Random mutagenesis of the M3 muscarinic acetylcholine receptor expressed in yeast: Identification of second-site mutations that restore function to a coupling-deficient mutant M3 receptor

Journal of Biological Chemistry

Volumn 280, Issue 7, 2005, Pages 5664-5675

  Li, Bo ^a   Nowak, Nicola M ^a   Kim, Soo Kyung ^a   Jacobson, Kenneth A ^a   Bagheri, Ali ^a   Schmidt, Clarice ^a   Wess, Jürgen ^a  

^a NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIVATION ANALYSIS; BIOLOGICAL MEMBRANES; CELLS; PROTEINS; YEAST;

G PROTEIN-COUPLED RECEPTORS (GPCR); MUSCARINIC ACETYLCHOLINE RECEPTORS; STRUCTURAL MECHANISMS; TRANSMEMBRANES;

MUTAGENESIS;

ARGININE; ASPARTIC ACID; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; MUSCARINIC M3 RECEPTOR; MUTANT PROTEIN; TYROSINE; LIGAND; PHOSPHATIDYLINOSITOL;

ANIMAL CELL; ARTICLE; CELL MEMBRANE; CELL STRAIN COS7; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CYTOPLASM; FUNGAL STRAIN; GENE IDENTIFICATION; GENE LIBRARY; GENE MUTATION; GENE REPRESSION; GENETIC CONSERVATION; GENETIC LINKAGE; GENETIC ORGANIZATION; GENETIC SCREENING; GENETIC TRANSFECTION; MAMMAL CELL; MONKEY; MUTAGENESIS; NONHUMAN; OBSERVATION; POINT MUTATION; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN INDUCTION; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE; WILD TYPE; YEAST; ALLELE; ANIMAL; CELL STRAIN COS1; CHEMISTRY; GENETICS; HYDROLYSIS; METABOLISM; RADIOASSAY; RAT; STRUCTURE ACTIVITY RELATION;

ANIMALIA; MAMMALIA; SACCHAROMYCES CEREVISIAE;

ALLELES; ANIMALS; ARGININE; COS CELLS; HYDROLYSIS; LIGANDS; MUTAGENESIS; PHOSPHATIDYLINOSITOLS; POINT MUTATION; RADIOLIGAND ASSAY; RATS; RECEPTOR, MUSCARINIC M3; SACCHAROMYCES CEREVISIAE; STRUCTURE-ACTIVITY RELATIONSHIP; SUPPRESSION, GENETIC; TYROSINE;

EID: 14044260794     PISSN: 00219258     EISSN: None     Source Type: Journal    
DOI: 10.1074/jbc.M411623200     Document Type: Article

References (71)

