Analysis of ordered and disordered protein complexes reveals structural features discriminating between stable and unstable monomers

Journal of Molecular Biology

Volumn 341, Issue 5, 2004, Pages 1327-1341

  Gunasekaran, Kannan ^a   Tsai, Chung Jung ^a   Nussinov, Ruth ^a,b  

^a SAIC FREDERICK INC   (United States)

^b TEL AVIV UNIVERSITY   (Israel)

Author keywords

disordered proteins; folding mechanisms; natively unstructured proteins; protein protein interactions; two state and three state complexes

Indexed keywords

MONOMER; PROTEIN DERIVATIVE; PROTEIN SUBUNIT; RIBOSOME PROTEIN;

ARTICLE; COMPLEX FORMATION; CRYSTAL STRUCTURE; HYDROPHOBICITY; MOLECULAR DYNAMICS; PHYSICAL CHEMISTRY; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FOLDING; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; PROTEIN STABILITY; PROTEIN STRUCTURE; PROTEOMICS; STRUCTURE ANALYSIS;

EID: 4143107222     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2004.07.002     Document Type: Article

References (71)

1. I.M.A. Nooren, and J.M. Thornton Diversity of protein-protein interactions EMBO J. 22 2003 3486 3492
2. S.J. Wodak, and J. Janin Structural basis of macromolecular recognition Advan. Protein Chem. 61 2002 9 73
3. A.V. Veselovsky, Y.D. Ivanov, A.S. Ivanov, A.I. Archakov, P. Lewi, and P. Janssen Protein-protein interactions: mechanisms and modification by drugs J. Mol. Recogn. 15 2002 405 422
4. A. Valencia, and F. Pazos Computational methods for the prediction of protein interactions Curr. Opin. Struct. Biol. 12 2002 368 373
5. Y. Levy, P.G. Wolynes, and J.N. Onuchic Protein topology determines binding mechanism Proc. Natl Acad. Sci. USA 101 2004 511 516
6. C. Chothia, and J. Janin Principles of protein-protein recognition Nature 256 1975 705 708
7. D. Xu, C.J. Tsai, and R. Nussinov Mechanism and evolution of protein dimerization Protein Sci. 7 1998 533 544
8. S. Jones, and J.M. Thornton Principles of protein-protein interactions Proc. Natl Acad. Sci. USA 93 1996 13 20
9. G. Tiana, and R.A. Broglia Design and folding of dimeric proteins Proteins: Struct. Funct. Genet. 49 2002 82 94
10. S. Dasgupta, G.H. Iyer, S.H. Bryant, C.E. Lawrence, and J.A. Bell Extent and nature of contacts between protein molecules in crystal lattices and between subunits of protein oligomers Proteins: Struct. Funct. Genet. 28 1997 494 514
11. H. Ponstingl, K. Henrick, and J.M. Thornton Discriminating between homodimeric and monomeric proteins in the crystalline state Proteins: Struct. Funct. Genet. 41 2000 47 57
12. R.P. Bahadur, P. Chakrabarti, F. Rodier, and J. Janin Dissecting subunit interfaces in homodimeric proteins Proteins: Struct. Funct. Genet. 53 2003 708 719
13. J. Janin Specific versus non-specific contacts in protein crystals Nature Struct. Biol. 4 1997 973 974
14. I.M.A. Nooren, and J.M. Thornton Structural characterisation and functional significance of transient protein-protein interactions J. Mol. Biol. 325 2003 991 1018
15. J. Janin, and F. Rodier Protein-protein interaction at crystal contacts Proteins: Struct. Funct. Genet. 23 1995 580 587
16. A.K. Dunker, C.J. Brown, J.D. Lawson, L.M. Iakoucheva, and Z. Obradovic Intrinsic disorder and protein function Biochemistry 41 2002 6573 6582
17. P.E. Wright, and H.J. Dyson Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm J. Mol. Biol. 293 1999 321 331
18. V.N. Uversky Natively unfolded proteins: a point where biology waits for physics Protein Sci. 11 2002 739 756
19. P. Tompa Intrinsically unstructured proteins Trends Biochem. Sci. 27 2002 527 533
20. K. Gunasekaran, C.J. Tsai, S. Kumar, D. Zanuy, and R. Nussinov Extended disordered proteins: targeting function with less scaffold Trends Biochem. Sci. 28 2003 81 85
21. C.J. Tsai, B.Y. Ma, Y.Y. Sham, S. Kumar, and R. Nussinov Structured disorder and conformational selection Proteins: Struct. Funct. Genet. 44 2001 418 427
22. A.S. Morar, A. Olteanu, G.B. Young, and G.J. Pielak Solvent-induced collapse of alpha-synuclein and acid-denatured cytochrome c Protein Sci. 10 2001 2195 2199
23. V.N. Uversky, J.R. Gillespie, and A.L. Fink Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins: Struct. Funct. Genet. 41 2000 415 427
