Oligomeric size of the M2 muscarinic receptor in live cells as determined by quantitative fluorescence resonance energy transfer

Journal of Biological Chemistry

Volumn 285, Issue 22, 2010, Pages 16723-16738

  Pisterzi, Luca F ^a   Jansma, David B ^a   Georgiou, John ^b   Woodside, Michael J ^c   Tai Chieh Chou, Judy ^a   Angers, Stéphane ^a   Raicu, Valericǎ ^d   Wells, James W ^a  

^a UNIVERSITY OF TORONTO   (Canada)

^b MOUNT SINAI HOSPITAL   (Canada)

^c HOSPITAL FOR SICK CHILDREN   (Canada)

^d UNIVERSITY OF WISCONSIN MILWAUKEE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHINESE HAMSTER OVARY CELLS; CHOLINERGIC RECEPTORS; DEQUENCHING; DONOR AND ACCEPTOR; EMISSION SPECTRUMS; ENHANCED GREEN FLUORESCENT PROTEIN; ENHANCED YELLOW FLUORESCENT PROTEINS; FITTED VALUES; FLUORESCENCE INTENSITIES; FLUORESCENCE LIFETIME IMAGING; FLUORESCENCE LIFETIMES; FLUORESCENCE PROPERTIES; FLUORESCENCE RESONANCE ENERGY TRANSFER; G PROTEIN COUPLED RECEPTORS; LIVE CELL; MUSCARINIC RECEPTOR; SIGNALING PROCESS; SINGLE DONOR; SPECTRAL DECONVOLUTION; TETRAMERS; YELLOW FLUORESCENT PROTEINS;

EMISSION SPECTROSCOPY; ENERGY TRANSFER; OLIGOMERS; PROTEINS; RESONANCE;

FLUORESCENCE;

DIMER; G PROTEIN COUPLED RECEPTOR; GREEN FLUORESCENT PROTEIN; MUSCARINIC M2 RECEPTOR; OLIGOMER; TETRAMER; YELLOW FLUORESCENT PROTEIN; BACTERIAL PROTEIN; PHOTOPROTEIN; YELLOW FLUORESCENT PROTEIN, BACTERIA;

AMINO TERMINAL SEQUENCE; ANIMAL CELL; ARTICLE; CHO CELL; CONTROLLED STUDY; DATA ANALYSIS; FLUORESCENCE; FLUORESCENCE IMAGING; FLUORESCENCE MICROSCOPY; FLUORESCENCE RESONANCE ENERGY TRANSFER; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; BIOLOGICAL MODEL; CHEMISTRY; CONFOCAL MICROSCOPY; CRICETULUS; HAMSTER; HUMAN; KINETICS; METABOLISM; METHODOLOGY; PROTEIN TERTIARY STRUCTURE; THEORETICAL MODEL;

CRICETULUS GRISEUS;

ANIMALS; BACTERIAL PROTEINS; CHO CELLS; CRICETINAE; CRICETULUS; FLUORESCENCE RESONANCE ENERGY TRANSFER; GREEN FLUORESCENT PROTEINS; HUMANS; KINETICS; LUMINESCENT PROTEINS; MICROSCOPY, CONFOCAL; MODELS, BIOLOGICAL; MODELS, THEORETICAL; PROTEIN STRUCTURE, TERTIARY; RECEPTOR, MUSCARINIC M2; RECEPTORS, G-PROTEIN-COUPLED;

EID: 77952757509     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M109.069443     Document Type: Article

References (73)

