Characterization of Arabidopsis thaliana AtFKBP42 that is membrane-bound and interacts with Hsp90

Plant Journal

Volumn 32, Issue 3, 2002, Pages 263-276

  Kamphausen, Thilo ^a   Fanghänel, Jörg ^a   Neumann, Dieter ^b   Schulz, Burkhard ^c,d   Rahfeld, Jens U ^a  

^a MAX PLANCK RESEARCH UNIT FOR ENZYMOLOGY OF PROTEIN FOLDING   (Germany)

^b LEIBNIZ INSTITUTE OF PLANT BIOCHEMISTRY   (Germany)

^c UNIVERSITY OF COLOGNE   (Germany)

^d ZMBP   (Germany)

Author keywords

Arabidopsis; Hsp90; Plasma membrane; PPlase; Signal transduction; Steroid hormone receptor

Indexed keywords

ELECTRON MICROSCOPY; GENES; PROTEINS; STOICHIOMETRY;

MUTANTS;

PLANTS (BOTANY);

AMINO ACID SEQUENCE; ARABIDOPSIS; ARABIDOPSIS PROTEINS; CALMODULIN-BINDING PROTEINS; CELL MEMBRANE; CIRCULAR DICHROISM; CITRATE (SI)-SYNTHASE; CLONING, MOLECULAR; GENE EXPRESSION REGULATION, PLANT; HSP90 HEAT-SHOCK PROTEINS; MEMBRANE PROTEINS; MICROSCOPY, ELECTRON; MOLECULAR SEQUENCE DATA; MUTATION; PEPTIDYLPROLYL ISOMERASE; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN INTERACTION MAPPING; SEQUENCE HOMOLOGY, AMINO ACID; SPECTRUM ANALYSIS; TACROLIMUS BINDING PROTEINS;

ARABIDOPSIS; ARABIDOPSIS THALIANA; EMBRYOPHYTA; MAMMALIA;

EID: 0036847334     PISSN: 09607412     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1365-313X.2002.01420.x     Document Type: Article

References (91)

