Regulation of peptide bond cis/trans isomerization by enzyme catalysis and its implication in physiological processes

  • G. FischerEmail author
  • T. Aumüller
Part of the Reviews of Physiology, Biochemistry and Pharmacology book series (REVIEWS, volume 148)


In some cases, the slow rotational movement underlying peptide bond cis/trans isomerizations is found to control the biological activity of proteins. Peptide bond cis/trans isomerases as cyclophilins, Fk506-binding proteins, parvulins, and bacterial hsp70 generally assist in the interconversion of the polypeptide substrate cis/trans isomers, and rate acceleration is the dominating mechanism of action in cells. We present evidence disputing the hypothesis that some of the molecular properties of these proteins play an auxiliary role in enzyme function.


Peptide Bond Trigger Factor FK506 Binding Protein Peptidyl Prolyl Isomerase PPIase Activity 
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  1. Aghdasi B, Ye K, Q, Resnick A, Huang A, Ha HC, Guo X, Dawson TM, Dawson VL, Snyder SH (2001) FKBP12, the 12-kDa FK506-binding protein, is a physiologic regulator of the cell cycle. Proc Natl Acad Sci USA 98:2425–2430PubMedGoogle Scholar
  2. Allain F, Vanpouille C, Carpentier M, Slomianny MC, Durieux S, Spik G (2002) Interaction with glycosaminoglycans is required for cyclophilin B to trigger integrin-mediated adhesion of peripheral blood T lymphocytes to extracellular matrix. Proc Natl Acad Sci USA 99:2714–2719PubMedGoogle Scholar
  3. Andreeva L, Motterlini R, Green CJ (1997) Cyclophilins are induced by hypoxia and heat stress in myogenic cells. Biochem Biophys Res Commun 237:6–9PubMedGoogle Scholar
  4. Ansari H, Greco G, Luban J (2002) Cyclophilin a peptidyl prolyl isomerase activity promotes ZPR1 nuclear export. Mol Cell Biol 22:6993–7003PubMedGoogle Scholar
  5. Arevalo-Rodriguez M, Cardenas ME, Wu XY, Hanes SD, Heitman J (2000) Cyclophilin A and Ess1 interact with and regulate silencing by the Sin3-Rpd3 histone deacetylase. EMBO J 19:3739–3749PubMedGoogle Scholar
  6. Arie JP, Sassoon N, Betton JM (2001) Chaperone function of FkpA, a heat shock prolyl isomerase, in the periplasm of Escherichia coli. Mol Microbiol 39:199–210PubMedGoogle Scholar
  7. Asea A, Kraeft SK, Kurt-Jones EA, Stevenson MA, Chen LB, Finberg RW, Koo GC, Calderwood, SK (2000) HSP70 stimulates cytokine production through a CD14-dependant pathway, demonstrating its dual role as a chaperone and cytokine. Nat Med 6:435–442PubMedGoogle Scholar
  8. Bächinger HP (1987) The influence of peptidyl prolyl cis/trans isomerase on the in vitro folding of type III collagen. J Biol Chem 262:17144–17148PubMedGoogle Scholar
  9. Baine P (1986) Comparison of rate constants determined by two-dimensional NMR spectroscopy with rate constants determined by other NMR techniques. Magn Reson Chem 24:304–307Google Scholar
  10. Balbach J, Steegborn C, Schindler T, Schmid FX (1999) A protein folding intermediate of ribonuclease T1 characterized at high resolution by 1D and 2D real-time NMR spectroscopy. J Mol Biol 285:829–42PubMedGoogle Scholar
  11. Barthelmess IB, Tropschug M (1993) FK506-binding protein of Neurospora crassa (NcFKBP) mediates sensitivity to the immunosuppressant FK506 resistant mutants identify two loci. Curr Genet 23:54–58PubMedGoogle Scholar
  12. Bartz SR, Hohenwalter E, Hu MK, Rich DH, Malkovsky M (1995) Inhibition of human immunodeficiency virus replication by nonimmunosuppressive analogs of cyclosporine A. Proc Natl Acad Sci USA 92:5381–5385PubMedGoogle Scholar
  13. Bassing CH, Shou WN, Muir S, Heitman J, Matzuk MM, Wang XF (1998) FKBP12 is not required for the modulation of transforming growth factor β receptor I signaling activity in embryonic fibroblasts and thymocytes. Cell Growth Differ 9:223–228PubMedGoogle Scholar
  14. Batiuk TD, Kung LN, Halloran PF (1997) Evidence that calcineurin is rate-limiting for primary human lymphocyte activation. J Clin Invest 100:1894–1901PubMedGoogle Scholar
  15. Batiuk TD, Pazderka F, Halloran PF (1995) Calcineurin activity is only partially inhibited in leukocytes of cyclosporine-treated patients. Transplantation 59: 1400–1404PubMedGoogle Scholar
  16. Batiuk TD, Urmson, J, Vincent D, Yatscoff RW, Halloran PF (1996) Quantitating immunosuppression. Estimating the 50% inhibitory concentration for in vivo cyclosporine in mice. Transplantation 61:1618–1624PubMedGoogle Scholar
  17. Baumgraβ R, Weiwad M, Erdmann F, Liu JO, Wunderlich D, Grabley S, Fischer G (2001) Reversible inhibition of calcineurin by the polyphenolic aldehyde gossypol. J Biol Chem 276:47914–47921Google Scholar
  18. Behrens S, Maier R, de Cock H, Schmid FX, Gross CA (2001) The SurA periplasmic PPlase lacking its parvulin domains functions in vivo and has chaperone activity. EMBO J 20:285–294PubMedGoogle Scholar
  19. Bennett PC, Singaretnam LG, Zhao WQ, Lawen A, Ng KT (1998) Peptidyl prolyl cis/trans isomerase activity may be necessary for memory formation. FEBS Lett 431:386–390PubMedGoogle Scholar
  20. Bernhardt TG, Roof WD, Young R (2002) The Escherichia coli FKBP-type PPIase SlyD is required for the stabilization of the E lysis protein of bacteriophage phi X174. Mol Microbiol 45:99–108PubMedGoogle Scholar
  21. Binsch G (1969) A unified theory of exchange effects on nuclear magnetic resonance line shapes. J Am Chem Soc 91: 1304–1309Google Scholar
  22. Bitto E, McKay DB (2002) Crystallographic structure of SurA, a molecular chaperone that facilitates folding of outer membrane proteins. Structure 10:1489–1498PubMedGoogle Scholar
  23. Bosco DA, Eisenmesser EZ, Pochapsky S, Sundquist WI, Kern D (2002) Catalysis of cis/trans isomerization in native HIV-1 capsid by human cyclophilin A. Proc Natl Acad Sci USA 99:5247–5252PubMedGoogle Scholar
  24. Bose S, Weikl T, Bugl H, Buchner J (1996) Chaperone function of hsp90-associated proteins. Science 274:1715–1717PubMedGoogle Scholar
  25. Braaten D, Luban J (2001) Cyclophilin A regulates HIV-1 infectivity, as demonstrated by gene targeting in human T cells. EMBO J 20:1300–1309PubMedGoogle Scholar
  26. Brandts JF, Halvorson HR, Brennan M (1975) Consideration of the possibility that the slow step in protein denaturation reactions is due to cis/trans isomerism of proline residues. Biochemistry 14:4953–4963PubMedGoogle Scholar
  27. Brown EJ, Albers MW, Shin TB, Ichikawa K, Keith CT, Lane WS, Schreiber SL (1994) A mammalian protein targeted by G1-arresting rapamycin-eceptor complex. Nature 369:756–758PubMedGoogle Scholar
