Structure-Activity Study on the Phe Side Chain Arrangement of Endomorphins Using Conformationally Constrained Analogues

Journal of Medicinal Chemistry

Volumn 47, Issue 3, 2004, Pages 735-743

  Tömböly, Csaba ^a   Kövér, Katalin E ^b   Péter, Antal ^c   Tourwé, Dirk ^d   Biyashev, Dauren ^a   Benyhe, Sándor ^a   Borsodi, Anna ^a   Al Khrasani, Mahmoud ^e   Rónai, András Z ^e   Tóth, Géza ^a  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b UNIVERSITY OF DEBRECEN   (Hungary)

^c UNIVERSITY OF SZEGED   (Hungary)

^d VRIJE UNIVERSITEIT BRUSSEL   (Belgium)

^e SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

[No Author keywords available]

Indexed keywords

AROMATIC COMPOUND; ENDOMORPHIN 1; ENDOMORPHIN 2; GUANOSINE 5' O (3 THIOTRIPHOSPHATE); MU OPIATE RECEPTOR; PHENYLALANINE;

ANIMAL TISSUE; ARTICLE; CARBOXY TERMINAL SEQUENCE; DRUG ACTIVITY; DRUG CONFORMATION; DRUG DETERMINATION; DRUG RECEPTOR BINDING; DRUG STABILITY; NONHUMAN; NUCLEAR MAGNETIC RESONANCE; RAT; STRUCTURE ACTIVITY RELATION; STRUCTURE ANALYSIS;

ANIMALS; BRAIN; MAGNETIC RESONANCE SPECTROSCOPY; MOLECULAR CONFORMATION; OLIGOPEPTIDES; RADIOLIGAND ASSAY; RATS; RATS, WISTAR; RECEPTORS, OPIOID, MU; STEREOISOMERISM; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 9144253110     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm0310028     Document Type: Article

References (63)

