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The Drosophila blood-brain barrier: development and function of a glial endothelium.

Limmer S, Weiler A, Volkenhoff A, Babatz F, Klämbt C - Front Neurosci (2014)

Bottom Line: Perineurial glial cells participate in nutrient uptake and establish a first diffusion barrier.The subperineurial glial (SPG) cells form septate junctions, which block paracellular diffusion and thus seal the nervous system from the hemolymph.We summarize the molecular basis of septate junction formation and address the different transport systems expressed by the blood-brain barrier forming glial cells.

View Article: PubMed Central - PubMed

Affiliation: Institut für Neuro- und Verhaltensbiologie, Universität Münster Münster, Germany.

ABSTRACT
The efficacy of neuronal function requires a well-balanced extracellular ion homeostasis and a steady supply with nutrients and metabolites. Therefore, all organisms equipped with a complex nervous system developed a so-called blood-brain barrier, protecting it from an uncontrolled entry of solutes, metabolites or pathogens. In higher vertebrates, this diffusion barrier is established by polarized endothelial cells that form extensive tight junctions, whereas in lower vertebrates and invertebrates the blood-brain barrier is exclusively formed by glial cells. Here, we review the development and function of the glial blood-brain barrier of Drosophila melanogaster. In the Drosophila nervous system, at least seven morphologically distinct glial cell classes can be distinguished. Two of these glial classes form the blood-brain barrier. Perineurial glial cells participate in nutrient uptake and establish a first diffusion barrier. The subperineurial glial (SPG) cells form septate junctions, which block paracellular diffusion and thus seal the nervous system from the hemolymph. We summarize the molecular basis of septate junction formation and address the different transport systems expressed by the blood-brain barrier forming glial cells.

No MeSH data available.


Related in: MedlinePlus

Organization of tricellular junctions. (A) Schematic view of septate junctions at tricellular contacts according to the tricellular plug model (Graf et al., 1982; Noirot-Timothée et al., 1982; Schulte et al., 2003). Septate junctions (red sinuous lines) span the membranes of two adjacent cells. At a central core (blue cylinder), emanating from transmembrane proteins (red balls), the septate junctions extend. (B) Transmission electron microscopic image of pleated septate junctions between two SPG cells.
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Figure 2: Organization of tricellular junctions. (A) Schematic view of septate junctions at tricellular contacts according to the tricellular plug model (Graf et al., 1982; Noirot-Timothée et al., 1982; Schulte et al., 2003). Septate junctions (red sinuous lines) span the membranes of two adjacent cells. At a central core (blue cylinder), emanating from transmembrane proteins (red balls), the septate junctions extend. (B) Transmission electron microscopic image of pleated septate junctions between two SPG cells.

Mentions: The most characteristic feature of the SPG is the formation of extensive septate junctions. This type of cell-cell junction has been particularly well studied in ectodermal cells, such as tracheal cells (Tepass and Hartenstein, 1994). Septate junctions are a complex crystalline array of comb-like structures built by a bewildering number of different proteins that connect individual cells, as revealed by freeze-fracture studies (Figure 2) (Lane and Swales, 1979; Lane, 1991). The cell-cell distance in these junctions is about 20 nm and thus a bit larger than in tight junctions that seal the brain endothelial cells in mammals (Farquhar and Palade, 1963, 1965). Many membrane-associated proteins are known to be involved in septate junction formation (Table 1). The core group of septate junction proteins contains the cation pump ATPalpha, the claudin family members Megatrachea and Sinous, the Ig-domain protein Neuroglian, the potassium pump subunit Nervana2, the Caspr homolog NeurexinIV and the two cytoplasmic proteins Coracle and Varicose (Oshima and Fehon, 2011, see also references in Table 1). These proteins recruit a large number of additional membrane proteins that together build the septate junctions (Table 1). Loss of most of these proteins results in the disruption of septate junctions.


