439
Views
8
CrossRef citations to date
0
Altmetric
Review Article

Adaptability in protein structures: structural dynamics and implications in ligand design

, , , , &
Pages 298-321 | Received 15 May 2013, Accepted 04 Dec 2013, Published online: 16 Jan 2014

References

  • Alonso,H.,Bliznyuk,A. A., &Gready,J. E. (2006).Combining docking and molecular dynamic simulations in drug design.Medicinal Research Reviews,26,531–568.10.1002/(ISSN)1098-1128
  • Amadei,A.,Linssen,A. B., &Berendsen,H. J. (1993).Essential dynamics of proteins.Proteins: Structure, Function, and Genetics,17,412–425.10.1002/(ISSN)1097-0134
  • Aravind, L., Anantharaman, V., & Iyer, L. M. (2003). Evolutionary connections between bacterial and eukaryotic signaling systems: A genomic perspective. Current Opinion in Microbiology, 6, 490–497.
  • Arold,S.,O’Brien,R.,Franken,P.,Strub,M. P.,Hoh,F.,Dumas,C., &Ladbury,J. E. (1998).RT loop flexibility enhances the specificity of Src family SH3 domains for HIV-1 Nef.Biochemistry,37,14683–14691.10.1021/bi980989q
  • Atilgan,A. R.,Durell,S. R.,Jernigan,R. L.,Demirel,M. C.,Keskin,O., &Bahar,I. (2001).Anisotropy of fluctuation dynamics of proteins with an elastic network model.Biophysical Journal,80,505–515.10.1016/S0006-3495(01)76033-X
  • Bahar,I.,Atilgan,A. R., &Erman,B. (1997).Direct evaluation of thermal fluctuations in proteins using a single-parameter harmonic potential.Folding and Design,2,173–181.10.1016/S1359-0278(97)00024-2
  • Bahar,I., &Rader,A. J. (2005).Coarse-grained normal mode analysis in structural biology.Current Opinion in Structural Biology,15,586–592.10.1016/j.sbi.2005.08.007
  • Bakan,A., &Bahar,I. (2009).The intrinsic dynamics of enzymes plays a dominant role in determining the structural changes induced upon inhibitor binding.Proceedings of the National Academy of Sciences,106,14349–14354.10.1073/pnas.0904214106
  • Bayliss,R.,Sardon,T.,Vernos,I., &Conti,E. (2003).Structural basis of Aurora-A activation by TPX2 at the mitotic spindle.Molecular Cell,12,851–862.10.1016/S1097-2765(03)00392-7
  • Bhattacharyya,R. P.,Remenyi,A.,Good,M. C.,Bashor,C. J.,Falick,A. M., &Lim,W. A. (2006).The Ste5 scaffold allosterically modulates signaling output of the yeast mating pathway.Science,311,822–826.10.1126/science.1120941
  • Biondi,R. M., &Nebreda,A. R. (2003).Signalling specificity of Ser/Thr protein kinases through docking-site-mediated interactions.Biochemical Journal,372,1–13.10.1042/BJ20021641
  • Boehr,D. D.,McElheny,D.,Dyson,H. J., &Wright,P. E. (2006).The dynamic energy landscape of dihydrofolate reductase catalysis.Science,313,1638–1642.10.1126/science.1130258
  • Boehr,D. D.,Nussinov,R., &Wright,P. E. (2009).The role of dynamic conformational ensembles in biomolecular recognition.Nature Chemical Biology,5,789–796.10.1038/nchembio.232
  • Borbulevych,O. Y.,Piepenbrink,K. H.,Gloor,B. E.,Scott,D. R.,Sommese,R. F.,Cole,D. K.,Sewell,A. K., &Baker,B. M. (2009).T cell receptor cross-reactivity directed by antigen-dependent tuning of peptide-MHC molecular flexibility.Immunity,31,885–896.10.1016/j.immuni.2009.11.003
  • Böttger,A.,Böttger,V.,Garcia-Echeverria,C.,Chène,P.,Hochkeppel,H. K.,Sampson,W.,Ang,K.,Howard,S. F.,Picksley,S. M., &Lane,D. P. (1997).Molecular characterization of the hdm2-p53 interaction.Journal of Molecular Biology,269,744–756.10.1006/jmbi.1997.1078
  • Brooks,B. R.,Brooks,C. L.,3rd,Mackerell,A. D.,Jr,Nilsson,L.,Petrella,R. J.,Roux,B., …Karplus,M. (2009).CHARMM: The biomolecular simulation program.Journal of Computational Chemistry,30,1545–1614.10.1002/jcc.v30:10
  • Brown,C. J.,Lain,S.,Verma,C. S.,Fersht,A. R., &Lane,D. P. (2009).Awakening guardian angels: drugging the p53 pathway.Nature Reviews Cancer,9,862–873.10.1038/nrc2763
  • Camacho,C. J., &Vajda,S. (2002).Protein–protein association kinetics and protein docking.Current Opinion in Structural Biology,12,36–40.10.1016/S0959-440X(02)00286-5
  • Carlson,H. A., &McCammon,J. A. (2000).Accommodating protein flexibility in computational drug design.Molecular Pharmacology,57,213–218.
