Interactions of the 18.5-kDa isoform of myelin basic protein with ca2+-calmodulin: In vitro studies using fluorescence microscopy and spectroscopy

Biochemistry and Cell Biology

Volumn 80, Issue 4, 2002, Pages 395-406

  Libich, David S ^a   Harauz, George ^a  

^a UNIVERSITY OF GUELPH   (Canada)

Author keywords

Ca2+ calmodulin; Cathepsin D; Intrinsic Trp fluorescence; MARCKS; Myelin basic protein

Indexed keywords

DISSOCIATION; FLUORESCENCE; PROTEINS; SPECTROSCOPY; SUBSTRATES;

SIGNAL TRANSDUCTION;

BIOCHEMISTRY;

ALANINE; CALCIUM ION; CALMODULIN DERIVATIVE; CATHEPSIN D; HISTIDINE DERIVATIVE; MYELIN BASIC PROTEIN; PROTEIN KINASE C; SODIUM CHLORIDE; UREA;

ARTICLE; BEHAVIOR; CARBOXY TERMINAL SEQUENCE; CATTLE; DISSOCIATION CONSTANT; FLUORESCENCE MICROSCOPY; IN VITRO STUDY; PROTEIN BINDING; PROTEIN INTERACTION; SIGNAL TRANSDUCTION; SPECTROSCOPY;

BOS TAURUS; BOVINAE; MURINAE;

EID: 0036436095     PISSN: 08298211     EISSN: None     Source Type: Journal    
DOI: 10.1139/o02-020     Document Type: Article

References (80)

