Islet1 selectively promotes peripheral axon outgrowth in Rohon‐Beard primary sensory neurons

Tanaka, Hideomi; Nojima, Yuki; Watanabe, Shôji; Sato, Miki; Nakayama, Ryoko; Ohshima, Toshio; Okamoto, Hitoshi

doi:10.1002/dvdy.22499

Cited by 27 publications

(43 citation statements)

References 41 publications

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“…In zebrafish embryos, inhibition of Isl2 results in aberrant axon positioning, as well as defective axon outgrowth and branching of Rohon-Beard and trigeminal sensory neurons (Andersen et al, 2011;Segawa et al, 2001). Similar defects have been reported upon inhibition of Isl1 in both mouse and zebrafish (Liang et al, 2011;Tanaka et al, 2011). Neuron-specific Islet target genes have begun to be identified, and they are important for neural morphology (Aoki et al, 2014).…”

Section: Discussionmentioning

confidence: 65%

Islet is a key determinant of ascidian palp morphogenesis

et al. 2014

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The anterior-most ectoderm of ascidian larvae contains the adhesive papillae, or palps, which play an important role in triggering the metamorphosis of swimming tadpoles. In Ciona intestinalis, the palps consist of three conical protrusions within a field of thickened epithelium that form late in embryogenesis, as tailbuds mature into larvae. The palp protrusions express the LIM-homeodomain transcription factor Islet. Protrusion occurs through differential cell elongation, probably mediated by Islet, as we find that ectopic expression of Islet is sufficient to promote cell lengthening. FGF signaling is required for both Islet expression and palp morphogenesis. Importantly, we show that Islet expression can rescue the palpdeficient phenotype that results from inhibition of FGF signaling. We conclude that Islet is a key regulatory factor governing morphogenesis of the palps. It is conceivable that Islet is also essential for the cellular morphogenesis of placode-derived sensory neurons in vertebrates.

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Section: Discussionmentioning

confidence: 65%

Islet is a key determinant of ascidian palp morphogenesis

et al. 2014

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“…To test the targeting of predicted transcription factors at these distal sites, we chose two factors for each stage for which genome-wide binding data sets were publicly available for matching stages of neuronal differentiation (SOX2 and SOX3 for NP; LHX3 and ISL1 for TND1; and CTCF and RFX1 for TND10) and were shown to be critical for the respective stages ( Fig. 3D-F; Uwanogho et al 1995;Sharma et al 1998;Tanaka et al 2011;Dekker 2012;Hirayama et al 2012;Lee et al 2012Lee et al , 2013. Comparative analysis of these ChIP-seq data sets with open and H3K27ac-positive sites revealed a high enrichment for these factors at distal regions in the respective stages (Fig.…”

Section: Distal Regulatory Elements Recruit Distinct Transcription Famentioning

confidence: 99%

Dynamics and function of distal regulatory elements during neurogenesis and neuroplasticity

et al. 2015

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Gene regulation in mammals involves a complex interplay between promoters and distal regulatory elements that function in concert to drive precise spatiotemporal gene expression programs. However, the dynamics of the distal gene regulatory landscape and its function in the transcriptional reprogramming that underlies neurogenesis and neuronal activity remain largely unknown. Here, we performed a combinatorial analysis of genome-wide data sets for chromatin accessibility (FAIREseq) and the enhancer mark H3K27ac, revealing the highly dynamic nature of distal gene regulation during neurogenesis, which gets progressively restricted to distinct genomic regions as neurons acquire a post-mitotic, terminally differentiated state. We further find that the distal accessible and active regions serve as target sites for distinct transcription factors that function in a stage-specific manner to contribute to the transcriptional program underlying neuronal commitment and maturation. Mature neurons respond to a sustained activity of NMDA receptors by epigenetic reprogramming at a large number of distal regulatory regions as well as dramatic reorganization of super-enhancers. Such massive remodeling of the distal regulatory landscape in turn results in a transcriptome that confers a transient loss of neuronal identity and gain of cellular plasticity. Furthermore, NMDA receptor activity also induces many novel prosurvival genes that function in neuroprotective pathways. Taken together, these findings reveal the dynamics of the distal regulatory landscape during neurogenesis and uncover novel regulatory elements that function in concert with epigenetic mechanisms and transcription factors to generate the transcriptome underlying neuronal development and activity.

