Novel mechanism of inhibition of human angiotensin-l-converting enzyme (ACE) by a highly specific phosphinic tripeptide

Biochemical Journal

Volumn 436, Issue 1, 2011, Pages 53-59

  Akif, Mohd ^a   Schwager, Sylva L ^b   Anthony, Colin S ^b   Czarny, Bertrand ^c   Beau, Fabrice ^c   Dive, Vincent ^c   Sturrock, Edward D ^b   Acharya, K Ravi ^a  

^a University of Bath   (United Kingdom)

^b UNIVERSITY OF CAPE TOWN   (South Africa)

^c SERVICE DE CHIMIE BIOORGANIQUE ET DE MARQUAGE   (France)

Author keywords

Angiotensin l converting enzyme (ACE); Cardivascular disease; Crystal structure; Inhibitor design; Metalloprotease

Indexed keywords

DIPEPTIDYL CARBOXYPEPTIDASE; DIPEPTIDYL CARBOXYPEPTIDASE INHIBITOR; ENDOTHELIN CONVERTING ENZYME; MEMBRANE METALLOENDOPEPTIDASE; PHOSPHINIC ACID DERIVATIVE; TRIPEPTIDE DERIVATIVE;

ARTICLE; BLOOD PRESSURE REGULATION; DRUG SYNTHESIS; ENZYME ACTIVE SITE; ENZYME INHIBITION; PEPTIDE SYNTHESIS; PRIORITY JOURNAL; PROTEIN DOMAIN; TESTIS;

ANGIOTENSIN-CONVERTING ENZYME INHIBITORS; ASPARTIC ACID ENDOPEPTIDASES; BINDING SITES; HUMANS; METALLOENDOPEPTIDASES; MODELS, MOLECULAR; OLIGOPEPTIDES; PEPTIDES; PEPTIDYL-DIPEPTIDASE A; PHOSPHINIC ACIDS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 79955529503     PISSN: 02646021     EISSN: 14708728     Source Type: Journal    
DOI: 10.1042/BJ20102123     Document Type: Article

References (47)

