Fruitless Recruits Two Antagonistic Chromatin Factors to Establish Single-Neuron Sexual Dimorphism

Ito, Hiroki; Sato, Kosei; Koganezawa, Masayuki; Oté, Manabu; Matsumoto, Ken; Hama, Chihiro; Yamamoto, Daisuke

doi:10.1016/j.cell.2012.04.025

Cited by 94 publications

(134 citation statements)

References 45 publications

(49 reference statements)

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“…In this attempt, we found that a null mutation in the bon gene suppresses the phenotypic effects of fru overexpression in the eye. 10,11 In our subsequent analysis, a bon null mutation was shown to exacerbate courtship behavior defects observed in male flies of fru hypomorphic mutants (fru 2 /fru sat ).…”

Section: Bon-dependent Association Of Fru With Two Chromatin Factorsmentioning

confidence: 91%

“…12,13 Our immunoprecipitation assays with Drosophila head extracts or S2 cell lysates showed that Bon mediates associations of Fru with HDAC1 or HP1a, which compete with each other for Bon. 11 Moreover, polytene chromosome immunostaining revealed that HDAC1 and HP1a colocalize with Fru at a number of Fru-binding chromosomal sites in a Bon-dependent manner.…”

mentioning

confidence: 99%

“…Our recent immunostaining of polytene chromosomes with an anti-FruCOM antibody that detects all isoforms of Fru revealed that Fru binds to approximately 130 distinct loci including five X-chromosomal bands: 1C, 2B, 3C, 3D and 3F. 11 The immunostaining with anti-HDAC and anti-HP1a antibodies indicated that HDAC1 binds to all five loci, while HP1a binds to only three: 3C, 3D and 3F. 11 Chip-seq analyses in the modENCODE project have shown that all five loci contain HDAC1-target regions, and that the 3C, 3D and 3F loci contain HP1a-target regions (www.…”

mentioning

confidence: 99%

“…11 The immunostaining with anti-HDAC and anti-HP1a antibodies indicated that HDAC1 binds to all five loci, while HP1a binds to only three: 3C, 3D and 3F. 11 Chip-seq analyses in the modENCODE project have shown that all five loci contain HDAC1-target regions, and that the 3C, 3D and 3F loci contain HP1a-target regions (www. modencode.org/).…”

mentioning

confidence: 99%

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Sex-switching of theDrosophilabrain by two antagonistic chromatin factors

Ito

Sato

Yamamoto

2013

Fly

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Section: Bon-dependent Association Of Fru With Two Chromatin Factorsmentioning

confidence: 91%

mentioning

confidence: 99%

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confidence: 99%

mentioning

confidence: 99%

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Sex-switching of theDrosophilabrain by two antagonistic chromatin factors

Ito

Sato

Yamamoto

2013

Fly

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“…Fru M appears to function in a complex with the transcription cofactor Bonus and either histone deacetylase 1 or heterochromatin protein 1a (14). Recent genome-wide screens of RNA expression levels or Fru M binding activity have identified potential Fru M targets, but have lacked independent confirmation of such regulation (15)(16)(17).…”

mentioning

confidence: 99%

Sex-specific regulation of Lgr3 in Drosophila neurons

Meissner

Luo

Dias

et al. 2016

Proc. Natl. Acad. Sci. U.S.A.

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The development of sexually dimorphic morphology and the potential for sexually dimorphic behavior in Drosophila are regulated by the Fruitless (Fru) and Doublesex (Dsx) transcription factors. Several direct targets of Dsx have been identified, but direct Fru targets have not been definitively identified. We show that Drosophila leucine-rich repeat G protein-coupled receptor 3 (Lgr3) is regulated by Fru and Dsx in separate populations of neurons. Lgr3 is a member of the relaxin-receptor family and a receptor for Dilp8, necessary for control of organ growth. Lgr3 expression in the anterior central brain of males is inhibited by the B isoform of Fru, whose DNA binding domain interacts with a short region of an Lgr3 intron. Fru A and C isoform mutants had no observed effect on Lgr3 expression. The female form of Dsx (Dsx F ) separately up-and down-regulates Lgr3 expression in distinct neurons in the abdominal ganglion through female-and male-specific Lgr3 enhancers. Excitation of neural activity in the Dsx F -up-regulated abdominal ganglion neurons inhibits female receptivity, indicating the importance of these neurons for sexual behavior. Coordinated regulation of Lgr3 by Fru and Dsx marks a point of convergence of the two branches of the sex-determination hierarchy.M ost animal species are comprised of female and male individuals, in which sex differences in form and behavior are specified by their genetic makeup. The developmental processes by which genes build sex-specific differences into the nervous system, and hence encode the potential for sex-specific behavior, have long been of interest (1).In Drosophila melanogaster the assessment of the number of X chromosomes leads to sex-differential splicing of transcripts from genes making up the sex-determination hierarchy, in particular the terminal genes of that hierarchy, fruitless (fru) and doublesex [dsx (2), reviewed in ref. 3]. fru and dsx encode sexspecific Zn-finger transcription factors that alter, either directly or indirectly, the expression of downstream genes to produce the sexually dimorphic elements of flies. The male-specific forms of Fru (Fru M ) act in a subset of the neurons within the male's nervous system to establish the potential for social interactions such as courtship behavior and aggression (reviewed in ref.3). In contrast, Dsx acts in subsets of both neural and nonneural tissues of males and females to regulate behavioral and nonbehavioral aspects of sexual development (reviewed in ref.3).Although the mechanisms regulating the production of the sexspecific isoforms of the Fru and Dsx proteins are well-established (4), how these proteins in turn function is only beginning to be elucidated. Several direct Dsx targets and a well-conserved 13-bp Dsx binding site have been identified (5-13). Many Dsx target genes encode well-known transcription factors and cell-cell signaling molecules that function sex-nonspecifically in most tissues in which they are expressed. However, in other tissues, Dsx directs the sexspecific expression of these gene...

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Chromatin regulators in neurodevelopment and disease: Analysis of fly neural circuits provides insights

Taniguchi

Moore

2014

BioEssays

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Disruptions in chromatin regulator genes are frequently the cause of neurodevelopmental and neuropsychiatric disorders. Chromatin regulators are widely expressed in the brain, yet symptoms suggest that specific circuits can be preferentially altered when they are mutated. Using Drosophila allows targeted manipulation of chromatin regulators in defined neuronal classes, lineages, or circuits, revealing their roles in neuronal precursor self-renewal, dendrite and axon targeting, neuron diversification, and the tuning of developmental signaling pathways. Phenotypes arising from chromatin regulator disruption are context dependent - defined by interaction networks between the regulators, transcription factors, and chromatin remodeling complex partners. Future challenges are to determine the complexity of partner interactions, and to ascertain the degree to which cognitive deficits are due to loss of chromatin regulator activity in building a circuit or in maintaining homeostasis and activity within it.

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Fruitless Recruits Two Antagonistic Chromatin Factors to Establish Single-Neuron Sexual Dimorphism

Cited by 94 publications

References 45 publications

Sex-switching of theDrosophilabrain by two antagonistic chromatin factors

Sex-switching of theDrosophilabrain by two antagonistic chromatin factors

Sex-specific regulation of Lgr3 in Drosophila neurons

Chromatin regulators in neurodevelopment and disease: Analysis of fly neural circuits provides insights

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