Single-molecule dynamics reveals cooperative binding-folding in protein recognition

PLoS Computational Biology

Volumn 2, Issue 7, 2006, Pages 0842-0852

  Wang, Jin ^a,b   Lu, Qiang ^b   Peter Lu, H ^c  

^a CHANGCHUN INSTITUTE OF APPLIED CHEMISTRY   (China)

^b STONY BROOK UNIVERSITY   (United States)

^c PACIFIC NORTHWEST NATIONAL LABORATORY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BINDING ENERGY; BIOCHEMISTRY; COARSE-GRAINED MODELING; CONFORMATIONS; INTERFACE STATES; MOLECULAR DYNAMICS; MOLECULES; PROTEINS;

BIOMOLECULAR RECOGNITION; CONFORMATIONAL CHANGE; CONFORMATIONAL STATE; COOPERATIVE BINDING; ENERGY MINIMA; FOLDINGS; MOLECULAR FUNCTION; PROTEIN RECOGNITION; SINGLE-MOLECULE DYNAMICS; SINGLE-MOLECULE STUDIES;

FREE ENERGY;

CELLULOSE; PROTEIN CDC42; PROTEIN;

ARTICLE; CORRELATION ANALYSIS; ENERGY; LANDSCAPE; MICROSCOPY; MOLECULAR DYNAMICS; MOLECULAR RECOGNITION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN INTERACTION; PROTEIN LOCALIZATION; PROTEIN STRUCTURE; QUANTITATIVE ANALYSIS; THERMAL CONDUCTIVITY; BIOLOGY; CHEMISTRY; HUMAN; METHODOLOGY; NUCLEOTIDE SEQUENCE; PROTEIN TERTIARY STRUCTURE; THEORETICAL MODEL; THERMODYNAMICS;

CDC42 GTP-BINDING PROTEIN; COMPUTATIONAL BIOLOGY; DNA MUTATIONAL ANALYSIS; HUMANS; MODELS, THEORETICAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STRUCTURE, TERTIARY; PROTEINS; THERMODYNAMICS;

EID: 33746607765     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.0020078     Document Type: Article

References (50)