1. Angers, S., Salahpour, A., and Bouvier, M. (2002) Annu. Rev. Pharmacol. Toxicol. 42, 409-435
2. Bai, M. (2004) Cell. Signal. 16, 175-186
3. Harrison, C., and van der Graaf, P. H. (2006) J. Pharmacol. Toxicol. Methods 54, 26-35
4. Ma, A. W., Redka, D. S., Pisterzi, L. F., Angers, S., and Wells, J. W. (2007) Biochemistry 46, 7907-7927
5. Park, P. S., and Wells, J. W. (2004) J. Neurochem. 90, 537-548
6. Lopez-Gimenez, J. F., Canals, M., Pediani, J. D., and Milligan, G. (2007) Mol. Pharmacol. 71, 1015-1029
7. Carriba, P., Navarro, G., Ciruela, F., Ferré, S., Casadó, V., Agnati, L., Cortés, A., Mallol, J., Fuxe, K., Canela, E. I., Lluís, C., and Franco, R. (2008) Nat. Methods 5, 727-733
8. Guo, W., Urizar, E., Kralikova, M., Mobarec, J. C., Shi, L., Filizola, M., and Javitch, J. A. (2008) EMBO J. 27, 2293-2304
9. Gandia, J., Galino, J., Amaral, O. B., Soriano, A., Lluís, C., Franco, R., and Ciruela, F. (2008) FEBS Lett. 582, 2979-2984
10. Maurel, D., Comps-Agrar, L., Brock, C., Rives, M. L., Bourrier, E., Ayoub, M. A., Bazin, H., Tinel, N., Durroux, T., Prézeau, L., Trinquet, E., and Pin, J. P. (2008) Nat. Methods 5, 561-567
11. Vidi, P. A., Chen, J., Irudayaraj, J. M., and Watts, V. J. (2008) FEBS Lett. 582, 3985-3990
12. Ayoub, M. A., Couturier, C., Lucas-Meunier, E., Angers, S., Fossier, P., Bouvier, M., and Jockers, R. (2002) J. Biol. Chem. 277, 21522-21528
13. Mercier, J. F., Salahpour, A., Angers, S., Breit, A., and Bouvier, M. (2002) J. Biol. Chem. 277, 44925-44931
14. Goin, J. C., and Nathanson, N. M. (2006) J. Biol. Chem. 281, 5416-5425
15. Harding, P. J., Attrill, H., Boehringer, J., Ross, S., Wadhams, G. H., Smith, E., Armitage, J. P., and Watts, A. (2009) Biophys. J. 96, 964-973
16. Veatch, W., and Stryer, L. (1977) J. Mol. Biol. 113, 89-102
17. Raicu, V. (2007) J. Biol. Phys. 33, 109-127
18. Wreggett, K. A., and Wells, J. W. (1995) J. Biol. Chem. 270, 22488-22499
19. Colozo, A. T., Park, P. S., Sum, C. S., Pisterzi, L. F., and Wells, J. W. (2007) Biochem. Pharmacol. 74, 236-255
20. Park, P. S., Sum, C. S., Pawagi, A. B., and Wells, J. W. (2002) Biochemistry 41, 5588-5604
21. Pisterzi, L. F., Jansma, D. B., Georgiou, J., Woodside, M. J., Chou, J. T., Angers, S., Raicu, V., and Wells, J. W. (2009) Biophys. J. 96, 169a
22. Weill, C., Galzi, J. L., Chasserot-Golaz, S., Goeldner, M., and Ilien, B. (1999) J. Neurochem. 73, 791-801
23. Tsien, R. Y. (1998) Annu. Rev. Biochem. 67, 509-544
24. Heim, R. (1999) Methods Enzymol. 302, 408-423
25. Lippincott-Schwartz, J., and Patterson, G. H. (2003) Science 300, 87-91
26. Zacharias, D. A., Violin, J. D., Newton, A. C., and Tsien, R. Y. (2002) Science 296, 913-916
27. Raymond, C. K., Sims, E. H., and Olson, M. V. (2002) Genome Res. 12, 190-197
28. Yang-Snyder, J., Miller, J. R., Brown, J. D., Lai, C. J., and Moon, R. T. (1996) Curr. Biol. 6, 1302-1306
29. Kuang, D., Yao, Y., Lam, J., Tsushima, R. G., and Hampson, D. R. (2005) J. Neurochem. 93, 383-391
30. Ma, D., and Wells, J. W. (2004) Biotechnol. Lett. 26, 1441-1446
31. Jordan, M., Schallhorn, A., and Wurm, F. M. (1996) Nucleic Acids Res. 24, 596-601
32. Chowdhury, E. H., Sasagawa, T., Nagaoka, M., Kundu, A. K., and Akaike, T. (2003) Anal. Biochem. 314, 316-318
33. Jordan, M., and Wurm, F. (2004) Methods 33, 136-143
34. Conklin, B. R., Farfel, Z., Lustig, K. D., Julius, D., and Bourne, H. R. (1993) Nature 363, 274-276
35. Kuang, D., Yao, Y., Wang, M., Pattabiraman, N., Kotra, L. P., and Hampson, D. R. (2003) J. Biol. Chem. 278, 42551-42559
36. Rasband, W. S., ImageJ, Version 1.41k, National Institutes of Health, rsb.info.nih.gov/ij/, 1997-2007
37. Raicu, V., Jansma, D. B., Miller, R. J., and Friesen, J. D. (2005) Biochem. J. 385, 265-277
38. Zimmermann, T., Rietdorf, J., Girod, A., Georget, V., and Pepperkok, R. (2002) FEBS Lett. 531, 245-249
39. Lakowicz, J. R. (2006) Principles of Fluorescence Spectroscopy, 3rd Ed., pp.445-447, Springer-Verlag Inc., New York
