Patterning of sexually dimorphic neurogenesis in the <i>Caenorhabditis elegans</i> ventral cord by Hox and TALE homeodomain transcription factors

Kalis, Andrea; Kissiov, Djem U.; Kolenbrander, Emily S.; Palchick, Zachary; Raghavan, Shraddha; Tetreault, Breanna J.; Williams, Erin R.; Loer, Curtis M.; Wolff, Jennifer Ross

doi:10.1002/dvdy.24043

Cited by 4 publications

(6 citation statements)

References 57 publications

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“…In addition, as amply demonstrated in the past, neurotransmitter identity serves as a useful entry point to study mechanisms of neuronal identity control (e.g., Lints and Emmons 1999;Sze et al 2002;Flames and Hobert 2009;Serrano-Saiz et al 2013;Kalis et al 2014;Zhang et al 2014;Pereira et al 2015;Gendrel et al 2016). We anticipate that our neurotransmitter atlas, summarized in Figure 8, will provide further entry points into studying neuron identity control.…”

Section: Sexual Dimorphisms In Neurotransmitter Usage In Sexshared Nementioning

confidence: 80%

“…subclassification does not correlate with the connectivity-based classification of "response rays" and "PVV rays" (Jarrell et al 2012). Neurotransmitter diversity is also seen in the CP ventral cord neuron class, which was reported to be distinct based on connectivity and patterns of serotonin and neuropeptide usage (Loer and Kenyon 1993;Jarrell et al 2012;Kalis et al 2014). The subclass-specific usage of Glu and GABA as well as the differential expression of unc-47/VGAT and unc-17/VACHT in subsets of CP neurons that we report here further corroborates a subclass diversification into at least six distinct subclasses (CP0, CP01-04, CP05-06, CP07, CP08, and CP09; Table S1).…”

Section: Neuronal Subclasses Express Distinct Neurotransmittersmentioning

confidence: 95%

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A Neurotransmitter Atlas of theCaenorhabditis elegansMale Nervous System Reveals Sexually Dimorphic Neurotransmitter Usage

et al. 2017

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The nervous system of most animals is sexually dimorphic but such dimorphisms are generally poorly mapped on an anatomical, cellular, and molecular level. The adult nervous system of the nematode displays a number of clearly defined anatomical sexual dimorphisms, but molecular features of sexually dimorphic neurons remain sparse. In this resource paper, we provide a comprehensive atlas of neurotransmitters used in the nervous system of the male and compare it to that of the hermaphrodite. Among the three major neurotransmitter systems, acetylcholine (ACh) is the most frequently used, followed by glutamate (Glu), and lastly γ-aminobutyric acid (GABA). Many male-specific neurons utilize multiple neurotransmitter systems. Interestingly, we find that neurons that are present in both sexes alter their neurotransmitter usage depending on the sex of the animal. One neuron scales up its usage of ACh, another becomes serotonergic in males, and another one adds a new neurotransmitter (glutamate) to its nonsex-specific transmitter (ACh). In all these cases, neurotransmitter changes are correlated with substantial changes in synaptic connectivity. We assembled the neurotransmitter maps of the male-specific nervous system into a comprehensive atlas that describes the anatomical position of all the neurons of the male-specific nervous system relative to the sex-shared nervous system. We exemplify the usefulness of the neurotransmitter atlas by using it as a tool to define the expression pattern of a synaptic organizer molecule in the male tail. Taken together, the male neurotransmitter atlas provides an entry point for future functional and developmental analysis of the male nervous system.

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Section: Sexual Dimorphisms In Neurotransmitter Usage In Sexshared Nementioning

confidence: 80%

Section: Neuronal Subclasses Express Distinct Neurotransmittersmentioning

confidence: 95%

A Neurotransmitter Atlas of theCaenorhabditis elegansMale Nervous System Reveals Sexually Dimorphic Neurotransmitter Usage

et al. 2017

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“…The regulatory mechanisms that implement this sexual dimorphism in lineage and cell fate remain largely unclear. Several factors contribute to patterning and fate specification in both sexes, including the Hox genes lin-39 and mab-5, and the TALE-homeodomain transcription factor genes unc-62 and ceh-20 (Clark et al 1993;Salser et al 1993;Liu et al 2006;Potts et al 2009;Kalis et al 2014). It seems likely that TRA-1A acts together with these and other factors in the ventral hypodermis to control its sexually dimorphic development.…”

