"Fluctuograms" reveal the intermittent intra-protein communication in subtilisin carlsberg and correlate mechanical coupling with co-evolution

PLoS Computational Biology

Volumn 7, Issue 3, 2011, Pages

  Silvestre Ryan, Jordi ^a   Lin, Yuchun ^b   Chu, Jhih Wei ^b  

^a University of California   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMINO ACIDS; ATOMS; BINDING SITES; MOLECULAR DYNAMICS;

ALLOSTERIC COUPLING; CA 2+; CO-EVOLUTION; COUPLING NETWORK; MECHANICAL COUPLING; MUTATION SITES; PROTEIN FUNCTIONS; STRUCTURE-PROPERTIES RELATIONSHIPS; SUBTILISIN; SUBTILISIN CARLSBERG;

PROTEINS;

CALCIUM ION; SUBTILISIN; SUBTILISIN CARLSBERG; UNCLASSIFIED DRUG; CALCIUM;

ALLOSTERISM; ARTICLE; BINDING SITE; BIOINFORMATICS; CALCIUM BINDING; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; ENZYME STABILITY; EXCITATION CONTRACTION COUPLING; FLUCTUOGRAM; GENE MUTATION; MATHEMATICAL MODEL; MOLECULAR DYNAMICS; MOLECULAR EVOLUTION; PROTEIN ANALYSIS; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN SYNTHESIS REGULATION; SEQUENCE ALIGNMENT; SOUND DETECTION; CHEMICAL STRUCTURE; CHEMISTRY; METABOLISM; MOLECULAR GENETICS; MUTATION;

BINDING SITES; CALCIUM; MODELS, MOLECULAR; MOLECULAR DYNAMICS SIMULATION; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN CONFORMATION; SEQUENCE ALIGNMENT; SUBTILISINS;

EID: 79953671764     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002023     Document Type: Article

References (81)

