Loss of syndecan-1 induces a pro-inflammatory phenotype in endothelial cells with a dysregulated response to atheroprotective flow

Journal of Biological Chemistry

Volumn 289, Issue 14, 2014, Pages 9547-9559

  Voyvodic, Peter L ^a   Min, Daniel ^a   Liu, Robert ^a   Williams, Evan ^a   Chitalia, Vipul ^b   Dunn, Andrew K ^a   Baker, Aaron B ^a  

^a The University of Texas at Austin   (United States)

^b BOSTON MEDICAL CENTER   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

CELL ADHESION; ENDOTHELIAL CELLS; GLYCOPROTEINS; MAMMALS; PHOSPHORYLATION; SHEAR FLOW; SHEAR STRESS;

FLUID SHEAR STRESS; GLYCOAMINOGLYCANS; HEMODYNAMIC FORCES; LEUKOCYTE ADHESION; PHENOTYPIC MODULATION; PHENOTYPIC SHIFTS; VASCULAR HOMEOSTASIS; VASCULAR PERMEABILITY;

CELL SIGNALING;

GLYCOPROTEIN; GLYCOSAMINOGLYCAN; PAXILLIN; PROTEIN KINASE B; PROTEOGLYCAN; RHOA GUANINE NUCLEOTIDE BINDING PROTEIN; SYNDECAN 1; TRANSCRIPTION FACTOR;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; ATHEROGENESIS; ATHEROSCLEROSIS; CONTROLLED STUDY; ENDOTHELIUM CELL; FLUORESCENCE RESONANCE ENERGY TRANSFER; GLYCOCALYX; INFLAMMATION; MONOCYTE; MOUSE; NONHUMAN; OXIDATIVE STRESS; PHENOTYPE; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION; PROTEIN PROTEIN INTERACTION; SHEAR STRESS; SIGNAL TRANSDUCTION; VASCULAR DISEASE;

ATHEROPROTECTIVE FLOW; ENDOTHELIAL CELL; FLOW; GLYCOCALYX; INFLAMMATION; LEUKOCYTE; MECHANOTRANSDUCTION; SHEAR STRESS; SYNDECAN-1;

ANIMALS; ATHEROSCLEROSIS; BLOOD FLOW VELOCITY; CELL ADHESION; CELL LINE; ENDOTHELIAL CELLS; GLYCOCALYX; HUMANS; INFLAMMATION; LEUKOCYTES; MECHANOTRANSDUCTION, CELLULAR; MICE; MICE, KNOCKOUT; SYNDECAN-1;

EID: 84898073682     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M113.541573     Document Type: Article

References (60)

