A coupling of homology modeling with multiple molecular dynamics simulation for identifying representative conformation of GPCR structures: a case study on human bombesin receptor subtype-3

References

• Allen, W. J., Lemkul, J. A., & Bevan, D. R. (2009). GridMAT-MD: A grid-based membrane analysis tool for use with molecular dynamics. Journal of Computational Chemistry, 30, 1952–1958. doi:10.1002/jcc.21172
   PubMed Web of Science ®Google Scholar
• Altschul, S. F., Gish, W., Miller, W., Myers, E. W., & Lipman, D. J. (1990). Basic local alignment search tool. Journal of Molecular Biology, 215, 403–410. doi:10.1016/S0022-2836(05)80360-2
   PubMed Web of Science ®Google Scholar
• Amadei, A., Linssen, A., & Berendsen, H. J. (1993). Essential dynamics of proteins. Proteins: Structure, Function, and Genetics, 17, 412–425. doi:10.1002/prot.340170408
   PubMed Web of Science ®Google Scholar
• Auffinger, P., Louise-May, S., & Westhof, E. (1995). Multiple molecular dynamics simulations of the anticodon loop of tRNAAsp in aqueous solution with counterions. Journal of the American Chemical Society, 117, 6720–6726. doi:10.1021/ja00130a011
   Web of Science ®Google Scholar
• Bairoch, A., & Apweiler, R. (2000). The SWISS-PROT protein sequence database and its supplement TrEMBL in 2000. Nucleic Acids Research, 28, 45–48. doi:10.1093/nar/28.1.45
   PubMed Web of Science ®Google Scholar
• Balsera, M. A., Wriggers, W., Oono, Y., & Schulten, K. (1996). Principal component analysis and long time protein dynamics. The Journal of Physical Chemistry, 100, 2567–2572. doi:10.1021/jp9536920
   Web of Science ®Google Scholar
• Banères, J.-L., & Parello, J. (2003). Structure-based analysis of GPCR function: Evidence for a novel pentameric assembly between the dimeric leukotriene B4 receptor BLT1 and the G-protein. Journal of Molecular Biology, 329, 815–829. doi:10.1016/S0022-2836(03)00439-X
   PubMed Web of Science ®Google Scholar
• Becker, O. M. (1997). Geometric versus topological clustering: An insight into conformation mapping. Proteins: Structure, Function, and Genetics, 27, 213–226. doi:10.1002/(SICI)1097-0134(199702)27:2<213:AID-PROT8>3.0.CO;2-G
   PubMed Web of Science ®Google Scholar
• Berendsen, H. J., Postma, J. P. M., van Gunsteren, W. F., DiNola, A., & Haak, J. (1984). Molecular dynamics with coupling to an external bath. The Journal of Chemical Physics, 81, 3684–3690. doi:10.1063/1.448118
   Web of Science ®Google Scholar
• Berger, O., Edholm, O., & Jähnig, F. (1997). Molecular dynamics simulations of a fluid bilayer of dipalmitoylphosphatidylcholine at full hydration, constant pressure, and constant temperature. Biophysical Journal, 72, 2002–2013. doi:10.1016/S0006-3495(97)78845-3
   PubMed Web of Science ®Google Scholar
• Berman, H. M., Westbrook, J., Feng, Z., Gilliland, G., Bhat, T., Weissig, H., … Bourne, P. E. (2000). The protein data bank. Nucleic Acids Research, 28, 235–242. doi:10.1093/nar/28.1.235
   PubMed Web of Science ®Google Scholar
• Bissantz, C., Bernard, P., Hibert, M., & Rognan, D. (2003). Protein-based virtual screening of chemical databases. II. Are homology models of g-protein coupled receptors suitable targets? Proteins: Structure, Function, and Bioinformatics, 50, 5–25. doi:10.1002/prot.10237
