Molecular and cellular characterization of the glial roof plate of the spinal cord and optic tectum: A possible role for a proteoglycan in the development of an axon barrier

Snow, Diane; Steindler, Dennis A.; Silver, Jerry

doi:10.1016/0012-1606(90)90203-u

Cited by 378 publications

(231 citation statements)

References 78 publications

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“…This midline structure has long been thought to represent a barrier to axonal growth in the developing CNS (see Snow et al, 1990;Steindler, 1993). The roof plateenriched expression of several chondroitin (Snow et al, 1991;Katoh-Semba et al, 1995;Engel et al, 1996;Katoh-Semba et al, 1998) and keratan (Cole and McCabe, 1991; sulfate proteoglycans which are capable of inhibiting neurite outgrowth in vitro, provides support for this hypothesis.…”

Section: Vertebrate Spinal Cord: Bone Morphogenetic Proteinsmentioning

confidence: 97%

“…These include Slit-1, Slit-2, Slit-3 (see Brose and TessierLavigne, 2000 and references therein), NPN-2 (Chen et al, 1997), B-class ephrins (Imondi et al, 2000), Annexin IV (Hamre et al, 1996), BMP-6 (see Lee et al, 2000), and VEMA (Runko et al, 1999). Given that the roof plate, like the floor plate, is thought to be an important source of guidance cues for extending axons (Snow et al, 1990;Augsburger et al, 1999), each of these proteins may play important roles in regulating the pathfinding of axons that grow near, or across, the dorsal midline of the spinal cord. In fact, the Slits (Brose et al, 1999;Zou et al, 2000), Neuropilin-2 (Chen et al, 1997), B-class ephrins (Flanagan and Vanderhaeghen, 1998) and BMPs (Augsburger et al, 1999) have previously been shown to mediate repulsive axon guidance events in several neural systems.…”

Section: Novel Midline Markersmentioning

confidence: 99%

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Axon guidance at the midline choice point

Kaprielian

Runko

Imondi

2001

Developmental Dynamics

145

108

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The central nervous system (CNS) of higher organisms is bilaterally-symmetric. The transfer of information between the two sides of the nervous system occurs through commissures formed by neurons that project axons across the midline to the contralateral side of the CNS. Interestingly, these axons cross the midline only once. Other neurons extend axons that never cross the midline; they project exclusively on their own (ipsilateral) side of the CNS. Thus, the midline is an important choice point for several classes of pathfinding axons. Recent studies demonstrate that specialized midline cells play critical roles in regulating the guidance of both crossing and non-crossing axons at the ventral midline of the developing vertebrate spinal cord and the Drosophila ventral nerve cord. For example, these cells secrete attractive cues that guide commissural axons over long distances to the midline of the CNS. Furthermore, shortrange interactions between guidance cues present on the surfaces of midline cells, and their receptors expressed on the surfaces of pathfinding axons, allow commissural axons to cross the midline only once and prevent ipsilaterally-projecting axons from entering the midline. Remarkably, the molecular composition of commissural axon surfaces is dynamically-altered as they cross the midline. Consequently, commissural axons become responsive to repulsive midline guidance cues that they had previously ignored on the ipsilateral side of the midline. Concomitantly, commissural axons lose responsiveness to attractive guidance cues that had initially attracted them to the midline. Thus, these exquisitely regulated guidance systems prevent commissural axons from lingering within the confines of the midline and allow them to pioneer an appropriate pathway on the contralateral side of the CNS. Many aspects of midline guidance are controlled by mechanistically and evolutionarily-conserved ligand-receptor systems. Strikingly, recent studies demonstrate that these receptors are modular; the ectodomains determine ligand recognition and the cytoplasmic domains specify the response of an axon to a given guidance cue. Despite rapid and dramatic progress in elucidating the molecular mechanisms that control midline guidance, many questions remain.

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Section: Vertebrate Spinal Cord: Bone Morphogenetic Proteinsmentioning

confidence: 97%

Section: Novel Midline Markersmentioning

confidence: 99%

Axon guidance at the midline choice point

Kaprielian

Runko

Imondi

2001

Developmental Dynamics

145

108

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“…In the diencephalon and midbrain midline, congregations of specialized glial cells (Barradas et al 1989, Snow et al 1990a, Wu et al 1995, transitory neurons (Sretavan et al 1994) and a growing number of molecules have been identified (Reviews: Mason and Sretavan 1997. For instance, the first retinal ganglion cell axons arriving at the embryonic mouse ventral diencephalon encounter an inverted V-shaped neuronal array defining the midline and posterior boundaries of the future optic chiasm.…”

Section: The Midline Of the Central Nervous Systemmentioning

confidence: 99%

“…The resident radial glial cells of the roof plate suffer changes in their arrangement and density and express selectively certain ECM molecules, such as keratan and chondroitin sulfates. The presence of these GAGs plus the behavior of dorsal root ganglion axons growing on a substrate containing keratan and chondroitin sulfate has led to the suggestion that glial cells at the roof plate may be responsible for preventing crossing of neurites through the dorsal midline (Snow et al 1990a). However, it is not clear whether the roof plate has similar properties along its entire rostro-caudal axis since the diencephalic roof plate (subcommissural organ), together with the rombencephalic floor plate are the source of secretory compounds of related nature that are not produced in any other level of the roof or floor midline (Yulis et al 1998).…”