1. Davies, P.F., Barbee, K.A., Volin, M. V., Robotewskyj, A., Chen, J., Joseph, L., Griem, M. L., Wernick, M. N., Jacobs, E., Polacek, D. C, dePaola, N., and Barakat, A. I. (1997) Spatial relationships in early signaling events of flow-mediated endothelial mechanotransduction. Annu. Rev. Physiol. 59, 527-549
2. Hahn, C, and Schwartz, M. A. (2009) Mechanotransduction in vascular physiology and atherogenesis. Nat. Rev. Mol. Cell Biol. 10, 53-62
3. Hoger, J. H., Ilyin, V. I., Forsyth, S., and Hoger, A. (2002) Shear stress regulates the endothelial Kir2.1 ion channel. Proc. Natl. Acad. Sci. U.S.A. 99, 7780-7785
4. Hutcheson, I. R., and Griffith, T. M. (1996) Mechanotransduction through the endothelial cytoskeleton: mediation of flow-but not agonist-induced EDRF release. Br. J. Pharmacol. 118, 720-726
5. Iomini, C., Tejada, K., Mo, W., Vaananen, H., and Piperno, G. (2004) Primary cilia of human endothelial cells disassemble under laminar shear stress. J. Cell Biol. 164, 811-817
6. Malek, A. M., Zhang, J., Jiang, J., Alper, S. L., and Izumo, S. (1999) Endothelin-1 gene suppression by shear stress: pharmacological evaluation of the role of tyrosine kinase, intracellular calcium, cytoskeleton, andmecha-nosensitive channels. J. Mol. Cell. Cardiol. 31, 387-399
7. Schwartz, M. A., and DeSimone, D. W. (2008) Cell adhesion receptors in mechanotransduction. Curr. Opin. Cell Biol. 20, 551-556
8. Parmar, K. M., Larman, H. B., Dai, G., Zhang, Y., Wang, E. T., Moorthy, S. N., Kratz, J. R., Lin, Z., Jain, M. K., Gimbrone, M. A., Jr., and García-Cardeña, G. (2006) Integration of flow-dependent endothelial phenotypes by Kruppel-like factor 2. J. Clin. Invest. 116, 49-58
9. Hamik, A., Lin, Z., Kumar, A., Balcells, M., Sinha, S., Katz, J., Feinberg, M. W., Gerzsten, R. E., Edelman, E. R., and Jain, M. K. (2007) Kruppel-like factor 4 regulates endothelial inflammation. J. Biol. Chem. 282, 13769-13779
10. Zhou, G., Hamik, A., Nayak, L., Tian, H., Shi, H., Lu, Y., Sharma, N., Liao, X., Hale, A., Boerboom, L., Feaver, R. E., Gao, H., Desai, A., Schmaier, A., Gerson, S. L., Wang, Y., Atkins, G. B., Blackman, B. R., Simon, D. I., and Jain, M. K. (2012) Endothelial Kruppel-like factor 4 protects against atherothrombosis in mice. J. Clin. Invest. 122, 4727-4731
11. Kumekawa, M., Fukuda, G., Shimizu, S., Konno, K., and Odawara, M. (2008) Inhibition of monocyte chemoattractant protein-1 by Kruppel-like factor 5 small interfering RNA in the tumor necrosis factor-a-activated human umbilical vein endothelial cells. Biol. Pharm. Bull. 31, 1609-1613
12. Tzima, E., Irani-Tehrani, M., Kiosses, W. B., Dejana, E., Schultz, D. A., Engelhardt, B., Cao, G., DeLisser, H., and Schwartz, M. A. (2005) A mecha-nosensory complex that mediates the endothelial cell response to fluid shear stress. Nature 437, 426-431
13. Ebong, E. E., Macaluso, F. P., Spray, D. C, and Tarbell, J. M. (2011) Imaging the endothelial glycocalyx in vitro by rapid freezing/freeze substitution transmission electron microscopy. Arterioscler. Thromb. Vasc. Biol. 31, 1908-1915
14. Weinbaum, S., Zhang, X., Han, Y., Vink, H, and Cowin, S. C. (2003) Mechanotransduction and flow across the endothelial glycocalyx. Proc. Natl. Acad. Sci. U.S.A. 100, 7988-7995
15. Florian, J. A., Kosky, J. R., Ainslie, K., Pang, Z., Dull, R. O., and Tarbell, J. M. (2003) Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circ. Res. 93, e136-142
