PKCε activation promotes FGF-2 exocytosis and induces endothelial cell proliferation and sprouting

Journal of Molecular and Cellular Cardiology

Volumn 63, Issue , 2013, Pages 107-117

  Monti, Martina ^a   Donnini, Sandra ^a   Morbidelli, Lucia ^a   Giachetti, Antonio ^a   Mochly Rosen, Daria ^b   Mignatti, Paolo ^c   Ziche, Marina ^a  

^a UNIVERSITY OF SIENA   (Italy)

^b STANFORD UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Angiogenesis; Endothelial cells; Exocytosis; Fibroblast growth factor 2; Protein kinase C ; Vascular endothelial growth factor

Indexed keywords

FIBROBLAST GROWTH FACTOR 2; FIBROBLAST GROWTH FACTOR RECEPTOR 1; METHYLAMINE; MITOGEN ACTIVATED PROTEIN KINASE 1; MITOGEN ACTIVATED PROTEIN KINASE 3; PROTEIN KINASE C EPSILON; PROTEIN TYROSINE KINASE INHIBITOR; STAT3 PROTEIN; VASCULOTROPIN;

ANIMAL CELL; ANTIANGIOGENIC ACTIVITY; ARTICLE; AUTOCRINE EFFECT; BIOTINYLATION; CELL GROWTH; CELL MEMBRANE; CELL PROLIFERATION; CONTROLLED STUDY; CORNEA; CORONARY VENULAR ENDOTHELIAL CELL; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME ACTIVITY; EXOCYTOSIS; IMMUNOFLUORESCENCE; IN VIVO STUDY; NONHUMAN; PARACRINE SIGNALING; PRIORITY JOURNAL; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; PROTEIN SYNTHESIS;

ORYCTOLAGUS CUNICULUS;

ANGIOGENESIS; ENDOTHELIAL CELLS; EXOCYTOSIS; FIBROBLAST GROWTH FACTOR-2; PROTEIN KINASE C Ε; VASCULAR ENDOTHELIAL GROWTH FACTOR;

ANIMALS; CATTLE; CELL MEMBRANE; CELL PROLIFERATION; ENDOTHELIAL CELLS; ENZYME ACTIVATION; EXOCYTOSIS; FIBROBLAST GROWTH FACTOR 2; GENE EXPRESSION REGULATION; MALE; MICE; NEOVASCULARIZATION, PHYSIOLOGIC; OLIGOPEPTIDES; PROTEIN KINASE C-EPSILON; PROTEIN TRANSPORT; RABBITS; VASCULAR ENDOTHELIAL GROWTH FACTOR A;

EID: 84882461852     PISSN: 00222828     EISSN: 10958584     Source Type: Journal    
DOI: 10.1016/j.yjmcc.2013.07.006     Document Type: Article

References (37)

