Structure modeling of the chemokine receptor CCR5: Implications for ligand binding and selectivity

Biophysical Journal

Volumn 83, Issue 6, 2002, Pages 3012-3031

  Paterlini, M Germana ^a,b  

^a UNIVERSITY OF MINNESOTA   (United States)

^b Certusoft Inc   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOKINE; CHEMOKINE RECEPTOR CCR1; CHEMOKINE RECEPTOR CCR2; CHEMOKINE RECEPTOR CCR5; DOCKING PROTEIN; EPITOPE; N [4 [[[6,7 DIHYDRO 2 (4 METHYLPHENYL) 5H BENZOCYCLOHEPTEN 8 YL]CARBONYL]AMINO]BENZYL] N,N DIMETHYL 2H TETRAHYDROPYRAN 4 AMINIUM CHLORIDE;

AMINO ACID SEQUENCE; ARTICLE; CONTROLLED STUDY; HUMAN IMMUNODEFICIENCY VIRUS 1; LIGAND BINDING; NONHUMAN; PROTEIN DOMAIN; PROTEIN STRUCTURE; SIMULATION;

HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1; RNA VIRUSES; RUMEX;

EID: 0036923938     PISSN: 00063495     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0006-3495(02)75307-1     Document Type: Article

References (94)

1. Altschul, S. F., T. L. Madden, A. A. Schaffer. J. Zhang, Z. Zhang, W. Miller, and D. J. Lipman. 1997. Gapped BLAST and PSI-BLAST: A new generation of protein database search programs. Nucleic Acids Res. 25:3389-3402.
2. Attwood, T. K., and J. B. C. Findlay. 1994. Fingerprinting G-protein coupled receptors. Protein Eng. 7:195-203.
3. Baba, M., O. Nishimura, N. Kanzaki, M. Okamoto, H. Sawada, Y. Iizawa, M. Shiraishi, Y. Aramaki, K. Okonogi, Y. Ogawa, K. Meguro, and M. Fujino. 1999. A small-molecule, nonpeptide CCR5 antagonist with highly potent and selective anti-HIV-1 activity. Proc. Natl. Acad. Sci. USA. 96:5698-5703.
4. Bairoch, A., and R. Apweiler. 2000. The SWISS-PROT protein sequence database and its supplement TrEMBL. Nucleic Acids Res. 28:45-48.
5. Baldwin, J. M., G. F. Schertler, and V. M. Unger. 1997. An alpha-carbon template for the transmembrane helices in the rhodopsin family of G-protein-coupled receptors. J. Mol. Biol. 272:144-164.
6. Ballesteros, J., S. Kitanovic, F. Guarnieri, P. Davies, B. J. Fromme, K. Konvicka, L. Chi, R. P. Millar, J. S. Davidson, H. Weinstein, and S. C. Sealfon. 1998. Functional microdomains in G-protein-coupled receptors. The conserved arginine-cage motif in the gonadotropin-releasing hormone receptor. J. Biol. Chem. 273:10445-10453.
7. Ballesteros, J. A., and H. Weinstein. 1995. Integrated methods for the construction of three dimensional models and computational probing of structure-function relations in G-protein coupled receptors. Methods Neurosci. 25:366-428.
8. Bayly, C. I., P. Cieplak, W. D. Cornell, and P. A. Kollman. 1993. A well-behaved electrostatic potential based method using charge restraints for determining atom-centered charges: The RESP model. J. Phys. Chem. 97:10269.
9. Befort, K., L. Tabarra, D. Kling, B. Maigret, and B. L. Kieffer. 1996. Role of aromatic transmembrane residues of the delta-opioid receptor in ligand recognition. J. Biol. Chem. 271:10161-10168.
10. Berger, E. A., R. W. Doms, E. M. Fenyo, B. T. Korber, D. R. Littman, J. P. Moore, Q. J. Sattentau, H. Schuitemaker, J. Sodroski, and R. A. Weiss. 1998. A new classification for HIV-1. Nature. 391:240.
11. Berman, H. M., J. Westbrook, Z. Feng, G. Gilliland, T. N. Bhat, H. Weissig, I. N. Shindyalov, and P. E. Bourne. 2000. The Protein Data Bank. Nucleic Acids Res. 28:235-242.
