New insights into shear stress-induced endothelial signalling and barrier function: Cell-free fluid versus blood flow

Cardiovascular Research

Volumn 113, Issue 5, 2017, Pages 508-518

  Xu, Sulei ^a   Li, Xiang ^a   Lapenna, Kyle Brian ^a   Yokota, Stanley David ^b   Huke, Sabine ^c   He, Pingnian ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b WEST VIRGINIA UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c University of Alabama at Birmingham   (United States)

Author keywords

ATP; Endothelial calcium; Microvessel permeability; Nitric oxide; Shear stress

Indexed keywords

ADENOSINE TRIPHOSPHATE; CALCIUM ION; ENDOTHELIAL NITRIC OXIDE SYNTHASE; CALCIUM; NITRIC OXIDE; NOS3 PROTEIN, RAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BIOLUMINESCENCE; BLOOD FLOW; CALCIUM CELL LEVEL; CELL FREE SYSTEM; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; ENZYME RELEASE; ERYTHROCYTE; FEMALE; FLOW RATE; FLUORESCENCE ANALYSIS; IMMUNOHISTOCHEMISTRY; INTRACELLULAR SIGNALING; NONHUMAN; PRIORITY JOURNAL; RAT; SHEAR STRESS; VASCULAR ENDOTHELIAL CELL; VENULE; VISCOSITY; ANIMAL; BLOOD FLOW VELOCITY; BLOOD VISCOSITY; CAPILLARY PERMEABILITY; COMPARATIVE STUDY; ENDOTHELIUM CELL; GAP JUNCTION; IN VITRO STUDY; MECHANICAL STRESS; MECHANOTRANSDUCTION; METABOLISM; PERFUSION; PHOSPHORYLATION; SPRAGUE DAWLEY RAT; TIME FACTOR;

ADENOSINE TRIPHOSPHATE; ANIMALS; BLOOD FLOW VELOCITY; BLOOD VISCOSITY; CALCIUM; CAPILLARY PERMEABILITY; ENDOTHELIAL CELLS; ENZYME ACTIVATION; ERYTHROCYTES; FEMALE; GAP JUNCTIONS; IN VITRO TECHNIQUES; MECHANOTRANSDUCTION, CELLULAR; NITRIC OXIDE; NITRIC OXIDE SYNTHASE TYPE III; PERFUSION; PHOSPHORYLATION; RATS, SPRAGUE-DAWLEY; REGIONAL BLOOD FLOW; STRESS, MECHANICAL; TIME FACTORS; VENULES;

EID: 85019143555     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvx021     Document Type: Article

References (46)

