Design of Elastic Networks with Evolutionary Optimized Long-Range Communication as Mechanical Models of Allosteric Proteins

Biophysical Journal

Volumn 113, Issue 3, 2017, Pages 558-571

  Flechsig, Holger ^a  

^a HIROSHIMA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

MYOSIN V;

ALLOSTERISM; CHEMISTRY; ELASTICITY; METABOLISM; MOLECULAR EVOLUTION; MOLECULAR MODEL; PROTEIN CONFORMATION;

ALLOSTERIC REGULATION; ELASTICITY; EVOLUTION, MOLECULAR; MODELS, MOLECULAR; MYOSIN TYPE V; PROTEIN CONFORMATION;

EID: 85026879710     PISSN: 00063495     EISSN: 15420086     Source Type: Journal    
DOI: 10.1016/j.bpj.2017.06.043     Document Type: Article

References (51)

1. Tsai, C.-J., Nussinov, R., A unified view of “how allostery works”. PLOS Comput. Biol., 10, 2014, e1003394.
2. Brüschweiler, S., Schanda, P., et al., Tollinger, M., Direct observation of the dynamic process underlying allosteric signal transmission. J. Am. Chem. Soc. 131 (2009), 3063–3068.
3. Grutsch, S., Brüschweiler, S., Tollinger, M., NMR methods to study dynamic allostery. PLOS Comput. Biol., 12, 2016, e1004620.
4. del Sol, A., Fujihashi, H., et al., Nussinov, R., Residues crucial for maintaining short paths in network communication mediate signaling in proteins. Mol. Syst. Biol., 2, 2006 2006;2:2006.0019. Epub 2006 May 2.
5. del Sol, A., Araúzo-Bravo, M.J., et al., Nussinov, R., Modular architecture of protein structures and allosteric communications: potential implications for signaling proteins and regulatory linkages. Genome Biol., 8, 2007, R92.
6. Daily, M.D., Upadhyaya, T.J., Gray, J.J., Contact rearrangements form coupled networks from local motions in allosteric proteins. Proteins 71 (2008), 455–466.
7. Chennubhotla, C., Bahar, I., Markov propagation of allosteric effects in biomolecular systems: application to GroEL-GroES. Mol. Syst. Biol., 2, 2006, 36.
8. Chennubhotla, C., Bahar, I., Signal propagation in proteins and relation to equilibrium fluctuations. PLOS Comput. Biol. 3 (2007), 1716–1726.
9. Lockless, S.W., Ranganathan, R., Evolutionarily conserved pathways of energetic connectivity in protein families. Science 286 (1999), 295–299.
10. Süel, G.M., Lockless, S.W., et al., Ranganathan, R., Evolutionarily conserved networks of residues mediate allosteric communication in proteins. Nat. Struct. Biol. 10 (2003), 59–69.
11. Dima, R.I., Thirumalai, D., Determination of network of residues that regulate allostery in protein families using sequence analysis. Protein Sci. 15 (2006), 258–268.
12. Tang, S., Liao, J.C., et al., Schmidt, J.P., Predicting allosteric communication in myosin via a pathway of conserved residues. J. Mol. Biol. 373 (2007), 1361–1373.
13. Ma, J., Sigler, P.B., et al., Karplus, M., A dynamic model for the allosteric mechanism of GroEL. J. Mol. Biol. 302 (2000), 303–313.
14. Ghosh, A., Vishveshwara, S., A study of communication pathways in methionyl- tRNA synthetase by molecular dynamics simulations and structure network analysis. Proc. Natl. Acad. Sci. USA 104 (2007), 15711–15716.
15. Cui, Q., Karplus, M., Allostery and cooperativity revisited. Protein Sci. 17 (2008), 1295–1307.
16. Dixit, A., Verkhivker, G.M., Computational modeling of allosteric communication reveals organizing principles of mutation-induced signaling in ABL and EGFR kinases. PLOS Comput. Biol., 7, 2011, e1002179.
17. Laine, E., Auclair, C., Tchertanov, L., Allosteric communication across the native and mutated KIT receptor tyrosine kinase. PLOS Comput. Biol., 8, 2012, e1002661.
18. Naithani, A., Taylor, P., et al., Walkinshaw, M.D., A molecular dynamics study of allosteric transitions in Leishmania mexicana pyruvate kinase. Biophys. J. 109 (2015), 1149–1156.
19. Hertig, S., Latorraca, N.R., Dror, R.O., Revealing atomic-level mechanisms of protein allostery with molecular dynamics simulations. PLOS Comput. Biol., 12, 2016, e1004746.
20. Xu, C., Tobi, D., Bahar, I., Allosteric changes in protein structure computed by a simple mechanical model: hemoglobin T↔R2 transition. J. Mol. Biol. 333 (2003), 153–168.
21. Zheng, W., Brooks, B.R., Thirumalai, D., Low-frequency normal modes that describe allosteric transitions in biological nanomachines are robust to sequence variations. Proc. Natl. Acad. Sci. USA 103 (2006), 7664–7669.
22. Chennubhotla, C., Yang, Z., Bahar, I., Coupling between global dynamics and signal transduction pathways: a mechanism of allostery for chaperonin GroEL. Mol. Biosyst. 4 (2008), 287–292.
23. Yang, Z., Májek, P., Bahar, I., Allosteric transitions of supramolecular systems explored by network models: application to chaperonin GroEL. PLOS Comput. Biol., 5, 2009, e1000360.
