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

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Reviews of Physiology, Biochemistry and Pharmacology

Part of the book series: Reviews of Physiology, Biochemistry and Pharmacology ((REVIEWS,volume 148))

Abstract

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.

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References

  • 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 98:2425–2430

    PubMed  CAS  Google Scholar 

  • 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 99:2714–2719

    PubMed  CAS  Google Scholar 

  • Andreeva L, Motterlini R, Green CJ (1997) Cyclophilins are induced by hypoxia and heat stress in myogenic cells. Biochem Biophys Res Commun 237:6–9

    PubMed  CAS  Google Scholar 

  • Ansari H, Greco G, Luban J (2002) Cyclophilin a peptidyl prolyl isomerase activity promotes ZPR1 nuclear export. Mol Cell Biol 22:6993–7003

    PubMed  CAS  Google Scholar 

  • 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 19:3739–3749

    PubMed  CAS  Google Scholar 

  • Arie JP, Sassoon N, Betton JM (2001) Chaperone function of FkpA, a heat shock prolyl isomerase, in the periplasm of Escherichia coli. Mol Microbiol 39:199–210

    PubMed  CAS  Google Scholar 

  • 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 6:435–442

    PubMed  CAS  Google Scholar 

  • Bächinger HP (1987) The influence of peptidyl prolyl cis/trans isomerase on the in vitro folding of type III collagen. J Biol Chem 262:17144–17148

    PubMed  Google Scholar 

  • Baine P (1986) Comparison of rate constants determined by two-dimensional NMR spectroscopy with rate constants determined by other NMR techniques. Magn Reson Chem 24:304–307

    CAS  Google Scholar 

  • 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 285:829–42

    PubMed  CAS  Google Scholar 

  • 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 23:54–58

    PubMed  CAS  Google Scholar 

  • 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 92:5381–5385

    PubMed  CAS  Google Scholar 

  • 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 9:223–228

    PubMed  CAS  Google Scholar 

  • Batiuk TD, Kung LN, Halloran PF (1997) Evidence that calcineurin is rate-limiting for primary human lymphocyte activation. J Clin Invest 100:1894–1901

    PubMed  CAS  Google Scholar 

  • Batiuk TD, Pazderka F, Halloran PF (1995) Calcineurin activity is only partially inhibited in leukocytes of cyclosporine-treated patients. Transplantation 59: 1400–1404

    PubMed  CAS  Google Scholar 

  • 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 61:1618–1624

    PubMed  CAS  Google Scholar 

  • 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 276:47914–47921

    Google Scholar 

  • 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 20:285–294

    PubMed  CAS  Google Scholar 

  • 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 431:386–390

    PubMed  CAS  Google Scholar 

  • 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 45:99–108

    PubMed  CAS  Google Scholar 

  • Binsch G (1969) A unified theory of exchange effects on nuclear magnetic resonance line shapes. J Am Chem Soc 91: 1304–1309

    CAS  Google Scholar 

  • Bitto E, McKay DB (2002) Crystallographic structure of SurA, a molecular chaperone that facilitates folding of outer membrane proteins. Structure 10:1489–1498

    PubMed  CAS  Google Scholar 

  • 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 99:5247–5252

    PubMed  CAS  Google Scholar 

  • Bose S, Weikl T, Bugl H, Buchner J (1996) Chaperone function of hsp90-associated proteins. Science 274:1715–1717

    PubMed  CAS  Google Scholar 

  • Braaten D, Luban J (2001) Cyclophilin A regulates HIV-1 infectivity, as demonstrated by gene targeting in human T cells. EMBO J 20:1300–1309

    PubMed  CAS  Google Scholar 

  • 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 14:4953–4963

    PubMed  CAS  Google Scholar 

  • 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 369:756–758

    PubMed  CAS  Google Scholar 

  • 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 99:9398–9403

    PubMed  CAS  Google Scholar 

  • Bukrinsky MI (2002) Cyclophilins: unexpected messengers in intercellular communications. Trends Immunol 23:323–325

    PubMed  CAS  Google Scholar 

  • Burbaum JJ, Raines RT, Albery WJ, Knowles JR (1989) Evolutionary optimization of the catalytic effectiveness of an enzyme. Biochemistry 28:9293–9305

    PubMed  CAS  Google Scholar 

  • Capano M, Virji S, Crompton M (2002) Cyclophilin-A is involved in excitotoxin-induced caspas activation in rat neuronal B50 cells. Biochem J 363:29–36