1. Adams, M.D., Celniker, S.E., Holt, R.A., Evans, C.A., Gocayne, J.D. et al. (2000) The genome sequence of Drosophila melanogaster. Science, 287, 2185-2195.
2. Aghdasi, B., Resnick, K.Q.,Ye, A., Huang, A., Ha, H.C., Guo, X., Dawson, T.M., Dawson, V.L. and Snyder, S.H. (2001) FKBP12, the 12-kDa FK506-binding protein, is a physiologic regulator of the cell cycle. Proc. Natl Acad. Sci. USA, 98, 2425-2430.
3. Altschul, S.F., Gish, W., Miller, W., Myers, E.W. and Lipman, D.J. (1990) Basic local alignment search tool. J. Mol. Biol. 215, 403-410.
4. Arbeitman, M.N. and Hogness, D.S. (2000) Molecular chaperones activate the Drosophila ecdysone receptor, an RxR heterodimer. Cell, 101, 67-77.
5. Aviezer, K., Kurek, I., Erel, N., Blecher, O., Devos, K. and Breiman, A. (1998) Studies on the expression of the wheat prolyl isomerase FKBP73 during plant development. Plant Sci. 139, 149-158.
6. Becraft, P.W. (2001) Plant steroids recognized at the cell surface. Trends Genet. 17, 60-62.
7. Berardini, T.Z., Bollman, K., Sun, H. and Poethig, R.S. (2001) Regulation of vegetative phase change in Arabidopsis thaliana by cyclophilin 40. Science, 291, 2405-2407.
8. Bishop, G.J. and Yokota, T. (2001) Plant steroid hormones, brassinosteroids: Current highlights of molecular aspects on their synthesis/metabolism, transport, perception and response. Plant Cell Physiol. 42, 114-120.
9. Blatch, G.L. and Lässle, M. (1999) The tetratricopeptide repeat: A structural motif mediating protein-protein interactions. Bioessays, 21, 932-939.
10. Borski, R.J. (2000) Nongenomic membrane actions of glucocorticoids in vertebrates. Trends Endocrin. Met. 11, 427-436.
11. Buchner, J., Grallert, H. and Jakob, U. (1998) Analysis of chaperone function using citrate synthase as nonnative substrate protein. Meth. Enzymol. 290, 323-338.
12. r 90 000 heat shock protein: Main structural features of a mammalian p59 protein. Proc. Natl Acad. Sci. USA, 89, 6270-6274.
13. Carol, R.J., Breiman, A., Erel, N., Vittorioso, P. and Bellini, C. (2001) Pasticcino 1 (AtFKBP70) is a nuclear-localised immunophilin required during Arabidopsis thaliana embryogenesis. Plant Sci. 161, 527-535.
14. Carrello, A., Ingley, E., Minchin, R.F., Tsai, S. and Ratajczak, T. (1999) The common tetratricopeptide repeat acceptor site for steroid receptor-associated immunophilins and hop is located in the dimerization domain of Hsp90. J. Biol. Chem. 274, 2682-2689.
15. DeCenzo, M.T., Park, S.T., 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.
16. Faure, J.D., Gingerich, D. and Howell, S.H. (1998a) An Arabidopsis immunophilin, AtFKBP12, binds to AtFIP37 (FKBP interacting protein) in an interaction that is disrupted by FK506. Plant J. 15, 783-789.
17. Faure, J.D., Vittorioso, P., Santoni, V., Fraisier, V., Prinsen, E., Barlier, I., Van Onckelen, H., Caboche, M. and Bellini, C. (1998b) The PASTICCINO genes of Arabidopsis thaliana are involved in the control of cell division and differentiation. Development, 125, 909-918.
18. Fischer, G. (1994) Peptidyl-prolyl cis/trans isomerases and their effectors. Angew. Chem. Int. Ed. Engl. 33, 1415-1436.
19. Fischer, G., Bang, H. and Mech, C. (1984) Nachweis einer enzymkatalyse fur die cis-trans-isomerisierung der peptidbindung in prolinhaltigen peptiden. Biomed. Biochim. Acta, 43, 1101-1111.
20. 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, 337, 476-478.
