Role of the membrane in the modulation of the activity of protein kinase C

Journal of Liposome Research

Volumn 9, Issue 1, 1999, Pages 21-41

  Mosior, Marian ^a,c   Epand, Richard M ^b  

^a UNIVERSITY OF CALIFORNIA   (United States)

^b MCMASTER UNIVERSITY   (Canada)

^c ELI LILLY AND COMPANY   (United States)

Author keywords

Calcium; Membrane binding; Membrane modulation of enzyme activity; Phosphatidylserine; Protein kinase C

Indexed keywords

CALCIUM; DIACYLGLYCEROL; LIPID; PHOSPHATIDYLSERINE; PROTEIN KINASE C;

CALCIUM BINDING; CELL MEMBRANE; ENZYME ACTIVITY; ENZYME BINDING; ENZYME REGULATION; HUMAN; MEMBRANE BINDING; MEMBRANE BIOLOGY; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 0032965149     PISSN: 08982104     EISSN: None     Source Type: Journal    
DOI: 10.3109/08982109909044490     Document Type: Review

References (102)

1. Vinton, B.B., Wertz, S.L., Jacob, J., Steere, J., Grisham, C.M., Cafiso, D.S., and Sando, J.J. 1998. Influence of lipid on the structure and phosphorylation of protein kinase C alpha substrate peptides. Biochem J 330:1433-1442.
2. 2+ phospholipid-dependent and independent phosphorylation of synthetic peptide substrates by protein kinase C. Eur J Biochem 163:481-487.
3. Bruins, R.H. and Epand, R.M. 1995. Substrate-induced translocation of PKC-alpha to the membrane. Arch Biochem Biophys 324:216-222.
4. Andrea, J.E., Sutherland, C., Winter, C.K., and Walsh, M.P. 1998. Substrate-dependent activation requirements and kinetic properties of protein kinase C. FEBS Lett 429:73-77.
5. Keranen, L.M., Dutil, E.M., and Newton, A.C. 1995. Protein kinase C is regulated in vivo by three functionally distinct phosphorylations. Curr Biol 5:1394-1403.
6. Stempka, L., Girod, A., Muller, H.J., Rincke, G., Marks, F., Gschwendt, M., and Bossemeyer, D. 1997. Phosphorylation of protein kinase Cdelta (PKCdelta) at threonine 505 is not a prerequisite for enzymatic activity. Expression of rat PKCd and an alanine 505 mutant in bacteria in a functional form. J Biol Chem 272:6805-6811.
7. Konishi, H., Tanaka, M., Takemura, Y., Matsuzaki, H., Ono, Y., Kikkawa, U., and Nishizuka, Y. 1997. Activation of protein kinase C by tyrosine phosphorylation in response to H2O2. Proc Natl Acad Sci U.S.A. 94:11233-11237.
8. Gschwendt, M., Kielbassa, K., Kittstein, W., and Marks, F. 1994. Tyrosine phosphorylation and stimulation of protein kinase C delta from porcine spleen by src in vitro. Dependence on the activated state of protein kinase Cδ. FEBS Lett 347: 85-89.
9. Li, W., Zhang, J., Bottaro, D.P., and Pierce, J.H. 1997. Identification of serine 643 of protein kinase C-delta as an important autophosphorylation site for its enzymatic activity. J Biol Chem 272:24550-24555.
10. Mochly-Rosen, D. 1995. Localization of protein kinases by anchoring proteins: a theme in signal transduction. Science 268:247-251.
11. Mochly-Rosen, D. and Gordon, A.S. 1998. Anchoring proteins for protein kinase C: a means for isozyme selectivity. FASEB J 12:35-42.
12. Jaken, S. 1996. Protein kinase C isozymes and substrates. Curr Opin Cell Biol 8: 168-173.
13. Keenan, C. and Kelleher, D. 1998. Protein kinase C and the cytoskeleton. Cell Signal 10:225-232.
14. Oh, E.S., Woods, A., Lim, S.T., Theibert, A.W., and Couchman, J.R. 1998. Syndecan-4 proteoglycan cytoplasmic domain and phosphatidylinositol 4,5-bisphosphate coordinately regulate protein kinase C activity. J Biol Chem 273:10624-10629.