    PubMed  CAS  Google Scholar 

  • 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 41:5222–5229

    PubMed  CAS  Google Scholar 

  • Carter P, Wells JA (1987) Engineering enzyme specificity by “substrate-assisted catalysis” Science 237:394–399

    PubMed  CAS  Google Scholar 

  • Chen YG, Liu F, Massague J (1997) Mechanism of TGF-β receptor inhibition by FKBP12. EMBO J 16:3866–3876

    PubMed  CAS  Google Scholar 

  • 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 274:20151–20158

    PubMed  CAS  Google Scholar 

  • Chow KC, Tung WL (1998) Overexpression of dnaK/dnaJ and groEL confers freeze tolerance to Escherichia coli. Biochem Biophys Res Commun 253:502–505

    PubMed  CAS  Google Scholar 

  • Christner C, Herdegen D, Fischer G (2001) FKBP ligands as novel therapeutics for neurological disorders. Mini Rev Med Chem 1:377–397

    PubMed  CAS  Google Scholar 

  • Cianciotto NP, Fields BS (1992) Legionella-Pneumophila-MIP gene potentiates intracellular infection of protozoa and human macrophages. Proc Natl Acad Sci USA 89:5188–5191

    PubMed  CAS  Google Scholar 

  • 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 277:34793–34799

    PubMed  CAS  Google Scholar 

  • 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 68:167–178

    PubMed  CAS  Google Scholar 

  • Counterman AE, Clemmer DE (2002) Cis/trans signatures of proline-containing tryptic peptides in the gas phase. Anal Chem 74:1946–1951

    PubMed  CAS  Google Scholar 

  • Cristillo AD, Bierer BE (2002) Identification of novel targets of immunosuppressive agents by cDNA-based microarray analysis. J Biol Chem 277:4465–4476

    PubMed  CAS  Google Scholar 

  • Dartigalongue C, Missiakas D, Raina S (2001) Characterization of the Escherichia coli sigma E regulon. J Biol Chem 276:20866–20875

    PubMed  CAS  Google Scholar 

  • 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 17:3968–3980

    PubMed  CAS  Google Scholar 

  • 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 264:8956–8962

    PubMed  CAS  Google Scholar 

  • de Crouy-Chanel A, Kohiyama M, Richarme G (1999) Interaction of DnaK with native proteins and membrane proteins correlates with their accessible hydrophobicity. Gene 230:163–170

    PubMed  Google Scholar 

  • Deuerling E, Schulze-Specking A, Tomoyasu T, Mogk A, Bukau B (1999) Trigger factor and DnaK cooperate in folding of newly synthesized proteins. Nature 400:693–696

    PubMed  CAS  Google Scholar 

  • Devasahayam G, Chaturvedi V, Hanes SD (2002) The ess1 prolyl isomerase is required for growth and morphogenetic switching in Candida albicans. Genetics 160:37–48

    PubMed  CAS  Google Scholar 

  • Dobson CM, Sali A, Karplus M (1998) Protein folding—a perspective from theory and experiment. Angew Chem Intern Ed Engl 37:868–893

    Google Scholar 

  • 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 94:13093–13098

    PubMed  CAS  Google Scholar 

  • 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 269:20159–20166

    PubMed  CAS  Google Scholar 

  • Evans PA, Kautz RA, Fox RO, Dobson CM (1989) A magnetization-transfer nuclear magnetic resonance study of the folding of staphylococcal nuclease. Biochemistry 28:362–70

    PubMed  CAS  Google Scholar 

  • Fischer G (1994a) Peptidyl prolyl cis/trans isomerases and their effectors. Angew Chem Intern Ed Engl 33:1415–1436

    Google Scholar 

  • Fischer G, Bang H, Berger E, Schellenberger A (1984a) Conformational specificity of chymotrypsin toward proline-containing substrates. Biochim Biophys Acta 791:87–97

    PubMed  CAS  Google Scholar 

  • 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 43:1101–1111

    PubMed  CAS  Google Scholar 

  • 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 742:452–462

    PubMed  CAS  Google Scholar 

  • Fischer G, Schutkowski M, Küllertz G (2001) Peptidic substrates for directly assaying enzyme activities. Pat. No. DE 100 23743 A1

