Exercise training reverses cancer-induced oxidative stress and decrease in muscle COPS2/TRIP15/ALIEN
We tested the hypothesis that exercise training would attenuate metabolic impairment in a model of severe cancer cachexia. We used multiple in vivo and in vitro methods to explore the mechanisms underlying the beneficial effects induced by exercise training in tumor-bearing rats. Exercise training i...
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| Published in | Molecular metabolism (Germany) Vol. 39; p. 101012 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
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Germany
Elsevier GmbH
01.09.2020
Elsevier |
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| Abstract | We tested the hypothesis that exercise training would attenuate metabolic impairment in a model of severe cancer cachexia.
We used multiple in vivo and in vitro methods to explore the mechanisms underlying the beneficial effects induced by exercise training in tumor-bearing rats.
Exercise training improved running capacity, prolonged lifespan, reduced oxidative stress, and normalized muscle mass and contractile function in tumor-bearing rats. An unbiased proteomic screening revealed COP9 signalosome complex subunit 2 (COPS2) as one of the most downregulated proteins in skeletal muscle at the early stage of cancer cachexia. Exercise training normalized muscle COPS2 protein expression in tumor-bearing rats and mice. Lung cancer patients with low endurance capacity had low muscle COPS2 protein expression as compared to age-matched control subjects. To test whether decrease in COPS2 protein levels could aggravate or be an intrinsic compensatory mechanism to protect myotubes from cancer effects, we performed experiments in vitro using primary myotubes. COPS2 knockdown in human myotubes affected multiple cellular pathways, including regulation of actin cytoskeleton. Incubation of cancer-conditioned media in mouse myotubes decreased F-actin expression, which was partially restored by COPS2 knockdown. Direct repeat 4 (DR4) response elements have been shown to positively regulate gene expression. COPS2 overexpression decreased the DR4 activity in mouse myoblasts, and COPS2 knockdown inhibited the effects of cancer-conditioned media on DR4 activity.
These studies demonstrated that exercise training may be an important adjuvant therapy to counteract cancer cachexia and uncovered novel mechanisms involving COPS2 to regulate myotube homeostasis in cancer cachexia.
•Exercise training prolongs lifespan, reduces oxidative stress, and improves skeletal muscle function in tumor-bearing rats.•Muscle COP9 signalosome complex subunit 2 (COPS2) protein is downregulated in cancer cachexia.•Exercise training restores COPS2 protein expression to control levels.•Cancer-conditioned media decreased F-actin expression in myotubes, which is partially restored by COPS2 knockdown.•COPS2 overexpression decreases DR4 activity and COPS2 knockdown inhibits cancer-conditioned media effects on DR4 activity. |
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| AbstractList | Objective: We tested the hypothesis that exercise training would attenuate metabolic impairment in a model of severe cancer cachexia. Methods: We used multiple in vivo and in vitro methods to explore the mechanisms underlying the beneficial effects induced by exercise training in tumor-bearing rats. Results: Exercise training improved running capacity, prolonged lifespan, reduced oxidative stress, and normalized muscle mass and contractile function in tumor-bearing rats. An unbiased proteomic screening revealed COP9 signalosome complex subunit 2 (COPS2) as one of the most downregulated proteins in skeletal muscle at the early stage of cancer cachexia. Exercise training normalized muscle COPS2 protein expression in tumor-bearing rats and mice. Lung cancer patients with low endurance capacity had low muscle COPS2 protein expression as compared to age-matched control subjects. To test whether decrease in COPS2 protein levels could aggravate or be an intrinsic compensatory mechanism to protect myotubes from cancer effects, we