The syndecan-4/protein kinase Cα pathway mediates prostaglandin E2-induced extracellular regulated kinase (ERK) activation in endothelial cells and angiogenesis in vivo

Journal of Biological Chemistry

Volumn 288, Issue 18, 2013, Pages 12712-12721

  Corti, Federico ^a   Finetti, Federica ^b   Ziche, Marina ^b   Simons, Michael ^a  

^a YALE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF SIENA   (Italy)

Author keywords

[No Author keywords available]

Indexed keywords

ANGIOGENESIS; CYTOPLASMIC DOMAINS; ERK ACTIVATION; EXTRACELLULAR REGULATED KINASE ACTIVATIONS; PROSTAGLANDINE; PROTEIN KINASE C; PROTEOGLYCANS; TUMOR GROWTH;

BACTERIOPHAGES; ENZYMES; LIPIDS; MAMMALS; PROTEINS;

ENDOTHELIAL CELLS;

MITOGEN ACTIVATED PROTEIN KINASE; PROSTAGLANDIN E2; PROTEIN KINASE C ALPHA; SYNDECAN 4;

ANGIOGENESIS; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; ENDOTHELIUM CELL; ENZYME ACTIVATION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; MUTANT; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; RNA ISOLATION; UMBILICAL VEIN ENDOTHELIAL CELL; WESTERN BLOTTING;

ANGIOGENESIS; CELL SIGNALING; PROSTAGLANDINS; PROTEIN KINASE C (PKC); PROTEOGLYCAN; SYNDECAN 4;

ANIMALS; DINOPROSTONE; ENZYME ACTIVATION; EXTRACELLULAR SIGNAL-REGULATED MAP KINASES; HUMAN UMBILICAL VEIN ENDOTHELIAL CELLS; HUMANS; MAP KINASE SIGNALING SYSTEM; MICE; MICE, KNOCKOUT; NEOVASCULARIZATION, PHYSIOLOGIC; PROTEIN KINASE C-ALPHA; SYNDECAN-4;

MUS;

EID: 84877131728     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.452383     Document Type: Article

References (44)

