Identifying G protein-coupled receptor dimers from crystal packings

Acta Crystallographica Section D: Structural Biology

Volumn 74, Issue 7, 2018, Pages 655-670

  Stenkamp, Ronald E ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

Crystal packing interactions; Dimers; G protein coupled receptors; GPCRs

Indexed keywords

G PROTEIN COUPLED RECEPTOR;

ANIMAL; CHEMISTRY; HUMAN; MOLECULAR MODEL; PROTEIN MULTIMERIZATION; X RAY CRYSTALLOGRAPHY;

ANIMALS; CRYSTALLOGRAPHY, X-RAY; HUMANS; MODELS, MOLECULAR; PROTEIN MULTIMERIZATION; RECEPTORS, G-PROTEIN-COUPLED;

EID: 85049448496     PISSN: None     EISSN: 20597983     Source Type: Journal    
DOI: 10.1107/S2059798318008136     Document Type: Article

References (128)

1. Baltoumas, F. A., Theodoropoulou, M. C. & Hamodrakas, S. J. (2016). J. Comput. Aided Mol. Des. 30, 489-512.
2. Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T. N., Weissig, H., Shindyalov, I. N. & Bourne, P. E. (2000). Nucleic Acids Res. 28, 235-242.
3. Blankenship, E., Vahedi-Faridi, A. & Lodowski, D. T. (2015). Structure, 23, 2358-2364.
4. Burg, J. S., Ingram, J. R., Venkatakrishnan, A. J., Jude, K. M., Dukkipati, A., Feinberg, E. N., Angelini, A., Waghray, D., Dror, R. O., Ploegh, H. L. & Garcia, K. C. (2015). Science, 347, 1113-1117.
5. Byrne, E. F. X., Sircar, R., Miller, P. S., Hedger, G., Luchetti, G., Nachtergaele, S., Tully, M. D., Mydock-McGrane, L., Covey, D. F., Rambo, R. P., Sansom, M. S. P., Newstead, S., Rohatgi, R. & Siebold, C. (2016). Nature (London), 535, 517-522.
6. Carpenter, B., Nehmé, R., Warne, T., Leslie, A. G. W. & Tate, C. G. (2016). Nature (London), 536, 104-107.
7. Cheng, R. K. Y., Fiez-Vandal, C. et al. (2017). Nature (London), 545, 112-115.
8. Cheng, R. K. Y., Segala, E., Robertson, N., Deflorian, F., Doré, A. S., Errey, J. C., Fiez-Vandal, C., Marshall, F. H. & Cooke, R. M. (2017). Structure, 25, 1275-1285.
9. Cherezov, V., Rosenbaum, D. M., Hanson, M. A., Rasmussen, S. G. F., Thian, F. S., Kobilka, T. S., Choi, H.-J., Kuhn, P., Weis, W. I., Kobilka, B. K. & Stevens, R. C. (2007). Science, 318, 1258-1265.
10. Chien, E. Y. T., Liu, W., Zhao, Q., Katritch, V., Won Han, G., Hanson, M. A., Shi, L., Newman, A. H., Javitch, J. A., Cherezov, V. & Stevens, R. C. (2010). Science, 330, 1091-1095.
11. Chrencik, J. E. et al. (2015). Cell, 161, 1633-1643.
12. Congreve, M., Andrews, S. P., Doré, A. S., Hollenstein, K., Hurrell, E., Langmead, C. J., Mason, J. S., Ng, I. W., Tehan, B., Zhukov, A., Weir, M. & Marshall, F. H. (2012). J. Med. Chem. 55, 1898-1903.
13. Doré, A. S., Bortolato, A., Hollenstein, K., Cheng, R. K. Y., Read, R. J. & Marshall, F. H. (2017). Curr. Mol. Pharmacol. 10, 334-344.
14. Doré, A. S., Okrasa, K., Patel, J. C., Serrano-Vega, M., Bennett, K., Cooke, R. M., Errey, J. C., Jazayeri, A., Khan, S., Tehan, B., Weir, M., Wiggin, G. R. & Marshall, F. H. (2014). Nature (London), 511, 557-562.
