Neuronal growth cone collapse triggers lateral extensions along trailing axons

Davenport, Roger W.; Thies, Edda; Cohen, Matthew

doi:10.1038/6360

Cited by 64 publications

(34 citation statements)

References 42 publications

(30 reference statements)

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“…Typically uncollapsed growth cones displayed the common ‘hand like’ morphology, and collapsed growth cones appeared as thin stumps. Growth cones were counted only at the end of neurites, even when significant growth cone-like processes were observed along the shaft of a neurite, as these lateral extensions can occur in response to the collapse of the leading growth cone [76]. Examples of collapsed versus uncollapsed growth cones are illustrated in Figure 7.…”

Section: Resultsmentioning

confidence: 99%

Changes in expression of Class 3 Semaphorins and their receptors during development of the rat retina and superior colliculus

et al. 2014

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BackgroundMembers of the Semaphorin 3 family (Sema3s) influence the development of the central nervous system, and some are implicated in regulating aspects of visual system development. However, we lack information about the timing of expression of the Sema3s with respect to different developmental epochs in the mammalian visual system. In this time-course study in the rat, we document for the first time changes in the expression of RNAs for the majority of Class 3 Semaphorins (Sema3s) and their receptor components during the development of the rat retina and superior colliculus (SC).ResultsDuring retinal development, transcript levels changed for all of the Sema3s examined, as well as Nrp2, Plxna2, Plxna3, and Plxna4a. In the SC there were also changes in transcript levels for all Sema3s tested, as well as Nrp1, Nrp2, Plxna1, Plxna2, Plxna3, and Plxna4a. These changes correlate with well-established epochs, and our data suggest that the Sema3s could influence retinal ganglion cell (RGC) apoptosis, patterning and connectivity in the maturing retina and SC, and perhaps guidance of RGC and cortical axons in the SC. Functionally we found that SEMA3A, SEMA3C, SEMA3E, and SEMA3F proteins collapsed purified postnatal day 1 RGC growth cones in vitro. Significantly this is a developmental stage when RGCs are growing into and within the SC and are exposed to Sema3 ligands.ConclusionThese new data describing the overall temporal regulation of Sema3 expression in the rat retina and SC provide a platform for further work characterising the functional impact of these proteins on the development and maturation of mammalian visual pathways.

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Section: Resultsmentioning

confidence: 99%

Changes in expression of Class 3 Semaphorins and their receptors during development of the rat retina and superior colliculus

et al. 2014

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“…For example, it is known that growth cones respond to increased NO by collapsing in a rapid and reversible manner (Hess et al, 1993;Renteria and Constantine-Paton, 1996), a process that may, in turn, stimulate back branching along the axon shaft (Davenport et al, 1999). Indeed, pauses in the forward extension of growth cones in vitro have been correlated with the later formation of interstitial branches (Szebenyi et al, 1998).…”

Section: Discussionmentioning

confidence: 99%

Nitric oxide modulates retinal ganglion cell axon arbor remodelingin vivo

Cogen

Cohen-Cory

2000

J. Neurobiol.

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“…EphA3-Fc binds to ephrin A ligands to inhibit their function, and this interferes with temporal axon branching from retinal explants in a modified stripe assay (12). By using an RGC-tectal cell coculture system, Davenport et al (27) showed an intriguing phenomenon that sprouting of branches from trailing axons was induced several hundred micrometers behind the collapse site of leading axons by ephrin-A ligands. This sprouting might be a fundamental in vivo mechanism for topographically specific branching.…”

Section: Discussionmentioning

confidence: 99%

“…Graded ephrin-A5 expression stops growth cone advance on the surface of the posterior tectum. Based on in vitro studies, ephrin-A5 may also trigger the formation of secondary arbors along the primary axon that dive to the deeper tectal layers (27). These arbors define the retinotopic map in the SFGS where ephrin-A5 acts again to restrict the topographically correct positions that will then be later refined by activity-dependent processes.…”

Section: Discussionmentioning

confidence: 99%

Ephrin-A5 restricts topographically specific arborization in the chick retinotectal projection in vivo

Sakurai

Wong

Drescher

et al. 2002

Proc. Natl. Acad. Sci. U.S.A.

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The retinotectal map is the best characterized model system to study how axons respond to guidance cues during the formation of the nervous system. Recent studies have shown that the critical event in forming this map is topographic-specific axon branching. To elucidate the in vivo role of the repulsive cue ephrin-A5 in this event, we used chromophore-assisted laser inactivation (CALI) to generate acute loss of ephrin-A5 function in localized areas of the posterior tectum of chick embryos in ovo and analyzed the resulting changes of retinal projections during initial outgrowth (E11) and when retinal axons arborize in the deep layers in the tectum (E12). We confirmed that ephrin-A5 functions to restrict initial axon outgrowth at E11. At E12, CALI of ephrin-A5 did not affect the extent of axon outgrowth on the tectal surface but instead caused ectopic arborization posterior to the topographically correct site in deeper layers of the tectum. This shows that ephrin-A5 restricts arborization during this critical process for developing the retinotopic map. CALI provides an approach to inactivate in vivo function in higher vertebrates with high temporal and spatial specificity that may have wide application.T he retinotectal projection is a well established model system to study mechanisms that form the topographic map of neural connections in the brain. It is thought that molecules expressed in gradients guide axons to their precise topographic targets. This chemoaffinity hypothesis proposed by Sperry (1) has been supported by the identification of molecular cues expressed in gradients in the retina and in the tectum (2). One important guidance cue is ephrin-A5 (3). The graded expression of ephrin-A ligands in the tectum coupled with expression of the Eph receptors that bind these ligands in retinal axons provides a potential molecular mechanism for defining the anteriorposterior (A-P) map (3, 4). Ephrin-A5 (5) is predominantly expressed in the posterior half of the chick tectum in a steep gradient, whereas a second ephrin, ephrin-A2 (6), is expressed in a shallower gradient across the entire tectum (7), and both gradients exist throughout the formation of the retinotectal map. These expression patterns suggest that ephrin-A5 and ephrin-A2 act in the graded repulsion of retinal axons involved in mapping. This notion is supported by aberrant retinal axon extension beyond their target areas observed in embryos with single and double deletions of the ephrin-A5 and ephrin-A2 genes (8, 9). These genetic deletion studies showed the overall importance of ephrin-A ligands as topographic labels, but how these ligands act in vivo has not been demonstrated.In mammals and avians, the development of topographical order occurs through a multistep process: initial axon outgrowth, topographically specific arborization, and remodeling (10, 11). Initial axon outgrowth is relatively inaccurate, and axons often overshoot beyond their correct termination zone (TZ). Topographically specific branching and arborization in higher vertebrates ...

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Neuronal growth cone collapse triggers lateral extensions along trailing axons

Cited by 64 publications

References 42 publications

Changes in expression of Class 3 Semaphorins and their receptors during development of the rat retina and superior colliculus

Changes in expression of Class 3 Semaphorins and their receptors during development of the rat retina and superior colliculus

Nitric oxide modulates retinal ganglion cell axon arbor remodelingin vivo

Ephrin-A5 restricts topographically specific arborization in the chick retinotectal projection in vivo

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