Investigation of subsite preferences in aminopeptidase A (EC 3.4.11.7) led to the design of the first highly potent and selective inhibitors of this enzyme

Journal of Medicinal Chemistry

Volumn 42, Issue 25, 1999, Pages 5197-5211

  David, Christelle ^a   Bischoff, Laurent ^a   Meudal, Hervé ^a   Mothé, Aurélie ^a   De Mota, Nadia ^b   DaNascimento, Sophie ^a   Llorens Cortes, Catherine ^b   Fournié Zaluski, Marie Claude ^a   Roques, Bernard P ^a  

^a Laboratoire de Pharmacochimie   (France)

^b INSERM   (France)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOTENSIN; CHOLECYSTOKININ OCTAPEPTIDE; GLUTAMYL AMINOPEPTIDASE; GLUTAMYL AMINOPEPTIDASE INHIBITOR; UNCLASSIFIED DRUG;

ARTICLE; DRUG DESIGN; DRUG POTENCY; DRUG STRUCTURE; DRUG SYNTHESIS; ENZYME ACTIVE SITE; ENZYME SUBSTRATE; NONHUMAN; STEREOCHEMISTRY; STRUCTURE ANALYSIS;

AMINOPEPTIDASES; ANIMALS; ANTIGENS, CD13; ENZYME INHIBITORS; GLUTAMYL AMINOPEPTIDASE; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR STRUCTURE; NEPRILYSIN; PEPTIDYL-DIPEPTIDASE A; RABBITS; RATS; RECOMBINANT PROTEINS; STEREOISOMERISM; SWINE;

EID: 0033576715     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm9903040     Document Type: Article

References (65)

