Early-life nicotine or cotinine exposure produces long-lasting sleep alterations and downregulation of hippocampal corticosteroid receptors in adult mice
Abstract Early-life exposure to environmental toxins like tobacco can permanently re-program body structure and function. Here, we investigated the long-term effects on mouse adult sleep phenotype exerted by early-life exposure to nicotine or to its principal metabolite, cotinine. Moreover, we inves...
| Main Authors: | , , , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Nature Portfolio
2021-12-01
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| Series: | Scientific Reports |
| Online Access: | https://doi.org/10.1038/s41598-021-03468-5 |
| _version_ | 1831717219101310976 |
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| author | Stefano Bastianini Viviana Lo Martire Sara Alvente Chiara Berteotti Gabriele Matteoli Laura Rullo Serena Stamatakos Alessandro Silvani Sanzio Candeletti Patrizia Romualdi Gary Cohen Giovanna Zoccoli |
| author_facet | Stefano Bastianini Viviana Lo Martire Sara Alvente Chiara Berteotti Gabriele Matteoli Laura Rullo Serena Stamatakos Alessandro Silvani Sanzio Candeletti Patrizia Romualdi Gary Cohen Giovanna Zoccoli |
| author_sort | Stefano Bastianini |
| collection | DOAJ |
| description | Abstract Early-life exposure to environmental toxins like tobacco can permanently re-program body structure and function. Here, we investigated the long-term effects on mouse adult sleep phenotype exerted by early-life exposure to nicotine or to its principal metabolite, cotinine. Moreover, we investigated whether these effects occurred together with a reprogramming of the activity of the hippocampus, a key structure to coordinate the hormonal stress response. Adult male mice born from dams subjected to nicotine (NIC), cotinine (COT) or vehicle (CTRL) treatment in drinking water were implanted with electrodes for sleep recordings. NIC and COT mice spent significantly more time awake than CTRL mice at the transition between the rest (light) and the activity (dark) period. NIC and COT mice showed hippocampal glucocorticoid receptor (GR) downregulation compared to CTRL mice, and NIC mice also showed hippocampal mineralocorticoid receptor downregulation. Hippocampal GR expression significantly and inversely correlated with the amount of wakefulness at the light-to-dark transition, while no changes in DNA methylation were found. We demonstrated that early-life exposure to nicotine (and cotinine) concomitantly entails long-lasting reprogramming of hippocampal activity and sleep phenotype suggesting that the adult sleep phenotype may be modulated by events that occurred during that critical period of life. |
| first_indexed | 2024-12-21T00:54:22Z |
| format | Article |
| id | doaj.art-141f2b013462458bb249050ba597c5bb |
| institution | Directory Open Access Journal |
| issn | 2045-2322 |
| language | English |
| last_indexed | 2024-12-21T00:54:22Z |
| publishDate | 2021-12-01 |
| publisher | Nature Portfolio |
| record_format | Article |
| series | Scientific Reports |
| spelling | doaj.art-141f2b013462458bb249050ba597c5bb2022-12-21T19:21:19ZengNature PortfolioScientific Reports2045-23222021-12-0111111310.1038/s41598-021-03468-5Early-life nicotine or cotinine exposure produces long-lasting sleep alterations and downregulation of hippocampal corticosteroid receptors in adult miceStefano Bastianini0Viviana Lo Martire1Sara Alvente2Chiara Berteotti3Gabriele Matteoli4Laura Rullo5Serena Stamatakos6Alessandro Silvani7Sanzio Candeletti8Patrizia Romualdi9Gary Cohen10Giovanna Zoccoli11PRISM Lab, Department of Biomedical and Neuromotor Sciences, Alma Mater Studiorum, University of BolognaPRISM Lab, Department of Biomedical and Neuromotor Sciences, Alma Mater Studiorum, University of BolognaPRISM Lab, Department of Biomedical and Neuromotor Sciences, Alma Mater Studiorum, University of BolognaPRISM Lab, Department of Biomedical and Neuromotor Sciences, Alma Mater Studiorum, University of BolognaPRISM Lab, Department of Biomedical and Neuromotor Sciences, Alma Mater Studiorum, University of BolognaDepartment of Pharmacy and Biotechnology, Alma Mater Studiorum, University of BolognaDepartment of Pharmacy and Biotechnology, Alma Mater Studiorum, University of BolognaPRISM Lab, Department of Biomedical and Neuromotor Sciences, Alma Mater Studiorum, University of BolognaDepartment of Pharmacy and Biotechnology, Alma Mater Studiorum, University of BolognaDepartment of Pharmacy and Biotechnology, Alma Mater Studiorum, University of BolognaDepartment of Women and Child Health, Karolinska InstitutetPRISM Lab, Department of Biomedical and Neuromotor Sciences, Alma Mater Studiorum, University of BolognaAbstract Early-life exposure to environmental toxins like tobacco can permanently re-program body structure and function. Here, we investigated the long-term effects on mouse adult sleep phenotype exerted by early-life exposure to nicotine or to its principal metabolite, cotinine. Moreover, we investigated whether these effects occurred together with a reprogramming of the activity of the hippocampus, a key structure to coordinate the hormonal stress response. Adult male mice born from dams subjected to nicotine (NIC), cotinine (COT) or vehicle (CTRL) treatment in drinking water were implanted with electrodes for sleep recordings. NIC and COT mice spent significantly more time awake than CTRL mice at the transition between the rest (light) and the activity (dark) period. NIC and COT mice showed hippocampal glucocorticoid receptor (GR) downregulation compared to CTRL mice, and NIC mice also showed hippocampal mineralocorticoid receptor downregulation. Hippocampal GR expression significantly and inversely correlated with the amount of wakefulness at the light-to-dark transition, while no changes in DNA methylation were found. We demonstrated that early-life exposure to nicotine (and cotinine) concomitantly entails long-lasting reprogramming of hippocampal activity and sleep phenotype suggesting that the adult sleep phenotype may be modulated by events that occurred during that critical period of life.https://doi.org/10.1038/s41598-021-03468-5 |
| spellingShingle | Stefano Bastianini Viviana Lo Martire Sara Alvente Chiara Berteotti Gabriele Matteoli Laura Rullo Serena Stamatakos Alessandro Silvani Sanzio Candeletti Patrizia Romualdi Gary Cohen Giovanna Zoccoli Early-life nicotine or cotinine exposure produces long-lasting sleep alterations and downregulation of hippocampal corticosteroid receptors in adult mice Scientific Reports |
| title | Early-life nicotine or cotinine exposure produces long-lasting sleep alterations and downregulation of hippocampal corticosteroid receptors in adult mice |
| title_full | Early-life nicotine or cotinine exposure produces long-lasting sleep alterations and downregulation of hippocampal corticosteroid receptors in adult mice |
| title_fullStr | Early-life nicotine or cotinine exposure produces long-lasting sleep alterations and downregulation of hippocampal corticosteroid receptors in adult mice |
| title_full_unstemmed | Early-life nicotine or cotinine exposure produces long-lasting sleep alterations and downregulation of hippocampal corticosteroid receptors in adult mice |
| title_short | Early-life nicotine or cotinine exposure produces long-lasting sleep alterations and downregulation of hippocampal corticosteroid receptors in adult mice |
| title_sort | early life nicotine or cotinine exposure produces long lasting sleep alterations and downregulation of hippocampal corticosteroid receptors in adult mice |
| url | https://doi.org/10.1038/s41598-021-03468-5 |
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