Intramolecular catalysis of amide isomerization: Kinetic consequences of the 5-NH- -N(a) hydrogen bond in prolyl peptides

Journal of the American Chemical Society

Volumn 120, Issue 41, 1998, Pages 10660-10668

  Cox, Christopher ^a   Lectka, Thomas ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ISOMERASE; PEPTIDE;

ARTICLE; CATALYSIS; HYDROGEN BOND; ISOMERISM; KINETICS; SPECTROSCOPY; STRUCTURE ANALYSIS;

EID: 0032556224     PISSN: 00027863     EISSN: None     Source Type: Journal    
DOI: 10.1021/ja9815071     Document Type: Article

References (62)

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11. a, prolyl amide nitrogen; H-bond, hydrogen bond; ST, saturation transfer NMR.; DHFR, dihydrofolate reductase; FKBP, binding protein for the immunosupressive agent FK-506; PPIase, peptidylprolyl isomerase (generic term for cyclophilin and/or FKBP); EDCI, 1-(3-dimethylaminopropyl)-3-ethylcarbodiimide hydrochloride, a water soluble carbodiimide used in peptide coupling.
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19. There have only been a few reports of PPIases acting as folding catalysts in vivo: (a) For the role of cyclophilin in the maturation of the collagen triple helix, see: Steinmann, B.; Bruckner, P.; Superti-Furga, A. J. Biol. Chem. 1991, 266, 1299. (b) For cyclophilin catalyzed folding of the monomeric protein transferrin, see: Lodish, H. F.; Kong, N. J. Biol. Chem. 1991, 266, 14835. (c) For the possible role of PPIases in protein biogenesis in a eukaryotic cytosol, see: Kruse, M.; Brunke, A. E.; Escher, A.; Szalay, A. A.; Tropschug, M.; Zimmermann, R. J. Biol. Chem. 1995, 270, 2588.
20. There have only been a few reports of PPIases acting as folding catalysts in vivo: (a) For the role of cyclophilin in the maturation of the collagen triple helix, see: Steinmann, B.; Bruckner, P.; Superti-Furga, A. J. Biol. Chem. 1991, 266, 1299. (b) For cyclophilin catalyzed folding of the monomeric protein transferrin, see: Lodish, H. F.; Kong, N. J. Biol. Chem. 1991, 266, 14835. (c) For the possible role of PPIases in protein biogenesis in a eukaryotic cytosol, see: Kruse, M.; Brunke, A. E.; Escher, A.; Szalay, A. A.; Tropschug, M.; Zimmermann, R. J. Biol. Chem. 1995, 270, 2588.
21. There have only been a few reports of PPIases acting as folding catalysts in vivo: (a) For the role of cyclophilin in the maturation of the collagen triple helix, see: Steinmann, B.; Bruckner, P.; Superti-Furga, A. J. Biol. Chem. 1991, 266, 1299. (b) For cyclophilin catalyzed folding of the monomeric protein transferrin, see: Lodish, H. F.; Kong, N. J. Biol. Chem. 1991, 266, 14835. (c) For the possible role of PPIases in protein biogenesis in a eukaryotic cytosol, see: Kruse, M.; Brunke, A. E.; Escher, A.; Szalay, A. A.; Tropschug, M.; Zimmermann, R. J. Biol. Chem. 1995, 270, 2588.
22. The terminology used in the literature for rotamase enzymes can be ambiguous. "PPIase" was originally synonymous with cyclophilin, but the current usage, and the one we adopt here, is to use PPIase as a generic term encompassing both cyclophilin and FKBP. When we wish to refer to a specific enzyme, we will clearly differentiate between them.
23. (a) Fruman, D. A.; Burakoff, S. J.; Bierer, B. E. FASEB J. 1994, 8, 391.