1. Wilk, S.; Healy, D. P. Glutamyl aminopeptidase (aminopeptidase A), the BP-1/6C3 antigen. Adv. Neuroimmunol. 1993, 3, 195-207.
2. Nagatsu, I.; Nagatsu, T.; Yamamoto, T.; Glenner, G. G.; Mehl, J. W. Purification of aminopeptidase A in human serum and degradation of angiotensin II by the purified enzyme. Biochim. Biophys. Acta 1970, 198, 255-270.
3. Wu, Q.; Lahti, J. M.; Avi, G. M.; Burrows, P. D.; Cooper, M. D. Molecular cloning of the murine BP-1/6C3 antigen: a member of the zinc-dependent metallopeptidase family. Proc. Natl. Acad. Sci. U.S.A. 1990, 87, 993-997.
4. Nanus, D. M.; Engelstein, D.; Gastl, G. A.; Gluck, L.; Vidal, M. J.; Morrison, M.; Finstad, C. L.; Bander, N. H.; Albino, A. P. Molecular cloning of the human kidney differentiation antigen gp160: human aminopeptidase A. Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 7069-7073.
5. Li, L.; Wang, J.; Cooper, M. D. cDNA cloning and expression of human glutamyl aminopeptidase (aminopeptidase A). Genomics 1993, 17, 657-664.
6. Benchetrit, T.; Bissery, V.; Mornon, J. P.; Devault, A.; Crine, P.; Roques, B. P. Primary structure homologies between two Zn-metallopeptidases, the neutral endopeptidase 24.11 enkephalinase and the thermolysin through clustering. Biochemistry 1988, 27, 592-596.
7. Roques, B. P. Zinc metallopeptidases: active site structure and design of selective and mixed inhibitors. New approach in the search for analgesics and antihypertensives. Biochem. Soc. Trans. 1993, 21, 678-685.
8. Roques, B. P.; Noble, F.; Daugé, V.; Fournié-Zaluski, M. C.; Beaumont, A. Neutral endopeptidase 24.11. Structure, inhibition, and experimental and clinical pharmacology. Pharmacol. Rev. 1993, 45 (1), 87-146.
9. Matthews, B. W. Structural basis of the action of thermolysin and related zinc peptidases. Acc. Chem. Res. 1988, 21, 333-340.
10. Jongeneel, C. V.; Bouvier, J.; Bairoch, A. A unique signature identifies a family of zinc-dependent metallopeptidases. FEBS Lett. 1989, 242, 211-214.
11. Rawling, N.; Barrett, A. Evolutionary families of metallopeptidases. Methods Enzymol. 1995, 290, 205-218.
12. Wang, J. Y.; Cooper, M. D. Histidine residue in the zinc-binding motif of aminopeptidase A is critical for enzymatic activity. Proc. Natl. Acad. Sci. U.S.A. 1993, 90, 1222-1226.
13. Vazeux, G.; Wang, J.; Corvol, P.; Llorens-Cortès, C. Identification of glutamate residues essential for catalytic activity and zinc coordination in aminopeptidase A. J. Biol. Chem. 1996, 271, 9069-9074.
14. Vazeux, G.; Iturrioz, X.; Corvol, P.; Llorens-Cortès, C. A tyrosine residue essential for catalytic activity in aminopeptidase A. Biochem. J. 1997, 327, 883-889.
15. Vazeux, G.; Iturrioz, X.; Corvol, P.; Llorens-Cortès, C. A glutamate residue contributes to the exopeptidase specificity in aminopeptidase A. Biochem. J. 1998, 334, 407-413.
16. Luciani, N.; Marie-Claire, C.; Ruffet, E.; Beaumont, A.; Roques, B. P.; Fournié-Zaluski, M.-C. Characterization of Glu 350 as a critical residue involved in the N-terminal amino binding site of aminopeptidase N (EC 3.4.11.2): Insights into its mechanism of action. Biochemistry 1998, 37, 686-692.
17. Zini, S.; Fournié-Zaluski, M.-C.; Chauvel, E.; Roques, B. P.; Corvol, P.; Llorens-Cortès, C. Identification of metabolic pathways of brain angiotensin II and III using specific aminopeptidase inhibitors: predominant role of angiotensin III in the control of vasopressin release. Proc. Natl. Acad. Sci. U.S.A. 1996, 93, 11968-11973.
18. Wright, J. W.; Mitzutani, S.; Murray, C. E.; Amir, H. Z.; Harding, J. W. Aminopeptidase-induced elevations and reductions in blood pressure in the spontaneously hypertensive rat. J. Hypertens. 1990, 8, 969-974.
19. Aoyagi, T.; Tobe, H.; Kojima, F.; Hamada, M.; Takeuchi, T.; Umezawa, H. Amastatin, an inhibitor of aminopeptidase A, produced by Actinomycetes. J. Antibiot. 1978, 31, 636-638.
20. Umezawa, H.; Aoyagi, T.; Suda, H.; Hamada, M.; Takeuchi, T. Bestatin, an inhibitor of aminopeptidase B, produced by Actinomycetes. J. Antibiot. 1976, 29, 97-99.
