PKC-delta and PKC-epsilon: Foes of the same family or strangers?

Journal of Molecular and Cellular Cardiology

Volumn 51, Issue 5, 2011, Pages 665-673

  Duquesnes, Nicolas ^a,b,c   Lezoualc'h, Frank ^d,e   Crozatier, Bertrand ^f,g  

^a L INSTITUT DU THORAX   (France)

^b CNRS   (France)

^c UNIVERSITÉ DE NANTES   (France)

^d University Hospital of Toulouse   (France)

^e UNIVERSITÉ PAUL SABATIER   (France)

^f UNIVERSITÉ PARIS SACLAY   (France)

^g INSERM   (France)

Author keywords

Activation; Localization; Protein kinase C; Signal transduction; Structure

Indexed keywords

ACTIN; CALCINEURIN; CONNEXIN 43; ENDOTHELIAL NITRIC OXIDE SYNTHASE; F ACTIN; INDUCIBLE NITRIC OXIDE SYNTHASE; MITOGEN ACTIVATED PROTEIN KINASE; MITOGEN ACTIVATED PROTEIN KINASE P38; PHOSPHATIDYLINOSITOL 3 KINASE; PROTEIN 14 3 3; PROTEIN KINASE B; PROTEIN KINASE C DELTA; PROTEIN KINASE C EPSILON; PROTEIN TYROSINE KINASE; STRESS ACTIVATED PROTEIN KINASE;

APOPTOSIS; CELL DIFFERENTIATION; CELL GROWTH; COMPLEX FORMATION; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME LOCALIZATION; ENZYME STRUCTURE; HEART FAILURE; HEART INFARCTION PREVENTION; HEART VENTRICLE HYPERTROPHY; HUMAN; NONHUMAN; PATHOPHYSIOLOGY; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REVIEW; SIGNAL TRANSDUCTION;

ANIMALS; APOPTOSIS; CELL DIFFERENTIATION; ENZYME ACTIVATION; ENZYME INHIBITORS; GUINEA PIGS; HUMANS; HYPERTROPHY, LEFT VENTRICULAR; ISOENZYMES; MICE; MYOCARDIAL ISCHEMIA; MYOCARDIUM; ORGAN SPECIFICITY; PROTEIN BINDING; PROTEIN KINASE C-ALPHA; PROTEIN KINASE C-DELTA; PROTEIN KINASE C-EPSILON; PROTEIN STRUCTURE, TERTIARY; RABBITS; RATS; SIGNAL TRANSDUCTION; TETRADECANOYLPHORBOL ACETATE;

EID: 80053268287     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2011.07.013     Document Type: Review

References (122)

