Literature DB >> 30988167

Sexually Dimorphic Regulation of Behavioral States by Dopamine in Caenorhabditis elegans.

Satoshi Suo1, Kazuki Harada2, Shogo Matsuda3, Koki Kyo4, Min Wang5, Kei Maruyama5, Takeo Awaji5, Takashi Tsuboi2,3.   

Abstract

Sex differences in behavior allow animals to effectively mate and reproduce. However, the mechanism by which biological sex regulates behavioral states, which underlie the regulation of sex-shared behaviors, such as locomotion, is largely unknown. In this study, we studied sex differences in the behavioral states of Caenorhabditis elegans and found that males spend less time in a low locomotor activity state than hermaphrodites and that dopamine generates this sex difference. In males, dopamine reduces the low activity state by acting in the same pathway as polycystic kidney disease-related genes that function in male-specific neurons. In hermaphrodites, dopamine increases the low activity state by suppression of octopamine signaling in the sex-shared SIA neurons, which have reduced responsiveness to octopamine in males. Furthermore, dopamine promotes exploration both inside and outside of bacterial lawn (the food source) in males and suppresses it in hermaphrodites. These results demonstrate that sexually dimorphic signaling allows the same neuromodulator to promote adaptive behavior for each sex.SIGNIFICANCE STATEMENT The mechanisms that generate sex differences in sex-shared behaviors, including locomotion, are not well understood. We show that there are sex differences in the regulation of behavioral states in the model animal Caenorhabditis elegans Dopamine promotes the high locomotor activity state in males, which must search for mates to reproduce, and suppresses it in self-fertilizing hermaphrodites through distinct molecular mechanisms. This study demonstrates that sex-specific signaling generates sex differences in the regulation of behavioral states, which in turn modulates the locomotor activity to suit reproduction for each sex.
Copyright © 2019 the authors.

Entities:  

Keywords:  C. elegans; behavioral state; dopamine; locomotion; neuromodulator; sex

Year:  2019        PMID: 30988167      PMCID: PMC6561698          DOI: 10.1523/JNEUROSCI.2985-18.2019

Source DB:  PubMed          Journal:  J Neurosci        ISSN: 0270-6474            Impact factor:   6.167


  61 in total

Review 1.  Octopamine in invertebrates.

Authors:  T Roeder
Journal:  Prog Neurobiol       Date:  1999-12       Impact factor: 11.685

2.  Genetic identification of neurons controlling a sexually dimorphic behaviour.

Authors:  S Gatti; J F Ferveur; J R Martin
Journal:  Curr Biol       Date:  2000-06-01       Impact factor: 10.834

3.  Evidence of a mate-finding cue in the hermaphrodite nematode Caenorhabditis elegans.

Authors:  Jasper M Simon; Paul W Sternberg
Journal:  Proc Natl Acad Sci U S A       Date:  2002-01-29       Impact factor: 11.205

4.  The Caenorhabditis elegans autosomal dominant polycystic kidney disease gene homologs lov-1 and pkd-2 act in the same pathway.

Authors:  M M Barr; J DeModena; D Braun; C Q Nguyen; D H Hall; P W Sternberg
Journal:  Curr Biol       Date:  2001-09-04       Impact factor: 10.834

5.  Identification of a dopamine receptor from Caenorhabditis elegans.

Authors:  Satoshi Suo; Noboru Sasagawa; Shoichi Ishiura
Journal:  Neurosci Lett       Date:  2002-02-08       Impact factor: 3.046

6.  Food and metabolic signalling defects in a Caenorhabditis elegans serotonin-synthesis mutant.

Authors:  J Y Sze; M Victor; C Loer; Y Shi; G Ruvkun
Journal:  Nature       Date:  2000-02-03       Impact factor: 49.962

7.  DAF-7/TGF-beta expression required for the normal larval development in C. elegans is controlled by a presumed guanylyl cyclase DAF-11.

Authors:  M Murakami; M Koga; Y Ohshima
Journal:  Mech Dev       Date:  2001-11       Impact factor: 1.882

8.  A polycystic kidney-disease gene homologue required for male mating behaviour in C. elegans.

Authors:  M M Barr; P W Sternberg
Journal:  Nature       Date:  1999-09-23       Impact factor: 49.962

9.  Patterning of dopaminergic neurotransmitter identity among Caenorhabditis elegans ray sensory neurons by a TGFbeta family signaling pathway and a Hox gene.

Authors:  R Lints; S W Emmons
Journal:  Development       Date:  1999-12       Impact factor: 6.868

10.  The homeodomain protein CePHOX2/CEH-17 controls antero-posterior axonal growth in C. elegans.

Authors:  N Pujol; P Torregrossa; J J Ewbank; J F Brunet
Journal:  Development       Date:  2000-08       Impact factor: 6.868

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  3 in total

Review 1.  Neuromodulators: an essential part of survival.

Authors:  Joy Alcedo; Veena Prahlad
Journal:  J Neurogenet       Date:  2020-11-10       Impact factor: 1.250

Review 2.  Neuropeptides and Behaviors: How Small Peptides Regulate Nervous System Function and Behavioral Outputs.

Authors:  Umer Saleem Bhat; Navneet Shahi; Siju Surendran; Kavita Babu
Journal:  Front Mol Neurosci       Date:  2021-12-02       Impact factor: 5.639

3.  Behavioral Differences between Male and Hermaphrodite C. elegans.

Authors:  Elizabeth Loxterkamp; Jaaram Cha; Katharine Wu; Janessa Sullivan; Olivia Holbrook; Hazar Ghaith; Lena Srun; Deborah E Bauer
Journal:  MicroPubl Biol       Date:  2021-07-30
  3 in total

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