Principal Component Analysis reveals correlation of cavities evolution and functional motions in proteins

Journal of Molecular Graphics and Modelling

Volumn 55, Issue , 2015, Pages 13-24

  Desdouits, Nathan ^a   Nilges, Michael ^a   Blondel, Arnaud ^a  

^a INSTITUT PASTEUR   (France)

Author keywords

Cavity geometry evolution; Drug design; Functional analysis; Molecular dynamics; Principal component analysis; Protein cavities

Indexed keywords

BIOLOGY; CARBON MONOXIDE; COMPLEX NETWORKS; CONFORMATIONS; FUNCTIONAL ANALYSIS; GEOMETRY; MOLECULAR DYNAMICS; PROTEINS;

BIOLOGICAL FUNCTIONS; CAVITY GEOMETRY; DRUG DESIGN; EFFICIENT ANALYSIS; FUNCTIONAL MOTIONS; MOLECULAR DYNAMICS SIMULATIONS; PROTEIN CAVITY; PROTEIN CONFORMATION;

PRINCIPAL COMPONENT ANALYSIS;

CARBON MONOXIDE; ENVELOPE PROTEIN; LYSOZYME; MYOGLOBIN; XENON; PROTEIN;

AMPLITUDE MODULATION; ARTICLE; BINDING SITE; COMPLEX FORMATION; CONTROLLED STUDY; CORRELATIONAL STUDY; DENGUE VIRUS; EVOLUTION; GEOMETRY; MOLECULAR DYNAMICS; MOTION; NONHUMAN; PRINCIPAL COMPONENT ANALYSIS; PROTEIN CONFORMATION; PROTEIN FUNCTION; SIMULATION; SPERM WHALE; ANIMAL; CHEMISTRY; CHICKEN; WHALE;

PHYSETERIDAE;

ANIMALS; BINDING SITES; CARBON MONOXIDE; CHICKENS; MOLECULAR DYNAMICS SIMULATION; MOTION; MURAMIDASE; MYOGLOBIN; PRINCIPAL COMPONENT ANALYSIS; PROTEIN CONFORMATION; PROTEINS; WHALES;

EID: 84949114871     PISSN: 10933263     EISSN: 18734243     Source Type: Journal    
DOI: 10.1016/j.jmgm.2014.10.011     Document Type: Article

References (53)