  • Case,D. A. (1994).Normal mode analysis of protein dynamics.Current Opinion in Structural Biology,4,285–290.10.1016/S0959-440X(94)90321-2
  • Case,D. A.,Cheatham,T. E.,3rd,Darden,T.,Gohlke,H.,Luo,R.,Merz,K. M.,Jr., …Woods,R. J. (2005).The Amber biomolecular simulation programs.Journal of Computational Chemistry,26,1668–1688.10.1002/(ISSN)1096-987X
  • Chakraborti,S.,Chakravarty,D.,Gupta,S.,Chatterji,B. P.,Dhar,G.,Poddar,A., …Bhattacharyya,B. (2012).Discrimination of ligands with different flexibilities resulting from the plasticity of the binding site in tubulin.Biochemistry,51,7138–7148.10.1021/bi300474q
  • Chauhan,D.,Velankar,M.,Brahmandam,M.,Hideshima,T.,Podar,K.,Richardson,P., …Anderson,K. C. (2007).A novel Bcl-2/Bcl-XL/Bcl-w inhibitor ABT-737 as therapy in multiple myeloma.Oncogene,26,2374–2380.10.1038/sj.onc.1210028
  • Chen,R.,Li,L., &Weng,Z. (2003).ZDOCK: An initial-stage protein-docking algorithm.Proteins: Structure, Function, and Genetics,52,80–87.10.1002/(ISSN)1097-0134
  • Chen,R., &Weng,Z. (2002).Docking unbound proteins using shape complementarity, desolvation, and electrostatics.Proteins: Structure, Function, and Genetics,47,281–294.10.1002/(ISSN)1097-0134
  • Chocholoušová,J., &Feig,M. (2006).Balancing an accurate representation of the molecular surface in generalized born formalisms with integrator stability in molecular dynamics simulations.Journal of Computational Chemistry,27,719–729.10.1002/jcc.v27:6
  • Cicchetti,P.,Mayer,B. J.,Thiel,G., &Baltimore,D. (1992).Identification of a protein that binds to the SH3 region of Abl and is similar to Bcr and GAP-rho.Science,257,803–806.10.1126/science.1379745
  • Cohen,P. (2002).Protein kinases–The major drug targets of the twenty-first century?Nature Reviews Drug Discovery,1,309–315.10.1038/nrd773
  • Comeau,S. R.,Gatchell,D. W.,Vajda,S., &Camacho,C. J. (2004).ClusPro: An automated docking and discrimination method for the prediction of protein complexes.Bioinformatics,20,45–50.10.1093/bioinformatics/btg371
  • Dar, A. C., Dever, T. E., & Sicheri, F. (2005). Higher-order substrate recognition of eIF2alpha by the RNA-dependent protein kinase PKR. Cell, 122, 887–900.
  • Dastidar,S. G.,Lane,D. P., &Verma,C. S. (2008).Multiple peptide conformations give rise to similar binding affinities: Molecular simulations of p53-MDM2.Journal of the American Chemical Society,130,13514–13515.10.1021/ja804289g
  • Dastidar,S. G.,Lane,D. P., &Verma,C. S. (2009).Modulation of p53 binding to MDM2: Computational studies reveal important roles of Tyr100.BMC Bioinformatics,10(Suppl 15),S6.10.1186/1471-2105-10-S15-S6
  • Dastidar,S. G.,Raghunathan,D.,Nicholson,J.,Hupp,T. R.,Lane,D. P., &Verma,C. S. (2011).Chemical states of the N-terminal “lid” of MDM2 regulate p53 binding: simulations reveal complexities of modulation.Cell Cycle,10,82–89.10.4161/cc
  • delSol,A.,Tsai,C. J.,Ma,B., &Nussinov,R. (2009).The origin of allosteric functional modulation: Multiple pre-existing pathways.Structure,17,1042–1050.10.1016/j.str.2009.06.008
  • Denisov,A. Y.,Madiraju,M. S.,Chen,G.,Khadir,A.,Beauparlant,P.,Attardo,G., …Gehring,K. (2003).Solution structure of human BCL-w: Modulation of ligand binding by the C-terminal helix.Journal of Biological Chemistry,278,21124–21128.10.1074/jbc.M301798200
  • Dominguez,C.,Boelens,R., &Bonvin,A. M. (2003).HADDOCK: A protein-protein docking approach based on biochemical or biophysical information.Journal of the American Chemical Society,125,1731–1737.10.1021/ja026939x
  • Fernandes,N., &Allbritton,N. L. (2009).Effect of the DEF motif on phosphorylation of peptide substrates by ERK.Biochemical and Biophysical Research Communications,387,414–418.10.1016/j.bbrc.2009.07.049
