The adaptive remodeling of endothelial glycocalyx in response to fluid shear stress

PLoS ONE

Volumn 9, Issue 1, 2014, Pages

  Zeng, Ye ^a,b   Tarbell, John M ^a  

^a City University of New York   (United States)

^b SICHUAN UNIVERSITY   (China)

Author keywords

[No Author keywords available]

Indexed keywords

ACTIN; CAVEOLIN 1; CHONDROITIN SULFATE; GLYPICAN 1; HEPARAN SULFATE; SYNDECAN 1; GANGLIOSIDE GM1; GLYPICAN; CYTOCHALASIN D;

ACTIN FILAMENT; ANIMAL CELL; ARTICLE; CAVEOLA; CELL MEMBRANE; CELL SURFACE; CONTROLLED STUDY; ENDOTHELIUM; GLYCOCALYX; LIPID RAFT; MECHANOTRANSDUCTION; NONHUMAN; RAT; SHEAR STRESS; ANIMAL; BOVINAE; CELL LINE; CYTOLOGY; ENDOTHELIUM CELL; HYDRODYNAMICS; MECHANICAL STRESS; METABOLISM; ULTRASTRUCTURE; BOVINE; CONFOCAL MICROSCOPY; EXPOSURE; IMMUNOFLUORESCENCE; PROTEIN SYNTHESIS;

ACTIN CYTOSKELETON; ANIMALS; CATTLE; CAVEOLIN 1; CELL LINE; ENDOTHELIAL CELLS; G(M1) GANGLIOSIDE; GLYCOCALYX; GLYPICANS; HYDRODYNAMICS; RATS; STRESS, MECHANICAL; SYNDECAN-1;

EID: 84899421150     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0086249     Document Type: Article

References (53)

