Role of Compensatory miRNA Networks in Cognitive Recovery from Heart Failure

<b>Background:</b> Heart failure (HF) is associated with an increased risk of cognitive impairment and hippocampal dysfunction, yet the underlying molecular mechanisms remain poorly understood. This study aims to investigate the role of microRNA (miRNA) networks in hippocampus-dependent...

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Main Authors: Verena Gisa, Md Rezaul Islam, Dawid Lbik, Raoul Maximilian Hofmann, Tonatiuh Pena, Dennis Manfred Krüger, Susanne Burkhardt, Anna-Lena Schütz, Farahnaz Sananbenesi, Karl Toischer, Andre Fischer
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Language:English
Published: MDPI AG 2025-06-01
Series:Non-Coding RNA
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Online Access:https://www.mdpi.com/2311-553X/11/3/45
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author Verena Gisa
Md Rezaul Islam
Dawid Lbik
Raoul Maximilian Hofmann
Tonatiuh Pena
Dennis Manfred Krüger
Susanne Burkhardt
Anna-Lena Schütz
Farahnaz Sananbenesi
Karl Toischer
Andre Fischer
author_facet Verena Gisa
Md Rezaul Islam
Dawid Lbik
Raoul Maximilian Hofmann
Tonatiuh Pena
Dennis Manfred Krüger
Susanne Burkhardt
Anna-Lena Schütz
Farahnaz Sananbenesi
Karl Toischer
Andre Fischer
author_sort Verena Gisa
collection DOAJ
description <b>Background:</b> Heart failure (HF) is associated with an increased risk of cognitive impairment and hippocampal dysfunction, yet the underlying molecular mechanisms remain poorly understood. This study aims to investigate the role of microRNA (miRNA) networks in hippocampus-dependent memory recovery in a mouse model of HF. <b>Methods:</b> CaMKIIδC transgenic (TG) mice, a model for HF, were used to assess hippocampal function at 3 and 6 months of age. Memory performance was evaluated using hippocampus-dependent behavioral tasks. Small RNA sequencing was performed to analyze hippocampal miRNA expression profiles across both time points. Bioinformatic analyses identified miRNAs that potentially regulate genes previously implicated in HF-induced cognitive impairment. <b>Results:</b> We have previously shown that at 3 months of age, CaMKIIδC TG mice exhibited significant memory deficits associated with dysregulated hippocampal gene expression. In this study, we showed that these impairments, memory impairment and hippocampal gene expression, were no longer detectable at 6 months, despite persistent cardiac dysfunction. However, small RNA sequencing revealed a dynamic shift in hippocampal miRNA expression, identifying 27 miRNAs as “compensatory miRs” that targeted 73% of the transcripts dysregulated at 3 months but reinstated by 6 months. Notably, miR-181a-5p emerged as a central regulatory hub, with its downregulation coinciding with restored memory function. <b>Conclusions:</b> These findings suggest that miRNA networks contribute to the restoration of hippocampal function in HF despite continued cardiac pathology and provide an important compensatory mechanism towards memory impairment. A better understanding of these compensatory miRNA mechanisms may provide novel therapeutic targets for managing HF-related cognitive dysfunction.
