The micelle-associated 3D structures of Boc-Y(SO3)-Nle-G-W-Nle- D-2-phenylethylester (JMV-180) and CCK-8(s) share conformational elements of a calculated CCK1 receptor-bound model

Journal of Medicinal Chemistry

Volumn 51, Issue 13, 2008, Pages 3742-3754

  Kumar, Mohanraja ^a,b   Reeve Jr , Joseph R ^a,b,e   Hu, Weidong ^c   Miller, Laurence J ^d   Keire, David A ^a,b  

^a VA GREATER LOS ANGELES HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c CITY OF HOPE NATIONAL MEDICAL CENTER   (United States)

^d MAYO GRADUATE SCHOOL   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHOLECYSTOKININ A RECEPTOR; CHOLECYSTOKININ OCTAPEPTIDE; DODECYLPHOSPHORYLCHOLINE; N TERT BUTYLOXYCARBONYLCHOLECYSTOKININ[27-32][28,31 NORLEUCINE] PHENETHYL ESTER;

AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CIRCULAR DICHROISM; DRUG CONFORMATION; DRUG RECEPTOR BINDING; DRUG STRUCTURE; FLUORESCENCE SPECTROSCOPY; MICELLE; PH; PROTON NUCLEAR MAGNETIC RESONANCE; STRUCTURE ANALYSIS; THREE DIMENSIONAL IMAGING;

CIRCULAR DICHROISM; IMAGING, THREE-DIMENSIONAL; MAGNETIC RESONANCE SPECTROSCOPY; MICELLES; MODELS, MOLECULAR; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTOR, CHOLECYSTOKININ A; SINCALIDE; SPECTROMETRY, FLUORESCENCE;

EID: 46849113424     PISSN: 00222623     EISSN: None     Source Type: Journal    
DOI: 10.1021/jm701401j     Document Type: Article

References (81)

