Binding of Two Intrinsically Disordered Peptides to a Multi-Specific Protein: A Combined Monte Carlo and Molecular Dynamics Study

PLoS Computational Biology

Volumn 8, Issue 9, 2012, Pages

  Staneva, Iskra ^a   Huang, Yongqi ^b   Liu, Zhirong ^b   Wallin, Stefan ^a  

^a LUND UNIVERSITY   (Sweden)

^b PEKING UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ASSOCIATION REACTIONS; HYDROPHOBICITY; MONTE CARLO METHODS; PROTEINS;

CELLULAR COMMUNICATION NETWORKS; DYNAMIC STUDIES; FOLDINGS; INTRINSICALLY DISORDERED PROTEINS; MANY-TO-ONE; MONTECARLO METHODS; PROTEIN A; PROTEIN SEQUENCES; PROTEIN TARGETS; SIGNALLING MECHANISMS;

MOLECULAR DYNAMICS;

AMINO ACID; INTRINSICALLY DISORDERED PEPTIDE; PEPTIDE; PROTEIN CAPZ; PROTEIN P53; PROTEIN S100B; PROTEIN TRTK 12; UNCLASSIFIED DRUG;

ALPHA HELIX; AMINO ACID SEQUENCE; ARTICLE; HYDROPHOBICITY; MOLECULAR BIOLOGY; MOLECULAR DYNAMICS; MONTE CARLO METHOD; PHYSICAL CHEMISTRY; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FOLDING; PROTEIN STABILITY; PROTEIN TARGETING; SEQUENCE HOMOLOGY; SIGNAL TRANSDUCTION; STATIC ELECTRICITY;

EID: 84866944317     PISSN: 1553734X     EISSN: 15537358     Source Type: Journal    
DOI: 10.1371/journal.pcbi.1002682     Document Type: Article

References (59)

