New force field on modeling intrinsically disordered proteins

Chemical Biology and Drug Design

Volumn 84, Issue 3, 2014, Pages 253-269

  Wang, Wei ^a   Ye, Wei ^a   Jiang, Cheng ^a   Luo, Ray ^b   Chen, Hai Feng ^a,c  

^a SHANGHAI JIAO TONG UNIVERSITY   (China)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c SHANGHAI CENTER FOR BIOINFORMATION TECHNOLOGY   (China)

Author keywords

CMAP; ff99IDPs; IDPs force field; MD simulation; dihedrals

Indexed keywords

INTRINSICALLY DISORDERED PROTEIN; PROTEIN P53;

CHEMISTRY; METABOLISM; MOLECULAR DYNAMICS; PROTEIN DATABASE; PROTEIN SECONDARY STRUCTURE; PROTEIN TERTIARY STRUCTURE; THERMODYNAMICS;

DATABASES, PROTEIN; INTRINSICALLY DISORDERED PROTEINS; MOLECULAR DYNAMICS SIMULATION; PROTEIN STRUCTURE, SECONDARY; PROTEIN STRUCTURE, TERTIARY; THERMODYNAMICS; TUMOR SUPPRESSOR PROTEIN P53;

EID: 84905820860     PISSN: 17470277     EISSN: 17470285     Source Type: Journal    
DOI: 10.1111/cbdd.12314     Document Type: Article

References (71)

