Dynamics and mechanism of the tanford transition of bovine β-lactoglobulin studied using heteronuclear NMR spectroscopy

Journal of Molecular Biology

Volumn 356, Issue 2, 2006, Pages 483-496

  Sakurai, Kazumasa ^a   Goto, Yuji ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

Loop dynamics; NMR; pH dependent conformational change; Tanford transition; lactoglobulin

Indexed keywords

BETA LACTOGLOBULIN; THIOL GROUP;

ARTICLE; CIRCULAR DICHROISM; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; COW; DISULFIDE BOND; HYDROGEN BOND; HYDROPHOBICITY; MATHEMATICAL ANALYSIS; NONHUMAN; NUCLEAR MAGNETIC RESONANCE SPECTROSCOPY; OPTICAL ROTATORY DISPERSION; PH; PRIORITY JOURNAL; X RAY ANALYSIS;

BOVINAE;

EID: 30744476205     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2005.11.038     Document Type: Article

References (40)

1. L.K. Nicholson, T. Yamazaki, D.A. Torchia, S. Grezesiek, A. Bax, and S.J. Stahl Flexibility and function in HIV-1 protease Nature Struct. Biol. 2 1995 274 280
2. D. McElheny, J.R. Schnell, J.C. Lansing, H.J. Dyson, and P.E. Wright Defining the role of active-site loop fluctuations in dihydrofolate reductase catalysis Proc. Natl Acad. Sci. USA 102 2005 5032 5037
3. N.R. Skrynnikov, F.A.A. Mulder, B. Hon, F.W. Dahlquist, and L.E. Kay Probing slow timescale dynamics at methyl-containing side-chains in proteins by relaxation dispersion NMR measurements: application to methionine residues in a cavity mutant of T4 lysozyme J. Am. Chem. Soc. 123 2001 4556 4666
4. F.A.A. Mulder, A. Mittermaier, B. Hon, F.W. Dahlquist, and L.E. Kay Studying excited states of proteins by NMR spectroscopy Nature Struct. Biol. 8 2001 932 935
5. J. Godovac-Zimmermann The structural motif of β-lactoglobulin and retinol-binding protein Trends Biochem. Sci. 13 1988 64 66
6. S.G. Hambling, A.S. MacAlpine, and L. Sawyer β-Lactoglobulin P.F. Fox Advanced Dairy Chemistry 1992 Elsevier Amsterdam 141 190
7. L. Sawyer, and G. Kontopidis The core lipocalin, bovine β-lactoglobulin Biochim. Biophys. Acta 1482 2000 136 148
8. S. Brownlow, J.H.M. Cabral, R. Cooper, D.R. Flower, S.J. Yewdall, and I. Polikarpov Bovine β-lactoglobulin at 1.8 Å resolution - still an enigmatic lipocalin Structure 5 1997 481 495
9. B.Y. Qin, M.C. Bewley, L.K. Creamer, H.M. Baker, E.N. Baker, and G.B. Jameson Structural basis of the Tanford transition of bovine β-lactoglobulin Biochemistry 37 1998 14014 14023
10. B.Y. Qin, L.K. Creamer, E.N. Baker, and G.B. Jameson 12-Bromododecanoic acid binds inside the calyx of bovine β-lactoglobulin FEBS Letters 438 1998 272 278
11. K. Kuwata, M. Hoshino, S. Era, C.A. Batt, and Y. Goto α→β Transition of β-lactoglobulin as evidenced by heteronuclear NMR J. Mol. Biol. 283 1998 731 739
12. K. Kuwata, M. Hoshino, V. Forge, S. Era, C.A. Batt, and Y. Goto Solution structure and dynamics of bovine β-lactoglobulin A Protein Sci. 8 1999 2541 2545
13. S. Uhrínová, M.H. Smith, G.B. Jameson, D. Uhrín, L. Sawyer, and P.N. Barlow Structural changes accompanying pH-induced dissociation of the β-lactoglobulin dimer Biochemistry 39 2000 3565 3574
14. S.-Y. Wu, M.D. Pérez, P. Puyol, and L. Sawyer βLactoglobulin binds palmitate within its central cavity J. Biol. Chem. 274 1999 170 174
15. G. Kontopidis, C. Holt, and L. Sawyer β-Lactoglobulin: binding properties, structure, and function J. Dairy Sci. 87 2004 785 796
16. M. Seppälä, R.N. Taylor, H. Koistinen, R. Koistinen, and E. Milgrom Glycodelin: a major lipocalin protein of the reproductive axis with diverse actions in cell recognition and differentiation Endocrine Rev. 23 2002 401 430
17. F.E. Cohen Protein misfolding and prion diseases J. Mol. Biol. 293 1999 313 320
18. C. Tanford, L.G. Bunville, and Y. Nozaki The reversible transformation of β-lactoglobulin at pH 7.5 J. Am. Chem. Soc. 81 1959 4032 4036
