Modulation of epithelial and endothelial paracellular permeability by leukocytes

Advanced Drug Delivery Reviews

Volumn 41, Issue 3, 2000, Pages 315-328

  Edens, Heather A ^a   Parkos, Charles A ^a  

^a EMORY UNIVERSITY   (United States)

Author keywords

Endothelium; Epithelium; Leukocytes; Paracellular permeability; Tight junctions

Indexed keywords

CELLS; MECHANICAL PERMEABILITY; TISSUE;

LEUKOCYTES; TIGHT JUNCTIONS;

CONTROLLED DRUG DELIVERY;

ACTIN; CALCIUM ION; CYCLIC AMP; CYTOKINE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; INOSITOL TRISPHOSPHATE; INTEGRIN; INTERCELLULAR ADHESION MOLECULE 1; RHO FACTOR;

ASTROCYTE; BLOOD BRAIN BARRIER; CELL MEMBRANE PERMEABILITY; DIFFUSION; ENDOTHELIUM; EPITHELIUM; IMMUNOFLUORESCENCE; LEUKOCYTE; LEUKOCYTE MIGRATION; MODULATION; NONHUMAN; PRIORITY JOURNAL; REVIEW;

EID: 0034733993     PISSN: 0169409X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-409X(00)00049-1     Document Type: Article

References (93)