1. Dunker A, Silman I, Uversky V, Sussman J, (2008) Function and structure of inherently disordered proteins. Curr Opin Struc Biol 18: 756-764.
2. Iakoucheva LM, Brown CJ, Lawson JD, Obradović Z, Dunker AK, (2002) Intrinsic disorder in cell-signaling and cancer-associated proteins. J Mol Biol 323: 573-584.
3. Dunker AK, Garner E, Guilliot S, Romero P, Albrecht K, et al. (1998) Protein disorder and the evolution of molecular recognition: theory, predictions and observations. Pac Symp Biocomput 1998: 473-484.
4. Shoemaker BA, Portman JJ, Wolynes PG, (2000) Speeding molecular recognition by using the folding funnel: the y-casting mechanism. Proc Natl Acad Sci US A 97: 8868-8873.
5. Gunasekaran K, Tsai CJ, Kumar S, Zanuy D, Nussinov R, (2003) Extended disordered proteins: targeting function with less scaffold. Trends Biochem Sci 28: 81-85.
6. Hilser VJ, Thompson EB, (2007) Intrinsic disorder as a mechanism to optimize allosteric coupling in proteins. Proc Natl Acad Sci U S A 104: 8311-8315.
7. Kriwacki RW, Hengst L, Tennant L, Reed SI, Wright PE, (1996) Structural studies of p21Waf1/Cip1/Sdi1 in the free and Cdk2-bound state: conformational disorder mediates binding diversity. Proc Natl Acad Sci U S A 93: 11504-11509.
8. Ekman D, Light S, Björklund ÅK, Elofsson A, (2006) What properties characterize the hub proteins of the protein-protein interaction network of Saccharomyces cerevisiae? Genome Biol 7: R45.
9. Haynes C, Oldfield CJ, Ji F, Klitgord N, Cusick ME, et al. (2006) Intrinsic disorder is a common feature of hub proteins from four eukaryotic interactomes. PLoS Comput Biol 2: e100.
10. Bálint È, Vousden KH, (2001) Activation and activities of the p53 tumour suppressor protein. Brit J Cancer 85: 1813-1823.
11. Avalos JL, Celic I, Muhammad S, Cosgrove MS, Boeke JD, et al. (2002) Structure of a Sir 2 enzyme bound to an acetylated p53 peptide. Mol Cell 10: 523-535.
12. Lowe ED, Tews I, Cheng KY, Brown NR, Gul S, et al. (2002) Specificity determinants of recruitment peptides bound to phospho-CDK2/cyclin A. Biochemistry 41: 15625-15634.
13. Mujtaba S, He Y, Zeng L, Yan S, Plotnikova O, et al. (2004) Structural mechanism of the bromodomain of the coactivator CBP in p53 transcriptional activation. Mol Cell 13: 251-263.
14. Oldfield CJ, Meng J, Yang JY, Yang MQ, Uversky VN, et al. (2008) Flexible nets: disorder and induced fit in the associations of p53 and 14-3-3 with their partners. BMC Genomics 9 Suppl 1: S1.
15. Dempsey B, Shaw G, (2011) Identification of calcium-dependent and calcium-enhanced binding between S100B and the dopamine D2 receptor. Biochemistry 50: 9056-9065.
16. Rustandi RR, Baldisseri DM, Weber DJ, (2000) Structure of the negative regulatory domain of p53 bound to S100B(β β). Nature Struct Biol 7: 570-574.
17. Barber KR, McClintock KA, Jamieson GA Jr, Dimlich RVW, Shaw GS, (1999) Specificity and Zn2+ enhancement of the S100B binding epitope TRTK-12. J Biol Chem 274: 1502-1508.
18. McClintock K, Shaw G, (2003) A novel target conformation is revealed by the solution structure of the Ca2+-S100B-TRTK-12 complex. J Biol Chem 278: 6251-6257.
19. Inman K, Yang R, Rustandi R, Miller K, Baldisseri D, et al. (2002) Solution NMR structure of S100B bound to the high-affinity target peptide TRTK-12. J Mol Biol 324: 1003-1014.
20. Charpentier T, Thompson L, Liriano M, Varney KM, Wilder P, et al. (2010) The effects of CapZ peptide (TRTK-12) binding to S100B-Ca2+ as examined by NMR and X-ray crystallography. J Mol Biol 396: 1227-1243.
21. Chen J, (2009) Intrinsically disordered p53 extreme C-terminus binds to S100B(β β) through "fly-casting". J Am Chem Soc 131: 2088-2089.
22. Allen W, Capelluto D, Finkelstein C, Bevan D, (2010) Modeling the relationship between the p53 C-terminal domain and its binding partners using molecular dynamics. J Phys Chem 114: 13201-13213.
23. Pirolli D, Alinovi CC, Capoluongo E, Satta MA, Concolino P, et al. (2011) Insight into a novel p53 single point mutation (G389E) by Molecular Dynamics simulations. Int J Mol Sci 12: 128-140.
24. Huang Y, Liu Z, (2011) Anchoring Intrinsically Disordered Proteins to Multiple Targets: Lessons from N-Terminus of the p53 Protein. Int J Mol Sci 12: 1410-1430.
25. Irbäck A, Samuelsson B, Sjunnesson F, Wallin S, (2003) Thermodynamics of alpha- and betastructure formation in proteins. Biophys J 85: 1466-1473.
26. Irbäck A, Mohanty S, (2006) PROFASI: A Monte Carlo simulation package for protein folding and aggregation. J Comput Chem 27: 1548-1555.
27. Irbäck A, Mitternacht S, Mohanty S, (2009) An effective all-atom potential for proteins. PMC Biophys 2: 2.
