Markov propagation of allosteric effects in biomolecular systems: Application to GroEL-GroES

Molecular Systems Biology

Volumn 2, Issue , 2006, Pages

  Chennubhotla, Chakra ^a   Bahar, Ivet ^a  

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

Author keywords

Allosteric effects; Chaperonins; Information propagation; Markov process; Network model

Indexed keywords

ARGININE; CHAPERONIN; GLUTAMIC ACID; PROLINE; PROTEIN SUBUNIT; THREONINE; NUCLEOTIDE;

ALGORITHM; ALLOSTERISM; ARTICLE; CIS ISOMER; CLUSTER ANALYSIS; INFORMATION PROCESSING; MOLECULAR MODEL; NETWORK LEARNING; NUCLEOTIDE BINDING SITE; PRIORITY JOURNAL; PROBABILITY; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN NUCLEIC ACID INTERACTION; PROTEIN STRUCTURE; SIGNAL TRANSDUCTION; STRUCTURAL PROTEOMICS; STRUCTURE ACTIVITY RELATION; TRANS ISOMER; BINDING SITE; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; PROTEIN TERTIARY STRUCTURE; STATISTICS;

BACTERIA (MICROORGANISMS);

ALLOSTERIC REGULATION; BINDING SITES; GROEL PROTEIN; GROES PROTEIN; MARKOV CHAINS; MODELS, MOLECULAR; NUCLEOTIDES; PROTEIN STRUCTURE, TERTIARY; PROTEIN SUBUNITS; STOCHASTIC PROCESSES;

EID: 33749055796     PISSN: 17444292     EISSN: 17444292     Source Type: Journal    
DOI: 10.1038/msb4100075     Document Type: Article

References (58)