The Drosophila blood-brain barrier: development and function of a glial endothelium.

Limmer S, Weiler A, Volkenhoff A, Babatz F, Klämbt C - Front Neurosci (2014)

Organization of tricellular junctions. (A) Schematic view of septate junctions at tricellular contacts according to the tricellular plug model (Graf et al., 1982; Noirot-Timothée et al., 1982; Schulte et al., 2003). Septate junctions (red sinuous lines) span the membranes of two adjacent cells. At a central core (blue cylinder), emanating from transmembrane proteins (red balls), the septate junctions extend. (B) Transmission electron microscopic image of pleated septate junctions between two SPG cells.
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4231875&req=5

Figure 2: Organization of tricellular junctions. (A) Schematic view of septate junctions at tricellular contacts according to the tricellular plug model (Graf et al., 1982; Noirot-Timothée et al., 1982; Schulte et al., 2003). Septate junctions (red sinuous lines) span the membranes of two adjacent cells. At a central core (blue cylinder), emanating from transmembrane proteins (red balls), the septate junctions extend. (B) Transmission electron microscopic image of pleated septate junctions between two SPG cells.
Mentions: The most characteristic feature of the SPG is the formation of extensive septate junctions. This type of cell-cell junction has been particularly well studied in ectodermal cells, such as tracheal cells (Tepass and Hartenstein, 1994). Septate junctions are a complex crystalline array of comb-like structures built by a bewildering number of different proteins that connect individual cells, as revealed by freeze-fracture studies (Figure 2) (Lane and Swales, 1979; Lane, 1991). The cell-cell distance in these junctions is about 20 nm and thus a bit larger than in tight junctions that seal the brain endothelial cells in mammals (Farquhar and Palade, 1963, 1965). Many membrane-associated proteins are known to be involved in septate junction formation (Table 1). The core group of septate junction proteins contains the cation pump ATPalpha, the claudin family members Megatrachea and Sinous, the Ig-domain protein Neuroglian, the potassium pump subunit Nervana2, the Caspr homolog NeurexinIV and the two cytoplasmic proteins Coracle and Varicose (Oshima and Fehon, 2011, see also references in Table 1). These proteins recruit a large number of additional membrane proteins that together build the septate junctions (Table 1). Loss of most of these proteins results in the disruption of septate junctions.

Bottom Line: Perineurial glial cells participate in nutrient uptake and establish a first diffusion barrier.The subperineurial glial (SPG) cells form septate junctions, which block paracellular diffusion and thus seal the nervous system from the hemolymph.We summarize the molecular basis of septate junction formation and address the different transport systems expressed by the blood-brain barrier forming glial cells.

View Article: PubMed Central - PubMed

Affiliation: Institut für Neuro- und Verhaltensbiologie, Universität Münster Münster, Germany.

ABSTRACT
The efficacy of neuronal function requires a well-balanced extracellular ion homeostasis and a steady supply with nutrients and metabolites. Therefore, all organisms equipped with a complex nervous system developed a so-called blood-brain barrier, protecting it from an uncontrolled entry of solutes, metabolites or pathogens. In higher vertebrates, this diffusion barrier is established by polarized endothelial cells that form extensive tight junctions, whereas in lower vertebrates and invertebrates the blood-brain barrier is exclusively formed by glial cells. Here, we review the development and function of the glial blood-brain barrier of Drosophila melanogaster. In the Drosophila nervous system, at least seven morphologically distinct glial cell classes can be distinguished. Two of these glial classes form the blood-brain barrier. Perineurial glial cells participate in nutrient uptake and establish a first diffusion barrier. The subperineurial glial (SPG) cells form septate junctions, which block paracellular diffusion and thus seal the nervous system from the hemolymph. We summarize the molecular basis of septate junction formation and address the different transport systems expressed by the blood-brain barrier forming glial cells.

No MeSH data available.


Related in: MedlinePlus