12. Blanpain, C., B. J. Doranz, J. Vakili, J. Rucker, C. Govaerts, S. S. Baik, O. Lorthioir, I. Migeotte, F. Libert, F. Baleux, G. Vassart, R. W. Doms, and M. Parmentier. 1999a. Multiple charged and aromatic residues in CCR5 amino-terminal domain are involved in high affinity binding of both chemokines and HIV-1 Env protein. J. Biol. Chem. 274:34719-34727.
13. Blanpain, C., B. Lee, J. Vakili, B. J. Doranz, C. Govaerts, I. Migeotte, M. Sharron, V. Dupriez, G. Vassart, R. W. Doms, and M. Parmentier. 1999b. Extracellular cysteines of CCR5 are required for chemokine binding, but dispensable for HIV-1 coreceptor activity. J. Biol. Chem. 274:18902-18908.
14. Burritt, J. B., S. C. Busse, D. Gizachew, D. W. Siemsen, M. T. Quinn, C. W. Bond, E. A. Dratz, and A. J. Jesaitis. 1998. Antibody imprint of a membrane protein surface. Phagocyte flavocytochrome b. J. Biol. Chem. 273:24847-24852.
15. Case, D. A., D. A. Pearlman, T. E. Caldwell, T. E. Cheatham III., W. S. Ross, C. L. Simmerling, T. A. Darden, K. M. Metz, R. V. Stanton, A. L. Cheng, J. J. Vincent, M. Crowley, D. M. Ferguson, R. J. Radmer, G. L. Deibel, U. C. Singh, P. K. Weiner, and P. A. Kollman. 1995. AMBER 5. University of California, San Francisco.
16. Cornell, W. D., P. Cieplak, C. I. Bayly, I. R. Gould, K. M. Metz, Jr., D. M. Ferguson, D. C. Spellmeyer, T. Fox, J. W. Caldwell, and P. A. Kollman. 1995. A second generation force field for the simulation of proteins and nucleic acids J. Am. Chem. Soc. 117:5179-5197.
17. Cotecchia, S., O. Rossier, F. Fanelli, A. Leonardi, and P. G. De Benedetti. 2000. The alpha 1a and alpha 1b-adrenergic receptor subtypes: Molecular mechanisms of receptor activation and of drug action. Pharm. Acta Helv. 74:173-179.
18. Donnelly, D., J. P. Overington, and T. L. Blundell. 1994. The prediction and orientation of alpha-helices from sequence alignments: The combined use of environment-dependent substitution tables, Fourier transform methods and helix capping rules. Protein Eng. 7:645-653.
19. Dragic, T., A. Trkola, S. W. Lin, K. A. Nagashima, F. Kajumo, L. Zhao, W. C. Olson, L. Wu, C. R. Mackay, G. P. Allaway, T. P. Sakmar, J. P. Moore, and P. J. Maddon. 1998. Amino-terminal substitutions in the CCR5 coreceptor impair gp120 binding and human immunodeficiency virus type 1 entry. J. Virol. 72:279-285.
20. Dragic, T., A. Trkola, D. A. Thompson, E. G. Cormier, F. A. Kajumo, E. Maxwell, S. W. Lin, W. Ying, S. O. Smith, T. P. Sakmar and J. P. Moore, J. P. 2000. A binding pocket for a small molecule inhibitor of HIV-1 entry within the transmembrane helices of CCR5. Proc. Natl. Acad. Sci. USA. 97:5639-5644.
21. Dunbrack, R. L., Jr., and M. Karplus. 1993. Backbone-dependent rotamer library for proteins. Application to side-chain prediction. J. Mol. Biol. 230:543-574.
22. Elling, C. E., U. Raffetseder, S. M. Nielsen, and T. W. Schwartz. 2000. Disulfide bridge engineering in the tachykinin NK1 receptor. Biochemistry. 39:667-675.
23. Elling, C. E., K. Thirstrup, S. M. Nielsen, S. A. Hjorth. and T. W. Schwartz. 1997. Metal-ion sites as structural and functional probes of helix-helix interactions in 7TM receptors. Ann. N.Y. Acad. Sci. 814:142-151.