1. Reeve, J., Jr.; Eysselein, V. E.; Ho, F. J.; Chew, P.; Vigna, S. R.; Liddle, R. A.; Evans, C. Natural and synthetic CCK-58. Novel reagents for studying cholecystokinin physiology. Ann. N.Y. Acad. Sci. 1994, 713, 11-21.
2. Matozaki, T.; Martinez, J.; Williams, J. A. A new CCK analogue differentiates two functionally distinct CCK receptors in rat and mouse pancreatic acini. Am. J. Physiol. 1989, 257 (4 Pt 1), 594-600.
3. Sato, S.; Stark, H. A.; Martinez, J.; Beaven, M. A.; Jensen, R. T.; Gardner, J. D. Receptor occupation, calcium mobilization, and amylase release in pancreatic acini: effect of CCK-JMV-180. Am. J. Physiol. 1989, 257 (2 Pt 1), G202-G209.
4. Stark, H. A.; Sharp, C. M.; Sutliff, V. E.; Martinez, J.; Jensen, R. T.; Gardner, J. D. CCK-JMV-180: a peptide that distinguishes high-affinity cholecystokinin receptors from low-affinity cholecystokinin receptors. Biochim. Biophys. Acta 1989, 1010 (2), 145-150.
5. Asin, K. E.; Bednarz, L. Differential effects of CCK-JMV-180 on food intake in rats and mice. Pharmacol. Biochem. Behav. 1992, 42 (2), 291-295.
6. Williams, J. A.; Blevins, G. T., Jr. Cholecystokinin and regulation of pancreatic acinar cell function. Physiol. Rev. 1993, 73 (4), 701-723.
7. Saluja, A. K.; Lerch, M. M.; Phillips, P. A.; Dudeja, V. Why Does Pancreatic Overstimulation Cause Pancreatitis? Annu. Rev. Physiol. 2006, 69, 249-269.
8. Dockray, G.; Dimaline, R.; Varro, A. Gastrin: old hormone, new functions. Pflugers Arch. 2005, 449 (4), 344-355.
9. Galas, M. C.; Lignon, M. F.; Rodriguez, M.; Mendre, C.; Fulcrand, P.; Laur, J.; Martinez, J. Structure-activity relationship studies on cholecystokinin: analogues with partial agonist activity. Am. J. Physiol. 1988, 254 (2 Pt 1), G176-G182.
10. Yule, D. I.; Tseng, M. J.; Williams, J. A.; Logdson, C. D. A cloned CCK-A receptor transduces multiple signals in response to full and partial agonists. Am. J. Physiol. 1993, 265 (5 Pt 1), G999-G1004.
11. Ji, B.; Kopin, A. S.; Logsdon, C. D. Species differences between rat and mouse CCKA receptors determine the divergent acinar cell response to the cholecystokinin analog JMV-180. J. Biol. Chem. 2000, 275 (25), 19115-19120.
12. Poosti, R.; di Malta, L.; Gagne, D.; Bernad, N.; Galleyrand, J. C.; Escrieut, C.; Silvente-Poirot, S.; Fourmy, D.; Martinez, J. The third intracellular loop of the rat and mouse cholecystokinin-A receptors is responsible for different patterns of gene activation. Mol. Pharmacol. 2000, 58 (6), 1381-1388.
13. Saluja, A. K.; Saluja, M.; Printz, H.; Zavertnik, A.; Sengupta, A.; Steer, M. L. Experimental pancreatitis is mediated by low-affinity cholecystokinin receptors that inhibit digestive enzyme secretion. Proc. Natl. Acad. Sci. U.S.A. 1989, 86 (22), 8968-8971.
14. 1H NMR spectroscopy, fluorescense-transfer measurements, and calculations. Biochemistry 1986, 25, 3778-3787.
15. Giragossian, C.; Mierke, D. F. Intermolecular interactions between cholecystokinin-8 and the third extracellular loop of the cholecystokinin A receptor. Biochemistry 2001, 40 (13), 3804-3809.
16. Pellegrini, M.; Mierke, D. F. Molecular complex of cholecystokinin-8 and N-terminus of the cholecystokinin A receptor by NMR spectroscopy. Biochemistry 1999, 38 (45), 14775-14783.
17. McDonnell, P. A.; Opella, S. J. Effect of detergent concentration on multidimensional solution NMR spectra of membrane proteins in micelles. J. Magn. Reson., Ser. B 1993, 102, 120-125.
18. Kallick, D. H.; Tessmer, M. R.; Watts, C. R.; Li, C. Y. The use of dodecylphosphocholine micelles in solution NMR. J. Magn. Reson., Ser. B 1995, 109, 60-65.
19. Keire, D. A.; Kumar, M.; Hu, W.; Sinnett-Smith, J.; Rozengurt, E. The lipid-associated 3D structure of SPA, a broad-spectrum neuropeptide antagonist with anticancer properties. Biophys. J. 2006, 91 (12), 4478-4489.
20. Keire, D. A.; Kobayashi, M. The orientation and dynamics of substance P in lipid environments. Protein Sci. 1998, 7 (11), 2438-2450.
21. Sargent, D. F.; Schwyzer, R. Membrane lipid phase as catalyst for peptide-receptor interactions. Proc. Natl. Acad. Sci. U.S.A. 1986, 83 (Aug), 5774-5778.
