Mass spectrometric analysis of agonist effects on posttranslational modifications of the β-2 adrenoceptor in mammalian cells

Biochemistry

Volumn 44, Issue 16, 2005, Pages 6133-6143

  Trester Zedlitz, Michelle ^a   Burlingame, Al ^a   Kobilka, Brian ^b   Von Zastrow, Mark ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b STANFORD UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; CONCENTRATION (PROCESS); MASS SPECTROMETRY; MODIFICATION; PURIFICATION;

B2AR; EPITOPE; PHOSPHORYLATION; RECEPTOR REGULATION;

CELLS;

ADRENALIN; AMINO ACID; BETA 2 ADRENERGIC RECEPTOR; CYSTEINE; DOPAMINE; EPITOPE; ISOPRENALINE; STABLE ISOTOPE;

ANTIBODY AFFINITY; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL CULTURE; CONTROLLED STUDY; CYTOPLASM; DRUG EFFECT; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; ISOTOPE LABELING; KIDNEY CELL; MAMMAL CELL; MASS SPECTROMETRY; PALMITOYLATION; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; PROTEIN PROCESSING; PURIFICATION; REGULATORY MECHANISM;

ADRENERGIC BETA-AGONISTS; AMINO ACID SEQUENCE; BINDING SITES; CELL LINE; DEUTERIUM; HUMANS; MOLECULAR SEQUENCE DATA; PALMITIC ACIDS; PHOSPHORYLATION; PROTEIN PROCESSING, POST-TRANSLATIONAL; PROTEIN STRUCTURE, TERTIARY; RECEPTORS, ADRENERGIC, BETA-2; RECOMBINANT PROTEINS; SPECTROMETRY, MASS, MATRIX-ASSISTED LASER DESORPTION-IONIZATION; TRANSFECTION;

MAMMALIA;

EID: 17644390240     PISSN: 00062960     EISSN: None     Source Type: Journal    
DOI: 10.1021/bi0475469     Document Type: Article

References (53)

