The parenting hub of the hypothalamus is a focus of imprinted gene action

Imprinted genes are subject to germline epigenetic modification resulting in parental-specific allelic silencing. Although genomic imprinting is thought to be important for maternal behaviour, this idea is based on serendipitous findings from a small number of imprinted genes. Here, we undertook an...

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Published inPLoS genetics Vol. 19; no. 10; p. e1010961
Main Authors Higgs, Matthew J., Webberley, Anna E., Allan, Alasdair J., Talat, Moaz, John, Rosalind M., Isles, Anthony R.
Format Journal Article
LanguageEnglish
Published United States Public Library of Science 19.10.2023
Public Library of Science (PLoS)
Subjects
Analysis
Animals
Antigens, Neoplasm - genetics
Behavior
Biology and Life Sciences
Brain
c-Fos protein
Datasets
Epigenetic inheritance
Epigenetics
Female
Galanin
Galanin - genetics
Galanin - metabolism
Gene expression
Genes
Genetic aspects
Genomic imprinting
Genomic Imprinting - genetics
Growth
Hypothalamus
Hypothalamus - metabolism
Maternal behavior
Medicine and Health Sciences
Mice
Mothers
Nest building
Neurons
Neuropeptides
Parental behavior
Parenting
Phenotype
Physiology
Preoptic area
Proteins - genetics
RNA
RNA sequencing
Social Sciences
United Kingdom
Online AccessGet full text
ISSN1553-7404
1553-7390
1553-7404
DOI10.1371/journal.pgen.1010961

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Abstract Imprinted genes are subject to germline epigenetic modification resulting in parental-specific allelic silencing. Although genomic imprinting is thought to be important for maternal behaviour, this idea is based on serendipitous findings from a small number of imprinted genes. Here, we undertook an unbiased systems biology approach, taking advantage of the recent delineation of specific neuronal populations responsible for controlling parental care, to test whether imprinted genes significantly converge to regulate parenting behaviour. Using single-cell RNA sequencing datasets, we identified a specific enrichment of imprinted gene expression in a recognised “parenting hub”, the galanin-expressing neurons of the preoptic area. We tested the validity of linking enriched expression in these neurons to function by focusing on MAGE family member L2 (Magel2) , an imprinted gene not previously linked to parenting behaviour. We confirmed expression of Magel2 in the preoptic area galanin expressing neurons. We then examined the parenting behaviour of Magel2 -null (+/p) mice. Magel 2-null mothers, fathers and virgin females demonstrated deficits in pup retrieval, nest building and pup-directed motivation, identifying a central role for this gene in parenting. Finally, we show that Magel2- null mothers and fathers have a significant reduction in POA galanin expressing cells, which in turn contributes to a reduced c-Fos response in the POA upon exposure to pups. Our findings identify a novel imprinted gene that impacts parenting behaviour and, moreover, demonstrates the utility of using single-cell RNA sequencing data to predict gene function from expression and in doing so here, have identified a purposeful role for genomic imprinting in mediating parental behaviour.
AbstractList Imprinted genes are subject to germline epigenetic modification resulting in parental-specific allelic silencing. Although genomic imprinting is thought to be important for maternal behaviour, this idea is based on serendipitous findings from a small number of imprinted genes. Here, we undertook an unbiased systems biology approach, taking advantage of the recent delineation of specific neuronal populations responsible for controlling parental care, to test whether imprinted genes significantly converge to regulate parenting behaviour. Using single-cell RNA sequencing datasets, we identified a specific enrichment of imprinted gene expression in a recognised "parenting hub", the galanin-expressing neurons of the preoptic area. We tested the validity of linking enriched expression in these neurons to function by focusing on MAGE family member L2 (Magel2), an imprinted gene not previously linked to parenting behaviour. We confirmed expression of Magel2 in the preoptic area galanin expressing neurons. We then examined the parenting behaviour of Magel2-null.sup.(+/p) mice. Magel2-null mothers, fathers and virgin females demonstrated deficits in pup retrieval, nest building and pup-directed motivation, identifying a central role for this gene in parenting. Finally, we show that Magel2-null mothers and fathers have a significant reduction in POA galanin expressing cells, which in turn contributes to a reduced c-Fos response in the POA upon exposure to pups. Our findings identify a novel imprinted gene that impacts parenting behaviour and, moreover, demonstrates the utility of using single-cell RNA sequencing data to predict gene function from expression and in doing so here, have identified a purposeful role for genomic imprinting in mediating parental behaviour.
