Effect of S 17092, a novel prolyl endopeptidase inhibitor, on substance P and α-melanocyte-stimulating hormone breakdown in the rat brain

Journal of Neurochemistry

Volumn 84, Issue 5, 2003, Pages 919-929

  Bellemère, Gaëlle ^a   Morain, Philippe ^b   Vaudry, Hubert ^a   Jégou, Sylvie ^a  

^a UNIVERSITÉ DE ROUEN   (France)

^b INSTITUT DE RECHERCHES INTERNATIONALES SERVIER   (France)

Author keywords

Catabolism; Central nervous system; Cognitive enhancer; Neuropeptides; Peptidase inhibitor

Indexed keywords

1 [(2 PHENYLCYCLOPROPYL)CARBONYL] 2 [(THIAZOLIDIN 3 YL)CARBONYL]OCTAHYDRO 1H INDOLE; ALPHA INTERMEDIN; BRAIN EXTRACT; NEUROPEPTIDE; PROLYL ENDOPEPTIDASE INHIBITOR; S 17092; SUBSTANCE P; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN; CENTRAL NERVOUS SYSTEM; COGNITION; CONTROLLED STUDY; DOSE RESPONSE; DRUG MECHANISM; ENZYME ACTIVITY; FRONTAL CORTEX; HORMONE METABOLISM; HYPOTHALAMUS; IMMUNOREACTIVITY; IN VITRO STUDY; IN VIVO STUDY; LONG TERM EXPOSURE; MALE; MEDULLA OBLONGATA; MEMORY DISORDER; NONHUMAN; PRIORITY JOURNAL; PROTEIN DEGRADATION; RAT;

ADMINISTRATION, ORAL; ALPHA-MSH; ANIMALS; BIOLOGICAL ASSAY; BRAIN; BRAIN CHEMISTRY; DOSE-RESPONSE RELATIONSHIP, DRUG; ENZYME ACTIVATION; FLAVOBACTERIUM; FRONTAL LOBE; HYPOTHALAMUS; INDOLES; MALE; MEDULLA OBLONGATA; PROTEASE INHIBITORS; RADIOIMMUNOASSAY; RATS; RATS, WISTAR; SERINE ENDOPEPTIDASES; SUBSTANCE P; THIAZOLES; THIAZOLIDINES;

ANIMALIA;

EID: 0037342917     PISSN: 00223042     EISSN: None     Source Type: Journal    
DOI: 10.1046/j.1471-4159.2003.01536.x     Document Type: Article

References (76)