1. Basu A., Sivaprasad U. Protein kinase C epsilon makes the life and death decision. Cell Signal 2007, 19(8):1633-1642.
2. 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(1):44-50.
3. Inagaki K., Churchill E., Mochly-Rosen D. Epsilon protein kinase C as a potential therapeutic target for the ischemic heart. Cardiovasc Res 2006, 70(2):222-230.
4. Monti M., Donnini S., Giachetti A., Mochly-Rosen D., Ziche M. deltaPKC inhibition or varepsilonPKC activation repairs endothelial vascular dysfunction by regulating eNOS post-translational modification. J Mol Cell Cardiol 2010, 48(4):746-756.
5. Budas G.R., Churchill E.N., Disatnik M.H., Sun L., Mochly-Rosen D. Mitochondrial import of PKC epsilon is mediated by HSP90: a role in cardioprotection from ischaemia and reperfusion injury. Cardiovasc Res 2010, 88(1):83-92.
6. Bright R., Sun G.H., Yenari M.A., Steinberg G.K., Mochly-Rosen D. Epsilon PKC confers acute tolerance to cerebral ischemic reperfusion injury. Neurosci Lett 2008, 441(1):120-124.
7. Bright R., Mochly-Rosen D. The role of protein kinase C in cerebral ischemic and reperfusion injury. Stroke 2005, 36(12):2781-2790.
8. Rask-Madsen C., King G.L. Differential regulation of VEGF signaling by PKC-alpha and PKC-epsilon in endothelial cells. Arterioscler Thromb Vasc Biol 2008, 28(5):919-924.
9. Murakami M., Nguyen L.T., Zhuang Z.W., Moodie K.L., Carmeliet P., Stan R.V., et al. The FGF system has a key role in regulating vascular integrity. J Clin Invest 2008, 118(10):3355-3366.
10. Pintucci G., Moscatelli D., Saponara F., Biernacki P.R., Baumann F.G., Bizekis C., et al. Lack of ERK activation and cell migration in FGF-2-deficient endothelial cells. FASEB J 2002, 16(6):598-600.
11. Gray M.O., Karliner J.S., Mochly-Rosen D. A selective epsilon-protein kinase C antagonist inhibits protection of cardiac myocytes from hypoxia-induced cell death. J Biol Chem 1997, 272(49):30945-30951.
12. 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(40):24962-24966.
13. 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 U S A 1999, 96(22):12798-12803.
14. Begley R., Liron T., Baryza J., Mochly-Rosen D. Biodistribution of intracellularly acting peptides conjugated reversibly to Tat. Biochem Biophys Res Commun 2004, 318(4):949-954.
15. Liron T., Chen L.E., Khaner H., Vallentin A., Mochly-Rosen D. Rational design of a selective antagonist of epsilon protein kinase C derived from the selective allosteric agonist, pseudo-RACK peptide. J Mol Cell Cardiol 2007, 42(4):835-841.
16. Schelling M.E., Meininger C.J., Hawker J.R., Granger H.J. Venular endothelial cells from bovine heart. Am J Physiol 1988, 254(6 Pt 2):H1211-H1217.
17. Ziche M., Morbidelli L., Masini E., Amerini S., Granger H.J., Maggi C.A., et al. Nitric oxide mediates angiogenesis in vivo and endothelial cell growth and migration in vitro promoted by substance P. J Clin Invest 1994, 94(5):2036-2044.
18. Finetti F., Basile A., Capasso D., Di Gaetano S., Di Stasi R., Pascale M., et al. Functional and pharmacological characterization of a VEGF mimetic peptide on reparative angiogenesis. Biochem Pharmacol 2012, 84(3):303-311.
19. Livak K.J., Schmittgen T.D. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) method. Methods 2001, 25(4):402-408.
20. Taverna S., Ghersi G., Ginestra A., Rigogliuso S., Pecorella S., Alaimo G., et al. Shedding of membrane vesicles mediates fibroblast growth factor-2 release from cells. J Biol Chem 2003, 278(51):51911-51919.
21. Gualandris A., Rusnati M., Belleri M., Nelli E.E., Bastaki M., Molinari-Tosatti M.P., et al. Basic fibroblast growth factor overexpression in endothelial cells: an autocrine mechanism for angiogenesis and angioproliferative diseases. Cell Growth Differ 1996, 7:147-160.
22. Pepper M.S., Mandriota S.J. Regulation of vascular endothelial growth factor receptor-2 (Flk-1) expression in vascular endothelial cells. Exp Cell Res 1998, 241(2):414-425.
23. Murakami M., Nguyen L.T., Hatanaka K., Schachterle W., Chen P.Y., Zhuang Z.W., et al. FGF-dependent regulation of VEGF receptor 2 expression in mice. J Clin Invest 2011, 121(7):2668-2678.
24. Finetti F., Donnini S., Giachetti A., Morbidelli L., Ziche M. Prostaglandin E(2) primes the angiogenic switch via a synergic interaction with the fibroblast growth factor-2 pathway. Circ Res 2009, 105(7):657-666.
25. Mignatti P., Morimoto T., Rifkin D.B. Basic fibroblast growth factor, a protein devoid of secretory signal sequence, is released by cells via a pathway independent of the endoplasmic reticulum-Golgi complex. J Cell Physiol 1992, 151(1):81-93.
26. Finetti F., Solito R., Morbidelli L., Giachetti A., Ziche M., Donnini S. Prostaglandin E2 regulates angiogenesis via activation of fibroblast growth factor receptor-1. J Biol Chem 2008, 283:2139-2146.
27. Tsopanoglou N.E., Pipili-Synetos E., Maragoudakis M.E. Protein kinase C involvement in the regulation of angiogenesis. J Vasc Res 1993, 30:202-208.
28. Taylor C.J., Motamed K., Lilly B. Protein kinase C and downstream signaling pathways in a three-dimensional model of phorbol ester-induced angiogenesis. Angiogenesis 2006, 9(2):39-51.
29. Jin Z.Q., Zhou H.Z., Zhu P., Honbo N., Mochly-Rosen D., Messing R.O., et al. Cardioprotection mediated by sphingosine-1-phosphate and ganglioside GM-1 in wild-type and PKC epsilon knockout mouse hearts. Am J Physiol Heart Circ Physiol 2002, 282(6):H1970-H1977.
30. Liu Q.H., Zheng Y.M., Korde A.S., Li X.Q., Ma J., Takeshima H., et al. Protein kinase C-epsilon regulates local calcium signaling in airway smooth muscle cells. Am J Respir Cell Mol Biol 2009, 40(6):663-671.
31. Schechtman D., Mochly-Rosen D. Isozyme-specific inhibitors and activators of protein kinase C. Methods Enzymol 2002, 345:470-489.
32. 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 U S A 2001, 98(20):11114-11119.
33. Brandman R., Disatnik M.H., Churchill E., Mochly-Rosen D. Peptides derived from the C2 domain of protein kinase C epsilon (epsilon PKC) modulate epsilon PKC activity and identify potential protein-protein interaction surfaces. J Biol Chem 2007, 282(6):4113-4123.
34. Nickel W. The mystery of nonclassical protein secretion. A current view on cargo proteins and potential export routes. Eur J Biochem 2003, 270:2109-2119.
35. Keller M., Ruegg A., Werner S., Beer H.D. Active caspase-1 is a regulator of unconventional protein secretion. Cell 2008, 132:818-831.
36. Seghezzi G., Patel S., Ren C.J., Gualandris A., Pintucci G., Robbins E.S., et al. Fibroblast growth factor-2 (FGF-2) induces vascular endothelial growth factor (VEGF) expression in the endothelial cells of forming capillaries: an autocrine mechanism contributing to angiogenesis. J Cell Biol 1998, 141(7):1659-1673.
37. Vuorio T., Jauhiainen S., Ylä-Herttuala S. Pro- and anti-angiogenic therapy and atherosclerosis with special emphasis on vascular endothelial growth factors. Expert Opin Biol Ther 2012, 12(1):79-92.