The Role of Water in Activation Mechanism of Human N-Formyl Peptide Receptor 1 (FPR1) Based on Molecular Dynamics Simulations

PLoS ONE

Volumn 7, Issue 11, 2012, Pages

  Yuan, Shuguang ^a,b   Ghoshdastider, Umesh ^a   Trzaskowski, Bartosz ^c   Latek, Dorota ^a   Debinski, Aleksander ^c   Pulawski, Wojciech ^c   Wu, Rongliang ^a   Gerke, Volker ^d   Filipek, Slawomir ^c  

^a INTERNATIONAL INSTITUTE OF MOLECULAR AND CELL BIOLOGY   (Poland)

^b NENCKI INSTITUTE OF EXPERIMENTAL BIOLOGY   (Poland)

^c UNIVERSITY OF WARSAW   (Poland)

^d UNIVERSITY OF MÜNSTER   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACID RECEPTOR STIMULATING AGENT; BETA ADRENERGIC RECEPTOR; CHEMOKINE RECEPTOR; CHEMOKINE RECEPTOR CXCR4; FORMYL PEPTIDE RECEPTOR 1; G PROTEIN COUPLED RECEPTOR; LIGAND; N FORMYLMETHIONYLLEUCYLPHENYLALANINE AGONIST; UNCLASSIFIED DRUG; WATER;

ARTICLE; BINDING SITE; BIOLOGICAL MODEL; BIOSENSOR; CELLULAR DISTRIBUTION; CRYSTAL STRUCTURE; CYTOPLASM; HUMAN; HYDROGEN BOND; MOLECULAR DOCKING; MOLECULAR DYNAMICS; PHYLOGENETIC TREE; PROTEIN BINDING; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; SIMULATION; STRUCTURAL HOMOLOGY;

BINDING SITES; HUMANS; HYDROGEN BONDING; LIGANDS; MOLECULAR DOCKING SIMULATION; MOLECULAR DYNAMICS SIMULATION; N-FORMYLMETHIONINE LEUCYL-PHENYLALANINE; PROTEIN BINDING; PROTEIN CONFORMATION; RECEPTORS, FORMYL PEPTIDE; RECEPTORS, LIPOXIN; WATER;

EID: 84869987897     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0047114     Document Type: Article

References (62)