1. S.J. Wodak, J. Janin, Structural basis of macromolecular recognition, in: J. Janin, S.J. Wodak (Eds.), Protein Modules and Protein-Protein Interaction, Volume 61 of Advances in Protein Chemistry, Academic Press, Amsterdam, 2002, pp. 9-73.
2. K.D. Corbett, T. Alber, The many faces of Ras: recognition of small GTP-binding proteins, Trends Biochem. Sci. 26 (12) (2001) 710-716.
3. R.L. DesJarlais, R.P. Sheridan, G.L. Seibel, S.J. Dixon, I.D. Kuntz, R. Venkataraghavan, Using shape complementarity as an initial screen in designing ligands for a receptor binding site of known three-dimensional structure, J. Med. Chem. 31 (4) (1988) 722-729.
4. R. Chen, Z. Weng, A novel shape complementarity scoring function for protein-protein docking, Proteins 51 (3) (2003) 397-408.
5. C.M. Venkatachalam, X. Jiang, T. Oldfield, M. Waldman, Ligandfit: a novel method for the shape-directed rapid docking of ligands to protein active sites, J. Mol. Gr. Modell. 21 (4) (2003) 289-307.
6. A. Elisabeth Eriksson, W.A. Baase, X.-J. Zhang, D.W. Heinz, M. Blaber, E.P. Baldwin, B.W. Matthews, Response of a protein structure to cavity-creating mutations and its relation to the hydrophobic effect, Science 255 (5041) (1992) 178-183.
7. R. Elber, M. Karplus, Enhanced sampling in molecular dynamics: use of the time-dependent hartree approximation for a simulation of carbon monoxide diffusion through myoglobin, J. Am. Chem. Soc. 112 (25) (1990) 9161-9175.
8. R. Elber, Ligand diffusion in globins: simulations versus experiment, Curr. Opin. Struct. Biol. 20 (2) (2010) 162-167.
9. R.C. Wade, P.J. Winn, I. Schlichting, Sudarko, A survey of active site access channels in cytochromes {P450}, J. Inorg. Biochem. 98 (7) (2004) 1175-1182.
10. Y. Miao, J. Baudry, Active-site hydration and water diffusion in cytochrome p450cam: a highly dynamic process, Biophys. J. 101 (6) (2011) 1493-1503.
11. A.G. Watts, I. Damager, M.L. Amaya, A. Buschiazzo, P. Alzari, A.C. Frasch, S.G. Withers, Trypanosoma cruzi trans-sialidase operates through a covalent sialylenzyme intermediate: tyrosine is the catalytic nucleophile, J. Am. Chem. Soc. 125 (25) (2003) 7532-7533.
12. S. Liu, J.S. Chang, J.T. Herberg, M.-M. Horng, P.K. Tomich, A.H. Lin, K.R. Marotti, Allosteric inhibition of Staphylococcus aureus D-alanine:D-alanine ligase revealed by crystallographic studies, Proc. Natl. Acad. Sci. U. S. A. 103 (41) (2006) 15178-15183.
13. R.D. Vale, R.A. Milligan, The way things move: looking under the hood of molecular motor proteins, Science 288 (5463) (2000) 88-95.
14. J. Simon, Hubbard, Patrick Argos, Cavities and packing at protein interfaces, Protein Sci. 3 (12) (1994) 2194-2206.
15. Shrihari Sonavane, Pinak Chakrabarti, Cavities and atomic packing in protein structures and interfaces, PLoS Comput. Biol. 4 (9) (2008) e1000188, 09.
16. Susanne Eyrisch, Volkhard Helms, What induces pocket openings on protein surface patches involved in protein-protein interactions? J. Comput. Aided Mol. Des. 23 (2) (2009) 73-86.
17. Cecilia Bossa, Andrea Amadei, Isabella Daidone, Massimiliano Anselmi, Beatrice Vallone, Maurizio Brunori, Alfredo Di Nola, Molecular dynamics simulation of sperm whale myoglobin: effects of mutations and trapped CO on the structure and dynamics of cavities, Biophys. J. 89 (1) (2005) 465-474.
18. J.Z. Ruscio, D. Kumar, M. Shukla, M.G. Prisant, T.M. Murali, A.V. Onufriev, Atomic level computational identification of ligand migration pathways between solvent and binding site in myoglobin, Proc. Natl. Acad. Sci. U. S. A. 105 (27) (2008) 9204-9209.