1. Fanning A.S., Mitic L.L., Anderson J.M. Transmembrane proteins in the tight junction barrier. J. Am. Soc. Nephrol. 10:1999;1337-1345.
2. Madara J.L. Regulation of the movement of solutes across tight junctions. Annu. Rev. Physiol. 60:1998;143-159.
3. Stevenson B.R., Keon B.H. The tight junction: morphology to molecules. Annu. Rev. Cell Dev. Biol. 14:1998;89-109.
4. Denker B.M., Nigam S.K. Molecular structure and assembly of the tight junction. Am. J. Physiol. 274:1998;F1-F9.
5. Dejana E., Zanetti A., Del Maschio A. Adhesive proteins at endothelial cell-to-cell junctions and leukocyte extravasation. Haemostasis. 26:(Suppl. 4):1996;210-219.
6. Simionescu M., Simionescu N. Endothelial transport of macromolecules: transcytosis and endocytosis. A look from cell biology. Cell Biol. Rev. 25:1991;5-78.
7. Powell D.W. Barrier function of epithelia. Am. J. Physiol. 241:1981;G275-G288.
8. Rubin L.L., Staddon J.M. The cell biology of the blood-brain barrier. Annu. Rev. Neurosci. 22:1999;11-28.
9. Madara J.L., Dharmsathaphorn K. Occluding junction structure-function relationships in a cultured epithelial monolayer. J. Cell Biol. 101:1985;2124-2133.
10. Balda M.S., Whitney J.A., Flores C., Gonzalez S., Cereijido M., Matter K. Functional dissociation of paracellular permeability and transepithelial electrical resistance and disruption of the apical-basolateral intramembrane diffusion barrier by expression of a mutant tight junction membrane protein. J. Cell Biol. 134:1996;1031-1049.
11. Rajasekaran A.K., Hojo M., Huima T., Rodriguez-Boulan E. Catenins and zonula occludens-1 form a complex during early stages in the assembly of tight junctions. J. Cell Biol. 132:1996;451-463.
12. Madara J.L. Intestinal absorptive cell tight junctions are linked to cytoskeleton. Am. J. Physiol. 253:1987;C171-C175.
13. Hordijk P.L., Anthony E., Mul F.P.J., Rientsma R., Oomen L.C.J.M. Vascular-endothelial-cadherin modulates endothelial monolayer permeability. J. Cell Sci. 112:1999;1915-1923.
14. Alexander J.S., Blaschuk O.W., Haselton F.R. An N-cadherin-like protein contributes to solute barrier maintenance in cultured endothelium. J. Cell Physiol. 156:1993;610-618.
15. Gotsch U., Borges E., Bosse R., Böggemeyer E., Simon M., Mossmann H., Vestweber D. VE-cadherin antibody accelerates neutrophil recruitment in vivo. J. Cell Sci. 110:1997;583-588.
16. Alexander J.S., Dayton T., Davis C., Hill S., Jackson T.H., Blaschuk O., Symonds M., Okayama N., Kevil C.G., Laroux F.S., Berney S.M., Kimpel D. Activated T-lymphocytes express occludin, a component of tight junctions. Inflammation. 22:1998;573-582.
17. Martin-Padura I., Lostaglio S., Schneemann M., Williams L., Romano M., Fruscella P., Panzeri C., Stoppacciaro A., Ruco L., Villa A., Simmons D., Dejana E. Junctional adhesion molecule, a novel member of the immunoglobulin superfamily that distributes at intercellular junctions and modulates monocyte transmigration. J. Cell Biol. 142:1998;117-127.
18. Parkos C.A. Cell adhesion and migration. I. Neutrophil adhesive interactions with intestinal epithelium. Am. J. Physiol. 273:1997;G763-G768.
19. Granger D.N. Cell adhesion and migration. II. Leukocyte-endothelial cell adhesion in the digestive system. Am. J. Physiol. 273:1997;G982-G986.
20. Springer T.A. Traffic signals on endothelium for lymphocyte recirculation and leukocyte emigration. Annu. Rev. Physiol. 57:1995;827-872.
21. Smith C.W. Leukocyte-endothelial cell interactions. Semin. Hematol. 30:1993;45-53.
22. Tan P., Luscinskas F.W., Homer-Vanniasinkam S. Cellular and molecular mechanisms of inflammation and thrombosis. Eur. J. Vasc. Endovasc. Surg. 17:1999;373-389.
23. Marcus B.C., Hynes K.L., Gewertz B.L. Loss of endothelial barrier function requires neutrophil adhesion. Surgery. 122:1997;420-426.
24. Gautam N., Hedqvist P., Lindbom L. Kinetics of leukocyte-induced changes in endothelial barrier function. Br. J. Pharmacol. 125:1998;1109-1114.
25. Huang A.J., Manning J.E., Bandak T.M., Ratau M.C., Hanser K.R., Silverstein S.C. Endothelial cell cytosolic free calcium regulates neutrophil migration across monolayers of endothelial cells. J. Cell Biol. 120:1993;1371-1380.
26. Staehelin L.A. Further observations on the fine structure of freeze-cleaved tight junctions. J. Cell Sci. 13:1973;763-786.
27. Tsukita S., Furuse M. Occludin and claudins in tight-junction strands: leading or supporting players? Trends Cell Biol. 9:1999;268-273.
