Abstract
Axons navigate step-wise, from one intermediate target to the next, until they reach their final destination target. In the central nervous system, intermediate targets are often glial cells, and final targeting is also aided by glia. In the peripheral nervous system, however, glial cells most often follow axons, which therefore navigate following other, nonglial clues. Even in the central nervous system, interactions between axons and glia are dynamic and reciprocal, as the neurons regulate migration, survival and proliferation of the glia cells they need for guidance. We review here the experimental evidence investigating roles of glia in axon guidance. Some molecules are known to influence either the neurons or the glia, but the molecular mechanisms underlying axon-glia interactions during pathfinding are only beginning to emerge.
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References
Bate CM. Pioneer neurones in an insect embryo. Nature 1976; 260:54–55.
Singer M, Nordlander RH, Egar M. Axonal guidance during embryogenesis and regeneration in the spinal cord of the newt: The blueprint hypothesis of neuronal patterning. J Comp Neurol 1979; 185:1–22.
Silver J, Lorenz SE, Wahlstein D et al. Axonal guidance during development of the great cerebral commissures: Descriptive and experimental studies in vivo on the role of the preformed glial pathways. J Comp Neurology 1982; 210:10–29.
Bastiani MJ, Goodman CS. Guidance of neuronal growth cones in the grasshopper embryo. III. Recognition of specific glial pathways. J Neurosci 1986; 6:3542–3551.
Hidalgo A, Booth GE. Glia dictate pioneer axon trajectories in the Drosophila embryonic CNS. Development 2000; 127:393–402.
Sepp KJ, Schulte J, Auld VJ. Peripheral glia direct axon guidance across the CNS/PNS transition zone. Developmental Biology 2001; 238:47–63.
Freeman M, Doherty J. Glial cell biology in Drosophila and vertebrates. Trends in Neurosciences 2006; 29:82–90.
Chotard C, Salecker I. Neurons and glia: Team players in axon guidance. Trends in Neurosciences 2004; 27:655–661.
Araujo SJ, Tear G. Axon guidance mechanisms and molecules: Lessons from invetebrates. Nature Reviews Neuroscience 2003; 4:916–922.
Long H et al. Conserved roles for Slit and Robo proteins in midline commissural axons. Neuron 2004; 42:213–223.
Jen J, al e. Mutations in a human Robo gene disrupt hindbrain axon pathway crossing and morphogenesis. Science 2004; 304:1509–1513.
Sabatier C et al. The divergent Robo family protein Rig-1/Robo3 is a negative regulator of Slit responsiveness required for midline crossing by commissural axons. Cell 2004; 117:157–169.
Kaprielian Z, Runko E, Imondi R. Axon guidance at the midline choice point. Developmental dynamics 2001; 221:154–181.
Lemke G. Glial control of neuronal development. Annu Rev Neurosci 2001; 24:87–105.
Zou Y, Stoeckli E, Chen H et al. Squeezing axons out of the gray matter: A role for Slit and Semaphorin proteins from midline and ventral spinal cord. Cell 2000; 102:363–375.
Charron F, Stein E, Jeong J et al. The morphogen Sonic Hedgehog is an axonal chemoattractant that collborates with Netrin-1 in midline axon guiidance. Cell 2003; 113:11–23.
Garrat AN, Britsch S, Birchmeier C. Neuregulin, a factor with many functions in the life of a Schwann cell. BioFssays 2000; 22:987–996.
Fernandez PA et al. Evidence that axon-derived Neuregulin promotes oligodendrocyte survival in the developing rat optic nerve. Neuron 2000; 28:81–90.
Lyons DA et al. Erbb3 and erbb2 are essential for Schwann cell migration and myelination in zebrafish. Current Biology 2005; 15:513–524.
Griffiths RL, Hidalgo A. Prospero maintains the mitotic potential of glial precursors enabling them to respond to neurons. EMBO J 2004; 23:2440–2450.
Hidalgo A, Kinrade EFV, Georgiou M. The Drosophila Neuregulin Vein maintains glial survival during axon guidance in the CNS. Developmental Cell 2001.
Sepp KJ, Auld VJ. Reciprocal interactions between neurons and glia are required for Drosophila peripheral nervous system development. The Journal of Neuroscience 2003; 23:8221–8230.
Bergmann A, Tugentman M, Shilo BZ et al. Regulation of cell number by MAPK-dependent control of apoptosis: A mechanism for trophic survival signaling. Dev Cell 2002; 2:159–170.
Hoch RV, Soriano P. Role of PDGF in animal development. Development 2003; 130:4769–4784.
Miller RH. Regulation of oligodendrocyte development in the vertebrate CNS. Progress in Neurobiology 2002; 67:451–467.
Bovoloenta P. Morphogen signalling at the vertebrate growth cone: A few cases or a general strategy? J Neurobiol 2005; 64:405–416.
Condron B. Spatially discrete FGF-mediated signalling directs glial morphogenesis. Development 1999; 126:4635–4641.
Shishido E, Ono N, Kojima T et al. Requirements of DFR1/Heartless, a mesoderm specific Drosophila FGFReceptor for the foromation of heart, visceral and somatic muscles, and ensheathing of longitudinal axon tracts in the CNS. Development 1997; 124:2119–2128.
