The pH-dependent unfolding mechanism of P2 myelin protein: An experimental and computational study

Journal of Structural Biology

Volumn 153, Issue 3, 2006, Pages 253-263

  Polverini, Eugenia ^a   Fornabaio, Micaela ^a,d   Fasano, Anna ^b   Carlone, Giulia ^c   Riccio, Paolo ^c   Cavatorta, Paolo ^a  

^a CNR   (Italy)

^b UNIVERSITY OF BARI   (Italy)

^c UNIVERSITY OF BASILICATA   (Italy)

^d VIRGINIA COMMONWEALTH UNIVERSITY   (United States)

Author keywords

Circular dichroism; Fatty acid binding proteins; Fluorescence; Molecular dynamics; Protein structure

Indexed keywords

MYELIN BASIC PROTEIN;

ALPHA HELIX; ARTICLE; CELL MEMBRANE; MATHEMATICAL COMPUTING; MOLECULAR DYNAMICS; MOLECULAR MECHANICS; PH MEASUREMENT; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN FOLDING; PROTEIN PURIFICATION; SIMULATION; SPECTROSCOPY;

ANIMALS; COMPUTATIONAL BIOLOGY; HYDROGEN-ION CONCENTRATION; MYELIN P2 PROTEIN; PROTEIN CONFORMATION; PROTEIN FOLDING;

EID: 32544450943     PISSN: 10478477     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jsb.2005.11.010     Document Type: Article

References (58)