15. Blobe, G.C., Stribling, D.S., Fabbro, D., Stabel, S., and Hannun, Y.A. 1996. Protein kinase C βII specifically binds to and is activated by F-actin. J Biol Chem 271: 15823-15830.
16. Schmitz-Peiffer, C., Browne, C.L., Walker, J.H., and Biden, T.J. 1998. Activated protein kinase C α associates with annexin VI from skeletal muscle. Biochem J 330 (Pt 2):675-681.
17. Oka, N., Yamamoto, M., Schwencke, C., Kawabe, J., Ebina, T., Ohno, S., Couet, J., Lisanti, M.P., and Ishikawa, Y. 1997. Caveolin interaction with protein kinase C. Isoenzyme-dependent regulation of kinase activity by the caveolin scaffolding domain peptide. J Biol Chem 272:33416-33421.
18. Slater, S.J., Ho, C., Kelly, M.B., Larkin, J.D., Taddeo, F.J., Yeager, M.D., and Stubbs, C.D. 1996. Protein kinase Cα contains two activator binding sites that bind phorbol esters and diacylglycerols with opposite affinities. J Biol Chem 271:4627-4631.
19. Slater, S.J., Taddeo, F.J., Mazurek, A., Stagliano, B.A., Kelly, M.B., Ho, C., and Stubbs, C.D. 1998. Inhibition of Membrane Lipid-Independent Protein Kinase Cα Activity by Phorbol Esters, Diacylglycerols, and Bryostatin-1. J Biol Chem 273: 23160-23168.
20. Ford, D.A., Horner, C.C., and Gross, R.W. 1998. Protein kinase C acylation by palmitoyl coenzyme A facilitates its translocation to membranes. Biochemistry 37: 11953-11961.
21. Inoue, M., Kishimoto, A., Takai, Y., and Nishizuka, Y. 1977. Studies on a cyclic nucleotide-independent protein kinase and its proenzyme in mammalian tissues. II. Proenzyme and its activation by calcium-dependent protease from rat brain. J Biol Chem 252:7610-7616.
22. Takai, Y., Kishimoto, A., Iwasa, Y., Kawahara, Y., Mon, T., and Nishizuka, Y. 1979. Calcium-dependent activation of a multifunctional protein kinase by membrane phospholipids. J Biol Chem 254:3692-3695.
23. Kishimoto, A., Takai, Y., Mori, T., Kikkawa, U., and Nishizuka, Y. 1980. Activation of calcium and phospholipid-dependent protein kinase by diacylglycerol, its possible relation to phosphatidylinositol turnover. J Biol Chem 255:2273-2276.
24. Kaibuchi, K., Takai, Y., and Nishizuka, Y. 1981. Cooperative roles of various membrane phospholipids in the activation of calcium-activated, phospholipid-dependent protein kinase. J Biol Chem 256:7146-7149.
25. Kikkawa, U., Takai, Y., Minakuchi, R., Inohara, S., and Nishizuka, Y. 1982. Calcium-activated, phospholipid-dependent protein kinase from rat brain. Subcellular distribution, purification, and properties. J Biol Chem 257:13341-13348.
26. Ono, Y., Fujii, T., Ogita, K., Kikkawa, U., Igarashi, K., and Nishizuka, Y. 1988. The structure, expression, and properties of additional members of the protein kinase C family. J Biol Chem 263:6927-6932.
27. Nishizuka, Y. 1988. The molecular heterogeneity of protein kinase C and its implications for cellular regulation. Nature 334:661-665.
28. Kaibuchi, K., Fukumoto, Y., Oku, N., Takai, Y., Arai, K., and Muramatsu, M. 1989. Molecular genetic analysis of the regulatory and catalytic domains of protein kinase C. J Biol Chem 264:13489-13496.
29. Nalefski, E.A. and Falke, J.J. 1996. The C2 domain calcium-binding motif: structural and functional diversity. Protein Sci 5:2375-2390.