  28. Bueno OF, Brandt EB, Rothenberg ME, Molkentin JD (2002) Defective T cell development and function in calcineurin A β-deficient mice. Proc Natl Acad Sci USA 99:9398–9403PubMedGoogle Scholar
  29. Bukrinsky MI (2002) Cyclophilins: unexpected messengers in intercellular communications. Trends Immunol 23:323–325PubMedGoogle Scholar
  30. Burbaum JJ, Raines RT, Albery WJ, Knowles JR (1989) Evolutionary optimization of the catalytic effectiveness of an enzyme. Biochemistry 28:9293–9305PubMedGoogle Scholar
  31. Capano M, Virji S, Crompton M (2002) Cyclophilin-A is involved in excitotoxin-induced caspas activation in rat neuronal B50 cells. Biochem J 363:29–36PubMedGoogle Scholar
  32. Carpentier M, Allain F, Slomianny MC, Durieux S, Vanpouille C, Haendler B, Spik G (2002) Receptor type I and type II binding regions and the peptidyl prolyl isomerase site of cyclophilin B are required for enhancement of T-lymphocyte adhesion to fibronectin. Biochemistry 41:5222–5229PubMedGoogle Scholar
  33. Carter P, Wells JA (1987) Engineering enzyme specificity by “substrate-assisted catalysis” Science 237:394–399PubMedGoogle Scholar
  34. Chen YG, Liu F, Massague J (1997) Mechanism of TGF-β receptor inhibition by FKBP12. EMBO J 16:3866–3876PubMedGoogle Scholar
  35. Chiti F, Taddei N, Giannoni E, van Nuland NAJ, Ramponi G, Dobson CM (1999) Development of enzymatic activity during protein folding—detection of a spectroscopically silent native-like intermediate of muscle acylphosphatase. J Biol Chem 274:20151–20158PubMedGoogle Scholar
  36. Chow KC, Tung WL (1998) Overexpression of dnaK/dnaJ and groEL confers freeze tolerance to Escherichia coli. Biochem Biophys Res Commun 253:502–505PubMedGoogle Scholar
  37. Christner C, Herdegen D, Fischer G (2001) FKBP ligands as novel therapeutics for neurological disorders. Mini Rev Med Chem 1:377–397PubMedGoogle Scholar
  38. Cianciotto NP, Fields BS (1992) Legionella-Pneumophila-MIP gene potentiates intracellular infection of protozoa and human macrophages. Proc Natl Acad Sci USA 89:5188–5191PubMedGoogle Scholar
  39. Clarke SJ, McStay GP, Halestrap AP (2002) Sanglifehrin A acts as a potent inhibitor of the mitochondrial permeability transition and reperfusion injury of the heart by binding to cyclophilin-D at a different site from cyclosporin A. J Biol Chem 277:34793–34799PubMedGoogle Scholar
  40. Colgan J, Asmal M, Luban J (2000) Isolation, characterization and targeted disruption of mouse Ppia: Cyclophilin A is not essential for mammalian cell viability. Genomics 68:167–178PubMedGoogle Scholar
  41. Counterman AE, Clemmer DE (2002) Cis/trans signatures of proline-containing tryptic peptides in the gas phase. Anal Chem 74:1946–1951PubMedGoogle Scholar
  42. Cristillo AD, Bierer BE (2002) Identification of novel targets of immunosuppressive agents by cDNA-based microarray analysis. J Biol Chem 277:4465–4476PubMedGoogle Scholar
  43. Dartigalongue C, Missiakas D, Raina S (2001) Characterization of the Escherichia coli sigma E regulon. J Biol Chem 276:20866–20875PubMedGoogle Scholar
  44. Dartigalongue C, Raina S (1998) A new heat shock gene PpiD, encodes a peptidyl prolyl isomerase required for folding of outer membrane proteins in E. coli. EMBO J 17:3968–3980PubMedGoogle Scholar
  45. Davis JM, Boswell BA, Bachinger HP (1989) Thermal stability and folding of type IV procollagen and effect of peptidyl-prolyl cis-trans-isomerase on the folding of the triple helix. J Biol Chem 264:8956–8962PubMedGoogle Scholar
  46. de Crouy-Chanel A, Kohiyama M, Richarme G (1999) Interaction of DnaK with native proteins and membrane proteins correlates with their accessible hydrophobicity. Gene 230:163–170PubMedGoogle Scholar
  47. Deuerling E, Schulze-Specking A, Tomoyasu T, Mogk A, Bukau B (1999) Trigger factor and DnaK cooperate in folding of newly synthesized proteins. Nature 400:693–696PubMedGoogle Scholar
  48. Devasahayam G, Chaturvedi V, Hanes SD (2002) The ess1 prolyl isomerase is required for growth and morphogenetic switching in Candida albicans. Genetics 160:37–48PubMedGoogle Scholar
  49. Dobson CM, Sali A, Karplus M (1998) Protein folding—a perspective from theory and experiment. Angew Chem Intern Ed Engl 37:868–893Google Scholar
  50. Dolinski K, Muir S, Cardenas M, Heitman J (1997) All cyclophilins and FK506 binding proteins are, individually and collectively, dispensable for viability in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 94:13093–13098PubMedGoogle Scholar
  51. Enghild JJ, Valnickova Z, Thogersen IB, Pizzo SV (1994) Complexes between serpins and inactive proteinases are not thermodynamically stable but are recognized by serpin receptors. J Biol Chem 269:20159–20166PubMedGoogle Scholar
  52. Evans PA, Kautz RA, Fox RO, Dobson CM (1989) A magnetization-transfer nuclear magnetic resonance study of the folding of staphylococcal nuclease. Biochemistry 28:362–70PubMedGoogle Scholar
  53. Fischer G (1994a) Peptidyl prolyl cis/trans isomerases and their effectors. Angew Chem Intern Ed Engl 33:1415–1436Google Scholar
  54. Fischer G, Bang H, Berger E, Schellenberger A (1984a) Conformational specificity of chymotrypsin toward proline-containing substrates. Biochim Biophys Acta 791:87–97PubMedGoogle Scholar
  55. Fischer G, Bang H, Mech C (1984b) Determination of enzymatic catalysis for the cis/trans isomerization of peptide bonds in proline-containing peptides. Biomed Biochim Acta 43:1101–1111PubMedGoogle Scholar
  56. Fischer G, Heins J, Barth A (1983) The conformation around the peptide bond between the P1-and P2-positions is important for catalytic activity of some proline-specific proteases. Biochim Biophys Acta 742:452–462PubMedGoogle Scholar
  57. Fischer G, Schutkowski M, Küllertz G (2001) Peptidic substrates for directly assaying enzyme activities. Pat. No. DE 100 23743 A1Google Scholar
  58. Fischer G, Tradler T, Zarnt T (1998) The mode of action of peptidyl prolyl cis/trans isomerases in vivo: binding versus catalysis. FEBS Lett 426:17–20PubMedGoogle Scholar
  59. Fischer G, Wittmann Liebold B, Lang K, Kiefhaber T, Schmid FX (1989) Cyclophilin and peptidyl-prolyl cis/trans isomerases are probably identical proteins. Nature 337:476–478PubMedGoogle Scholar
  60. Fischer G, Wöllner S, Schönbrunner R, Scherer G (1994b) Inhibitors for Peptidyl prolyl cis/trans isomerases. Proceedings of the 5th Akabori Conference, Max-Planck Society, Dresden, pp 142–145Google Scholar
  61. Franke EK, Luban J (1996) Inhibition of HIV-1 replication by cyclosporin A or related compounds correlates with the ability to disrupt the gag-cyclophilin A interaction. Virology 222:279–282PubMedGoogle Scholar