1. Fischer E (1890) . Fischer E (1890) Ueber die Optischen Isomeren des Traubenzuckers, der Gluconsaure und der Zuckersaure. Ber Dtsch Chem Ges 23: 2611-2620.
2. Koshland DE (1958) Application of a theory of enzyme specificity to protein synthesis. Proc Natl Acad Sci U S A 44: 98-104.
3. Dunker AK, Brown CJ, Lawson JD, Iakoucheva LM, Obradovic Z (2002) Intrinsic disorder and protein function. Biochemistry 41: 6573-6582.
4. Shoemaker BA, Portman JJ, Wolynes PG (2000) Speeding molecular recognition by using the folding funnel: The fly-casting mechanism. Proc Natl Acad Sci U S A 97: 8868-8873.
5. Papoian GA, Wolynes PG (2003) The physics and bioinformatics of binding and folding - An energy landscape perspective. Biopolymers 68: 333-349.
6. Levy Y, Wolynes PG, Onuchic JN (2004) Protein topology determines binding mechanism. Proc Natl Acad Sci U S A 101: 511-516.
7. Frauenfelder H, Sligar SG, Wolynes PG (1991) The energy landscapes and motions of proteins. Science 254: 1598-1603.
8. Wang J, Wolynes P (1995) Intermittency of single-molecule reaction dynamics in fluctuating environments. Phys Rev Lett 74: 4317-4320.
9. Geva E, Skinner JL (1998) Two-state dynamics of single biomolecules in solution. Chem Phys Lett 288: 225-229.
10. Yang SL, Cao JS (2001) Two-event echos in single-molecule kinetics: A signature of conformational fluctuations. J Phys Chem B Condens Matter Mater Surf Interfaces Biophys 105: 6536-6549.
11. Moerner WE (1996) High-resolution optical spectroscopy of single molecules in solids. Acc Chem Res 29: 563-571.
12. Lu HP, Xun LY, Xie XS (1998) Single-molecule enzymatic dynamics. Science 282: 1877-1882.
13. Edman L, Rigler R (2000) Memory landscapes of single-enzyme molecules. Proc Natl Acad Sci U S A 97: 8266-8271.
14. Zhuang XW, Bartley LE, Babcock HP, Russell R, Ha TJ, et al. (2000) A single-molecule study of RNA catalysis and folding. Science 288: 2048-2051.
15. Abdul-Manan N, Aghazadeh B, Liu GA, Majumdar A, Ouerfelli O, et al. (1999) Structure of Cdc42 in complex with the GPTase-binding domain of the 'Wiskott-Aldrich syndrome' protein. Nature 399: 379-383.
16. Rudolph MG, Bayer P, Abo A, Kuhlmann J, Vetter IR, et al. (1998) The Cdc42/Rac interactive binding region motif of the Wiskott Aldrich syndrome protein (WASP) is necessary but not sufficient for tight binding to Cdc42 and structure formation. J Biol Chem 273: 18067-18076.
17. Erickson JW, Cerione RA (2001) Multiple roles for Cdc42 in cell regulation. Curr Opin Cell Biol 13: 153-157.
18. Nalbant P, Hodgson L, Kraynov V, Toutchkine A, Hahn KM (2004) Activation of endogenous Cdc42 visualized in living cells. Science 305: 1615-1619.
19. Tan X, Nalbant P, Toutchkine A, Hu DH, Vorpagel ER, et al. (2004) Single-molecule study of protein-protein interaction dynamics in a cell signaling system. J Phys Chem B Condens Matter Mater Surf Interfaces Biophys 108: 737-744.
20. Lu HP (2005) Probing single-molecule protein conformational dynamics. Acc Chem Res 38: 557-565.
21. Lu HP, Iakoucheva LM, Ackerman EJ (2001) Single-molecule conformational dynamics of fluctuating noncovalent DNA-protein interactions in DNA damage recognition. J Am Chem Soc 123: 9184-9185.
22. Levinthal C (1969) How to fold graciously. In: DeBrunner JTP, Munck E, editors. Mössbauer spectroscopy in biological systems: Proceedings of a meeting held at Allerton House, Monticello, Illinois. Urbana (Illinois): University of Illinois Press. pp. 22-24.
23. Rejto PA, Verkhivker GM (1996) Unraveling principles of lead discovery: From unfrustrated energy landscapes to novel molecular anchors. Proc Natl Acad Sci U S A 93: 8945-8950.
24. Janin J (1996) Quantifying biological specificity: The statistical mechanics of molecular recognition. Proteins 25: 438-445.
25. Tsai CJ, Kumar S, Ma BY, Nussinov R (1999) Folding funnels, binding funnels, and protein function. Protein Sci 8: 1181-1190.
26. Wang J, Verkhivker GM (2003) Energy landscape theory, funnels, specificity, and optimal criterion of biomolecular binding. Phys Rev Lett 90: 188101.
27. Go N (1983) Theoretical studies of protein folding. Annual Review of Biophysics and Bioengineering 12: 183-210.
