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PMID: 12496074 Published · ppublish English Comparative Study Evaluation Study Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S. Validation Study

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

Biophysical journal ·Vol. 83 ·No. 6 ·2002-12-00 ·Pages 3012-31

Paterlini MG

Abstract

The G-protein coupled receptor CCR5 is the main co-receptor for macrophage-tropic HIV-1 strains. I have built a structural model of the chemokine receptor CCR5 and used it to explain the binding and selectivity of the antagonist TAK779. Models of the extracellular (EC) domains of CCR5 have been constructed and used to rationalize current biological data on the binding of HIV-1 and chemokines. Residues spanning the transmembrane region of CCR5 have been modeled after rhodopsin, and their functional significance examined using the evolutionary trace method. The receptor cavity shares six residues with CC-chemokine receptors CCR1 through CCR4, while seven residues are unique to CCR5. The contribution of these residues to ligand binding and selectivity is tested by molecular docking simulations of TAK779 to CCR1, CCR2, and CCR5. TAK779 binds to CCR5 in the cavity formed by helices 1, 2, 3, and 7 with additional interactions with helices 5 and 6. TAK779 did not dock to either CCR1 or CCR2. The results are consistent with current site-directed mutagenesis data and with the observed selectivity of TAK779 for CCR5 over CCR1 and CCR2. The specific residues responsible for the observed selectivity are identified. The four EC regions of CCR5 have been modeled using constrained simulated annealing simulations. Applied dihedral angle constraints are representative of the secondary structure propensities of these regions. Tertiary interactions, in the form of distance constraints, are generated from available epitope mapping data. Analysis of the 250 simulated structures provides new insights to the design of experiments aimed at determining residue-residue contacts across the EC domains and for mapping CC-chemokines on the surface of the EC domains.

MeSH Terms
Amides/chemistry Amino Acid Sequence Amino Acids/chemistry Animals CCR5 Receptor Antagonists Computer Simulation Extracellular Space Humans Ligands Membrane Proteins/chemistry Mice Models, Biological Models, Molecular Molecular Sequence Data Peptide Fragments/chemistry Protein Binding Protein Conformation Protein Structure, Tertiary Quaternary Ammonium Compounds/chemistry Receptors, CCR5/chemistry Receptors, Chemokine/chemistry Reproducibility of Results Sensitivity and Specificity Sequence Analysis, Protein Structure-Activity Relationship
Chemicals
Amides Amino Acids CCR5 Receptor Antagonists Ligands Membrane Proteins Peptide Fragments Quaternary Ammonium Compounds Receptors, CCR5 Receptors, Chemokine TAK 779
Authors & Affiliations
1 authors, click to expand affiliations / ORCID
Paterlini M Germana
Department of Medicinal Chemistry and Supercomputer Institute, University of Minnesota, Minneapolis, MN 55455, USA. germana@certusoft.com
References (82)
82 references, click to expand
  1. Comparative protein modelling by satisfaction of spatial restraints.
    J Mol Biol. 1993 Dec 5;234(3):779-815 PMID: 8254673
  2. A reciprocal mutation supports helix 2 and helix 7 proximity in the gonadotropin-releasing hormone receptor.
    Mol Pharmacol. 1994 Feb;45(2):165-70 PMID: 8114667
  3. Fingerprinting G-protein-coupled receptors.
    Protein Eng. 1994 Feb;7(2):195-203 PMID: 8170923
  4. -mu opiate receptor. Charged transmembrane domain amino acids are critical for agonist recognition and intrinsic activity.
    J Biol Chem. 1994 Aug 12;269(32):20548-53 PMID: 8051154
  5. 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. 1994 May;7(5):645-53 PMID: 8073034
  6. Volume changes on protein folding.
    Structure. 1994 Jul 15;2(7):641-9 PMID: 7922041
  7. Structure and function of G protein-coupled receptors.
    Annu Rev Biochem. 1994;63:101-32 PMID: 7979235
  8. CLUSTAL W: improving the sensitivity of progressive multiple sequence alignment through sequence weighting, position-specific gap penalties and weight matrix choice.
