Endothelial surface glycocalyx can regulate flow-induced nitric oxide production in microvessels in vivo

PLoS ONE

Volumn 10, Issue 1, 2015, Pages

  Yen, Wanyi ^a   Cai, Bin ^a   Yang, Jinlin ^a   Zhang, Lin ^a   Zeng, Min ^a   Tarbell, John M ^a   Fu, Bingmei M ^a  

^a City College of New York   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ENDOTHELIAL NITRIC OXIDE SYNTHASE; HEPARAN SULFATE; HEPARANASE; NITRIC OXIDE; 3',6'-DIACETYLFLUORESCEIN; FLUORESCEIN DERIVATIVE; HEPARITINSULFATE LYASE; N(G) METHYLARGININE; POLYSACCHARIDE LYASE;

ADULT; ANIMAL TISSUE; ARTERIOLE; ARTICLE; BLOOD FLOW VELOCITY; CONTROLLED STUDY; ENDOTHELIAL SURFACE GLYCOCALYX; ENDOTHELIUM CELL; ENZYME ACTIVATION; ENZYME INHIBITION; FEMALE; FLUORESCENCE MICROSCOPY; GLYCOCALYX; IN VIVO STUDY; MECHANOTRANSDUCTION; MESENTERY; NONHUMAN; RAT; VENULE; ANIMAL; ANTAGONISTS AND INHIBITORS; CHEMISTRY; DRUG EFFECTS; HEMODYNAMICS; INTRAVITAL MICROSCOPY; METABOLISM; MICROVASCULATURE; PHYSIOLOGY; SPRAGUE DAWLEY RAT; VASCULAR ENDOTHELIUM;

RATTUS;

ANIMALS; ARTERIOLES; BLOOD FLOW VELOCITY; ENDOTHELIUM, VASCULAR; FEMALE; FLUORESCEINS; GLYCOCALYX; HEMODYNAMICS; INTRAVITAL MICROSCOPY; MICROVESSELS; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; OMEGA-N-METHYLARGININE; POLYSACCHARIDE-LYASES; RATS; RATS, SPRAGUE-DAWLEY;

EID: 84920842003     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0117133     Document Type: Article

References (67)