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25. It is known that the catalysis of cis-trans amide isomerization is not the direct function of the PPIases in immunosupression; rather, a complex of the immunosupressive drug and the enzyme is believed to bind to the protein phosphatase calcineurin, and thereby inhibit T-cell activation. The immunosupressive drugs do, however, bind in the active site of isomerase activity; see: Schreiber, S. L.; Crabtree, G. R. Immunol. Today 1992, 13, 136. It is interesting to speculate why these enzymes apparently perform two unrelated tasks by utilizing the same active site.
26. Other postulated roles of the PPIases in vivo include: (a) Acting as chaperones, especially for escorting rhodopsin from the ER through the secretory pathway to its cellular target, see: Baker, E. K.; Colley, N. J.; Zuker, C. S. EMBO J. 1994, 13, 4886. (b) Effectors of Xaa-Pro bonds which may act as "molecular switches" to trigger actions such as voltage-gated ion channel opening; see: Suchyna, T. M.; Xu, L. X.; Gao, F.; Fourtner, C. R.; Nicholoson, B. J. Nature 1993, 365, 847. (c) Modulation of calcium release by interaction with calcium release channels; see: Jayaraman, T.; Brillantes, A.-M.; Timerman, A. P.; Fleischer, S.; Erdjument-Bromage, H.; Tempst, P.; Marks, A. R. J. Biol. Chem. 1992, 267, 9474. (d) Helping with protein degradation by catalyzing unfolding and prevention of partially unfolded proteins from precipitation, see: Andres, C. J.; Macdonald, T. L.; Ocain, T. D.; Longhi, D. J. Org. Chem. 1993, 58, 6609. (e) Functioning as an auxiliary enzyme in HIV-1 protease-mediated reactions, see: Vance, J. E.; LeBlanc, D. A.; Wingfield, P.; London, R. E. J. Biol. Chem. 1997, 272, 15603.
27. Other postulated roles of the PPIases in vivo include: (a) Acting as chaperones, especially for escorting rhodopsin from the ER through the secretory pathway to its cellular target, see: Baker, E. K.; Colley, N. J.; Zuker, C. S. EMBO J. 1994, 13, 4886. (b) Effectors of Xaa-Pro bonds which may act as "molecular switches" to trigger actions such as voltage-gated ion channel opening; see: Suchyna, T. M.; Xu, L. X.; Gao, F.; Fourtner, C. R.; Nicholoson, B. J. Nature 1993, 365, 847. (c) Modulation of calcium release by interaction with calcium release channels; see: Jayaraman, T.; Brillantes, A.-M.; Timerman, A. P.; Fleischer, S.; Erdjument-Bromage, H.; Tempst, P.; Marks, A. R. J. Biol. Chem. 1992, 267, 9474. (d) Helping with protein degradation by catalyzing unfolding and prevention of partially unfolded proteins from precipitation, see: Andres, C. J.; Macdonald, T. L.; Ocain, T. D.; Longhi, D. J. Org. Chem. 1993, 58, 6609. (e) Functioning as an auxiliary enzyme in HIV-1 protease-mediated reactions, see: Vance, J. E.; LeBlanc, D. A.; Wingfield, P.; London, R. E. J. Biol. Chem. 1997, 272, 15603.
28. Other postulated roles of the PPIases in vivo include: (a) Acting as chaperones, especially for escorting rhodopsin from the ER through the secretory pathway to its cellular target, see: Baker, E. K.; Colley, N. J.; Zuker, C. S. EMBO J. 1994, 13, 4886. (b) Effectors of Xaa-Pro bonds which may act as "molecular switches" to trigger actions such as voltage-gated ion channel opening; see: Suchyna, T. M.; Xu, L. X.; Gao, F.; Fourtner, C. R.; Nicholoson, B. J. Nature 1993, 365, 847. (c) Modulation of calcium release by interaction with calcium release channels; see: Jayaraman, T.; Brillantes, A.-M.; Timerman, A. P.; Fleischer, S.; Erdjument-Bromage, H.; Tempst, P.; Marks, A. R. J. Biol. Chem. 1992, 267, 9474. (d) Helping with protein degradation by catalyzing unfolding and prevention of partially unfolded proteins from precipitation, see: Andres, C. J.; Macdonald, T. L.; Ocain, T. D.; Longhi, D. J. Org. Chem. 1993, 58, 6609. (e) Functioning as an auxiliary enzyme in HIV-1 protease-mediated reactions, see: Vance, J. E.; LeBlanc, D. A.; Wingfield, P.; London, R. E. J. Biol. Chem. 1997, 272, 15603.