1. L. Banaszak, N. Winter, Z. Xu, D.A. Bernlohr, S. Cowan, and T.A. Jones Lipid-binding proteins: a family of fatty acid and retinoid transport proteins Adv. Protein Chem. 45 1994 89 151
2. D. Bashford, and D.A. Case Generalized born models of macromolecular solvation effects Annu. Rev. Phys. Chem. 51 2000 129 152
3. I.R. Bates, P. Matharu, N. Ishiyama, D. Rochon, D.D. Wood, E. Polverini, M.A. Moscarello, N.J. Viner, and G. Harauz Characterization of a recombinant murine 18.5-kDa myelin basic protein Protein Expr. Purif. 20 2000 285 299
4. H.M. Berman, J. Westbrook, Z. Feng, G. Gilliland, T.N. Bhat, H. Weissig, I.N. Shindyalov, and P.E. Bourne The Protein Data Bank Nucleic Acids Res. 28 2000 235 242
5. T.A. Binkowski, S. Naghibzadeh, and J. Liang CASTp: computed atlas of surface topography of proteins Nucleic Acids Res. 31 2003 3352 3355
6. B.R. Brooks, R.E. Bruccoleri, B.D. Olafson, D.J. States, S. Swaminathan, and M. Karplus CHARMM: a program for macromolecular energy minimization and dynamic calculations J. Comput. Chem. 4 1983 187 217
7. M.K. Buelt, Z. Xu, L.J. Banaszak, and D.A. Bernlohr Structural and functional characterization of the phosphorylated adipocyte lipid-binding protein (pp15) Biochemistry 31 1992 3493 3499
8. S.K. Burley, and G.A. Petsko Amino-aromatic interactions in proteins FEBS Lett. 203 1986 139 143
9. V.E. Bychkova, R. Berni, G.L. Rossi, V.P. Kutyshenko, and O.B. Ptitsyn Retinol-binding protein is in the molten globule state at low pH Biochemistry 31 1992 7566 7571
10. A. Caflisch, and M. Karplus Acid and thermal denaturation of barnase investigated by molecular dynamics simulations J. Mol. Biol. 252 1995 672 708
11. P.L. Clark, Z.P. Liu, J. Zhang, and L.M. Gierasch Intrinsic tryptophans of CRABPI as probes of structure and folding Protein Sci. 5 1996 1108 1117
12. S.W. Cowan, M.E. Newcomer, and T.A. Jones Crystallographic studies on a family of cellular lipophilic transport proteins. Refinement of P2 myelin protein and the structure determination and refinement of cellular retinol-binding protein in complex with all-trans-retinol J. Mol. Biol. 230 1993 1225 1246
13. J.K. Davies, A.E. Thumser, and D.C. Wilton Binding of recombinant rat liver fatty acid-binding protein to small anionic phospholipid vesicles results in ligand release: a model for interfacial binding and fatty acid targeting Biochemistry 38 1999 16932 16940
14. C.M. Dobson, and A.R. Fersht Protein Folding 1996 Cambridge University Press Cambridge
15. M. Feig, and C.L. Brooks 3rd. Evaluating CASP4 predictions with physical energy functions Proteins 49 2002 232 245
16. S.C. Gill, and P.H. von Hippel Calculation of protein extinction coefficients from amino acid sequence data Anal. Biochem. 182 1989 319 326
17. Y. Goto, L.J. Calciano, and A.L. Fink Acid-induced folding of proteins Proc. Natl. Acad. Sci. USA 87 1990 573 577
18. L.H. Gutierrez Gonzalez, C. Ludwig, C. Hohoff, M. Rademacher, T. Hanhoff, H. Ruterjans, F. Spener, and C. Lucke Solution structure and backbone dynamics of human epidermal-type fatty acid-binding protein (E-FABP) Biochem. J. 364 2002 725 737
19. H.P. Hartung, J.D. Pollard, G.K. Harvey, and K.V. Toyka Immunopathogenesis and treatment of the Guillain-Barré syndrome-part I Muscle Nerve 18 1995 137 153
20. C. Hohoff, T. Borchers, B. Rustow, F. Spener, and H. van Tilbeurgh Expression, purification, and crystal structure determination of recombinant human epidermal-type fatty acid binding protein Biochemistry 38 1999 12229 12239
21. R.C. Hresko, R.D. Hoffman, J.R. Flores Riveros, and M.D. Lane Insulin receptor tyrosine kinase-catalyzed phosphorylation of 422(aP2) protein. Substrate activation by long-chain fatty acid J. Biol. Chem. 265 1990 21075 21085
22. W. Humphrey, A. Dalke, and K. Schulten VMD: visual molecular dynamics J. Mol. Graphics 14 1996 33 38
23. R.S. Jamison, B. Kakkad, D.H. Ebert, M.E. Newcomer, and D.E. Ong Test of the contribution of an amino-aromatic hydrogen bond to protein function Biochemistry 34 1995 11128 11132
24. W.C. Johnson Analyzing protein circular dichroism spectra for accurate secondary structures Proteins 35 1999 307 312
25. T.A. Jones, T. Bergfors, J. Sedzik, and T. Unge The three-dimensional structure of P2 myelin protein EMBO J. 7 1988 1597 1604
26. W. Kabsch, and C. Sander Dictionary of protein secondary structure: pattern recognition of hydrogen-bonded and geometrical features Biopolymers 22 1983 2577 2637
27. R. Koradi, M. Billeter, and K. Wuthrich MOLMOL: a program for display and analysis of macromolecular structures J. Mol. Graphics 14 1996 51 55
28. E. Krissinel, and K. Henrick Secondary-structure matching (SSM), a new tool for fast protein structure alignment in three dimensions Acta Crystallogr. D 60 1 2004 2256 2268
29. A. Li, and V. Daggett Identification and characterization of the unfolding transition state of chymotrypsin inhibitor 2 by molecular dynamics simulations J. Mol. Biol. 257 1996 412 429
