The pyruvate-lactate axis modulates cardiac hypertrophy and heart failure
The metabolic rewiring of cardiomyocytes is a widely accepted hallmark of heart failure (HF). These metabolic changes include a decrease in mitochondrial pyruvate oxidation and an increased export of lactate. We identify the mitochondrial pyruvate carrier (MPC) and the cellular lactate exporter mono...
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| Published in | Cell metabolism Vol. 33; no. 3; pp. 629 - 648.e10 |
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| Main Authors | , , , , , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Elsevier Inc
02.03.2021
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| Subjects | |
| Online Access | Get full text |
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| Abstract | The metabolic rewiring of cardiomyocytes is a widely accepted hallmark of heart failure (HF). These metabolic changes include a decrease in mitochondrial pyruvate oxidation and an increased export of lactate. We identify the mitochondrial pyruvate carrier (MPC) and the cellular lactate exporter monocarboxylate transporter 4 (MCT4) as pivotal nodes in this metabolic axis. We observed that cardiac assist device-induced myocardial recovery in chronic HF patients was coincident with increased myocardial expression of the MPC. Moreover, the genetic ablation of the MPC in cultured cardiomyocytes and in adult murine hearts was sufficient to induce hypertrophy and HF. Conversely, MPC overexpression attenuated drug-induced hypertrophy in a cell-autonomous manner. We also introduced a novel, highly potent MCT4 inhibitor that mitigated hypertrophy in cultured cardiomyocytes and in mice. Together, we find that alteration of the pyruvate-lactate axis is a fundamental and early feature of cardiac hypertrophy and failure.
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•Myocardial MPC expression coincides with LVAD-mediated recovery in chronic HF patients•Loss of the MPC in cells or mouse hearts is sufficient to induce hypertrophy and HF•MPC overexpression attenuates drug-induced hypertrophy in a cell-autonomous manner•Inhibition of MCT4 can mitigate hypertrophy in cultured cardiomyocytes and in mice
Cluntun et al. identify the pyruvate-lactate axis as a critical node in cardiac homeostasis and health. This axis is maintained by a careful regulation of the disposition of pyruvate, including mitochondrial import and cellular export as lactate. During hypertrophy and heart failure, this balance is disrupted. Regaining this balance by inhibiting MCT4 ameliorated the hypertrophic phenotype. |
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| AbstractList | The metabolic rewiring of cardiomyocytes is a widely accepted hallmark of heart failure (HF). These metabolic changes include a decrease in mitochondrial pyruvate oxidation and an increased export of lactate. We identify the Mitochondrial Pyruvate Carrier (MPC) and the cellular lactate exporter Monocarboxylate Transporter 4 (MCT4), as pivotal nodes in this metabolic axis. We observed that cardiac assist device-induced myocardial recovery in chronic HF patients was coincident with increased myocardial expression of the MPC. Moreover, the genetic ablation of the MPC in cultured cardiomyocytes and in adult murine hearts was sufficient to induce hypertrophy and HF. Conversely, MPC overexpression attenuated drug-induced hypertrophy in a cell-autonomous manner. We also introduced a novel, highly potent MCT4 inhibitor that mitigated hypertrophy in cultured cardiomyocytes and in mice. Together, we find that alteration of the pyruvate-lactate axis is a fundamental and early feature of cardiac hypertrophy and failure.
Cluntun, et al identify the pyruvate-lactate axis as a critical node in cardiac homeostasis and health. This axis is maintained by a careful regulation of the disposition of pyruvate, including mitochondrial import and cellular export as lactate. During hypertrophy and HF, this balance is disrupted. Regaining this balance by inhibiting MCT4 ameliorated the hypertrophic phenotype. The metabolic rewiring of cardiomyocytes is a widely accepted hallmark of heart failure (HF). These metabolic changes include a decrease in mitochondrial pyruvate oxidation and an increased export of lactate. We identify the mitochondrial pyruvate carrier (MPC) and the cellular lactate exporter monocarboxylate transporter 4 (MCT4) as pivotal nodes in this metabolic axis. We observed that cardiac assist device-induced myocardial recovery in chronic HF patients was coincident with increased myocardial expression of the MPC. Moreover, the genetic ablation of the MPC in cultured