1. Pries AR, Secomb TW, Gaehtgens P (2000) The endothelial surface layer. Pflugers Arch 440: 653-666.
2. Tarbell JM, Ebong EE (2008) The endothelial glycocalyx: a mechano-sensor and -transducer. Sci Signal 1: pt8.
3. Fu BM, Tarbell JM (2013) Mechano-sensing and transduction by endothelial surface glycocalyx: composition, structure, and function. Wiley Interdiscip Rev Syst Biol Med 5: 381-390.
4. Curry FE, Adamson RH (2012) Endothelial glycocalyx: permeability barrier and mechanosensor. Ann Biomed Eng 40: 828-839.
5. Tarbell JM (2010) Shear stress and the endothelial transport barrier. Cardiovasc Res 87: 320-330.
6. Lipowsky HH (2011) Protease Activity and the Role of the Endothelial Glycocalyx in Inflammation. Drug Discov Today Dis Models 8: 57-62.
7. Zeng Y, Waters M, Andrews A, Honarmandi P, Ebong E, et al. (2013) Fluid Shear Stress induces the Clustering of Heparan Sulfate via Mobility of Glypican-1 in Lipid Rafts. Am J Physiol Heart Circ Physiol.
8. Tarbell JM, Pahakis MY (2006) Mechanotransduction and the glycocalyx. J Intern Med 259: 339-350. (Pubitemid 43384225)
9. Kokenyesi R, Bernfield M (1994) Core protein structure and sequence determine the site and presence of heparan sulfate and chondroitin sulfate on syndecan-1. J Biol Chem 269: 12304-12309. (Pubitemid 24196737)
10. Couchman JR (2010) Transmembrane signaling proteoglycans. Annu Rev Cell Dev Biol 26: 89-114.
11. Filmus J, Capurro M, Rast J (2008) Glypicans. Genome Biol 9: 224.
12. Schnitzer JE, McIntosh DP, Dvorak AM, Liu J, Oh P (1995) Separation of caveolae from associated microdomains of GPI-anchored proteins. Science 269: 1435-1439.
13. Lisanti MP, Scherer PE, Vidugiriene J, Tang Z, Hermanowski-Vosatka A, et al. (1994) Characterization of caveolin-rich membrane domains isolated from an endothelial-rich source: implications for human disease. J Cell Biol 126: 111-126. (Pubitemid 24214933)
14. Lindner R, Naim HY (2009) Domains in biological membranes. Exp Cell Res 315: 2871-2878.
15. Parton RG (1994) Ultrastructural localization of gangliosides; GM1 is concentrated in caveolae. J Histochem Cytochem 42: 155-166.
16. De Haan L, Hirst TR (2004) Cholera toxin: a paradigm for multi-functional engagement of cellular mechanisms (Review). Mol Membr Biol 21: 77-92. (Pubitemid 38524366)
17. Navarro A, Anand-Apte B, Parat MO (2004) A role for caveolae in cell migration. FASEB J 18: 1801-1811. (Pubitemid 39602266)
18. Parton RG, del Pozo MA (2013) Caveolae as plasma membrane sensors, protectors and organizers. Nat Rev Mol Cell Biol 14: 98-112.
19. Thomsen P, Roepstorff K, Stahlhut M, van Deurs B (2002) Caveolae are highly immobile plasma membrane microdomains, which are not involved in constitutive endocytic trafficking. Mol Biol Cell 13: 238-250. (Pubitemid 34106072)
20. Lingwood D, Simons K (2010) Lipid rafts as a membrane-organizing principle. Science 327: 46-50.
21. Simons K, Sampaio JL (2011) Membrane organization and lipid rafts. Cold Spring Harb Perspect Biol 3: a004697.
22. Malek AM, Izumo S (1996) Mechanism of endothelial cell shape change and cytoskeletal remodeling in response to fluid shear stress. J Cell Sci 109 (Pt 4): 713-726. (Pubitemid 26134374)
23. Gotlieb AI (1990) The endothelial cytoskeleton: organization in normal and regenerating endothelium. Toxicol Pathol 18: 603-617.
24. Li YS, Haga JH, Chien S (2005) Molecular basis of the effects of shear stress on vascular endothelial cells. J Biomech 38: 1949-1971. (Pubitemid 41111740)
25. Sanger JM, Sanger JW (1980) Banding and polarity of actin filaments in interphase and cleaving cells. J Cell Biol 86: 568-575. (Pubitemid 10016278)
26. Satcher R, Dewey CF, Jr., Hartwig JH (1997) Mechanical remodeling of the endothelial surface and actin cytoskeleton induced by fluid flow. Microcirculation 4: 439-453. (Pubitemid 127675118)
27. Yao Y, Rabodzey A, Dewey CF, Jr. (2007) Glycocalyx modulates the motility and proliferative response of vascular endothelium to fluid shear stress. Am J Physiol Heart Circ Physiol 293: H1023-1030. (Pubitemid 47254201)
28. Thi MM, Tarbell JM, Weinbaum S, Spray DC (2004) The role of the glycocalyx in reorganization of the actin cytoskeleton under fluid shear stress: a "bumpercar" model. Proc Natl Acad Sci U S A 101: 16483-16488. (Pubitemid 39557739)
29. Moon JJ, Matsumoto M, Patel S, Lee L, Guan JL, et al. (2005) Role of cell surface heparan sulfate proteoglycans in endothelial cell migration and mechanotransduction. J Cell Physiol 203: 166-176. (Pubitemid 40328183)
