Structural features of angiotensin-I converting enzyme catalytic sites: Conformation studies in solution, homology models and comparison with other zinc metallopeptidases

Current Topics in Medicinal Chemistry

Volumn 4, Issue 4, 2004, Pages 403-429

  Spyroulias, Georgios A ^a   Galanis, Athanassios S ^a   Pairas, George ^a   Manessi Zoupa, Evy ^a   Cordopatis, Paul ^a  

^a UNIVERSITY OF PATRAS   (Greece)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIHYPERTENSIVE AGENT; CAPTOPRIL; DIPEPTIDYL CARBOXYPEPTIDASE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; ENALAPRIL; ENALAPRILAT; FOSINOPRIL; FOSINOPRILAT; ISOPROTEIN; LISINOPRIL; METALLOPROTEINASE; PEPTIDE; THERMOLYSIN; TRANDOLAPRIL; TRANDOLAPRILAT; ZINC;

AMINO ACID SEQUENCE; BLOOD PRESSURE REGULATION; CARBOXY TERMINAL SEQUENCE; COMPUTER MODEL; DRUG BINDING; DRUG DESIGN; DRUG STRUCTURE; ENZYME ACTIVE SITE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME CONFORMATION; ENZYME INHIBITION; ENZYME STRUCTURE; ENZYME SUBSTRATE; ENZYME SYNTHESIS; HUMAN; HYDROLYSIS; NONHUMAN; PROTEIN DEGRADATION; PROTEIN FAMILY; PROTEIN STRUCTURE; RENIN ANGIOTENSIN ALDOSTERONE SYSTEM; REVIEW; SEQUENCE HOMOLOGY; X RAY ANALYSIS;

AMINO ACID MOTIFS; AMINO ACID SEQUENCE; ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; CARBOXYPEPTIDASES A; CATALYTIC DOMAIN; HUMANS; HYPERTENSION; METALLOPROTEASES; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; NUCLEAR MAGNETIC RESONANCE, BIOMOLECULAR; PEPTIDYL-DIPEPTIDASE A; PROTEIN CONFORMATION; STRUCTURAL HOMOLOGY, PROTEIN; THERMOLYSIN; ZINC;

EID: 3042720167     PISSN: 15680266     EISSN: None     Source Type: Journal    
DOI: 10.2174/1568026043451294     Document Type: Review

References (150)

1. Inagami, T. The renin-angiotensin system. Essays Biochem. 1994, 28, 147-164.
2. Ondetti, M. A.; Cushman, D. W. Enzymes of the renin-angiotensin system and their inhibitors. Annu. Rev. Biochem. 1982, 51, 283-308.
3. Roks, A.; Buikema, H.; Pinto, Y. M.; van Gilst, W. H. The renin-angiotensin system and vascular function. The role of angiotensin II, angiotensin-converting enzyme, and alternative conversion of angiotensin I. Heart Vessels 1997, 12, 119-124.
4. Skeggs, L. T.; Kahn, J. R.; Shumway, N. P. Preparation and function of the hypertension converting enzyme. J. Exp. Med. 1956, 103, 295-299.
5. Soffer, R. L. Angiotensin-converting enzyme and the regulation of vasoactive peptides. Annu. Rev. Biochem. 1976;45, 73-94.
6. Ehlers, M. R.; Riordan, J. F. Angiotensin-converting enzyme: new concepts concerning its biological role. Biochemistry 1989, 28, 5311-5318.
7. Dorer, F. E.; Kahn, J. R.; Lentz, K. E.; Levine, M.; Skeggs, L. T. Hydrolysis of bradykinin by angiotensin-converting enzyme. Circ. Res. 1974, 24, 824-827.
8. Kokkonen, J. O.; Lindstedt, K. A.; Kuoppala, A.; Kovanen, P. T. Kinin-degrading pathways in the human heart. Trends Cardiovasc. Med. 2000, 10, 42-45.
9. Yang, H. Y. Y.; Erdös, E. G.; Levin, V. A dipeptidyl carboxypeptidase that converts angiotensin I and inactivates bradykinin. Biochem. Biophys. Acta 1970, 214, 374-376.
10. Soubrier, F.; Alhenc-Gelas, F.; Hubert, C.; Allegrini, J.; John, M.; Tregear, G.; Corvol, P. Two putative active centers in human angiotensin I-converting enzyme revealed by molecular cloning. Proc. Natl. Acad. Sci. U.S.A. 1988, 85, 9386-9390.
11. Williams, T. A.; Corvol, P.; Soubrier, F. Identification of two active site residues in human angiotensin I-converting enzyme. J. Biol. Chem. 1994, 269, 29430-29434.
12. 2- and COOH-terminal tripeptides from the luteinizing hormone-releasing hormone. Proc. Natl. Acad. Sci. U.S.A. 1985, 82, 1025-1029.