28. Wolburg H., Neuhaus J., Kniesel U., Krauss B., Schmid E.M., Ocalan M., Farrell C., Risau W. Modulation of tight junction structure in blood-brain barrier endothelial cells. Effects of tissue culture, second messengers and cocultured astrocytes. J. Cell Sci. 107:1994;1347-1357.
29. Takeichi M. Cadherin cell adhesion receptors as a morphogenetic regulator. Science. 251:1991;1451-1455.
30. Lampugnani M.G., Resnati M., Raiteri M., Pigott R., Pisacane A., Houen G., Ruco L.P., Dejana E. A novel endothelial-specific membrane protein is a marker of cell-cell contacts. J. Cell Biol. 118:1992;1511-1522.
31. Wong R.K., Baldwin A.L., Heimark R.L. Cadherin-5 redistribution at sites of TNF-α and IFN-γ-induced permeability in mesenteric venules. Am. J. Physiol. 276:1999;H736-H748.
32. Wójciak-Stothard B., Entwistle A., Garg R., Ridley A.J. Regulation of TNF-α-induced reorganization of the actin cytoskeleton and cell-cell junctions by rho, rac, and cdc42 in human endothelial cells. J. Cell. Physiol. 176:1998;150-165.
33. Stewart P.A., Wiley M.J. Developing nervous tissue induces formation of blood-brain barrier characteristics in invading endothelial cells: a study using quail-chick transplantation chimeras. Dev. Biol. 84:1981;183-192.
34. Janzer R.C., Raff M.C. Astrocytes induce blood-brain barrier properties in endothelial cells. Nature. 325:1987;253-257.
35. Stanness K.A., Westrum L.E., Fornaciari E., Mascagni P., Nelson J.A., Stenglein S.G., Myers T., Janigro D. Morphological and functional characterization of an in vitro blood-brain barrier model. Brain Res. 771:1997;329-342.
36. Yamagata K., Tagami M., Nara Y., Mitani M., Kubota A., Fujino H., Numano F., Kato T., Yamori Y. Astrocyte-conditioned medium induces blood-brain barrier properties in endothelial cells. Clin. Exp. Pharmacol. Physiol. 24:1997;710-713.
37. Kuchler-Bopp S., Delaunoy J.P., Artault J.C., Zaepfel M., Dietrich J.B. Astrocytes induce several blood-brain barrier properties in non-neural endothelial cells. Neuroreport. 10:1999;1347-1353.
38. Rubin L.L., Hall D.E., Porter S., Barbu K., Cannon C., Horner H.C., Janatpour M., Liaw C.W., Manning K., Morales J. A cell culture model of the blood-brain barrier. J. Cell Biol. 115:1991;1725-1735.
39. Rist R.J., Romero I.A., Chan M.W., Couraud P.O., Roux F., Abbott N.J. F-actin cytoskeleton and sucrose permeability of immortalised rat brain microvascular endothelial cell monolayers: effects of cyclic AMP and astrocytic factors. Brain Res. 768:1997;10-18.
40. Igarashi Y., Utsumi H., Chiba H., Yamada-Sasamori Y., Tobioka H., Kamimura Y., Furuuchi K., Kokai Y., Nakagawa T., Mori M., Sawada N. Glial cell line-derived neurotrophic factor induces barrier function of endothelial cells forming the blood-brain barrier. Biochem. Biophys. Res. Commun. 261:1999;108-112.
41. Leybaert L., Paemeleire K., Strahonja A., Sanderson M.J. Inositol-triphosphate-dependent intercellular calcium signaling in and between astrocytes and endothelial cells. Glia. 24:1998;298-407.
42. Tontsch U., Bauer H.C. Glial cells and neurons induce blood-brain barrier related enzymes in cultured cerebral endothelial cells. Brain Res. 539:1991;247-253.
43. Anthony D.C., Bolton S.J., Fearn S., Perry V.H. Age-related effects of interleukin-1β on polymorphonuclear neutrophil-dependent increases in blood-brain barrier permeability in rats. Brain. 120:1997;435-444.
44. Bolton S.J., Anthony D.C., Perry V.H. Loss of the tight junction proteins occludin and zonula occludens-1 from cerebral vascular endothelium during neutrophil-induced blood-brain barrier breakdown in vivo. Neuroscience. 86:1998;1245-1257.
45. Matter K., Balda M.S. Occludin and the functions of tight junctions. Int. Rev. Cytol. 186:1999;117-146.
46. Issekutz A.C., Rowter D., Springer T.A. Role of ICAM-1 and ICAM-2 and alternate CD11/CD18 ligands in neutrophil transendothelial migration. J. Leukocyte Biol. 65:1999;117-126.
47. Chow J., Hartley R.B., Jagger C., Dilly S.A. ICAM-1 expression in renal disease. J. Clin. Pathol. 45:1992;880-884.
48. Adamson P.A., Etienne S., Couraud P.-O., Calder V., Greenwood J. Lymphocyte migration through brain endothelial cell monolayers involves signaling through endothelial ICAM-1 via a Rho-dependent pathway. J. Immunol. 162:1999;2964-2973.
49. Durieu-Trautmann O., Chaverot N., Cazaubon S., Strosberg A.D., Couraud P.O. Intercellular adhesion molecule 1 activation induces tyrosine phosphorylation of the cytoskeleton-associated protein cortactin in brain microvessel endothelial cells. J. Biol. Chem. 269:1994;12536-12540.
50. Beagley K.W., Husband A.J. Intraepithelial lymphocytes: origins, distribution, and function. Crit. Rev. Immunol. 18:1998;237-254.