1. Adan R. A., Oosterom J., Ludvigsdottir G., Brakkee J. H., Burbach J. P. and Gispen W. H. (1994) Identification of antagonists for melanocortin MC3, MC4 and MC5 receptors. Eur. J. Pharmacol 269, 331-337.
2. Ahmad S., Wang L. and Ward P. E. (1992) Dipeptidyl (amino) peptidase IV and aminopeptidase M metabolize circulating substance P in vivo. J. Pharmacol. Exp. Ther. 260, 1257-1261.
3. Akiyama K., Yamamura H. I., Wilkes B. C., Cody W. L., Hruby V. J., Castrucci A. M. and Hadley M. E. (1984) Relative stability of α-melanotropin and related analogues to rat brain homogenates. Peptides 5, 1191-1195.
4. Ang L. C. and Shul D. D. (1995) Peptidergic neurons of subcortical white matter in aging and Alzheimer's brain. Brain Res. 674, 329-335.
5. Arai H., Moroji T., Kosaka K. and Iizuka R. (1986) Extrahypophyseal distribution of α-melanocyte stimulating hormone (α-MSH)-like immunoreactivity in postmortem brains from normal subjects and Alzheimer-type dementia patients. Brain Res. 377, 305-10.
6. Barelli H., Petit A., Hirsch E., Wilk S., De Nanteuil G., Morain P. and Checler F. (1999) S 17092, a highly potent, specific and cell permeant inhibitor of human proline endopeptidase. Biochem. Biophys. Res. Commun. 257, 657-661.
7. Beal M. F. and Mazurek M. F. (1987) Substance P-like immunoreactivity is reduced in Alzheimer's disease cerebral cortex. Neurology 37, 1205-1209.
8. Boix F., Sandor P., Nogueira P. J., Huston J. P. and Schwarting R. K. W. (1995) Relationship between dopamine release in nucleus accumbens and place preference induced by substance P injected into the nucleus basalis magnocellularis region. Neuroscience 64, 1045-1055.
9. Bouras C., Vallet P. G., Hof P. R., Charnay Y., Golaz J. and Constantinidis J. (1990) Substance P immunoreactivity in Alzheimer disease: a study in cases presenting symmetric or asymmetric cortical atrophy. Alzheimer Dis. Assoc. Disord. 4, 24-34.
10. Castrucci A. M., Hadley M. E., Sawyer T. K. and Hruby V. J. (1984) Enzymological studies of melanotropins. Comp. Biochem. Physiol. 78B, 519-524.
11. Chappell M. C., Tallant E. A., Brosnthan K. B. and Ferrario C. M. (1990) Processing of angiotensin peptides by NG108-15 neuroblastoma x glioma hybrid cell line. Peptides 11, 375-380.
12. Checler F., Amar S., Kitabgi P. and Vincent J. P. (1986) Catabolism of neurotensin by neural (neuroblastoma clone N1E115) and extraneural (HT29) cell lines. Peptides 7, 1071-1077.
13. Clevens R. A. and Beal M. F. (1989) Substance P-like immunoreactivity in brains with pathological features of Parkinson's and Alzheimer's diseases. Brain Res. 486, 387-390.
14. Conlon J. M. (1991) Regionally Specific Antisera to Human B-Preprotachykinin, in Methods in Neurosciences, Vol. 6 (Conn P. M., ed.), pp. 207-231. Academic Press, San Diego.
15. Crystal H. A. and Davies P. (1982) Cortical substance P-like immuno-reactivity in cases of Alzheimer's disease and senile dementia of the Alzheimer type. J. Neurochem. 38, 1781-1784.
16. Dahms P. and Mentlein R. (1992) Purification of the main somatostatin-degrading proteases from rat and pig brains, their action on other neuropeptides, and their identification as endopeptidases 24.15 24.16. Eur. J. Biochem. 208, 145-154.
17. Daly D. J., Maskrey P. and Pennington R. J. T. (1985) Characterization of proline endopeptidase from skeletal muscle. Int. J. Biochem. 17, 521-524.
18. De Wied D. (1966) Inhibitory effect of ACTH and related peptides on extinction of conditioned avoidance behavior in rats. Proc. Soc. Exp. Biol. Medical 122, 28-32.
19. De Wied D. (1999) Behavioral pharmacology of neuropeptides related to melanocortins and the neurohypophyseal hormones. Eur. J. Pharmacol. 375, 1-11.
20. Dresdner K., Barker L. A., Orlowski M. and Wilk S. (1982) Subcellular distribution of prolyl endopeptidase and cation-sensitive neutral endopeptidase in rabbit brain. J. Neurochem. 38, 1151-1154.