Imprinted genes are subject to germline epigenetic modification resulting in parental-specific allelic silencing. Although genomic imprinting is thought to be important for maternal behaviour, this idea is based on serendipitous findings from a small number of imprinted genes. Here, we undertook an unbiased systems biology approach, taking advantage of the recent delineation of specific neuronal populations responsible for controlling parental care, to test whether imprinted genes significantly converge to regulate parenting behaviour. Using single-cell RNA sequencing datasets, we identified a specific enrichment of imprinted gene expression in a recognised "parenting hub", the galanin-expressing neurons of the preoptic area. We tested the validity of linking enriched expression in these neurons to function by focusing on MAGE family member L2 (Magel2), an imprinted gene not previously linked to parenting behaviour. We confirmed expression of Magel2 in the preoptic area galanin expressing neurons. We then examined the parenting behaviour of Magel2-null(+/p) mice. Magel2-null mothers, fathers and virgin females demonstrated deficits in pup retrieval, nest building and pup-directed motivation, identifying a central role for this gene in parenting. Finally, we show that Magel2-null mothers and fathers have a significant reduction in POA galanin expressing cells, which in turn contributes to a reduced c-Fos response in the POA upon exposure to pups. Our findings identify a novel imprinted gene that impacts parenting behaviour and, moreover, demonstrates the utility of using single-cell RNA sequencing data to predict gene function from expression and in doing so here, have identified a purposeful role for genomic imprinting in mediating parental behaviour.Imprinted genes are subject to germline epigenetic modification resulting in parental-specific allelic silencing. Although genomic imprinting is thought to be important for maternal behaviour, this idea is based on serendipitous findings from a small number of imprinted genes. Here, we undertook an unbiased systems biology approach, taking advantage of the recent delineation of specific neuronal populations responsible for controlling parental care, to test whether imprinted genes significantly converge to regulate parenting behaviour. Using single-cell RNA sequencing datasets, we identified a specific enrichment of imprinted gene expression in a recognised "parenting hub", the galanin-expressing neurons of the preoptic area. We tested the validity of linking enriched expression in these neurons to function by focusing on MAGE family member L2 (Magel2), an imprinted gene not previously linked to parenting behaviour. We confirmed expression of Magel2 in the preoptic area galanin expressing neurons. We then examined the parenting behaviour of Magel2-null(+/p) mice. Magel2-null mothers, fathers and virgin females demonstrated deficits in pup retrieval, nest building and pup-directed motivation, identifying a central role for this gene in parenting. Finally, we show that Magel2-null mothers and fathers have a significant reduction in POA galanin expressing cells, which in turn contributes to a reduced c-Fos response in the POA upon exposure to pups. Our findings identify a novel imprinted gene that impacts parenting behaviour and, moreover, demonstrates the utility of using single-cell RNA sequencing data to predict gene function from expression and in doing so here, have identified a purposeful role for genomic imprinting in mediating parental behaviour.
Imprinted genes are subject to germline epigenetic modification resulting in parental-specific allelic silencing. Although genomic imprinting is thought to be important for maternal behaviour, this idea is based on serendipitous findings from a small number of imprinted genes. Here, we undertook an unbiased systems biology approach, taking advantage of the recent delineation of specific neuronal populations responsible for controlling parental care, to test whether imprinted genes significantly converge to regulate parenting behaviour. Using single-cell RNA sequencing datasets, we identified a specific enrichment of imprinted gene expression in a recognised “parenting hub”, the galanin-expressing neurons of the preoptic area. We tested the validity of linking enriched expression in these neurons to function by focusing on MAGE family member L2 (Magel2) , an imprinted gene not previously linked to parenting behaviour. We confirmed expression of Magel2 in the preoptic area galanin expressing neurons. We then examined the parenting behaviour of Magel2 -null (+/p) mice. Magel 2-null mothers, fathers and virgin females demonstrated deficits in pup retrieval, nest building and pup-directed motivation, identifying a central role for this gene in parenting. Finally, we show that Magel2- null mothers and fathers have a significant reduction in POA galanin expressing cells, which in turn contributes to a reduced c-Fos response in the POA upon exposure to pups. Our findings identify a novel imprinted gene that impacts parenting behaviour and, moreover, demonstrates the utility of using single-cell RNA sequencing data to predict gene function from expression and in doing so here, have identified a purposeful role for genomic imprinting in mediating parental behaviour.
Imprinted genes are subject to germline epigenetic modification resulting in parental-specific allelic silencing. Although genomic imprinting is thought to be important for maternal behaviour, this idea is based on serendipitous findings from a small number of imprinted genes. Here, we undertook an unbiased systems biology approach, taking advantage of the recent delineation of specific neuronal populations responsible for controlling parental care, to test whether imprinted genes significantly converge to regulate parenting behaviour. Using single-cell RNA sequencing datasets, we identified a specific enrichment of imprinted gene expression in a recognised “parenting hub”, the galanin-expressing neurons of the preoptic area. We tested the validity of linking enriched expression in these neurons to function by focusing on MAGE family member L2 (Magel2), an imprinted gene not previously linked to parenting behaviour. We confirmed expression of Magel2 in the preoptic area galanin expressing neurons. We then examined the parenting behaviour of Magel2-null(+/p) mice. Magel2-null mothers, fathers and virgin females demonstrated deficits in pup retrieval, nest building and pup-directed motivation, identifying a central role for this gene in parenting. Finally, we show that Magel2-null mothers and fathers have a significant reduction in POA galanin expressing cells, which in turn contributes to a reduced c-Fos response in the POA upon exposure to pups. Our findings identify a novel imprinted gene that impacts parenting behaviour and, moreover, demonstrates the utility of using single-cell RNA sequencing data to predict gene function from expression and in doing so here, have identified a purposeful role for genomic imprinting in mediating parental behaviour.
