The Semaphorin Receptor PlexinA3 Mediates Neuronal Apoptosis during Dorsal Root Ganglia Development

Ben-Zvi, Ayal; Manor, Osnat; Schachner, Melitta; Yaron, Avraham; Tessier‐Lavigne, Marc; Behar, Oded

doi:10.1523/jneurosci.3573-08.2008

Cited by 52 publications

(55 citation statements)

References 33 publications

(40 reference statements)

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“…Intriguingly, Sema3A displays differential effects on neurons cultured in the presence of different combinations of neurotrophic factors, suggesting that it could act in combination with them to trigger apoptosis of specific sensory neuron populations (Ben-Zvi et al 2006). A first in vivo confirmation of these findings was recently provided by the analysis of sensory neurons in Plexin-A3 knockout mice (Ben-Zvi et al 2008). Disruption of Plexin-A3 results in a decrease in the rate of apoptosis of dorsal root ganglion (DRG) neurons in vivo, particularly at early stages of development.…”

Section: Semaphorinsmentioning

confidence: 97%

Guidance Molecules in Axon Pruning and Cell Death

Vanderhaeghen¹,

Cheng²

2010

Cold Spring Harbor Perspectives in Biology

111

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Axon pruning and neuronal cell death constitute two major regressive events that enable the establishment of fully mature brain architecture and connectivity. Although the cellular mechanisms for these two events are thought to be distinct, recent evidence has indicated the direct involvement of axon guidance molecules, including semaphorins, netrins, and ephrins, in controlling both processes. Here, we review how axon guidance cues regulate regressive events in paradigmatic models of neural development, from early control of apoptosis of neural progenitors, to later maintenance of neuronal survival and stereotyped pruning of axonal branches. These new findings are also discussed in the context of neural diseases and the potential links between axon pruning and degeneration. REGRESSIVE EVENTS IN NEURONAL DEVELOPMENT

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Section: Semaphorinsmentioning

confidence: 97%

Guidance Molecules in Axon Pruning and Cell Death

Vanderhaeghen¹,

Cheng²

2010

Cold Spring Harbor Perspectives in Biology

111

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“…Netrin receptors can stimulate neuronal death when netrin is absent (Llambi et al 2001) whereas semaphorin3A acting through its receptor Plexin-A3 for long periods can promote sensory neuron death (Ben-Zvi et al 2008). Tropic cues can play fundamentally important roles in determining cell fates during development.…”

Section: The Limits Of Categorizationmentioning

confidence: 99%

Cellular Strategies of Axonal Pathfinding

Raper

Mason

2010

Cold Spring Harbor Perspectives in Biology

157

129

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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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“…The plexin A cytoplasmic domain is essential for Sema3A signaling (Takahashi et al, 1999;Tamagnone et al, 1999). Although Sema3A can induce apoptosis when applied to cultured neurons in vitro, to what extent Sema3A directly induces apoptosis in vivo via Npn1 and plexin A proteins is debated (Ben-Zvi et al, 2008;Haupt et al, 2010).…”

Section: Introductionmentioning

confidence: 99%

Semaphorin 3A is a retrograde cell death signal in developing sympathetic neurons

et al. 2016

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During development of the peripheral nervous system, excess neurons are generated, most of which will be lost by programmed cell death due to a limited supply of neurotrophic factors from their targets. Other environmental factors, such as ‘competition factors' produced by neurons themselves, and axon guidance molecules have also been implicated in developmental cell death. Semaphorin 3A (Sema3A), in addition to its function as a chemorepulsive guidance cue, can also induce death of sensory neurons in vitro. The extent to which Sema3A regulates developmental cell death in vivo, however, is debated. We show that in compartmentalized cultures of rat sympathetic neurons, a Sema3A-initiated apoptosis signal is retrogradely transported from axon terminals to cell bodies to induce cell death. Sema3A-mediated apoptosis utilizes the extrinsic pathway and requires both neuropilin 1 and plexin A3. Sema3A is not retrogradely transported in older, survival factor-independent sympathetic neurons, and is much less effective at inducing apoptosis in these neurons. Importantly, deletion of either neuropilin 1 or plexin A3 significantly reduces developmental cell death in the superior cervical ganglia. Taken together, a Sema3A-initiated apoptotic signaling complex regulates the apoptosis of sympathetic neurons during the period of naturally occurring cell death.

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The Semaphorin Receptor PlexinA3 Mediates Neuronal Apoptosis during Dorsal Root Ganglia Development

Cited by 52 publications

References 33 publications

Guidance Molecules in Axon Pruning and Cell Death

Guidance Molecules in Axon Pruning and Cell Death

Cellular Strategies of Axonal Pathfinding

Semaphorin 3A is a retrograde cell death signal in developing sympathetic neurons

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