  • Fernandez-Recio,J.,Totrov,M., &Abagyan,R. (2003).ICM-DISCO docking by global energy optimization with fully flexible side-chains.Proteins: Structure, Function, and Genetics,52,113–117.10.1002/(ISSN)1097-0134
  • Fischer,E. (1894).Einfluss der Configuration auf die Wirkung der Enzyme [Influence of configuration on the effect of enzyme].Berichte der deutschen chemischen Gesellschaft[Reports of the German Chemical Society],27,2985–2993.10.1002/(ISSN)1099-0682
  • Fischer,D. (2006).Servers for protein structure prediction.Current Opinion in Structural Biology,16,178–182.10.1016/j.sbi.2006.03.004
  • Gabb,H. A.,Jackson,R. M., &Sternberg,M. J. (1997).Modelling protein docking using shape complementarity, electrostatics and biochemical information.Journal of Molecular Biology,272,106–120.10.1006/jmbi.1997.1203
  • Gabdoulline,R. R., &Wade,R. C. (1997).Simulation of the diffusional association of barnase and barstar.Biophysical Journal,72,1917–1929.10.1016/S0006-3495(97)78838-6
  • Gabdoulline,R. R., &Wade,R. C. (1998).Brownian dynamics simulation of protein–protein diffusional encounter.Methods,14,329–341.10.1006/meth.1998.0588
  • Gardiner,E. J.,Willett,P., &Artymiuk,P. J. (2001).Protein docking using a genetic algorithm.Proteins: Structure, Function, and Genetics,44,44–56.10.1002/(ISSN)1097-0134
  • Gaudreault,F.,Chartier,M., &Najmanovich,R. (2012).Side-chain rotamer changes upon ligand binding: common, crucial, correlate with entropy and rearrange hydrogen bonding.Bioinformatics,28,i423–i430.10.1093/bioinformatics/bts395
  • Goel,M.,Krishnan,L.,Kaur,S.,Kaur,K. J., &Salunke,D. M. (2004).Plasticity within the antigen-combining site may manifest as molecular mimicry in the humoral immune response.Journal of Immunology,173,7358–7367.
  • Gray,J. J.,Moughon,S.,Wang,C.,Schueler-Furman,O.,Kuhlman,B.,Rohl,C. A., &Baker,D. (2003).Protein–protein docking with simultaneous optimization of rigid-body displacement and side-chain conformations.Journal of Molecular Biology,331,281–299.10.1016/S0022-2836(03)00670-3
  • Gunsteren,P. D. W. F., &Berendsen,P. D. H. J. C (1990).Computer simulation of molecular dynamics: Methodology, applications, and perspectives in chemistry.Angewandte Chemie International Edition in English,29,992–1023.
  • Halperin,I.,Ma,B.,Wolfson,H., &Nussinov,R. (2002).Principles of docking: An overview of search algorithms and a guide to scoring functions.Proteins: Structure, Function, and Genetics,47,409–443.10.1002/(ISSN)1097-0134
  • Hanasaki,I.,Haga,T., &Kawano,S. (2008).The antigen–antibody unbinding process through steered molecular dynamics of a complex of an Fv fragment and lysozyme.Journal of Physics: Condensed Matter,20, 255238–255347.
  • Herman,M. D.,Nyman,T.,Welin,M.,Lehtio,L.,Flodin,S.,Tresaugues,L., …Nordlund,P. (2008).Completing the family portrait of the anti-apoptotic Bcl-2 proteins: Crystal structure of human Bfl-1 in complex with Bim.FEBS Letters,582,3590–3594.10.1016/j.febslet.2008.09.028
  • Hoofnagle,A. N.,Resing,K. A.,Goldsmith,E. J., &Ahn,N. G. (2001).Changes in protein conformational mobility upon activation of extracellular regulated protein kinase-2 as detected by hydrogen exchange.Proceedings of the National Academy of Sciences,98,956–961.10.1073/pnas.98.3.956
  • Horiuchi,T., &Go,N. (1991).Projection of Monte Carlo and molecular dynamics trajectories onto the normal mode axes: Human lysozyme.Proteins: Structure, Function, and Genetics,10,106–116.10.1002/(ISSN)1097-0134
  • Hubbard, S. R. (2004). Juxtamembrane autoinhibition in receptor tyrosine kinases. Nature Reviews Molecular Cell Biology, 5, 464–471.