Imprinted genes are subject to germline epigenetic modification resulting in parental-specific allelic silencing. Although genomic imprinting is thought to be important for maternal behaviour, this idea is based on serendipitous findings from a small number of imprinted genes. Here, we undertook an unbiased systems biology approach, taking advantage of the recent delineation of specific neuronal populations responsible for controlling parental care, to test whether imprinted genes significantly converge to regulate parenting behaviour. Using single-cell RNA sequencing datasets, we identified a specific enrichment of imprinted gene expression in a recognised “parenting hub”, the galanin-expressing neurons of the preoptic area. We tested the validity of linking enriched expression in these neurons to function by focusing on MAGE family member L2 (Magel2) , an imprinted gene not previously linked to parenting behaviour. We confirmed expression of Magel2 in the preoptic area galanin expressing neurons. We then examined the parenting behaviour of Magel2 -null (+/p) mice. Magel 2-null mothers, fathers and virgin females demonstrated deficits in pup retrieval, nest building and pup-directed motivation, identifying a central role for this gene in parenting. Finally, we show that Magel2- null mothers and fathers have a significant reduction in POA galanin expressing cells, which in turn contributes to a reduced c-Fos response in the POA upon exposure to pups. Our findings identify a novel imprinted gene that impacts parenting behaviour and, moreover, demonstrates the utility of using single-cell RNA sequencing data to predict gene function from expression and in doing so here, have identified a purposeful role for genomic imprinting in mediating parental behaviour. Genomic imprinting is a fascinating phenomenon that affects a small sub-group of the approximately 22,000 found in mammals. Unlike most genes that are equally expressed from both inherited parental copies (or alleles), so called imprinted genes are only expressed from one inherited allele, and this is usually fixed so that some imprinted genes are only active from the maternal copy, whereas others are only active from the paternal copy. This silencing of one of the parental copies makes genomic imprinting and evolutionary conundrum and the best way to understand why imprinted genes exist is to investigate the physiologies upon which they impact. Here we investigated imprinted gene expression in the brain circuitry that controls parental behaviours in mammals. We show that as a group the imprinted genes are disproportionately represented in the gene expression profile of the key neurons in this circuitry. We then tested this approach by showing that loss expression of a gene called Magel2 that was one of those imprinted genes identified in this brain circuitry, leads to deficits in parental behaviour in mice. Taken together with previous work, our findings indicate that genomic imprinting plays a particularly important role in the control of parenting behaviour.
Audience Academic
Author John, Rosalind M.
Higgs, Matthew J.
Allan, Alasdair J.
Talat, Moaz
Webberley, Anna E.
Isles, Anthony R.
AuthorAffiliation 1 Behavioural Genetics Group, Centre for Neuropsychiatric, Genetics and Genomics, Neuroscience and Mental Health Innovation Institute, Cardiff University, Cardiff, United Kingdom
2 The Mary Lyon Centre, MRC Harwell, Didcot, United Kingdom
3 School of Biosciences, Cardiff University, Cardiff, United Kingdom
University of Pennsylvania, UNITED STATES
AuthorAffiliation_xml – name: 3 School of Biosciences, Cardiff University, Cardiff, United Kingdom
– name: 2 The Mary Lyon Centre, MRC Harwell, Didcot, United Kingdom
– name: University of Pennsylvania, UNITED STATES
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License Copyright: © 2023 Higgs et al. This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.
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The authors have declared that no competing interests exist.
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0000-0002-7587-5712
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Snippet Imprinted genes are subject to germline epigenetic modification resulting in parental-specific allelic silencing. Although genomic imprinting is thought to be...
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StartPage e1010961
SubjectTerms Analysis
Animals
Antigens, Neoplasm - genetics
Behavior
Biology and Life Sciences
Brain
c-Fos protein
Datasets
Epigenetic inheritance
Epigenetics
Female
Galanin
Galanin - genetics
Galanin - metabolism
Gene expression
Genes
Genetic aspects
Genomic imprinting
Genomic Imprinting - genetics
Growth
Hypothalamus
Hypothalamus - metabolism
Maternal behavior
Medicine and Health Sciences
Mice
Mothers
Nest building
Neurons
Neuropeptides
Parental behavior
Parenting
Phenotype
Physiology
Preoptic area
Proteins - genetics
RNA
RNA sequencing
Social Sciences
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Title The parenting hub of the hypothalamus is a focus of imprinted gene action
URI https://www.ncbi.nlm.nih.gov/pubmed/37856383
https://www.proquest.com/docview/3069179642
https://www.proquest.com/docview/2880095980
https://pubmed.ncbi.nlm.nih.gov/PMC10586610
https://doaj.org/article/1f2126a47df8452f857b46edee61ac03
http://dx.doi.org/10.1371/journal.pgen.1010961
Volume 19
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