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Functional New World monkey oxytocin forms elicit an altered signaling profile and promotes parental care in rats.

ABSTRACT: The neurohormone oxytocin is a key player in the modulation of reproductive and social behavioral traits, such as parental care. Recently, a correlation between different forms of oxytocin and behavioral phenotypes has been described in the New World Monkeys (NWMs). Here, we demonstrate that, compared with the Leu⁸OXT found in most placental mammals, the Cebidae Pro⁸OXT and Saguinus Val³Pro⁸OXT taxon-specific variants act as equi-efficacious agonists for the G_q-dependent pathway but are weaker agonists for the β-arrestin engagement and subsequent endocytosis toward the oxytocin receptor (OXTR). Upon interaction with the AVPR1a, Pro⁸OXT and the common Leu⁸OXT yielded similar signaling profiles, being equally efficacious on G_q and β-arrestin, while Val³Pro⁸OXT showed reduced relative efficacy toward β-arrestin. Intranasal treatment with either of the variants increased maternal behavior and also promoted unusual paternal care in rats, as measured by pup-retrieval tests. We therefore suggest that Val³Pro⁸OXT and Pro⁸OXT are functional variants, which might have been evolutionarily co-opted as an essential part of the adaptive genetic repertoire that allowed the emergence of taxon-specific complex social behaviors, such as intense parental care in the Cebidae and the genus Saguinus.

SUBMITTER: Parreiras-E-Silva LT

PROVIDER: S-EPMC5576844 | biostudies-literature | 2017 Aug

REPOSITORIES: biostudies-literature

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Functional New World monkey oxytocin forms elicit an altered signaling profile and promotes parental care in rats.

Parreiras-E-Silva Lucas T LT Vargas-Pinilla Pedro P Duarte Diego A DA Longo Dânae D Espinoza Pardo Grace Violeta GV Dulor Finkler Andrea A Paixão-Côrtes Vanessa Rodrigues VR Paré Pâmela P Rovaris Diego L DL Oliveira Eduardo B EB Caceres Rafael Andrade RA Gonçalves Gislene L GL Bouvier Michel M Salzano Francisco M FM Lucion Aldo B AB Costa-Neto Claudio M CM Bortolini Maria Cátira MC

Proceedings of the National Academy of Sciences of the United States of America 20170807 34

The neurohormone oxytocin is a key player in the modulation of reproductive and social behavioral traits, such as parental care. Recently, a correlation between different forms of oxytocin and behavioral phenotypes has been described in the New World Monkeys (NWMs). Here, we demonstrate that, compared with the Leu8OXT found in most placental mammals, the Cebidae Pro8OXT and Saguinus Val3Pro8OXT taxon-specific variants act as equi-efficacious ago ...[more]

PMID: 28784762

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Project description:Oxytocin (OT) has an important role in bond formation and social reciprocity, and animal studies indicate that OT functioning is transferred from parent to child through patterns of parental care. Perspectives on attachment suggest that the individual's various attachment bonds are underpinned by the oxytocinergic system. However, prospective human studies that demonstrate the cross-generation transfer of OT as mediated by early caregiving and its impact on children's multiple attachments are lacking. To address these concerns, the current study included 160 mothers and fathers and their firstborn child who participated in a 3-year longitudinal study. At the first and sixth postpartum months, parents' plasma OT was assayed, parent-infant interactions were videotaped and micro-coded, and allelic variations on the OXTR(rs2254298, rs1042778) and CD38rs3796863 genes were measured. At 3 years, parents' and child's salivary OT was assessed and children's social reciprocity observed during interactions with mother, father, and their first best friend. Parents' OT levels were individually stable across the 3-year period, correlated with low-risk OXTR and CD38 alleles, and predicted child OT. Child's social reciprocity with friend was associated with child OT levels, mother's OT-related genes and hormones, and mother-child reciprocity, but not with father's genes, hormones, or behavior. A cross-generation gene-by-environment effect emerged, with low child OT levels predicted by the interaction of maternal high-risk CD38 allele and diminished maternal care in infancy. These results demonstrate individual stability in peripheral OT across several years and describe a cross-generation transfer of OT through caregiving in humans within a prospective longitudinal design. Consistent with other mammals, biobehavioral experiences within the parent-infant bond shape children's affiliative biology and social behavior across multiple attachments. Our findings bear important implications for conditions involving disruptions to maternal-infant bonding and underscore the potential for peer-based interventions.

Dataset Information

Functional New World monkey oxytocin forms elicit an altered signaling profile and promotes parental care in rats.

Publications

Functional New World monkey oxytocin forms elicit an altered signaling profile and promotes parental care in rats.

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