  62. Freeman BC, Toft DO, Morimoto RI (1996) Molecular chaperone machines—chaperone activities of the cyclophilin Cyp-40 and steroid receptor associated protein p24. Science 274:1718–1720PubMedGoogle Scholar
  63. Friedman J, Weissman I (1991) Two cytoplasmic candidates for immunophilin action are revealed by affinity for a new cyclophilin—one in the presence and one in the absence of CsA. Cell 66:799–806PubMedGoogle Scholar
  64. Frydman J (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Ann Rev Biochem 70:603–647PubMedGoogle Scholar
  65. Fujimori F, Gunji W, Kikuchi J, Mogi T, Ohashi Y, Makino T, Oyama A, Okuhara K, Uchida T, Murakami Y (2001) Crosstalk of prolyl isomerases, Pin1/Ess1, and cyclophilin A. Biochem Biophys Res Commun 289:181–190PubMedGoogle Scholar
  66. Fujimori F, Takahashi K, Uchida C, Uchida T (1999) Mice lacking Pin1 develop normally, but are defective in entering cell cycle from G(0) arrest. Biochem Biophys Res Commun 265:658–663PubMedGoogle Scholar
  67. Fuller TE, Martin S, Teel JF, Alaniz GR, Kennedy MJ, Lowery DE (2000) Identification of Actinobacillus pleuropneumoniae virulence genes using signature-tagged mutagenesis in a swine infection model. Microb Pathog 29: 39–51PubMedGoogle Scholar
  68. Furutani M, Ideno A, Iida T, Maruyama T (2000) FK506 binding protein from a thermophilic archaeon, Methanococcus thermolithotrophicus, has chaperone-like activity in vitro. Biochemistry 39:453–462PubMedGoogle Scholar
  69. Gamble TR, Vajdos FF, Yoo SH, Worthylake DK, Houseweart M, Sundquist WI, Hill CP (1996) Crystal structure of human cyclophilin A bound to the amino-terminal domain of HIV-1 capsid. Cell 87:1285–1294PubMedGoogle Scholar
  70. Garcia-Echeverria C, Kofron JL, Kuzmic P, Kishore V, Rich DH (1992) Continuous flourometric direct (uncoupled) assay for peptidyl prolyl cis/trans isomerases. J Am Chem Soc 114:2758–2759Google Scholar
  71. Garcia-Echeverria C, Kofron JL, Kuzmic P, Rich DH (1993) A continuous spectrophotometric direct assay for peptidyl prolyl cis/trans isomerases. Biochem Biophys Res Commun 191:70–75PubMedGoogle Scholar
  72. Gothel SF, Scholz C, Schmid FX, Marahiel MA (1998) Cyclophilin and trigger factor from Bacillus subtilis catalyze in vitro protein folding and are necessary for viability under starvation conditions. Biochemistry 37:13392–13399PubMedGoogle Scholar
  73. Griffith JP, Kim JL, Kim EE, Sintchak MD, Thomson JA, Fitzgibbon MJ, Fleming MA, Caron PR, Hsiao K, Navia MA (1995) X-ray structure of calcineurin inhibited by the immunophilin-immunosuppressant FKBP12-FK506 complex. Cell 82:507–522PubMedGoogle Scholar
  74. Guthrie B, Wickner W (1990) Trigger factor depletion or overproduction causes defective cell division but does not block protein export. J Bacteriol 172:5555–5562PubMedGoogle Scholar
  75. Halestrap AP, McStay GP, Clarke SJ (2002) The permeability transition pore complex: another view. Biochimie 84:153–166PubMedGoogle Scholar
  76. Halloran PF, Kung L, Noujaim J (1998) Calcineurin and the biological effects of cyclosporine and tacrolimus. Transplant Proc 30:2167–2170PubMedGoogle Scholar
  77. Hani J, Stumpf G, Domdey H (1995) PTF1 encodes an essential protein in Saccharomyces cerevisiae, which shows strong homology with a new putative family of PPIases. FEBS Lett 365:198–202PubMedGoogle Scholar
  78. Hardwick JS, Kuruvilla FG, Tong JK, Shamji AF, Schreiber SL (1999) Rapamycin-modulated transcription defines the subset of nutrient-sensitive signaling pathways directly controlled by the Tor proteins. Proc Natl Acad Sci USA 96:14866–14870PubMedGoogle Scholar
  79. Harrar Y, Bellini C, Faure JD (2001) FKBPs: at the crossroads of folding and transduction. Trends Plant Sci 6:426–431PubMedGoogle Scholar
  80. Hassidim M, Schwarz R, Liemanhurwitz J, Marco E, Ronentarazi M, Kaplan A (1992) A cyanobacterial gene encoding peptidyl prolyl cis/trans isomerase. Plant Physiol 100:1982–1986PubMedGoogle Scholar
  81. Heitman J, Movva NR, Hiestand PC, Hall MN (1991) FK 506-binding protein proline rotamase is a target for the immunosuppressive agent FK 506 in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 88:1948–1952PubMedGoogle Scholar
  82. Herrler M, Bang H, Marahiel MA (1994) Cloning and characterization of Ppib, a Bacillus subtilis gene which encodes a cyclosporin A-sensitive peptidyl prolyl cis/trans isomerase. Mol Microbiol 11:1073–1083PubMedGoogle Scholar
  83. Hesterkamp T, Bukau B (1998) Role of the DnaK and HscA homologs of Hsp70 chaperones in protein folding in E.coli. EMBO J 17:4818–4828PubMedGoogle Scholar
  84. Horne SM, Kottom TJ, Nolan LK, Young KD (1997) Decreased intracellular survival of an fkpA mutant of Salmonella typhimurium Copenhagen. Infect Immun 85:806–810Google Scholar
  85. Horne SM, Young KD (1995) Escherichia coli and other species of the Enterobacteriaceae encode a protein similar to the family of Mip-like FK506-binding proteins. Arch Microbiol 163:357–365PubMedGoogle Scholar
  86. Hsu T, McRackan D, Vincent TS, de Couet HG (2001) Drosophila Pin1 prolyl isomerase Dodo is a MAP kinase signal responder during oogenesis. Nat Cell Biol 3:538–543PubMedGoogle Scholar
  87. Hsu VL, Handschumacher RE, Armitage IM (1990) Peptidyl prolyl cis/trans isomerase activity of cyclophilin studied by one-dimensional 1H nuclear magnetic resonance spectroscopy. J Am Chem Soc 112:6745–6747Google Scholar
  88. Huai Q, Kim HY, Liu YD, Zhao YD, Mondragon A, Liu JO, Ke HM (2002) Crystal structure of calcineurin-cyclophilin-cyclosporin shows common but distinct recognition of immunophilin-drug complexes. Proc Natl Acad Sci USA 99:12037–12042PubMedGoogle Scholar
  89. Huang HK, Forsburg SL, John UP, O’Connell MJ, Hunter T (2001) Isolation and characterization of the Pin1/Ess1p homolog in Schizosaccharomyces pombe. J Cell Sci 114:3779–3788PubMedGoogle Scholar
  90. Hübner D, Drakenberg T, Forsen S, Fischer G (1991) Peptidyl prolyl cis/trans isomerase activity as studied by dynamic proton NMR spectroscopy. FEBS Lett 284:79–81PubMedGoogle Scholar
  91. Huse M, Chen YG, Massague J, Kuriyan J (1999) Crystal structure of the cytoplasmic domain of the type I TGF-β receptor in complex with FKBP12. Cell 96:425–436PubMedGoogle Scholar
  92. Janowski B, Wöllner S, Schutkowski M, Fischer G (1997) A protease free assay for peptidyl prolyl cis/trans isomerases using standard peptide substrates. Anal Biochem 252:299–307PubMedGoogle Scholar
