Vascular permeability modulation at the cell, microvessel, or whole organ level: Towards closing gaps in our knowledge

Cardiovascular Research

Volumn 87, Issue 2, 2010, Pages 218-229

  Curry, Fitz Roy E ^a   Adamson, Roger H ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Endothelial cell heterogeneity; Endothelial glycocalyx; Glycocalyx volume; Perfusion and permeability; Rac1 and endothelial permeability; Thrombin; VE cadherin and inflammation; Wound healing

Indexed keywords

PHOSPHODIESTERASE; THROMBIN; WATER; AUTACOID;

BLOOD TRANSFUSION; BLOOD VESSEL PERMEABILITY; CELL LEVEL; ENDOTHELIUM CELL; GLYCOCALYX; INFLAMMATION; MACROMOLECULE; MICROVASCULATURE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REVIEW; ANIMAL; ANIMAL MODEL; BIOLOGICAL MODEL; BLOOD FLOW; BODY FLUID; CAPILLARY PERMEABILITY; EDEMA; HUMAN; IMMUNOLOGY; METABOLISM; MOUSE; OSMOTIC PRESSURE; PATHOPHYSIOLOGY; VASCULAR ENDOTHELIUM;

ANIMALS; BODY FLUIDS; CAPILLARY PERMEABILITY; EDEMA; ENDOTHELIUM, VASCULAR; GLYCOCALYX; HUMANS; INFLAMMATION; INFLAMMATION MEDIATORS; MICE; MICROVESSELS; MODELS, ANIMAL; MODELS, CARDIOVASCULAR; OSMOTIC PRESSURE; REGIONAL BLOOD FLOW; THROMBIN;

EID: 77954343077     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvq115     Document Type: Review

References (105)

