Molecular dynamics simulations of N-terminal peptides from a nucleotide binding protein

Proteins: Structure, Function and Genetics

Volumn 24, Issue 4, 1996, Pages 450-466

  Van Der Spoel, David ^a   Vogel, Hans J ^b   Berendsen, Herman J C ^a  

^a UNIVERSITY OF GRONINGEN   (Netherlands)

^b UNIVERSITY OF CALGARY   (Canada)

Author keywords

cotranslational folding; lactate dehydrogenase; Rossmann fold

Indexed keywords

LACTATE DEHYDROGENASE; NUCLEOTIDE BINDING PROTEIN;

AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; CRYSTAL STRUCTURE; HYDROPHOBICITY; MOLECULAR DYNAMICS; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN SECONDARY STRUCTURE; PROTEIN STABILITY; PROTEIN TERTIARY STRUCTURE;

AMINO ACID SEQUENCE; L-LACTATE DEHYDROGENASE; MODELS, MOLECULAR; MOLECULAR SEQUENCE DATA; PEPTIDES; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; SALTS; SOLVENTS;

EID: 0029990294     PISSN: 08873585     EISSN: None     Source Type: Journal    
DOI: 10.1002/(SICI)1097-0134(199604)24:4<450::AID-PROT5>3.0.CO;2-I     Document Type: Article

References (84)