24. P. Romero, Z. Obradovic, X. Li, E.C. Garner, C.J. Brown, and A.K. Dunker Sequence complexity of disordered protein Proteins: Struct. Funct. Genet. 42 2001 38 48
25. B.A. Shoemaker, J.J. Portman, and P.G. Wolynes Speeding molecular recognition by using the folding funnel: the fly-casting mechanism Proc. Natl Acad. Sci. USA 97 2000 8868 8873
26. G.M. Verkhivker, D. Bouzida, D.K. Gehlhaar, P.A. Rejto, S.T. Freer, and P.W. Rose Simulating disorder-order transitions in molecular recognition of unstructured proteins: where folding meets binding Proc. Natl Acad. Sci. USA 100 2003 5148 5153
27. C.M. Teschke, and J. King Folding and assembly of oligomeric proteins in Escherichia coli Curr. Opin. Biotechnol. 3 1992 468 473
28. P.B. Moore The three-dimensional structure of the ribosome and its components Annu. Rev. Biophys. Biomol. Struct. 27 1998 35 58
29. D.E. Draper, and L.P. Reynaldo RNA binding strategies of ribosomal proteins Nucl. Acids. Res. 27 1999 381 388
30. F.C. Bernstein, T.F. Koetzle, G.J. Williams, E.F. Meyer Jr, M.D. Brice, and J.R. Rodgers The Protein Data Bank: a computer-based archival file for macromolecular structures J. Mol. Biol. 112 1977 535 542
31. S. Miller, J. Janin, A.M. Lesk, and C. Chothia Interior and surface of monomeric proteins J. Mol. Biol. 196 1987 641 656
32. L.N. Serdyuk, O.V. Galzitskaya, and A.A. Timchenko Roughness of the globular protein surface Biofizika 42 1997 1197 1207
33. J.S. Richardson, D.C. Richardson, N.B. Tweedy, K.M. Gernert, T.P. Quinn, and M.H. Hecht Looking at proteins: representations, folding, packing, and design. Biophysical Society National Lecture, 1992 Biophys. J. 63 1992 1185 1209
34. W.F. DeGrado, C.M. Summa, V. Pavone, F. Nastri, and A. Lombardi De novo design and structural characterization of proteins and metalloproteins Annu. Rev. Biochem. 68 1999 779 819
35. S. Jones, D.T.A. Daley, N.M. Luscombe, H.M. Berman, and J.M. Thornton Protein-RNA interactions: a structural analysis Nucl. Acids Res. 29 2001 943 954
36. C.J. Tsai, S.L. Lin, H.J. Wolfson, and R. Nussinov Studies of protein-protein interfaces: a statistical analysis of the hydrophobic effect Protein Sci. 6 1997 53 64
37. O. Carugo, and P. Argos Protein-protein crystal-packing contacts Protein Sci. 6 1997 2261 2263
38. L. Lo Conte, C. Chothia, and J. Janin The atomic structure of protein-protein recognition sites J. Mol. Biol. 285 1999 2177 2198
39. A. Berchanski, B. Shapira, and M. Eisenstein Hydrophobic complementarity in protein-protein docking Proteins: Struct. Funct. Genet. 56 2004 130 142
40. J. Janin, S. Miller, and C. Chothia Surface, subunit interfaces and interior of oligomeric proteins J. Mol. Biol. 204 1988 155 164
41. I.B. Kuznetsov, and S. Rackovsky On the properties and sequence context of structurally ambivalent fragments in proteins Protein. Sci. 12 2003 2420 2433
42. K.A. Dill, and H.S. Chan From Levinthal to pathways to funnels Nature Struct. Biol. 4 1997 10 19
43. A. Shrake, and J.A. Rupley Environment and exposure to solvent of protein atoms. Lysozyme and insulin J. Mol. Biol. 79 1973 351 371
44. C.J. Tsai, and R. Nussinov Hydrophobic folding units derived from dissimilar monomer structures and their interactions Protein Sci. 6 1997 24 42
45. P.J. Kraulis MOLSCRIPT - a program to produce both detailed and schematic plots of protein structures J. Appl. Crystallog. 24 1991 946 950
46. D. Bacon, and W.F. Anderson A fast algorithm for rendering space-filling molecule pictures J. Mol. Graph. 6 1988 219 220
47. R. Dawson, L. Muller, A. Dehner, C. Klein, H. Kessler, and J. Buchner The N-terminal domain of p53 is natively unfolded J. Mol. Biol. 332 2003 1131 1141
48. 13C alpha NMR chemical shifts and local unfolding curves Biophys. J. 73 1997 1031 1041
49. D.E. Timm, P.L. de Haseth, and K.E. Neet Comparative equilibrium denaturation studies of the neurotrophins: nerve growth factor, brain-derived neurotrophic factor, neurotrophin 3, and neurotrophin 4/5 Biochemistry 33 1994 4667 4676
50. C.J. Mann, C.A. Royer, and C.R. Matthews Tryptophan replacements in the trp aporepressor from Escherichia coli: probing the equilibrium and kinetic folding models Protein Sci. 2 1993 1853 1861