1. Dejana E, Tournier-Lasserve E, Weinstein BM. The control of vascular integrity by endothelial cell junctions: molecular basis and pathological implications. Dev Cell 2009;16:209-221.
2. Garcia JG. Concepts in microvascular endothelial barrier regulation in health and disease. Microvasc Res 2009;77:1-3.
3. van der Heijden M, van Nieuw Amerongen GP, Chedamni S, van Hinsbergh VW, Johan Groeneveld AB. The angiopoietin-Tie2 system as a therapeutic target in sepsis and acute lung injury. Expert Opin Ther Targets 2009;13:39-53.
4. Spindler V, Schlegel N, Waschke J. Role of GTPases in control of microvascular permeability. Cardiovasc Res 2010;87:243-253.
5. Boerma EC. The microcirculation as a clinical concept: work in progress. Curr Opin Crit Care 2009;15:261-265.
6. Crone C. The Malpighi lecture. From 'Porositates carnis' to cellular microcirculation. Int J Microcirc Clin Exp 1987;6:101-122.
7. Iversen VV, Nedrebo T, Borge BA, Salvesen GS, Reed RK. Platelet activating factor (PAF) increases plasma protein extravasation and induces lowering of interstitial fluid pressure (P) in rat skin. Acta Physiol Scand 2005;185:5-12.
8. Reed RK, Rubin K. Transcapillary exchange: role and importance of the interstitial fluid pressure and the extracellular matrix. Cardiovasc Res 2010;87:211-217.
9. Fox JL, von der Weid PY. Effects of histamine on the contractile and electrical activity in isolated lymphatic vessels of the guinea-pig mesentery. Br J Pharmacol 2002;136:1210-1218.
10. Aird WC. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ Res 2007;100:158-173.
11. Chiu JJ, Usami S, Chien S. Vascular endothelial responses to altered shear stress: pathologic implications for atherosclerosis. Ann Med 2009;41:19-28.
12. Wasserman SM, Topper JN. Adaptation of the endothelium to fluid flow: in vitro analyses of gene expression and in vivo implications. Vasc Med 2004;9:35-45.
13. Curry FR. Microvascular solute and water transport. Microcirculation 2005;12:17-31.
14. Singh A, Satchell SC, Neal CR, McKenzie EA, Tooke JE, Mathieson PW. Glomerular endothelial glycocalyx constitutes a barrier to protein permeability. J Am Soc Nephrol 2007;18:2885-2893.
15. van den Berg BM, Nieuwdorp M, Stroes ES, Vink H. Glycocalyx and endothelial (dys) function: from mice to men. Pharmacol Rep 2006;58(Suppl.):75- 80.
16. Adamson RH, Lenz JF, Zhang X, Adamson GN, Weinbaum S, Curry FE. Oncotic pressures opposing filtration across non-fenestrated rat microvessels. J Physiol 2004;557:889-907.
17. Levick JR, Michel C. Microvascular fluid exchange and the revised Starling principle. Cardiovasc Res 2010;87:198-210.
18. Becker BF, Chappell D, Brügger D, Annecke T, Jacob M. Therapeutic strategies targeting the endothelial glycocalyx: acute deficits, but great potential. Cardiovasc Res 2010;87:300-310.
19. VanTeeffelen JWGE, Brands J, Vink H. Agonist-induced impairment of glycocalyx exclusion properties: contribution to coronary effects of adenosine. Cardiovasc Res 2010;87:311-319.
20. Gouverneur M, Spaan JA, Pannekoek H, Fontijn RD, Vink H. Fluid shear stress stimulates incorporation of hyaluronan into endothelial cell glycocalyx. Am J Physiol Heart Circ Physiol 2006;290:H458-H452.
21. Potter DR, Jiang J, Damiano ER. The recovery time course of the endothelial cell glycocalyx in vivo and its implications in vitro. Circ Res 2009;104:1318-1325.
22. Feletou M, Bonnardel E, Canet E. Bradykinin and changes in microvascular permeability in the hamster cheek pouch: role of nitric oxide. Br J Pharmacol 1996; 118:1371-1376.
23. Durán WN, Breslin JW, Sánchez FA. The NO cascade, eNOS location and micro-vascular permeability. Cardiovasc Res 2010;87:254-261.
24. Bates DO. Vascular endothelial growth factors and vascular permeability. Cardiovasc Res 2010; doi:10.1093/cvr/cvq105. Published online ahead of print 16 April 2010.
25. Nagy JA, Benjamin L, Zeng H, Dvorak AM, Dvorak HF. Vascular permeability, vascular hyperpermeability and angiogenesis. Angiogenesis 2008;11:109-119.
26. Renkin EM, Tucker VL. Measurement of microvascular transport parameters of macromolecules in tissues and organs of intact animals. Microcirculation 1998;5: 139-152.
27. Tucker VL, Simanonok KE, Renkin EM. Tissue-specific effects of physiological ANP infusion on blood-tissue albumin transport. Am J Physiol 1992;263:R945-R953.
28. Nedrebo T, Reed RK, Berg A. Effect of alpha-trinositol on interstitial fluid pressure, edema generation, and albumin extravasation after ischemia-reperfusion injury in rat hind limb. Shock 2003;20:149-153.