21. Eberle A. N. (1988) The melanotropins: Chemistry, Physiology and Mechanism of Action. Karger, Basel.
22. Eskay R. L., Giraud P., Oliver C. and Brown-Stein M. J. (1979) Distribution of α-melanocyte-stimulating hormone in the rat brain: evidence that α-MSH-containing cells in the arcuate region send projections to extrahypothalamic areas. Brain Res. 178, 55-67.
23. Galimberti D., Baron P., Meda L., Prat E., Scarpini E., Delgado R., Catania A., Lipton J. M. and Scarlato G. (1999) α-MSH peptides inhibit production of nitric oxide and tumor necrosis factor-α by microglial cells activated with β-amyloid and interferon γ. Biochem. Biophys. Res. Commun. 263, 251-256.
24. Gerhardt P., Hasenöhrl R. U. and Huston J. P. (1992) Enhanced learning produced by injection of neurokinin substance P into the region of the nucleus basalis magnocellularis: mediation by the N-terminal sequence. Exp. Neurol. 118, 302-308.
25. Hasenöhrl R. U., Huston J. P. and Schuurman T. (1990) Neuropeptide substance P improves water maze performance in aged rats. Psychopharmacology 101, 23-26.
26. Hasenöhrl R. U., Frisch C., Nikolaus S. and Huston J. P. (1994) Chronic administration of neurokinin SP improves maze performance in aged Rattus norvegicus. Behav Neural. Biol. 62, 110-120.
27. Hasenöhrl R. U., De Souza-Silva M. A., Nikolaus S., Tomaz C., Brandao M. L., Schwarting R. K. W. and Huston J. P. (2000) Substance P and its role in neural mechanisms governing learning, anxiety and functional recovery. Neuropeptides 34, 272-280.
28. Husain M. M. and Nemeroff C. B. (1990) Neuropeptides and Alzheimer's disease. J. Am. Geriatr. Soc. 38, 918-925.
29. Huston J. P. and Hasenöhrl R. U. (1995) The role of neuropeptides in learning: focus on the neurokinin substance P. Behav. Brain. Res. 66, 117-127.
30. Huston J. P. and Oitzl M. S. (1989) The relationship between reinforcement and memory: parallels in the rewarding and mnemonic effects of the neuropeptide substance P. Neurosci. Biobehav. Rev. 13, 171-180.
31. Irazusta J., Larrinaga G., González-Maeso J., Gil J., Meana J. J. and Casis L. (2002) Distribution of prolyl endopeptidase activities in rat and human brain. Neurochem. Int. 40, 337-345.
32. Jacobowitz D. M. and O'Donohue T. L. (1978) α-Melanocyte-stimulating hormone: immunohistochemical identification and mapping in neurons of rat brain. Proc. Natl. Acad. Sci. USA 75, 6300-6304.
33. Jégou S., Tonon M. C., Lcroux P., Leboulenger F., Delarue C., Pelletier G., Dupont A. and Vaudry H. (1981) Effect of hypophysectomy and pituitary stalk transection on α-melanocyte-stimulating hormone-like immunoreactivity in the brain of the frog, Rana ridibunda Pallas. Brain Res. 220, 287-298.
34. Kalwant S. and Porter A. G. (1991) Purification and characterization of human brain prolyl endopeptidase. Biochem. J. 276, 237-244.
35. Kato A., Fukunari A., Sakai Y. and Nakajima T. (1997) Prevention of amyloid-like deposition by a selective prolyl endopeptidase inhibitor, Y-29794, in senescence-accelerated mouse. J. Pharmacol. Exp. Ther. 283, 328-335.
36. Kato T., Okada M. and Nagatsu T. (1980) Distribution of post-proline cleaving enzyme in human brain and the peripheral tissues. Mol. Cell. Biochem. 32, 117-121.
37. Koida M. and Walter R. (1976) Post-proline cleaving enzyme. Purification of this endopeptidase by affinity chromatography. J. Biol. Chem. 251, 7593-7599.
38. Kouznetsova M. and Nistri A. (2000) Facilitation of cholinergic transmission by substance P methyl ester in the mouse hippocampal slice preparation. Eur. J. Neurosci. 12, 585-594.
39. Kovács G. L. and De Wied D. (1994) Peptidergic modulation of learning and memory processes. Pharmacol. Rev. 46, 269-291.
40. Kowall N. W., Beal M. F., Busciglio J., Duffy L. K. and Yankner B. A. (1991) An in vivo model for the neurodegenerative effects of β amyloid and protection by substance P. Proc. Natl. Acad. Sci. USA 88, 7247-7251.