15. Duarte, J. M., Biyani, N., Baskaran, K. & Capitani, G. (2013). BMC Struct. Biol. 13, 21.
16. Duarte, J. M., Srebniak, A., Schärer, M. A. & Capitani, G. (2012). BMC Bioinformatics, 13, 334.
17. Egloff, P., Hillenbrand, M., Klenk, C., Batyuk, A., Heine, P., Balada, S., Schlinkmann, K. M., Scott, D. J., Schütz, M. & Plückthun, A. (2014). Proc. Natl Acad. Sci. USA, 111, E655-E662.
18. Emsley, P., Lohkamp, B., Scott, W. G. & Cowtan, K. (2010). Acta Cryst. D66, 486-501.
19. Farran, B. (2017). Pharmacol. Res. 117, 303-327.
20. Fenalti, G., Giguere, P. M., Katritch, V., Huang, X.-P., Thompson, A. A., Cherezov, V., Roth, B. L. & Stevens, R. C. (2014). Nature (London), 506, 191-196.
21. Fenalti, G. et al. (2015). Nature Struct. Mol. Biol. 22, 265-268.
22. Ferré, S., Casadó, V., Devi, L. A., Filizola, M., Jockers, R., Lohse, M. J., Milligan, G., Pin, J.-P. & Guitart, X. (2014). Pharmacol. Rev. 66, 413-434.
23. Filipek, S., Krzysko, K. A., Fotiadis, D., Liang, Y., Saperstein, D. A., Engel, A. & Palczewski, K. (2004). Photochem. Photobiol. Sci. 3, 628-638.
24. Fotiadis, D., Jastrzebska, B., Philippsen, A., Müller, D. J., Palczewski, K. & Engel, A. (2006). Curr. Opin. Struct. Biol. 16, 252-259.
25. Fotiadis, D., Liang, Y., Filipek, S., Saperstein, D. A., Engel, A. & Palczewski, K. (2003). Nature (London), 421, 127-128.
26. Gahbauer, S. & Böckmann, R. A. (2016). Front. Physiol. 7, 494.
27. Glukhova, A., Thal, D. M., Nguyen, A. T., Vecchio, E. A., Jörg, M., Scammells, P. J., May, L. T., Sexton, P. M. & Christopoulos, A. (2017). Cell, 168, 867-877.
28. Granier, S., Manglik, A., Kruse, A. C., Kobilka, T. S., Thian, F. S., Weis, W. I. & Kobilka, B. K. (2012). Nature (London), 485, 400-404.
29. Gulati, S., Jastrzebska, B., Banerjee, S., Placeres, A. L., Miszta, P., Gao, S., Gunderson, K., Tochtrop, G. P., Filipek, S., Katayama, K., Kiser, P. D., Mogi, M., Stewart, P. L. & Palczewski, K. (2017). Proc. Natl Acad. Sci. USA, 114, E2608-E2615.
30. Haga, K., Kruse, A. C., Asada, H., Yurugi-Kobayashi, T., Shiroishi, M., Zhang, C., Weis, W. I., Okada, T., Kobilka, B. K., Haga, T. & Kobayashi, T. (2012). Nature (London), 482, 547-551.
31. Hanson, M. A., Roth, C. B., Jo, E., Griffith, M. T., Scott, F. L., Reinhart, G., Desale, H., Clemons, B., Cahalan, S. M., Schuerer, S. C., Sanna, M. G., Han, G. W., Kuhn, P., Rosen, H. & Stevens, R. C. (2012). Science, 335, 851-855.
32. Hino, T., Arakawa, T., Iwanari, H., Yurugi-Kobayashi, T., Ikeda-Suno, C., Nakada-Nakura, Y., Kusano-Arai, O., Weyand, S., Shimamura, T., Nomura, N., Cameron, A. D., Kobayashi, T., Hamakubo, T., Iwata, S. & Murata, T. (2012). Nature (London), 482, 237-240.
33. Hollenstein, K., Kean, J., Bortolato, A., Cheng, R. K. Y., Doré, A. S., Jazayeri, A., Cooke, R. M., Weir, M. & Marshall, F. H. (2013). Nature (London), 499, 438-443.
