Maternal melatonin programs the daily pattern of energy metabolism in adult offspring.

<h4>Background</h4>Shift work was recently described as a factor that increases the risk of Type 2 diabetes mellitus. In addition, rats born to mothers subjected to a phase shift throughout pregnancy are glucose intolerant. However, the mechanism by which a phase shift transmits metaboli...

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Autores principales: Danilo S Ferreira, Fernanda G Amaral, Caroline C Mesquita, Ana Paula L Barbosa, Camilo Lellis-Santos, Ariane O Turati, Laila R Santos, Carolina S Sollon, Patricia R Gomes, Juliana A Faria, José Cipolla-Neto, Silvana Bordin, Gabriel F Anhê
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Publicado: Public Library of Science (PLoS) 2012
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spelling oai:doaj.org-article:8ee39f7afc544238a15d9490caaeb68c2021-11-18T07:15:42ZMaternal melatonin programs the daily pattern of energy metabolism in adult offspring.1932-620310.1371/journal.pone.0038795https://doaj.org/article/8ee39f7afc544238a15d9490caaeb68c2012-01-01T00:00:00Zhttps://www.ncbi.nlm.nih.gov/pmc/articles/pmid/22719949/?tool=EBIhttps://doaj.org/toc/1932-6203<h4>Background</h4>Shift work was recently described as a factor that increases the risk of Type 2 diabetes mellitus. In addition, rats born to mothers subjected to a phase shift throughout pregnancy are glucose intolerant. However, the mechanism by which a phase shift transmits metabolic information to the offspring has not been determined. Among several endocrine secretions, phase shifts in the light/dark cycle were described as altering the circadian profile of melatonin production by the pineal gland. The present study addresses the importance of maternal melatonin for the metabolic programming of the offspring.<h4>Methodology/principal findings</h4>Female Wistar rats were submitted to SHAM surgery or pinealectomy (PINX). The PINX rats were divided into two groups and received either melatonin (PM) or vehicle. The SHAM, the PINX vehicle and the PM females were housed with male Wistar rats. Rats were allowed to mate and after weaning, the male and female offspring were subjected to a glucose tolerance test (GTT), a pyruvate tolerance test (PTT) and an insulin tolerance test (ITT). Pancreatic islets were isolated for insulin secretion, and insulin signaling was assessed in the liver and in the skeletal muscle by western blots. We found that male and female rats born to PINX mothers display glucose intolerance at the end of the light phase of the light/dark cycle, but not at the beginning. We further demonstrate that impaired glucose-stimulated insulin secretion and hepatic insulin resistance are mechanisms that may contribute to glucose intolerance in the offspring of PINX mothers. The metabolic programming described here occurs due to an absence of maternal melatonin because the offspring born to PINX mothers treated with melatonin were not glucose intolerant.<h4>Conclusions/significance</h4>The present results support the novel concept that maternal melatonin is responsible for the programming of the daily pattern of energy metabolism in their offspring.Danilo S FerreiraFernanda G AmaralCaroline C MesquitaAna Paula L BarbosaCamilo Lellis-SantosAriane O TuratiLaila R SantosCarolina S SollonPatricia R GomesJuliana A FariaJosé Cipolla-NetoSilvana BordinGabriel F AnhêPublic Library of Science (PLoS)articleMedicineRScienceQENPLoS ONE, Vol 7, Iss 6, p e38795 (2012)
institution DOAJ
collection DOAJ
language EN
topic Medicine
R
Science
Q
spellingShingle Medicine
R
Science
Q
Danilo S Ferreira
Fernanda G Amaral
Caroline C Mesquita
Ana Paula L Barbosa
Camilo Lellis-Santos
Ariane O Turati
Laila R Santos
Carolina S Sollon
Patricia R Gomes
Juliana A Faria
José Cipolla-Neto
Silvana Bordin
Gabriel F Anhê
Maternal melatonin programs the daily pattern of energy metabolism in adult offspring.
description <h4>Background</h4>Shift work was recently described as a factor that increases the risk of Type 2 diabetes mellitus. In addition, rats born to mothers subjected to a phase shift throughout pregnancy are glucose intolerant. However, the mechanism by which a phase shift transmits metabolic information to the offspring has not been determined. Among several endocrine secretions, phase shifts in the light/dark cycle were described as altering the circadian profile of melatonin production by the pineal gland. The present study addresses the importance of maternal melatonin for the metabolic programming of the offspring.<h4>Methodology/principal findings</h4>Female Wistar rats were submitted to SHAM surgery or pinealectomy (PINX). The PINX rats were divided into two groups and received either melatonin (PM) or vehicle. The SHAM, the PINX vehicle and the PM females were housed with male Wistar rats. Rats were allowed to mate and after weaning, the male and female offspring were subjected to a glucose tolerance test (GTT), a pyruvate tolerance test (PTT) and an insulin tolerance test (ITT). Pancreatic islets were isolated for insulin secretion, and insulin signaling was assessed in the liver and in the skeletal muscle by western blots. We found that male and female rats born to PINX mothers display glucose intolerance at the end of the light phase of the light/dark cycle, but not at the beginning. We further demonstrate that impaired glucose-stimulated insulin secretion and hepatic insulin resistance are mechanisms that may contribute to glucose intolerance in the offspring of PINX mothers. The metabolic programming described here occurs due to an absence of maternal melatonin because the offspring born to PINX mothers treated with melatonin were not glucose intolerant.<h4>Conclusions/significance</h4>The present results support the novel concept that maternal melatonin is responsible for the programming of the daily pattern of energy metabolism in their offspring.
format article
author Danilo S Ferreira
Fernanda G Amaral
Caroline C Mesquita
Ana Paula L Barbosa
Camilo Lellis-Santos
Ariane O Turati
Laila R Santos
Carolina S Sollon
Patricia R Gomes
Juliana A Faria
José Cipolla-Neto
Silvana Bordin
Gabriel F Anhê
author_facet Danilo S Ferreira
Fernanda G Amaral
Caroline C Mesquita
Ana Paula L Barbosa
Camilo Lellis-Santos
Ariane O Turati
Laila R Santos
Carolina S Sollon
Patricia R Gomes
Juliana A Faria
José Cipolla-Neto
Silvana Bordin
Gabriel F Anhê
author_sort Danilo S Ferreira
title Maternal melatonin programs the daily pattern of energy metabolism in adult offspring.
title_short Maternal melatonin programs the daily pattern of energy metabolism in adult offspring.
title_full Maternal melatonin programs the daily pattern of energy metabolism in adult offspring.
title_fullStr Maternal melatonin programs the daily pattern of energy metabolism in adult offspring.
title_full_unstemmed Maternal melatonin programs the daily pattern of energy metabolism in adult offspring.
title_sort maternal melatonin programs the daily pattern of energy metabolism in adult offspring.
publisher Public Library of Science (PLoS)
publishDate 2012
url https://doaj.org/article/8ee39f7afc544238a15d9490caaeb68c
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