    Nucleic Acids Res. 1994 Nov 11;22(22):4673-80 PMID: 7984417
  9. Arrangement of transmembrane domains in adrenergic receptors. Similarity to bacteriorhodopsin.
    J Biol Chem. 1996 Feb 2;271(5):2387-9 PMID: 8576196
  10. An evolutionary trace method defines binding surfaces common to protein families.
    J Mol Biol. 1996 Mar 29;257(2):342-58 PMID: 8609628
  11. Construction of a high affinity zinc switch in the kappa-opioid receptor.
    J Biol Chem. 1996 Apr 5;271(14):7875-8 PMID: 8626461
  12. Role of aromatic transmembrane residues of the delta-opioid receptor in ligand recognition.
    J Biol Chem. 1996 Apr 26;271(17):10161-8 PMID: 8626577
  13. CD4-induced interaction of primary HIV-1 gp120 glycoproteins with the chemokine receptor CCR-5.
    Nature. 1996 Nov 14;384(6605):179-83 PMID: 8906795
  14. Application of the message-address concept to the docking of naltrexone and selective naltrexone-derived opioid antagonists into opioid receptor models.
    Neurochem Res. 1996 Nov;21(11):1287-94 PMID: 8947918
  15. PDB-based protein loop prediction: parameters for selection and methods for optimization.
    J Mol Biol. 1997 Apr 11;267(4):975-1001 PMID: 9135125
  16. Metal-ion sites as structural and functional probes of helix-helix interactions in 7TM receptors.
    Ann N Y Acad Sci. 1997 Apr 24;814:142-51 PMID: 9160966
  17. Constitutive activation of the beta2 adrenergic receptor alters the orientation of its sixth membrane-spanning segment.
    J Biol Chem. 1997 Jul 25;272(30):18546-9 PMID: 9228019
  18. Gapped BLAST and PSI-BLAST: a new generation of protein database search programs.
    Nucleic Acids Res. 1997 Sep 1;25(17):3389-402 PMID: 9254694
  19. Dopamine D4/D2 receptor selectivity is determined by A divergent aromatic microdomain contained within the second, third, and seventh membrane-spanning segments.
    Mol Pharmacol. 1999 Dec;56(6):1116-26 PMID: 10570038
  20. 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. 1999 Dec 3;274(49):34719-27 PMID: 10574939
  21. Discovery of novel non-peptide CCR1 receptor antagonists.
    J Med Chem. 1999 Nov 4;42(22):4680-94 PMID: 10579830
  22. The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000.
    Nucleic Acids Res. 2000 Jan 1;28(1):45-8 PMID: 10592178
  23. The Protein Data Bank.
    Nucleic Acids Res. 2000 Jan 1;28(1):235-42 PMID: 10592235
  24. Molecular modeling and site-directed mutagenesis of CCR5 reveal residues critical for chemokine binding and signal transduction.
    Eur J Immunol. 2000 Jan;30(1):164-73 PMID: 10602038
  25. Exploring the conformational diversity of loops on conserved frameworks.
    Protein Eng. 1999 Dec;12(12):1075-86 PMID: 10611401
  26. Disulfide bridge engineering in the tachykinin NK1 receptor.
    Biochemistry. 2000 Feb 1;39(4):667-75 PMID: 10651631
  27. Molecular docking reveals a novel binding site model for fentanyl at the mu-opioid receptor.
    J Med Chem. 2000 Feb 10;43(3):381-91 PMID: 10669565
  28. A regulator of G protein signaling interaction surface linked to effector specificity.
    Proc Natl Acad Sci U S A. 2000 Feb 15;97(4):1483-8 PMID: 10677488
  29. A network of conserved intramolecular contacts defines the off-state of the transmembrane switch mechanism in a seven-transmembrane receptor.
    J Biol Chem. 2000 Feb 25;275(8):5682-6 PMID: 10681552
  30. Predicting ligand-binding function in families of bacterial receptors.
    Proc Natl Acad Sci U S A. 2000 Apr 11;97(8):3965-70 PMID: 10737762
  31. HIV-1 nomenclature proposal.
    Science. 2000 Apr 7;288(5463):55-6 PMID: 10766634
  32. A binding pocket for a small molecule inhibitor of HIV-1 entry within the transmembrane helices of CCR5.
    Proc Natl Acad Sci U S A. 2000 May 9;97(10):5639-44 PMID: 10779565
  33. The alpha 1a and alpha 1b-adrenergic receptor subtypes: molecular mechanisms of receptor activation and of drug action.
    Pharm Acta Helv. 2000 Mar;74(2-3):173-9 PMID: 10812955
  34. Identification and characterization of a potent, selective, and orally active antagonist of the CC chemokine receptor-1.
