Modulation of tight junction structure in blood-brain barrier endothelial cells: Effects of tissue culture, second messengers and cocultured astrocytes

Journal of Cell Science

Volumn 107, Issue 5, 1994, Pages 1347-1357

  Wolburg, Hartwig ^a   Neuhaus, Jochen ^a,d   Kniesel, Uwe ^a,c   Krauß, Bodo ^a   Schmid, Eva Maria ^a   Öcalan, Mücella ^b   Farrell, Catherine ^b,e   Risau, Werner ^b,c  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b MAX PLANCK INSTITUTE OF PSYCHIATRY   (Germany)

^c MAX PLANCK INSTITUTE FOR HEART AND LUNG RESEARCH   (Germany)

^d MAX DELBRÜCK CENTER FOR MOLECULAR MEDICINE   (Germany)

^e AMGEN INC   (United States)

Author keywords

Blood brain barrier; Camp astrocyte; Endothelium; Freeze fracture; Permeability; Tight junction

Indexed keywords

CYCLIC AMP; MEMBRANE LIPID;

ANIMAL CELL; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN CAPILLARY; CONTROLLED STUDY; ELECTRIC RESISTANCE; ELECTRON MICROSCOPY; ENDOTHELIUM; ENDOTHELIUM CELL; FIBROBLAST; FREEZE FRACTURE; LIPID BILAYER; NONHUMAN; PERMEABILITY; PRIORITY JOURNAL; SECOND MESSENGER; TIGHT JUNCTION;

ANIMALS; ASTROCYTES; BLOOD-BRAIN BARRIER; CATTLE; CULTURE TECHNIQUES; ENDOTHELIUM, VASCULAR; FREEZE FRACTURING; INTERCELLULAR JUNCTIONS; MICE; MICROSCOPY, ELECTRON; PERMEABILITY; RATS; SECOND MESSENGER SYSTEMS;

EID: 0028246186     PISSN: 00219533     EISSN: None     Source Type: Journal    
DOI: None     Document Type: Article

References (51)

