Topological Frustration in βα-Repeat Proteins: Sequence Diversity Modulates the Conserved Folding Mechanisms of α/β/α Sandwich Proteins

Journal of Molecular Biology

Volumn 398, Issue 2, 2010, Pages 332-350

  Hills, Ronald D ^a   Kathuria, Sagar V ^b   Wallace, Louise A ^b   Day, Iain J ^b   Brooks, Charles L ^a,c   Matthews, C Robert ^b  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UNIVERSITY OF MASSACHUSETTS MEDICAL SCHOOL   (United States)

^c UNIVERSITY OF MICHIGAN   (United States)

Author keywords

Coarse grained molecular dynamics; Global analysis; Protein folding landscape; Response regulators; Topological frustration

Indexed keywords

CHEY PROTEIN; ISOLEUCINE; LEUCINE; NITROGEN REGULATORY PROTEIN C; REGULATOR PROTEIN; UNCLASSIFIED DRUG; VALINE;

ALPHA HELIX; AMINO ACID SEQUENCE; AMINO TERMINAL SEQUENCE; ARTICLE; BETA SHEET; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN CONFORMATION; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN LOCALIZATION; PROTEIN MOTIF; SIMULATION;

ISLA VISTA VIRUS;

EID: 77951711256     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.03.001     Document Type: Article

References (83)