40. Wells, J. W. (1992) in Receptor-Ligand Interactions: A Practical Approach (Hulme, E. C., ed) pp. 289-395, Oxford University Press, Oxford, UK
41. Gordon, G. W., Berry, G., Liang, X. H., Levine, B., and Herman, B. (1998) Biophys. J. 74, 2702-2713
42. Skrabanek, L., Campagne, F., and Weinstein, H. (2003) Nucleic Acids Res. 31, 3856-3858
43. Raicu, V., Jansma, D. B., and Michalski, K. (2006) in Proceedings of SPIE, Imaging, Manipulation, and Analysis of Biomolecules, Cells, and Tissues IV (Farkas, D. L., Nicolau, D. V., and Leif, R. C., eds) 60880A 60881-60880A 60889
44. Dinant, C., van Royen, M. E., Vermeulen, W., and Houtsmuller, A. B. (2008) J. Microsc. 231, 97-104
45. Adams, S. R., Campbell, R. E., Gross, L. A., Martin, B. R., Walkup, G. K., Yao, Y., Llopis, J., and Tsien, R. Y. (2002) J. Am. Chem. Soc. 124, 6063-6076
46. Jordan, B. A., Trapaidze, N., Gomes, I., Nivarthi, R., and Devi, L. A. (2001) Proc. Natl. Acad. Sci. U.S.A. 98, 343-348
47. Pathak, A., Smih, F., Galinier, M., Verwaerde, P., Rouet, P., Philip-Couderc, P., Montastruc, J. L., and Senard, J. M. (2005) Int. J. Obes. 29, 176-182
48. Peterson, G. L., and Schimerlik, M. I. (1984) Prep. Biochem. 14, 33-74
49. Mattera, R., Pitts, B. J., Entman, M. L., and Birnbaumer, L. (1985) J. Biol. Chem. 260, 7410-7421
50. Sum, C. S., Pyo, N., and Wells, J. W. (2001) Biochem. Pharmacol. 62, 829-851
51. Kaykas, A., Yang-Snyder, J., Héroux, M., Shah, K. V., Bouvier, M., and Moon, R. T. (2004) Nat. Cell Biol. 6, 52-58
52. Berrie, C. P., Birdsall, N. J., Burgen, A. S., and Hulme, E. C. (1979) Biochem. Biophys. Res. Commun. 87, 1000-1005
53. Chidiac, P., Green, M. A., Pawagi, A. B., and Wells, J. W. (1997) Biochemistry 36, 7361-7379
54. Tota, M. R., Kahler, K. R., and Schimerlik, M. I. (1987) Biochemistry 26, 8175-8182
55. Shiozaki, K., and Haga, T. (1992) Biochemistry 31, 10634-10642
56. Raicu, V., Stoneman, M. R., Fung, R., Melnichuk, M., Jansma, D. B., Pisterzi, L. F., Rath, S., Fox, M., Wells, J. W., and Saldin, D. K. (2009) Nature Photonics 3, 107-113
57. Liang, Y., Fotiadis, D., Filipek, S., Saperstein, D. A., Palczewski, K., and Engel, A. (2003) J. Biol. Chem. 278, 21655-21662
58. Fung, J. J., Deupi, X., Pardo, L., Yao, X. J., Velez-Ruiz, G. A., Devree, B. T., Sunahara, R. K., and Kobilka, B. K. (2009) EMBO J. 28, 3315-3328
59. Gazi, L., López-Giménez, J. F., Rüdiger, M. P., and Strange, P. G. (2003) Eur. J. Biochem. 270, 3928-3938
60. Park, P., Sum, C. S., Hampson, D. R., Van Tol, H. H., and Wells, J. W. (2001) Eur. J. Pharmacol. 421, 11-22
61. Redka, D. S., Pisterzi, L. F., and Wells, J. W. (2008) Mol. Pharmacol. 74, 834-843
62. Dupré, D. J., Robitaille, M., Ethier, N., Villeneuve, L. R., Mamarbachi, A. M., and Hébert, T. E. (2006) J. Biol. Chem. 281, 34561-34573
63. Dupré, D. J., Baragli, A., Rebois, R. V., Ethier, N., and Hébert, T. E. (2007) Cell. Signal. 19, 481-489
64. Dorsch, S., Klotz, K. N., Engelhardt, S., Lohse, M. J., and Bünemann, M. (2009) Nat. Methods 6, 225-230
65. Fonseca, J. M., and Lambert, N. A. (2009) Mol. Pharmacol. 75, 1296-1299
66. Whorton, M. R., Bokoch, M. P., Rasmussen, S. G., Huang, B., Zare, R. N., Kobilka, B., and Sunahara, R. K. (2007) Proc. Natl. Acad. Sci. U.S.A. 104, 7682-7687
67. Kuszak, A. J., Pitchiaya, S., Anand, J. P., Mosberg, H. I., Walter, N. G., and Sunahara, R. K. (2009) J. Biol. Chem. 284, 26732-26741
68. Bayburt, T. H., Leitz, A. J., Xie, G., Oprian, D. D., and Sligar, S. G. (2007) J. Biol. Chem. 282, 14875-14881
69. Whorton, M. R., Jastrzebska, B., Park, P. S., Fotiadis, D., Engel, A., Palczewski, K., and Sunahara, R. K. (2008) J. Biol. Chem. 283, 4387-4394
70. Green, M. A., Chidiac, P., and Wells, J. W. (1997) Biochemistry 36, 7380-7394
71. Birdsall, N. J., Burgen, A. S., and Hulme, E. C. (1977) Adv. Behav. Biol. 24, 25-33
72. Ehlert, F. J. (1985) Mol. Pharmacol. 28, 410-421
73. Zeng, F. Y., and Wess, J. (1999) J. Biol. Chem. 274, 19487-19497