    Google Scholar 

  • Fischer G, Tradler T, Zarnt T (1998) The mode of action of peptidyl prolyl cis/trans isomerases in vivo: binding versus catalysis. FEBS Lett 426:17–20

    PubMed  CAS  Google Scholar 

  • Fischer G, Wittmann Liebold B, Lang K, Kiefhaber T, Schmid FX (1989) Cyclophilin and peptidyl-prolyl cis/trans isomerases are probably identical proteins. Nature 337:476–478

    PubMed  CAS  Google Scholar 

  • 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 142–145

    Google Scholar 

  • 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 222:279–282

    PubMed  CAS  Google Scholar 

  • Freeman BC, Toft DO, Morimoto RI (1996) Molecular chaperone machines—chaperone activities of the cyclophilin Cyp-40 and steroid receptor associated protein p24. Science 274:1718–1720

    PubMed  CAS  Google Scholar 

  • 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 66:799–806

    PubMed  CAS  Google Scholar 

  • Frydman J (2001) Folding of newly translated proteins in vivo: the role of molecular chaperones. Ann Rev Biochem 70:603–647

    PubMed  CAS  Google Scholar 

  • 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 289:181–190

    PubMed  CAS  Google Scholar 

  • 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 265:658–663

    PubMed  CAS  Google Scholar 

  • 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: 39–51

    PubMed  CAS  Google Scholar 

  • 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 39:453–462

    PubMed  CAS  Google Scholar 

  • 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 87:1285–1294

    PubMed  CAS  Google Scholar 

  • 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 114:2758–2759

    CAS  Google Scholar 

  • 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 191:70–75

    PubMed  CAS  Google Scholar 

  • 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 37:13392–13399

    PubMed  CAS  Google Scholar 

  • 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 82:507–522

    PubMed  CAS  Google Scholar 

  • Guthrie B, Wickner W (1990) Trigger factor depletion or overproduction causes defective cell division but does not block protein export. J Bacteriol 172:5555–5562

    PubMed  CAS  Google Scholar 

  • Halestrap AP, McStay GP, Clarke SJ (2002) The permeability transition pore complex: another view. Biochimie 84:153–166

    PubMed  CAS  Google Scholar 

  • Halloran PF, Kung L, Noujaim J (1998) Calcineurin and the biological effects of cyclosporine and tacrolimus. Transplant Proc 30:2167–2170

    PubMed  CAS  Google Scholar 

  • 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 365:198–202

    PubMed  CAS  Google Scholar 

  • 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 96:14866–14870

    PubMed  CAS  Google Scholar 

  • Harrar Y, Bellini C, Faure JD (2001) FKBPs: at the crossroads of folding and transduction. Trends Plant Sci 6:426–431

    PubMed  CAS  Google Scholar 

  • Hassidim M, Schwarz R, Liemanhurwitz J, Marco E, Ronentarazi M, Kaplan A (1992) A cyanobacterial gene encoding peptidyl prolyl cis/trans isomerase. Plant Physiol 100:1982–1986

    PubMed  CAS  Google Scholar 

  • 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 88:1948–1952

    PubMed  CAS  Google Scholar 

  • 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 11:1073–1083

    PubMed  CAS  Google Scholar 

  • Hesterkamp T, Bukau B (1998) Role of the DnaK and HscA homologs of Hsp70 chaperones in protein folding in E.coli. EMBO J 17:4818–4828

    PubMed  CAS  Google Scholar 

  • Horne SM, Kottom TJ, Nolan LK, Young KD (1997) Decreased intracellular survival of an fkpA mutant of Salmonella typhimurium Copenhagen. Infect Immun 85:806–810

    Google Scholar 

  • 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 163:357–365

    PubMed  CAS  Google Scholar 

  • 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 3:538–543

    PubMed  CAS  Google Scholar 

  • 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 112:6745–6747

    CAS  Google Scholar 

  • 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 99:12037–12042

    PubMed  CAS  Google Scholar 

  • 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 114:3779–3788

    PubMed  CAS  Google Scholar 

  • Hübner D, Drakenberg T, Forsen S, Fischer G (1991) Peptidyl prolyl cis/trans isomerase activity as studied by dynamic proton NMR spectroscopy. FEBS Lett 284:79–81