  93. Jiang HS, Xiong F, Kong SM, Ogawa T, Kobayashi M, Liu JO (1997) Distinct tissue and cellular distribution of two major isoforms of calcineurin. Mol Immunol 34:663–669PubMedGoogle Scholar
  94. Jin JG, Melaragno MG, Liao DF, Yan C, Haendeler J, Suh YA, Lambeth JD, Berk BC (2000) Cyclophilin A is a secreted growth factor induced by oxidative stress. Circ Res 87:789–796PubMedGoogle Scholar
  95. Jin L, Harrison SC, (2002) Crystal structure of human calcineurin complexed with cyclosporin A and human cyclophilin. Proc Natl Acad Sci USA 99:13522–13526PubMedGoogle Scholar
  96. Joseph J D, Heitman J, Means AR (1999) Molecular cloning and characterization of Aspergillus nidulans cyclophilin B. Fungal Genet Biol 27:55–66PubMedGoogle Scholar
  97. Kamphausen T, Fanghänel J, Neumann D, Schulz B, Rahfeld JU (2002) Characterization of Arabidopsis thaliana AtFKBP42 that is membrane-bound and interacts with Hsp90. Plant J 32:263–276PubMedGoogle Scholar
  98. Kandror O, Goldberg AL (1997) Trigger factor is induced upon cold shock and enhances viability of Escherichia coli at low temperatures. Proc Natl Acad Sci USA 94:4978–4981PubMedGoogle Scholar
  99. Kern D, Drakenberg T, Wikstrom M, Forsen S, Bang H, Fischer G (1993) The cis/trans interconversion of the calcium regulating hormone calcitonin is catalyzed by cyclophilin. FEBS Lett 323:198–202PubMedGoogle Scholar
  100. Kern D, Kern G, Scherer G, Fischer G, Drakenberg T (1995) Kinetic analysis of cyclophilin-catalyzed prolyl cis/trans isomerization by dynamic NMR spectroscopy. Biochemistry 34:13594–13602PubMedGoogle Scholar
  101. Kern G, Kern D, Schmid FX, Fischer G (1994) Reassessment of the putative chaperone function of prolyl cis/trans isomerases. FEBS Lett 348:145–148PubMedGoogle Scholar
  102. Kiefhaber T, Quaas R, Hahn U, Schmid FX (1990a) Folding of ribonuclease T1. 1. Existence of multiple unfolded states created by proline isomerization. Biochemistry 29:3053–3061PubMedGoogle Scholar
  103. Kiefhaber T, Quaas R, Hahn U, Schmid FX (1990b) Folding of ribonuclease T1. 2. Kinetic models for the folding and unfolding reactions. Biochemistry 29:3061–3070PubMedGoogle Scholar
  104. Kleerebezem M, Heutink M, Tommassen J (1995) Characterization of an Escherichia coli rotA mutant, affected in periplasmic peptidyl prolyl cis/trans isomerase. Mol Microbiol 18:313–320PubMedGoogle Scholar
  105. Kofron JL, Kuzmic P, Kishore V, Colon Bonilla E, Rich DH (1991) Determination of kinetic constants for peptidyl prolyl cis/trans isomerases by an improved spectrophotometric assay. Biochemistry 30:6127–6134PubMedGoogle Scholar
  106. Kok RG, Christoffels VM, Vosman B, Hellingwerf KJ (1994) A gene of Acinetobacter calcoaceticus BD413 encodes a periplasmic peptidyl prolyl cis/trans isomerase of the cyclophilin sub-class that is not essential for growth. Biochim Biophys Acta 1219:601–606PubMedGoogle Scholar
  107. Kontinen VP, Sarvas M (1993) The PrsA lipoprotein is essential for protein secretion in Bacillus subtilis and sets a limit for high-level secretion. Mol Microbiol 8:727–737PubMedGoogle Scholar
  108. Kramer ML, Fischer G (1997) FKBP-like catalysis of peptidyl prolyl bond isomerization by micelles and membranes. Biopolymers 42:49–60Google Scholar
  109. Küllertz G, Lüthe S, Fischer G (1998) Semiautomated microtiter plate assay for monitoring peptidyl prolyl cis/trans isomerase activity in normal and pathological human sera. Clin Chem 44:502–508PubMedGoogle Scholar
  110. Kung L, Halloran PF (2002) Immunophilins may limit calcineurin inhibition by cyclosporine and tacrolimus at high drug concentrations. Transplantation 70:327–335Google Scholar
  111. Kurek I, Aviezer K, Erel N, Herman E, Breiman A (1999) The wheat peptidyl prolyl cis/trans isomerase FKBP77 is heat induced and developmentally regulated. Plant Physiol 119:693–703PubMedGoogle Scholar
  112. Kurek I, Pirkl F, Fischer E, Buchner J, Breiman A (2002) Wheat FKBP73 functions in vitro as a molecular chaperone independently of its peptidyl prolyl cis/trans isomerase activity. Planta 215:119–126PubMedGoogle Scholar
  113. Lang K, Schmid FX, Fischer G (1987) Catalysis of protein folding by prolyl isomerase. Nature 329:268–70PubMedGoogle Scholar
  114. Langer T, Lu C, Echols H, Flanagan J, Hayer MK, Hartl FU (1992) Successive action of DnaK, DnaJ and GroEL along the pathway of chaperone-mediated protein folding. Nature 356:683–689PubMedGoogle Scholar
  115. Lee JP, Palfrey HC, Bindokas VP, Ghadge GD, Ma L, Miller RJ, Roos RP (1999) The role of immunophilins in mutant superoxide dismutase-1-linked familial amyotrophic lateral sclerosis. Proc Natl Acad Sci USA 96:3251–3256PubMedGoogle Scholar
  116. Leiva MC, Lyttle CR (1992) Leukocyte chemotactic activity of FKBP and inhibition by FK506. Biochem Biophys Res Commun 186:1178–1183PubMedGoogle Scholar
  117. Leverson JD, Ness SA (1998) Point mutations in v-myb disrupt cyclophilin-catalyzed negative regulatory mechanism. Mol Cell 1:203–211PubMedGoogle Scholar
  118. Li HB, Oberhauser AF, Redick SD, Carrion-Vazquez M, Erickson HP, Fernandez JM (2001a) Multiple conformations of PEVK proteins detected by single-molecule techniques. Proc Natl Acad Sci USA 98:10682–10686PubMedGoogle Scholar
  119. Li TK, Baksh S, Cristillo AD, Bierer BE (2002) Calcium-and FK506-independent interaction between the immunophilin FKBP51 and calcineurin. J Cell Biochem 84:460–471PubMedGoogle Scholar
  120. Li ZY, Liu CP, Zhu LQ, Jing GZ, Zhou JM (2001b) The chaperone activity of trigger factor is distinct from its isomerase activity during coexpression with adenylate kinase in Escherichia coli. FEBS Lett 506:108–112PubMedGoogle Scholar
  121. Lin DT, Lechleiter JD (2002) Mitochondrial targeted cyclophilin D protects cells from cell death by peptidyl prolyl isomerization. J Biol Chem 277:31134–31141PubMedGoogle Scholar
  122. Lin LN, Brandts JF (1979) Evidence suggesting that some proteolytic enzymes may cleave only the trans form of the peptide bond. Biochemistry 18:43–47PubMedGoogle Scholar
  123. Lin LN, Brandts JF (1985) Isomer-specific proteolysis of model substrates: influence that the location of the proline residue exerts on cis/trans specificity. Biochemistry 24:6533–6538PubMedGoogle Scholar
  124. Lin LN, Hasumi H, Brandts JF (1988) Catalysis of proline isomerization during protein-folding reactions. Biochim Biophys Acta 956:256–266PubMedGoogle Scholar
  125. Liou YC, Ryo A, Huang HK, Lu PJ, Bronson R, Fujimori F, Uchida T, Hunter T, Lu KP (2002) Loss of Pin1 function in the mouse causes phenotypes resembling cyclin D1-null phenotypes. Proc Natl Acad Sci USA 99:1335–1340PubMedGoogle Scholar