30. V.A. Likic, and F.G. Prendergast Structure and dynamics of the fatty acid binding cavity in apo rat intestinal fatty acid binding protein Protein Sci. 8 1999 1649 1657
31. Z.P. Liu, J. Rizo, and L.M. Gierasch Equilibrium folding studies of cellular retinoic acid binding protein, a predominantly beta-sheet protein Biochemistry 33 1994 134 142
32. R.E. Martenson, and K. Uyemura Myelin P2, a neuritogenic member of the family of cytoplasmic lipid-binding proteins R.E. Martenson Myelin: Biology and Chemistry 1992 CRC Press Boca Raton, FL 509 528
33. S. McLaughlin The electrostatic properties of membranes Annu. Rev. Biophys. Biophys. Chem. 18 1989 113 136
34. S.U. Nielsen, and F. Spener Fatty acid-binding protein from rat heart is phosphorylated on Tyr19 in response to insulin stimulation J. Lipid Res. 34 1993 1355 1366
35. A. Perczel, M. Hollosi, G. Tusnady, and G.D. Fasman Convex constraint analysis: a natural deconvolution of circular dichroism curves of proteins Protein Eng. 4 1991 669 679
36. A. Perczel, K. Park, and G.D. Fasman Analysis of the circular dichroism spectrum of proteins using the convex constraint algorithm: a practical guide Anal. Biochem. 203 1992 83 93
37. J.W. Ponder, and F.M. Richards An efficient Newton-like method for molecular mechanics energy minimization of large molecules J. Comput. Chem. 8 1987 1016 1024
38. M. Prats, J. Teissie, and J.F. Tocanne Lateral proton conduction at lipid-water interfaces and its implications for the chemiosmotic-coupling hypothesis Nature 322 1986 756 758
39. D. Qiu, P.S. Shenkin, F.P. Hollinger, and W.C. Still The GB/SA continuum model for solvation. A fast analytical method for the calculation of approximate Born radii J. Phys. Chem. A 101 1997 3005 3014
40. P. Riccio, F. Zito, A. Fasano, G.M. Liuzzi, F. Lolli, E. Polverini, and P. Cavatorta Purification of bovine P2 myelin protein with bound lipids Neuroreport 9 1998 2769 2773
41. M.R. Rich, and J.S. Evans Molecular dynamics simulations of adipocyte lipid-binding protein: effect of electrostatics and acyl chain unsaturation Biochemistry 35 1996 1506 1515
42. G.V. Richieri, R.T. Ogata, A.W. Zimmerman, J.H. Veerkamp, and A.M. Kleinfeld Fatty acid binding proteins from different tissues show distinct patterns of fatty acid interactions Biochemistry 39 2000 7197 7204
43. J. Sedzik, T. Bergfors, T.A. Jones, and M. Weise Bovine P2 myelin basic protein crystallizes in three different forms J. Neurochem. 50 1988 1908 1913
44. J. Sedzik, G. Carlone, A. Fasano, G.M. Liuzzi, and P. Riccio Crystals of P2 myelin protein in lipid-bound form J. Struct. Biol. 142 2003 292 300
45. C.D. Snow, H. Nguyen, V.S. Pande, and M. Gruebele Absolute comparison of simulated and experimental protein-folding dynamics Nature 420 2002 102 106
46. N. Sreerama, and R.W. Woody A self-consistent method for the analysis of protein secondary structure from circular dichroism Anal. Biochem. 209 1993 32 44
47. N. Sreerama, and R.W. Woody Estimation of protein secondary structure from circular dichroism spectra: comparison of CONTIN, SELCON, and CDSSTR methods with an expanded reference set Anal. Biochem. 287 2000 252 260
48. N. Sreerama, and R.W. Woody Structural composition of betaI- and betaII-proteins Protein Sci. 12 2003 384 388
49. N. Sreerama, and R.W. Woody Computation and analysis of protein circular dichroism spectra Methods Enzymol. 383 2004 318 351
50. J. Storch, and A.E. Thumser The fatty acid transport function of fatty acid-binding proteins Biochim. Biophys. Acta 1486 2000 28 44
51. J. Thompson, J. Ory, A. Reese Wagoner, and L. Banaszak The liver fatty acid binding protein-comparison of cavity properties of intracellular lipid-binding proteins Mol. Cell. Biochem. 192 1999 9 16
52. B.D. Trapp, M. Dubois Dalcq, and R.H. Quarles Ultrastructural localization of P2 protein in actively myelinating rat Schwann cells J. Neurochem. 43 1984 944 948
53. K. Uyemura, C. Tobari, and S. Hirano Purifications and properties of basic proteins in pig spinal cord and peripheral nerve Biochim. Biophys. Acta 214 1970 190 197
54. F.G. van der Goot, J.M. Gonzalez Manas, J.H. Lakey, and F. Pattus A 'molten-globule' membrane-insertion intermediate of the pore-forming domain of colicinA Nature 354 1991 408 410
55. T.B. Woolf Simulations of fatty acid-binding proteins suggest sites important for function. I. Stearic acid Biophys. J. 74 1998 681 693
56. J. Wu, J.T. Yang, and C.S. Wu Beta-II conformation of all-beta proteins can be distinguished from unordered form by circular dichroism Anal. Biochem. 200 1992 359 364
57. X.F. Xia, and S.F. Sui The membrane insertion of trichosanthin is membrane-surface-pH dependent Biochem. J. 349 Pt. 3 2000 835 841
58. J.T. Yang, C.S. Wu, and H.M. Martinez Calculation of protein conformation from circular dichroism Methods Enzymol. 130 1986 208 269