1. Nishizuka Y. The role of protein kinase C in cell surface signal transduction and tumour promotion. Nature 1984, 308:693-698.
2. Nishizuka Y. Intracellular signaling by hydrolysis of phospholipids and activation of protein kinase C. Science 1992, 258:607-614.
3. Nishizuka Y. Protein kinase C and lipid signaling for sustained cellular responses. FASEB J 1995, 9:484-496.
4. Bogoyevitch M.A., Parker P.J., Sugden P.H. Characterization of protein kinase C isotype expression in adult rat heart. Protein kinase C-epsilon is a major isotype present, and it is activated by phorbol esters, epinephrine, and endothelin. Circ Res 1993, 72:757-767.
5. Mackay K., Mochly-Rosen D. Localization, anchoring, and functions of protein kinase C isozymes in the heart. J Mol Cell Cardiol 2001, 33:1301-1307.
6. Rouet-Benzineb P., Mohammadi K., Perennec J., Poyard M., Bouanani Nel H., Crozatier B. Protein kinase C isoform expression in normal and failing rabbit hearts. Circ Res 1996, 79:153-161.
7. Ping P., Zhang J., Qiu Y., Tang X.L., Manchikalapudi S., Cao X., et al. Ischemic preconditioning induces selective translocation of protein kinase C isoforms epsilon and eta in the heart of conscious rabbits without subcellular redistribution of total protein kinase C activity. Circ Res 1997, 81:404-414.
8. Mischak H., Goodnight J.A., Kolch W., Martiny-Baron G., Schaechtle C., Kazanietz M.G., et al. Overexpression of protein kinase C-delta and -epsilon in NIH 3T3 cells induces opposite effects on growth, morphology, anchorage dependence, and tumorigenicity. J Biol Chem 1993, 268:6090-6096.
9. Cacace A.M., Guadagno S.N., Krauss R.S., Fabbro D., Weinstein I.B. The epsilon isoform of protein kinase C is an oncogene when overexpressed in rat fibroblasts. Oncogene 1993, 8:2095-2104.
10. Perletti G.P., Folini M., Lin H.C., Mischak H., Piccinini F., Tashjian A.H. Overexpression of protein kinase C epsilon is oncogenic in rat colonic epithelial cells. Oncogene 1996, 12:847-854.
11. Watanabe T., Ono Y., Taniyama Y., Hazama K., Igarashi K., Ogita K., et al. Cell division arrest induced by phorbol ester in CHO cells overexpressing protein kinase C-delta subspecies. Proc Natl Acad Sci USA 1992, 89:10159-10163.
12. Mischak H., Pierce J.H., Goodnight J., Kazanietz M.G., Blumberg P.M., Mushinski J.F. Phorbol ester-induced myeloid differentiation is mediated by protein kinase C-alpha and -delta and not by protein kinase C-beta II, -epsilon, -zeta, and -eta. J Biol Chem 1993, 268:20110-20115.
13. Reyland M.E., Anderson S.M., Matassa A.A., Barzen K.A., Quissell D.O. Protein kinase C delta is essential for etoposide-induced apoptosis in salivary gland acinar cells. J Biol Chem 1999, 274:19115-19123.
14. Gorin M.A., Pan Q. Protein kinase C epsilon: an oncogene and emerging tumor biomarker. Mol Cancer 2009, 8:9.
15. Budas G.R., Churchill E.N., Mochly-Rosen D. Cardioprotective mechanisms of PKC isozyme-selective activators and inhibitors in the treatment of ischemia-reperfusion injury. Pharmacol Res 2007, 55:523-536.
16. Chen L., Hahn H., Wu G., Chen C.H., Liron T., Schechtman D., et al. Opposing cardioprotective actions and parallel hypertrophic effects of delta PKC and epsilon PKC. Proc Natl Acad Sci USA 2001, 98:11114-11119.
17. Oestreich E.A., Malik S., Goonasekera S.A., Blaxall B.C., Kelley G.G., Dirksen R.T., et al. Epac and phospholipase Cepsilon regulate Ca2+ release in the heart by activation of protein kinase Cepsilon and calcium-calmodulin kinase II. J Biol Chem 2009, 284:1514-1522.
