Advertisement

New Selective Aminopeptidase N Inhibitors as Potential Therapeutics

  • Marie-Claude Fournié-Zaluski
  • Bernard P. Roques
Chapter

Abstract

Aminopeptidase N (EC 3.4.11.2, APN) is a monomeric or homodimeric type II membrane-bound zinc metallopeptidase initially identified by Pfleiderer and coworkers in pig kidney (Pfleiderer and Celliers, 1963; Wachsmuth et al 1966).

Keywords

Boronic Acid Inhibitory Potency Neutral Endopeptidase Phosphinic Acid Transition State Analogue 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.

References

  1. Abe, F., Shibuya, K., Uchida, M., Takahashi, K., Matsuda, A., Ishizuka, M., Takeuchi, T., and Umezawa, H., 1984, Effect of bestatin on syngeneic tumors in mice. Gann 75: 89–94.PubMedGoogle Scholar
  2. Andersson, L., Isley, T.C., and Wolfenden, R., 1982, □-aminoaldehydes : Transition state analogue inhibitors of leucine aminopeptidase. Biochemistry 21: 4177–4180.PubMedCrossRefGoogle Scholar
  3. Aoyagi, T., Tobe, H., Kojima, F., Hamada, M., Takeuchi, T., and Umezawa, H., 1978, Amastatin, an inhibitor of aminopeptidase A, produced by actinomycetes. J. Antìbiot 31: 636–638.PubMedCrossRefGoogle Scholar
  4. Aoyagi, T., Yoshida, S., Nakamura, Y., Shigihara, Y., Hamada, and Takeuchi, T., 1990, Probestin, a new inhibitor of aminopeptidase M, produced by streptomyces azureus MH663-2F6. I. Taxonomy, production, isolation, physico-chemical properties and biological activities, k 43: 143–148.Google Scholar
  5. Aoyagi, T., Yoshida, S., Matsuda, N., Ikeda, T., Hamada, M, and Takeuchi, T., 1991, Leuhistin, a new inhibitor of aminopeptidase M, produced by Bacillus laterosporus BMI156-14F1. I. Taxonomy, production, isolation, physico-chemical properties and biological activities. J. Antibiot. 44: 573–578.PubMedCrossRefGoogle Scholar
  6. Ashmun, R.A., Shapiro, L.H., and Look, A.T., 1992, Deletion of the zinc-binding motif of CD13/aminopeptidase N molecules results in loss of epitopes that mediate binding of inhibitory antibodies. Blood 79: 3344–3349.PubMedGoogle Scholar
  7. Atherton, A.J., Monaghan, P., Warburton, M.J., and Gusterson, B.A., 1992, Immunocytochemical localization of the ectoenzyme aminopeptidase N in the human breast J. Histochem. Cytochem. 40: 705–710.PubMedCrossRefGoogle Scholar
  8. Bausback, H.H., and Ward, P.E., 1988, Kallidin and bradykinin metabolism by isolated cerebral microvessels. Biochem. Pharmacol 37: 2973–2978.PubMedCrossRefGoogle Scholar
  9. Boudinot, E., Morin-Surun, M.-P., Foutz, A.S., Fournié-Zaluski, M.C., Roques, B.P., and Denavit-Saubié, M., 2001, Effects of the potent analgesic enkephalin-catabolizing enzyme inhibitors RB 101 and kelatorphan on respiration. Pain 90: 7–13.PubMedCrossRefGoogle Scholar
  10. Bourgoin, S., Le Bars, D., Artaud, F., Clot, A.-M., Bouboutou, R., Fournié-Zaluski, M.-C., Roques, B.P., Hamon, M., and Cesselin, F., 1986, Effects of kelatorphan and other peptidase inhibitors on the in vitro and in vivo release of methionine-enkephalin-like material from the rat spinal cord.J. Pharmacol Exp. Ther 238: 360–366.PubMedGoogle Scholar
  11. Bryce, G.F., and Rabin, B.R., 1964, The assay and reaction kinetics of leucine aminopeptidase from swine kidney. Biochem. J. 90: 509–517.PubMedGoogle Scholar
  12. Burley, S.K., David, P.R., and Lipscomb, W.N., 1991, Leucine-aminopeptidase : Bestatin inhibition and a model for enzyme-catalyzed peptide hydrolysis. Proc. Natl Acad. Sci.USA 88: 6916–6920.PubMedCrossRefGoogle Scholar
  13. Chan, W.W.-C., Denis, P., Demmer, W., and Brand, K., 1982, Inhibition of leucine aminopeptidase by amino acid hydroxamate. J. Biol. Chem. 257: 7955–7957.PubMedGoogle Scholar
  14. Chan, W.W.-C., 1983, L-leucinthiol - A potent inhibitor of leucine aminopeptidase. Biochem. Biophys. Res. Commun. 116: 297–302.PubMedCrossRefGoogle Scholar
  15. Chavagnat, F., Casey, M.G., and Meyer, J., 1999, Purification, characterization, gene cloning, sequencing, and overexpression of aminopeptidase N from Streptococcus thermophilus A. App. Environm. Microbiol 65: 3001–3007.Google Scholar
  16. Chen, H., Kinzer, C.A., and Paul, W.E., 1986, PI61, a murine membrane protein expressed on mast cells and some macrophages, is mouse cdl3/aminopeptidase N. J. Immunol 157: 2593–2600.Google Scholar
