The impact of exercise on mitochondrial dynamics and the role of Drp1 in exercise performance and training adaptations in skeletal muscle
Mitochondria are organelles primarily responsible for energy production, and recent evidence indicates that alterations in size, shape, location, and quantity occur in response to fluctuations in energy supply and demand. We tested the impact of acute and chronic exercise on mitochondrial dynamics s...
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| Published in | Molecular metabolism (Germany) Vol. 21; pp. 51 - 67 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
Germany
Elsevier GmbH
01.03.2019
Elsevier |
| Subjects | |
| Online Access | Get full text |
| ISSN | 2212-8778 2212-8778 |
| DOI | 10.1016/j.molmet.2018.11.012 |
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| Abstract | Mitochondria are organelles primarily responsible for energy production, and recent evidence indicates that alterations in size, shape, location, and quantity occur in response to fluctuations in energy supply and demand. We tested the impact of acute and chronic exercise on mitochondrial dynamics signaling and determined the impact of the mitochondrial fission regulator Dynamin related protein (Drp)1 on exercise performance and muscle adaptations to training.
Wildtype and muscle-specific Drp1 heterozygote (mDrp1+/−) mice, as well as dysglycemic (DG) and healthy normoglycemic men (control) performed acute and chronic exercise. The Hybrid Mouse Diversity Panel, including 100 murine strains of recombinant inbred mice, was used to identify muscle Dnm1L (encodes Drp1)-gene relationships.
Endurance exercise impacted all aspects of the mitochondrial life cycle, i.e. fission-fusion, biogenesis, and mitophagy. Dnm1L gene expression and Drp1Ser616 phosphorylation were markedly increased by acute exercise and declined to baseline during post-exercise recovery. Dnm1L expression was strongly associated with transcripts known to regulate mitochondrial metabolism and adaptations to exercise. Exercise increased the expression of DNM1L in skeletal muscle of healthy control and DG subjects, despite a 15% ↓(P = 0.01) in muscle DNM1L expression in DG at baseline. To interrogate the role of Dnm1L further, we exercise trained male mDrp1+/− mice and found that Drp1 deficiency reduced muscle endurance and running performance, and altered muscle adaptations in response to exercise training.
Our findings highlight the importance of mitochondrial dynamics, specifically Drp1 signaling, in the regulation of exercise performance and adaptations to endurance exercise training.
•Skeletal muscle expression of the mitochondrial fission regulator Dnm1L (encodes Drp1) is increased in mice and men during acute exercise.•DNM1L expression is reduced in muscle from dysglycemic vs. normoglycemic men at rest and during exercise.•Phospho-Drp1Ser616 (activation) is elevated in muscle from male and female mice during acute exercise and returns to baseline during post-exercise recovery.•Dnm1L expression is critical for exercise performance and muscle adaptations in response to endurance exercise training. |
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| AbstractList | •
Skeletal muscle expression of the mitochondrial fission regulator
Dnm1L
(encodes Drp1) is increased in mice and men during acute exercise.
•
DNM1L
expression is reduced in muscle from dysglycemic vs. normoglycemic men at rest and during exercise.
•
Phospho-Drp1
Ser616
(activation) is elevated in muscle from male and female mice during acute exercise and returns to baseline during post-exercise recovery.