1. Aharoni A, Horovitz A (1996) Inter-ring communication is disrupted in the GroEL mutant Arg13 → Gly; Ala126 → Val with known crystal structure. J Mol Biol 258: 732-735
2. Aharoni A, Horovitz A (1997) Detection of changes in pairwise interactions during allosteric transitions: coupling between local and global conformational changes in GroEL. Proc Natl Acad Sci 94: 1698-1702
3. Atilgan AR, Durell SR, Jernigan RL, Demirel MC, Keskin O, Bahar I (2001) Anisotropy of fluctuation dynamics of proteins with an elastic network model. Biophys J 80: 505
4. Bahar I, Rader AJ (2005) Coarse-grained normal mode analysis in structural biology. Curr Opin Struct Biol 15: 1-7
5. Bahar I, Erman B, Monnerie L (1994) Effect of molecular structures on local chain dynamics: analytical approaches and computational methods. Adv Polym Sci 116: 151-206
6. Bahar I, Atilgan AR, Erman B (1997) Direct evaluation of thermal fluctuations in protein using a single parameter harmonic potential. Folding Des 2: 173-181
7. Berman HM, Westbrook J, Feng Z, Gilliland G, Bhat TN, Weissig H, Shindyalov IN, Bourne PE (2000) The Protein Data Bank. Nucleic Acids Res 28: 235-242
8. Braig K, Otwinowski Z, Hegde R, Boisvert D, Joachimiak A, Horwich AL, Sigler PB (1994) The crystal structure of the bacterial chaperonin at 2.8å. Nature 371: 578-586
9. Changeux JP, Edelstein SJ (2005) Allosteric mechanisms of signal transduction. Science 308: 1424-1428
10. Chennubhotla C, Bahar I (2006) Markov models for hierarchical coarse-graining of large protein dynamics. Lecture Notes in Computer Science 3909: 379-393
11. Chennubhotla C, Jepson A (2005) Hierarchical eigensolver for transition matrices in spectral methods. In LK Saul, Y Weiss & L Bottou (eds) Adv. in Neural Information Processing Systems 17, 273-280. Cambridge, MA: MIT Press
12. Chennubhotla C, Rader AJ, Yang LW, Bahar I (2005) Elastic network models for understanding biomolecular machinery: from enzymes to supramolecular assemblies. Phys Biol 2: S173-S180
13. Chung FRK (1997) Spectral Graph Theory, CBMS Lectures. AM. Math. Soc., Providence, RL, USA
14. Coifman RR, Lafon S, Lee AB, Maggioni M, Nadler B, Warner F, Zucker SW (2005) Geometric diffusion as a tool for harmonic analysis and structure definition of data, part I:. Proc Natl Acad Sci USA 102: 21
15. Cormen TH, Leiserson CE, Rivest RL (1990) Introduction to Algorithms. Cambridge, MA, USA: MIT Press
16. Danziger O, Rivenzon-Segal D, Wolf S, Horovitz A (2003) Conversion of the allosteric transition of GroEL from concerted to sequential by the single mutation. Proc Natl Acad Sci USA 100: 13797-13802
17. de Groot BL, Vriend G, Berendsen HJC (1999) Conformational changes in the chaperonin GroEL: new insights into the allosteric mechanism. J Mol Biol 286: 1241-1249
18. Doruker P, Atilgan AR, Bahar I (2000) Dynamics of proteins predicted by molecular dynamics simulations and analytical approaches: application to α-amylase inhibitor. Proteins 40: 512-524
19. Fenton W, Kashi Y, Furtak K, Horwich A (1994) Residues in chaperonin GroEL required for polypeptide binding and release. Nature 371: 614-619
20. Flory PJ (1976) Statistical thermodynamics of random networks. Proc Roy Soc London A 351: 351-378
21. Haliloglu T, Bahar I, Erman B (1997) Gaussian dynamics of folded proteins. Phys Rev Lett 79: 3090-3093
22. Hinsen K (1998) Analysis of domain motions by approximate normal mode calculations. Proteins 33: 417
23. Hohfeld J, Hartl FU (1994) Role of the chaperonin cofactor hsp10 in protein folding and sorting in yeast mitochondria. J Cell Biol 126: 305-315
24. Horovitz A, Willison KR (2005) Allosteric regulation of chaperonins. Curr Opin Struct Biol 15: 1-6
25. Horovitz A, Amir A, Danziger O, Kafri G (2002) φ value analysis of heterogeneity in pathways of allosteric transitions: evidence for parallel pathways of ATP-induced conformational changes in GroEL ring. Proc Natl Acad Sci USA 99: 14095-14097
26. Kass I, Horovitz A (2002) Mapping pathways of allosteric communication in GroEL by analysis of correlated mutations. Proteins 48: 611-617
27. Keskin O, Bahar I, Flatow D, Covell DG, Jernigan RL (2002) Molecular mechanisms of chaperonin GroEL-GroES function. Biochemistry 41: 491-501
28. Koshland DE, Nemethy G, Filmer D (1966) Comparison of experimental binding data and theoretical models in proteins containing subunits. Biochemistry 5: 365-385
