The interaction of zinc with membrane-associated 18.5 kDa myelin basic protein: An attenuated total reflectance-Fourier transform infrared spectroscopic study

Amino Acids

Volumn 39, Issue 3, 2010, Pages 739-750

  Smith, Graham S T ^a   Chen, Lin ^a   Bamm, Vladimir V ^a   Dutcher, John R ^a   Harauz, George ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Attenuated total reflectance (ATR) spectroscopy; Circular dichroism (CD); Fourier transform infrared (FTIR) spectroscopy; Induced folding Isothermal titration calorimetry (ITC); Intrinsically disordered protein; Myelin basic protein (MBP)

Indexed keywords

MYELIN BASIC PROTEIN; ZINC; PROTEIN BINDING;

AQUEOUS SOLUTION; ARTICLE; CIRCULAR DICHROISM; CONTROLLED STUDY; DISSOCIATION CONSTANT; INFRARED SPECTROSCOPY; ISOTHERMAL TITRATION CALORIMETRY; MOUSE; NONHUMAN; PLASMID; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN INTERACTION; PROTEIN PURIFICATION; PROTEIN SECONDARY STRUCTURE; REVERSED PHASE HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; SITE DIRECTED MUTAGENESIS; ANIMAL; CELL MEMBRANE; CHEMISTRY; GENETICS; KINETICS; METABOLISM; MOLECULAR GENETICS; MOLECULAR WEIGHT;

ANIMALS; CELL MEMBRANE; KINETICS; MICE; MOLECULAR SEQUENCE DATA; MOLECULAR WEIGHT; MYELIN BASIC PROTEINS; PROTEIN BINDING; PROTEIN STRUCTURE, SECONDARY; SPECTROSCOPY, FOURIER TRANSFORM INFRARED; ZINC; MYELIN BASIC PROTEIN;

EID: 77956916946     PISSN: 09394451     EISSN: None     Source Type: Journal    
DOI: 10.1007/s00726-010-0513-7     Document Type: Article

References (70)