•
Dnm1L
expression is critical for exercise performance and muscle adaptations in response to endurance exercise training. Mitochondria are organelles primarily responsible for energy production, and recent evidence indicates that alterations in size, shape, location, and quantity occur in response to fluctuations in energy supply and demand. We tested the impact of acute and chronic exercise on mitochondrial dynamics signaling and determined the impact of the mitochondrial fission regulator Dynamin related protein (Drp)1 on exercise performance and muscle adaptations to training. Wildtype and muscle-specific Drp1 heterozygote (mDrp1+/−) mice, as well as dysglycemic (DG) and healthy normoglycemic men (control) performed acute and chronic exercise. The Hybrid Mouse Diversity Panel, including 100 murine strains of recombinant inbred mice, was used to identify muscle Dnm1L (encodes Drp1)-gene relationships. Endurance exercise impacted all aspects of the mitochondrial life cycle, i.e. fission-fusion, biogenesis, and mitophagy. Dnm1L gene expression and Drp1Ser616 phosphorylation were markedly increased by acute exercise and declined to baseline during post-exercise recovery. Dnm1L expression was strongly associated with transcripts known to regulate mitochondrial metabolism and adaptations to exercise. Exercise increased the expression of DNM1L in skeletal muscle of healthy control and DG subjects, despite a 15% ↓(P = 0.01) in muscle DNM1L expression in DG at baseline. To interrogate the role of Dnm1L further, we exercise trained male mDrp1+/− mice and found that Drp1 deficiency reduced muscle endurance and running performance, and altered muscle adaptations in response to exercise training. Our findings highlight the importance of mitochondrial dynamics, specifically Drp1 signaling, in the regulation of exercise performance and adaptations to endurance exercise training. •Skeletal muscle expression of the mitochondrial fission regulator Dnm1L (encodes Drp1) is increased in mice and men during acute exercise.•DNM1L expression is reduced in muscle from dysglycemic vs. normoglycemic men at rest and during exercise.•Phospho-Drp1Ser616 (activation) is elevated in muscle from male and female mice during acute exercise and returns to baseline during post-exercise recovery.•Dnm1L expression is critical for exercise performance and muscle adaptations in response to endurance exercise training. Mitochondria are organelles primarily responsible for energy production, and recent evidence indicates that alterations in size, shape, location, and quantity occur in response to fluctuations in energy supply and demand. We tested the impact of acute and chronic exercise on mitochondrial dynamics signaling and determined the impact of the mitochondrial fission regulator Dynamin related protein (Drp)1 on exercise performance and muscle adaptations to training.OBJECTIVEMitochondria are organelles primarily responsible for energy production, and recent evidence indicates that alterations in size, shape, location, and quantity occur in response to fluctuations in energy supply and demand. We tested the impact of acute and chronic exercise on mitochondrial dynamics signaling and determined the impact of the mitochondrial fission regulator Dynamin related protein (Drp)1 on exercise performance and muscle adaptations to training.Wildtype and muscle-specific Drp1 heterozygote (mDrp1+/-) mice, as well as dysglycemic (DG) and healthy normoglycemic men (control) performed acute and chronic exercise. The Hybrid Mouse Diversity Panel, including 100 murine strains of recombinant inbred mice, was used to identify muscle Dnm1L (encodes Drp1)-gene relationships.METHODSWildtype and muscle-specific Drp1 heterozygote (mDrp1+/-) mice, as well as dysglycemic (DG) and healthy normoglycemic men (control) performed acute and chronic exercise. The Hybrid Mouse Diversity Panel, including 100 murine strains of recombinant inbred mice, was used to identify muscle Dnm1L (encodes Drp1)-gene relationships.Endurance exercise impacted all aspects of the mitochondrial life cycle, i.e. fission-fusion, biogenesis, and mitophagy. Dnm1L gene expression and Drp1Ser616 phosphorylation were markedly increased by acute exercise and declined to baseline during post-exercise recovery. Dnm1L expression was strongly associated with transcripts