30. Essen, L.O., Perisic, O., Cheung, R., Katan, M., and Williams, R.L. 1996. Crystal structure of a mammalian phosphoinositide-specific phospholipase C δ. Nature 380: 595-602.
31. 2+/phospholipid-binding fold. Cell 80:929-938.
32. 2+-binding motif in C2 domains of synaptotagmin and protein kinase C. Science 273:248-251.
33. Perisic, O., Fong, S., Lynch, D.E., Bycroft, M., and Williams, R.L. 1998. Crystal structure of a calcium-phospholipid binding domain from cytosolic phospholipase A2. J Biol Chem 273:1596-1604.
34. Xu, R.X., Pawelczyk, T., Xia, T.H., and Brown, S.C. 1997. NMR structure of a protein kinase C-gamma phorbol-binding domain and study of protein-lipid micelle interactions. Biochemistry 36:10709-10717.
35. 1. J Biol Chem 273:11650-11659.
36. Mosior, M. and Epand, R.M. 1997. Protein kinase C: an example of a calcium-regulated protein binding to membranes (review). Mol Membr Biol 14:65-70.
37. Medkova, M. and Cho, W. 1998. Mutagenesis of the C2 domain of protein kinase C-alpha. Differential roles of Ca2+ ligands and membrane binding residues. J Biol Chem 273:17544-17552.
38. Edwards, A.S. and Newton, A.C. 1997. Regulation of protein kinase C betaII by its C2 domain. Biochemistry 36:15615-15623.
39. Bazzi, M.D. and Nelsestuen, G.L. 1991. Extensive segregation of acidic phospholipids in membranes induced by protein kinase C and related proteins. Biochemistry 30:7961-7969.
40. Swairjo, M.A., Concha, N.O., Kaetzel, M.A., Dedman, J.R., and Seaton, B.A. 1995. Ca(2+)-bridging mechanism and phospholipid head group recognition in the membrane-binding protein annexin V. Nat Struct Biol 2:968-974.
41. Mosior, M. and Epand, R.M. 1997. Protein kinase C: an example of a calcium-regulated protein binding to membranes (review). Mol.Membr.Biol. 14:65-70.
42. 2+ differentially regulates conventional protein kinase Cs' membrane interaction and activation. J Biol Chem 272:25959-25967.
43. Bosca, L. and Moran, F. 1993. Circular dichroism analysis of ligand-induced conformational changes in protein kinase C. Mechanism of translocation of the enzyme from the cytosol to the membranes and its implications. Biochem J 290:827-832.
44. Edwards, A.S. and Newton, A.C. 1997. Phosphorylation at conserved carboxyl-terminal Hydrophobic motif regulates the catalytic and regulatory domains of protein kinase C. J Biol Chem 272:18382-18390.
45. Luo, J.H. and Weinstein, I.B. 1993. Calcium-dependent activation of protein kinase C. The role of the C2 domain in divalent cation selectivity. J Biol Chem 268: 23580-23584.
46. 1 in the presence of phosphatidylserine. Carcinogenesis 16:897-905.
47. Maurer, M.C., Sando, J.J., and Grisham, C.M. 1992. High-affinity Ca(2+)-and substrate-binding sites on protein kinase C α as determined by nuclear magnetic resonance spectroscopy. Biochemistry 31:7714-7721.
48. Castagna, M., Takai, Y., Kaibuchi, K., Sano, K., Kikkawa, U., and Nishizuka, Y. 1982. Direct activation of calcium-activated, phospholipid-dependent protein kinase by tumor-promoting phorbol esters. J Biol Chem 257:7847-7851.
49. Ono, Y., Fujii, T., Igarashi, K., Kuno, T., Tanaka, C., Kikkawa, U., and Nishizuka, Y. 1989. Phorbol ester binding to protein kinase C requires a cysteine-rich zinc-finger-like sequence. Proc Natl Acad Sci U.S.A. 86:4868-4871.
50. Burns, D.J. and Bell, R.M. 1991. Protein kinase C contains two phorbol ester binding domains. J Biol Chem 266:18330-18338.