1. Stone PH, Coskun AU, Kinlay S, Clark ME, Sonka M, Wahle A, Ilegbusi OJ, Yeghiazarians Y, Popma JJ, Orav J, Kuntz RE, Feldman CL. Effect of endothelial shear stress on the progression of coronary artery disease, vascular remodeling, and instent restenosis in humans: in vivo 6-month follow-up study. Circulation 2003;108: 438-444
2. Bodin P, Bailey D, Burnstock G. Increased flow-induced ATP release from isolated vascular endothelial cells but not smooth muscle cells. Br J Pharmacol 1991;103: 1203-1205
3. Bodin P, Burnstock G. Purinergic signalling: ATP release. Neurochem Res 2001;26: 959-969
4. Wang S, Chennupati R, Kaur H, Iring A, Wettschureck N, Offermanns S. Endothelial cation channel PIEZO1 controls blood pressure by mediating flow-induced ATP release. J Clin Invest 2016;126:4527-4536
5. Wang S, Iring A, Strilic B, Albarran Juarez J, Kaur H, Troidl K, Tonack S, Burbiel JC, Muller CE, Fleming I, Lundberg JO, Wettschureck N, Offermanns S. P2Y(2) and Gq/ G(1)(1) control blood pressure by mediating endothelial mechanotransduction. J Clin Invest 2015;125:3077-3086
6. Tarbell JM, Simon SI, Curry FR. Mechanosensing at the vascular interface. Annu Rev Biomed Eng 2014;16:505-532
7. Mendoza SA, Fang J, Gutterman DD, Wilcox DA, Bubolz AH, Li R, Suzuki M, Zhang DX. TRPV4-mediated endothelial Ca2 and thorn influx and vasodilation in response to shear stress. Am J Physiol Heart Circ Physiol 2010;298:H466-H476
8. Geiger RV, Berk BC, Alexander RW, Nerem RM. Flow-induced calcium transients in single endothelial cells: spatial and temporal analysis. Am J Physiol 1992;262: C1411-C1417
9. Curry FR, Adamson RH. Vascular permeability modulation at the cell, microvessel, or whole organ level: towards closing gaps in our knowledge. Cardiovasc Res 2010;87:218-229
10. Forsyth AM, Wan J, Owrutsky PD, Abkarian M, Stone HA. Multiscale approach to link red blood cell dynamics, shear viscosity, and ATP release. Proc Natl Acad Sci USA 2011;108:10986-10991
11. Wan J, Ristenpart WD, Stone HA. Dynamics of shear-induced ATP release from red blood cells. Proc Natl Acad Sci USA 2008;105:16432-16437
12. Edwards J, Sprung R, Sprague R, Spence D. Chemiluminescence detection of ATP release from red blood cells upon passage through microbore tubing. Analyst 2001;126:1257-1260
13. Sprague RS, Ellsworth ML, Stephenson AH, Lonigro AJ. ATP: the red blood cell link to NO and local control of the pulmonary circulation. Am J Physiol 1996;271: H2717-H2722
14. Price AK, Martin RS, Spence DM. Monitoring erythrocytes in a microchip channel that narrows uniformly: towards an improved microfluidic-based mimic of the microcirculation. J Chromatogr A 2006;1111:220-227
15. Neal CR, Bates DO. Measurement of hydraulic conductivity of single perfused Rana mesenteric microvessels between periods of controlled shear stress. J Physiol 2002; 543:947-957
16. Williams DA. A shear stress component to the modulation of capillary hydraulic conductivity (Lp). Microcirculation 1996;3:229-232
17. Adamson RH, Sarai RK, Altangerel A, Clark JF, Weinbaum S, Curry FE. Microvascular permeability to water is independent of shear stress, but dependent on flow direction. Am J Physiol Heart Circ Physiol 2013;304:H1077-H1084
18. Muller JM, Davis MJ, Kuo L, Chilian WM. Changes in coronary endothelial cell Ca2 and thorn concentration during shear stress-and agonist-induced vasodilation. Am J Physiol 1999;276:H1706-H1714
19. Ungvari Z, Sun D, Huang A, Kaley G, Koller A. Role of endothelial [Ca2 and thorn ]i in activation of eNOS in pressurized arterioles by agonists and wall shear stress. Am J Physiol Heart Circ Physiol 2001;281:H606-H612
20. Kajimura M, Head SD, Michel CC. The effects of flow on the transport of potassium ions through the walls of single perfused frog mesenteric capillaries. J Physiol 1998;511 (pt. 3):707-718
21. Zweifach BW, Lipowsky HH. Quantitative studies of microcirculatory structure and function. III. Microvascular hemodynamics of cat mesentery and rabbit omentum. Circ Res 1977;41:380-390