18. Duquesnes N., Derangeon M., Metrich M., Lucas A., Mateo P., Li L., et al. Epac stimulation induces rapid increases in connexin43 phosphorylation and function without preconditioning effect. Pflugers Arch 2010, 460:731-741.
19. de Rooij J., Zwartkruis F.J., Verheijen M.H., Cool R.H., Nijman S.M., Wittinghofer A., et al. Epac is a Rap1 guanine-nucleotide-exchange factor directly activated by cyclic AMP. Nature 1998, 396:474-477.
20. Schmidt M., Evellin S., Weernink P.A., von Dorp F., Rehmann H., Lomasney J.W., et al. A new phospholipase-C-calcium signalling pathway mediated by cyclic AMP and a Rap GTPase. Nat Cell Biol 2001, 3:1020-1024.
21. Orr J.W., Newton A.C. Intrapeptide regulation of protein kinase C. J Biol Chem 1994, 269:8383-8387.
22. Nishikawa K., Toker A., Johannes F.J., Songyang Z., Cantley L.C. Determination of the specific substrate sequence motifs of protein kinase C isozymes. J Biol Chem 1997, 272:952-960.
23. Newton A.C. Protein kinase C: structure, function, and regulation. J Biol Chem 1995, 270:28495-28498.
24. Keranen L.M., Dutil E.M., Newton A.C. Protein kinase C is regulated in vivo by three functionally distinct phosphorylations. Curr Biol 1995, 5:1394-1403.
25. Parekh D.B., Ziegler W., Parker P.J. Multiple pathways control protein kinase C phosphorylation. EMBO J 2000, 19:496-503.
26. Toker A., Newton A.C. Cellular signaling: pivoting around PDK-1. Cell 2000, 103:185-188.
27. Chou M.M., Hou W., Johnson J., Graham L.K., Lee M.H., Chen C.S., et al. Regulation of protein kinase C zeta by PI 3-kinase and PDK-1. Curr Biol 1998, 8:1069-1077.
28. Cenni V., Doppler H., Sonnenburg E.D., Maraldi N., Newton A.C., Toker A. Regulation of novel protein kinase C epsilon by phosphorylation. Biochem J 2002, 363:537-545.
29. Rybin V.O., Guo J., Sabri A., Elouardighi H., Schaefer E., Steinberg S.F. Stimulus-specific differences in protein kinase C delta localization and activation mechanisms in cardiomyocytes. J Biol Chem 2004, 279:19350-19361.
30. Goodnight J.A., Mischak H., Kolch W., Mushinski J.F. Immunocytochemical localization of eight protein kinase C isozymes overexpressed in NIH 3T3 fibroblasts. Isoform-specific association with microfilaments, Golgi, endoplasmic reticulum, and nuclear and cell membranes. J Biol Chem 1995, 270:9991-10001.
31. Majumder P.K., Pandey P., Sun X., Cheng K., Datta R., Saxena S., et al. Mitochondrial translocation of protein kinase C delta in phorbol ester-induced cytochrome c release and apoptosis. J Biol Chem 2000, 275:21793-21796.
32. Sumitomo M., Ohba M., Asakuma J., Asano T., Kuroki T., Hayakawa M. Protein kinase Cdelta amplifies ceramide formation via mitochondrial signaling in prostate cancer cells. J Clin Invest 2002, 109:827-836.
33. Baines C.P., Song C.X., Zheng Y.T., Wang G.W., Zhang J., Wang O.L., et al. Protein kinase Cepsilon interacts with and inhibits the permeability transition pore in cardiac mitochondria. Circ Res 2003, 92:873-880.
34. + channel opening and H2O2 inhibit the mitochondrial permeability transition. J Biol Chem 2006, 281:20801-20808.
35. Clerk A., Bogoyevitch M.A., Anderson M.B., Sugden P.H. Differential activation of protein kinase C isoforms by endothelin-1 and phenylephrine and subsequent stimulation of p42 and p44 mitogen-activated protein kinases in ventricular myocytes cultured from neonatal rat hearts. J Biol Chem 1994, 269:32848-32857.