22. Schwyzer, R. Membrane-assisted molecular mechanism of neurokinin receptor subtype selection. EMBO J. 1987, 6 (8), 2255-2259.
23. Schwyzer, R. 100 years lock-and-key concept: Are peptides shaped and guided to their receptors by the target cell membrane. Biopolymers (Pept. Sci.) 1995, 37, 5-16.
24. Giragossian, C.; Mierke, D. F. Determination of ligand-receptor interactions of cholecystokinin by nuclear magnetic resonance. Life Sci. 2003, 73 (6), 705-713.
25. Shacham, S.; Marantz, Y.; Bar-Haim, S.; Kalid, O.; Warshaviak, D.; Avisar, N.; Inbal, B.; Heifetz, A.; Fichman, M.; Topf, M.; Naor, Z.; Noiman, S.; Becker, O. M. PREDICT modeling and in-silico screening for G-protein coupled receptors. Proteins 2004, 57 (1), 51-86.
26. Cherezov, V.; Rosenbaum, D. M.; Hanson, M. A.; Rasmussen, S. G.; Thian, F. S.; Kobilka, T. S.; Choi, H. J.; Kuhn, P.; Weis, W. I.; Kobilka, B. K.; Stevens, R. C. High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science 2007, 318 (5854), 1258-1265.
27. Rosenbaum, D. M.; Cherezov, V.; Hanson, M. A.; Rasmussen, S. G.; Thian, F. S.; Kobilka, T. S.; Choi, H. J.; Yao, X. J.; Weis, W. I.; Stevens, R. C.; Kobilka, B. K. GPCR engineering yields high-resolution structural insights into beta2-adrenergic receptor function. Science 2007, 318 (5854), 1266-1273.
28. Kobilka, B. K.; Deupi, X. Conformational complexity of G-protein-coupled receptors. Trends Pharmacol. Sci. 2007, 28 (8), 397-406.
29. Inooka, H.; Ohtaki, T.; Kitahara, O.; Ikegami, T.; Endo, S.; Kitada, C.; Ogi, K.; Onda, H.; Fujino, M.; Shirakawa, M. Conformation of a peptide ligand bound to its G-protein coupled receptor. Nat. Struct. Biol. 2001, 8 (2), 161-165.
30. Luca, S.; White, J. F.; Sohal, A. K.; Filippov, D. V.; van Boom, J. H.; Grisshammer, R.; Baldus, M. The conformation of neurotensin bound to its G protein-coupled receptor. Proc. Natl. Acad. Sci. U.S.A. 2003, 100 (19), 10706-10711.
31. Heise, H.; Luca, S.; de Groot, B. L.; Grubmuller, H.; Baldus, M. Probing conformational disorder in neurotensin by two-dimensional solid-state NMR and comparison to molecular dynamics simulations. Biophys. J. 2005, 89 (3), 2113-2120.
32. Dong, M.; Ding, X. Q.; Thomas, S. E.; Gao, F.; Lam, P. C.; Abagyan, R.; Miller, L. J. Role of lysine187 within the second extracellular loop of the type A cholecystokinin receptor in agonist-induced activation. Use of complementary charge-reversal mutagenesis to define a functionally important interdomain interaction. Biochemistry 2007, 46 (15), 4522-4531.
33. Archer-Lahlou, E.; Tikhonova, I.; Escrieut, C.; Dufresne, M.; Seva, C.; Pradayrol, L.; Moroder, L.; Maigret, B.; Fourmy, D. Modeled structure of a G-protein-coupled receptor: the cholecystokinin-1 receptor. J. Med. Chem. 2005, 48 (1), 180-191.
34. Archer-Lahlou, E.; Escrieut, C.; Clerc, P.; Martinez, J.; Moroder, L.; Logsdon, C.; Kopin, A.; Seva, C.; Dufresne, M.; Pradayrol, L.; Maigret, B.; Fourmy, D. Molecular mechanism underlying partial and full agonism mediated by the human cholecystokinin-1 receptor. J. Biol. Chem. 2005, 280 (11), 10664-10674.
35. Wuthrich, K. NMR of Proteins and Nucleic Acids; John Wiley and Sons: New York, 1986.
36. Braunschweiler, L.; Ernst, R. R. Coherence transfer by isotropic mixing: application to proton correlation spectroscopy. J. Magn. Reson. 1983, 53, 521-528.
37. Jeener, J.; Meier, B. H.; Bachmann, P.; Ernst, R. R. Investigation of exchange processes by two-dimensional NMR spectroscopy. J. Magn. Reson. 1979, 71, 4546.
38. Bothner-By, A. A.; Stephens, R. L.; Lee, J.-M.; Warren, C. D.; Jeanloz, R. W. Structure determination of a tetrasacchride: transient nuclear Overhauser effects in the rotating frame. J. Am. Chem. Soc. 1984, 106, 811-813.
39. Piotto, M.; Saudek, V.; Sklenar, V. Gradient-tailored excitation for single-quantum NMR spectroscopy of aqueous solutions. J Biomol NMR 1992, 2 (6), 661-665.
40. Sklenar, V. Suppression of radiation damping in multidimensional NMR experiments using magnetic field gradients. J. Magn. Reson. 1995, A114, 132-135.
