Effect of phosphorylation of phosphatidylinositol on myelin basic protein-mediated binding of actin filaments to lipid bilayers in vitro

Biochimica et Biophysica Acta - Biomembranes

Volumn 1818, Issue 9, 2012, Pages 2217-2227

  Boggs, Joan M ^a,b   Rangaraj, Godha ^a   Dicko, Awa ^c  

^a HOSPITAL FOR SICK CHILDREN RESEARCH INSTITUTE   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c Celator Pharmaceuticals Corp   (Canada)

Author keywords

Calmodulin; Cytoskeleton; Lipid vesicle; Oligodendrocyte; Phosphoinositide; Signal transduction

Indexed keywords

ACTIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE; INOSITOL; MYELIN; MYELIN BASIC PROTEIN; PHOSPHATIDYLCHOLINE; PHOSPHATIDYLGLYCEROL; PHOSPHATIDYLINOSITOL; PHOSPHATIDYLINOSITOL 4 PHOSPHATE; PHOSPHATIDYLINOSITOL 4,5 BISPHOSPHATE; SCAFFOLD PROTEIN;

ACTIN FILAMENT; ARTICLE; CONTROLLED STUDY; DISSOCIATION; ENZYME ACTIVITY; IN VITRO STUDY; LIPID BILAYER; LIPID COMPOSITION; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LIPID INTERACTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION;

ACTIN CYTOSKELETON; ACTINS; ANIMALS; CALCIUM; CALMODULIN; CATTLE; CENTRIFUGATION, DENSITY GRADIENT; CYTOSOL; HUMANS; LIPID BILAYERS; LIPIDS; MYELIN BASIC PROTEIN; MYELIN SHEATH; PHOSPHATIDYLINOSITOL PHOSPHATES; PHOSPHATIDYLINOSITOLS; PHOSPHORYLATION; PROTEIN BINDING; SIGNAL TRANSDUCTION; SWINE;

EID: 84861830755     PISSN: 00052736     EISSN: 18792642     Source Type: Journal    
DOI: 10.1016/j.bbamem.2012.04.006     Document Type: Article

References (67)