performed experiments in vitro using primary myotubes. COPS2 knockdown in human myotubes affected multiple cellular pathways, including regulation of actin cytoskeleton. Incubation of cancer-conditioned media in mouse myotubes decreased F-actin expression, which was partially restored by COPS2 knockdown. Direct repeat 4 (DR4) response elements have been shown to positively regulate gene expression. COPS2 overexpression decreased the DR4 activity in mouse myoblasts, and COPS2 knockdown inhibited the effects of cancer-conditioned media on DR4 activity. Conclusions: These studies demonstrated that exercise training may be an important adjuvant therapy to counteract cancer cachexia and uncovered novel mechanisms involving COPS2 to regulate myotube homeostasis in cancer cachexia. We tested the hypothesis that exercise training would attenuate metabolic impairment in a model of severe cancer cachexia.OBJECTIVEWe tested the hypothesis that exercise training would attenuate metabolic impairment in a model of severe cancer cachexia.We used multiple in vivo and in vitro methods to explore the mechanisms underlying the beneficial effects induced by exercise training in tumor-bearing rats.METHODSWe used multiple in vivo and in vitro methods to explore the mechanisms underlying the beneficial effects induced by exercise training in tumor-bearing rats.Exercise training improved running capacity, prolonged lifespan, reduced oxidative stress, and normalized muscle mass and contractile function in tumor-bearing rats. An unbiased proteomic screening revealed COP9 signalosome complex subunit 2 (COPS2) as one of the most downregulated proteins in skeletal muscle at the early stage of cancer cachexia. Exercise training normalized muscle COPS2 protein expression in tumor-bearing rats and mice. Lung cancer patients with low endurance capacity had low muscle COPS2 protein expression as compared to age-matched control subjects. To test whether decrease in COPS2 protein levels could aggravate or be an intrinsic compensatory mechanism to protect myotubes from cancer effects, we performed experiments in vitro using primary myotubes. COPS2 knockdown in human myotubes affected multiple cellular pathways, including regulation of actin cytoskeleton. Incubation of cancer-conditioned media in mouse myotubes decreased F-actin expression, which was partially restored by COPS2 knockdown. Direct repeat 4 (DR4) response elements have been shown to positively regulate gene expression. COPS2 overexpression decreased the DR4 activity in mouse myoblasts, and COPS2 knockdown inhibited the effects of cancer-conditioned media on DR4 activity.RESULTSExercise training improved running capacity, prolonged lifespan, reduced oxidative stress, and normalized muscle mass and contractile function in tumor-bearing rats. An unbiased proteomic screening revealed COP9 signalosome complex subunit 2 (COPS2) as one of the most downregulated proteins in skeletal muscle at the early stage of cancer cachexia. Exercise training normalized muscle COPS2 protein expression in tumor-bearing rats and mice. Lung cancer patients with low endurance capacity had low muscle COPS2 protein expression as compared to age-matched control subjects. To test whether decrease in COPS2 protein levels could aggravate or be an intrinsic compensatory mechanism to protect myotubes from cancer effects, we performed experiments in vitro using primary myotubes. COPS2 knockdown in human myotubes affected multiple cellular pathways, including regulation of actin cytoskeleton. Incubation of cancer-conditioned media in mouse myotubes decreased F-actin expression, which was partially restored by COPS2 knockdown. Direct repeat 4 (DR4) response elements have been shown to positively regulate gene expression. COPS2 overexpression decreased the DR4 activity in mouse myoblasts, and COPS2 knockdown inhibited the effects of cancer-conditioned media on DR4 activity.These studies demonstrated that exercise training may be an important adjuvant therapy to counteract cancer cachexia and uncovered novel mechanisms involving COPS2 to regulate myotube homeostasis in cancer