MARCKS, membranes, and calmodulin: Kinetics of their interaction

Biochimica et Biophysica Acta - Reviews on Biomembranes

Volumn 1376, Issue 3, 1998, Pages 369-379

  Arbuzova, Anna ^a   Murray, Diana ^a   McLaughlin, Stuart ^a  

^a STONY BROOK UNIVERSITY   (United States)

Author keywords

Diffusion limited process; Electrostatics; Membrane binding; Signal transduction

Indexed keywords

CALMODULIN; MARCKS PROTEIN; MYOSIN LIGHT CHAIN KINASE;

CATTLE; ELECTRON SPIN RESONANCE; FLUORESCENCE; NONHUMAN; PHOSPHOLIPID VESICLE; PRIORITY JOURNAL; REVIEW;

ANIMALS; CA(2+)-CALMODULIN DEPENDENT PROTEIN KINASE; CALMODULIN; DIFFUSION; ENZYME ACTIVATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LIPID BILAYERS; MEMBRANE PROTEINS; MYOSIN-LIGHT-CHAIN KINASE; PROTEINS;

BOVINAE;

EID: 0031795796     PISSN: 03044157     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0304-4157(98)00011-2     Document Type: Review

References (81)

1. Berridge M.J. Inositol trisphosphate and calcium signalling. Nature. 361:1993;315-325.
2. Clapham D.E. Calcium signaling. Cell. 80:1995;259-268.
3. Nishizuka Y. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science. 258:1992;607-614.
4. Newton A.C. Protein kinase C: Structure, function and regulation. J. Biol. Chem. 270:1995;28495-28498.
5. Aderem A. The MARCKS brothers: a family of protein kinase C substrates. Cell. 71:1992;713-716.
6. Blackshear P.J. The MARCKS family of cellular protein kinase C substrates. J. Biol. Chem. 268:1993;1501-1504.
7. Myat M.M., Anderson S., Allen L.H., Aderem A. MARCKS regulates membrane ruffling and cell spreading. Curr. Biol. 7:1997;611-614.
8. Thelen M., Rosen A., Nairn A.C., Aderem A. Regulation by phosphorylation of reversible association of a myristoylated protein kinase C substrate with the plasma membrane. Nature. 351:1991;320-322.
9. Rosen A., Keenan K.F., Thelen M., Nairn A.C., Aderem A. Activation of protein kinase C results in the displacement of its myristoylated, alanine-rich substrate from punctate structures in macrophage filopodia. J. Exp. Med. 172:1990;1211-1215.
10. Allen L.A., Aderem A. A role for MARCKS, the a isozyme of protein kinase C and myosin I in zymosan phagocytosis by macrophages. J. Exp. Med. 182:1995;829-840.
11. Herget T., Brooks S.F., Broad S., Rozengurt E. Expression of the major protein kinase C substrate, the acidic 80-kilodalton myristoylated alanine-rich C kinase substrate, increases sharply when Swiss 3T3 cells move out of cycle and enter G0. Proc. Natl. Acad. Sci. U.S.A. 90:1993;2945-2949.
12. Albert K.A., Nairn A.C., Greengard P. The 87-kDa protein, a major specific substrate for protein kinase C: purification from bovine brain and characterization. Proc. Natl. Acad. Sci. U.S.A. 84:1987;7046-7050.
13. r 80,000 protein phosphorylated in response to phorbol esters and growth factors in intact fibroblasts. Distinction from protein kinase C and prominence in brain. J. Biol. Chem. 261:1986;1459-1469.
14. Stumpo D.J., Bock C.B., Tuttle J.S., Blackshear P.J. MARCKS deficiency in mice leads to abnormal brain development and perinatal death. Proc. Natl. Acad. Sci. U.S.A. 92:1995;944-948.
15. Blackshear P.J., Silver J., Nairn A.C., Sulik K.K., Squier M.V., Stumpo D.J., Tuttle J.S. Widespread neuronal ectopia associated with secondary defects in cerebrocortical chondroitin sulfate proteoglycans and basal lamina in MARCKS-deficient mice. Exp. Neurol. 145:1997;46-61.
16. Manenti S., Sorokine O., Van Dorsselaer A., Taniguchi H. Affinity purification and characterization of myristoylated alanine-rich protein kinase C substrate (MARCKS) from bovine brain. Comparison of the cytoplasmic and the membrane-bound forms. J. Biol. Chem. 267:1992;22310-22315.
17. Graff J.M., Young T.N., Johnson J.D., Blackshear P.J. Phosphorylation-regulated calmodulin binding to a prominent cellular substrate for protein kinase C. J. Biol. Chem. 264:1989;21818-21823.