41. Kowall N. W., Quigley B. J., Krause J. E., Lu F., Kosofsky B. E. and Ferrante R. J. (1993) Substance P and substance P receptor histochemistry in human neurodegenerative diseases. Regul. Pept. 46, 174-185.
42. Krall W. J., Sramek J. J. and Cutler N. R. (1999) Cholinesterase inhibitors: a therapeutic strategy for Alzheimer disease. Ann. Pharmacother. 33, 441-450.
43. Lamour Y., Senut M. C., Dutar P. and Bassant M. H. (1988) Neuropeptides and septo-hippocampal neurons: electrophysiological effects and distributions of immunoreactivity. Peptides 9, 1351-1359.
44. Lestage P., Lebrun C., Iop F., Hugot A., Rogez N., Grève P., Favale D., Gandon M. H., Raimbault O. and Lépagnol J. (1998) S 17092, a New Post-Proline Cleaving Enzyme Inhibitor: Memory Enhancing Effects and Substance P Neuromodulatoty Activity, in Advances in Behavioral Biology, Vol. 49: Progress in Alzheimer's and Parkinson's Diseases (Fischer A., Hanin I. and Yoshida M., eds), pp. 653-660. Plenum Press, New York.
45. Lino-de-Oliveira C., Sales A. J., Del Bel E. A., Silveira M. C. and Guimarães F. S. (2001) Effects of acute and chronic fluoxetine treatments on restraint stress-induced Fos expression. Brain Res. Bull. 55, 747-754.
46. Marighetto A., Touzani K., Etchamendy N., Cortes Torrea. C., De Nanteuil G., Guez D., Jaffard R. and Morain P. (2000) Further evidence for a dissociation between different forms of mnemonic expressions in a mouse model of age-related cognitive decline: effects of tacrine and S 17092, a novel prolyl endopeptidase inhibitor. Learn Mem. 7, 159-169.
47. Marks N., Stern F. and Kastin A. J. (1976) Biodegradation of α-MSH and derived peptides by rat brain extracts, and by rat and human serum. Brain Res. Bull. 1, 591-593.
48. Matsas R., Rattray M., Kenny A. J. and Turner A. J. (1985) The metabolism of neuropeptides. Endopeptidase-24.11 in human synaptic membrane preparations hydrolyses substance P. Biochem. J. 228, 487-492.
49. Mentlein R., von Kolszynski M., Sprang R. and Lucius R. (1990) Proline-specific proteases in cultivated neuronal and glial cells. Brain Res. 527, 159-162.
50. Mongeau R., Blier P. and de Montigny C. (1997) The serotonergic and noradrenergic systems of the hippocampus: their interactions and the effects of antidepressant treatments. Brain Res. Rev. 23, 145-195.
51. Nibuya M., Nestler E. J. and Duman R. S. (1996) Chronic antidepressant administration increases the expression of cAMP response element binding protein (CREB) in rat hippocampus. J. Neurosci. 16, 2365-2372.
52. O'Leary R. M. and O'Connor B. (1995) Identification and localisation of a synaptosomal membrane prolyl endopeptidase from bovine brain. Eur. J. Biochem. 227, 277-283.
53. O'Leary R. M., Gallagher S. P. and O'Connor B. (1996) Purification and characterization of a novel membrane-bound form of prolyl endopeptidase from bovine brain. Int. J. Biochem. Cell Biol. 28, 441-449.
54. Petit A., Barelli H., Morain P. and Checler F. (2000) Novel proline endopeptidase inhibitors do not modify Aβ 40/42 formation and degradation by human cells expressing wild-type and swedish mutated β-amyloid precursor protein. Br. J. Pharmacol. 130, 1613-1617.
55. Pitsikas N., Spruijt B. M., Josephy M., Algeri S. and Gispen W. H. (1991) Effect of Org2766, an ACTH (4-9) analogue, on recovery after bilateral transection of the fimbria fornix in the rat. Pharmacol. Biochem. Behav. 38, 931-934.
56. Portevin B., Benoist A., Remond G., Hervé Y., Vincent M., Lépagnol J. and De Nanteuil G. (1996) New prolyl endopeptidase inhibitors: in vitro and in vivo activities of azabicyclo[2.2.2] octane, azabicyclo[2.2.1]heptane, and perhydroindole derivatives. J. Med. Chem. 39, 2379-2391.
57. Potaman V. N., Alfeeva L. Y., Kamensky A. A. and Nezavibatko V. N. (1993) Degradation of ACTH/MSH (4-10) and its synthetic analog semax by rat serum enzymes: an inhibitor study. Peptides 14, 491-495.