   PubMed Web of Science ®Google Scholar
• Caves, L. S., Evanseck, J. D., & Karplus, M. (1998). Locally accessible conformations of proteins: Multiple molecular dynamics simulations of crambin. Protein Science, 7, 649–666. doi:10.1002/pro.5560070314
   PubMed Web of Science ®Google Scholar
• Costanzi, S., Siegel, J., Tikhonova, I. G., & Jacobson, K. A. (2009). Rhodopsin and the others: A historical perspective on structural studies of G protein-coupled receptors. Current Pharmaceutical Design, 15, 3994–4002. doi:10.2174/138161209789824795
   PubMed Web of Science ®Google Scholar
• Darden, T., York, D., & Pedersen, L. (1993). Particle mesh Ewald: An N log (N) method for Ewald sums in large systems. The Journal of Chemical Physics, 98, 10089–10092. doi:10.1063/1.464397
   Web of Science ®Google Scholar
• Drews, J. (2000). Drug discovery: A historical perspective. Science, 287, 1960–1964. doi:10.1126/science.287.5460.1960
   PubMed Web of Science ®Google Scholar
• Fan, H., & Mark, A. E. (2004). Refinement of homology-based protein structures by molecular dynamics simulation techniques. Protein Science, 13, 211–220. doi:10.1110/ps.03381404
   PubMed Web of Science ®Google Scholar
• Fathi, Z., Corjay, M., Shapira, H., Wada, E., Benya, R., Jensen, R., … Battey, J. (1993). BRS-3: A novel bombesin receptor subtype selectively expressed in testis and lung carcinoma cells. Journal of Biological Chemistry, 268, 5979–5984.
   PubMed Web of Science ®Google Scholar
• Fiser, A., Do, R. K. G., & Šali, A. (2000). Modeling of loops in protein structures. Protein Science, 9, 1753–1773. doi:10.1110/ps.9.9.1753
   PubMed Web of Science ®Google Scholar
• Frauenfelder, H., Sligar, S. G., & Wolynes, P. G. (1991). The energy landscapes and motions of proteins. Science, 254, 1598–1603. doi:10.1126/science.1749933
   PubMed Web of Science ®Google Scholar
• Gayen, A., Goswami, S. K., & Mukhopadhyay, C. (2011). NMR evidence of GM1-induced conformational change of Substance P using isotropic bicelles. Biochimica et Biophysica Acta (BBA)-Biomembranes, 1808, 127–139. doi: 10.1016/j.bbamem.2010.09.02310.1016/j.bbamem.2010.09.023
   PubMed Web of Science ®Google Scholar
• Gonzalez, N., Hocart, S. J., Portal-Nuñez, S., Mantey, S. A., Nakagawa, T., Zudaire, E., … Jensen, R. T. (2008). Molecular basis for agonist selectivity and activation of the orphan bombesin receptor subtype 3 receptor. Journal of Pharmacology and Experimental Therapeutics, 324, 463–474. doi:10.1124/jpet.107.132332
   PubMed Web of Science ®Google Scholar
• Grossfield, A., Feller, S. E., & Pitman, M. C. (2007). Convergence of molecular dynamics simulations of membrane proteins. Proteins: Structure, Function, and Bioinformatics, 67, 31–40. doi:10.1002/prot.21308
   PubMed Web of Science ®Google Scholar
• Guan, X.-M., Metzger, J. M., Yang, L., Raustad, K. A., Wang, S.-P., Spann, S. K., … Faidley, T. D. (2011). Antiobesity effect of MK-5046, a novel bombesin receptor subtype-3 agonist. Journal of Pharmacology and Experimental Therapeutics, 336, 356–364. doi:10.1124/jpet.110.174763