  17. Chen, H., Noble, F., Coric, P., Fournié-Zaluski, M.C., and Roques, B.P., 1998, Aminophosphinic inhibitors as transition state analogues of enkephalin-degrading enzymes: A class of central analgesics. Proc. Natl. Acad. Sci. USA 95: 12028–12033.PubMedCrossRefGoogle Scholar
  18. Chen, H., Roques, B.P., and Fournié-Zaluski, M.C., 1999, Design of the first highly potent and selective aminopeptidase N (EC 3.4.11.2) inhibitors. Bioorg. Med. Chem. Lett. 9: 1511–1516.PubMedCrossRefGoogle Scholar
  19. Chen, H., Bischoff, L., Fournié-Zaluski, M.C., and Roques, B.P., 2000a, Synthesis of 2(S)-benzyl-3-[hydroxy( 1’(R)-aminoethyl)phosphinyl]propanoyl-L-3-[125I]-iodotyrosine : A radiolabelled inhibitor of aminopeptidase N. J. Labelled Cpd. Radiopharm. 43: 103–111.CrossRefGoogle Scholar
  20. Chen, H., Noble, F., Mothé, A., Meudal, H., Coric, P., Danascimento, S., Roques, B.P., George, P., and Fournié-Zaluski, M.C., 2000b, Phosphinic derivatives as new dual enkephalin-degrading enzyme inhibitors: Synthesis, biological properties, and antinociceptive activities. J. Med. Chem. 43: 1398–1408.PubMedCrossRefGoogle Scholar
  21. Chen, H., Noble, F., Roques, B.P., and Fournié-Zaluski, M.C., 2001, Long lasting antinociceptive properties of enkephalin degrading enzyme (NEP and APN) inhibitor prodrugs. J. Med. Chem. 44: 3523–3530.PubMedCrossRefGoogle Scholar
  22. Chérot, P., Fournié-Zaluski, M.C., and Laval, J., 1986, Purification and characterization of an enkephalin-degrading dipeptidyl-aminopeptidase from porcine brain. Biochemistry 25: 8184–8191.PubMedCrossRefGoogle Scholar
  23. Chevrier, B., D’Orchymont, H., Schalk, C., Tarnus, C., and Moras, D., 1996, The structure of the Aeromonos proteolytica aminopeptidase complexed with a hydroxamate inhibitor. Involvement in catalysis of Glul51 and two zinc ions of the co-catalytic unit. Eur. J. Biochem. 237: 393–398.PubMedCrossRefGoogle Scholar
  24. Chung, M.-C., Chun, H.-K., Han, K.-H., Lee, H.-J., Lee, C.-H., and Kho, Y.-H., 1996, MR387 A and B, new aminopeptidase N inhibitors, produced by Streptomyces neyagawaensis SL-387. J. Antibiot. 49: 99–102.PubMedCrossRefGoogle Scholar
  25. Coletti-Previero, M.-A., Crastes de Paulet, A., Mattras, H., and Previero, A., 1982, Amino acid hydroxamates as inhibitors of the human enkephalin-degrading aminopeptidase. Biochem. Biophys. Res. Commun. 107: 465–169.PubMedCrossRefGoogle Scholar
  26. Danielsen, E.M., Cowell, G.M., Noren, O., and Sjöström, H., 1984, Biosynthesis of microvillar proteins. Biochem. J. 221: 1–14.PubMedGoogle Scholar
  27. Delmas, B., Gelfi, J., L’Haridon, R., Vogel L.K., Sjöström, H., Noren, O., and Laude, H., 1992, Aminopeptidase N is a major receptor for the enteropathogenic coronavirus TGEV. Nature 357: 417–420.PubMedCrossRefGoogle Scholar
  28. Delmas, B., Gelfi, J., Kut, E., Sjöström, H., Noren, O., and Laude, H., 1994, Determinants essential for the transmissible gastroenteritis virus-receptor interaction reside within a domain of aminopeptidase N that is distinct from the enzymatic site. J. Virol. 68: 5216–5224.PubMedGoogle Scholar
  29. DiGregorio, M., Pickering, D.S., and Chan, W.W.-C., 1988, Multiple sites and synergism in the binding of inhibitors to microsomal aminopeptidase. Biochem. 27: 3613–3617.CrossRefGoogle Scholar
  30. Dive, V., Lucet-Levannier, K., Georgiadis, D., Cotton, J., Vassiliou, S., Cuniasse, P., and Yiotakis, A., 2000, Phosphinic peptide inhibitors as tools in the study of the function of zinc metallopeptidases. Biochem. Soc Trans. 28: 455–460.PubMedCrossRefGoogle Scholar
  31. Feracci, H., Bemadac, A., Hovsepian, S., Fayet, G., and Maroux, S., 1981, Aminopeptidase N is a marker for the apical pole of porcine thyroid epithelial cells in vivo and in culture. Cell Tissue Res. 221: 137–146.PubMedCrossRefGoogle Scholar
  32. Fournié-Zaluski, M.C., Chaillet, P., Bouboutou, R., Coulaud, A., Chérot, P., Waksman, G., Costentin, and Roques, B.P., 1984, Analgesic effects of kelatorphan, a new highly potent inhibitor of multiple enkephalin degrading enzymes. Eur. J. Pharmacol. 102: 525–528.PubMedCrossRefGoogle Scholar
  33. Fournié-Zaluski, M.C., Coulaud, A., Bouboutou, R., Chaillet, P., Devin, J., Waksman, G., Costentin, J., and Roques, B.P., 1985, New bidentates as full inhibitors of enkephalin- degrading enzymes : Synthesis and analgesic properties. J. Med. Chem. 28: 1158–1169.PubMedCrossRefGoogle Scholar