13. Ehlers, M. R.; Riordan, J. F. Angiotensin-converting enzyme: zinc- and inhibitor-binding stoichiometries of the somatic and testis isozymes. Biochemistry 1991, 30, 7118-7126.
14. Gavras, H. Angiotensin converting enzyme inhibition and its impact on cardiovascular disease. Circulation 1990, 81, 381-388.
15. Ferreira, S. H.; Bartelt, D. C.; Greene, L. J. Isolation of bradykinin-potentiating peptides from Bothrops jararaca venom. Biochemistry 1970, 9, 2583-2593.
16. Ondetti, M. A.; Williams, N. J.; Sabo, E. F.; Pluscec, J.; Weaver, E. R.; Kocy, O. Angiotensin-converting enzyme inhibitors from the venom of Bothrops jararaca. Isolation, elucidation of structure, and synthesis. Biochemistry 1971, 10, 4033-4039.
17. Cheung, H. S.; Cushman, D. W. Inhibition of homogenous angiotensin-converting enzyme of rabbit lung by synthetic venom peptides of Bothrops jararaca. Biochim. Biophys. Acta 1973, 293, 451-463.
18. Steitz, T. A.; Ludwig, M. L.; Quiocho, F. A.; Lipscomb, W. N. The structure of carboxypeptidase A. V. Studies of enzyme-substrate and enzyme-inhibitor complexes at 6 Å resolution. J. Biol. Chem. 1967, 242, 4662-4668.
19. Cushman, D. W.; Ondetti, M. A. Design of angiotensin converting enzyme inhibitors. Nat. Med. 1999, 5, 1110-1113.
20. Vallee, B. L.; Auld, D. S. Zinc Coordination, Function, and Structure of Zinc Enzymes and Other Proteins. Biochemistry 1990, 29, 5647-5659.
21. Vallee, B. L.; Auld, D. S. New Perspective on Zinc Biochemistry: Cocatalytic Sites in Multi-Zinc Enzymes. Biochemistry 1993, 32, 6493-6500.
22. 2O of zinc enzymes. Proc. Natl. Acad. Sci. U.S.A. 1990, 87, 220-224.
23. Auld, D. S. Zinc sites in metalloenzymes and related proteins. In Handbook on Metallopreoteins; Bertini, I.; Sigel, A.; Sigel, H., Eds, Marcel Dekker, 2001, pp. 881-959.
24. Hooper, N. M. Families of zinc metalloproteases. FEBS Lett. 1994, 354, 1-6.
25. Thunnissen, M. M. G. M.; Nordlund, P. N.; Haeggstrom, J. Z. Crystal Structure of Human Leukotriene A4 Hydrolase, a Bifunctional Enzyme in Inflammation. Nat. Struct. Biol. 2001, 8, 131-135.
26. Brown, C. K.; Madauss, K.; Lian, W.; Beck, M. R.; Tolbert, W. D.; Rodgers, D. W. Structure of Neurolysin Reveals a Deep Channel that Limits Substrate Access. Proc. Nat. Acad. Sci. U.S.A. 2001, 98, 3127-3132.
27. Holland, D. R.; Hausrath, A. C.; Juers, D.; Matthews, B. W. Structural analysis of zinc substitutions in the active site of thermolysin. Protein Sci. 1995, 4, 1955-1965.
28. Oefner, C.; D'Arcy, A.; Hennig, M.; Winkler, F. K.; Dale, G. E. Structure of Human Neutral Endopeptidase (Neprilysin) Complexed with Phosphoramidon. J. Mol. Biol. 2000, 296, 341-349
29. Lacy, D. B.; Tepp, W.; Cohen, A. C.; Dasgupta, B. R.; Stevens, R. C. Crystal Structure of Botulinum Neurotoxin Type a and Implications for Toxicity. Nat. Struct. Biol. 1998, 5, 898-902.
30. Pannifer, A. D.; Wong, T. Y.; Schwarzenbacher, R.; Renatus, M.; Petosa, C.; Bienkowska, J.; Lacy, D. B.; Collier, R. J.; Park, S.; Leppla, S. H.; Hanna, P.; Liddington, R. C. Crystal Structure of the Anthrax Lethal Factor. Nature 2001, 414, 229-233
31. Kurisu, G.; Kinoshita, T.; Sugimoto, A.; Nagara, A.; Kai, Y.; Kasai, N.; Harada, S. Structure of the zinc endoprotease from Streptomyces caespitosus. J. Biochem. 1997, 121, 304-308.
32. Schlagenhauf, E.; Etges, R.; Metcalf, P. The crystal structure of the Leishmania major surface proteinase leishmanolysin (gp63). Structure 1998, 6, 1035-1046.