29. Kovalenko O, Yifrach O, Horovitz A (1994) Residue lysine-34 in GroES modulates allosteric transitions in GroEL. Biochemistry 33: 14974-14978
30. Kullback S (1959) Information Theory and Statistics. NY: Dover Publications
31. Landry SJ, Zeilstra-Ryalls J, Fayet O, Georgopoulos C, Gierasch LM (1993) Characterization of a functionally important mobile domain of GroES. Nature 364: 255-258
32. Lockless SW, Ranganathan R (1999) Evolutionarily conserved pathways of energetic connectivity in protein families. Science 286: 295-299
33. Ma J (2005) Usefulness and limitations of normal mode analysis in modeling dynamics of biomolecular complexes. Curr Opin Struct Biol 13: 373-380
34. Ma J, Karplus M (1998) The allosteric mechanism of the chaperonin GroEL: a dynamic analysis. Proc Natl Acad Sci USA 95: 8502-8507
35. Ma J, Sigler PB, Xu ZH, Karplus M (2000) A dynamic model for the allosteric mechanism of GroEL. J Mol Biol 302: 303-313
36. McLachlan GJ, Basford KE (1988) Mixture Models: Inference and Applications to Clustering. Marcel Dekker, New York
37. Ming D, Wall ME (2005) Quantifying allosteric effects in proteins. Proteins Struct Funct Bioinformatics 59: 697-707
38. Monod J, Wyman J, Changeux JP (1965) Allosteric proteins and cellular control systems. J Mol Biol 12: 88-118
39. Nadler B, Lafon S, Coifman RR, Kevrekidis IG (2006) Diffusion maps, spectral clustering, and the reaction coordinates of dynamical systems. J Appl Comp Harmonic Anal (in press)
40. Norris JR (1997) Markov Chain. Cambridge: Cambridge University Press
41. Richardson A, Georgopoulos C (1999) Genetic analysis of the bacteriophage t4-encoded cochaperonin gp31. Genetics 152: 1449-1457
42. Richardson A, van der Vies SM, Keppel F, Taher A, Landry SJ, Georgopoulos C (1999) Compensatory changes in GroEL/gp31 affinity as a mechanism for allele-specific genetic interaction. J Biol Chem 274: 52-58
43. Richardson A, Schwager F, Landry SJ, Georgopoulos C (2001) The importance of a mobile loop in regulating chaperonin/co-chaperonin interaction: humans versus Escherichia coli. J Biol Chem 276: 4981-4987
44. Saibil HR, Ranson NR (2002) The chaperonin folding machine. Trends Biochem Sci 627-632
45. Sewell BT, Best RB, Chen S, Roseman AM, Farr GW, Horwich AL, Saibil HR (2004) A mutant chaperonin with rearranged inter-ring electrostatic contacts and temperature-sensitive disassociation. Nat Struct Mol Biol 11: 1128-1133
46. Shewmaker F, Maskos K, Simmerling C, Landry S (2001) The disordered mobile loop of GroES folds into a defined beta-hairpin upon binding GroEL. J Biol Chem 276: 31257-31264
47. Shewmaker F, Kerner MJ, Hayer-Hartl M, Klein G, Georgopoulos C, Landry SJ (2004) A mobile loop order-disorder transition modulates the speed of chaperoin cycling. Protein Sci 13: 2139-2148
48. Sigler PB, Xu ZH, Rye HS, Burston WA, Fenton SG, Horwich AL (1998) Structure and function in GroEL-mediated protein folding. Annu Rev Biochem 67: 581-608
49. Stan G, Thirumalai D, Lorimer G, Brooks B (2003) Annealing function of GroEL: structural and bioinformatic analysis. Biophys Chem 100: 453-467
50. Suel GM, Lockless SW, Wall MA, Ranganathan R (2003) Evolutionarily conserved networks of residues mediate allosteric communication in proteins. Nat Struct Biol 10: 59-68
51. Thirumalai D, Lorimer GH (2001) Chaperonin-mediated protein folding. Annu Rev Biophys Biomol Struct 30: 245-269
52. Tobi D, Bahar I (2005) Structural changes involved in protein binding correlate with intrinsic motions of proteins in the unbound state. Proc Natl Acad Sci USA 102: 18908-18913
53. White HE, Chen S, Roseman AM, Yifrach O, Horovitz A, Saibil HR (1997) Structural basis of allosteric changes in the GroEL mutant Arg197 → Ala. Nat Struct Mol Biol 4: 690-694
54. Xu C, Tobi D, Bahar I (2003) Allosteric changes in protein structure computed by a simple mechanical model: hemoglobin t → r2 transition. J Mol Biol 333: 153-168
55. 7 chaperonin complex. Nature 388: 741-750
56. Yang LW, Bahar I (2005) Coupling between catalytic site and collective dynamics: a requirement for mechanochemical activity of enzymes. Structure 13: 893-904
57. Yifrach O, Horovitz A (1995) Nested cooperativity in the ATPase activity of the oligomeric chaperonin GroEL. Biochemistry 34: 5303-5308
58. Yifrach O, Horovitz A (1998) Mapping the transition state of the allosteric pathway of GroEL by protein engineering. J Am Chem Soc 120: 13262-13263