1. Ohguro, H., Van Hooser, J. P., Milam, A. H., and Palczewski, K. (1995) Rhodopsin phosphorylation and dephosphorylation in vivo, J. Biol. Chem. 270, 14259-14262.
2. January, B., Seibold, A., Whaley, B., Hipkin, R. W., Lin, D., Schonbrunn, A., Barber, R., and Clark, R. B. (1997) beta2-adrenergic receptor desensitization, internalization, and phosphorylation in response to full and partial agonists, J. Biol. Chem. 272, 23871-23879.
3. Bouvier, M., Hausdorff, W. P., De Blasi, A., O'Dowd, B. F., Kobilka, B. K., Caron, M. G., and Lefkowitz, R. J. (1988) Removal of phosphorylation sites from the beta 2-adrenergic receptor delays onset of agonist-promoted desensitization, Nature 333, 370-373.
4. Sibley, D. R., Strasser, R. H., Benovic, J. L., Daniel, K., and Lefkowitz, R. J. (1986) Phosphorylation/dephosphorylation of the beta-adrenergic receptor regulates its functional coupling to adenylate cyclase and subcellular distribution, Proc. Natl. Acad. Sci. U.S.A. 83, 9408-9412.
5. El Kouhen, R., Burd, A. L., Erickson-Herbrandson, L. J., Chang, C. Y., Law, P. Y., and Loh, H. H. (2001) Phosphorylation of Ser363, Thr370, and Ser375 residues within the carboxyl tail differentially regulates mu-opioid receptor internalization, J. Biol. Chem. 276, 12774-12780.
6. Soskic, V., Nyakatura, E., Roos, M., Muller-Esterl, W., and Godovac-Zimmermann, J. (1999) Correlations in palmitoylation and multiple phosphorylation of rat bradykinin B2 receptor in Chinese hamster ovary cells, J. Biol. Chem. 274, 8539-8545.
7. Borgland, S. L., Connor, M., Osborne, P. B., Furness, J. B., and Christie, M. J. (2003) Opioid agonists have different efficacy profiles for G protein activation, rapid desensitization, and endocytosis of mu-opioid receptors, J. Biol. Chem. 278, 18776-18784.
8. January, B., Seibold, A., Allal, C., Whaley, B. S., Knoll, B. J., Moore, R. H., Dickey, B. F., Barber, R., and Clark, R. B. (1998) Salmeterol-induced desensitization, internalization and phosphorylation of the human beta2-adrenoceptor, Br. J. Pharmacol. 123, 701-711.
9. Swaminath, G., Xiang, Y., Lee, T. W., Steenhuis, J., Parnot, C., and Kobilka, B. K. (2004) Sequential binding of agonists to the beta2 adrenoceptor. Kinetic evidence for intermediate conformational states, J. Biol. Chem. 279, 686-691.
10. Keith, D. E., Anton, B., Murray, S. R., Zaki, P. A., Chu, P. C., Lissin, D. V., Monteillet, A. G., Stewart, P. L., Evans, C. J., and von Zastrow, M. (1998) mu-Opioid receptor internalization: opiate drugs have differential effects on a conserved endocytic mechanism in vitro and in the mammalian brain, Mol. Pharmacol. 53, 377-384.
11. Willins, D. L., Alsayegh, L., Berry, S. A., Backstrom, J. R., Sanders-Bush, E., Friedman, L., Khan, N., and Roth, B. L. (1998) Serotonergic antagonist effects on trafficking of serotonin 5-HT2A receptors in vitro and in vivo, Ann. N.Y. Acad. Sci. 861, 121-127.
12. Kenakin, T. (2004) Principles: Receptor theory in pharmacology, Trends Pharmacol. Sci. 25, 186-192.
13. von Zastrow, M., Keith, D. E. J., and Evans, C. J. (1993) Agonist-induced state of the delta-opioid receptor that discriminates between opioid peptides and opiate alkaloids, Mol. Pharmacol. 44, 166-172.
14. Alvarez, V. A., Arttamangkul, S., Dang, V., Salem, A., Whistler, J. L., Von Zastrow, M., Grandy, D. K., and Williams, J. T. (2002) mu-Opioid receptors: Ligand-dependent activation of potassium conductance, desensitization, and internalization, J. Neurosci. 22, 5769-5776.
15. Benovic, J. L., Staniszewski, C., Mayor, F., Jr., Caron, M. G., and Lefkowitz, R. J. (1988) beta-Adrenergic receptor kinase. Activity of partial agonists for stimulation of adenylate cyclase correlates with ability to promote receptor phosphorylation, J. Biol. Chem. 263, 3893-3897.
16. Fredericks, Z. L., Pitcher, J. A., and Lefkowitz, R. J. (1996) Identification of the G protein-coupled receptor kinase phosphorylation sites in the human beta2-adrenergic receptor, J. Biol. Chem. 271, 13796-13803.