1. Lander, E. S., Linton, L. M., Birren, B., Nusbaum, C., Zody, M. C., Baldwin, J., Devon, K., Dewar, K., Doyle, M., FitzHugh, W., Funke, R., Gage, D., Harris, K., Heaford, A., Howland, J., Kann, L., Lehoczky, J., LeVine, R., McEwan, F., McKerman, K., Meldrim, J., Mesirov, J. P., Miranda, C., Morris, W., Naylor, J., Raymond, C., Rosetti, M., Santos, R., Sheridan, A., Sougnez, C., Stange-Thomann, N., Stojanovic, N., Subramanian, A., Wyman, D., Rogers, J., Sulston, J., Ainscough, R., Beck, S., Bentley, D., Burton, J., Clee, C., Carter, N., Coulson, A., Deadman, R., Deloukas, F., Dunham, A., Dunham, I., Durbin, R., French, L., Grafham, D., Gregory, S., Hubbard, T., Humphray, S., Hunt, A., Jones, M., Lloyd, C., McMurray, A., Matthews, L., Mercer, S., Milne, S., Mullikin, J. C., Mungall, A., Plumb, R., Ross, M., Shownkeen, R., Sims, S., Waterston, R. H., Wilson, R. K., Hillier, L. W., McPherson, J. D., Marra, M. A., Mardis, E. R., Fulton, L. A., Chinwalla, A. T., Pepin, K. H., Gish, Chissoe, S. L., Wendl, M. C., Delehaunty, K. D., Miner, T. L., Delehaunty, A., Kramer, J. B., Cook, L. L., Fulton, R. S., Johnson, D. L., Minx, P. J., Clifton, S. W., Hawkins, T., Branscomb, E., Predki, P., Richardson, P., Wenning, S., Slezak, T., Doggett, N., Cheng, J. F., Olsen, A., Lucas, S., Elkin, C., Uberbacher, E., Frazier, M., Gibbs, R. A., Muzny, D. M., Scherer, S. E., Bouck, J. B., Sodergren, E. J., Worley, K. C., Rives, C. M., Gorrell, J. H., Metzker, M. L., Naylor, S. L., Kucherlapati, R. S., Nelson, D. L., Weinstock, G. M., Sakaki, Y., Fujiyama, A., Hattori, M., Yada, T., Toyoda, A., Itoh, T., Kawagoe, C., Watanabe, H., Totoki, Y., Taylor, T., Weissenbach, J., Heilig, R., Saurin, W., Artiguenave, F., Brottier, P., Bruls, T., Pelletier, E., Robert, C., Wincker, P., Smith, D. R., Doucette-Stamm, L., Rubenfield, M., Weinstock, K., Lee, H. M., Dubois, J., Rosenthal, A., Platzer, M., Nyakatura, G., Taudien, S., Rump, A., Yang, H., Yu, J., Wang, J., Huang, G., Gu, J., Hood, L., Rowen, L., Madan, A., Qin, S., Davis, R. W., Federspiel, N. A., Abola, A. P., Proctor, M. J., Myers, R. M., Schmutz, J., Dickson, M., Grimwood, J., Cox, D. R., Olson, M. V., Kaul, R., Raymond, C., Shimizu, N., Kawasaki, K., Minoshima, S., Evans, G. A., Athanasiou, M., Schultz, R., Roe, B. A., Chen, F., Pan, H., Ramser, J., Lehrach, H., Reinhardt, R., McCombie, W. R., de la Bastide, M., Dedhia, N., Blocker, H., Hornischer, K., Nordsiek, G., Agarwala, R., Aravind, L., Bailey, J. A., Bateman, A., Batzoglou, S., Birney, E., Bork, P., Brown, D. G., Burge, C. B., Cerutti, L., Chen, H. C., Church, D., Clamp, M., Copley, R. R., Doerks, T., Eddy, S. R., Eichler, E. E., Furey, T. S., Galagan, J., Gilbert, J. G., Harmon, C., Hayashizaki, Y., Haussler, D., Hermjakob, H., Hokamp, K., Jang, W., Johnson, L. S., Jones, T. A., Kasif, S., Kaspryzk, A., Kennedy, S., Kent, W. J., Kitts, P., Koonin, E. V., Korf, I., Kulp, D., Lancet, D., Lowe, T. M., McLysaght, A., Mikkelsen, T., Moran, J. V., Mulder, N., Pollara, V. J., Ponting, C. P., Schuler, G., Schultz, J., Slater, G., Smit, A. F., Stupka, E., Szustakowski, J., Thierry-Mieg, D., Thierry-Mieg, J., Wagner, L., Wallis, J., Wheeler, R., Williams, A., Wolf, Y. I., Wolfe, K. H., Yang, S. P., Yeh, R. F., Collins, F., Guyer, M. S., Peterson, J., Felsenfeld, A., Wetterstrand, K. A., Patrinos, A., Morgan, M. J., de Jong, P., Catanese, J. J., Osoegawa, K., Shizuya, H., Choi, S., Chen, Y. J., Szustakowki, J., and the International Human Genome Sequencing Consortium (2001) Nature 409, 860-921
2. Venter, J. C., Adams, M. D., Myers, E. W., Li, P. W., Mural, R. J., Sutton, G. G., Smith, H. O., Yandell, M., Evans, C. A., Holt, R. A., Gocayne, J. D., Amanatides, P., Ballew, R. M., Huson, D. H., Wortman, J. R., Zhang, Q., Kodira, C. D., Zheng, X. H., Chen, L. Skupski, M., Subramanian, G., Thomas, P. D., Zhang, J., Miklos, G. L. G., Nelson, C., Broder, S., Clark, A. G., Nadeau, J., McKusick, V. A., Zinder, N., Levine, A. J., Roberts, R. J., Simon, M., Slayman, C., Hunkapiller, M., Bolanos, R., Delcher, A., Dew, I., Fasulo, D., Flanigan, M., Florea, L., Halpern, A., Hannenhalli, S., Kravitz, S., Levy, S., Mobarry, C., Reinert, K., Remington, K., Abu-Threideh, J., Beasley, E., Biddick, K., Bonazzi, V., Brandon, R., Cargill, M., Chandramouliswaran, I., Charlab, R., Chaturvedi, K., Deng, Z., Di Francesco, V., Dunn, P., Eilbeck, K., Evangelista, C., Gabrielian, A. E., Gan, W., Ge, W., Gong, F., Gu, Z., Guan, P., Heiman, T. J., Higgins, M. E., Ji, R.-R., Ke, Z., Ketchum, K. A., Lai, Z., Lei, Y., Li, Z., Li, J., Liang, Y., Lin, X., Lu, F., Merkulov, G. V., Milshina, N., Moore, H. M., Naik, A. K., Narayan, V. A., Neelam, B., Nusskern, D., Rusch, D. B., Salzberg, S., Shao, W., Shue, B., Sun, J., Wang, Z. Y., Wang, A., Wang, X., Wang, J., Wei, M.-H., Wides, R., Xiao, C., Yan, C., Yao, A., Ye, J., Zhan, M., Zhang, W., Zhang, H., Zhao, Q., Zheng, L., Zhong, F., Zhong, W., Zhu, S. C., Zhao, S., Gilbert, D., Baumhueter, S., Spier, G., Carter, C., Cravchik, A., Woodage, T., Ali, F., An, H., Awe, A., Baldwin, D., Baden, H., Barnstead, M., Barrow, I., Beeson, K., Busam, D., Carver, A., Center, A., Cheng, M. L., Curry, L., Danaher, S., Davenport, L., Desuets, R., Dietz, S., Dodson, K., Doup, L., Ferriera, S., Garg, N., Gluecksmann, A., Hart, B., Haynes, J., Haynes, C., Heiner, C., Hladun, S., Hostin, D., Houck, J., Howland, T., Ibegwam, C., Johnson, J., Kalush, F., Kline, L., Koduru, S., Love, A., Mann, F., May, D., McCawley, S., McIntosh, T., McMullen, I., Moy, M., Moy, L., Murphy, B., Nelson, K., Pfannkoch, C., Pratts, E., Puri, V., Qureshi, H., Reardon, M., Rodriguez, R., Rogers, Y.