known to regulate mitochondrial metabolism and adaptations to exercise. Exercise increased the expression of DNM1L in skeletal muscle of healthy control and DG subjects, despite a 15% ↓(P = 0.01) in muscle DNM1L expression in DG at baseline. To interrogate the role of Dnm1L further, we exercise trained male mDrp1+/- mice and found that Drp1 deficiency reduced muscle endurance and running performance, and altered muscle adaptations in response to exercise training.RESULTSEndurance exercise impacted all aspects of the mitochondrial life cycle, i.e. fission-fusion, biogenesis, and mitophagy. Dnm1L gene expression and Drp1Ser616 phosphorylation were markedly increased by acute exercise and declined to baseline during post-exercise recovery. Dnm1L expression was strongly associated with transcripts known to regulate mitochondrial metabolism and adaptations to exercise. Exercise increased the expression of DNM1L in skeletal muscle of healthy control and DG subjects, despite a 15% ↓(P = 0.01) in muscle DNM1L expression in DG at baseline. To interrogate the role of Dnm1L further, we exercise trained male mDrp1+/- mice and found that Drp1 deficiency reduced muscle endurance and running performance, and altered muscle adaptations in response to exercise training.Our findings highlight the importance of mitochondrial dynamics, specifically Drp1 signaling, in the regulation of exercise performance and adaptations to endurance exercise training.CONCLUSIONOur findings highlight the importance of mitochondrial dynamics, specifically Drp1 signaling, in the regulation of exercise performance and adaptations to endurance exercise training. Objective Mitochondria are organelles primarily responsible for energy production, and recent evidence indicates that alterations in size, shape, location, and quantity occur in response to fluctuations in energy supply and demand. We tested the impact of acute and chronic exercise on mitochondrial dynamics signaling and determined the impact of the mitochondrial fission regulator Dynamin related protein (Drp)1 on exercise performance and muscle adaptations to training. Methods Wildtype and muscle-specific Drp1 heterozygote (mDrp1+/−) mice, as well as dysglycemic (DG) and healthy normoglycemic men (control) performed acute and chronic exercise. The Hybrid Mouse Diversity Panel, including 100 murine strains of recombinant inbred mice, was used to identify muscle Dnm1L (encodes Drp1)-gene relationships. Results Endurance exercise impacted all aspects of the mitochondrial life cycle, i.e. fission-fusion, biogenesis, and mitophagy. Dnm1L gene expression and Drp1Ser616 phosphorylation were markedly increased by acute exercise and declined to baseline during post-exercise recovery. Dnm1L expression was strongly associated with transcripts known to regulate mitochondrial metabolism and adaptations to exercise. Exercise increased the expression of DNM1L in skeletal muscle of healthy control and DG subjects, despite a 15% ↓(P = 0.01) in muscle DNM1L expression in DG at baseline. To interrogate the role of Dnm1L further, we exercise trained male mDrp1+/− mice and found that Drp1 deficiency reduced muscle endurance and running performance, and altered muscle adaptations in response to exercise training. Conclusion Our findings highlight the importance of mitochondrial dynamics, specifically Drp1 signaling, in the regulation of exercise performance and adaptations to endurance exercise training. Objective: Mitochondria are organelles primarily responsible for energy production, and recent evidence indicates that alterations in size, shape, location, and quantity occur in response to fluctuations in energy supply and demand. We tested the impact of acute and chronic exercise on mitochondrial dynamics signaling and determined the impact of the mitochondrial fission regulator Dynamin related protein (Drp)1 on exercise performance and muscle adaptations to training. Methods: Wildtype and muscle-specific Drp1 heterozygote (mDrp1+/−) mice, as well as dysglycemic (DG) and healthy normoglycemic men (control) performed acute and chronic exercise. The Hybrid Mouse Diversity Panel, including 100 murine strains of recombinant inbred mice, was used to identify muscle Dnm1L (encodes Drp1)-gene relationships. Results: Endurance exercise impacted all aspects of the mitochondrial life