cachexia.CONCLUSIONSThese studies demonstrated that exercise training may be an important adjuvant therapy to counteract cancer cachexia and uncovered novel mechanisms involving COPS2 to regulate myotube homeostasis in cancer cachexia. • Exercise training prolongs lifespan, reduces oxidative stress, and improves skeletal muscle function in tumor-bearing rats. • Muscle COP9 signalosome complex subunit 2 (COPS2) protein is downregulated in cancer cachexia. • Exercise training restores COPS2 protein expression to control levels. • Cancer-conditioned media decreased F-actin expression in myotubes, which is partially restored by COPS2 knockdown. • COPS2 overexpression decreases DR4 activity and COPS2 knockdown inhibits cancer-conditioned media effects on DR4 activity. We tested the hypothesis that exercise training would attenuate metabolic impairment in a model of severe cancer cachexia. We used multiple in vivo and in vitro methods to explore the mechanisms underlying the beneficial effects induced by exercise training in tumor-bearing rats. Exercise training improved running capacity, prolonged lifespan, reduced oxidative stress, and normalized muscle mass and contractile function in tumor-bearing rats. An unbiased proteomic screening revealed COP9 signalosome complex subunit 2 (COPS2) as one of the most downregulated proteins in skeletal muscle at the early stage of cancer cachexia. Exercise training normalized muscle COPS2 protein expression in tumor-bearing rats and mice. Lung cancer patients with low endurance capacity had low muscle COPS2 protein expression as compared to age-matched control subjects. To test whether decrease in COPS2 protein levels could aggravate or be an intrinsic compensatory mechanism to protect myotubes from cancer effects, we performed experiments in vitro using primary myotubes. COPS2 knockdown in human myotubes affected multiple cellular pathways, including regulation of actin cytoskeleton. Incubation of cancer-conditioned media in mouse myotubes decreased F-actin expression, which was partially restored by COPS2 knockdown. Direct repeat 4 (DR4) response elements have been shown to positively regulate gene expression. COPS2 overexpression decreased the DR4 activity in mouse myoblasts, and COPS2 knockdown inhibited the effects of cancer-conditioned media on DR4 activity. These studies demonstrated that exercise training may be an important adjuvant therapy to counteract cancer cachexia and uncovered novel mechanisms involving COPS2 to regulate myotube homeostasis in cancer cachexia. •Exercise training prolongs lifespan, reduces oxidative stress, and improves skeletal muscle function in tumor-bearing rats.•Muscle COP9 signalosome complex subunit 2 (COPS2) protein is downregulated in cancer cachexia.•Exercise training restores COPS2 protein expression to control levels.•Cancer-conditioned media decreased F-actin expression in myotubes, which is partially restored by COPS2 knockdown.•COPS2 overexpression decreases DR4 activity and COPS2 knockdown inhibits cancer-conditioned media effects on DR4 activity. We tested the hypothesis that exercise training would attenuate metabolic impairment in a model of severe cancer cachexia. We used multiple in vivo and in vitro methods to explore the mechanisms underlying the beneficial effects induced by exercise training in tumor-bearing rats. Exercise training improved running capacity, prolonged lifespan, reduced oxidative stress, and normalized muscle mass and contractile function in tumor-bearing rats. An unbiased proteomic screening revealed COP9 signalosome complex subunit 2 (COPS2) as one of the most downregulated proteins in skeletal muscle at the early stage of cancer cachexia. Exercise training normalized muscle COPS2 protein expression in tumor-bearing rats and mice. Lung cancer patients with low endurance capacity had low muscle COPS2 protein expression as compared to age-matched control subjects. To test whether decrease in COPS2 protein levels could aggravate or be an intrinsic compensatory mechanism to protect myotubes from cancer effects, we performed experiments in vitro using primary myotubes. COPS2 knockdown in