36. Lehel C., Olah Z., Jakab G., Anderson W.B. Protein kinase C epsilon is localized to the Golgi via its zinc-finger domain and modulates Golgi function. Proc Natl Acad Sci USA 1995, 92:1406-1410.
37. Huang X.P., Pi Y., Lokuta A.J., Greaser M.L., Walker J.W. Arachidonic acid stimulates protein kinase C-epsilon redistribution in heart cells. J Cell Sci 1997, 110(Pt 14):1625-1634.
38. Disatnik M.H., Buraggi G., Mochly-Rosen D. Localization of protein kinase C isozymes in cardiac myocytes. Exp Cell Res 1994, 210:287-297.
39. Disatnik M.H., Jones S.N., Mochly-Rosen D. Stimulus-dependent subcellular localization of activated protein kinase C; a study with acidic fibroblast growth factor and transforming growth factor-beta 1 in cardiac myocytes. J Mol Cell Cardiol 1995, 27:2473-2481.
40. Bowling N., Huang X., Sandusky G.E., Fouts R.L., Mintze K., Esterman M., et al. Protein kinase C-alpha and -epsilon modulate connexin-43 phosphorylation in human heart. J Mol Cell Cardiol 2001, 33:789-798.
41. Paul K., Ball N.A., Dorn G.W., Walsh R.A. Left ventricular stretch stimulates angiotensin II-mediated phosphatidylinositol hydrolysis and protein kinase C epsilon isoform translocation in adult guinea pig hearts. Circ Res 1997, 81:643-650.
42. VanWinkle W.B., Snuggs M.B., De Hostos E.L., Buja L.M., Woods A., Couchman J.R. Localization of the transmembrane proteoglycan syndecan-4 and its regulatory kinases in costameres of rat cardiomyocytes: a deconvolution microscopic study. Anat Rec 2002, 268:38-46.
43. Russell B., Curtis M.W., Koshman Y.E., Samarel A.M. Mechanical stress-induced sarcomere assembly for cardiac muscle growth in length and width. J Mol Cell Cardiol 2010, 48:817-823.
44. Vincent F., Duquesnes N., Christov C., Damy T., Samuel J.L., Crozatier B. Dual level of interactions between calcineurin and PKC-epsilon in cardiomyocyte stretch. Cardiovasc Res 2006, 71:97-107.
45. Gordon A.S., Yao L., Wu Z.L., Coe I.R., Diamond I. Ethanol alters the subcellular localization of delta- and epsilon protein kinase C in NG108-15 cells. Mol Pharmacol 1997, 52:554-559.
46. Jude S., Martel E., Vincent F., Besson P., Couet C., Ogilvie G.K., et al. Dietary long-chain n-3 fatty acids modify blood and cardiac phospholipids and reduce protein kinase-C-delta and protein kinase-C-epsilon translocation. Br J Nutr 2007, 98:1143-1151.
47. Miyamae M., Rodriguez M.M., Camacho S.A., Diamond I., Mochly-Rosen D., Figueredo V.M. Activation of epsilon protein kinase C correlates with a cardioprotective effect of regular ethanol consumption. Proc Natl Acad Sci USA 1998, 95:8262-8267.
48. Reddig P.J., Dreckschmidt N.E., Ahrens H., Simsiman R., Tseng C.P., Zou J., et al. Transgenic mice overexpressing protein kinase Cdelta in the epidermis are resistant to skin tumor promotion by 12-O-tetradecanoylphorbol-13-acetate. Cancer Res 1999, 59:5710-5718.
49. Ferreira JC, Brum PC, Mochly-Rosen D. betaIIPKC and epsilonPKC isozymes as potential pharmacological targets in cardiac hypertrophy and heart failure. J Mol Cell Cardiol in press [Ahead of print, Oct 28, 2010].
50. Lawson C.S., Downey J.M. Preconditioning: state of the art myocardial protection. Cardiovasc Res 1993, 27:542-550.
51. Inagaki K., Begley R., Ikeno F., Mochly-Rosen D. Cardioprotection by epsilon-protein kinase C activation from ischemia: continuous delivery and antiarrhythmic effect of an epsilon-protein kinase C-activating peptide. Circulation 2005, 111:44-50.
52. Inagaki K., Chen L., Ikeno F., Lee F.H., Imahashi K., Bouley D.M., et al. Inhibition of delta-protein kinase C protects against reperfusion injury of the ischemic heart in vivo. Circulation 2003, 108:2304-2307.