51. Etienne-Manneville S., Chaverot N., Strosberg A.D., Couraud P.-O. ICAM-1-coupled sinaling pathways in astrocytes converge to cyclic AMP response element-binding protein phosphorylation and TNF-α secretion. J. Immunol. 163:1999;668-674.
52. Huang A.J., Furie M.B., Nicholson S.C., Fischbarg J., Liebovitch L.S., Silverstein S.C. Effects of human neutrophil chemotaxis across human endothelial cell monolayers on the permeability of these monolayers to ions and macromolecules. J. Cell Physiol. 135:1988;355-366.
53. Wedmore C.V., Williams T.J. Control of vascular permeability by polymorphonuclear leukocytes in inflammation. Nature. 289:1981;646-650.
54. Nusrat A., Parkos C.A., Liang T.W., Carnes D.K., Madara J.L. Neutrophil migration across model intestinal epithelia: monolayer disruption and subsequent events in epithelial repair. Gastroenterology. 113:1997;1489-1500.
55. Pfau S., Leitenberg D., Rinder H., Smith B.R., Pardi R., Bender J.R. Lymphocyte adhesion-dependent calcium signaling in human endothelial cells. J. Cell Biol. 128:1995;969-978.
56. Del Maschio A., Zanetti A., Corada M., Rival Y., Ruco L., Lampugnani M.G., Dejana E. Polymorphonuclear leukocyte adhesion triggers the disorganization of endothelial cell-to-cell adherens junctions. J. Cell Biol. 135:1996;497-510.
57. Allport J.R., Ding H., Collins T., Gerritsen M.E., Luscinskas F.W. Endothelial-dependent mechanisms regulate leukocyte transmigration: a process involving the proteasome and disruption of the vascular endothelial-cadherin complex at endothelial cell-to-cell junctions. J. Exp. Med. 186:1997;517-527.
58. Moll T., Dejana E., Vestweber D. In vitro degradation of endothelial catenins by a neutrophil protease. J. Cell Biol. 140:1998;403-407.
59. Cassatella M.A. The production of cytokines by polymorphonuclear neutrophils. Immunol. Today. 16:1995;21-25.
60. Duchini A., Govindarajan S., Santucci M., Zampi G., Hofman F.M. Effects of tumor necrosis factor-alpha and interleukin-6 on fluid-phase permeability and ammonia diffusion in CNS-derived endothelial cells. J. Invest. Med. 44:1999;474-482.
61. Yi E.S., Ulich T.R. Endotoxin, interleukin-1, and tumor necrosis factor cause neutrophil-dependent microvascular leakage in postcapillary venules. Am. J. Pathol. 140:1992;659-663.
62. Persidsky Y., Stins M., Way D., Witte M.H., Weinand M., Kim K.S., Bock P., Gendelman H.E., Fiala M. A model for monocyte migration through the blood-brain barrier during HIV-1 encephalitis. J. Immunol. 158:1997;3499-3510.
63. Sandig M., Negrou E., Rogers K.A. Changes in the distribution of LFA-1, catenins, and F-actin during transendothelial migration of monocytes in culture. J. Cell Sci. 110:1997;2807-2818.
64. Ozaki H., Ishii K., Horiuchi H., Arai H., Kawamoto T., Okawa K., Iwamatsu A., Kita T. Cutting edge: combined treatment of TNF-alpha and IFN-gamma causes redistribution of junctional adhesion molecule in human endothelial cells. J. Immunol. 163:1999;553-557.
65. Cepek K.L., Rimm D.L., Brenner M.B. Expression of a candidate cadherin in T lymphocytes. Proc. Natl. Acad. Sci. USA. 93:1996;6567-6571.
66. Parsons P.E., Sugahara K., Cott G.R., Mason R.J., Henson P.M. The effect of neutrophil migration of prolonged neutrophil contact on epithelial permeability. Am. J. Pathol. 129:1987;302-312.
67. Nash S., Stafford J., Madara J.L. Effects of polymorphonuclear leukocyte transmigration on the barrier function of cultured intestinal epithelial monolayers. J. Clin. Invest. 80:1987;1104-1113.
68. Parkos C.A., Colgan S.P., Madara J.L. Interactions of neutrophils with epithelial cells: lessons from the intestine. J. Am. Soc. Nephrol. 2:1994;138-152.
69. Parkos C.A., Delp C., Arnaout M.A., Madara J.L. Neutrophil migration across a cultured intestinal epithelium: dependence on a CD11b/CD18-mediated event and enhanced efficiency in the physiologic direction. J. Clin. Invest. 88:1991;1605-1612.
70. Shaw S.K., Hermanowski-Vosatka A., Shibahara T., McCormick B.A., Parkos C.A., Carlson S.L., Ebert E.C., Brenner M.B., Madara J.L. Migration of intestinal intraepithelial lymphocytes into a polarized epithelial monolayer. Am. J. Physiol. 275:1998;G584-G591.
71. Higgins J.M., Mandlebrot D.A., Shaw S.K., Russell G.J., Murphy E.A., Chen Y.T., Nelson W.J., Parker C.M., Brenner M.B. Direct and regulated interaction of integrin alphaEbeta7 with E-cadherin. J. Cell Biol. 140:1998;197-210.