  • Hyeon,C.,Jennings,P. A.,Adams,J. A., &Onuchic,J. N. (2009).Ligand-induced global transitions in the catalytic domain of protein kinase A.Proceedings of the National Academy of Sciences,106,3023–3028.10.1073/pnas.0813266106
  • James,L. C., &Tawfik,D. S. (2003).Conformational diversity and protein evolution – A 60-year-old hypothesis revisited.Trends in Biochemical Sciences,28,361–368.10.1016/S0968-0004(03)00135-X
  • Janin,J.,Henrick,K.,Moult,J.,Eyck,L. T.,Sternberg,M. J.,Vajda,S., …Critical Assessment of P. I (2003).CAPRI: A critical assessment of predicted interactions.Proteins: Structure, Function, and Genetics,52,2–9.10.1002/(ISSN)1097-0134
  • Jeong,S. Y.,Gaume,B.,Lee,Y. J.,Hsu,Y. T.,Ryu,S. W.,Yoon,S. H., &Youle,R. J. (2004).Bcl-xL sequesters its C-terminal membrane anchor in soluble, cytosolic homodimers.The EMBO Journal,23,2146–2155.10.1038/sj.emboj.7600225
  • Jubb,H.,Higueruelo,A. P.,Winter,A., &Blundell,T. L. (2012).Structural biology and drug discovery for protein–protein interactions.Trends in Pharmacological Sciences,33,241–248.10.1016/j.tips.2012.03.006
  • Juin,P.,Geneste,O.,Raimbaud,E., &Hickman,J. A. (2004).Shooting at survivors: Bcl-2 family members as drug targets for cancer.Biochimica et Biophysica Acta,1644,251–260.10.1016/j.bbamcr.2003.10.010
  • Karplus,M., &McCammon,J. A. (2002).Molecular dynamics simulations of biomolecules.Nature Structural Biology,9,646–652.10.1038/nsb0902-646
  • Katchalski-Katzir,E.,Shariv,I.,Eisenstein,M.,Friesem,A. A.,Aflalo,C., &Vakser,I. A. (1992).Molecular surface recognition: determination of geometric fit between proteins and their ligands by correlation techniques.Proceedings of the National Academy of Sciences,89,2195–2199.10.1073/pnas.89.6.2195
  • Kaufmann,T.,Schinzel,A., &Borner,C. (2004).Bcl-w(edding) with mitochondria.Trends in Cell Biology,14,8–12.10.1016/j.tcb.2003.11.005
  • Kerkela,R.,Grazette,L.,Yacobi,R.,Iliescu,C.,Patten,R.,Beahm,C.,, …Force,T. (2006).Cardiotoxicity of the cancer therapeutic agent imatinib mesylate.Nature Medicine,12,908–916.10.1038/nm1446
  • Knegtel,R. M.,Kuntz,I. D., &Oshiro,C. M. (1997).Molecular docking to ensembles of protein structures.Journal of Molecular Biology,266,424–440.10.1006/jmbi.1996.0776
  • Koshland,D. E. (1958).Application of a theory of enzyme specificity to protein synthesis.Proceedings of the National Academy of Sciences,44,98–104.10.1073/pnas.44.2.98
  • Kozakov,D.,Brenke,R.,Comeau,S. R., &Vajda,S. (2006).PIPER: An FFT-based protein docking program with pairwise potentials.Proteins: Structure, Function, and Bioinformatics,65,392–406.10.1002/prot.21117
  • Krishnan,L.,Sahni,G.,Kaur,K. J., &Salunke,D. M. (2008).Role of antibody paratope conformational flexibility in the manifestation of molecular mimicry.Biophysical Journal,94,1367–1376.10.1529/biophysj.107.108654
  • Krol,M.,Chaleil,R. A.,Tournier,A. L., &Bates,P. A. (2007).Implicit flexibility in protein docking: cross-docking and local refinement.Proteins: Structure, Function, and Bioinformatics,69,750–757.10.1002/prot.21698
  • Krol,M.,Tournier,A. L., &Bates,P. A. (2007).Flexible relaxation of rigid-body docking solutions.Proteins: Structure, Function, and Bioinformatics,68,159–169.10.1002/prot.21391
  • Kussie,P. H.,Gorina,S.,Marechal,V.,Elenbaas,B.,Moreau,J.,Levine,A. J., &Pavletich,N. P. (1996).Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain.Science,274,948–953.10.1126/science.274.5289.948
  • Lai,Z. Z.,Lu,Q., &Wang,J. (2011).Exploring the thermodynamic landscape, kinetics, and structural evolution of a protein conformational transition with a microscopic double-well model.The Journal of Physical Chemistry B,115,4147–4159.10.1021/jp110845u
  • Lane,D. P.,Cheok,C. F., &Lain,S. (2010).p53-based cancer therapy.Cold Spring Harbour Perspectives Biology,2,a001222.
  • Leach,A. R. (2001).Molecular modelling: Principles and applications.Harlow: Prentice Hall.
  • Lessene,G.,Czabotar,P. E.,Sleebs,B. E.,Zobel,K.,Lowes,K. N.,Adams,J. M., …Watson,K. G. (2013).Structure-guided design of a selective BCL-X inhibitor.Nature Chemical Biology,6,1–6.
  • Li,L.,Chen,R., &Weng,Z. (2003).RDOCK: Refinement of rigid-body protein docking predictions.Proteins: Structure, Function, and Genetics,53,693–707.10.1002/(ISSN)1097-0134
  • Li,M.,Fang,H.,Du,L.,Xia,L., &Wang,B. (2008).Computational studies of the binding site of α1A-adrenoceptor antagonists.Journal of Molecular Modeling,14,957–966.10.1007/s00894-008-0342-8
  • Liu,Y., &Gray,N. S. (2006).Rational design of inhibitors that bind to inactive kinase conformations.Nature Chemical Biology,2,358–364.10.1038/nchembio799
  • Ma,B.,Kumar,S.,Tsai,C. J.,Hu,Z., &Nussinov,R. (2000).Transition-state ensemble in enzyme catalysis: Possibility, reality, or necessity?Journal of Theoretical Biology,203,383–397.10.1006/jtbi.2000.1097
  • Ma,B.,Kumar,S.,Tsai,C. J., &Nussinov,R. (1999).Folding funnels and binding mechanisms.Protein Engineering Design and Selection,12,713–720.10.1093/protein/12.9.713
  • Ma,B., &Nussinov,R. (2002).Molecular dynamics simulations of alanine rich beta-sheet oligomers: Insight into amyloid formation.Protein Science,11,2335–2350.