53. Inagaki K., Churchill E., Mochly-Rosen D. Epsilon protein kinase C as a potential therapeutic target for the ischemic heart. Cardiovasc Res 2006, 70:222-230.
54. + channel copurify and coreconstitute to form a functioning signaling module in proteoliposomes. Circ Res 2006, 99:878-883.
55. Baines C.P., Zhang J., Wang G.W., Zheng Y.T., Xiu J.X., Cardwell E.M., et al. Mitochondrial PKCepsilon and MAPK form signaling modules in the murine heart: enhanced mitochondrial PKCepsilon-MAPK interactions and differential MAPK activation in PKCepsilon-induced cardioprotection. Circ Res 2002, 90:390-397.
56. Ping P. Identification of novel signaling complexes by functional proteomics. Circ Res 2003, 93:595-603.
57. Churchill E.N., Mochly-Rosen D. The roles of PKCdelta and epsilon isoenzymes in the regulation of myocardial ischaemia/reperfusion injury. Biochem Soc Trans 2007, 35:1040-1042.
58. Naitoh K., Yano T., Miura T., Itoh T., Miki T., Tanno M., et al. Roles of Cx43-associated protein kinases in suppression of gap junction-mediated chemical coupling by ischemic preconditioning. Am J Physiol Heart Circ Physiol 2009, 296:H396-H403.
59. Li X., Heinzel F.R., Boengler K., Schulz R., Heusch G. Role of connexin 43 in ischemic preconditioning does not involve intercellular communication through gap junctions. J Mol Cell Cardiol 2004, 36:161-163.
60. Schulz R., Heusch G. Connexin 43 and ischemic preconditioning. Cardiovasc Res 2004, 62:335-344.
61. Takeishi Y., Ping P., Bolli R., Kirkpatrick D.L., Hoit B.D., Walsh R.A. Transgenic overexpression of constitutively active protein kinase C epsilon causes concentric cardiac hypertrophy. Circ Res 2000, 86:1218-1223.
62. Mochly-Rosen D., Wu G., Hahn H., Osinska H., Liron T., Lorenz J.N., et al. Cardiotrophic effects of protein kinase C epsilon: analysis by in vivo modulation of PKCepsilon translocation. Circ Res 2000, 86:1173-1179.
63. Goldspink P.H., Montgomery D.E., Walker L.A., Urboniene D., McKinney R.D., Geenen D.L., et al. Protein kinase Cepsilon overexpression alters myofilament properties and composition during the progression of heart failure. Circ Res 2004, 95:424-432.
64. Gu X., Bishop S.P. Increased protein kinase C and isozyme redistribution in pressure-overload cardiac hypertrophy in the rat. Circ Res 1994, 75:926-931.
65. Takeishi Y., Bhagwat A., Ball N.A., Kirkpatrick D.L., Periasamy M., Walsh R.A. Effect of angiotensin-converting enzyme inhibition on protein kinase C and SR proteins in heart failure. Am J Physiol 1999, 276:H53-H62.
66. Simonis G., Briem S.K., Schoen S.P., Bock M., Marquetant R., Strasser R.H. Protein kinase C in the human heart: differential regulation of the isoforms in aortic stenosis or dilated cardiomyopathy. Mol Cell Biochem 2007, 305:103-111.
67. Morel O.E., Buvry A., Le Corvoisier P., Tual L., Favret F., Leon-Velarde F., et al. Effects of nifedipine-induced pulmonary vasodilatation on cardiac receptors and protein kinase C isoforms in the chronically hypoxic rat. Pflugers Arch 2003, 446:356-364.
68. Mohammadi K., Rouet-Benzineb P., Laplace M., Crozatier B. Protein kinase C activity and expression in rabbit left ventricular hypertrophy. J Mol Cell Cardiol 1997, 29:1687-1694.
69. Fryer L.G., Holness M.J., Decock J.B., Sugden M.C. Cardiac protein kinase C expression in two models of cardiac hypertrophy associated with an activated cardiac renin-angiotensin system: effects of experimental hyperthyroidism and genetic hypertension (the mRen-2 rat). J Endocrinol 1998, 158:27-33.