1. Ahmed MA, Bamm VV, Shi L, Steiner-Mosonyi M, Dawson JF, Brown L, Harauz G, Ladizhansky V (2009) Induced secondary structure and polymorphism in an intrinsically disordered structural linker of the CNS: solid-state NMR and FTIR spectroscopy of myelin basic protein bound to actin. Biophys J 96:180-191
2. Bailey RW, Dunker AK, Brown CJ, Garner EC, Griswold MD (2001) Clusterin, a binding protein with a molten globule-like region. Biochemistry 40:11828-11840
3. Bamm VV, Harauz G (2008) Expression and purification of the active variant of recombinant murine Golli-interacting protein (GIP)-characterization of its phosphatase activity and interaction with Golli-BG21. Protein Expr Purif 62:36-43
4. Baran C, Smith GS, Bamm VV, Harauz G, Lee JS (2010) Divalent cations induce a compaction of intrinsically disordered myelin basic protein. Biochem Biophys Res Commun 391:224-229
5. Barth A (2007) Infrared spectroscopy of proteins. Biochim Biophys Acta 1767:1073-1101
6. Bartlett G (1959) Phosphorus assay in column chromatography. J Biol Chem 234:466-468
7. Bates IR, Matharu P, Ishiyama N, Rochon D, Wood DD, Polverini E, Moscarello MA, Viner NJ, Harauz G (2000) Characterization of a recombinant murine 18.5-kDa myelin basic protein. Protein Expr Purif 20:285-299
8. Bates IR, Libich DS, Wood DD, Moscarello MA, Harauz G (2002) An Arg/Lys-> Gln mutant of recombinant murine myelin basic protein as a mimic of the deiminated form implicated in multiple sclerosis. Protein Expr Purif 25:330-341
9. Benfatto M, Della LS, Qin Y, Li Q, Pan G, Wu Z, Morante S (2004) The role of Zn in the interplay among Langmuir-Blodgett multilayer and myelin basic protein: a quantitative analysis of XANES spectra. Biophys Chem 110:191-201
10. Berlet HH, Ilzenhofer H, Gass P (1991) Restricted endogenous proteolysis of myelin basic protein of zinc-treated myelin. Acta Neurol (Napoli) 13:145-152
11. Berlet HH, Bischoff H, Weinhardt F (1994) Divalent metals of myelin and their differential binding by myelin basic protein of bovine central nervous system. Neurosci Lett 179:75-78
12. Boggs JM (2006) Myelin basic protein: a multifunctional protein. Cell Mol Life Sci 63:1945-1961
13. Boggs JM (2008) Myelin basic protein. Nova Science Publishers, Hauppauge
14. Boggs JM, Yip PM, Rangaraj G, Jo E (1997) Effect of posttransla-tional modifications to myelin basic protein on its ability to aggregate acidic lipid vesicles. Biochemistry 36:5065-5071
15. Byler DM, Susi H (1986) Examination of the secondary structure of proteins by deconvolved FTIR spectra. Biopolymers 25:469-487
16. Cabiaux V, Agerberth B, Johansson J, Homble F, Goormaghtigh E, Ruysschaert JM (1994) Secondary structure and membrane interaction of PR-39, a Pro + Arg-rich antibacterial peptide. Eur J Biochem 224:1019-1027
17. Carré JL, Goetz BD, O'Connor LT, Bremer Q, Duncan ID (2002) Mutations in the rat myelin basic protein gene are associated with specific alterations in other myelin gene expression. Neurosci Lett 330:17-20
18. Cavatorta P, Giovanelli S, Bobba A, Riccio P, Szabo AG, Quagliariello E (1994) Myelin basic protein interaction with zinc and phosphate: fluorescence studies on the water-soluble form of the protein. Biophys J 66:1174-1179
19. Earl C, Chantry A, Mohammad N, Glynn P (1988) Zinc ions stabilise the association of basic protein with brain myelin membranes. J Neurochem 51:718-724
20. Gatewood JM, Schroth GP, Schmid CW, Bradbury EM (1990) Zinc-induced secondary structure transitions in human sperm prota-mines. J Biol Chem 265:20667-20672
21. Goormaghtigh E, Gasper R, Benard A, Goldsztein A, Raussens V (2009) Protein secondary structure content in solution, films and tissues: redundancy and complementarity of the information content in circular dichroism, transmission and ATR FTIR spectra. Biochim Biophys Acta 1794:1332-1343
22. Harauz G, Libich DS (2009) The classic basic protein of myelin-conserved structural motifs and the dynamic molecular barcode involved in membrane adhesion and protein-protein interactions. Curr Protein Peptide Sci 10:196-215
23. Harauz G, Ishiyama N, Hill CMD, Bates IR, Libich DS, Farès C (2004) Myelin basic protein-diverse conformational states of an intrinsically unstructured protein and its roles in myelin assembly and multiple sclerosis. Micron 35:503-542
24. Harauz G, Ladizhansky V, Boggs JM (2009) Structural polymorphism and multifunctionality of myelin basic protein. Biochemistry 48:8094-8104
