ProteotoxomiRs: Diagnostic and pathologic miRNA signatures for reductive stress induced proteotoxic heart disease

Proteotoxic stress progressively leads to irreversible cardiac abnormalities. Using a mouse model of reductive stress-induced proteotoxic cardiomyopathy, we identified novel microRNA signatures, termed “ProteotoxomiRs,” which reflect stage-specific and transgene-specific responses to proteotoxic str...

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Main Authors: Santhosh Kumar Karthikeyan, Palanisamy Nallasamy, Jarrell Matthew Cleveland, Ahila Arulmani, Ashvanthi Raveendran, Mariam Karimi, Mohammad Owais Ansari, Anil Kumar Challa, Moorthy P. Ponnusamy, Ivor J. Benjamin, Sooryanarayana Varambally, Namakkal S. Rajasekaran
Format: Article
Language:English
Published: Elsevier 2025-04-01
Series:Redox Biology
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Online Access:http://www.sciencedirect.com/science/article/pii/S2213231725000382
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author Santhosh Kumar Karthikeyan
Palanisamy Nallasamy
Jarrell Matthew Cleveland
Ahila Arulmani
Ashvanthi Raveendran
Mariam Karimi
Mohammad Owais Ansari
Anil Kumar Challa
Moorthy P. Ponnusamy
Ivor J. Benjamin
Sooryanarayana Varambally
Namakkal S. Rajasekaran
author_facet Santhosh Kumar Karthikeyan
Palanisamy Nallasamy
Jarrell Matthew Cleveland
Ahila Arulmani
Ashvanthi Raveendran
Mariam Karimi
Mohammad Owais Ansari
Anil Kumar Challa
Moorthy P. Ponnusamy
Ivor J. Benjamin
Sooryanarayana Varambally
Namakkal S. Rajasekaran
author_sort Santhosh Kumar Karthikeyan
collection DOAJ
description Proteotoxic stress progressively leads to irreversible cardiac abnormalities. Using a mouse model of reductive stress-induced proteotoxic cardiomyopathy, we identified novel microRNA signatures, termed “ProteotoxomiRs,” which reflect stage-specific and transgene-specific responses to proteotoxic stress. Seven microRNAs were uniquely linked to the human mutant R120G-αB-Crystallin transgene, indicating their direct association with the pathogenic protein. Additionally, we uncovered two distinct microRNA profiles associated with the early (pre-onset) and late (cardiomyopathy/heart failure) stages of disease progression. Early-stage signatures primarily modulate signaling pathways essential for cardiac health, including mTOR and MAPK, while late-stage signatures reveal regulatory disruptions in calcium signaling and autophagy insufficiency, driving irreversible cardiac damage caused by reductive stress (RS) and proteotoxicity in transgenic mice. These findings reveal stage-specific miRNA biomarkers with potential diagnostic and prognostic value, offering new insights into the molecular underpinnings of proteotoxic cardiac disease. Moreover, our miRNA-mRNA interaction analysis uncovered potential targets unique to the transgene-specific, early, and late stages of the disease, including several promising druggable candidates, warranting further validation for translational applications.