1. Romero P., Obradovic Z., Li X., Garner E.C., Brown C.J., Dunker A.K., (2001) Sequence complexity of disordered protein. Proteins; 42: 38-48.
2. Dunker A.K., Obradovic Z., Romero P., Garner E.C., Brown C.J., (2000) Intrinsic protein disorder in complete genomes. Genome Inform Ser Workshop Genome Inform; 11: 161-171.
3. Dunker A.K., Brown C.J., Lawson J.D., Iakoucheva L.M., Obradovic Z., (2002) Intrinsic disorder and protein function. Biochemistry; 41: 6573-6582.
4. Jirgensons B., (1966) Classification of proteins according to conformation. Die Makromolekulare Chemie; 91: 74-86.
5. Wright P.E., Dyson H.J., (1999) Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J Mol Biol; 293: 321-331.
6. Dunker A.K., Lawson J.D., Brown C.J., Williams R.M., Romero P., Oh J.S., Oldfield C.J., Campen A.M., Ratliff C.M., Hipps K.W., (2001) Intrinsically disordered protein. J Mol Graph Model; 19: 26-59.
7. Uversky V.N., Oldfield C.J., Dunker A.K., (2008) Intrinsically disordered proteins in human diseases: introducing the D2 concept. Annu Rev Biophys; 37: 215-246.
8. Dunker A.K., Babu M.M., Barbar E., Blackledge M., Bondos S.E., Dosztányi Z., Dyson H.J., Forman-Kay J., Fuxreiter M., Gsponer J., (2013) What's in a name? Why these proteins are intrinsically disordered. Intrinsically Disord Proteins; 1: e24157.
9. Theillet F.-X., Kalmar L., Tompa P., Han K.-H., Selenko P., Dunker A.K., Daughdrill G.W., Uversky V.N., (2013) The alphabet of intrinsic disorder I. Act like a Pro: on the abundance and roles of proline residues in intrinsically disordered proteins. Intrinsically Disordered. Proteins; 1: e24360.
10. Iakoucheva L.M., Brown C.J., Lawson J.D., Obradovic̈ Z., Dunker A.K., (2002) Intrinsic disorder in cell-signaling and cancer-associated proteins. J Mol Biol; 323: 573-584.
11. Tsai C.-J., Ma B., Nussinov R., (2009) Protein-protein interaction networks: how can a hub protein bind so many different partners? Trends Biochem Sci; 34: 594-600.
12. Collavin L., Lunardi A., Del Sal G., (2010) p53-family proteins and their regulators: hubs and spokes in tumor suppression. Cell Death Differ; 17: 901-911.
13. Chouard T., (2011) Structural biology: breaking the protein rules. Nature; 471: 151-153.
14. Uversky V.N., Oldfield C.J., Midic U., Xie H., Xue B., Vucetic S., Iakoucheva L.M., Obradovic Z., Dunker A.K., (2009) Unfoldomics of human diseases: linking protein intrinsic disorder with diseases. BMC Genomics; 10 (Suppl. 1): S7.
15. Wenning G.K., Jellinger K.A., (2005) The role of [alpha]-synuclein and tau in neurodegenerative movement disorders. Curr Opin Neurol; 18: 357-362.
16. Pawar A.P., Dubay K.F., Zurdo J., Chiti F., Vendruscolo M., Dobson C.M., (2005) Prediction of "aggregation-prone" and "aggregation- susceptible" regions in proteins associated with neurodegenerative diseases. J Mol Biol; 350: 379-392.
17. Hampel H., Blennow K., Shaw L.M., Hoessler Y.C., Zetterberg H., Trojanowski J.Q., (2010) Total and phosphorylated tau protein as biological markers of Alzheimer's disease. Exp Gerontol; 45: 30-40.
18. Goedert M., Spillantini M., Jakes R., Rutherford D., Crowther R., (1989) Multiple isoforms of human microtubule-associated protein tau: sequences and localization in neurofibrillary tangles of Alzheimer's disease. Neuron; 3: 519-526.
19. Gamblin T.C., Berry R.W., Binder L.I., (2003) Modeling tau polymerization in vitro: a review and synthesis. Biochemistry; 42: 15009-15017.
20. Cheng Y., LeGall T., Oldfield C.J., Dunker A.K., Uversky V.N., (2006) Abundance of intrinsic disorder in protein associated with cardiovascular disease. Biochemistry; 45: 10448-10460.
21. Riek R., Hornemann S., Wider G., Glockshuber R., Wuthrich K., (1997) NMR characterization of the full-length recombinant murine prion protein, mPrP(23-231). FEBS Lett; 413: 282-288.
22. Klepeis J.L., Lindorff-Larsen K., Dror R.O., Shaw D.E., (2009) Long-timescale molecular dynamics simulations of protein structure and function. Curr Opin Struct Biol; 19: 120-127.
23. Lindorff-Larsen K., Piana S., Palmo K., Maragakis P., Klepeis J.L., Dror R.O., Shaw D.E., (2010) Improved side-chain torsion potentials for the Amber ff99SB protein force field. Proteins; 78: 1950-1958.
24. Ye W., Wang W., Jiang C., Yu Q., Chen H., (2013) Molecular dynamics simulations of amyloid fibrils: an in silico approach. Acta Biochim Biophys Sin (Shanghai); 45: 503-508.
25. Pearlman D.A., Case D.A., Caldwell J.W., Ross W.S., Cheatham T.E. III, DeBolt S., Ferguson D., Seibel G., Kollman P., (1995) AMBER, a package of computer programs for applying molecular mechanics, normal mode analysis, molecular dynamics and free energy calculations to simulate the structural and energetic properties of molecules. Comput Phys Commun; 91: 1-41.
