Alpha-bulges in G protein-coupled receptors

International Journal of Molecular Sciences

Volumn 15, Issue 5, 2014, Pages 7841-7864

  van der Kant, Rob ^a,b   Vriend, Gert ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

^b UNIVERSITY OF LEUVEN   (Belgium)

Author keywords

GPCR; GPCR activation; Random forest; Structure function; bulge; helix

Indexed keywords

ADENOSINE A2A RECEPTOR; BETA 1 ADRENERGIC RECEPTOR; BETA 2 ADRENERGIC RECEPTOR; CHEMOKINE RECEPTOR CCR5; CHEMOKINE RECEPTOR CXCR4; DELTA OPIATE RECEPTOR; DOPAMINE 3 RECEPTOR; G PROTEIN COUPLED RECEPTOR; GUANINE NUCLEOTIDE BINDING PROTEIN; HISTAMINE H1 RECEPTOR; MUSCARINIC M2 RECEPTOR; NEUROTENSIN RECEPTOR; OPSIN; PROTEINASE ACTIVATED RECEPTOR 1; RHODOPSIN; SEROTONIN 1B RECEPTOR; SEROTONIN 2B RECEPTOR; SPHINGOSINE 1 PHOSPHATE RECEPTOR; STRUCTURAL PROTEIN; LIGAND;

ALPHA BULGE; ALPHA HELIX; ARTICLE; DIMERIZATION; LIGAND BINDING; PROLINE RICH PROTEIN DOMAIN; PROTEIN CROSS LINKING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN MOTIF; PROTEIN SECONDARY STRUCTURE; PROTEIN STRUCTURE; PROTEIN SUBUNIT; STRUCTURE ANALYSIS; TERMINAL SEQUENCE; AGONISTS; AMINO ACID SEQUENCE; ANIMAL; CHEMICAL STRUCTURE; CHEMISTRY; DRUG EFFECTS; HUMAN; METABOLISM; MOLECULAR GENETICS;

AMINO ACID SEQUENCE; ANIMALS; HUMANS; LIGANDS; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PROTEIN STRUCTURE, SECONDARY; RECEPTORS, G-PROTEIN-COUPLED;

EID: 84899914806     PISSN: 16616596     EISSN: 14220067     Source Type: Journal    
DOI: 10.3390/ijms15057841     Document Type: Article

References (70)