  • Ma,B.,Shatsky,M.,Wolfson,H. J., &Nussinov,R. (2002).Multiple diverse ligands binding at a single protein site: A matter of pre-existing populations.Protein Science,11,184–197.
  • Ma,B.,Tsai,C. J., &Nussinov,R. (2000).Binding and folding: In search of intramolecular chaperone-like building block fragments.Protein Engineering Design and Selection,13,617–627.10.1093/protein/13.9.617
  • Madhumalar,A.,H. J.,Lee,Brown,C. J.,Lane,D., &Verma,C. (2009).Design of a novel MDM2 binding peptide based on the p53 family.Cell Cycle,8,2828–2836.10.4161/cc
  • Mashiach,E.,Schneidman-Duhovny,D.,Andrusier,N.,Nussinov,R., &Wolfson,H. J. (2008).FireDock: A web server for fast interaction refinement in molecular docking.Nucleic Acids Research,36,W229–W232.10.1093/nar/gkn186
  • Mayer, B. J. (2001). SH3 domains: Complexity in moderation. Journal of Cell Science, 114, 1253–1263.
  • Mereghetti,P.,Gabdoulline,R. R., &Wade,R. C. (2010).Brownian dynamics simulation of protein solutions: Structural and dynamical properties.Biophysical Journal,99,3782–3791.10.1016/j.bpj.2010.10.035
  • Mereghetti,P., &Wade,R. C. (2011).Diffusion of hydrophobin proteins in solution and interactions with a graphite surface.BMC Biophysics,4,11.10.1186/2046-1682-4-9
  • Nabuurs,S. B.,Wagener,M., &deVlieg,J. (2007).A flexible approach to induced fit docking.Journal of Medicinal Chemistry,50,6507–6518.10.1021/jm070593p
  • Norel,R.,Petrey,D.,Wolfson,H. J., &Nussinov,R. (1999).Examination of shape complementarity in docking of Unbound proteins.Proteins: Structure, Function, and Genetics,36,307–317.10.1002/(ISSN)1097-0134
  • Novak,W.,Wang,H., &Krilov,G. (2009).Role of protein flexibility in the design of Bcl-XL targeting agents: Insight from molecular dynamics.Journal of Computer-Aided Molecular Design,23,49–61.10.1007/s10822-008-9237-0
  • Nowakowski,J.,Cronin,C. N.,McRee,D. E.,Knuth,M. W.,Nelson,C. G.,Pavletich,N. P., …Thompson,D. A. (2002).Structures of the cancer-related Aurora-A, FAK, and EphA2 protein kinases from nanovolume crystallography.Structure,10,1659–1667.10.1016/S0969-2126(02)00907-3
  • Okazaki,K., &Takada,S. (2008).Dynamic energy landscape view of coupled binding and protein conformational change: Induced-fit versus population-shift mechanisms.Proceedings of the National Academy of Sciences,105,11182–11187.10.1073/pnas.0802524105
  • Okimoto,N.,Futatsugi,N.,Fuji,H.,Suenaga,A.,Morimoto,G.,Yanai,R., …Taiji,M. (2009).High-performance drug discovery: Computational screening by combining docking and molecular dynamics simulations.PLoS Computational Biology,5,e1000528.10.1371/journal.pcbi.1000528
  • Ortega,G.,Castaño,D.,Diercks,T., &Millet,O. (2012).Carbohydrate affinity for the glucose–galactose binding protein is regulated by allosteric domain motions.Journal of the American Chemical Society,134,19869–19876.10.1021/ja3092938
  • Osguthorpe,D. J.,Sherman,W., &Hagler,A. T. (2012).Exploring protein flexibility: Incorporating structural ensembles from crystal structures and simulation into virtual screening protocols.The Journal of Physical Chemistry B,116,6952–6959.10.1021/jp3003992
  • Osterberg,F.,Morris,G. M.,Sanner,M. F.,Olson,A. J., &Goodsell,D. S. (2002).Automated docking to multiple target structures: Incorporation of protein mobility and structural water heterogeneity in AutoDock.Proteins: Structure, Function, and Genetics,46,34–40.10.1002/(ISSN)1097-0134
  • Padyana, A. K., Qiu, H., Roll-Mecak, A., Hinnebusch, A. G., & Burley, S. K. (2005). Structural basis for autoinhibition and mutational activation of eukaryotic initiation factor 2alpha protein kinase GCN2. Journal of Biological Chemistry, 280, 29289–29299.