33. Li, J.; Brick, P.; O'Hare, M. C.; Skarzynski, T.; Lloyd, L. F.; Curry, V. A.; Clark, I. M.; Bigg, H. F.; Hazleman, B. L.; Cawston, T. E.; Blow, D. M. Structure of full-length porcine synovial collagenase reveals a C-terminal domain containing a calcium-linked, four-bladed beta-propeller. Structure 1995, 3, 541-549.
34. Bode, W.; Gomis-Ruth, F. X.; Huber, R.; Zwilling, R.; Stocker, W. Structure of astacin and implications for activation of astacins and zinc-ligation of collagenases. Nature 1992, 358, 164-167.
35. Mcauley, K. E.; Jia-Xing, Y.; Dodson, E. J.; Lehmbeck, J.; Ostergaard, P. R.; Wilson, K. S. A Quick Solution: Ab Initio Structure Determination of a 19 kDa Metalloproteinase Using Acorn Acta Crystallogr., Sect. D 2001, 57, 1571-1578.
36. Greenblatt, H. M.; Feinberg, H.; Tucker, P. A.; Shoham, G. Carboxypeptidase A: native, zinc-removed and mercury-replaced forms. Acta Crystallogr., Sect. D. 1998, 54, 289-305.
37. 2+-containing D-alanyl-D-alanine-cleaving carboxypeptidase at 2.5 A resolution. Nature 1982 299, 469-470.
38. Taylor, A. B.; Smith, B. S.; Kitada, S.; Kojima, K.; Miyaura, H.; Otwinowski, Z.; Ito, A.; Deisenhofer, J. Crystal Structures of Mitochondrial Processing Peptidase Reveal the Mode for Specific Cleavage of Import Signal Sequences. Structure 2001, 9, 615-625.
39. Burley, S. K.; David, P. R.; Taylor, A.; Lipscomb, W. N. Molecular structure of leucine aminopeptidase at 2.7-A resolution. Proc. Natl. Acad. Sci. U.S.A. 1990, 87, 6878-6882.
40. Roderick, S. L.; Matthews, B. W. Structure of the cobalt-dependent methionine aminopeptidase from Escherichia coli: a new type of proteolytic enzyme. Biochemistry 1993, 32, 3907-3912.
41. Rowsell, S.; Pauptit, R. A.; Tucker, A. D.; Melton, R. G.; Blow, D. M.; Brick, P. Crystal structure of carboxypeptidase G2, a bacterial enzyme with applications in cancer therapy. Structure 1997, 5, 337-347.
42. Chevrier, B.; Schalk, C.; D'Orchymont, H.; Rondeau, J. M.; Moras, D.; Tarnus, C. Crystal structure of Aeromonas proteolytica aminopeptidase: a prototypical member of the co-catalytic zinc enzyme family. Structure 1994, 2, 283-291.
43. Pearson, M. A.; Michel, L. O.; Hausinger, R. P.; Karplus, P. A. Structures of Cys319 variants and acetohydroxamate-inhibited Klebsiella aerogenes urease. Biochemistry 1997, 36, 8164-8172.
44. Fritsche, E.; Paschos, A.; Beisel, H.-G.; Bock, A.; Huber, R. Crystal Structure of the Hydrogenase Maturating Endopeptidase Hybd from Escherichia Coli. J. Mol. Biol. 1999, 288, 989-998.
45. Laszlo, P.; Blundell, T. L. Sequences and topology. Curr. Opin. Struct. Biol. 1995, 5, 357-359
46. Jongeneel, C. V.; Bouvier, J.; Bairoch, A. A unique signature identifies a family of zinc-dependent metallopeptidases. FEBS Lett. 1989, 242, 211-214.
47. Vallee, B. L.; Auld, D. S. Short and long spacer sequences and other structural features of zinc binding sites in zinc enzymes. FEBS Lett. 1989, 257, 138-140.
48. Jiang, W.; Bond, J. S. Families of metalloendopeptidases and their relationships. FEBS Lett. 1992, 312, 110-114.
49. Bode, W.; Gomis-Rüth, F.-X.; Stöckler, W. Astacins, serralysins, snake venom and matrix metalloproteinases exhibit identical zinc-binding environments (HEXXHXXGXXH and Met-turn) and topologies and should be grouped into a common family, the 'metzincins'. FEBS Lett. 1993, 331, 134-140.
50. Rawlings, N. D.; Barrett, A. J. Evolutionary families of peptidases. Biochem. J. 1993, 290, 205-218.
51. Blundell, T. L. Metalloproteinase superfamilies and drug design. Nat. Struct. Biol. 1994, 1, 73-75.
52. Bode, W.; Stöckler, W. Structural features of a superfamily of zinc-endopeptidases: the metzincins. Curr. Opin.. Struct. Biol. 1995, 5, 383-390.
53. Colman, P. M; Jansonius, J. N.; Matthews, B. W. The structure of thermolysin: an electron density map at 2-3 A resolution. J. Mol. Biol. 1972, 70, 701-24.