1. PubMed. Available online: http://www.ncbi.nlm.nih.gov/pubmed (accessed on 19 April 2014).
2. 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., et al. Crystal structure of rhodopsin: A G protein-coupled receptor. Science 2000, 289, 739-745.
3. GPCR Network. Available online: http://gpcr.scripps.edu/ (accessed on 19 April 2014).
4. Kouranov, A., Xie, L., de la Cruz, J., Chen, L., Westbrook, J., Bourne, P.E., Berman, H.M. The RCSB PDB information portal for structural genomics. Nucleic Acids Res. 2006, 34, D302-D305.
5. Vroling, B., Sanders, M., Baakman, C., Borrmann, A., Verhoeven, S., Klomp, J., Oliveira, L., de Vlieg, J., Vriend, G. GPCRDB: Information system for G protein-coupled receptors. Nucleic Acids Res. 2011, 39, D309-D319.
6. Horn, F., Bettler, E., Oliveira, L., Campagne, F., Cohen, F.E., Vriend, G. GPCRDB information system for G protein-coupled receptors. Nucleic Acids Res. 2003, 31, 294-297.
7. Van Durme, J., Horn, F., Costagliola, S., Vriend, G., Vassart, G. GRIS: Glycoprotein-hormone receptor information system. Mol. Endocrinol. 2006, 20, 2247-2255.
8. Oliveira, L., Paiva, A.C., Vriend, G. A low resolution model for the interaction of G proteins with G protein-coupled receptors. Protein Eng. 1999, 12, 1087-1095.
9. Oliveira, L., Hulsen, T., Lutje Hulsik, D., Paiva, A.C., Vriend, G. Heavier-than-air flying machines are impossible. FEBS Lett. 2004, 564, 269-273.
10. Oliveira, L., Paiva, A.C., Sander, C., Vriend, G. A common step for signal transduction in G protein-coupled receptors. Trends Pharmacol. Sci. 1994, 15, 170-172.
11. Rasmussen, S.G., DeVree, B.T., Zou, Y., Kruse, A.C., Chung, K.Y., Kobilka, T.S., Thian, F.S., Chae, P.S., Pardon, E., Calinski, D., et al. Crystal structure of the β2 adrenergic receptor-Gs protein complex. Nature 2011, 477, 549-555.
12. Wacker, D., Fenalti, G., Brown, M.A., Katritch, V., Abagyan, R., Cherezov, V., Stevens, R.C. Conserved binding mode of human β2 adrenergic receptor inverse agonists and antagonist revealed by X-ray crystallography. J. Am. Chem. Soc. 2010, 132, 11443-11445.
13. Chun, E., Thompson, A.A., Liu, W., Roth, C.B., Griffith, M.T., Katritch, V., Kunken, J., Xu, F., Cherezov, V., Hanson, M.A., et al. Fusion partner toolchest for the stabilization and crystallization of G protein-coupled receptors. Structure 2012, 20, 967-976.
14. Lebon, G., Warne, T., Edwards, P.C., Bennett, K., Langmead, C.J., Leslie, A.G., Tate, C.G. Agonist-bound adenosine A2A receptor structures reveal common features of GPCR activation. Nature 2011, 474, 521-525.
15. Rasmussen, S.G., Choi, H.J., Fung, J.J., Pardon, E., Casarosa, P., Chae, P.S., Devree, B.T., Rosenbaum, D.M., Thian, F.S., Kobilka, T.S., et al. Structure of a nanobody-stabilized active state of the β2 adrenoceptor. Nature 2011, 469, 175-180.
16. Warne, T., Serrano-Vega, M.J., Baker, J.G., Moukhametzianov, R., Edwards, P.C., Henderson, R., Leslie, A.G., Tate, C.G., Schertler, G.F. Structure of a β1-adrenergic G protein-coupled receptor. Nature 2008, 454, 486-491.
17. Doré, A.S., Robertson, N., Errey, J.C., Ng, I., Hollenstein, K., Tehan, B., Hurrell, E., Bennett, K., Congreve, M., Magnani, F., et al. Structure of the adenosine A2A receptor in complex with ZM241385 and the xanthines XAC and caffeine. Structure 2011, 19, 1283-1293.
18. Van der Kant RWA., GPCR Activation: What Moves Where?. Available online: http://swift.cmbi.ru.nl/gv/GPCR/ (accessed on 19 April 2014).
19. White, J.F., Noinaj, N., Shibata, Y., Love, J., Kloss, B., Xu, F., Gvozdenovic-Jeremic, J., Shah, P., Shiloach, J., Tate, C.G., et al. Structure of the agonist-bound neurotensin receptor. Nature 2012, 490, 508-513.
20. Mason, J.S., Bortolato, A., Congreve, M., Marshall, F.H. New insights from structural biology into the druggability of G protein-coupled receptors. Trends Pharmacol. Sci. 2012, 33, 249-260.
21. Hino, T., Arakawa, T., Iwanari, H., Yurugi-Kobayashi, T., Ikeda-Suno, C., Nakada-Nakura, Y., Kusano-Arai, O., Weyand, S., Shimamura, T., Nomura, N., et al. G protein-coupled receptor inactivation by an allosteric inverse-agonist antibody. Nature 2012, 482, 237-240.
22. Katritch, V., Reynolds, K.A., Cherezov, V., Hanson, M.A., Roth, C.B., Yeager, M., Abagyan, R. Analysis of full and partial agonists binding to β2-adrenergic receptor suggests a role of transmembrane helix V in agonist-specific conformational changes. J. Mol. Recognit. 2009, 22, 307-318.