-H., Romblad, D., Ruhfel, B., Scott, R., Sitter, C., Smallwood, M., Stewart, E., Strong, R., Suh, E., Thomas, R., Tint, N. N., Tse, S., Vech, C., Wang, G., Wetter, J., Williams, S., Williams, M., Windsor, S., Winn-Deen, E., Wolfe, K., Zaveri, J., Zaveri, K., Abril, J. F., Guigo, R., Campbell, M. J., Sjolander, K. V., Karlak, B., Kejariwal, A., Mi, H., Lazareva, B., Hatton, T., Narechania, A., Diemer, K., Muruganujan, A., Quo, N., Sato, S., Bafna, V., Istrail, S., Lippert, R., Schwartz, R., Walenz, B., Yooseph, S., Allen, D., Basu, A., Baxendale, J., Blick, L., Caminha, M., Carnes-Stine, J., Caulk, P., Chiang, Y.-H., Coyne, M., Dahlke, C., Mays, A. D., Dombroski, M., Donnelly, M., Ely, D., Esparham, S., Fosler, C., Gire, H., Glanowski, S., Glasser, K., Glodek, A., Gorokhov, M., Graham, K., Gropman, B., Harris, M., Heil, J., Henderson, S., Hoover, J., Jennings, D., Jordan, C., Jordan, J., Kasha, J., Kagan, L., Kraft, C., Levitsky, A., Lewis, M., Liu, X., Lopez, J., Ma, D., Majoros, W., McDaniel, J., Murphy, S., Newman, M., Nguyen, T., Nguyen, N., Nodell, M., Pan, S., Peck, J., Peterson, M., Rowe, W., Sanders, R., Scott, J., Simpson, M., Smith, T., Sprague, A., Stockwell, T., Turner, R., Venter, E., Wang, M., Wen, M., Wu, D., Wu, M., Xia, A., Zandieh, A., and Zhu, X. (2001) Science 291, 1304-1350
3. Takeda, S., Kadowaki, S., Haga, T., Takaesu, H., and Mitaku, S. (2002) FEBS Lett. 520, 97-101
4. Pierce, K. L., Premont, R. T., and Lefkowitz, R. J. (2002) Nat. Rev. Mol. Cell. Biol. 3, 639-650
5. Gether, U. (2000) Endocr. Rev. 21, 90-113
6. Bockaert, J., and Pin, J. P. (1999) EMBO J. 18, 1723-1729
7. Wess, J. (1998) Pharmacol. Ther. 80, 231-264
8. Baldwin, J. M., Schertler, G. F., and Unger, V. M. (1997) J. Mol. Biol. 272, 144-164
9. Palczewski, K., Kumasaka, T., Hori, T., Behnke, C. A., Motoshima, H., Fox, B. A., Le Trong, I., Teller, D. C., Okada, T., Stenkamp, R. E., Yamamoto, M., and Miyano, M. (2000) Science 289, 739-745
10. Teller, D. C., Okada, T., Behnke, C. A., Palczewski, K., and Stenkamp, R. E. (2001) Biochemistry 40, 7761-7772
11. Li, J., Edwards, P. C., Burghammer, M., Villa, C., and Schertler, G. F. (2004) J. Mol. Biol. 343, 1409-1438
12. Ballesteros, J. A., Shi, L., and Javitch, J. A. (2001) Mol. Pharmacol. 60, 1-19
13. Wess, J. (1996) Crit. Rev. Neurobiol. 10, 69-99
14. Erlenbach, I., Kostenis, E., Schmidt, C., Hamdan, F. F., Pausch, M. H., and Wess, J. (2001) J. Neurochem. 77, 1327-1337
15. Schmidt, C., Li, B., Bloodworth, L., Erlenbach, I., Zeng, F. Y., and Wess, J. (2003) J. Biol. Chem. 278, 30248-30260
16. Erlenbach, I., Kostenis, E., Schmidt, C., Serradeil-Le Gal, C., Raufaste, D., Dumont, M. E., Pausch, M. H., and Wess, J. (2001) J. Biol. Chem. 276, 29382-29392