19. M.A. Scorciapino, A. Robertazzi, M. Casu, P. Ruggerone, M. Ceccarelli, Breathing motions of a respiratory protein revealed by molecular dynamics simulations, J. Am. Chem. Soc. 131 (33) (2009) 11825-11832.
20. M. Gabba, S. Abbruzzetti, F. Spyrakis, F. Forti, S. Bruno, A. Mozzarelli, F. Javier Luque, C. Viappiani, P. Cozzini, M. Nardini, F. Germani, M. Bolognesi, L. Moens, S. Dewilde, CO rebinding kinetics and molecular dynamics simulations highlight dynamic regulation of internal cavities in human cytoglobin, PLOS ONE 8 (1) (2013) e49770, 01.
21. Susanne Eyrisch, Volkhard Helms, Transient pockets on protein surfaces involved in protein-protein interaction, J. Med. Chem. 50 (15) (2007) 3457-3464.
22. P. Schmidtke, A. Bidon-Chanal, F. Javier Luque, X. Barril, MDpocket: open-source cavity detection and characterization on molecular dynamics trajectories, Bioinformatics 27 (23) (2011) 3276-3285.
23. M. Krone, M. Falk, S. Rehm, J. Pleiss, T. Ertl, Interactive exploration of protein cavities, Comput. Gr. Forum 30 (3) (2011) 673-682.
24. Alexander Metz, Christopher Pfleger, Hannes Kopitz, Stefania Pfeiffer-Marek, Karl-Heinz Baringhaus, Holger Gohlke, Hot spots and transient pockets: predicting the determinants of small-molecule binding to a protein-protein interface, J. Chem. Inf. Model. 52 (1) (2012) 120-133.
25. P. Ashford, D. Moss, A. Alex, S. Yeap, A. Povia, I. Nobeli, M. Williams, Visualisation of variable binding pockets on protein surfaces by probabilistic analysis of related structure sets, BMC Bioinformatics 13 (1) (2012) 39.
26. D.B. Kokh, S. Richter, S. Henrich, P. Czodrowski, F. Rippmann, R.C. Wade, TRAPP: a tool for analysis of transient binding pockets in proteins, J. Chem. Inf. Model. 53 (5) (2013) 1235-1252.
27. B. Lee, F.M. Richards, The interpretation of protein structures: estimation of static accessibility, J. Mol. Biol. 55 (3) (1971) 379-400.
28. M.L. Connolly, Solvent-accessible surfaces of proteins and nucleic acids, Science 221 (4612) (1983) 709-713.
29. J. Liang, C. Woodward, C. Woodward, H. Edelsbrunner, H. Edelsbrunner, Anatomy of protein pockets and cavities: measurement of binding site geometry and implications for ligand design, Protein Sci. 7 (9) (1998) 1884-1897.
30. S.J. Lee, M.S. McCormick, S.J. Lippard, U.-S. Cho, Control of substrate access to the active site in methane monooxygenase, Nature 494 (7437) (2013) 380-384, 02.
31. B.W. Matthews, Structural and genetic analysis of the folding and function of t4 lysozyme, FASEB J. 10 (1) (1996) 35-41.
32. S.J. Hubbard, P. Argos, A functional role for protein cavities in domain:domain motions, J. Mol. Biol. 261 (2) (1996) 289-300.
33. Y. Modis, S. Ogata, D. Clements, S.C. Harrison, Structure of the dengue virus envelope protein after membrane fusion, Nature 427 (6972) (2004) 313-319.
34. E. Laine, C. Goncalves, J.C. Karst, A. Lesnard, S. Rault, W.-J. Tang, T.E. Malliavin, D. Ladant, A. Blondel, Use of allostery to identify inhibitors of calmodulin-induced activation of Bacillus anthracis edema factor, Proc. Natl. Acad. Sci. U. S. A. 107 (25) (2010) 11277-11282.
35. I.D. Kuntz, J.M. Blaney, S.J. Oatley, R. Langridge, T.E. Ferrin, A geometric approach to macromolecule-ligand interactions, J. Mol. Biol. 161 (2) (1982) 269-288.
36. S. Pérot, S. Olivier, M.A. Miteva, A.-C. Camproux, B.O. Villoutreix, Druggable pockets and binding site centric chemical space: a paradigm shift in drug discovery, Drug Discov. Today 15 (15-16) (2010) 656-667.
37. C. B-Rao, J. Subramanian, S.D. Sharma, Managing protein flexibility in docking and its applications, Drug Discov. Today 14 (7-8) (2009) 394-400.
