Differential docking of high-affinity peptide ligands to type A and B cholecystokinin receptors demonstrated by photoaffinity labeling

Biochemistry

Volumn 44, Issue 17, 2005, Pages 6693-6700

  Dong, Maoqing ^a   Liu, Guangming ^a   Pinon, Delia I ^a   Miller, Laurence J ^a  

^a MAYO CLINIC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BROMINE; DEGRADATION; ENZYMES; PROTEINS;

CHEMICAL CLEAVAGE; HIGH-AFFINITY PEPTIDES; HOMOLOGOUS RECEPTORS; LIGANDS;

BIOCHEMISTRY;

4 BENZOYLPHENYLALANINE; CHOLECYSTOKININ A RECEPTOR; CHOLECYSTOKININ B RECEPTOR; CHOLECYSTOKININ OCTAPEPTIDE; CYANOGEN BROMIDE; MUTANT PROTEIN; PEPTIDE DERIVATIVE; PHENYLALANINE DERIVATIVE; TRYPTOPHAN; UNCLASSIFIED DRUG;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; BINDING AFFINITY; CALCIUM CELL LEVEL; CONTROLLED STUDY; COVALENT BOND; ENZYME DEGRADATION; MOLECULAR PROBE; MUTANT; NONHUMAN; PHOTOAFFINITY LABELING; PRIORITY JOURNAL; PROTEIN STRUCTURE; RECEPTOR BINDING; WILD TYPE;

AMINO ACID SEQUENCE; ANIMALS; BENZOPHENONES; CELL MEMBRANE; CHO CELLS; CRICETINAE; EXTRACELLULAR SPACE; HUMANS; LIGANDS; MOLECULAR SEQUENCE DATA; PEPTIDE FRAGMENTS; PEPTIDE MAPPING; PHENYLALANINE; PHOTOAFFINITY LABELS; PROTEIN BINDING; PROTEIN STRUCTURE, TERTIARY; RECEPTOR, CHOLECYSTOKININ A; RECEPTOR, CHOLECYSTOKININ B;

EID: 17844390997     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi050130q     Document Type: Article

References (36)