18. Hartwig J.H., Thelen M., Rosen A., Janmey P.A., Nairn A.C., Aderem A. MARCKS is an actin filament crosslinking protein regulated by protein kinase C and calcium-calmodulin. Nature. 356:1992;618-622.
19. Taniguchi H., Manenti S. Interaction of myristoylated alanine-rich protein kinase C substrate (MARCKS) with membrane phospholipids. J. Biol. Chem. 268:1993;9960-9963.
20. Swierczynski S.L., Blackshear P.J. Myristoylation-dependent and electrostatic interactions exert independent effects on the membrane association of the Myristoylated Alanine-rich C-kinase Substrate. J. Biol. Chem. 271:1996;23424-23430.
21. Seykora J.T., Myat M.M., Allen L.A., Ravetch J.V., Aderem A. Molecular determinants of the myristoyl-electrostatic switch of MARCKS. J. Biol. Chem. 271:1996;18797-18802.
22. A. Schmitz, E. Schleiff, G. Vergeres, Cross-talk between calmodulin and protein kinase C, in: K. Wirtz (Ed.), Molecular Mechanisms of Signaling and Membrane Transport, Springer, Berlin, 1997, pp. 127-150.
23. Graff J.M., Stumpo D.J., Blackshear P.J. Characterization of the phosphorylation sites in the chicken and bovine myristoylated alanine-rich C kinase substrate protein, a prominent cellular substrate for protein kinase C. J. Biol. Chem. 264:1989;11912-11919.
24. Verghese G.M., Johnson J.D., Vasulka C., Haupt D.M., Stumpo D.J., Blackshear P.J. Protein kinase C-mediated phosphorylation and calmodulin binding of recombinant myristoylated alanine-rich C kinase substrate (MARCKS) and MARCKS-related protein. J. Biol. Chem. 269:1994;9361-9367.
25. McLaughlin S., Aderem A. The myristoyl-electrostatic switch: A modulator of reversible protein-membrane interactions. Trends Biochem. Sci. 20:1995;272-276.
26. Resh M.D. Regulation of cellular signalling by fatty acid acylation and prenylation of signal transduction proteins. Cell. Signal. 8:1996;403-412.
27. Bhatnagar R.S., Gordon J.I. Understanding covalent modifications of proteins by lipids: where cell biology and biophysics mingle. Trends Cell Biol. 7:1997;14-21.
28. Peitzsch R.M., McLaughlin S. Binding of acylated peptides and fatty acids to phospholipid vesicles: pertinence to myristoylated proteins. Biochemistry. 32:1993;10436-10443.
29. Resh M.D. Myristylation and palmitylation of Src family members: the fats of the matter. Cell. 76:1994;411-413.
30. Byers D.M., Palmer F.B., Spence M.W., Cook H.W. Dissociation of phosphorylation and translocation of a myristoylated protein kinase C substrate (MARCKS protein) in C6 glioma and N1E-115 neuroblastoma cells. J. Neurochem. 60:1993;1414-1421.
31. Kim J., Shishido T., Jiang X., Aderem A., McLaughlin S. Phosphorylation, high ionic strength, and calmodulin reverse the binding of MARCKS to phospholipid vesicles. J. Biol. Chem. 269:1994;28214-28219.
32. Swierczynski S.L., Blackshear P.J. Membrane association of the myristoylated alanine-rich C kinase substrate (MARCKS) protein. Mutational analysis provides evidence for complex interactions. J. Biol. Chem. 270:1995;13436-13445.
33. Hinrichsen R.D., Blackshear P.J. Regulation of peptide-calmodulin complexes by protein kinase C in vivo. Proc. Natl. Acad. Sci. U.S.A. 90:1993;1585-1589.
34. 2+-induced keratinocyte differentiation. Selective blockade of MARCKS phosphorylation by calmodulin. J. Biol. Chem. 270:1995;1362-1368.
35. 2+·calmodulin prevents myristoylated alanine-rich kinase C substrate protein phosphorylation by protein kinase Cs in C6 rat glioma cells. J. Biol. Chem. 270:1995;24911-24916.
36. Herget T., Broad S., Rozengurt E. Overexpression of the myristoylated alanine-rich C-kinase substrate in Rat1 cells increases sensitivity to calmodulin antagonists. Eur. J. Biochem. 225:1994;549-556.