54. Matthews B.W., Weaver L.H., Kester W.R. The conformation of thermolysin. J. Biol. Chem. 1974, 249, 8030-8044.
55. Holmes MA, Matthews BW. Structure of thermolysin refined at 1.6 A resolution. J. Mol. Biol. 1982, 160, 623-639.
56. Baumann U. Crystal structure of the 50 kDa metallo protease from Serratia marcescens. J. Mol. Biol. 1994, 242, 244-251.
57. Katsuya, Y.; Hamada, K.; Hata, Y.; Tanaka, N.; Sato, M., Katsube, Y.; Kakiuchi, K.; Miyata, K. Preliminary X-ray studies on Serratia protease. J. Biochem. 1985, 98, 1139-1142.
58. pdb code 1srp is linked to the reference: Hamada, K.; Hiramatsu, H.; Katsuya, Y.; Hata, Y.; Matsuura, Y.; Katsube, Y. Structural Analysis of Serratia Protease. Acta Crystallogr., Sect. A 1993, 49, 153. However, this citation seems to be a misprint, as it does not exist to the corresponding journal. A relative article to serralysin structure should be the following : Katsuya, Y.; Hamada, K.; Hata, Y.; Tanaka, N.; Sato, M.; Katsube, Y.; Kakiuchi, K.; Miyata, K.; Preliminary X-ray studies on Serratia protease. J. Biochem. 1985 98, 1139-1142.
59. Spurlino, J. C.; Smallwood, A. M.; Carlton, D. D.; Banks, T. M.; Vavra, K. J.; Johnson, J. S.; Cook, E. R.; Falvo, J.; Wahl, R. C.; Pulvino, T. A.; Wendoloski, J. J.; Smith, D. L. 1.56 Å structure of mature truncated human fibroblast collagenase. Proteins 1994, 19, 98-109.
60. Browner M. F.; Smith W. W.; Castelhano A. L. Matrilysin-inhibitor complexes : common themes among metalloproteases. Biochemistry 1995, 34, 6602-6610.
61. Gomis-Ruth, F. X.; Kress, L. F.; Bode, W. First structure of a snake venom metalloproteinase: a prototype for matrix metalloproteinases/collagenases. EMBO J. 1993, 12, 4151-4157.
62. Hori, T.; Kumasaka, T.; Yamamoto, M.; Nonaka, T.; Tanaka, N.; Hashimoto, Y.; Ueki, T.; Takio, K. Structure of a New 'Aspzincin' Metalloendopeptidase from Grifola Frondosa: Implications for the Catalytic Mechanism and Substrate Specificity Based on Several Different Crystal Forms. Acta Crystallogr., Sect. D 2001, 57, 361-368.
63. Christianson, D. W.; David, P. R.; Lipscomb, W. N. Mechanism of carboxypeptidase A: hydration of a ketonic substrate analogue. Proc. Natl. Acad. Sci. U.S.A. 1987, 84, 1512-1515.
64. Christianson, D. W.; Lipscomb, W. B. Carboxypeptidase-A. Acc. Chem. Res. 1989, 22, 62-69.
65. Osterman, A. L.; Grishin, N. V.; Smulevitch, S. V.; Matz, M. V.; Zagnitko, O. P.; Revina, L. P.; Stepanov, V. M. Primary structure of carboxypeptidase T: Delineation of functionally relevant features in Zn-carboxypeptidase family. J. Protein Chem. 1992, 11, 561-570.
66. Lipscomb, W. N.; Sträter N. Recent Advances in Zinc Enzymology. Chem. Rev. 1996, 96, 2375-2433.
67. Makarova, K. S.; Grishin, N. V. The Zn-peptidase superfamily: functional convergence after evolutionary divergence. J. Mol. Biol. 1999, 292, 11-17.
68. Greenblatt, H. M.; Feinberg, H.; Tucker, P. A.; Shoham, G. Carboxypeptidase A: native, zinc-removed and mercury-replaced forms. Acta Crystallogr., Sect. D 1998, 54, 289-305.
69. Blundell T. L. Metalloproteinase superfamilies and drug design. Nat. Struct. Biol. 1992, 2, 73-75.
70. Cushman, D. W.; Pluscec, J.; Williams, N. J.; Weaver, E. R.; Sabo, E. F.; Kocy, O.; Cheung, H. S.; Ondetti, M. A. Inhibition of angiotensin-coverting enzyme by analogs of peptides from Bothrops jararaca venom. Experientia 1973, 29, 1032-1035.
71. Elisseeva, Y. E.; Orekhovich, V. N.; Pavlikhina, L. V.; Alexeenko, L. P. Carboxycathepsin--a key regulatory component of two physiological systems involved in regulation of blood pressure. Clin. Chim. Acta. 1971, 31, 413-419.
