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

Barrios, Arantza; Ghosh, Rajarshi; Fang, C. H.; Emmons, Scott W.; Barr, Maureen M.

doi:10.1038/nn.3253

Cited by 114 publications

(147 citation statements)

References 48 publications

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“…3d). Notably, both odr-10 ON and AWA-feminized males continued to exhibit significant exploratory behavior, indicating that other male-specific exploratory drives [27, 28] likely act in parallel with AWA modulation. Together, these results demonstrate that AWA and odr-10 are important regulators of male behavioral prioritization.…”

Section: Resultsmentioning

confidence: 99%

“…While the reasons for this are unclear, this result might indicate that feminization disrupts other properties of AWA that are important for food detection in males. It also suggests that the sexual state of AWA acts in parallel with exploratory drives promoted by the male tail sensory rays and PDF neuropeptide signaling [27, 28] to determine the animal’s behavioral program.…”

Section: Resultsmentioning

confidence: 99%

“…This behavioral choice also depends on developmental stage (sexually immature larval males do not engage in mate-searching) and feeding status (transient starvation leads to the temporary re-prioritization of feeding over mate-searching behavior) [25]. While input from male-specific neurons and peptide signals are important for generating the male exploratory drive [27, 28], the neural effectors of the this feeding-vs.-exploration decision are unknown, as are the mechanisms by which multiple internal variables modulate this decision.…”

Section: Introductionmentioning

confidence: 99%

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Sex, Age, and Hunger Regulate Behavioral Prioritization through Dynamic Modulation of Chemoreceptor Expression

et al. 2014

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Background Adaptive behavioral prioritization requires flexible outputs from fixed neural circuits. In C. elegans, the prioritization of feeding vs. mate-searching depends on biological sex (males will abandon food to search for mates, while hermaphrodites will not) as well as developmental stage and feeding status. Previously, we found that males are less attracted than hermaphrodites to the food-associated odorant diacetyl, suggesting that sensory modulation may contribute to behavioral prioritization. Results We find that somatic sex acts cell-autonomously to reconfigure the olfactory circuit by regulating a key chemoreceptor, odr-10, in the AWA neurons. Moreover, we find that odr-10 has a significant role in food detection, the regulation of which contributes to sex differences in behavioral prioritization. Overexpression of odr-10 increases male food attraction and decreases off-food exploration; conversely, odr-10 loss impairs food taxis in both sexes. In larvae, both sexes prioritize feeding over exploration; correspondingly, the sexes have equal odr-10 expression and food attraction. Food deprivation, which transiently favors feeding over exploration in adult males, increases male food attraction by activating odr-10 expression. Furthermore, the weak expression of odr-10 in well-fed adult males has important adaptive value, allowing males to efficiently locate mates in a patchy food environment. Conclusions We find that modulated expression of a single chemoreceptor plays a key role in naturally occurring variation in the prioritization of feeding and exploration. The convergence of three independent regulatory inputs—somatic sex, age, and feeding status—on chemoreceptor expression highlights sensory function as a key source of plasticity in neural circuits.

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Section: Resultsmentioning

confidence: 99%

Section: Resultsmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Sex, Age, and Hunger Regulate Behavioral Prioritization through Dynamic Modulation of Chemoreceptor Expression

et al. 2014

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“…Genetic analysis of C. elegans male mating behavior identified two types of TM spanning receptors. The Secretin-like class 2 GPCR pigment dispersing factor receptor (PDFR)-1 modulates the neural circuit that promotes mate searching and male sex drive (Barrios et al, 2012).…”

Section: Animal Models To Discover and Validate Molecular Conceptsmentioning

confidence: 99%

Model Organisms in G Protein–Coupled Receptor Research

Langenhan

Barr

Bruchas

et al. 2015

Molecular Pharmacology

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The study of G protein-coupled receptors (GPCRs) has benefited greatly from experimental approaches that interrogate their functions in controlled, artificial environments. Working in vitro, GPCR receptorologists discovered the basic biologic mechanisms by which GPCRs operate, including their eponymous capacity to couple to G proteins; their molecular makeup, including the famed serpentine transmembrane unit; and ultimately, their three-dimensional structure. Although the insights gained from working outside the native environments of GPCRs have allowed for the collection of low-noise data, such approaches cannot directly address a receptor's native (in vivo) functions. An in vivo approach can complement the rigor of in vitro approaches: as studied in model organisms, it imposes physiologic constraints on receptor action and thus allows investigators to deduce the most salient features of receptor function. Here, we briefly discuss specific examples in which model organisms have successfully contributed to the elucidation of signals controlled through GPCRs and other surface receptor systems. We list recent examples that have served either in the initial discovery of GPCR signaling concepts or in their fuller definition. Furthermore, we selectively highlight experimental advantages, shortcomings, and tools of each model organism.

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“…Therefore, the male is motivated to search for mates (Barrios Review in this issue). In the absence of potential mates, males exhibit mate-searching behavior: males leave a food source, while hermaphrodites do not [17]. lov-1 and pkd-2 mutant males are defective in mate-searching behavior [18].…”

Section: Additional Mating Behaviors In C Elegans That Require the Pmentioning

confidence: 99%

Mating behavior, male sensory cilia, and polycystins in Caenorhabditis elegans

O’Hagan

Wang

Barr

2014

Seminars in Cell & Developmental Biology

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The investigation of C. elegans males and the male-specific sensory neurons required for mating behaviors has provided insight into the molecular function of polycystins and mechanisms that are needed for polycystin ciliary localization. In humans, polycystin 1 and polycystin 2 are needed for kidney function; loss of polycystin function leads to autosomal dominant polycystic kidney disease (ADPKD). Polycystins localize to cilia in C. elegans and mammals, a finding that has guided research into ADPKD. The discovery that the polycystins form ciliary receptors in male-specific neurons needed for mating behaviors has also helped to unlock insights into two additional exciting new areas: the secretion of extracellular vesicles; and mechanisms of ciliary specialization. First, we will summarize the studies done in C. elegans regarding the expression, localization, and function of the polycystin 1 and 2 homologs, LOV-1 and PKD-2, and discuss insights gained from this basic research. Molecules that are co-expressed with the polycystins in the male-specific neurons may identify evolutionarily conserved molecular mechanisms for polycystin function and localization. We will discuss the finding that polycystins are secreted in extracellular vesicles that evoke behavioral change in males, suggesting that such vesicles provide a novel form of communication to conspecifics in the environment. In humans, polycystin-containing extracellular vesicles are secreted in urine and can be taken up by cilia, and quickly internalized. Therefore, communication by polycystin-containing extracellular vesicles may also use mechanisms that are evolutionarily conserved from nematode to human. Lastly, different cilia display structural and functional differences that specialize them for particular tasks, despite the fact that virtually all cilia are built by a conserved Intraflagellar Transport (IFT) mechanism and share some basic structural features. Comparative analysis of the male-specific cilia with the well-studied cilia of the amphid and phasmid neurons has allowed identification of molecules that specialize the male cilia. We will discuss the molecules that shape the male-specific cilia. The cell biology of cilia in male-specific neurons demonstrates that C. elegans can provide an excellent model of ciliary specialization.

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

Cited by 114 publications

References 48 publications

Sex, Age, and Hunger Regulate Behavioral Prioritization through Dynamic Modulation of Chemoreceptor Expression

Sex, Age, and Hunger Regulate Behavioral Prioritization through Dynamic Modulation of Chemoreceptor Expression

Model Organisms in G Protein–Coupled Receptor Research

Mating behavior, male sensory cilia, and polycystins in Caenorhabditis elegans

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