1. Barakat AI (2008) Dragging along: the glycocalyx and vascular endothelial cell mechanotransduction. Circulation research 102: 747-748. doi: 10.1161/CIRCRESAHA.108.174839 PMID: 18403731
2. Tarbell JM, Pahakis MY (2006) Mechanotransduction and the glycocalyx. Journal of internal medicine 259: 339-350. doi: 10.1111/j.1365-2796.2006.01620.x PMID: 16594902
3. Weinbaum S, Tarbell JM, Damiano ER (2007) The structure and function of the endothelial glycocalyx layer. Annual review of biomedical engineering 9: 121-167. doi: 10.1146/annurev.bioeng.9.060906. 51959 PMID: 17373886
4. 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. doi: 10.1002/wsbm. 211 PMID: 23401243
5. Becker BF, Chappell D, Jacob M (2010) Endothelial glycocalyx and coronary vascular permeability: the fringe benefit. Basic research in cardiology 105: 687-701. doi: 10.1007/s00395-010-0118-z PMID: 20859744
6. Curry FR, Adamson RH (2010) Vascular permeability modulation at the cell, microvessel, or whole organ level: towards closing gaps in our knowledge. Cardiovascular research 87: 218-229. doi: 10. 1093/cvr/cvq115 PMID: 20418473
7. van den Berg BM, Vink H, Spaan JA (2003) The endothelial glycocalyx protects against myocardial edema. Circulation research 92: 592-594. doi: 10.1161/01.RES.0000065917.53950.75 PMID: 12637366
8. van Haaren PM, VanBavel E, Vink H, Spaan JA (2003) Localization of the permeability barrier to solutes in isolated arteries by confocal microscopy. American journal of physiology Heart and circulatory physiology 285: H2848-2856. PMID: 12907418
9. Constantinescu AA, Vink H, Spaan JA (2003) Endothelial cell glycocalyx modulates immobilization of leukocytes at the endothelial surface. Arteriosclerosis, thrombosis, and vascular biology 23: 1541-1547. doi: 10.1161/01.ATV.0000085630.24353.3D PMID: 12855481
10. Mulivor AW, Lipowsky HH (2009) Inhibition of glycan shedding and leukocyte-endothelial adhesion in postcapillary venules by suppression of matrixmetalloprotease activity with doxycycline. Microcirculation 16: 657-666. doi: 10.3109/10739680903133714 PMID: 19905966
11. Pries AR, Secomb TW, Gaehtgens P (2000) The endothelial surface layer. Pflugers Archiv: European journal of physiology 440: 653-666. doi: 10.1007/s004240000307 PMID: 11007304
12. Wu Q, Andreopoulos Y, Weinbaum S (2004) From red cells to snowboarding: a new concept for a train track. Physical Review Letters 93: 194501. doi: 10.1103/PhysRevLett.93.194501 PMID: 15600838
13. Chappell D, Heindl B, Jacob M, Annecke T, Chen C, et al. (2011) Sevoflurane Reduces Leukocyte and Platelet Adhesion after Ischemia-Reperfusion by Protecting the Endothelial Glycocalyx. Anesthesiology 115: 483-491. doi: 10.1097/ALN.0b013e3182289988 PMID: 21785339
14. Reitsma S, Slaaf DW, Vink H, van Zandvoort MA, oude Egbrink MG (2007) The endothelial glycocalyx: composition, functions, and visualization. Pflugers Archiv: European journal of physiology 454: 345-359. doi: 10.1007/s00424-007-0212-8 PMID: 17256154
15. VanTeeffelen JW, Brands J, Vink H (2010) Agonist-induced impairment of glycocalyx exclusion properties: contribution to coronary effects of adenosine. Cardiovascular research 87: 311-319. doi: 10.1093/ cvr/cvq114 PMID: 20418474
16. Padberg JS, Wiesinger A, di Marco GS, Reuter S, Grabner A, et al. (2014) Damage of the endothelial glycocalyx in chronic kidney disease. Atherosclerosis 234: 335-343. doi: 10.1016/j.atherosclerosis. 2014.03.016 PMID: 24727235
17. Cai B, Fan J, Zeng M, Zhang L, Fu BM (2012) 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. doi: 10.1152/japplphysiol.00479.2012
18. Forstermann U, Sessa WC (2012) Nitric oxide synthases: regulation and function. European heart journal 33: 829-837, 837a-837d. doi: 10.1093/eurheartj/ehr304 PMID: 21890489
