Global low-frequency motions in protein allostery: CAP as a model system

Biophysical Reviews

Volumn 7, Issue 2, 2015, Pages 175-182

  Townsend, Philip D ^a   Rodgers, Thomas L ^a,b   Pohl, Ehmke ^a   Wilson, Mark R ^a   McLeish, Tom C B ^a   Cann, Martin J ^a  

^a DURHAM UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

Allostery; Catabolite activator protein; Dynamics; Elastic network model; Normal modes; Protein

Indexed keywords

CYCLIC AMP BINDING PROTEIN; PROTEIN VARIANT;

ALLOSTERISM; ARTICLE; DNA BINDING; DNA BINDING DOMINE; DYNAMICS; ELASTIC NETWORK MODEL; ENTROPY; ESCHERICHIA COLI; GLOBAL PROTEIN MOTION; ISOTHERMAL TITRATION CALORIMETRY; LIGAND BINDING; LIGAND BINDING DOMINE; MOTION; MUTATION; NONHUMAN; NORMAL MODE ANALYSIS; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DYNAMICS; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN STRUCTURE; THERMODYNAMICS;

ESCHERICHIA COLI;

EID: 84929162811     PISSN: 18672450     EISSN: 18672469     Source Type: Journal    
DOI: 10.1007/s12551-015-0163-9     Document Type: Article

References (43)