1. Arbuzova, A., Murray, D., and McLaughlin, S. 1998. MARCKS, membranes, and calmodulin: kinetics of their interaction. Biochim. Biophys. Acta, 1376: 369-379.
2. Babu, Y.S., Bugg, C.E., and Cook, W.J. 1988. Structure of calmodulin refined at 2.2 Å resolution. J. Mol. Biol. 204: 191-204.
3. 2+-calmodulin-modulated regulation of F-actin - Myelin basic protein interaction. Eur. J. Cell Biol. 35: 327-335.
4. Bates, I.R., Matharu, P., Ishiyama, N., Rochon, D., Wood, D.D., Polverini, E., Moscarello, M.A., Viner, N.J., and Harauz, G. 2000. Characterization of a recombinant murine 18.5 kDa myelin basic protein. Protein Expression Purif. 20: 285-299.
5. Beniac, D.R., Luckevich, M.D., Czarnota, G.J., Tompkins, T.A., Ridsdale, R.A., Ottensmeyer, F.P., Moscarello, M.A., and Harauz, G. 1997. Three-dimensional structure of myelin basic protein. I. Reconstruction via angular reconstitution of randomly oriented single particles. J. Biol. Chem. 272: 4261-4268.
6. Beniac, D.R., Wood, D.D., Palaniyar, P., Ottensmeyer, F.P., Moscarello, M.A., and Harauz, G. 2000. Cryoelectron microscopy of protein-lipid complexes of human myelin basic protein charge isomers differing in degree of citrullination. J. Struct. Biol. 129: 80-95.
7. Boggs, J.M., and Rangaraj, G. 2000. Interaction of lipid-bound myelin basic protein with actin filaments and calmodulin. Biochemistry, 39: 7799-7806.
8. Campagnoni, A.T., and Magno, C.S. 1974. Molecular weight estimation of mouse and guinea-pig myelin basic proteins by polyacrylamide gel electrophoresis in the presence of sodium dodecyl sulphate: influence of ionic strength. J. Neurochem. 23: 887-890.
9. Campagnoni, A.T., and Skoff, R.P. 2001. The pathobiology of myelin mutants reveal novel biological functions of the MBP and PLP genes. Brain Pathol. 11: 74-91.
10. Cavatorta, P., Masotti, L., Szabo, A.G., Juretic, D., Riccio, P., and Quagliariello, E. 1988. Fluorescence spectral resolution of myelin basic protein conformers in complexes with lysophosph-atidylcholine. Cell Biophys. 13: 201-215.
11. Cavatorta, P., Giovanelli, S., Bobba, A., Riccio, P., Szabo, A.G., and 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.
12. Chan, K.-F.J., Robb, N.D., and Chen, W.H. 1990. Myelin basic protein: Interaction with calmodulin and gangliosides. J. Neurosci. Res. 25: 535-544.
13. Cicchetti, G., Maurer, P., Wagener, P., and Kocks, C. 1999. Actin and phosphoinositide binding by the ActA protein of the bacterial pathogen Listeria monocytogenes. J. Biol. Chem. 274: 33 616 - 33 626.
14. Cuzner, M.L., and Davison, A.N. 1973. Changes in cerebral lysosomal enzyme activity and lipids in multiple sclerosis. J. Neurol. Sci. 19: 29-36.
15. Dobrowolski, Z., Baryłko, B., and Drabikowski, W. 1986a. Interaction of tropomyosin with myelin basic protein and its effect on the ATPase activity of actomyosin. Eur. J. Cell Biol. 41: 65-71.
16. Dobrowolski, Z., Osinska, H., Mossakowska, M., and Baryłko, B. 1986b. Ca(2+)-calmodulin-dependent polymerization of actin by myelin basic protein. Eur. J. Cell Biol. 42: 17-26.
17. 3H] Verapamil radioligand-binding assay. J. Pharmacol. Exp. Ther. 288: 348-357.
18. Dyer, C.A. 1997. Myelin proteins as mediators of signal transduction. In Cell Biology and Pathology of Myelin: Evolving Biological Concepts and Therapeutic Approaches. Edited by B.H.J. Juurlink, R.M. Devon, J.R. Doucette, A.J. Nazarali, D.J. Schreyer, and V.M.K. Verge. Plenum Press, New York. pp. 69-74.
19. Dyer, C.A., Philibotte, T.M., Billings-Gagliardi, S., and Wolf, M.K. 1995. Cytoskeleton in myelin-basic-protein-deficient shiverer oligodendrocytes. Dev. Neurosci. 17: 53-62.