   PubMed Web of Science ®Google Scholar
• Hanson, M. A., Roth, C. B., Jo, E., Griffith, M. T., Scott, F. L., Reinhart, G., … Schuerer, S. C. (2012). Crystal structure of a lipid G protein-coupled receptor. Science, 335, 851–855. doi:10.1126/science.1215904
   PubMed Web of Science ®Google Scholar
• Henzler-Wildman, K., & Kern, D. (2007). Dynamic personalities of proteins. Nature, 450, 964–972. doi:10.1038/nature06522
   PubMed Web of Science ®Google Scholar
• Hess, B. (2000). Similarities between principal components of protein dynamics and random diffusion. Physical Review E, 62, 8438–8448. doi:10.1103/PhysRevE.62.8438
   PubMed Web of Science ®Google Scholar
• Hess, B. (2002). Convergence of sampling in protein simulations. Physical Review E, 65, 031910-1–031910-10. doi:10.1103/PhysRevE.65.031910
   Web of Science ®Google Scholar
• Hess, B., Bekker, H., Berendsen, H. J., & Fraaije, J. G. (1997). LINCS: A linear constraint solver for molecular simulations. Journal of Computational Chemistry, 18, 1463–1472. doi:10.1002/(SICI)1096-987X(199709)18:12<1463:AID-JCC4>3.0.CO;2-H
   Web of Science ®Google Scholar
• Humphrey, W., Dalke, A., & Schulten, K. (1996). VMD: Visual molecular dynamics. Journal of Molecular Graphics, 14, 33–38. doi:10.1016/0263-7855(96)00018-5
   PubMed Web of Science ®Google Scholar
• Jensen, R., Battey, J., Spindel, E., & Benya, R. (2008). International Union of Pharmacology. LXVIII. Mammalian bombesin receptors: Nomenclature, distribution, pharmacology, signaling, and functions in normal and disease states. Pharmacological Reviews, 60(1), 1–42. doi:10.1124/pr.107.07108
   PubMed Web of Science ®Google Scholar
• Ji, T. H., Grossmann, M., & Ji, I. (1998). G protein-coupled receptors: I. Diversity of receptor–ligand interactions. Journal of Biological Chemistry, 273, 17299–17302. doi:10.1074/jbc.273.28.17299
   PubMed Web of Science ®Google Scholar
• Kabsch, W., & Sander, C. (1983). Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers, 22, 2577–2637. doi:10.1002/bip.360221211
   PubMed Web of Science ®Google Scholar
• Kandt, C., Ash, W. L., & Peter Tieleman, D. (2007). Setting up and running molecular dynamics simulations of membrane proteins. Methods, 41, 475–488. doi:10.1016/j.ymeth.2006.08.006
   PubMed Web of Science ®Google Scholar
• Karplus, M., & McCammon, J. A. (2002). Molecular dynamics simulations of biomolecules. Nature Structural & Molecular Biology, 9, 646–652. doi:10.1038/nsb0902-646
   Web of Science ®Google Scholar
• Klabunde, T., & Hessler, G. (2002). Drug design strategies for targeting G-protein-coupled receptors. ChemBioChem, 3, 928–944. doi:10.1002/1439-7633(20021004)3:10<928:AID-CBIC928>3.0.CO;2-5
   PubMed Web of Science ®Google Scholar
• Krieger, E., Joo, K., Lee, J., Lee, J., Raman, S., Thompson, J., … Karplus, K. (2009). Improving physical realism, stereochemistry, and side-chain accuracy in homology modeling: Four approaches that performed well in CASP8. Proteins: Structure, Function, and Bioinformatics, 77(S9), 114–122. doi:10.1002/prot.22570
   PubMed Web of Science ®Google Scholar