19. Cooke JP, Stamler J, Andon N, Davies PF, McKinley G, et al. (1990) Flow stimulates endothelial cells to release a nitrovasodilator that is potentiated by reduced thiol. Am J Physiol 259: H804-812. PMID: 2396689
20. Forstermann U, Munzel T (2006) Endothelial nitric oxide synthase in vascular disease: from marvel to menace. Circulation 113: 1708-1714. doi: 10.1161/CIRCULATIONAHA.105.602532 PMID: 16585403
21. Florian JA, Kosky JR, Ainslie K, Pang Z, Dull RO, et al. (2003) Heparan sulfate proteoglycan is a mechanosensor on endothelial cells. Circulation research 93: e136-142. doi: 10.1161/01.RES. 0000101744.47866.D5 PMID: 14563712
22. Ziegler T, Bouzourene K, Harrison VJ, Brunner HR, Hayoz D (1998) Influence of oscillatory and unidirectional flow environments on the expression of endothelin and nitric oxide synthase in cultured endothelial cells. Arteriosclerosis, thrombosis, and vascular biology 18: 686-692. doi: 10.1161/01.ATV.18. 5.686 PMID: 9598825
23. Pritchard KA Jr, Groszek L, Smalley DM, Sessa WC, Wu M, et al. (1995) Native low-density lipoprotein increases endothelial cell nitric oxide synthase generation of superoxide anion. Circulation research 77: 510-518. doi: 10.1161/01.RES.77.3.510 PMID: 7543827
24. Guo X, Kassab GS (2009) Role of shear stress on nitrite and NOS protein content in different size conduit arteries of swine. Acta Physiol (Oxf) 197: 99-106. doi: 10.1111/j.1748-1716.2009.01999.x
25. Pohl U, Herlan K, Huang A, Bassenge E (1991) EDRF-mediated shear-induced dilation opposes myogenic vasoconstriction in small rabbit arteries. Am J Physiol 261: H2016-2023. PMID: 1721502
26. Kuchan MJ, Frangos JA (1994) Role of calcium and calmodulin in flow-induced nitric oxide production in endothelial cells. Am J Physiol 266: C628-636. PMID: 8166225
27. 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. doi: 10. 1016/j.bbrc.2007.01.137 PMID: 17291452
28. Lopez-Quintero SV, Amaya R, Pahakis M, Tarbell JM (2009) The endothelial glycocalyx mediates shear-induced changes in hydraulic conductivity. American journal of physiology Heart and circulatory physiology 296: H1451-1456. doi: 10.1152/ajpheart.00894.2008 PMID: 19286951
29. Koo A, Nordsletten D, Umeton R, Yankama B, Ayyadurai S, et al. (2013) In silico modeling of shear-stress-induced nitric oxide production in endothelial cells through systems biology. Biophys J 104: 2295-2306. doi: 10.1016/j.bpj.2013.03.052 PMID: 23708369
30. Stevens HY MB, Bell KS, Yun S, Yeh JC, Frangos JA (2008) PECAM-1 is a critical mediator of atherosclerosis. Disease Models & Mechanisms 1: 175-181. doi: 10.1242/dmm.000547
31. Schwartz MA, DeSimone DW (2008) Cell adhesion receptors in mechanotransduction. Curr Opin Cell Biol 20: 551-556. doi: 10.1016/j.ceb.2008.05.005 PMID: 18583124
32. Gojova A, Barakat AI (2005) Vascular endothelial wound closure under shear stress: role of membrane fluidity and flow-sensitive ion channels. J Appl Physiol (1985) 98: 2355-2362. doi: 10.1152/ japplphysiol.01136.2004
33. Gautam M, Shen Y, Thirkill TL, Douglas GC, Barakat AI (2006) Flow-activated chloride channels in vascular endothelium. Shear stress sensitivity, desensitization dynamics, and physiological implications. J Biol Chem 281: 36492-36500. doi: 10.1074/jbc.M605866200 PMID: 16973617
34. Yamamoto K, Ando J (2011) New molecular mechanisms for cardiovascular disease:blood flow sensing mechanism in vascular endothelial cells. J Pharmacol Sci 116: 323- 331. doi: 10.1254/jphs. 10R29FM PMID: 21757846
35. Tabouillot T, Muddana HS, Butler PJ (2011) Endothelial Cell Membrane Sensitivity to Shear Stress is Lipid Domain Dependent. Cell Mol Bioeng 4: 169-181. doi: 10.1007/s12195-010-0136-9 PMID: 22247740