Section: Sex-specific Neurogenesis: Regulation Of Cell Lineage and DImentioning

confidence: 99%

Sexual Dimorphism and Sex Differences in Caenorhabditis elegans Neuronal Development and Behavior

2018

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As fundamental features of nearly all animal species, sexual dimorphisms and sex differences have particular relevance for the development and function of the nervous system. The unique advantages of the nematode have allowed the neurobiology of sex to be studied at unprecedented scale, linking ultrastructure, molecular genetics, cell biology, development, neural circuit function, and behavior. Sex differences in the nervous system encompass prominent anatomical dimorphisms as well as differences in physiology and connectivity. The influence of sex on behavior is just as diverse, with biological sex programming innate sex-specific behaviors and modifying many other aspects of neural circuit function. The study of these differences has provided important insights into mechanisms of neurogenesis, cell fate specification, and differentiation; synaptogenesis and connectivity; principles of circuit function, plasticity, and behavior; social communication; and many other areas of modern neurobiology.

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“…UNC-62, along with LIN-39, promotes survival of the VCs by ensuring CEH-20 localizes to the nucleus; the LIN-39/CEH-20 complex then represses egl-1 transcription (Liu et al 2006;Potts et al 2009). Sexual determination of the Pn.aap cells is established by the first larval (L1) stage (as VCs in hermaphrodites and the precursors of CAs and CPs in males) (Kalis et al 2014). It was also shown that LIN-39 is not required for the expression of the VC terminal differentiation feature ida-1.…”

Section: Introductionmentioning

confidence: 99%

“…Moreover, since the surviving descendants from P1, P2, and P9-12 still express ida-1::gfp in lin-39(lf); ced-3(lf) double mutants, it was concluded that the role of LIN-39 is most likely restricted to VC survival, not differentiation (Kalis et al 2014). However, recent evidence has implicated a role for LIN-39 in the expression of a VC marker srb-16 (Feng et al 2020).…”

Section: Introductionmentioning

confidence: 99%

The Conserved ASCL1/MASH-1 Ortholog HLH-3 Specifies Sex-Specific Ventral Cord Motor Neuron Fate inCaenorhabditis elegans

Perez¹,

Alfonso²

2020

G3 Genes|Genomes|Genetics

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Neural specification is regulated by one or many transcription factors that control expression of effector genes that mediate function and determine neuronal type. Here we identify a novel role for one conserved proneural factor, the bHLH protein HLH-3, implicated in the specification of sex-specific ventral cord motor neurons in Caenorhabditis elegans. Proneural genes act in early stages of neurogenesis in early progenitors, but here, we demonstrate a later role for hlh-3. First, we document that differentiation of the ventral cord type C motor neuron class (VC) within their neuron class, is dynamic in time and space. Expression of VC class-specific and subclass-specific identity genes is distinct through development and is dependent on the VC position along the A-P axis and their proximity to the vulva. Our characterization of the expression of VC class and VC subclass-specific differentiation markers in the absence of hlh-3 function reveals that VC fate specification, differentiation, and morphology requires hlh-3 function. Finally, we conclude that hlh-3 cell-autonomously specifies VC cell fate.

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Patterning of sexually dimorphic neurogenesis in the Caenorhabditis elegans ventral cord by Hox and TALE homeodomain transcription factors

Cited by 4 publications

References 57 publications

A Neurotransmitter Atlas of theCaenorhabditis elegansMale Nervous System Reveals Sexually Dimorphic Neurotransmitter Usage

A Neurotransmitter Atlas of theCaenorhabditis elegansMale Nervous System Reveals Sexually Dimorphic Neurotransmitter Usage

Sexual Dimorphism and Sex Differences in Caenorhabditis elegans Neuronal Development and Behavior

The Conserved ASCL1/MASH-1 Ortholog HLH-3 Specifies Sex-Specific Ventral Cord Motor Neuron Fate inCaenorhabditis elegans

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