  34. Fournié-Zaluski, MC, Hernandez, J.-F., Soleilhac, J.M., Renwart, N., Peyroux, J., Xie, J., and Roques, B.P., 1989, Enkephalin-degrading enzyme inhibitors. Crucial role of the Cterminal residue on the inhibitory potencies of retro-hydroxamate dipeptides. Int. J. Pept. Prot Res. 33: 146–153.CrossRefGoogle Scholar
  35. Fournié-Zaluski, M.C., Coric, P., Turcaud, S., Bruetschy, L., Lucas, E., Noble, F., and Roques, B.P., 1992, Potent and systemically active aminopeptidase N inhibitors designed from active-site investigation. J. Med. Chem. 35: 1259–1266.PubMedCrossRefGoogle Scholar
  36. Funkhouser, J.D., Tangada, S.D., and Peterson, R.D., 1991, Ectopeptidases of alveolar epithelium : Candidates for roles in alveolar regulatory mechanisms. Am. J. Physiol. 260: L381–L385.PubMedGoogle Scholar
  37. Garcia-Lopez, T., Gonzalez-Muniz, R., Hartoa, J.R., Gomez-Monterrey, I., Pérez, C., De Ceballos, M.L., Lopez, E., and Del Rio, J., 1992, Synthesis and inhibitory activities againsts aminopeptidase B and enkephalin-degrading enzymes of ketomethylene dipeptide analogues of arphamenines. Arch. Pharm. 325: 3–8.CrossRefGoogle Scholar
  38. Giannousis, P.P., and Bartlett, P.A., 1987, Phosphorus amino acid analogues as inhibitors of leucine aminopeptidase. J. Med. Chem. 30: 1603–1609.PubMedCrossRefGoogle Scholar
  39. Gill, S.S., Cowles, E.A., and Francis, V., 1995, Identification, isolation, and cloning of a Bacillus thuringiensis CrylAc toxin-binding protein from the midgut of the lepidopteran insect Heliothis virescens. J. Biol. Chem. 270: 27277–27282.PubMedCrossRefGoogle Scholar
  40. Gordon, E.M., Godfrey, J.D., Delaney, N.G., Asaas, M.M., Von Langen, D., and Cushman, D.W., 1988, Design of novel inhibitors of aminopeptidases. Synthesis of peptide-derived diamino thiols and sulfur replacement analogues of bestatin. J. Med. Chem. 31: 2199–2211.PubMedCrossRefGoogle Scholar
  41. Greenberg, L.J., 1962, Fluorometric measurement of alkaline phosphatase and aminopeptidase activities in the order of 10-14 mole. Biochem. Biophys. Res. Commun. 9: 430–435.PubMedCrossRefGoogle Scholar
  42. Gros, C., Giros, B., and Schwartz, J.-C., 1985, Identification of aminopeptidase M as enkephalin-inactivating enzyme in rat cerebral membranes. Biochem. 24: 2179–2185.CrossRefGoogle Scholar
  43. Hachisu, M., Hiranuma, T., Murata, S., Aoyagi, T., and Umezawa, H., 1987, Analgesic effect of actinonin, a new potent inhibitor of multiple enkephalin degrading enzymes. Life Sci. 41: 235–240.PubMedCrossRefGoogle Scholar
  44. Harbeson, S.L., and Rich, D.H., 1989, Inhibition of aminopeptidases by peptides containing ketomethylene and hydroxyethylene amide bond replacements. J. Med. Chem. 32: 1378–1392.PubMedCrossRefGoogle Scholar
  45. Hélène, A., Beaumont, A., and Roques, B.P., 1991, Functional residues at the active site of aminopeptidase N. Eur. J. Biochem. 196: 385–393.PubMedCrossRefGoogle Scholar
  46. Hernandez, J.F., Soleilhac, J.M., Roques, B.P., and Fournié-Zaluski, M.C., 1988, Retroinverso concept applied to the complete inhibitors of enkephalin-degrading enzymes. J. Med. Chem. 31: 1825–1831.PubMedCrossRefGoogle Scholar
  47. Herranz, R., Vinuesa, S., Pérez, C., Garcia-Lopez, M.T., De Ceballos, M.L., Murillo, F.M., and Del Rio, J., 1992, Aminopeptidase inhibitory properties and anlgesic activity of (2S,3R)-3,7-diamino-2-hydroxy-heptanoic acid containing tripeptide analogues of the Nterminal tripeptide of probestin. Arch. Pharm. 325: 515–518.CrossRefGoogle Scholar
  48. Herranz, R., Castro-Pichel, J., Garcia-Lopez, M.T., Gomez-Monterrey, I., Pérez, C., and Vinuesa, S., 1993, Ketomethylenebestatin : Synthesis and aminopeptidase inhibition. Arch. Pharm. 326: 395–398.CrossRefGoogle Scholar
  49. Hersh, L.B., 1985, Characterization of membrane-bound aminopeptidases from rat brain : Identification of the enkephalin-degrading aminopeptidase. J. Neurochem. 44: 1427–1435.PubMedCrossRefGoogle Scholar
  50. Hersh, L.B., Aboukhair, N., and Watson, S., 1987, Immunohistochemical localization of aminopeptidase M in rat brain and periphery : Relationship of enzyme localization and enkephalin metabolism. Peptides 8 : 523–532.PubMedCrossRefGoogle Scholar
  51. Holmes, M.A., and Matthews, B.W., 1981, Binding of hydroxamic acid inhibitors to crystalline thermolysin suggests a pentacoordinate zinc intermediate in catalysis. Biochemistry 20 : 6912–6920.PubMedCrossRefGoogle Scholar
