Adaptability of protein structures to enable functional interactions and evolutionary implications

Current Opinion in Structural Biology

Volumn 35, Issue , 2015, Pages 17-23

  Haliloglu, Turkan ^a,b   Bahar, Ivet ^b  

^a BOGAZICI UNIVERSITY   (Turkey)

^b UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALLOSTERISM; AMINO ACID SEQUENCE; COMPLEX FORMATION; CONFORMATIONAL TRANSITION; DRUG PROTEIN BINDING; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; MOLECULAR INTERACTION; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN MULTIMERIZATION; PROTEIN PROTEIN INTERACTION; PROTEIN STRUCTURE; REVIEW; SEQUENCE ANALYSIS; SIGNAL TRANSDUCTION; SOFT MODE; STRUCTURE ACTIVITY RELATION; SURFACE PROPERTY; CHEMISTRY; METABOLISM; MOVEMENT (PHYSIOLOGY);

PROTEIN; PROTEIN BINDING;

ALLOSTERIC REGULATION; EVOLUTION, MOLECULAR; MOVEMENT; PROTEIN BINDING; PROTEIN MULTIMERIZATION; PROTEINS;

EID: 84938900365     PISSN: 0959440X     EISSN: 1879033X     Source Type: Journal    
DOI: 10.1016/j.sbi.2015.07.007     Document Type: Review

References (70)