51. Szallasi, Z., Bogi, K., Gohari, S., Biro, T., Acs, P., and Blumberg, P.M. 1996. Non-equivalent roles for the first and second zinc fingers of protein kinase Cδ. Effect of their mutation on phorbol ester-induced translocation in NIH 3T3 cells. J Biol Chem 271:18299-18301.
52. Sharkey, N.A., Leach, K.L., and Blumberg, P.M. 1984. Competitive inhibition by diacylglycerol of specific phorbol ester binding. Proc Natl Acad Sci U.S.A. 81: 607-610.
53. Kazanietz, M.G., Barchi, J.J.J., Omichinski, J.G., and Blumberg, P.M. 1995. Low affinity binding of phorbol esters to protein kinase C and its recombinant cysteine-rich region in the absence of phospholipids. J Biol Chem 270:14679-14684.
54. Zhang, G., Kazanietz, M.G., Blumberg, P.M., and Hurley, J.H. 1995. Crystal structure of the cys2 activator-binding domain of protein kinase C δ in complex with phorbol ester. Cell 81:917-924.
55. Kazanietz, M.G., Wang, S., Milne, G.W., Lewin, N.E., Liu, H.L., and Blumberg, P.M. 1995. Residues in the second cysteine-rich region of protein kinase C δ relevant to phorbol ester binding as revealed by site-directed mutagenesis. J Biol Chem 270:21852-21859.
56. Mosior, M. and Epand, R.M. 1993. Mechanism of activation of protein kinase C: roles of diolein and phosphatidylserine. Biochemistry 32:66-75.
57. Mosior, M. and Newton, A.C. 1996. Calcium-independent binding to interfacial phorbol esters causes protein kinase C to associate with membranes in the absence of acidic lipids. Biochemistry 35:1612-1623.
58. Szallasi, Z., Smith, C.B., and Blumberg, P.M. 1994. Dissociation of phorbol esters leads to immediate redistribution to the cytosol of protein kinases C α and C δ in mouse keratinocytes. J Biol Chem 269:27159-27162.
59. Mosior, M. and Newton, A.C. 1995. Mechanism of interaction of protein kinase C with phorbol esters. Reversibility and nature of membrane association. J Biol Chem 270:25526-25533.
60. Bazzi, M.D. and Nelsestuen, G.L. 1987. Association of protein kinase C with phospholipid vesicles. Biochemistry 26:115-122.
61. Hannun, Y.A. and Bell, R.M. 1990. Rat brain protein kinase C. Kinetic analysis of substrate dependence, allosteric regulation, and autophosphorylation. J Biol Chem 265:2962-2972.
62. Lee, M.H. and Bell, R.M. 1989. Phospholipid functional groups involved in protein kinase C activation, phorbol ester binding, and binding to mixed micelles. J Biol Chem 264:14797-14805.
63. Orr, J.W. and Newton, A.C. 1992. Interaction of protein kinase C with phosphatidylserine. 1. Cooperativity in lipid binding. Biochemistry 31:4661-4667
64. Orr, J.W., Keranen, L.M., and Newton, A.C. 1992. Reversible exposure of the pseudosubstrate domain of protein kinase C by phosphatidylserine and diacylglycerol. J Biol Chem 267:15263-15266.
65. Hannun, Y.A., Loomis, C.R., and Bell, R.M. 1985. Activation of protein kinase C by Triton X-100 mixed micelles containing diacylglycerol and phosphatidylserine. J Biol Chem 260:10039-10043.
66. Newton, A.C. and Koshland, D.E.J. 1989. High cooperativity, specificity, and multiplicity in the protein kinase C-lipid interaction. J Biol Chem 264:14909-14915.
67. Huang, K.P., Huang, F.L., Nakabayashi, H., and Yoshida, Y. 1988. Biochemical characterization of rat brain protein kinase C isozymes. J Biol Chem 263:14839-14845.
