Sphingosine-1-phosphate Maintains Normal Vascular Permeability by Preserving Endothelial Surface Glycocalyx in Intact Microvessels

Microcirculation

Volumn 23, Issue 4, 2016, Pages 301-310

  Zhang, Lin ^a   Zeng, Min ^a   Fan, Jie ^a   Tarbell, John M ^a   Curry, Fitz Roy E ^b   Fu, Bingmei M ^a  

^a City College of New York   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

heparan sulfate; in situ immunostaining; matrix metalloproteinase; rat mesentery; transport model for the inter endothelial cleft

Indexed keywords

ALBUMIN; SPHINGOSINE 1 PHOSPHATE; LYSOPHOSPHOLIPID; SPHINGOSINE; SPHINGOSINE 1-PHOSPHATE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; CONTROLLED STUDY; FEMALE; GLYCOCALYX; MATHEMATICAL MODEL; MESENTERY; MICROVASCULATURE; NONHUMAN; PREDICTION; RAT; VASCULAR ENDOTHELIUM; VENULE; ANALOGS AND DERIVATIVES; ANIMAL; CAPILLARY PERMEABILITY; CELL CULTURE; PHYSIOLOGY; SPRAGUE DAWLEY RAT; ULTRASTRUCTURE; VASCULARIZATION;

ANIMALS; CAPILLARY PERMEABILITY; CELLS, CULTURED; ENDOTHELIUM, VASCULAR; FEMALE; GLYCOCALYX; LYSOPHOSPHOLIPIDS; MESENTERY; MICROVESSELS; RATS; RATS, SPRAGUE-DAWLEY; SPHINGOSINE;

EID: 85011407745     PISSN: 10739688     EISSN: 15498719     Source Type: Journal    
DOI: 10.1111/micc.12278     Document Type: Article

References (43)