16. Bishop, J. R., Schuksz, M., and Esko, J. D. (2007) Heparan sulphate proteoglycans fine-tune mammalian physiology. Nature 446, 1030-1037
17. Hsia, E., Richardson, T. P., and Nugent, M. A. (2003) Nuclear localization of basic fibroblast growth factor is mediated by heparan sulfate proteoglycans through protein kinase C signaling. J. Cell. Biochem. 88, 1214-1225
18. Tkachenko, E., Rhodes, J. M., and Simons, M. (2005) Syndecans: new kids on the signaling block. Circ. Res. 96, 488-500
19. Rapraeger, A. C. (2013) Synstatin: a selective inhibitor of the syndecan-1-coupled IGF1R-av/33 integrin complex in tumorigenesis and angiogene-sis. FEBSJ. 280, 2207-2215
20. Okina, E., Manon-Jensen, T., Whiteford, J. R., and Couchman, J. R. (2009) Syndecan proteoglycan contributions to cytoskeletal organization and contractility. Scand. J. Med. Sci. Sports 19, 479-489
21. Roper, J. A., Williamson, R. C, and Bass, M. D. (2012) Syndecan and integrin interactomes: large complexes in small spaces. Curr. Opin. Struct. Biol. 22, 583-590
22. Dong, Q. G., Bernasconi, S., Lostaglio, S., De Calmanovici, R. W., Martin-Padura, I., Breviario, F., Garlanda, C., Ramponi, S., Mantovani, A., and Vecchi, A. (1997) A general strategy for isolation of endothelial cells from murine tissues. Characterization of two endothelial cell lines from the murine lung and subcutaneous sponge implants. Arterioscler. Thromb. Vasc. Biol. 17, 1599-1604
23. Mostoslavsky, G., Kotton, D. N, Fabian, A. J., Gray, J. T., Lee, J. S., and Mulligan, R. C. (2005) Efficiency of transduction of highly purified murine hematopoietic stem cells by lentiviral and oncoretroviral vectors under conditions of minimal in vitro manipulation. Mol. Ther. 11, 932-940
24. Voyvodic, P. L., Min, D., and Baker, A. B. (2012) A multichannel dampened flow system for studies on shear stress-mediated mechanotransduc-tion. Lab Chip 12, 3322-3330
25. Baker, A. B., Ettenson, D. S., Jonas, M., Nugent, M. A., Iozzo, R. V., and Edelman, E. R. (2008) Endothelial cells provide feedback control for vascular remodeling through a mechanosensitive autocrine TGF-/3 signaling pathway. Circ. Res. 103, 289-297
26. Pertz, O., Hodgson, L., Klemke, R. L., and Hahn, K. M. (2006) Spatiotem-poral dynamics of RhoA activity in migrating cells. Nature 440, 1069-1072
27. Koskinas, K. C., Feldman, C. L., Chatzizisis, Y. S., Coskun, A. U., Jonas, M., Maynard, C., Baker, A. B., Papafaklis, M. I., Edelman, E. R., and Stone, P. H. (2010) Natural history of experimental coronary atherosclerosis and vascular remodeling in relation to endothelial shear stress: a serial, in vivo intravascular ultrasound study. Circulation 121, 2092-2101
28. Chatzizisis, Y. S., Baker, A. B., Sukhova, G. K., Koskinas, K. C, Papafaklis, M. I., Beigel, R., Jonas, M., Coskun, A. U., Stone, B. V., Maynard, C, Shi, G. P., Libby, P., Feldman, C. L., Edelman, E. R., and Stone, P. H. (2011) Augmented expression and activity of extracellular matrix-degrading enzymes in regions of low endothelial shear stress colocalize with coronary atheromata with thin fibrous caps in pigs. Circulation 123, 621-630
29. Alexander, C. M., Reichsman, F., Hinkes, M. T., Lincecum, J., Becker, K. A., Cumberledge, S., and Bernfield, M. (2000) Syndecan-1 is required for Wnt-1-induced mammary tumorigenesis in mice. Nat. Genet. 25, 329-332