  126. Liu J, Farmer JD, Jr. Lane WS, Friedman J, Weissman I, Schreiber SL (1991) Calcineurin is a common target of cyclophilin-cyclosporin A and FKBP-FK506 complexes. Cell 66:807–815PubMedGoogle Scholar
  127. London RE, Davis DG, Vavrek RJ, Stewart JM, Handschumacher RE (1990) Bradykinin and its Gly6 analog are substrates of cyclophilin: a fluorine-19 magnetization transfer study. Biochemistry 29:10298–10302PubMedGoogle Scholar
  128. Lopezilasaca M, Schiene C, Küllertz G, Tradler T, Fischer G, Wetzker R (1998) Effects of FK506 binding protein 12 and FK506 on autophosphorylation of epidermal growth factor receptor. J Biol Chem 273:9430–9434Google Scholar
  129. Lu KP, Liou YC, Zhou XZ (2002) Pinning down proline-directed phosphorylation signaling. Trends Cell Biol 12:164–172PubMedGoogle Scholar
  130. Lu PJ, Zhou XZ, Shen MH, Lu KP (1999) Function of WW domains as phosphoserine-or phosphothreonine-binding modules. Science 283:1325–1328PubMedGoogle Scholar
  131. Luban J (1996) Absconding with the chaperone—essential cyclophilin gag interaction in HIV-1 virions. Cell 87:1157–1159PubMedGoogle Scholar
  132. Lyon WR, Gibson CM, Caparon MG (1998) A role for trigger factor and rgg-like regulator in the transcription, secretion and processing of the cysteine proteinase of Streptococcus pyogenes. EMBO J 17:6263–6275PubMedGoogle Scholar
  133. MacArthur MW, Thornton JM (1991) Influence of proline residues on protein conformation. J Mol Biol 218:397–412PubMedGoogle Scholar
  134. Maier R, Scholz C, Schmid FX (2001) Dynamic association of trigger factor with protein substrates. J Mol Biol 314:1181–1190PubMedGoogle Scholar
  135. Maleszka R, Hanes SD, Hackett RL, deCouet HG, Miklos GLG (1996) The Drosophila melanogaster dodo (dod) gene, conserved in humans, is functionally interchangeable with the ESS1 cell division gene of Saccharomyces. Proc Natl Acad Sci USA 93:447–451PubMedGoogle Scholar
  136. Mallis RJ, Brazin KN, Fulton DB, Andreotti AH (2002) Structural characterization of a proline-driven conformational switch within the Itk SH2 domain. Nat Struct Biol 9:900–905PubMedGoogle Scholar
  137. Mamane Y, Sharma S, Petropoulos L, Lin RT, Hiscott J (2000) Posttranslational regulation of IRF-4 activity by the immunophilin FKBP52. Immunity 12:129–140PubMedGoogle Scholar
  138. Marivet J, Frendo P, Burkard G (1992) Effects of abiotic stresses on cyclophilin gene expression in maize and bean and sequence analysis of bean cyclophilin cDNA. Plant Sci 84:171–178Google Scholar
  139. Mayr LM, Odefey C, Schutkowski M, Schmid FX (1996) Kinetic analysis of the unfolding and refolding of ribonuclease T1 by stopped-flow double-mixing technique. Biochemistry 35:5550–5561PubMedGoogle Scholar
  140. Mayr LM, Schmid FX (1993) Kinetic models for unfolding and refolding of ribonuclease T1 with substitution of cis-proline 39 by alanine. J Mol Biol 231:913–926PubMedGoogle Scholar
  141. Mayr LM, Willbold D, Rosch P, Schmid FX (1994) Generation of a nonprolyl cis peptide bond in ribonuclease T1. J Mol Biol 240:288–293PubMedGoogle Scholar
  142. McCarthy AA, Haebel PW, Torronen A, Rybin V, Baker EN, Metcalf P (2000) Crystal structure of the protein disulfide bond isomerase, DsbC, from Escherichia coli. Nat Struct Biol 7:196–199PubMedGoogle Scholar
  143. McCornack MA, Kakalis LT, Caserta C, Handschumacher RE, Armitage IM (1997) HIV protease substrate conformation—modulation by cyclophilin A. FEBS Lett 414:84–88PubMedGoogle Scholar
  144. Meng X, Lu XJ, Morris CA, Keating MT (1998) Novel human gene FKBP6 is deleted in Williams-syndrome. Genomics 52:130–137PubMedGoogle Scholar
  145. Merker MP, Dawson CA (1995) Cyclophilin-facilitated bradykinin inactivation in the perfused rat lung. Biochem Pharmacol 50:2085–2091PubMedGoogle Scholar
  146. Merker MP, Dawson CA, Bongard RD, Roerig DL, Haworth ST, Linehan JH (1993) Angiotensin-converting enzyme preferentially hydrolyzes trans isomer of proline-containing substrate. J Appl Physiol 75:1519–1524PubMedGoogle Scholar
  147. Meyer S, Jabs A, Schutkowski M, Fischer G (1994) Separation of cis/trans isomers of a prolyl peptide bond by capillary zone electrophoresis. Electrophoresis 15:1151–1157PubMedGoogle Scholar
  148. Mihatsch MJ, Kyo M, Morozumi K, Yamaguchi Y, Nickeleit V, Ryffel B (1998) The side effects of cyclosporin A and tacrolimus. Clin Nephrol 49:356–363PubMedGoogle Scholar
  149. Montague JW, Gaido ML, Frye C, Cidlowski JA (1994) A calcium-dependent nuclease from apoptotic rat thymocytes is homologous with cyclophilin-recombinant cyclophilins A, B, and C have nuclease activity. J Biol Chem 269:18877–18880PubMedGoogle Scholar
  150. Moritz R, Reinstadler D, Fabian H, Naumann D (2002) Time-resolved FTIR difference spectroscopy as tool for investigating refolding reactions of ribonuclease T1 synchronized with trans to cis prolyl isomerization. Biopolymers 67:145–155PubMedGoogle Scholar
  151. Mücke M, Schmid FX (1992) Enzymatic catalysis of prolyl isomerization in an unfolding protein. Biochemistry 31:7848–7854PubMedGoogle Scholar
  152. Navia MA (1996) Protein-drug complexes important for immunoregulation and organ transplantation. Curr Opin Struct Biol 6:838–847PubMedGoogle Scholar
  153. Odefey C, Mayr LM, Schmid FX (1995) Nonprolyl cis/trans peptide bond isomerization as a rate-determining step in protein unfolding and refolding. J Mol Biol 245:69–78PubMedGoogle Scholar
  154. Ohta T, Ishimura K, Takitanis S (1993) Selective online enrichment and separation of peptides having aromatic amino acids at their C-termini by column switching using an anhydrochymotrypsin-immobilized precolumn. J Chromatogr 637: 35–41PubMedGoogle Scholar
  155. Olson ST, Bock PE, Kvassman J, Shore JD, Lawrence DA, Ginsburg D, Bjork I (1995) Role of the catalytic serine in the interactions of serine proteinases with protein inhibitors of the serpin family. Contribution of a covalent interaction to the binding energy of serpin-proteinase complexes. J Biol Chem 270:30007–30017PubMedGoogle Scholar
  156. Ou WB, Luo W, Park YD, Zhou HM (2000) Chaperone-like activity of peptidyl prolyl cis/trans isomerase during creatine kinase refolding. Protein Sci 10:2346–2353Google Scholar
  157. Paek KH, Walker GC (1987) Escherichia coli DnaK null mutants are inviable at high temperature. J Bacteriol 169:283–290PubMedGoogle Scholar
  158. Pappenberger G, Aygun H, Engels JW, Reimer U, Fischer G, Kiefhaber T (2001) Nonprolyl cis peptide bonds in unfolded proteins cause complex folding kinetics. Nat Struct Biol 8:452–458PubMedGoogle Scholar