19. F. Fogolari, E. Moroni, M. Wojciechowski, M. Baginski, L. Ragona, and H. Molinari MM/PBSA analysis of molecular dynamics simulations of bovine β-lactoglobulin: free energy gradients in conformational transitions? Proteins: Struct. Funct. Genet. 59 2005 91 103
20. 15N chemical shifts for bovine β-lactoglobulin: secondary structure and topology of the native state is retained in a partially unfolded form J. Biol. NMR 12 1998 89 107
21. F. Fogolari, L. Ragona, S. Licciardi, S. Romagnoli, R. Michelutti, R. Ugolini, and H. Molinari Electrostatic properties of bovine β-lactoglobulin Proteins: Struct. Funct. Genet. 39 2000 317 330
22. G. Lipari, and A. Szabo Model-free approach to the interpretation of nuclear magnetic resonance relaxation in macromolecules. 1. Theory and range of validity J. Am. Chem. Soc. 104 1982 4546 4559
23. S. Bagby, K.I. Tong, and M. Ikura Optimization of protein solubility and stability for protein nuclear magnetic resonance Methods Enzymol. 339 2001 20 41
24. K. Sakurai, and Y. Goto Manipulating monomer-dimer equilibrium of bovine β-lactoglobulin by amino acid substitution J. Biol. Chem. 277 2002 25735 25740
25. R.B. Freedman Protein disulfide isomerase: Multiple roles in the modification of nascent secretory proteins Cell 57 1989 1069 1072
26. M. Yagi, K. Sakurai, C. Kalidas, C.A. Batt, and Y. Goto Reversible unfolding of bovine β-lactoglobulin mutants without a free thiol group J. Biol. Chem. 278 2003 47009 47015
27. P. Dosset, J.-C. Hus, M. Blackedge, and D. Marion Efficient analysis of macromolecular rotational diffusion from heteronuclear relaxation data J. Biomol. NMR 16 2000 23 28
28. K. Shiraki, M. Kudou, R. Sakamoto, I. Yanagihara, and M. Takagi Amino acid esters prevent thermal inactivation and aggregation of lysozyme Biotechnol. Prog. 2 2005 640 643
29. M. Kudou, K. Shiraki, S. Fujiwara, T. Imanaka, and M. Takagi Prevention of thermal inactivation and aggregation of lysozyme by polyamines Eur. J. Biochem. 22 2003 4547 4554
30. K. Sakurai, M. Oobatake, and Y. Goto Salt-dependent monomer-dimer equilibrium of bovine β-lactoglobulin at pH 3 Protein Sci. 10 2001 2325 2335
31. D. Hamada, and C.M. Dobson A kinetic study of β-lactoglobulin amyloid fibril formation promoted by urea Protein Sci. 11 2002 2417 2426
32. J.P. Loria, M. Rance, and A.G. Palmer III A relaxation compensated Carr-Perucell-Meiboom-Gill sequence for characterizing chemical exchange by NMR spectroscopy J. Am. Chem. Soc. 121 1999 2331 2332
33. N. Guex, and M.C. Peitsch SWISS-MODEL and the Swiss-PdbViewer: an environment for comparative protein modeling Electrophoresis 18 1997 2714 2723
34. S.N. Ho, H.D. Hunt, R.M. Horton, J.K. Pullen, and L.R. Pease Site-directed mutagenesis by overlap extension using the polymerase chain reaction Gene 77 1989 51 59
35. T.-R. Kim, Y. Goto, N. Hirota, K. Kuwata, H. Denton, and S.-Y. Wu High-level expression of bovine β-lactoglobulin in Pichia pastoris and characterization of its physical properties Protein Eng. 10 1997 1339 1345
36. S.C. Gill, and P.H. von Hippel Calculation of protein extinction coefficients from amino acid sequence data Anal. Biochem. 182 1989 319 326
37. J.K. Myers, C.N. Pace, and J.M. Scholtz Denaturant m values and heat capacity changes: relation to changes in accessible surface areas of protein unfolding Protein Sci. 4 1995 2138 2148
38. 15N inverse detected heteronuclear NMR spectroscopy: application to staphylococcal nuclease Biochemistry 28 1989 8972 8979
39. R. Koradi, M. Billeter, and K. Wüthrich MOLMOL: a program for display and analysis of macromolecular structures J. Mol. Graph. 14 1996 51 55
40. S.C. Lovell, I.W. Davis, W.B. Arendall III, P.I.W de Bakker, J.M. Word, and M.G. Prisant Structure validation by Cα geometry: φ, ψ, and Cβ deviation Proteins: Struct. Funct. Genet. 50 2003 437 450