1. Tchekanda E., Sivanesan D., Michnick S.W. An infrared reporter to detect spatiotemporal dynamics of protein-protein interactions. Nat Methods 2014, 11:641-644.
2. Kim T.J., Zheng S., Sun J., Muhamed I., Wu J., Lei L., Kong X., Leckband D.E., Wang Y. Dynamic visualization of alpha-catenin reveals rapid, reversible conformation switching between tension states. Curr Biol 2015, 25:218-224.
3. Bahar I., Lezon T.R., Yang L.W., Eyal E. Global dynamics of proteins: bridging between structure and function. Annu Rev Biophys 2010, 39:23-42.
4. Fuglebakk E., Tiwari S.P., Reuter N. Comparing the intrinsic dynamics of multiple protein structures using elastic network models. Biochim Biophys Acta 2015, 1850:911-922.
5. Feher V.A., Durrant J.D., Van Wart A.T., Amaro R.E. Computational approaches to mapping allosteric pathways. Curr Opin Struct Biol 2014, 25:98-103.
6. Dobbins S.E., Lesk V.I., Sternberg M.J. Insights into protein flexibility: the relationship between normal modes and conformational change upon protein-protein docking. Proc Natl Acad Sci U S A 2008, 105:10390-10395.
7. Landes C.F., Rambhadran A., Taylor J.N., Salatan F., Jayaraman V. Structural landscape of isolated agonist-binding domains from single AMPA receptors. Nat Chem Biol 2011, 7:168-173.
8. Phillips A.H., Zhang Y., Cunningham C.N., Zhou L., Forrest W.F., Liu P.S., Steffek M., Lee J., Tam C., Helgason E., Murray J.M., Kirkpatrick D.S., Fairbrother W.J., Corn J.E. Conformational dynamics control ubiquitin-deubiquitinase interactions and influence in vivo signaling. Proc Natl Acad Sci U S A 2013, 110:11379-11384.
9. Cronin M., Coolbaugh M.J., Nellis D., Zhu J., Wood D.W., Nussinov R., Ma B. Dynamics differentiate between active and inactive inteins. Eur J Med Chem 2015, 91:51-62.
10. James L.C., Roversi P., Tawfik D.S. Antibody multispecificity mediated by conformational diversity. Science 2003, 299:1362-1367.
11. Tawfik D.S. Accuracy-rate tradeoffs: how do enzymes meet demands of selectivity and catalytic efficiency?. Curr Opin Chem Biol 2014, 21:73-80.
12. Tokuriki N., Tawfik D.S. Protein dynamism and evolvability. Science 2009, 324:203-207.
13. Marsh J.A., Teichmann S.A. Parallel dynamics and evolution: protein conformational fluctuations and assembly reflect evolutionary changes in sequence and structure. Bioessays 2014, 36:209-218.
14. Perica T., Kondo Y., Tiwari S.P., McLaughlin S.H., Kemplen K.R., Zhang X., Steward A., Reuter N., Clarke J., Teichmann S.A. Evolution of oligomeric state through allosteric pathways that mimic ligand binding. Science 2014, 346:1254346.
15. Toth-Petroczy A., Tawfik D.S. The robustness and innovability of protein folds. Curr Opin Struct Biol 2014, 26:131-138.
16. Leioatts N., Romo T.D., Grossfield A. Elastic network models are robust to variations in formalism. J Chem Theory Comput 2012, 8:2424-2434.
17. Michielssens S., de Groot B.L., Grubmüller H. Binding affinities controlled by shifting conformational equilibria: opportunities and limitations. Biophys J 2015, 108:2585-2590.
18. Yang L., Song G., Carriquiry A., Jernigan R.L. Close correspondence between the motions from principal component analysis of multiple HIV-1 protease structures and elastic network modes. Structure 2008, 16:321-330.
19. Yang L.W., Eyal E., Bahar I., Kitao A. Principal component analysis of native ensembles of biomolecular structures (PCA_NEST): insights into functional dynamics. Bioinformatics 2009, 25:606-614.
20. Bahar I. On the functional significance of soft modes predicted by coarse-grained models for membrane proteins. J Gen Physiol 2010, 135:563-573.
21. Skjaerven L., Martinez A., Reuter N. Principal component and normal mode analysis of proteins; a quantitative comparison using the GroEL subunit. Proteins 2011, 79:232-243.
22. Lange O.F., Lakomek N.A., Fares C., Schroder G.F., Walter K.F., Becker S., Meiler J., Grubmuller H., Griesinger C., de Groot B.L. Recognition dynamics up to microseconds revealed from an RDC-derived ubiquitin ensemble in solution. Science 2008, 320:1471-1475.
23. Gabba M., Poblete S., Rosenkranz T., Katranidis A., Kempe D., Zuchner T., Winkler R.G., Gompper G., Fitter J. Conformational state distributions and catalytically relevant dynamics of a hinge-bending enzyme studied by single-molecule FRET and a coarse-grained simulation. Biophys J 2014, 107:1913-1923.
24. Meireles L., Gur M., Bakan A., Bahar I. Pre-existing soft modes of motion uniquely defined by native contact topology facilitate ligand binding to proteins. Protein Sci 2011, 20:1645-1658.
25. Tobi D., Bahar I. Structural changes involved in protein binding correlate with intrinsic motions of proteins in the unbound state. Proc Natl Acad Sci U S A 2005, 102:18908-18913.
26. Bakan A., Bahar I. The intrinsic dynamics of enzymes plays a dominant role in determining the structural changes induced upon inhibitor binding. Proc Natl Acad Sci U S A 2009, 106:14349-14354.