38. J.D. Durrant, J.A. McCammon, Computer-aided drug-discovery techniques that account for receptor flexibility, Curr. Opin. Pharmacol. 10 (6) (2010) 770-774.
39. C.D. Wassman, R. Baronio, Ö. Demir, B.D. Wallentine, C.-K. Chen, L.V. Hall, F. Salehi, D.-W. Lin, B.P. Chung, G. Wesley Hatfield, A. Richard Chamberlin, H. Luecke, R.H. Lathrop, P. Kaiser, R.E. Amaro, Computational identification of a transiently open l1/s3 pocket for reactivation of mutant p53, Nat. Commun. 4 (January) (2013) 1407.
40. I.M. Withers, M.P. Mazanetz, H. Wang, P.M. Fischer, C.A. Laughton, Active site pressurization: a new tool for structure-guided drug design and other studies of protein flexibility, J. Chem. Inf. Model. 48 (7) (2008) 1448-1454.
41. R. Abagyan, I. Kufareva, The flexible pocketome engine for structural chemogenomics, in: E. Jacoby (Ed.), Chemogenomics, Volume 575 of Methods in Molecular Biology, Humana Press, Clifton, NJ, 2009, pp. 249-279.
42. G. Bottegoni, I. Kufareva, M. Totrov, R. Abagyan, A new method for ligand docking to flexible receptors by dual alanine scanning and refinement (SCARE), J. Comput. Aided Mol. Des. 22 (5) (2008) 311-325.
43. T. Kawabata, Detection of multiscale pockets on protein surfaces using mathematical morphology, Proteins 78 (5) (2010) 1195-1211.
44. R.F. Tilton, I.D. Kuntz, G.A. Petsko, Cavities in proteins: structure of a metmyoglobin xenon complex solved to 1.9. ang, Biochemistry 23 (13) (1984) 2849-2857.
45. L. Maragliano, G. Cottone, G. Ciccotti, E. Vanden-Eijnden, Mapping the network of pathways of CO diffusion in myoglobin, J. Am. Chem. Soc. 132 (3) (2010) 1010-1017.
46. A. Amadei, M.A. Ceruso, A. Di Nola, On the convergence of the conformational coordinates basis set obtained by the essential dynamics analysis of proteins' molecular dynamics simulations, Proteins 36 (4) (1999) 419-424.
47. J.C. Phillips, R. Braun, W. Wang, J. Gumbart, E. Tajkhorshid, E. Villa, C. Chipot, R.D. Skeel, L. Kalé, K. Schulten, Scalable molecular dynamics with NAMD, J. Comput. Chem. 26 (16) (2005) 1781-1802.
48. B.R. Brooks, C.L. Brooks, A.D. Mackerell, L. Nilsson, R.J. Petrella, B. Roux, Y. Won, G. Archontis, C. Bartels, S. Boresch, A. Caflisch, L. Caves, Q. Cui, A.R. Dinner, M. Feig, S. Fischer, J. Gao, M. Hodoscek, W. Im, K. Kuczera, T. Lazaridis, J. Ma, V. Ovchinnikov, E. Paci, R.W. Pastor, C.B. Post, J.Z. Pu, M. Schaefer, B. Tidor, R.M. Venable, H.L. Woodcock, X. Wu, W. Yang, D.M. York, M. Karplus, CHARMM: the biomolecular simulation program, J. Comput. Chem. 30 (10) (2009) 1545-1614.
49. M. Ester, H.-P. Kriegel, Jörg Sander, X. Xu, A density-based algorithm for discovering clusters in large spatial databases with noise KDD, vol. 96, 1996, pp. 226-231.
50. L. Benkaidali, F. André, B. Maouche, P. Siregar, M. Benyettou, F. Maurel, M. Petitjean, Computing cavities, channels, pores and pockets in proteins from non-spherical ligands models, Bioinformatics 30 (6) (2014) 792-800.
51. J. Abramson, I. Smirnova, V. Kasho, G. Verner, H. Ronald Kaback, S. Iwata, Structure and mechanism of the lactose permease of Escherichia coli, Science 301 (5633) (2003) 610-615.
52. I. Smirnova, V. Kasho, J. Sugihara, H. Ronald Kaback, Opening the periplasmic cavity in lactose permease is the limiting step for sugar binding, Proc. Natl. Acad. Sci. U. S. A. 108 (37) (2011) 15147-15151.
53. V. Chaptal, S. Kwon, M.R. Sawaya, L. Guan, H. Ronald Kaback, J. Abramson, Crystal structure of lactose permease in complex with an affinity inactivator yields unique insight into sugar recognition, Proc. Natl. Acad. Sci. U. S. A. 108 (23) (2011) 9361-9366.