    PubMed  Google Scholar 

  • 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 96:425–436

    PubMed  CAS  Google Scholar 

  • 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 252:299–307

    PubMed  CAS  Google Scholar 

  • 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 34:663–669

    PubMed  CAS  Google Scholar 

  • 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 87:789–796

    PubMed  CAS  Google Scholar 

  • Jin L, Harrison SC, (2002) Crystal structure of human calcineurin complexed with cyclosporin A and human cyclophilin. Proc Natl Acad Sci USA 99:13522–13526

    PubMed  CAS  Google Scholar 

  • Joseph J D, Heitman J, Means AR (1999) Molecular cloning and characterization of Aspergillus nidulans cyclophilin B. Fungal Genet Biol 27:55–66

    PubMed  CAS  Google Scholar 

  • 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 32:263–276

    PubMed  CAS  Google Scholar 

  • 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 94:4978–4981

    PubMed  CAS  Google Scholar 

  • 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 323:198–202

    PubMed  CAS  Google Scholar 

  • 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 34:13594–13602

    PubMed  CAS  Google Scholar 

  • Kern G, Kern D, Schmid FX, Fischer G (1994) Reassessment of the putative chaperone function of prolyl cis/trans isomerases. FEBS Lett 348:145–148

    PubMed  CAS  Google Scholar 

  • Kiefhaber T, Quaas R, Hahn U, Schmid FX (1990a) Folding of ribonuclease T1. 1. Existence of multiple unfolded states created by proline isomerization. Biochemistry 29:3053–3061

    PubMed  CAS  Google Scholar 

  • Kiefhaber T, Quaas R, Hahn U, Schmid FX (1990b) Folding of ribonuclease T1. 2. Kinetic models for the folding and unfolding reactions. Biochemistry 29:3061–3070

    PubMed  CAS  Google Scholar 

  • Kleerebezem M, Heutink M, Tommassen J (1995) Characterization of an Escherichia coli rotA mutant, affected in periplasmic peptidyl prolyl cis/trans isomerase. Mol Microbiol 18:313–320

    PubMed  CAS  Google Scholar 

  • 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 30:6127–6134

    PubMed  CAS  Google Scholar 

  • 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 1219:601–606

    PubMed  Google Scholar 

  • 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 8:727–737

    PubMed  CAS  Google Scholar 

  • Kramer ML, Fischer G (1997) FKBP-like catalysis of peptidyl prolyl bond isomerization by micelles and membranes. Biopolymers 42:49–60

    CAS  Google Scholar 

  • 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 44:502–508

    PubMed  Google Scholar 

  • Kung L, Halloran PF (2002) Immunophilins may limit calcineurin inhibition by cyclosporine and tacrolimus at high drug concentrations. Transplantation 70:327–335

    Google Scholar 

  • 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 119:693–703

    PubMed  CAS  Google Scholar 

  • 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 215:119–126

    PubMed  CAS  Google Scholar 

  • Lang K, Schmid FX, Fischer G (1987) Catalysis of protein folding by prolyl isomerase. Nature 329:268–70

    PubMed  CAS  Google Scholar 

  • 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 356:683–689

    PubMed  CAS  Google Scholar 

  • 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 96:3251–3256

    PubMed  CAS  Google Scholar 

  • Leiva MC, Lyttle CR (1992) Leukocyte chemotactic activity of FKBP and inhibition by FK506. Biochem Biophys Res Commun 186:1178–1183

    PubMed  CAS  Google Scholar 

  • Leverson JD, Ness SA (1998) Point mutations in v-myb disrupt cyclophilin-catalyzed negative regulatory mechanism. Mol Cell 1:203–211

    PubMed  CAS  Google Scholar 

  • 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 98:10682–10686

    PubMed  CAS  Google Scholar 

  • Li TK, Baksh S, Cristillo AD, Bierer BE (2002) Calcium-and FK506-independent interaction between the immunophilin FKBP51 and calcineurin. J Cell Biochem 84:460–471

    PubMed  Google Scholar 

  • 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 506:108–112

    PubMed  CAS  Google Scholar 

  • Lin DT, Lechleiter JD (2002) Mitochondrial targeted cyclophilin D protects cells from cell death by peptidyl prolyl isomerization. J Biol Chem 277:31134–31141

    PubMed  CAS  Google Scholar 

  • Lin LN, Brandts JF (1979) Evidence suggesting that some proteolytic enzymes may cleave only the trans form of the peptide bond. Biochemistry 18:43–47