58. Rainero I., May C., Kaye J. A., Friedland R. P. and Rapoport S. I. (1988) CSF a-MSH in dementia of the Alzheimer type. Neurology 38, 1281-1284.
59. Rossor M. N., Emson P. C., Dawbarn D., Mountjoy C. Q. and Roth M. (1986) Neuropeptides and dementia. Prog. Brain Res. 66, 143-159.
60. Sakurada C., Watanabe C., Sakurada S., Tan-No K. and Sakurada T. (1999) Major metabolites of substance P degraded by spinal synaptic membranes antagonize the behavioral response to substance P in rats. J. Pharm. Sci. 88, 1127-1132.
61. Schiöth H. B., Mutulis F., Muceniece R., Prusis P. and Wikberg J. E. (1998) Selective properties of C- and N-terminals and core residues of the melanocyte-stimulating hormone on binding to the human melanocortin receptor subtypes. Eur. J. Pharmacol. 349, 359-366.
62. Schneider J. S., Giardiniere M. and Morain P. (2002) Effects of the prolyl endopeptidase inhibitor S 17092 on cognitive deficits in chronic low dose MPTP-treated monkeys. Neuropsychopharmacology 26, 176-182.
63. Shinoda M., Toide K., Ohsawa I. and Kohsaka S. (1997) Specific inhibitor for prolyl endopeptidase suppresses the generation of amyloid β protein in NG108-15 cells. Biochem. Biophys. Res. Commun. 235, 641-645.
64. Sudo J. and Tanabe T. (1985) Distributions of post-proline cleaving enzyme-, converting enzyme-, trypsin- and chymotrypsin-like activities in various nephron segments and in brush-border membranes isolated from rat kidney. Chem. Pharm. Bull. (Tokyo) 33, 1694-1702.
65. Svenningsson P., Tzavara E. T., Witkin J. M., Fienberg A. A., Nomikos G. G. and Greengard P. (2002) Involvement of striatal and extrastriatal DARPP-32 in biochemical and behavioral effects of fluoxetine (Prozac). Proc. Natl. Acad. Sci. USA 99, 3182-3187.
66. Taylor W. L. and Dixon J. E. (1980) Catabolism of neuropeptides by a brain proline endopeptidase. Biochem. Biophys. Res. Commun. 94, 9-15.
67. Toide K., Shinoda M., Iwamoto Y., Fujiwara T., Okamiya K. and Uemura A. (1997) A novel prolyl endopeptidase inhibitor, JTP-4819, with potential for treating Alzheimer's disease. Behav. Brain Res. 83, 147-151.
68. Toide K., Shinoda M. and Miyazaki A. (1998) A novel prolyl endopeptidase inhibitor, JTP-4819. Its behavioral and neurochemical properties for the treatment of Alzheimer's disease. Rev. Neurosci. 9, 17-29.
69. Vaudry H., Tonon M. C., Delarue C., Vaillant R. and Kraicer J. (1978) Biological and radioimmunological evidence for melanocyte stimulating hormones (MSH) of extrapituitary origin in the rat brain. Neuroendocrinology 27, 9-24.
70. Walter R., Shlank H., Glass J. D., Schwartz I. L. and Kerenyi T. D. (1971) Leucylglycinamide released from oxytocin by human uterine enzyme. Science 173, 827-829.
71. Wilk S. (1983) Prolyl endopeptidase. Life Sci. 33, 2149-2157.
72. Yamakawa N., Soeda S., Shuneno H. and Nagamatsu A. (1986) Purification and characterization of proline endopeptidase from rat liver. Chem. Pharm. Bull. (Tokyo) 34, 256-263.
73. Yankner B. A., Duffy L. K. and Kirschner D. A. (1990) Neurotrophic and neurotoxic effects of amyloid β protein: reversal by tachykinin neuropeptides. Science 250, 279-282.
74. Yew D. T., Li W. P., Webb S. E., Lai H. W. and Zhang L. (1999) Neurotransmitters, peptides, and neural cell adhesion molecules in the cortices of normal elderly humans and Alzheimer patients: a comparison. Exp. Gerontol. 34, 117-133.
75. Yoshimoto T., Kado K., Matsubara F., Koriyama N., Kaneto H. and Tsuru D. (1987) Specific inhibitors for prolyl endopeptidase and their anti-amnesic effect. J. Pharmacobiodyn. 10, 730-735.
76. Yoshimoto T., Oyama H., Koriyama N. and Tsuru D. (1988) Prolyl endopeptidase from bovine testis: purification, characterization and comparison with the enzymes from other tissues. Chem. Pharm. Bull. (Tokyo) 36, 1456-1462.