21. Chan, W. W. C. L-Leucine thiol. A potent inhibitor of leucine aminopeptidase. Biochem. Biophys. Res. Commun. 1983, 116, 297-302.
22. Fournié-Zaluski, M.-C.; Coric, P.; Turcaud, S.; Bruetschy, L.; Lucas, E.; Noble, F.; Roques, B. P. Potent and systemically active aminopeptidase N inhibitors from active-site investigation. J. Med. Chem. 1992, 35, 1259-1266.
23. Wilk, S.; Thurston, L. S. Inhibition of angiotensin III formation by thiol derivatives of acidic amino acids. Neuropeptides 1990, 16, 163-168.
24. Chauvel, E. N.; Coric, P.; Llorens-Cortès, C.; Wilk, S.; Roques, B. P.; Fournié-Zaluski, M.-C. Differential inhibition of aminopeptidase A and aminopeptidase N by new β-amino thiols. J. Med. Chem. 1994, 37, 2950-2957.
25. Roberts, J. C.; Gao, H.; Gopalsamy, A.; Kongsjahju, A.; Patch, R. J. Neopentyl ester protecting groups for arylsulfonic acids. Tetrahedron Lett. 1997, 38, 355-358.
26. Bischoff, L.; David, C.; Martin, L.; Meudal, H.; Roques, B. P.; Fournié-Zaluski, M.-C. 2,4-Dinitrophenyl 4-methoxybenzyl disulfide: A new reagent for the electrophilic sulfenylation of β-amino ester enolates. J. Org. Chem. 1997, 62, 4848-4850.
27. Gordon, E. M.; Godfrey, J. D.; Delaney, N. G.; Aaaad, M. M.; Von Langen, D.; Cushman, D. W. Design of novel inhibitors of aminopeptidases. Synthesis of peptide-derived diamino-thiols and sulfur containing replacement analogues of bestatin. J. Med. Chem. 1988, 31, 2199-2211.
28. Wei, Z. Y.; Knaus, E. E. A regioselective tandem reduction-Wittig Horner reaction involving the α-ester moiety of diethyl aspartate or glutamate. Tetrahedron Lett. 1994, 35, 2305-2308.
29. Wang, S. S.; Gisin, B. F.; Winter, D. P.; Makofske, R.; kulesha, I. D.; Tsougraki, C.; Meienhofer, J. Facile synthesis of amino acids and dipeptide esters under mild conditions via cesium salts. J. Org. Chem. 1977, 42, 1286-1290.
30. Dhaon, M. K.; Olsen, R. K.; Ramasamy, K. Esterification of N-Protected α-amino acids with alcohol/Carbodiimide/4-(Dim-ethylamino)-pyridine. Racemization of aspartic and glutamic derivatives. J. Org. Chem. 1982, 47, 1962-1965.
31. 6. J. Am. Chem. Soc. 1988, 110, 291-293.
32. 6. Compatibility with halogen, sulfonate, and y-oxygen and sulfur substituents. Tetrahedron Lett. 1990, 31, 3237-324.
33. Bischoff, L.; David, C.; Roques, B. P.; Fournié-Zaluski, M.-C. Side-chain-modified sufonic analogues of aspartic and glutamic acids: Synthesis, protection and incorporation into peptides. J. Org. Chem. 1999, 64, 1420-1423.
34. Cotton, R.; Johnstone, A. N. C.; North, M. Asymmetric synthesis of 3-carboxyproline and derivatives suitable for peptide synthesis. Tetrahedron 1995, 51, 8525-8544.
35. Martin, L.; Cornille, F.; Turcaud, S.; Meudal, H.; Roques, B. P.; Fournié-Zaluski, M.-C. Metallopeptidase inhibitors of tetanus toxin: a combinatorial approach. J. Med. Chem. 1999, 42, 515-525.
36. Xie, J.; Soleilhac, J. M.; Schmidt, C.; Peyroux, J.; Roques, B. P.; Fournié-Zaluski, M. C. New kelatorphan-related inhibitors of enkephalin metabolism: improved antinociceptive properties. J. Med. Chem. 1989, 32, 1497-1503.
37. Ocain, T. D.; Rich, D. H. Synthesis of sulfur-containing analogues of bestatin. Inhibition of aminopeptidases by α-thiol bestatin analogues. J. Med. Chem. 1988, 31, 2193-2199.
38. Chen, H.; Noble, F.; Coric, P.; Fournié-Zaluski, M. C.; Roques, B. P. Aminophosphinic inhibitors as transition states analogues of enkephalin-degrading enzymes: A class of central analgesics. Proc. Natl. Acad. Sci. U.S.A. 1998, 95, 12028-12033.
39. Rich, D. H.; Moon, B. J.; Harbeson, S. Inhibition of aminopeptidases by amastatin and bestatin derivatives. Effect of inhibitor structure and slow-binding processes. J. Med. Chem. 1984, 27, 417-422.
40. Kim, H.; Lipscomb, W. N. X-ray crystallographic determination of the structure of bovine Lens leucine aminopeptidase complexed with amastatin: Formulation of a catalytic mechanism featuring a gem-diolate transition state. Biochemistry 1993, 32, 8465-8478.
41. Kim, H.; Burley, S. K.; Lipscomb, W. N. Re-refinement of the X-ray crystal structure of bovine Lens leucine aminopeptidase complexed with bestatin. J. Mol. Biol. 1993, 230, 722-724.
