The Diaphragms of Fenestrated Endothelia: Gatekeepers of Vascular Permeability and Blood Composition

Developmental Cell

Volumn 23, Issue 6, 2012, Pages 1203-1218

  Stan, Radu V ^a   Tse, Dan ^a   Deharvengt, Sophie J ^a   Smits, Nicole C ^a   Xu, Yan ^a   Luciano, Marcus R ^a   McGarry, Caitlin L ^a   Buitendijk, Maarten ^a   Nemani, Krishnamurthy V ^a   Elgueta, Raul ^a   Kobayashi, Takashi ^a   Shipman, Samantha L ^a   Moodie, Karen L ^a   Daghlian, Charles P ^a   Ernst, Patricia A ^a   Lee, Hong Kee ^a   Suriawinata, Arief A ^a   Schned, Alan R ^a   Longnecker, Daniel S ^a   Fiering, Steven N ^a   Noelle, Randolph J ^a   Gimi, Barjor ^a   Shworak, Nicholas W ^a   Carrière, Catherine ^a   more..

^a DARTMOUTH MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PLASMA PROTEIN; PROTEIN; PROTEIN PV1; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BLOOD VESSEL PERMEABILITY; CONTROLLED STUDY; DIAPHRAGM; ENDOTHELIUM CELL; GENE DELETION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOSING GASTROENTEROPATHY; SURVIVAL;

ANIMALS; BLOOD PROTEINS; CAPILLARIES; CAPILLARY PERMEABILITY; CARRIER PROTEINS; CAVEOLAE; CELL MEMBRANE; ENDOTHELIUM, VASCULAR; MEMBRANE PROTEINS; MICE; MICE, TRANSGENIC; PROTEIN-LOSING ENTEROPATHIES;

ANIMALIA; MUS;

EID: 84870798143     PISSN: 15345807     EISSN: 18781551     Source Type: Journal    
DOI: 10.1016/j.devcel.2012.11.003     Document Type: Article

References (52)