72. Ondetti, M. A.; Rubin, B.; Cushman, D. W. Design of specific inhibitors of angiotensin-converting enzyme: new class of orally active antihypertensive agents. Science 1977, 196, 441-444.
73. Quiocho, F. A.; Lipscombe, W. N. Carboxypeptidase A: a protein and an enzyme. Adv. Protein Chem. 1971, 25, 1-78.
74. Pelmenschikov, V.; Blomberg, M. R. A.; Siegbahn, P. E. M. A theoretical study of the mechanism for peptide hydrolysis by thermolysin. J. Biol. Inorg. Chem. 2002, 7, 284-298.
75. Kester, W. R.; Matthews, B. W. Crystallographic study of the binding of dipeptide inhibitors to thermolysin: implications for the mechanism of catalysis. Biochemistry 1977, 16, 2506-2516.
76. Holmes, M. A.; Matthews, B. W. Binding of hydroxamic acid inhibitors to crystalline thermolysin suggests a pentacoordinate zinc intermediate in catalysis. Biochemistry 1981, 20, 6912-6920.
77. Hangauer, D. G.; Monzingo A. F.; Matthews, B. W. An interactive computer graphics study of thermolysin-catalyzed peptide cleavage and inhibition by N-carboxymethyl dipeptides. Biochemistry 1984, 23, 5730-5741.
78. Holden, H. M.; Tronrud, D. E.; Monzingo, A. F.; Weaver, L. H.; Matthews, B. W. Slow- and fast-binding inhibitors of thermolysin display different modes of binding: crystallographic analysis of extended phosphonamidate transition-state analogues. Biochemistry 1987, 26, 8542-8553.
79. Tronrud, D. E.; Holden, H. M.; Matthews, B. W. Structures of two thermolysin-inhibitor complexes that differ by a single hydrogen bond. Science 1987, 30, 571-574.
80. Matthews, B. W. Structural Basis of the Action of Thermolysin and Related Zinc Peptidases. Acc. Chem. Res. 1988, 21, 333-340.
81. Jaspard, E.; Wei, L.; Alhenc-Gelas, F. Differences in the properties and enzymatic specificities of the two active sites of angiotensin I-converting enzyme (kininase II). Studies with bradykinin and other natural peptides. J. Biol. Chem. 1993, 268, 9496-9503.
82. Erdös, E. G.; Deddish, P. A.; Marcic, B. M. Potentiation of Bradykinin Actions by ACE Inhibitors. Trends Endocrinol. Metab. 1999, 10, 223-229.
83. 2- and COOH-terminal tripeptides from the luteinizing hormone-releasing hormone. Proc. Natl. Acad. Sci. U. S. A. 1985, 82, 1025-1029.
84. Ehlers, M. R.; Riordan, J. F. Angiotensin-converting enzyme: zinc- and inhibitor-binding stoichiometries of the somatic and testis isozymes. Biochemistry 1991, 30, 7118-7126.
85. Casarini, D. E.; Plavinik, F. L.; Zanella, M. T.; Marson, O.; Krieger, J. E.; Hirata, I.Y.; Stella, R. C. Angiotensin converting enzymes from human urine of mild hypertensive untreated patients resemble the N-terminal fragment of human angiotensin I-converting enzyme. Int. J. Biochem. Cell Biol. 2001, 33, 75-85.
86. Deddish, P. A.; Marcic, B.; Jackman, H. L.; Wang, H. Z.; Skidgel, R. A.; Erdös, E. G. N-domain-specific substrate and C-domain inhibitors of angiotensin-converting enzyme: angiotensin-(1-7) and keto-ACE. Hypertension 1998, 31, 912-917.
87. Dive, V.; Cotton, J.; Yiotakis, A.; Michaud, A.; Vassiliou, S.; Jiracek, J.; Vazeux, G.; Chauvet, M. T.; Cuniasse, P.; Corvol, P. RXP 407, a phosphinic peptide, is a potent inhibitor of angiotensin I converting enzyme able to differentiate between its two active sites. Proc. Natl. Acad. Sci. U. S. A. 1999, 96, 4330-4335.
88. Junot, C.; Gonzales, M. F.; Ezan, E.; Cotton, J.; Vazeux, G.; Michaud, A.; Azizi, M.; Vassiliou, S.; Yiotakis, A.; Corvol, P.; Dive, V. RXP 407, a selective inhibitor of the N-domain of angiotensin I-converting enzyme, blocks in vivo the degradation of hemoregulatory peptide acetyl-Ser-Asp-Lys-Pro with no effect on angiotensin I hydrolysis. J. Pharmacol. Exp. Ther. 2001, 297, 606-611.
89. Corvol, P.; Williams, T. A. In Handbook of Proteolytic Enzymes; Barrett, A. J.; Rawlings, N. D.; Woessner, J. F., Eds.; Academic Press: New York, 1998; pp 1066-1076.
