Protein oligomerization through domain swapping: Role of inter-molecular interactions and protein concentration

Journal of Molecular Biology

Volumn 352, Issue 1, 2005, Pages 202-211

  Yang, Sichun ^a   Levine, Herbert ^a   Onuchic, José N ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Domain swapping; Protein aggregation; Protein concentration; Protein oligomerization; Second virial coefficient

Indexed keywords

PROTEIN;

ARTICLE; MOLECULAR INTERACTION; MOLECULAR MODEL; OLIGOMERIZATION; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN ANALYSIS; PROTEIN ASSEMBLY; PROTEIN DOMAIN; PROTEIN PROCESSING; PROTEIN STRUCTURE; SIMULATION; STRUCTURE ANALYSIS; THERMODYNAMICS;

EID: 23944448528     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.06.062     Document Type: Article

References (67)

1. M. Bennett, S. Choe, and D. Eisenberg Domain swapping: entangling alliances between proteins Proc. Natl Acad. Sci. USA 91 1994 3127 3131
2. R. Jaenicke, and H. Lilie Folding and association of oligomeric and multimeric proteins Advan. Protein Chem. 53 2000 329 362
3. Y. Liu, and D. Eisenberg 3D domain swapping: as domains continue to swap Protein Sci. 11 2002 1285 1299
4. H.A. Lashuel, D. Hartley, B.M. Petre, T. Walz, and P.T. Lansbury Neurodegenerative disease: amyloid pores from pathogenic mutations Nature 418 2002 291
5. C.M. Dobson Protein folding and misfolding Nature 426 2003 884 890
6. D.J. Selkoe Folding proteins in fatal ways Nature 426 2003 900 904
7. R. Dima, and D. Thirumalai Exploring protein aggregation and self-propagation using lattice models: phase diagram and kinetics Protein Sci. 11 2002 1036 1049
8. S. Yang, S.S. Cho, Y. Levy, M.S. Cheung, H. Levine, P.G. Wolynes, and J.N. Onuchic Domain swapping is a consequence of minimal frustration Proc. Natl Acad. Sci. USA 101 2004 13786 13791
9. Yang, S.; Levine, H. Onuchic, J. N. & Cox, D. L. (2005) Structure of infectious prions: stabilization by domain swapping. FASEB J. In the press.
10. F. Ding, N.V. Dokholyan, S.V. Buldyrev, H.E. Stanley, and E.I. Shakhnovich Molecular dynamics simulation of the SH3 domain aggregation suggests a generic amyloidogenesis mechanism J. Mol. Biol. 324 2002 851 857
11. M. Nilsson, X. Wang, S. Rodziewicz-Motowidlo, R. Janowski, V. Lindstrom, and P. Onnerfjord Prevention of domain swapping inhibits dimerization and amyloid fibril formation of Cystatin C J. Biol. Chem. 279 2004 24236 24245
12. K.J. Knaus, M. Morillas, W. Swietnicki, M. Malone, W.K. Surewicz, and V.C. Yee Crystal structure of the human prion protein reveals a mechanism for oligomerization Nature Struct. Biol. 8 2001 770 774
13. S. Lee, and D. Eisenberg Seeded conversion of recombinant prion protein to a disulfide-bonded oligomer by a reduction-oxidation process Nature Struct. Biol. 10 2003 725 730
14. K.V. Kishan, G. Scita, W. Wong, P. Di Fiore, and M. Newcomer The SH3 domain of Eps8 exists as a novel intertwined dimer Nature Struct. Biol. 4 1997 739 743
15. K.V. Kishan, M.E. Newcomer, T.H. Rhodes, and S.D. Guilliot Effect of pH and salt bridges on structural assembly: molecular structures of the monomer and intertwined dimer of the Eps8 SH3 domain Protein Sci. 10 2001 1046 1055
16. N. Khazanovich, K. Bateman, M. Chernaia, M. Michalak, and M. James Crystal structure of the yeast cell-cycle control protein, p13suc1, in a strand-exchanged dimer Structure 4 1996 299 309
17. J. Schymkowitz, F. Rousseau, L. Irvine, and L.L. Itzhaki The folding pathway of the cell-cycle regulatory protein p13suc1: clues for the mechanism of domain swapping Structure 8 2000 89 100
18. F. Rousseau, J.W.H. Schymkowitz, H.R. Wilkinson, and L.S. Itzhaki Three-dimensional domain swapping in p13suc1 occurs in the unfolded state and is controlled by conserved proline residues Proc. Natl Acad. Sci. USA 98 2001 5596 5601
19. F. Rousseau, J.W.H. Schymkowitz, H.R. Wilkinson, and L.S. Itzhaki Intermediates control domain swapping during folding of p13suc1 J. Biol. Chem. 279 2004 8368 8377
20. R.A. Staniforth, J.L.E. Dean, Q. Zhong, E. Zerovnik, A.R. Clarke, and J.P. Waltho The major transition state in folding need not involve the immobilization of side chains Proc. Natl Acad. Sci. USA 97 2000 5790 5795