68. Burns, D.J., Bloomenthal, J., Lee, M.H., and Bell, R.M. 1990. Expression of the alpha, beta II, and gamma protein kinase C isozymes in the baculovirus-insect cell expression system. Purification and characterization of the individual isoforms. J Biol Chem 265:12044-12051.
69. Mosior, M., Golini, E.S., and Epand, R.M. 1996. Chemical specificity and physical properties of the lipid bilayer in the regulation of protein kinase C by anionic phospholipids: evidence for the lack of a specific binding site for phosphatidylserine. Proc Natl Acad Sci U.S.A. 93:1907-1912.
70. Igarashi, K., Kaneda, M., Yamaji, A., Saido, T.C., Kikkawa, U., Ono, Y., Inoue, K., and Umeda, M. 1995. A novel phosphatidylserine-binding peptide motif defined by an anti-idiotypic monoclonal antibody. Localization of phosphatidylserine-specific binding sites on protein kinase C and phosphatidylserine decarboxylase. J Biol Chem 270:29075-29078.
71. Johnson, J.E., Edwards, A.S., and Newton, A.C. 1997. A putative phosphatidylserine binding motif is not involved in the lipid regulation of protein kinase C. J Biol Chem 272:30787-30792.
72. Murray, N.R. and Fields, A.P. 1998. Phosphatidylglycerol is a physiologic activator of nuclear protein kinase C. J Biol Chem 273:11514-11520.
73. Medkova, M. and Cho, W. 1998. Differential membrane-binding and activation mechanisms of protein kinase C-alpha and -epsilon. Biochemistry 37:4892-4900.
74. Newton, A.C. and Keranen, L.M. 1994. Phosphatidyl-L-serine is necessary for protein kinase C's high-affinity interaction with diacylglycerol-containing membranes. Biochemistry 33:6651-6658.
75. Epand, R.M., Stevenson, C., Bruins, R.H., Schram, V., and Glaser, M. 1998. The chirality of phosphatidylserine and the activation of protein kinase C. Biochemistry 37:12068-12073.
76. Yang, L. and Glaser, M. 1996. Formation of membrane domains during the activation of protein kinase C. Biochemistry 35:13966-13974.
77. Johnson, J.E., Zimmerman, M.L., Daleke, D.L., and Newton, A.C. 1998. Lipid structure and not membrane structure is the major determinant in the regulation of protein kinase C by phosphatidylserine. Biochemistry 37:12020-12025.
78. Chauhan, V.P. and Brockerhoff, H. 1988. Phosphatidylinositol-4,5-bisphosphate may antecede diacylglycerol as activator of protein kinase C. Biochem Biophys Res Commun 155:18-23.
79. Huang, F.L. and Huang, K.P. 1991. Interaction of protein kinase C isozymes with phosphatidylinositol 4,5-bisphosphate. J Biol Chem 266:8727-8733.
80. Lee, M.H. and Bell, R.M. 1991. Mechanism of protein kinase C activation by phosphatidylinositol 4,5-bisphosphate. Biochemistry 30:1041-1049.
81. Toker, A., Meyer, M., Reddy, K.K., Falck, J.R., Aneja, R., Aneja, S., Parra, A., Burns, D.J., Ballas, L.M., and Cantley, L.C. 1994. Activation of protein kinase C family members by the novel polyphosphoinositides PtdIns-3,4-P2 and PtdIns-3,4,5-P3. J Biol Chem 269:32358-32367.
82. Nakanishi, H., Brewer, K.A., and Exton, J.H. 1993. Activation of the zeta isozyme of protein kinase C by phosphatidylinositol 3,4,5-trisphosphate. J Biol Chem 268: 13-16.
83. Pepio, A.M. and Sossin, W.S. 1998. The C2 domain of the Ca(2+)-independent protein kinase C Ap1 II inhibits phorbol ester binding to the C1 domain in a phosphatidic acid-sensitive manner. Biochemistry 37:1256-1263.
84. Nalefski, E.A., Sultzman, L.A., Martin, D.M., Kriz, R.W., Towler, P.S., Knopf, J.L., and Clark, J.D. 1994. Delineation of two functionally distinct domains of cytosolic phospholipase A2, a regulatory Ca(2+)-dependent lipid-binding domain and a Ca(2+)-independent catalytic domain. J Biol Chem 269:18239-18249.