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“…Knockdown of Crmp4 affects peripheral axon growth of RB neurons, and this phenotype is similar to Sema3D morphants (Liu and Halloran 2005;Tanaka et al 2011). Additionally, double knockdown of Sema3D and Crmp4 shows synergistic effects on peripheral axon growth.…”

Section: Sensory Axon Guidance In Zebrafishmentioning

confidence: 84%

“…Isl1 is also important for regulating the expression of collapsin-response mediator protein 4 (Crmp4), which is involved in the semaphorin-mediated signaling pathway controlling cytoskeleton and endocytosis regulation in RB neurons (Schmidt and Strittmatter 2007;Tanaka et al 2011). Knockdown of Crmp4 affects peripheral axon growth of RB neurons, and this phenotype is similar to Sema3D morphants (Liu and Halloran 2005;Tanaka et al 2011).…”

Section: Sensory Axon Guidance In Zebrafishmentioning

confidence: 95%

“…Interestingly, both Sema3D and Crmp4 knockdown do not affect central projections of RB neurons. Only peripheral axons were shown to respond to ectopic Sema3D (Liu and Halloran 2005;Tanaka et al 2011), indicating that Sema3D-Crmp4 signaling primarily affects the growth of peripheral axons. It has been hypothesized that the expression of Sema3D in the midline roof plate might repel peripheral axons from the spinal cord (Fig.…”

Section: Sensory Axon Guidance In Zebrafishmentioning

confidence: 96%

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Axon Guidance in the Spinal Cord

Imai

Yoshida

2015

Semaphorins

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Neural circuit assembly requires the coordination of various developmental processes, including axon guidance and synapse formation. Growth cones, the leading edges of axons, navigate by interacting with different kinds of attractive and repulsive axon guidance cues along their trajectories and at target areas.Spinal cords consist of different types of neural circuits, such as sensory-motor, commissural, and sympathetic circuits. Each neural circuit provides an unique model system to understand the cellular and molecular mechanisms underlying neural circuit formation. Studies of sensory-motor circuits have outlined the basic events leading to circuit formation. First, both sensory and motor axons project to the appropriate peripheral muscles. Sensory axons then form precise monosynaptic connections with a select group of motor neuron pools in the ventral spinal cord, and these pools of motor neurons ultimately develop their appropriate dendrite morphologies. Examination of commissural neurons and their axon trajectories in the spinal cord has contributed important data on how attractants and repellents influence the midline crossing of axons. Finally, studies of sympathetic neurons have led toward a greater overall understanding of the cellular and molecular mechanisms underlying neuronal survival, retrograde signaling, neuronal migration, and axon guidance.Semaphorin signaling in neural circuit assembly has been studied extensively in the spinal cord. Importantly, the first mammalian semaphorin, Sema3A, was identified by monitoring growth cone collapse in sensory neurons in vitro. Here, we review the current knowledge on semaphorin signaling in various steps of vertebrate neural circuit assembly in the spinal cord, including axon guidance, synaptic specificity, synapse formation, and dendrite development, highlighting the different neural circuit systems that have helped to broaden our understanding of semaphorins and their functions in the developing nervous system.

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Islet1 selectively promotes peripheral axon outgrowth in Rohon‐Beard primary sensory neurons

Cited by 27 publications

References 41 publications

Islet is a key determinant of ascidian palp morphogenesis

Islet is a key determinant of ascidian palp morphogenesis

Dynamics and function of distal regulatory elements during neurogenesis and neuroplasticity

Axon Guidance in the Spinal Cord

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