EphB Forward Signaling Controls Directional Branch Extension and Arborization Required for Dorsal-Ventral Retinotopic Mapping

Hindges, Robert; McLaughlin, Todd; Genoud, Nicolas; Henkemeyer, Mark; O’Leary, Dennis D.M.

doi:10.1016/s0896-6273(02)00799-7

Cited by 281 publications

(351 citation statements)

References 49 publications

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“…In such a case, the primary axons of ND RGCs might terminate in the appropriate zone, preserving nearest-neighbor connectivity, but additional interstitial branches would be misguided and form multiple anteriorly shifted ectopic TZs. A similar mechanism has been demonstrated in the EphB2/EphB3 double mutant where RGC axons extend interstitial branches beyond the primary TZ location, in addition to a TZ in the correct location (Hindges et al, 2002). However, the failure to demonstrate multiple TZs in mutant and control SCs retrogradely labeled in the posteriallateral region suggests an alternative mechanism for ectopic TZs in Phr1 retinal mutants.…”

Section: Discussionsupporting

confidence: 58%

Phr1 is required for proper retinocollicular targeting of nasal–dorsal retinal ganglion cells

Bloom

Culican

2011

Vis Neurosci

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Precise targeting of retinal projections is required for the normal development of topographic maps in the mammalian primary visual system. During development, retinal axons project to and occupy topographically appropriate positions in the dorsal lateral geniculate nucleus (dLGN) and superior colliculus (SC). Phr1 retinal mutant mice, which display mislocalization of the ipsilateral retinogeniculate projection independent of activity and ephrin-A signaling, were found to have a more global disruption of topographic specificity of retinofugal inputs. The retinocollicular projection lacks local refinement of terminal zones and multiple ectopic termination zones originate from the dorsal-nasal (DN) retinal quadrant. Similarly, in the dLGN, the inputs originating from the contralateral DN retina are poorly refined in the Phr1 mutant. These results show that Phr1 is an essential regulator of retinal ganglion cell projection during both dLGN and SC topographic map development.

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Section: Discussionsupporting

confidence: 58%

Phr1 is required for proper retinocollicular targeting of nasal–dorsal retinal ganglion cells

Bloom

Culican

2011

Vis Neurosci

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“…He proposed that the retina and the tectum have a system of complementary chemical cues that help map the innervating axons onto their appropriate locations in the tectum (Sperry 1963). Subsequent work by many groups has shown that retinal axons compete amongst themselves in an activity dependent manner for tectal territory, and can thereby redistribute themselves within the target, but the basic finding that retinal axons initially prefer to grow to or branch in specific target locations has been vindicated by the discovery that counter gradients of Ephs and ephrins help establish retinotopy in visual centers (Cheng et al 1995;Feldheim et al 2000;Hindges et al 2002;McLaughlin et al 2003) (see Feldheim and O'Leary 2010). …”

Section: Axons Extend In Vivo In a Directed Mannermentioning

confidence: 99%

“…However, even surface localized guidance cues can be used to generate a gradient of guidance information. For example, gradients of ephrin expression in the tectum and superior colliculus help organize the retinotopic projections of retinal ganglion cells onto their target fields (Cheng et al 1995;Feldheim et al 2000;Hindges et al 2002;McLaughlin et al 2003;O'Leary 2010).…”