24. Farzan, M., H. Choe, L. Vaca, K. Martin, Y. Sun, E. Desjardins, N. Ruffing, L. Wu, R. Wyatt, N. Gerard, C. Gerard, and J. Sodroski. 1998. A tyrosine-rich region in the N terminus of CCR5 is important for human immunodeficiency virus type 1 entry and mediates an association between gp120 and CCR5. J. Virol. 72:1160-1164.
25. Fiser, A., R. K. Gian Do, and A. Sali. 2000. Modeling of loops in protein structures. Protein Sci. 9:1753-1773.
26. Flanagan, C. A., W. Zhou, L. Chi, T. Yuen, V. Rodic, D. Robertson, M. Johnson, P. Holland, R. P. Millar, H. Weinstein, R. Mitchell, and S. C. Sealfon. 1999. The functional microdomain in transmembrane helices 2 and 7 regulates expression, activation, and coupling pathways of the gonadotropin-releasing hormone receptor. J. Biol. Chem. 274:28880-28886.
27. Frisch, M. J., G. W. Trucks, H. B. Schlegel, G. E. Scuseria, M. A. Robb, J. R. Cheeseman, V. G. Zakrzewski, J. A. Montgomery, Jr., R. E. Stratmann, J. C. Burant, S. Dapprich, J. M. Millam, A. D. Daniels, K. N. Kudin, M. C. Strain, O. Farkas, J. Tomasi, V. Barone, M. Cossi, R. Cammi, B. Mennucci, C. Pomelli, C. Adamo, S. Clifford, J. Ochterski, G. A. Petersson, P. Y. Ayala, Q. Cui, K. Morokuma, P. Salvador, J. J. Dannenberg, D. K. Malick, A. D. Rabuck, K. Raghavachari, J. B. Foresman, J. Cioslowski, J. V. Ortiz, A. G. Baboul, B. B. Stefanov, G. Liu, A. Liashenko, P. Piskorz, I. Komaromi, R. Gomperts, R. L. Martin, D. J. Fox, T. Keith, M. A. Al-Laham, C. Y. Peng, A. Nanayakkara, M. Challacombe, P. M. W. Gill, B. Johnson. W. Chen, M. W. Wong, J. L. Andres, C. Gonzalez, M. Head-Gordon, E. S. Replogle, and J. A. Pople. 2001. Gaussian 98, Gaussian, Inc., Pittsburgh, PA.
28. Genoud, S., F. Kajumo, F., Y. Guo, D. Thompson, and T. Dragic. 1999. CCR5-mediated human immunodeficiency virus entry depends on an amino-terminal gp120-binding site and on the conformational integrity of all four extracellular domains. J. Virol. 73:1645-1648.
29. Govaerts, C., C. Blanpain, X. Deupi, S. Ballet, J. A. Ballesteros, S. J. Wodak, G. Vassart, L. Pardo, and M. Parmentier. 2001a. The TXP motif in the second transmembrane helix of CCR5. J. Biol. Chem. 276:13217-13225.
30. Govaerts, C., A. Lefort, S. Costagliola, S. J. Wodak, J. A. Ballesteros, J. Van Sande, S. J. Wodak, L. Pardo, and G. Vassart. 2001b. A conserved Asn in transmembrane helix 7 is an on/off switch in the activation of the thyrotropin receptor. J. Biol. Chem. 276:22991-22999.
31. Harpaz, Y., M. Gerstein, and C. Chothia. 1994. Volume changes on protein folding. Structure. 2:641-649.
32. Hill, C. M., D. Kwon, M. Jones, C. B. Davis, S. Marmon, B. L. Daugherty, J. A. DeMartino, M. S. Springer, D. Unutmaz, and D. R. Littman. 1998. The amino terminus of human CCR5 is required for its function as a receptor for diverse human and simian immunodeficiency virus envelope glycoproteins. Virology. 248:357-371.
33. Hoffman, T. L., C. C. LaBranche, W. Zhang, G. Canziani, J. Robinson, I. Chaiken, J. A. Hoxie, and R. W. Doms. 1999. Stable exposure of the coreceptor-binding site in a CD4-independent HIV-1 envelope protein. Proc. Natl. Acad. Sci. USA. 96:6359-6364.
