Elimination of the C-cap in ubiquitin-structure, dynamics and thermodynamic consequences

Biophysical Chemistry

Volumn 126, Issue 1-3, 2007, Pages 25-35

  Ermolenko, Dmitri N ^a,c   Dangi, Bindi ^b,d   Gvritishvili, Anzor ^a   Gronenborn, Angela M ^b   Makhatadze, George I ^a  

^a PENN STATE COLLEGE OF MEDICINE   (United States)

^b NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^c BACH INSTITUTE OF BIOCHEMISTRY   (Russian Federation)

^d Martek Biosciences Corporation   (United States)

Author keywords

Circular dichroism spectroscopy; Cooperativity of unfolding; Differential scanning calorimetry; Heteronuclear NMR; Protein stability; Protein structure

Indexed keywords

8 ANILINO 1 NAPHTHALENESULFONIC ACID; PROLINE; UBIQUITIN;

ALPHA HELIX; ANALYTIC METHOD; ARTICLE; CONFORMATIONAL TRANSITION; DENATURATION; DIFFERENTIAL SCANNING CALORIMETRY; HYDROPHOBICITY; PRIORITY JOURNAL; PROTEIN STRUCTURE; THERMODYNAMICS; WILD TYPE;

AMINO ACID SEQUENCE; AMINO ACID SUBSTITUTION; CALORIMETRY, DIFFERENTIAL SCANNING; CIRCULAR DICHROISM; MOLECULAR SEQUENCE DATA; MUTAGENESIS, SITE-DIRECTED; MUTATION; PROLINE; PROTEIN CONFORMATION; PROTEIN DENATURATION; PROTEIN FOLDING; PROTEIN STRUCTURE, SECONDARY; THERMODYNAMICS; UBIQUITIN;

EID: 33846649161     PISSN: 03014622     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.bpc.2006.03.017     Document Type: Article

References (64)