1. Anfinsen C.B., Scheraga H.A. Experimental and theoretical aspects of protein folding. Adv. Protein Chem. 1975, 29:205-300.
2. Onuchic J.N., Wolynes P.G. Theory of protein folding. Curr. Opin. Struct. Biol. 2004, 14:70-75.
3. Plaxco K.W., Simons K.T., Baker D. Contact order, transition state placement and the refolding rates of single domain proteins. J. Mol. Biol. 1998, 277:985-994.
4. Ivankov D.N., Garbuzynskiy S.O., Alm E., Plaxco K.W., Baker D., Finkelstein A.V. Contact order revisited: influence of protein size on the folding rate. Protein Sci. 2003, 12:2057-2062.
5. Kamagata K., Kuwajima K. Surprisingly high correlation between early and late stages in non-two-state protein folding. J. Mol. Biol. 2006, 357:1647-1654.
6. Jackson S.E. How do small single-domain proteins fold?. Folding Des. 1998, 3:R81-91.
7. Scott K.A., Batey S., Hooton K.A., Clarke J. The folding of spectrin domains I: wild-type domains have the same stability but very different kinetic properties. J. Mol. Biol. 2004, 344:195-205.
8. Wensley B.G., Gartner M., Choo W.X., Batey S., Clarke J. Different members of a simple three-helix bundle protein family have very different folding rate constants and fold by different mechanisms. J. Mol. Biol. 2009, 390:1074-1085.
9. Friel C.T., Capaldi A.P., Radford S.E. Structural analysis of the rate-limiting transition states in the folding of Im7 and Im9: similarities and differences in the folding of homologous proteins. J. Mol. Biol. 2003, 326:293-305.
10. Volz K., Matsumura P. Crystal structure of Escherichia coli CheY refined at 1.7-Å resolution. J. Biol. Chem. 1991, 266:15511-15519.
11. Kern D., Volkman B.F., Luginbuhl P., Nohaile M.J., Kustu S., Wemmer D.E. Structure of a transiently phosphorylated switch in bacterial signal transduction. Nature 1999, 402:894-898.
12. Madhusudan M., Zapf J., Whiteley J.M., Hoch J.A., Xuong N.H., Varughese K.I. Crystal structure of a phosphatase-resistant mutant of sporulation response regulator Spo0F from Bacillus subtilis. Structure 1996, 4:679-690.
13. Lopez-Hernandez E., Serrano L. Structure of the transition state for folding of the 129 aa protein CheY resembles that of a smaller protein, CI-2. Folding Des. 1996, 1:43-55.
14. Larkin M.A., Blackshields G., Brown N.P., Chenna R., McGettigan P.A., McWilliam H., et al. Clustal W and Clustal X version 2.0. Bioinformatics 2007, 23:2947-2948.
15. Wallace L.A., Robert Matthews C. Highly divergent dihydrofolate reductases conserve complex folding mechanisms. J. Mol. Biol. 2002, 315:193-211.
16. Forsyth W.R., Matthews C.R. Folding mechanism of indole-3-glycerol phosphate synthase from Sulfolobus solfataricus: a test of the conservation of folding mechanisms hypothesis in (beta(alpha))(8) barrels. J. Mol. Biol. 2002, 320:1119-1133.
17. Forsyth W.R., Bilsel O., Gu Z., Matthews C.R. Topology and sequence in the folding of a TIM barrel protein: global analysis highlights partitioning between transient off-pathway and stable on-pathway folding intermediates in the complex folding mechanism of a (betaalpha)8 barrel of unknown function from B. subtilis. J. Mol. Biol. 2007, 372:236-253.
18. Bollen Y.J.M., van Mierlo C.P.M. Protein topology affects the appearance of intermediates during the folding of proteins with a flavodoxin-like fold. Biophys. Chem. 2005, 114:181-189.
19. Kathuria S.V., Day I.J., Wallace L.A., Matthews C.R. Kinetic traps in the folding of beta/alpha-repeat proteins: CheY initially misfolds before accessing the native conformation. J. Mol. Biol. 2008, 382:467-484.
20. Hills R.D., Brooks C.L. Subdomain competition, cooperativity, and topological frustration in the folding of CheY. J. Mol. Biol. 2008, 382:485-495.
21. Clementi C., Nymeyer H., Onuchic J.N. Topological and energetic factors: what determines the structural details of the transition state ensemble and "en-route" intermediates for protein folding? An investigation for small globular proteins. J. Mol. Biol. 2000, 298:937-953.
22. Formaneck M.S., Ma L., Cui Q. Reconciling the "old" and "new" views of protein allostery: a molecular simulation study of chemotaxis Y protein (CheY). Proteins 2006, 63:846-867.
23. Lee S.Y., Cho H.S., Pelton J.G., Yan D.L., Henderson R.K., King D.S., et al. Crystal structure of an activated response regulator bound to its target. Nat. Struct. Biol. 2001, 8:52-56.
24. Stock A.M., Guhaniyogi J. A new perspective on response regulator activation. J. Bacteriol. 2006, 188:7328-7330.
25. Nelson E.D., Grishin N.V. Alternate pathways for folding in the flavodoxin fold family revealed by a nucleation-growth model. J. Mol. Biol. 2006, 358:646-653.
26. Sola M., Lopez-Hernandez E., Cronet P., Lacroix E., Serrano L., Coll M., Parraga A. Towards understanding a molecular switch mechanism: thermodynamic and crystallographic studies of the signal transduction protein CheY. J. Mol. Biol. 2000, 303:213-225.
27. Zhu X.Y., Rebello J., Matsumura P., Volz K. Crystal structures of CheY mutants Y106W and T871/Y106W-CheY activation correlates with movement of residue 106. J. Biol. Chem. 1997, 272:5000-5006.