1. Jaenicke, R. What does protein refolding in vitro tell us about protein folding in the cell? Philos. Trans. R. Soc. Lond. 339:287-295, 1993.
2. Anfinsen, C.B. Principles that govern the folding of protein chains. Science 181:223-230, 1973.
3. Ohgushi, M., Wada, A. 'Molten-globule state': A compact form of globular proteins with mobile side-chains. FEES Lett. 164:21-24, 1983.
4. Kuwajima, K. The molten globule state as a clue for understanding the folding and cooperativity of globular-protein structure. Proteins 6:87-103, 1989.
5. Ptitsyn, O.E., Pain, R.H., Semisotnov, G.V., Zerovnik, E., Razgulyaev, O.I. Evidence for a molten globule state as a general intermediate in protein folding. FEBS Lett. 262: 20-24, 1990.
6. Kim, P.S., Baldwin, R.L. Intermediates in the folding reactions of small proteins. Annu. Rev. Biochem. 60:631-660, 1990.
7. Roder, H., Elöve, G. A., Englander, S.W. Structural characterization of folding intermediates in cytochrome c by H-exchange labeling and proton NMR. Nature 335:700-704, 1988.
8. Udgaonkar, J.B., Baldwin, R.L. NMR evidence for an early framework intermediate on the folding pathway of ribonuclease A. Nature 335:694-699, 1988.
9. Englander, S.W., Mayne, L. Protein folding studied using hydrogen-exchange labeling and two-dimensional NMR. Annu. Rev. Biophys. 21:243-265, 1992.
10. Sosnick, T.R., Mayne, L., Hiller, R., Englander, S.W. The barriers in protein folding. Nature Struct. Biol. 1:149-156, 1994.
11. Creighton, T.E. The energetic ups and downs of protein folding. Nature Struct. Biol. 1:135-138, 1994.
12. Wright, P.E., Dyson, H.J., Lerner, R.A. Conformation of peptide fragments of proteins in aqueous solution: Implications for initiation of protein folding. Biochemistry 27: 7167-7175, 1988.
13. Dyson, H.J., Wright, P.E. Peptide conformation and protein folding. Curr. Opin. Struct. Biol. 3:60-65, 1993.
14. Shin, H.-C., Merutka, G., Waltho, J.P., Tennant, L.L., Dyson, H.J., Wright, P.E. Peptide models of protein folding initiation sites. 3. The G-H helical hairpin of myoglobin. Biochemistry 32:6356-6364, 1993.
15. Schulz, G.E., Schirmer, R.H. "Principles of Protein Structure." New York: Springer Verlag, 1978.
16. Tsou, C.-L. Folding of the nascent peptide chain into a biologically active protein. Biochemistry 27:1807-1812, 1988.
17. Fedorov, A.N., Friguet, B., Djavadi-Ohaniance, L., Alakhov, Y.B., Goldberg, M.E. Folding on the ribosome of Escherichia coli tryptophan synthase βsubunit nascent chains probed with a conformation-dependent monoclonal antibody. J. Mol. Biol. 228:351-358, 1992.
18. Fedorov, A.N., Baldwin, T.O. Contribution of cotranslational folding to the rate of formation of native protein structure. Proc. Natl. Acad. Sci. USA 92:1227-1231, 1995.
19. Hata-Tamake, A., Kawai, G., Yamasaki, K., Ito, Y., Kajiura, H., Ha, J.-M., Miyazawa, T., Yokoyama, S., Nishimura, S. Spin-labeling proton NMR study on aromatic amino acid residues in the guanine nucleotide binding site of human c-Ha-ras(1-171) protein. Biochemistry 28:9550-9556, 1989.
20. Minara, P., Hall, L., Betton, J.-M., Missiakis, D., Yon, J.M. Efficient expression and characterization of isolated structural domains of yeast phosphateglycerate kinase generated by site-directed mutagenesis. Protein Eng. 3:55-60, 1989.
21. Eder, J., Kirschner, K. Stable substructures of eightfold βα-barrel proteins: Fragment complementation of phosphoribosylanthranilate isomerase. Biochemistry 31:3617-3635, 1992.
22. Jecht, M., Tomschy, A., Kirschner, K., Jaenicke, R. Autonomous folding of the excised coenzyme-binding domain of an D-glyceraldehyde 3-phosphate dehydrogenase from Thermotoga maritima. Protein Sci. 3:411-418, 1994.
23. Schulz, G.E. Binding of nucleotides by proteins. Curr. Opin. Struct. Biol. 2:61-67, 1992.
24. Baker, P.J., Britton, K.L., Rice, D.W., Stillman, A.R.T.J. Structural consequences of sequence patterns in the fingerprint region of the nucleotide binding fold. J. Mol. Biol. 228:662-671, 1992.
25. Saraste, M., Sibbald, P.R., Wittinghofer, A. The P-loop - a common motif in ATP and GTP binding proteins. Trends Biochem. Sci. 15:430-434, 1990.
26. Bossemeyer, D. The glycine-rich sequence of protein kinases: A multifunctional element. Trends Biochem. Sci. 19:201-205, 1994.
27. Wierenga, R.K., Terpstra, P., Hol, W.G.J. Prediction of the occurence of the ADP-binding βαβ-fold in proteins, using an amino acid sequence fingerprint. J. Mol. Biol. 187:101-107, 1986.
28. Krasheninnikov, I.A., Komar, A.A., Adzhubei, I.A. Frequencies of utilization of codons in mRNA and coding of the domain structure of proteins. Dokl. Akad. Nauk. SSSR 305:1006-1012, 1989.
29. Opitz, U., Rudolph, R., Jaenicke, R., Ericsson, L., Neurath, H. Proteolytic dimers of porcine muscle lactate dehydrogenase: Characterisation, folding, and reconstitution of the truncated and nicked polypeptide chain. Biochemistry 26: 1399-1406, 1987.