21. Fischer, T., Beyermann, M. and Koch, K.W. (2001) Application of different surface plasmon resonance biosensor chips to monitor the interaction of the Cam-binding site of nitric oxide synthase I and calmodulin. Biochem. Biophys. Res. Commun. 285, 463-469.
22. Flores-Delgado, G., Bringas, P., Buckley, S., Anderson, K.D. and Warburton, D. (2001) Nongenomic estrogen action in human lung myofibroblasts. Biochem. Biophys. Res. Commun. 283, 661-667.
23. Friedrichsen, D. and Chory, J. (2001) Steroid signaling in plants: From the cell surface to the nucleus. Bioessays, 23, 1028-1036.
24. Friedrichsen, D.M., Joazeiro, C.A.P., Li, J.M., Hunter, T. and Chory, J. (2000) Brassinosteroid-insensitive-1 is a ubiquitously expressed leucine-rich repeat receptor serine/threonine kinase. Plant Physiol. 123, 1247-1255.
25. Galigniana, M.D., Radanyi, C., Renoir, J.M., Housley, P.R. and Pratt, W.B. (2001) Evidence that the peptidylprolyl isomerase domain of the Hsp90-binding immunophilin FKBP52 is involved in both dynein interaction and glucocorticoid receptor movement to the nucleus. J. Biol. Chem. 276, 14884-14889.
26. Greenfield, N.J. (1996) Methods to estimate the conformation of proteins and polypeptides from circular dichroism data. Anal. Biochem. 235, 1-10.
27. Hani, J., Schelbert, B., Bernhardt, A., Domdey, H., Fischer, G., Wiebauer, K. and Rahfeld, J.U. (1999) Mutations in a peptidyl-prolyl-cis/trans-isomerase gene lead to a defect in 3′-end formation of a pre-mRNA in Saccharomyces cerevisiae. J. Biol. Chem. 274, 108-116.
28. Harrar, Y., Bellini, C. and Faure, J.D. (2001) FKBPs: At the crossroads of folding and transduction. Trends Plant Sci. 6, 426-431.
29. Hubbard, M.J. and Klee, C.B. (1987) Calmodulin binding by calcineurin. Ligand-induced renaturation of protein immobilized on nitrocellulose. J. Biol. Chem. 262, 15062-15070.
30. Hueros, G., Rahfeld, J., Salamini, F. and Thompson, R. (1998) A maize FK506-sensitive immunophilin, mzFKBP-66, is a peptidyl-proline cis-trans-isomerase that interacts with calmodulin and a 36-kDa cytoplasmic protein. Planta, 205, 121-131.
31. Ivery, M.T.G. (2000) Immunophilins: Switched on protein binding domains? Med. Res. Rev. 20, 452-484.
32. Janowski, B., Wöllner, S., Schutkowski, M. and Fischer, G. (1997) A protease-free assay for peptidyl prolyl cis/trans isomerases using standard peptide substrates. Anal. Biochem. 252, 299-307.
33. Kammerloher, W., Fischer, U., Piechottka, G.P. and Schaffner, A.R. (1994) Water channels in the plant plasma-membrane cloned by immunoselection from a mammalian expression system. Plant J. 6, 187-199.
34. Kay, J.E. (1996) Structure-function relationships in the FK506-binding protein (FKBP) family of peptidylprolyl cis-trans isomerases. Biochem. J. 314, 361-385.
35. Krishna, P. and Gloor, G. (2001) The Hsp90 family of proteins in Arabidopsis thaliana. Cell Stress Chaperones, 6, 238-246.
36. Kurek, I., Aviezer, K., Erel, N., Herman, E. and Breiman, A. (1999) The wheat peptidyl prolyl cis-trans-isomerase FKBP77 is heat induced and developmentally regulated. Plant Physiol. 119, 693-703.
37. Laemmli, U.K. (1970) Cleavage of structural proteins during assembly of head of bacteriophage-T4. Nature, 227, 680.
38. Lam, E., Martin, M. and Wiederrecht, G. (1995) Isolation of a cDNA encoding a novel human FK506-binding protein homolog containing leucine zipper and tetratricopeptide repeat motifs. Gene, 160, 297-302.