1. Zadina, J. E.; Hackler, L.; Ge, L. J.; Kastin, A. J. A potent and selective endogenous agonist for the mu-opiate receptor. Nature 1997, 386, 499-502.
2. Martin-Schild, S.; Zadina, J. E.; Gerall, A. A.; Vigh, S.; Kastin, A. J. Localization of endomorphin-2-like immunoreactivity in the rat medulla and spinal cord. Peptides 1997, 18, 1641-1649.
3. Gong, J.; Strong, J. A.; Zhang, S.; Yue, X.; DeHaven, R. N.; Daubert, J. D.; Cassel, J. A.; Yu, G.; Mansson, E.; Yu, L. Endomorphins fully activate a cloned human mu opioid receptor. FEBS. Lett. 1998, 439, 152-156.
4. Harrison, C.; McNulty, S.; Smart, D.; Rowbotham, D. J.; Grandy, D. K.; Devi, L. A.; Lambert, D. G. The effects of endomorphin-1 and endomorphin-2 in CHO cells expressing recombinant mu-opioid receptors and SH-SY5Y cells. Br. J. Pharmacol. 1999, 128, 472-478.
5. McConalogue, K.; Grady, E. F.; Minnis, J.; Balestra, B.; Tonini, M.; Brecha, N. C.; Bunnett, N. W.; Sternini, C. Activation and internalization of the mu-opioid receptor by the newly discovered endogenous agonists, endomorphin-1 and endomorphin-2. Neuroscience 1999, 90, 1051-1059.
6. Horváth, Gy. Endomorphin-1 and endomorphin-2: pharmacology of the selective endogenous mu-opioid receptor agonists. Pharmacol. Ther. 2000, 88, 437-463.
7. Goldberg, I. E.; Rossi, G. C.; Letchworth, S. R.; Mathis, J. P.; Ryan-Moro, J.; Leventhal, L.; Su, W.; Emmel, D.; Bolan, E. A.; Pasternak, G. W. Pharmacological characterization of endomorphin-1 and endomorphin-2 in mouse brain. J. Pharmacol. Exp. Ther. 1998, 286, 1007-1013.
8. Przewlocka, B.; Mika, J.; Labuz, D.; Tóth, G.; Przewlocki, R. Spinal analgesic action of endomorphins in acute, inflammatory and neuropathic pain in rats. Eur. J. Pharmacol. 1999, 367, 189-196.
9. Spetea, M.; Monory, K.; Tömböly, Cs.; Tóth, G.; Tzavara, E.; Benyhe, S.; Hanoune, J.; Borsodi, A. In vitro binding and signaling profile of the novel mu opioid receptor agonist endomorphin-2 in rat brain membranes. Biochem. Biophys. Res. Commun. 1998, 250, 720-725.
10. Monory, K.; Bourin, M. C.; Spetea, M.; Tömböly, Cs.; Tóth, G.; Matthes, H. W.; Kieffer, B. L.; Hanoune, J.; Borsodi, A. Specific activation of the mu opioid receptor (MOR) by endomorphin-1 and endomorphin-2. Eur. J. Neurosci. 2000, 12, 577-584.
11. (ll) Rónai, A. Z.; Timár, J.; Makó, É.; Erdo, F.; Gyarmati, Z.; Tóth, G.; Orosz, Gy.; Fürst, S.; Székely, J. I. Diprotin A, an inhibitor of dipeptidyl aminopeptidase IV (EC 3.4.14.5) produces naloxone-reversible analgesia in rats. Life Sci. 1999, 64, 145-152.
12. Grathwohl, C.; Wüthrich, K. NMR-Studies of the rates of proline cis-trans isomerization in oligopeptides. Biopolymers 1981, 20, 2623-2633.
13. Podlogar, B. L.; Paterlini, M. G.; Ferguson, D. M.; Leo, G. C.; Demeter, D. A.; Brown, F. K.; Reitz, A. B. Conformational analysis of the endogenous mu-opioid agonist endomorphin-1 using NMR spectroscopy and molecular modeling. FEBS Lett. 1998, 439, 13-20.
14. Fiori, S.; Renner, C.; Cramer, J.; Pegoraro, S.; Moroder, L. Preferred conformation of endomorphin-1 in aqueous and membrane-mimetic environments. J. Mol. Biol. 1999, 291, 163-175.
15. Paterlini, M. G.; Avitabile, F.; Ostrowski, B. G.; Ferguson, D. M.; Portoghese, P. S. Stereochemical requirements for receptor recognition of the mu-opioid peptide endomorphin-1. Biophys. J. 2000, 78, 590-599.
16. 1H NMR spectroscopy and molecular modeling calculation. J. Pept. Res. 2001, 58, 399-412.
17. Lengyel, I.; Orosz, Gy.; Biyashev, D.; Kocsis, L.; Al Khrasani, M.; Rónai, A. Z.; Tömböly, Cs.; Fürst, Z.; Tóth, G.; Borsodi, A. Side chain modifications change the binding and agonist properties of endomorphin-2. Biochem. Biophys. Res. Commun. 2002, 290, 153-161.
18. Péter, A.; Tóth, G.; Tömböly, Cs.; Laus, G.; Tourwé, D. Liquid chromatographic study of the enzymatic degradation of endomorphins, with identification by electrospray ionization mass spectrometry. J. Chromatogr. A. 1999, 846, 39-48.