1. Ermolenko D.N., Thomas S.T., Aurora R., Gronenborn A.M., and Makhatadze G.I. Hydrophobic interactions at the Ccap position of the C-capping motif of alpha-helices. J. Mol. Biol. 322 (2002) 123-135
2. Thomas S.T., Loladze V.V., and Makhatadze G.I. Hydration of the peptide backbone largely defines the thermodynamic propensity scale of residues at the C′ position of the C-capping box of alpha-helices. Proc. Natl. Acad. Sci. U. S. A. 98 (2001) 10670-10675
3. Aurora R., and Rose G.D. Helix capping. Protein Sci. 7 (1998) 21-38
4. Makhatadze G.I., Loladze V.V., Ermolenko D.N., Chen X., and Thomas S.T. Contribution of surface salt bridges to protein stability: guidelines for protein engineering. J. Mol. Biol. 327 (2003) 1135-1148
5. 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
6. Lopez M.M., and Makhatadze G.I. Differential scanning calorimetry. Methods Mol. Biol. 173 (2002) 113-119
7. Gribenko A.V., and Makhatadze G.I. Oligomerization and divalent ion binding properties of the S100P protein: a Ca2+/Mg2+-switch model. J. Mol. Biol. 283 (1998) 679-694
8. Lopez M.M., Yutani K., and Makhatadze G.I. Interactions of the major cold shock protein of Bacillus subtilis CspB with single-stranded DNA templates of different base composition. J. Biol. Chem. 274 (1999) 33601-33608
9. Gribenko A.V., Guzman-Casado M., Lopez M.M., and Makhatadze G.I. Conformational and thermodynamic properties of peptide binding to the human S100P protein. Protein Sci. 11 (2002) 1367-1375
10. Loladze V.V., Ermolenko D.N., and Makhatadze G.I. Heat capacity changes upon burial of polar and nonpolar groups in proteins. Protein Sci. 10 (2001) 1343-1352
11. Bax A., and Grzesiek S. Methodological advances in protein NMR. Accounts Chem. Res. 26 (1993) 131-138
12. Fesik S.W., and Zuiderweg E.R. Heteronuclear three-dimensional NMR spectroscopy of isotopically labelled biological macromolecules. Q. Rev. Biophys. 23 (1990) 97-131
13. Logan T.M., Olejniczak E.T., Xu R.X., and Fesik S.W. Side chain and backbone assignments in isotopically labeled proteins from two heteronuclear triple resonance experiments. FEBS Lett. 314 (1992) 413-418
14. Marion D., Driscoll P.C., Kay L.E., Wingfield P.T., Bax A., Gronenborn A.M., and Clore G.M. Overcoming the overlap problem in the assignment of 1H NMR spectra of larger proteins by use of three-dimensional heteronuclear 1H-15N Hartmann-Hahn-multiple quantum coherence and nuclear Overhauser-multiple quantum coherence spectroscopy: application to interleukin 1 beta. Biochemistry 28 (1989) 6150-6156
15. Clore G.M., Bax A., Driscoll P.C., Wingfield P.T., and Gronenborn A.M. Assignment of the side-chain 1H and 13C resonances of interleukin-1 beta using double- and triple-resonance heteronuclear three-dimensional NMR spectroscopy. Biochemistry 29 (1990) 8172-8184
16. Clore G.M., and Gronenborn A.M. Structures of larger proteins in solution: three- and four-dimensional heteronuclear NMR spectroscopy. Science 252 (1991) 1390-1399
17. Ruckert M., and Otting G. Alignment of biological macromolecules in novel nonionic liquid crystalline media for NMR experiments. J. Am. Chem. Soc. 122 (2000) 7793-7797
18. Chou J.J., Gaemers S., Howder B., Louis J.M., and Bax A. A simple apparatus for generating stretched polyacrylamide gels, yielding uniform alignment of proteins and detergent micelles. J. Biomol. NMR 21 (2001) 377-382
19. Ding K., and Gronenborn A.M. Sensitivity-enhanced E.COSY-type HSQC experiments for accurate measurements of one-bond 15N-1H(N) and 15N-13C′ and two-bond 13C′-1H(N) residual dipolar couplings in proteins. J. Magn. Reson. 158 (2002) 173-177
20. Brunger AT., Adams P.D., Clore G.M., DeLano W.L., Gros P., Grosse-Kunstleve R.W., Jiang J.S., Kuszewski J., Nilges M., Pannu N.S., Read R.J., Rice L.M., Simonson T., and Warren G.L. Crystallography and NMR system: a new software suite for macromolecular structure determination. Acta Crystallogr., D Biol. Crystallogr. 54 Pt 5 (1998) 905-921
21. Zweckstetter M., and Bax A. Prediction of sterically induced alignment in a dilute liquid crystalline phase: aid to protein structure determination by NMR. J. Am. Chem. Soc. 122 (2000) 3379-3791
22. Kay L.E., Torchia D.A., and Bax A. Backbone dynamics of proteins as studied by 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease. Biochemistry 28 (1989) 8972-8979
23. Farrow N.A., Zhang O., Forman-Kay J.D., and Kay L.E. Characterization of the backbone dynamics of folded and denatured states of an SH3 domain. Biochemistry 36 (1997) 2390-2402
24. Garrett D., Powers R., Gronenborn A.M., and Clore G.M. A common sense approach to peak picking in two-, three- and four-dimensional spectra using automatic computer analysis of contour diagrams. J. Magn. Reson. 95 (1991) 214-220
25. Tjandra N., Kuboniwa H., Ren H., and Bax A. Rotational dynamics of calcium-free calmodulin studied by 15N-NMR relaxation measurements. Eur. J. Biochem. 230 (1995) 1014-1024
26. Wishart D.S., Sykes B.D., and Richards F.M. The chemical shift index: a fast and simple method for the assignment of protein secondary structure through NMR spectroscopy. Biochemistry 31 (1992) 1647-1651
27. Cornilescu G., Delaglio F., and Bax A. Protein backbone angle restraints from searching a database for chemical shift and sequence homology. J. Biomol. NMR 13 (1999) 289-302
28. Guex N., and Peitsch M.C. SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling. Electrophoresis 18 (1997) 2714-2723
29. Laskowski R.A., Rullmannn J.A., MacArthur M.W., Kaptein R., and Thornton J.M. AQUA and PROCHECK-NMR: programs for checking the quality of protein structures solved by NMR. J. Biomol. NMR 8 (1996) 477-486
30. R. Koradi, M. Billeter, K. Wuthrich, MOLMOL: a program for display and analysis of macromolecular structures, J. Mol. Graph. 14 (1996), 51-55, 29-32.