34. Howard, O. M., K. Shirakawa, J. A. Turpin, A. Maynard, G. J. Tobin, M. Carrington, J. Oppenheim, and M. Dean. 1999. Naturally occurring CCR5 extracellular and transmembrane domain variants affect HIV-1 co-receptor and ligand binding function. J. Biol. Chem. 274:16228-16234.
35. Hubbard, S. J., and J. M. Thornton. 1993. NACCESS. Computer Program, Department of Biochemistry and Molecular Biology, University College, London.
36. Hubbell, W. L., D. S. Cafiso, and C. Altenbach. 2000. Identifying conformational changes with site-directed spin labeling. Nat. Struct. Biol. 7:735-739.
37. Javadpour, M. M., M. Eilers, M. Groesbeek, and S. O. Smith. 1999. Helix packing in polytopic membrane proteins: Role of glycine in transmembrane helix association. Biophys. J. 77:1609-1618.
38. Javitch, J. A., J. A. Ballesteros, H. Weinstein, and J. Chen. 1998. A cluster of aromatic residues in the sixth transmembrane-spanning segment of the dopamine D2 receptor is accessible in the binding-site crevice. Biochemistry. 37:998-1006.
39. Javitch, J. A., D. Fu, G. Liapakis, and J. Chen. 1997. Constitutive activation of the beta2 adrenergic receptor alters the orientation of its sixth membrane-spanning segment. J. Biol. Chem. 272:18546-18549.
40. Johnson, J. M., and G. M. Church. 2000. Predicting ligand-binding function in families of bacterial receptors. Proc. Natl. Acad. Sci. USA. 97:3965-3970.
41. Kolakowski, Jr., L. F. 1994. GCRDb: A G-protein-coupled receptor database. Receptors, Channels. 2:1-7.
42. Kolchinsky, P., T. Mirzabekov, M. Farzan, E. Kiprilov, M. Cayabyab, L. J. Mooney, H. Choe, and J. Sodroski. 1999. Adaptation of a CCR5-using, primary human immunodeficiency virus type 1 isolate for CD4-independent replication. J. Virol. 73:8120-8126.
43. Laskowski, R. A., M. W. MacArthur, D. S. Moss, and J. M. Thornton. 1993. PROCHECK: A program to check the stereochemical quality of protein structures. J. Appl. Crystallogr. 26:283-291.
44. Lee, B., M. Sharron, C. Blanpain, B. J. Doranz, J. Vakili, P. Setoh, E. Berg, G. Liu, H. R. Guy, S. R. Durell, M. Parmentier, C. N. Chang, K. Price, M. Tsang, and R. W. Doms. 1999. Epitope mapping of CCR5 reveals multiple conformational states and distinct but overlapping structures involved in chemokine and coreceptor function. J. Biol. Chem. 274:9617-9626.
45. Li, W., S. Liang, R. Wang, L. Lai, and Y. Han. 1999. Exploring the conformational diversity of loops on conserved frameworks. Protein Eng. 12:1075-1086.
46. Liang, M., C. Mallari, M. Rosser, H. P. Ng, K. May, S. Monahan, J. G. Bauman, I. Islam, A. Ghannam, B. Buckman, K. Shaw, G. P. Wei, W. Xu, Z. Zhao, E. Ho, J. Shen, H. Oanh, B. Subramanyam, R. Vergona, D. Taub, L. Dunning, S. Harvey, R. M. Snider, J. Hesselgesser, M. M. Morrissey, and H. D. Perez. 2000. Identification and characterization of a potent, selective, and orally active antagonist of the CC chemokine receptor-1. J. Biol. Chem. 275:19000-19008.
47. Lichtarge, O., H. R. Bourne, and F. E. Cohen. 1996. An evolutionary trace method defines binding surfaces common to protein families. J. Mol. Biol. 257:342-358.
48. Lu, Z. L., and E. C. Hulme. 2000. A network of conserved intramolecular contacts defines the off-state of the transmembrane switch mechanism in a seven-transmembrane receptor. J. Biol. Chem. 275:5682-5686.
