A mechanism for the guidance and topographic patterning of retinal ganglion cell axons

Silver, Jerry; Sidman, Richard L.

doi:10.1002/cne.901890106

Cited by 317 publications

(100 citation statements)

References 26 publications

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“…In newt spinal cord (Singer et al, 1979), it has been shown in electron micrographs that rostro-caudally oriented spaces between columns of cells in the spinal cord are packed with axons as development progresses. In mouse retina, Silver and Robb (1979) have shown that intercellular channels appear to be routes for outgrowth of optic nerve fibres, and serial sections through the developing retina show that the orientation of these channels is consistent with that of the later growing axons (Silver and Sidman, 1980). Other studies in chick spinal cord have demonstrated a relationship between extracellular spaces and axonal extension, but as in the present study, have not addressed the question of whether there is a specific signaling mechanism between extracellular matrix and growth cones or axons.…”

Section: Discussionmentioning

confidence: 97%

Cellular morphology and extracellular space at rhombomere boundaries in the chick embryo hindbrain

Heyman

Kent

Lumsden

1993

Developmental Dynamics

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The chick embryo hindbrain is a segmented region of the CNS characterised by repeated blocks of neuroepithelial cells, known as rhombomeres. Individual rhombomeres are polyclonal compartments, defined both by cell lineage restriction and by the restricted expression of development control genes, that later acquire specific patterns of neuronal differentiation and axon outgrowth. The interfaces between adjacent rhombomeres are defined by boundaries across which cells do not move; the boundaries contain specialised cells and are preferentially colonised at early stages of development by extending axons. In this study, routine electron microscopy and high-pressure cryopreservation, a technique that avoids artifacts of chemical fixation, have been used to examine the morphology of rhombomere boundaries through a staged series of chick embryos. We find that the boundary regions contain enlarged extracellular spaces and that these form conduits for axons subsequently extending in the circumferential plane of the hindbrain. Labeling the ventricular surface of the neuroepithelium with DiI crystals in aqueous suspension revealed the morphology of individual cells in the intact neural tube, and demonstrated unusual fan-shaped arrays of cells at the boundaries. These findings contribute further to the evidence that cells at rhombomere boundaries differ from those in rhombomere centres, and leads to hypotheses about both the mechanism of development of the boundaries, and the role they may play in hindbrain patterning. o 1993 Wiley-Liss, Inc.

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Section: Discussionmentioning

confidence: 97%

Cellular morphology and extracellular space at rhombomere boundaries in the chick embryo hindbrain

Heyman

Kent

Lumsden

1993

Developmental Dynamics

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“…CSPG may be synthesised by the immature radial glia at rhombomere boundaries, participating in the formation of the large intercellular spaces. Spaces between glial endfeet have been implicated as axon guidance channels in newts (Singer et al, 1979), and also in the developing mouse retina (Silver and Sidman, 1980). In rat spinal cord, specialised glia-like cells of the floor plate attract commissural axons (Tessier-Lavigne et al, 19881, and are known to express the putative chemoattractant netrin-1 Kennedy et al, 1994).…”

Section: Radial Glia At Rhombomere Boundaries As Axon Guidesmentioning

confidence: 99%

Cell and matrix specialisations of rhombomere boundaries

Heyman

Faissner

Lumsden

1995

Developmental Dynamics

128

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Hindbrain segments, rhombomeres, define distinct cellular and molecular domains which furnish the ground plan for important aspects of neural and cranial development. In this study, further evidence is presented that the interfaces between rhombomeres, rhombomere boundaries, contain both cells and extracellular matrix with specialised characteristics. Cells at rhombomere boundaries show temporally and spatially distinct expression patterns of developmentally important genes. Towards the end of the developmental period when rhombomeres are present, a fan-shaped array of cells at rhombomere boundaries, that constitute the ventricular ridge, shows decreased expression of two genes Woxb-1 and Kmx-20), which earlier in development were expressed in all cells of specific rhombomeres. In contrast, these boundary cells show increased expression of another gene, Pax-6, which earlier in development has a rhombomerespecific expression pattern. A specialised identity for boundary cells is further suggested by increased labelling with an anti-vimentin antibody at rhombomere boundaries, indicating that at least some boundary cells are radial glia or glial precursors. In addition to distinct cellular properties, the extracellular domain at rhombomere boundaries is also specialised. Chondroitin sulphate proteoglycan (CSPG) immunoreactivity is increased and, as revealed by immuno-electron microscopy, localised to extracellular spaces. CSPG is also enriched in boundaries regenerated after ablation, or boundaries generated ectopically by rhombomere transplantation. We propose that rhombomere boundaries form their characteristic morphology at the interface between groups of cells with differing molecular characteristics, representing different cell states. A specialised band of cells then develops at the interface. Both the boundary cells and extracellular matrix have characteristics which could be important in later events of neural development such as axon guidance and cell migration. o 1995 Wiley-Liss, Inc.

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“…It has been well established that, in the injured as well as in the intact developing brain, the growth of axons occurs in the presence of astrocytes that may serve as guides (Schmechel and Rakic, 1979;Silver and Sidman, 1980;Silver et al, 1993). In contrast, regrowth of axotomized axons does not occur in the adult brain, and in this regard the inhibitory role of the astroglial scar has been well documented (for review, see Reier, 1986;Reier and Houle, 1988).…”

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confidence: 99%

Neuritic Outgrowth Associated with Astroglial Phenotypic Changes Induced by Antisense Glial Fibrillary Acidic Protein (GFAP) mRNA in Injured Neuron–Astrocyte Cocultures

et al. 1997

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In the adult CNS, axons fail to regenerate after injury. Among the cell interactions that lead to this failure are those developed with astrocytes. In an effort to elucidate the mechanisms underlying these negative interactions, we have used astrocytes treated with antisense glial fibrillary acidic protein (GFAP) mRNA to inhibit the formation of gliofilaments, indispensable for the astroglial morphological response to injury, and have studied their permissivity for neuritic outgrowth. In a neuronastrocyte coculture, a mechanical lesion led to hypertrophy of astrocytes neighboring the lesion. Neuronal cell bodies and neurites were absent both from the area of lesion and from its surroundings. Reactive astrocytes appeared, therefore, to be a nonpermissive substrate. Transfection that used antisense GFAP mRNA blocked astroglial morphological changes and was characterized by both a persistence of neuronal cell bodies in the vicinity of the lesion site and a growth of neurites into the same region. These morphological differences were associated with a 46% decrease in the GFAP translation capacity and a 50% increase in the concentration of GAP-43 in the treated cultures. Neurons were associated mainly with an extracellular laminin network, which was predominant at the lesion site in treated cocultures. In contrast, those astrocytes highly lamininimmunoreactive appeared to be a nonpermissive substrate for neurons. These results show that inhibition in GFAP synthesis, leading to a reduction of astroglial hypertrophy, relieves the blockade of neuritic outgrowth that normally is observed after a lesion. The mechanisms may involve changes in the secretion of extracellular matrix molecules by astrocytes.

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A mechanism for the guidance and topographic patterning of retinal ganglion cell axons

Cited by 317 publications

References 26 publications

Cellular morphology and extracellular space at rhombomere boundaries in the chick embryo hindbrain

Cellular morphology and extracellular space at rhombomere boundaries in the chick embryo hindbrain

Cell and matrix specialisations of rhombomere boundaries

Neuritic Outgrowth Associated with Astroglial Phenotypic Changes Induced by Antisense Glial Fibrillary Acidic Protein (GFAP) mRNA in Injured Neuron–Astrocyte Cocultures

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