28. De Carlo S., Chen B.Y., Hoover T.R., Kondrashkina E., Nogales E., Nixon B.T. The structural basis for regulated assembly and function of the transcriptional activator NtrC. Genes Dev. 2006, 20:1485-1495.
29. Hu X.H., Wang Y.M. Molecular dynamic simulations of the N-terminal receiver domain of NtrC reveal intrinsic conformational flexibility in the inactive state. J. Biomol. Struct. Dyn. 2006, 23:509-517.
30. Volkman B.F., Lipson D., Wemmer D.E., Kern D. Two-state allosteric behavior in a single-domain signaling protein. Science 2001, 291:2429-2433.
31. Fraser J.S., Clarkson M.W., Degnan S.C., Erion R., Kern D., Alber T. Hidden alternative structures of proline isomerase essential for catalysis. Nature 2009, 462:669-673.
32. Dyer C.M., Dahlquist F.W. Switched or not?: the structure of unphosphorylated CheY bound to the N terminus of FliM. J. Bacteriol. 2006, 188:7354-7363.
33. Simonovic M., Volz K. A distinct meta-active conformation in the 1.1-angstrom resolution structure of wild-type apoCheY. J. Biol. Chem. 2001, 276:28637-28640.
34. Gardino A.K., Volkman B.F., Cho H.S., Lee S.Y., Wemmer D.E., Kern D. The NMR solution structure of BeF3-activated Spo0F reveals the conformational switch in a phosphorelay system. J. Mol. Biol. 2003, 331:245-254.
35. Madhusudan M., Zapf J., Hoch J.A., Whiteley J.M., Xuong N.H., Varughese K.I. A response regulatory protein with the site of phosphorylation blocked by an arginine interaction: crystal structure of Spo0F from Bacillus subtilis. Biochemistry 1997, 36:12739-12745.
36. Varughese K.I., Tsigelny I., Zhao H.Y. The crystal structure of beryllofluoride Spo0F in complex with the phosphotransferase Spo0B represents a phosphotransfer pretransition state. J. Bacteriol. 2006, 188:4970-4977.
37. Wu Y., Vadrevu R., Kathuria S., Yang X., Matthews C.R. A tightly packed hydrophobic cluster directs the formation of an off-pathway sub-millisecond folding intermediate in the alpha subunit of tryptophan synthase, a TIM barrel protein. J. Mol. Biol. 2007, 366:1624-1638.
38. Munoz V., Lopez E.M., Jager M., Serrano L. Kinetic characterization of the chemotactic protein from Escherichia coli, CheY. Kinetic analysis of the inverse hydrophobic effect. Biochemistry 1994, 33:5858-5866.
39. Otzen D.E., Oliveberg M. Salt-induced detour through compact regions of the protein folding landscape. Proc. Natl Acad. Sci. USA 1999, 96:11746-11751.
40. Fernandez-Recio J., Genzor C.G., Sancho J. Apoflavodoxin folding mechanism: an alpha/beta protein with an essentially off-pathway intermediate. Biochemistry 2001, 40:15234-15245.
41. Du R., Pande V.S., Grosberg A.Y., Tanaka T., Shakhnovich E.S. On the transition coordinate for protein folding. J. Chem. Phys. 1998, 108:334-350.
42. Snow C.D., Rhee Y.M., Pande V.S. Kinetic definition of protein folding transition state ensembles and reaction coordinates. Biophys. J. 2006, 91:14-24.
43. Juraszek J., Bolhuis P.G. Rate constant and reaction coordinate of Trp-cage folding in explicit water. Biophys. J. 2008, 95:4246-4257.
44. Cho S.S., Levy Y., Wolynes P.G. P versus Q: structural reaction coordinates capture protein folding on smooth landscapes. Proc. Natl Acad. Sci. USA 2006, 103:586-591.
45. Karanicolas J., Brooks C.L. Improved Go-like models demonstrate the robustness of protein folding mechanisms towards non-native interactions. J. Mol. Biol. 2003, 334:309-325.
46. Rey-Stolle M.F., Enciso M., Rey A. Topology-based models and NMR structures in protein folding simulations. J. Comput. Chem. 2009, 30:1212-1219.
47. Prieto L., Rey A. Simulations of the protein folding process using topology-based models depend on the experimental structure. J. Chem. Phys. 2008, 129:115101.
48. Chavez L.L., Gosavi S., Jennings P.A., Onuchic J.N. Multiple routes lead to the native state in the energy landscape of the beta-trefoil family. Proc. Natl Acad. Sci. USA 2006, 103:10254-10258.
49. Gosavi S., Chavez L.L., Jennings P.A., Onuchic J.N. Topological frustration and the folding of interleukin-1 beta. J. Mol. Biol. 2006, 357:986-996.
50. Gosavi S., Whitford P.C., Jennings P.A., Onuchic J.N. Extracting function from a beta-trefoil folding motif. Proc. Natl Acad. Sci. USA 2008, 105:10384-10389.
51. Finke J.M., Onuchic J.N. Equilibrium and kinetic folding pathways of a TIM barrel with a funneled energy landscape. Biophys. J. 2005, 89:488-505.
52. Gu Z., Rao M.K., Forsyth W.R., Finke J.M., Matthews C.R. Structural analysis of kinetic folding intermediates for a TIM barrel protein, indole-3-glycerol phosphate synthase, by hydrogen exchange mass spectrometry and Go model simulation. J. Mol. Biol. 2007, 374:528-546.
53. Jakob R.P., Schmid F.X. Energetic coupling between native-state prolyl isomerization and conformational protein folding. J. Mol. Biol. 2008, 377:1560-1575.
54. Jakob R.P., Schmid F.X. Molecular determinants of a native-state prolyl isomerization. J. Mol. Biol. 2009, 387:1017-1031.
55. Fowler S.B., Clarke J. Mapping the folding pathway of an immunoglobulin domain: structural detail from Phi value analysis and movement of the transition state. Structure 2001, 9:355-366.