49. Luo, Z., D. J. Butcher, and Z. Huang. 1997. Molecular modeling of interleukin-8 receptor beta and analysis of the receptor-ligand interaction. Protein Eng. 10:1039-1045.
50. McFadyen, I. J., T. G. Metzger, M. G. Paterlini, and D. M. Ferguson. 2001. Exploring the unique pharmacology of a novel opioid receptor, ZFOR1, using molecular modeling and the "message-address" concept. Protein Eng. 14:953-960.
51. Meng, E. C., B. K. Shoichet, and I. D. Kuntz. 1992. Molecular docking using shape descriptors. J. Comp. Chem. 13:266-278.
52. Metzger, T. G., M. G. Paterlini, D. M. Ferguson, and P. S. Portoghese. 2001. Investigation of the selectivity of oxymorphone- and naltrexone-derived ligands via site-directed mutagenesis of opioid receptors: Exploring the "address" recognition locus. J. Med. Chem. 44:857-862.
53. Metzger, T. G., M. G. Paterlini, P. S. Portoghese, and D. M. Ferguson. 1996. Application of the message-address concept to the docking of naltrexone and selective naltrexone-derived opioid antagonists into opioid receptor models. Neurochem. Res. 21:1287-1294.
54. Mirzadegan, T., F. Diehl, B. Ebi, S. Bhakta, I. Polsky, D. McCarley, M. Mulkins, G. S. Weatherhead, J. M. Lapierre, J. Dankwardt, D. Morgans, R. Wilhelm, and K. Jarnagin. 2000. Identification of the binding site for a novel class of CCR2b chemokine receptor antagonists: Binding to a common chemokine receptor motif within the helical bundle J. Biol. Chem. 275:25562-25571.
55. Mizobe, T., M. Maze, V. Lam, S. Suryanarayana, and B. K. Kobilka. 1996. Arrangement of transmembrane domains in adrenergic receptors. Similarity to bacteriorhodopsin. J. Biol. Chem. 271:2387-2389.
56. Moro, S., C. Hoffmann, and K. A. Jacobson. 1999. Role of the extracellular loops of G protein-coupled receptors in ligand recognition: A molecular modeling study of the human P2YI receptor. Biochemistry. 38:3498-3507.
57. Nardese, V., R. Longhi, S. Polo, F. Sironi, C. Arcelloni, R. Paroni, C. DeSantis, P. Sarmientos, M. Rizzi, M. Bolognesi, V. Pavone, and P. Lusso. 2001. Structural determinants of CCR5 recognition and HIV-a blockade in RANTES. Nat. Struct. Biol. 8:611-615.
58. Naya, A., Y. Sagara, K. Ohwaki, T. Saeki, D. Ichikawa, Y. Iwasawa, K. Noguchi, and N. Ohtake. 2001. Design, synthesis, and discovery of a novel CCR1 antagonist. J. Med. Chem. 44:1429-1435.
59. Némety, G., K. D. Gibson, K. A. Palmer, C. N. Yoon, M. G. Paterlini, A. Zagari, S. Rumsey, and H. A. Scheraga. 1992. Energy parameters in polypeptides. 10. Improved geometrical parameters and nonbonded interactions for use in the ECEPP/3 algorithm, with application to proline-containing peptides. J. Phys. Chem. 96:6472-6484.
60. Ng, H. P., K. May, J. G. Bauman, A. Ghannam, I. Islam, M. Liang, R. Horuk, J. Hesselgesser, R. M. Snider, H. D. Perez, and M. M. Morrissey. 1999. Discovery of novel non-peptide CCR1 receptor antagonists. J. Med. Chem. 42:4680-4694.
61. Odile-Colson, A., J. H. Perlman, A. Smolyar, M. C. Gershengorn, and R. Osman. 1998. Static and dynamic roles of extracellular loops in G-protein-coupled receptors: A mechanism for sequential binding of thyrotropin-releasing hormone to its receptor. Biophys. J. 74:1087-1100.