1. Aoki, T., and Narumiya, S. (2012) Prostaglandins and chronic inflammation. Trends Pharmacol. Sci. 33, 304-311
2. Wang, D., and Dubois, R. N. (2010) Eicosanoids and cancer. Nat. Rev. Cancer 10, 181-193
3. Finetti, F., Solito, R., Morbidelli, L., Giachetti, A., Ziche, M., and Donnini, S. (2008) Prostaglandin E2 regulates angiogenesis via activation of fibroblast growth factor receptor-1. J. Biol. Chem. 283, 2139-2146
4. Buchanan, F. G., Gorden, D. L., Matta, P., Shi, Q., Matrisian, L. M., and DuBois, R. N. (2006) Role of β-arrestin 1 in the metastatic progression of colorectal cancer. Proc. Natl. Acad. Sci. U.S.A. 103, 1492-1497 (Pubitemid 43191193)
5. Liang, X., Lin, L., Woodling, N. S., Wang, Q., Anacker, C., Pan, T., Merchant, M., and Andreasson, K. (2011) Signaling via the prostaglandin E(2) receptor EP4 exerts neuronal and vascular protection in a mouse model of cerebral ischemia. J. Clin. Invest. 121, 4362-4371
6. Xin, X., Majumder, M., Girish, G. V., Mohindra, V., Maruyama, T., and Lala, P. K. (2012) Targeting COX-2 and EP4 to control tumor growth, angiogenesis, lymphangiogenesis and metastasis to the lungs and lymph nodes in a breast cancer model. Lab. Invest. 92, 1115-1128
7. Tkachenko, E., Rhodes, J. M., and Simons, M. (2005) Syndecans. New kids on the signaling block. Circ. Res. 96, 488-500 (Pubitemid 40463457)
8. Volk, R., Schwartz, J. J., Li, J., Rosenberg, R. D., and Simons, M. (1999) The role of syndecan cytoplasmic domain in basic fibroblast growth factor-dependent signal transduction. J. Biol. Chem. 274, 24417-24424
9. Chua, C. C., Rahimi, N., Forsten-Williams, K., and Nugent, M. A. (2004) Heparan sulfate proteoglycans function as receptors for fibroblast growth factor-2 activation of extracellular signal-regulated kinases 1 and 2. Circ. Res. 94, 316-323 (Pubitemid 38240722)
10. Elfenbein, A., Rhodes, J. M., Meller, J., Schwartz, M. A., Matsuda, M., and Simons, M. (2009) Suppression of RhoG activity is mediated by a syndecan 4-synectin-RhoGDI1 complex and is reversed by PKCα in a Rac1 activation pathway. J. Cell Biol. 186, 75-83
11. Horowitz, A., and Simons, M. (1998) Phosphorylation of the cytoplasmic tail of syndecan-4 regulates activation of protein kinase Cα. J. Biol. Chem. 273, 25548-25551 (Pubitemid 28475771)
12. Echtermeyer, F., Streit, M., Wilcox-Adelman, S., Saoncella, S., Denhez, F., Detmar, M., and Goetinck, P. (2001) Delayed wound repair and impaired angiogenesis in mice lacking syndecan-4. J. Clin. Invest. 107, R9-R14 (Pubitemid 32096841)
13. Matsui, Y., Ikesue, M., Danzaki, K., Morimoto, J., Sato, M., Tanaka, S., Kojima, T., Tsutsui, H., and Uede, T. (2011) Syndecan-4 prevents cardiac rupture and dysfunction after myocardial infarction. Circ. Res. 108, 1328-1339
14. Ishiguro, K., Kadomatsu, K., Kojima, T., Muramatsu, H., Iwase, M., Yoshikai, Y., Yanada, M., Yamamoto, K., Matsushita, T., Nishimura, M., Kusugami, K., Saito, H., and Muramatsu, T. (2001) Syndecan-4 deficiency leads to high mortality of lipopolysaccharide-injected mice. J. Biol. Chem. 276, 47483-47488
15. Allport, J. R., Lim, Y. C., Shipley, J. M., Senior, R. M., Shapiro, S. D., Matsuyoshi, N., Vestweber, D., and Luscinskas, F. W. (2002) Neutrophils from MMP-9- or neutrophil elastase-deficient mice show no defect in transendothelial migration under flow in vitro. J. Leukocyte Biol. 71, 821-828
16. Partovian, C., Ju, R., Zhuang, Z. W., Martin, K. A., and Simons, M. (2008) Syndecan-4 regulates subcellular localization of mTOR complex 2 and Akt activation in a PKCα-dependent manner in endothelial cells. Mol. Cell 32, 140-149
17. Coleman, R. A., Grix, S. P., Head, S. A., Louttit, J. B., Mallett, A., and Sheldrick, R. L. (1994) A novel inhibitory prostanoid receptor in piglet saphenous vein. Prostaglandins 47, 151-168 (Pubitemid 24089361)
18. Schneider, C. A., Rasband, W. S., and Eliceiri, K. W. (2012) NIH Image to ImageJ: 25 years of image analysis. Nat. Meth. 9, 671-675
19. Gassmann, M., Grenacher, B., Rohde, B., and Vogel, J. (2009) Quantifying Western blots. Pitfalls of densitometry. Electrophoresis 30, 1845-1855
20. Meijering, E., Jacob, M., Sarria, J. C., Steiner, P., Hirling, H., and Unser, M. (2004) Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images. Cytometry A 58, 167-176 (Pubitemid 38509178)
21. Finetti, F., Donnini, S., Giachetti, A., Morbidelli, L., and Ziche, M. (2009) Prostaglandin E(2) primes the angiogenic switch via a synergic interaction with the fibroblast growth factor-2 pathway. Circ. Res. 105, 657-666
22. Fujino, H., Xu, W., and Regan, J. W. (2003) Prostaglandin E2 induced functional expression of early growth response factor-1 by EP4, but not EP2, prostanoid receptors via the phosphatidylinositol 3-kinase and extracellular signal-regulated kinases. J. Biol. Chem. 278, 12151-12156 (Pubitemid 36800194)