23. Rasmussen, S.G., 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., et al. Crystal structure of the human β2 adrenergic G protein-coupled receptor. Nature 2007, 450, 383-387.
24. Rey, J., Deville, J., Chabbert, M. Structural determinants stabilizing helical distortions related to proline. J. Struct. Biol. 2010, 171, 266-276.
25. Van Arnam, E.B., Lester, H.A., Dougherty, D.A. Dissecting the functions of conserved prolines within transmembrane helices of the D2 dopamine receptor. ACS Chem. Biol. 2011, 6, 1063-1068.
26. Cartailler, J.P., Luecke, H. Structural and functional characterization of pi bulges and other short intrahelical deformations. Structure 2004, 12, 133-144.
27. Worth, C.L., Kreuchwig, A., Kleinau, G., Krause, G. GPCR-SSFE: A comprehensive database of G protein-coupled receptor template predictions and homology models. BMC Bioinform. 2011, 12, 185.
28. Deupi, X. Quantification of structural distortions in the transmembrane helices of GPCRs. Methods Mol. Biol. 2012, 914, 219-235.
29. Devillé, J., Rey, J., Chabbert, M. An indel in transmembrane helix 2 helps to Trace the molecular evolution of class A G protein-coupled receptors. J. Mol. Evol. 2009, 68, 475-489.
30. Gonzalez, A., Cordomí, A., Caltabiano, G., Pardo, L. Impact of helix irregularities on sequence alignment and homology modeling of G protein-coupled receptors. Chembiochem 2012, 13, 1393-1399.
31. Isberg, V., Vroling, B., van der Kant, R., Li, K., Vriend, G., Gloriam, D. GPCRDB: An information system for G protein-coupled receptors. Nucleic Acids Res. 2014, 42, D422-D425.
32. Strobl, C., Boulesteix, A.L., Kneib, T., Augustin, T., Zeileis, A. Conditional variable importance for random forests. BMC Bioinform. 2008, 9, 307:1-307:11.
33. Toloşi, L., Lengauer, T. Classification with correlated features: Unreliability of feature ranking and solutions. Bioinformatics 2011, 27, 1986-1994.
34. Hofmann, K.P., Scheerer, P., Hildebrand, P.W., Choe, H.W., Park, J.H., Heck, M., Ernst, O.P. A G protein-coupled receptor at work: The rhodopsin model. Trends Biochem. Sci. 2009, 34, 540-552.
35. Vogel, R., Sakmar, T.P., Sheves, M., Siebert, F. Coupling of protonation switches during rhodopsin activation. Photochem. Photobiol. 2007, 83, 286-292.
36. Fritze, O., Filipek, S., Kuksa, V., Palczewski, K., Hofmann, K.P., Ernst, O.P. Role of the conserved NPxxY(x)5,6F motif in the rhodopsin ground state and during activation. Proc. Natl. Acad. Sci. USA 2003, 100, 2290-2295.
37. Yohannan, S., Faham, S., Yang, D., Whitelegge, J.P., Bowie, J.U. The evolution of transmembrane helix kinks and the structural diversity of G protein-coupled receptors. Proc. Natl. Acad. Sci. USA 2004, 101, 959-963.
38. Ceruso, M.A., Weinstein, H. Structural mimicry of proline kinks: Tertiary packing interactions support local structural distortions. J. Mol. Biol. 2002, 318, 1237-1249.
39. Riek, R.P., Rigoutsos, I., Novotny, J., Graham, R.M. Non-α-helical elements modulate polytopic membrane protein architecture. J. Mol. Biol. 2001, 306, 349-362.
40. Hong, S., Ryu, K.S., Oh, M.S., Ji, I., Ji, T.H. Roles of transmembrane prolines and proline-induced kinks of the lutropin/choriogonadotropin receptor. J. Biol. Chem. 1997, 272, 4166-4171.
41. Geetha, V. Distortions in protein helices. Int. J. Biol. Macromol. 1996, 19, 81-89.
42. Von Heijne, G. Proline kinks in transmembrane α-helices. J. Mol. Biol. 1991, 218, 499-503.
43. Conner, A.C., Hay, D.L., Simms, J., Howitt, S.G., Schindler, M., Smith, D.M., Wheatley, M., Poyner, D.R. A key role for transmembrane prolines in calcitonin receptor-like receptor agonist binding and signalling: Implications for family B G protein-coupled receptors. Mol. Pharmacol. 2005, 67, 20-31.
44. Krieger, E., Vriend, G. Models@Home: Distributed computing in bioinformatics using a screensaver based approach. Bioinformatics 2002, 18, 315-318.
45. 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., et al. Crystal structure of a lipid G protein-coupled receptor. Science 2012, 335, 851-855.
46. Jaakola, V.P., Griffith, M.T., Hanson, M.A., Cherezov, V., Chien, E.Y., Lane, J.R., Ijzerman, A.P., Stevens, R.C. The 2.6 Ångstrom crystal structure of a human A2A adenosine receptor bound to an antagonist. Science 2008, 322, 1211-1217.
