Glucocorticoid-Dependent Hippocampal Transcriptome in Male Rats: Pathway-Specific Alterations With Aging
Although glucocorticoids (GCs) are known to exert numerous effects in the hippocampus, their chronic regulatory functions remain poorly understood. Moreover, evidence is inconsistent regarding the long-standing hypothesis that chronic GC exposure promotes brain aging/Alzheimer disease. Here, we adre...
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Published in | Endocrinology (Philadelphia) Vol. 154; no. 8; pp. 2807 - 2820 |
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Main Authors | , , , , , , , |
Format | Journal Article |
Language | English |
Published |
Chevy Chase, MD
Oxford University Press
01.08.2013
Endocrine Society |
Subjects | |
Online Access | Get full text |
ISSN | 0013-7227 1945-7170 1945-7170 |
DOI | 10.1210/en.2013-1139 |
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Abstract | Although glucocorticoids (GCs) are known to exert numerous effects in the hippocampus, their chronic regulatory functions remain poorly understood. Moreover, evidence is inconsistent regarding the long-standing hypothesis that chronic GC exposure promotes brain aging/Alzheimer disease. Here, we adrenalectomized male F344 rats at 15 months of age, maintained them for 3 months with implanted corticosterone (CORT) pellets producing low or intermediate (glucocorticoid receptor–activating) blood levels of CORT, and performed microarray/pathway analyses in hippocampal CA1. We defined the chronic GC-dependent transcriptome as 393 genes that exhibited differential expression between intermediate and low CORT groups. Short-term CORT (4 days) did not recapitulate this transcriptome. Functional processes/pathways overrepresented by chronic CORT–up-regulated genes included learning/plasticity, differentiation, glucose metabolism, and cholesterol biosynthesis, whereas processes overrepresented by CORT–down-regulated genes included inflammatory/immune/glial responses and extracellular structure. These profiles indicate that GCs chronically activate neuronal/metabolic processes while coordinately repressing a glial axis of reactivity/inflammation. We then compared the GC transcriptome with a previously defined hippocampal aging transcriptome, revealing a high proportion of common genes. Although CORT and aging moved expression of some common genes in the same direction, the majority were shifted in opposite directions by CORT and aging (eg, glial inflammatory genes down-regulated by CORT are up-regulated with aging). These results contradict the hypothesis that GCs simply promote brain aging and also suggest that the opposite direction shifts during aging reflect resistance to CORT regulation. Therefore, we propose a new model in which aging-related GC resistance develops in some target pathways, whereas GC overstimulation develops in others, together generating much of the brain aging phenotype. |
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AbstractList | Although glucocorticoids (GCs) are known to exert numerous effects in the hippocampus, their chronic regulatory functions remain poorly understood. Moreover, evidence is inconsistent regarding the long-standing hypothesis that chronic GC exposure promotes brain aging/Alzheimer disease. Here, we adrenalectomized male F344 rats at 15 months of age, maintained them for 3 months with implanted corticosterone (CORT) pellets producing low or intermediate (glucocorticoid receptor-activating) blood levels of CORT, and performed microarray/pathway analyses in hippocampal CA1. We defined the chronic GC-dependent transcriptome as 393 genes that exhibited differential expression between intermediate and low CORT groups. Short-term CORT (4 days) did not recapitulate this transcriptome. Functional processes/pathways overrepresented by chronic CORT-up-regulated genes included learning/plasticity, differentiation, glucose metabolism, and cholesterol biosynthesis, whereas processes overrepresented by CORT-down-regulated genes included inflammatory/immune/glial responses and extracellular structure. These profiles indicate that GCs chronically activate neuronal/metabolic processes while coordinately repressing a glial axis of reactivity/inflammation. We then compared