20. Dyer, C.A., Phillbotte, T., Wolf, M.K., and Billings-Gagliardi, S. 1997. Regulation of cytoskeleton by myelin components: Studies on shiverer oligodendrocytes carrying an Mbp transgene. Dev. Neurosci. 19: 395-409.
21. Givogri, M.I., Bongarzone, E.R., and Campagnoni, A.T. 2000. New insights on the biology of myelin basic protein gene: the neural-immune connection. J. Neurosci. Res. 59: 153-159.
22. Gomes, A.V., Barnes, J.A., and Vogel, H.J. 2000. Spectroscopic characterization of the interaction between calmodulin-dependent protein kinase I and calmodulin. Arch. Biochem. Biophys. 379: 28-36.
23. Grand, R.J.A., and Perry, S.V. 1980. The binding of calmodulin to myelin basic protein and histone H2B. Biochem. J. 189: 227-240.
24. Han, B.-G., Nunomuram, W., Takakuwa, Y., Mohandas, N., and Jap, B.K. 2000. Protein 4.1R core domain structure and insights into regulation of cytoskeletal organization. Nat. Struct. Biol. 7: 871-875.
25. Harauz, G., Ishiyama, N., and Bates, I.R. 2000. Analogous structural motifs in myelin basic protein and in MARCKS. Mol. Cell. Biochem. 209: 155-163.
26. Ishiyama, N., Bates, I.R., Hill, C.M., Wood, D.D., Matharu, P., Viner, N.J., Moscarello, M.A., and Harauz, G. 2001. The effects of deimination of myelin basic protein on structures formed by its interaction with phosphoinositide-containing lipid monolayers. J. Struct. Biol. 136: 30-45.
27. Itano, T., Itano, R., and Penniston, R.J. 1980. Interactions of basic polypeptides and proteins with calmodulin. Biochem. J. 189: 455-459.
28. Iwasa, Y., Iwasa, T., Matsui, K., Higashi, K., and Miyamoto, E. 1981. Interaction of calmodulin with chromatin associated proteins and myelin basic protein. Life Sci. 29: 1369-1377.
29. Jones, A.J., and Rumsby, M.G. 1975. The intrinsic fluorescence characteristics of the myelin basic protein. J. Neurochem. 25: 565-572.
30. Karthigasan, J., Inouye, H., and Kirschner, D.A. 1995. Implications of the sequence similarities between tau and myelin basic protein. Med. Hypotheses, 45: 235-240.
31. Kataoka, M., Head, J.F., Seaton, B.F., and Engelman, D.M. 1989. Melittin binding causes a large calcium-dependent conformational change in calmodulin. Proc. Natl. Acad. Sci. U.S.A. 86: 6944-6948.
32. Kursula, P. 2001. The current status of structural studies on proteins of the myelin sheath (review). Int. J. Mol. Med. 8: 475-479.
33. Lakowicz, J.R. 1999. Principles of Fluorescence Spectroscopy. 2nd Ed. Kluwer Academic Publishers, New York.
34. Lakowicz, J.R., Gryczynski, I., Laczko, G., Wiczk, W., and Johnson, M.L. 1994. Distribution of distances between the tryptophan and the N-terminal residue of melittin in its complex with calmodulin, troponin C, and phospholipids. Protein Sci. 3: 628-637.
35. Laws, W.R., and Contino, P.B. 1992. Fluorescence quenching studies: Analysis of nonlinear Stern-Volmer data. Methods Enzymol. 210: 448-463.
36. Li, Y., Li, H., Dimasi, N., McCormick, J.K., Martin, R., Schuck, P., Schlievert, P.M., and Mariuzza, R.A. 2001. Crystal structure of a superantigen bound to the high-affinity, zinc-dependent site on MHC class II. Immunity, 14: 93-104.
37. Lintner, R.N., and Dyer, C.A. 2000. Redistribution of cholesterol in oligodendrocyte membrane sheets after activation of distinct signal transduction pathways. J. Neurosci. Res. 60: 437-449.
38. Liu, R., and Sharom, F.J. 1996. Site-directed fluorescence labeling of P-glycoprotein on cysteine residues in the nucleotide domains. Biochemistry, 35: 11 865 - 11 873.
39. Liu, R., Siemiarczuk, A., and Sharom, F.J. 2000. Intrinsic fluorescence of the P-glycoprotein multidrug transporter: sensitivity of tryptophan residues to binding of drugs and nucleotides. Biochemistry, 39: 14 927 - 14 938.
40. 2+. J. Biol. Chem. 272: 23 050 - 23 056.