1. Koshland DE, (1958) Application of a theory of enzyme specificity to protein synthesis. Proc Natl Acad Sci USA 44: 98-104.
2. Monod J, Wyman J, Changeux JP, (1965) An nature of allosteric transitions- A plausible model. J Mol Biol 12: 88-118.
3. Yu EW, Koshland DE, (2001) Propagating conformational changes over long (and short) distances in proteins. Proc Natl Acad Sci USA 98: 9517-9520.
4. Kraut J, (1977) Serine proteases- Structure and mechanism of catalysis. Annu Rev Biochem 46: 331-358.
5. Barrette-Ng IH, Ng KKS, Cherney MM, Pearce G, Ryan CA, et al. (2003) Structural basis of inhibition revealed by a 1: 2 complex of the two-headed tomato inhibitor-II and subtilisin Carlsberg. J Biol Chem 278: 24062-24071.
6. Bryan PN, (2000) Protein engineering of subtilisin. BBA-Protein Struct M 1543: 203-222.
7. Wells JA, Estell DA, (1988) Subtilisin- An enzyme designed to be engineered. Trends Biochem Sci 13: 291-297.
8. Smock RG, Gierasch LM, (2009) Sending signals dynamically. Science 324: 198-203.
9. Ma B, Nussinov R, (2009) Amplification of signaling via cellular allosteric relay and protein disorder. Proc Natl Acad Sci USA 106: 6887-6888.
10. McNicholl ET, Das R, SilDas S, Taylor SS, Melacini G, (2010) Communication between tandem camp binding domains in the regulatory subunit of protein kinase A-I alpha as revealed by domain-silencing mutations. J Biol Chem 285: 15523-15537.
11. Whitley MJ, Lee AL, (2009) Frameworks for understanding long-range intra-protein communication. Curr Protein Pept Sci 10: 116-127.
12. Tsai C-J, del Sol A, Nussinov R, (2009) Protein allostery, signal transmission and dynamics: a classification scheme of allosteric mechanisms. Mol Biosyst 5: 207-216.
13. Cui Q, Karplus M, (2008) Allostery and cooperativity revisited. Protein Sci 17: 1295-1307.
14. Zheng WJ, Brooks BR, Thirumalai D, (2006) Low-frequency normal modes that describe allosteric transitions in biological nanomachines are robust to sequence variations. Proc Natl Acad Sci USA 103: 7664-7669.
15. Chennubhotla C, Bahar I, (2006) Markov propagation of allosteric effects in biomolecular systems: application to GroEL-GroES. Mol Syst Biol 2: 36.
16. Del Sol A, Tsai C-J, Ma B, Nussinov R, (2009) The Origin of Allosteric Functional Modulation: Multiple Pre-existing Pathways. Structure 17: 1042-1050.
17. Bahar I, Lezon TR, Yang L-W, Eyal E, (2010) Global Dynamics of Proteins: Bridging Between Structure and Function. Annu Rev Biophys 39: 23-42.
18. Sherwood P, Brooks BR, Sansom MS, (2008) Multiscale methods for macromolecular simulations. Curr Opin Struct Biol 18: 630.
19. Hilser VJ, Dowdy D, Oas TG, Freire E, (1998) The structural distribution of cooperative interactions in proteins: Analysis of the native state ensemble. Proc Natl Acad Sci USA 95: 9903-9908.
20. Hilser VJ, Garcia-Moreno B, Oas TG, Kapp G, Whitten ST, (2006) A statistical thermodynamic model of the protein ensemble. Chem Rev 106: 1545-1558.
21. Noid WG, Chu J-W, Ayton GS, Krishna V, Izvekov S, et al. (2008) The multiscale coarse-graining method. I. A rigorous bridge between atomistic and coarse-grained models. J Chem Phys 128: 244114.
22. Cho H, Chu J-W, (2009) Inversion of Radial Distribution Functions to Pair Forces by Solving the Yvon-Born-Green Equation Iteratively. J Chem Phys 131: 134107.
23. Lee S, Jang DJ, (2000) Cation-binding sites of subtilisin Carlsberg probed with Eu(III) luminescence. Biophys J 79: 2171-2177.
24. Alexander PA, Ruan B, Bryan PN, (2001) Cation-dependent stability of subtilisin. Biochemistry 40: 10634-10639.
25. Gallagher T, Bryan PN, Gilliland GL, (1993) Calcium-independent subtilisin by design. Proteins 16: 205-213.
26. Tirion MM, (1996) Large amplitude elastic motions in proteins from a single-parameter, atomic analysis. Phys Rev Lett 77: 1905-1908.
27. Bahar I, Atilgan AR, Jernigan RL, Erman B, (1997) Understanding the recognition of protein structural classes by amino acid composition. Proteins 29: 172-185.
28. Chu J-W, Voth GA, (2006) Coarse-grained modeling of the actin filament derived from atomistic-scale simulations. Biophys J 90: 1572-1582.
29. Lyman E, Pfaendtner J, Voth GA, (2008) Systematic Multiscale Parameterization of Heterogeneous Elastic Network Models of Proteins. Biophys J 95: 4183-4192.