21. R.A. Staniforth, S. Giannini, L.D. Higgins, M.J. Conroy, A.M. Hounslow, and R. Jerala Three-dimensional domain swapping in the folded and molten-globule states of cystatins, an amyloid-forming structural superfamily EMBO J. 20 2001 4774 4781
22. R. Janowski, M. Kozak, E. Jankowska, Z. Grzonka, A. Grubb, M. Abrahamson, and M. Jaskolski Human cystatin, an amyloidogenic protein, dimerizes through three-dimensional domain swapping Nature Struct. Biol. 8 2001 316 320
23. A. Sanders, C. Jeremy Craven, L.D. Higgins, S. Giannini, M.J. Conroy, and A.M. Hounslow Cystatin forms a tetramer through structural rearrangement of domain-swapped dimers prior to amyloidogenesis J. Mol. Biol. 336 2004 165 178
24. R. Janowski, M. Abrahamson, A. Grubb, and M. Jaskolski Domain swapping intruncated human cystatin J. Mol. Biol. 341 2004 151 160
25. A. Zdanov, C. Schalk-Hihi, A. Gustchina, M. Tsang, J. Weatherbee, and A. Wlodawer Crystal structure of interleukin-10 reveals the functional dimer with an unexpected topological similarity to interferon γ Structure 3 1995 591 601
26. N.J. Marianayagam, M. Sunde, and J.M. Matthews The power of two: protein dimerization in biology Trends Biochem. Sci. 29 2004 618 625
27. M.E. Newcomer Protein folding and three-dimensional domain swapping: a strained relationship? Curr. Opin. Struct. Biol. 12 2002 48 53
28. A.P. Minton Implications of macromolecular crowding for protein assembly Curr. Opin. Struct. Biol. 10 2000 34 39
29. R.J. Ellis Macromolecular crowding: an important but neglected aspect of the intracellular environment Curr. Opin. Struct. Biol. 11 2001 114 119
30. A. George, and W. Wilson Predicting protein crystallization from a dilute solution property Acta Crystallog. sect. D 50 1994 361 365
31. A.P. Minton Molecular crowding: analysis of effects of high concentrations of inert cosolutes on biochemical equilibria and rates in terms of volume exclusion Methods Enzymol. 295 1998 127 149
32. J. Bloustine, V. Berejnov, and S. Fraden Measurements of protein-protein interactions by size exclusion chromatography Biophys. J. 85 2003 2619 2623
33. S. Xu, and B. Lin The mechanism of oxidation-induced low-density lipoprotein aggregation: an analogy to colloidal aggregation and beyond? Biophys. J. 81 2001 2403 2413
34. S. Xu, B. Bevis, and M.F. Arnsdorf The assembly of amyloidogenic yeast sup35 as assessed by scanning (atomic) force microscopy: an analogy to linear colloidal aggregation? Biophys. J. 81 2001 446 454
35. V.N. Uversky, and A.L. Fink Conformational constraints for amyloid fibrillation: the importance of being unfolded Biochim. Biophys. Acta 1698 2004 131 153
36. E.Y. Chi, S. Krishnan, B.S. Kendrick, B.S. Chang, J.F. Carpenter, and T.W. Randolph Roles of conformational stability and colloidal stability in the aggregation of recombinant human granulocyte colony-stimulating factor Protein Sci. 12 2003 903 913
37. J.G.S. Ho, A.P.J. Middelberg, P. Ramage, and H.P. Kocher The likelihood of aggregation during protein renaturation can be assessed using the second virial coefficient Protein Sci. 12 2003 708 716
38. L.M. Gloss, B. Robert Simler, and C. Robert Matthews Rough energy landscapes in protein folding: dimeric E. coli Trp repressor folds through three parallel channels J. Mol. Biol. 312 2001 1121 1134
39. J.D. Bryngelson, and P.G. Wolynes Spin glasses and the statistical mechanics of protein folding Proc. Natl Acad. Sci. USA 84 1987 7524 7528
40. P.E. Leopold, M. Montal, and J.N. Onuchic Protein folding funnels: kinetic pathways through compact conformational space Proc. Natl Acad. Sci. USA 89 1992 8721 8725
41. J.D. Bryngelson, J.N. Onuchic, N.D. Socci, and P.G. Wolynes Funnels, pathways and the energy landscape of protein folding Proteins: Struct. Funct. Genet. 21 1995 167 195
42. J.N. Onuchic, and P.G. Wolynes Theory of protein folding Curr. Opin. Struct. Biol. 14 2004 70 75
43. K.A. Dill, and H.S. Chan From levinthal to pathways to funnels: the new view of protein folding kinetics Nature Struct. Biol. 4 1997 10 19
