Thermodynamics, Kinetics, and Salt dependence of Folding of YopM, a Large Leucine-rich Repeat Protein

Journal of Molecular Biology

Volumn 383, Issue 5, 2008, Pages 1195-1209

  Kloss, Ellen ^a   Barrick, Doug ^a  

^a JOHNS HOPKINS UNIVERSITY   (United States)

Author keywords

cooperative folding; electrostatics; folding kinetics; leucine rich repeat; repeat protein

Indexed keywords

LEUCINE RICH REPEAT KINASE 2; SODIUM CHLORIDE;

ARTICLE; ENERGY; KINETICS; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FOLDING; PROTEIN STRUCTURE; THERMODYNAMICS;

EID: 53649096641     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2008.08.069     Document Type: Article

References (72)

1. Kloss E., Courtemanche N., and Barrick D. Repeat-protein folding: new insights into origins of cooperativity, stability, and topology. Arch. Biochem. Biophys. 469 (2008) 83-99
2. Main E.R., Lowe A.R., Mochrie S.G., Jackson S.E., and Regan L. A recurring theme in protein engineering: the design, stability and folding of repeat proteins. Curr. Opin. Struct. Biol. 15 (2005) 464-471
3. Freiberg A., Machner M.P., Pfeil W., Schubert W.D., Heinz D.W., and Seckler R. Folding and stability of the leucine-rich repeat domain of internalin B from Listeri monocytogenes. J. Mol. Biol. 337 (2004) 453-461
4. Courtemanche N., and Barrick D. Folding thermodynamics and kinetics of the leucine-rich repeat domain of the virulence factor Internalin B. Protein Sci. 17 (2008) 43-53
5. Tevelev A., Byeon I.J., Selby T., Ericson K., Kim H.J., Kraynov V., and Tsai M.D. Tumor suppressor p16INK4A: structural characterization of wild-type and mutant proteins by NMR and circular dichroism. Biochemistry 35 (1996) 9475-9487
6. Boice J.A., and Fairman R. Structural characterization of the tumor suppressor p16, an ankyrin-like repeat protein. Protein Sci. 5 (1996) 1776-1784
7. Zhang B., and Peng Z. Defective folding of mutant p16(INK4) proteins encoded by tumor-derived alleles. J. Biol. Chem. 271 (1996) 28734-28737
8. Mosavi L.K., Williams S., and Peng Zy Z.Y. Equilibrium folding and stability of myotrophin: a model ankyrin repeat protein. J. Mol. Biol. 320 (2002) 165-170
9. Zweifel M.E., and Barrick D. Studies of the ankyrin repeats of the Drosophila melanogaster Notch receptor. 2. Solution stability and cooperativity of unfolding. Biochemistry 40 (2001) 14357-14367
10. Wetzel S.K., Settanni G., Kenig M., Binz H.K., and Pluckthun A. Folding and unfolding mechanism of highly stable full-consensus ankyrin repeat proteins. J. Mol. Biol. 376 (2008) 241-257
11. Kajander T., Cortajarena A.L., Main E.R., Mochrie S.G., and Regan L. A new folding paradigm for repeat proteins. J. Am. Chem. Soc. 127 (2005) 10188-10190
12. Stumpp M.T., Forrer P., Binz H.K., and Pluckthun A. Designing repeat proteins: modular leucine-rich repeat protein libraries based on the mammalian ribonuclease inhibitor family. J. Mol. Biol. 332 (2003) 471-487
13. Kamen D.E., and Woody R.W. A partially folded intermediate conformation is induced in pectate lyase C by the addition of 8-anilino-1-naphthalenesulfonate (ANS). Protein Sci. 10 (2001) 2123-2130
14. Junker M., Schuster C.C., McDonnell A.V., Sorg K.A., Finn M.C., Berger B., and Clark P.L. Pertactin beta-helix folding mechanism suggests common themes for the secretion and folding of autotransporter proteins. Proc. Natl Acad. Sci. USA 103 (2006) 4918-4923
15. Werbeck N.D., and Itzhaki L.S. Probing a moving target with a plastic unfolding intermediate of an ankyrin-repeat protein. Proc. Natl Acad. Sci. USA 104 (2007) 7863-7868
16. Evdokimov A.G., Anderson D.E., Routzahn K.M., and Waugh D.S. Unusual molecular architecture of the Yersinia pestis cytotoxin YopM: a leucine-rich repeat protein with the shortest repeating unit. J.¢Mol. Biol. 312 (2001) 807-821
17. Kajava A.V., and Kobe B. Assessment of the ability to model proteins with leucine-rich repeats in light of the latest structural information. Protein Sci. 11 (2002) 1082-1090
18. Cantor C.R., and Schimmel P.R. The behavior of biological macromolecules. Biophysical Chemistry Part III (1980), W.H. Freeman and Company, New York
19. Myers J.K., Pace C.N., and Scholtz J.M. Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding. Protein Sci. 4 (1995) 2138-2148
20. Auton M., Holthauzen L.M., and Bolen D.W. Anatomy of energetic changes accompanying urea-induced protein denaturation. Proc. Natl Acad. Sci. USA 104 (2007) 15317-15322
