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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

Comparison of Drosophila and mammalian blood-brain barriers. (A) Schematic view of a cross-section of a Drosophila ventral nerve cord. The nervous system is covered by a sheath of extracellular matrix, called neural lamella (NL). The outermost glial layer consists of perineurial glial cells (PG). The subperineurial glia (SPG) forms pleated septate junctions (SJ) and blocks paracellular transport. Neurons (N) project into the neuropil (NP). Neuronal cell bodies and neuroblasts (NB) are surrounded by cortex glia (CG). The neuropil is covered by ensheathing glia (EG). Astrocytes (AG) invade the neuropil. In the peripheral nerves, wrapping glia (WG) ensheath axons. (B) In Drosophila, the blood-brain barrier is built by perineurial and subperineurial glia. The latter form septate junctions (SJ) to prevent paracellular diffusion. The different glial cells are connected via gap junctions (GJ). (C) The mammalian blood-brain barrier is built by endothelial cells (EC) that form tight junctions (TJ) to prevent paracellular diffusion. The endothelium is in close contact with pericytes (PC). Both are surrounded by the basal membrane (BM). Gap junctions (GJ) can be found between the endothelial cells and between the astrocytes (AG). Gap junction hemichannels (HJ) can be found in all the cell types.
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Figure 1: Comparison of Drosophila and mammalian blood-brain barriers. (A) Schematic view of a cross-section of a Drosophila ventral nerve cord. The nervous system is covered by a sheath of extracellular matrix, called neural lamella (NL). The outermost glial layer consists of perineurial glial cells (PG). The subperineurial glia (SPG) forms pleated septate junctions (SJ) and blocks paracellular transport. Neurons (N) project into the neuropil (NP). Neuronal cell bodies and neuroblasts (NB) are surrounded by cortex glia (CG). The neuropil is covered by ensheathing glia (EG). Astrocytes (AG) invade the neuropil. In the peripheral nerves, wrapping glia (WG) ensheath axons. (B) In Drosophila, the blood-brain barrier is built by perineurial and subperineurial glia. The latter form septate junctions (SJ) to prevent paracellular diffusion. The different glial cells are connected via gap junctions (GJ). (C) The mammalian blood-brain barrier is built by endothelial cells (EC) that form tight junctions (TJ) to prevent paracellular diffusion. The endothelium is in close contact with pericytes (PC). Both are surrounded by the basal membrane (BM). Gap junctions (GJ) can be found between the endothelial cells and between the astrocytes (AG). Gap junction hemichannels (HJ) can be found in all the cell types.

Mentions: In all animals, an efficient separation of metabolic and ionic balance between nervous system and circulation is necessary. This in consequence led to the evolution of the so-called blood-brain barrier (Abbott et al., 2006). Vertebrates are characterized by a highly vascularized nervous system, while the insect nervous system floats in the hemolymph, which circulates through the body by the action of a primitive heart (Figures 1A–C). In the mammalian nervous system, the blood-brain barrier is established by an interplay of polarized endothelial cells and pericytes that leads to the formation of endothelial tight junctions (Armulik et al., 2010, 2011; Daneman et al., 2010b). These tight junctions prevent uncontrolled paracellular leakage of solutes into the brain. In more primitive vertebrates such as in elasmobranch fish (sharks, skates, and rays), but also in some bony fish (sturgeon), the blood-brain barrier is formed by perivascular astrocytes. These glial cells form interdigitating lamellae but do not establish tight junctions (Bundgaard and Abbott, 2008). A morphologically similar blood-brain barrier is found in insects. Here, only the outer surface of the nervous system, which is formed exclusively by glial cells, contacts the hemolymph. Although this glial barrier appears to be related to the evolutionary ancestral form of the blood-brain barrier, Drosophila has only recently emerged as a genetic model to study blood-brain barrier biology (Carlson et al., 2000; Abbott et al., 2006). Here, we summarize what is currently known on the organization and the physiological properties of the Drosophila blood-brain barrier.