44. V. Munoz, P.A. Thompson, J. Hofrichter, and W.A. Eaton Folding dynamics and mechanism of beta-hairpin formation Nature 390 1997 196 199
45. H. Nymeyer, A.E. García, and J.N. Onuchic Folding funnels and frustration in off-lattice minimalist models Proc. Natl Acad. Sci. USA 95 1998 5921 5928
46. C. Clementi, H. Nymeyer, and J.N. Onuchic Topological and energetic factors: what determines the structural details of the transition state ensemble and "on route" intermediates for protein folding? An investigation for small globular proteins J. Mol. Biol. 298 2000 937 953
47. S.S. Plotkin, and J.N. Onuchic Understanding protein folding with energy landscape theory. Part I: basic concepts Quart. Rev. Biophys. 35 2002 111 167
48. Y. Sugita, and Y. Okamoto Replica-exchange molecular dynamics method for protein folding Chem. Phys. Letters 314 1999 141 151
49. K. Sanbonmatsu, and A.E. García Structure of met-enkephalin in explicit aqueous solution using replica exchange molecular dynamics Proteins: Struct. Funct. Genet. 46 2002 225 234
50. A.E. Garcia, and J.N. Onuchic Folding a protein in a computer: an atomic description of the folding/unfolding of protein A Proc. Natl Acad. Sci. USA 100 2003 13898 13903
51. A. Mitsutake, Y. Sugita, and Y. Okamoto Generalized-ensemble algorithms for molecular simulations of biopolymers Biopolymers 60 2001 96 123
52. A.M. Ferrenberg, and R.H. Swendsen New Monte Carlo technique for studying phase transitions Phys. Rev. Letters 61 1988 2635 2638
53. S. Kumar, D. Bouzida, R.H. Swendsen, P.A. Kollman, and J.M. Rosenberg The weighted histogram analysis method for free-energy calculations on biomolecules. I. The method J. Comput. Chem. 13 1992 1011 1021
54. Z. Guo, and C.L. Brooks Thermodynamics of protein folding: a statistical mechanical study of a small all β protein Biopolymers 42 1997 745 757
55. J.E. Shea, and C.L. Brooks From folding surfaces to folding proteins: a review and assessment of simulation studies of protein folding and unfolding Annu. Rev. Phys. Chem. 52 2001 499 535
56. J. Zurdo, J.I. Guijarro, J.L. Jimenez, H.R. Saibil, and C.M. Dobson Dependence on solution conditions of aggregation and amyloid formation by an SH3 domain J. Mol. Biol. 311 2001 325 340
57. J.T. Jarrett, and P.T. Lansbury Jr Amyloid fibril formation requires a chemically discriminating nucleation event: studies of an amyloidogenic sequence from the bacterial protein osmb Biochemistry 31 1992 12345 12352
58. J.D. Harper, J. Lansbury, and P.T. Models of amyloid seeding in alzheimer's disease and scrapie: mechanistic truths and physiological consequences of the time-dependent solubility of amyloid proteins Annu. Rev. Biochem. 66 1997 385 407
59. A. Lomakin, D.S. Chung, G.B. Benedek, D.A. Kirschner, and D.B. Teplow On the nucleation and growth of amyloid β-protein fibrils: detection of nuclei and quantitation of rate constants Proc. Natl Acad. Sci. USA 93 1996 1125 1129
60. A. Lomakin, D.B. Teplow, D.A. Kirschner, and G.B. Benedek Kinetic theory of fibrillogenesis of amyloid β-protein Proc. Natl Acad. Sci. USA 94 1997 7942 7947
61. I. Zegers, J. Deswarte, and L. Wyns Trimeric domain-swapped barnase Proc. Natl Acad. Sci. USA 96 1999 818 822
62. Y. Liu, G. Gotte, M. Libonati, and D. Eisenberg Structures of the two 3D domain-swapped RNase A trimers Protein Sci. 11 2002 371 380
63. R. Zahn, A. Liu, T. Luhrs, R. Riek, C. von Schroetter, and F. Lopez Garcia NMR solution structure of the human prion protein Proc. Natl Acad. Sci. USA 97 2000 145 150
64. M.P. Schlunegger, M.J. Bennett, and D. Eisenberg Oligomer formation by 3D domain swapping: a model for protein assembly and misassembly Advan. Protein Chem. 50 1997 61 122
65. F.E. Cohen Pathologic conformations of prion proteins Annu. Rev. Biochem. 67 1998 793 819
66. Y. Liu, G. Gotte, M. Libonati, and D. Eisenberg A domain-swapped RNase A dimmer with implications for amyloid formation Nature Struct. Biol. 8 2001 211 214
67. N. Sinha, C.-J. Tsai, and R. Nussinov A proposed structural model for amyloid fibril elongation: domain swapping forms an interdigitating beta-structure polymer Protein Eng. 14 2001 93 103