41. Mendz, G.L., Brown, L.R., and Martenson, R.E. 1990. Interactions of myelin basic protein with mixed dodecylphosphocholine/palmitoyllysophosphatidic acid micelles. Biochemistry, 29: 2304-2311.
42. Mendz, G.L., Miller, D.J., and Ralston, G.B. 1995. Interactions of myelin basic protein with palmitoyllysophosphatidylcholine: Characterization of the complexes and conformations of the protein. Eur. Biophys. J. 24: 39-53.
43. Modesti, N.M., and Barra, H.S. 1986. The interaction of myelin basic protein with tubulin and the inhibition of tubulin carboxypeptidase activity. Biochem. Biophys. Res. Commun. 136: 482-489.
44. Moscarello, M.A. 1997. Myelin basic protein, the "executive" molecule of the myelin membrane. In Cell Biology and Pathology of Myelin: Evolving Biological Concepts and Therapeutic Approaches. Edited by B.H.J. Juurlink, R.M. Devon, J.R. Doucette, A.J. Nazarali, D.J. Schreyer, and V.M.K. Verge. Plenum Press, New York. pp. 13-25.
45. Noonan, D.J., Lou, D., Griffith, N., and Vanaman, T.C. 2002. A calmodulin binding site in the tuberous sclerosis 2 gene product is essential for regulation of transcription events and is altered by mutations linked to tuberous sclerosis and lymphangioleiomyomatosis. Arch. Biochem. Biophys. 398: 132-140.
46. Nowak, M.W., and Berman, H.A. 1991. Fluorescence studies on the interactions of myelin basic protein in electrolyte solutions. Biochemistry, 30: 7642-7651.
47. Olwin, B.B., and Storm, D.R. 1985. Calcium binding to complexes of calmodulin and calmodulin binding proteins. Biochemistry, 24: 8081-8086.
48. 2+-calmodulin-dependent kinase kinase. Nat. Struct. Biol. 6: 819-824.
49. Pedraza, L., Fidler, L., Staugaitis, S.M., and Colman, D.R. 1997. The active transport of myelin basic protein into the nucleus suggests a regulatory role in myelination. Neuron, 18: 579-589.
50. Pirollet, F., Derancourt, J., Haiech, J., Job, D., and Margolis, R.L. 1992. Ca(2+)-calmodulin regulated effectors of microtubule stability in bovine brain. Biochemistry, 31: 8849-8855.
51. Polverini, E., Fasano, A., Zito, F., Riccio, P., and Cavatorta, P. 1999. Conformation of bovine myelin basic protein purified with bound lipids. Eur. Biophys. J. 28: 351-355.
52. Prasad, K., Barouch, W., Martin, B.M., Greene, L.E., and Eisenberg, E. 1995. Purification of a new clathrin assembly protein from bovine brain and its identification as myelin basic protein. J. Biol. Chem. 270: 30 551 - 30 556.
53. Pritzker, L.B., Joshi, S., Gowan, J.J., Harauz, G., and Moscarello, M.A. 2000a. The effect of deimination of arginyl residues of myelin basic protein on its structure and susceptibility to digestion by cathepsin D. Biochemistry, 39: 5374-5381.
54. Pritzker, L.B., Joshi, S., Harauz, G., and Moscarello, M.A. 2000b. Effect of methylation of MBP on its deimination by peptidyl arginine deiminase. Biochemistry, 39: 5382-5388.
55. Rasmussen, C., and Garen, C. 1993. Activation of calmodulin-dependent enzymes can be selectively inhibited by histone H1. J. Biol. Chem. 268: 23 788 - 23 791.
56. Rhoads, A.R., and Friedberg, F. 1997. Sequence motifs for calmodulin recognition. FASEB J. 11: 331-340.
57. Ridsdale, R.A., Beniac, D.R., Tompkins, T.A., Moscarello, M.A., and Harauz, G. 1997. Three-dimensional structure of myelin basic protein. II. Molecular modelling and considerations of predicted structures in multiple sclerosis. J. Biol. Chem. 272: 4269-4275.
58. Roth, G.A., Gonzalez, M.D., Monferran, C.G., DeSantis, M.L., and Cumar, F.A. 1993. Myelin basic protein domains involved in the interaction with actin. Neurochem. Int. 23: 459-465.
59. Samsó, M., Daban, J.-R., Hansen, S., and Jones, G.R. 1995. Evidence for sodium dodecyl sulfate/protein complexes adopting a necklace structure. Eur. J. Biochem. 232: 818-824.