23. Pozzi, A., Yan, X., Macias-Perez, I., Wei, S., Hata, A. N., Breyer, R. M., Morrow, J. D., and Capdevila, J. H. (2004) Colon carcinoma cell growth is associated with prostaglandin E2/EP4 receptor-evoked ERK activation. J. Biol. Chem. 279, 29797-29804 (Pubitemid 38915863)
24. Rao, R., Redha, R., Macias-Perez, I., Su, Y., Hao, C., Zent, R., Breyer, M. D., and Pozzi, A. (2007) Prostaglandin E2-EP4 receptor promotes endothelial cell migration via ERK activation and angiogenesis in vivo. J. Biol. Chem. 282, 16959-16968 (Pubitemid 47093223)
25. Horowitz, A., Tkachenko, E., and Simons, M. (2002) Fibroblast growth factor-specific modulation of cellular response by syndecan-4. J. Cell Biol. 157, 715-725 (Pubitemid 34839798)
26. Tkachenko, E., and Simons, M. (2002) Clustering induces redistribution of syndecan-4 core protein into raft membrane domains. J. Biol. Chem. 277, 19946-19951 (Pubitemid 34967516)
27. Horowitz, A., and Simons, M. (1998) Regulation of syndecan-4 phosphorylation in vivo. J. Biol. Chem. 273, 10914-10918 (Pubitemid 28204929)
28. Murakami, M., Horowitz, A., Tang, S., Ware, J. A., and Simons, M. (2002) Protein kinase C (PKC) Δ regulates PKCα activity in a Syndecan-4-dependent manner. J. Biol. Chem. 277, 20367-20371 (Pubitemid 34967331)
29. Mastyugin, V., McWhinnie, E., Labow, M., and Buxton, F. (2004) A quantitative high-throughput endothelial cell migration assay. J. Biomol. Screen. 9, 712-718
30. Pai, R., Szabo, I. L., Soreghan, B. A., Atay, S., Kawanaka, H., and Tarnawski, A. S. (2001) PGE(2) stimulates VEGF expression in endothelial cells via ERK2/JNK1 signaling pathways. Biochem. Biophys. Res. Commun. 286, 923-928 (Pubitemid 32924860)
31. Dormond, O., Bezzi, M., Mariotti, A., and Ruegg, C. (2002) Prostaglandin E2 promotes integrin α Vβ 3-dependent endothelial cell adhesion, Rac-activation, and spreading through cAMP/PKA-dependent signaling. J. Biol. Chem. 277, 45838-45846 (Pubitemid 35417562)
32. Salcedo, R., Zhang, X., Young, H. A., Michael, N., Wasserman, K., Ma, W. H., Martins-Green, M., Murphy, W. J., and Oppenheim, J. J. (2003) Angiogenic effects of prostaglandin E2 are mediated by up-regulation of CXCR4 on human microvascular endothelial cells. Blood 102, 1966-1977 (Pubitemid 37122368)
33. Zhang, Y., and Daaka, Y. (2011) PGE2 promotes angiogenesis through EP4 and PKA Cγ pathway. Blood 118, 5355-5364
34. Dada, S., Demartines, N., and Dormond, O. (2008) mTORC2 regulates PGE2-mediated endothelial cell survival and migration. Biochem. Biophys. Res. Commun. 372, 875-879
35. Wang, A., Nomura, M., Patan, S., and Ware, J. A. (2002) Inhibition of protein kinase Cα prevents endothelial cell migration and vascular tube formation in vitro and myocardial neovascularization in vivo. Circ. Res. 90, 609-616 (Pubitemid 34640912)
36. Kolch, W., Heidecker, G., Kochs, G., Hummel, R., Vahidi, H., Mischak, H., Finkenzeller, G., Marmé, D., and Rapp, U. R. (1993) Protein kinase C α activates RAF-1 by direct phosphorylation. Nature 364, 249-252 (Pubitemid 23257085)
37. Marais, R., Light, Y., Mason, C., Paterson, H., Olson, M. F., and Marshall, C. J. (1998) Requirement of Ras-GTP-Raf complexes for activation of Raf-1 by protein kinase C. Science 280, 109-112 (Pubitemid 28169093)
38. Clark, J. A., Black, A. R., Leontieva, O. V., Frey, M. R., Pysz, M. A., Kunneva, L., Woloszynska-Read, A., Roy, D., and Black, J. D. (2004) Involvement of the ERK signaling cascade in protein kinase C-mediated cell cycle arrest in intestinal epithelial cells. J. Biol. Chem. 279, 9233-9247 (Pubitemid 38295987)
39. Xu, H., Czerwinski, P., Hortmann, M., Sohn, H. Y., Förstermann, U., and Li, H. (2008) Protein kinase C α promotes angiogenic activity of human endothelial cells via induction of vascular endothelial growth factor. Cardiovasc. Res. 78, 349-355 (Pubitemid 351556090)
40. Favata, M. F., Horiuchi, K. Y., Manos, E. J., Daulerio, A. J., Stradley, D. A., Feeser, W. S., Van Dyk, D. E., Pitts, W. J., Earl, R. A., Hobbs, F., Copeland, R. A., Magolda, R. L., Scherle, P. A., and Trzaskos, J. M. (1998) Identification of a novel inhibitor of mitogen-activated protein kinase kinase. J. Biol. Chem. 273, 18623-18632 (Pubitemid 28334795)
41. Nakanishi, M., and Rosenberg, D. W. (2013) Multifaced roles of PGE2 in inflammation and cancer. Sem. Immunopathol. 35, 123-137
42. Rothwell, P. M., Price, J. F., Fowkes, F. G., Zanchetti, A., Roncaglioni, M. C., Tognoni, G., Lee, R., Belch, J. F., Wilson, M., Mehta, Z., and Meade, T. W. (2012) Short-term effects of daily aspirin on cancer incidence, mortality, and non-vascular death. Analysis of the time course of risks and benefits in 51 randomised controlled trials. Lancet 379, 1602-1612
43. Rothwell, P. M., Wilson, M., Price, J. F., Belch, J. F., Meade, T. W., and Mehta, Z. (2012) Effect of daily aspirin on risk of cancer metastasis. A study of incident cancers during randomised controlled trials. Lancet 379, 1591-1601
44. Harris, R. E. (2009) Cyclooxygenase-2 (cox-2) blockade in the chemoprevention of cancers of the colon, breast, prostate, and lung. Inflammopharmacology 17, 55-67