17. Celic, A., Connelly, S. M., Martin, N. P., and Dumont, M. E. (2004) Methods Mol. Biol. 237, 105-120
18. Geva, A., Lassere, T. B, Lichtarge, O., Pollitt, S. K., and Baranski, T. J. (2000) J. Biol. Chem. 275, 35393-35401
19. Baranski, T. J., Herzmark, P., Lichtarge, O., Gerber, B. O., Trueheart, J., Meng, E. C., Iiri, T., Sheikh, S. P., and Bourne, H. R. (1999) J. Biol. Chem. 274, 15757-15765
20. Sommers, C. M., and Dumont, M. E. (1997) J. Mol. Biol. 266, 559-575
21. Konopka, J. B., Margarit, S. M., and Dube, P. (1996) Proc. Natl. Acad. Sci. U. S. A. 93, 6764-6769
22. Stefan, C. J., and Blumer, K. J. (1994) Mol. Cell. Biol. 14, 3339-3349
23. Prioleau, C., Visiers, I., Ebersole, B. J., Weinstein, H., and Sealfon, S. C. (2002) J. Biol. Chem. 277, 36577-36584
24. Ward, R. J., and Milligan, G. (2002) Cell. Signal. 14, 139-144
25. Donnelly, D., Maudsley, S., Gent, J. P., Moser, R. N., Hurrell, C. R., and Findlay, J. B. (1999) Biochem. J. 339, 55-61
26. Sealfon, S., Chi, L., Ebersole, B. J., Rodic, V., Zhang, D., Ballesteros, J. A., and Weinstein, H. (1995) J. Biol. Chem. 270, 16683-16688
27. Zhou, W., Flanagan, C., Ballesteros, J. A., Konvicka, K., Davidson, J. S., Weinstein, H., Millar, R. P., and Sealfon, S. C. (1994) Mol. Pharmacol. 45, 165-170
28. Ballesteros, J. A., and Weinstein, H. (1995) Methods Neurosci. 25, 366-428
29. Chung, F. Z., Wang, C. D., Potter, P. C., Venter, J. C., and Fraser, C. M. (1988) J. Biol. Chem. 263, 4052-4055
30. Strader, C. D., Sigal, I. S., Candelore, M. R., Rands, E., Hill, W. S., and Dixon, R. A. (1988) J. Biol. Chem. 263, 10267-10271
31. Fraser, C. M., Wang, C. D., Robinson, D. A., Gocayne, J. D., and Venter, J. C. (1989) Mol. Pharmacol. 36, 840-847
32. Wang, C. D., Buck, M. A., and Fraser, C. M. (1991) Mol. Pharmacol. 40, 168-179
33. Neve, K. A., Cox, B. A., Henningsen, R. A., Spanoyannis, A., and Neve, R. L. (1991) Mol. Pharmacol. 39, 733-739
34. Ji, I., and Ji, T. H. (1991) J. Biol. Chem. 266, 14953-14957
35. Surprenant, A., Horstman, D. A., Akbarali, H., and Limbird, L. E. (1992) Science 257, 977-980
36. Ho, B. Y., Karschin, A., Branchek, T., Davidson, N., and Lester, H. A. (1992) FEBS Lett. 312, 259-262
37. Bihoreau, C., Monnot, C., Davies, E., Teutsch, B., Bernstein, K. E., Corvol, P., and Clauser, E. (1993) Proc. Natl. Acad. Sci. U. S. A. 90, 5133-5137
38. Nussenzveig, D. R., Heinflink, M., and Gershengorn, M. C. (1993) Mol. Endocrinol. 7, 1105-1111
39. Wang, C. D., Gallaher, T. K., and Shih, J. C. (1993) Mol. Pharmacol. 43, 931-940
40. Rose, P. M., Krystek, S. R., Jr., Patel, P. S., Liu, E. C., Lynch, J. S., Lach, D. A., Fisher, S. M., and Webb, M. L. (1995) FEBS Lett. 361, 243-249
41. Prossnitz, E. R., Schreiber, R. E., Bokoch, G. M., and Ye, R. D. (1995) J. Biol. Chem. 270, 10686-10694