cardiomyocytes and in adult murine hearts was sufficient to induce hypertrophy and HF. Conversely, MPC overexpression attenuated drug-induced hypertrophy in a cell-autonomous manner. We also introduced a novel, highly potent MCT4 inhibitor that mitigated hypertrophy in cultured cardiomyocytes and in mice. Together, we find that alteration of the pyruvate-lactate axis is a fundamental and early feature of cardiac hypertrophy and failure.The metabolic rewiring of cardiomyocytes is a widely accepted hallmark of heart failure (HF). These metabolic changes include a decrease in mitochondrial pyruvate oxidation and an increased export of lactate. We identify the mitochondrial pyruvate carrier (MPC) and the cellular lactate exporter monocarboxylate transporter 4 (MCT4) as pivotal nodes in this metabolic axis. We observed that cardiac assist device-induced myocardial recovery in chronic HF patients was coincident with increased myocardial expression of the MPC. Moreover, the genetic ablation of the MPC in cultured cardiomyocytes and in adult murine hearts was sufficient to induce hypertrophy and HF. Conversely, MPC overexpression attenuated drug-induced hypertrophy in a cell-autonomous manner. We also introduced a novel, highly potent MCT4 inhibitor that mitigated hypertrophy in cultured cardiomyocytes and in mice. Together, we find that alteration of the pyruvate-lactate axis is a fundamental and early feature of cardiac hypertrophy and failure. The metabolic rewiring of cardiomyocytes is a widely accepted hallmark of heart failure (HF). These metabolic changes include a decrease in mitochondrial pyruvate oxidation and an increased export of lactate. We identify the mitochondrial pyruvate carrier (MPC) and the cellular lactate exporter monocarboxylate transporter 4 (MCT4) as pivotal nodes in this metabolic axis. We observed that cardiac assist device-induced myocardial recovery in chronic HF patients was coincident with increased myocardial expression of the MPC. Moreover, the genetic ablation of the MPC in cultured cardiomyocytes and in adult murine hearts was sufficient to induce hypertrophy and HF. Conversely, MPC overexpression attenuated drug-induced hypertrophy in a cell-autonomous manner. We also introduced a novel, highly potent MCT4 inhibitor that mitigated hypertrophy in cultured cardiomyocytes and in mice. Together, we find that alteration of the pyruvate-lactate axis is a fundamental and early feature of cardiac hypertrophy and failure. The metabolic rewiring of cardiomyocytes is a widely accepted hallmark of heart failure (HF). These metabolic changes include a decrease in mitochondrial pyruvate oxidation and an increased export of lactate. We identify the mitochondrial pyruvate carrier (MPC) and the cellular lactate exporter monocarboxylate transporter 4 (MCT4) as pivotal nodes in this metabolic axis. We observed that cardiac assist device-induced myocardial recovery in chronic HF patients was coincident with increased myocardial expression of the MPC. Moreover, the genetic ablation of the MPC in cultured cardiomyocytes and in adult murine hearts was sufficient to induce hypertrophy and HF. Conversely, MPC overexpression attenuated drug-induced hypertrophy in a cell-autonomous manner. We also introduced a novel, highly potent MCT4 inhibitor that mitigated hypertrophy in cultured cardiomyocytes and in mice. Together, we find that alteration of the pyruvate-lactate axis is a fundamental and early feature of cardiac hypertrophy and failure. [Display omitted] •Myocardial MPC expression coincides with LVAD-mediated recovery in chronic HF patients•Loss of the MPC in cells or mouse hearts is sufficient to induce hypertrophy and HF•MPC overexpression attenuates drug-induced hypertrophy in a cell-autonomous manner•Inhibition of MCT4 can mitigate hypertrophy in cultured cardiomyocytes and in mice Cluntun et al. identify the pyruvate-lactate axis as a critical node in cardiac homeostasis and health. This axis is maintained by a careful regulation of the disposition of pyruvate, including mitochondrial import and cellular export as lactate. During hypertrophy and heart failure, this balance is disrupted. Regaining this balance by inhibiting MCT4 ameliorated the hypertrophic phenotype. |
| Author | Fogarty, Sarah Lettlova, Sandra Tatum, Sean M. Cluntun, Ahmad A. Rutter, Jared Drakos, Stavros G. Skedros, Sophia Navankasattusas, Sutip Van Ry, Tyler Swiatek, Wojciech I. McKellar, Stephen H. Berg, Jordan A. Diakos, Nikolaos A. Bott, Alex J. Parnell, K. Mark Luo, Bai Krokidi, Aspasia Thodou Shankar, Thirupura S. Badolia, Rachit Merx, Shannon Cox, James E. Olson, Kristofor A. Yu, Xuejing Cunningham, Corey N. Holland, William L. Taleb, Iosif Ducker, Gregory S. |