Section: The Midline Of the Central Nervous Systemmentioning

confidence: 99%

“…It has been known for some time that nonneuronal cells in the dorsal brain stem midline differ from their lateral neighbors in their ability to take up exogenous label borne by afferent axons (Barradas et al 1989, Kageyama andRobertson 1993) as well as in glycogen deposition, binding of antibodies against S-100 protein, RC1 and R2D5 anti- gens, cytoskeletal components and annexins (Van Hartesveldt et al 1986, Barradas et al 1989, Snow et al 1990a, Mori et al 1990, McCabe and Cole 1992, Hamre et al 1996, Wu et al 1995. It is interesting to notice that both the floor plate and the roof plate at both cord and midbrain (median ventricular formation) levels, together with the lamina terminalis, are part of the discrete embryonic sites containing cells which have exited the cell cycle very early during embryogenesis (Raedler et al 1981, Kahane andKalcheim 1998).…”

Section: The Midline Of the Central Nervous Systemmentioning

confidence: 99%

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Modulators of axonal growth and guidance at the brain midline with special reference to glial heparan sulfate proteoglycans

Cavalcante

Garcia-Abreu

Moura‐Neto

et al. 2002

An. Acad. Bras. Ciênc.

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Bilaterally symmetric organisms need to exchange information between the left and right sides of their bodies to integrate sensory input and to coordinate motor control. Thus, an important choice point for developing axons is the Central Nervous System (CNS) midline. Crossing of this choice point is influenced by highly conserved, soluble or membrane-bound molecules such as the L1 subfamily, laminin, netrins, slits, semaphorins, Eph-receptors and ephrins, etc. Furthermore, there is much circumstantial evidence for a role of proteoglycans (PGs) or their glycosaminoglycan (GAG) moieties on axonal growth and guidance, most of which was derived from simplified models. A model of intermediate complexity is that of cocultures of young neurons and astroglial carpets (confluent cultures) obtained from medial and lateral sectors of the embryonic rodent midbrain soon after formation of its commissures. Neurite production in these cocultures reveals that, irrespective of the previous location of neurons in the midbrain, medial astrocytes exerted an inhibitory or nonpermissive effect on neuritic growth that was correlated to a higher content of both heparan and chondroitin sulfates (HS and CS). Treatment with GAG lyases shows minor effects of CS and discloses a major inhibitory or non-permissive role for HS. The results are discussed in terms of available knowledge on the binding of HSPGs to interative proteins and underscore the importance of understanding glial polysaccharide arrays in addition to its protein complement for a better understanding of neuron-glial interactions.

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Chondroitin sulfate proteoglycans in the developing central nervous system. II. Immunocytochemical localization of neurocan and phosphacan

et al. 1996

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Using immunocytochemistry, we have compared the distribution of neurocan and phosphacan in the developing central nervous system. At embryonic day 13 (E13), phosphacan surrounds the radially oriented neuroepithelial cells of the telencephalon, whereas neurocan staining of brain parenchyma is very weak. By E16-19, strong staining of both neurocan and phosphacan is seen in the marginal zone and subplate of the neocortex, and phosphacan is present in the ventricular zone and also has a diffuse distribution in other brain areas. Phosphacan is also widely distributed in embryonic spinal cord, where it is strongly expressed throughout the gray and white matter, in the dorsal and ventral nerve roots, and in the roof plate at E13, when neurocan immunoreactivity is seen only in the mesenchyme of the future spinal canal. Neurocan first begins to appear in the spinal cord at E16-19, in the region of ventral motor neurons. In early postnatal and adult cerebellum, neurocan immunoreactivity is seen in the prospective white matter and in the granule cell, Purkinje cell, and molecular layers, whereas phosphacan immunoreactivity is associated with Bergmann glial fibers in the molecular layer and their cell bodies (the Golgi epithelial cells) below the Purkinje cells. These immunocytochemical results demonstrate that the expression of neurocan and phosphacan follow different developmental time courses not only in postnatal brain (as previously demonstrated by radioimmunoassay) but also in the embryonic central nervous system. The specific localization and different temporal expression patterns of these two proteoglycans are consistent with other evidence indicating that they have overlapping or complementary roles in axon guidance, cell interactions, and neurite outgrowth during nervous tissue histogenesis.

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Molecular and cellular characterization of the glial roof plate of the spinal cord and optic tectum: A possible role for a proteoglycan in the development of an axon barrier

Cited by 378 publications

References 78 publications

Axon guidance at the midline choice point

Axon guidance at the midline choice point

Modulators of axonal growth and guidance at the brain midline with special reference to glial heparan sulfate proteoglycans

Chondroitin sulfate proteoglycans in the developing central nervous system. II. Immunocytochemical localization of neurocan and phosphacan

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