30. Johnson K, (2003) Acoustic and Auditory Phonetics Malden Blackwell Publishing.
31. Zhao H, Arnold F, (1999) Directed evolution converts subtilisin E into a functional equivalent of thermitase. Protein Eng 12: 47-53.
32. Strausberg S, Alexander P, Gallagher D, Gilliland G, Barnett B, et al. (1995) Directed evolution of a subtilisin with calcium-independent stability. Biotechnology 13: 669-673.
33. Strausberg S, Ruan B, Fisher K, Alexander P, Bryan P, (2005) Directed coevolution of stability and catalytic activity in calcium-free subtilisin. Biochemistry 44: 3272-3279.
34. Rollence ML, Filpula D, Pantoliano MW, Bryan PN, (1988) Engineering thermostability in subtilisin BPN' by in vitro mutagenesis. CRC Crit Rev Biotech 8: 217-224.
35. Chen K, Arnold F, (1991) Enzyme engineering for nonaqueous solvents- random mutagenesis to enhance activity of subtilisin-E in polar organic media. Biotechnology 9: 1073-1077.
36. Chen K, Arnold F, (1993) Tuning the activity of an enzyme for unusual environments- sequential random mutagenesis of subtilisin-E for catalysis in dimethylformamide. Proc Natl Acad Sci USA 90: 5618-5622.
37. Suel GM, Lockless SW, Wall MA, Ranganathan R, (2003) Evolutionarily conserved networks of residues mediate allosteric communication in proteins. Nat Struct Biol 10: 59-69.
38. Halabi N, Rivoire O, Leibler S, Ranganathan R, (2009) Protein sectors: Evolutionary units of three-dimensional structure. Cell 138: 774-786.
39. Zhou HX, (2004) Polymer models of protein stability, folding, and interactions. Biochemistry 43: 2141-2154.
40. Tracewell CA, Arnold FH, (2009) Directed enzyme evolution: climbing fitness peaks one amino acid at a time. Curr Opin Chem Biol 13: 3-9.
41. Eppler RK, Komor RS, Huynh J, Dordick JS, Reimer JA, et al. (2006) Water dynamics and salt-activation of enzymes in organic media: Mechanistic implications revealed by NMR spectroscopy. Proc Natl Acad Sci USA 103: 5706-5710.
42. Eppler RK, Hudson EP, Chase SD, Dordick JS, Reimer JA, et al. (2008) Biocatalyst activity in nonaqueous environments correlates with centisecond-range protein motions. Proc Natl Acad Sci USA.
43. Hudson EP, Eppler RK, Beaudoin JM, S. DJ, Reimer JA, et al. (2009) Active-Site Motions and Polarity Enhance Catalytic Turnover of Hydrated Subtilisin Dissolved in Organic Solvents. J Am Chem Soc 131: 7.
44. Pantoliano MW, Whitlow M, Wood JF, Rollence ML, Finzel BC, et al. (1988) The engineering of binding-affinity at metal-ion binding-sites for the stabilization of proteins- Subtilisin as a test case. Biochemistry 27: 8311-8317.
45. Tsai C-J, Del Sol A, Nussinov R, (2008) Allostery: Absence of a change in shape does not imply that allostery is not at play. J Mol Biol 378: 1-11.
46. Plerou V, Gopikrishnan P, Rosenow B, Amaral LAN, Guhr T, et al. (2002) Random matrix approach to cross correlations in financial data. Phys Rev E 65: 066126.
47. Fisher KE, Ruan B, Alexander PA, Wang L, Bryan PN, (2007) Mechanism of the kinetically-controlled folding reaction of subtilisin. Biochemistry 46: 640-651.
48. Daily MD, Upadhyaya TJ, Gray JJ, (2008) Contact rearrangements form coupled networks from local motions in allosteric proteins. Proteins 71: 455-466.
49. Vendruscolo M, Paci E, Dobson CM, Karplus M, (2001) Three key residues form a critical contact network in a protein folding transition state. Nature 409: 641-645.
50. Vendruscolo M, Dokholyan NV, Paci E, Karplus M, (2002) Small-world view of the amino acids that play a key role in protein folding. Phys Rev E 65: 061910.
51. del Sol A, Fujihashi H, Amoros D, Nussinov R, (2006) Residues crucial for maintaining short paths in network communication mediate signaling in proteins. Mol Syst Biol 2: 2006.0019.
52. Ghosh A, Vishveshwara S, (2007) A study of communication pathways in methionyl-tRNA synthetase by molecular dynamics simulations and structure network analysis. Proc Natl Acad Sci USA 104: 15711-15716.
53. Zheng W, Brooks BR, Thirumalai D, (2009) Allosteric transitions in biological nanomachines are described by robust normal modes of elastic networks. Curr Protein Pept Sc 10: 128-132.
54. Fodor AA, Aldrich RW, (2004) On evolutionary conservation of thermodynamic coupling in proteins. J Biol Chem 279: 19046-19050.