1. Arthur, F. E., Shivers, R. R. and Bowman, P. D. (1987). Astrocyte-mediated induction of tight junctions in brain capillary endothelium: an efficient in vitro model. Dev. Brain Res. 36, 155-159.
2. Brightman, M. W. and Reese, T. S. (1969). Junctions between intimately apposed cell membranes in the vertebrate brain. J. Cell Biol. 40, 648-677.
3. Bundgaard, M., Cserr, H. and Murray, M. (1979). Impermeability of hagfish cerebral capillaries to horseradish peroxidase An ultrastructural study. Cell Tiss. Res. 198, 65-77.
4. Butt, A. M., Jones, H. C. and Abbott, N. J. (1990). Electrical-resistance across the blood-brain barrier in anesthetized rats - a developmental study. J. Physiol. 429, 47-62.
5. Cereijido, M., González-Mariscal, L. and Contreras, B. (1989). Tight junction: barrier between higher organisms and environment. NIPS 4, 72-75.
6. Citi, S. (1993). The molecular-organization of tight junctions. J. Cell Biol. 121, 485-489.
7. Claude, P. and Goodenough, D. A. (1973). Fracture faces of zonulae occludentes from "tight" and "leaky" epithelia. J. Cell Biol. 58, 390-400.
8. Claude, P. (1978). Morphological factors influencing transepithehal permeability: a model for the resistance of the zonula occludens. J. Membr. Biol. 32, 219-232.
9. Dermietzel, R. and Krause, D. (1991). Molecular anatomy of the blood-brain-barrier as defined by immunocytochemistry. Int. Rev. Cytol. 127, 57-109.
10. Drenckhahn, D. and Dermietzel, R. (1988). Organization of the actin filament cytoskeleton in the intestinal brush border: a quantitative and qualitative immunoelectron microscope study. J. Cell Biol. 107, 1037-1048.
11. Frey A., Meckelein, B., Weilerguttler, H., Mockel, B., Flach, R. and Gassen, H. G. (1991). Pericytes of the brain microvasculature express gamma-glutamyl transpeptidase. Eur. J. Biochem. 202, 421-429.
12. Gumbiner, B. and Simons, K. (1986). A functional assay for proteins involved in establishing an epithelial occluding barrier: identification of a uvomorulin-like polypeptide. J. Cell Biol. 102, 457-468.
13. Itoh, M., Nagafuchi, A., Yonemura, S., Kitani-Yasuda, T., Tsukita, S. and Tsukita, S. (1993). The 220-kD protein colocalizing with cadherins in nonepithelial cells is identical to ZO-1, a tight junction-associated protein in epithelial cells: cDNA cloning and immunoelectron microscopy. J. Cell Biol. 121, 491-502.
14. Janzer, R. C. and Raff, M. C. (1987). Astrocytes induce blood-brain barrier properties in endothelial cells. Nature 325, 253-257.
15. Kintner, C. (1992). Regulation of embryonic cell adhesion by the cadherin cytoplasmic domain. Cell 69, 225-236.
16. Kniesel, U. and Wolburg, H. (1993). Tight junction complexity in the retinal-pigment epithelium of the chicken during development. Neurosci. Lett. 149, 71-74.
17. Krause, D., Mischeck, U., Galla, H. J. and Dermietzel, R. (1991). Correlation of zonula-occludens ZO-1 antigen expression and transendothelial resistance in porcine and rat cultured cerebral endothelial-cells. Neurosci. Lett. 128, 301-304.
18. Lampugnani, M. G., Resnati, M., Raiteri, M., Pigott, R., Pisacane, A., Houen, G., Ruco, L. P. and Dejana, E. (1992). A novel endothelial-specific membrane-protein is a marker of cell-cell contacts. J. Cell Biol. 118, 1511-1522.
19. Madara, J. L. and Dharmsathaphorn, K. (1985). Occluding junction structure-function relationships in a cultured epithelial monlayer. J. Cell Biol. 101, 2124-2133.
20. Madara, J. L. (1987). Intestinal absorptive cell tight junctions are linked to cytoskeleton. Amer. J. Physiol. 253, C171-C175.
21. Madara, J. L. and Pappenheimer, J. R. (1987). Structural basis for physiological regulation of paracellular pathways in intestinal epithelia. J. Membr. Biol. 100, 149-164.
22. Mandel, L. J., Bacallao, R. and Zampighi, G. (1993). Uncoupling of the molecular fence and paracellular gate functions in epithelial tight junctions. Nature 361, 552-555.
23. Marcial, M. A., Carlson, S. L. and Madar, J. L. (1984). Partitioning of paracellular conductance along the ileal crypt-villus axis: a hypothesis based on structural analysis with detailed considerations of tight junction structure-function relationship. J. Membr. Biol. 80, 59-80.
24. Meyer, J., Rauh J. and Galla, H. J. (1991). The susceptibility of cerebral endothelial-cells to astroglial induction of blood-brain-barrier enzymes depends on their proliferative state. J. Neurochem. 57, 1971-1977.
25. Mühleisen, H., Wolburg, H. and Betz, E. (1989). Freeze-fracture analysis of endothelial cell membranes in rabbit carotid arteries subjected to short-term atherogenic stimuli. Virch. Arch. B Cell Pathol. 56, 413-417.
26. Nagy, Z., Peters, H. and Hüttner, I. (1984). Fracture faces of cell junctions in cerebral endothelium during normal and hyperosmotic conditions. Lab. Invest. 50, 313-322.
