Maternal care boosted by paternal imprinting in mammals.
In mammals, mothers are the primary caregiver, programmed, in part, by hormones produced during pregnancy. High-quality maternal care is essential for the survival and lifelong health of offspring. We previously showed that the paternally silenced imprinted gene pleckstrin homology-like domain famil...
| Main Authors: | , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Public Library of Science (PLoS)
2018-07-01
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| Series: | PLoS Biology |
| Online Access: | https://doi.org/10.1371/journal.pbio.2006599 |
| _version_ | 1819289741995016192 |
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| author | H D J Creeth G I McNamara S J Tunster R Boque-Sastre B Allen L Sumption J B Eddy A R Isles R M John |
| author_facet | H D J Creeth G I McNamara S J Tunster R Boque-Sastre B Allen L Sumption J B Eddy A R Isles R M John |
| author_sort | H D J Creeth |
| collection | DOAJ |
| description | In mammals, mothers are the primary caregiver, programmed, in part, by hormones produced during pregnancy. High-quality maternal care is essential for the survival and lifelong health of offspring. We previously showed that the paternally silenced imprinted gene pleckstrin homology-like domain family A member 2 (Phlda2) functions to negatively regulate a single lineage in the mouse placenta called the spongiotrophoblast, a major source of hormones in pregnancy. Consequently, the offspring's Phlda2 gene dosage may influence the quality of care provided by the mother. Here, we show that wild-type (WT) female mice exposed to offspring with three different doses of the maternally expressed Phlda2 gene-two active alleles, one active allele (the extant state), and loss of function-show changes in the maternal hypothalamus and hippocampus during pregnancy, regions important for maternal-care behaviour. After birth, WT dams exposed in utero to offspring with the highest Phlda2 dose exhibit decreased nursing and grooming of pups and increased focus on nest building. Conversely, 'paternalised' dams, exposed to the lowest Phlda2 dose, showed increased nurturing of their pups, increased self-directed behaviour, and a decreased focus on nest building, behaviour that was robustly maintained in the absence of genetically modified pups. This work raises the intriguing possibility that imprinting of Phlda2 contributed to increased maternal care during the evolution of mammals. |
| first_indexed | 2024-12-24T03:11:41Z |
| format | Article |
| id | doaj.art-21db42a2146a49fb95759af3e030476e |
| institution | Directory Open Access Journal |
| issn | 1544-9173 1545-7885 |
| language | English |
| last_indexed | 2024-12-24T03:11:41Z |
| publishDate | 2018-07-01 |
| publisher | Public Library of Science (PLoS) |
| record_format | Article |
| series | PLoS Biology |
| spelling | doaj.art-21db42a2146a49fb95759af3e030476e2022-12-21T17:17:46ZengPublic Library of Science (PLoS)PLoS Biology1544-91731545-78852018-07-01167e200659910.1371/journal.pbio.2006599Maternal care boosted by paternal imprinting in mammals.H D J CreethG I McNamaraS J TunsterR Boque-SastreB AllenL SumptionJ B EddyA R IslesR M JohnIn mammals, mothers are the primary caregiver, programmed, in part, by hormones produced during pregnancy. High-quality maternal care is essential for the survival and lifelong health of offspring. We previously showed that the paternally silenced imprinted gene pleckstrin homology-like domain family A member 2 (Phlda2) functions to negatively regulate a single lineage in the mouse placenta called the spongiotrophoblast, a major source of hormones in pregnancy. Consequently, the offspring's Phlda2 gene dosage may influence the quality of care provided by the mother. Here, we show that wild-type (WT) female mice exposed to offspring with three different doses of the maternally expressed Phlda2 gene-two active alleles, one active allele (the extant state), and loss of function-show changes in the maternal hypothalamus and hippocampus during pregnancy, regions important for maternal-care behaviour. After birth, WT dams exposed in utero to offspring with the highest Phlda2 dose exhibit decreased nursing and grooming of pups and increased focus on nest building. Conversely, 'paternalised' dams, exposed to the lowest Phlda2 dose, showed increased nurturing of their pups, increased self-directed behaviour, and a decreased focus on nest building, behaviour that was robustly maintained in the absence of genetically modified pups. This work raises the intriguing possibility that imprinting of Phlda2 contributed to increased maternal care during the evolution of mammals.https://doi.org/10.1371/journal.pbio.2006599 |
| spellingShingle | H D J Creeth G I McNamara S J Tunster R Boque-Sastre B Allen L Sumption J B Eddy A R Isles R M John Maternal care boosted by paternal imprinting in mammals. PLoS Biology |
| title | Maternal care boosted by paternal imprinting in mammals. |
| title_full | Maternal care boosted by paternal imprinting in mammals. |
| title_fullStr | Maternal care boosted by paternal imprinting in mammals. |
| title_full_unstemmed | Maternal care boosted by paternal imprinting in mammals. |
| title_short | Maternal care boosted by paternal imprinting in mammals. |
| title_sort | maternal care boosted by paternal imprinting in mammals |
| url | https://doi.org/10.1371/journal.pbio.2006599 |
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