Metabolomics assessment reveals oxidative stress and altered energy production in the heart after ischemic acute kidney injury in mice

Acute kidney injury (AKI) is a systemic disease associated with widespread effects on distant organs, including the heart. Normal cardiac function is dependent on constant ATP generation, and the preferred method of energy production is via oxidative phosphorylation. Following direct ischemic cardia...

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Published in:	Kidney international Vol. 95; no. 3; p. 590
Main Authors:	Fox, Benjamin M, Gil, Hyo-Wook, Kirkbride-Romeo, Lara, Bagchi, Rushita A, Wennersten, Sara A, Haefner, Korey R, Skrypnyk, Nataliya I, Brown, Carolyn N, Soranno, Danielle E, Gist, Katja M, Griffin, Benjamin R, Jovanovich, Anna, Reisz, Julie A, Wither, Matthew J, D'Alessandro, Angelo, Edelstein, Charles L, Clendenen, Nathan, McKinsey, Timothy A, Altmann, Christopher, Faubel, Sarah
Format:	Journal Article
Language:	English
Published:	United States 01.03.2019
Subjects:	Acute Kidney Injury - complications Acute Kidney Injury - etiology Acute Kidney Injury - metabolism Animals Cardio-Renal Syndrome - diagnosis Cardio-Renal Syndrome - etiology Cardio-Renal Syndrome - metabolism Disease Models, Animal Echocardiography Energy Metabolism Heart - diagnostic imaging Heart Failure, Diastolic - diagnosis Heart Failure, Diastolic - etiology Heart Failure, Diastolic - metabolism Humans Ischemia - complications Ischemia - etiology Ischemia - metabolism Kidney - blood supply Kidney - pathology Male Metabolome Metabolomics Mice Myocardium - metabolism Myocardium - pathology Oxidative Stress acute kidney injury organ crosstalk metabolomics cardiorenal syndrome
ISSN:	1523-1755, 1523-1755
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Abstract	Acute kidney injury (AKI) is a systemic disease associated with widespread effects on distant organs, including the heart. Normal cardiac function is dependent on constant ATP generation, and the preferred method of energy production is via oxidative phosphorylation. Following direct ischemic cardiac injury, the cardiac metabolome is characterized by inadequate oxidative phosphorylation, increased oxidative stress, and increased alternate energy utilization. We assessed the impact of ischemic AKI on the metabolomics profile in the heart. Ischemic AKI was induced by 22 minutes of renal pedicle clamping, and 124 metabolites were measured in the heart at 4 hours, 24 hours, and 7 days post-procedure. Forty-one percent of measured metabolites were affected, with the most prominent changes observed 24 hours post-AKI. The post-AKI cardiac metabolome was characterized by amino acid depletion, increased oxidative stress, and evidence of alternative energy production, including a shift to anaerobic forms of energy production. These metabolomic effects were associated with significant cardiac ATP depletion and with echocardiographic evidence of diastolic dysfunction. In the kidney, metabolomics analysis revealed shifts suggestive of energy depletion and oxidative stress, which were reflected systemically in the plasma. This is the first study to examine the cardiac metabolome after AKI, and demonstrates that effects of ischemic AKI on the heart are akin to the effects of direct ischemic cardiac injury.