1. Adamson RH, Clark JF, Radeva M, Kheirolomoom A, Ferrara KW, Curry FE. Albumin modulates S1P delivery from red blood cells in perfused microvessels: mechanism of the protein effect. Am J Physiol Heart Circ Physiol 306: H1011–H1017, 2014.
2. Adamson RH, Lenz JF, Zhang X, Adamson GN, Weinbaum S, Curry FE. Oncotic pressures opposing filtration across non-fenestrated rat microvessels. J Physiol 557: 889–907, 2004.
3. Adamson RH, Michel CC. Pathways through the intercellular clefts of frog mesenteric capillaries. J Physiol 466: 303–327, 1993.
4. Adamson RH, Sarai RK, Altangerel A, Thirkill TL, Clark JF, Curry FR. Sphingosine-1-phosphate modulation of basal permeability and acute inflammatory responses in rat venular microvessels. Cardiovasc Res 88: 344–351, 2010.
5. Adamson RH, Sarai RK, Clark JF, Altangerel A, Thirkill TL, Curry FE. Attenuation by sphingosine-1-phosphate of rat microvessel acute permeability response to bradykinin is rapidly reversible. Am J Physiol Heart Circ Physiol 302: H1929–H1935, 2012.
6. Arkill KP, Knupp C, Michel CC, Neal CR, Qvortrup K, Rostgaard J, Squire JM. Similar endothelial glycocalyx structures in microvessels from a range of mammalian tissues: evidence for a common filtering mechanism? Biophys J 101: 1046–1056, 2011.
7. Bode CSS, Peest U, Beutel G, Thol F, Levkau B, Li Z, Bittman RHT, Tolle M, van der Giet M, Graler MH. Erythrocytes serve as a reservoir for cellular and extracellular sphingosine 1-phosphate. J Cell Biochem 109: 1232–1243, 2010.
8. Bouma HR, Kroese FG, Kok JW, Talaei F, Boerema AS, Herwig A, Draghiciu O, van Buiten A, Epema AH, van Dam A, Strijkstra AM, Henning RH. Low body temperature governs the decline of circulating lymphocytes during hibernation through sphingosine-1-phosphate. Proc Natl Acad Sci USA 108: 2052–2057, 2011.
9. Cai B, Fan J, Zeng M, Zhang L, Fu BM. Adhesion of malignant mammary tumor cells MDA-MB-231 to microvessel wall increases microvascular permeability via degradation of endothelial surface glycocalyx. J Appl Physiol (1985) 113: 1141–1153, 2012.
10. Constantinescu AA, Vink H, Spaan JA. Endothelial cell glycocalyx modulates immobilization of leukocytes at the endothelial surface. Arterioscler Thromb Vasc Biol 23: 1541–1547, 2003.
11. Curry FR, Adamson RH. Vascular permeability modulation at the cell, microvessel, or whole organ level: towards closing gaps in our knowledge. Cardiovasc Res 87: 218–229, 2010.
12. Curry FE, Clark JF, Adamson RH. Erythrocyte-derived sphingosine-1-phosphate stabilizes basal hydraulic conductivity and solute permeability in rat microvessels. Am J Physiol Heart Circ Physiol 303: H825–H834, 2012.
13. Curry FR, Noll T. Spotlight on microvascular permeability. Cardiovasc Res 87: 195–197, 2010.
14. Fu BM, Shen S. Acute VEGF effect on solute permeability of mammalian microvessels in vivo. Microvasc Res 68: 51–62, 2004.
15. Fu BM, Tarbell JM. Mechano-sensing and transduction by endothelial surface glycocalyx: composition, structure, and function. Wiley Interdiscip Rev Syst Biol Med 5: 381–390, 2013.
16. Fu BM, Weinbaum S, Tsay RY, Curry FE. A junction-orifice-fiber entrance layer model for capillary permeability: application to frog mesenteric capillaries. J Biomech Eng 116: 502–513, 1994.
17. Gao L, Lipowsky HH. Composition of the endothelial glycocalyx and its relation to its thickness and diffusion of small solutes. Microvasc Res 80: 394–401, 2010.
18. Garcia JG, Liu F, Verin AD, Birukova A, Dechert MA, Gerthoffer WT, Bamberg JR, English D. Sphingosine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cytoskeletal rearrangement. J Clin Invest 108: 689–701, 2001.
19. Hanel P, Andreani P, Graler MH. Erythrocytes store and release sphingosine 1-phosphate in blood. FASEB J 21: 1202–1209, 2007.
20. Hla T. Physiological and pathological actions of sphingosine 1-phosphate. Semin Cell Dev Biol 15: 513–520, 2004.
21. Lee MJVBJ, Thangada S, Liu CH, Hand AR, Menzeleev R, Spiegel S, Hla T. Sphingosine-1-phosphate as a ligand for the G protein-coupled receptor EDG-1. Science 279: 1552–1555, 1998.
22. Liu Q, Zeng M, Fu BM. Microvascular hyperpermeability and thrombosis induced by light/dye treatment. Biomech Model Mechanobiol 10: 235–247, 2011.
23. McVerry BJ, Garcia JG. Endothelial cell barrier regulation by sphingosine 1-phosphate. J Cell Biochem 92: 1075–1085, 2004.
24. Minnear FL, Zhu L, He P. Sphingosine 1-phosphate prevents platelet-activating factor-induced increase in hydraulic conductivity in rat mesenteric venules: pertussis toxin sensitive. Am J Physiol Heart Circ Physiol 289: H840–H844, 2005.
25. Mulivor AW, Lipowsky HH. Inhibition of glycan shedding and leukocyte-endothelial adhesion in postcapillary venules by suppression of matrixmetalloprotease activity with doxycycline. Microcirculation 16: 657–666, 2009.
26. Ohkawa R, Nakamura K, Okubo S, Hosogaya S, Ozaki Y, Tozuka M, Osima N, Yokota H, Ikeda H, Yatomi Y. Plasma sphingosine-1-phosphate measurement in healthy subjects: close correlation with red blood cell parameters. Ann Clin Biochem 45: 356–363, 2008.
27. Oohira A, Wight TN, Bornstein P. Sulfated proteoglycans synthesized by vascular endothelial cells in culture. J Biol Chem 258: 2014–2021, 1983.
28. Pries AR, Secomb TW, Gaehtgens P. The endothelial surface layer. Pflugers Arch 440: 653–666, 2000.
29. Rasband WS. ImageJ. U. S. National Institutes of Health, Bethesda, Maryland, USA, 1997–2012.
30. Reitsma S, oude Egbrink MG, Vink H, van den Berg BM, Passos VL, Engels W, Slaaf DW, van Zandvoort MA. Endothelial glycocalyx structure in the intact carotid artery: a two-photon laser scanning microscopy study. J Vasc Res 48: 297–306, 2011.
31. Reitsma S, Slaaf DW, Vink H, van Zandvoort MA, oude Egbrink MG. The endothelial glycocalyx: composition, functions, and visualization. Pflugers Arch 454: 345–359, 2007.
32. Schnitzer JE, Carley WW, Palade GE. Albumin interacts specifically with a 60-kDa microvascular endothelial glycoprotein. Proc Natl Acad Sci USA 85: 6773–6777, 1988.
33. Shen S, Fan J, Cai B, Lv Y, Zeng M, Hao Y, Giancotti FG, Fu BM. Vascular endothelial growth factor enhances cancer cell adhesion to microvascular endothelium in vivo. Exp Physiol 95: 369–379, 2010.
34. Smith ML, Long DS, Damiano ER, Ley K. Near-wall micro-PIV reveals a hydrodynamically relevant endothelial surface layer in venules in vivo. Biophys J 85: 637–645, 2003.
35. Sugihara-Sekia M, Fu BM. Blood flow and permeability in microvessels. Fluid Dyn Res 37: 82–132, 2005.
36. Tarbell JM, Pahakis MY. Mechanotransduction and the glycocalyx. J Intern Med 259: 339–350, 2006.
37. Tauseef M, Kini V, Knezevic N, Brannan M, Ramchandaran R, Fyrst H, Saba J, Vogel SM, Malik AB, Mehta D. Activation of sphingosine kinase-1 reverses the increase in lung vascular permeability through sphingosine-1-phosphate receptor signaling in endothelial cells. Circ Res 103: 1164–1172, 2008.
38. Wang L, Dudek SM. Regulation of vascular permeability by sphingosine 1-phosphate. Microvasc Res 77: 39–45, 2009.
39. Yen WY, Cai B, Yang JL, Zhang L, Zeng M, Tarbell JM, Fu BMM. Endothelial surface glycocalyx can regulate flow-induced nitric oxide production in microvessels in vivo. PLoS ONE 10: 1–20, 2015.
40. Yen WY, Cai B, Zeng M, Tarbell JM, Fu BM. Quantification of the endothelial surface glycocalyx on rat and mouse blood vessels. Microvasc Res 83: 337–346, 2012.
41. Yuan W, Lv YG, Zeng M, Fu BM. Non-invasive measurement of solute permeability in cerebral microvessels of the rat. Microvasc Res 77: 166–173, 2009.
42. Zeng Y, Adamson RH, Curry FR, Tarbell JM. Sphingosine-1-phosphate protects endothelial glycocalyx by inhibiting syndecan-1 shedding. Am J Physiol Heart Circ Physiol 306: H363–H372, 2014.
43. Zhang G, Xu S, Qian Y, He P. Sphingosine-1-phosphate prevents permeability increases via activation of endothelial sphingosine-1-phosphate receptor 1 in rat venules. Am J Physiol Heart Circ Physiol 299: H1494–H1504, 2010.