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The Journal of Neuroscience, January 16, 2008, 28(3):587-597; doi:10.1523/JNEUROSCI.4367-07.2008

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Development/Plasticity/Repair
Organization and Function of the Blood–Brain Barrier in Drosophila

Tobias Stork,¹ Daniel Engelen,¹ Alice Krudewig,¹ Marion Silies,¹ Roland J. Bainton,² and Christian Klämbt¹

¹Institut für Neurobiologie, Universität Münster, D-48149 Münster Germany, and ²Department of Anesthesia and Perioperative Care, University of California, San Francisco, California 94158-2517

Correspondence should be addressed to Christian Klämbt, Institut für Neurobiologie, Universität Münster, Badestrasse 9, D-48149 Münster, Germany. Email: klaembt{at}uni-muenster.de

The function of a complex nervous system depends on an intricate interplay between neuronal and glial cell types. One of the many functions of glial cells is to provide an efficient insulation of the nervous system and thereby allowing a fine tuned homeostasis of ions and other small molecules. Here, we present a detailed cellular analysis of the glial cell complement constituting the blood–brain barrier in Drosophila. Using electron microscopic analysis and single cell-labeling experiments, we characterize different glial cell layers at the surface of the nervous system, the perineurial glial layer, the subperineurial glial layer, the wrapping glial cell layer, and a thick layer of extracellular matrix, the neural lamella. To test the functional roles of these sheaths we performed a series of dye penetration experiments in the nervous systems of wild-type and mutant embryos. Comparing the kinetics of uptake of different sized fluorescently labeled dyes in different mutants allowed to conclude that most of the barrier function is mediated by the septate junctions formed by the subperineurial cells, whereas the perineurial glial cell layer and the neural lamella contribute to barrier selectivity against much larger particles (i.e., the size of proteins). We further compare the requirements of different septate junction components for the integrity of the blood–brain barrier and provide evidence that two of the six Claudin-like proteins found in Drosophila are needed for normal blood–brain barrier function.

Key words: Drosophila; blood–brain barrier; glial cells; septate junction; development; perineurial glia; subperineurial glia

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Received June 11, 2007; revised Nov. 13, 2007; accepted Dec. 4, 2007.

Correspondence should be addressed to Christian Klämbt, Institut für Neurobiologie, Universität Münster, Badestrasse 9, D-48149 Münster, Germany. Email: klaembt{at}uni-muenster.de

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