39. Lamb, J.R., Tugendreich, S. and Hieter, P. (1995) Tetratrico peptide repeat interactions - To TPR or not to TPR. Trends Biochem. Sci. 20, 257-259.
40. Landrieu, I., De Veylder, L., Fruchart, J.S., Odaert, B., Casteels, P., Portetelle, D., Van Montagu, M., Inze, D. and Lippens, G. (2000) The Arabidopsis thaliana Pin1At gene encodes a single-domain phosphorylation-dependent peptidyl prolyl cis/trans isomerase. J. Biol. Chem. 275, 10577-10581.
41. Li, J.M. and Nam, K.H. (2002) Regulation of brassinosteroid signaling by a GSK3/SHAGGY-like kinase. Science, 295, 1299-1301.
42. Li, J.M., Nam, K.H., Vafeados, D. and Chory, J. (2001) Bin2, a new brassinosteroid-insensitive locus in Arabidopsis. Plant Physiol. 127, 14-22.
43. Liang, L., Lim, K.L., Seow, K.T., Ng, C.H. and Pallen, C.J. (2000) Calmodulin binds to and inhibits the activity of the membrane distal catalytic domain of receptor protein-tyrosine phosphatase alpha. J. Biol. Chem. 275, 30075-30081.
44. Lu, P.J., Zhou, X.Z., Shen, M.H. and Lu, K.P. (1999) Function of WW domains as phosphoserine- or phosphothreonine-binding modules. Science, 283, 1325-1328.
45. Massol, N., Lebeau, M.C., Renoir, J.M., Faber, L.E. and Baulieu, E.E. (1992) Rabbit FKBP59-heat shock protein binding immunophillin (HBI) is a calmodulin binding protein. Biochem. Biophys. Res. Commun. 187, 1330-1335.
46. Metzner, M., Stoller, G., Rücknagel, K.P., Lu, K.P., Fischer, G., Luckner, M. and Küllertz, G. (2001) Functional replacement of the essential Ess1 in yeast by the plant parvulin D/Par13. J. Biol. Chem. 276, 13524-13529.
47. Michnick, S.W., Rosen, M.K., Wandless, T.J., Karplus, M. and Schreiber, S.L. (1991) Solution structure of FKBP, a rotamase enzyme and receptor for FK506 and rapamycin. Science, 252, 836-839.
48. Milioni, D. and Hatzopoulos, P. (1997) Genomic organization of Hsp90 gene family in Arabidopsis. Plant Mol. Biol. 35, 955-961.
49. Mondragon, A., Griffith, E.C., Sun, L., Xiong, F., Armstrong, C. and Liu, J.O. (1997) Overexpression and purification of human calcineurin alpha from Escherichia coli and assessment of catalytic functions of residues surrounding the binuclear metal center. Biochemistry, 36, 4934-4942.
50. Moorthy, A.K., Gopal, B., Satish, P.R., Bhattacharya, S., Bhattacharya, A., Murthy, M.R. and Surolia, A. (1999) Thermodynamics of target peptide recognition by calmodulin and a calmodulin analogue: Implications for the role of the central linker. FEBS Lett. 461, 19-24.
51. Müssig, C. and Altmann, T. (2001) Brassinosteroid signaling in plants. Trends Endocrin. Met. 12, 398-402.
52. Nair, S., Rimerman, R., Toran, E., Chen, S., Prapapanich, V., Butts, R. and Smith, D. (1997) Molecular cloning of human FKBP51 and comparisons of immunophilin interactions with Hsp90 and progesterone receptor. Mol. Cell. Biol. 17, 594-603.
53. Neumann, D., zur Nieden, U., Manteuffel, R., Walter, G., Scharf, K.D. and Nover, L. (1987) Intracellular localization of heat-shock proteins in tomato cell cultures. Eur. J. Cell Biol. 43, 71-81.
54. Oh, M.H., Ray, W.K., Huber, S.C., Asara, J.M., Gage, D.A. and Clouse, S.D. (2000) Recombinant brassinosteroid insensitive 1 receptor-like kinase autophosphorylates on serine and threonine residues and phosphorylates a conserved peptide motif in vitro. Plant Physiol. 124, 751-765.
55. Owens-Grillo, J.K., Stancato, L.F., Hoffmann, K., Pratt, W.B. and Krishna, P. (1996) Binding of immunophilins to the 90 kDa heat shock protein (Hsp90) via a tetratricopeptide repeat domain is a conserved protein interaction in plants. Biochemistry, 35, 15249-15255.