1. Aird W.C. Phenotypic heterogeneity of the endothelium: I. Structure, function, and mechanisms. Circ. Res. 2007, 100:158-173.
2. Bankston P.W., Pino R.M. The development of the sinusoids of fetal rat liver: morphology of endothelial cells, Kupffer cells, and the transmural migration of blood cells into the sinusoids. Am. J. Anat. 1980, 159:1-15.
3. Bates D.O. Vascular endothelial growth factors and vascular permeability. Cardiovasc. Res. 2010, 87:262-271.
4. Bearer E.L., Orci L. Endothelial fenestral diaphragms: a quick-freeze, deep-etch study. J. Cell Biol. 1985, 100:418-428.
5. Carson-Walter E.B., Hampton J., Shue E., Geynisman D.M., Pillai P.K., Sathanoori R., Madden S.L., Hamilton R.L., Walter K.A. Plasmalemmal vesicle associated protein-1 is a novel marker implicated in brain tumor angiogenesis. Clin. Cancer Res. 2005, 11:7643-7650.
6. Chen J., Stahl A., Krah N.M., Seaward M.R., Joyal J.S., Juan A.M., Hatton C.J., Aderman C.M., Dennison R.J., Willett K.L., et al. Retinal expression of Wnt-pathway mediated genes in low-density lipoprotein receptor-related protein 5 (Lrp5) knockout mice. PLoS ONE 2012, 7:e30203.
7. Chen M.J., Yokomizo T., Zeigler B.M., Dzierzak E., Speck N.A. Runx1 is required for the endothelial to haematopoietic cell transition but not thereafter. Nature 2009, 457:887-891.
8. Clementi F., Palade G.E. Intestinal capillaries. I. Permeability to peroxidase and ferritin. J. Cell Biol. 1969, 41:33-58.
9. Clementi F., Palade G.E. Intestinal capillaries. II. Structural effects of EDTA and histamine. J. Cell Biol. 1969, 42:706-714.
10. Deharvengt S.J., Tse D., Sideleva O., McGarry C., Gunn J.R., Longnecker D.S., Carriere C., Stan R.V. PV1 down-regulation via shRNA inhibits the growth of pancreatic adenocarcinoma xenografts. J. Cell. Mol. Med. 2012, 16:2690-2700.
11. Dvorak H.F. Vascular permeability to plasma, plasma proteins, and cells: an update. Curr. Opin. Hematol. 2010, 17:225-229.
12. Hallmann R., Mayer D.N., Berg E.L., Broermann R., Butcher E.C. Novel mouse endothelial cell surface marker is suppressed during differentiation of the blood brain barrier. Dev. Dyn. 1995, 202:325-332.
13. Herrnberger L., Ebner K., Junglas B., Tamm E.R. The role of plasmalemma vesicle-associated protein (PLVAP) in endothelial cells of Schlemm's canal and ocular capillaries. Exp. Eye Res. 2012, 105C:27-33.
14. Herrnberger L., Seitz R., Kuespert S., Bösl M.R., Fuchshofer R., Tamm E.R. Lack of endothelial diaphragms in fenestrae and caveolae of mutant Plvap-deficient mice. Histochem. Cell Biol. 2012, 138:709-724.
15. Hisatsune H., Matsumura K., Ogawa M., Uemura A., Kondo N., Yamashita J.K., Katsuta H., Nishikawa S., Chiba T., Nishikawa S. High level of endothelial cell-specific gene expression by a combination of the 5' flanking region and the 5' half of the first intron of the VE-cadherin gene. Blood 2005, 105:4657-4663.
16. Hnasko R., Ben-Jonathan N. Developmental regulation of PV-1 in rat lung: association with the nuclear envelope and limited colocalization with Cav-1. Am. J. Physiol. Lung Cell. Mol. Physiol. 2005, 288:L275-L284.
17. Hnasko R., McFarland M., Ben-Jonathan N. Distribution and characterization of plasmalemma vesicle protein-1 in rat endocrine glands. J. Endocrinol. 2002, 175:649-661.
18. Hnasko R., Carter J.M., Medina F., Frank P.G., Lisanti M.P. PV-1 labels trans-cellular openings in mouse endothelial cells and is negatively regulated by VEGF. Cell Cycle 2006, 5:2021-2028.
19. Hnasko R., Frank P.G., Ben-Jonathan N., Lisanti M.P. PV-1 is negatively regulated by VEGF in the lung of caveolin-1, but not caveolin-2, null mice. Cell Cycle 2006, 5:2012-2020.
20. Ichimura K., Stan R.V., Kurihara H., Sakai T. Glomerular endothelial cells form diaphragms during development and pathologic conditions. J. Am. Soc. Nephrol. 2008, 19:1463-1471.
21. Ioannidou S., Deinhardt K., Miotla J., Bradley J., Cheung E., Samuelsson S., Ng Y.S., Shima D.T. An in vitro assay reveals a role for the diaphragm protein PV-1 in endothelial fenestra morphogenesis. Proc. Natl. Acad. Sci. USA 2006, 103:16770-16775.
22. Keuschnigg J., Henttinen T., Auvinen K., Karikoski M., Salmi M., Jalkanen S. The prototype endothelial marker PAL-E is a leukocyte trafficking molecule. Blood 2009, 114:478-484.
23. King J., Hamil T., Creighton J., Wu S., Bhat P., McDonald F., Stevens T. Structural and functional characteristics of lung macro- and microvascular endothelial cell phenotypes. Microvasc. Res. 2004, 67:139-151.
24. Komarova Y., Malik A.B. Regulation of endothelial permeability via paracellular and transcellular transport pathways. Annu. Rev. Physiol. 2010, 72:463-493.
25. Levick J.R., Smaje L.H. An analysis of the permeability of a fenestra. Microvasc. Res. 1987, 33:233-256.
26. Levick J.R., Michel C.C. Microvascular fluid exchange and the revised Starling principle. Cardiovasc. Res. 2010, 87:198-210.