AbstractList	Acute kidney injury (AKI) is a systemic disease associated with widespread effects on distant organs, including the heart. Normal cardiac function is dependent on constant ATP generation, and the preferred method of energy production is via oxidative phosphorylation. Following direct ischemic cardiac injury, the cardiac metabolome is characterized by inadequate oxidative phosphorylation, increased oxidative stress, and increased alternate energy utilization. We assessed the impact of ischemic AKI on the metabolomics profile in the heart. Ischemic AKI was induced by 22 minutes of renal pedicle clamping, and 124 metabolites were measured in the heart at 4 hours, 24 hours, and 7 days post-procedure. Forty-one percent of measured metabolites were affected, with the most prominent changes observed 24 hours post-AKI. The post-AKI cardiac metabolome was characterized by amino acid depletion, increased oxidative stress, and evidence of alternative energy production, including a shift to anaerobic forms of energy production. These metabolomic effects were associated with significant cardiac ATP depletion and with echocardiographic evidence of diastolic dysfunction. In the kidney, metabolomics analysis revealed shifts suggestive of energy depletion and oxidative stress, which were reflected systemically in the plasma. This is the first study to examine the cardiac metabolome after AKI, and demonstrates that effects of ischemic AKI on the heart are akin to the effects of direct ischemic cardiac injury. Acute kidney injury (AKI) is a systemic disease associated with widespread effects on distant organs, including the heart. Normal cardiac function is dependent on constant ATP generation, and the preferred method of energy production is via oxidative phosphorylation. Following direct ischemic cardiac injury, the cardiac metabolome is characterized by inadequate oxidative phosphorylation, increased oxidative stress, and increased alternate energy utilization. We assessed the impact of ischemic AKI on the metabolomics profile in the heart. Ischemic AKI was induced by 22 minutes of renal pedicle clamping, and 124 metabolites were measured in the heart at 4 hours, 24 hours, and 7 days post-procedure. Forty-one percent of measured metabolites were affected, with the most prominent changes observed 24 hours post-AKI. The post-AKI cardiac metabolome was characterized by amino acid depletion, increased oxidative stress, and evidence of alternative energy production, including a shift to anaerobic forms of energy production. These metabolomic effects were associated with significant cardiac ATP depletion and with echocardiographic evidence of diastolic dysfunction. In the kidney, metabolomics analysis revealed shifts suggestive of energy depletion and oxidative stress, which were reflected systemically in the plasma. This is the first study to examine the cardiac metabolome after AKI, and demonstrates that effects of ischemic AKI on the heart are akin to the effects of direct ischemic cardiac injury.Acute kidney injury (AKI) is a systemic disease associated with widespread effects on distant organs, including the heart. Normal cardiac function is dependent on constant ATP generation, and the preferred method of energy production is via oxidative phosphorylation. Following direct ischemic cardiac injury, the cardiac metabolome is characterized by inadequate oxidative phosphorylation, increased oxidative stress, and increased alternate energy utilization. We assessed the impact of ischemic AKI on the metabolomics profile in the heart. Ischemic AKI was induced by 22 minutes of renal pedicle clamping, and 124 metabolites were measured in the heart at 4 hours, 24 hours, and 7 days post-procedure. Forty-one percent of measured metabolites were affected, with the most prominent changes observed 24 hours post-AKI. The post-AKI cardiac metabolome was characterized by amino acid depletion, increased oxidative stress, and evidence of alternative energy production, including a shift to anaerobic forms of energy production. These metabolomic effects were associated with significant cardiac ATP depletion and with echocardiographic evidence of diastolic dysfunction. In the kidney, metabolomics analysis revealed shifts suggestive of energy depletion and oxidative stress, which were reflected systemically in the plasma. This is the first study to examine the cardiac metabolome after AKI, and demonstrates that effects of ischemic AKI on the heart are akin to the effects of direct ischemic cardiac injury.
Author	Brown, Carolyn N Haefner, Korey R D'Alessandro, Angelo Clendenen, Nathan Gist, Katja M Bagchi, Rushita A Wennersten, Sara A Edelstein, Charles L Altmann, Christopher McKinsey, Timothy A Fox, Benjamin M Skrypnyk, Nataliya I Gil, Hyo-Wook Jovanovich, Anna Griffin, Benjamin R Reisz, Julie A Faubel, Sarah Soranno, Danielle E Kirkbride-Romeo, Lara Wither, Matthew J
