Sex-Specific Impact of Fkbp5 on Hippocampal Response to Acute Alcohol Injection: Involvement in Alterations of Metabolism-Related Pathways

High levels of alcohol intake alter brain gene expression and can produce long-lasting effects. FK506-binding protein 51 (FKBP51) encoded by Fkbp5 is a physical and cellular stress response gene and has been associated with alcohol consumption and withdrawal severity. Fkbp5 has been previously linke...

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Published in:	Cells (Basel, Switzerland) Vol. 13; no. 1; p. 89
Main Authors:	Williams, Kent E., Zou, Yi, Qiu, Bin, Kono, Tatsuyoshi, Guo, Changyong, Garcia, Dawn, Chen, Hanying, Graves, Tamara, Lai, Zhao, Evans-Molina, Carmella, Ma, Yao-Ying, Liangpunsakul, Suthat, Yong, Weidong, Liang, Tiebing
Format:	Journal Article
Language:	English
Published:	Switzerland MDPI AG 31.12.2023 MDPI
Subjects:	Alcohol Drinking Alcohol use Alcohol-Related Disorders Animals Axon guidance Axonogenesis Brain research Calcium metabolism Calcium signalling Cell signaling Cellular signal transduction Cellular stress response Cytology Drinking of alcoholic beverages Drug dosages Epigenetics Ethanol Ethanol - pharmacology Female Females Fkbp5 Gender differences Gene expression Genetic aspects Glycine Health aspects Hippocampus Hippocampus (Brain) Injections Laboratory animals Lipid Metabolism Male Metabolic regulation Mice mitochondria Morphology Neurons Neuroprotection Physiological aspects Post-translation Potassium Proteins RNA-seq Sex differences Signal transduction Software Tacrolimus Tacrolimus-binding protein United States United States > US RNA-seq hippocampus mitochondria Fkbp5 lipid metabolism
ISSN:	2073-4409, 2073-4409
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Abstract	High levels of alcohol intake alter brain gene expression and can produce long-lasting effects. FK506-binding protein 51 (FKBP51) encoded by Fkbp5 is a physical and cellular stress response gene and has been associated with alcohol consumption and withdrawal severity. Fkbp5 has been previously linked to neurite outgrowth and hippocampal morphology, sex differences in stress response, and epigenetic modification. Presently, primary cultured Fkbp5 KO and WT mouse neurons were examined for neurite outgrowth and mitochondrial signal with and without alcohol. We found neurite specification differences between KO and WT; particularly, mesh-like morphology was observed after alcohol treatment and confirmed higher MitoTracker signal in cultured neurons of Fkbp5 KO compared to WT at both naive and alcohol-treated conditions. Brain regions that express FKBP51 protein were identified, and hippocampus was confirmed to possess a high level of expression. RNA-seq profiling was performed using the hippocampus of naïve or alcohol-injected (2 mg EtOH/Kg) male and female Fkbp5 KO and WT mice. Differentially expressed genes (DEGs) were identified between Fkbp5 KO and WT at baseline and following alcohol treatment, with female comparisons possessing a higher number of DEGs than male comparisons. Pathway analysis suggested that genes affecting calcium signaling, lipid metabolism, and axon guidance were differentially expressed at naïve condition between KO and WT. Alcohol treatment significantly affected pathways and enzymes involved in biosynthesis (Keto, serine, and glycine) and signaling (dopamine and insulin receptor), and neuroprotective role. Functions related to cell morphology, cell-to-cell signaling, lipid metabolism, injury response, and post-translational modification were significantly altered due to alcohol. In summary, Fkbp5 plays a critical role in the response to acute alcohol treatment by altering metabolism and signaling-related genes.