30. Rossmann, M.G., Moras, D., Olsen, K.W. Chemical and biological evolution of a nucleotide-binding protein. Nature 250:194-199, 1974.
31. Daggett, V., Levitt, M. Realistic simulations of native-protein dynamics. Annu. Rev. Biophys. Biomol. Struct. 22: 353-380, 1993.
32. Caflisch, A., Karplus, M. Molecular dynamics studies of protein and peptide folding and unfolding. In: "The Protein Folding Problem and Tertiary Structure Prediction." Merz Jr., K.M., Le Grand, S.M. (eds.). Boston: Birkhäuser, 1994: 193-230.
33. Mark, A.E., van Gunsteren, W.F. Simulation of the thermal denaturation of hen egg white lysozym: Trapping the molten globule state. Biochemistry 31:7745-7748, 1992.
34. Daggett, V., Levitt, M. A model of the molten globule state from molecular dynamics simulations. Proc. Natl. Acad. Sci. USA 89:5142-5146, 1992.
35. Brooks III, C.L. Molecular simulations of peptide and protein unfolding: In quest of a molten globule. Curr. Opin. Struct. Biol. 3:92-98, 1993.
36. Tirado-Rives, J., Jorgensen, W.L. Molecular dynamics simulations of the unfolding of apomyoglobin in water. Biochemistry 33:4175-4184, 1993.
37. DiCapua, F.M., Swaminathan, S., Beveridge, D.L. Theoretical evidence for destabilization of an α helix by water insertion: Molecular dynamics of hydrated decaalanine. J. Am. Chem. Soc. 112:6768-6771, 1990.
38. Tirado-Rives, J., Jorgensen, W.L. Molecular dynamics simulations of the unfolding of an α-helical analogue of ribonuclease A S-peptide in water. Biochemistry 30:3864-3871, 1991.
39. deLoof, H., Nilsson, L., Rigler, R. Molecular dynamics simulations of galanin in aqueous and nonaqueous solution. J. Am. Chem. Soc. 114:4028-4035, 1992.
40. van Buuren, A.R., Berendsen, H.J.C. Molecular dynamics simulation of the stability of a 22 residue alpha-helix in water and 30% trifluoroethanol. Biopolymers 33:1159-1166, 1993.
41. Hermans, J. Molecular dynamics simulations of helix and turn propensities in model peptides. Curr. Opin. Struct. Biol. 3:270-276, 1993.
42. Mierke, D.F., Kessler, H. Improved molecular dynamics simulations for the determination of peptide structures. Biopolymers 33:1003-1017, 1993.
43. Soman, K.V., Karimi, A., Case, D.A. Molecular dynamics analysis of a ribonuclease c-peptide analogue. Biopolymers 33:1567-1580, 1993.
44. Kazmirski, S.L., Alonso, D.O.V., Cohen, F.E., Prusiner, S.B., Daggett, V. Theoretical studies of sequence effects on the conformational properties of a fragment of the prion protein: Implications for scrapie formation. Curr. Biol. 2:305-315, 1995.
45. Hirst, J.D., Brooks III, C.L. Molecular dynamics simulations of isolated helices of myoglobin. Biochemistry 34: 7614-7621, 1995.
46. Kovacs, H., Mark, A.E., Johansson, J., van Gunsteren, W.F. The effect of environment on the stability of an integral membrane helix: Molecular dynamics simulations of surfactant protein c in chloroform, methanol and water. J. Mol. Biol. 247:808-822, 1995.
47. Braxenthaler, M., Avbelj, F., Moult, J. Structure, dynamics and energetics of initiation sites in protein folding: I. Analysis of a 1 ns molecular dynamics trajectory of an early folding unit in water: The helix I/loop I-fragment of barnase. J. Mol. Biol. 250:239-257, 1995.
48. Pugliese, L., Prévost, M , Wodak, S.J. Unfolding simulations of the 85-102 β-hairpin of barnase. J. Mol. Biol. 251: 432-447, 1995.
49. Hinds, D.A., Levitt, M. Simulation of protein-folding pathways: Lost in (conformational) space. Trends Biotech. 13: 23-27, 1995.
50. Abad-Zapatero, C., Griffith, J.P., Sussman, J.L., Rossmann, M.G. Refined crystal structure of M4 dogfish apo-lactate dehydrogenase. J. Mol. Biol. 198:445-467, 1987.
51. Berendsen, H.J.C., Postma, J.P.M., van Gunsteren, W.F., Hermans, J. Interaction models for water in relation to protein hydration. In: "Intermolecular Forces." Dordrecht: D. Reidel Publishing Company, 1981:331-342.
52. Allen, M.P., Tildesley, D.J. "Computer Simulations of Liquids." Oxford: Oxford Science Publications, 1987.
53. Smith, P.E., Pettitt, B.M. Peptides in ionic solutions: A comparison of the Ewald and switching function techniques. J. Chem. Phys. 95:8430-8441, 1991.
54. Hockney, R. W., Eastwood, J.W. "Computer Simulation Using Particles." New York: McGraw-Hill, 1981.
55. Luty, B.A., Davies, M.E., Tironi, I.G., van Gunsteren, W.F. A comparison of particle-particle, particle-mesh and Ewald methods for calculating electrostatic interactions in periodic molecular systems. Mol. Sim. 14:11-20, 1994.
56. Tironi, I.G., Sperb, R., Smith, P.E., van Gunsteren, W.F. A generalized reaction field method for molecular dynamics simulations. J Chem. Phys. 102:5451-5459, 1995.
57. Berendsen, H.J.C. Electrostatic interactions. In: "Computer Simulation of Biomolecular Systems." van Gunsteren, W.F., Wilkinson, P.K.W. (eds.) Leiden: ESCOM, 1993:161-181.