27. Bodmer N.K., Theisen K.E., Dima R.I. Molecular investigations into the mechanics of a muscle anchoring complex. Biophys J 2015, 108:2322-2332.
28. Gur M., Madura J.D., Bahar I. Global transitions of proteins explored by a multiscale hybrid methodology: application to adenylate kinase. Biophys J 2013, 105:1643-1652.
29. Uyar A., Kantarci-Carsibasi N., Haliloglu T., Doruker P. Features of large hinge-bending conformational transitions. Prediction of closed structure from open state. Biophys J 2014, 106:2656-2666.
30. Michino M., Free R.B., Doyle T.B., Sibley D.R., Shi L. Structural basis for Na(+)-sensitivity in dopamine D2 and D3 receptors. Chem Commun (Camb) 2015, 51:8618-8621.
31. Stolzenberg S., Quick M., Zhao C., Gotfryd K., Khelashvili G., Gether U., Loland C.J., Javitch J.A., Noskov S., Weinstein H., Shi L. Mechanism of the association between Na+ binding and conformations at the intracellular gate in neurotransmitter:sodium symporters. J Biol Chem 2015, 290:13992-14003.
32. Ph. Biophys J 2012, 102:1331-1340.
33. Rodgers T.L., Townsend P.D., Burnell D., Jones M.L., Richards S.A., McLeish T.C., Pohl E., Wilson M.R., Cann M.J. Modulation of global low-frequency motions underlies allosteric regulation: demonstration in CRP/FNR family transcription factors. PLoS Biol 2013, 11:e1001651.
34. Townsend P.D., Rodgers T.L., Pohl E., Wilson M.R., McLeish T.C., Cann M.J. Global low-frequency motions in protein allostery: CAP as a model system. Biophys Rev 2015, 7:175-182.
35. Aykac F., Tutar Y., Haliloglu T. Dynamic fluctuations provide the basis of a conformational switch mechanism in apo cyclic AMP receptor protein. PLoS Comput Biol 2013, 9:e1003141.
36. Sahillioglu A.C., Sumbul F., Ozoren N., Haliloglu T. Structural and dynamics aspects of ASC speck assembly. Structure 2014, 22:1722-1734.
37. Meigh L., Greenhalgh S.A., Rodgers T.L., Cann M.J., Roper D.I., Dale N. CO(2)directly modulates connexin 26 by formation of carbamate bridges between subunits. Elife 2013, 2:e01213.
38. Kolan D., Fonar G., Samson A.O. Elastic network normal mode dynamics reveal the GPCR activation mechanism. Proteins 2014, 82:579-586.
39. Gofman Y., Shats S., Attali B., Haliloglu T., Ben-Tal N. How does KCNE1 regulate the Kv7.1 potassium channel? Model-structure, mutations, and dynamics of the Kv7.1-KCNE1 complex. Structure 2012, 20:1343-1352.
40. Korkmaz E.N., Nussinov R., Haliloglu T. Conformational control of the binding of the transactivation domain of the MLL protein and c-Myb to the KIX domain of CREB. PLoS Comput Biol 2012, 8:e1002420.
41. Bohnuud T., Kozakov D., Vajda S. Evidence of conformational selection driving the formation of ligand binding sites in protein-protein interfaces. PLoS Comput Biol 2014, 10:e1003872.
42. Lin J.J., Lin Z.L., Hwang J.K., Huang T.T. On the packing density of the unbound protein-protein interaction interface and its implications in dynamics. BMC Bioinformatics 2015, 16(Suppl 1):S7.
43. Visscher K.M., Kastritis P.L., Bonvin A.M. Non-interacting surface solvation and dynamics in protein-protein interactions. Proteins 2015, 83:445-458.
44. Jones M.R., Liu C., Wilson A.K. Molecular dynamics studies of the protein-protein interactions in inhibitor of κB kinase-β. J Chem Inf Model 2014, 54:562-572.
45. Lee H.S., Qi Y., Im W. Effects of N-glycosylation on protein conformation and dynamics: Protein Data Bank analysis and molecular dynamics simulation study. Sci Rep 2015, 5:8926.
46. Healy A.R., Houston D.R., Remnant L., Huart A.-S., Brychtova V., Maslon M.M., Meers O., Muller P., Krejci A., Blackburn E.A., Vojtesek B., Hernychova L., Walkinshaw M.D., Westwood N.J., Hupp T.R. Discovery of a novel ligand that modulates the protein-protein interactions of the AAA+superfamily oncoprotein reptin. Chem Sci 2015, 15:3109-3116.
47. Fleishman S.J., Whitehead T.A., Strauch E.M., Corn J.E., Qin S., Zhou H.X., Mitchell J.C., Demerdash O.N., Takeda-Shitaka M., Terashi G., Moal I.H., Li X., Bates P.A., Zacharias M., Park H., Ko J.S., Lee H., Seok C., Bourquard T., Bernauer J., Poupon A., Aze J., Soner S., Ovali S.K., Ozbek P., Tal N.B., Haliloglu T., Hwang H., Vreven T., Pierce B.G., Weng Z., Perez-Cano L., Pons C., Fernandez-Recio J., Jiang F., Yang F., Gong X., Cao L., Xu X., Liu B., Wang P., Li C., Wang C., Robert C.H., Guharoy M., Liu S., Huang Y., Li L., Guo D., Chen Y., Xiao Y., London N., Itzhaki Z., Schueler-Furman O., Inbar Y., Potapov V., Cohen M., Schreiber G., Tsuchiya Y., Kanamori E., Standley D.M., Nakamura H., Kinoshita K., Driggers C.M., Hall R.G., Morgan J.L., Hsu V.L., Zhan J., Yang Y., Zhou Y., Kastritis P.L., Bonvin A.M., Zhang W., Camacho C.J., Kilambi K.P., Sircar A., Gray J.J., Ohue M., Uchikoga N., Matsuzaki Y., Ishida T., Akiyama Y., Khashan R., Bush S., Fouches D., Tropsha A., Esquivel-Rodriguez J., Kihara D., Stranges P.B., Jacak R., Kuhlman B., Huang S.Y., Zou X., Wodak S.J., Janin J., Baker D. Community-wide assessment of protein-interface modeling suggests improvements to design methodology. J Mol Biol 2011, 414:289-302.