| AuthorAffiliation | 3 Vettore Biosciences, 1700 Owens Street Suite 515, San Francisco, CA 94158, USA 1 Department of Biochemistry, University of Utah, Salt Lake City, UT 84132, USA 7 Drug Discovery Core Facility, University of Utah, Salt Lake City, UT 84112, USA 5 Metabolomics, Proteomics and Mass Spectrometry Core Facility, University of Utah, Salt Lake City, UT 84112, USA 2 Nora Eccles Harrison Cardiovascular Research and Training Institute, University of Utah, Salt Lake City, UT 84112, USA 4 Department of Nutrition and Integrative Physiology and the Diabetes and Metabolism Research Center, University of Utah, Salt Lake City, UT 84112, USA 13 Lead Contact 8 U.T.A.H. (Utah Transplant Affiliated Hospitals) Cardiac Transplant Program: University of Utah Healthcare and School of Medicine, Intermountain Medical Center, Salt Lake VA (Veterans Affairs) Health Care System, Salt Lake City, UT, USA 10 These authors contributed equally 9 Howard Hughes Medical Institute, University of Utah School of Medicine, Salt Lake City |
| AuthorAffiliation_xml | – name: 7 Drug Discovery Core Facility, University of Utah, Salt Lake City, UT 84112, USA – name: 4 Department of Nutrition and Integrative Physiology and the Diabetes and Metabolism Research Center, University of Utah, Salt Lake City, UT 84112, USA – name: 12 Present address: Department of Surgery and Perioperative Care, Dell Medical School, University of Texas, Austin, TX 78712, USA – name: 13 Lead Contact – name: 3 Vettore Biosciences, 1700 Owens Street Suite 515, San Francisco, CA 94158, USA – name: 2 Nora Eccles Harrison Cardiovascular Research and Training Institute, University of Utah, Salt Lake City, UT 84112, USA – name: 8 U.T.A.H. (Utah Transplant Affiliated Hospitals) Cardiac Transplant Program: University of Utah Healthcare and School of Medicine, Intermountain Medical Center, Salt Lake VA (Veterans Affairs) Health Care System, Salt Lake City, UT, USA – name: 10 These authors contributed equally – name: 1 Department of Biochemistry, University of Utah, Salt Lake City, UT 84132, USA – name: 11 Present address: Division of Cardiology, Tufts Medical Center, Boston, MA 02111, USA – name: 6 University of Utah, School of Medicine, Salt Lake City, Utah; Division of Cardiothoracic Surgery, Department of Surgery, Salt Lake City, UT 84132, USA – name: 9 Howard Hughes Medical Institute, University of Utah School of Medicine, Salt Lake City, UT 84132, USA – name: 5 Metabolomics, Proteomics and Mass Spectrometry Core Facility, University of Utah, Salt Lake City, UT 84112, USA |
| Author_xml | – sequence: 1 givenname: Ahmad A. surname: Cluntun fullname: Cluntun, Ahmad A. organization: Department of Biochemistry, University of Utah, Salt Lake City, UT 84132, USA – sequence: 2 givenname: Rachit surname: Badolia fullname: Badolia, Rachit organization: Nora Eccles Harrison Cardiovascular Research and Training Institute, University of Utah, Salt Lake City, UT 84112, USA – sequence: 3 givenname: Sandra surname: Lettlova fullname: Lettlova, Sandra organization: Department of Biochemistry, University of Utah, Salt Lake City, UT 84132, USA – sequence: 4 givenname: K. Mark surname: Parnell fullname: Parnell, K. Mark organization: Vettore Biosciences, 1700 Owens Street Suite 515, San Francisco, CA 94158, USA – sequence: 5 givenname: Thirupura S. surname: Shankar fullname: Shankar, Thirupura S. organization: Nora Eccles Harrison Cardiovascular Research and Training Institute, University of Utah, Salt Lake City, UT 84112, USA – sequence: 6 givenname: Nikolaos A. surname: Diakos fullname: Diakos, Nikolaos A. organization: Nora Eccles Harrison Cardiovascular Research and Training Institute, University of Utah, Salt Lake City, UT 84112, USA – sequence: 7 givenname: Kristofor A. surname: Olson fullname: Olson, Kristofor A. organization: Department of Biochemistry, University of Utah, Salt Lake City, UT 84132, USA – sequence: 8 givenname: Iosif surname: Taleb fullname: Taleb, Iosif organization: Nora Eccles Harrison Cardiovascular Research and Training Institute, University of Utah, Salt Lake City, UT 84112, USA – sequence: 9 givenname: Sean M. surname: Tatum fullname: Tatum, Sean M. organization: Department of Nutrition and Integrative Physiology and the Diabetes and Metabolism Research Center, University of Utah, Salt Lake City, UT 84112, USA – sequence: 10 givenname: Jordan A. surname: Berg fullname: Berg, Jordan A. organization: Department of Biochemistry, University of Utah, Salt Lake City, UT 84132, USA – sequence: 11 givenname: Corey N. surname: Cunningham fullname: Cunningham, Corey N. organization: Department of Biochemistry, University of Utah, Salt