1. J.M. Boggs, M.A. Moscarello, D. Papahadjopoulos, in: P. Jost, O.H. Griffith (Eds.), Structural Organization of Myelin. Role of Lipid-Protein Interactions Determined in Model Systems, Lipid-protein interactions, vol. 2, John Wiley and Sons, New York, 1982, pp. 1-51.
2. F.X. Omlin, H.D. Webster, C.G. Palkovits, S.R. Cohen, Immunocytochemical localization of basic protein in major dense line regions of central and peripheral myelin, J. Cell Biol. 95 (1982) 242-248. (Pubitemid 13197094)
3. C. Readhead, N. Takasashi, H.D. Shine, R. Saavedra, R. Sidman, L. Hood, Role of myelin basic protein in the formation of central nervous system myelin, Ann. N. Y. Acad. Sci. 605 (1990) 280-285.
4. J.M. Boggs, Myelin basic protein: a multifunctional protein, Cell. Mol. Life Sci. 63 (2006) 1945-1961. (Pubitemid 44359737)
5. J.M. Boggs, Myelin basic protein interactions with actin and tubulin in vitro: binding, assembly, and regulation, in: J.M. Boggs (Ed.), Myelin Basic Protein, Intrinsically Disordered Proteins, Nova Science Publishers, New York, 2008, pp. 149-167.
6. G. Harauz, V. Ladizhansky, J.M. Boggs, Structural polymorphism and multifunctionality of myelin basic protein, Biochemistry 48 (2009) 8094-8104.
7. G. Harauz, N. Ishiyama, C.M.D. Hill, I.R. Bates, D.S. Libich, C. Farès, Myelin basic protein - diverse conformational states of an intrinsically unstructured protein and its roles in myelin assembly and multiple sclerosis, Micron 35 (2004) 503-542. (Pubitemid 38836830)
8. J. Karthigasan, B. Kosaras, J. Nguyen, D.A. Kirschner, Protein and lipid composition of radial component-enriched CNS myelin, J. Neurochem. 62 (1994) 1203-1213. (Pubitemid 24064537)
9. E. Polverini, G. Rangaraj, D.S. Libich, J.M. Boggs, G. Harauz, Binding of the prolinerich segment of myelin basic protein to SH3-domains - spectroscopic, microarray, andmodelling studies of ligand conformation and effects of post-translationalmodifications, Biochemistry 47 (2008) 267-282.
10. 2+-calmodulin-dependent regulation of F-actin- myelin basic protein interaction, Eur. J. Cell Biol. 35 (1984) 327-335.
11. 2+-calmodulindependent polymerization of actin by myelin basic protein, Eur. J. Cell Biol. 42 (1986) 17-26.
12. C.M.D. Hill, G. Harauz, Charge effects modulate actin assembly by classic myelin basic protein isoforms, Biochem. Biophys. Res. Commun. 329 (2005) 362-369. (Pubitemid 40255462)
13. M.A.M. Ahmed, V.V. Bamm, L. Shi, M. Steiner-Mosonyi, J.F. Dawson, L. Brown, G. Harauz, V. Ladizhansky, 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 (2009) 180-191.
14. V.V. Bamm, M.A. Ahmed, G. Harauz, Interaction of myelin basic protein with actin in the presence of dodecylphosphocholine micelles, Biochemistry 49 (2010) 6903-6915.
15. J.M. Boggs, G. Rangaraj, Interaction of lipid-bound myelin basic protein with actin filaments and calmodulin, Biochemistry 39 (2000) 7799-7806. (Pubitemid 30439608)
16. J.M. Boggs, G. Rangaraj, C.M.D. Hill, I.R. Bates, Y.M. Heng, G. Harauz, Effect of arginine loss in myelin basic protein, as occurs in its deiminated charge isoform, on mediation of actin polymerization and actin binding to a lipid membrane in vitro, Biochemistry 44 (2005) 3524-3534. (Pubitemid 40322022)
17. J.M. Boggs, G. Rangaraj, W. Gao, Y.M. Heng, Effect of phosphorylation of myelin basic protein by MAPK on its interactions with actin and actin binding to a lipid membrane in vitro, Biochemistry 45 (2006) 391-401. (Pubitemid 43100406)
18. J.M. Boggs, G. Rangaraj, Y.-M. Heng, Y. Liu, G. Harauz, Myelin basic protein binds microtubules to a membrane surface and to actin filaments in vitro: effect of phosphorylation and deimination, Biochim. Biophys. Acta Biomembr. 1808 (2011) 761-773.
19. L. Homchaudhuri, E. Polverini, W. Gao, G. Harauz, J.M. Boggs, Influence of membrane surface charge and post-translational modifications to myelin basic protein on its ability to tether the Fyn-SH3 domain to a membrane in vitro, Biochemistry 48 (2009) 2385-2393.
20. C.A. Dyer, T.M. Philibotte, M.K. Wolf, S. Billings-Gagliardi, Myelin basic protein mediates extracellular signals that regulate microtubule stability in oligodendrocyte membrane sheets, J. Neurosci. Res. 39 (1994) 97-107. (Pubitemid 24286539)
21. J.M. Boggs, W. Gao, Y. Hirahara, Myelin glycosphingolipids, galactosylceramide and sulfatide, participate in carbohydrate-carbohydrate interactions between apposed membranes and may form glycosynapses between oligodendrocyte and/or myelin membranes, Biochim. Biophys. Acta 1780 (2008) 445-455.