  52. Huang, K., Takahara, S., Kinouchi, T., Takeyama, M., Ishida, T., Ueyama, H., Nishi, K., and Ohkubo, I. 1997, Alanyl aminopeptidase from human seminal plasma: Purification, characterization, and immunohistochemical localization in the male genital tract. J. Biochem. 122 : 779–787.PubMedCrossRefGoogle Scholar
  53. Hussain, M.M., Tranum-Jensen, J., Noren, O., Sjöstròm, H., and Christiansen, K., 1981, Reconstitution of purified amphiphilic pig intestinal microvillus aminopeptidase. Biochem. J. 199: 179–186.PubMedGoogle Scholar
  54. Imai, K., Kanzaki, H., Fujiwara, H., Maeda, M., Ueda, M., Suginami, H., and Mori, T., 1994, Expression and localization of aminopeptidase N, neutral endopeptidase, and dipeptidyl peptidase IV in the human placenta and fetal membranes. Am. J. Obstet. Gynecol. 170 : 1163–1168.PubMedGoogle Scholar
  55. Jiang, X., Tangada, S., Peterson, R.D., and Funkhouser, J.D., 1992, Expression of aminopeptidase N in fetal rat lung during development. Am. J. Physiol. 263 : L460–L465.PubMedGoogle Scholar
  56. Kanayama, N., Kajiwara, Y., Goto, J., el Maradny, E., Maehara, K., Andou, K., and Terao, T., Inactivation of interleukin-8 by aminopeptidase N (CD13). J. Leukoc. Biol. 57 : 129-134.Google Scholar
  57. Kayser, V., Fournié-Zaluski, M.C., Guilbaud, G., and Roques, B.P., 1989, Potent antinociceptive effects of kelatorphan (a highly efficient inhibitor of multiple enkephalin-degrading enzymes) systemically administered in normal and arthritic rats. Brain Res. 497:94–101.PubMedCrossRefGoogle Scholar
  58. Kenny, A.J., Booth, A.G., and MacNair, R.D.C., 1977, Peptidases of the kidney microvillus membrane. ActaBiol. Med. Ger. 36 : 1575–1585.Google Scholar
  59. Kenny, A.J., and Maroux, S., 1982, Topology of microvillar membrane hydrolases of kidney and intestine. Physiol. Rev. 62 : 91–128.PubMedGoogle Scholar
  60. Kitabgi, P., Dubuc, I., Nouel, D., Costentin, J., Cuber, J.-C., Fulcrand, H., Doulut, S., Rodriguez, M., and Martinez, J., 1992, Effects of thiorphan, bestatin and a novel metallopeptidase inhibitor JMV 390-1 on the recovery of neurotensin and neuromedin N released from mouse hypothalamus. Neurosci. Lett. 142 : 200–204.PubMedCrossRefGoogle Scholar
  61. Krapcho, J., Turk, C., Cushman, D.W., Powell, J.R., DeForrest, J.M., Spitzmiller, E.R., Karanewsky, D.S., Duggan, M., Rovnyak, G., Schwartz, J., Natarajan, S., Godfrey, J.D., Ryono, D.E., Neubeck, R., Atwal, K.S., and Petrillo, Jr., E.W., 1988, Angiotensin converting enzyme inhibitors. Mercaptan, carboxyalkyl dipeptide, and phosphinic acid inhibitors incorporating 4-substituted prolines. J. Med. Chem. 31:1148–1160.PubMedCrossRefGoogle Scholar
  62. Kruse, O.A., Bolund, L., Grzeschik, K.-H., Ropers, H.H., Olsen, J., Sjöström, H., and Noren, O., 1988, Assignment of the human aminopeptidase N (peptidase E) gene to chromosome 15ql3-qter. FEBS Lett. 239(2): 305–308.PubMedCrossRefGoogle Scholar
  63. Lalu, K., Lampelo, S., and Vanha-Perttula, T., 1986, Characterization of three aminopeptidases purified from maternal serum. Biochim. Biophys. Acta 873 : 190–197.PubMedCrossRefGoogle Scholar
  64. Larsen, S.L., Pedersen, L.O., Buus, S., and Stryhn, A., 1996, T cell responses affected by aminopeptidase N (CD13)-mediated trimming of major histocompatibility complex class II-bound peptides. J. Exp. Med. 184 : 183–189.PubMedCrossRefGoogle Scholar
  65. Lejczak, B., Kafarski, P., and Zygmunt, J., 1989, Inhibition of aminopeptidases by aminophosphonates, Biochemistry 28 : 3549–3555.PubMedCrossRefGoogle Scholar
  66. Lejczak, B., Popiel de Choszczak, M., and Kafarski, P., 1993, Inhibition of aminopeptidases by phosphonic acid and phosphinic acid analogues of aspartic and glutamic acids. J. Enz. Inhib. 7 : 97–103.CrossRefGoogle Scholar
  67. Look, A.T., Peiper, S.C., Rebentish, M.B., Ashmun, R.A., Roussel, M.F., Lemons, R.S., Le Beau, M.M., Rubin, C.M., and Sherr, C.J., 1986, Molecular cloning, expression, and chromosomal localization of the gene encoding a human myeloid membrane antigen (gpl50). J. Clin. Invest. 78 : 914–921.PubMedCrossRefGoogle Scholar
  68. Look, AT., Ashmun, R.A., Shapiro, L.H., and Peiper, S.C., 1989, Human myeloid plasma membrane glycoprotein CD 13 (gpl50) is identical to aminopeptidase N. J. Clin. Invest. 83 : 1299–1307.PubMedCrossRefGoogle Scholar