    PubMed  CAS  Google Scholar 

  • 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 24:6533–6538

    PubMed  CAS  Google Scholar 

  • Lin LN, Hasumi H, Brandts JF (1988) Catalysis of proline isomerization during protein-folding reactions. Biochim Biophys Acta 956:256–266

    PubMed  CAS  Google Scholar 

  • 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 99:1335–1340

    PubMed  CAS  Google Scholar 

  • 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 66:807–815

    PubMed  CAS  Google Scholar 

  • 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 29:10298–10302

    PubMed  CAS  Google Scholar 

  • 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 273:9430–9434

    CAS  Google Scholar 

  • Lu KP, Liou YC, Zhou XZ (2002) Pinning down proline-directed phosphorylation signaling. Trends Cell Biol 12:164–172

    PubMed  CAS  Google Scholar 

  • Lu PJ, Zhou XZ, Shen MH, Lu KP (1999) Function of WW domains as phosphoserine-or phosphothreonine-binding modules. Science 283:1325–1328

    PubMed  CAS  Google Scholar 

  • Luban J (1996) Absconding with the chaperone—essential cyclophilin gag interaction in HIV-1 virions. Cell 87:1157–1159

    PubMed  CAS  Google Scholar 

  • 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 17:6263–6275

    PubMed  CAS  Google Scholar 

  • MacArthur MW, Thornton JM (1991) Influence of proline residues on protein conformation. J Mol Biol 218:397–412

    PubMed  CAS  Google Scholar 

  • Maier R, Scholz C, Schmid FX (2001) Dynamic association of trigger factor with protein substrates. J Mol Biol 314:1181–1190

    PubMed  CAS  Google Scholar 

  • 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 93:447–451

    PubMed  CAS  Google Scholar 

  • 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 9:900–905

    PubMed  CAS  Google Scholar 

  • Mamane Y, Sharma S, Petropoulos L, Lin RT, Hiscott J (2000) Posttranslational regulation of IRF-4 activity by the immunophilin FKBP52. Immunity 12:129–140

    PubMed  CAS  Google Scholar 

  • 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 84:171–178

    CAS  Google Scholar 

  • 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 35:5550–5561

    PubMed  CAS  Google Scholar 

  • 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 231:913–926

    PubMed  CAS  Google Scholar 

  • Mayr LM, Willbold D, Rosch P, Schmid FX (1994) Generation of a nonprolyl cis peptide bond in ribonuclease T1. J Mol Biol 240:288–293

    PubMed  CAS  Google Scholar 

  • 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 7:196–199

    PubMed  CAS  Google Scholar 

  • McCornack MA, Kakalis LT, Caserta C, Handschumacher RE, Armitage IM (1997) HIV protease substrate conformation—modulation by cyclophilin A. FEBS Lett 414:84–88

    PubMed  CAS  Google Scholar 

  • Meng X, Lu XJ, Morris CA, Keating MT (1998) Novel human gene FKBP6 is deleted in Williams-syndrome. Genomics 52:130–137

    PubMed  CAS  Google Scholar 

  • Merker MP, Dawson CA (1995) Cyclophilin-facilitated bradykinin inactivation in the perfused rat lung. Biochem Pharmacol 50:2085–2091

    PubMed  CAS  Google Scholar 

  • 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 75:1519–1524

    PubMed  CAS  Google Scholar 

  • Meyer S, Jabs A, Schutkowski M, Fischer G (1994) Separation of cis/trans isomers of a prolyl peptide bond by capillary zone electrophoresis. Electrophoresis 15:1151–1157

    PubMed  CAS  Google Scholar 

  • Mihatsch MJ, Kyo M, Morozumi K, Yamaguchi Y, Nickeleit V, Ryffel B (1998) The side effects of cyclosporin A and tacrolimus. Clin Nephrol 49:356–363

    PubMed  CAS  Google Scholar 

  • 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 269:18877–18880

    PubMed  CAS  Google Scholar 

  • 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 67:145–155

    PubMed  CAS  Google Scholar 

  • Mücke M, Schmid FX (1992) Enzymatic catalysis of prolyl isomerization in an unfolding protein. Biochemistry 31:7848–7854

    PubMed  Google Scholar 

  • Navia MA (1996) Protein-drug complexes important for immunoregulation and organ transplantation. Curr Opin Struct Biol 6:838–847