28. Clementi C, Nymeyer H, Onuchic JN (2000) Topological and energetic factors: What determines the structural details of the transition state ensemble and "en-route" intermediates for protein folding? An investigation for small globular proteins. J Mol Biol 298: 937-953.
29. Clementi C, Jennings PA, Onuchic JN. (2001) Prediction of folding mechanism for circluar-permuted proteins. J Mol Biol 311: 879-890.
30. Shea JE, Onuchic JN, Brooks CL (2000) Energetic frustration and the nature of the transition state in protein folding. J Chem Phys 113: 7663-7671.
31. Shea JE, Onuchic JN, Brooks CL (2002) Probing the folding free energy landscape of the Src-SH3 protein Domain. Proc Natl Acad Sci U S A 99: 16064-16068.
32. Cheung MS, Garcia AE, Onuchic JN (2002). Protein folding mediated by solvation: Water expulsion and formation of the hydrophobic core occur after the structural collapse. Proc Natl Acad Sci U S A 99: 685-690.
33. Cheung MS, Finke JM, Callahan B, Onuchic JN (2003) Exploring the interplay of topology and secondary structural formation in the protein folding problem. J Phys Chem B Condens Matter Mater Surf Interfaces Biophys 107: 11193-11200.
34. Fernandez-Escamilla AM, Cheung MS, Vega MC, Wilmanns M, Onuchic JN, et al. (2004) Solvation in protein folding analysis: Combination of theoretical and experimental approaches. Proc Natl Acad Sci U S A 101: 2834-2839.
35. Stoycheva AD, Brooks CL, Onuchic JN (2004) Gatekeepers in the ribosomal protein S6: Thermodynamics, kinetics, and folding pathways revealed by a minimalist protein model. J Mol Biol 340: 571-585.
36. Roy M, Chavez LL, Finke JM, Heidary DK, Onuchic JN, et al. (2005) The native energy landscape for interleukin-1beta. Modulation of the population ensemble through native-state topology. J Mol Biol 348: 335-347.
37. Plaxco KW, Simons KT Baker D (1998). Contact order, transition state placement and the refolding rates of single domain proteins. J Mol Biol 277: 985-994.
38. Ivankov DN Garbuzynskiy SO, Alm E, Plaxco KW, Baker D, et al. (2003). Contact order revisited: Influence of protein size on the folding rate. Protein Sci 12,: 2057-2062.
39. Shoemaker BA, Wang J, Wolynes PG (1997) Structural correlations in protein folding funnels. Proc Natl Acad Sci U S A 94: 777-782.
40. Shoemaker BA, Wang J, Wolynes PG (1999) Exploring structures in protein folding funnels with free energy functionals: The transition state ensemble. J Mol Biol 287: 675-694.
41. Ejtehadi MR, Avall SP, Plotkin SS (2004) Three-body interactions improve the prediction of rate and mechanism in protein folding models. Proc Natl Acad Sci U S A 101: 15088-15093.
42. Sugita Y, Okamoto Y (1999) Replica-exchange molecular dynamics method for protein folding. Chem Phys Lett 314: 141-151.
43. Sugita Y, Okamoto Y (2000) Replica-exchange multicanonical algorithm and multicanonical replica-exchange method for simulating systems with rough energy landscape. Chem Phys Lett 329: 261-270.
44. Mitsutake A, Sugita Y, Okamoto Y (2003) Replica-exchange multicanonical algorithm and multicanonical replica-exchange Monte Carlo simulations of peptides. I. Formulation and benchmark test. J Chem Phys 118: 6664-6675.
45. Mitsutake A, Sugita Y, Okamoto Y (2003) Replica-exchange multicanonical algorithm and multicanonical replica-exchange Monte Carlo simulations of peptides. II. Application to a more complex system. J Chem Phys 118: 6676-6688.
46. Kumar S, Rosenberg JM, Bouzida D, Swendsen RH, Kollman PA (1992) The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method. J Comput Chem 13: 1011-1021.
47. Mitsutake A, Okamoto Y (2000) Replica-exchange simulated tempering method for simulations of frustrated systems. Chem Phys Lett 332: 131-138.
48. Itzhaki LS, Otzen DE, Fersht AR (1995) The structure of the transition state for folding of chymotrypsin inhibitor 2 analysed by protein engineering methods: Evidence for a nucleation-condensation mechanism for protein folding. J Mol Biol 254: 260-288.
49. Spolar RS, Record MT (1994) Coupling of local folding to site-specific binding of proteins to DNA. Science 263: 777-784.
50. Dyson HJ, Wright PE (2002) Coupling of folding and binding for unstructured proteins. Curr Opin Struct Biol 12: 54-60.