1. Bahar I, Atilgan AR, Demirel MC, Erman B (1998) Vibrational dynamics of folded proteins: Significance of slow and fast motions in relation to function and stability. Phys Rev Lett 80:2733–2736
2. Bakan A, Meireles LM, Bahar I (2011) ProDy: protein dynamics inferred from theory and experiments. Bioinformatics 27:1575–1577. doi:10.1093/bioinformatics/btr168
3. Balabin IA, Yang W, Beratan DN (2009) Coarse-grained modeling of allosteric regulation in protein receptors. Proc Natl Acad Sci U S A 106:14253–14258. doi:10.1073/pnas.0901811106
4. Brooks B, Karplus M (1983) Harmonic dynamics of proteins: normal modes and fluctuations in bovine pancreatic trypsin inhibitor. Proc Natl Acad Sci U S A 80:6571–6575
5. Brown A (2009) Analysis of cooperativity by isothermal titration calorimetry. Int J Mol Sci 10:3457–3477. doi:10.3390/ijms10083457
6. Cooper A, Dryden DT (1984) Allostery without conformational change. A plausible model. Eur Biophys J 11:103–109. The first overt theoretical description of dynamic allostery demonstrating the relevance of a purely entropic thermodynamic contribution to protein function
7. Cornish-Bowden A (2014) Understanding allosteric and cooperative interactions in enzymes. FEBS J 281:621–632. doi:10.1111/febs.12469
8. Delarue M, Sanejouand YH (2002) Simplified normal mode analysis of conformational transitions in DNA-dependent polymerases: the elastic network model. J Mol Biol 320:1011–1024
9. Durand P, Trinquier G, Sanejouand YH (1994) New Approach for Determining Low-Frequency Normal-Modes in Macromolecules. Biopolymers 34:759–771
10. Go N, Noguti T, Nishikawa T (1983) Dynamics of a small globular protein in terms of low-frequency vibrational modes. Proc Natl Acad Sci U S A 80:3696–3700
11. Gorke B, Stulke J (2008) Carbon catabolite repression in bacteria: many ways to make the most out of nutrients. Nat Rev Microbiol 6:613–624. doi:10.1038/nrmicro1932
12. Hawkins RJ, McLeish TC (2004) Coarse-grained model of entropic allostery. Phys Rev Lett 93:098104
13. Hawkins RJ, McLeish TC (2006a) Dynamic allostery of protein alpha helical coiled-coils. J R Soc Interface 3:125–138. doi:10.1098/rsif.2005.0068
14. Hawkins RJ, McLeish TCB (2006b) Coupling of global and local vibrational modes in dynamic allostery of proteins. Biophys J 91:2055–2062
15. Hawkins RJ, McLeish TCB (2006c) Dynamic allostery of protein alpha helical coiled-coils. J R Soc Interface 3:125–138
16. Hilser VJ, Wrabl JO, Motlagh HN (2012) Structural and energetic basis of allostery. Annu Rev Biophys 41:585–609. doi:10.1146/annurev-biophys-050511-102319
17. Koshland DE Jr, Nemethy G, Filmer D (1966) Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5:365–385
18. Liu T, Whitten ST, Hilser VJ (2007) Functional residues serve a dominant role in mediating the cooperativity of the protein ensemble. Proc Natl Acad Sci U S A 104:4347–4352
19. Maguid S, Fernandez-Alberti S, Parisi G, Echave J (2006) Evolutionary conservation of protein backbone flexibility. J Mol Evol 63:448–457. doi:10.1007/s00239-005-0209-x
20. Maguid S, Fernandez-Alberti S, Echave J (2008) Evolutionary conservation of protein vibrational dynamics. Gene 422:7–13. doi:10.1016/j.gene.2008.06.002
21. Manley G, Rivalta I, Loria JP (2013) Solution NMR and computational methods for understanding protein allostery. J Phys Chem B 117:3063–3073. doi:10.1021/jp312576v
22. McLeish TC, Rodgers TL, Wilson MR (2013) Allostery without conformation change: modelling protein dynamics at multiple scales. Phys Biol 10:056004. doi:10.1088/1478-3975/10/5/056004
23. Monod J, Wyman J, Changeux JP (1965) On the Nature of Allosteric Transitions - a Plausible Model. J Mol Biol 12:88–118
24. Motlagh HN, Hilser VJ (2012) Agonism/antagonism switching in allosteric ensembles. Proc Natl Acad Sci U S A 109:4134–4139
25. Motlagh HN, Wrabl JO, Li J, Hilser VJ (2014) The ensemble nature of allostery. Nature 508:331–339. doi:10.1038/nature13001
26. Nicolay S, Sanejouand YH (2006) Functional modes of proteins are among the most robust. Phys Rev Lett 96:078104
27. Popovych N, Sun S, Ebright RH, Kalodimos CG (2006) Dynamically driven protein allostery. Nat Struct Mol Biol 13:831–838. The first experimental demonstration of purely dynamically driven allostery using the CAP protein as a model
28. Raimondi F, Orozco M, Fanelli F (2010) Deciphering the deformation modes associated with function retention and specialization in members of the Ras superfamily. Structure 18:402–414. doi:10.1016/j.str.2009.12.015
29. Reynolds KA, McLaughlin RN, Ranganathan R (2011) Hot spots for allosteric regulation on protein surfaces. Cell 147:1564–1575. doi:10.1016/j.cell.2011.10.049
30. Rodgers TL, Burnell D, Townsend PD, Pohl E, Cann MJ, Wilson MR, McLeish TC (2013a) ΔΔPT: a comprehensive toolbox for the analysis of protein motion. BMC Bioinforma 14:183. doi:10.1186/1471-2105-14-183
31. Rodgers TL et al (2013b) Modulation of Global Low-Frequency Motions Underlies Allosteric Regulation: Demonstration in CRP/FNR Family Transcription Factors. PLoS Biol 11:e1001651. doi:10.1371/journal.pbio.1001651. A key paper that links a theoretical analysis for the role of low frequence backbone motion in CAP to experimentally validated predictive engineering of allostery
32. Suhre K, Sanejouand YH (2004) ElNemo: a normal mode web server for protein movement analysis and the generation of templates for molecular replacement. Nucleic Acids Res 32:W610–W614. doi:10.1093/nar/gkh368
33. Tama F, Sanejouand YH (2001) Conformational change of proteins arising from normal mode calculations. Protein Eng 14:1–6
34. Tirion MM (1996) Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys Rev Lett 77:1905–1908
35. Toncrova H, McLeish TC (2010) Substrate-modulated thermal fluctuations affect long-range allosteric signaling in protein homodimers: exemplified in CAP. Biophys J 98:2317–2326. doi:10.1016/j.bpj.2010.01.039
36. Townsend PD et al (2014) The Crystal Structures of Apo and cAMP-Bound GlxR from Corynebacterium glutamicum Reveal Structural and Dynamic Changes upon cAMP Binding in CRP/FNR Family Transcription Factors. PLoS ONE 9:e113265. doi:10.1371/journal.pone.0113265
37. Tzeng SR, Kalodimos CG (2009) Dynamic activation of an allosteric regulatory protein. Nature 462:368–372. doi:10.1038/nature08560
38. Tzeng SR, Kalodimos CG (2012) Protein activity regulation by conformational entropy. Nature 488:236–240. doi:10.1038/nature11271
39. Valadie H, Lacapcre JJ, Sanejouand YH, Etchebest C (2003) Dynamical properties of the MscL of Escherichia coli: a normal mode analysis. J Mol Biol 332:657–674
40. Wand AJ (2013) The dark energy of proteins comes to light: conformational entropy and its role in protein function revealed by NMR relaxation. Curr Opin Struct Biol 23:75–81. doi:10.1016/j.sbi.2012.11.005
41. Zhuravleva A, Gierasch LM (2011) Allosteric signal transmission in the nucleotide-binding domain of 70-kDa heat shock protein (Hsp70) molecular chaperones. Proc Natl Acad Sci U S A 108:6987–6992. doi:10.1073/pnas.1014448108
42. Zhuravleva A, Clerico EM, Gierasch LM (2012) An Interdomain Energetic Tug-of-War Creates the Allosterically Active State in Hsp70. Mol Chaperones Cell 151:1296–1307. doi:10.1016/j.cell.2012.11.002
43. Zimmermann MT, Kloczkowski A, Jernigan RL (2011) MAVENs: motion analysis and visualization of elastic networks and structural ensembles. BMC Bioinforma 12:264. doi:10.1186/1471-2105-12-264