90. Shapiro, R.; Holmquist, B.; Riordan, J. F. Anion activation of angiotensin converting enzyme: dependence on nature of substrate. Biochemistry 1983, 22, 3850-3857.
91. - of angiotensin-converting enzyme is evolutionarily conserved: purification and properties of an angiotensin-converting enzyme from the housefly, Musca domestica. Biochem. J. 1996, 314, 639-646.
92. Wei, L.; Alhenc-Gelas, F.; Corvol, P.; Clauser, E. The two Homologous Domais of Human Angiotensin I-converting Enzyme Are Both Catalically Active. J. Biol. Chem. 1991, 266, 9002-9006.
93. Kester, W. R.; Matthews, B. W. Comparison of the structures of carboxypeptidase A and thermolysin. J. Biol. Chem. 1977, 252, 7704-7710.
94. Mayer, M.; Meyer, B. Mapping the active site of angiotensin-converting enzyme by Transferred NOE Spectroscopy. J. Med. Chem 2000, 43, 2093-2097.
95. Bünning, P.; Holmquist, B.; Riordan, J. F. Substrate specificity and kinetic characteristics of angiotensin converting enzyme. Biochemistry 1983, 22, 103-110.
96. Patchett, A. A.; Cordes, E. H. The design and properties of N-carboxyalkyldipeptide inhibitors of angiotensin-converting enzyme. Adv. Enzymol. Relat. Areas Mol. Biol. 1985, 57, 1-84.
97. Patchett, A. A.; Harris, E.; Tristram, E. W.; Wyvratt, M. J.; Wu, M. T.; Taub, D. Peterson, E. R.; Ikeler, T.; ten Broeke, J.; Payne, L. G.; Ondeyka, D. L.; Thorsett, E. D.; Greenlee, W. J.; Lohr, N. S.; Hoffsommer, R. D.; Joshua, H.; Ruyle, W. V.; Rothrock, J. W.; Aster, S. D.; Maycock, A. L.; Robinson, F. M.; Hirschmann, R.; Sweet, C. S.; Ulm, E. H.; Gross, D. M.; Vassil, T. C.; Stone, C. A. A new class of angiotensin-converting enzyme inhibitors. Nature 1980, 288, 280-283.
98. Moore, V. A.; Irwin, W. J.; Timmins, P.; Chong, S.; Dando, S. A.; Morrison, R. A. A rapid screening system to determine drug affinities for the intestinal dipeptide transporter 1 : system characterisation. Inter. J. Pharm. 2000, 210, 15-27.
99. Moore, V. A.; Irwin, W. J.; Timmins, P.; Chong, S.; Dando, S. A.; Morrison, R. A. A rapid screening system to determine drug affinities for the intestinal dipeptide transporter 2: affinities of ACE inhibitors. Inter. J. Pharm. 2000, 210, 29-44.
100. Cushman, D. W.; Cheung, H. S.; Sabo, E. F.; Ondetti, M. A. Design of potent competitive inhibitors of angiotensin-converting enzyme. Carboxyalkanoyl and mercaptoalkanoyl amino acids Biochemistry 1977, 16, 5484-5491.
101. Petrillo, E. W.; Ondetti, M. A. Angiotensin-converting enzyme inhibitors: medicinal chemistry and biological actions. Med. Res. Rev. 1982, 2, 1-41.
102. Cushman, D. W.; Cheung, H. S.; Sabo, E. F.; Ondetti, M. A. Development and design of specific inhibitors of angiotensin-converting enzyme. Am. J. Cardiol. 1982, 49, 1390-1394.
103. Wu, M. T.; Douglas, A. W.; Ondeyka, D. L.; Payne, L. G.; Ikeler, T. J. Joshua, H.; Patchett, A. A.; Synthesis of N2-[(S)-1-carboxy-3-phenylpropyl]-L-lysyl-L-proline (lisinopril). J. Pharm. Sci. 1985, 74, 352-354.
104. Krapcho, J.; Turk, C.; Cushman, D. W.; Powell, J. R.; DeForrest, J. M.; Spitzmiller, E. R.; Karanewsky, D. S.; Duggan, M.; Rovnsak, G.; Schwartz, J.; Natarajan, S.; Godfrey, J. D.; Ryono, D. E.; Neubeck, R.; Atwal, K. S.; Petrillo, E. W. Jr. Angiotensin-converting enzyme inhibitors. Mercaptan, carboxyalkyl dipeptide, and phosphinic acid inhibitors incorporating 4-substituted prolines. J. Med. Chem. 1988, 31, 1148-1160.
105. Michaud, A.; Chauvet, M. T.; Corvol, P. N-domain selectivity of angiotensin I-converting enzyme as assessed by structure-function studies of its highly selective substrate, N-acetyl-seryl-aspartyl-lysyl-proline. Biochem. Pharmacol. 1999, 57, 611-618.