1. Dohlman, H. G., Caron, M. G., Strader, C. D., Amlaiky, N., and Lefkowitz, R. J. (1988) Identification and sequence of a binding site peptide of the β2-adrenergic receptor, Biochemistry 27, 1813-1817.
2. Strader, C. D., Gaffney, T., Sugg, E. E., Candelore, M. R., Keys, R., Patchett, A. A., and Dixon, R. A. F. (1991) Allele-specific activation of genetically engineered receptors, J. Biol. Chem. 266, 5-8.
3. Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Trong, I. Le., Teller, D. C., Okada, T., Stenkamp, R. E., Yamamoto, M., and Miyano, M. (2000) Crystal structure of rhodopsin: A G protein-coupled receptor, Science 289, 739-745.
4. Vigna, S. R., Thorndyke, M. C., and Williams, J. A. (1986) Evidence for a common evolutionary origin of brain and pancreas cholecystokinin receptors, Proc. Natl. Acad. Sci. U.S.A. 83, 4355-4359.
5. Johnsen, A. H., and Rehfeld, J. F. (1992) Identification of cholecystokinin/gastrin peptides in frog and turtle. Evidence that cholecystokinin is phylogenetically older than gastrin, Eur. J. Biochem. 207, 419-428.
6. Noble, F., and Roques, B. P. (1999) CCK-B receptor: Chemistry, molecular biology, biochemistry, and pharmacology, Prog. Neurobiol. 58, 349-379.
7. Noble, F., Wank, S. A., Crawley, J. N., Bradwejn, J., Seroogy, K. B., Hamon, M., and Roques, B. P. (1999) International union of pharmacology. XXI. Structure, distribution, and functions of cholecystokinin receptors, Pharmacol. Rev. 51, 745-781.
8. Kopin, A. S., Lee, Y. M., McBride, E. W., Miller, L. J., Lu, M., Lin, H. Y., Kolakowski, L. F., and Beinborn, M. (1992) Expression cloning and characterization of the canine parietal cell gastrin receptor, Proc. Natl. Acad. Sci. U.S.A. 89, 3605-3609.
9. Wank, S. A., Harkins, R., Jensen, R. T., Shapira, H., De Weerth, A., and Slattery, T. (1992) Purification, molecular cloning, and functional expression of the cholecystokinin receptor from rat pancreas, Proc. Natl. Acad. Sci. U.S.A. 89, 3125-3129.
10. Schmitz, F., Prat, D. S., Wu, M. J., Kolakowski, L. F., Jr., Beinborn, M., and Kopin, A. S. (1996) Identification of cholecystokinin-B/gastrin receptor domains that confer high gastrin affinity: Utilization of a novel Xenopus laevis cholecystokinin receptor, Mol. Pharmacol. 50, 436-441.
11. Ji, Z., Hadac, E. M., Henne, R. M., Patel, S. A., Lybrand, T. P., and Miller, L. J. (1997) Direct identification of a distinct site of interaction between the carboxyl-terminal residue of cholecystokinin and the type A cholecystokinin receptor using photoaffinity labeling, J. Biol. Chem. 272, 24393-24401.
12. Hadac, E. M., Pinon, D. I., Ji, Z., Holicky, E. L., Henne, R. M., Lybrand, T. P., and Miller, L. J. (1998) Direct identification of a second distinct site of contact between cholecystokinin and its receptor, J. Biol. Chem. 273, 12988-12993.
13. Hadac, E. M., Ji, Z. S., Pinon, D. I., Henne, R. M., Lybrand, T. P., and Miller, L. J. (1999) A peptide agonist acts by occupation of a monomeric G protein-coupled receptor: Dual sites of covalent attachment to domains near TM1 and TM7 of the same molecule make biologically significant domain-swapped dimerization unlikely, J. Med. Chem. 42, 2105-2111.
14. Ding, X. Q., Dolu, V., Hadac, E. M., Holicky, E. L., Pinon, D. I., Lybrand, T. P., and Miller, L. J. (2001) Refinement of the structure of the ligand-occupied cholecystokinin receptor using a photolabile amino-terminal probe, J. Biol. Chem. 276, 4236-4244.
15. Anders, J., Bluggel, M., Meyer, H. E., Kuhne, R., Ter Laak, A. M., Kojro, E., and Fahrenholz, F. (1999) Direct identification of the agonist binding site in the human brain cholecystokinin B receptor, Biochemistry 38, 6043-6055.
16. Pearson, R. K., Miller, L. J., Hadac, E. M., and Powers, S. P. (1987) Analysis of the carbohydrate composition of the pancreatic plasmalemmal glycoprotein affinity labeled by short probes for the cholecystokinin receptor, J. Biol. Chem. 262, 13850-13856.
17. 33)CCK-26-33), J. Biol. Chem. 263, 5295-5300.
18. Powers, S. P., Pinon, D. I., and Miller, L. J. (1988) Use of N,O-bis-Fmoc-D-Tyr-ONSu for introduction of an oxidative iodination site into cholecystokinin family peptides, Int. J. Pept. Protein Res. 31, 429-434.