  159. Patzelt H, Rüdiger S, Brehmer D, Kramer G, Vorderwulbecke S, Schaffitzel E, Waitz A, Hesterkamp T, Dong L, Schneider-Mergener J, Bukau B (2001) Binding specificity of Escherichia coli trigger factor. Proc Natl Acad Sci USA 98:14244–14249PubMedGoogle Scholar
  160. Pereira PJB, Vega MC, Gonzalez-Rey E, Fernandez-Carazo R, Macedo-Ribeiro S, Gomis-Ruth FX, Gonzalez A, Coll M (2002) Trypanosoma cruzi macrophage infectivity potentiator has a rotamase core and a highly exposed α-helix. EMBO Rep 3:88–94PubMedGoogle Scholar
  161. Perez-Perez JM, Ponce MR, Micol JL (2001) 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(S1): 49–50Google Scholar
  162. Pirkl F, Fischer E, Modrow S, Buchner J (2001) Localization of the chaperone domain of FKBP52. J Biol Chem 276:37034–37041PubMedGoogle Scholar
  163. Pissavin C, Hugouvieuxcottepattat N (1997) Characterization of a periplasmic peptidyl prolyl cis/trans isomerase in Erwinia chrysanthemi. FEMS Microbiol Lett 157:59–65PubMedGoogle Scholar
  164. Pushkarsky T, Zybarth G, Dubrovsky L, Yurchenko V, Tang H, Guo HM, Toole B, Sherry B, Bukrinsky M (2001) CD147 facilitates HIV-1 infection by interacting with virus-associated cyclophilin A. Proc Natl Acad Sci USA 98:6360–6365PubMedGoogle Scholar
  165. Ramm K, Plückthun A (2000) The periplasmic Escherichia coli peptidyl prolyl cis/trans isomerase FkpA—II Isomerase-independent chaperone activity in vitro. J Mol Biol 310:485–498Google Scholar
  166. Ramm K, Plückthun, A (2001) High enzymatic activity and chaperone function are mechanistically related features of the dimeric E. coli peptidyl prolyl isomerase FkpA. J Biol Chem 275:17106–17113Google Scholar
  167. Ranganathan R, Lu KP, Hunter T, Noel JP (1997) Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation. Cell 89:875–886PubMedGoogle Scholar
  168. Reimer U, Fischer G (2002) Local structural changes caused by peptidyl prolyl cis/trans isomerization in the native state of proteins. Biophys Chem 96:203–212PubMedGoogle Scholar
  169. Reimer U, Scherer G, Drewello M, Kruber S, Schutkowski M, Fischer G (1998) Side-chain effects on peptidyl prolyl cis/trans isomerization. J Mol Biol 279:449–460PubMedGoogle Scholar
  170. Reyes DY, Yoshikawa H (2002) DnaK chaperone machine and trigger factor are only partially required for normal growth of Bacillus subtilis. Biosci Biotechnol Biochem 66:1583–1586PubMedGoogle Scholar
  171. Riboldi-Tunnicliffe A, König B, Jessen S, Weiss MS, Rahfeld J, Hacker J, Fischer G, Hilgenfeld R (2001) Crystal structure of Mip, a prolylisomerase from Legionella pneumophila. Nat Struct Biol 8:779–783PubMedGoogle Scholar
  172. Rippmann JF, Hobbie S, Daiber C, Guilliard B, Bauer M, Birk J, Nar H, Garin-Chesa P, Rettig WJ, Schnapp A (2000) Phosphorylation-dependent proline isomerization catalyzed by Pin1 is essential for tumor cell survival and entry into mitosis. Cell Growth Differ 11:409–416PubMedGoogle Scholar
  173. Rizzitello AE, Harper JR, Silhavy TJ (2001) Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli. J Bacteriol 183:6794–6800PubMedGoogle Scholar
  174. Robson T, Joiner MC, Wilson GD, McCullough W, Price ME, Logan I, Jones H, McKeown SR, Hirst DG (1999) A novel human stress response-related gene with a potential role in induced radioresistance. Radiat Res 152:451–461PubMedGoogle Scholar
  175. Roof WD, Horne SM, Young KD, Young R (1994) SlyD, a host gene required for phi X174 lysis, is related to the FK506-binding protein family of peptidyl prolyl cis/trans isomerases. J Biol Chem 269:2902–2910PubMedGoogle Scholar
  176. Rycyzyn MA, Clevenger CV (2002) The intranuclear prolactin/cyclophilin B complex as a transcriptional inducer. Proc Natl Acad Sci USA 99:6790–6795PubMedGoogle Scholar
  177. Rycyzyn MA, Reilly SC, O’Malley K, Clevenger CV (2000) Role of cyclophilin B in prolactin signal transduction and nuclear retrotranslocation. Mol Endocrinol 14:1175–1186PubMedGoogle Scholar
  178. Sabers CJ, Martin MM, Brunn GJ, Williams JM, Dumont FJ, Wiederrecht G, Abraham RT (1995) Isolation of a protein target of the FKBP12-rapamycin complex in mammalian cells. J Biol Chem 270:815–822PubMedGoogle Scholar
  179. Saphire ACS, Bobardt MD, Gallay PA (2002) Transcomplementation rescue of cyclophilin A-deficient viruses reveals that the requirement for cyclophilin A in human immunodeficiency virus type 1. J Virol 76:2255–2262PubMedGoogle Scholar
  180. Schaffitzel E, Rüdiger S, Bukau B, Deuerling E (2001) Functional dissection of trigger factor and DnaK: Interactions with nascent polypeptides and thermally denatured proteins. Biol Chem 382:1235–1243PubMedGoogle Scholar
  181. Scherer G, Kramer ML, Schutkowski M, Reimer U, Fischer G (1998) Barriers to rotation of secondary amide peptide bonds. J Amer Chem Soc 120:5568–5574Google Scholar
  182. Schiene C, Reimer U, Schutkowski M, Fischer G (1998) Mapping the stereospecificity of peptidyl prolyl cis/trans isomerases. FEBS Lett 432:202–206PubMedGoogle Scholar
  183. Schiene-Fischer C, Fischer G (2001) Direct measurement indicates a slow cis/trans isomerization at the secondary amide peptide bond of glycylglycine. J Amer Chem Soc 123:6227–6231Google Scholar
  184. Schiene-Fischer C, Habazettl J, Schmid FX, Fischer G (2002a) The hsp70 chaperone DnaK is a secondary amide peptide bond cis/trans isomerase. Nat Struct Biol 9:419–424PubMedGoogle Scholar
  185. Schiene-Fischer C, Habazettl J, Tradler T, Fischer G (2002b) Evaluation of similarities in the cis/trans isomerase function of trigger factor and DnaK. Biol Chem 383:1865–1875PubMedGoogle Scholar
  186. Schiene-Fischer C, Yu C (2001) Receptor accessory folding helper enzymes: the functional role of peptidyl prolyl cis/trans isomerases. FEBS Lett 495:1–6PubMedGoogle Scholar
  187. Schmid FX (1986) Fast-folding and slow-folding forms of unfolded proteins. Methods Enzymol 131:70–82PubMedGoogle Scholar
  188. Schmidt B, Tradler T, Rahfeld JU, Ludwig B, Jain B, Mann K, Rücknagel KP, Janowski B, Schierhorn A, Küllertz G, Hacker J, Fischer G (1996) A cyclophilin-like peptidyl prolyl cis/trans isomerases from Legionella pneumophila-characterization, molecular cloning, and overexpression. Mol Microbiol 21:1147–1160PubMedGoogle Scholar
  189. Scholz C, Mücke M, Rape M, Pecht A, Pahl A, Bang H, Schmid FX (1998a) Recognition of protein substrates by the prolyl isomerase trigger factor is independent of proline residues. J Mol Biol 277:723–732PubMedGoogle Scholar