62. Olson, W. C., E. E. R. Gwénaël, K. A. Nagashima, D. N. H. Tran, D. J. Anselma, S. P. Monard, J. P. Segal, D. A. D. Thompson, F. Kajumo, Y. Guo, J. P. Moore, P. J. Maddon, and T. Dragic. 1999. Differential inhibition of human immunodeficiency virus type 1 fusion, gp120 binding, and CC-chemokine activity by monoclonal antibodies to CCR5. J. Virol. 73:4145-4155.
63. Overington, J., D. Donnelly, M. S. Johnson, A. Sali, and T. L. Blundell. 1992. Environment-specific amino acid substitution tables: Tertiary templates and prediction of protein folds. Protein Sci. 1:216-226.
64. Palczewski, K., T. Kumasaka, T. Hori, C. A. Behnke, H. Motoshima, B. A. Fox, T. Le, D. C. Teller, T. Okada, R. E. Stenkamp, M. Yamamoto, and M. Miyano. 2000. Crystal structure of rhodopsin: A G protein-coupled receptor. Science. 289:739-745.
65. Paterlini, G., P. S. Portoghese, and D. M. Ferguson. 1997. Molecular simulation of dynorphin A-(1-10) binding to extracellular loop 2 of the kappa-opioid receptor. A model for receptor activation. J. Med. Chem. 40:3254-3262.
66. Pogozheva, I. D., A. L. Lomize, and H. I. Mosberg. 1998. Opioid receptor three-dimensional structures from distance geometry calculations with hydrogen bonding constraints. Biophys. J. 75:612-634.
67. Prieto, J., and L. Serrano. 1997. C-capping and helix stability: The Pro C-capping motif. J. Mol. Biol. 274:276-288.
68. Rabut, G. E., J. A. Konner, F. Kajumo, J. P. Moore, and T. Dragic. 1998. Alanine substitutions of polar and nonpolar residues in the aminoterminal domain of CCR5 differently impair entry of macrophage and dualtropic isolates of human immunodeficiency virus type 1. J. Virol. 72:3464-3468.
69. Rizzuto, C. D., R. Wyatt, N. Hernandez-Ramos, Y. Sun, P. D. Kwong, W. A. Hendrickson, and J. Sodroski. 1998. A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding. Science. 280:1949-1953.
70. Robertson, D. L., J. P. Anderson, J. A. Bradac, J. K. Carr, B. Foley, R. K. Funkhouser, F. Gao, B. H. Hahn, M. L. Kalish, C. Kuiken, G. H. Learn, T. Leitner, F. McCutchan, S. Osmanov, M. Peeters, D. Pieniazek, M. Salminen, P. M. Sharp, S. Wolinsky, and B. Korber. 2000. HIV-1 nomenclature proposal. Science. 288:55-56.
71. Sabroe, I., M. J. Peck, B. J. Van Keulen, A. Jorritsma, G. Simmons, P. R. Clapham, and J. E. Williams Pease. 2000. A small molecule antagonist of chemokine receptors CCR1 and CCR3. Potent inhibition of eosinophil function and CCR3-mediated HIV-1 entry. J. Biol. Chem. 275:25985-25992.
72. Sali, A., and T. L. Blundell. 1993. Comparative protein modeling by satisfaction of spatial restraints. J. Mol. Biol. 234:779-815.
73. Samson, M., G. LaRosa, F. Libert, P. Paindavoine, M. Detheux, G. Vassart, and M. Parmentier. 1997. The second extracellular loop of CCR5 is the major determinant of ligand specificity. J. Biol. Chem. 272:24934-24941.
74. Sanchez, R., and A. Sali. 1999. Comparative protein structure modeling in genomics. J. Comp. Phys. 151:388-401.
75. Sankararamakrishnan, R., and S. Vishveshwara. 1992. Geometry of proline-containing alpha-helices in proteins. Int. J. Pept. Protein Res. 39:356-363.
76. Simpson, M. M., J. A. Ballesteros, V. Chiappa, J. Chen, M. Suchiro, D. S. Hartman, T. Godel, L. A. Snyder, T. P. Sakmar, and J. A. Javitch. 1999. Dopamine D4/D2 receptor selectivity is determined by A divergent aromatic microdomain contained within the second, third, and seventh membrane-spanning segments. Mol. Pharmacol. 56:1116-1126.