Author_xml	– sequence: 1 givenname: Benjamin M surname: Fox fullname: Fox, Benjamin M organization: Division of Renal Diseases and Hypertension, University of Colorado Denver, Aurora, Colorado, USA – sequence: 2 givenname: Hyo-Wook surname: Gil fullname: Gil, Hyo-Wook organization: Division of Renal Diseases and Hypertension, University of Colorado Denver, Aurora, Colorado, USA; Department of Internal Medicine, Soonchunhyang University Cheonan Hospital, Cheonan, Republic of Korea – sequence: 3 givenname: Lara surname: Kirkbride-Romeo fullname: Kirkbride-Romeo, Lara organization: Division of Renal Diseases and Hypertension, University of Colorado Denver, Aurora, Colorado, USA – sequence: 4 givenname: Rushita A surname: Bagchi fullname: Bagchi, Rushita A organization: Division of Cardiology, Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora, Colorado, USA; Consortium for Fibrosis Research and Translation, University of Colorado Anschutz Medical Campus, Aurora, Colorado, USA – sequence: 5 givenname: Sara A surname: Wennersten fullname: Wennersten, Sara A organization: Division of Cardiology, Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora, Colorado, USA; Consortium for Fibrosis Research and Translation, University of Colorado Anschutz Medical Campus, Aurora, Colorado, USA – sequence: 6 givenname: Korey R surname: Haefner fullname: Haefner, Korey R organization: Department of Pediatrics and Bioengineering, University of Colorado Denver, Aurora, Colorado, USA; Division of Pediatric Cardiology, Department of Pediatrics, University of Colorado Denver, Children's Hospital Colorado, Aurora, Colorado, USA – sequence: 7 givenname: Nataliya I surname: Skrypnyk fullname: Skrypnyk, Nataliya I organization: Division of Renal Diseases and Hypertension, University of Colorado Denver, Aurora, Colorado, USA – sequence: 8 givenname: Carolyn N surname: Brown fullname: Brown, Carolyn N organization: Division of Renal Diseases and Hypertension, University of Colorado Denver, Aurora, Colorado, USA – sequence: 9 givenname: Danielle E surname: Soranno fullname: Soranno, Danielle E organization: Department of Pediatrics and Bioengineering, University of Colorado Denver, Aurora, Colorado, USA – sequence: 10 givenname: Katja M surname: Gist fullname: Gist, Katja M organization: Division of Pediatric Cardiology, Department of Pediatrics, University of Colorado Denver, Children's Hospital Colorado, Aurora, Colorado, USA – sequence: 11 givenname: Benjamin R surname: Griffin fullname: Griffin, Benjamin R organization: Division of Renal Diseases and Hypertension, University of Colorado Denver, Aurora, Colorado, USA – sequence: 12 givenname: Anna surname: Jovanovich fullname: Jovanovich, Anna organization: Division of Renal Diseases and Hypertension, University of Colorado Denver, Aurora, Colorado, USA – sequence: 13 givenname: Julie A surname: Reisz fullname: Reisz, Julie A organization: Department of Biochemistry and Molecular Genetics, School of Medicine, University of Colorado Denver, Aurora, Colorado, USA – sequence: 14 givenname: Matthew J surname: Wither fullname: Wither, Matthew J organization: Department of Biochemistry and Molecular Genetics, School of Medicine, University of Colorado Denver, Aurora, Colorado, USA – sequence: 15 givenname: Angelo surname: D'Alessandro fullname: D'Alessandro, Angelo organization: Department of Biochemistry and Molecular Genetics, School of Medicine, University of Colorado Denver, Aurora, Colorado, USA – sequence: 16 givenname: Charles L surname: Edelstein fullname: Edelstein, Charles L organization: Division of Renal Diseases and Hypertension, University of Colorado Denver, Aurora, Colorado, USA; Denver VA Medical Center, Division of Nephrology, Department of Medicine, Denver, Colorado, USA – sequence: 17 givenname: Nathan surname: Clendenen fullname: Clendenen, Nathan organization: Department of Anesthesiology, University of Colorado Anschutz Medical Campus, Aurora, Colorado, USA – sequence: 18 givenname: Timothy A surname: McKinsey fullname: McKinsey, Timothy A organization: Division of Cardiology, Department of Medicine, University of Colorado Anschutz Medical Campus, Aurora, Colorado, USA; Consortium for Fibrosis Research and Translation, University of Colorado Anschutz Medical Campus, Aurora, Colorado, USA – sequence: 19 givenname: Christopher surname: Altmann fullname: Altmann, Christopher organization: Division of Renal Diseases and Hypertension, University of Colorado Denver, Aurora, Colorado, USA – sequence: 20 givenname: Sarah surname: Faubel fullname: Faubel, Sarah email: Sarah.faubel@ucdenver.edu organization: Division of Renal Diseases and Hypertension, University of Colorado Denver, Aurora, Colorado, USA; Denver VA Medical Center, Division of Nephrology, Department of Medicine, Denver, Colorado, USA. Electronic address: Sarah.faubel@ucdenver.edu
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SubjectTerms	Acute Kidney Injury - complications Acute Kidney Injury - etiology Acute Kidney Injury - metabolism Animals Cardio-Renal Syndrome - diagnosis Cardio-Renal Syndrome - etiology Cardio-Renal Syndrome - metabolism Disease Models, Animal Echocardiography Energy Metabolism Heart - diagnostic imaging Heart Failure, Diastolic - diagnosis Heart Failure, Diastolic - etiology Heart Failure, Diastolic - metabolism Humans Ischemia - complications Ischemia - etiology Ischemia - metabolism Kidney - blood supply Kidney - pathology Male Metabolome Metabolomics Mice Myocardium - metabolism Myocardium - pathology Oxidative Stress
Title	Metabolomics assessment reveals oxidative stress and altered energy production in the heart after ischemic acute kidney injury in mice
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