Sleep Deprivation Alters the Pituitary Stress Transcriptome in Male and Female Mice
Poor sleep hygiene is a growing problem, with detrimental effects on many biological systems. The pituitary gland plays a crucial role in the regulation of sleep and the stress response, and its dysfunction leads to sleep-related disorders. However, the interaction between these critical functions r...
| Main Authors: | , , , , , , , , , |
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| Format: | Article |
| Language: | English |
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Frontiers Media S.A.
2019-10-01
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| Series: | Frontiers in Endocrinology |
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| Online Access: | https://www.frontiersin.org/article/10.3389/fendo.2019.00676/full |
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| author | Mario G. Oyola Mario G. Oyola Mario G. Oyola Elizabeth A. Shupe Anthony R. Soltis Anthony R. Soltis Gauthaman Sukumar Gauthaman Sukumar Marcelo Paez-Pereda Darwin O. Larco Matthew D. Wilkerson Matthew D. Wilkerson Stephen Rothwell Clifton L. Dalgard Clifton L. Dalgard T. John Wu T. John Wu |
| author_facet | Mario G. Oyola Mario G. Oyola Mario G. Oyola Elizabeth A. Shupe Anthony R. Soltis Anthony R. Soltis Gauthaman Sukumar Gauthaman Sukumar Marcelo Paez-Pereda Darwin O. Larco Matthew D. Wilkerson Matthew D. Wilkerson Stephen Rothwell Clifton L. Dalgard Clifton L. Dalgard T. John Wu T. John Wu |
| author_sort | Mario G. Oyola |
| collection | DOAJ |
| description | Poor sleep hygiene is a growing problem, with detrimental effects on many biological systems. The pituitary gland plays a crucial role in the regulation of sleep and the stress response, and its dysfunction leads to sleep-related disorders. However, the interaction between these critical functions remains unclear. Thus, we performed a comparative, whole-transcriptome, analysis to identify stress-induced genes and relevant pathways that may be affected by sleep deprivation. One day following 12 h of Paradoxical Sleep Deprivation (PSD), mice were restrained for 20 min. Gene expression changes in the pituitary were assessed via RNA-Seq and Gene Ontology in PSD and/or restrained groups compared to controls. We show that restraint triggers transcriptional responses involved in hormone secretion, the glucocorticoid response, and apoptosis in both sexes, with 285 differentially expressed genes in females and 93 in males. When PSD preceded restraint stress, the numbers of differentially expressed genes increased to 613 in females and 580 in males. The pituitary transcriptome of restraint+PSD animals was enriched for microglia and macrophage proliferation, cellular response to corticosteroids, and apoptosis, among others. Finally, we identify sex-specific differences in restraint-induced genes following PSD. These findings provide genetic targets to consider when studying sleep and the response to stress. |
| first_indexed | 2024-12-13T09:07:21Z |
| format | Article |
| id | doaj.art-a533483f069b45edbbcb9212811af827 |
| institution | Directory Open Access Journal |
| issn | 1664-2392 |
| language | English |
| last_indexed | 2024-12-13T09:07:21Z |
| publishDate | 2019-10-01 |
| publisher | Frontiers Media S.A. |
| record_format | Article |
| series | Frontiers in Endocrinology |
| spelling | doaj.art-a533483f069b45edbbcb9212811af8272022-12-21T23:53:03ZengFrontiers Media S.A.Frontiers in Endocrinology1664-23922019-10-011010.3389/fendo.2019.00676483707Sleep Deprivation Alters the Pituitary Stress Transcriptome in Male and Female MiceMario G. Oyola0Mario G. Oyola1Mario G. Oyola2Elizabeth A. Shupe3Anthony R. Soltis4Anthony R. Soltis5Gauthaman Sukumar6Gauthaman Sukumar7Marcelo Paez-Pereda8Darwin O. Larco9Matthew D. Wilkerson10Matthew D. Wilkerson11Stephen Rothwell12Clifton L. Dalgard13Clifton L. Dalgard14T. John Wu15T. John Wu16Department of Obstetrics and Gynecology, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesCenter for Neuroscience and Regenerative Medicine, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, United StatesDepartment of Obstetrics and Gynecology, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, United