106. Araujo, M. C.; Melo, R. L.; Cesari, M. H.; Juliano, M. A.; Juliano, L.; Carmona, A. K. Peptidase specificity characterization of C- and N-terminal catalytic sites of angiotensin I-converting enzyme. Biochemistry 2000, 39, 8519-8525.
107. Ehlers, M. R. W.; Kirsch, R. E. Catalysis of Angiotensin I Hydrolysis by Human Angiotensin-Converting Enzyme: Effect of Chloride and pH. Biochemistry, 1988, 27, 5538-5544.
108. Liu, X.; Fernandez, M.; Wouters, M. A.; Heyberger, S.; Husain, A. Arg(1098) is critical for the chloride dependence of human angiotensin I-converting enzyme C-domain catalytic activity. J. Biol. Chem. 2001, 276, 33518-33525.
109. Bünning, P.; Holmquist, B.; Riordan, J. F. Functional residues at the active site of angiotensin converting enzyme. Biochem. Biophys. Res. Commun. 1978, 83, 1442-1449.
110. Shapiro, R.; Riordan, J. F. Critical Lysine Residue at the Chloride Binding Site of Angiotensin Converting Enzyme. Biochemistry 1983, 22, 5315-5321.
111. Fernandez, M.; Liu, X.; Wouters, M. A.; Heyberger, S.; Husain, A. Angiotensin I-converting enzyme transition state stabilization by His1089: evidence for a catalytic mechanism distinct from other gluzincin metalloproteinases. J. Biol. Chem. 2001, 276, 4998-5004.
112. Chen, Y. N.; Ehlers, M. R.; Riordan, J. F. The functional role of tyrosine-200 in human testis angiotensin-converting enzyme. Biochem. Biophys. Res. Commun. 1992, 184, 306-309.
113. Sen, I.; Kasturi, S.; Abdul Jabbar, M.; Sen, G. C. Mutations in two specific residues of testicular angiotensin-converting enzyme change its catalytic properties. J. Biol. Chem. 1993, 268, 25748-25754.
114. Thompson, J. D.; Gibson, T. J.; Plewniak, F.; Jeanmougin, F.; Higgins, D. G. The CLUSTAL_X windows interface: flexible strategies for multiple sequence alignment aided by quality analysis tools. Nucleic Acids Res. 1997, 25, 4876-4882.
115. Martí-Renom, M. A.; Stuart, A. C.; Fiser, A.; Sánchez, R.; Melo, F.; Šali, A. Comparative protein structure modeling of genes and genomes. Annu. Rev. Biophys. Biomol. Struct. 2000, 29, 291-325.
116. Combet, C.; Blanchet, C.; Geourjon, C.; Deléage, G. NPS" Network Protein Sequence Analysis. TIBS 2000, 25, 147-150.
117. Garnier, J.; Osguthorpe, D. J.; Robson, B. Analysis of the accuracy and implications of simple methods for predicting the secondary structure of globular proteins. J. Mol. Biol. 1978, 120, 97-120.
118. Gibrat, J. F.; Garnier, J.; Robson, B. Further developments of protein secondary structure prediction using information theory. New parameters and consideration of residue pairs. J. Mol. Biol. 1987, 198, 425-443.
119. Garnier, J.; Gibrat, J. F.; Robson, B. GOR method for predicting protein secondary structure from amino acid sequence. Methods Enzymol. 1996, 266, 540-553.
120. Merrifield R. B. Solid Phase Synthesis. I. The synthesis of a Tetrapeptide. J. Am. Chem. Soc. 1963, 85, 2149-2154.
121. Veglia, G.; Porcelli, F.; DeSilva, T.; Prantner, A.; Opella, S.J. The structure of the metal-binding motiff GMTCAAC is similar in an 18-residue linear peptide and the mercury binding protein Merp. J. Am. Chem. Soc. 2000, 122, 2389-2390.
122. Opella, S. J.; DeSilva, T. M.; Veglia, G. Structural biology of metal-binding sequence. Curr. Opin. Chem. Biol. 2002, 6, 217-223.
123. DeSilva, T. M.; Veglia, T.; Porcelli, F.; Prantner, A. M.; Opella, S. J. Selectivity in heavy metal-binding to peptides and proteins. Biopolymers 2002, 64, 189-197.
124. Carpino, L. A.; Han, G. Y.; 9-Fluorenylmethoxycarbonyl function, a new base-sensitive amino-protecting group J. Am. Chem. Soc. 1970, 92, 5748-5749.
125. Barlos, K.; Gatos, D.; Kallitsis, J.; Papaphotiou, G.; Sotiriou, P.; Wenquing, Y.; Shafer, W. Darstellung geshützter peptid-fragmente unter einsatz substituierter triphenylmethyl-harze, Tetraedron Lett. 1989, 30, 3943-3946.