37. Sawai T., Negishi M., Nishigaki N., Ohno T., Ichikawa A. Enhancement by protein kinase C of prostacyclin receptor-mediated activation of adenylate cyclase through a calmodulin/myristoylated alanine-rich C kinase substrate (MARCKS) system in IC2 mast cells. J. Biol. Chem. 268:1993;1995-2000.
38. Douglas D.N., Fink H.S., Rose S.D., Ridgway N.D., Cook H.W., Byers D.M. Inhibitors of actin polymerization and calmodulin binding enhance protein kinase C-induced translocation of MARCKS in C6 glioma cells. Biochim. Biophys. Acta. 1356:1997;121-130.
39. Peitzsch R.M., Eisenberg M., Sharp K.A., McLaughlin S. Calculations of the electrostatic potential adjacent to model phospholipid bilayers. Biophys. J. 68:1995;729-738.
40. Nicholls A., Sharp K.A., Honig B. Protein folding and association: insights from the interfacial and thermodynamic properties of hydrocarbon. Proteins Struct. Funct. Genet. 11:1991;281-296.
41. Coburn C., Eisenberg J., Eisenberg M., McLaughlin S., Runnels L. Calculations of electrostatic potentials adjacent to membranes and peptides that mimic the calmodulin-binding domains of neuromodulin and the MARCKS protein. Biophys. J. 64:1993;A60.
42. Qin Z., Cafiso D.S. Membrane structure of the protein kinase C and calmodulin binding domain of Myristoylated Alanine Rich C Kinase Substrate determined by site-directed spin labeling. Biochemistry. 35:1996;2917-2925.
43. Glaser M., Wanaski S., Buser C.A., Boguslavsky V., Rashidzada W., Morris A., Rebecchi M., Scarlata S.F., Runnels L.W., Prestwich G.D., Chen J., Aderem A., Ahn J., McLaughlin S. MARCKS produces reversible inhibition of phospholipase C by sequestering phosphatidylinositol 4,5-bisphosphate in lateral domains. J. Biol. Chem. 271:1996;26187-26193.
44. Kim J., Blackshear P.J., Johnson J.D., McLaughlin S. Phosphorylation reverses the membrane association of peptides that correspond to the basic domains of MARCKS and neuromodulin. Biophys. J. 67:1994;227-237.
45. Arbuzova A., Wang J., Murray D., Jacob J., Cafiso D.S., McLaughlin S. Kinetics of interaction of the myristoylated alanine-rich C kinase substrate, membranes, and calmodulin. J. Biol. Chem. 272:1997;27167-27177.
46. Prendergast F.G., Meyer M., Carlson G.L., Iida S., Potter J.D. Synthesis, spectral properties, and use of 6-acryloyl-2-dimethylaminonaphthalene (acrylodan). J. Biol. Chem. 258:1983;7541-7544.
47. Schwarz G. Basic kinetics of binding and incorporation with supramolecular aggregates. Biophys. Chem. 26:1987;163-169.
48. R.M. Noyes, Effects of diffusion rates on chemical kinetics, in: G. Porter (Ed.), Progress in Reaction Kinetics, Pergamon, New York, 1961, pp. 129-160.
49. H.C. Berg, Random Walks in Biology, Princeton University Press, Princeton, 1983, pp. 17-27.
50. 31P NMR study of pentalysine interaction with headgroup deuterated phosphatidylcholine and phosphatidylserine. Eur. Biophys. J. 16:1988;267-273.
51. Ben-Tal N., Honig B., Peitzsch R.M., Denisov G., McLaughlin S. Binding of small basic peptides to membranes containing acidic lipids: Theoretical models and experimental results. Biophys. J. 71:1996;561-575.
52. Lu Y., Bazzi M.D., Nelsestuen G.L. Kinetics of annexin VI, calcium, and phospholipid association and dissociation. Biochemistry. 34:1995;10777-10785.
53. Schwarz G., Gerke H., Rizzo V., Stankowski S. Incorporation kinetics in a membrane, studied with the pore-forming peptide alamethicin. Biophys. J. 52:1987;685-692.
54. Schwarz G., Beschiaschvili G. Thermodynamic and kinetic studies on the association of melittin with a phospholipid bilayer. Biochim. Biophys. Acta. 979:1989;82-90.
55. Eigen M. Proton transfer, acid-base catalysis, and enzymatic hydrolysis. Angew. Chem. Int. Ed. Engl. 3:1964;1-72.
56. Schleiff E., Schmitz A., McIlhinney R.A.J., Manenti S., Vergeres G. Myristoylation does not modulate the properties of MARCKS-related protein (MRP) in solution. J. Biol. Chem. 271:1996;26794-26802.