human myotubes affected multiple cellular pathways, including regulation of actin cytoskeleton. Incubation of cancer-conditioned media in mouse myotubes decreased F-actin expression, which was partially restored by COPS2 knockdown. Direct repeat 4 (DR4) response elements have been shown to positively regulate gene expression. COPS2 overexpression decreased the DR4 activity in mouse myoblasts, and COPS2 knockdown inhibited the effects of cancer-conditioned media on DR4 activity. These studies demonstrated that exercise training may be an important adjuvant therapy to counteract cancer cachexia and uncovered novel mechanisms involving COPS2 to regulate myotube homeostasis in cancer cachexia. |
| ArticleNumber | 101012 |
| Author | Chammas, Roger de Paula Faria, Daniele Wisloff, Ulrik Negrão, Carlos E. Sharma, Animesh Slupphaug, Geir Jannig, Paulo R. Voltarelli, Vanessa A. Moreira, José B.N. Swoboda, Kathryn J. Hagen, Lars Neves, Willian das Eichelberger, Eric J. Bechara, Luiz R.G. Alves, Christiano R.R. Hirshman, Michael F. Ruas, Jorge L. Alves, Maria J.N. de Castro Jr, Gilberto Brum, Patricia C. de Almeida, Ney R. Goodyear, Laurie J. Tobias, Gabriel C. |
| Author_xml | – sequence: 1 givenname: Christiano R.R. orcidid: 0000-0002-2646-9689 surname: Alves fullname: Alves, Christiano R.R. email: calves2@mgh.harvard.edu organization: School of Physical Education and Sport, University of Sao Paulo, Sao Paulo, Brazil – sequence: 2 givenname: Willian das surname: Neves fullname: Neves, Willian das organization: School of Physical Education and Sport, University of Sao Paulo, Sao Paulo, Brazil – sequence: 3 givenname: Ney R. surname: de Almeida fullname: de Almeida, Ney R. organization: School of Physical Education and Sport, University of Sao Paulo, Sao Paulo, Brazil – sequence: 4 givenname: Eric J. surname: Eichelberger fullname: Eichelberger, Eric J. organization: Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA – sequence: 5 givenname: Paulo R. surname: Jannig fullname: Jannig, Paulo R. organization: School of Physical Education and Sport, University of Sao Paulo, Sao Paulo, Brazil – sequence: 6 givenname: Vanessa A. surname: Voltarelli fullname: Voltarelli, Vanessa A. organization: School of Physical Education and Sport, University of Sao Paulo, Sao Paulo, Brazil – sequence: 7 givenname: Gabriel C. surname: Tobias fullname: Tobias, Gabriel C. organization: School of Physical Education and Sport, University of Sao Paulo, Sao Paulo, Brazil – sequence: 8 givenname: Luiz R.G. surname: Bechara fullname: Bechara, Luiz R.G. organization: School of Physical Education and Sport, University of Sao Paulo, Sao Paulo, Brazil – sequence: 9 givenname: Daniele surname: de Paula Faria fullname: de Paula Faria, Daniele organization: Department of Radiology and Oncology, Faculdade de Medicina da Universidade de São Paulo, Sao Paulo, Brazil – sequence: 10 givenname: Maria J.N. surname: Alves fullname: Alves, Maria J.N. organization: Heart Institute, School of Medicine, University of Sao Paulo, Sao Paulo, Brazil – sequence: 11 givenname: Lars surname: Hagen fullname: Hagen, Lars organization: Department of Clinical and Molecular Medicine, Norwegian University of Science and Technology, Trondheim, Norway – sequence: 12 givenname: Animesh surname: Sharma fullname: Sharma, Animesh organization: Department of Clinical and Molecular Medicine, Norwegian University of Science and Technology, Trondheim, Norway – sequence: 13 givenname: Geir surname: Slupphaug fullname: Slupphaug, Geir organization: Department of Clinical and Molecular Medicine, Norwegian University of Science and Technology, Trondheim, Norway – sequence: 14 givenname: José B.N. surname: Moreira fullname: Moreira, José B.N. organization: K.G. Jebsen Center of Exercise in Medicine at Department of Circulation and Medical Imaging, Norwegian University of Science and Technology, Trondheim, Norway – sequence: 15 givenname: Ulrik surname: Wisloff fullname: Wisloff, Ulrik organization: K.G. Jebsen Center of Exercise in Medicine at Department of Circulation and Medical Imaging, Norwegian University of Science and Technology, Trondheim, Norway – sequence: 