Stephanie M Jones, Sarah Jo Sleiman, Katharine E McCann, Alan K Jarmusch, Georgia M Alexander, Serena M Dudek
{"title":"产前暴露于矿质皮质激素受体拮抗剂螺内酯会破坏小鼠海马CA2区的连接并改变其行为。","authors":"Stephanie M Jones, Sarah Jo Sleiman, Katharine E McCann, Alan K Jarmusch, Georgia M Alexander, Serena M Dudek","doi":"10.1038/s41386-024-01971-7","DOIUrl":null,"url":null,"abstract":"<p><p>In the brain, the hippocampus is enriched with mineralocorticoid receptors (MR; Nr3c2), a ligand-dependent transcription factor stimulated by the stress hormone corticosterone in rodents. Recently, we discovered that MR is required for the acquisition and maintenance of many features of mouse area CA2 neurons. Notably, we observed that immunofluorescence for the vesicular glutamate transporter 2 (vGluT2), likely representing afferents from the supramammillary nucleus (SuM), was disrupted in the embryonic, but not postnatal, MR knockout mouse CA2. To test whether pharmacological perturbation of MR activity in utero similarly disrupts CA2 connectivity, we implanted slow-release pellets containing the MR antagonist spironolactone in mouse dams during mid-gestation. After confirming that at least one likely active metabolite crossed from the dams' serum into the embryonic brains, we found that spironolactone treatment caused a significant reduction of CA2 axon fluorescence intensity in the CA1 stratum oriens, where CA2 axons preferentially project, and that vGluT2 staining was significantly decreased in both CA2 and dentate gyrus in spironolactone-treated animals. We also found that spironolactone-treated animals exhibited increased reactivity to novel objects, an effect similar to what is seen with embryonic or postnatal CA2-targeted MR knockout. However, we found no difference in preference for social novelty between the treatment groups. We infer these results to suggest that persistent or more severe disruptions in MR function may be required to interfere with this type of social behavior. These findings do indicate, though, that developmental disruption in MR signaling can have persistent effects on hippocampal circuitry and behavior.</p>","PeriodicalId":19143,"journal":{"name":"Neuropsychopharmacology","volume":" ","pages":""},"PeriodicalIF":6.6000,"publicationDate":"2024-09-05","publicationTypes":"Journal Article","fieldsOfStudy":null,"isOpenAccess":false,"openAccessPdf":"","citationCount":"0","resultStr":"{\"title\":\"Prenatal exposure to the mineralocorticoid receptor antagonist spironolactone disrupts hippocampal area CA2 connectivity and alters behavior in mice.\",\"authors\":\"Stephanie M Jones, Sarah Jo Sleiman, Katharine E McCann, Alan K Jarmusch, Georgia M Alexander, Serena M Dudek\",\"doi\":\"10.1038/s41386-024-01971-7\",\"DOIUrl\":null,\"url\":null,\"abstract\":\"<p><p>In the brain, the hippocampus is enriched with mineralocorticoid receptors (MR; Nr3c2), a ligand-dependent transcription factor stimulated by the stress hormone corticosterone in rodents. Recently, we discovered that MR is required for the acquisition and maintenance of many features of mouse area CA2 neurons. Notably, we observed that immunofluorescence for the vesicular glutamate transporter 2 (vGluT2), likely representing afferents from the supramammillary nucleus (SuM), was disrupted in the embryonic, but not postnatal, MR knockout mouse CA2. To test whether pharmacological perturbation of MR activity in utero similarly disrupts CA2 connectivity, we implanted slow-release pellets containing the MR antagonist spironolactone in mouse dams during mid-gestation. After confirming that at least one likely active metabolite crossed from the dams' serum into the embryonic brains, we found that spironolactone treatment caused a significant reduction of CA2 axon fluorescence intensity in the CA1 stratum oriens, where CA2 axons preferentially project, and that vGluT2 staining was significantly decreased in both CA2 and dentate gyrus in spironolactone-treated animals. We also found that spironolactone-treated animals exhibited increased reactivity to novel objects, an effect similar to what is seen with embryonic or postnatal CA2-targeted MR knockout. However, we found no difference in preference for social novelty between the treatment groups. We infer these results to suggest that persistent or more severe disruptions in MR function may be required to interfere with this type of social behavior. These findings do indicate, though, that developmental disruption in MR signaling can have persistent effects on hippocampal circuitry and behavior.