28. Staneva I, Wallin S, (2009) All-atom Monte Carlo approach to protein-peptide binding. J Mol Biol 393: 1118-1128.
29. Staneva I, Wallin S, (2011) Binding free energy landscape of domain-peptide interactions. PLoS Comput Biol 7: e1002131.
30. Petsalaki E, Stark A, García-Urdiales E, Russell RB, (2009) Accurate prediction of peptide binding sites on protein surfaces. PLoS Comput Biol 5: e1000335.
31. Raveh B, London N, Zimmerman L, Schueler-Furman O, (2011) Rosetta FlexPepDock ab-initio: simultaneous folding, docking and refinement of peptides onto their receptors. PLoS ONE 6: e18934.
32. Dagliyan O, Proctor EA, D'Auria KM, Ding F, Dokholyan NV, (2011) Structural and dynamic determinants of protein-peptide recognition. Structure 19: 1837-1845.
33. Schreiber G, (2002) Kinetic studies of protein-protein interactions. Curr Opin Struct Biol 12: 41-47.
34. Wright PE, Dyson HJ, (2009) Linking folding and binding. Curr Opin Struct Biol 19: 31-38.
35. Sugase K, Dyson HJ, Wright PE, (2007) Mechanism of coupled folding and binding of an intrinsically disordered protein. Nature 447: 1021-1025.
36. Ahmad M, Gu W, Helms V, (2008) Mechanism of fast peptide recognition by SH3 domains. Angew Chem Int Ed Engl 47: 7626-7630.
37. Huang Y, Liu Z, (2009) Kinetic Advantage of Intrinsically Disordered Proteins in Coupled FoldingBinding Process: A Critical Assessment of the "Fly-Casting" Mechanism. J Mol Biol 393: 1143-1159.
38. Huang Y, Liu Z, (2010) Nonnative interactions in coupled folding and binding processes of intrinsically disordered proteins. PLoS ONE 5: e15375.
39. Rustandi RR, Drohat AC, Baldisseri DM, Wilder PT, Weber DJ, (1998) The Ca2+-dependent interaction of S100(β β) with a peptide derived from p53. Biochemistry 37: 1951-1960.
40. Burgi R, Pitera J, van Gunsteren WF, (2001) Assessing the effect of conformational averaging on the measured values of observables. J Biomol NMR 19: 305-320.
41. Zagrovic B, van Gunsteren WF, (2006) Comparing atomistic simulation data with the NMR experiment: how much can NOEs actually tell us? Proteins 63: 210-218.
42. Arendt Y, Bhaumik A, Del Conte R, Luchinat C, Mori M, et al. (2007) Fragment docking to S100 proteins reveals a wide diversity of weak interaction sites. Chem Med Chem 2: 1648-1654.
43. Pawson T, Nash P, (2003) Assembly of cell regulatory systems through protein interaction domains. Science 300: 445-452.
44. Lee HJ, Zheng JJ, (2010) PDZ domains and their binding partners: structure, specificity, and modification. Cell Commun Signal 8: 8.
45. Bhattacharya S, Large E, Heizmann CW, Hemmings B, Chazin WJ, (2003) Structure of the Ca2+/S100B/NDR kinase peptide complex: insights into S100 target specificity and activation of the kinase. Biochemistry 42: 14416-14426.
46. Berendsen H, van der Spoel D, Drunen R, (1995) GROMACS: a message-passing parallel molecular dynamics implementation. Comp Phys Comm 91: 43-56.
47. Hess B, Kutzner C, van der Spoel D, Lindahl E, (2008) GROMACS 4: algorithms for highly efficient, load-balanced, and scalable molecular simulations. J Chem Theory Comput 4: 435-447.
48. Kaminski G, Friesner R, Tirado-Rives J, Jorgensen W, (2001) Evaluation and reparametrization of the OPLS-AA force field for proteins via comparison with accurate quantum chemical calculations on peptides. J Phys Chem B 105: 6474-6487.
49. Berendsen H, Grigera J, Straatsma T, (1987) The missing term in effective pair potentials. J Phys Chem 91: 6269-6271.
50. Darden T, York D, Pedersen L, (1993) Particle mesh Ewald: an N{dot operator}log(N) method for Ewald sums in large systems. J Chem Phys 98: 10089-10092.
51. Hess B, Bekker H, Berendsen H, Fraaije J, (1997) LINCS: a linear constraint solver for molecular simulations. J Comput Chem 18: 1463-1472.
52. Bussi G, Donadio D, Parrinello M, (2007) Canonical sampling through velocity rescaling. J Chem Phys 126: 014101.
53. Parrinello M, Rahman A, (1981) Polymorphic transitions in single crystals: a new molecular dynamics method. J Appl Phys 52: 7182-7190.
54. Lyubartsev A, Martsinovski A, Shevkunov S, Vorontsov-Velyaminov P, (1992) New approach to Monte Carlo calculation of the free energy: Method of expanded ensembles. J Chem Phys 96: 1776-1783.
55. Marinari E, Parisi G, (1992) Simulated tempering: a new Monte Carlo scheme. Europhys Lett 19: 451-458.
56. Frishman D, Argos P, (1995) Knowledge-based protein secondary structure assignment. Proteins 23: 566-579.
57. de Hoon MJ, Imoto S, Nolan J, Miyano S, (2004) Open source clustering software. Bioinformatics 20: 1453-1454.
58. Miller RG, (1974) The jackknife - a review. Biometrika 61: 1-15.
59. Delano WL (2011) The PyMOL Molecular Graphics System, Version 1.4.1. Schrödinger, LLC.