Exercise in vivo marks human myotubes in vitro: Training-induced increase in lipid metabolism
Physical activity has preventive as well as therapeutic benefits for overweight subjects. In this study we aimed to examine effects of in vivo exercise on in vitro metabolic adaptations by studying energy metabolism in cultured myotubes isolated from biopsies taken before and after 12 weeks of exten...
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| Published in | PLOS ONE Vol. 12; no. 4; p. e0175441 |
|---|---|
| Main Authors | , , , , , , , , , , , , , , , , , , |
| Format | Journal Article |
| Language | English |
| Published |
United States
Public Library of Science (PLoS)
12.04.2017
Public Library of Science |
| Subjects | |
| Online Access | Get full text |
| ISSN | 1932-6203 1932-6203 |
| DOI | 10.1371/journal.pone.0175441 |
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| Abstract | Physical activity has preventive as well as therapeutic benefits for overweight subjects. In this study we aimed to examine effects of in vivo exercise on in vitro metabolic adaptations by studying energy metabolism in cultured myotubes isolated from biopsies taken before and after 12 weeks of extensive endurance and strength training, from healthy sedentary normal weight and overweight men.
Healthy sedentary men, aged 40-62 years, with normal weight (body mass index (BMI) < 25 kg/m2) or overweight (BMI ≥ 25 kg/m2) were included. Fatty acid and glucose metabolism were studied in myotubes using [14C]oleic acid and [14C]glucose, respectively. Gene and protein expressions, as well as DNA methylation were measured for selected genes.
The 12-week training intervention improved endurance, strength and insulin sensitivity in vivo, and reduced the participants' body weight. Biopsy-derived cultured human myotubes after exercise showed increased total cellular oleic acid uptake (30%), oxidation (46%) and lipid accumulation (34%), as well as increased fractional glucose oxidation (14%) compared to cultures established prior to exercise. Most of these exercise-induced increases were significant in the overweight group, whereas the normal weight group showed no change in oleic acid or glucose metabolism.
12 weeks of combined endurance and strength training promoted increased lipid and glucose metabolism in biopsy-derived cultured human myotubes, showing that training in vivo are able to induce changes in human myotubes that are discernible in vitro. |
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| AbstractList | Background and aims Physical activity has preventive as well as therapeutic benefits for overweight subjects. In this study we aimed to examine effects of in vivo exercise on in vitro metabolic adaptations by studying energy metabolism in cultured myotubes isolated from biopsies taken before and after 12 weeks of extensive endurance and strength training, from healthy sedentary normal weight and overweight men. Methods Healthy sedentary men, aged 40-62 years, with normal weight (body mass index (BMI) < 25 kg/m.sup.2) or overweight (BMI [greater than or equal to] 25 kg/m.sup.2) were included. Fatty acid and glucose metabolism were studied in myotubes using [.sup.14 C]oleic acid and [.sup.14 C]glucose, respectively. Gene and protein expressions, as well as DNA methylation were measured for selected genes. Results The 12-week training intervention improved endurance, strength and insulin sensitivity in vivo, and reduced the participants' body weight. Biopsy-derived cultured human myotubes after exercise showed increased total cellular oleic acid uptake (30%), oxidation (46%) and lipid accumulation (34%), as well as increased fractional glucose oxidation (14%) compared to cultures established prior to exercise. Most of these exercise-induced increases were significant in the overweight group, whereas the normal weight group showed no change in oleic acid or glucose metabolism. Conclusions 12 weeks of combined endurance and strength training promoted increased lipid and glucose metabolism in biopsy-derived cultured human myotubes, showing that training in vivo are able to induce changes in human myotubes that are discernible in vitro. Background and aims Physical activity has preventive as well as therapeutic benefits for overweight subjects. In this study we aimed to examine effects of in vivo exercise on in vitro metabolic adaptations by studying energy metabolism in cultured myotubes isolated from biopsies taken before and after 12 weeks of extensive endurance and strength training, from healthy sedentary normal weight and overweight men. Methods Healthy sedentary men, aged 40–62 years, with normal weight (body mass index (BMI) < 25 kg/m2) or overweight (BMI ≥ 25 kg/m2) were included. Fatty acid and glucose metabolism were studied in myotubes using [14C]oleic acid and [14C]glucose, respectively. Gene and protein expressions, as well as DNA methylation were measured for selected genes. Results The 12-week training intervention improved endurance, strength and insulin sensitivity in vivo, and reduced the participants’ body weight. Biopsy-derived cultured human myotubes after exercise showed increased total cellular oleic acid