  190. Scholz C, Scherer G, Mayr LM, Schindler T, Fischer G, Schmid FX (1998b) Prolyl isomerases do not catalyze isomerization of nonprolyl peptide bonds. Biol Chem 379:361–365PubMedGoogle Scholar
  191. Scholz C, Stoller G, Zarnt T, Fischer G, Schmid FX (1997) Cooperation of enzymatic and chaperone functions of trigger factor in the catalysis of protein folding. EMBO J 16:54–58PubMedGoogle Scholar
  192. Schreiber SL, Crabtree GR (1992) The mechanism of action of cyclosporin-A and FK506. Immunol Today 13:136–142PubMedGoogle Scholar
  193. Schreier MH, Baumann G, Zenke G (1993) Inhibition of T-Cell signaling pathways by immunophilin drug complexes are side effects inherent to immunosuppressive properties. Transplant Proc 25:502–507PubMedGoogle Scholar
  194. Schutkowski M, Drewello M, Wöllner S, Jakob M, Reimer U, Scherer G, Schierhorn A, Fischer G (1996b) Extended binding sites of cyclophilin as revealed by HIV-1 gag polyprotein-derived oligopeptides. FEBS Lett 394:289–294PubMedGoogle Scholar
  195. Schutkowski M, Wöllner S, Fischer G (1996a) Inhibition of peptidyl prolyl cis/trans isomerase activity by substrate analog structures: Thioxo tetrapeptide-4-nitroanilides. Biochemistry 34:13016–13026Google Scholar
  196. Sekerina E, Rahfeld JU, Müller J, Fanghänel J, Rascher C, Fischer G, Bayer P (2000) NMR solution structure of hPar14 reveals similarity to the peptidyl prolyl cis/trans isomerase domain of the mitotic regulator hPin1 but indicates a different functionality of the protein. J Mol Biol 301:1003–1017PubMedGoogle Scholar
  197. Sharma S, Mamane Y, Grandvaux N, Bartlett J, Petropoulos L, Lin RT, Hiscott J (2000) Activation and regulation of interferon regulatory factor 4 in HTLV type 1-infected T lymphocytes. AIDS Res Hum Retroviruses 16:1613–1622PubMedGoogle Scholar
  198. Shaw PE (2002) Peptidyl prolyl isomerases: a new twist to transcription EMBO Rep 3:521–526PubMedGoogle Scholar
  199. Sherman MY, Goldberg AL (1992) Involvement of the chaperonin DnaK in the rapid degradation of a mutant protein in Escherichia coli. EMBO J 11:71–77PubMedGoogle Scholar
  200. Shou WN, Aghdasi B, Armstrong DL, Guo QX, Bao SD, Charng MJ, Mathews LM, Schneider MD, Hamilton SL, Matzuk MM (1998) Cardiac defects and altered ryanodine receptor function in mice lacking FKBP12. Nature 391:489–492PubMedGoogle Scholar
  201. Sigal NH, Dumont F, Durette P, Siekierka JJ, Peterson L, Rich DH, Dunlap BE, Staruch MJ, Melino MR, Koprak SL, Willimas D, Witzel B, Pisano JM (1991) Is cyclophilin involved in the immunosuppressive and nephrotoxic mechanism of action of cyclosporin A? J Exp Med 173:619–628PubMedGoogle Scholar
  202. Somers PK, Wandless TJ, Schreiber SL (1991) Synthesis and analysis of 506BD, a high affinity ligand for the immunophilin FKBP. J Am Chem Soc 113:8045–8056Google Scholar
  203. Spiess C, Beil A, Ehrmann M (1999) A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97:339–347PubMedGoogle Scholar
  204. Steiner JP, Connolly MA, Valentine HI, Hamilton GS, Dawson TM, Hester L, Snyder SH (1997) Neurotrophic actions of nonimmunosuppressive analogs of immunosuppressive drugs FK506, rapamycin and cyclosporine. Nat Med 3:421–428PubMedGoogle Scholar
  205. Stukenberg PT, Kirschner MW (2001) Pin1 acts catalytically to promote a conformational change in Cdc25. Mol Cell 7:1071–1083PubMedGoogle Scholar
  206. Sydenham M, Douce G, Bowe F, Ahmed S, Chatfield S, Dougan G (2000) Salmonella enterica serovar Typhimurium surA mutants are attenuated and effective live oral vaccines. Infect Immun 68:1109–1115PubMedGoogle Scholar
  207. Sykes K, Gething MJ, Sambrook J (1993) Proline isomerases function during heat shock. Proc Natl Acad Sci USA 90:5853–5857PubMedGoogle Scholar
  208. Tang WX, Chen YF, Zou AP, Campbell WB, Li PL (2002) Role of FKBP12.6 in cADPR-induced activation of reconstituted ryanodine receptors from arterial smooth muscle. Am J Physiol 282: H1304–H1310Google Scholar
  209. Teter SA, Houry WA, Ang D, Tradler T, Rockabrand D, Fischer G, Blum P, Georgopoulos C, Hartl FU (1999) Polypeptide flux through bacterial Hsp70: DnaK cooperates with trigger factor in chaperoning nascent chains. Cell 97:755–765PubMedGoogle Scholar
  210. Thomson JA, Shirley BA, Grimsley GR, Pace CN (1989) Conformational stability and mechanism of folding of ribonuclease T1. J Biol Chem 264:11614–11620PubMedGoogle Scholar
  211. Thunecke F, Fischer G (1998) Separation of cis/trans conformers of human and salmon calcitonin by low temperature capillary electrophoresis. Electrophoresis 19:288–294PubMedGoogle Scholar
  212. Tormo A, Almiron M, Kolter R (1990) SurA, an Escherichia coli gene essential for survival in stationary phase. J Bacteriol 172:4339–4347PubMedGoogle Scholar
  213. Truffa-Bachi P, Lefkovits I, Frey JR (2000) Proteomic analysis of T cell activation in the presence of cyclosporin A: immunosuppressor and activator removal induces de novo protein synthesis. Mol Immunol 37:21–28PubMedGoogle Scholar
  214. Tsai CJ, Ma B, Nussinov R (1999) Folding and binding cascades: shifts in energy landscapes. Proc Natl Acad Sci USA 96:9970–9972PubMedGoogle Scholar
  215. Van Melderen L, Gottesman S (1999) Substrate sequestration by a proteolytically inactive Lon mutant. Proc Natl Acad Sci USA 96:6064–6071PubMedGoogle Scholar
  216. Vance JE, Leblanc DA, London RE (1997b) Cleavage of the X-Pro peptide bond by pepsin is specific for the trans isomer. Biochemistry 36:13232–13240PubMedGoogle Scholar
  217. Vance JE, Leblanc DA, Wingfield P, London RE (1997a) Conformational selectivity of HIV-1 protease cleavage of Xaa-Pro bonds and its implications. J Biol Chem 272:15603–15606PubMedGoogle Scholar
  218. Videen JS, Stamnes MA, Hsu VL, Goodman M (1994) Thermodynamics of cyclophilin catalyzed peptidyl prolyl isomerization by NMR spectroscopy. Biopolymers 34:171–175PubMedGoogle Scholar
  219. Vittorioso P, Cowling R, Faure JD, Caboche M, Bellini C (1998) Mutations in the Arabidopsis paticcino1 gene, which encodes a new FK506-binding protein-like protein, has a dramatic effect on plant development. Mol Cell Biol 18:3034–3043PubMedGoogle Scholar
  220. Vogel KW, Briesewitz R, Wandless TJ, Crabtree GR (2001) Calcineurin inhibitors and the generalization of the presenting protein strategy. Adv Protein Chem 56:253–291PubMedGoogle Scholar
  221. von Ahsen O, Lim JH, Caspers P, Martin F, Schönfeld HJ, Rassow J, Pfanner N (2000) Cyclophilin-promoted folding of mouse dihydrofolate reductase does not include the slow conversion of the late-folding intermediate to the active enzyme. J Mol Biol 294:809–818Google Scholar