AbstractList	High levels of alcohol intake alter brain gene expression and can produce long-lasting effects. FK506-binding protein 51 (FKBP51) encoded by Fkbp5 is a physical and cellular stress response gene and has been associated with alcohol consumption and withdrawal severity. Fkbp5 has been previously linked to neurite outgrowth and hippocampal morphology, sex differences in stress response, and epigenetic modification. Presently, primary cultured Fkbp5 KO and WT mouse neurons were examined for neurite outgrowth and mitochondrial signal with and without alcohol. We found neurite specification differences between KO and WT; particularly, mesh-like morphology was observed after alcohol treatment and confirmed higher MitoTracker signal in cultured neurons of Fkbp5 KO compared to WT at both naive and alcohol-treated conditions. Brain regions that express FKBP51 protein were identified, and hippocampus was confirmed to possess a high level of expression. RNA-seq profiling was performed using the hippocampus of naïve or alcohol-injected (2 mg EtOH/Kg) male and female Fkbp5 KO and WT mice. Differentially expressed genes (DEGs) were identified between Fkbp5 KO and WT at baseline and following alcohol treatment, with female comparisons possessing a higher number of DEGs than male comparisons. Pathway analysis suggested that genes affecting calcium signaling, lipid metabolism, and axon guidance were differentially expressed at naïve condition between KO and WT. Alcohol treatment significantly affected pathways and enzymes involved in biosynthesis (Keto, serine, and glycine) and signaling (dopamine and insulin receptor), and neuroprotective role. Functions related to cell morphology, cell-to-cell signaling, lipid metabolism, injury response, and post-translational modification were significantly altered due to alcohol. In summary, Fkbp5 plays a critical role in the response to acute alcohol treatment by altering metabolism and signaling-related genes. High levels of alcohol intake alter brain gene expression and can produce long-lasting effects. FK506-binding protein 51 (FKBP51) encoded by Fkbp5 is a physical and cellular stress response gene and has been associated with alcohol consumption and withdrawal severity. Fkbp5 has been previously linked to neurite outgrowth and hippocampal morphology, sex differences in stress response, and epigenetic modification. Presently, primary cultured Fkbp5 KO and WT mouse neurons were examined for neurite outgrowth and mitochondrial signal with and without alcohol. We found neurite specification differences between KO and WT; particularly, mesh-like morphology was observed after alcohol treatment and confirmed higher MitoTracker signal in cultured neurons of Fkbp5 KO compared to WT at both naive and alcohol-treated conditions. Brain regions that express FKBP51 protein were identified, and hippocampus was confirmed to possess a high level of expression. RNA-seq profiling was performed using the hippocampus of naïve or alcohol-injected (2 mg EtOH/Kg) male and female Fkbp5 KO and WT mice. Differentially expressed genes (DEGs) were identified between Fkbp5 KO and WT at baseline and following alcohol treatment, with female comparisons possessing a higher number of DEGs than male comparisons. Pathway analysis suggested that genes affecting calcium signaling, lipid metabolism, and axon guidance were differentially expressed at naïve condition between KO and WT. Alcohol treatment significantly affected pathways and enzymes involved in biosynthesis (Keto, serine, and glycine) and signaling (dopamine and insulin receptor), and neuroprotective role. Functions related to cell morphology, cell-to-cell signaling, lipid metabolism, injury response, and post-translational modification were significantly altered due to alcohol. In summary, Fkbp5 plays a critical role in the response to acute alcohol treatment by altering metabolism and signaling-related genes.High levels of alcohol intake alter brain gene expression and can produce long-lasting effects. FK506-binding protein 51 (FKBP51) encoded by Fkbp5 is a physical and cellular stress response gene and has been associated with alcohol consumption and withdrawal severity. Fkbp5 has been previously linked to neurite outgrowth and hippocampal morphology, sex differences in stress response, and epigenetic modification. Presently, primary cultured Fkbp5 KO and WT mouse neurons were examined for neurite outgrowth and mitochondrial signal with and without alcohol. We found neurite specification differences between KO and WT; particularly, mesh-like morphology was observed after alcohol treatment and confirmed higher MitoTracker signal in cultured neurons of Fkbp5 KO compared to WT at both naive and alcohol-treated conditions. Brain regions that express FKBP51 protein were identified, and hippocampus was confirmed to possess a high level of expression. RNA-seq profiling was performed using the hippocampus of naïve or alcohol-injected (2 mg EtOH/Kg) male and female Fkbp5 KO and WT mice. Differentially expressed genes (DEGs) were identified between Fkbp5 KO and WT at baseline and following alcohol treatment, with female comparisons possessing a higher number of DEGs than male comparisons. Pathway analysis suggested that genes affecting calcium signaling, lipid metabolism, and axon guidance were differentially expressed at naïve condition between KO and WT. Alcohol treatment significantly affected pathways and enzymes involved in biosynthesis (Keto, serine, and glycine) and signaling (dopamine and insulin receptor), and neuroprotective role. Functions related to cell morphology, cell-to-cell signaling, lipid metabolism, injury response, and post-translational modification were significantly altered due to alcohol. In summary, Fkbp5 plays a critical role in the response to acute alcohol treatment by altering metabolism and signaling-related genes. High levels of alcohol intake alter brain gene expression and can produce long-lasting effects. FK506-binding protein 51 (FKBP51) encoded by is a physical and cellular stress response gene and has been associated with alcohol consumption and withdrawal severity. has been previously linked to neurite outgrowth and hippocampal morphology, sex differences in stress response, and epigenetic modification. Presently, primary cultured KO and WT mouse neurons were examined for neurite outgrowth and mitochondrial signal with and without alcohol. We found neurite specification differences between KO and WT; particularly, mesh-like morphology was observed after alcohol treatment and confirmed higher MitoTracker signal in cultured neurons of KO compared to WT at both naive and alcohol-treated conditions. Brain regions that express FKBP51 protein were identified, and hippocampus was confirmed to possess a high level of expression. RNA-seq profiling was performed using the hippocampus of naïve or alcohol-injected (2 mg EtOH/Kg) male and female KO and WT mice. Differentially expressed genes (DEGs) were identified between KO and WT at baseline and following alcohol treatment, with female comparisons possessing a higher number of DEGs than male comparisons. Pathway analysis suggested that genes affecting calcium signaling, lipid metabolism, and axon guidance were differentially expressed at naïve condition between KO and WT. Alcohol treatment significantly affected pathways and enzymes involved in biosynthesis (Keto, serine, and glycine) and signaling (dopamine and insulin receptor), and neuroprotective role. Functions related to cell morphology, cell-to-cell signaling, lipid metabolism, injury response, and post-translational modification were significantly altered due to alcohol. In summary, plays a critical role in the response to acute alcohol treatment by altering metabolism and signaling-related genes.
