Reciprocal regulation of syndecan-2 and notch signaling in vascular smooth muscle cells

Journal of Biological Chemistry

Volumn 287, Issue 20, 2012, Pages 16111-16120

  Zhao, Ning ^a,b   Liu, Hua ^c   Lilly, Brenda ^a,b  

^a NATIONWIDE CHILDREN S HOSPITAL   (United States)

^b OHIO STATE UNIVERSITY   (United States)

^c MEDICAL COLLEGE OF GEORGIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BLOOD VESSELS; CELL MEMBRANES; CELL SIGNALING; CYTOLOGY; ENDOTHELIAL CELLS; GENE EXPRESSION; PROTEINS; SIGNALING; SULFUR COMPOUNDS;

CELL SURFACE RECEPTORS; DIFFERENTIATION MARKERS; RECEPTOR INTERACTION; RECIPROCAL REGULATION; SIGNALING INTERACTIONS; SIGNALING MOLECULES; SMOOTH MUSCLE CELLS; VASCULAR SMOOTH MUSCLE CELLS;

MUSCLE;

ALPHA SMOOTH MUSCLE ACTIN; NOTCH RECEPTOR; NOTCH2 RECEPTOR; NOTCH3 RECEPTOR; SYNDECAN 2;

ARTICLE; CELL COMMUNICATION; CELL CONTACT; CELL DIFFERENTIATION; CELL INTERACTION; CONTROLLED STUDY; ENDOTHELIUM CELL; GENE EXPRESSION; HUMAN; HUMAN CELL; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; SMOOTH MUSCLE FIBER; VASCULAR SMOOTH MUSCLE;

EID: 84860843367     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.322107     Document Type: Article

References (39)