16 givenname: Michael F. surname: Hirshman fullname: Hirshman, Michael F. organization: Section on Integrative Physiology and Metabolism, Joslin Diabetes Center, Harvard Medical School, Boston, MA, USA – sequence: 17 givenname: Carlos E. surname: Negrão fullname: Negrão, Carlos E. organization: School of Physical Education and Sport, University of Sao Paulo, Sao Paulo, Brazil – sequence: 18 givenname: Gilberto surname: de Castro Jr fullname: de Castro Jr, Gilberto organization: Instituto do Cancer do Estado de Sao Paulo ICESP, Hospital das Clinicas HC FMUSP, Faculdade de Medicina da Universidade de Sao Paulo, Sao Paulo, Brazil – sequence: 19 givenname: Roger surname: Chammas fullname: Chammas, Roger organization: Department of Radiology and Oncology, Faculdade de Medicina da Universidade de São Paulo, Sao Paulo, Brazil – sequence: 20 givenname: Kathryn J. surname: Swoboda fullname: Swoboda, Kathryn J. organization: Center for Genomic Medicine, Massachusetts General Hospital, Boston, MA, USA – sequence: 21 givenname: Jorge L. surname: Ruas fullname: Ruas, Jorge L. organization: Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden – sequence: 22 givenname: Laurie J. surname: Goodyear fullname: Goodyear, Laurie J. organization: Section on Integrative Physiology and Metabolism, Joslin Diabetes Center, Harvard Medical School, Boston, MA, USA – sequence: 23 givenname: Patricia C. surname: Brum fullname: Brum, Patricia C. email: topcbrum@usp.br organization: School of Physical Education and Sport, University of Sao Paulo, Sao Paulo, Brazil |
| BackLink | https://www.ncbi.nlm.nih.gov/pubmed/32408015$$D View this record in MEDLINE/PubMed http://kipublications.ki.se/Default.aspx?queryparsed=id:144503237$$DView record from Swedish Publication Index |
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| Keywords | Atrophy Endurance exercise Cancer cachexia Muscle wasting Response elements |
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| Snippet | We tested the hypothesis that exercise training would attenuate metabolic impairment in a model of severe cancer cachexia.
We used multiple in vivo and in... We tested the hypothesis that exercise training would attenuate metabolic impairment in a model of severe cancer cachexia.OBJECTIVEWe tested the hypothesis... • Exercise training prolongs lifespan, reduces oxidative stress, and improves skeletal muscle function in tumor-bearing rats. • Muscle COP9 signalosome complex... Objective: We tested the hypothesis that exercise training would attenuate metabolic impairment in a model of severe cancer cachexia. Methods: We used multiple... |
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| StartPage | 101012 |
| SubjectTerms | Animals Atrophy Biomarkers Cachexia - etiology Cachexia - metabolism Cancer cachexia Cell Line, Tumor COP9 Signalosome Complex - genetics COP9 Signalosome Complex - metabolism Cytokines - metabolism Disease Models, Animal Endurance exercise Energy Metabolism Gene Knockdown Techniques Humans Male Mice Muscle Fibers, Skeletal - metabolism Muscle wasting Muscle, Skeletal - metabolism Muscular Atrophy - etiology Muscular Atrophy - metabolism Myoblasts - metabolism Neoplasms - complications Neoplasms - metabolism Original Oxidation-Reduction Oxidative Stress Physical Conditioning, Animal Proteomics - methods Rats Receptors, TNF-Related Apoptosis-Inducing Ligand - genetics Receptors, TNF-Related Apoptosis-Inducing Ligand - metabolism Repressor Proteins - genetics Repressor Proteins - metabolism Response elements Signal Transduction |
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| Title | Exercise training reverses cancer-induced oxidative stress and decrease in muscle COPS2/TRIP15/ALIEN |
| URI | https://www.clinicalkey.com/#!/content/1-s2.0-S2212877820300867 https://dx.doi.org/10.1016/j.molmet.2020.101012 https://www.ncbi.nlm.nih.gov/pubmed/32408015 https://www.proquest.com/docview/2404047155 https://pubmed.ncbi.nlm.nih.gov/PMC7283151 http://kipublications.ki.se/Default.aspx?queryparsed=id:144503237 https://doaj.org/article/be8202df0b80459fac41942eb9eb9047 |
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