1. Petrillo, E. W. J. and Ondetti, M. A. (1982) Angiotensin-converting enzyme inhibitors: medicinal chemistry and biological actions. Med. Res. Rev. 2, 1-41
2. Roques, B. P., Noble, F., Daugé, V., Fournié-Zaluski, M. C. and Beaumont, A. (1993) Neutral endopeptidase 2411: structure, inhibition, and experimental and clinical pharmacology. Pharmacol. Rev. 45, 87-146 (Pubitemid 23108243)
3. Jeng, A. Y. (2003) Utility of endothelin-converting enzyme inhibitors for the treatment of cardiovascular diseases. Curr. Opin. Investig. Drugs 4, 1076-1081 (Pubitemid 37321401)
4. Acharya, K. R., Sturrock, E. D., Riordan, J. F. and Ehlers, M. R. W. (2003) ACE revisited: a new target for structure-based drug design. Nat. Rev. Drug Discovery 2, 891-902 (Pubitemid 37407795)
5. Cerdeira, A. S., Brás-Silva, C. and Leite-Moreira, A. F. (2008) Endothelin-converting enzyme inhibitors: their application in cardiovascular diseases. Rev. Port. Cardiol. 27, 385-408 (Pubitemid 351631807)
6. Dive, V., Chang, C., Yiotakis, A. and Sturrock, E. D. (2009) Inhibition of zinc metallopeptidases in cardiovascular disease: from unity to trinity, or duality? Curr. Pharm. Des. 15, 3606-3621
7. Antonios, T. F. and MacGregor, G. A. (1995) Angiotensin converting enzyme inhibitors in hypertension: potential problems. J. Hypertens. Suppl. 13, S11-S16
8. Israili, Z. H. and Hall, W. D. (1992) Cough and angioneurotic edema associated with angiotensin-converting enzyme inhibitor therapy. A review of the literature and pathophysiology. Ann. Intern. Med. 117, 234-242
9. Wei, C. C., Hase, N., Inoue, Y., Bradley, E. W., Yahiro, E., Li, M., Naqvi, N., Powell, P. C., Shi, K., Takahashi, Y. et al. (2010) Mast cell chymase limits the cardiac efficacy of Ang I-converting enzyme inhibitor therapy in rodents. J. Clin. Invest. 120, 1229-1239
10. Elijovich, F. and Laffer, C. (2009) A role for single-pill triple therapy in hypertension. Ther. Adv. Cardiovasc. Dis. 3, 231-240
11. Gros, C., Noel, N., Souque, A., Schwartz, J. C., Danvy, D., Plaquevent, J. C., Duhamel, L., Duhamel, P., Lecomte, J. M. and Bralet, J. (1991) Mixed inhibitors of angiotensin-converting enzyme and enkephalinase: rational design, properties, and potential cardiovascular applications of glycopril and alatriopril. Proc. Natl. Acad. Sci. U.S.A. 88, 4210-4214 (Pubitemid 21914509)
12. Worthley, M. I., Corti, R. and Worthley, S. G. (2004) Vasopeptidase inhibitors: will they have a role in clinical practice? Br. J. Clin. Pharmacol. 57, 27-36 (Pubitemid 38067947)
13. Daull, P., Jeng, A. Y. and Battistini, B. (2007) Towards triple vasopeptidase inhibitors for the treatment of cardiovascular diseases. J. Cardiovasc. Pharmacol. 50, 247-256 (Pubitemid 47428971)
14. Campbell, D.J. (2003) Vasopeptidase inhibition: a double-edged sword? Hypertension 41, 383-389 (Pubitemid 36314604)
15. Jullien, N., Makritis, A., Georgiadis, D., Beau, F., Yiotakis, A. and Dive, V. (2010) Phosphinic tripeptides as dual angiotensin-converting enzyme C-domain and endothelin-converting enzyme-1 inhibitors. J. Med. Chem. 53, 208-220
16. Soubrier, F., Alhenc-Gelas, F., Hubert, C., Allegrini, J., John, M., Tregear, G. and Corvol, P. (1988) Two putative active centers in human angiotensin I-converting enzyme revealed by molecular cloning. Proc. Natl. Acad. Sci. U.S.A. 85, 9386-9390 (Pubitemid 19027137)
17. Ehlers, M. R. and Riordan, J. F. (1989) Angiotensin-converting enzyme: new concepts concerning its biological role. Biochemistry 28, 5311-5318 (Pubitemid 19175737)
18. Fuchs, S., Xiao, H. D., Hubert, C., Michaud, A., Campbell, D. J., Adams, J. W., Capecchi, M. R., Corvol, P. and Bernstein, K. E. (2008) Angiotensin-converting enzyme C-terminal catalytic domain is the main site of angiotensin I cleavage in vivo. Hypertension 51, 267-274 (Pubitemid 351159938)
19. Rousseau, A., Michaud, A, Chauvet, M. T., Lenfant, M. and Corvol, P. (1995) The hemoregulatory peptide N-acetyl-Ser-Asp-Lys-Pro is a natural and specific substrate of the N-terminal active site of human angiotensin-converting enzyme. J. Biol. Chem. 270, 3656-3661
20. Li, P., Xiao, H. D., Xu, J., Ong, F. S., Kwon, M., Roman, J., Gal, A., Bernstein, K. E. and Fuchs, S. (2010) Angiotensin-converting enzyme N-terminal inactivation alleviates bleomycin-induced lung injury. Am. J. Pathol. 177, 1113-1121
21. Voronov, S., Zueva, N., Orlov, V., Arutyunyan, A. and Kost, O. (2002) Temperature-induced selective death of the C-domain within angiotensin- converting enzyme molecule. FEBS Lett. 522, 77-82 (Pubitemid 34722501)
22. Sturrock, E. D., Danilov, S. M. and Riordan, J. F. (1997) Limited proteolysis of human kidney angiotensin-converting enzyme and generation of catalytically active N- and C-terminal domains. Biochem. Biophys. Res. Commun. 236, 16-19 (Pubitemid 27341830)
23. Wei, L., Clauser, E., Alhenc-Gelas, F. and Corvol, P. (1992) The two homologous domains of human angiotensin I-converting enzyme interact differently with competitive inhibitors. J. Biol. Chem. 267, 13398-13405
24. Jaspard, E., Wei, L. and Alhenc-Gelas, F. (1993) 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. 268, 9496-9503 (Pubitemid 23146003)