cycle, i.e. fission-fusion, biogenesis, and mitophagy. Dnm1L gene expression and Drp1Ser616 phosphorylation were markedly increased by acute exercise and declined to baseline during post-exercise recovery. Dnm1L expression was strongly associated with transcripts known to regulate mitochondrial metabolism and adaptations to exercise. Exercise increased the expression of DNM1L in skeletal muscle of healthy control and DG subjects, despite a 15% ↓(P = 0.01) in muscle DNM1L expression in DG at baseline. To interrogate the role of Dnm1L further, we exercise trained male mDrp1+/− mice and found that Drp1 deficiency reduced muscle endurance and running performance, and altered muscle adaptations in response to exercise training. Conclusion: Our findings highlight the importance of mitochondrial dynamics, specifically Drp1 signaling, in the regulation of exercise performance and adaptations to endurance exercise training. Keywords: Mitochondrial dynamics, Drp1, Exercise performance, Exercise training Mitochondria are organelles primarily responsible for energy production, and recent evidence indicates that alterations in size, shape, location, and quantity occur in response to fluctuations in energy supply and demand. We tested the impact of acute and chronic exercise on mitochondrial dynamics signaling and determined the impact of the mitochondrial fission regulator Dynamin related protein (Drp)1 on exercise performance and muscle adaptations to training. Wildtype and muscle-specific Drp1 heterozygote (mDrp1 ) mice, as well as dysglycemic (DG) and healthy normoglycemic men (control) performed acute and chronic exercise. The Hybrid Mouse Diversity Panel, including 100 murine strains of recombinant inbred mice, was used to identify muscle Dnm1L (encodes Drp1)-gene relationships. Endurance exercise impacted all aspects of the mitochondrial life cycle, i.e. fission-fusion, biogenesis, and mitophagy. Dnm1L gene expression and Drp1 phosphorylation were markedly increased by acute exercise and declined to baseline during post-exercise recovery. Dnm1L expression was strongly associated with transcripts known to regulate mitochondrial metabolism and adaptations to exercise. Exercise increased the expression of DNM1L in skeletal muscle of healthy control and DG subjects, despite a 15% ↓(P = 0.01) in muscle DNM1L expression in DG at baseline. To interrogate the role of Dnm1L further, we exercise trained male mDrp1 mice and found that Drp1 deficiency reduced muscle endurance and running performance, and altered muscle adaptations in response to exercise training. Our findings highlight the importance of mitochondrial dynamics, specifically Drp1 signaling, in the regulation of exercise performance and adaptations to endurance exercise training. |
| Author | Cory, Kevin Zhou, Zhenqi Shirihai, Orian Moore, Timothy M. Lee, Sindre Strumwasser, Alexander R. Ho, Theodore Ho, Timothy Hevener, Andrea L. Lin, Amanda J. Norheim, Frode Whitney, Kate Lee, Joseph L. Whitelegge, Julian P. Mahata, Sushil K. Kalajian, Nareg Lusis, Aldons J. Turcotte, Lorraine P. Drevon, Christian A. Cohn, Whitaker van der Bliek, Alexander M. Rucker, Daniel H. Seldin, Marcus M. |
| AuthorAffiliation | 9 VA San Diego Healthcare System, San Diego, CA 92161, USA 10 Department of Medicine, University of California, San Diego, La Jolla, CA 92093, USA 8 Department of Endocrinology, Morbid Obesity and Preventive Medicine, Institute of Clinical Medicine, University of Oslo, Oslo, Norway 1 Department of Biological Sciences, Dana & David Dornsife College of Letters, Arts, and Sciences, University of Southern California, CA 90089-0372, USA 3 David Geffen School of Medicine, Department of Psychiatry and Biobehavioral Sciences, The Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, CA 90095, USA 2 David Geffen School of Medicine, Department of Medicine, University of California, Los Angeles, CA 90095, USA 5 David Geffen School of Medicine, Department of Biological Chemistry, University of California, Los Angeles, CA 90095, USA 7 University Department of Nutrition, Institute of Basic Medical Sciences, University of Oslo, Oslo, Norway 4 David Geffen School of Medic |