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spelling doaj-art-99e24fec026742be99cd1aee74506b5d2025-08-20T03:27:21ZengMDPI AGNon-Coding RNA2311-553X2025-06-011134510.3390/ncrna11030045Role of Compensatory miRNA Networks in Cognitive Recovery from Heart FailureVerena Gisa0Md Rezaul Islam1Dawid Lbik2Raoul Maximilian Hofmann3Tonatiuh Pena4Dennis Manfred Krüger5Susanne Burkhardt6Anna-Lena Schütz7Farahnaz Sananbenesi8Karl Toischer9Andre Fischer10Department for Epigenetics and Systems Medicine in Neurodegenerative Diseases, German Center for Neurodegenerative Diseases, Von Siebold Street 3A, 37075 Goettingen, GermanyDepartment for Epigenetics and Systems Medicine in Neurodegenerative Diseases, German Center for Neurodegenerative Diseases, Von Siebold Street 3A, 37075 Goettingen, GermanyClinic of Cardiology and Pneumology, Georg-August-University, Robert-Koch Street 38, 37075 Goettingen, GermanyClinic of Cardiology and Pneumology, Georg-August-University, Robert-Koch Street 38, 37075 Goettingen, GermanyDepartment for Epigenetics and Systems Medicine in Neurodegenerative Diseases, German Center for Neurodegenerative Diseases, Von Siebold Street 3A, 37075 Goettingen, GermanyDepartment for Epigenetics and Systems Medicine in Neurodegenerative Diseases, German Center for Neurodegenerative Diseases, Von Siebold Street 3A, 37075 Goettingen, GermanyDepartment for Epigenetics and Systems Medicine in Neurodegenerative Diseases, German Center for Neurodegenerative Diseases, Von Siebold Street 3A, 37075 Goettingen, GermanyResearch Group for Genome Dynamics in Brain Diseases, German Center for Neurodegenerative Diseases, Von Siebold Street 3A, 37075 Göttingen, GermanyResearch Group for Genome Dynamics in Brain Diseases, German Center for Neurodegenerative Diseases, Von Siebold Street 3A, 37075 Göttingen, GermanyClinic of Cardiology and Pneumology, Georg-August-University, Robert-Koch Street 38, 37075 Goettingen, GermanyDepartment for Epigenetics and Systems Medicine in Neurodegenerative Diseases, German Center for Neurodegenerative Diseases, Von Siebold Street 3A, 37075 Goettingen, Germany<b>Background:</b> Heart failure (HF) is associated with an increased risk of cognitive impairment and hippocampal dysfunction, yet the underlying molecular mechanisms remain poorly understood. This study aims to investigate the role of microRNA (miRNA) networks in hippocampus-dependent memory recovery in a mouse model of HF. <b>Methods:</b> CaMKIIδC transgenic (TG) mice, a model for HF, were used to assess hippocampal function at 3 and 6 months of age. Memory performance was evaluated using hippocampus-dependent behavioral tasks. Small RNA sequencing was performed to analyze hippocampal miRNA expression profiles across both time points. Bioinformatic analyses identified miRNAs that potentially regulate genes previously implicated in HF-induced cognitive impairment. <b>Results:</b> We have previously shown that at 3 months of age, CaMKIIδC TG mice exhibited significant memory deficits associated with dysregulated hippocampal gene expression. In this study, we showed that these impairments, memory impairment and hippocampal gene expression, were no longer detectable at 6 months, despite persistent cardiac dysfunction. However, small RNA sequencing revealed a dynamic shift in hippocampal miRNA expression, identifying 27 miRNAs as “compensatory miRs” that targeted 73% of the transcripts dysregulated at 3 months but reinstated by 6 months. Notably, miR-181a-5p emerged as a central regulatory hub, with its downregulation coinciding with restored memory function. <b>Conclusions:</b> These findings suggest that miRNA networks contribute to the restoration of hippocampal function in HF despite continued cardiac pathology and provide an important compensatory mechanism towards memory impairment. A better understanding of these compensatory miRNA mechanisms may provide novel therapeutic targets for managing HF-related cognitive dysfunction.https://www.mdpi.com/2311-553X/11/3/45heart failurecognitive impairmenthippocampal functionMicroRNAtranscriptional homeostasismemory recovery
spellingShingle Verena Gisa
Md Rezaul Islam
Dawid Lbik
Raoul Maximilian Hofmann
Tonatiuh Pena
Dennis Manfred Krüger
Susanne Burkhardt
Anna-Lena Schütz
Farahnaz Sananbenesi
Karl Toischer
Andre Fischer
Role of Compensatory miRNA Networks in Cognitive Recovery from Heart Failure
Non-Coding RNA
heart failure
cognitive impairment
hippocampal function
MicroRNA
transcriptional homeostasis
memory recovery
title Role of Compensatory miRNA Networks in Cognitive Recovery from Heart Failure
title_full Role of Compensatory miRNA Networks in Cognitive Recovery from Heart Failure
title_fullStr Role of Compensatory miRNA Networks in Cognitive Recovery from Heart Failure
title_full_unstemmed Role of Compensatory miRNA Networks in Cognitive Recovery from Heart Failure
title_short Role of Compensatory miRNA Networks in Cognitive Recovery from Heart Failure
title_sort role of compensatory mirna networks in cognitive recovery from heart failure
topic heart failure
cognitive impairment
hippocampal function
MicroRNA
transcriptional homeostasis
memory recovery
url https://www.mdpi.com/2311-553X/11/3/45
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