Audience	Academic
Author	Yong, Weidong Ma, Yao-Ying Garcia, Dawn Zou, Yi Qiu, Bin Chen, Hanying Evans-Molina, Carmella Liang, Tiebing Guo, Changyong Williams, Kent E. Kono, Tatsuyoshi Lai, Zhao Graves, Tamara Liangpunsakul, Suthat
AuthorAffiliation	5 Department Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, IN 46202, USA; guo14@iu.edu (C.G.); ym9@iu.edu (Y.-Y.M.) 7 Roudebush Veterans Administration Medical Center, Indianapolis, IN 46202, USA 1 Division of Gastroenterology and Hepatology, Department of Medicine, Indiana University, Indianapolis, IN 46202, USA; kew5@iu.edu (K.E.W.); tharris1@iu.edu (T.G.); sliangpu@iu.edu (S.L.) 6 Department Medical and Molecular Genetics, Indiana University School of Medicine, Indianapolis, IN 46202, USA; hanchen@iu.edu 2 Greehey Children’s Cancer Research Institute, The University of Texas Health Science Center at San Antonio, San Antonio, TX 78229, USA; zou@uthscsa.edu (Y.Z.); datgarcia5@sbcglobal.net (D.G.); laiz@uthscsa.edu (Z.L.) 4 Diabetes Research Center, Division of Endocrinology, Department of Medicine, Indiana University School of Medicine, Indianapolis, IN 46202, USA; konot@iu.edu (T.K.); cevansmo@iu.edu (C.E.-M.) 3 Department of Pharmacology, Yale Universit
AuthorAffiliation_xml	– name: 3 Department of Pharmacology, Yale University School of Medicine, New Haven, CT 06520, USA; kennyqiu@live.com – name: 9 Department of Surgery, Indiana University School of Medicine, Indianapolis, IN 46202, USA; yongwd@hotmail.com – name: 8 Department of Biochemistry and Molecular Biology, Indiana University School of Medicine, Indianapolis, IN 46202, USA – name: 4 Diabetes Research Center, Division of Endocrinology, Department of Medicine, Indiana University School of Medicine, Indianapolis, IN 46202, USA; konot@iu.edu (T.K.); cevansmo@iu.edu (C.E.-M.) – name: 5 Department Pharmacology and Toxicology, Indiana University School of Medicine, Indianapolis, IN 46202, USA; guo14@iu.edu (C.G.); ym9@iu.edu (Y.-Y.M.) – name: 7 Roudebush Veterans Administration Medical Center, Indianapolis, IN 46202, USA – name: 6 Department Medical and Molecular Genetics, Indiana University School of Medicine, Indianapolis, IN 46202, USA; hanchen@iu.edu – name: 1 Division of Gastroenterology and Hepatology, Department of Medicine, Indiana University, Indianapolis, IN 46202, USA; kew5@iu.edu (K.E.W.); tharris1@iu.edu (T.G.); sliangpu@iu.edu (S.L.) – name: 2 Greehey Children’s Cancer Research Institute, The University of Texas Health Science Center at San Antonio, San Antonio, TX 78229, USA; zou@uthscsa.edu (Y.Z.); datgarcia5@sbcglobal.net (D.G.); laiz@uthscsa.edu (Z.L.)
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CitedBy_id	crossref_primary_10_1016_j_ynstr_2025_100762 crossref_primary_10_1038_s41598_025_92400_2 crossref_primary_10_1038_s41386_024_02008_9
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Snippet	High levels of alcohol intake alter brain gene expression and can produce long-lasting effects. FK506-binding protein 51 (FKBP51) encoded by Fkbp5 is a... High levels of alcohol intake alter brain gene expression and can produce long-lasting effects. FK506-binding protein 51 (FKBP51) encoded by is a physical and...
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StartPage	89
SubjectTerms	Alcohol Drinking Alcohol use Alcohol-Related Disorders Animals Axon guidance Axonogenesis Brain research Calcium metabolism Calcium signalling Cell signaling Cellular signal transduction Cellular stress response Cytology Drinking of alcoholic beverages Drug dosages Epigenetics Ethanol Ethanol - pharmacology Female Females Fkbp5 Gender differences Gene expression Genetic aspects Glycine Health aspects Hippocampus Hippocampus (Brain) Injections Laboratory animals Lipid Metabolism Male Metabolic regulation Mice mitochondria Morphology Neurons Neuroprotection Physiological aspects Post-translation Potassium Proteins RNA-seq Sex differences Signal transduction Software Tacrolimus Tacrolimus-binding protein
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Title	Sex-Specific Impact of Fkbp5 on Hippocampal Response to Acute Alcohol Injection: Involvement in Alterations of Metabolism-Related Pathways
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