| AuthorAffiliation_xml | – name: 5 David Geffen School of Medicine, Department of Biological Chemistry, University of California, Los Angeles, CA 90095, USA – name: 6 David Geffen School of Medicine, Microbiology, Immunology, and Molecular Genetics, University of California, Los Angeles, CA 90095, USA – name: 10 Department of Medicine, University of California, San Diego, La Jolla, CA 92093, USA – name: 1 Department of Biological Sciences, Dana & David Dornsife College of Letters, Arts, and Sciences, University of Southern California, CA 90089-0372, USA – name: 8 Department of Endocrinology, Morbid Obesity and Preventive Medicine, Institute of Clinical Medicine, University of Oslo, Oslo, Norway – name: 3 David Geffen School of Medicine, Department of Psychiatry and Biobehavioral Sciences, The Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, CA 90095, USA – name: 11 Iris Cantor-UCLA Women's Health Research Center, Los Angeles, CA 90095, USA – name: 2 David Geffen School of Medicine, Department of Medicine, University of California, Los Angeles, CA 90095, USA – name: 4 David Geffen School of Medicine, Human Genetics, University of California, Los Angeles, CA 90095, USA – name: 9 VA San Diego Healthcare System, San Diego, CA 92161, USA – name: 7 University Department of Nutrition, Institute of Basic Medical Sciences, University of Oslo, Oslo, Norway |
| Author_xml | – sequence: 1 givenname: Timothy M. surname: Moore fullname: Moore, Timothy M. organization: Department of Biological Sciences, Dana & David Dornsife College of Letters, Arts, and Sciences, University of Southern California, CA 90089-0372, USA – sequence: 2 givenname: Zhenqi surname: Zhou fullname: Zhou, Zhenqi organization: David Geffen School of Medicine, Department of Medicine, University of California, Los Angeles, CA 90095, USA – sequence: 3 givenname: Whitaker surname: Cohn fullname: Cohn, Whitaker organization: David Geffen School of Medicine, Department of Psychiatry and Biobehavioral Sciences, The Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, CA 90095, USA – sequence: 4 givenname: Frode surname: Norheim fullname: Norheim, Frode organization: David Geffen School of Medicine, Human Genetics, University of California, Los Angeles, CA 90095, USA – sequence: 5 givenname: Amanda J. surname: Lin fullname: Lin, Amanda J. organization: David Geffen School of Medicine, Department of Medicine, University of California, Los Angeles, CA 90095, USA – sequence: 6 givenname: Nareg surname: Kalajian fullname: Kalajian, Nareg organization: David Geffen School of Medicine, Department of Medicine, University of California, Los Angeles, CA 90095, USA – sequence: 7 givenname: Alexander R. surname: Strumwasser fullname: Strumwasser, Alexander R. organization: David Geffen School of Medicine, Department of Medicine, University of California, Los Angeles, CA 90095, USA – sequence: 8 givenname: Kevin surname: Cory fullname: Cory, Kevin organization: David Geffen School of Medicine, Department of Medicine, University of California, Los Angeles, CA 90095, USA – sequence: 9 givenname: Kate surname: Whitney fullname: Whitney, Kate organization: David Geffen School of Medicine, Department of Medicine, University of California, Los Angeles, CA 90095, USA – sequence: 10 givenname: Theodore orcidid: 0000-0002-2670-0852 surname: Ho fullname: Ho, Theodore organization: David Geffen School of Medicine, Department of Medicine, University of California, Los Angeles, CA 90095, USA – sequence: 11 givenname: Timothy surname: Ho fullname: Ho, Timothy organization: David Geffen School of Medicine, Department of Medicine, University of California, Los Angeles, CA 90095, USA – sequence: 12 givenname: Joseph L. surname: Lee fullname: Lee, Joseph L. organization: David Geffen School of Medicine, Department of Medicine, University of California, Los Angeles, CA 90095, USA – sequence: 13 givenname: Daniel H. surname: Rucker fullname: Rucker, Daniel H. organization: David Geffen School of Medicine, Department of Medicine, University of California, Los Angeles, CA 90095, USA – sequence: 14 givenname: Orian orcidid: 0000-0001-8466-3431 surname: Shirihai fullname: Shirihai, Orian organization: David Geffen School of Medicine, Department of Medicine, University of California, Los Angeles, CA 90095, USA – sequence: 15 givenname: Alexander M. surname: van der Bliek fullname: van der Bliek, Alexander M. organization: David Geffen School of Medicine, Department of Biological Chemistry, University of California, Los Angeles, CA 