1. Capra V, Accomazzo MR, Gardoni F, Barbieri S, Rovati GE, (2010) A role for inflammatory mediators in heterologous desensitization of CysLT1 receptor in human monocytes. J Lipid Res 51: 1075-1084.
2. Jin Y, Arita M, Zhang Q, Saban DR, Chauhan SK, et al. (2009) Anti-angiogenesis effect of the novel anti-inflammatory and pro-resolving lipid mediators. Invest Ophthalmol Vis Sci 50: 4743-4752.
3. Filep JG, El Kebir D, (2009) Neutrophil apoptosis: a target for enhancing the resolution of inflammation. J Cell Biochem 108: 1039-1046.
4. Brandenburg LO, Seyferth S, Wruck CJ, Koch T, Rosenstiel P, et al. (2009) Involvement of Phospholipase D 1 and 2 in the subcellular localization and activity of formyl-peptide-receptors in the human colonic cell line HT29. Mol Membr Biol 26: 371-383.
5. Zhang Y, Syed R, Uygar C, Pallos D, Gorry MC, et al. (2003) Evaluation of human leukocyte N-formylpeptide receptor (FPR1) SNPs in aggressive periodontitis patients. Genes Immun 4: 22-29.
6. Yousefi S, Cooper PR, Potter SL, Mueck B, Jarai G, (2001) Cloning and expression analysis of a novel G-protein-coupled receptor selectively expressed on granulocytes. J Leukoc Biol 69: 1045-1052.
7. Rabiet MJ, Huet E, Boulay F, (2007) The N-formyl peptide receptors and the anaphylatoxin C5a receptors: an overview. Biochimie 89: 1089-1106.
8. Fu H, Karlsson J, Bylund J, Movitz C, Karlsson A, et al. (2006) Ligand recognition and activation of formyl peptide receptors in neutrophils. J Leukoc Biol 79: 247-256.
9. Migeotte I, Communi D, Parmentier M, (2006) Formyl peptide receptors: a promiscuous subfamily of G protein-coupled receptors controlling immune responses. Cytokine Growth Factor Rev 17: 501-519.
10. Ye RD, Boulay F, Wang JM, Dahlgren C, Gerard C, et al. (2009) International Union of Basic and Clinical Pharmacology. LXXIII. Nomenclature for the Formyl Peptide Receptor (FPR) Family. Pharmacol Rev 61: 119-161.
11. Palczewski K, Kumasaka T, Hori T, Behnke CA, Motoshima H, et al. (2000) Crystal structure of rhodopsin: A G protein-coupled receptor. Science 289: 739-745.
12. Okada T, Sugihara M, Bondar AN, Elstner M, Entel P, et al. (2004) The retinal conformation and its environment in rhodopsin in light of a new 2.2 angstrom crystal structure. J Mol Biol 342: 571-583.
13. Fujita H, Kato T, Watanabe N, Takahashi T, Kitagawa S, (2011) Stimulation of human formyl peptide receptors by calpain inhibitors: homology modeling of receptors and ligand docking simulation. Arch Biochem Biophys 516: 121-127.
14. Khlebnikov AI, Schepetkin IA, Kirpotina LN, Brive L, Dahlgren C, et al. (2012) Molecular docking of 2-(benzimidazol-2-ylthio)-N-phenylacetamide-derived small-molecule agonists of human formyl peptide receptor 1. J Mol Model 18: 2831-2843.
15. Movitz C, Brive L, Hellstrand K, Rabiet MJ, Dahlgren C, (2010) The annexin I sequence gln(9)-ala(10)-trp(11)-phe(12) is a core structure for interaction with the formyl peptide receptor 1. J Biol Chem 285: 14338-14345.
16. Walther A, Riehemann K, Gerke V, (2000) A novel ligand of the formyl peptide receptor: annexin I regulates neutrophil extravasation by interacting with the FPR. Mol Cell 5: 831-840.
17. Mills JS, Miettinen HM, Barnidge D, Vlases MJ, Wimer-Mackin S, et al. (1998) Identification of a ligand binding site in the human neutrophil formyl peptide receptor using a site-specific fluorescent photoaffinity label and mass spectrometry. J Biol Chem 273: 10428-10435.
18. Wu B, Chien EY, Mol CD, Fenalti G, Liu W, et al. (2010) Structures of the CXCR4 chemokine GPCR with small-molecule and cyclic peptide antagonists. Science 330: 1066-1071.