</p>\",\"PeriodicalId\":19143,\"journal\":{\"name\":\"Neuropsychopharmacology\",\"volume\":\" \",\"pages\":\"\"},\"PeriodicalIF\":6.6000,\"publicationDate\":\"2024-09-05\",\"publicationTypes\":\"Journal Article\",\"fieldsOfStudy\":null,\"isOpenAccess\":false,\"openAccessPdf\":\"\",\"citationCount\":\"0\",\"resultStr\":null,\"platform\":\"Semanticscholar\",\"paperid\":null,\"PeriodicalName\":\"Neuropsychopharmacology\",\"FirstCategoryId\":\"3\",\"ListUrlMain\":\"https://doi.org/10.1038/s41386-024-01971-7\",\"RegionNum\":1,\"RegionCategory\":\"医学\",\"ArticlePicture\":[],\"TitleCN\":null,\"AbstractTextCN\":null,\"PMCID\":null,\"EPubDate\":\"\",\"PubModel\":\"\",\"JCR\":\"Q1\",\"JCRName\":\"NEUROSCIENCES\",\"Score\":null,\"Total\":0}","platform":"Semanticscholar","paperid":null,"PeriodicalName":"Neuropsychopharmacology","FirstCategoryId":"3","ListUrlMain":"https://doi.org/10.1038/s41386-024-01971-7","RegionNum":1,"RegionCategory":"医学","ArticlePicture":[],"TitleCN":null,"AbstractTextCN":null,"PMCID":null,"EPubDate":"","PubModel":"","JCR":"Q1","JCRName":"NEUROSCIENCES","Score":null,"Total":0}
Prenatal exposure to the mineralocorticoid receptor antagonist spironolactone disrupts hippocampal area CA2 connectivity and alters behavior in mice.
In the brain, the hippocampus is enriched with mineralocorticoid receptors (MR; Nr3c2), a ligand-dependent transcription factor stimulated by the stress hormone corticosterone in rodents. Recently, we discovered that MR is required for the acquisition and maintenance of many features of mouse area CA2 neurons. Notably, we observed that immunofluorescence for the vesicular glutamate transporter 2 (vGluT2), likely representing afferents from the supramammillary nucleus (SuM), was disrupted in the embryonic, but not postnatal, MR knockout mouse CA2. To test whether pharmacological perturbation of MR activity in utero similarly disrupts CA2 connectivity, we implanted slow-release pellets containing the MR antagonist spironolactone in mouse dams during mid-gestation. After confirming that at least one likely active metabolite crossed from the dams' serum into the embryonic brains, we found that spironolactone treatment caused a significant reduction of CA2 axon fluorescence intensity in the CA1 stratum oriens, where CA2 axons preferentially project, and that vGluT2 staining was significantly decreased in both CA2 and dentate gyrus in spironolactone-treated animals. We also found that spironolactone-treated animals exhibited increased reactivity to novel objects, an effect similar to what is seen with embryonic or postnatal CA2-targeted MR knockout. However, we found no difference in preference for social novelty between the treatment groups. We infer these results to suggest that persistent or more severe disruptions in MR function may be required to interfere with this type of social behavior. These findings do indicate, though, that developmental disruption in MR signaling can have persistent effects on hippocampal circuitry and behavior.
期刊介绍:
Neuropsychopharmacology is a reputable international scientific journal that serves as the official publication of the American College of Neuropsychopharmacology (ACNP). The journal's primary focus is on research that enhances our knowledge of the brain and behavior, with a particular emphasis on the molecular, cellular, physiological, and psychological aspects of substances that affect the central nervous system (CNS). It also aims to identify new molecular targets for the development of future drugs.
The journal prioritizes original research reports, but it also welcomes mini-reviews and perspectives, which are often solicited by the editorial office. These types of articles provide valuable insights and syntheses of current research trends and future directions in the field of neuroscience and pharmacology.