51. R.R. Singh, and A.G. Appu Rao Reductive unfolding and oxidative refolding of a Bowman-Birk inhibitor from horsegram seeds (Dolichos biflorus): evidence for "hyperreactive" disulfide bonds and rate-limiting nature of disulfide isomerization in folding Biochim. Biophys. Acta. 1597 2002 280 291
52. C. Steif, P. Weber, H.J. Hinz, J. Flossdorf, G. Cesareni, and M. Kokkinidis Subunit interactions provide a significant contribution to the stability of the dimeric four-alpha-helical-bundle protein ROP Biochemistry 32 1993 3867 3876
53. M.E. Milla, and R.T. Sauer P22 Arc repressor: folding kinetics of a single-domain, dimeric protein Biochemistry 33 1994 1125 1133
54. V. Karantza, A.D. Baxevanis, E. Freire, and E.N. Moudrianakis Thermodynamic studies of the core histones: ionic strength and pH dependence of H2A-H2B dimer stability Biochemistry 34 1995 5988 5996
55. C.M. Johnson, A. Cooper, and P.G. Stockley Differential scanning calorimetry of thermal unfolding of the methionine repressor protein (MetJ) from Escherichia coli Biochemistry 31 1992 9717 9724
56. K. Bachhawat, M. Kapoor, T.K. Dam, and A. Surolia The reversible two-state unfolding of a monocot mannose-binding lectin from garlic bulbs reveals the dominant role of the dimeric interface in its stabilization Biochemistry 40 2001 7291 7300
57. M. Horiuchi, Y. Kurihara, M. Katahira, T. Maeda, T. Saito, S. Uesugi, and N.A. Dimerization binding facilitate alpha-helix formation of Max in solution J. Biochem. (Tokyo) 122 1997 711 716
58. G. Ferrieres, C. Calzolari, J.C. Mani, D. Laune, S. Trinquier, and M. Laprade Human cardiac troponin I: precise identification of antigenic epitopes and prediction of secondary structure Clin. Chem. 44 1998 487 493
59. L.M. Rice, P. Brennwald, and A.T. Brunger Formation of a yeast SNARE complex is accompanied by significant structural changes FEBS Letters 415 1997 49 55
60. B. Agianian, K. Leonard, E. Bonte, H. Van der Zandt, P.B. Becker, and P.A. Tucker The glutamine-rich domain of the Drosophila GAGA factor is necessary for amyloid fibre formation in vitro, but not for chromatin remodelling J. Mol. Biol. 285 1999 527 544
61. S.L. Flaugh, and K.J. Lumb Effects of macromolecular crowding on the intrinsically disordered proteins c-Fos and p27(Kip1) Biomacromolecules 2 2001 538 540
62. S. Venyaminov, A.T. Gudkov, Z.V. Gogia, and L.G. Tumanova Absorbtion and Circular Dichroism Spectra of Individual Proteins from Escherichia coli Ribosomes 1981 Biological Research Center, Institute of Protein Research Pushchino, AS USSR
63. T.V. Borchert, J.P. Zeelen, W. Schliebs, M. Callens, W. Minke, R. Jaenicke, and R.K. Wierenga An interface point-mutation variant of triosephosphate isomerase is compactly folded and monomeric at low protein concentrations FEBS Letters 367 1995 315 318
64. A. Aceto, A.M. Caccuri, P. Sacchetta, T. Bucciarelli, B. Dragani, and N. Rosato Dissociation and unfolding of Pi-class glutathione transferase. Evidence for a monomeric inactive intermediate Biochem. J. 285 1992 241 245
65. M. Herold, and K. Kirschner Reversible dissociation and unfolding of aspartate aminotransferase from Escherichia coli: characterization of a monomeric intermediate Biochemistry 29 1990 1907 1913
66. C.R. Zetina, and M.E. Goldberg Reversible unfolding of the beta 2 subunit of Escherichia coli tryptophan synthetase and its proteolytic fragments J. Mol. Biol. 137 1980 401 414
67. S.E. Jackson How do small single-domain proteins fold? Fold. Des. 3 1998 R81 R91
68. S.M. Doyle, E.H. Braswell, and C.M. Teschke SecA folds via a dimeric intermediate Biochemistry 39 2000 11667 11676
69. G. Mei, A. Di Venere, M. Buganza, P. Vecchini, N. Rosato, and A. Finazzi-Agro Role of quaternary structure in the stability of dimeric proteins: the case of ascorbate oxidase Biochemistry 36 1997 10917 10922
70. G.B. Reddy, S. Bharadwaj, and A. Surolia Thermal stability and mode of oligomerization of the tetrameric peanut agglutinin: a differential scanning calorimetry study Biochemistry 38 1999 4464 4470
71. B.W. Noland, L.J. Dangott, and T.O. Baldwin Folding, stability, and physical properties of the alpha subunit of bacterial luciferase Biochemistry 38 1999 16136 16145