  222. Waldmeier PC, Feldtrauer JJ, Qian T, Lemasters JJ (2002) Inhibition of the mitochondrial permeability transition by the nonimmunosuppressive cyclosporin derivative NIM811. Mol Pharmacol 62:22–29PubMedGoogle Scholar
  223. Wang P, Cardenas ME, Cox CM, Perfect JR, Heitman J (2001) Two cyclophilin A homologs with shared and distinct functions important for growth and virulence of Cryptococcus neoformans. EMBO Rep 2:511–518PubMedGoogle Scholar
  224. Webb HM, Ruddock LW, Marchant RJ, Jonas K, Klappa P (2001) Interaction of the periplasmic peptidyl prolyl cis/trans isomerase SurA with model peptides—The N-terminal region of SurA is essential and sufficient for peptide binding. J Biol Chem 276:45622–45627PubMedGoogle Scholar
  225. Webel R, Menon I, O’Tousa JE, Colley NJ (2000) Role of asparagine-linked oligosaccharides in rhodopsin maturation and association with its molecular chaperone, NinaA. J Biol Chem 275:24752–24759PubMedGoogle Scholar
  226. Weisman R, Finkelstein S, Choder M (2001) Rapamycin blocks sexual development in fission yeast through inhibition of the cellular function of an FKBP12 homolog. J Biol Chem 276:24736–24742PubMedGoogle Scholar
  227. Weisshoff H, Frost K, Brandt W, Henklein P, Mügge C, Frommel C (1995) Novel disulfide-constrained pentapeptides as models for β-VIa turns in proteins. FEBS Lett 372:203–209PubMedGoogle Scholar
  228. Weiwad M, Küllertz G, Schutkowski M, Fischer G (2000) Evidence that the substrate backbone conformation is critical to phosphorylation by p42 MAP kinase. FEBS Lett 478:39–42PubMedGoogle Scholar
  229. Wiederrecht G, Brizuela L, Elliston K, Sigal NH, Siekierka JJ (1991) FKB1 encodes a nonessential FK 506-binding protein in Saccharomyces cerevisiae and contains regions suggesting homology to the cyclophilins. Proc Natl Acad Sci USA 88:1029–1033PubMedGoogle Scholar
  230. Winkler KE, Swenson KI, Kornbluth S, Means AR (2000) Requirement of the prolyl isomerase Pin1 for the replication checkpoint. Science 287:1644–1647PubMedGoogle Scholar
  231. Wintermeyer E, Ludwig B, Steinert M, Schmidt B, Fischer G, Hacker J (1995) Influence of site specifically altered Mip proteins on intracellular survival of Legionella pneumophila in eukaryotic cells. Infect Immun 63:4576–4583PubMedGoogle Scholar
  232. Witte A, Schrot G, Schon P, Lubitz W (1997) Proline 21, a residue within the α-helical domain of phiX174 lysis protein E, is required for its function in Escherichia coli. Mol Microbiol 26:337–346PubMedGoogle Scholar
  233. Wong CYF, Heuzenroeder MW, Quinn DM, Flower RLP (1997) Cloning and characterization of two immunophilin-like genes IlpA and FkbpA on a single 3.9-kilobase fragment of Aeromonas hydrophila genomic DNA. J Bacteriol 179: 3397–3403PubMedGoogle Scholar
  234. Wu XY, Wilcox CB, Devasahayam G, Hackett RL, Arevalo-Rodriguez M, Cardenas ME, Heitman J, Hanes SD (2000) The Ess1 prolyl isomerase is linked to chromatin remodeling complexes and the general transcription machinery. EMBO J 19:3727–3738PubMedGoogle Scholar
  235. Wüthrich K, Grathwohl C (1974) A novel approach for studies of the molecular conformations in flexible polypeptides. FEBS Lett 43:337–340PubMedGoogle Scholar
  236. Xin HB, Senbonmatsu T, Cheng DS, Wang YX, Copello JA, Ji GJ, Collier ML, Deng KY, Jeyakumar LH, Magnuson MA, Inagami T, Kotlikoff MI, Fleischer S (2002) Estrogen protects FKBP12.6 null mice from cardiac hypertrophy. Nature 416:334–337PubMedGoogle Scholar
  237. Xu Q, Leiva MC, Fischkoff SA, Handschumacher RE, Lyttle CR (1992) Leukocyte chemotactic activity of cyclophilin. J Biol Chem 267:11968–11971PubMedGoogle Scholar
  238. Yaffe MB, Schutkowski M, Shen MH, Zhou XZ, Stukenberg PT, Rahfeld JU, Xu J, Kuang J, Kirschner MW, Fischer G, Cantley LC, Lu KP (1997) Sequence-specific and phosphorylation-dependent proline isomerization: A potential mitotic regulatory mechanism. Science 278:1957–1960PubMedGoogle Scholar
  239. Yang WM, Yao YL, Seto E (2001) The FK506-binding protein 25 functionally associates with histone deacetylases and with transcription factor YY1. EMBO J 20:4814–4825PubMedGoogle Scholar
  240. Yao J, Feher VA, Espejo BF, Reymond MT, Wright PE, Dyson HJ (1994) Stabilization of a type VI turn in a family of linear peptides in water solution. J Mol Biol 243:736–753PubMedGoogle Scholar
  241. Yoo SH, Myszka DG, Yeh CY, McMurray M, Hill CP, Sundquist WI (1997) Molecular recognition in the HIV-1 capsid/cyclophilin A complex. J Mol Biol 269: 780–795PubMedGoogle Scholar
  242. Yuan XM, Werner JM, Knott V, Handford PA, Campbell ID, Downing AK (1998) Effects of proline cis/trans isomerization on TB domain secondary structure. Protein Sci 7:2127–2135PubMedGoogle Scholar
  243. Yurchenko V, O’Connor M, Dai WW, Guo HM, Toole B, Sherry B, Bukrinsky M (2001) CD147 is a signaling receptor for cyclophilin B. Biochem Biophys Res Commun 288:786–788PubMedGoogle Scholar
  244. Yurchenko V, Zybarth G, O’Connor M, Dai WW, Franchin G, Hao T, Guo HM, Hung HC, Toole B, Gallay P, Sherry B, Bukrinsky M (2002) Active site residues of cyclophilin A are crucial for its signaling activity via CD147. J Biol Chem 277:22959–22965PubMedGoogle Scholar
  245. Zenke G, Strittmatter U, Fuchs S, Quesniaux VFJ, Brinkmann V, Schuler W, Zurini M, Enz A, Billich A, Sanglier JJ, Fehr T (2001) Sanglifehrin A, a novel cyclophilin-binding compound showing immunosuppressive activity with a new mechanism of action. J Immunol 166:7165–7171PubMedGoogle Scholar
  246. Zhang W, Zimmer G, Chen JZ, Ladd D, Li E, Alt FW, Wiederrecht G, Cryan J, Oneill EA, Seidman CE, Abbas AK, Seidman JG (1996) T cell response in calcineurin A α-deficient mice. J Exp Med 183:413–420PubMedGoogle Scholar
  247. Zhang YX, Fussel S, Reimer U, Schutkowski M, Fischer G (2002) Substrate-based design of reversible Pin1 inhibitors. Biochemistry 41:11868–11877PubMedGoogle Scholar
  248. Zhao YD, Chen YQ, Schutkowski M, Fischer G, Ke HM (1997) Cyclophilin A complexed with a fragment of HIV-1 gag protein—insights into HIV-1 infectious activity. Structure 5:139–146PubMedGoogle Scholar
  249. Zhou XZ, Kops O, Werner A, Lu PJ, Shen MH, Stoller G, Küllertz G, Stark M, Fischer G, Lu KP (2000) Pin1-dependent prolyl isomerization regulates dephosphorylation of Cdc25C and tproteins. Mol Cell 6:873–883PubMedGoogle Scholar

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© Springer-Verlag 2003

Authors and Affiliations

  1. 1.Max Planck Research Unit for Enzymology of Protein FoldingHalleGermany

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