19. Eguchi, M.; Shen, R. Y.; Shea, J. P.; Lee, M. S.; Kahn, M. Design, synthesis, and evaluation of opioid analogues with nonpeptidic β-turn scaffold: enkephalin and endomorphin mimetics. J. Med. Chem. 2002, 45, 1395-1398.
20. Keller, M.; Boissard, C.; Patiny, L.; Chung, N. N.; Lemieux, C.; Mutter, M.; Schiller, P. W. Pseudoproline-containing analogues of morphiceptin and endomorphin-2: evidence for a cis Tyr-Pro amide bond in the bioactive conformation. J. Med. Chem. 2001, 44, 3896-3903.
21. 2): a potent and specific agonist for morphine (mu) receptors. Science 1981, 212, 75-77.
22. Chang, K. J.; Wei, E. T.; Killian, A.; Chang, J. K. Potent morphiceptin analogues: structure activity relationships and morphine-like activities. J. Pharmacol. Exp. Ther. 1983, 227, 403-408.
23. Érchegyi, J.; Kastin, A. J.; Zadina, J. E. Isolation of a novel tetrapeptide with opiate and antiopiate activity from human brain cortex: Tyr-Pro-Trp-Gly-NH2 (Tyr-W-MIF-1). Peptides 1992, 13, 623-631.
24. Hackler, L.; Kastin, A. J.; Érchegyi, J.; Zadina, J. E. Isolation of Tyr-W-MIF-1 from bovine hypothalami. Neuropeptides 1993, 24, 159-164.
25. 2, and examination of their opioid receptor binding activities and solution conformation. Biochem. Biophys. Res. Commun. 2000, 276, 7-11.
26. Cardillo, G.; Gentilucci, L.; Melchiorre, P.; Spampinato, S. Synthesis and binding activity of endomorphin-1 analogues containing beta-amino acids. Bioorg. Med. Chem. Lett. 2000, 10, 2755-2758.
27. Cardillo, G.; Gentilucci, L.; Qasem, A. R.; Sgarzi, F.; Spampinato, S. Endomorphin-1 analogues containing beta-proline are mu-opioid receptor agonists and display enhanced enzymatic hydrolysis resistance. J. Med. Chem. 2002, 45, 2571-2578.
28. Yamazaki, T.; Ro, S.; Goodman, M.; Chung, N. N.; Schiller, P. W. A topochemical approach to explain morphiceptin bioactivity. J. Med. Chem. 1993, 36, 708-719.
29. Szatmári, I.; Biyashev, D.; Tömböly, Cs.; Tóth, G.; Mácsai, M.; Szabó, Gy.; Borsodi, A.; Lengyel, I. Influence of degradation on binding properties and biological activity of endomorphin-1. Biochem. Biophys. Res. Commun. 2001, 284, 771-776.
30. Hruby, V. J.; Al-Obeidi, F.; Kazmierski, W. Emerging approaches in the molecular design of receptor-selective peptide ligands: conformational, topographical and dynamic considerations. Biochem. J. 1990, 268, 249-262.
31. 5]enkephalin. J. Med. Chem. 1991, 34, 1823-1830.
32. Hruby, V. J.; Li, G.; Haskell-Luevano, C.; Shenderovich, M. Design of peptides, proteins, and peptidomimetics in chi space. Biopolymers 1997, 43, 219-266.
33. Tóth, G.; Lebl, M.; Hruby, V. J. Chiral TLC separation of modified phenylalanine and tyrosine derivatives. J. Chromatogr. 1990, 504, 450-455.
34. Tömböly, Cs.; Dixit, R.; Lengyel, I.; Borsodi, A.; Tóth, G. Preparation of specifically tritiated endomorphins. J. Labelled Compds. Radiopharm. 2001, 44, 355-363.
35. Tömböly, Cs.; Péter, A.; Tóth, G. In vitro quantitative study of the degradation of endomorphins. Peptides 2002, 23, 1573.
36. Goldstein, A.; Naidu, A. Multiple opioid receptors: ligand selectivity profiles and binding site signatures. Mol. Pharmacol. 1989, 36, 265-272.
37. Erspamer, G. F.; Severini, C. Guinea-pig ileum (GPI) and mouse vas deferens (MVD) preparations in the discovery, discrimination and parallel bioassay of opioid peptides. Pharmacol. Res. 1992, 26, 109-121.
38. Al-Khrasani, M.; Orosz, Gy.; Kocsis, L.; Farkas, V.; Magyar, A.; Lengyel, I.; Benyhe, S.; Borsodi, A.; Rónai, A. Z. Receptor constants for endomorphin-1 and endomorphin-1-ol indicate differences in efficacy and receptor occupancy. Eur. J. Pharmacol. 2001, 421, 61-67.
39. Wüthrich, K. NMR of proteins and nucleic acids; Wiley: New York, 1986.