31. Hubbard S.J., and Thornton J.M. 'NACCESS', Computer Program Department of Biochemistry and Molecular Biology (1993), University College London
32. Chothia C. Hydrophobic bonding and accessible surface area in proteins. Nature 248 (1974) 338-339
33. Kumar S., and Bansal M. Dissecting alpha-helices: position-specific analysis of alpha-helices in globular proteins. Proteins 31 (1998) 460-476
34. Penel S., Hughes E., and Doig A.J. Side-chain structures in the first turn of the alpha-helix. J. Mol. Biol. 287 (1999) 127-143
35. Schimmel P.R., and Flory P.J. Conformational energies and configurational statistics of copolypeptides containing l-proline. J. Mol. Biol. 34 (1968) 105-120
36. Loladze V.V., Ibarra-Molero B., Sanchez-Ruiz J.M., and Makhatadze G.I. Engineering a thermostable protein via optimization of charge-charge interactions on the protein surface. Biochemistry 38 (1999) 16419-16423
37. Gronenborn A.M., and Clore G.M. Rapid screening for structural integrity of expressed proteins by heteronuclear NMR spectroscopy. Protein Sci. 5 (1996) 174-177
38. Ding K., Louis J.M., and Gronenborn A.M. Insights into conformation and dynamics of protein GB1 during folding and unfolding by NMR. J. Mol. Biol. 335 (2004) 1299-1307
39. Kitahara R., Yokoyama S., and Akasaka K. NMR snapshots of a fluctuating protein structure: ubiquitin at 30 bar-3 kbar. J. Mol. Biol. 347 (2005) 277-285
40. Johnson E.C., Lazar G.A., Desjarlais J.R., and Handel T.M. Solution structure and dynamics of a designed hydrophobic core variant of ubiquitin structure. Fold. Des. 7 (1999) 967-976
41. Lazar G.A., Desjarlais J.R., and Handel T.M. De novo design of the hydrophobic core of ubiquitin. Protein Sci. 6 (1997) 1167-1178
42. Makhatadze G.I., and Privalov P.L. Energetics of protein structure. Adv. Protein Chem. 47 (1995) 307-425
43. Lazaridis T., Archontis G., and Karplus M. Enthalpic contribution to protein stability: insights from atom-based calculations and statistical mechanics. Adv. Protein Chem. 47 (1995) 231-306
44. Loladze V.V., Ermolenko D.N., and Makhatadze G.I. Thermodynamic consequences of burial of polar and non-polar amino acid residues in the protein interior. J. Mol. Biol. 320 (2002) 343-357
45. Scholtz J.M., Marqusee S., Baldwin R.L., York E.J., Stewart J.M., Santoro M., and Bolen D.W. Calorimetric determination of the enthalpy change for the alpha-helix to coil transition of an alanine peptide in water. Proc. Natl. Acad. Sci. U. S. A. 88 (1991) 2854-2858
46. Lopez M.M., Chin D.H., Baldwin R.L., and Makhatadze G.I. The enthalpy of the alanine peptide helix measured by isothermal titration calorimetry using metal-binding to induce helix formation. Proc. Natl. Acad. Sci. U. S. A. 99 (2002) 1298-1302
47. Richardson J.M., McMahon K.W., MacDonald C.C., and Makhatadze G.I. MEARA sequence repeat of human CstF-64 polyadenylation factor is helical in solution. A spectroscopic and calorimetric study. Biochemistry 38 (1999) 12869-12875
48. Richardson J.M., and Makhatadze G.I. Temperature dependence of the thermodynamics of helix-coil transition. J. Mol. Biol. 335 (2004) 1029-1037
49. Richardson J.M., Lopez M.M., and Makhatadze G.I. Enthalpy of helix-coil transition: missing link in rationalizing the thermodynamics of helix-forming propensities of the amino acid residues. Proc. Natl. Acad. Sci. U. S. A. 102 (2005) 1413-1418
50. Makhatadze G.I., and Privalov P.L. Heat capacity of proteins: I. Partial molar heat capacity of individual amino acid residues in aqueous solution: hydration effect. J. Mol. Biol. 213 (1990) 375-384
51. Privalov P.L., and Makhatadze G.I. Heat capacity of proteins: II. Partial molar heat capacity of the unfolded polypeptide chain of proteins: protein unfolding effects. J. Mol. Biol. 213 (1990) 385-391
52. Spolar R.S., Livingstone J.R., and Record Jr. M.T. Use of liquid hydrocarbon and amide transfer data to estimate contributions to thermodynamic functions of protein folding from the removal of nonpolar and polar surface from water. Biochemistry 31 (1992) 3947-3955
53. Murphy K.P., and Freire E. Thermodynamics of structural stability and cooperative folding behavior in proteins. Adv. Protein Chem. 43 (1992) 313-361
54. Schellman J.A. Solvent denaturation. Biopolymers 17 (1978) 1305-1322
55. Alonso D.O., and Dill K.A. Solvent denaturation and stabilization of globular proteins. Biochemistry 30 (1991) 5974-5985
56. 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
57. Goto Y., Azuma T., and Hamaguchi K. Refolding of the immunoglobulin light chain. J. Biochem. (Tokyo) 85 (1979) 1427-1438
58. Lakowitcz J.R. Principles of Fluorescence Spectroscopy (1983), Plenum Press, New York
59. Teschke C.M., King J., and Prevelige Jr. P.E. Inhibition of viral capsid assembly by 1,1′-bi(4-anilinonaphthalene-5-sulfonic acid). Biochemistry 32 (1993) 10658-10665
60. Matulis D., and Lovrien R. 1-Anilino-8-naphthalene sulfonate anion-protein binding depends primarily on ion pair formation. Biophys. J. 74 (1998) 422-429
61. Privalov P.L., and Khechinashvili N.N. A thermodynamic approach to the problem of stabilization of globular protein structure: a calorimetric study. J. Mol. Biol. 86 (1974) 665-684
62. Briggs M.S., and Roder H. Early hydrogen-bonding events in the folding reaction of ubiquitin. Proc. Natl. Acad. Sci. U. S. A. 89 (1992) 2017-2021
63. Krantz B.A., Dothager R.S., and Sosnick T.R. Discerning the structure and energy of multiple transition states in protein folding using psi-analysis. J. Mol. Biol. 337 (2004) 463-475
64. Went H.M., and Jackson S.E. Ubiquitin folds through a highly polarized transition state. Protein Eng., Des. Sel. 18 (2005) 229-237