  69. Luciani, N., Marie-Claire, C., Ruffet, E., Beaumont, A., Roques, B.P., and Fournié-Zaluski, M.C., 1998, Characterization of Glu350 as a critical residue involved in the N-terminal amine binding site of aminopeptidase N (EC 3.4.11.2): Insights into its mechanism of action. Biochemistry 37 : 686–692.PubMedCrossRefGoogle Scholar
  70. Maldonado, R., Valverde, O., Turcaud, S., Fournié-Zaluski, M.C., and Roques, B.P., 1994, Antinociceptive response induced by mixed inhibitors of enkephalin catabolism in peripheral inflammation. Pain 58 : 77–83.PubMedCrossRefGoogle Scholar
  71. Malfroy, B., Kado-Fong, H., Gros, C., Giros, B., Schwartz, J.-C., and Hellmiss, R., 1989, Molecular cloning and amino acid sequence of rat kidney aminopeptidase M : A member of a super family of zinc-metallohydrolases. Biochem. Biophys. Res. Commun. 161 : 236–241.PubMedCrossRefGoogle Scholar
  72. Mantle, D., Hardy, M.F., Lauffart, B., McDermott, J.R., Smith, A.I., and Pennington, J.T., 1983, Purification and characterization of the major aminopeptidase from human skeletal muscle. Biochem. J. 211 : 567–573.PubMedGoogle Scholar
  73. Maroux, S., Louvard, D., and Baiatti, J., 1973, The aminopeptidase from hog intestinal brush border. Biochim. Biophys. Acta 321 : 282–295.Google Scholar
  74. Matthews, B.W., 1988, Structural basis of the action of thermolysin and related zinc peptidases. Ace. Chem. Res. 21 : 333–340.CrossRefGoogle Scholar
  75. McDonald, J.K., and Barrett, A.J., 1986, Microsomal alanyl aminopeptidase. In Mammalian Proteinases. A glossary and bibliography. Barrett, A.J. and McDonald, J.K. (eds.), Academic Press, New York Vol. 2, pp. 59–71.Google Scholar
  76. Miyachi, H., Kato, M., Kato, F., and Hashimoto, Y., 1998, Novel potent nonpeptide aminopeptidase N inhibitors with a cyclic imide skeleton. J. Med. Chem. 41 : 263–265.PubMedCrossRefGoogle Scholar
  77. Montiel, J.L., Cornille, F., Roques, B.P., and Noble, F., 1997, Nociceptin/orphanin FQ metabolism. Role of aminopeptidase and endopeptidase 24.15. J. Neurochem. 68 : 354–361.PubMedCrossRefGoogle Scholar
  78. Nagai, M., Kojima, F., Naganawa, H., Hamada, M., Aoyagi, H., and Takeuchi, T., 1997,Phebestin, a new inhibitor of aminopeptidase N, produced by Streptomyces sp. MJ716-m3.J. Antibiot. 50 : 82–84.PubMedCrossRefGoogle Scholar
  79. Nakanishi, M., Moriyama, A., Narita, Y., and Sasaki, M., 1989, Aminopeptidase M from human liver. I. Solibilization, purification, and some properties of the enzyme. J. Biochem.106 : 818–825.PubMedGoogle Scholar
  80. Naquet, P., Vivier, L., Gorvel, J.P., Brekelmans, P., Barad, M, Bernard, A.M., and Pierres, M., 1989, Activation of mouse T lymphocytes by a monoclonal antibody to a developmentally regulated surface aminopeptidase (THAM). Immunol. Rev. 111 : 177–193.PubMedCrossRefGoogle Scholar
  81. Nishimura, K., and Hazato, T., 1993, Isolation and identification of an endogenous inhibitor of enkephalin-degrading enzymes from bovine spinal cord. Biochem. Biophys. Res.Commun. 194 : 713–719.CrossRefGoogle Scholar
  82. Nishino, N., and Powers, J.C., 1978, Peptide hydroxamic acids as inhibitors of thermolysin.Biochemistry 17 : 2846–2850.PubMedCrossRefGoogle Scholar
  83. Nishino, N., and Powers, J.C., 1979, Design of potent reversible inhibitors for thermolysin.Peptides containing zinc coordinating ligands and their use in affinity chromatography.Biochemistry 18 : 4340–1347.PubMedCrossRefGoogle Scholar
  84. Nishizawa, R., Saino T., Takita, T., Suda, H., and Aoyagi, T., 1977, Synthesis and structureactivity relationships of bestatin analogues, inhibitors of aminopeptidase B. J. Med. Chem.20:510–515.PubMedCrossRefGoogle Scholar
  85. Noble, F., Soleilhac, J.M., Soroca-Lucas, E., Turcaud, S., Fournié-Zaluski, M.C., andRoques,B.P., 1992a, Inhibition of the enkephalin metabolizing enzymes by the first systemically active mixed inhibitor prodrug RB 101 induces potent analgesic responses in mice and rats. J. Pharmacol. Exp. Ther. 261 : 181–190.PubMedGoogle Scholar
  86. Noble, F., Turcaud, S., Fournié-Zaluski, M.C., and Roques, B.P., 1992b, Repeated systemic administration of the mixed inhibitor of enkephalin-degrading enzymes, RB 101, does not induce either antinociceptive tolerance or cross-tolerance with morphine. Eur. J.Pharmacol. 223 : 83–89.PubMedCrossRefGoogle Scholar
  87. Noble, F., Coric, P., Fournié-Zaluski, M.C., and Roques, B.P., 1992c, Lack of physical dependence development in mice following repeated systemic administration of the mixed inhibitor prodrug of enkephalin-degrading enzymes, RB 101. Eur. J. Pharmacol. 223 : 91–96.PubMedCrossRefGoogle Scholar