47. Murakami, M., Kouyama, T. Crystal structure of squid rhodopsin. Nature 2008, 453, 363-367.
48. Wu, B., Chien, E.Y., Mol, C.D., Fenalti, G., Liu, W., Katritch, V., Abagyan, R., Brooun, A., Wells, P., Bi, F.C., et al. Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science 2010, 330, 1066-1071.
49. Haga, K., Kruse, A.C., Asada, H., Yurugi-Kobayashi, T., Shiroishi, M., Zhang, C., Weis, W.I., Okada, T., Kobilka, B.K., Haga, T., et al. Structure of the human M2 muscarinic acetylcholine receptor bound to an antagonist. Nature 2012, 482, 547-551.
50. Park, J.H., Scheerer, P., Hofmann, K.P., Choe, H.W., Ernst, O.P. Crystal structure of the ligand-free G protein-coupled receptor opsin. Nature 2008, 454, 183-187.
51. Granier, S., Manglik, A., Kruse, A.C., Kobilka, T.S., Thian, F.S., Weis, W.I., Kobilka, B.K. Structure of the δ-opioid receptor bound to naltrindole. Nature 2012, 485, 400-404.
52. Chien, E.Y., Liu, W., Zhao, Q., Katritch, V., Han, G.W., Hanson, M.A., Shi, L., Newman, A.H., Javitch, J.A., Cherezov, V., et al. Structure of the human dopamine D3 receptor in complex with a D2/D3 selective antagonist. Science 2010, 330, 1091-1095.
53. Schwartz, T.W., Frimurer, T.M., Holst, B., Rosenkilde, M.M., Elling, C.E. Molecular mechanism of 7TM receptor activation-A global toggle switch model. Annu. Rev. Pharmacol. Toxicol. 2006, 46, 481-519.
54. 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., et al. Discovery of 1,2,4-triazine derivatives as adenosine A2A antagonists using structure based drug design. J. Med. Chem. 2012, 55, 1898-1903.
55. Xu, F., Wu, H., Katritch, V., Han, G.W., Jacobson, K.A., Gao, Z.G., Cherezov, V., Stevens, R.C. Structure of an agonist-bound human A2A adenosine receptor. Science 2011, 332, 322-327.
56. Cherezov, V., Rosenbaum, D.M., Hanson, M.A., Rasmussen, S.G., Thian, F.S., Kobilka, T.S., Choi, H.J., Kuhn, P., Weis, W.I., Kobilka, B.K., et al. High-resolution crystal structure of an engineered human β2-adrenergic G protein-coupled receptor. Science 2007, 318, 1258-1265.
57. Hanson, M.A., Cherezov, V., Griffith, M.T., Roth, C.B., Jaakola, V.P., Chien, E.Y., Velasquez, J., Kuhn, P., Stevens, R.C. A specific cholesterol binding site is established by the 2.8 Å structure of the human β2-adrenergic receptor. Structure 2008, 16, 897-905.
58. Berman, H.M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T.N., Weissig, H., Shindyalov, I.N., Bourne, P.E. The protein data bank. Nucleic Acids Res. 2000, 28, 235-242.
59. Oliveira, L., Paiva, A.C.M., Vriend, G. A common motif in G protein-coupled seven transmembrane helix receptors. J. Comput-Aided Mol. Des. 1993, 7, 649-658.
60. Vroling, B., Thorne, D., McDermott, P., Attwood, T.K., Vriend, G., Pettifer, S. Integrating GPCR-specific information with full text articles. BMC Bioinform. 2011, 12, 362:1-362:10.
61. GPCRDB. Available online: http://www.gpcr.org/7tm/ (accessed on 19 April 2014).
62. Konagurthu, A.S., Whisstock, J.C., Stuckey, P.J., Lesk, A.M. MUSTANG: A multiple structural alignment algorithm. Proteins Struct. Funct. Bioinform. 2006, 64, 559-574.
63. Vriend, G. WHAT IF: A molecular modelling and drug design program. J. Mol. Graph. 1990, 8, 52-56.
64. Vriend, G., Sander, C. Detection of common three-dimensional substructures in proteins. Proteins 1991, 11, 52-58.
65. Liaw, A., Wiener, M. Classification and regression by randomForest. R News 2002, 2, 18-22.
66. R Development Core Team. R: A Language and Environment for Statistical Computing, R Foundation for Statistical Computing: Vienna, Austria, 2008. Available online: http://www. R-project.org (accessed on 19 April 2014).
67. Kabsch, W., Sander, C. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 1983, 22, 2577-2637.
68. Joosten, R.P., te Beek, T.A., Krieger, E., Hekkelman, M.L., Hooft, R.W., Schneider, R., Sander, C., Vriend, G. A series of PDB related databases for everyday needs. Nucleic Acids Res. 2011, 39, D411-D419.
69. CMBI Protein Structure Bioinformatics Facilities. Available online: http://swift.cmbi.ru.nl/gv/ facilities/ (accessed on 19 April 2014).
70. Index of Software DSSP. Available online: http://www.ftp.cmbi.ru.nl/pub/software/dssp/ (accessed on 19 April 2014).