30. Dunn, A. K. (2012) Laser speckle contrast imaging of cerebral blood flow. Ann. Biomed. Eng. 40, 367-377
31. Dai, G., Vaughn, S., Zhang, Y., Wang, E. T., Garcia-Cardena, G., and Gim-brone, M. A., Jr. (2007) Biomechanical forces in atherosclerosis-resistant vascular regions regulate endothelial redox balance via phosphoinositol 3-kinase/Akt-dependent activation of Nrf2. Circ. Res. 101, 723-733
32. Dimmeler, S., Assmus, B., Hermann, C, Haendeler, J., and Zeiher, A. M. (1998) Fluid shear stress stimulates phosphorylation of Akt in human endothelial cells: involvement in suppression of apoptosis. Circ. Res. 83, 334-341
33. Dimmeler, S., Fleming, I., Fisslthaler, B., Hermann, C, Busse, R., and Zeiher, A. M. (1999) Activation of nitric oxide synthase in endothelial cells by Akt-dependent phosphorylation. Nature 399, 601-605
34. Zaidel-Bar, R., Kam, Z., and Geiger, B. (2005) Polarized downregulation of the paxillin-p130CAS-Rac1 pathway induced by shear flow. J. Cell Sci. 118, 3997-4007
35. Orr, A. W., Ginsberg, M. H, Shattil, S. J., Deckmyn, H, and Schwartz, M. A. (2006) Matrix-specific suppression of integrin activation in shear stress signaling. Mol. Biol. Cell 17, 4686-4697
36. 3-mediated FGF-2 release. J. Vasc. Res. 48, 453-464
37. 3 detected with a novel patch-engineered monovalent ligand. J. Biol. Chem. 274, 21609-21616
38. Cicha, I., Goppelt-Struebe, M., Muehlich, S., Yilmaz, A., Raaz, D., Daniel, W. G., and Garlichs, C. D. (2008) Pharmacological inhibition of RhoA signaling prevents connective tissue growth factor induction in endothelial cells exposed to non-uniform shear stress. Atherosclerosis 196, 136-145
39. Yang, B., Radel, C, Hughes, D., Kelemen, S., and Rizzo, V. (2011) p190 RhoGTPase-activating protein links the/31 integrin/caveolin-1 mecha-nosignaling complex to RhoA and actin remodeling. Arterioscler. Thromb. Vasc. Biol. 31, 376-383
40. Tzima, E. (2006) Role of small GTPases in endothelial cytoskeletal dynamics and the shear stress response. Circ. Res. 98, 176-185
41. Hoshino, Y., Kurabayashi, M., Kanda, T., Hasegawa, A., Sakamoto, H, Okamoto, E., Kowase, K., Watanabe, N, Manabe, I., Suzuki, T., Nakano, A., Takase, S., Wilcox, J. N, and Nagai, R. (2000) Regulated expression of the BTEB2 transcription factor in vascular smooth muscle cells: analysis of developmental and pathological expression profiles shows implications as a predictive factor for restenosis. Circulation 102, 2528-2534
42. Kumagai, R., Lu, X., and Kassab, G. S. (2009) Role of glycocalyx in flow-induced production of nitric oxide and reactive oxygen species. Free Radic. Biol. Med. 47, 600-607
43. Pahakis, M. Y., Kosky, J. R., Dull, R. O., and Tarbell, J. M. (2007) The role of endothelial glycocalyx components in mechanotransduction of fluid shear stress. Biochem. Biophys. Res. Commun. 355, 228-233
44. Pohl, U., Herlan, K., Huang, A., and Bassenge, E. (1991) EDRF-mediated shear-induced dilation opposes myogenic vasoconstriction in small rabbit arteries. Am. J. Physiol. 261, H2016-H2023
45. Kamiya, A., Bukhari, R., and Togawa, T. (1984) Adaptive regulation of wall shear stress optimizing vascular tree function. Bull. Math. Biol. 46, 127-137
46. Hecker, M., Mülsch, A., Bassenge, E., and Busse, R. (1993) Vasoconstriction and increased flow: two principal mechanisms of shear stress-dependent endothelial autacoid release. Am. J. Physiol. 265, H828-H833