22. He P, Zhang X, Curry FE. Ca2 and thorn entry through conductive pathway modulates receptormediated increase in microvessel permeability. Am J Physiol 1996;271:H2377-H2387
23. Zhou X, He P. Improved measurements of intracellular nitric oxide in intact microvessels using 4,5-diaminofluorescein diacetate. Am J Physiol Heart Circ Physiol 2011;301:H108-H114
24. Zhou X, Yuan D, Wang M, He P. H2O2-induced endothelial NO production contributes to vascular cell apoptosis and increased permeability in rat venules. Am J Physiol Heart Circ Physiol 2013;304:H82-H93
25. Jiang Y, Wen K, Zhou X, Schwegler-Berry D, Castranova V, He P. Three-dimensional localization and quantification of PAF-induced gap formation in intact venular microvessels. Am J Physiol Heart Circ Physiol 2008;295:H898-H906
26. Lipowsky HH, Kovalcheck S, Zweifach BW. The distribution of blood rheological parameters in the microvasculature of cat mesentery. Circ Res 1978;43:738-749
27. Pries AR, Neuhaus D, Gaehtgens P. Blood viscosity in tube flow: dependence on diameter and hematocrit. Am J Physiol 1992;263:H1770-H1778
28. Secomb TW. Flow-dependent rheological properties of blood in capillaries. Microvasc Res 1987;34:46-58
29. Locovei S, Bao L, Dahl G. Pannexin 1 in erythrocytes: function without a gap. Proc Natl Acad Sci USA 2006;103:7655-7659
30. 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 2014;306:H1011-H1017
31. 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 2012;303:H825-H834
32. 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 2010;299:H1494-H1504
33. Ellsworth ML, Ellis CG, Sprague RS. Role of erythrocyte-released ATP in the regulation of microvascular oxygen supply in skeletal muscle. Acta Physiol (Oxf) 2016;216:265-276
34. Lohman AW, Billaud M, Isakson BE. Mechanisms of ATP release and signalling in the blood vessel wall. Cardiovasc Res 2012;95:269-280
35. Shen J, Luscinskas FW, Connolly A, Dewey CF Jr, Gimbrone MA Jr. Fluid shear stress modulates cytosolic free calcium in vascular endothelial cells. Am J Physiol 1992;262:C384-C390
36. Buga GM, Gold ME, Fukuto JM, Ignarro LJ. Shear stress-induced release of nitric oxide from endothelial cells grown on beads. Hypertension 1991;17:187-193
37. Kuchan MJ, Frangos JA. Role of calcium and calmodulin in flow-induced nitric oxide production in endothelial cells. Am J Physiol 1994;266:C628-C636
38. Jourd'heuil D. Increased nitric oxide-dependent nitrosylation of 4,5-diaminofluorescein by oxidants: implications for the measurement of intracellular nitric oxide. Free Radic Biol Med 2002;33:676-684
39. Xu S, Zhou X, Yuan D, Xu Y, He P. Caveolin-1 scaffolding domain promotes leukocyte adhesion by reduced basal endothelial nitric oxide-mediated ICAM-1 phosphorylation in rat mesenteric venules. Am J Physiol Heart Circ Physiol 2013;305:H1484-H1493
40. Fleming I, Busse R. Molecular mechanisms involved in the regulation of the endothelial nitric oxide synthase. Am J Physiol Regul Integr Comp Physiol 2003;284:R1-R12
41. Fleming I, Fisslthaler B, Dimmeler S, Kemp BE, Busse R. Phosphorylation of Thr(495) regulates Ca(2 and thorn )/calmodulin-dependent endothelial nitric oxide synthase activity. Circ Res 2001;88:E68-E75
42. Cortese-Krott MM, Kelm M. Endothelial nitric oxide synthase in red blood cells: key to a new erythrocrine function? Redox Biol 2014;2:251-258
43. Montermini D, Winlove CP, Michel C. Effects of perfusion rate on permeability of frog and rat mesenteric microvessels to sodium fluorescein. J Physiol 2002;543:959-975
44. Yuan Y, Granger HJ, Zawieja DC, Chilian WM. Flow modulates coronary venular permeability by a nitric oxide-related mechanism. Am J Physiol 1992;263:H641-H646
45. Bargiotas P, Krenz A, Monyer H, Schwaninger M. Functional outcome of pannexindeficient mice after cerebral ischemia. Channels (Austin) 2012;6:453-456
46. Dvoriantchikova G, Ivanov D, Barakat D, Grinberg A, Wen R, Slepak VZ, Shestopalov VI. Genetic ablation of Pannexin1 protects retinal neurons from ischemic injury. PLoS One 2012;7:e31991