60. Schagger, H., and von Jagow, G. 1987. Tricine - Sodium dodecyl sulfate - Polyacrylamide gel electrophoresis for the separation of proteins in the range from 1 to 100 kDa. Anal. Biochem. 166: 368-379.
61. Schleiff, E., Schmitz, A., McIlhinney, R.A.J., Manenti, S., and Vergères, G. 1996. Myristoylation does not modulate the properties of MARCKS-related protein (MRP) in solution. J. Biol. Chem. 271: 26 794 - 26 802.
62. 2+/calmodulin. Nature (Lond.), 410: 1120-1124.
63. Sedzik, J., and Kirschner, D.A. 1992. Is myelin basic protein crystallizable? Neurochem. Res. 17: 157-166.
64. Smith, R. 1985. The encephalitogenic protein of myelin forms hexamers in which the polypeptides have a pleated-sheet structure. FEBS Lett. 183: 331-334.
65. Smith, R. 1992. The basic protein of CNS myelin: Its structure and ligand binding. J. Neurochem. 59: 1589-1608.
66. Smith, K.R., Pyrdol, J., Gauthier, L., Wiley, D.C., and Wucherpfennig, K.W. 1998. Crystal structure of HLA-DR2 (DRA *0101, DRB1*1501) complexed with a peptide from human myelin basic protein. J. Exp. Med. 188: 1511-1520.
67. Staugaitis, S.M., Colman, D.R., and Pedraza, L. 1996. Membrane adhesion and other functions for the myelin basic proteins. BioEssays, 18: 13-18.
68. Tompkins, T.A., and Moscarello, M.A. 1994. The mechanism of stimulation of brain phospholipase C-alpha by myelin basic protein involves specific interactions. Biochim. Biophys. Acta, 1206: 208-214.
69. Ulrich, A., Schmitz, A.A.P., Braun, T., Yuan, T., Vogel, H.J., and Vergères, G. 2000. Mapping the interface between calmodulin and MARCKS-related protein by fluorescence spectroscopy. Proc. Natl. Acad. Sci. U.S.A. 97: 5191-5196.
70. Uversky, V.N., Gillespie, J.R., and Fink, A.L. 2000. Why are "natively unfolded" proteins unstructured under physiologic conditions? Proteins: Struct. Funct. Gen. 41: 415-427.
71. Whitaker, J.N., and Seyer, J.M. 1981. The influence of pH on the degradation of bovine myelin basic protein by bovine brain cathepsin D. Biochim. Biophys. Acta, 661: 334-341.
72. Wood, D.D., and Moscarello, M.A. 1997. Molecular biology of the glia: Components of myelin - Myelin basic protein - The implication of post-translational changes for demyelinating disease. In The molecular biology of multiple sclerosis. Edited by W. Russell. Wiley, New York. pp. 37-54.
73. Wood, D.D., Bilbao, J.M., O'Connors, P., and Moscarello, M.A. 1996. Acute multiple sclerosis (Marburg type) is associated with extensive modifications of myelin basic protein. Ann. Neurol. 40: 18-24.
74. Wright, P.E., and Dyson, H.J. 1999. Intrinsically unstructured proteins: re-assessing the protein structure-function paradigm. J. Mol. Biol. 293: 321-331.
75. Yap, K.L., Kim, J., Truong, K., Sherman, M., Yuan, T., and Ikura, M. 2000. Calmodulin target database. J. Struct. Funct. Genomics, 1: 8-14.
76. Yuan, T., Mietzner, T.A., Montelaro, R.C., and Vogel, H.J. 1995. Characterization of the calmodulin binding domain of SIV transmembrane glycoprotein by NMR and CD spectroscopy. Biochemistry, 34: 10 690 - 10 696.
77. Zand, R., Li, M.X., Jin, X., and Lubman, D. 1998. Determination of the sites of posttranslational modifications in the charge isomers of bovine myelin basic protein by capillary electrophoresis - Mass spectroscopy. Biochemistry, 24: 2441-2449.
78. Zhan, Q., Wong, S.S., and Wang, C.-L.A. 1991. A calmodulinbinding peptide of caldesmon. J. Biol. Chem. 266: 21 810 - 21 814.
79. Zhang, M., Tanaka, T., and Ikura, M. 1995. Calcium-induced conformational transition revealed by the solution structure of apo calmodulin. Nat. Struct. Biol. 2: 758-767.
80. Zuiderweg, E.R.P. 2002. Mapping protein-protein interactions in solution by NMR spectroscopy. Biochemistry, 41: 1-7.