27. Nico, B., Cantino, D., Bertossi, M., Ribatti, D., Sassoe, M. and Roncali, L. (1992). Tight endothelial junctions in the developing microvasculature - a thin-section and freeze-fracture study in the chick-embryo optic tectum. J. Submicrosc: Cytol. P 24, 85-95.
28. Nigam, S. K., Denisenko, N., Rodriguez-Boulan, E. and Citi, S. (1991). The role of phosphorylation in development of tight junctions in cultured renal epithelial (mdck) cells. Biochem. Biophys. Res. Commun. 181, 548-553.
29. Noble, M., Fok-Seang, J. and Cohen, J. (1984). Glia are a unique substrate for the in vitro growth of central nervous system neurons. J. Neurosci. 4, 1892-1903.
30. Ozawa, M. and Kemler, R. (1992). Molecular-organization of the uvomorulin-catenin complex. J. Cell Biol. 116, 989-996.
31. Reese, T. S. and Karnovsky, M. J. (1967). Fine structural localization of a blood-brain barrier to exogenous peroxidase. J. Cell Biol. 34, 207-217.
32. Risau, W., Hallmann, R. and Albrecht, U. (1986a). Differentiation-dependent expression of protein in brain endothelium during development of the blood-brain barrier. Dev. Biol. 117, 537-545.
33. Risau, W., Hallmann, R., Albrecht, U. and Henke-Fahle, S. (1986b) Brain induces the expression of an early cell surface marker for blood-brain barrier specific endothelium. EMBO J. 5, 3179-3183.
34. Risau, W., Engelhardt, B. and Wekerle, H. (1990). Immune function of the blood-brain barrier: Incomplete presentation of protein (auto-)antigens by rat brain microvascular endothelium in vitro. J. Cell Biol. 110, 1757-1766.
35. Risau, W. and Wolburg, H. (1990). Development of the blood-brain barrier. Trends Neurosci. 13, 174-178.
36. Risau, W. (1991). Vasculogenesis, angiogenesis and endothelial cell differentiation during embryonic development. In The Development of the Vascular System (ed. R. N. Feinberg, G. K. Sherer and R. Auerbach), 14th edn, pp. 58-68. Karger, Basel.
37. Risau, W. and Wolburg, H. (1991). The importance of the blood-brain barrier in fetuses and embryos - reply. Trends Neurosci. 14, 15-15.
38. Risau, W., Dingler, A., Albrecht, U., Dehouck, M.-P. and Cecchelli, R. (1992). Blood-brain barrier pericytes are the main source of gamma-glutamyltranspeptidase activity in brain capillaries. J. Neurochem. 58, 667-672.
39. Rubin, L. L., Hall, D. E., Porter, S., Barbu, K., Cannon, C., Horner, H. C., Janatpour, M., Liaw, C. W., Manning, K., Morales, J., Tanner, L. I., Tomaselli, K. J., et al. (1991). A cell-culture model of the blood-brain barrier. J. Cell Biol. 115, 1725-1735.
40. Saunders, N. R., Dziegielewska, K. M. and Mollgard, K. (1991). The importance of the blood-brain barrier in fetuses and embryos. Trends Neurosci. 14, 14-14.
41. Schulze, C. and Firth, J. A. (1992). Interendothelial junctions during blood-brain barrier development in the rat, morphological changes at the level of individual tight junctional contacts. Dev. Brain Res. 69, 85-95.
42. Seulberger, H., Lottspeich, F. and Risau, W. (1990). The inducible blood-brain barrier specific molecule HT7 is a novel immunoglobulin-like cell surface glycoprotein. EMBO J. 9, 2151-2158.
43. Simionescu, M., Ghinea, N., Fixman, A., Lasser, M., Kukes, L., Simionescu, N. and Palade, G. E. (1988). The cerebral microvasculature of the rat: structure and luminal surface properties during early development. J. Submicrosc. Cytol. 20, 243-261.
44. Stevenson, B. R., Anderson, J. M., Godenough, D. A. and Mooseker, M. S. (1988). Tight junction structure and ZO-1 content are identical in two strains of Madin-Darby canine kidney cells which differ in transepithelial resistance. J. Cell Biol. 107, 2401-2408.
45. Stevenson, B. R., Anderson, J. M., Braun, D. and Mooseker, M. S. (1989). Phosphorylation of the tight-junction protein ZO-1 in two strains of Madin-Darby canine kidney cells which differ in transepithelial resistance. Biochem. J. 263, 597-599.
46. Stewart, P. A. and Wiley, M. J. (1981). Developing nervous tissue induces formation of blood-brain barrier characteristics in invading endothelial cells: A study using quail-chick transplantation chimeras. Dev. Biol. 84, 183-192.
47. Stewart, P. A. and Hayakawa, E. M. (1987). Interendothelial junctional changes underlie the developmental 'tightening' of the blood-brain barrier. Dev. Brain Res. 32, 271-281.
48. Tao-Cheng, J., Nagy, Z. and Brightman, M. W. (1987). Tight junctions of brain endothelium in vitro are enhanced by astroglia. J. Neurosci. 7, 3293-3299.
49. van Deurs, B. and Luft, J. H. (1979). Effects of glutaraldehyde fixation on the structure of tight junctions. A quantitative freeze-fracture analysis. J. Ultrastruct. Res. 68, 160-172.
50. Wakai, S. and Hirokawa, N. (1978). Development of the blood-brain barrier to horseradish peroxidase in the chick embryo. Cell Tiss. Res 195, 195-203.
51. Zampighi, G., Bacallao, R., Mandel, L. and Cereijido, M. (1991). Structural differences of the tight junction between low and high resistance MDCK monolayers. J. Cell Biol. 115, 479a; abstract.