29. Wallace JR, Powers MR, Bell DR. Transvascular albumin and IgG flux in skin and skeletal muscle following plasmapheresis. Microvasc Res 1992;44:295-306.
30. Curry FR, Rygh CB, Karlsen T, Wiig H, Adamson RH, Clark JF et al. Atrial natriuretic peptide modulation of albumin clearance and contrast agent permeability in mouse skeletal muscle and skin: role in regulation of plasma volume. J Physiol 2010;588: 325-339.
31. Samardzic H, Lenz JF, Adamson RH, Renkin EM, Reed RK, Curry FE. A dual label fluorescence technique for measuring macromolecular clearance in the mouse. FASEB J 2006;20:A708.
32. Huxley VH, Curry FE, Adamson RH. Quantitative fluorescence microscopy on single capillaries: alpha-lactalbumin transport. Am J Physiol 1987;252:H188-H197.
33. Fu BM, Shen S. Acute VEGF effect on solute permeability of mammalian microves-sels in vivo. Microvasc Res 2004;68:51-62.
34. Huxley VH, Wang JJ, Sarelius IH. Adaptation of coronary microvascular exchange in arterioles and venules to exercise training and a role for sex in determining permeability responses. Am J Physiol Heart Circ Physiol 2007;293:H1196-H1205.
35. Zhou X, Wen K, Yuan D, Ai L, He P. Calcium influx-dependent differential actions of superoxide and hydrogen peroxide on microvessel permeability. Am J Physiol Heart Circ Physiol 2009;296:H1096-H1107.
36. Kim MH, Curry FR, Simon SI. Dynamics of neutrophil extravasation and vascular permeability are uncoupled during aseptic cutaneous wounding. Am J Physiol 2009; 296:C848-C856.
37. Sarelius IH, Kuebel JM, Wang J, Huxley VH. Macromolecule permeability of in situ and excised rodent skeletal muscle arterioles and venules. Am J Physiol Heart Circ Physiol 2006;290:H474-H480.
38. Brekke-Rygh C, Seo JW, Qin SP, Mahakian LM, Zhang H, Kukis DL et al. Longitudinal investigation of permeability and distribution of macromolecules in mouse tumor development and malignant transformation using PET. FASEB J 2010;24:592.9.
39. Tofts PS, Berkowitz B, Schnall MD. Quantitative analysis of dynamic Gd-DTPA enhancement in breast tumors using a permeability model. Magn Reson Med 1995; 33:564-568.
40. Henderson E, Sykes J, Drost D, Weinmann HJ, Rutt BK, Lee TY. Simultaneous MRI measurement of blood flow, blood volume, and capillary permeability in mammary tumors using two different contrast agents. J Magn Reson Imaging 2000;12:991-1003.
41. Harris NR, Whitt SP, Zilberberg J, Alexander JS, Rumbaut RE. Extravascular transport of fluorescently labeled albumins in the rat mesentery. Microcirculation 2002; 9:177-187.
42. Hu DE, Easton AS, Fraser PA. TRPV1 activation results in disruption of the blood-brain barrier in the rat. Br J Pharmacol 2005;146:576-584.
43. Kendall S, Michel CC. The measurement of permeability in single rat venules using the red cell microperfusion technique. Exp Physiol 1995;80:359-372.
44. Kim MH, Harris NR, Tarbell JM. Regulation of capillary hydraulic conductivity in response to an acute change in shear. Am J Physiol Heart Circ Physiol 2005;289: H2126-H2135.
45. Salmon AH, Neal CR, Sage LM, Glass CA, Harper SJ, Bates DO. Angiopoietin-1 alters microvascular permeability coefficients in vivo via modification of endothelial glycocalyx. Cardiovasc Res 2009;83:24-33.
46. Victorino GP, Ramirez RM, Chong TJ, Curran B, Sadjadi J. Ischemia-reperfusion injury in rats affects hydraulic conductivity in two phases that are temporally and mechanistically separate. Am J Physiol Heart Circ Physiol 2008;295:H2164-H2171.
47. Yuan SY, Wu MH, Ustinova EE, Guo M, Tinsley JH, De Lanerolle P et al. Myosin light chain phosphorylation in neutrophil-stimulated coronary microvascular leakage. Circ Res 2002;90:1214-1221.
48. MacPhee PJ, Michel CC. Fluid uptake from the renal medulla into the ascending vasa recta in anaesthetized rats. J Physiol 1995;487:169-183.
49. Shen Q, Rigor RR, Pivetti CD, Wu MH, Yuan SY. Myosin light chain kinase in micro-vascular endothelial barrier function. Cardiovasc Res 2010;87:272-280.
50. Adamson RH, Michel CC. Pathways through the intercellular clefts of frog mesen-teric capillaries. J Physiol 1993;466:303-327.
51. Hu X, Adamson RH, Liu B, Curry FE, Weinbaum S. Starling forces that oppose filtration after tissue oncotic pressure is increased. Am J Physiol Heart Circ Physiol 2000; 279:H1724-H1736.
52. Bundgaard M. The three-dimensional organization of tight junctions in a capillary endothelium revealed by serial-section electron microscopy. J Ultrastruct Res 1984; 88:1-17.
53. Michel CC, Curry FE. Microvascular permeability. Physiol Rev 1999;79:703-761.