58. Luty, B.A., van Gunsteren, W.F. Calculating electrostatic interactions using the particle-particle, particle-mesh method with non-periodic long-range interactions. Submitted.
59. Berendsen, H J.C., Postma, J.P.M., DiNola, A., Haak, J.R. Molecular dynamics with coupling to an external bath. J. Chem. Phys. 81:8, 1984.
60. van Gunsteren, W.F., Berendsen, H.J.C. "Gromos-87 Manual." Biomos BV Nijenborgh 4, 9747 AG Groningen, The Netherlands 1987.
61. van Buuren, A.R., Marrink, S.J., Berendsen, H.J.C. A molecular dynamics study of the decane/water interface. J. Phys. Chem 97:9206-9212, 1993.
62. Ryckaert, J.P., Ciccotti, G., Berendsen, H.J.C. Numerical integration of the cartesian equations of motion of a system with constraints; molecular dynamics of n-alkanes. J. Comp. Phys. 23:327-341, 1977.
63. van der Spoel, D., Berendsen, H.J.C., van Buuren, A.R., Apol, E., Meulenhoff, P.J., Sijbers, A.L.T.M., van Drunen, R. "Gromacs User Manual." Nijenborgh 4, 9747 AG Groningen, The Netherlands. Internet: http://rugmd0.chem. rug.nl/∼gmx 1995.
64. Bekker, H., Berendsen, H.J.C., Dijkstra, E.J., Achterop, S., van Drunen, R., van der Spoel, D., Sijbers, A., Keegstra, H., Reitsma, B., Renardus, M.K.R. Gromacs: A parallel computer for molecular dynamics simulations. In: "Physics Computing 92." de Groot, R.A., Nadrchal, J. (eds.). Singapore: World Scientific, 1993.
65. Berendsen, H.J.C., van der Spoel, D., van Drunen, R. Gromacs: A message-passing parallel molecular dynamics implementation. Comp. Phys. Commun. 91:43-56, 1995.
66. Kabsch, W., Sander, C. Dictionary of protein secondary structure: Pattern recognition of hydrogen-bonded and geometrical features. Biopolymers 22:2577-2637, 1983.
67. Das, B., Chattopadhyay, S., Gupta, C.D. Reactivation of denatured fungal glucose 6-phosphate dehydrogenase and E. coli alkaline phosphatase with E. coli ribosome. Biochem. Biophys. Res. Commun. 183:774-780, 1992.
68. Bera, A.K., Das, B., Chattapahyay, S., Dasgupta, C. Refolding of denatured restriction endonucleases with ribosomal preparations from Methanoscarcina barkeri. Biochem. Biophys. Res. Commun. 32:315-323, 1994.
69. Girg, R., Jaenicke, R., Rudolph, R. Dimers of porcine skeletal muscle lactate dehydrogenase produced by limited proteolysis during reassociation are enzymatically active in the presence of stabilizing salt. Bioch. Int. 7:433-441, 1983.
70. Dill, K.A., Fiebig, K.M., Chan, H.S. Cooperativity in protein-folding kinetics. Proc. Natl. Acad. Sci. USA 90:1942-1946, 1993.
71. Tobias, D.J., Mertz, J.E., Brooks III, C.L. Nanosecond timescale folding dynamics of a pentapeptide in water. Biochemistry 30:6054-6058, 1991.
72. Blanco, F.J., Jimenez, M.A., Herranz, J., Rico, M., Santoro, J., Nieto, J.L. NMR evidence of a short linear peptide that folds into a β-hairpin in aqueous solution. J. Am. Chem. Soc. 115:5887-5888, 1993.
73. 1 domain: evidence of trifluoroethanol induced native-like β-hairpin formation. Biochemistry 33:6004-6014, 1994.
74. Wierenga, R.K., de Maeyer, M.C.H., Hol., W.G.J. Interaction of phosphate moieties with α-helices in dinucleotide binding proteins. Biochemistry 24:1346-1357, 1985.
75. Stroup, A.N., Gierasch, L.M. Reduced tendency to form a β turn in peptides from the p22 tailspike protein correlates with a temperature-sensitive folding defect. Biochemistry 29:9765-9771, 1990.
76. Fry, D.C., Kuby, S.A., Mildvan, A.S. NMR studies of the MgATP binding site of adenylate kinase and of a 45-residue peptide fragment of the enzyme. Biochemistry 24: 4630-4694, 1985.
77. Fry, D.C., Byler, D.M., Susi, H., Brown, E.M., Kuby, S.A., Mildvan, A.S. Solution structure of the 45-residue MgATP-binding peptide of adenylate kinase as examined by 2D-NMR. FTIR, and CD spectroscopy. Biochemistry 27: 3588-3598, 1988.
78. Tobias, D.J., Sneddon, S.F., Brooks III, C.L. Stability of a model β-sheet in water. J. Mol. Biol. 227:1244-1252, 1992.
79. Dobson, C.M., Evans, P A., Radford, S.E. Understanding how proteins fold: The lysozyme story so far. Trends Biochem. Sci. 19:31-37, 1994.
80. Tweedy, N.B., Hurle, M.R., Chrunyk, B.A., Matthews, C.R. Multiple replacements at position 211 in the α subunit of tryptophan synthase as a probe of the folding unit association reaction. Biochemistry 29:1539-1545, 1990.
81. Schafmeister, C.E., Miercke, L.J.W., Stroud, R.M. Structure at 2.5 Å of a designed peptide that maintains solubility of membrane proteins. Science 262:734-738, 1993.
82. Monera, O.D., Kay, C.M., Hodges, R.S. Electrostatic interactions control the parallel and antiparallel orientation of α-helical chains in two stranded α-helical coiled coils. Biochemistry 33:3862-3871, 1994.
83. Alexandrov, N. Structural arguments for N-terminal initiation of protein folding. Protein Sci. 2:1989-1991, 1993.
84. Kraulis, P.J. MOLSCRIPT: A program to produce both detailed and schematic plots of protein structures. J. Appl. Crystallogr. 24:946-950, 1991.