Angiopoietin-1 alters microvascular permeability coefficients in vivo via modification of endothelial glycocalyx

Cardiovascular Research

Volumn 83, Issue 1, 2009, Pages 24-33

  Salmon, Andrew H J ^a   Neal, Christopher R ^a   Sage, Leslie M ^a   Glass, Catherine A ^a   Harper, Steven J ^a   Bates, David O ^a  

^a UNIVERSITY OF BRISTOL   (United Kingdom)

Author keywords

Angiopoietin 1; Glomerulus; Glycocalyx; Microvessel; Permeability

Indexed keywords

ANGIOPOIETIN 1; GLYCOSAMINOGLYCAN; PRONASE;

ANIMAL TISSUE; ARTICLE; BLOOD VESSEL PERMEABILITY; CONTROLLED STUDY; FROG; GLYCOCALYX; IN VIVO STUDY; MESENTERY BLOOD VESSEL; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; RAT;

ALBUMINS; ANGIOPOIETIN-1; ANIMALS; BREFELDIN A; CELL MEMBRANE PERMEABILITY; ENDOTHELIUM, VASCULAR; GLYCOCALYX; GLYCOSAMINOGLYCANS; HUMANS; KIDNEY GLOMERULUS; MICROVESSELS; MODELS, BIOLOGICAL; PRONASE; PROTEIN SYNTHESIS INHIBITORS; RANA TEMPORARIA; RATS; RATS, WISTAR; RECOMBINANT PROTEINS; WATER;

EID: 67649345892     PISSN: 00086363     EISSN: 17553245     Source Type: Journal    
DOI: 10.1093/cvr/cvp093     Document Type: Article

References (41)