56. Pedersen, K.M., Finsen, B., Celis, J.E. and Jensen, N.A. (1999) muFKBP38: A novel murine immunophilin homolog differentially expressed in Schwannoma cells and central nervous system neurons in vivo. Electrophoresis, 20, 249-255.
57. Perez-Perez, J.M., Ponce, M.R. and Micol, J.L. (2001a) Mutations in the ULTRACURVATA2 gene of Arabidopsis thaliana, which encodes a FKBP-like protein, cause dwarfism, leaf epinasty and helical rotation of several organs. Int. J. Dev. Biol. 45, S49-S50.
58. Perez-Perez, J.M., Ponce, M.R. and Micol, J.L. (2001b) ULTRACURVATA1, a SHAGGY-like Arabidopsis gene required for cell elongation. Int. J. Dev. Biol. 45, S51-S52.
59. Perez-Perez, J.M., Ponce, M.R. and Micol, J.L. (2002) The UCU1 Arabidopsis gene encodes a SHAGGY/GSK3-like kinase required for cell expansion along the proximodistal axis. Dev. Biol. 242, 161-173.
60. Pierce, M.M., Raman, C.S. and Nall, B.T. (1999) Isothermal titration calorimetry of protein-protein interactions. Methods - A Companion to Methods in Enzymology, 19, 213-221.
61. Pirkl, F. and Buchner, J. (2001) Functional analysis of the Hsp90-associated human peptidyl prolyl cis/trans isomerases FKBP51, FKBP52 and cyp40. J. Mol. Biol. 308, 795-806.
62. Pirkl, F., Fischer, E., Modrow, S. and Buchner, J. (2001) Localization of the chaperone domain of FKBP52. J. Biol. Chem. 276, 37034-37041.
63. Pratt, W.B. (1998) The Hsp90-based chaperone system - Involvement in signal transduction from a variety of hormone and growth factor receptors. Proc. Soc. Exp. Biol. Med. 217, 420-434.
64. Pratt, W.B. and Toft, D.O. (1997) Steroid receptor interactions with heat shock protein and immunophilin chaperones. Endocrin. Rev. 18, 306-360.
65. Pratt, W.B., Krishna, P. and Olsen, L.J. (2001) Hsp90-binding immunophilins in plants: The protein movers. Trends Plant Sci. 6, 54-58.
66. Reddy, R.K., Kurek, I., Silverstein, A.M., Chinkers, M., Breiman, A. and Krishna, P. (1998) High-molecular-weight FK506-binding proteins are components of heat-shock protein 90 heterocomplexes in wheat germ lysate. Plant Physiol. 118, 1395-1401.
67. Richter, K. and Buchner, J. (2001) Hsp90: Chaperoning signal transduction. J. Cell. Physiol. 188, 281-290.
68. Scheufler, C., Brinker, A., Bourenkov, G., Pegoraro, S., Moroder, L., Bartunik, H., Hartl, F.U. and Moarefi, I. (2000) Structure of TPR domain-peptide complexes: Critical elements in the assembly of the Hsp70-Hsp90 multichaperone machine. Cell, 101, 199-210.
69. Schiene, C. and Fischer, G. (2000) Enzymes that catalyse the restructuring of proteins. Curr. Opin. Struct. Biol. 10, 40-45.
70. Schiene-Fischer, C. and Yu, C. (2001) Receptor accessory folding helper enzymes: The functional role of peptidyl prolyl cis/trans isomerases. FEBS Lett. 495, 1-6.
71. Schmid, F.X., Frech, C., Scholz, C. and Walter, S. (1996) Catalyzed and assisted protein folding of ribonuclease T1. Biol. Chem. 377, 417-424.
72. Schmidt, B.M.W., Gerdes, D., Feuring, M., Falkenstein, E., Christ, M. and Wehling, M. (2000) Rapid, nongenomic steroid actions: A new age?. Front. Neuroendocrinol. 21, 57-94.
73. Schultz, J., Milpetz, F., Bork, P. and Ponting, C.P. (1998) SMART, a simple modular architecture research tool: Identification of signaling domains. Proc. Natl Acad. Sci. USA, 95, 5857-5864.