Section: Tropic Guidance Cuesmentioning

confidence: 99%

Cellular Strategies of Axonal Pathfinding

Raper

Mason

2010

Cold Spring Harbor Perspectives in Biology

157

130

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Axons follow highly stereotyped and reproducible trajectories to their targets. In this review we address the properties of the first pioneer neurons to grow in the developing nervous system and what has been learned over the past several decades about the extracellular and cell surface substrata on which axons grow. We then discuss the types of guidance cues and their receptors that influence axon extension, what determines where cues are expressed, and how axons respond to the cues they encounter in their environment.T his article provides an overview of how growth cones respond to the cellular substrata and molecular cues they encounter as they extend through the developing nervous system. It elaborates on the primer by Kolodkin and TessierLavigne (2010) and touches on many of the topics covered in greater detail in the articles that follow. The first sections describe how axons extend in a directed manner, the substrata on which they grow, interactions between pioneer and follower axons, and growth cone behaviors in emerging tracts and at decision points. The subsequent sections discuss examples of specific cues, their distributions, how their distributions are determined, and how growth cones integrate multiple cues during pathfinding. AXONS EXTEND IN VIVO IN A DIRECTED MANNERThe first person to visualize the growing tips of axons, Ramon y Cajal, recognized that axons for the most part grow very efficiently towards their ultimate targets. He was a strong advocate for axons finding their way in response to chemotactic cues:"If one admits that neuroblasts are endowed with chemotactic properties, then one might also imagine that they are capable of ameboid movements, initiated by factors secreted from epithelial, neural, or mesodermal elements. As a result, their processes may be oriented in the direction of chemical gradients, and thus guided to the secreting cells" (Ramon y Cajal 1892; trans. English, 1995).This surprisingly modern outlook emphasizing directed guidance was temporarily derailed by the views of Weiss during the 1920s and 1930s. He first argued that functional specificity did not arise as a consequence of specific axonal connections (Weiss 1936), and later argued that nonspecific mechanical guidance cues play a predominant role in guiding axons and organizing them into nerves and tracts

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“…Factors that have been shown to shape axonal arbor growth include not only extracellular guidance cues (Yates et al, 2001;Hindges et al, 2002) but also synaptic activity (O'Rourke et al, 1994;Debski and Cline, 2002;Ruthazer and Cline, 2004) and intracellular and intercellular signaling (Hall et al, 2000;CohenCory and Lom, 2004;Govek et al, 2005). Similarly, progress has been made in elucidating the molecular mechanisms by which synapses are assembled (Goda and Davis, 2003;Li and Sheng, 2003;Ziv and Garner, 2004).…”

Section: Introductionmentioning

confidence: 99%

Evidence fromIn VivoImaging That Synaptogenesis Guides the Growth and Branching of Axonal Arbors by Two Distinct Mechanisms

Meyer¹,

Smith²

2006

J. Neurosci.

264

318

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To explore the relationship between axon arbor growth and synaptogenesis, developing retinal ganglion cell (RGC) axon arbors in zebrafish optic tectum were imaged in vivo at high temporal and spatial resolution using two-photon microscopy. Individual RGC axons were dually labeled by expression of a cytosolic red fluorescent protein (DsRed Express) to mark arbor structure and a fusion of the synaptic vesicle protein synaptophysin with green fluorescent protein (Syp:GFP) to mark presynaptic vesicles. Analysis of time-lapse sequences acquired at 10 min intervals revealed unexpectedly rapid kinetics of both axon branch and vesicle cluster turnover. Nascent axonal branches exhibited short average lifetimes of 19 min, and only 17% of newly extended axonal processes persisted for periods exceeding 3 h. The majority (70%) of Syp:GFP puncta formed on newly extended axonal processes. Syp:GFP puncta also exhibited short average lifetimes of 30 min, and only 34% of puncta were stabilized for periods exceeding 3 h. Moreover, strongly correlated dynamics of Syp:GFP puncta and branch structure suggest that synaptogenesis exerts strong influences on both the extension and the selective stabilization of nascent branches. First, new branches form almost exclusively at newly formed Syp:GFP puncta. Second, stabilized nascent branches invariably bear Syp:GFP puncta, and the detailed dynamics of branch retraction suggest strongly that nascent synapses can act at branch tips to arrest retraction. These observations thus provide evidence that synaptogenesis guides axon arbor growth by first promoting initial branch extension and second by selective branch stabilization.

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EphB Forward Signaling Controls Directional Branch Extension and Arborization Required for Dorsal-Ventral Retinotopic Mapping

Cited by 281 publications

References 49 publications

Phr1 is required for proper retinocollicular targeting of nasal–dorsal retinal ganglion cells

Phr1 is required for proper retinocollicular targeting of nasal–dorsal retinal ganglion cells

Cellular Strategies of Axonal Pathfinding

Evidence fromIn VivoImaging That Synaptogenesis Guides the Growth and Branching of Axonal Arbors by Two Distinct Mechanisms

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