34. Hua, T. et al. (2016). Cell, 167, 750-762.
35. Hua, T. et al. (2017). Nature (London), 547, 468-471.
36. Huang, J., Chen, S., Zhang, J. J. & Huang, X.-Y. (2013). Nature Struct. Mol. Biol. 20, 419-425.
37. Huang, W. et al. (2015). Nature (London), 524, 315-321.
38. Isberg, V., Mordalski, S., Munk, C., Rataj, K., Harpsøe, K., Hauser, A. S., Vroling, B., Bojarski, A. J., Vriend, G. & Gloriam, D. E. (2016). Nucleic Acids. Res. 44, D356-D364.
39. Ishchenko, A., Wacker, D., Kapoor, M., Zhang, A., Han, G. W., Basu, S., Patel, N., Messerschmidt, M., Weierstall, U., Liu, W., Katritch, V., Roth, B. L., Stevens, R. C. & Cherezov, V. (2017). Proc. Natl Acad. Sci. USA, 114, 8223-8228.
40. Jaakola, V.-P., Griffith, M. T., Hanson, M. A., Cherezov, V., Chien, E. Y. T., Lane, J. R., Ijzerman, A. P. & Stevens, R. C. (2008). Science, 322, 1211-1217.
41. Janin, J. (1997). Nature Struct. Biol. 4, 973-974.
42. Jastrzebska, B., Comar, W. D., Kaliszewski, M. J., Skinner, K. C., Torcasio, M. H., Esway, A. S., Jin, H., Palczewski, K. & Smith, A.W. (2017). Biochemistry, 56, 61-72.
43. Jastrzebska, B., Ringler, P., Lodowski, D. T., Moiseenkova-Bell, V., Golczak, M., Müller, S. A., Palczewski, K. & Engel, A. (2011). J. Struct. Biol. 176, 387-394.
44. Jastrzebska, B., Ringler, P., Palczewski, K. & Engel, A. (2013). J. Struct. Biol. 182, 164-172.
45. Jazayeri, A. et al. (2016). Nature (London), 533, 274-277.
46. Jazayeri, A. et al. (2017). Nature (London), 546, 254-258.
47. Kasai, R. S. & Kusumi, A. (2014). Curr. Opin. Cell Biol. 27, 78-86.
48. Katritch, V., Cherezov, V. & Stevens, R. C. (2013). Annu. Rev. Pharmacol. Toxicol. 53, 531-556.
49. Kraulis, P. J. (1991). J. Appl. Cryst. 24, 946-950.
50. Krissinel, E. & Henrick, K. (2004). Acta Cryst. D60, 2256-2268.
51. Krumm, B. E., Lee, S., Bhattacharya, S., Botos, I., White, C. F., Du, H., Vaidehi, N. & Grisshammer, R. (2016). Sci. Rep. 6, 38564.
52. Krumm, B. E., White, J. F., Shah, P. & Grisshammer, R. (2015). Nature Commun. 6, 7895.
53. Kruse, A. C., Hu, J., Pan, A. C., Arlow, D. H., Rosenbaum, D. M., Rosemond, E., Green, H. F., Liu, T., Chae, P. S., Dror, R. O., Shaw, D. E., Weis, W. I., Wess, J. & Kobilka, B. K. (2012). Nature (London), 482, 552-556.
54. Lebon, G., Edwards, P. C., Leslie, A. G. W. & Tate, C. G. (2015). Mol. Pharmacol. 87, 907-915.
55. Lebon, G., Warne, T., Edwards, P. C., Bennett, K., Langmead, C. J., Leslie, A. G. W. & Tate, C. G. (2011). Nature (London), 474, 521-525.
56. Lee, B. & Richards, F. M. (1971). J. Mol. Biol. 55, 379-400.
57. Leslie, A. G. W., Warne, T. & Tate, C. G. (2015). Nature Struct. Mol. Biol. 22, 941-942.
58. Liang, Y., Fotiadis, D., Filipek, S., Saperstein, D. A., Palczewski, K. & Engel, A. (2003). J. Biol. Chem. 278, 21655-21662.