    PubMed  CAS  Google Scholar 

  • 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 245:69–78

    PubMed  CAS  Google Scholar 

  • 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: 35–41

    PubMed  CAS  Google Scholar 

  • 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 270:30007–30017

    PubMed  CAS  Google Scholar 

  • Ou WB, Luo W, Park YD, Zhou HM (2000) Chaperone-like activity of peptidyl prolyl cis/trans isomerase during creatine kinase refolding. Protein Sci 10:2346–2353

    Google Scholar 

  • Paek KH, Walker GC (1987) Escherichia coli DnaK null mutants are inviable at high temperature. J Bacteriol 169:283–290

    PubMed  CAS  Google Scholar 

  • 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 8:452–458

    PubMed  CAS  Google Scholar 

  • 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 98:14244–14249

    PubMed  CAS  Google Scholar 

  • 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 3:88–94

    PubMed  CAS  Google Scholar 

  • 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): 49–50

    Google Scholar 

  • Pirkl F, Fischer E, Modrow S, Buchner J (2001) Localization of the chaperone domain of FKBP52. J Biol Chem 276:37034–37041

    PubMed  CAS  Google Scholar 

  • Pissavin C, Hugouvieuxcottepattat N (1997) Characterization of a periplasmic peptidyl prolyl cis/trans isomerase in Erwinia chrysanthemi. FEMS Microbiol Lett 157:59–65

    PubMed  CAS  Google Scholar 

  • 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 98:6360–6365

    PubMed  CAS  Google Scholar 

  • 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 310:485–498

    Google Scholar 

  • 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 275:17106–17113

    Google Scholar 

  • Ranganathan R, Lu KP, Hunter T, Noel JP (1997) Structural and functional analysis of the mitotic rotamase Pin1 suggests substrate recognition is phosphorylation. Cell 89:875–886

    PubMed  CAS  Google Scholar 

  • Reimer U, Fischer G (2002) Local structural changes caused by peptidyl prolyl cis/trans isomerization in the native state of proteins. Biophys Chem 96:203–212

    PubMed  CAS  Google Scholar 

  • 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 279:449–460

    PubMed  CAS  Google Scholar 

  • Reyes DY, Yoshikawa H (2002) DnaK chaperone machine and trigger factor are only partially required for normal growth of Bacillus subtilis. Biosci Biotechnol Biochem 66:1583–1586

    PubMed  CAS  Google Scholar 

  • 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 8:779–783

    PubMed  CAS  Google Scholar 

  • 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 11:409–416

    PubMed  CAS  Google Scholar 

  • Rizzitello AE, Harper JR, Silhavy TJ (2001) Genetic evidence for parallel pathways of chaperone activity in the periplasm of Escherichia coli. J Bacteriol 183:6794–6800

    PubMed  CAS  Google Scholar 

  • 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 152:451–461

    PubMed  CAS  Google Scholar 

  • 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 269:2902–2910

    PubMed  CAS  Google Scholar 

  • Rycyzyn MA, Clevenger CV (2002) The intranuclear prolactin/cyclophilin B complex as a transcriptional inducer. Proc Natl Acad Sci USA 99:6790–6795

    PubMed  CAS  Google Scholar 

  • Rycyzyn MA, Reilly SC, O’Malley K, Clevenger CV (2000) Role of cyclophilin B in prolactin signal transduction and nuclear retrotranslocation. Mol Endocrinol 14:1175–1186

    PubMed  CAS  Google Scholar 

  • 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 270:815–822

    PubMed  CAS  Google Scholar 

  • 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 76:2255–2262

    PubMed  CAS  Google Scholar 

  • 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 382:1235–1243

    PubMed  CAS  Google Scholar 

  • Scherer G, Kramer ML, Schutkowski M, Reimer U, Fischer G (1998) Barriers to rotation of secondary amide peptide bonds. J Amer Chem Soc 120:5568–5574

    CAS  Google Scholar 

  • Schiene C, Reimer U, Schutkowski M, Fischer G (1998) Mapping the stereospecificity of peptidyl prolyl cis/trans isomerases. FEBS Lett 432:202–206

    PubMed  CAS  Google Scholar 

  • 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 123:6227–6231

    CAS  Google Scholar 

  • 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 9:419–424

    PubMed  CAS  Google Scholar 

  • 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 383:1865–1875

    PubMed  CAS  Google Scholar 

  • Schiene-Fischer C, Yu C (2001) Receptor accessory folding helper enzymes: the functional role of peptidyl prolyl cis/trans isomerases. FEBS Lett 495:1–6