22. G.S.T. Smith, L. Homchaudhuri, J.M. Boggs, G. Harauz, Classic 18.5- and 21.5-kDa myelin basic protein isoforms associate with cytoskeletal and SH3-domain proteins in the immortalized N19-oligodendroglial cell line stimulated by phorbol ester and IGF-1, Neurochem. Res. (2012), http://dx.doi.org/10.1007/s11064-011-0700-2.
23. R.J.A. Grand, S.V. Perry, The binding of calmodulin to myelin basic protein and histone H2B, Biochem. J. 189 (1980) 227-240.
24. K.-F.J. Chan, N.D. Robb, W.H. Chen, Myelin basic protein: interaction with calmodulin and gangliosides, J. Neurosci. Res. 25 (1990) 535-544. (Pubitemid 20148412)
25. 2+- calmodulin: effects of deimination assessed by intrinsic Trp fluorescence spectroscopy, dynamic light scattering, and circular dichroism, Protein Sci. 12 (2003) 1507-1521.
26. V. Majava, C. Wang, M. Myllykoski, S.M. Kangas, S.U. Kang, K. Hayashi, P. Baumgärtel, A.M. Heape, G. Lubec, P. Kursula, Structural analysis of the complex between calmodulin and full-length myelin basic protein, an intrinsically disordered molecule, Amino Acids 39 (2010) 59-71.
27. J.X. Tang, P.A. Janmey, The polyelectrolyte nature of F-actin and the mechanism of actin bundle formation, J. Biol. Chem. 271 (1996) 8556-8563. (Pubitemid 26123271)
28. I.V. Ouporov, H.R. Knull, K.A. Thomasson, Brownian dynamics simulations of interactions between aldolase and G- or F-actin, Biophys. J. 76 (1999) 17-27. (Pubitemid 29202434)
29. T.E. Angelini, R. Golestanian, R.H. Coridan, J.C. Butler, A. Beraud, M. Krisch, H. Sinn, K.S. Schweizer, G.C. Wong, Counterions between charged polymers exhibit liquid-like organization and dynamics, Proc. Natl. Acad. Sci. U. S. A. 103 (2006) 7962-7967. (Pubitemid 43801036)
30. D.D. Wood, M.A. Moscarello, The isolation, characterization, and lipid-aggregating properties of a citrulline containing myelin basic protein, J. Biol. Chem. 264 (1989) 5121-5127. (Pubitemid 19092925)
31. G.R. Bartlett, Phosphorus assay in column chromatography, J. Biol. Chem. 234 (1959) 466-468.
32. S. Cheifetz, M.A. Moscarello, Effect of bovine basic protein charge microheterogeneity on protein-induced aggregation of unilamellar vesicles containing a mixture of acidic and neutral phospholipids, Biochemistry 24 (1985) 1909-1914. (Pubitemid 15019785)
33. F.C.-H. Chou, C.-H.J. Chou, R. Shapira, R.F. Kibler, Basis of microheterogeneity of myelin basic protein, J. Biol. Chem. 251 (1976) 2671-2679.
34. S. Cheifetz, M.A. Moscarello, C.M. Deber, NMR investigation of the charge isomers of bovine myelin basic protein, Arch. Biochem. Biophys. 233 (1984) 151-160. (Pubitemid 14071010)
35. G.L. Peterson, A simplification of the protein assay method of Lowry et al. which is more generally applicable, Anal. Biochem. 83 (1977) 346-356. (Pubitemid 8269786)
36. J.M. Boggs, N. Samji, M.A. Moscarello, G.A. Hashim, E.D. Day, Immune lysis of reconstituted myelin basic protein-lipid vesicles and myelin vesicles, J. Immunol. 130 (1983) 1687-1694. (Pubitemid 13091618)
37. S. Kaufmann, J. Kas, W.H. Goldmann, E. Sackmann, G. Isenberg, Talin anchors and nucleates actin filaments at lipid membranes. A direct demonstration, FEBS Lett. 314 (1992) 203-205.
38. D.J. Gordon, J.L. Boyer, E.D. Korn, Comparative biochemistry of non-muscle actins, J. Biol. Chem. 252 (1977) 8300-8309.
39. A. Gambhir, G. Hangyas-Mihalyne, I. Zaitseva, D.S. Cafiso, J. Wang, D. Murray, S.N. Pentyala, S.O. Smith, S. McLaughlin, Electrostatic sequestration of PIP2 on phospholipid membranes by basic/aromatic regions of proteins, Biophys. J. 86 (2004) 2188-2207. (Pubitemid 38524409)
40. J.M. Boggs, P.M. Yip, G. Rangaraj, E. Jo, Effect of posttranslational modifications to myelin basic protein on its ability to aggregate acidic lipid vesicles, Biochemistry 36 (1997) 5065-5071. (Pubitemid 27180988)
41. E.G. Bligh, W.J. Dyer, A rapid method of total lipid extraction and purification, Can. J. Biochem. Physiol. 37 (1959) 911-917.
42. K. Kimura, S. Hattori, Y. Kabuyama, Y. Shizawa, J. Takayangi, S. Nakamura, S. Toki, Y. Matsuda, K. Onodera, Neurite outgrowth of PC12 cells is suppressed by wortmannin, a specific inhibitor of phosphatidylinositol 3-kinase, J. Biol. Chem. 269 (1994) 18961-18967.
43. J. Wang, A. Gambhir, G. Hangyas-Mihalyne, D. Murray, U. Golebiewska, S. McLaughlin, Lateral sequestration of phosphatidylinositol 4,5-bisphosphate by the basic effector domain ofmyristoylated alanine-rich C kinase substrate is due to non-specific electrostatic interactions, J. Biol. Chem. 277 (2002) 34401-34412.