• Laberge, M., & Yonetani, T. (2008). Molecular dynamics simulations of hemoglobin A in different states and bound to DPG: Effector-linked perturbation of tertiary conformations and HbA concerted dynamics. Biophysical Journal, 94, 2737–2751. doi:10.1529/biophysj.107.114942
   PubMed Web of Science ®Google Scholar
• Laskowski, R. A., MacArthur, M. W., Moss, D. S., & Thornton, J. M. (1993). PROCHECK: A program to check the stereochemical quality of protein structures. Journal of Applied Crystallography, 26, 283–291. doi:10.1107/S0021889892009944
   Web of Science ®Google Scholar
• Levy, R., Srinivasan, A., Olson, W., & McCammon, J. (1984). Quasi-harmonic method for studying very low frequency modes in proteins. Biopolymers, 23, 1099–1112. doi:10.1002/bip.360230610
   PubMed Web of Science ®Google Scholar
• Li, X., Jacobson, M. P., & Friesner, R. A. (2004). High-resolution prediction of protein helix positions and orientations. Proteins: Structure, Function, and Bioinformatics, 55, 368–382. doi:10.1002/prot.20014
   PubMed Web of Science ®Google Scholar
• Maisuradze, G. G., & Leitner, D. M. (2006). Principal component analysis of fast-folding λ-repressor mutants. Chemical Physics Letters, 421, 5–10. doi:10.1016/j.cplett.2006.01.044
   Web of Science ®Google Scholar
• Maisuradze, G. G., & Leitner, D. M. (2007). Free energy landscape of a biomolecule in dihedral principal component space: Sampling convergence and correspondence between structures and minima. Proteins: Structure, Function, and Bioinformatics, 67, 569–578. doi:10.1002/prot.21344
   PubMed Web of Science ®Google Scholar
• Marianayagam, N. J., & Jackson, S. E. (2005). Native-state dynamics of the ubiquitin family: Implications for function and evolution. Journal of The Royal Society Interface, 2, 47–54. doi:10.1098/rsif.2004.0025
   PubMed Web of Science ®Google Scholar
• Morris, G. M., Goodsell, D. S., Halliday, R. S., Huey, R., Hart, W. E., Belew, R. K., & Olson, A. J. (1998). Automated docking using a Lamarckian genetic algorithm and an empirical binding free energy function. Journal of Computational Chemistry, 19, 1639–1662. doi:10.1002/(SICI)1096-987X(19981115)19:14<1639:AID-JCC10>3.0.CO;2-B
   Web of Science ®Google Scholar
• Moult, J. (2005). A decade of CASP: Progress, bottlenecks and prognosis in protein structure prediction. Current Opinion in Structural Biology, 15, 285–289. doi:10.1016/j.sbi.2005.05.011
   PubMed Web of Science ®Google Scholar
• Mu, Y., Nguyen, P. H., & Stock, G. (2005). Energy landscape of a small peptide revealed by dihedral angle principal component analysis. Proteins: Structure, Function, and Bioinformatics, 58, 45–52. doi:10.1002/prot.20310
   PubMed Web of Science ®Google Scholar
• Ng, H. W., Laughton, C. A., & Doughty, S. W. (2013). Molecular dynamics simulations of the adenosine A2a receptor: Structural stability, sampling, and convergence. Journal of Chemical Information and Modeling, 53, 1168–1178. doi:10.1021/ci300610w
   PubMed Web of Science ®Google Scholar
• Nurisso, A., Daina, A., & Walker, R. C. (2012). A practical introduction to molecular dynamics simulations: Applications to homology modeling. In Andrew J. W. Orry & Ruben Abagyan (Eds.), Homology Modeling: Methods and Protocols (pp. 137–173). New york, NY: Springer.