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spelling doaj-art-4a5128cbc29d439d9d1dd596012a36e22025-08-20T02:07:19ZengElsevierRedox Biology2213-23172025-04-018110352510.1016/j.redox.2025.103525ProteotoxomiRs: Diagnostic and pathologic miRNA signatures for reductive stress induced proteotoxic heart diseaseSanthosh Kumar Karthikeyan0Palanisamy Nallasamy1Jarrell Matthew Cleveland2Ahila Arulmani3Ashvanthi Raveendran4Mariam Karimi5Mohammad Owais Ansari6Anil Kumar Challa7Moorthy P. Ponnusamy8Ivor J. Benjamin9Sooryanarayana Varambally10Namakkal S. Rajasekaran11Department of Pathology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, USADepartment of Pathology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, USA; Department of Biochemistry and Molecular Biology, University of Nebraska Medical Center, Omaha, NE, USADepartment of Pathology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, USADepartment of Pathology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, USADepartment of Pathology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, USADepartment of Pathology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, USADepartment of Pathology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, USADepartment of Pathology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, USADepartment of Biochemistry and Molecular Biology, University of Nebraska Medical Center, Omaha, NE, USADepartment of Medicine, Cardiovascular Center, Medical College of Wisconsin, Milwaukee, WI, USADepartment of Pathology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, USA; Corresponding author. Division of Molecular & Cellular Pathology, Department of Pathology, UAB | The University of Alabama at Birmingham, Birmingham, AL, 35294-2180, USA.Department of Pathology, Heersink School of Medicine, University of Alabama at Birmingham, Birmingham, AL, USA; Department of Medicine, University of Utah, School of Medicine, Salt Lake City, UT, USA; Cardiac Aging & Redox Signaling Laboratory, Molecular and Cellular Pathology, Department of Pathology/Center for Free Radical Biology, University of Alabama at Birmingham, Birmingham, AL, USA; Corresponding author. Cardiac Aging & Redox Signaling Laboratory, Center for Free Radical Biology, Division of Molecular & Cellular Pathology, Department of Pathology, UAB | The University of Alabama at Birmingham, BMR2 Room 533|901 19th Street South, Birmingham, AL, 35294-2180, USA.Proteotoxic stress progressively leads to irreversible cardiac abnormalities. Using a mouse model of reductive stress-induced proteotoxic cardiomyopathy, we identified novel microRNA signatures, termed “ProteotoxomiRs,” which reflect stage-specific and transgene-specific responses to proteotoxic stress. Seven microRNAs were uniquely linked to the human mutant R120G-αB-Crystallin transgene, indicating their direct association with the pathogenic protein. Additionally, we uncovered two distinct microRNA profiles associated with the early (pre-onset) and late (cardiomyopathy/heart failure) stages of disease progression. Early-stage signatures primarily modulate signaling pathways essential for cardiac health, including mTOR and MAPK, while late-stage signatures reveal regulatory disruptions in calcium signaling and autophagy insufficiency, driving irreversible cardiac damage caused by reductive stress (RS) and proteotoxicity in transgenic mice. These findings reveal stage-specific miRNA biomarkers with potential diagnostic and prognostic value, offering new insights into the molecular underpinnings of proteotoxic cardiac disease. Moreover, our miRNA-mRNA interaction analysis uncovered potential targets unique to the transgene-specific, early, and late stages of the disease, including several promising druggable candidates, warranting further validation for translational applications.http://www.sciencedirect.com/science/article/pii/S2213231725000382Protein aggregationmiRNAReductive stressCardiomyopathyProteotoxomiRs
spellingShingle Santhosh Kumar Karthikeyan
Palanisamy Nallasamy
Jarrell Matthew Cleveland
Ahila Arulmani
Ashvanthi Raveendran
Mariam Karimi
Mohammad Owais Ansari
Anil Kumar Challa
Moorthy P. Ponnusamy
Ivor J. Benjamin
Sooryanarayana Varambally
Namakkal S. Rajasekaran
ProteotoxomiRs: Diagnostic and pathologic miRNA signatures for reductive stress induced proteotoxic heart disease
Redox Biology
Protein aggregation
miRNA
Reductive stress
Cardiomyopathy
ProteotoxomiRs
title ProteotoxomiRs: Diagnostic and pathologic miRNA signatures for reductive stress induced proteotoxic heart disease
title_full ProteotoxomiRs: Diagnostic and pathologic miRNA signatures for reductive stress induced proteotoxic heart disease
title_fullStr ProteotoxomiRs: Diagnostic and pathologic miRNA signatures for reductive stress induced proteotoxic heart disease
title_full_unstemmed ProteotoxomiRs: Diagnostic and pathologic miRNA signatures for reductive stress induced proteotoxic heart disease
title_short ProteotoxomiRs: Diagnostic and pathologic miRNA signatures for reductive stress induced proteotoxic heart disease
title_sort proteotoxomirs diagnostic and pathologic mirna signatures for reductive stress induced proteotoxic heart disease
topic Protein aggregation
miRNA
Reductive stress
Cardiomyopathy
ProteotoxomiRs
url http://www.sciencedirect.com/science/article/pii/S2213231725000382
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