19. Manglik A, Kruse AC, Kobilka TS, Thian FS, Mathiesen JM, et al. (2012) Crystal structure of the micro-opioid receptor bound to a morphinan antagonist. Nature 485: 321-326.
20. Granier S, Manglik A, Kruse AC, Kobilka TS, Thian FS, et al. (2012) Structure of the delta-opioid receptor bound to naltrindole. Nature 485: 400-404.
21. Wu H, Wacker D, Mileni M, Katritch V, Han GW, et al. (2012) Structure of the human kappa-opioid receptor in complex with JDTic. Nature 485: 327-332.
22. Thompson AA, Liu W, Chun E, Katritch V, Wu H, et al. (2012) Structure of the nociceptin/orphanin FQ receptor in complex with a peptide mimetic. Nature 485: 395-399.
23. Ballesteros JA, Weinstein H, (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.
24. Ye RD, Cavanagh SL, Quehenberger O, Prossnitz ER, Cochrane CG, (1992) Isolation of a Cdna That Encodes a Novel Granulocyte N-Formyl Peptide Receptor. Biochem Biophys Res Commun 184: 582-589.
25. Quehenberger O, Prossnitz ER, Cavanagh SL, Cochrane CG, Ye RD, (1993) Multiple domains of the N-formyl peptide receptor are required for high-affinity ligand binding. Construction and analysis of chimeric N-formyl peptide receptors. J Biol Chem 268: 18167-18175.
26. Murphy PM, Ozcelik T, Kenney RT, Tiffany HL, McDermott D, et al. (1992) A structural homologue of the N-formyl peptide receptor. Characterization and chromosome mapping of a peptide chemoattractant receptor family. J Biol Chem 267: 7637-7643.
27. Kufareva I, Rueda M, Katritch V, Stevens RC, Abagyan R, (2011) Status of GPCR modeling and docking as reflected by community-wide GPCR Dock 2010 assessment. Structure 19: 1108-1126.
28. Boulay F, Tardif M, Brouchon L, Vignais P, (1990) The human N-formylpeptide receptor. Characterization of two cDNA isolates and evidence for a new subfamily of G-protein-coupled receptors. Biochemistry 29: 11123-11133.
29. Lala A, Sharma A, Sojar HT, Radel SJ, Genco RJ, et al. (1993) Recombinant expression and partial characterization of the human formyl peptide receptor. Biochim Biophys Acta 1178: 302-306.
30. Mills JS, Miettinen HM, Cummings D, Jesaitis AJ, (2000) Characterization of the binding site on the formyl peptide receptor using three receptor mutants and analogs of Met-Leu-Phe and Met-Met-Trp-Leu-Leu. J Biol Chem 275: 39012-39017.
31. Prossnitz ER, Quehenberger O, Cochrane CG, Ye RD, (1993) Signal transducing properties of the N-formyl peptide receptor expressed in undifferentiated HL60 cells. J Immunol 151: 5704-5715.
32. Trzaskowski B, Latek D, Yuan S, Ghoshdastider U, Debinski A, et al. (2012) Action of molecular switches in GPCRs- theoretical and experimental studies. Curr Med Chem 19: 1090-1109.
33. Vanni S, Neri M, Tavernelli I, Rothlisberger U, (2011) Predicting novel binding modes of agonists to beta adrenergic receptors using all-atom molecular dynamics simulations. PLoS Comput Biol 7: e1001053.
34. Bokoch MP, Zou Y, Rasmussen SGF, Liu CW, Nygaard R, et al. (2010) Ligand-specific regulation of the extracellular surface of a G-protein-coupled receptor. Nature 463: 108-112.
35. Kolinski M, Filipek S, (2008) Molecular dynamics of mu opioid receptor complexes with agonists and antagonists. TOSBJ 2: 8-20.
36. Kolinski M, Filipek S, (2009) Studies of the activation steps concurrent to ligand binding in DOR and KOR opioid receptors based on molecular dynamics simulations. TOSBJ 3: 51-63.
37. Kolinski M, Filipek S, (2010) Study of a structurally similar kappa opioid receptor agonist and antagonist pair by molecular dynamics simulations. J Mol Model 16: 1567-1576.
38. Haga K, Kruse AC, Asada H, Yurugi-Kobayashi T, Shiroishi M, et al. (2012) Structure of the human M2 muscarinic acetylcholine receptor bound to an antagonist. Nature 482: 547-551.