the GC transcriptome with a previously defined hippocampal aging transcriptome, revealing a high proportion of common genes. Although CORT and aging moved expression of some common genes in the same direction, the majority were shifted in opposite directions by CORT and aging (eg, glial inflammatory genes down-regulated by CORT are up-regulated with aging). These results contradict the hypothesis that GCs simply promote brain aging and also suggest that the opposite direction shifts during aging reflect resistance to CORT regulation. Therefore, we propose a new model in which aging-related GC resistance develops in some target pathways, whereas GC overstimulation develops in others, together generating much of the brain aging phenotype. Although glucocorticoids (GCs) are known to exert numerous effects in the hippocampus, their chronic regulatory functions remain poorly understood. Moreover, evidence is inconsistent regarding the long-standing hypothesis that chronic GC exposure promotes brain aging/Alzheimer disease. Here, we adrenalectomized male F344 rats at 15 months of age, maintained them for 3 months with implanted corticosterone (CORT) pellets producing low or intermediate (glucocorticoid receptor-activating) blood levels of CORT, and performed microarray/pathway analyses in hippocampal CA1. We defined the chronic GC-dependent transcriptome as 393 genes that exhibited differential expression between intermediate and low CORT groups. Short-term CORT (4 days) did not recapitulate this transcriptome. Functional processes/pathways overrepresented by chronic CORT-up-regulated genes included learning/plasticity, differentiation, glucose metabolism, and cholesterol biosynthesis, whereas processes overrepresented by CORT-down-regulated genes included inflammatory/immune/glial responses and extracellular structure. These profiles indicate that GCs chronically activate neuronal/metabolic processes while coordinately repressing a glial axis of reactivity/inflammation. We then compared the GC transcriptome with a previously defined hippocampal aging transcriptome, revealing a high proportion of common genes. Although CORT and aging moved expression of some common genes in the same direction, the majority were shifted in opposite directions by CORT and aging (eg, glial inflammatory genes down-regulated by CORT are up-regulated with aging). These results contradict the hypothesis that GCs simply promote brain aging and also suggest that the opposite direction shifts during aging reflect resistance to CORT regulation. Therefore, we propose a new model in which aging-related GC resistance develops in some target pathways, whereas GC overstimulation develops in others, together generating much of the brain aging phenotype.Although glucocorticoids (GCs) are known to exert numerous effects in the hippocampus, their chronic regulatory functions remain poorly understood. Moreover, evidence is inconsistent regarding the long-standing hypothesis that chronic GC exposure promotes brain aging/Alzheimer disease. Here, we adrenalectomized male F344 rats at 15 months of age, maintained them for 3 months with implanted corticosterone (CORT) pellets producing low or intermediate (glucocorticoid receptor-activating) blood levels of CORT, and performed microarray/pathway analyses in hippocampal CA1. We defined the chronic GC-dependent transcriptome as 393 genes that exhibited differential expression between intermediate and low CORT groups. Short-term CORT (4 days) did not recapitulate this transcriptome. Functional processes/pathways overrepresented by chronic CORT-up-regulated genes included learning/plasticity, differentiation, glucose metabolism, and cholesterol biosynthesis, whereas processes overrepresented by CORT-down-regulated genes included inflammatory/immune/glial responses and extracellular structure. These profiles indicate that GCs chronically activate neuronal/metabolic processes while coordinately repressing a glial axis of reactivity/inflammation. We then compared the GC transcriptome with a previously defined hippocampal aging transcriptome, revealing a high proportion of common genes. Although CORT and aging moved expression of some common genes in the same direction, the majority were shifted in opposite directions by CORT and aging (eg, glial inflammatory genes down-regulated by CORT are up-regulated with aging). These results contradict the hypothesis that GCs simply promote brain aging and also suggest that the opposite direction shifts during aging reflect resistance to CORT regulation. Therefore, we propose a new model in which aging-related GC resistance develops in some target pathways, whereas GC overstimulation develops in others, together generating much of the brain aging phenotype. |