90095, USA – sequence: 16 givenname: Julian P. surname: Whitelegge fullname: Whitelegge, Julian P. organization: David Geffen School of Medicine, Department of Psychiatry and Biobehavioral Sciences, The Semel Institute for Neuroscience and Human Behavior, University of California, Los Angeles, CA 90095, USA – sequence: 17 givenname: Marcus M. surname: Seldin fullname: Seldin, Marcus M. organization: David Geffen School of Medicine, Human Genetics, University of California, Los Angeles, CA 90095, USA – sequence: 18 givenname: Aldons J. surname: Lusis fullname: Lusis, Aldons J. organization: David Geffen School of Medicine, Human Genetics, University of California, Los Angeles, CA 90095, USA – sequence: 19 givenname: Sindre orcidid: 0000-0002-0670-7555 surname: Lee fullname: Lee, Sindre organization: University Department of Nutrition, Institute of Basic Medical Sciences, University of Oslo, Oslo, Norway – sequence: 20 givenname: Christian A. surname: Drevon fullname: Drevon, Christian A. organization: University Department of Nutrition, Institute of Basic Medical Sciences, University of Oslo, Oslo, Norway – sequence: 21 givenname: Sushil K. surname: Mahata fullname: Mahata, Sushil K. organization: VA San Diego Healthcare System, San Diego, CA 92161, USA – sequence: 22 givenname: Lorraine P. surname: Turcotte fullname: Turcotte, Lorraine P. organization: Department of Biological Sciences, Dana & David Dornsife College of Letters, Arts, and Sciences, University of Southern California, CA 90089-0372, USA – sequence: 23 givenname: Andrea L. surname: Hevener fullname: Hevener, Andrea L. email: ahevener@mednet.ucla.edu organization: David Geffen School of Medicine, Department of Medicine, University of California, Los Angeles, CA 90095, USA |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/30591411$$D View this record in MEDLINE/PubMed |
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| ContentType | Journal Article |
| Copyright | 2018 The Authors Copyright © 2018 The Authors. Published by Elsevier GmbH.. All rights reserved. info:eu-repo/semantics/openAccess 2018 The Authors 2018 |
| Copyright_xml | – notice: 2018 The Authors – notice: Copyright © 2018 The Authors. Published by Elsevier GmbH.. All rights reserved. – notice: info:eu-repo/semantics/openAccess – notice: 2018 The Authors 2018 |
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| Snippet | Mitochondria are organelles primarily responsible for energy production, and recent evidence indicates that alterations in size, shape, location, and quantity... Objective Mitochondria are organelles primarily responsible for energy production, and recent evidence indicates that alterations in size, shape, location, and... • Skeletal muscle expression of the mitochondrial fission regulator Dnm1L (encodes Drp1) is increased in mice and men during acute exercise. • DNM1L expression... Objective: Mitochondria are organelles primarily responsible for energy production, and recent evidence indicates that alterations in size, shape, location,... |
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| StartPage | 51 |
| SubjectTerms | Adaptation, Physiological Adult Aged Animals Blood Glucose - metabolism Drp1 Dynamins - genetics Dynamins - metabolism Exercise performance Exercise training Female Gene Deletion GTP Phosphohydrolases - metabolism Humans Male Mice Mice, Inbred BALB C Mice, Inbred C3H Mice, Inbred C57BL Microtubule-Associated Proteins - metabolism Middle Aged Mitochondria - metabolism Mitochondrial dynamics Mitochondrial Dynamics - physiology Mitochondrial Proteins - metabolism Muscle, Skeletal - physiology Original Phosphorylation Physical Conditioning, Animal - physiology Physical Endurance Physical Functional Performance |
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| Title | The impact of exercise on mitochondrial dynamics and the role of Drp1 in exercise performance and training adaptations in skeletal muscle |
| URI | https://www.clinicalkey.com/#!/content/1-s2.0-S2212877818307865 https://dx.doi.org/10.1016/j.molmet.2018.11.012 https://www.ncbi.nlm.nih.gov/pubmed/30591411 https://www.proquest.com/docview/2161697963 http://hdl.handle.net/10852/67499 https://pubmed.ncbi.nlm.nih.gov/PMC6407367 https://doaj.org/article/f4c435b7db244bd4901d48d7eb8c99e8 |
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