    J Biol Chem. 2000 Jun 23;275(25):19000-8 PMID: 10748002
  35. Crystal structure of rhodopsin: A G protein-coupled receptor.
    Science. 2000 Aug 4;289(5480):739-45 PMID: 10926528
  36. 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. 2000 Aug 18;275(33):25562-71 PMID: 10770925
  37. A small molecule antagonist of chemokine receptors CCR1 and CCR3. Potent inhibition of eosinophil function and CCR3-mediated HIV-1 entry.
    J Biol Chem. 2000 Aug 25;275(34):25985-92 PMID: 10854442
  38. Identifying conformational changes with site-directed spin labeling.
    Nat Struct Biol. 2000 Sep;7(9):735-9 PMID: 10966640
  39. Modeling of loops in protein structures.
    Protein Sci. 2000 Sep;9(9):1753-73 PMID: 11045621
  40. 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. 2001 Mar 15;44(6):857-62 PMID: 11300867
  41. The TXP motif in the second transmembrane helix of CCR5. A structural determinant of chemokine-induced activation.
    J Biol Chem. 2001 Apr 20;276(16):13217-25 PMID: 11278962
  42. Design, synthesis, and discovery of a novel CCR1 antagonist.
    J Med Chem. 2001 Apr 26;44(9):1429-35 PMID: 11311066
  43. A conserved Asn in transmembrane helix 7 is an on/off switch in the activation of the thyrotropin receptor.
    J Biol Chem. 2001 Jun 22;276(25):22991-9 PMID: 11312274
  44. Structural determinants of CCR5 recognition and HIV-1 blockade in RANTES.
    Nat Struct Biol. 2001 Jul;8(7):611-5 PMID: 11427892
  45. NMR and modeling studies of a synthetic extracellular loop II of the kappa opioid receptor in a DPC micelle.
    Biochemistry. 2002 Jan 8;41(1):61-8 PMID: 11772003
  46. Exploring the unique pharmacology of a novel opioid receptor, ZFOR1, using molecular modeling and the 'message-address' concept.
    Protein Eng. 2001 Dec;14(12):953-60 PMID: 11809925
  47. Arrangement of rhodopsin transmembrane alpha-helices.
    Nature. 1997 Sep 11;389(6647):203-6 PMID: 9296501
  48. An alpha-carbon template for the transmembrane helices in the rhodopsin family of G-protein-coupled receptors.
    J Mol Biol. 1997 Sep 12;272(1):144-64 PMID: 9299344
  49. The second extracellular loop of CCR5 is the major determinant of ligand specificity.
    J Biol Chem. 1997 Oct 3;272(40):24934-41 PMID: 9312096
  50. 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. 1997 Sep 26;40(20):3254-62 PMID: 9379445
  51. C-capping and helix stability: the Pro C-capping motif.
    J Mol Biol. 1997 Nov 28;274(2):276-88 PMID: 9398533
  52. Amino-terminal substitutions in the CCR5 coreceptor impair gp120 binding and human immunodeficiency virus type 1 entry.
    J Virol. 1998 Jan;72(1):279-85 PMID: 9420225
  53. A new classification for HIV-1.
    Nature. 1998 Jan 15;391(6664):240 PMID: 9440686
  54. 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. 1998 Feb;72(2):1160-4 PMID: 9445013
  55. Molecular modeling of interleukin-8 receptor beta and analysis of the receptor-ligand interaction.
    Protein Eng. 1997 Sep;10(9):1039-45 PMID: 9464567
  56. A cluster of aromatic residues in the sixth membrane-spanning segment of the dopamine D2 receptor is accessible in the binding-site crevice.
    Biochemistry. 1998 Jan 27;37(4):998-1006 PMID: 9454590
  57. 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. 1998 Mar;74(3):1087-100 PMID: 9512011
  58. Alanine substitutions of polar and nonpolar residues in the amino-terminal domain of CCR5 differently impair entry of macrophage- and dualtropic isolates of human immunodeficiency virus type 1.
    J Virol. 1998 Apr;72(4):3464-8 PMID: 9525683
  59. Functional microdomains in G-protein-coupled receptors. The conserved arginine-cage motif in the gonadotropin-releasing hormone receptor.