48. Sours K.M., Xiao Y., Ahn N.G. Extracellular-regulated kinase 2 is activated by the enhancement of hinge flexibility. J Mol Biol 2014, 426:1925-1935.
49. Ozer N., Ozen A., Schiffer C.A., Haliloglu T. Drug-resistant HIV-1 protease regains functional dynamics through cleavage site coevolution. Evol Appl 2015, 8:185-198.
50. Ma B., Nussinov R. Druggable orthosteric and allosteric hot spots to target protein-protein interactions. Curr Pharm Des 2014, 20:1293-1301.
51. Hines C.S., Ray K., Schmidt J.J., Xiong F., Feenstra R.W., Pras-Raves M., de Moes J.P., Lange J.H., Melikishvili M., Fried M.G., Mortenson P., Charlton M., Patel Y., Courtney S.M., Kruse C.G., Rodgers D.W. Allosteric inhibition of the neuropeptidase neurolysin. J Biol Chem 2014, 289:35605-35619.
52. General I.J., Liu Y., Blackburn M.E., Mao W., Gierasch L.M., Bahar I. ATPase subdomain IA is a mediator of interdomain allostery in Hsp70 molecular chaperones. PLoS Comput Biol 2014, 10:e1003624.
53. Arora J., Hickey J.M., Majumdar R., Esfandiary R., Bishop S.M., Samra H.S., Middaugh C.R., Weis D.D., Volkin D.B. Hydrogen exchange mass spectrometry reveals protein interfaces and distant dynamic coupling effects during the reversible self-association of an IgG1 monoclonal antibody. MAbs 2015, 7:525-539.
54. Traverso J.J., Manoranjan V.S., Bishop A.R., Rasmussen K.O., Voulgarakis N.K. Allostery through protein-induced DNA bubbles. Sci Rep 2015, 5:9037.
55. Otero L.H., Rojas-Altuve A., Llarrull L.I., Carrasco-Lopez C., Kumarasiri M., Lastochkin E., Fishovitz J., Dawley M., Hesek D., Lee M., Johnson J.W., Fisher J.F., Chang M., Mobashery S., Hermoso J.A. How allosteric control of Staphylococcus aureus penicillin binding protein 2a enables methicillin resistance and physiological function. Proc Natl Acad Sci U S A 2013, 110:16808-16813.
56. Maguid S., Fernandez-Alberti S., Ferrelli L., Echave J. Exploring the common dynamics of homologous proteins. Application to the globin family. Biophys J 2005, 89:3-13.
57. Leo-Macias A., Lopez-Romero P., Lupyan D., Zerbino D., Ortiz A.R. An analysis of core deformations in protein superfamilies. Biophys J 2005, 88:1291-1299.
58. Raimondi F., Orozco M., Fanelli F. Deciphering the deformation modes associated with function retention and specialization in members of the Ras superfamily. Structure 2010, 18:402-414.
59. Liu Y., Bahar I. Sequence evolution correlates with structural dynamics. Mol Biol Evol 2012, 29:2253-2263.
60. Seeber M., Felline A., Raimondi F., Mariani S., Fanelli F. WebPSN: a web server for high-throughput investigation of structural communication in biomacromolecules. Bioinformatics 2015, 31:779-781.
61. Jones D.T., Buchan D.W., Cozzetto D., Pontil M. PSICOV: precise structural contact prediction using sparse inverse covariance estimation on large multiple sequence alignments. Bioinformatics 2012, 28:184-190.
62. Jones D.T., Singh T., Kosciolek T., Tetchner S. MetaPSICOV: combining coevolution methods for accurate prediction of contacts and long range hydrogen bonding in proteins. Bioinformatics 2015, 31:999-1006.
63. Mao W., Kaya C., Dutta A., Horovitz A., Bahar I. Comparative study of the effectiveness and limitations of current methods for detecting sequence coevolution. Bioinformatics 2015, 31:1929-1937.
64. Morcos F., Pagnani A., Lunt B., Bertolino A., Marks D.S., Sander C., Zecchina R., Onuchic J.N., Hwa T., Weigt M. Direct-coupling analysis of residue coevolution captures native contacts across many protein families. Proc Natl Acad Sci U S A 2011, 108:E1293-E1301.
65. Ovchinnikov S., Kamisetty H., Baker D. Robust and accurate prediction of residue-residue interactions across protein interfaces using evolutionary information. Elife 2014, 3:e02030.
66. Jeon J., Nam H.J., Choi Y.S., Yang J.S., Hwang J., Kim S. Molecular evolution of protein conformational changes revealed by a network of evolutionarily coupled residues. Mol Biol Evol 2011, 28:2675-2685.
67. Butler B.M., Gerek Z.N., Kumar S., Ozkan S.B. Conformational dynamics of nonsynonymous variants at protein interfaces reveals disease association. Proteins 2015, 83:428-435.
68. Nichols S.E., Hernandez C.X., Wang Y., McCammon J.A. Structure-based network analysis of an evolved G protein-coupled receptor homodimer interface. Protein Sci 2013, 22:745-754.
69. Marsh J.A., Teichmann S.A. Protein flexibility facilitates quaternary structure assembly and evolution. PLoS Biol 2014, 12:e1001870.
70. Marsh J.A., Teichmann S.A. Structure, dynamics, assembly, and evolution of protein complexes. Annu Rev Biochem 2014, 84:551-575.