17. Papac, D. I., Thornburg, K. R., Bullesbach, E. E., Crouch, R. K., and Knapp, D. R. (1992) Palmitylation of a G-protein coupled receptor. Direct analysis by tandem mass spectrometry, J. Biol. Chem. 267, 16889-16894.
18. Cadene, M., and Chait, B. T. (2000) A robust, detergent-friendly method for mass spectrometric analysis of integral membrane proteins, Anal. Chem. 72, 5655-5658.
19. Seibold, A., January, B. G., Friedman, J., Hipkin, R. W., and Clark, R. B. (1998) Desensitization of beta2-adrenergic receptors with mutations of the proposed G protein-coupled receptor kinase phosphorylation sites, J. Biol. Chem. 273, 7637-7642.
20. Seibold, A., Williams, B., Huang, Z. F., Friedman, J., Moore, R. H., Knoll, B. J., and Clark, R. B. (2000) Localization of the sites mediating desensitization of the beta(2)-adrenergic receptor by the GRK pathway, Mol. Pharmacol. 58, 1162-1173.
21. Moffett, S., Adam, L., Bonin, H., Loisel, T. P., Bouvier, M., and Mouillac, B. (1996) Palmitoylated cysteine 341 modulates phosphorylation of the beta2-adrenergic receptor by the cAMP-dependent protein kinase, J. Biol. Chem. 271, 21490-21497.
22. Clark, R. B., and Knoll, B. J. (2002) Measurement of receptor desensitization and internalization in intact cells, Methods Enzymol. 343, 506-529.
23. Papac, D. I., Oatis, J. E., Jr., Crouch, R. K., and Knapp, D. R. (1993) Mass spectrometric identification of phosphorylation sites in bleached bovine rhodopsin, Biochemistry 32, 5930-5934.
24. Karoor, V., Baltensperger, K., Paul, H., Czech, M. P., and Malbon, C. C. (1995) Phosphorylation of tyrosyl residues 350/354 of the beta-adrenergic receptor is obligatory for counterregulatory effects of insulin, J. Biol. Chem. 270, 25305-25308.
25. Kobilka, B. K. (1995) Amino and carboxyl terminal modifications to facilitate the production and purification of a G protein-coupled receptor, Anal. Biochem. 231, 269-271.
26. McLachlin, D. T., and Chait, B. T. (2001) Analysis of phosphorylated proteins and peptides by mass spectrometry, Curr. Opin. Chem. Biol. 5, 591-602.
27. Kalume, D. E., Molina, H., and Pandey, A. (2003) Tackling the phosphoproteome: tools and strategies, Curr. Opin. Chem. Biol. 7, 64-69.
28. Posewitz, M. C., and Tempst, P. (1999) Immobilized gallium(III) affinity chromatography of phosphopeptides. Anal. Chem. 71, 2883-2892.
29. Oda, Y., Huang, K., Cross, F. R., Cowburn, D., and Chait, B. T. (1999) Accurate quantitation of protein expression and site-specific phosphorylation, Proc. Natl. Acad. Sci. U.S.A. 96, 6591-6596.
30. Ibarrola, N., Kalume, D. E., Gronborg, M., Iwahori, A., and Pandey, A. (2003) A proteomic approach for quantitation of phosphorylation using stable isotope labeling in cell culture, Anal. Chem. 75, 6043-6049.
31. Ong, S. E., Blagoev, B., Kratchmarova, I., Kristensen, D. B., Steen, H., Pandey, A., and Mann, M. (2002) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics, Mol. Cell Proteomics 1, 376-386.
32. Ong, S. E., Foster, L. J., and Mann, M. (2003) Mass spectrometric-based approaches in quantitative proteomics, Methods 29, 124-130.
33. Julka, S., and Regnier, F. (2004) Quantification in proteomics through stable isotope coding: a review, J. Proteome Res. 3, 350-363.
34. von Zastrow, M., and Kobilka, B. K. (1992) Ligand-regulated internalization and recycling of human beta 2-adrenergic receptors between the plasma membrane and endosomes containing transferrin receptors, J. Biol. Chem. 267, 3530-3538.
35. Cao, T. C., Mays, R. W., and von Zastrow, M. (1998) Regulated endocytosis of G protein-coupled receptors by a biochemically and functionally distinct subpopulation of clathrin-coated pits, J. Biol. Chem. 273, 24592-24602.
36. Trester-Zedlitz, M., Kamada, K., Burley, S. K., Fenyo, D., Chait, B. T., and Muir, T. W. (2003) A modular cross-linking approach for exploring protein interactions, J. Am. Chem. Soc. 125, 2416-2425.
