Regulation of <i>Caenorhabditis elegans</i> Male Mate Searching Behavior by the Nuclear Receptor DAF-12

Kleemann, Gunnar; Liu, Jia; Emmons, Scott W.

doi:10.1534/genetics.108.093773

Cited by 18 publications

(18 citation statements)

References 46 publications

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“…Sexual maturation in many animal species is controlled by gonadal hormones (Avendano et al, 2017). In C. elegans, the gonad has been shown to be required for the establishment of sex-specific adult behaviors (Arantes-Oliveira et al, 2002;Fujiwara et al, 2016;Kleemann et al, 2008;Lipton et al, 2004). Therefore, we first examined whether signals from the germline or gonad may affect the AIM neurotransmitter switch.…”

Section: Effects Of the Heterochronic Lin-28/let-7/lin-41 Pathway On mentioning

confidence: 99%

Timing mechanism of sexually dimorphic nervous system differentiation

Pereira

Aeschimann

Wang

et al. 2018

Preprint

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In all animals, sexual differentiation of somatic tissue is precisely timed, yet the molecular mechanisms that control the timing of sexual differentiation, particularly in the brain, are poorly understood. We have used sexually dimorphic molecular, anatomical and behavioral features of the C. elegans nervous system to decipher a regulatory pathway that controls the precise timing of sexual differentiation. We find that the sexually dimorphic differentiation of postmitotic neurons in the male nervous system is abrogated in animals that carry a mutation in the miRNA let-7 and prematurely executed in animals either lacking the let-7 inhibitor lin-28, or the direct let-7 target lin-41, an RNA-binding, posttranscriptional regulator. We show that an isoform of a phylogenetically conserved transcription factor, lin-29a, is a critical target of LIN-41 in controlling sexual maturation of sex-shared neurons. lin-29a is expressed in a male-specific manner in a subset of sex-shared neurons at the onset of sexual maturation. lin-29a acts cell-autonomously in these neurons to control the expression of sexually dimorphic neurotransmitter switches, sensory receptor expression, neurite anatomy and connectivity, and locomotor behavior. lin-29a is not only required but also sufficient to impose male-specific features at earlier stages of development and in the opposite sex. The temporal, sexual and spatial specificity of lin-29a expression is controlled intersectionally through the lin-28/let-7/lin-41 heterochronic pathway, sex chromosome configuration and neuron type-specific terminal selector transcription factors. Two Doublesex-like transcription factors represent additional neuron-type specific targets of LIN-41 and are regulated in a similar intersectional manner, indicating the existence of modular outputs downstream of the heterochronic pathway. In conclusion, we have provided insights into the molecular logic of the timing of sexual differentiation in the C. elegans nervous system. Remarkably, the lin28/let7 axis also controls the timing of sexual differentiation in mice and humans thereby hinting toward a striking universality of the control mechanisms of sexual differentiation.

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Section: Effects Of the Heterochronic Lin-28/let-7/lin-41 Pathway On mentioning

confidence: 99%

Timing mechanism of sexually dimorphic nervous system differentiation

Pereira

Aeschimann

Wang

et al. 2018

Preprint

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“…A period of starvation also suppresses mate-searching behavior in the absence of mates. Internal signals that indicate the nutritional and reproductive status of the male are conveyed through an insulin-like signaling pathway and a steroid nuclear hormone receptor respectively 6,8 . External environmental cues, i.e.…”

Section: Introductionmentioning

confidence: 99%

PDF-1 neuropeptide signaling modulates a neural circuit for mate-searching behavior in C. elegans

et al. 2012

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Appetitive behaviors require complex decision-making, involving the integration of environmental stimuli and physiological needs. C. elegans mate searching is a male-specific exploratory behavior regulated by two competing needs: food versus reproductive appetite. Here we show that the Pigment Dispersing Factor Receptor (PDFR-1) modulates the circuit that encodes the male reproductive drive promoting male exploration upon mate-deprivation. PDFR-1 and its ligand PDF-1 stimulate mate searching in the male but not in the hermaphrodite. pdf-1 is required in the gender-shared interneuron AIM and the receptor acts in internal and external environment-sensing neurons of the shared nervous system (URY, PQR and PHA) to produce mate-searching behavior. Thus, the pdf-1/pdfr-1 pathway functions in non sex-specific neurons to produce a male-specific, goal-oriented exploratory behavior. Our results indicate that secretin neuropeptidergic signaling plays an ancient role in regulating motivational internal states.

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“…DAs are also required during larval development for proper gonadal migration (Gerisch et al 2001; Motola et al 2006) and expression of let-7 -family microRNAs that coordinate the timing of cell divisions (Bethke et al 2009; Hammell et al 2009). In adult males, DAs are required for normal mate searching behavior (Kleemann et al 2008). …”

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confidence: 99%

Influence of Steroid Hormone Signaling on Life Span Control byCaenorhabditis elegansInsulin-Like Signaling

Dumas

Guo

Shih

et al. 2013

G3 Genes|Genomes|Genetics

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Sterol-sensing nuclear receptors and insulin-like growth factor signaling play evolutionarily conserved roles in the control of aging. In the nematode Caenorhabditis elegans, bile acid-like steroid hormones known as dafachronic acids (DAs) influence longevity by binding to and regulating the activity of the conserved nuclear receptor DAF-12, and the insulin receptor (InsR) ortholog DAF-2 controls life span by inhibiting the FoxO transcription factor DAF-16. How the DA/DAF-12 pathway interacts with DAF-2/InsR signaling to control life span is poorly understood. Here we specifically investigated the roles of liganded and unliganded DAF-12 in life span control in the context of reduced DAF-2/InsR signaling. In animals with reduced daf-2/InsR activity, mutations that either reduce DA biosynthesis or fully abrogate DAF-12 activity shorten life span, suggesting that liganded DAF-12 promotes longevity. In animals with reduced DAF-2/InsR activity induced by daf-2/InsR RNAi, both liganded and unliganded DAF-12 promote longevity. However, in daf-2/InsR mutants, liganded and unliganded DAF-12 act in opposition to control life span. Thus, multiple DAF-12 activities influence life span in distinct ways in contexts of reduced DAF-2/InsR signaling. Our findings establish new roles for a conserved steroid signaling pathway in life span control and elucidate interactions among DA biosynthetic pathways, DAF-12, and DAF-2/InsR signaling in aging.

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Regulation of Caenorhabditis elegans Male Mate Searching Behavior by the Nuclear Receptor DAF-12

Cited by 18 publications

References 46 publications

Timing mechanism of sexually dimorphic nervous system differentiation

Timing mechanism of sexually dimorphic nervous system differentiation

PDF-1 neuropeptide signaling modulates a neural circuit for mate-searching behavior in C. elegans

Influence of Steroid Hormone Signaling on Life Span Control byCaenorhabditis elegansInsulin-Like Signaling

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