85. Davletov, B.A. and Sudhof, T.C. 1993. A single C2 domain from synaptotagmin I is sufficient for high affinity Ca2+/phospholipid binding. J Biol Chem 268:26386-26390.
86. Murray, D., Hermida-Matsumoto, L., Buser, C.A., Tsang, J., Sigal, C.T., Ben-Tal, N., Honig, B., Resh, M.D., and McLaughlin, S. 1998. Electrostatics and the membrane association of Src: theory and experiment. Biochemistry 37:2145-2159
87. Epand, R.M. 1985. Diacylglycerols, lysolecithin, or hydrocarbons markedly alter the bilayer to hexagonal phase transition temperature of phosphatidylethanolamines. Biochemistry 24:7092-7095.
88. Epand, R.M. 1987. The relationship between the effects of drugs on bilayer stability and on protein kinase C activity. Chem Biol. Interact 63:239-247.
89. Epand, R.M., Epand, R.F., Leon, B.T., Menger, F.M., and Kuo, J.F. 1991. Evidence for the regulation of the activity of protein kinase C through changes in membrane properties. Biosci Rep 11:59-64.
90. II lipid liquid crystal phase transition: Hydrocarbon packing versus intrinsic curvature. J Phys (Paris) 46:761-769.
91. Rand, R.P., Fuller, N.L., Gruner, S.M., and Parsegian, V.A. 1990. Membrane curvature, lipid segregation, and structural transitions for phospholipids under dual-solvent stress. Biochemistry 29:76-87.
92. Hamm, M. and Kozlov, M. 1998. Elastic energy of tilt and bending of fluid membranes. Biophys J, in press.
93. Hamm, M. and Kozlov, M. 1998. Tilt model of inverted amphiphilic mesophases. Biophys J, in press.
94. Luzzati, V., Delacroix, H., Gulik-Krzywicki, T., Mariani, P., and Vargas, R., The Cubic Phases of Lipids in Lipid Polymorphism and Membrane Properties. Epand, R.M. (ed.), pp. 3-24, Academic Press, San Diego, CA. 1997.
95. Anderson, D.M., Gruner, S.M., and Leibler, S. 1988. Geometrical aspects of the frustration in the cubic phases of lyotropic liquid crystals. Proc Natl Acad Sci U.S.A. 85:5364-5368.
96. Giorgione, J.R., Huang, Z., and Epand, R.M. 1998. Increased activation of protein kinase C with cubic phase lipid compared with liposomes. Biochemistry 37:2384-2392.
97. Keller, S.L., Gruner, S.M., and Gawrisch, K. 1996. Small concentrations of alamethicin induce a cubic phase in bulk phosphatidylethanolamine mixtures. Biochim Biophys Acta 1278:241-246.
98. Brown, M.F., Influence of Nonlamellar-Forming Lipids in Rhodopsin in Lipid Polymorphism and Membrane Properties. Epand, R.M. (ed.), pp. 285-356, Academic Press, San Diego, CA. 1997.
99. Epand, R.M., Fuller, N., and Rand, R.P. 1996. Role of the position of unsaturation on the phase behavior and intrinsic curvature of phosphatidylethanolamines. Biophys J 71:1806-1810.
100. Giorgione, J.R., Kraayenhof, R., and Epand, R.M. 1998. Interfacial membrane properties modulate protein kinase C activation: role of the position of acyl chain unsaturation. Biochemistry 37:10956-10960.
101. Ahn, T. and Kim, H. 1998. Effects of nonlamellar-prone lipids on the ATPase activity of SecA bound to model membranes. J Biol Chem 273:21692-21698.
102. Matsuzaki, K., Sugishita, K., Ishibe, N., Ueha, M., Nakata, S., Miyajima, K., and Epand, R.M. 1998. Relationship of membrane curvature to the formation of pores by magainin 2. Biochemistry 37:11856-11863.