StatesCollaborative Health Initiative Research Program, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesHenry M. Jackson Foundation for the Advancement of Military Medicine, Bethesda, MD, United StatesCollaborative Health Initiative Research Program, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesDepartment of Translational Research in Psychiatry, Max Planck Institute of Psychiatry, Munich, GermanyDepartment of Obstetrics and Gynecology, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesCollaborative Health Initiative Research Program, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesDepartment of Anatomy, Physiology and Genetics, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesDepartment of Anatomy, Physiology and Genetics, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesCollaborative Health Initiative Research Program, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesDepartment of Anatomy, Physiology and Genetics, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesDepartment of Obstetrics and Gynecology, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesCenter for Neuroscience and Regenerative Medicine, Uniformed Services University of the Health Sciences, Bethesda, MD, United StatesPoor sleep hygiene is a growing problem, with detrimental effects on many biological systems. The pituitary gland plays a crucial role in the regulation of sleep and the stress response, and its dysfunction leads to sleep-related disorders. However, the interaction between these critical functions remains unclear. Thus, we performed a comparative, whole-transcriptome, analysis to identify stress-induced genes and relevant pathways that may be affected by sleep deprivation. One day following 12 h of Paradoxical Sleep Deprivation (PSD), mice were restrained for 20 min. Gene expression changes in the pituitary were assessed via RNA-Seq and Gene Ontology in PSD and/or restrained groups compared to controls. We show that restraint triggers transcriptional responses involved in hormone secretion, the glucocorticoid response, and apoptosis in both sexes, with 285 differentially expressed genes in females and 93 in males. When PSD preceded restraint stress, the numbers of differentially expressed genes increased to 613 in females and 580 in males. The pituitary transcriptome of restraint+PSD animals was enriched for microglia and macrophage proliferation, cellular response to corticosteroids, and apoptosis, among others. Finally, we identify sex-specific differences in restraint-induced genes following PSD. These findings provide genetic targets to consider when studying sleep and the response to stress.https://www.frontiersin.org/article/10.3389/fendo.2019.00676/fullpituitary glandtranscriptomesleep deprivationstress responsesex differenceshypothalamic-pituitary-adrenal axis |
| spellingShingle | Mario G. Oyola Mario G. Oyola Mario G. Oyola Elizabeth A. Shupe Anthony R. Soltis Anthony R. Soltis Gauthaman Sukumar Gauthaman Sukumar Marcelo Paez-Pereda Darwin O. Larco Matthew D. Wilkerson Matthew D. Wilkerson Stephen Rothwell Clifton L. Dalgard Clifton L. Dalgard T. John Wu T. John Wu Sleep Deprivation Alters the Pituitary Stress Transcriptome in Male and Female Mice Frontiers in Endocrinology pituitary gland transcriptome sleep deprivation stress response sex differences hypothalamic-pituitary-adrenal axis |
| title | Sleep Deprivation Alters the Pituitary Stress Transcriptome in Male and Female Mice |
| title_full | Sleep Deprivation Alters the Pituitary Stress Transcriptome in Male and Female Mice |
| title_fullStr | Sleep Deprivation Alters the Pituitary Stress Transcriptome in Male and Female Mice |
| title_full_unstemmed | Sleep Deprivation Alters the Pituitary Stress Transcriptome in Male and Female Mice |
| title_short | Sleep Deprivation Alters the Pituitary Stress Transcriptome in Male and Female Mice |
| title_sort | sleep deprivation alters the pituitary stress transcriptome in male and female mice |
| topic | pituitary gland transcriptome sleep deprivation stress response sex differences hypothalamic-pituitary-adrenal axis |
| url | https://www.frontiersin.org/article/10.3389/fendo.2019.00676/full |
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