30. Marcum JA, Rosenberg RD (1985) Heparinlike molecules with anticoagulant activity are synthesized by cultured endothelial cells. Biochem Biophys Res Commun 126: 365-372. (Pubitemid 15173570)
31. Zeng Y, Ebong EE, Fu BM, Tarbell JM (2012) The structural stability of the endothelial glycocalyx after enzymatic removal of glycosaminoglycans. PLoS One 7: e43168.
32. Cancel LM, Tarbell JM (2011) The role of mitosis in LDL transport through cultured endothelial cell monolayers. Am J Physiol Heart Circ Physiol 300: H769-776.
33. Ainslie KM, Garanich JS, Dull RO, Tarbell JM (2005) Vascular smooth muscle cell glycocalyx influences shear stress-mediated contractile response. J Appl Physiol (1985) 98: 242-249.
34. Zeng Y, Sun HR, Yu C, Lai Y, Liu XJ, et al. (2011) CXCR1 and CXCR2 are novel mechano-sensors mediating laminar shear stress-induced endothelial cell migration. Cytokine 53: 42-51.
35. White CR, Frangos JA (2007) The shear stress of it all: the cell membrane and mechanochemical transduction. Philos Trans R Soc Lond B Biol Sci 362: 1459-1467. (Pubitemid 47195034)
36. Chien S (2007) Mechanotransduction and endothelial cell homeostasis: the wisdom of the cell. Am J Physiol Heart Circ Physiol 292: H1209-1224.
37. Zhang J, Friedman MH (2012) Adaptive response of vascular endothelial cells to an acute increase in shear stress magnitude. Am J Physiol Heart Circ Physiol 302: H983-991.
38. Warboys CM, Eric Berson R, Mann GE, Pearson JD, Weinberg PD (2010) Acute and chronic exposure to shear stress have opposite effects on endothelial permeability to macromolecules. Am J Physiol Heart Circ Physiol 298: H1850-1856.
39. Pahakis MY, Kosky JR, Dull RO, Tarbell JM (2007) The role of endothelial glycocalyx components in mechanotransduction of fluid shear stress. Biochem Biophys Res Commun 355: 228-233. (Pubitemid 46273392)
40. Florian JA, Kosky JR, Ainslie K, Pang Z, Dull RO, et al. (2003) Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circ Res 93: e136-142.
41. Ebong EE, Macaluso FP, Spray DC, Tarbell JM (2011) Imaging the endothelial glycocalyx in vitro by rapid freezing/freeze substitution transmission electron microscopy. Arterioscler Thromb Vasc Biol 31: 1908-1915.
42. Arisaka T, Mitsumata M, Kawasumi M, Tohjima T, Hirose S, et al. (1995) Effects of shear stress on glycosaminoglycan synthesis in vascular endothelial cells. Ann N Y Acad Sci 748: 543-554.
43. Yen WY, Cai B, Zeng M, Tarbell JM, Fu BM (2012) Quantification of the endothelial surface glycocalyx on rat and mouse blood vessels. Microvasc Res 83: 337-346.
44. GouverneurM, Spaan JA, Pannekoek H, Fontijn RD, Vink H (2006) Fluid shear stress stimulates incorporation of hyaluronan into endothelial cell glycocalyx. Am J Physiol Heart Circ Physiol 290: H458-452.
45. Koo A, Dewey CF, Jr., Garcia-Cardena G (2013) Hemodynamic shear stress characteristic of atherosclerosis-resistant regions promotes glycocalyx formation in cultured endothelial cells. Am J Physiol Cell Physiol 304: C137-146.
46. Koo A, García-Cardeña G, dewey CF Jr (2011) Flow regulated endothelial glycocalyx expression and its function as a protective barrier against leukocyte adhesion; Harford, Connecticut.
47. Rizzo V, Morton C, DePaola N, Schnitzer JE, Davies PF (2003) Recruitment of endothelial caveolae into mechanotransduction pathways by flow conditioning in vitro. Am J Physiol Heart Circ Physiol 285: H1720-1729. (Pubitemid 37169528)
48. Chakravarti R, Sapountzi V, Adams JC (2005) Functional role of syndecan-1 cytoplasmic V region in lamellipodial spreading, actin bundling, and cell migration. Mol Biol Cell 16: 3678-3691. (Pubitemid 41077078)
49. Carey DJ, Bendt KM, Stahl RC (1996) The cytoplasmic domain of syndecan-1 is required for cytoskeleton association but not detergent insolubility. Identification of essential cytoplasmic domain residues. J Biol Chem 271: 15253-15260. (Pubitemid 26195007)
50. Yu J, Bergaya S, Murata T, Alp IF, Bauer MP, et al. (2006) Direct evidence for the role of caveolin-1 and caveolae in mechanotransduction and remodeling of blood vessels. J Clin Invest 116: 1284-1291.
51. Davies PF (2009) Hemodynamic shear stress and the endothelium in cardiovascular pathophysiology. Nat Clin Pract Cardiovasc Med 6: 16-26.
52. Drake-Holland AJ, Noble MI (2012) Update on the important new drug target in cardiovascular medicine - the vascular glycocalyx. Cardiovasc Hematol Disord Drug Targets 12: 76-81.
53. Lemkes BA, Nieuwdorp M, Hoekstra JB, Holleman F (2012) The glycocalyx and cardiovascular disease in diabetes: should we judge the endothelium by its cover? Diabetes Technol Ther 14 Suppl 1: S3-10.