   Google Scholar
• Oostenbrink, C., Villa, A., Mark, A. E., & Van Gunsteren, W. F. (2004). A biomolecular force field based on the free enthalpy of hydration and solvation: The GROMOS force-field parameter sets 53A5 and 53A6. Journal of Computational Chemistry, 25, 1656–1676. doi:10.1002/jcc.20090
   PubMed Web of Science ®Google Scholar
• Papaleo, E., Mereghetti, P., Fantucci, P., Grandori, R., & De Gioia, L. (2009). Free-energy landscape, principal component analysis, and structural clustering to identify representative conformations from molecular dynamics simulations: The myoglobin case. Journal of Molecular Graphics and Modelling, 27, 889–899. doi:10.1016/j.jmgm.2009.01.006
   PubMed Web of Science ®Google Scholar
• Papaleo, E., Pasi, M., Riccardi, L., Sambi, I., Fantucci, P., & Gioia, L. D. (2008). Protein flexibility in psychrophilic and mesophilic trypsins. Evidence of evolutionary conservation of protein dynamics in trypsin-like serine-proteases. FEBS Letters, 582, 1008–1018. doi:10.1016/j.febslet.2008.02.048
   PubMed Web of Science ®Google Scholar
• Paris, G., Ramseyer, C., & Enescu, M. (2014). A principal component analysis of the dynamics of subdomains and binding sites in human serum albumin. Biopolymers, 101, 561–572. doi:10.1002/bip.22418
   PubMed Web of Science ®Google Scholar
• Patra, M., Karttunen, M., Hyvönen, M. T., Falck, E., Lindqvist, P., & Vattulainen, I. (2003). Molecular dynamics simulations of lipid bilayers: Major artifacts due to truncating electrostatic interactions. Biophysical Journal, 84, 3636–3645. doi:10.1016/S0006-3495(03)75094-2
   PubMed Web of Science ®Google Scholar
• Petrey, D., Xiang, Z., Tang, C. L., Xie, L., Gimpelev, M., Mitros, T., … Schlessinger, A. (2003). Using multiple structure alignments, fast model building, and energetic analysis in fold recognition and homology modeling. Proteins: Structure, Function, and Genetics, 53(S6), 430–435. doi:10.1002/prot.10550
   PubMed Web of Science ®Google Scholar
• Pierce, K. L., Premont, R. T., & Lefkowitz, R. J. (2002). Signalling: Seven-transmembrane receptors. Nature Reviews Molecular Cell Biology, 3, 639–650. doi:10.1038/nrm908
   PubMed Web of Science ®Google Scholar
• Rosenbaum, D. M., Cherezov, V., Hanson, M. A., Rasmussen, S. G., Thian, F. S., Kobilka, T. S., … Stevens, R. C. (2007). GPCR engineering yields high-resolution structural insights into β2-adrenergic receptor function. Science, 318, 1266–1273. doi:10.1126/science.1150609
   PubMed Web of Science ®Google Scholar
• Šali, A., & Blundell, T. L. (1993). Comparative protein modelling by satisfaction of spatial restraints. Journal of Molecular Biology, 234, 779–815. doi:10.1006/jmbi.1993.1626
   PubMed Web of Science ®Google Scholar
• Sebhat, I. K., Franklin, C., Lo, M. M.-C., Chen, D., Jewell, J. P., Miller, R., … Kelly, T. M. (2010). Discovery of MK-5046, a potent, selective bombesin receptor subtype-3 agonist for the treatment of obesity. ACS Medicinal Chemistry Letters, 2, 43–47. doi:10.1021/ml100196d
   PubMed Web of Science ®Google Scholar
• Shahlaei, M., Fassihi, A., Papaleo, E., & Pourfarzam, M. (2013). Molecular dynamics simulation of chemokine receptors in lipid bilayer: A case study on C-C chemokine receptor type 2. Chemical Biology & Drug Design, 82, 534–545. doi:10.1111/cbdd.12179
   PubMed Web of Science ®Google Scholar
• Shahlaei, M., Madadkar-Sobhani, A., Fassihi, A., & Saghaie, L. (2011). Exploring a model of a chemokine receptor/ligand complex in an explicit membrane environment by molecular dynamics simulation: The human CCR1 receptor. Journal of Chemical Information and Modeling, 51, 2717–2730. doi:10.1021/ci200261f
   PubMed Web of Science ®Google Scholar