1. Armulik, A., Genové, G., and Betsholtz, C. (2011) Pericytes: developmental, physiological, and pathological perspectives, problems, and promises. Dev. Cell 21, 193-215
2. Gaengel, K., Genové, G., Armulik, A., and Betsholtz, C. (2009) Endothelial- mural cell signaling in vascular development and angiogenesis. Arterioscler. Thromb. Vasc. Biol. 29, 630-638
3. Brouillard, P., and Vikkula, M. (2003) Vascular malformations: localized defects in vascular morphogenesis. Clin. Genet. 63, 340-351 (Pubitemid 36944077)
4. Mombouli, J. V., and Vanhoutte, P. M. (1999) Endothelial dysfunction: from physiology to therapy. J. Mol. Cell. Cardiol. 31, 61-74
5. Gridley, T. (2007) Notch signaling in vascular development and physiology. Development 134, 2709-2718
6. Morrow, D., Guha, S., Sweeney, C., Birney, Y., Walshe, T., O'Brien, C., Walls, D., Redmond, E. M., and Cahill, P. A. (2008) Notch and vascular smooth muscle cell phenotype. Circ. Res. 103, 1370-1382
7. Baron, M. (2003) An overview of the Notch signaling pathway. Semin. Cell Dev. Biol. 14, 113-119
8. Bray, S. J. (2006) Notch signalling: a simple pathway becomes complex. Nat. Rev. Mol. Cell. Biol. 7, 678-689
9. Fischer, A., and Gessler, M. (2007) Delta-Notch-and then? Protein interactions and proposed modes of repression by Hes and Hey bHLH factors. Nucleic Acids Res. 35, 4583-4596 (Pubitemid 47250333)
10. Gridley, T. (2010) Notch signaling in the vasculature. Curr. Top. Dev. Biol. 92, 277-309
11. High, F. A., Lu, M. M., Pear, W. S., Loomes, K. M., Kaestner, K. H., and Epstein, J. A. (2008) Endothelial expression of the Notch ligand Jagged1 is required for vascular smooth muscle development. Proc. Natl. Acad. Sci. U.S.A. 105, 1955-1959 (Pubitemid 351439446)
12. Liu, H., Kennard, S., and Lilly, B. (2009)NOTCH3expression is induced in mural cells through an autoregulatory loop that requires endothelial expressed JAGGED1. Circ. Res. 104, 466-475
13. Alexopoulou, A. N., Multhaupt, H. A., and Couchman, J. R. (2007) Syndecans in wound healing, inflammation, and vascular biology. Int. J. Biochem. Cell Biol. 39, 505-528 (Pubitemid 46099032)
14. Tkachenko, E., Rhodes, J. M., and Simons, M. (2005) Syndecans: new kids on the signaling block. Circ. Res. 96, 488-500 (Pubitemid 40463457)
15. Essner, J. J., Chen, E., and Ekker, S. C. (2006) Syndecan-2. Int. J. Biochem. Cell Biol. 38, 152-156 (Pubitemid 41619444)
16. Chen, E., Hermanson, S., and Ekker, S. C. (2004) Syndecan-2 is essential for angiogenic sprouting during zebrafish development. Blood 103, 1710-1719 (Pubitemid 38268963)
17. Fears, C. Y., Gladson, C. L., and Woods, A. (2006) Syndecan-2 is expressed in the microvasculature of gliomas and regulates angiogenic processes in microvascular endothelial cells. J. Biol. Chem. 281, 14533-14536 (Pubitemid 43855155)
18. Noguer, O., Villena, J., Lorita, J., Vilaró, S., and Reina, M. (2009) Syndecan- 2 down-regulation impairs angiogenesis in human microvascular endothelial cells. Exp. Cell Res. 315, 795-808
19. Kramer, K. L., and Yost, H. J. (2002) Ectodermal syndecan-2 mediates left-right axis formation in migrating mesoderm as a cell-nonautonomous Vg1 cofactor. Dev. Cell 2, 115-124 (Pubitemid 34065911)
20. Granés, F., García, R., Casaroli-Marano, R. P., Castel, S., Rocamora, N., Reina, M., Ureña, J. M., and Vilaró, S. (1999) Syndecan-2 induces filopodia by active cdc42Hs. Exp. Cell Res. 248, 439-456
21. Arrington, C. B., and Yost, H. J. (2009) Extra-embryonic syndecan-2 regulates organ primordial migration and fibrillogenesis throughout the zebrafish embryo. Development 136, 3143-3152
22. Choi, S., Kim, Y., Park, H., Han, I. O., Chung, E., Lee, S. Y., Kim, Y. B., Lee, J. W., Oh, E. S., and Yi, J. Y. (2009) Syndecan-2 overexpression regulates adhesion and migration through cooperation with integrin α2. Biochem. Biophys. Res. Commun. 384, 231-235
23. Couchman, J. R. (2010) Transmembrane signaling proteoglycans. Annu. Rev. Cell Dev. Biol. 26, 89-114
24. Chen, L., Klass, C., and Woods, A. (2004) Syndecan-2 regulates transforming growth factor-β signaling. J. Biol. Chem. 279, 15715-15718 (Pubitemid 38509254)
25. McCright, B., Gao, X., Shen, L., Lozier, J., Lan, Y., Maguire, M., Herzlinger, D., Weinmaster, G., Jiang, R., and Gridley, T. (2001) Defects in development of the kidney, heart, and eye vasculature in mice homozygous for a hypomorphic Notch2 mutation. Development 128, 491-502 (Pubitemid 32229592)
26. Krebs, L. T., Xue, Y., Norton, C. R., Sundberg, J. P., Beatus, P., Lendahl, U., Joutel, A., and Gridley, T. (2003) Characterization of Notch3-deficient mice: normal embryonic development and absence of genetic interactions with a Notch1 mutation. Genesis 37, 139-143 (Pubitemid 37486875)
27. Kennard, S., Liu, H., and Lilly, B. (2008) Transforming growth factor-β(TGF- 1) down-regulates Notch3 in fibroblasts to promote smooth muscle gene expression. J. Biol. Chem. 283, 1324-1333
28. Lilly, B., and Kennard, S. (2009) Differential gene expression in a coculture model of angiogenesis reveals modulation of select pathways and a role for Notch signaling. Physiol. Genomics 36, 69-78
29. Weng, A. P., Nam, Y., Wolfe, M. S., Pear, W. S., Griffin, J. D., Blacklow, S. C., and Aster, J. C. (2003) Growth suppression of pre-T acute lymphoblastic leukemia cells by inhibition of notch signaling. Mol. Cell. Biol. 23, 655-664 (Pubitemid 36050558)
30. Domenga, V., Fardoux, P., Lacombe, P., Monet, M., Maciazek, J., Krebs, L. T., Klonjkowski, B., Berrou, E., Mericskay, M., Li, Z., Tournier-Lasserve, E., Gridley, T., and Joutel, A. (2004) Notch3 is required for arterial identity and maturation of vascular smooth muscle cells. Genes Dev. 18, 2730-2735 (Pubitemid 39507766)
31. Li, Y., Takeshita, K., Liu, P. Y., Satoh, M., Oyama, N., Mukai, Y., Chin, M. T., Krebs, L., Kotlikoff, M. I., Radtke, F., Gridley, T., and Liao, J. K. (2009) Smooth muscle Notch1 mediates neointimal formation after vascular injury. Circulation 119, 2686-2692
32. Varadkar, P. A., Kraman, M., and McCright, B. (2009) Generation of mice that conditionally express the activation domain of Notch2. Genesis 47, 573-578
33. Liu, H., Zhang, W., Kennard, S., Caldwell, R. B., and Lilly, B. (2010) Notch3 is critical for proper angiogenesis and mural cell investment. Circ. Res. 107, 860-870
34. Fukai, N., Kenagy, R. D., Chen, L., Gao, L., Daum, G., and Clowes, A. W. (2009) Syndecan-1: an inhibitor of arterial smooth muscle cell growth and intimal hyperplasia. Arterioscler. Thromb. Vasc. Biol. 29, 1356-1362
35. Ikesue, M., Matsui, Y., Ohta, D., Danzaki, K., Ito, K., Kanayama, M., Kurotaki, D., Morimoto, J., Kojima, T., Tsutsui, H., and Uede, T. (2011) Syndecan- 4 deficiency limits neointimal formation after vascular injury by regulating vascular smooth muscle cell proliferation and vascular progenitor cell mobilization. Arterioscler. Thromb. Vasc. Biol. 31, 1066-1074
36. Rauch, B. H., Millette, E., Kenagy, R. D., Daum, G., Fischer, J. W., and Clowes, A. W. (2005) Syndecan-4 is required for thrombin-induced migration and proliferation in human vascular smooth muscle cells. J. Biol. Chem. 280, 17507-17511 (Pubitemid 41389223)
37. Halden, Y., Rek, A., Atzenhofer, W., Szilak, L., Wabnig, A., and Kungl, A. J. (2004) Interleukin-8 binds to syndecan-2 on human endothelial cells. Biochem. J. 377, 533-538 (Pubitemid 38142209)
38. Cizmeci-Smith, G., Langan, E., Youkey, J., Showalter, L. J., and Carey, D. J. (1997) Syndecan-4 is a primary-response gene induced by basic fibroblast growth factor and arterial injury in vascular smooth muscle cells. Arterioscler. Thromb. Vasc. Biol. 17, 172-180 (Pubitemid 27057340)
39. Pisconti, A., Cornelison, D. D., Olguín, H. C., Antwine, T. L., and Olwin, B. B. (2010) Syndecan-3 and Notch cooperate in regulating adult myogenesis. J. Cell Biol. 190, 427-441