  • Palma,P. N.,Krippahl,L.,Wampler,J. E., &Moura,J. J. (2000).BiGGER: A new (soft) docking algorithm for predicting protein interactions.Proteins: Structure, Function, and Genetics,39,372–384.10.1002/(ISSN)1097-0134
  • Paschalidis,I. C.,Shen,Y.,Vakili,P., &Vajda,S. (2007).SDU: A semidefinite programming-based underestimation method for stochastic global optimization in protein docking.IEEE Transactions on Automatic Control,52,664–676.10.1109/TAC.2007.894518
  • Perutz,M. F., &Mathews,F. S. (1966).An X-ray study of azide methaemoglobin.Journal of Molecular Biology,21,199–202.10.1016/0022-2836(66)90088-X
  • Pierce,B., &Weng,Z. (2007).ZRANK: Reranking protein docking predictions with an optimized energy function.Proteins: Structure, Function, and Bioinformatics,67,1078–1086.10.1002/prot.21373
  • Porter,J.,Payne,A.,deCandole,B.,Ford,D.,Hutchinson,B.,Trevitt,G.,, …Stubberfield,C. (2009).Tetrahydroisoquinoline amide substituted phenyl pyrazoles as selective Bcl-2 inhibitors.Bioorganic & Medicinal Chemistry Letters,19,230–233.10.1016/j.bmcl.2008.10.113
  • Qi,M., &Elion,E. A. (2005).MAP kinase pathways.Journal of Cell Science,118,3569–3572.
  • Rautureau,G. J.,Yabal,M.,Yang,H.,Huang,D. C.,Kvansakul,M., &Hinds,M. G. (2012).The restricted binding repertoire of Bcl-B leaves Bim as the universal BH3-only prosurvival Bcl-2 protein antagonist.Cell Death and Disease,3,e443.10.1038/cddis.2012.178
  • Rosenfeld,R.,Vajda,S., &DeLisi,C. (1995).Flexible docking and design.Annual Review of Biophysics and Biomolecular Structure,24,677–700.10.1146/annurev.bb.24.060195.003333
  • Salmon,L.,Bouvignies,G.,Markwick,P.,Lakomek,N.,Showalter,S.,Li,D. W., …Blackledge,M. (2009).Protein conformational flexibility from structure-free analysis of NMR dipolar couplings: Quantitative and absolute determination of backbone motion in ubiquitin.Angewandte Chemie International Edition,48,4154–4157.10.1002/anie.v48:23
  • Sasi,N.,Hwang,M.,Jaboin,J.,Csiki,I., &Lu,B. (2009).Regulated cell death pathways: new twists in modulation of BCL2 family function.Molecular Cancer Therapeutics,8,1421–1429.10.1158/1535-7163.MCT-08-0895
  • Sattler,M.,Liang,H.,Nettesheim,D.,Meadows,R. P.,Harlan,J. E.,Eberstadt,M., …Fesik,S. W. (1997).Structure of Bcl-xL-Bak peptide complex: Recognition between regulators of apoptosis.Science,275,983–986.10.1126/science.275.5302.983
  • Sawaya,M. R.,Prasad,R.,Wilson,S. H.,Kraut,J., &Pelletier,H. (1997).Crystal structures of human DNA polymerase beta complexed with gapped and nicked DNA: Evidence for an induced fit mechanism.Biochemistry,36,11205–11215.10.1021/bi9703812
  • Schneidman-Duhovny,D.,Inbar,Y.,Nussinov,R., &Wolfson,H. J. (2005).PatchDock and SymmDock: Servers for rigid and symmetric docking.Nucleic Acids Research,33,W363–W367.10.1093/nar/gki481
  • Schneidman-Duhovny,D.,Nussinov,R., &Wolfson,H. J. (2007).Automatic prediction of protein interactions with large scale motion.Proteins: Structure, Function, and Bioinformatics,69,764–773.10.1002/prot.21759
  • Shapovalov,M. V., &Dunbrack,R. L.,Jr. (2011).A smoothed backbone-dependent rotamer library for proteins derived from adaptive kernel density estimates and regressions.Structure,19,844–858.10.1016/j.str.2011.03.019
  • Shi,Z.,Resing,K. A., &Ahn,N. G. (2006).Networks for the allosteric control of protein kinases.Current Opinion in Structural Biology,16,686–692.10.1016/j.sbi.2006.10.011
  • Skjaerven,L.,Martinez,A., &Reuter,N. (2011).Principal component and normal mode analysis of proteins; a quantitative comparison using the GroEL subunit.Proteins: Structure, Function, and Bioinformatics,79,232–243.10.1002/prot.22875
  • Smith,G. R., &Sternberg,M. J. (2002).Prediction of protein–protein interactions by docking methods.Current Opinion in Structural Biology,12,28–35.10.1016/S0959-440X(02)00285-3
  • Souers,A. J.,Leverson,J. D.,Boghaert,E. R.,Ackler,S. L.,Catron,N. D.,Chen,J., …Elmore,S. W. (2013).ABT-199, a potent and selective BCL-2 inhibitor, achieves antitumor activity while sparing platelets.Nature Medicine,19,202–208.10.1038/nm.3048