39. Standfuss J, Edwards PC, D'Antona A, Fransen M, Xie G, et al. (2011) The structural basis of agonist-induced activation in constitutively active rhodopsin. Nature 471: 656-660.
40. Marti-Renom MA, Stuart AC, Fiser A, Sanchez R, Melo F, et al. (2000) Comparative protein structure modeling of genes and genomes. Annu Rev Biophys Biomol Struct 29: 291-325.
41. Accelrys Software Inc (2011) Discovery Studio Modeling Environment, Release 3.1.
42. Cherezov V, Rosenbaum DM, Hanson MA, Rasmussen SG, Thian FS, et al. (2007) High-resolution crystal structure of an engineered human beta2-adrenergic G protein-coupled receptor. Science 318: 1258-1265.
43. Edgar RC, (2004) MUSCLE: multiple sequence alignment with high accuracy and high throughput. Nucleic Acids Res 32: 1792-1797.
44. Shen MY, Sali A, (2006) Statistical potential for assessment and prediction of protein structures. Protein Sci 15: 2507-2524.
45. Lomize MA, Lomize AL, Pogozheva ID, Mosberg HI, (2006) OPM: Orientations of proteins in membranes database. Bioinformatics 22: 623-625.
46. Jacobson MP, Pincus DL, Rapp CS, Day TJF, Honig B, et al. (2004) A hierarchical approach to all-atom protein loop prediction. Proteins 55: 351-367.
47. Banks JL, Beard HS, Cao YX, Cho AE, Damm W, et al. (2005) Integrated modeling program, applied chemical theory (IMPACT). J Comput Chem 26: 1752-1780.
48. Shivakumar D, Williams J, Wu YJ, Damm W, Shelley J, et al. (2010) Prediction of Absolute Solvation Free Energies using Molecular Dynamics Free Energy Perturbation and the OPLS Force Field. J Chem Theory Comput 6: 1509-1519.
49. Maestro, version 9.2. Schrödinger, LLC.
50. Berendsen HJC, Postma JPM, Vangunsteren WF, Dinola A, Haak JR, (1984) Molecular-Dynamics with Coupling to an External Bath. J Chem Phys 81: 3684-3690.
51. Krautler V, Van Gunsteren WF, Hunenberger PH, (2001) A fast SHAKE: Algorithm to solve distance constraint equations for small molecules in molecular dynamics simulations. J Comput Chem 22: 501-508.
52. Darden T, Perera L, Li LP, Pedersen L, (1999) New tricks for modelers from the crystallography toolkit: the particle mesh Ewald algorithm and its use in nucleic acid simulations. Struct Fold Des 7: R55-R60.
53. Tuckerman M, Berne BJ, Martyna GJ, (1992) Reversible Multiple Time Scale Molecular-Dynamics. J Chem Phys 97: 1990-2001.
54. MacroModel, version 9.9. Schrödinger, LLC.
55. Friesner RA, Banks JL, Murphy RB, Halgren TA, Klicic JJ, et al. (2004) Glide: a new approach for rapid, accurate docking and scoring. 1. Method and assessment of docking accuracy. J Med Chem 47: 1739-1749.
56. Halgren TA, Murphy RB, Friesner RA, Beard HS, Frye LL, et al. (2004) Glide: a new approach for rapid, accurate docking and scoring. 2. Enrichment factors in database screening. J Med Chem 47: 1750-1759.
57. Gaussian 09, Revision A.1. Frisch MJ, Trucks GW, Schlegel HB, Scuseria GE, Robb MA, et al. (2009). Wallingford CT: Gaussian, Inc.
58. Dupradeau FY, Pigache A, Zaffran T, Savineau C, Lelong R, et al. (2010) The R.E.D. tools: advances in RESP and ESP charge derivation and force field library building. Phys Chem Chem Phys 12: 7821-7839.
59. MacKerell AD, Bashford D, Bellott M, Dunbrack RL, Evanseck JD, et al. (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B 102: 3586-3616.
60. Raval A, Piana S, Eastwood MP, Dror RO, Shaw DE, (2012) Refinement of protein structure homology models via long, all-atom molecular dynamics simulations. Proteins 80: 2071-2079.
61. Humphrey W, Dalke A, Schulten K, (1996) VMD: visual molecular dynamics. J Mol Graph 14: 33-38, 33-38, 27-38.
62. The PyMOL Molecular Graphics System, Version 1.5. Schrödinger, LLC.