59. Liu, X., Ahn, S., Kahsai, A. W., Meng, K.-C., Latorraca, N. R., Pani, B., Venkatakrishnan, A. J., Masoudi, A., Weis, W. I., Dror, R. O., Chen, X., Lefkowitz, R. J. & Kobilka, B. (2017). Nature (London), 548, 480-484.
60. Lu, J. et al. (2017). Nature Struct. Mol. Biol. 24, 570-577.
61. Ma, Y. et al. (2017). Structure, 25, 858-866.e4.
62. Manglik, A., Kruse, A. C., Kobilka, T. S., Thian, F. S., Mathiesen, J. M., Sunahara, R. K., Pardo, L., Weis, W. I., Kobilka, B. K. & Granier, S. (2012). Nature (London), 485, 321-326.
63. McRee, D. E. (1999). J. Struct. Biol. 125, 156-165.
64. Merritt, E. A. & Bacon, D. J. (1997). Methods Enzymol. 277, 505-524.
65. Miller, R. L., Thompson, A. A., Trapella, C., Guerrini, R., Malfacini, D., Patel, N., Han, G. W., Cherezov, V., Caló, G., Katritch, V. & Stevens, R. C. (2015). Structure, 23, 2291-2299.
66. Miller-Gallacher, J. L., Nehmé, R., Warne, T., Edwards, P. C., Schertler, G. F. X., Leslie, A. G.W. & Tate, C. G. (2014). PLoS One, 9, e92727.
67. Moukhametzianov, R., Warne, T., Edwards, P. C., Serrano-Vega, M. J., Leslie, A. G. W., Tate, C. G. & Schertler, G. F. (2011). Proc. Natl Acad. Sci. USA, 108, 8228-8232.
68. Murakami, M. & Kouyama, T. (2008). Nature (London), 453, 363-367.
69. Okada, T. (2012). PLoS One, 7, e35802.
70. Okada, T., Sugihara, M., Bondar, A.-N., Elstner, M., Entel, P. & Buss, V. (2004). J. Mol. Biol. 342, 571-583.
71. Oswald, C., Rappas, M., Kean, J., Doré, A. S., Errey, J. C., Bennett, K., Deflorian, F., Christopher, J. A., Jazayeri, A., Mason, J. S., Congreve, M., Cooke, R. M. & Marshall, F. H. (2016). Nature (London), 540, 462-465.
72. 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. & Miyano, M. (2000). Science, 289, 739-745.
73. Palczewski, K. & Orban, T. (2013). Annu. Rev. Neurosci. 36, 139-164.
74. Piscitelli, C. L., Kean, J., de Graaf, C. & Deupi, X. (2015). Mol. Pharmacol. 88, 536-551.
75. Qin, L., Kufareva, I., Holden, L. G., Wang, C., Zheng, Y., Zhao, C., Fenalti, G., Wu, H., Han, G.W., Cherezov, V., Abagyan, R., Stevens, R. C. & Handel, T. M. (2015). Science, 347, 1117-1122.
76. Rasmussen, S. G. F., Choi, H.-J. et al. (2011). Nature (London), 469, 175-180.
77. Rasmussen, S. G. F., Choi, H. J., Rosenbaum, D. M., Kobilka, T. S., Thian, F. S., Edwards, P. C., Burghammer, M., Ratnala, V. R., Sanishvili, R., Fischetti, R. F., Schertler, G. F., Weis, W. I. & Kobilka, B. K. (2007). Nature (London), 450, 383-387.
78. Rasmussen, S. G. F., DeVree, B. T. et al. (2011). Nature (London), 477, 549-555.
79. Ring, A. M., Manglik, A., Kruse, A. C., Enos, M. D., Weis, W. I., Garcia, K. C. & Kobilka, B. K. (2013). Nature (London), 502, 575-579.
80. Rosenbaum, D. M. et al. (2011). Nature (London), 469, 236-240.
81. Saff, E. B. & Kuijlaars, A. B. J. (1997). Math. Intell. 19, 5-11.