  • Stelzl,U.,Worm,U.,Lalowski,M.,Haenig,C.,Brembeck,F. H.,Goehler,H., …Wanker,E. E. (2005).A human protein-protein interaction network: A resource for annotating the proteome.Cell,122,957–968.10.1016/j.cell.2005.08.029
  • Suzuki,M.,Youle,R. J., &Tjandra,N. (2000).Structure of Bax: Coregulation of dimer formation and intracellular localization.Cell,103,645–654.10.1016/S0092-8674(00)00167-7
  • Taylor,J. S., &Burnett,R. M. (2000).DARWIN: A program for docking flexible molecules.Proteins: Structure, Function, and Genetics,41,173–191.10.1002/(ISSN)1097-0134
  • Taylor,R. D.,Jewsbury,P. J., &Essex,J. W. (2003).FDS: Flexible ligand and receptor docking with a continuum solvent model and soft-core energy function.Journal of Computational Chemistry,24,1637–1656.10.1002/(ISSN)1096-987X
  • Tirion,M. M. (1996).Large amplitude elastic motions in proteins from a single-parameter, atomic analysis.Physical Review Letters,77,1905–1908.10.1103/PhysRevLett.77.1905
  • Tolman,J. R. (2009).Structural biology: Protein dynamics from disorder.Nature,459,1063–1064.10.1038/4591063a
  • Totrov,M., &Abagyan,R. (2008).Flexible ligand docking to multiple receptor conformations: A practical alternative.Current Opinion in Structural Biology,18,178–184.10.1016/j.sbi.2008.01.004
  • Tournier,A. L., &Smith,J. C. (2003).Principal components of the protein dynamical transition.Physical Review Letters,91,208106.10.1103/PhysRevLett.91.208106
  • Tsai,C. J.,delSol,A., &Nussinov,R. (2008).Allostery: Absence of a change in shape does not imply that allostery is not at play.Journal of Molecular Biology,378,1–11.10.1016/j.jmb.2008.02.034
  • Tsai,C. D.,Ma,B.,Kumar,S.,Wolfson,H., &Nussinov,R. (2001).Protein folding: Binding of conformationally fluctuating building blocks via population selection.Critical Reviews in Biochemistry and Molecular Biology,36,399–433.10.1080/20014091074228
  • Tsai,C. J.,Ma,B., &Nussinov,R. (1999).Folding and binding cascades: Shifts in energy landscapes.Proceedings of the National Academy of Sciences,96,9970–9972.10.1073/pnas.96.18.9970
  • Tsai,C. J.,Ma,B., &Nussinov,R. (2009).Intra-molecular chaperone: The role of the N-terminal in conformational selection and kinetic control.Physical Biology,6,013001.10.1088/1478-3975/6/1/013001
  • Tsai,C. J.,Ma,B.,Sham,Y. Y.,Kumar,S., &Nussinov,R. (2001).Structured disorder and conformational selection.Proteins: Structure, Function, and Genetics,44,418–427.10.1002/(ISSN)1097-0134
  • Tse,C.,Shoemaker,A. R.,Adickes,J.,Anderson,M. G.,Chen,J.,Jin,S., …Elmore,S. W. (2008).ABT-263: A potent and orally bioavailable Bcl-2 family inhibitor.Cancer Research,68,3421–3428.10.1158/0008-5472.CAN-07-5836
  • Tzeng,S. R., &Kalodimos,C. G. (2009).Dynamic activation of an allosteric regulatory protein.Nature,462,368–372.10.1038/nature08560
  • Uhrinova,S.,Uhrin,D.,Powers,H.,Watt,K.,Zheleva,D.,Fischer,P., …Barlow,P. N. (2005).Structure of free MDM2 N-terminal domain reveals conformational adjustments that accompany p53-binding.Journal of Molecular Biology,350,587–598.10.1016/j.jmb.2005.05.010
  • Vajda,S., &Kozakov,D. (2009).Convergence and combination of methods in protein–protein docking.Current Opinion in Structural Biology,19,164–170.10.1016/j.sbi.2009.02.008
  • Vakser,I. A.,Matar,O. G., &Lam,C. F. (1999).A systematic study of low-resolution recognition in protein–protein complexes.Proceedings of the National Academy of Sciences,96,8477–8482.10.1073/pnas.96.15.8477
  • vanAalten,D. M.,Amadei,A.,Linssen,A. B.,Eijsink,V. G.,Vriend,G., &Berendsen,H. J. (1995).The essential dynamics of thermolysin: Confirmation of the hinge-bending motion and comparison of simulations in vacuum and water.Proteins: Structure, Function, and Genetics,22,45–54.10.1002/(ISSN)1097-0134
  • vanMontfort,R. L., &Workman,P. (2009).Structure-based design of molecular cancer therapeutics.Trends in Biotechnology,27,315–328.10.1016/j.tibtech.2009.02.003
  • Vanommeslaeghe,K.,Hatcher,E.,Acharya,C.,Kundu,S.,Zhong,S.,Shim,J., …Mackerell,A. D.,Jr. (2010).CHARMM general force field: A force field for drug-like molecules compatible with the CHARMM all-atom additive biological force fields.Journal of Computational Chemistry,31,671–690.