36. Egorova AD vdHK, Poelmann RE, Hierck BP (2012) Primary cilia as biomechanical sensors in regulating endothelial function. Differentiation 83: S56-61. doi: 10.1016/j.diff.2011.11.007 PMID: 22169885
37. Matsui TS, Kaunas R, Kanzaki M, Sato M, Deguchi S (2011) Non-muscle myosin II induces disassembly of actin stress fibres independently of myosin light chain dephosphorylation. Interface Focus 1: 754-766. doi: 10.1098/rsfs.2011.0031 PMID: 23050080
38. Morgan JT, Pfeiffer ER, Thirkill TL, Kumar P, Peng G, et al. (2011) Nesprin-3 regulates endothelial cell morphology, perinuclear cytoskeletal architecture, and flow-induced polarization. Mol Biol Cell 22: 4324-4334. doi: 10.1091/mbc.E11-04-0287 PMID: 21937718
39. Wang N, Tytell JD, Ingber DE (2009) Mechanotransduction at a distance: mechanically coupling the extracellular matrix with the nucleus. Nat Rev Mol Cell Biol 10: 75-82. doi: 10.1038/nrm2594 PMID: 19197334
40. Kang H, Fan Y, Deng X (2011) Vascular smooth muscle cell glycocalyx modulates shear-induced proliferation, migration, and NO production responses. American journal of physiology Heart and circulatory physiology 300: H76-83. doi: 10.1152/ajpheart.00905.2010 PMID: 21037235
41. Juffer P, Bakker AD, Klein-Nulend J, Jaspers RT (2014) Mechanical loading by fluid shear stress of myotube glycocalyx stimulates growth factor expression and nitric oxide production. Cell Biochem Biophys 69: 411-419. doi: 10.1007/s12013-013-9812-4 PMID: 24402674
42. Mochizuki S, Vink H, Hiramatsu O, Kajita T, Shigeto F, et al. (2003) Role of hyaluronic acid glycosaminoglycans in shear-induced endothelium-derived nitric oxide release. American journal of physiology Heart and circulatory physiology 285: H722-726. PMID: 12730059
43. Kumagai R, Lu X, Kassab GS (2009) Role of glycocalyx in flow-induced production of nitric oxide and reactive oxygen species. Free Radic Biol Med 47: 600-607. doi: 10.1016/j.freeradbiomed.2009.05.034 PMID: 19500664
44. Giantsos-Adams KM, Koo AJ, Song S, Sakai J, Sankaran J, et al. (2013) Heparan Sulfate Regrowth Profiles Under Laminar Shear Flow Following Enzymatic Degradation. Cell Mol Bioeng 6: 160-174. doi: 10.1007/s12195-013-0273-z PMID: 23805169
45. Koo A, Dewey CF Jr, Garcia-Cardena G (2013) Hemodynamic shear stress characteristic of athero-sclerosis-resistant regions promotes glycocalyx formation in cultured endothelial cells. Am J Physiol Cell Physiol 304: C137-146. doi: 10.1152/ajpcell.00187.2012 PMID: 23114962
46. Zeng Y, Tarbell JM (2014) The adaptive remodeling of endothelial glycocalyx in response to fluid shear stress. PLoS One 9: e86249. doi: 10.1371/journal.pone.0086249 PMID: 24465988
47. Yao Y, Rabodzey A, Dewey CF Jr (2007) Glycocalyx modulates the motility and proliferative response of vascular endothelium to fluid shear stress. American journal of physiology Heart and circulatory physiology 293: H1023-1030. doi: 10.1152/ajpheart.00162.2007 PMID: 17468337
48. VanTeeffelen JW, Brands J, Jansen C, Spaan JA, Vink H (2007) Heparin impairs glycocalyx barrier properties and attenuates shear dependent vasodilation in mice. Hypertension 50: 261-267. doi: 10. 1161/HYPERTENSIONAHA.107.089250 PMID: 17452501
49. Zhou X, He P (2011) Improved measurements of intracellular nitric oxide in intact microvessels using 4,5-diaminofluorescein diacetate. American journal of physiology Heart and circulatory physiology 301: H108-114. doi: 10.1152/ajpheart.00195.2011 PMID: 21536843
50. Yen WY, Cai B, Zeng M, Tarbell JM, Fu BM (2012) Quantification of the endothelial surface glycocalyx on rat and mouse blood vessels. Microvascular research. doi: 10.1016/j.mvr.2012.02.005 PMID: 22349291