82. Salom, D., Lodowski, D. T., Stenkamp, R. E., Le Trong, I., Golczak, M., Jastrzebska, B., Harris, T., Ballesteros, J. A. & Palczewski, K. (2006). Proc. Natl Acad. Sci. USA, 103, 16123-16128.
83. Sato, T., Kawasaki, T., Mine, S. & Matsumura, H. (2016). Int. J. Mol. Sci. 17, 1930.
84. Shao, Z., Yin, J., Chapman, K., Grzemska, M., Clark, L., Wang, J. & Rosenbaum, D. M. (2016). Nature (London), 540, 602-606.
85. Shihoya, W., Nishizawa, T., Okuta, A., Tani, K., Dohmae, N., Fujiyoshi, Y., Nureki, O. & Doi, T. (2016). Nature (London), 537, 363-368.
86. Shihoya, W., Nishizawa, T., Yamashita, K., Inoue, A., Hirata, K., Kadji, F.M. N., Okuta, A., Tani, K., Aoki, J., Fujiyoshi, Y., Doi, T. & Nureki, O. (2017). Nature Struct. Mol. Biol. 24, 758-764.
87. Shimamura, T., Hiraki, K., Takahashi, N., Hori, T., Ago, H., Masuda, K., Takio, K., Ishiguro, M. & Miyano, M. (2008). J. Biol. Chem. 283, 17753-17756.
88. Shimamura, T., Shiroishi, M., Weyand, S., Tsujimoto, H., Winter, G., Katritch, V., Abagyan, R., Cherezov, V., Liu, W., Han, G. W., Kobayashi, T., Stevens, R. C. & Iwata, S. (2011). Nature (London), 475, 65-70.
89. Siu, F. Y. et al. (2013). Nature (London), 499, 444-449.
90. Song, G. et al. (2017). Nature (London), 546, 312-315.
91. Staus, D. P. et al. (2016). Nature (London), 535, 448-452.
92. Stenkamp, R. E. (2008). Acta Cryst. D64, 902-904.
93. Sun, B., Bachhawat, P., Chu, M. L.-H., Wood, M., Ceska, T., Sands, Z. A., Mercier, J., Lebon, F., Kobilka, T. S. & Kobilka, B. K. (2017). Proc. Natl Acad. Sci. USA, 114, 2066-2071.
94. Tan, Q. et al. (2013). Science, 341, 1387-1390.
95. Taniguchi, R. et al. (2017). Nature (London), 548, 356-360.
96. Thal, D. M., Sun, B., Feng, D., Nawaratne, V., Leach, K., Felder, C. C., Bures, M. G., Evans, D. A., Weis, W. I., Bachhawat, P., Kobilka, T. S., Sexton, P. M., Kobilka, B. K. & Christopoulos, A. (2016). Nature (London), 531, 335-340.
97. Thorsen, T. S., Matt, R., Weis, W. I. & Kobilka, B. K. (2014). Structure, 22, 1657-1664.
98. Tian, H., Fürstenberg, A. & Huber, T. (2017). Chem. Rev. 117, 186-245.
99. Vischer, H. F., Castro, M. & Pin, J.-P. (2015). Mol. Pharmacol. 88, 561-571.
100. Wacker, D., Wang, C., Katritch, V., Han, G. W., Huang, X. P., Vardy, E., McCorvy, J. D., Jiang, Y., Chu, M., Siu, F. Y., Liu, W., Xu, H. E., Cherezov, V., Roth, B. L. & Stevens, R. C. (2013). Science, 340, 615-619.
101. Wang, C., Jiang, Y. et al. (2013). Science, 340, 610-614.
102. Wang, C., Wu, H., Evron, T., Vardy, E., Han, G. W., Huang, X.-P., Hufeisen, S. J., Mangano, T. J., Urban, D. J., Katritch, V., Cherezov, V., Caron, M. G., Roth, B. L. & Stevens, R. C. (2014). Nature Commun. 5, 4355.
103. Wang, C., Wu, H., Katritch, V., Han, G. W., Huang, X.-P., Liu, W., Siu, F. Y., Roth, B. L., Cherezov, V. & Stevens, R. C. (2013). Nature (London), 497, 338-343.