41. 15N HSQC experiments optimized to retain full sensitivity. J. Magn. Reson., Ser. A 1993, 102, 241-245.
42. Marion, D.; Wuthrich, K. Application of phase sensitive two-dimensional correlated spectroscopy (COSY) for measurements of 1H-1H spin-spin coupling constants in proteins. Biochem. Biophys. Res. Commun. 1983, 113 (3), 967-974.
43. States, D. J.; Haberkorn, R. A.; Ruben, D. J. A two-dimensional nuclear Overhauser experiment with pure absorption phase in four quadrants. J. Magn. Reson. 1982, 48, 286.
44. Hwang, T.; Shaka, A. Water suppression that works, excitation sculpting using arbitrary wave-forms and pulsed-field gradients. J. Magn. Reson., Ser. A 1995, 112, 275-279.
45. Shaka, A.; Lee, C.; Pines, A. Iterative schemes for bilinear operators: application to spin decoupling. J. Magn. Reson. 1988, 77 (2), 274-293.
46. Brunger, A. T. X-PLOR: Version 3.1: A System for X-ray Crystallography and NMR. Yale Unviersity Press: New Haven, CT, 1992.
47. Wuthrich, K.; Billeter, M.; Braun, W. Pseudo-structures for the 20 common amino acids for use in studies of protein conformations by measurement of intramolecular proton-proton distance constraints with nuclear magnetic resonance. J. Mol. Biol. 1983, 169, 949-961.
48. Nigles, M.; Clore, G. M.; Gronenborn, A. M. Determination of three-dimensional structures of proteins from the interproton distance data by hybrid distance geometry-dynamical simulated annealing calculations. FEBS Lett. 1988, 2, 317-324.
49. Perczel, A.; Hollosi, M. Turns. In Circular Dichroism and the Conformational Analysis of Biomolecules; Fasman, G. Ed.; Plenum Press:New York, 1996; pp 285-380.
50. Woody, R. W. Contributions of tryptophan side chains to the far-ultraviolet circular dichroism of proteins. Eur. Biophys. J. 1994, 23 (4), 253-262.
51. Rozek, A.; Friedrich, C. L.; Hancock, R. E. Structure of the bovine antimicrobial peptide indolicidin bound to dodecylphosphocholine and sodium dodecyl sulfate micelles. Biochemistry 2000, 39 (51), 15765-15774.
52. Ladokhin, A. S.; Selsted, M. E.; White, S. H. CD spectra of indolicidin antimicrobial peptides suggest turns, not polyproline helix. Biochemistry 1999, 38 (38), 12313-12319.
53. Keire, D. A.; Solomon, T. E.; Reeve, J. R., Jr. NMR evidence for different conformations of the bioactive region of rat CCK-8 and CCK-58. Biochem. Biophys. Res. Commun. 2002, 293 (3), 1014-1020.
54. Keire, D. A.; Solomon, T. E.; Reeve, J. R., Jr. Identical primary sequence but different conformations of the bioactive regions of canine CCK-8 and CCK-58. Biochem. Biophys. Res. Commun. 1999, 266 (2), 400-404.
55. 15N chemical shift referencing in biomolecular NMR. J. Biomol. NMR 1995, 6, 135-140.
56. 15N random coil NMR chemical shifts of the common amino acids. 1. investigations of nearest-neighbor effects. J. Biomol. NMR 1995, 5 (1), 67-81.
57. Laskowski, R. A.; Rullmannn, J. A.; MacArthur, M. W.; Kaptein, R.; Thornton, J. M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 1996, 8 (4), 477-486.
58. Clore, G. M.; Robien, M. A.; Gronenborn, A. M. Exploring the limits of precision and accuracy of protein structures determined by nuclear magnetic resonance spectroscopy. J. Mol. Biol. 1993, 231 (1), 82-102.
59. Whitehead, T. L.; McNair, S. D.; Hadden, C. E.; Young, J. K.; Hicks, R. P. Membrane-induced secondary structures of neuropeptides: a comparison of the solution conformations adopted by agonists and antagonists of the mammalian tachykinin NK1 receptor. J. Med. Chem. 1998, 41 (9), 1497-1506.
60. Keire, D. A.; Fletcher, T. G. The conformation of substance P in lipid environments. Biophys. J. 1996, 70 (4), 1716-1727.
61. Lee, A. G. How lipids affect the activities of integral membrane proteins. Biochim. Biophys. Acta 2004, 1666 (1-2), 62-87.
62. Pucadyil, T. J.; Kalipatnapu, S.; Harikumar, K. G.; Rangaraj, N.; Karnik, S. S.; Chattopadhyay, A. G-protein-dependent cell surface dynamics of the human serotonin1A receptor tagged to yellow fluorescent protein. Biochemistry 2004, 43 (50), 15852-15862.
