Syndecan-4 shedding impairs macrovascular angiogenesis in diabetes mellitus

Biochemical and Biophysical Research Communications

Volumn 474, Issue 1, 2016, Pages 15-21

  Li, Ran ^a   Xie, Jun ^a   Wu, Han ^a   Li, Guannan ^a   Chen, Jianzhou ^a   Chen, Qinhua ^a   Wang, Lian ^a   Xu, Biao ^a  

^a MEDICAL SCHOOL OF NANJING UNIVERSITY   (China)

Author keywords

Diabetes mellitus; Shedding; Syndecan 4

Indexed keywords

ADVANCED GLYCATION END PRODUCT; SYNDECAN 4; SDC4 PROTEIN, MOUSE;

ADENOVIRIDAE; ANGIOGENESIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; AORTA ENDOTHELIUM; AORTIC RING (SLICE); ARTICLE; CONTROLLED STUDY; DIABETES MELLITUS; ENZYME LINKED IMMUNOSORBENT ASSAY; GENE; HUMAN; HUMAN CELL; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; RAT; SYND4 GENE; VASCULAR ENDOTHELIUM; VIRUS RECOMBINANT; WESTERN BLOTTING; ANIMAL; DIABETIC ANGIOPATHY; ENDOTHELIUM CELL; METABOLISM; NEOVASCULARIZATION (PATHOLOGY); PATHOLOGY; SPRAGUE DAWLEY RAT;

ANIMALS; DIABETIC ANGIOPATHIES; ENDOTHELIAL CELLS; MALE; MICE; NEOVASCULARIZATION, PATHOLOGIC; RATS; RATS, SPRAGUE-DAWLEY; SYNDECAN-4;

EID: 84964240707     PISSN: 0006291X     EISSN: 10902104     Source Type: Journal    
DOI: 10.1016/j.bbrc.2016.03.112     Document Type: Article

References (26)