54. Kajimura M, Michel CC. Flow modulates the transport of K+ through the walls of single perfused mesenteric venules in anaesthetised rats. J Physiol 1999;521:665-677.
55. 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.
56. Pearse RM. Water, taken in moderation, cannot hurt anybody (Mark Twain 1835-1910). J Physiol 2010;588:281-282.
57. Sun X, Shikata Y, Wang L, Ohmori K, Watanabe N, Wada J et al. Enhanced interaction between focal adhesion and adherens junction proteins: involvement in sphin-gosine 1-phosphate-induced endothelial barrier enhancement. Microvasc Res 2009; 77:304-313.
58. Lee MJ, Thangada S, Claffey KP, Ancellin N, Liu CH, Kluk M et al. Vascular endothelial cell adherens junction assembly and morphogenesis induced by sphingosine-1-phosphate. Cell 1999;99:301-312.
59. Mehta D, Konstantoulaki M, Ahmmed GU, Malik AB. Sphingosine 1-phosphate-induced mobilization of intracellular Ca2+ mediates rac activation and adherens junction assembly in endothelial cells. J Biol Chem 2005;280: 17320-17328.
60. Garcia JG, Liu F, Verin AD, Birukova A, Dechert MA, Gerthoffer WT et al. Sphingo-sine 1-phosphate promotes endothelial cell barrier integrity by Edg-dependent cyto-skeletal rearrangement. J Clin Invest 2001;108:689-701.
61. Xu M, Waters CL, Hu C, Wysolmerski RB, Vincent PA, Minnear FL. Sphingosine 1-phosphate rapidly increases endothelial barrier function independently of VE-cadherin but requires cell spreading and Rho kinase. Am J Physiol 2007;293: C1309-C1318.
62. Adam AP, Sharenko AL, Pumiglia K, Vincent PA. SRC-induced tyrosine phosphoryl-ation of VE-cadherin is not sufficient to decrease barrier function of endothelial monolayers. J Biol Chem 2010;285:7045-7055.
63. Noda K, Zhang J, Fukuhara S, Kunimoto S, Yoshimura M, Mochizuki N. Vascular endothelial-cadherin stabilizes at cell-cell junctions by anchoring to circumferential actin bundles through alpha-and beta-Catenins in cyclic AMP-Epac-Rap1 signal-activated endothelial cells. Mol Biol Cell 2010;21:584-596.
64. Adamson RH, Ly JC, Sarai RK, Lenz JF, Altangerel A, Drenckhahn D et al. Epac/Rap1 pathway regulates microvascular hyperpermeability induced by PAF in rat mesentery. Am J Physiol Heart Circ Physiol 2008;294:H1188-H1196.
65. 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 2005;289:H840-H844.
66. Birukova AA, Smurova K, Birukov KG, Kaibuchi K, Garcia JG, Verin AD. Role of Rho GTPases in thrombin-induced lung vascular endothelial cells barrier dysfunction. Microvasc Res 2004;67:64-77.
67. Vandenbroucke E, Mehta D, Minshall R, Malik AB. Regulation of endothelial junc-tional permeability. Ann N Y Acad Sci 2008;1123:134-145.
68. Liebner S, Kniesel U, Kalbacher H, Wolburg H. Correlation of tight junction morphology with the expression of tight junction proteins in blood-brain barrier Endothelial cells. Eur J Cell Biol 2000;79:707-717.
69. Dai G, Kaazempur-Mofrad MR, Natarajan S, Zhang Y, Vaughn S, Blackman BR et al. Distinct endothelial phenotypes evoked by arterial waveforms derived from atherosclerosis-susceptible and-resistant regions of human vasculature. Proc Natl Acad Sci USA 2004;101:14871-14876.
70. Davies PF. Hemodynamic shear stress and the endothelium in cardiovascular patho-physiology. Nat Clin Pract Cardiovasc Med 2009;6:16-26.
71. Baluk P, Hirata A, Thurston G, Fujiwara T, Neal CR, Michel CC et al. Endothelial gaps: time course of formation and closure in inflamed venules of rats. Am J Physiol 1997;272:L155-L170.
72. McDonald DM, Thurston G, Baluk P. Endothelial gaps as sites for plasma leakage in inflammation. Microcirculation 1999;6:7-22.
73. Michel CC, Neal CR. Openings through endothelial cells associated with increased microvascular permeability. Microcirculation 1999;6:45-54.
74. Majno G, Palade GE. Studies on inflammation. 1. The effect of histamine and serotonin on vascular permeability: an electron microscopic study. J Biophys Biochem Cytol 1961;11:571-605.
75. Adamson RH, Zeng M, Adamson GN, Lenz JF, Curry FE. PAF-and bradykinin-induced hyperpermeability of rat venules is independent of actin-myosin contraction. Am J Physiol Heart Circ Physiol 2003;285:H406-H417.
76. Beckers CM, van Hinsbergh VW, van Nieuw Amerongen GP. Driving Rho GTPase activity in endothelial cells regulates barrier integrity. Thromb Haemost 2010;103: 40-55.
77. Waschke J, Drenckhahn D, Adamson RH, Curry FE. Role of adhesion and contraction in Rac 1-regulated endothelial barrier function in vivo and in vitro. Am J Physiol Heart Circ Physiol 2004;287:H704-H711.