25. Haris PI, Chapman D (1995) The conformational analysis of peptides using Fourier transform IR spectroscopy. Biopolymers 37:251-263
26. Hill CMD, Haines JD, Antler CE, Bates IR, Libich DS, Harauz G (2003) Terminal deletion mutants of myelin basic protein: new insights into self-association and phospholipid interactions. Micron 34:25-37
27. Ho SY, Catalanotto FA, Lisak RP, Dore-Duffy P (1986) Zinc in multiple sclerosis II: Correlation with disease activity and elevated plasma membrane-bound zinc in erythrocytes from patients with multiple sclerosis. Ann Neurol 20:712-715
28. Inouye H, Kirschner DA (1984) Effects of ZnCl2 on membrane interactions in myelin of normal and shiverer mice. Biochim Biophys Acta 776:197-208
29. Inouye H, Kirschner DA (1988) Membrane interactions in nerve myelin: II. Determination of surface charge from biochemical data. Biophys J 53:247-260
30. Itoh M, Ebadi M, Swanson S (1983) The presence of zinc-binding proteins in brain. J Neurochem 41:823-829
31. Iyengar GV, Koomer WE, Bown HJM (1978) The elemental composition of human tissues and body fluids. Verlag-Chemie, New York
32. Jeganathan S, von Bergen M, Brutlach H, Steinhoff HJ, Mandelkow E (2006) Global hairpin folding of tau in solution. Biochemistry 45:2283-2293
33. Keen CL, Taubeneck MW, Daston GP, Rogers JM, Gershwin ME (1993) Primary and secondary zinc deficiency as factors underlying abnormal CNS development. Ann N Y Acad Sci 678:37-47
34. Kim JK, Mastronardi FG, Wood DD, Lubman DM, Zand R, Moscarello MA (2003) Multiple sclerosis: an important role for post-translational modifications of myelin basic protein in pathogenesis. Mol Cell Proteomics 2:453-462
35. Koh JY (2001) Zinc and disease of the brain. Mol Neurobiol 24:99-106
36. Laird DJ, Mulvihill MM, Lillig JA (2009) Membrane-induced peptide structural changes monitored by infrared and circular dichroism spectroscopy. Biophys Chem 145:72-78
37. Libich DS, Harauz G (2008a) Backbone dynamics of the 18.5 kDa isoform of myelin basic protein reveals transient α-helices and a calmodulin-binding site. Biophys J 94:4847-4866
38. Libich DS, Harauz G (2008b) Solution NMR and CD spectroscopy of an intrinsically disordered, peripheral membrane protein: evaluation of aqueous and membrane-mimetic solvent conditions for studying the conformational adaptability of the 18.5 kDa isoform of myelin basic protein (MBP). Eur Biophys J 37:1015-1029
39. Libich DS, Robertson VJ, Monette MM, Harauz G (2004) Backbone resonance assignments of the 18.5 kDa isoform of murine myelin basic protein (MBP). J Biomol NMR 29:545-546
40. Libich DS, Ahmed MAM, Zhong L, Bamm VV, Ladizhansky V, Harauz G (2010) Fuzzy complexes of myelin basic protein-NMR spectroscopic investigations of a polymorphic organizational linker of the central nervous system. Biochem Cell Biol (Special issue on Protein Folding: Principles and Diseases). doi: 10.1139/O09-123
41. Majava V, Petoukhov MV, Hayashi N, Pirila P, Svergun DI, Kursula P (2008) Interaction between the C-terminal region of human myelin basic protein and calmodulin: analysis of complex formation and solution structure. BMC Struct Biol 8:10
42. Majava V, Wang C, Myllykoski M, Kangas SM, Kang SU, Hayashi K, Baumgärtel P, Heape AM, Lubec G, Kursula P (2009) Structural analysis of the complex between calmodulin and full-length myelin basic protein, an intrinsically disordered molecule. Amino Acids. doi:10.1007/s00726-009-0364-2
43. Mittag T, Kay LE, Forman-Kay JD (2009) Protein dynamics and conformational disorder in molecular recognition. J Mol Recognit 23:105-116
44. Mo ZY, Zhu YZ, Zhu HL, Fan JB, Chen J, Liang Y (2009) Low micromolar zinc accelerates the fibrillization of human Tau via bridging Cys291 and Cys322. J Biol Chem 284:34648-34657
45. Morante S (2001) The zinc environment in Langmuir-Blodgett phospholipid multi-layers. J Synchrotron Radiat 8:975-977
46. Moscarello MA, Murdoch D, Wood DD (1968) The effect of metals on the binding of 131-I-labelled acid-soluble protein to myelin in vitro. Can J Biochem 46:235-240
47. Mukrasch MD, Bibow S, Korukottu J, Jeganathan S, Biernat J, Griesinger C, Mandelkow E, Zweckstetter M (2009) Structural polymorphism of 441-residue tau at single residue resolution. PLoS Biol 7:e34
48. Musse AA, Boggs JM, Harauz G (2006) Deimination of membrane-bound myelin basic protein in multiple sclerosis exposes an immunodominant epitope. Proc Natl Acad Sci USA 103:4422-4427