44. P.A. van Paridon, B. de Kruijff, R. Ouwerkerk, K.W.A. Wirtz, Polyphosphoinositides undergo charge neutralization in the physiological pH range: a 31P-NMR study, Biochim. Biophys. Acta 877 (1986) 216-219. (Pubitemid 16060212)
45. D. Murray, A. Arbuzova, G. Hangyas-Mihalyne, A. Gambhir, N. Ben-Tal, B. Honig, S. McLaughlin, Electrostatic properties of membranes containing acidic lipids and adsorbed basic peptides: theory and experiment, Biophys. J. 77 (1999) 3176-3188.
46. J. Wang, A. Arbuzova, G. Hangyas-Mihalyne, S. McLaughlin, The effector domain of myristoylated alanine-rich C kinase substrate binds strongly to phosphatidylinositol 4,5-bisphosphate, J. Biol. Chem. 276 (2001) 5012-5019.
47. S. McLaughlin, D. Murray, Plasma membrane phosphoinositide organization by protein electrostatics, Nature 438 (2005) 605-611. (Pubitemid 41740564)
48. A.A. Musse, W. Gao, L. Homchaudhuri, J.M. Boggs, G. Harauz, Myelin basic protein as a "PI(4,5)P2-modulin": a new biological function for a major central nervous system protein, Biochemistry 47 (2008) 10372-10382.
49. S. Nawaz, A. Kippert, A.S. Saab, H.B. Werner, T. Lang, K.A. Nave, M. Simons, Phosphatidylinositol 4,5-bisphosphate-dependent interaction of myelin basic protein with the plasma membrane in oligodendroglial cells and its rapid perturbation by elevated calcium, J. Neurosci. 29 (2009) 4794-4807.
50. M. Toner, G. Vajo, A. McLaughlin, S. McLaughlin, Adsorption of cations to phosphatidylinositol 4,5-bisphosphate, Biochemistry 27 (1988) 7435-7443.
51. T.G. Kutateladze, Translation of the phosphoinositide code by PI effectors, Nat. Chem. Biol. 6 (2010) 507-513.
52. T. Berggard, G. Arrigoni, O. Olsson, M. Fex, S. Linse, P. James, 140 mouse brain proteins identified by Ca2+-calmodulin affinity chromatography and tandem mass spectrometry, J. Proteome Res. 5 (2006) 669-687. (Pubitemid 43364108)
53. P.A. Janmey, W. Xian, L.A. Flanagan, Controlling cytoskeleton structure by phosphoinositide- protein interactions: phosphoinositide binding protein domains and effects of lipid packing, Chem. Phys. Lipids 101 (1999) 93-107. (Pubitemid 29385554)
54. T. Nebl, S.W. Oh, E.J. Luna, Membrane cytoskeleton: PIP(2) pulls the strings, Curr. Biol. 10 (2000) R351-R354. (Pubitemid 30308305)
55. P.A. Janmey, U. Lindberg, Cytoskeletal regulation: rich in lipids, Nat. Rev. Mol. Cell Biol. 5 (2004) 658-666. (Pubitemid 39025066)
56. T.S. Fraley, C.B. Pereira, T.C. Tran, C.A. Singleton, J.A. Greenwood, Phosphoinositide binding regulates á-actinin dynamics, J. Biol. Chem. 280 (2005) 15479-15482.
57. V. Papayannopoulos, C. Co, K.E. Prehoda, S. Snapper, J. Taunton,W.A. Lim, A polybasic motif allows N-WASP to act as a sensor of PIP2 density,Mol. Cell 17 (2005) 181-191. (Pubitemid 40138614)
58. E. Macia, S. Paris, M. Chabre, Binding of the PH and polybasic C-terminal domains of ARNO to phosphoinositides and to acidic lipids, Biochemistry 39 (2000) 5893-5901. (Pubitemid 30307979)
59. E.J. Luna, A.L. Hitt, Cytoskeleton-plasma membrane interactions, Science 258 (1992) 955-964.
60. N. Yonezawa, E. Nishida, K. Iida, I. Yahara, H. Sakai, Inhibition of the interactions of cofilin, destrin, and deoxyribonuclease I with actin by phosphoinositides, J. Biol. Chem. 265 (1990) 8382-8386.
61. T.S. Fraley, T.C. Tran, A.M. Corgan, C.A. Nash, J. Hao, D.R. Critchley, J.A. Greenwood, Phosphoinositide binding inhibits á-actinin bundling activity, J. Biol. Chem. 278 (2003) 24039-24045. (Pubitemid 36830236)
62. P.A. Steimle, J.D. Hoffert, N.B. Adey, S.W. Craig, Polyphosphoinositides inhibit the interaction of vinculin with actin filaments, J. Biol. Chem. 274 (1999) 18414-18420.
63. D.W. Kahn, P. Morell, Phosphatidic acid and phosphoinositide turnover in myelin and its stimulation by acetylcholine, J. Neurochem. 50 (1988) 1542-1550.
64. W.T. Norton, Isolation and characterization of myelin, in: P. Morell (Ed.), Myelin, Plenum Press, N. Y., 1977, pp. 161-199.
65. D.S. Deshmukh, S. Kuizon, W.D. Bear, H. Brockerhoff, Distribution of phosphoinositides among subfractions of rat brain myelin, Lipids 15 (1980) 14-18. (Pubitemid 10103277)
66. C. Fressinaud, J.M. Vallat, M. Rigaud, C. Cassagne, G. Labourdette, L.L. Sarlieve, Investigation of myelination in vitro: Polar lipid content and fatty acid composition of myelinating oligodendrocytes in rat oligodendrocyte cultures, Neurochem. Int. 16 (1990) 27-39. (Pubitemid 20049353)
67. L.J. Macala, R.K. Yu, S. Ando, Analysis of brain lipids by high performance thin-layer chromatography and densitometry, J. Lipid Res. 24 (1983) 1243-1250. (Pubitemid 14236574)