42. Wyvratt, M. J.; Patchett, A. A. Recent developments in the design of angiotensin converting enzyme inhibitors. Med. Res. Rev. 1985, 5, 483-531.
43. Roques, B. P.; Fournié-Zaluski, M. C.; Soroca, E.; Lecomte, J. M.; Malfroy, B.; Llorens, C.; Schwartz, J. C. The enkephalinase inhibitor thiorphan shows antinociceptive activity in mice. Nature 1980, 288, 286-288.
44. Berger, J. A novel approach to analgesia: synthesis and structure activity relationship of some potent and selective inhibitors of enkephalinase A. 19th National Medicinal Chemistry Symposium, Tucson, 1984.
45. Kanno, H.; Osanai, K.; Nishi, T.; Iino, M.; Katakura, S.; Furugohri, T.; Watanabe, Y. Synthesis and evaluation of 2-(biphenylmethyl)glutaric acid amide derivatives as neutral endopeptidase inhibitors. Bioorg. Med. Chem. Lett. 1996, 6, 1487-1490.
46. Fournié-Zaluski, M. C.; Llorens, C.; Gacel, G.; Malfroy, B.; Swerts, J. P.; Lecomte, J. M.; Schwartz, J. C.; Roques, B. P. Synthesis and biological properties of highly potent enkephalinase inhibitors. In Peptides; ed. Brunfeld, K., Ed.; Scriptor: Copenhagen, Denmark, 1981; pp 476-481.
47. Wilk, S.; Wilk, E.; Magnusson, R. P. Purification, characterization and cloning of a cytosolic aspartyl aminopeptidase. J. Biol. Chem. 1998, 273, 15961-15970.
48. Vazeux, G.; Wilk, S.; Wilk, E.; Corvol, P.; Llorens-Cortes, C. Production and properties of a recombinant soluble form of aminopeptidase A. Eur. J. Biochem. 1998, 254, 671-678.
49. Aubry, M.; Bertheloot, A.; Beaumont, A.; Roques, B. P.; Crine, P. The use of a monoclonal antibody for the high yield purification of kidney enkephalinase solubilized in β-octylglucoside. Biochem. Cell Biol. 1987, 65, 398-404.
50. Pantaliano, M. W.; Holmquist, B.; Riordan, J. F. Affinity chromatographic purification of angiotensin converting enzyme. Biochemistry 1984, 23, 1037-1042.
51. 2)Phe-βAla, a specific fluorogenic substrate for neutral endopeptidase 24.11. Anal. Biochem. 1994, 219, 87-95.
52. Piquilloud, Y.; Reinharz, A.; Roth, M. Studies of the angiotensin converting enzyme with different substrates. Biochim. Biophys. Acta 1970, 206, 136-142.
53. Goldbarg, J. A.; Rutenberg, A. M. The colorimetric determination of leucine aminopeptidase in urine and serum of normal subjects and patients with cancer and other diseases. Cancer 1958, 11, 283-291.
54. Cheung, H. S.; Cushman, D. W. Inhibition of homogeneous angiotensin converting enzyme of rabbit lung by synthetic venom peptides of both rops jararaca. Biochim. Biophys. Acta 1973, 293, 451-457.
55. 50) of an enzyme reaction. Biochem. Pharmacol. 1973, 22, 3099-3108.
56. Bergmann, M.; Zervas, L. A general method of peptide synthesis. Chem. Ber. 1932, 65, 1192-1201.
57. Brenner, M.; Huber, W. Preparation of α-amino ester by alcoholysis of methyl ester. Helv. Chim. Acta 1953, 36, 1109-1115.
58. Von Pechmann, H. About diazomethane. Chem. Ber. 1894, 27, 1888.
59. Ondetti, M. A.; Engel, S. L. Bradykinin analogues containing β-homoamino acids. J. Med. Chem. 1975, 18, 761-763.
60. Cheng, P. T. W.; Poss, M. A. Produgs esters of phosphonosulfonate squalene synthetase inhibitors and method. US Patent 1997, 5, 618,964.
61. Jennings, L. J.; Macchia, M.; Parkin, A. Synthesis of analogues of 5-iodo-2′-deoxyuridine-5′-diphosphate. J. Chem. Soc., Perkin Trans. 1992, 1, 2197-2202.
62. Saady, M., Lebeau, L.; Mioskowski, C. First use of benzyl phosphites in the Michaelis-Arbuzov reaction. Helv. Chim. Acta 1995, 78, 670-678.
63. Schwyzer, R.; Castopanagiotis, A.; Sieber, P. Two synthesis of α-melanotropins (α-MSH) with facile cleavage for the protecting groups. Helv 1963, 46, 870-889.
64. Castro, B.; Dormoy, J. R.; Evin, G.; Selve, C. Reactifs de couplage peptidique IV (1) - L'hexafluorophosphate de benzotriazolyl N-oxy-tridimethylamino phosphonium (B.O.P.). Tetrahedron Lett. 1975, 14, 1219-1222.
65. Mancuso, A. J.; Swern, D. Activated dimethyl sulfoxide: useful reagent for synthesis. Synthesis 1981, 165-185.