  88. Noble, F., Fournié-Zaluski, M.C., and Roques, B.P., 1993, Unlike morphine, the endogenous enkephalins protected by RB 101 are unable to establish a conditioned place preference in mice. Eur. J. Pharmacol. 230 : 139–149.PubMedCrossRefGoogle Scholar
  89. Noble, F., and Roques, B.P., 1997, Association of aminopeptidase N and endopeptidase 24.15 inhibitors potentiate behavioral effects mediated by nociceptin/orphanin FQ in mice. FEBS Lett. 401 : 227–229.PubMedCrossRefGoogle Scholar
  90. Noble, F., Luciani, N., Da Nascimento, S., Laï-Kuen, R., Bischoff, L., Chen, H., Fournié-Zaluski, M.C., and Roques, B.P., 2000, Binding properties of a highly potent and selective iodinated aminopeptidase N inhibitor appropriate for radioautography. FEBS Lett. 467 :81–86.PubMedCrossRefGoogle Scholar
  91. Noble, F., Banisadr, G., Jardinaud, F., Popovici, T., Laï-Kuen, R., Chen, H., Bischoff, L.,Melik Parsadaniantz, S., Fournié-Zaluski, M.C., and Roques, B.P., 2001, First discrete autoradiographic distribution of aminopeptidase N in various structures of rat brain and spinal cord using the selective iodinated inhibitor [125I]RB 129. Neuroscience 105 : 479–488.PubMedCrossRefGoogle Scholar
  92. Noren, O., Dabelsteen, E., Hoyer, P.E., Olsen, J., Sjöström, H., and Hansen, G.H., 1989,Onset of transcription of the aminopeptidase N (leukemia antigen CD 13) gene at the crypt/villus transition zone during rabbit enterocyte differentiation. FEBS Lett. 259 : 107–112.PubMedCrossRefGoogle Scholar
  93. Noren, O., Sjöström, H., Danielsen, E.M., Cowell, G.M., and Skovbjerg, H., 1986, The enzymes of Ihe enterocyte plasma membrane. In Molecular and Cellular Basis of Digestion (P. Desnuelle, H. Sjöström and O. Noren, eds), Elsevier, Amsterdam, pp. 335–365.Google Scholar
  94. Noren, O., Sjöström, H., and Olsen, J., 1997, Aminopeptidase N. In Cell-Surface Peptidases in Health & Disease (A.J. Kenny, and C.M. Boustead, eds), Bioscientific Publishers, pp. 175–191.Google Scholar
  95. Ocain, T.D., and Rich, D.H., 1988, Synthesis of sulfur-containing analogues of bestatin. Inhibition of aminopeptidases by a-thiolbestatin analogues. J. Med. Chem. 31 :2193–2199.PubMedCrossRefGoogle Scholar
  96. Ohuchi, S., Suda, H., Naganawa, H., Kawamura, K., Aoyagi, T., and Umezawa, H., 1985, Structure-activity relationships among derivatives of arphamenines, inhibitors of aminopeptidase B. J. Antibiot. 37 : 1741–1743.CrossRefGoogle Scholar
  97. Olsen, J., Cowell, G.M., Konigshofer, E., Danielsen, E.M., Moller, J., Laustsen, L., Hansen, O.C., Welinder, K.G., Engberg, J., Hunziker, W., Spiess, M., Sjöström, H., and Noren, O., 1988, Complete amino acid sequence of human intestinal aminopeptidase N as deduced from cloned cDNA. FEBS Lett. 238 : 307–314.PubMedCrossRefGoogle Scholar
  98. Olsen, J., Sjöström, H., and Noren, O., 1989, Cloning of the pig aminopeptidase N gene. FEBS Lett. 251 : 275–281.PubMedCrossRefGoogle Scholar
  99. Pasqualini, R., Koivunen, E., Kain, R., Lahdenranta, J., Sakamoto, M., Stryhn, A., Ashmun, R.A., Arap, W., and Ruoslahti, E., 2000, Aminopeptidase N is a receptor for tumorhoming peptides and a target for inhibiting angiogenesis. Cancer Res. 60 : 722–727.PubMedGoogle Scholar
  100. Pickering, D.S., Krishna, M.V., Miller, D.C., and Chan, W.W.-C, 1985, Structural requirements for specific inhibition of microsomal aminopeptidase by mercaptoamines. Arch. Biochem. Biophys. 239 : 368–374.Google Scholar
  101. Pfleiderer, G., and Celliers, P.G., 1963, Isolation of an aminopeptidase from kidney microsomal functions. Biochem. 339 : 186–189.Google Scholar
  102. Porteous, J.W., and Clark, B., 1965, The isolation and characterization of subcellular components of the epithelial cells of rabbit small intestine. Biochem. J. 96 : 159–171.PubMedGoogle Scholar
  103. Rawlings, N.D., and Barrett, A.J., 1995, Evolutionary families of metallopeptidases. Methods Enzymol. 248 : 183–228.PubMedCrossRefGoogle Scholar
  104. Réaux, A., de Mota, N., Zini, S., Cadel, S., Fournié-Zaluski, M.C., Roques, B.P., Corvol., P., and Llorens-Cortes, C., 1999, PC 18, a specific aminopeptidase N inhibitor, induces vasopressin release by increasing the half-life of brain angiotensin III. Neuroendocrinology 69 : 370–376.PubMedCrossRefGoogle Scholar