77. Sowa, M. E., W. He, T. G. Wensel, and O. Lichtarge. 2000. A regulator of G protein signaling interaction surface linked to effector specificity. Proc. Natl. Acad. Sci. USA. 97:1483-1488.
78. Strader, C. D., T. M. Fong, M. R. Tota, D. Underwood, and R. A. Dixon. 1994. Structure and function of G protein-coupled receptors. Annu. Rev. Biochem. 63:101-132.
79. Struthers, M., H. Yu, M. Kono, and D. D. Oprian. 1999. Tertiary interactions between the fifth and sixth transmembrane segments of rhodopsin. Biochemistry. 38:6597-6603.
80. Subramaniam. S. 1998. The Biology Workbench - A seamless database and analysis environment for the biologist [editorial]. Proteins. 32:1-2.
81. Subramanian, G., M. G. Paterlini, D. L. Larson, P. S. Portoghese, and D. M. Ferguson. 1998. Conformational analysis and automated receptor docking of selective arylacetamide-based kappa-opioid agonists. J. Med. Chem. 41:4777-4789.
82. Subramanian, G., M. G. Paterlini, P. S. Portoghese, and D. M. Ferguson. 2000. Molecular docking reveals a novel binding site model for fentanyl at the mu-opioid receptor. J. Med. Chem. 43:381-391.
83. Surratt, C. K., P. S. Johnson, A. Moriwaki, B. K. Seidleck, C. J. Claschak, J. B. Wang, and G. R. Uhl. 1994. Mu opiate receptor. Charged transmembrane domain amino acids are critical for agonist recognition and intrinsic activity. J. Biol. Chem. 269:20548-20553.
84. Thirstrup, K., C. E. Elling, S. A. Hjorth, and T. W. Schwartz. 1996. Construction of a high affinity zinc switch in the kappa-opioid receptor. J. Biol. Chem. 271:7875-7878.
85. Thompson, J. D., D. G. Higgins, and T. J. Gibson. 1994. CLUSTAL W: Improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice. Nucleic Acids Res. 22:4673-4680.
86. Unger, V. M., P. A. Hargrave, J. M. Baldwin, and G. F. Schertler. 1997. Arrangement of rhodopsin transmembrane alpha-helices. Nature. 389:203-206.
87. Van Vlijmen, H. W. T., and M. Karplus. 1997. PDB-based protein loop prediction: Parameters for selection and methods for optimization. J. Mol. Biol. 267:975-1001.
88. Viguera, A. R., and L. Serrano. 1999. Stable proline box motif at the N-terminal end of alpha-helices. Protein Sci. 8:1733-1742.
89. White, S. H. 1994. Hydropathy plots and prediction of membrane protein topology. In Membrane Protein Structure: Experimental Approaches. S. H. White. editor. Oxford University Press, New York. 97-126.
90. Wu, L., N. P. Gerard, R. Wyatt, H. Choe, C. Parolin, N. Ruffing, A. Borsetti, A. A. Cardoso, E. Desjardin, W. Newman, C. Gerard, and J. Sodroski. 1996. CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5 [see comments]. Nature. 384:179-183.
91. Zhang, L., R. N. DeHaven, and M. Goodman. 2002b. NMR and modeling studies of a synthetic extracellular loop II of the κ opioid receptor in DPC micelle. Biochemistry. 41:61-68.
92. Zhang, C., J. Hou, and S.-H. Kim. 2002a. Fold prediction of helical proteins using torsion angle dynamics and predicted restraints. Proc. Natl. Acad. Sci. USA. 99:3581-3585.
93. Zhou, W., C. Flanagan, J. A. Ballesteros, K. Konvicka, J. S. Davidson, H. Weinstein, R. P. Millar, and S. C. Sealfon. 1994. A reciprocal mutation supports helix 2 and helix 7 proximity in the gonadotropin-releasing hormone receptor. Mol. Pharmacol. 45:165-170.
94. Zhou, N., Z. Luo, J. W. Hall, J. Luo, X. Han, and Z. Huang. 2000. Molecular modeling and site-directed mutagenesis of CCR5 reveal residues critical for chemokine binding and signal transduction. Eur. J. Immunol. 30:164-173.