    PubMed  CAS  Google Scholar 

  • Schmid FX (1986) Fast-folding and slow-folding forms of unfolded proteins. Methods Enzymol 131:70–82

    PubMed  CAS  Google Scholar 

  • 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 21:1147–1160

    PubMed  CAS  Google Scholar 

  • 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 277:723–732

    PubMed  CAS  Google Scholar 

  • 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 379:361–365

    PubMed  CAS  Google Scholar 

  • 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 16:54–58

    PubMed  CAS  Google Scholar 

  • Schreiber SL, Crabtree GR (1992) The mechanism of action of cyclosporin-A and FK506. Immunol Today 13:136–142

    PubMed  CAS  Google Scholar 

  • 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 25:502–507

    PubMed  CAS  Google Scholar 

  • 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 394:289–294

    PubMed  CAS  Google Scholar 

  • Schutkowski M, Wöllner S, Fischer G (1996a) Inhibition of peptidyl prolyl cis/trans isomerase activity by substrate analog structures: Thioxo tetrapeptide-4-nitroanilides. Biochemistry 34:13016–13026

    Google Scholar 

  • 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 301:1003–1017

    PubMed  CAS  Google Scholar 

  • 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 16:1613–1622

    PubMed  CAS  Google Scholar 

  • Shaw PE (2002) Peptidyl prolyl isomerases: a new twist to transcription EMBO Rep 3:521–526

    PubMed  CAS  Google Scholar 

  • Sherman MY, Goldberg AL (1992) Involvement of the chaperonin DnaK in the rapid degradation of a mutant protein in Escherichia coli. EMBO J 11:71–77

    PubMed  CAS  Google Scholar 

  • 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 391:489–492

    PubMed  CAS  Google Scholar 

  • 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 173:619–628

    PubMed  CAS  Google Scholar 

  • Somers PK, Wandless TJ, Schreiber SL (1991) Synthesis and analysis of 506BD, a high affinity ligand for the immunophilin FKBP. J Am Chem Soc 113:8045–8056

    CAS  Google Scholar 

  • Spiess C, Beil A, Ehrmann M (1999) A temperature-dependent switch from chaperone to protease in a widely conserved heat shock protein. Cell 97:339–347

    PubMed  CAS  Google Scholar 

  • 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 3:421–428

    PubMed  CAS  Google Scholar 

  • Stukenberg PT, Kirschner MW (2001) Pin1 acts catalytically to promote a conformational change in Cdc25. Mol Cell 7:1071–1083

    PubMed  CAS  Google Scholar 

  • 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 68:1109–1115

    PubMed  CAS  Google Scholar 

  • Sykes K, Gething MJ, Sambrook J (1993) Proline isomerases function during heat shock. Proc Natl Acad Sci USA 90:5853–5857

    PubMed  CAS  Google Scholar 

  • 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–H1310

    CAS  Google Scholar 

  • 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 97:755–765

    PubMed  CAS  Google Scholar 

  • Thomson JA, Shirley BA, Grimsley GR, Pace CN (1989) Conformational stability and mechanism of folding of ribonuclease T1. J Biol Chem 264:11614–11620

    PubMed  CAS  Google Scholar 

  • Thunecke F, Fischer G (1998) Separation of cis/trans conformers of human and salmon calcitonin by low temperature capillary electrophoresis. Electrophoresis 19:288–294

    PubMed  CAS  Google Scholar 

  • Tormo A, Almiron M, Kolter R (1990) SurA, an Escherichia coli gene essential for survival in stationary phase. J Bacteriol 172:4339–4347

    PubMed  CAS  Google Scholar 

  • 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 37:21–28

    PubMed  CAS  Google Scholar 

  • Tsai CJ, Ma B, Nussinov R (1999) Folding and binding cascades: shifts in energy landscapes. Proc Natl Acad Sci USA 96:9970–9972

    PubMed  CAS  Google Scholar 

  • Van Melderen L, Gottesman S (1999) Substrate sequestration by a proteolytically inactive Lon mutant. Proc Natl Acad Sci USA 96:6064–6071

    PubMed  Google Scholar 

  • Vance JE, Leblanc DA, London RE (1997b) Cleavage of the X-Pro peptide bond by pepsin is specific for the trans isomer. Biochemistry 36:13232–13240