Lake City, UT 84132, USA – sequence: 12 givenname: Tyler surname: Van Ry fullname: Van Ry, Tyler organization: Department of Biochemistry, University of Utah, Salt Lake City, UT 84132, USA – sequence: 13 givenname: Alex J. surname: Bott fullname: Bott, Alex J. organization: Department of Biochemistry, University of Utah, Salt Lake City, UT 84132, USA – sequence: 14 givenname: Aspasia Thodou surname: Krokidi fullname: Krokidi, Aspasia Thodou organization: Nora Eccles Harrison Cardiovascular Research and Training Institute, University of Utah, Salt Lake City, UT 84112, USA – sequence: 15 givenname: Sarah surname: Fogarty fullname: Fogarty, Sarah organization: Department of Biochemistry, University of Utah, Salt Lake City, UT 84132, USA – sequence: 16 givenname: Sophia surname: Skedros fullname: Skedros, Sophia organization: Nora Eccles Harrison Cardiovascular Research and Training Institute, University of Utah, Salt Lake City, UT 84112, USA – sequence: 17 givenname: Wojciech I. surname: Swiatek fullname: Swiatek, Wojciech I. organization: Department of Biochemistry, University of Utah, Salt Lake City, UT 84132, USA – sequence: 18 givenname: Xuejing surname: Yu fullname: Yu, Xuejing organization: University of Utah, School of Medicine, Salt Lake City, UT 84132, USA – sequence: 19 givenname: Bai surname: Luo fullname: Luo, Bai organization: Drug Discovery Core Facility, University of Utah, Salt Lake City, UT 84112, USA – sequence: 20 givenname: Shannon surname: Merx fullname: Merx, Shannon organization: Vettore Biosciences, 1700 Owens Street Suite 515, San Francisco, CA 94158, USA – sequence: 21 givenname: Sutip surname: Navankasattusas fullname: Navankasattusas, Sutip organization: Nora Eccles Harrison Cardiovascular Research and Training Institute, University of Utah, Salt Lake City, UT 84112, USA – sequence: 22 givenname: James E. surname: Cox fullname: Cox, James E. organization: Department of Biochemistry, University of Utah, Salt Lake City, UT 84132, USA – sequence: 23 givenname: Gregory S. surname: Ducker fullname: Ducker, Gregory S. organization: Department of Biochemistry, University of Utah, Salt Lake City, UT 84132, USA – sequence: 24 givenname: William L. surname: Holland fullname: Holland, William L. organization: Department of Nutrition and Integrative Physiology and the Diabetes and Metabolism Research Center, University of Utah, Salt Lake City, UT 84112, USA – sequence: 25 givenname: Stephen H. surname: McKellar fullname: McKellar, Stephen H. organization: University of Utah, School of Medicine, Salt Lake City, UT 84132, USA – sequence: 26 givenname: Jared surname: Rutter fullname: Rutter, Jared email: rutter@biochem.utah.edu organization: Department of Biochemistry, University of Utah, Salt Lake City, UT 84132, USA – sequence: 27 givenname: Stavros G. surname: Drakos fullname: Drakos, Stavros G. email: stavros.drakos@hsc.utah.edu organization: Nora Eccles Harrison Cardiovascular Research and Training Institute, University of Utah, Salt Lake City, UT 84112, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/33333007$$D View this record in MEDLINE/PubMed |
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| Snippet | The metabolic rewiring of cardiomyocytes is a widely accepted hallmark of heart failure (HF). These metabolic changes include a decrease in mitochondrial... |
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| SubjectTerms | Animals Anion Transport Proteins - antagonists & inhibitors Anion Transport Proteins - genetics Anion Transport Proteins - metabolism cardiac metabolism Cardiomegaly - chemically induced Cardiomegaly - complications Cardiomegaly - pathology heart failure Heart Failure - etiology Heart Failure - pathology Heart-Assist Devices Humans hypertrophy lactate Lactic Acid - metabolism LVAD MCT4 Membrane Potential, Mitochondrial Mice Mice, Inbred C57BL Mice, Knockout mitochondria Mitochondria - metabolism Mitochondrial Membrane Transport Proteins - antagonists & inhibitors Mitochondrial Membrane Transport Proteins - genetics Mitochondrial Membrane Transport Proteins - metabolism Monocarboxylic Acid Transporters - antagonists & inhibitors Monocarboxylic Acid Transporters - genetics Monocarboxylic Acid Transporters - metabolism MPC Muscle Proteins - antagonists & inhibitors Muscle Proteins - metabolism Myocytes, Cardiac - cytology Myocytes, Cardiac - metabolism pyruvate Pyruvic Acid - metabolism Reactive Oxygen Species - metabolism RNA Interference RNA, Small Interfering - metabolism VB124 Ventricular Function, Left - physiology |
| Title | The pyruvate-lactate axis modulates cardiac hypertrophy and heart failure |
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