24. Morra, G., Verkhivker, G., Colombo, G., Modeling signal propagation mechanisms and ligand-based conformational dynamics of the Hsp90 molecular chaperone full-length dimer. PLOS Comput. Biol., 5, 2009, e1000323.
25. Erman, B., A fast approximate method of identifying paths of allosteric communication in proteins. Proteins 81 (2013), 1097–1101.
26. Krieger, J., Bahar, I., Greger, I.H., Structure, dynamics, and allosteric potential of ionotropic glutamate receptor N-terminal domains. Biophys. J. 109 (2015), 1136–1148.
27. Bahar, I., Chennubhotla, C., Tobi, D., Intrinsic dynamics of enzymes in the unbound state and relation to allosteric regulation. Curr. Opin. Struct. Biol. 17 (2007), 633–640.
28. Bahar, I., Lezon, T.R., et al., Eyal, E., Global dynamics of proteins: bridging between structure and function. Annu. Rev. Biophys. 39 (2010), 23–42.
29. Daily, M.D., Gray, J.J., Local motions in a benchmark of allosteric proteins. Proteins 67 (2007), 385–399.
30. Togashi, Y., Mikhailov, A.S., Nonlinear relaxation dynamics in elastic networks and design principles of molecular machines. Proc. Natl. Acad. Sci. USA 104 (2007), 8697–8702.
31. Cressman, A., Togashi, Y., et al., Kapral, R., Mesoscale modeling of molecular machines: cyclic dynamics and hydrodynamical fluctuations. Phys. Rev. E Stat. Nonlin. Soft Matter Phys., 77, 2008, 050901 (R).
32. Huang, M.-J., Kapral, R., et al., Chen, H.-Y., Coarse-grain simulations of active molecular machines in lipid bilayers. J. Chem. Phys., 138, 2013, 195101.
33. Sakaue, T., Kapral, R., Mikhailov, A.S., Nanoscale swimmers: hydrodynamic interactions and propulsion of molecular machines. Eur. Phys. J. B 75 (2010), 381–387.
34. Sarkar, A., Flechsig, H., Mikhailov, A.S., Towards synthetic molecular motors: a model elastic-network study. New J. Phys., 18, 2016, 043006.
35. Flechsig, H., Mikhailov, A.S., Tracing entire operation cycles of molecular motor hepatitis C virus helicase in structurally resolved dynamical simulations. Proc. Natl. Acad. Sci. USA 107 (2010), 20875–20880.
36. Flechsig, H., Popp, D., Mikhailov, A.S., In silico investigation of conformational motions in superfamily 2 helicase proteins. PLoS One, 6, 2011, e21809.
37. Düttmann, M., Togashi, Y., et al., Mikhailov, A.S., Myosin-V as a mechanical sensor: an elastic network study. Biophys. J. 102 (2012), 542–551.
38. Tirion, M.M., Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys. Rev. Lett. 77 (1996), 1905–1908.
39. Haliloglu, T., Bahar, I., Erman, B., Gaussian dynamics of folded proteins. Phys. Rev. Lett. 79 (1997), 3090–3093.
40. Houdusse, A., Sweeney, H.L., How myosin generates force on actin filaments. Trends Biochem. Sci. 41 (2016), 989–997.
41. Coureux, P.-D., Sweeney, H.L., Houdusse, A., Three myosin V structures delineate essential features of chemo-mechanical transduction. EMBO J. 23 (2004), 4527–4537.
42. Cecchini, M., Houdusse, A., Karplus, M., Allosteric communication in myosin V: from small conformational changes to large directed movements. PLOS Comput. Biol., 4, 2008, e1000129.
43. Monod, J., Wyman, J., Changeux, J.P., On the nature of allosteric transitions: a plausible model. J. Mol. Biol. 12 (1965), 88–118.
44. Koshland, D.E. Jr., Némethy, G., Filmer, D., Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5 (1966), 365–385.
45. Flechsig, H., Nucleotide-induced conformational dynamics in ABC transporters from structure-based coarse grained modeling. Front. Phys., 4, 2016, 3.
46. Yan, L., Ravasio, R., et al., Wyart, M., Architecture and coevolution of allosteric materials. Proc. Natl. Acad. Sci. USA 114 (2017), 2526–2531.
47. Rocks, J.W., Pashine, N., et al., Nagel, S.R., Designing allostery-inspired response in mechanical networks. Proc. Natl. Acad. Sci. USA 114 (2017), 2520–2525.
48. Flechsig, H. 2016. Evolutionary optimization of simple polymer networks: models of synthetic allosteric proteins. In NIG International Symposium 2016 Japan Q-Bio week, Tokyo Symposium, Jan 9–11, 2016. https://q-bio.jp/wiki/IIS_Sympo#NIG_International_Symposium_2016.
49. Miyashita, O., Onuchic, J.N., Wolynes, P.G., Nonlinear elasticity, protein quakes, and the energy landscapes of functional transitions in proteins. Proc. Natl. Acad. Sci. USA 100 (2003), 12570–12575.
50. Togashi, Y., Yanagida, T., Mikhailov, A.S., Nonlinearity of mechanochemical motions in motor proteins. PLOS Comput. Biol., 6, 2010, e1000814.
51. Humphrey, W., Dalke, A., Schulten, K., VMD: visual molecular dynamics. J. Mol. Graph. 14 (1996), 27–38.