    PubMed  CAS  Google Scholar 

  • 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 272:15603–15606

    PubMed  CAS  Google Scholar 

  • Videen JS, Stamnes MA, Hsu VL, Goodman M (1994) Thermodynamics of cyclophilin catalyzed peptidyl prolyl isomerization by NMR spectroscopy. Biopolymers 34:171–175

    PubMed  CAS  Google Scholar 

  • 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 18:3034–3043

    PubMed  CAS  Google Scholar 

  • Vogel KW, Briesewitz R, Wandless TJ, Crabtree GR (2001) Calcineurin inhibitors and the generalization of the presenting protein strategy. Adv Protein Chem 56:253–291

    PubMed  CAS  Google Scholar 

  • 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 294:809–818

    Google Scholar 

  • Waldmeier PC, Feldtrauer JJ, Qian T, Lemasters JJ (2002) Inhibition of the mitochondrial permeability transition by the nonimmunosuppressive cyclosporin derivative NIM811. Mol Pharmacol 62:22–29

    PubMed  CAS  Google Scholar 

  • 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 2:511–518

    PubMed  CAS  Google Scholar 

  • 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 276:45622–45627

    PubMed  CAS  Google Scholar 

  • 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 275:24752–24759

    PubMed  CAS  Google Scholar 

  • 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 276:24736–24742

    PubMed  CAS  Google Scholar 

  • 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 372:203–209

    PubMed  CAS  Google Scholar 

  • 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 478:39–42

    PubMed  CAS  Google Scholar 

  • 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 88:1029–1033

    PubMed  CAS  Google Scholar 

  • Winkler KE, Swenson KI, Kornbluth S, Means AR (2000) Requirement of the prolyl isomerase Pin1 for the replication checkpoint. Science 287:1644–1647

    PubMed  CAS  Google Scholar 

  • 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 63:4576–4583

    PubMed  CAS  Google Scholar 

  • 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 26:337–346

    PubMed  CAS  Google Scholar 

  • 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: 3397–3403

    PubMed  CAS  Google Scholar 

  • 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 19:3727–3738

    PubMed  CAS  Google Scholar 

  • Wüthrich K, Grathwohl C (1974) A novel approach for studies of the molecular conformations in flexible polypeptides. FEBS Lett 43:337–340

    PubMed  Google Scholar 

  • 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 416:334–337

    PubMed  CAS  Google Scholar 

  • Xu Q, Leiva MC, Fischkoff SA, Handschumacher RE, Lyttle CR (1992) Leukocyte chemotactic activity of cyclophilin. J Biol Chem 267:11968–11971

    PubMed  CAS  Google Scholar 

  • 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 278:1957–1960

    PubMed  CAS  Google Scholar 

  • Yang WM, Yao YL, Seto E (2001) The FK506-binding protein 25 functionally associates with histone deacetylases and with transcription factor YY1. EMBO J 20:4814–4825

    PubMed  CAS  Google Scholar 

  • 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 243:736–753

    PubMed  CAS  Google Scholar 

  • 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: 780–795

    PubMed  CAS  Google Scholar 

  • 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 7:2127–2135

    PubMed  CAS  Google Scholar 

  • 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 288:786–788

    PubMed  CAS  Google Scholar 

  • 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 277:22959–22965

    PubMed  CAS  Google Scholar 

  • 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 166:7165–7171

    PubMed  CAS  Google Scholar 

  • 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 183:413–420

    PubMed  CAS  Google Scholar 

  • Zhang YX, Fussel S, Reimer U, Schutkowski M, Fischer G (2002) Substrate-based design of reversible Pin1 inhibitors. Biochemistry 41:11868–11877

    PubMed  CAS  Google Scholar 

  • 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 5:139–146

    PubMed  CAS  Google Scholar 

  • 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 6:873–883

    PubMed  CAS  Google Scholar 

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  1. Max Planck Research Unit for Enzymology of Protein Folding, Weinbergweg 22, 06120, Halle, Germany

    G. Fischer & T. Aumüller

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  1. G. Fischer
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Fischer, G., Aumüller, T. (2003). Regulation of peptide bond cis/trans isomerization by enzyme catalysis and its implication in physiological processes. In: Reviews of Physiology, Biochemistry and Pharmacology. Reviews of Physiology, Biochemistry and Pharmacology, vol 148. Springer, Berlin, Heidelberg. https://doi.org/10.1007/s10254-003-0011-3

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  • DOI: https://doi.org/10.1007/s10254-003-0011-3

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