• Shahlaei, M., Madadkar-Sobhani, A., Mahnam, K., Fassihi, A., Saghaie, L., & Mansourian, M. (2011). Homology modeling of human CCR5 and analysis of its binding properties through molecular docking and molecular dynamics simulation. Biochimica et Biophysica Acta (BBA)-Biomembranes, 1808, 802–817. doi:10.1016/j.bbamem.2010.12.00410.1016/j.bbamem.2010.12.004
   PubMed Web of Science ®Google Scholar
• Shu, F., Ramakrishnan, V., & Schoenborn, B. P. (2000). Enhanced visibility of hydrogen atoms by neutron crystallography on fully deuterated myoglobin. Proceedings of the National academy of Sciences of the United States of America , 97, 3872–3877. doi:10.1073/pnas.060024697
   PubMed Web of Science ®Google Scholar
• Stenkamp, R., Filipek, S., Driessen, C., Teller, D., & Palczewski, K. (2002). Crystal structure of rhodopsin: A template for cone visual pigments and other G protein-coupled receptors. Biochimica et Biophysica Acta (BBA)-Biomembranes, 1565, 168–182. doi:10.1016/S0005-2736(02)00567-910.1016/S0005-2736(02)00567-9
   PubMed Web of Science ®Google Scholar
• Stevens, R. C., Cherezov, V., Katritch, V., Abagyan, R., Kuhn, P., Rosen, H., & Wüthrich, K. (2013). The GPCR Network: A large-scale collaboration to determine human GPCR structure and function. Nature Reviews Drug Discovery, 12, 25–34. doi:10.1038/nrd3859
   PubMed Web of Science ®Google Scholar
• Thompson, A. A., Liu, W., Chun, E., Katritch, V., Wu, H., Vardy, E., … Calo, G. (2012). Structure of the nociceptin/orphanin FQ receptor in complex with a peptide mimetic. Nature, 485, 395–399. doi:10.1038/nature11085
   PubMed Web of Science ®Google Scholar
• van Aalten, D. M., Bywater, R., Findlay, J. B., Hendlich, M., Hooft, R. W., & Vriend, G. (1996). PRODRG, a program for generating molecular topologies and unique molecular descriptors from coordinates of small molecules. Journal of Computer-Aided Molecular Design, 10, 255–262. doi:10.1007/BF00355047
   PubMed Web of Science ®Google Scholar
• Van Der Spoel, D., Lindahl, E., Hess, B., Groenhof, G., Mark, A. E., & Berendsen, H. J. (2005). GROMACS: Fast, flexible, and free. Journal of Computational Chemistry, 26, 1701–1718. doi:10.1002/jcc.20291
   PubMed Web of Science ®Google Scholar
• Wales, D. J. (2005). The energy landscape as a unifying theme in molecular science. Philosophical Transactions of the Royal Society A: Mathematical, Physical and Engineering Sciences, 363, 357–377. doi:10.1098/rsta.2004.1497
   PubMed Web of Science ®Google Scholar
• Warne, T., Moukhametzianov, R., Baker, J. G., Nehmé, R., Edwards, P. C., Leslie, A. G., … Tate, C. G. (2011). The structural basis for agonist and partial agonist action on a β1-adrenergic receptor. Nature, 469, 241–244. doi:10.1038/nature09746
   PubMed Web of Science ®Google Scholar
• Warne, T., Serrano-Vega, M. J., Baker, J. G., Moukhametzianov, R., Edwards, P. C., Henderson, R., … Schertler, G. F. (2008). Structure of a β1-adrenergic G-protein-coupled receptor. Nature, 454, 486–491. doi:10.1038/nature07101
   PubMed Web of Science ®Google Scholar
• Wlodek, S. T., Clark, T. W., Scott, L. R., & McCammon, J. A. (1997). Molecular dynamics of acetylcholinesterase dimer complexed with tacrine. Journal of the American Chemical Society, 119, 9513–9522. doi:10.1021/ja971226d
   Web of Science ®Google Scholar
• Xiang, Z. (2006). Advances in homology protein structure modeling. Current protein & peptide science, 7, 217–227. doi:10.2174/138920306777452312.
   PubMed Web of Science ®Google Scholar
• Zagrovic, B., & Pande, V. S. (2004). How does averaging affect protein structure comparison on the ensemble level? Biophysical Journal, 87, 2240–2246. doi:10.1529/biophysj.104.042184
   PubMed Web of Science ®Google Scholar