1. Brindle NP, Saharinen P, Alitalo K. Signaling and functions of angiopoietin-1 in vascular protection. Circ Res 2006;98:1014-1023.
2. Satchell S, Harper S, Mathieson P. Angiopoietin-1 is normally expressed by periendothelial cells. Thromb Haemost 2001;86:1597-1598.
3. Wong A, Haroon Z, Werner S, Dewhirst M, Greenberg C, Peters K. Tie2 expression and phosphorylation in angiogenic and quiescent adult tissues. Circ Res 1997;81:567-574.
4. Nagamine K, Furue M, Fukui A, Asashima M. Induction of cells expressing vascular endothelium markers from undifferentiated Xenopus presumptive ectoderm by co-treatment with activin and angiopoietin-2. Zool Sci 2005;22:755-761.
5. Iwama A, Hamaguchi I, Hashiyama M, Murayama Y, Yasunaga K, Suda T. Molecular cloning and characterisation of mouse Tie and Tek receptor tyrosine kinase genes and their expression in haematopoietic stem cells. Biochem Biophys Res Commun 1993;195:301.
6. Joussen A, Poulaki V, Tsujikawa A, Qin W, Qaum T, Xu Q et al. Supression of diabetic retinopathy with angiopoietin-1. Am J Pathol 2002;160:1683-1693.
7. Suri C, McClain J, Thurston G, McDonald DM, Zhou H, Oldmixon EH et al. Increased vascularization in mice overexpressing angiopoietin-1. Science 1998;282:468-471.
8. Thurston G, Wang Q, Baffert F, Rudge J, Papadopoulos N, Jean-Guillaume D et al. Angiopoietin 1 causes vessel enlargement, without angiogenic sprouting, during a critical developmental period. Development 2005;132:3317-3326.
9. Thurston G, Suri C, Smith K, McClain J, Sato T, Yancopoulos G et al. Leakage-resistant blood vessels in mice transgenically overexpressing angiopoietin-1. Science 1999;286:2511-2514.
10. Baffert F, Le T, Thurston G, McDonald DM. Angiopoietin-1 decreases plasma leakage by reducing number and size of endothelial gaps in venules. Am J Physiol Heart Circ Physiol 2006;290:H107-H118.
11. Roviezzo F, Tsigkos S, Kotanidou A, Bucci M, Brancaleone V, Cirino G et al. Angiopoietin-2 causes inflammation in vivo by promoting vascular leakage. J Pharmacol Exp Ther 2005;314:738-744.
12. Hall E, Brookes ZL. Angiopoietin-1 increases arteriolar vasoconstriction to phenylephrine during sepsis. Regul Pept 2005;131:34-37.
13. Bates DO, Lodwick D, Williams B. Vascular endothelial growth factor and microvascular permeability. Microcirculation 1999;6:83-96.
14. Gamble JR, Drew J, Trezise L, Underwood A, Parsons M, Kasminkas L et al. Angiopoietin-1 is an antipermeability and anti-inflammatory agent in vitro and targets cell junctions. Circ Res 2000;87:603-607.
15. Satchell SC, Anderson KL, Mathieson PW. Angiopoietin 1 and vascular endothelial growth factor modulate human glomerular endothelial cell barrier properties. J Am Soc Nephrol 2004;15:566-574.
16. Curry FR. Microvascular solute and water transport. Microcirculation 2005;12:17-31.
17. Michel CC, Curry FE. Microvascular permeability. Physiol Rev 1999;79:703-761.
18. Deen WM, Lazzara MJ, Myers BD. Structural determinants of glomerular permeability. Am J Physiol Renal Physiol 2001;281:F579-F596.
19. Hillman NJ, Whittles CE, Pocock TM, Williams B, Bates DO. Differential effects of vascular endothelial growth factor-C and placental growth factor-1 on the hydraulic conductivity of frog mesenteric capillaries. J Vasc Res 2001;38:176-186.
20. Salmon AH, Neal CR, Bates DO, Harper SJ. Vascular endothelial growth factor increases the ultrafiltration coefficient in isolated intact Wistar rat glomeruli. J Physiol 2006;570:141-156.
21. Adamson RH. Permeability of frog mesenteric capillaries after partial pronase digestion of the endothelial glycocalyx. J Physiol 1990;428:1-13.
22. Wann AK, Ingram KR, Coleman PJ, McHale N, Levick JR. Mechanosensitive hyaluronan secretion: stimulus-response curves and role of transcriptiondtranslation-translocation in rabbit joints. Exp Physiol 2009;94:350-361.
23. Farndale RW, Buttle DJ, Barrett AJ. Improved quantitation and discrimination of sulphated glycosaminoglycans by use of dimethylmethylene blue. Biochim Biophys Acta 1986;883:173-177.
24. Farndale RW, Sayers CA, Barrett AJ. A direct spectrophotometric microassay for sulfated glycosaminoglycans in cartilage cultures. Connect Tissue Res 1982;9:247-248.
25. Gold EW. The quantitative spectrophotometric estimation of total sulfated glycosaminoglycan levels. Formation of soluble Alcian Blue complexes. Biochim Biophys Acta 1981;673:408-415.
26. Michel CC, Mason JC, Curry FE, Tooke JE, Hunter PJ. A development of the Landis technique for measuring the filtration coefficient of individual capillaries in the frog mesentery. Q J Exp Physiol Cogn Med Sci 1974;59:283-309.
27. Michel CC. Filtration coefficients and osmotic reflexion coefficients of the walls of single frog mesenteric capillaries. J Physiol 1980;309:341-355.
28. Kendall S, Michel CC. The measurement of permeability in single rat venules using the red cell microperfusion technique. Exp Physiol 1995;80:359-372.
29. Thurston G, Rudge J, Ioffe E, Zhou H, Ross L, Croll S et al. Angiopoietin-1 protects the adult vasculature against plasma leakage. Nat Med 2000;6:460-463.
30. Benest AV, Salmon AH, Wang W, Glover CP, Uney J, Harper SJ et al. VEGF and angiopoietin-1 stimulate different angiogenic phenotypes that combine to enhance functional neovascularization in adult tissue. Microcirculation 2006;13:423-437.
31. Adamson RH, Liu B, Fry GN, Rubin LL, Curry FE. Microvascular permeability and number of tight junctions are modulated by cAMP. Am J Physiol 1998;274:H1885-H1894.
32. Wang Y, Pampou S, Fujikawa K, Varticovski L. Opposing effect of angiopoietin-1 on VEGF-mediated disruption of endothelial cell-cell interactions requires activation of PKC beta. J Cell Physiol 2004;198:53-61.
33. Levick JR. Flow through interstitium and other fibrous matrices. Q J Exp Physiol 1987;72:409-437.
34. Curry FE, Michel CC. A fiber matrix model of capillary permeability. Microvasc Res 1980;20:96-99.
35. Rostgaard J, Qvortrup K. Electron microscopic demonstrations of filamentous molecular sieve plugs in capillary fenestrae. Microvasc Res 1997;53:1-13.
36. 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.
37. Jeansson M, Haraldsson B. Morphological and functional evidence for an important role of the endothelial cell glycocalyx in the glomerular barrier. Am J Physiol Renal Physiol 2006;290:F111-F116.
38. 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.
39. Rilla K, Siiskonen H, Spicer AP, Hyttinen JM, Tammi MI, Tammi RH. Plasma membrane residence of hyaluronan synthase is coupled to its enzymatic activity. J Biol Chem 2005;280:31890-31897.
40. Fukuhara S, Sako K, Minami T, Noda K, Kim HZ, Kodama T et al. Differential function of Tie2 at cell-cell contacts and cell-substratum contacts regulated by angiopoietin-1. Nat Cell Biol 2008;10:513-526.
41. De Almeida JB, Stow JL. Disruption of microtubules alters polarity of basement membrane proteoglycan secretion in epithelial cells. Am J Physiol 1991;261:C691-C700.