    J Biol Chem. 1998 Apr 24;273(17):10445-53 PMID: 9553103
  60. A conserved HIV gp120 glycoprotein structure involved in chemokine receptor binding.
    Science. 1998 Jun 19;280(5371):1949-53 PMID: 9632396
  61. The Biology Workbench--a seamless database and analysis environment for the biologist.
    Proteins. 1998 Jul 1;32(1):1-2 PMID: 9672036
  62. Opioid receptor three-dimensional structures from distance geometry calculations with hydrogen bonding constraints.
    Biophys J. 1998 Aug;75(2):612-34 PMID: 9675164
  63. The amino terminus of human CCR5 is required for its function as a receptor for diverse human and simian immunodeficiency virus envelope glycoproteins.
    Virology. 1998 Sep 1;248(2):357-71 PMID: 9721244
  64. Antibody imprint of a membrane protein surface. Phagocyte flavocytochrome b.
    J Biol Chem. 1998 Sep 18;273(38):24847-52 PMID: 9733789
  65. Conformational analysis and automated receptor docking of selective arylacetamide-based kappa-opioid agonists.
    J Med Chem. 1998 Nov 19;41(24):4777-89 PMID: 9822548
  66. 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. 1999 Feb;73(2):1645-8 PMID: 9882373
  67. Role of the extracellular loops of G protein-coupled receptors in ligand recognition: a molecular modeling study of the human P2Y1 receptor.
    Biochemistry. 1999 Mar 23;38(12):3498-507 PMID: 10090736
  68. Epitope mapping of CCR5 reveals multiple conformational states and distinct but overlapping structures involved in chemokine and coreceptor function.
    J Biol Chem. 1999 Apr 2;274(14):9617-26 PMID: 10092648
  69. Differential inhibition of human immunodeficiency virus type 1 fusion, gp120 binding, and CC-chemokine activity by monoclonal antibodies to CCR5.
    J Virol. 1999 May;73(5):4145-55 PMID: 10196311
  70. A small-molecule, nonpeptide CCR5 antagonist with highly potent and selective anti-HIV-1 activity.
    Proc Natl Acad Sci U S A. 1999 May 11;96(10):5698-703 PMID: 10318947
  71. Stable exposure of the coreceptor-binding site in a CD4-independent HIV-1 envelope protein.
    Proc Natl Acad Sci U S A. 1999 May 25;96(11):6359-64 PMID: 10339592
  72. Naturally occurring CCR5 extracellular and transmembrane domain variants affect HIV-1 Co-receptor and ligand binding function.
    J Biol Chem. 1999 Jun 4;274(23):16228-34 PMID: 10347178
  73. Tertiary interactions between the fifth and sixth transmembrane segments of rhodopsin.
    Biochemistry. 1999 May 18;38(20):6597-603 PMID: 10350478
  74. Extracellular cysteines of CCR5 are required for chemokine binding, but dispensable for HIV-1 coreceptor activity.
    J Biol Chem. 1999 Jul 2;274(27):18902-8 PMID: 10383387
  75. Helix packing in polytopic membrane proteins: role of glycine in transmembrane helix association.
    Biophys J. 1999 Sep;77(3):1609-18 PMID: 10465772
  76. Adaptation of a CCR5-using, primary human immunodeficiency virus type 1 isolate for CD4-independent replication.
    J Virol. 1999 Oct;73(10):8120-6 PMID: 10482561
  77. Stable proline box motif at the N-terminal end of alpha-helices.
    Protein Sci. 1999 Sep;8(9):1733-42 PMID: 10493574
  78. The functional microdomain in transmembrane helices 2 and 7 regulates expression, activation, and coupling pathways of the gonadotropin-releasing hormone receptor.
    J Biol Chem. 1999 Oct 8;274(41):28880-6 PMID: 10506131
  79. Fold prediction of helical proteins using torsion angle dynamics and predicted restraints.
    Proc Natl Acad Sci U S A. 2002 Mar 19;99(6):3581-5 PMID: 11904420
  80. Geometry of proline-containing alpha-helices in proteins.
    Int J Pept Protein Res. 1992 Apr;39(4):356-63 PMID: 1428525
  81. Backbone-dependent rotamer library for proteins. Application to side-chain prediction.
    J Mol Biol. 1993 Mar 20;230(2):543-74 PMID: 8464064
  82. Environment-specific amino acid substitution tables: tertiary templates and prediction of protein folds.
    Protein Sci. 1992 Feb;1(2):216-26 PMID: 1304904
Article Info
Journal
Biophysical journal
Abbr.
Biophys J
ISSN
0006-3495
Published
2002-12-00
Pages
3012-31
Language
English
Region
United States
NLM ID
0370626
PMCID
PMC1302382
Subset
IM
Grants
NIDA NIH HHS · 5 K01 DA 0073 · United States
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