21. Auton M., and Bolen D.W. Application of the transfer model to understand how naturally occurring osmolytes affect protein stability. Methods Enzymol. 428 (2007) 397-418
22. Privalov P.L. Stability of proteins: small globular proteins. Adv. Protein Chem. 33 (1979) 167-241
23. Reimer U., Scherer G., Drewello M., Kruber S., Schutkowski M., and Fischer G. Side-chain effects on peptidyl-prolyl cis/trans isomerisation. J. Mol. Biol. 279 (1998) 449-460
24. Schmid F.X. Fast-folding and slow-folding forms of unfolded proteins. Methods Enzymol. 131 (1986) 70-82
25. Brandts J.F., Halvorson H.R., and Brennan M. Consideration of the possibility that the slow step in protein denaturation reactions is due to cis-trans isomerism of proline residues. Biochemistry 14 (1975) 4953-4963
26. Nall B.T., Garel J.R., and Baldwin R.L. Test of the extended two-state model for the kinetic intermediates observed in the folding transition of ribonuclease A. J. Mol. Biol. 118 (1978) 317-330
27. Dang Q., and Frieden C. New PC versions of the kinetic-simulation and fitting programs, KINSIM and FITSIM. Trends Biochem. Sci. 22 (1997) 317
28. Mello C.C., Bradley C.M., Tripp K.W., and Barrick D. Experimental characterization of the folding kinetics of the notch ankyrin domain. J. Mol. Biol. 352 (2005) 266-281
29. Bradley C.M., and Barrick D. The notch ankyrin domain folds via a discrete, centralized pathway. Structure 14 (2006) 1303-1312
30. Low C., Weininger U., Zeeb M., Zhang W., Laue E.D., Schmid F.X., and Balbach J. Folding mechanism of an ankyrin repeat protein: scaffold and active site formation of human CDK inhibitor p19(INK4d). J. Mol. Biol. 373 (2007) 219-231
31. Kiefhaber T., Kohler H.H., and Schmid F.X. Kinetic coupling between protein folding and prolyl isomerization. I. Theoretical models. J. Mol. Biol. 224 (1992) 217-229
32. Dominy B.N., Perl D., Schmid F.X., and Brooks III C.L. The effects of ionic strength on protein stability: the cold shock protein family. J. Mol. Biol. 319 (2002) 541-554
33. Collins K.D., and Washabaugh M.W. The Hofmeister effect and the behaviour of water at interfaces. Q. Rev. Biophys. 18 (1985) 323-422
34. Schleich P.H.V.H.a.T. Ion effects on the solution structure of biological macromolecules. Acc. Chem. Res. 2 (1969) 257-265
35. Wyman Jr. J. Linked functions and reciprocal effects in hemoglobin: a second look. Adv. Protein Chem. 19 (1964) 223-286
36. Greene Jr. R.F., and Pace C.N. Urea and guanidine hydrochloride denaturation of ribonuclease, lysozyme, alpha-chymotrypsin, and beta-lactoglobulin. J. Biol. Chem. 249 (1974) 5388-5393
37. Thomson J.A., Shirley B.A., Grimsley G.R., and Pace C.N. Conformational stability and mechanism of folding of ribonuclease T1. J. Biol. Chem. 264 (1989) 11614-11620
38. Santoro M.M., and Bolen D.W. A test of the linear extrapolation of unfolding free energy changes over an extended denaturant concentration range. Biochemistry 31 (1992) 4901-4907
39. Agashe V.R., and Udgaonkar J.B. Thermodynamics of denaturation of barstar: evidence for cold denaturation and evaluation of the interaction with guanidine hydrochloride. Biochemistry 34 (1995) 3286-3299
40. Nicholson E.M., and Scholtz J.M. Conformational stability of the Escherichia coli HPr protein: test of the linear extrapolation method and a thermodynamic characterization of cold denaturation. Biochemistry 35 (1996) 11369-11378
41. Zeeb M., Rosner H., Zeslawski W., Canet D., Holak T.A., and Balbach J. Protein folding and stability of human CDK inhibitor p19(INK4d). J. Mol. Biol. 315 (2002) 447-457
42. Mello C.C., and Barrick D. An experimentally determined protein folding energy landscape. Proc. Natl Acad. Sci. USA 101 (2004) 14102-14107
43. Street T.O., Bradley C.M., and Barrick D. Predicting coupling limits from an experimentally determined energy landscape. Proc. Natl Acad. Sci. USA 104 (2007) 4907-4912
44. Courtemanche N., and Barrick D. The leucine-rich repeat domain of internalin B Folds along a polarized N-terminal pathway. Structure 16 (2008) 705-714
45. Otzen D.E., Kristensen O., Proctor M., and Oliveberg M. Structural changes in the transition state of protein folding: alternative interpretations of curved chevron plots. Biochemistry 38 (1999) 6499-6511
46. Sanchez I.E., and Kiefhaber T. Evidence for sequential barriers and obligatory intermediates in apparent two-state protein folding. J. Mol. Biol. 325 (2003) 367-376
47. Main E.R., Stott K., Jackson S.E., and Regan L. Local and long-range stability in tandemly arrayed tetratricopeptide repeats. Proc. Natl Acad. Sci. USA 102 (2005) 5721-5726