26. Brooks B.R., Bruccoleri R.E., Olafson B.D., Swaminathan S., Karplus M., (1983) CHARMM: A program for macromolecular energy, minimization, and dynamics calculations. J Comput Chem; 4: 187-217.
27. Berendsen H.J., van der Spoel D., van Drunen R., (1995) GROMACS: A message-passing parallel molecular dynamics implementation. Comput Phys Commun; 91: 43-56.
28. Jorgensen W.L., Tirado-Rives J., (1988) The OPLS [optimized potentials for liquid simulations] potential functions for proteins, energy minimizations for crystals of cyclic peptides and crambin. J Am Chem Soc; 110: 1657-1666.
29. Bernstein F.C., Koetzle T.F., Williams G.J., Meyer E.F. Jr, Brice M.D., Rodgers J.R., Kennard O., Shimanouchi T., Tasumi M., (1977) The Protein Data Bank: a computer-based archival file for macromolecular structures. J Mol Biol; 112: 535-542.
30. Allen F.H., Bellard S., Brice M., Cartwright B.A., Doubleday A., Higgs H., Hummelink T., Hummelink-Peters B., Kennard O., Motherwell W., (1979) The Cambridge Crystallographic Data Centre: computer-based search, retrieval, analysis and display of information. Acta Crystall B-Stru; 35: 2331-2339.
31. Wang Z.X., Zhang W., Wu C., Lei H., Cieplak P., Duan Y., (2006) Strike a balance: optimization of backbone torsion parameters of AMBER polarizable force field for simulations of proteins and peptides. J Comput Chem; 27: 781-790.
32. Antila H.S., Salonen E., (2013) Polarizable force fields. In:, Luca M., Emppu S., editors. Biomolecular Simulations. New York, NY: Humana Press; p. 215-241.
33. Halgren T.A., Damm W., (2001) Polarizable force fields. Curr Opin Struct Biol; 11: 236-242.
34. Ponder J.W., Wu C., Ren P., Pande V.S., Chodera J.D., Schnieders M.J., Haque I., Mobley D.L., Lambrecht D.S., DiStasio R.A. Jr, (2010) Current status of the AMOEBA polarizable force field. J Phys Chem B; 114: 2549-2564.
35. Garcia A.E., Sanbonmatsu K.Y., (2002) Alpha-helical stabilization by side chain shielding of backbone hydrogen bonds. Proc Natl Acad Sci U S A; 99: 2782-2787.
36. Sorin E.J., Pande V.S., (2005) Exploring the helix-coil transition via all-atom equilibrium ensemble simulations. Biophys J; 88: 2472-2493.
37. Hornak V., Abel R., Okur A., Strockbine B., Roitberg A., Simmerling C., (2006) Comparison of multiple Amber force fields and development of improved protein backbone parameters. Proteins; 65: 712-725.
38. Mathura V., Braun W., Garner E., Young J., Takayama S., Brown C., Dunker A., (2001) The protein non-folding problem: amino acid determinants of intrinsic order and disorder. 89-100.
39. Midic U., Obradovic Z., (2011) Intrinsic disorder in putative protein sequences. Proteome Sci; 10: S19.
40. MacKerell A.D., Feig M., Brooks C.L., (2004) Improved treatment of the protein backbone in empirical force fields. J Am Chem Soc; 126: 698-699.
41. MacKerell A.D., Feig M., Brooks C.L., (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.
42. Wright P.E., Dyson H.J., (2009) Linking folding and binding. Curr Opin Struct Biol; 19: 31-38.
43. Brown C.J., Johnson A.K., Dunker A.K., Daughdrill G.W., (2011) Evolution and disorder. Curr Opin Struct Biol; 21: 441-446.
44. Longhi S., Receveur-Bréchot V., Karlin D., Johansson K., Darbon H., Bhella D., Yeo R., Finet S., Canard B., (2003) The C-terminal domain of the measles virus nucleoprotein is intrinsically disordered and folds upon binding to the C-terminal moiety of the phosphoprotein. J Biol Chem; 278: 18638-18648.
45. Bourhis J.-M., Johansson K., Receveur-Bréchot V., Oldfield C.J., Dunker K.A., Canard B., Longhi S., (2004) The C-terminal domain of measles virus nucleoprotein belongs to the class of intrinsically disordered proteins that fold upon binding to their physiological partner. Virus Res; 99: 157-167.
46. Bourhis J.M., Receveur-Bréchot V., Oglesbee M., Zhang X., Buccellato M., Darbon H., Canard B., Finet S., Longhi S., (2005) The intrinsically disordered C-terminal domain of the measles virus nucleoprotein interacts with the C-terminal domain of the phosphoprotein via two distinct sites and remains predominantly unfolded. Protein Sci; 14: 1975-1992.
47. Wang Y., Chu X., Longhi S., Roche P., Han W., Wang E., Wang J., (2013) Multiscaled exploration of coupled folding and binding of an intrinsically disordered molecular recognition element in measles virus nucleoprotein. Proc Natl Acad Sci U S A; 110: E3743-E3752.