126. Papazacharias, S.; Pairas, G.; Kouimtzoglou, E.; Dermitzaki, E.; Manessi-Zoupa, E.; Gravanis, A.; Cordopatis, P. Synthesis and Biological Evaluation of New h/rCRH Peptide Analogs. In Peptides 2000; Martinez, J.; Fehrentz, J.-A., Eds, EDK, 2001, pp. 933-934.
127. King, D. S.; Fields, C. G.; Fields G. B. A cleavage method which minimizes side reactions following Fmoc solid phase peptide synthesis. Int. J. Pept. Protein Res. 1990, 36, 255-266
128. Braunschweiler, L.; Ernst, R. R. Coherence transfer by isotropic mixing : application to proton correlation spectroscopy. J. Magn. Reson. 1983, 53; 521-528.
129. Bax, A.; Davis, D. G. MLEV-17-based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Reson. 1985, 65, 355-360.
130. 1H spin-spin coupling constants in proteins. Biochem. Biophys. Res. Commun. 1983, 113, 967-974.
131. Jeener, J., Meier, B. H., Bachmann, P.; Ernst R.R. Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Chem. Phys. 1979, 71, 4546-4553.
132. Wüthrich, K. In NMR of Proteins and Nucleic Acids; Wiley: New York, 1986.
133. HNHα coupling constants from TOCSY or NOESY spectra. J. Biomol. NMR 1997, 10, 373-382.
134. Smith, L. J.; Bolin, K. A.; Schwalbe, H.; MacArthur, M. W.; Thorton, J. M.; Dobson, C. M. Analysis of main chain torsion angles in proteins: prediction of NMR coupling constants for native and random coil conformations. J. Mol. Biol. 1996, 255, 494-506.
135. Wishart, D.; Sykes, B.; Richards, F. Relationship between nuclear magnetic resonance chemical shift and protein secondary structure. J. Mol. Biol. 1991, 222, 311-333.
136. Wishart, D.; Sykes, B.; Richards, F. The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry 1992, 31, 1647-1651.
137. 1H chemical shifts obtained as a function of temperature and trifluoroethanol concentration for the peptide series GGXGG. J. Biomol. NMR 1995, 5, 14-24.
138. c active sites model peptides. In preparation.
139. Güntert, P.; Braun, W.; Wüthrich, K. Efficient computation of three-dimensional protein structures in solution from nuclear magnetic resonance data using the program DIANA and the supporting programs CALIBA, HABAS and GLOMSA. J. Mol. Biol. 1991, 217, 517-530.
140. Güntert, P.; Mumenthaler, C.; Wüthrich, K. Torsion angle dynamics for NMR structure calculation with the new program DYANA. J. Mol. Biol. 1997, 273, 283-298.
141. Pearlman, D. A.; Case, D. A.; Caldwell, J. W.; Ross, W. S.; Cheatham, T. E.; Ferguson, D. M.; Seibel, G. L.; Singh, U. C.; Weiner, P. K.; Kollman, P. A. AMBER 5.0. University of California, San Francisco, 1997.
142. Pearlman, D. A.; Case, D. A.; Caldwell, G. C.; Siebel, G. L.; Singh, U. C.; Weiner, P.; Kollman, P. A. AMBER 4.0. University of California, San Francisco, 1991.
143. Shortle, D.; Clarke, N. Alpha helix propensity of amino acids. Science 1993, 260, 1637-1640.
144. Shortle, D.; Clarke, N. Alpha helix propensity of amino acids. Science 1993, 262, 917-918.
145. Zuiderweg, E. R. P. Mapping Protein-Protein Interactions in Solution by NMR Spectroscopy. Biochemistry, 2002, 41, 1-7.
146. 1H NMR & Chemical Shift Perturbation Mapping. Biopolymers, 2003, 69, 244-252.
147. Koradi, R.; Billeter, M.; Wüthrich, K. MOLMOL: a program for display and analysis of macromolecular structures. J. Mol. Graph. 1996, 14, 51-55.
148. Natesh, R.; Schwager, S. L. U.; Sturrock, E. D.; Acharya, K. R. Crystal structure of the human angiotensin-converting enzyme-lisinopril complex. Nature 2003, 421, 551-554
149. Kim, H. M.; Shin, D. R.; Yoo, O. J.; Lee, H.; Lee, J. O. Crystal structure of Drosophila angiotensin I-converting enzyme bound to captopril and lisinopril. FEBS Lett. 2003, 538, 65-70
150. Arndt, J. W.; Hao, B.; Ramakrishnan, V.; Cheng, T.; Chan, S. I.; Chan, M. K. Crystal structure of a novel carboxypeptidase from the hyperthermophilic archaeon Pyrococcus furiosus. Structure 2002, 215-224.