48. Perl D., and Schmid F.X. Electrostatic stabilization of a thermophilic cold shock protein. J. Mol. Biol. 313 (2001) 343-357
49. Wada A., and Nakamura H. Nature of the charge distribution in proteins. Nature 293 (1981) 757-758
50. Lee K.K., Fitch C.A., Lecomte J.T., and Garcia-Moreno E.B. Electrostatic effects in highly charged proteins: salt sensitivity of pKa values of histidines in staphylococcal nuclease. Biochemistry 41 (2002) 5656-5667
51. de Los Rios M.A., and Plaxco K.W. Apparent Debye-Huckel electrostatic effects in the folding of a simple, single domain protein. Biochemistry 44 (2005) 1243-1250
52. Pace C.N., and Grimsley G.R. Ribonuclease T1 is stabilized by cation and anion binding. Biochemistry 27 (1988) 3242-3246
53. Maldonado S., Irun M.P., Campos L.A., Rubio J.A., Luquita A., et al. Salt-induced stabilization of apoflavodoxin at neutral pH is mediated through cation-specific effects. Protein Sci. 11 (2002) 1260-1273
54. Record Jr. M.T., Zhang W., and Anderson C.F. Analysis of effects of salts and uncharged solutes on protein and nucleic acid equilibria and processes: a practical guide to recognizing and interpreting polyelectrolyte effects, Hofmeister effects, and osmotic effects of salts. Adv. Protein Chem. 51 (1998) 281-353
55. Dryden D.T. DNA mimicry by proteins and the control of enzymatic activity on DNA. Trends Biotechnol. 24 (2006) 378-382
56. Batey S., Randles L.G., Steward A., and Clarke J. Cooperative folding in a multi-domain protein. J. Mol. Biol. 349 (2005) 1045-1059
57. Shortle D. Staphylococcal nuclease: a showcase of m-value effects. Adv. Protein Chem. 46 (1995) 217-247
58. Crick S.L., Jayaraman M., Frieden C., Wetzel R., and Pappu R.V. Fluorescence correlation spectroscopy shows that monomeric polyglutamine molecules form collapsed structures in aqueous solutions. Proc. Natl Acad. Sci. USA 103 (2006) 16764-16769
59. Pace C.N., Laurents D.V., and Thomson J.A. pH dependence of the urea and guanidine hydrochloride denaturation of ribonuclease A and ribonuclease T1. Biochemistry 29 (1990) 2564-2572
60. Wrabl J., and Shortle D. A model of the changes in denatured state structure underlying m value effects in staphylococcal nuclease. Nature Struct. Biol. 6 (1999) 876-883
61. Swint-Kruse L., and Robertson A.D. Hydrogen bonds and the pH dependence of ovomucoid third domain stability. Biochemistry 34 (1995) 4724-4732
62. Oliveberg M., Vuilleumier S., and Fersht A.R. Thermodynamic study of the acid denaturation of barnase and its dependence on ionic strength: evidence for residual electrostatic interactions in the acid/thermally denatured state. Biochemistry 33 (1994) 8826-8832
63. Oliveberg M., Arcus V.L., and Fersht A.R. pKA values of carboxyl groups in the native and denatured states of barnase: the pKA values of the denatured state are on average 0.4 units lower than those of model compounds. Biochemistry 34 (1995) 9424-9433
64. Tan Y.J., Oliveberg M., Davis B., and Fersht A.R. Perturbed pKA-values in the denatured states of proteins. J. Mol. Biol. 254 (1995) 980-992
65. Kuhlman B., Luisi D.L., Young P., and Raleigh D.P. pKa values and the pH dependent stability of the N-terminal domain of L9 as probes of electrostatic interactions in the denatured state. Differentiation between local and nonlocal interactions. Biochemistry 38 (1999) 4896-4903
66. Whitten S.T., and Garcia-Moreno E.B. pH dependence of stability of staphylococcal nuclease: evidence of substantial electrostatic interactions in the denatured state. Biochemistry 39 (2000) 14292-14304
67. Pace C.N., Alston R.W., and Shaw K.L. Charge-charge interactions influence the denatured state ensemble and contribute to protein stability. Protein Sci. 9 (2000) 1395-1398
68. Edelhoch H. Spectroscopic determination of tryptophan and tyrosine in proteins. Biochemistry 6 (1967) 1948-1954
69. Street T.O., Courtemanche N., and Barrick D. Protein folding and stability using denaturants. Methods Cell Biol. 84 (2008) 295-325
70. Pace C.N. Determination and analysis of urea and guanidine hydrochloride denaturation curves. Methods Enzymol. 131 (1986) 266-280
71. Santoro M.M., and Bolen D.W. Unfolding free energy changes determined by the linear extrapolation method. 1. Unfolding of phenylmethanesulfonyl alpha-chymotrypsin using different denaturants. Biochemistry 27 (1988) 8063-8068
72. Chou P.Y., and Fasman G.D. Beta-turns in proteins. J. Mol. Biol. 115 (1977) 135-175