70. Braun M.U., LaRosee P., Simonis G., Borst M.M., Strasser R.H. Regulation of protein kinase C isozymes in volume overload cardiac hypertrophy. Mol Cell Biochem 2004, 262:135-143.
71. Koide Y., Tamura K., Suzuki A., Kitamura K., Yokoyama K., Hashimoto T., et al. Differential induction of protein kinase C isoforms at the cardiac hypertrophy stage and congestive heart failure stage in Dahl salt-sensitive rats. Hypertens Res 2003, 26:421-426.
72. 2+-sensitive isoforms in the failing human heart. Circulation 1999, 99:384-391.
73. Ron D., Chen C.H., Caldwell J., Jamieson L., Orr E., Mochly-Rosen D. Cloning of an intracellular receptor for protein kinase C: a homolog of the beta subunit of G proteins. Proc Natl Acad Sci USA 1994, 91:839-843.
74. Csukai M., Chen C.H., De Matteis M.A., Mochly-Rosen D. The coatomer protein beta'-COP, a selective binding protein (RACK) for protein kinase Cepsilon. J Biol Chem 1997, 272:29200-29206.
75. Johnson J.A., Gray M.O., Chen C.H., Mochly-Rosen D. A protein kinase C translocation inhibitor as an isozyme-selective antagonist of cardiac function. J Biol Chem 1996, 271:24962-24966.
76. Dorn G.W., Souroujon M.C., Liron T., Chen C.H., Gray M.O., Zhou H.Z., et al. Sustained in vivo cardiac protection by a rationally designed peptide that causes epsilon protein kinase C translocation. Proc Natl Acad Sci USA 1999, 96:12798-12803.
77. Sossin W.S., Schwartz J.H. Ca(2+)-independent protein kinase Cs contain an amino-terminal domain similar to the C2 consensus sequence. Trends Biochem Sci 1993, 18:207-208.
78. 2+/phospholipid-binding fold. Cell 1995, 80:929-938.
79. Essen L.O., Perisic O., Cheung R., Katan M., Williams R.L. Crystal structure of a mammalian phosphoinositide-specific phospholipase C delta. Nature 1996, 380:595-602.
80. Perisic O., Fong S., Lynch D.E., Bycroft M., Williams R.L. Crystal structure of a calcium-phospholipid binding domain from cytosolic phospholipase A2. J Biol Chem 1998, 273:1596-1604.
81. Pappa H., Murray-Rust J., Dekker L.V., Parker P.J., McDonald N.Q. Crystal structure of the C2 domain from protein kinase C-delta. Structure 1998, 6:885-894.
82. Ochoa W.F., Garcia-Garcia J., Fita I., Corbalan-Garcia S., Verdaguer N., Gomez-Fernandez J.C. Structure of the C2 domain from novel protein kinase Cepsilon. A membrane binding model for Ca(2+)-independent C2 domains. J Mol Biol 2001, 311:837-849.
83. Corbalan-Garcia S., Sanchez-Carrillo S., Garcia-Garcia J., Gomez-Fernandez J.C. Characterization of the membrane binding mode of the C2 domain of PKC epsilon. Biochemistry 2003, 42:11661-11668.
84. Benes C.H., Wu N., Elia A.E., Dharia T., Cantley L.C., Soltoff S.P. The C2 domain of PKCdelta is a phosphotyrosine binding domain. Cell 2005, 121:271-280.
85. Corbalan-Garcia S., Gomez-Fernandez J.C. Protein kinase C regulatory domains: the art of decoding many different signals in membranes. Biochim Biophys Acta 2006, 1761:633-654.
86. Giorgione J.R., Lin J.H., McCammon J.A., Newton A.C. Increased membrane affinity of the C1 domain of protein kinase Cdelta compensates for the lack of involvement of its C2 domain in membrane recruitment. J Biol Chem 2006, 281:1660-1669.
87. Stahelin R.V., Digman M.A., Medkova M., Ananthanarayanan B., Melowic H.R., Rafter J.D., et al. Diacylglycerol-induced membrane targeting and activation of protein kinase Cepsilon: mechanistic differences between protein kinases Cdelta and Cepsilon. J Biol Chem 2005, 280:19784-19793.