Author | Curran-Rauhut, Meredith A. Landfield, Philip W. Chen, Kuey-Chu Porter, Nada M. Kadish, Inga Blalock, Susan J. Blalock, Eric M. Brewer, Lawrence |
Author_xml | – sequence: 1 givenname: Kuey-Chu surname: Chen fullname: Chen, Kuey-Chu organization: 1Department of Molecular and Biomedical Pharmacology, University of Kentucky College of Medicine, Lexington, Kentucky 40536 – sequence: 2 givenname: Eric M. surname: Blalock fullname: Blalock, Eric M. organization: 1Department of Molecular and Biomedical Pharmacology, University of Kentucky College of Medicine, Lexington, Kentucky 40536 – sequence: 3 givenname: Meredith A. surname: Curran-Rauhut fullname: Curran-Rauhut, Meredith A. organization: 1Department of Molecular and Biomedical Pharmacology, University of Kentucky College of Medicine, Lexington, Kentucky 40536 – sequence: 4 givenname: Inga surname: Kadish fullname: Kadish, Inga organization: 1Department of Molecular and Biomedical Pharmacology, University of Kentucky College of Medicine, Lexington, Kentucky 40536 – sequence: 5 givenname: Susan J. surname: Blalock fullname: Blalock, Susan J. organization: 1Department of Molecular and Biomedical Pharmacology, University of Kentucky College of Medicine, Lexington, Kentucky 40536 – sequence: 6 givenname: Lawrence surname: Brewer fullname: Brewer, Lawrence organization: 1Department of Molecular and Biomedical Pharmacology, University of Kentucky College of Medicine, Lexington, Kentucky 40536 – sequence: 7 givenname: Nada M. surname: Porter fullname: Porter, Nada M. organization: 1Department of Molecular and Biomedical Pharmacology, University of Kentucky College of Medicine, Lexington, Kentucky 40536 – sequence: 8 givenname: Philip W. surname: Landfield fullname: Landfield, Philip W. email: pwland@uky.edu. organization: 1Department of Molecular and Biomedical Pharmacology, University of Kentucky College of Medicine, Lexington, Kentucky 40536 |
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Keywords | Vertebrata Mammalia Rat Animal Ageing Rodentia Central nervous system Alteration Male Glucocorticoid Hippocampus Encephalon |
Language | English |
License | CC BY 4.0 This is an Open Access article distributed under the terms of the Creative Commons Attribution Non-Commercial License (http://creativecommons.org/licenses/by-nc/3.0/us/) which permits unrestricted non-commercial use, distribution, and reproduction in any medium, provided the original work is properly cited. |
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SubjectTerms | Adrenalectomy Aging Aging - genetics Alzheimer's disease Animals Biological and medical sciences Biosynthesis Blood levels Body Weight - drug effects Brain CA1 Region, Hippocampal - metabolism Cholesterol Corticosterone Corticosterone - blood Corticosterone - pharmacology DNA microarrays Drinking - drug effects Drug Implants Eating - drug effects Fundamental and applied biological sciences. Psychology Gene expression Gene regulation Genes Glial Fibrillary Acidic Protein - genetics Glial Fibrillary Acidic Protein - metabolism Glucocorticoid receptors Glucocorticoids Glucocorticoids - pharmacology Glucose metabolism Hippocampus Hypotheses Immunohistochemistry Inflammation Lipid metabolism Male Males Neurodegenerative diseases Neuroendocrinology Neuronal-glial interactions Oligonucleotide Array Sequence Analysis Phenotypes Rats Rats, Inbred F344 Receptors, Glucocorticoid - genetics Receptors, Glucocorticoid - metabolism Reverse Transcriptase Polymerase Chain Reaction Signal Transduction - genetics Transcriptome - drug effects Transcriptomes Vertebrates: endocrinology |
Title | Glucocorticoid-Dependent Hippocampal Transcriptome in Male Rats: Pathway-Specific Alterations With Aging |
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