74. Schultz, J., Copley, R.R., Doerks, T., Ponting, C.P. and Bork, P. (2000) SMART: A web-based tool for the study of genetically mobile domains. Nucl. Acids Res. 28, 231-234.
75. Shou, W.N., Aghdasi, B., Armstrong, D.L. et al. (1998) Cardiac defects and altered ryanodine receptor function in mice lacking FKBP12. Nature, 391, 489-492.
76. Siekierka, J.J., Hung, S.H., Poe, M., Lin, C.S. and Sigal, N.H. (1989) A cytosolic binding protein for the immunosuppressant FK506 has peptidyl-prolyl isomerase activity but is distinct from cyclophilin. Nature, 341, 755-757.
77. Silverstein, A.M., Galigniana, M.D., Kanelakis, K.C., Radanyi, C., Renoir, J.M. and Pratt, W.B. (1999) Different regions of the immunophilin FKBP52 determine its association with the glucocorticoid receptor, hsp90, and cytoplasmic dynein. J. Biol. Chem. 274, 36980-36986.
78. Song, Q., Alnemri, E.S., Litwack, G. and Gilbert, L.I. (1997) An immunophilin is a component of the insect ecdysone receptor (EcR) complex. Insect Biochem. Mol. Biol. 27, 973-982.
79. Stancato, L.F., Hutchison, K.A., Krishna, P. and Pratt, W.B. (1996) Animal and plant cell lysates share a conserved chaperone system that assembles the glucocorticoid receptor into a functional heterocomplex with Hsp90. Biochemistry, 35, 554-561.
80. Taylor, P., Dornan, J., Carrello, A., Minchin, R.F., Ratajczak, T. and Walkinshaw, M.D. (2001) Two structures of cyclophilin 40: Folding and fidelity in the TPR domains. Structure, 9, 431-438.
81. Thompson, J.D., Higgins, D.G. and Gibson,T.J. (1994) clustalW-improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucl. Acids Res. 22, 4673-4680.
82. 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. Modulation by FKBP mutants deficient in peptidyl-prolyl isomerase activity. J. Biol. Chem. 270, 2451-2459.
83. Tradler, T., Stoller, G., Rücknagel, K.P., Schierhorn, A., Rahfeld, J.-U. and Fischer, G. (1997) Comparative mutational analysis of peptidyl prolyl cis/trans isomerases: active sites of Escherichia coli trigger factor and human FKBP12. FEBS Lett. 407, 184-190.
84. Uchida, T., Fujimori, F., Tradler, T., Fischer, G. and Rahfeld, J.U. (1999) Identification and characterization of a 14 kDa human protein as a novel parvulin-like peptidyl prolyl cis/trans isomerase. FEBS Lett. 446, 278-282.
85. Vener, A.V. (2001) Peptidyl-prolyl isomerases and regulation of photosynthetic functions. Regul. Photosynth. 11, 177-193.
86. Vittorioso, P., Cowling, R., Faure, J.D., Caboche, M. and Bellini, C. (1998) Mutation in the Arabidopsis Pasticcino1 gene, which encodes a new FK506-binding protein-like protein, has a dramatic effect on plant development. Mol. Cell. Biol. 18, 3034-3043.
87. Vucich, V.A. and Gasser, C.S. (1996) Novel structure of a high molecular weight FK506 binding protein from Arabidopsis thaliana. Mol. Gen. Genet. 252, 510-517.
88. Wang, Z.Y., Seto, H., Fujioka, S., Yoshida, S. and Chory, J. (2001) BRI1 is a critical component of a plasma-membrane receptor for plant steroids. Nature, 410, 380-383.
89. Woody, R.W. (1995) Circular dichroism. Meth. Enzymol. 246, 34-71.
90. Yin, Y.H., Wang, Z.Y., Mora-Garcia, S., Li, J.M., Yoshida, S., Asami, T. and Chory, J. (2002) BES1 accumulates in the nucleus in response to brassinosteroids to regulate gene expression and promote stem elongation. Cell, 109, 181-191.
91. Young, J.C., Obermann, W.M.J. and Hartl, F.U. (1998) Specific binding of tetratricopeptide repeat proteins to the C-Terminal 12-kDa domain of Hsp90. J. Biol. Chem. 273, 18007-18010.