88. Zhang G., Kazanietz M.G., Blumberg P.M., Hurley J.H. Crystal structure of the cys2 activator-binding domain of protein kinase C delta in complex with phorbol ester. Cell 1995, 81:917-924.
89. Hurley J.H., Meyer T. Subcellular targeting by membrane lipids. Curr Opin Cell Biol 2001, 13:146-152.
90. Sanchez-Bautista S., Corbalan-Garcia S., Perez-Lara A., Gomez-Fernandez J.C. A comparison of the membrane binding properties of C1B domains of PKCgamma, PKCdelta, and PKCepsilon. Biophys J 2009, 96:3638-3647.
91. Wang Q.J., Fang T.W., Fenick D., Garfield S., Bienfait B., Marquez V.E., et al. The lipophilicity of phorbol esters as a critical factor in determining the pattern of translocation of protein kinase C delta fused to green fluorescent protein. J Biol Chem 2000, 275:12136-12146.
92. Stahelin R.V., Digman M.A., Medkova M., Ananthanarayanan B., Rafter J.D., Melowic H.R., et al. Mechanism of diacylglycerol-induced membrane targeting and activation of protein kinase Cdelta. J Biol Chem 2004, 279:29501-29512.
93. Kronfeld I., Kazimirsky G., Lorenzo P.S., Garfield S.H., Blumberg P.M., Brodie C. Phosphorylation of protein kinase Cdelta on distinct tyrosine residues regulates specific cellular functions. J Biol Chem 2000, 275:35491-35498.
94. Dries D.R., Gallegos L.L., Newton A.C. A single residue in the C1 domain sensitizes novel protein kinase C isoforms to cellular diacylglycerol production. J Biol Chem 2007, 282:826-830.
95. Lehel C., Olah Z., Jakab G., Szallasi Z., Petrovics G., Harta G., et al. Protein kinase C epsilon subcellular localization domains and proteolytic degradation sites. A model for protein kinase C conformational changes. J Biol Chem 1995, 270:19651-19658.
96. Steinberg S.F. Structural basis of protein kinase C isoform function. Physiol Rev 2008, 88:1341-1378.
97. Denning M.F., Wang Y., Nickoloff B.J., Wrone-Smith T. Protein kinase Cdelta is activated by caspase-dependent proteolysis during ultraviolet radiation-induced apoptosis of human keratinocytes. J Biol Chem 1998, 273:29995-30002.
98. Hoppe J., Hoppe V., Schafer R. Selective degradation of the PKC-epsilon isoform during cell death in AKR-2B fibroblasts. Exp Cell Res 2001, 266:64-73.
99. Sakurai Y., Onishi Y., Tanimoto Y., Kizaki H. Novel protein kinase C delta isoform insensitive to caspase-3. Biol Pharm Bull 2001, 24:973-977.
100. Jiang K., Apostolatos A.H., Ghansah T., Watson J.E., Vickers T., Cooper D.R., et al. Identification of a novel antiapoptotic human protein kinase C delta isoform, PKCdeltaVIII in NT2 cells. Biochemistry 2008, 47:787-797.
101. Shirai Y., Murakami T., Kuramasu M., Iijima L., Saito N. A novel PIP2 binding of epsilonPKC and its contribution to the neurite induction ability. J Neurochem 2007, 102:1635-1644.
102. Rybin V.O., Guo J., Gertsberg Z., Elouardighi H., Steinberg S.F. Protein kinase Cepsilon (PKCepsilon) and Src control PKCdelta activation loop phosphorylation in cardiomyocytes. J Biol Chem 2007, 282:23631-23638.
103. Sumandea M.P., Rybin V.O., Hinken A.C., Wang C., Kobayashi T., Harleton E., et al. Tyrosine phosphorylation modifies protein kinase C delta-dependent phosphorylation of cardiac troponin I. J Biol Chem 2008, 283:22680-22689.
104. Wang Q.J., Lu G., Schlapkohl W.A., Goerke A., Larsson C., Mischak H., et al. The V5 domain of protein kinase C plays a critical role in determining the isoform-specific localization, translocation, and biological function of protein kinase C-delta and -epsilon. Mol Cancer Res 2004, 2:129-140.