49. Nabet A, Boggs JM, Pezolet M (1994) Study by infrared spectroscopy of the interaction of bovine myelin basic protein with phospha-tidic acid. Biochemistry 33:14792-14799
50. Nuzzo S, Meneghini C, Mobilioo S, Haas H, Riccio P, Fasano A, Cavatorta P, Morante S (2002) An x-ray absorption spectroscopy study of the zinc environment in Langmuir-Blodgett phospho-lipid multilayers. Biophys J 83:3507-3512 (Pubitemid 36041967)
51. Permyakov SE, Oberg KA, Cherskaya AM, Shavlovsky MM, Permyakov EA, Uversky VN (2002) Human alpha-fetoprotein as a Zn(2 +)-binding protein. Tight cation binding is not accompanied by global changes in protein structure and stability. Biochim Biophys Acta 1586:1-10
52. Polverini E, Fasano A, Zito F, Riccio P, Cavatorta P (1999) Conformation of bovine myelin basic protein purified with bound lipids. Eur Biophys J 28:351-355
53. Readhead C, Hood L (1990) The dysmyelinating mouse mutations shiverer (shi) and myelin deficient (shimld). Behav Genet 20:213-234
54. Riccio P, Giovannelli S, Bobba A, Romito E, Fasano A, Bleve-Zacheo T, Favilla R, Quagliariello E, Cavatorta P (1995) Specificity of zinc binding to myelin basic protein. Neurochem Res 20:1107-1113
55. Saeidian S, Saboury AA, Sanati H, Moosavi-Movahedi AA (2001) Thermodynamics of binding zinc ion on myelin basic protein (Meeting Poster Abstract). Biophys J 79(Supplement)
56. Sandstead HH, Frederickson CJ, Penland JG (2000) History of zinc as related to brain function. J Nutr 130:496S-502S
57. Stuart BH (1996) A Fourier transform infrared spectroscopic study of the secondary structure of myelin basic protein in reconstituted myelin. Biochem Mol Biol Int 38:839-845
58. Surewicz WK, Moscarello MA, Mantsch HH (1987) Fourier transform infrared spectroscopic investigation of the interaction between myelin basic protein and dimyristoylphosphatidylgly-cerol bilayers. Biochemistry 26:3881-3886
59. Susi H, Timasheff SN, Stevens L (1967) Infrared spectra and protein conformations in aqueous solutions. I. The amide I band in H2O and D2O solutions. J Biol Chem 242:5460-5466
60. Takeda A (2001) Zinc homeostasis and functions of zinc in the brain. Biometals 14:343-351
61. Tompa P, Fuxreiter M (2008) Fuzzy complexes: polymorphism and structural disorder in protein-protein interactions. Trends Biochem Sci 33:2-8
62. Tsang D, Tsang YS, Ho WK, Wong RN (1997) Myelin basic protein is a zinc-binding protein in brain: possible role in myelin compaction. Neurochem Res 22:811-819
63. Unal B, Tan H, Orbak Z, Kiki I, Bilici M, Bilici N, Aslan H, Kaplan S (2005) Morphological alterations produced by zinc deficiency in rat sciatic nerve: a histological, electron microscopic, and stereological study. Brain Res 1048:228-234
64. Uversky VN (2009) Intrinsically disordered proteins and their environment: effects of strong denaturants, temperature, pH, counter ions, membranes, binding partners, osmolytes, and macromolecular crowding. Protein J 28:305-325
65. Uversky VN, Gillespie JR, Millett IS, Khodyakova AV, Vasilenko RN, Vasiliev AM, Rodionov IL, Kozlovskaya GD, Dolgikh DA, Fink AL, Doniach S, Permyakov EA, Abramov VM (2000) Zn(2+)-mediated structure formation and compaction of the ''natively unfolded'' human prothymosin alpha. Biochem Biophys Res Commun 267:663-668
66. Uversky VN, Permyakov SE, Zagranichny VE, Rodionov IL, Fink AL, Cherskaya AM, Wasserman LA, Permyakov EA (2002) Effect of zinc and temperature on the conformation of the gamma subunit of retinal phosphodiesterase: a natively unfolded protein. J Proteome Res 1:149-159
67. Velazquez-Campoy A, Leavitt SA, Freire E (2004) Characterization of protein-protein interactions by isothermal titration calorime-try. Methods Mol Biol 261:35-54
68. von Bergen M, Barghorn S, Jeganathan S, Mandelkow EM, Mandelkow E (2006) Spectroscopic approaches to the conformation of tau protein in solution and in paired helical filaments. Neurodegener Dis 3:197-206
69. Wiseman T, Williston S, Brandts JF, Lin LN (1989) Rapid measurement of binding constants and heats of binding using a new titration calorimeter. Anal Biochem 179:131-137
70. Zhong L, Bamm VV, Ahmed MA, Harauz G, Ladizhansky V (2007) Solid-state NMR spectroscopy of 18.5 kDa myelin basic protein reconstituted with lipid vesicles: spectroscopic characterisation and spectral assignments of solvent-exposed protein fragments. Biochim Biophys Acta (Biomembranes) 1768:3193-3205