57. Meyer T., Hanson P.I., Stryer L., Schulman H. Calmodulin trapping by calcium-calmodulin-dependent protein kinase. Science. 256:1992;1199-1202.
58. 2+/calmodulin. J. Biol. Chem. 267:1992;5346-5354.
59. Diebler H., Eigen M., Ilgenfritz G., Maass G., Winkler R. Kinetics and mechanism of reactions of main group metal ions with biological carriers. Pure Appl. Chem. 20:1969;93-115.
60. Meador W.E., Means A.R., Quiocho F.A. Modulation of calmodulin plasticity in molecular recognition on the basis of X-ray structures. Science. 262:1993;1718-1721.
61. Klapper I., Hagstrom R., Fine R., Sharp K., Honig B. Focusing of electric fields in the active site of Cu-Zn superoxide dismutase: effects of ionic strength and amino-acid modification. Proteins Struct. Funct. Genet. 1:1986;47-59.
62. Honig B.H., Nicholls A. Classical electrostatics in biology and chemistry. Science. 268:1995;1144-1149.
63. Schreiber G., Fersht A.R. Rapid, electrostatically assisted association of proteins. Nature Struct. Biol. 3:1996;427-431.
64. Gabdoulline R.R., Wade R.C. Simulation of the diffusional association of barnase and barstar. Biophys. J. 72:1997;1917-1929.
65. Murray D., Ben-Tal N., Honig B., McLaughlin S. Electrostatic interaction of myristoylated proteins with membranes: simple physics, complicated biology. Structure. 5:1997;985-989.
66. Wimley W.C., White S.H. Experimentally determined hydrophobicity scale for proteins at membrane interfaces. Nature Struct. Biol. 3:1996;842-848.
67. 2+-dependent binding of calmodulin to an N-terminal motif of the heterotrimeric G protein beta subunit. J. Biol. Chem. 272:1997;18801-18807.
68. Wang K.L., Khan M.T., Roufogalis B.D. Identification and characterization of a calmodulin-binding domain in Ral-A, a Ras-related GTP-binding protein purified from human erythrocyte membrane. J. Biol. Chem. 272:1997;16002-16009.
69. Fischer R., Wei Y., Anagli J., Berchtold M.W. Calmodulin binds to and inhibits GTP binding of the Ras-like GTPase KIR/GEM. J. Biol. Chem. 271:1996;25067-25070.
70. Moyers J.S., Bilan P.J., Zhu J.H., Kahn C.R. Rad and Rad-related GTPases interact with calmodulin and calmodulin-dependent protein kinase II. J. Biol. Chem. 272:1997;11832-11839.
71. 2+/calmodulin causes Rab3A to dissociate from synaptic membranes. J. Biol. Chem. 272:1997;20857-20865.
72. Pronin A.N., Benovic J.L. Regulation of the G protein-coupled receptor kinase GRK5 by protein kinase C. J. Biol. Chem. 272:1997;3806-3812.
73. Matsuoka Y., Hughes C.A., Bennett V. Adducin regulation. Definition of the calmodulin-binding domain and sites of phosphorylation by protein kinases A and C. J. Biol. Chem. 271:1996;25157-25166.
74. 2+/calmodulin. J. Biol. Chem. 272:1997;17038-17044.
75. Chapin S.J., Enrich C., Aroeti B., Havel R.J., Mostov K.E. Calmodulin binds to the basolateral targeting signal of the polymeric immunoglobulin receptor. J. Biol. Chem. 271:1996;1336-1342.
76. Ehlers M.D., Zhang S., Bernhadt J.P., Huganir R.L. Inactivation of NMDA receptors by direct interaction of calmodulin with the NR1 subunit. Cell. 84:1996;745-755.
77. Soderling T.R. Protein kinases regulation by autoinhibitory domains. J. Biol. Chem. 265:1990;1823-1826.
78. Braun A.P., Schulman H. The multifunctional calcium/calmodulin-dependent protein kinase: From form to function. Annu. Rev. Physiol. 57:1995;417-445.
79. Crivici A., Ikura M. Molecular and structural basis of target recognition by calmodulin. Annu. Rev. Biophys. Biomol. Struct. 24:1995;85-116.
80. 2+ oscillations. Science. 279:1998;227-230.
81. Krueger J.K., Olah G.A., Rokop S.E., Zhi G., Stull J.T., Trewhella J. Structure of calmodulin and a functional myosin light chain kinase in the activated complex: a neutron scattering study. Biochemistry. 36:1997;6017-6023.