105. Aitken A., Collinge D.B., van Heusden B.P., Isobe T., Roseboom P.H., Rosenfeld G., et al. 14-3-3 proteins: a highly conserved, widespread family of eukaryotic proteins. Trends Biochem Sci 1992, 17:498-501.
106. Aitken A. 14-3-3 proteins: a historic overview. Semin Cancer Biol 2006, 16:162-172.
107. Toker A., Ellis C.A., Sellers L.A., Aitken A. Protein kinase C inhibitor proteins. Purification from sheep brain and sequence similarity to lipocortins and 14-3-3 protein. Eur J Biochem 1990, 191:421-429.
108. Isobe T., Hiyane Y., Ichimura T., Okuyama T., Takahashi N., Nakajo S., et al. Activation of protein kinase C by the 14-3-3 proteins homologous with Exo1 protein that stimulates calcium-dependent exocytosis. FEBS Lett 1992, 308:121-124.
109. Tanji M., Horwitz R., Rosenfeld G., Waymire J.C. Activation of protein kinase C by purified bovine brain 14-3-3: comparison with tyrosine hydroxylase activation. J Neurochem 1994, 63:1908-1916.
110. Gannon-Murakami L., Murakami K. Selective association of protein kinase C with 14-3-3 zeta in neuronally differentiated PC12 Cells. Stimulatory and inhibitory effect of 14-3-3 zeta in vivo. J Biol Chem 2002, 277:23116-23122.
111. Saurin A.T., Durgan J., Cameron A.J., Faisal A., Marber M.S., Parker P.J. The regulated assembly of a PKCepsilon complex controls the completion of cytokinesis. Nat Cell Biol 2008, 10:891-901.
112. Kostelecky B., Saurin A.T., Purkiss A., Parker P.J., McDonald N.Q. Recognition of an intra-chain tandem 14-3-3 binding site within PKCepsilon. EMBO Rep 2009, 10:983-989.
113. Diouf B., Collazos A., Labesse G., Macari F., Choquet A., Clair P., et al. A 20-amino acid module of protein kinase C{epsilon} involved in translocation and selective targeting at cell-cell contacts. J Biol Chem 2009, 284:18808-18815.
114. Ping P., Zhang J., Pierce W.M., Bolli R. Functional proteomic analysis of protein kinase C epsilon signaling complexes in the normal heart and during cardioprotection. Circ Res 2001, 88:59-62.
115. Klauck T.M., Faux M.C., Labudda K., Langeberg L.K., Jaken S., Scott J.D. Coordination of three signaling enzymes by AKAP79, a mammalian scaffold protein. Science 1996, 271:1589-1592.
116. Prekeris R., Mayhew M.W., Cooper J.B., Terrian D.M. Identification and localization of an actin-binding motif that is unique to the epsilon isoform of protein kinase C and participates in the regulation of synaptic function. J Cell Biol 1996, 132:77-90.
117. Prekeris R., Hernandez R.M., Mayhew M.W., White M.K., Terrian D.M. Molecular analysis of the interactions between protein kinase C-epsilon and filamentous actin. J Biol Chem 1998, 273:26790-26798.
118. Nakhost A., Forscher P., Sossin W.S. Binding of protein kinase C isoforms to actin in Aplysia. J Neurochem 1998, 71:1221-1231.
119. Huang X., Walker J.W. Myofilament anchoring of protein kinase C-epsilon in cardiac myocytes. J Cell Sci 2004, 117:1971-1978.
120. Violin J.D., Zhang J., Tsien R.Y., Newton A.C. A genetically encoded fluorescent reporter reveals oscillatory phosphorylation by protein kinase C. J Cell Biol 2003, 161:899-909.
121. Braun D.C., Garfield S.H., Blumberg P.M. Analysis by fluorescence resonance energy transfer of the interaction between ligands and protein kinase Cdelta in the intact cell. J Biol Chem 2005, 280:8164-8171.
122. Churchill E.N., Qvit N., Mochly-Rosen D. Rationally designed peptide regulators of protein kinase C. Trends Endocrinol Metab 2009, 20:25-33.