72. Cepek K.L., Shaw S.K., Parker C.M., Russell G.J., Morrow J.S., Rimm D.L., Brenner M.B. Adhesion between epithelial cells and T lymphocytes mediated by E-cadherin and the αEβ7 integrin. Nature. 372:1994;190-193.
73. Kaoutzani P., Colgan S.P., Cepek K.L., Burkard P.G., Carlson S., Delp-Archer C., Brenner M.B., Madara J.L. Reconstitution of cultured intestinal epithelial monolayers with a mucosal-derived T lymphocyte cell line. Modulation of epithelial phenotype dependent on lymphocyte-basolateral membrane apposition. J. Clin. Invest. 94:1994;788-796.
74. Madara J.L., Stafford J. Interferon-gamma directly affects barrier function of cultured intestinal epithelial monolayers. J. Clin. Invest. 83:1989;724-727.
75. Planchon S., Fiocchi C., Takafuji V., Roche J.K. Transforming growth factor-beta1 preserves epithelial barrier function: identification of receptors, biochemical intermediates, and cytokine antagonists. J. Cell Physiol. 181:1999;55-66.
76. Colgan S.P., Parkos C.A., Delp C., Arnaout M.A., Madara J.L. Neutrophil migration across cultured intestinal epithelial monolayers is modulated by epithelial exposure to IFN-g in a highly polarized fashion. J. Cell Biol. 120:1993;785-798.
77. Colgan S.P., Resnick M.B., Parkos C.A., Delp-Archer C., McGuirk D., Bacarra A.E., Weller P.F., Madara J.L. IL-4 directly modulates function of a model human intestinal epithelium. J. Immunol. 153:1994;2122-2129.
78. Schmitz H., Barmeyer C., Fromm M., Runkel N., Foss H.D., Bentzel C.J., Riecken E.O., Schulzke J.D. Altered tight junction structure contributes to the impaired epithelial barrier function in ulcerative colitis. Gastroenterology. 116:1999;301-309.
79. Winter M., Wilson J.S., Bedell K., Shasby D.M. The conductance of cultured epithelial cell monolayers: oxidants, adenosine triphosphate, and phorbol dibutyrate. Am. J. Respir. Cell Mol. Biol. 2:1990;355-363.
80. Nash S., Stafford J., Madara J.L. The selective and superoxide-independent disruption of intestinal epithelial tight junctions during leukocyte transmigration. Lab. Invest. 59:1988;531-537.
81. Bogomolski-Yaholom V., Matzner Y. Disorders of neutrophil function. Blood Rev. 9:1995;183-190.
82. Siflinger-Birnboim A., Goligorsky M.S., Del vecchio P.J., Malik A.B. Activation of protein kinase c pathway contributes to hydrogen peroxide-induced increase in endothelial permeability. Lab. Invest. 67:1992;24-30.
83. Nygaard S.D., Ganz T., Peterson M.W. Defensins reduce the barrier integrity of a cultured epithelial monolayer without cytotoxicity. Am. J. Respir. Cell Mol. Biol. 8:1993;193-200.
84. Colgan S.P., Dzus A.L., Parkos C.A. Epithelial exposure to hypoxis modulates neutrophil transepithelial migration. J. Exp. Med. 184:1996;1003-1015.
85. McCormick B.A., Parkos C.A., Colgan S.P., Carnes D.K., Madara J.L. Apical secretion of a pathogen-elicited epithelial chemoattractant activity in response to surface colonization of intestinal epithelia by Salmonella typhimurium. J. Immunol. 160:1998;455-466.
86. Migliorisi G., Folkes E., Cramer E.B. Differences in the ability of neutrophils and monocytes to traverse epithelial occluding junctions. J. Leukocyte Biol. 44:1988;485-492.
87. Hofman P., d'Andrea L., Carnes D., Colgan S.P., Madara J.L. Intestinal epithelial cytoskeleton selectively constrains lumen-to-tissue migration of neutrophils. Am. J. Physiol. 271:1996;C312-C320.
88. Parkos C.A., Colgan S.P., Diamond M.S., Nusrat A., Liang T.W., Springer T.A., Madara J.L. Expression and polarization of intercellular adhesion molecule-1 on human intestinal epithelia: consequences for CD11b/CD18-mediated interactions with neutrophils. Mol. Med. 2:1996;489-505.
89. Almenar-Queralt A., Duperray A., Miles L.A., Felez J., Altieri D.C. Apical topography and modulation of ICAM-1 expression on activated endothelium. Am. J. Pathol. 147:1995;1278-1288.
90. Lhotta K., Neumayer H.P., Joannidis M., Geissler D., Konig P. Renal expression of intercellular adhesion molecule-1 in different forms of glomerulonephritis. Clin. Sci. (Colch.). 81:1991;477-481.
91. Cooper D., Lindberg F.P., Gamble J.R., Brown E.J., Vadas M.A. Transendothelial migration of neutrophils involves integrin-associated protein (CD47). Proc. Natl. Acad. Sci. USA. 92:1995;3978-3982.
92. Parkos C.A., Colgan S.P., Liang T.W., Nusrat A., Bacarra A.E., Carnes D.K., Madara J.L. CD47 mediates post-adhesive events required for neutrophil migration across polarized intestinal epithelia. J. Cell Biol. 132:1996;437-450.
93. Mazzone A., Ricevuti G. Leukocyte CD11/CD18 integrins: biological and clinical relevance. Haematologica. 80:1995;161-175.