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Modes and regulation of glial migration in vertebrates and invertebrates

Nature Reviews Neuroscience volume 10, pages 769–779 (2009)Cite this article

Key Points

  • Vertebrates and invertebrates have similar sets of glial cells that perform comparable functional tasks.

  • A hallmark of all glial cells is their pronounced migratory ability. Glial cells in the PNS and in the CNS can be discriminated by distinct migratory strategies.

  • In the PNS, glial cells generally move in cohorts, a migration mode that has been termed collective migration.

  • In the CNS, glial cells generally migrate as single cells.

  • Model systems such as Drosophila melanogaster provide excellent tools to study glial migration with single-cell resolution.

  • Given the evolutionary conservation of glial cells, invertebrate models are expected to advance our understanding of glial cell migration.

Abstract

Neurons and glial cells show mutual interdependence in many developmental and functional aspects of their biology. To establish their intricate relationships with neurons, glial cells must migrate over what are often long distances. In the CNS glial cells generally migrate as single cells, whereas PNS glial cells tend to migrate as cohorts of cells. How are their journeys initiated and directed, and what stops the migratory phase once glial cells are aligned with their neuronal counterparts? A deeper understanding of glial migration and the underlying neuron–glia interactions may contribute to the development of therapeutics for demyelinating diseases or glial tumours.

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Figure 1: Glial migration in vertebrates.
Figure 2: Glial migration in Drosophila melanogaster.
Figure 3: Single cell and chain migration.
Figure 4: Molecular mechanisms underlying single-cell and chain migration.

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Acknowledgements

I am grateful for many discussions with and excellent comments from B. Zalc, E. Raz, M. Silies, H. Aberle, S. Bogdan, A. Püschel, W. Paulus and T. Hummel. Work in my laboratory is supported by the Deutsche Forschungsgemeinschaft, the European Commission and the German Israeli Foundation.

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    Christian Klämbt

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Glossary

Enhancer trap

A technique in which mobile genetic elements carrying a neutral promoter and a reporter gene are randomly inserted in the genome. The expression of the reporter indicates the presence of flanking enhancer elements.

Tip cell

A cell leading a group of migratory cells. Tip cells generally have extensive filopodia that allow them to explore their environment.

Clonal analysis

A technique in which genetic mosaic animals are generated, either by the transplantation of cells of a specific genotype into a host organism or by mitotic recombination induced in a heterozygous host. Clonal analysis is used to determine the cell autonomy of a particular gene function.

Neural crest

Groups of cells that migrate from the neural tube to the periphery, where they give rise to a wide variety of cell types.

Lateral line

In fish, the lateral line contains mechanosensory organs (neuromasts) and is located along the entire length of the body axis.

Ventricular zone

An area in the vertebrate CNS, located next to the ventricles, which contains progenitor cells that give rise to neurons and glia.

Floor plate

The ventral midline structure of the CNS. It has a role in neuronal patterning and axon guidance.

Chemorepellent

A molecule that stimulates an aversive reaction by migrating cells or growth cones.

Dorsal closure

The developmental process during D. melanogaster embryogenesis by which lateral epidermal cells move over the forming gut at the dorsal side. The process resembles wound healing.

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Klämbt, C. Modes and regulation of glial migration in vertebrates and invertebrates. Nat Rev Neurosci 10, 769–779 (2009). https://doi.org/10.1038/nrn2720

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