25. Deddish, P. A., Jackman, H. L., Skidgel, R. A. and Erdös, E. G. (1997) Differences in the hydrolysis of enkephalin congeners by the two domains of angiotensin converting enzyme. Biochem. Pharmacol. 53, 1459-1463 (Pubitemid 27356118)
26. Deddish, P. A., Marcic, B., Jackman, H. L., Wang, H. Z., Skidgel, R. A. and Erdös, E. G. (1998) N-domain-specific substrate and C-domain inhibitors of angiotensin-converting enzyme: angiotensin-(1-7) and keto-ACE. Hypertension 31, 912-917 (Pubitemid 28185567)
27. Natesh, R., Schwager, S. L. U., Sturrock, E. D. and Acharya, K. R. (2003) Crystal structure of the human angiotensin-converting enzyme-lisinopril complex. Nature 421, 551-554 (Pubitemid 36168450)
28. Natesh, R., Schwager, S. L. U., Evans, H. R., Sturrock, E. D. and Acharya, K. R. (2004) Structural details on the binding of antihypertensive drugs captopril and enalaprilat to human testicular angiotensin I-converting enzyme. Biochemistry 43, 8718-8724 (Pubitemid 38880042)
29. Corradi, H. R., Schwager, S. L. U., Nchinda, A. T., Sturrock, E. D. and Acharya, K. R. (2006) Crystal structure of the N domain of human somatic angiotensin I-converting enzyme provides a structural basis for domain-specific inhibitor design. J. Mol. Biol. 357, 964-974
30. Corradi, H. R., Chitapi, I., Sewell, B. T., Georgiadis, D., Dive, V., Sturrock, E. D. and Acharya, K. R. (2007) The structure of testis angiotensin-converting enzyme in complex with the C domain-specific inhibitor RXPA380. Biochemistry 46, 5473-5478 (Pubitemid 46717270)
31. Watermeyer, J. M., Kröger, W. L., O'Neill, H. G., Sewell, B. T. and Sturrock, E. D. (2008) Probing the basis of domain-dependent inhibition using novel ketone inhibitors of angiotensin-converting enzyme. Biochemistry 47, 5942-5950 (Pubitemid 351770024)
32. Watermeyer, J. M., Kroöger, W. L., O'Neill, H. G., Sewell, B. T. and Sturrock, E. D. (2010) Characterization of domain-selective inhibitor binding in angiotensin-converting enzyme using a novel derivative of lisinopril. Biochem. J. 428, 67-74
33. Anthony, C. S., Corradi, H. R., Schwager, S. L. U., Redelinghuys, P., Georgiadis, D., Dive, V., Acharya, K. R. and Sturrock, E. D. (2010) The N domain of human angiotensin-I converting enzyme: the role of N-glycosylation and the crystal structure in complex with an N domain specific phosphinic inhibitor RXP407. J. Biol. Chem. 285, 35685-35693
34. Jullien, N. D., Cuniasse, P., Georgiadis, D., Yiotakis, A. and Dive, V. (2006) Combined use of selective inhibitors and fluorogenic substrates to study the specificity of somatic wild-type angiotensin-converting enzyme. FEBS J. 273, 1772-1781 (Pubitemid 43779829)
35. Gordon, K., Redelinghuys, P., Schwager, S. L. U., Ehlers, M. R. W., Papageorgiou, A. C., Natesh, R., Acharya, K. R. and Sturrock, E. D. (2003) Deglycosylation, processing and crystallization of human testis angiotensin-converting enzyme. Biochem. J. 371, 437-442 (Pubitemid 36547627)
36. Otwinoswski, Z. and Minor, W. (1997) Processing of X-ray diffraction data collected in oscillation mode. Methods Enzymol. 276, 307-326 (Pubitemid 27085611)
37. Collaborative Computational Project, Number 4 (1994) The CCP4 suite: programs for protein crystallography. Acta Crystallogr. Sect. D Biol. Crystallogr. 50, 760-763
38. McCoy, A. J., Grosse-Kunstleve, R. W. P., Adams, P. D., Winn, M. D., Storoni, L. C. and Read, R. J. (2007) PHASER crystallographic software. J. Appl. Crystallogr. 40, 658-674 (Pubitemid 47080256)
39. Murshudov, G. N., Vagin, A. A. and Dodson, E. J. (1997) Refinement of macromolecular structures by the maximum-likelihood method. Acta Crystallogr. Sect. D Biol. Crystallogr. D53, 240-255 (Pubitemid 27235885)
40. Brünger, A. T. (1992) Free R value: a novel statistical quantity for assessing the accuracy of crystal structures. Nature 355, 472-475
41. Emsley, P. and Cowtan, K. (2004) COOT: model-building tools for molecular graphics. Acta Crystallogr. Sect. D Biol. Crystallogr. D60, 2126-2132 (Pubitemid 41742764)
42. Schüttelkopf, A. W. and van Aalten, D. M. F. (2004) PRODRG: a tool for high-throughput crystallography of protein-ligand complexes. Acta Crystallogr. Sect. D Biol. Crystallogr. D60, 1355-1363 (Pubitemid 41079731)
43. Laskowski, R. A., Moss, D. S. and Thornton, J. M. (1993) Main-chain bond lengths and bond angles in protein structures. J. Mol. Biol. 231, 1049-1067 (Pubitemid 23209879)
44. Davis, I. W., Leaver-Fay, A., Chen, V. B., Block, J. N., Kapral, G. J., Wang, X., Murray, L. W., Arendall, III, W. B., Snoeyink, J., Richardson, J. S. and Richardson, D. C. (2007) MOLPROBITY: all-atom contacts and structure validation for proteins and nucleic acids. Nucleic Acids Res. 35, W375-W383
45. McDonald, I. K. and Thornton, J. M. (1994) Satisfying hydrogen bonding potential in proteins. J. Mol. Biol. 238, 777-793 (Pubitemid 24168633)
46. Yu, X. C., Sturrock, E. D., Wu, Z., Biemann, K., Ehlers, M. R. and Riordan, J. F. (1997) Identification of N-linked glycosylation sites in human testis angiotensin-converting enzyme and expression of an active deglycosylated form. J. Biol. Chem. 272, 3511-3519 (Pubitemid 27066852)
47. Georgiadis, D., Cuniasse, P., Cotton, J., Yiotakis, A. and Dive, V (2004) Structural determinants of RXPA380, a potent and highly selective inhibitor of the angiotensin-converting enzyme C-domain. Biochemistry 43, 8048-8054 (Pubitemid 38808259)