem. 270, 27531-27537.
44. Lorenz, M.C., Muir, R.S., Lim, E., McElver, J., Weber, S.C., and Heitman, J. (1995). Gene disruption with PCR products in Saccharomyces cerevisiae. Gene 158, 113-117.
45. Lu, K.P., Hanes, S.D., and Hunter, T. (1996). A human peptidylprolyl isomerase essential for regulation of mitosis. Nature 380, 544-547.
46. Luban, J. (1996). Absconding with the chaperone: essential cyclophilin-Gag interaction in HIV-1 virions. Cell 87, 1157-1159.
47. Luban, J., Bossolt, K.L., Franke, E.K., Kalpana, G.V., and Goff, S.P. (1993). Human immunodeficiency virus type 1 gag protein binds to cyclophilins A and B. Cell 73, 1067-1078.
48. Manning-Krieg, U.C., Henriquez, R., Cammas, F., Graff, P., Gaveriaux, S., and Movva, N.R. (1994). Purification of FKBP-70, a novel immunophilin from Saccharomyces cerevisiae, and cloning of its structural gene, FPR3. FEBS Lett. 352, 98-103.
49. Manning-Krieg, U.C., Scherer, P.E., and Schatz, G. (1991). Sequential action of mitochondrial chaperones in protein import into the matrix. EMBO J. 10, 3273-3280.
50. Matouschek, A., Rospert, S., Schmid, K., Click, B.S., and Schatz, G. (1995). Cyclophilin catalyzes protein folding in yeast mitochondria. Proc. Natl. Acad. Sci. USA 92, 6319-6323.
51. Mayr, L.M., Odefey, C., Schutkowski, M., and Schmid, F.X. (1996). Kinetic analysis of the unfolding and refolding of ribonuclease T1 by a stopped-flow double-mixing technique. Biochemistry 35, 5550-5561.
52. Mikol, V., Kallen, J., Pflugl, G., and Walkinshaw, M.D. (1993). X-ray structure of a monomeric cyclophilin A-cyclosporin A crystal complex at 2.1 A resolution. J. Mol. Biol. 234, 1119-1130.
53. Mücke, M., and Schmid, F.X. (1993). Folding mechanism of ribonuclease T1 in the absence of the disulfide bonds. Biochemistry 33, 14608-14619.
54. Mücke, M., and Schmid, F.X. (1994). Intact disulfide bonds decelerate the folding of ribonuclease T1. J. Mol. Biol. 239, 713-725.
55. Nakamura, T., Liu, Y., Hirata, D., Namba, H., Harada, S.-I., Hirokawa, T., and Miyakawa, T. (1993). Protein phosphatase type 2B (calcineurin)-mediated, FK506-sensitive regulation of intracellular ions in yeast is an important determinant for adaptation to high salt stress conditions. EMBO J. 12, 4063-4071.
56. Nielsen, J.B., Poor, F., Siekierka, J.J., Hsu, M.-J., Ramadan, N., Morin, N., Shafiee, A., Dahl, A.M., Brizuela, L., Chrebet, G., Bostian, K.A., and Parent, S.A. (1992). Yeast FKBP-13 is a membrane-associated FK506-binding protein encoded by the nonessential gene FKB2, Proc. Natl. Acad. Sci. USA 89, 7471-7475.
57. Pfanner, N., Muller, H.K., Harmey, M.A., and Neupert, W. (1987). Mitochondrial protein import: involvement of the mature part of a cleavable precursor protein in the binding to receptor sites. EMBO J. 6, 3449-3454.
58. Rassow, J., Mohrs, K., Koidl, S., Barthelmess, LB., Pfanner, N., and Tropschug, M. (1995). Cyclophilin 20 is involved in mitochondrial protein folding in cooperation with molecular chaperones hsp70 and hsp60. Mol. Cell. Biol. 15, 2654-2662.
59. Rospert, S., Looser, R., Dubaquie, Y., Matouschek, A., Click, B.S., and Schatz, G. (1996). Hsp60-independent protein folding in the matrix of yeast mitochondria. EMBO J. 15, 764-774.