1. R. Yarom, H. Zirkin, G. Stammler, and A.G. Rose Human coronary microvessels in diabetes and ischaemia. morphometric study of autopsy material J. Pathol. 166 1992 265 270
2. J. Waltenberger Impaired collateral vessel development in diabetes: potential cellular mechanisms and therapeutic implications Cardiovasc Res. 49 2001 554 560
3. A. Elfenbein, and M. Simons Syndecan-4 signaling at a glance J. Cell Sci. 126 2013 3799 3804
4. O. Haddad, E. Guyot, N. Marinval, F. Chevalier, L. Maillard, L. Gadi, C. Laguillier-Morizot, O. Oudar, A. Sutton, N. Charnaux, and H. Hlawaty Heparanase and syndecan-4 are involved in low molecular weight fucoidan-induced angiogenesis Mar. Drugs 13 2015 6588 6608
5. F. Corti, F. Finetti, M. Ziche, and M. Simons The syndecan-4/protein kinase Calpha pathway mediates prostaglandin E2-induced extracellular regulated kinase (ERK) activation in endothelial cells and angiogenesis in vivo J. Biol. Chem. 288 2013 12712 12721
6. S. Das, A.J. Monteforte, G. Singh, M. Majid, M.B. Sherman, A.K. Dunn, and A.B. Baker Syndecan-4 enhances therapeutic angiogenesis after hind limb ischemia in mice with type 2 diabetes Adv. Healthc. Mater. 2016
7. Y. Matsui, M. Ikesue, K. Danzaki, J. Morimoto, M. Sato, S. Tanaka, T. Kojima, H. Tsutsui, and T. Uede Syndecan-4 prevents cardiac rupture and dysfunction after myocardial infarction Circ. Res. 108 2011 1328 1339
8. F. Echtermeyer, M. Streit, S. Wilcox-Adelman, S. Saoncella, F. Denhez, M. Detmar, and P. Goetinck Delayed wound repair and impaired angiogenesis in mice lacking syndecan-4 J. Clin. Invest. 107 2001 R9 R14
9. T.T. Vuong, T.M. Reine, A. Sudworth, T.G. Jenssen, and S.O. Kolset Syndecan-4 is a major syndecan in primary human endothelial cells in vitro, modulated by inflammatory stimuli and involved in wound healing J. Histochem. Cytochem. 63 2015 280 292
10. S.V. Subramanian, M.L. Fitzgerald, and M. Bernfield Regulated shedding of syndecan-1 and -4 ectodomains by thrombin and growth factor receptor activation J. Biol. Chem. 272 1997 14713 14720
11. M.L. Fitzgerald, Z. Wang, P.W. Park, G. Murphy, and M. Bernfield Shedding of syndecan-1 and -4 ectodomains is regulated by multiple signaling pathways and mediated by a TIMP-3-sensitive metalloproteinase J. Cell Biol. 148 2000 811 824
12. M.A. Julien, P. Wang, C.A. Haller, J. Wen, and E.L. Chaikof Mechanical strain regulates syndecan-4 expression and shedding in smooth muscle cells through differential activation of MAP kinase signaling pathways Am. J. Physiol. Cell Physiol. 292 2007 C517 C525
13. R. Ramnath, R.R. Foster, Y. Qiu, G. Cope, M.J. Butler, A.H. Salmon, P.W. Mathieson, R.J. Coward, G.I. Welsh, and S.C. Satchell Matrix metalloproteinase 9-mediated shedding of syndecan 4 in response to tumor necrosis factor alpha: a contributor to endothelial cell glycocalyx dysfunction Faseb J. 28 2014 4686 4699
14. X. Tan, N. Khalil, C. Tesarik, K. Vanapalli, V. Yaputra, H. Alkhouri, B.G. Oliver, C.L. Armour, and J.M. Hughes Th1 cytokine-induced syndecan-4 shedding by airway smooth muscle cells is dependent on mitogen-activated protein kinases Am. J. Physiol. Lung Cell Mol. Physiol. 302 2012 L700 L710
15. A. Schmidt, F. Echtermeyer, A. Alozie, K. Brands, and E. Buddecke Plasmin- and thrombin-accelerated shedding of syndecan-4 ectodomain generates cleavage sites at Lys(114)-Arg(115) and Lys(129)-Val(130) bonds J. Biol. Chem. 280 2005 34441 34446
16. M. Houston, M.A. Julien, S. Parthasarathy, and E.L. Chaikof Oxidized linoleic acid regulates expression and shedding of syndecan-4 Am. J. Physiol. Cell Physiol. 288 2005 C458 C466
17. J. Xie, J. Wang, R. Li, Q. Dai, Y. Yong, B. Zong, Y. Xu, E. Li, A. Ferro, and B. Xu Syndecan-4 over-expression preserves cardiac function in a rat model of myocardial infarction J. Mol. Cell Cardiol. 53 2012 250 258
18. M. Baker, S.D. Robinson, T. Lechertier, P.R. Barber, B. Tavora, G. D'Amico, D.T. Jones, B. Vojnovic, and K. Hodivala-Dilke Use of the mouse aortic ring assay to study angiogenesis Nat. Protoc. 7 2012 89 104
19. M.E. Strand, K.M. Herum, Z.A. Rana, B. Skrbic, E.T. Askevold, C.P. Dahl, M. Vistnes, A. Hasic, H. Kvaloy, I. Sjaastad, C.R. Carlson, T. Tonnessen, L. Gullestad, G. Christensen, and I.G. Lunde Innate immune signaling induces expression and shedding of the heparan sulfate proteoglycan syndecan-4 in cardiac fibroblasts and myocytes, affecting inflammation in the pressure-overloaded heart Febs J. 280 2013 2228 2247
20. T. Kojima, A. Takagi, M. Maeda, T. Segawa, A. Shimizu, K. Yamamoto, T. Matsushita, and H. Saito Plasma levels of syndecan-4 (ryudocan) are elevated in patients with acute myocardial infarction Thromb. Haemost. 85 2001 793 799
21. R. Takahashi, K. Negishi, A. Watanabe, M. Arai, F. Naganuma, Y. Ohyama, and M. Kurabayashi Serum syndecan-4 is a novel biomarker for patients with chronic heart failure J. Cardiol. 57 2011 325 332
22. M. Ikesue, Y. Matsui, D. Ohta, K. Danzaki, K. Ito, M. Kanayama, D. Kurotaki, J. Morimoto, T. Kojima, H. Tsutsui, and T. Uede 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 2011 1066 1074
23. B.H. Rauch, E. Millette, R.D. Kenagy, G. Daum, J.W. Fischer, and A.W. Clowes Syndecan-4 is required for thrombin-induced migration and proliferation in human vascular smooth muscle cells J. Biol. Chem. 280 2005 17507 17511
24. G. Cizmeci-Smith, E. Langan, J. Youkey, L.J. Showalter, and D.J. Carey 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 1997 172 180
25. R. Pankov, Y. Endo, S. Even-Ram, M. Araki, K. Clark, E. Cukierman, K. Matsumoto, and K.M. Yamada A Rac switch regulates random versus directionally persistent cell migration J. Cell Biol. 170 2005 793 802
26. K. Ishiguro, K. Kadomatsu, T. Kojima, H. Muramatsu, E. Nakamura, M. Ito, T. Nagasaka, H. Kobayashi, K. Kusugami, H. Saito, and T. Muramatsu Syndecan-4 deficiency impairs the fetal vessels in the placental labyrinth Dev. Dyn. 219 2000 539 544