78. Adamson RH, Curry FE, Adamson G, Liu B, Jiang Y, Aktories K et al. Rho and rho kinase modulation of barrier properties: cultured endothelial cells and intact micro-vessels of rats and mice. J Physiol 2002;539:295-308.
79. Curry FE, Zeng M, Adamson RH. Thrombin increases permeability only in venules exposed to inflammatory conditions. Am J Physiol Heart Circ Physiol 2003;285: H2446-H2453.
80. Waypa GB, Vincent PA, Morton CA, Minnear FL. Thrombin increases fluid flux in isolated rat lungs by a hemodynamic and not a permeability mechanism. J Appl Physiol 1996;80:1197-1204.
81. Curry FE. Microvascular injury: mechanisms and modulation. Int J Angiol 2002;11: 1-6.
82. Ly JC, Lenz JF, Adamson RH, Curry FE. Six hour exposure to inflammatory conditions induces responsiveness to thrombin in single perfused rat venules. FASEB J 2005;19:A1262.
83. Waschke J, Baumgartner W, Adamson RH, Zeng M, Aktories K, Barth H et al. Requirement of Rac activity for maintenance of capillary endothelial barrier properties. Am J Physiol Heart Circ Physiol 2004;286:H394-H401.
84. Surapisitchat J, Jeon KI, Yan C, Beavo JA. Differential regulation of endothelial cell permeability by cGMP via phosphodiesterases 2 and 3. Circ Res 2007;101:811-818.
85. Lee JF, Gordon S, Estrada R, Wang L, Siow DL, Wattenberg BW et al. Balance of S1P1 and S1P2 signaling regulates peripheral microvascular permeability in rat cre-master muscle vasculature. Am J Physiol Heart Circ Physiol 2009;296:H33-H42.
86. Gregg D, Rauscher FM, Goldschmidt-Clermont PJ. Rac regulates cardiovascular superoxide through diverse molecular interactions: more than a binary GTP switch. Am J Physiol Cell Physiol 2003;285:C723-C734.
87. Monaghan-Benson E, Burridge K. The regulation of vascular endothelial growth factor-induced microvascular permeability requires Rac and reactive oxygen species. J Biol Chem 2009;284:25602-25611.
88. Wang J, Bingaman S, Huxley VH. Intrinsic sex-specific differences in microvascular endothelial cell phosphodiesterases. Am J Physiol Heart Circ Physiol 2010;298: H1146-H1154.
89. Michel CC. Starling: the formulation of his hypothesis of microvascular fluid exchange and its significance after 100 years. Exp Physiol 1997;82:1-30.
90. Wu Q, Andreopoulos Y, Weinbaum S. From red cells to snowboarding: a new concept for a train track. Phys Rev Lett 2004;93:194501.
91. Pries AR, Secomb TW, Gaehtgens P. The endothelial surface layer. Pflugers Arch 2000;440:653-666.
92. Mulivor AW, Lipowsky HH. Inhibition of glycan shedding and leukocyte-endothelial adhesion in postcapillary venules by suppression of matrixmetalloprotease activity with doxycycline. Microcirculation 2009;16:657-666.
93. Mulivor AW, Lipowsky HH. Inflammation-and ischemia-induced shedding of venular glycocalyx. Am J Physiol Heart Circ Physiol 2004;286:H1672-H1680.
94. Tarbell J. Shear stress and the endothelial transport barrier. Cardiovasc Res 2010;87: 320-330.
95. Chappell D, Jacob M, Paul O, Rehm M, Welsch U, Stoeckelhuber M et al. The gly-cocalyx of the human umbilical vein endothelial cell: an impressive structure ex vivo but not in culture. Circ Res 2009;104:1313-1317.
96. Squire JM, Chew M, Nneji G, Neal C, Barry J, Michel C. Quasi-periodic substructure in the microvessel endothelial glycocalyx: a possible explanation for molecular filtering? J Struct Biol 2001;136:239-255.
97. 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 1994;116:502-513.
98. Hu X, Weinbaum S. A new view of Starling's hypothesis at the microstructural level. Microvasc Res 1999;58:281-304.
99. Secomb TW. Theoretical models for regulation of blood flow. Microcirculation 2008; 15:765-775.
100. Pries AR, Kuebler WM. Normal endothelium. Handb Exp Pharmacol 2006;176:1-40.
101. Noble MI, Drake-Holland AJ, Vink H. Hypothesis: arterial glycocalyx dysfunction is the first step in the atherothrombotic process. QJM 2008;101:513-518.
102. Satchell SC, Tooke JE. What is the mechanism of microalbuminuria in diabetes: a role for the glomerular endothelium? Diabetologia 2008;51:714-725.
103. Trung DT, Wills B. Systemic vascular leakage associated with dengue infections\the clinical perspective. Curr Top Microbiol Immunol 2010;338:57-66.
104. Michel CC, Curry FR. Glycocalyx volume: a critical review of tracer dilution methods for its measurement. Microcirculation 2009;16:213-219.
105. Curry FR, Rygh CB, Karlsen T, Wiig H, Adamson RH, Clark JF et al. Atrial natriuretic peptide modulation of albumin clearance and contrast agent permeability in mouse skeletal muscle and skin: role in regulation of plasma volume. J Physiol 2010;588: 325-339.