  • Verdine,G. L., &Walensky,L. D. (2007).The challenge of drugging undruggable targets in cancer: Lessons learned from targeting BCL-2 family members.Clinical Cancer Research,13,7264–7270.10.1158/1078-0432.CCR-07-2184
  • Walensky, L. D., Kung, A. L., Escher, I., Malia, T. J., Barbuto, S., Wright, R. D., … Korsmeyer, S. J. (2004). Activation of apoptosis in vivo by a hydrocarbon-stapled BH3 helix. Science, 305, 1466–1470.
  • Wang,C.,Schueler-Furman,O.,Andre,I.,London,N.,Fleishman,S. J.,Bradley,P., …Baker,D. (2007).RosettaDock in CAPRI rounds 6-12.Proteins: Structure, Function, and Bioinformatics,69,758–763.10.1002/prot.21684
  • Wang,C.,Schueler-Furman,O., &Baker,D. (2005).Improved side-chain modeling for protein–protein docking.Protein Science,14,1328–1339.10.1110/(ISSN)1469-896X
  • Wang,J.,Wang,W.,Kollman,P. A., &Case,D. A. (2006).Automatic atom type and bond type perception in molecular mechanical calculations.Journal of Molecular Graphics and Modelling,25,247–260.10.1016/j.jmgm.2005.12.005
  • Weinkam,P.,Pons,J., &Sali,A. (2012).Structure-based model of allostery predicts coupling between distant sites.Proceedings of the National Academy of Sciences,109,4875–4880.10.1073/pnas.1116274109
  • Whisstock, J. C., & Lesk, A. M. (1999). SH3 domains in prokaryotes. Trends in Biochemical Sciences, 24, 132–133.
  • Wysoczanski,P.,Mart,R. J.,Loveridge,E. J.,Williams,C.,Whittaker,S. B.,Crump,M. P., &Allemann,R. K. (2012).NMR solution structure of a photoswitchable apoptosis activating Bak peptide bound to Bcl-xL.Journal of the American Chemical Society,134,7644–7647.10.1021/ja302390a
  • Xu,H.,Ye,H.,Osman,N. E.,Sadler,K.,Won,E. Y.,Chi,S. W., &Yoon,H. S. (2009).The MDM2-binding region in the transactivation domain of p53 also acts as a Bcl-X(L)-binding motif.Biochemistry,48,12159–12168.10.1021/bi901188s
  • Yang,J.,Garrod,S. M.,Deal,M. S.,Anand,G. S.,Woods,V. L.,Jr, &Taylor,S. (2005).Allosteric network of cAMP-dependent protein kinase revealed by mutation of Tyr204 in the P+1 loop.Journal of Molecular Biology,346,191–201.10.1016/j.jmb.2004.11.030
  • Yu,H.,Braun,P.,Yildirim,M. A.,Lemmens,I.,Venkatesan,K.,Sahalie,J., …Vidal,M. (2008).High-quality binary protein interaction map of the yeast interactome network.Science,322,104–110.10.1126/science.1158684
  • Zacharias,M. (2003).Protein-protein docking with a reduced protein model accounting for side-chain flexibility.Protein Science,12,1271–1282.10.1110/(ISSN)1469-896X
  • Zhang,X.,Gureasko,J.,Shen,K.,Cole,P. A., &Kuriyan,J. (2006).An allosteric mechanism for activation of the kinase domain of epidermal growth factor receptor.Cell,125,1137–1149.10.1016/j.cell.2006.05.013
  • Zhang,J.,Yang,P. L., &Gray,N. S. (2009).Targeting cancer with small molecule kinase inhibitors.Nature Reviews Cancer,9,28–39.10.1038/nrc2559
  • Zhang,H.,Zhao,Q.,Bhattacharya,S.,Waheed,A. A.,Tong,X.,Hong,A., …Debnath,A. K. (2008).A cell-penetrating helical peptide as a potential HIV-1 inhibitor.Journal of Molecular Biology,378,565–580.10.1016/j.jmb.2008.02.066
  • Zhao,Y., &Sanner,M. F. (2007).FLIPDock: Docking flexible ligands into flexible receptors.Proteins: Structure, Function, and Bioinformatics,68,726–737.10.1002/prot.21423
  • Zhou,P.,Wang,C.,Ren,Y.,Yang,C., &Tian,F. (2013).Computational peptidology: A new and promising approach to therapeutic peptide design.Current Medicinal Chemistry,20,1985–1996.10.2174/0929867311320150005
  • Zhu,T.,Lee,H.,Lei,H.,Jones,C.,Patel,K.,Johnson,M. E., &Hevener,K. E. (2013).Fragment-based drug discovery using a multidomain, Parallel MD-MM/PBSA Screening Protocol.Journal of Chemical Information and Modeling, 53, 560572.
  • Zondlo,S. C.,Lee,A. E., &Zondlo,N. J. (2006).Determinants of specificity of MDM2 for the activation domains of p53 and p65: Proline27 disrupts the MDM2-binding motif of p53.Biochemistry,45,11945–11957.10.1021/bi060309g

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.