Klämbt C, Glazer L, Shilo BZ. Breathless, a Drosophila FGF receptor homolog, is essenlian for migration of tracheal and specific midline glial cells. Genes Dev 1992; 6:1668–1678.
Hummel T, Leifker K, Klämbt C. The Drosophila HEM-2/NAP1 homolog KETTE contorls axonal pathfinding and cytoskeletal organization. Genes Dev 2000; 14:863–873.
Poeck B, Fischer S, Gunning D et al. Glial cells mediate target layer selection of retinal axons in the developing visual system of Drosophila. Neuron 2001; 29:99–113.
Mast JD, Prakash S, Chen PL et al. The mechanisms and molecules that connect photoreceptor axons to their targets in Drosophila. Seminars in Cell and Developmental Biology 2005.
Gibson N, Tolbert L. Activation of epidermal growth factor receptor mediates receptor axon sroting and extension in the developing olfactory system of the moth Manduca sexta. J Comparative Neurology 2006; 495:554–572.
Hummel T, Krukkert K, Roos J et al. Drosophila Futsch/22c10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 2000; 26:357–370.
Sepp KJ, Schulte J, Auld V. Developmental dynamics of peripheral glia in Drosophila melanogaster. Glia 2000; 30:122–133.
Vincent A, West A, Chuah M. Morphological and functional plasticity of olfactory ensheathing cells. Journal of Neurocytology 2005; 34:65–80.
Aigouy B, Van de Bor V, Boeglin M et al. Time-lapse and cell ablation reveal the role of cell interactions in fly glial migration and proliferation. Development 2004; 131:5127–5138.
Giangrande A. Glia in the fly wing are clonally related to epithelial cells and use the nerve as a pathway for migration. Development 1994; 120:523–534.
Gilmour D, al e. Migration and function of a glial subtype in the vertebrate peripheral nervous system. Neuron 2002; 34:577–588.
Gilmour D, NKnaut H, Maischein HM et al. Towing of sensory axons by their migrating target cells in vivo. Nature Neuroscience 2004; 7:491–492.
Barresi M, Hutson L, Chien CB et al. Hedgehog regulated Slit expression determines commissure and glial cell position in the zebrafish forebrain. Development 2005; 132:3643–3656.
McDermott K, Barry D, McMahon S. Role of radial glia in cytogenesis, patterning and boundary formation in the developing spinal cord. J Anat 2005; 207:241–250.
Hidalgo A, Urban J, Brand AH. Targeted ablation of glia disrupts axon tract formation in the Drosophila CNS. Development 1995; 121:3703–3712.
Rajagopalan S, Vivancos V, Nicolas E et al. Selecting a longitudinal pathway: Robo receptors specify the lateral position of axons in the Drosophila CNS. Cell 2000; 103:1033–1045.
Simpson JH, Bland KS, Fetter RD et al. Short-range and long-range guidance by Slit and its Robo receptors: A combinatorial code of Robo receptors control lateral position. 2000; 103.
Kinrade E, Hidalgo A. Lateral neuron-glia interactions steer the response of axons to the Robo code. Neuron Glia Biology 2004; 1:101–112.
Rangarajan R, Gong R, Gaul U. Migration and function of glia in the developing Drosophila eye. Development 1999; 126:3285–3292.
Klämbt C, Jacobs JR, Goodman CS. The midline of the Drosophila central nervous system: A model for the genetic analysis of cell fate, cell migration and growth cone guidance. Cell 1991; 64:801–815.
Sonnenfeld MJ, Jacobs JR. Apoptosis of the midline glia during Drosophila embryogenesis: A correlation with axon contact. Development 1995; 121:569–578.
Kinrade EFV, Brates T, Tear G et al. Roundabout signalling, cell contact and trophic support confine longitudinal glia and axons in the drosophila CNS. Development 2001; 128:207–216.
Huang Z, Kunes S. Hedgehog, transmitted along retinal axons, triggers neurogenesis in the developing visual centers of the Drosophila brain. Cell 1996; 86:411–422.
Dearborn R, JKunes J. An axon scaffold induced by retinal axons directs glia to destinations in the Drosophila optic lobe. Development 2004; 131:2291–2303.
Arendt D, Nübler-Jung K. Comparison of early nerve cord development in insects and vertebrates. Development 1999; 126:2309–2325.
Barres BA, Raff MC. Control of oligodendrocyte number in the developing rat optic nerve. Neuron 1994; 12:935–942.
Raff M et al. Programmed cell death and the control of cell survival: Lessons from the nervous system. Science 1993; 262:695–700.
Ramon-Cueto A, Cordero M, Santos-Benito F et al. Functional recovery of paraplegic rats and motor axon regeneration in their spinal cords by olfactory ensheathing glia. Neuron 2000; 25:425–435.
Li Y, Carlstedt T, Berthold CH et al. Interaction of transplanted olfactory-ensheathing cells and host astrocytic processes provides a bridge for axons to regenrate acress the dorsal root entry zone. Experimental Neurology 2004; 188:300–308.
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Learte, A.R., Hidalgo, A. (2007). The Role of Glial Cells in Axon Guidance, Fasciculation and Targeting. In: Bagnard, D. (eds) Axon Growth and Guidance. Advances in Experimental Medicine and Biology, vol 621. Springer, New York, NY. https://doi.org/10.1007/978-0-387-76715-4_12
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DOI: https://doi.org/10.1007/978-0-387-76715-4_12
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