  105. Rich, D.H., Moon, B.J., and Harbeson, S., 1984, Inhibition of aminopeptidases by amastatin and bestatin derivatives. Effect of inhibitor structure on slow-binding processes. J. Med. Chem. 27: 417–422.PubMedCrossRefGoogle Scholar
  106. Riemann, D., Kehlen, A., and Langner, J., 1999, CD 13 - not just a marker in leukemia typing. Immunol. Today 20 : 83–88.PubMedCrossRefGoogle Scholar
  107. Roques, B.P., Fournié-Zaluski, M.C., Soroca, E., Lecomte, J.M., Malfroy, B., Llorens, and Schwartz, J.C., 1980, The enkephalinase inhibitor thiorphan shows antinociceptive activity in mice. Nature 288 : 286–288.PubMedCrossRefGoogle Scholar
  108. Roques, B.P., Noble, F., Daugé, V., Fournié-Zaluski, M.C., and Beaumont, A., 1993, Neutral endopeptidase 24.11 Structure, inhibition, and experimental and clinical pharmacology. Pharmacol. Rev. 45 : 87–146.PubMedGoogle Scholar
  109. Roques, B.P., 2000, Novel approaches to targeting neuropeptide systems. Trends Pharmacol. Sci. 21 : 475–483.PubMedCrossRefGoogle Scholar
  110. Safavi, A., and Hersh, L.B., 1995, Degradation of dynorphin-related peptides by the puromycin-sensitive aminopeptidase and aminopeptidase M. J. Neurochem. 65 : 389–395.PubMedCrossRefGoogle Scholar
  111. Saiki, I., Fujii, H., Yoneda, J., Abe, F., Nakajima, M., Tsuruo, T., and Azuma, I., 1993, Role of aminopeptidase N (CD 13) in tumor-cell invasion and extracellular matrix degradation. Int. J. Cancer 54: 137–143.PubMedCrossRefGoogle Scholar
  112. Schalk, C, d’Orchymont, H., Jauch, M.-F., and Tarnus, C., 1994, 3-amino-2tetralone derivatives : Novel potent and selective inhibitors of aminopeptidase M (EC 3.4.11.2). Arch. Biochem. Biophys. 311 : 42–46.PubMedCrossRefGoogle Scholar
  113. Schechter, I., and Berger, A., 1967, On the size of the active site in proteases. I. Papain. Biochem. Biophys. Res. Commun. 27 : 157–162.CrossRefGoogle Scholar
  114. Schmidt, C., Peyroux, J., Fournié-Zaluski, M.C., and Roques, B.P., 1991, Analgesic responses elicited by endogenous enkephalins (protected by mixed peptidase inhibitors) in a variety of morphine-sensitive noxious tests. Eur. J. Pharmacol. 192 : 253–262.PubMedCrossRefGoogle Scholar
  115. Semenza, G., 1986, Anchoring and biosynthesis of stalked brush border membrane proteins : Glycosidases and peptidases of enterocytes and renal tubuli. Annu. Rev. Cell Biol. 2 :255–313.PubMedCrossRefGoogle Scholar
  116. Shenvi, A.B., 1986, a-aminoboronic acid derivatives: Effective inhibitors of aminopeptidases. Biochemistry 25 : 1286–1291.PubMedCrossRefGoogle Scholar
  117. Shimamura, M., Hazato, T., and Iwaguchi, T., 1991, Enkephalin-degrading aminopeptidase in the longitudinal muscle layer of guinea pig small intestine : Its properties and action on neuropeptides. J. Biochem. 109 : 492–497.PubMedGoogle Scholar
  118. Shimazawa, R., Takayama, H., Fujimoto, Y., Komoda, M., Dodo, K., Yamasaki, R., Shirai, R., Koiso, Y., Miyata, K., Kato, F., Kato, M., Miyachi, H., and Hashimoto, Y., 1999, Novel small molecule nonpeptide aminopeptidase N inhibitors with a cyclic imide skeleton. J. Enzyme Inhibition 14 : 259–275.CrossRefGoogle Scholar
  119. Sidorowicz, W., Jackson, G.C., and Behal, E.J., 1980, Multiple molecular forms of human pancreas alanine aminopeptidase. Clin. Chim. Acta 104 : 169–179.PubMedCrossRefGoogle Scholar
  120. Soleilhac, J.M., Lucas, E., Beaumont, A., Turcaud, S., Michel, J.B., Ficheux, D., Fournié-Zaluski,M.C., and Roques, B.P., 1992, A 94-kDa protein, identified as neutral endopeptidase 24.11, can inactivate atrial natriuretic peptide in the vascular endothelium. Mol. Pharmacol. 41 : 609–614.PubMedGoogle Scholar
  121. Solhonne, B., Gros, C., Pollard, H., and Schwartz, J.-C., 1987, Major localization of aminopeptidase M in rat brain microvessels. Neuroscience 22 : 225–232.PubMedCrossRefGoogle Scholar
  122. Thunnissen, M.M.G.M., Nordlund, P., and Haeggström, J.Z., 2001, Crystal structure of human leukotriene A4 hydrolase, a bifunctional enzyme in inflammation. Nature Struct. Biol. 8: 131–135.PubMedCrossRefGoogle Scholar
  123. Tresnan, D.B., Levis, R., and Holmes, K.V., 1996, Feline aminopeptidase N serves as a receptor for feline, canine, porcine, and human coronaviruses in serogroup I. J. Virol. 70 : 8669–8674.PubMedGoogle Scholar