55. Chi CN, Elfstrom L, Shi Y, Snall T, Engstrom A, et al. (2008) Reassessing a sparse energetic network within a single protein domain. Proc Natl Acad Sci USA 105: 4679-4684.
56. Liu Z, Chen J, Thirumalai D, (2009) On the accuracy of inferring energetic coupling between distant sites in protein families from evolutionary imprints: Illustrations using lattice model. Proteins 77: 823-831.
57. Kleywegt G, Zou J, Divne C, Davies G, Sinning I, et al. (1997) The crystal structure of the catalytic core domain of endoglucanase I from Trichoderma reesei at 3.6 angstrom resolution, and a comparison with related enzymes. J Mol Biol 272: 383-397.
58. Csermely P, Palotai R, Nussinov R, (2010) Induced fit, conformational selection and independent dynamic segments: an extended view of binding events. Trends Biochem Sci 35: 539-546.
59. Brokaw J, Chu J-W, (2010) On the Roles of Substrate Binding and Hinge Unfolding in Conformational Changes of Adenylate Kinase. Biophys J 99: 3420-3429.
60. Brokaw JB, Haas KR, Chu J-W, (2009) Reaction Path Optimization with Holonomic Constraints and Kinetic-Energy Potentials. J Chem Theory Comput 5: 2050-2061.
61. Haas RK, Chu J-W, (2009) Decomposition of energy and free energy changes by following the flow of work along reaction path. J Chem Phys 131: 144105.
62. Mackerell AD, (2004) Empirical force fields for biological macromolecules: Overview and issues. J Comput Chem 25: 1584-1604.
63. Mackerell AD, Feig M, Brooks CL, (2004) Extending the treatment of backbone energetics in protein force fields: limitations of gas-phase quantum mechanics in reproducing protein conformational distributions in molecular dynamics simulations. J Comput Chem 25: 1400-1415.
64. Darden T, York D, Pederson L, (1993) Particle mesh Ewald: an Nlog(N) method for Ewald sums in large systems. J Chem Phys 98: 10089.
65. Allen MP, Tildesley DJ, (1987) Computer Simulation of Liquids New York Oxford.
66. Feller SE, Zhang YH, Pastor RW, Brooks BR, (1995) Constant-pressure molecular-dynamics simulation- The Langevin piston method. J Chem Phys 103: 4613-4621.
67. Phillips JC, Braun R, Wang W, Gumbart J, Tajkhorshid E, et al. (2005) Scalable molecular dynamics with NAMD. J Comput Chem 26: 1781-1802.
68. Brooks BR, Brooks CL, Mackerell AD, Nilsson L, Petrella RJ, et al. (2009) CHARMM: The Biomolecular Simulation Program. J Comput Chem 30: 1545-1614.
69. Humphrey W, Dalke A, Schulten K, (1996) VMD: Visual molecular dynamics. J Mol Graphics 14: 33-38.
70. Lezon TR, Sali A, Bahar I, (2009) Global Motions of the Nuclear Pore Complex: Insights from Elastic Network Models. Plos Comput Biol 5: e1000496.
71. Ming D, Wall ME, (2005) Allostery in a coarse-grained model of protein dynamics. Phys Rev Lett 95: 198103.
72. Maragakis P, Karplus M, (2005) Large amplitude conformational change in proteins explored with a plastic network model: Adenylate kinase. J Mol Biol 352: 807-822.
73. Chu J-W, Voth GA, (2007) Coarse-grained free energy functions for studying protein conformational changes: A double-well network model. Biophys J 93: 3860-3871.
74. Tama F, Valle M, Frank J, Brooks CL, (2003) Dynamic reorganization of the functionally active ribosome explored by normal mode analysis and cryo-electron microscopy. Proc Natl Acad Sci USA 100: 9319-9323.
75. Ma JP, (2005) Usefulness and limitations of normal mode analysis in modeling dynamics of biomolecular complexes. Structure 13: 373-380.
76. Yang L, Song G, Jernigan RL, (2009) Protein elastic network models and the ranges of cooperativity. Proc Natl Acad Sci USA 106: 12347-12352.
77. Brooks BR, Janezic D, Karplus M, (1995) Harmonic-analysis of large systems. 1. methodology. J Comput Chem 16: 1522-1542.
78. Pearson WR, Lipman DJ, (1988) Improved tools for biological sequence comparison. Proc Natl Acad Sci USA 85: 2444-2448.
79. Finn RD, Mistry J, Tate J, Coggill P, Heger A, et al. (2010) The Pfam protein families database. Nucleic Acids Res 38: D211-D222.
80. Katoh K, Kuma K, Toh H, Miyata T, (2005) MAFFT version 5: improvement in accuracy of multiple sequence alignment. Nucleic Acids Res 33: 511-518.
81. Altschul SF, Madden TL, Schaffer AA, Zhang JH, Zhang Z, et al. (1997) Gapped BLAST and PSI-BLAST: a new generation of protein database search programs. Nucleic Acids Res 25: 3389-3402.