51. Fu BM, Shen S (2004) Acute VEGF effect on solute permeability of mammalian microvessels in vivo. Microvascular research 68: 51-62. doi: 10.1016/j.mvr.2004.03.004 PMID: 15219420
52. Shen S, Fan J, Cai B, Lv Y, Zeng M, et al. (2010) Vascular endothelial growth factor enhances cancer cell adhesion to microvascular endothelium in vivo. Experimental physiology 95: 369-379. doi: 10. 1113/expphysiol.2009.050260 PMID: 19880535
53. Chappell D, Jacob M, Rehm M, Stoeckelhuber M, Welsch U, et al. (2008) Heparinase selectively sheds heparan sulphate from the endothelial glycocalyx. Biol Chem 389: 79-82. doi: 10.1515/BC.2008.005 PMID: 18095872
54. Guo P, Cai B, Lei M, Liu Y, Fu BM (2014) Differential arrest and adhesion of tumor cells and microbeads in the microvasculature. Biomech Model Mechanobiol 13: 537-550. doi: 10.1007/s10237-013-0515-y PMID: 23880911
55. Liu Q, Mirc D, Fu BM (2008) Mechanical mechanisms of thrombosis in intact bent microvessels of rat mesentery. J Biomech 41: 2726-2734. doi: 10.1016/j.jbiomech.2008.06.013 PMID: 18656200
56. Baker M, Wayland H (1974) On-line volume flow rate and velocity profile measurement for blood in microvessels. Microvascular research 7: 131-143. doi: 10.1016/0026-2862(74)90043-0 PMID: 4821168
57. Williams DA (2007) Change in shear stress (Deltatau)/hydraulic conductivity (Lp) relationship after pronase treatment of individual capillaries in situ. Microvascular research 73: 48-57. doi: 10.1016/j.mvr. 2006.08.003 PMID: 17030043
58. Kojima H NN, Kikuchi K, Urano Y, Higuchi T, Tanaka J, et al. (1998) Direct evidence of NO production in rat hippocampus and cortex using a new fluorescent indicator: DAF-2 DA. NeuroReport 9: 3345-3348. doi: 10.1097/00001756-199810260-00001 PMID: 9855277
59. Yi FX, Zhang AY, Campbell WB, Zou AP, Van Breemen C, et al. (2002) Simultaneous in situ monitoring of intracellular Ca2+ and NO in endothelium of coronary arteries. American journal of physiology Heart and circulatory physiology 283: H2725-2732. PMID: 12388315
60. Zhu L, He P (2005) Platelet-activating factor increases endothelial [Ca2+]i and NO production in individually perfused intact microvessels. American journal of physiology Heart and circulatory physiology 288: H2869-2877. doi: 10.1152/ajpheart.01080.2004 PMID: 15665052
61. Reitsma S, oude Egbrink MG, Vink H, van den Berg BM, Passos VL, et al. (2011) Endothelial glycocalyx structure in the intact carotid artery: a two-photon laser scanning microscopy study. J Vasc Res 48: 297-306. doi: 10.1159/000322176 PMID: 21273784
62. Chang YS, Yaccino JA, Lakshminarayanan S, Frangos JA, Tarbell JM (2000) Shear-induced increase in hydraulic conductivity in endothelial cells is mediated by a nitric oxide-dependent mechanism. Arteriosclerosis, thrombosis, and vascular biology 20: 35-42. doi: 10.1161/01.ATV.20.1.35 PMID: 10634798
63. Rosenberg RD, Shworak NW, Liu J, Schwartz JJ, Zhang L (1997) Heparan sulfate proteoglycans of the cardiovascular system. Specific structures emerge but how is synthesis regulated? J Clin Invest 100: S67-75.
64. Ebong EE, Lopez-Quintero SV, Rizzo V, Spray DC, Tarbell JM (2014) Shear-induced endothelial NOS activation and remodeling via heparan sulfate, glypican-1, and syndecan-1. Integr Biol (Camb) 6: 338-347. doi: 10.1039/c3ib40199e
65. Gao L, Lipowsky HH (2010) Composition of the endothelial glycocalyx and its relation to its thickness and diffusion of small solutes. Microvascular research 80: 394-401. doi: 10.1016/j.mvr.2010.06.005 PMID: 20600162
66. 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. doi: 10.1371/journal.pone.0043168 PMID: 22905223
67. Tarbell JM (2010) Shear stress and the endothelial transport barrier. Cardiovascular research 87: 320-330. doi: 10.1093/cvr/cvq146 PMID: 20543206