60. Rotonda, J., Burbaum, J.J., Chan, H.K., Marcy, A.I., and Becker, J.W. (1993). Improved calcineurin inhibition by yeast FBKP-drug complexes. J. Biol. Chem. 268, 7607-7609.
61. Schmid, F.X. (1993). Prolyl isomerase-enzymatic catalysis of slow protein-folding reactions. Annu. Rev. Biophys. Biomol. Struct. 22, 123-143.
62. Schmid, F.X., Mayr, L.M., Mücke, M., and Schönbrunner, E.R. (1993) Prolyl isomerases: role in protein folding. Adv. Protein Chem. 44, 25-66.
63. Schneuwly, S., Shortridge, R.D., Larrivee, D.C., Ono, T., Ozaki, M., and Pak, W.L. (1989). Drosophila ninaA gene encodes an eye-specific cyclophilin (cyclosporin A binding protein). Proc. Natl. Acad. Sci. USA 86, 5390-5394.
64. Scholz, C., Stoller, G., Zarnt, T., Fischer, G., and Schmid, F.X. (1997a). Cooperation of enzymatic and chaperone functions of trigger factor in the catalysis of protein folding. EMBO J. 16, 54-58.
65. Scholz, C., Schindler, T., Dolinski, K., Heitman, J., and Schmid, F.X. (1997b). Cyclophilin active site mutants have native prolyl isomerase activity with a protein substrate. FEBS Lett. 414, 69-73.
66. Schönbrunner, E.R., Mayer, S., Tropschug, M., Fischer, G., Takahashi, N., and Schmid, F.X. (1991). Catalysis of protein folding by cyclophilins from different species. J. Biol. Chem. 266, 3630-3635.
67. Schreiber, S.L., and Crabtree, G.R. (1992). The mechanism of action of cyclosporin A and FK506. Immunol. Today 13, 136-142.
68. Shieh, B.-H., Stamnes, M.A., Seavello, S., Harris, G.L., and Zuker, C.S. (1989). The ninaA gene required for visual transduction in Drosophila encodes a homologue of cyclosporin A-binding protein. Nature 338, 67-70.
69. 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.
70. 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.
71. Stein, R.L., (1993). Mechanism of enzymatic and nonenzymatic prolyl isomerization. Adv. Protein Chem. 44, 1-24.
72. 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 cis-trans-isomerase. J. Biol. Chem. 266, 1299-1303.
73. Stueber, D., Ibrahim, I., Cutler, D., Dobberstein, B., and Bujard, H. (1984). A novel in vitro transcription-translation system: accurate and efficient synthesis of single proteins from cloned DNA sequences. EMBO J. 3, 3143-3148.
74. Takahashi, K., Uchida, T., and Egami, F. (1970). Ribonuclease T1: structure and function. Adv. Biophys. 1, 53-98.
75. Timerman, A.P., Wiederrecht, G., Marcy, A., and Fleischer, S. (1995). Characterization of an exchange reaction between soluble FKBP-12 and the FKBP-ryanodine receptor complex. J. Biol. Chem. 270, 2451-2459.
76. Tropschug, M., Wachter, E., Mayer, S., Schönbrunner, E.R., and Schmid, F.X. (1990). Isolation and sequence of an FK506-binding protein from N. crassa which catalyses protein folding. Nature 346, 674-677.
77. Van Duyne, G.D., Standaert, R.F., Karplus, P.A., Schreiber, S.L., and Clardy, J. (1991). Atomic structure of FKBP-FK506, an immunophilin-immunosuppressant complex. Science 252, 839-842.
78. Yaffe, M.P. (1991). Analysis of Mitochondrial Function and Assembly, ed. G.R. Fink and C. Guthrie, Vol. 194, Pasadena, CA: Academic Press, 627-643.
79. Zhao, Y., Chen, Y., Schutkowski, M., Fischer, G., and Ke, H. (1997). Cyclophilin A complexed with a fragment of HIV-1 gag protein: insights into HIV-1 infectious activity. Structure 5, 139-146.
80. Zhao, Y., and Ke, H. (1996). Crystal structure implies that cyclophilin predominantly catalyzes the trans to cis isomerization. Biochemistry 35, 7356-7361.
81. 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 Sci. 1, 1092-1099.