56. Gu Z., Zitzewitz J.A., Matthews C.R. Mapping the structure of folding cores in TIM barrel proteins by hydrogen exchange mass spectrometry: the roles of motif and sequence for the indole-3-glycerol phosphate synthase from Sulfolobus solfataricus. J. Mol. Biol. 2007, 368:582-594.
57. Bollen Y.J.M., Kamphuis M.B., van Mierlo C.P.M. The folding energy landscape of apoflavodoxin is rugged: hydrogen exchange reveals nonproductive misfolded intermediates. Proc. Natl Acad. Sci. USA 2006, 103:4095-4100.
58. Radzicka A., Wolfenden R. Comparing the polarities of the amino acids: side-chain distribution coefficients between the vapor phase, cyclohexane, 1-octanol, and neutral aqueous solution. Biochemistry 1988, 27:1664-1670.
59. Schell D., Tsai J., Scholtz J.M., Pace C.N. Hydrogen bonding increases packing density in the protein interior. Proteins 2006, 63:278-282.
60. Olofsson M., Hansson S., Hedberg L., Logan D.T., Oliveberg M. Folding of S6 structures with divergent amino acid composition: pathway flexibility within partly overlapping foldons. J. Mol. Biol. 2007, 365:237-248.
61. Lappalainen I., Hurley M.G., Clarke J. Plasticity within the obligatory folding nucleus of an immunoglobulin-like domain. J. Mol. Biol. 2008, 375:547-559.
62. Lam A.R., Borreguero J.M., Ding F., Dokholyan N.V., Buldyrev S.V., Stanley H.E., Shakhnovich E. Parallel folding pathways in the SH3 domain protein. J. Mol. Biol. 2007, 373:1348-1360.
63. Kister A.E., Finkelstein A.V., Gelfand I.M. Common features in structures and sequences of sandwich-like proteins. Proc. Natl Acad. Sci. USA 2002, 99:14137-14141.
64. Wilson C.J., Wittung-Stafshede P. Snapshots of a dynamic folding nucleus in zinc-substituted Pseudomonas aeruginosa azurin. Biochemistry 2005, 44:10054-10062.
65. Mirny L., Shakhnovich E. Evolutionary conservation of the folding nucleus. J. Mol. Biol. 2001, 308:123-129.
66. Nagano N., Orengo C.A., Thornton J.M. One fold with many functions: the evolutionary relationships between TIM barrel families based on their sequences, structures and functions. J. Mol. Biol. 2002, 321:741-765.
67. Nohaile M., Kern D., Wemmer D., Stedman K., Kustu S. Structural and functional analyses of activating amino acid substitutions in the receiver domain of NtrC: evidence for an activating surface. J. Mol. Biol. 1997, 273:299-316.
68. Zapf J.W., Hoch J.A., Whiteley J.M. A phosphotransferase activity of the Bacillus subtilis sporulation protein Spo0F that employs phosphoramidate substrates. Biochemistry 1996, 35:2926-2933.
69. John A.S. Solvent denaturation. Biopolymers 1978, 17:1305-1322.
70. Pace C.N. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 1986, 131:266-280.
71. Ionescu R.M., Smith V.F., O'Neill J.C., Matthews C.R. Multistate equilibrium unfolding of Escherichia coli dihydrofolate reductase: thermodynamic and spectroscopic description of the native, intermediate, and unfolded ensembles. Biochemistry 2000, 39:9540-9550.
72. Gualfetti P.J., Bilsel O., Matthews C.R. The progressive development of structure and stability during the equilibrium folding of the alpha subunit of tryptophan synthase from Escherichia coli. Protein Sci. 1999, 8:1623-1635.
73. Matthews C.R. Effect of point mutations on the folding of globular proteins. Methods Enzymol. 1987, 154:498-511.
74. Marquardt D.W. An algorithm for least-squares estimation of nonlinear parameters. J. Soc. Ind. Appl. Math. 1963, 11:431-441.
75. Bilsel O., Zitzewitz J.A., Bowers K.E., Matthews C.R. Folding mechanism of the alpha-subunit of tryptophan synthase, an alpha/beta barrel protein: global analysis highlights the interconversion of multiple native, intermediate, and unfolded forms through parallel channels. Biochemistry 1999, 38:1018-1029.
76. Sobolev V., Sorokine A., Prilusky J., Abola E.E., Edelman M. Automated analysis of interatomic contacts in proteins. Bioinformatics 1999, 15:327-332.
77. Karanicolas J., Brooks C.L. The origins of asymmetry in the folding transition states of protein L and protein G. Protein Sci. 2002, 11:2351-2361.
78. Miyazawa S., Jernigan R.L. Residue-residue potentials with a favorable contact pair term and an unfavorable high packing density term, for simulation and threading. J. Mol. Biol. 1996, 256:623-644.
79. Brooks B.R., Bruccoleri R.E., Olafson B.D., States D.J., Swaminathan S., Karplus M. CHARMM-a program for macromolecular energy, minimization, and dynamics calculations. J. Comput. Chem. 1983, 4:187-217.
80. Feig M., Karanicolas J., Brooks C.L. MMTSB Tool Set: enhanced sampling and multiscale modeling methods for applications in structural biology. J. Mol. Graphics 2004, 22:377-395.
81. Sugita Y., Okamoto Y. Replica-exchange molecular dynamics method for protein folding. Chem. Phys. Lett. 1999, 314:141-151.
82. Kumar S., Bouzida D., Swendsen R.H., Kollman P.A., Rosenberg J.M. The weighted histogram analysis method for free-energy calculations on biomolecules. 1. The method. J. Comput. Chem. 1992, 13:1011-1021.
83. Gallicchio E., Andrec M., Felts A.K., Levy R.M. Temperature weighted histogram analysis method, replica exchange, and transition paths. J. Phys. Chem. B 2005, 109:6722-6731.