63. Harikumar, K. G.; Puri, V.; Singh, R. D.; Hanada, K.; Pagano, R. E.; Miller, L. J. Differential effects of modification of membrane cholesterol and sphingolipids on the conformation, function, and trafficking of the G protein-coupled cholecystokinin receptor. J. Biol. Chem. 2005, 280 (3), 2176-2185.
64. Paila, Y. D.; Pucadyil, T. J.; Chattopadhyay, A. The cholesterol- complexing agent digitonin modulates ligand binding of the bovine hippocampal serotonin 1A receptor. Mol. Membr. Biol. 2005, 22 (3), 241-249.
65. Chachisvilis, M.; Zhang, Y. L.; Frangos, J. A. G protein-coupled receptors sense fluid shear stress in endothelial cells. Proc. Natl. Acad. Sci. U.S.A. 2006, 103 (42), 15463-15468.
66. Raghuraman, H.; Chattopadhyay, A. Melittin: A Membrane-active Peptide with Diverse Functions. Biosci. Rep. 2006, 27, 189-223.
67. Romano, R.; Musiol, H. J.; Weyher, E.; Dufresne, M.; Moroder, L. Peptide hormone-membrane interactions: the aggregational and conformational state of lipogastrin derivatives and their receptor binding affinity. Biopolymers 1992, 32 (11), 1545-1558.
68. Romano, R.; Dufrense, M.; Prost, M. C.; Bali, J. P.; Bayerl, T. M.; Moroder, L. Peptide hormone-membrane interactions. Intravesicular transfer of lipophilic gastrin derivatives to artificial membranes and their bioactivities. Biochim. Biophys. Acta 1993, 1145, 235-242.
69. Lutz, J.; Romano-Gotsch, R.; Escrieut, C.; Fourmy, D.; Matha, B.; Muller, G.; Kessler, H.; Moroder, L. Mapping of ligand binding sites of the cholecystokinin-B/gastrin receptor with lipogastrin peptides and molecular modeling. Biopolymers 1997, 41 (7), 799-817.
70. Moroder, L. On the mechanism of hormone recognition and binding by the CCK-B/gastrin receptor. J. Pept. Sci. 1997, 3 (1), 1-14.
71. Moroder, L.; Romano, R.; Guba, W.; Mierke, D. F.; Kessler, H.; Delporte, C.; Winand, J.; Christophe, J. New evidence for a membrane-bound pathway in hormone receptor binding. Biochemistry 1993, 32 (49), 13551-13559.
72. Giragossian, C.; Mierke, D. F. Intermolecular interactions between cholecystokinin-8 and the third extracellular loop of the cholecystokinin-2 receptor. Biochemistry 2002, 41 (14), 4560-4566.
73. Giragossian, C.; Pellegrini, M.; Mierke, D. F. NMR studies of CCK-8/CCK1 complex support membrane-associated pathway for ligand-receptor interaction. Can. J. Physiol. Pharmacol. 2002, 80 (5), 383-387.
74. Giragossian, C.; Stone, S.; Papini, A. M.; Moroder, L.; Mierke, D. F. Conformational and molecular modeling studies of sulfated cholecystokinin-15. Biochem. Biophys. Res. Commun. 2002, 293 (3), 1053-1059.
75. Albrizio, S.; Carotenuto, A.; Fattorusso, C.; Moroder, L.; Picone, D.; Temussi. P. A.; D'Ursi, A. Environmental mimic of receptor interaction: conformational analysis of CCK-15 in solution. J. Med. Chem. 2002, 45 (4), 762-769.
76. Jacobs, R. E.; White, S. H. The nature of the hydrophobic binding of small peptides at the bilayer interface: implications for the insertion of transbilayer helicies. Biochemistry 1989, 28, 3421-3437.
77. Wishart, D. S.; Sykes, B. D.; Richards, F. M. The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry 1992, 31 (6), 1647-1651.
78. de Planque, M. R.; Bonev, B. B.; Demmers, J. A.; Greathouse, D. V.;.; Koeppe, R. E., 2nd; Separovic, F.; Watts, A.; Killian, J. A. Interfacial anchor properties of tryptophan residues in transmembrane peptides can dominate over hydrophobic matching effects in peptide-lipid interactions. Biochemistry 2003, 42 (18), 5341-5348.
79. Fournie-Zaluski, M. C.; Durieux, C.; Lux, B.; Belleney, J.; Pham, P.; Gerard, D.; Roques, B. P. Conformational analysis of cholecystokinin fragments CCK4, CCK5, and CCK6 by 1H-NMR spectroscopy and fluorescence-transfer measurements. Biopolymers 1985, 24, 1663-1681.
80. Loomis, R. E.; Lee, P. C.; Tseng, C. C. Conformational analysis of the cholecystokinin C-terminal octapeptide: a nuclear magnetic resonance and computer-simulation approach. Biochim. Biophys. Acta 1987, 911 (2), 168-179.
81. Moroder, L.; D'Ursi, A.; Picone, D.; Amodeo, P.; Temussi, P. A. Solution conformation of CCK9, a cholecystokinin analog. Biochem. Biophys. Res. Commun. 1993, 190 (3), 741-746.