47. Van Teeffelen, J. W., Brands, J., Stroes, E. S., and Vink, H. (2007) Endothelial glycocalyx: sweet shield of blood vessels. Trends. Cardiovasc. Med. 17, 101-105
48. Koo, A., Dewey, C. F., Jr., and García-Cardena, G. (2013) Hemodynamic shear stress characteristic of atherosclerosis-resistant regions promotes glycocalyx formation in cultured endothelial cells. Am. J. Physiol. Cell Physiol. 304, C137-C146
49. Savery, M. D., Jiang, J. X., Park, P. W., and Damiano, E. R. (2013) The endothelial glycocalyx in syndecan-1 deficient mice. Microvasc. Res. 87, 83-91
50. Nam, E. J., and Park, P. W. (2012) Shedding of cell membrane-bound proteoglycans. Methods Mol. Biol. 836, 291-305
51. Das, S., Singh, G., and Baker, A. B. (2014) Overcoming disease-induced growth factor resistance in therapeutic angiogenesis using recombinant co-receptors delivered by a liposomal system. Biomaterials 35, 196-205
52. Ramani, V. C, Purushothaman, A., Stewart, M. D., Thompson, C. A., Vlodavsky, I., Au, J. L., and Sanderson, R. D. (2013) The heparanase/syndecan-1 axis in cancer: mechanisms and therapies. FEBS J. 280, 2294-2306
53. Baker, A. B., Gibson, W. J., Kolachalama, V. B., Golomb, M., Indolfi, L., Spruell, C, Zcharia, E., Vlodavsky, I., and Edelman, E. R. (2012) Heparanase regulates thrombosis in vascular injury and stent-induced flow disturbance. J. Am. Coll. Cardiol. 59, 1551-1560
54. Mobine, H. R., Baker, A. B., Wang, L., Wakimoto, H., Jacobsen, K. C., Seidman, C. E., Seidman, J. G., and Edelman, E. R. (2009) Pheochromocy-toma- induced cardiomyopathy is modulated by the synergistic effects of cell-secreted factors. Circ. Heart. Fail. 2, 121-128
55. Blich, M., Golan, A., Arvatz, G., Sebbag, A., Shafat, I., Sabo, E., Cohen-Kaplan, V., Petcherski, S., Avniel-Polak, S., Eitan, A., Hammerman, H., Aronson, D., Axelman, E., Ilan, N., Nussbaum, G., and Vlodavsky, I. (2013) Macrophage activation by heparanase is mediated by TLR-2 and TLR-4 and associates with plaque progression. Arterioscler. Thromb. Vasc. Biol. 33, e56-e65
56. Schmidt, E. P., Yang, Y., Janssen, W. J., Gandjeva, A., Perez, M. J., Barthel, L., Zemans, R. L., Bowman, J. C., Koyanagi, D. E., Yunt, Z. X., Smith, L. P., Cheng, S. S., Overdier, K. H., Thompson, K. R., Geraci, M. W., Douglas, I. S., Pearse, D. B., and Tuder, R. M. (2012) The pulmonary endothelial glycocalyx regulates neutrophil adhesion and lung injury during experimental sepsis. Nat. Med. 18, 1217-1223
57. Potter, D. R., and Damiano, E. R. (2008) The hydrodynamically relevant endothelial cell glycocalyx observed in vivo is absent in vitro. Circ. Res. 102, 770-776
58. Potter, D. R., Jiang, J., and Damiano, E. R. (2009) The recovery time course of the endothelial cell glycocalyx in vivo and its implications in vitro. Circ. Res. 104, 1318-1325
59. Baker, A. B., Chatzizisis, Y. S., Beigel, R., Jonas, M., Stone, B. V., Coskun, A. U., Maynard, C., Rogers, C., Koskinas, K.C., Feldman, C.L., Stone, P. H., and Edelman, E. R. (2010) Regulation of heparanase expression in coronary artery disease in diabetic, hyperlipidemic swine. Atherosclerosis 213, 436-442
60. Baker, A. B., Groothuis, A., Jonas, M., Ettenson, D. S., Shazly, T., Zcharia, E., Vlodavsky, I., Seifert, P., and Edelman, E. R. (2009) Heparanase alters arterial structure, mechanics, and repair following endovascular stenting in mice. Circ. Res. 104, 380-387