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)

Comparison of Drosophila and mammalian blood-brain barriers. (A) Schematic view of a cross-section of a Drosophila ventral nerve cord. The nervous system is covered by a sheath of extracellular matrix, called neural lamella (NL). The outermost glial layer consists of perineurial glial cells (PG). The subperineurial glia (SPG) forms pleated septate junctions (SJ) and blocks paracellular transport. Neurons (N) project into the neuropil (NP). Neuronal cell bodies and neuroblasts (NB) are surrounded by cortex glia (CG). The neuropil is covered by ensheathing glia (EG). Astrocytes (AG) invade the neuropil. In the peripheral nerves, wrapping glia (WG) ensheath axons. (B) In Drosophila, the blood-brain barrier is built by perineurial and subperineurial glia. The latter form septate junctions (SJ) to prevent paracellular diffusion. The different glial cells are connected via gap junctions (GJ). (C) The mammalian blood-brain barrier is built by endothelial cells (EC) that form tight junctions (TJ) to prevent paracellular diffusion. The endothelium is in close contact with pericytes (PC). Both are surrounded by the basal membrane (BM). Gap junctions (GJ) can be found between the endothelial cells and between the astrocytes (AG). Gap junction hemichannels (HJ) can be found in all the cell types.
© Copyright Policy - open-access
Related In: Results  -  Collection

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

Figure 1: Comparison of Drosophila and mammalian blood-brain barriers. (A) Schematic view of a cross-section of a Drosophila ventral nerve cord. The nervous system is covered by a sheath of extracellular matrix, called neural lamella (NL). The outermost glial layer consists of perineurial glial cells (PG). The subperineurial glia (SPG) forms pleated septate junctions (SJ) and blocks paracellular transport. Neurons (N) project into the neuropil (NP). Neuronal cell bodies and neuroblasts (NB) are surrounded by cortex glia (CG). The neuropil is covered by ensheathing glia (EG). Astrocytes (AG) invade the neuropil. In the peripheral nerves, wrapping glia (WG) ensheath axons. (B) In Drosophila, the blood-brain barrier is built by perineurial and subperineurial glia. The latter form septate junctions (SJ) to prevent paracellular diffusion. The different glial cells are connected via gap junctions (GJ). (C) The mammalian blood-brain barrier is built by endothelial cells (EC) that form tight junctions (TJ) to prevent paracellular diffusion. The endothelium is in close contact with pericytes (PC). Both are surrounded by the basal membrane (BM). Gap junctions (GJ) can be found between the endothelial cells and between the astrocytes (AG). Gap junction hemichannels (HJ) can be found in all the cell types.
Mentions: In all animals, an efficient separation of metabolic and ionic balance between nervous system and circulation is necessary. This in consequence led to the evolution of the so-called blood-brain barrier (Abbott et al., 2006). Vertebrates are characterized by a highly vascularized nervous system, while the insect nervous system floats in the hemolymph, which circulates through the body by the action of a primitive heart (Figures 1A–C). In the mammalian nervous system, the blood-brain barrier is established by an interplay of polarized endothelial cells and pericytes that leads to the formation of endothelial tight junctions (Armulik et al., 2010, 2011; Daneman et al., 2010b). These tight junctions prevent uncontrolled paracellular leakage of solutes into the brain. In more primitive vertebrates such as in elasmobranch fish (sharks, skates, and rays), but also in some bony fish (sturgeon), the blood-brain barrier is formed by perivascular astrocytes. These glial cells form interdigitating lamellae but do not establish tight junctions (Bundgaard and Abbott, 2008). A morphologically similar blood-brain barrier is found in insects. Here, only the outer surface of the nervous system, which is formed exclusively by glial cells, contacts the hemolymph. Although this glial barrier appears to be related to the evolutionary ancestral form of the blood-brain barrier, Drosophila has only recently emerged as a genetic model to study blood-brain barrier biology (Carlson et al., 2000; Abbott et al., 2006). Here, we summarize what is currently known on the organization and the physiological properties of the Drosophila blood-brain barrier.

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