104. Wang, S., Wacker, D., Levit, A., Che, T., Betz, R. M., McCorvy, J. D., Venkatakrishnan, A. J., Huang, X.-P., Dror, R. O., Shoichet, B. K. & Roth, B. L. (2017). Science, 358, 381-386.
105. Warne, T., Edwards, P. C., Leslie, A. G. W. & Tate, C. G. (2012). Structure, 20, 841-849.
106. Warne, T., Serrano-Vega, M. J., Baker, J. G., Moukhametzianov, R., Edwards, P. C., Henderson, R., Leslie, A. G. W., Tate, C. G. & Schertler, G. F. (2008). Nature (London), 454, 486-491.
107. Weierstall, U. et al. (2014). Nature Commun. 5, 3309.
108. Weinert, T. et al. (2017). Nature Commun. 8, 542.
109. White, J. F., Noinaj, N., Shibata, Y., Love, J., Kloss, B., Xu, F., Gvozdenovic Jeremic, J., Shah, P., Shiloach, J., Tate, C. G. & Grisshammer, R. (2012). Nature (London), 490, 508-513.
110. Winn, M. D. et al. (2011). Acta Cryst. D67, 235-242.
111. Wu, B., Chien, E. Y. T., Mol, C. D., Fenalti, G., Liu, W., Katritch, V., Abagyan, R., Brooun, A., Wells, P., Bi, F. C., Hamel, D. J., Kuhn, P., Handel, T. M., Cherezov, V. & Stevens, R. C. (2010). Science, 330, 1066-1071.
112. Wu, H. et al. (2012). Nature (London), 485, 327-332.
113. Wu, H., Wang, C., Gregory, K. J., Han, G. W., Cho, H. P., Xia, Y., Niswender, C. M., Katritch, V., Meiler, J., Cherezov, V., Conn, P. J. & Stevens, R. C. (2014). Science, 344, 58-64.
114. Yin, J., Babaoglu, K., Brautigam, C. A., Clark, L., Shao, Z., Scheuermann, T. H., Harrell, C. M., Gotter, A. L., Roecker, A. J., Winrow, C. J., Renger, J. J., Coleman, P. J. & Rosenbaum, D. M. (2016). Nature Struct. Mol. Biol. 23, 293-299.
115. Yin, J., Mobarec, J. C., Kolb, P. & Rosenbaum, D. M. (2015). Nature (London), 519, 247-250.
116. Zhang, C., Srinivasan, Y., Arlow, D. H., Fung, J. J., Palmer, D., Zheng, Y., Green, H. F., Pandey, A., Dror, R. O., Shaw, D. E., Weis, W. I., Coughlin, S. R. & Kobilka, B. K. (2012). Nature (London), 492, 387-392.
117. Zhang, D., Gao, Z.-G. et al. (2015). Nature (London), 520, 317-321.
118. Zhang, H., Han, G. W. et al. (2017). Nature (London), 544, 327-332.
119. Zhang, H., Qiao, A. et al. (2017). Nature (London), 546, 259-264.
120. Zhang, H., Unal, H., Desnoyer, R., Han, G.W., Patel, N., Katritch, V., Karnik, S. S., Cherezov, V. & Stevens, R. C. (2015). J. Biol. Chem. 290, 29127-29139.
121. Zhang, H., Unal, H., Gati, C. et al. (2015). Cell, 161, 833-844.
122. Zhang, J., Zhang, K., Gao, Z.-G., Paoletta, S. et al. (2014). Nature (London), 509, 119-122.
123. Zhang, K., Zhang, J., Gao, Z.-G., Zhang, D. et al. (2014). Nature (London), 509, 115-118.
124. Zhang, X., Zhao, F. et al. (2017). Nature Commun. 8, 15383.
125. Zheng, Y., Han, G.W., Abagyan, R., Wu, B., Stevens, R. C., Cherezov, V., Kufareva, I. & Handel, T. M. (2017). Immunity, 46, 1005-1017.
126. Zheng, Y. et al. (2016). Nature (London), 540, 458-461.
127. Zhou, X. E. et al. (2017). Cell, 170, 457-469.
128. Zou, Y., Weis, W. I. & Kobilka, B. K. (2012). PLoS One, 7, e46039.