37. Choi, B. K., Cho, Y. M., Bae, S. H., Zoubaulis, C. C., and Paik, Y. K. (2003) Single-step perfusion chromatography with a throughput potential for enhanced peptide detection by matrix-assisted laser desorption/ionization-mass spectrometry, Proteomics 3, 1955-1961.
38. Guan, X. M., Kobilka, T. S., and Kobilka, B. K. (1992) Enhancement of membrane insertion and function in a type IIIb membrane protein following introduction of a cleavable signal peptide, J. Biol. Chem. 267, 21995-21998.
39. Tsao, P. I., and von Zastrow, M. (2000) Type-specific sorting of G protein-coupled receptors after endocytosis, J. Biol. Chem. 275, 11130-11140.
40. 13C-substituted arginine in stable isotope labeling by amino acids in cell culture (SILAC), J. Proteome Res. 2, 173-181.
41. Steinberg, T. H., Agnew, B. J., Gee, K. R., Leung, W. Y., Goodman, T., Schulenberg, B., Hendrickson, J., Beechem, J. M., Haugland, R. P., and Patton, W. F. (2003) Global quantitative phosphoprotein analysis using multiplexed proteomics technology, Proteomics 3, 1128-1144.
42. Schulenberg, B., Aggeler, R., Beechem, J. M., Capaldi, R. A., and Patton, W. F. (2003) Analysis of steady-state protein phosphorylation in mitochondria using a novel fluorescent phosphosensor dye, J. Biol. Chem. 278, 27251-27255.
43. O'Dowd, B. F., Hnatowich, M., Caron, M. G., Lefkowitz, R. J., and Bouvier, M. (1989) Palmitoylation of the human beta 2-adrenergic receptor. Mutation of Cys341 in the carboxyl tail leads to an uncoupled nonpalmitoylated form of the receptor, J. Biol. Chem. 264, 7564-7569.
44. Bouvier, M., Moffett, S., Loisel, T. P., Mouillac, B., Hebert, T., and Chidiac, P. (1995) Palmitoylation of G-protein-coupled receptors: a dynamic modification with functional consequences, Biochem. Soc. Trans. 23, 116-120.
45. Loisel, T. P., Ansanay, H., Adam, L., Marullo, S., Seifert, R., Lagace, M., and Bouvier, M. (1999) Activation of the beta(2)-adrenergic receptor-Galpha(s) complex leads to rapid depalmitoylation and inhibition of repalmitoylation of both the receptor and Galpha(s), J. Biol. Chem. 274, 31014-31019.
46. Loisel, T. P., Adam, L., Hebert, T. E., and Bouvier, M. (1996) Agonist stimulation increases the turnover rate of beta 2AR-bound palmitate and promotes receptor depalmitoylation, Biochemistry 35, 15923-15932.
47. Jones, T. L., Degtyarev, M. Y., and Backlund, P. S., Jr. (1997) The stoichiometry of G alpha(s) palmitoylation in its basal and activated states, Biochemistry 36, 7185-7191.
48. Tran, T. M., Friedman, J., Qunaibi, E., Baameur, F., Moore, R. H., and Clark, R. B. (2004) Characterization of agonist stimulation of cAMP-dependent protein kinase and G protein-coupled receptor kinase phosphorylation of the beta2-adrenergic receptor using phosphoserine-specific antibodies, Mol. Pharmacol. 65, 196-206.
49. Lefkowitz, R. J., Pitcher, J., Krueger, K., and Daaka, Y. (1998) Mechanisms of beta-adrenergic receptor desensitization and resensitization, Adv. Pharmacol. 42, 416-420.
50. Menard, L., Ferguson, S. S., Zhang, J., Lin, F. T., Lefkowitz, R. J., Caron, M. G., and Barak, L. S. (1997) Synergistic regulation of beta2-adrenergic receptor sequestration: intracellular complement of beta-adrenergic receptor kinase and beta-arrestin determine kinetics of internalization, Mol. Pharmacol. 51, 800-808.
51. Hausdorff, W. P., Campbell, P. T., Ostrowski, J., Yu, S. S., Caron, M. G., and Lefkowitz, R. J. (1991) A small region of the beta-adrenergic receptor is selectively involved in its rapid regulation, Proc. Natl. Acad. Sci. U.S.A. 88, 2979-2983.
52. Seibold, A., January, B. G., Friedman, J., Hipkin, R. W., and Clark, R. B. (1998) Desensitization of beta2-adrenergic receptors with mutations of the proposed G protein-coupled receptor kinase phosphorylation sites, J. Biol.Chem. 273, 7637-7642.
53. 13C]tyrosine, J. Biol. Chem. 279, 15805-15813.