  124. Umezawa, H., Aoyagi, T., Suda, H., Hamada, M., and Takeuchi, T., 1976, Bestatin, an inhibitor of aminopeptidase B, produced by actinomycetes. J. Antibiot. 29 : 97–103.PubMedCrossRefGoogle Scholar
  125. Umezawa, H., Aoyagi, T., Tanaka, T., Suda, H., Okuyama, A., Naganawa, H., Hamada, M., and Takeuchi, T., 1985, Production of actinonin, an inhibitor of aminopeptidase M, by actinomycetes. J. Antibiot. 38 : 1629–1630.PubMedCrossRefGoogle Scholar
  126. Vazeux, G., Iturrioz, X., Corvol, P., and Llorens-Cortes, C., 1997, A tyrosine residue essential for catalytic activity in aminopeptidase A. Biochem. J. 327 : 883–889.PubMedGoogle Scholar
  127. Vazeux, G., Iturrioz, X., Corvol, P., and Llorens-Cortes, C., 1998, A glutamate residue contributes to the exopeptidase specificity in aminopeptidase A. Biochem. J. 334 : 407–413.PubMedGoogle Scholar
  128. Vogel, Z., and Altstein, M., 1977, The absorption of enkephalins to porous polystyrene beads : A simple assay for enkephalin hydrolysis. FEBS Lett. 80 : 332–335.PubMedCrossRefGoogle Scholar
  129. Wachsmuth, E.D., Fritze, I., and Pfleiderer, G., 1966, An aminopeptidase occurring in pig kidney. I. An improved method of preparation. Physical and enzymic properties. Biochemistry 5, 169–174.PubMedCrossRefGoogle Scholar
  130. Waksman, G., Bouboutou, R., Devin, J., Bourgoin, S., Cesselin, F., Hamon, M., Fournié-Zaluski, M.C., and Roques B.P., 1985, In vitro and in vivo effects of kelatorphan on enkephalin metabolism in rodent brain. Eur. J. Pharmacol. 117: 233–243.PubMedCrossRefGoogle Scholar
  131. Watt, V.M., and Yip, C.C., 1989, Amino acid sequence deduced from a rat kidney cDNA suggests it encodes the Zn-peptidase aminopeptidase N. J. Biol. Chem. 264 : 5480–5487.PubMedGoogle Scholar
  132. Weiss, B., Hui, K.-S., Hui, M, and Lajtha, A., 1988, Aminothiols : Synthesis and effect on chicken brain aminopeptidases. Res. Commun. Chem. Pathol. Pharmacol. 62 : 113–123.Google Scholar
  133. Wilkes, S.H., and Prescott, J.M., 1983, Stereospecificity of amino acid hydroxamate inhibition of aminopeptidases. J. Biol. Chem. 258 : 13517–13521.PubMedGoogle Scholar
  134. Wilkes, S.H., and Prescott, J.M., 1985, The slow, tight binding of bestatin and amastatin to aminopeptidases. J. Biol. Chem. 260 : 13154–13162.PubMedGoogle Scholar
  135. Xie, J., Soleilhac, J.M., Schmidt, C., Peyroux, J., Roques, B.P., and Fournié-Zaluski, M.C., 1989a, New kelatorphan-related inhibitors of enkephalin metabolism: Improved antinociceptive properties. J. Med. Chem. 32 : 1497–1503.PubMedCrossRefGoogle Scholar
  136. Xie, J., Soleilhac, J.M., Renwart, N., Peyroux, J., Roques, B.P., and Fournié-Zaluski, M.C., 1989b, Inhibitors of the enkephalin degrading enzymes. Int. J. Pept. Prot. Res. 34, 246–255.CrossRefGoogle Scholar
  137. Yamamoto, Y., Kanazawa, H., Shimamura, M., Ueki, M., and Hazato, T., 1998, Inhibitory action of spinorphin, an endogenous regulator of enkephalin-degrading enzymes, on carrageenan-induced polymorphonuclear neutrophil accumulation in mouse air-pouches. LifeSci. 62: 1767–1773.CrossRefGoogle Scholar
  138. Yang, X.-F., Milhiet, P.E., Gaudoux, F., Crine, P., andBoileau, G., 1993, Complete sequence of rabbit kidney aminopeptidase N and mRNA localization in rabbit kidney by in situ hybridization. Biochem. Cell Biol. 71 : 278–287.PubMedCrossRefGoogle Scholar
  139. Yaoi, K., Nakanishi, K., Kadotani, T., hnamura, M., Koizumi, N., Iwahana, H., and Sato, R., 1999, cDNA cloning and expression of Bacillus thuringiensis CrylAa toxin binding 120 kDa aminopeptidase N from Bombyx mori. Biochim. Biophys. Acta 1444 : 131–137.PubMedCrossRefGoogle Scholar
  140. Yeager, C.L., Ashmun, R.A., Williams, R.K., Cardellichio, C.B., Shapiro, L.H., Look, A.T., and Holmes, K.V., 1992, Human aminopeptidase N is a receptor for human coronavirus 229E. Nature 357 : 420–422.PubMedCrossRefGoogle Scholar
  141. Zajac, J.M., Charnay, Y., Soleilhac, J.M., Sales, N., and Roques, B.P., 1987, Enkephalin-degrading enzymes and angiotensin-converting enzyme in human and rat meninges. FEBS Lett. 216:118–122.PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media New York 2002

Authors and Affiliations

  • Marie-Claude Fournié-Zaluski
    • 1
  • Bernard P. Roques
    • 2
  1. 1.Département de Pharmacochimie Moléculaire et Structurale INSERM U266, CNRS UMR 8600UFR des Sciences Pharmaceutiques et biologiquesParis Cedex 06France
  2. 2.PHARMALEADSParis Cedex 06France

Personalised recommendations