19. Cheng, Z. J., Harikumar, K. G., Holicky, E. L., and Miller, L. J. (2003) Heterodimerization of type A and B cholecystokinin receptors enhance signaling and promote cell growth, J. Biol. Chem. 278, 52972-52979.
20. Sanger, F., Nicklen, S., and Coulson, A. R. (1977) DNA sequencing with chain-terminating inhibitors, Proc. Natl. Acad. Sci. U.S.A. 74, 5463-5467.
21. Holtmann, M. H., Ganguli, S., Hadac, E. M., Dolu, V., and Miller, L. J. (1996) Multiple extracellular loop domains contribute critical determinants for agonist binding and activation of the secretin receptor, J. Biol. Chem. 271, 14944-14949.
22. Hadac, E. M., Ghanekar, D. V., Holicky, E. L., Pinon, D. I., Dougherty, R. W., and Miller, L. J. (1996) Relationship between native and recombinant cholecystokinin receptors - Role of differential glycosylation, Pancreas 13, 130-139.
23. Munson, P. J., and Rodbard, D. (1980) LIGAND: A versatile computerized approach for characterization of ligand-binding systems, Anal. Biochem. 107, 220-239.
24. Harikumar, K. G., Pinon, D. L., Wessels, W. S., Prendergast, F. G., and Miller, L. J. (2002) Environment and mobility of a series of fluorescent reporters at the amino terminus of structurally related peptide agonists and antagonists bound to the cholecystokinin receptor, J. Biol. Chem. 277, 18552-18560.
25. Grynldewicz, G., Poenie, M., and Tsien, R. Y. (1985) A new generation of calcium indicators with greatly improved fluorescence properties, J. Biol. Chem. 260, 3440-3450.
26. Laemmli, U. K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4, Nature 227, 680-685.
27. Dong, M., Wang, Y., Pinon, D. I., Hadac, E. M., and Miller, L. J. (1999) Demonstration of a direct interaction between residue 22 in the carboxyl-terminal half of secretin and the amino-terminal tail of the secretin receptor using photoaffinity labeling, J. Biol. Chem. 274, 903-909.
28. Harikumar, K. G., Clain, J., Pinon, D. I., Dong, M., and Miller, L. J. (2005) Distinct molecular mechanisms for agonist peptide binding to types A and B cholecystokinin receptors demonstrated using fluorescence spectroscopy, J. Biol. Chem. 280, 1044-1050.
29. Kopin, A. S., McBride, E. W., Quinn, S. M., Kolakowski, L. F., Jr., and Beinborn, M. (1995) The role of the cholecystokinin-B/gastrin receptor transmembrane domains in determining affinity for subtype-selective ligands, J. Biol. Chem. 270, 5019-5023.
30. Silvente-Poirot, S., and Wank, S. A. (1996) A segment of five amino acids in the second extracellular loop of the cholecystokinin-B receptor is essential for selectivity of the peptide agonist gastrin, J. Biol. Chem. 271, 14698-14706.
31. Dawson, E. S., Henne, R. M., Miller, L. J., and Lybrand, T. P. (2002) Molecular models for cholecystokinin-A receptor, Pharmacol. Toxicol. 91, 290-296.
32. Ding, X. Q., Pinon, D. I., Furse, K. E., Lybrand, T. P., and Miller, L. J. (2002) Refinement of the conformation of a critical region of charge-charge interaction between cholecystokinin and its receptor, Mol. Pharmacol. 61, 1041-1052.
33. Harikumar, K. G., and Miller, L. J. (2002) Applications of fluorescence in the characterization of the ligand-binding domain and activation of the cholecystokinin receptor, Pharmacol. Toxicol. 91, 286-289.
34. Harikumar, K. G., Pinon, D. I., Wessels, W. S., Dawson, E. S., Lybrand, T. P., Prendergast, F. G., and Miller, L. J. (2004) Mesurement of intermolecular distances for the natural agonist peptide docked at the cholecystokinin receptor expressed in situ using fluorescence resonance energy transfer, Mol. Pharmacol. 65, 28-35.
35. Charpentier, B., Dor, A., Roy, P., England, P., Pham, H., Durieux, C., and Roques B. P. (1989) Synthesis and binding affinities of cyclic and related linear analogues of CCK8 selective for central receptors, J. Med. Chem. 32, 1184-1190.
36. Rodriguez, M., Lignon, M. F., Galas, M. C., Amblard, M., and Martinez, J. (1990) Cyclic cholecystokinin analogues that are highly selective for rat and guinea pig central cholecystokinin receptors, Mol. Pharmacol. 38, 333-341.