40. Nardi, F.; Kemmink, J.; Sattler, M.; Wade, R. C. The cisproline-(i-1)-aromatic(i) interaction: Folding of the Ala-cis-Pro-Tyr peptide characterized by NMR and theoretical approaches. J. Biomol. NMR 2000, 17, 63-77.
41. Wu, W. J.; Raleigh, D. P. Local control of peptide conformation: Stabilization of cis proline peptide bonds by aromatic proline interactions. Biopolymers 1998, 45, 381-394.
42. n-Tyr-OH peptides. Biopolymers 1993, 33, 781-795.
43. Bystrov, V. F. Spin-spin coupling and the conformational states of peptide systems. Prog. NMR Spectrosc. 1976, 10, 41-81.
44. β bond in peptides. Biopolymers 1982, 21, 953-967.
45. Kessler, H.; Griesinger, C.; Wagner, K. Peptide conformations. 42. Conformation of side chains in peptides using heteronuclear coupling constants obtained by two-dimensional NMR spectroscopy. J. Am. Chem. Soc. 1987, 109, 6927-6933.
46. 3 replacements in the cyclic delta receptor selective tetrapeptide Tyr-c[D-Cys-Phe-D-Pen]-OH (JOM-13). J. Med. Chem. 1994, 37, 4384-4391.
47. Mosberg, H. I. Complementarity of delta opioid ligand pharmacophore and receptor models. Biopolymers 1999, 51, 426-439.
48. Przewlocki, R.; Labuz, D.; Mika, J.; Przewlocka, B.; Tömböly, Cs.; Tóth, G. Pain inhibition by endomorphins. Ann. N. Y. Acad. Sci. 1999, 897, 154-164.
49. 5.6deltorphin II. Neuropeptides 1994, 26, 261-265.
50. Bax, A.; Davis, D. G. MLEV-17-Based two-dimensional homonuclear magnetization transfer spectroscopy. J. Magn. Res. 2003, 65, 355-360.
51. Kövér, K. E.; Uhrin, D.; Hruby, V. J. Gradient- and sensitivity-enhanced TOCSY experiments. J. Magn. Res. 1998, 130, 162-168.
52. Bothner-By, A. A.; Stephens, R. L.; Lee, J. M. Structure determination of a tetrasaccharide: transient nuclear Overhauser effects in the rotating frame. J. Am. Chem. Soc. 1984, 106, 811-813.
53. Bax, A.; Davis, D. G. Practical aspects of two-dimensional transverse NOE spectroscopy. J. Magn. Res. 1985, 63, 207-213.
54. Palmer III, A. G.; Cavanagh, J.; Wright, P. E.; Rance, M. Sensitivity improvement in proton-detected two-dimensional heteronuclear correlation NMR spectroscopy. J. Magn. Res. 1991, 93, 151-170.
55. 1) half- filtered TOCSY experiment for measuring long-range coupling constants. J. Magn. Res. 1998, 130, 155-161.
56. Kozminski, W.; Nanz, D. HECADE: HMQC- and HSQC-based 2D NMR experiments for accurate and sensitive determination of heteronuclear coupling constants from TOCSY-type crosspeaks. J. Magn. Res. 1997, 124, 383-392.
57. Kataoka, Y.; Seto, Y.; Yamamoto, M.; Yamada, T.; Kuwata, S.; Watanabe, H. Studies of unusual amino acids and their peptides. VI. The synthesis and the optical resolutions of β-methylphenylalanine and its dipeptide present in bottromycin. Bull. Chem. Soc. Jpn. 1976, 49, 1081-1084.
58. Simon, J.; Benyhe, S.; Abutidze, K.; Borsodi, A.; Szucs, M.; Tóth, G.; Wollemann, M. Kinetics and physical parameters of rat brain opioid receptors solubilized by digitonin and CHAPS. J. Neurochem. 1986, 46, 695-701.
59. Bradford, M. M. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal. Biochem. 1976, 72, 248-254.
60. 35S]thio)triphosphate binding to membranes from human neuroblastoma SH-SY5Y cells. Mol. Pharmacol. 1995, 47, 848-854.
61. Paton, W. D. M.; Vizi, E. S. The inhibitory action of noradrenaline and adrenaline on acetylcholine output by guinea-pig muscle strips. Br. J. Pharmacol. 1969, 35, 10-28.
62. Henderson, G.; Hughes, J.; Kosterlitz, H. W. A new example of a morphine-sensitive neuro-effector junction: adrenergic transmission in the mouse vas deferens. Br. J. Pharmacol. 1972, 46, 764-766.
63. Rónai, A. Z.; Gráf, L.; Székely, J. I.; Dunai-Kovács, Zs.; Bajusz, S. Differential behaviour of LPH-(61-91)-peptide in different model systems: comparison of the opioid activities of LPH-(61-91)-peptide and its fragments. FEBS Lett. 1977, 74, 182-184.