48. Wells M., Tidow H., Rutherford T.J., Markwick P., Jensen M.R., Mylonas E., Svergun D.I., Blackledge M., Fersht A.R., (2008) Structure of tumor suppressor p53 and its intrinsically disordered N-terminal transactivation domain. Proc Natl Acad Sci U S A; 105: 5762-5767.
49. Chen H.F., Luo R., (2007) Binding induced folding in p53-MDM2 complex. J Am Chem Soc; 129: 2930-2937.
50. Kabsch W., Sander C., (1983) Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features. Biopolymers; 22: 2577-2637.
51. Joosten R.P., te Beek T.A., Krieger E., Hekkelman M.L., Hooft R.W., Schneider R., Sander C., Vriend G., (2011) A series of PDB related databases for everyday needs. Nucleic Acids Res; 39: D411-D419.
52. MacKerell A.D., Bashford D., Bellott M., Dunbrack R., Evanseck J., Field M.J., Fischer S., Gao J., Guo H., Ha S., (1998) All-atom empirical potential for molecular modeling and dynamics studies of proteins. J Phys Chem B; 102: 3586-3616.
53. Case D.A., Cheatham T.E., Darden T., Gohlke H., Luo R., Merz K.M., Onufriev A., Simmerling C., Wang B., Woods R.J., (2005) The Amber biomolecular simulation programs. J Comput Chem; 26: 1668-1688.
54. Case D., Darden T., Cheatham T. III, Simmerling C., Wang J., Duke R., Luo R., Walker R., Zhang W., Merz K., (2012) AMBER 12. San Francisco: University of California.
55. Cornell W.D., Cieplak P., Bayly C.I., Gould I.R., Merz K.M., Ferguson D.M., Spellmeyer D.C., Fox T., Caldwell J.W., Kollman P.A., (1995) A second generation force field for the simulation of proteins, nucleic acids, and organic molecules. J Am Chem Soc; 117: 5179-5197.
56. Wilcox R., (2005) Kolmogorov-Smirnov test. Encyclopedia of Biostatistics.
57. Berger V.W., Zhou Y., (2005) Kolmogorov-Smirnov tests. Encyclopedia of Statistics in Behavioral Science. 2: 1023-1006.
58. Wlodarski T., Zagrovic B., (2009) Conformational selection and induced fit mechanism underlie specificity in noncovalent interactions with ubiquitin. Proc Natl Acad Sci U S A; 106: 19346-19351.
59. Darden T., York D., Pedersen L., (1993) Particle mesh Ewald: an N.log(N) method for Ewald sums in large systems. J Chem Phys; 98: 10089-10092.
60. Goetz A., Salomon-Ferrer R., Poole D., Grand S., Walker R., (2013) Routine microsecond molecular dynamics simulations with AMBER. Part II: particle mesh Ewald. J Chem Theory Comput; 9: 3878-3888.
61. Götz A.W., Williamson M.J., Xu D., Poole D., Le Grand S., Walker R.C., (2012) Routine microsecond molecular dynamics simulations with AMBER on GPUs. 1. Generalized born. J Chem Theory Comput; 8: 1542.
62. Ryckaert J.P., Ciccotti G., Berendsen H.J.C., (1977) Numerical integration of the Cartesian equations of motion of a system with constraints: molecular dynamics of n-alkanes. J Comput Phys; 23: 327-341.
63. Kingston R.L., Hamel D.J., Gay L.S., Dahlquist F.W., Matthews B.W., (2004) Structural basis for the attachment of a paramyxoviral polymerase to its template. Proc Natl Acad Sci U S A; 101: 8301-8306.
64. Kussie P.H., Gorina S., Marechal V., Elenbaas B., Moreau J., Levine A.J., Pavletich N.P., (1996) Structure of the MDM2 oncoprotein bound to the p53 tumor suppressor transactivation domain. Science; 274: 948-953.
65. Feig M., Karanicolas J., Brooks C.L. III, (2004) MMTSB Tool Set: enhanced sampling and multiscale modeling methods for applications in structural biology. J Mol Graph Model; 22: 377-395.
66. Ulrich E.L., Akutsu H., Doreleijers J.F., Harano Y., Ioannidis Y.E., Lin J., Livny M., Mading S., Maziuk D., Miller Z., (2008) BioMagResBank. Nucleic Acids Res; 36: D402-D408.
67. Shen Y., Bax A., (2007) Protein backbone chemical shifts predicted from searching a database for torsion angle and sequence homology. J Biomol NMR; 38: 289-302.
68. Ozenne V., Bauer F., Salmon L., Huang J.-R., Jensen M.R., Segard S., Bernadõ P., Charavay C., Blackledge M.,. (2012) Flexible-meccano: a tool for the generation of explicit ensemble descriptions of intrinsically disordered proteins and their associated experimental observables. Bioinformatics; 28: 1463-1470.
69. Jensen M.R., Communie G., Ribeiro E.A. Jr, Martinez N., Desfosses A., Salmon L., Mollica L., Gabel F., Jamin M., Longhi S., Ruigrok R.W., Blackledge M., (2011) Intrinsic disorder in measles virus nucleocapsids. Proc Natl Acad Sci U S A; 108: 9839-9844.
70. Mao A.H., Crick S.L., Vitalis A., Chicoine C.L., Pappu R.V., (2010) Net charge per residue modulates conformational ensembles of intrinsically disordered proteins. Proc Natl Acad Sci U S A; 107: 8183-8188.
71. Jensen M.R., Communie G., Ribeiro E.A., Martinez N., Desfosses A., Salmon L., Mollica L., Gabel F., Jamin M., Longhi S., (2011) Intrinsic disorder in measles virus nucleocapsids. Proc Natl Acad Sci U S A; 108: 9839-9844.