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Curr Biol. 2017 Jan 23;27(2):199-209. doi: 10.1016/j.cub.2016.11.045. Epub 2017 Jan 5.

Sexually Dimorphic Differentiation of a C. elegans Hub Neuron Is Cell Autonomously Controlled by a Conserved Transcription Factor.

Author information

1
Department of Biological Sciences, Columbia University, Howard Hughes Medical Institute, New York, NY 10027, USA. Electronic address: es2754@columbia.edu.
2
Department of Biological Sciences, Columbia University, Howard Hughes Medical Institute, New York, NY 10027, USA.
3
Department of Biological Sciences, Columbia University, Howard Hughes Medical Institute, New York, NY 10027, USA. Electronic address: or38@columbia.edu.

Abstract

Functional and anatomical sexual dimorphisms in the brain are either the result of cells that are generated only in one sex or a manifestation of sex-specific differentiation of neurons present in both sexes. The PHC neuron pair of the nematode C. elegans differentiates in a strikingly sex-specific manner. In hermaphrodites the PHC neurons display a canonical pattern of synaptic connectivity similar to that of other sensory neurons, but in males PHC differentiates into a densely connected hub sensory neuron/interneuron, integrating a large number of male-specific synaptic inputs and conveying them to both male-specific and sex-shared circuitry. We show that the differentiation into such a hub neuron involves the sex-specific scaling of several components of the synaptic vesicle machinery, including the vesicular glutamate transporter eat-4/VGLUT, induction of neuropeptide expression, changes in axonal projection morphology, and a switch in neuronal function. We demonstrate that these molecular and anatomical remodeling events are controlled cell autonomously by the phylogenetically conserved Doublesex homolog dmd-3, which is both required and sufficient for sex-specific PHC differentiation. Cellular specificity of dmd-3 action is ensured by its collaboration with non-sex-specific terminal selector-type transcription factors, whereas the sex specificity of dmd-3 action is ensured by the hermaphrodite-specific transcriptional master regulator of hermaphroditic cell identity tra-1, which represses the transcription of dmd-3 in hermaphrodite PHC. Taken together, our studies provide mechanistic insights into how neurons are specified in a sexually dimorphic manner.

PMID:
28065609
PMCID:
PMC5805387
DOI:
10.1016/j.cub.2016.11.045
[Indexed for MEDLINE]
Free PMC Article

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