27. Madden S.L., Cook B.P., Nacht M., Weber W.D., Callahan M.R., Jiang Y., Dufault M.R., Zhang X., Zhang W., Walter-Yohrling J., et al. Vascular gene expression in nonneoplastic and malignant brain. Am. J. Pathol. 2004, 165:601-608.
28. Milici A.J., L'Hernault N., Palade G.E. Surface densities of diaphragmed fenestrae and transendothelial channels in different murine capillary beds. Circ. Res. 1985, 56:709-717.
29. Mozer A.B., Whittemore S.R., Benton R.L. Spinal microvascular expression of PV-1 is associated with inflammation, perivascular astrocyte loss, and diminished EC glucose transport potential in acute SCI. Curr. Neurovasc. Res. 2010, 7:238-250.
30. Niemelä H., Elima K., Henttinen T., Irjala H., Salmi M., Jalkanen S. Molecular identification of PAL-E, a widely used endothelial-cell marker. Blood 2005, 106:3405-3409.
31. Paes K.T., Wang E., Henze K., Vogel P., Read R., Suwanichkul A., Kirkpatrick L.L., Potter D., Newhouse M.M., Rice D.S. Frizzled 4 is required for retinal angiogenesis and maintenance of the blood-retina barrier. Invest. Ophthalmol. Vis. Sci. 2011, 52:6452-6461.
32. Predescu S.A., Predescu D.N., Malik A.B. Molecular determinants of endothelial transcytosis and their role in endothelial permeability. Am. J. Physiol. Lung Cell. Mol. Physiol. 2007, 293:L823-L842.
33. Reeves W.H., Kanwar Y.S., Farquhar M.G. Assembly of the glomerular filtration surface. Differentiation of anionic sites in glomerular capillaries of newborn rat kidney. J. Cell Biol. 1980, 85:735-753.
34. Rippe B., Rosengren B.I., Carlsson O., Venturoli D. Transendothelial transport: the vesicle controversy. J. Vasc. Res. 2002, 39:375-390.
35. Rostgaard J., Qvortrup K. Electron microscopic demonstrations of filamentous molecular sieve plugs in capillary fenestrae. Microvasc. Res. 1997, 53:1-13.
36. Salomon D., Ayalon O., Patel-King R., Hynes R.O., Geiger B. Extrajunctional distribution of N-cadherin in cultured human endothelial cells. J. Cell Sci. 1992, 102:7-17.
37. Sarin H. Physiologic upper limits of pore size of different blood capillary types and another perspective on the dual pore theory of microvascular permeability. J. Angiogenes Res. 2010, 2:14.
38. Schäfer N.F., Luhmann U.F., Feil S., Berger W. Differential gene expression in Ndph-knockout mice in retinal development. Invest. Ophthalmol. Vis. Sci. 2009, 50:906-916.
39. Shearer G.C., Kaysen G.A. Endothelial bound lipoprotein lipase (LpL) depletion in hypoalbuminemia results from decreased endothelial binding, not decreased secretion. Kidney Int. 2006, 70:647-653.
40. Simionescu M., Simionescu N., Silbert J.E., Palade G.E. Differentiated microdomains on the luminal surface of the capillary endothelium. II. Partial characterization of their anionic sites. J. Cell Biol. 1981, 90:614-621.
41. Stadtfeld M., Graf T. Assessing the role of hematopoietic plasticity for endothelial and hepatocyte development by non-invasive lineage tracing. Development 2005, 132:203-213.
42. Stan R.V. Multiple PV1 dimers reside in the same stomatal or fenestral diaphragm. Am. J. Physiol. Heart Circ. Physiol. 2004, 286:H1347-H1353.
43. Stan R.V., Roberts W.G., Predescu D., Ihida K., Saucan L., Ghitescu L., Palade G.E. Immunoisolation and partial characterization of endothelial plasmalemmal vesicles (caveolae). Mol. Biol. Cell 1997, 8:595-605.
44. Stan R.V., Ghitescu L., Jacobson B.S., Palade G.E. Isolation, cloning, and localization of rat PV-1, a novel endothelial caveolar protein. J. Cell Biol. 1999, 145:1189-1198.
45. Stan R.V., Kubitza M., Palade G.E. PV-1 is a component of the fenestral and stomatal diaphragms in fenestrated endothelia. Proc. Natl. Acad. Sci. USA 1999, 96:13203-13207.
46. Stan R.V., Arden K.C., Palade G.E. cDNA and protein sequence, genomic organization, and analysis of cis regulatory elements of mouse and human PLVAP genes. Genomics 2001, 72:304-313.
47. Stan R.V., Tkachenko E., Niesman I.R. PV1 is a key structural component for the formation of the stomatal and fenestral diaphragms. Mol. Biol. Cell 2004, 15:3615-3630.
48. Tkachenko E., Tse D., Sideleva O., Deharvengt S.J., Luciano M.R., Xu Y., McGarry C.L., Chidlow J., Pilch P.F., Sessa W.C., et al. Caveolae, fenestrae and transendothelial channels retain PV1 on the surface of endothelial cells. PLoS ONE 2012, 7:e32655.
49. Tse D., Stan R.V. Morphological heterogeneity of endothelium. Semin. Thromb. Hemost. 2010, 36:236-245.
50. Villaschi S., Johns L., Cirigliano M., Pietra G.G. Binding and uptake of native and glycosylated albumin-gold complexes in perfused rat lungs. Microvasc. Res. 1986, 32:190-199.
51. Wisse E. An electron microscopic study of the fenestrated endothelial lining of rat liver sinusoids. J. Ultrastruct. Res. 1970, 31:125-150.
52. Yoshino G., Hirano T., Nagata K., Maeda E., Naka Y., Murata Y., Kazumi T., Kasuga M. Hypertriglyceridemia in nephrotic rats is due to a clearance defect of plasma triglyceride: overproduction of triglyceride-rich lipoprotein is not an obligatory factor. J. Lipid Res. 1993, 34:875-884.