29. Other postulated roles of the PPIases in vivo include: (a) Acting as chaperones, especially for escorting rhodopsin from the ER through the secretory pathway to its cellular target, see: Baker, E. K.; Colley, N. J.; Zuker, C. S. EMBO J. 1994, 13, 4886. (b) Effectors of Xaa-Pro bonds which may act as "molecular switches" to trigger actions such as voltage-gated ion channel opening; see: Suchyna, T. M.; Xu, L. X.; Gao, F.; Fourtner, C. R.; Nicholoson, B. J. Nature 1993, 365, 847. (c) Modulation of calcium release by interaction with calcium release channels; see: Jayaraman, T.; Brillantes, A.-M.; Timerman, A. P.; Fleischer, S.; Erdjument-Bromage, H.; Tempst, P.; Marks, A. R. J. Biol. Chem. 1992, 267, 9474. (d) Helping with protein degradation by catalyzing unfolding and prevention of partially unfolded proteins from precipitation, see: Andres, C. J.; Macdonald, T. L.; Ocain, T. D.; Longhi, D. J. Org. Chem. 1993, 58, 6609. (e) Functioning as an auxiliary enzyme in HIV-1 protease-mediated reactions, see: Vance, J. E.; LeBlanc, D. A.; Wingfield, P.; London, R. E. J. Biol. Chem. 1997, 272, 15603.
30. Other postulated roles of the PPIases in vivo include: (a) Acting as chaperones, especially for escorting rhodopsin from the ER through the secretory pathway to its cellular target, see: Baker, E. K.; Colley, N. J.; Zuker, C. S. EMBO J. 1994, 13, 4886. (b) Effectors of Xaa-Pro bonds which may act as "molecular switches" to trigger actions such as voltage-gated ion channel opening; see: Suchyna, T. M.; Xu, L. X.; Gao, F.; Fourtner, C. R.; Nicholoson, B. J. Nature 1993, 365, 847. (c) Modulation of calcium release by interaction with calcium release channels; see: Jayaraman, T.; Brillantes, A.-M.; Timerman, A. P.; Fleischer, S.; Erdjument-Bromage, H.; Tempst, P.; Marks, A. R. J. Biol. Chem. 1992, 267, 9474. (d) Helping with protein degradation by catalyzing unfolding and prevention of partially unfolded proteins from precipitation, see: Andres, C. J.; Macdonald, T. L.; Ocain, T. D.; Longhi, D. J. Org. Chem. 1993, 58, 6609. (e) Functioning as an auxiliary enzyme in HIV-1 protease-mediated reactions, see: Vance, J. E.; LeBlanc, D. A.; Wingfield, P.; London, R. E. J. Biol. Chem. 1997, 272, 15603.
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38. See for example: (a) Shoham, G.; Lipscomb, W. N.; Wieland, T. J. Am. Chem. Soc. 1989, 111, 4791. (b) Kopple, K. D.; Bhandary, K. K.; Kartha, G.; Yang, Y.-S.; Parameswaran, K. N. J. Am. Chem. Soc. 1986, 108, 4637. (c) Springer, J. P.; Cole, R. J.; Dorner, J. W.; Cox, R. H.; Richard, J. L.; Barnes, C. L.; van der Helm, D. J. Am. Chem. Soc. 1984, 106, 2388. (d) Montelione, G. T.; Arnold, E.; Meinwald, Y. C.; Stimson, E. R.; Denton, J. B.; Huang, S. G.; Clardy, J.; Scheraga, H. A. J. Am. Chem. Soc. 1984, 106, 6, 7946. (e) Karle, I. L. J. Am. Chem. Soc. 1979, 101, 181.
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