42. Tao, Q., and Abood, M. E. (1998) J. Pharmacol. Exp. Ther. 285, 651-658
43. Fanelli, F., Barbier, P., Zanchetta, D., de Benedetti, P. G., and Chini, B. (1999) Mol. Pharmacol. 56, 214-225
44. Ascoli, M., Fanelli, F., and Segaloff, D. L. (2002) Endocr. Rev. 23, 141-174
45. Schöneberg, T., Liu, J., and Wess, J. (1995) J. Biol. Chem. 270, 18000-18006
46. Maggio, R., Barbier, P., Fornai, F., and Corsini, G. U. (1996) J. Biol. Chem. 271, 31055-31060
47. Zeng, F.-Y., Soldner, A., Schöneberg, T., and Wess, J. (1999) J. Neurochem. 72, 2404-2414
48. Sherman, F. (1991) Methods Enzymol. 194, 3-21
49. Agatep, R., Kirkpatrick, R. D., Parchaliuk, D. L., Woods, R. A., and Gietz, R. D. (1998) Technical Tips Online 1:51:P01525, tto.trends.com
50. Cadwell, R. C., and Joyce, G. F. (1994) PCR Meth. Appl. 3, S136-S140
51. Oldenburg, K. R., Vo, K. T., Michaelis, S., and Paddon, C. (1997) Nucleic Acids Res. 25, 451-452
52. Sommers, C. M., and Dumont, M. E. (1999) in Structure-Function Analysis of G Protein-coupled Receptors (Wess J., ed) pp. 141-166, John Wiley & Sons, New York
53. Berridge, M. J., Dawson, M. C., Downes, C. P., Heslop, J. P., and Irvine, R. F. (1983) Biochem. J. 212, 473-482
54. Mumberg, D., Müller, R., and Funk, M. (1995) Gene (Amst.) 156, 119-122
55. Blüml, K., Mutschler, E., and Wess, J. (1994) J. Biol. Chem. 269, 11537-11541
56. Rath, P., DeCaluwe, L. L., Bovee-Geurts, P. H., DeGrip, W. J., and Rothschild, K. J. (1993) Biochemistry 32, 10277-10282
57. Nagata, T., Terakita, A., Kandori, H., Shichida, Y., and Maeda, A. (1998) Biochemistry 37, 17216-17222
58. Lu, Z. L., Saldanha, J. W., and Hulme, E. C. (2002) Trends Pharmacol. Sci. 23, 140-146
59. Franke, R. R., König, B., Sakmar, T. P., Khorana, H. G., and Hofmann, K., P. (1990) Science 250, 123-125
60. Ernst, O. P., Hofmann, K. P., and Sakmar, T. P. (1995) J. Biol. Chem. 270, 10850-10856
61. Jones, P. G., Curtis, C. A. M., and Hulme, E. C. (1995) Eur. J. Pharmacol. 288, 251-257
62. Nikiforovich, G. V., and Marshall, G. R. (2003) Biochemistry 42, 9110-9120
63. Angers, S., Salahpour, A., and Bouvier, M. (2002) Annu. Rev. Pharmacol. Toxicol. 42, 409-435
64. Javitch, J. A. (2004) Mol. Pharmacol. 66, 1077-1082
65. Zeng, F. Y., and Wess, J. (1999) J. Biol. Chem. 274, 19487-19497
66. Overton, M. C., and Blumer, K. J. (2002) J. Biol. Chem. 277, 41463-41472
67. Liang, Y., Fotiadis, D., Filipek, S., Saperstein, D. A., Palczewski, K., and Engel, A. (2003) J. Biol. Chem. 278, 21655-21662
68. Klco, J. M., Lassere, T. B., and Baranski, T. J. (2003) J. Biol. Chem. 278, 35345-35353
69. Carrillo, J. J., Lopez-Gimenez, J. F., and Milligan, G. (2004) Mol. Pharmacol. 66, 1123-1137
70. Bonner, T. I., Buckley, N. J., Young, A. C., and Brann, M. R. (1987) Science 237, 527-532
71. Cheng, Y., and Prusoff, W.H. (1973) Biochem. Pharmacol. 22, 3099-3108