uptake (30%), oxidation (46%) and lipid accumulation (34%), as well as increased fractional glucose oxidation (14%) compared to cultures established prior to exercise. Most of these exercise-induced increases were significant in the overweight group, whereas the normal weight group showed no change in oleic acid or glucose metabolism. Conclusions 12 weeks of combined endurance and strength training promoted increased lipid and glucose metabolism in biopsy-derived cultured human myotubes, showing that training in vivo are able to induce changes in human myotubes that are discernible in vitro. Physical activity has preventive as well as therapeutic benefits for overweight subjects. In this study we aimed to examine effects of in vivo exercise on in vitro metabolic adaptations by studying energy metabolism in cultured myotubes isolated from biopsies taken before and after 12 weeks of extensive endurance and strength training, from healthy sedentary normal weight and overweight men. Healthy sedentary men, aged 40-62 years, with normal weight (body mass index (BMI) < 25 kg/m2) or overweight (BMI ≥ 25 kg/m2) were included. Fatty acid and glucose metabolism were studied in myotubes using [14C]oleic acid and [14C]glucose, respectively. Gene and protein expressions, as well as DNA methylation were measured for selected genes. The 12-week training intervention improved endurance, strength and insulin sensitivity in vivo, and reduced the participants' body weight. Biopsy-derived cultured human myotubes after exercise showed increased total cellular oleic acid uptake (30%), oxidation (46%) and lipid accumulation (34%), as well as increased fractional glucose oxidation (14%) compared to cultures established prior to exercise. Most of these exercise-induced increases were significant in the overweight group, whereas the normal weight group showed no change in oleic acid or glucose metabolism. 12 weeks of combined endurance and strength training promoted increased lipid and glucose metabolism in biopsy-derived cultured human myotubes, showing that training in vivo are able to induce changes in human myotubes that are discernible in vitro. Background and aims Physical activity has preventive as well as therapeutic benefits for overweight subjects. In this study we aimed to examine effects of in vivo exercise on in vitro metabolic adaptations by studying energy metabolism in cultured myotubes isolated from biopsies taken before and after 12 weeks of extensive endurance and strength training, from healthy sedentary normal weight and overweight men. Methods Healthy sedentary men, aged 40–62 years, with normal weight (body mass index (BMI) < 25 kg/m2) or overweight (BMI ≥ 25 kg/m2) were included. Fatty acid and glucose metabolism were studied in myotubes using [14C]oleic acid and [14C]glucose, respectively. Gene and protein expressions, as well as DNA methylation were measured for selected genes. Results The 12-week training intervention improved endurance, strength and insulin sensitivity in vivo, and reduced the participants’ body weight. Biopsy-derived cultured human myotubes after exercise showed increased total cellular oleic acid uptake (30%), oxidation (46%) and lipid accumulation (34%), as well as increased fractional glucose oxidation (14%) compared to cultures established prior to exercise. Most of these exercise-induced increases were significant in the overweight group, whereas the normal weight group showed no change in oleic acid or glucose metabolism. Conclusions 12 weeks of combined endurance and strength training promoted increased lipid and glucose metabolism in biopsy-derived cultured human myotubes, showing that training in vivo are able to induce changes in human myotubes that are discernible in vitro. Background and aims Physical activity has preventive as well as therapeutic benefits for overweight subjects. In this study we aimed to examine effects of in vivo exercise on in vitro metabolic adaptations by studying energy metabolism in cultured myotubes isolated from biopsies taken before and after 12 weeks of extensive endurance and strength training, from healthy sedentary normal weight and overweight men. Methods Healthy sedentary men, aged 40±62 years, with normal weight (body mass index (BMI) < 25 kg/m2) or overweight (BMI 25 kg/m2) were included. Fatty acid and glucose metabolism were studied in myotubes using [14C]oleic acid and [14C]glucose, respectively. Gene and protein expressions, as well as DNA methylation were measured for selected genes. Results The 12-week training intervention improved endurance, strength and insulin sensitivity in vivo, and reduced the participants' body weight. Biopsy-derived cultured human myotubes after exercise showed increased total cellular oleic acid uptake (30%), oxidation (46%) and lipid accumulation (34%), as well as increased fractional glucose oxidation (14%) compared to cultures established prior to exercise. Most of these exercise-induced increases were significant in the overweight group, whereas the normal weight group showed no change in oleic acid or glucose metabolism. Conclusions 12 weeks of combined endurance and strength training promoted increased lipid and glucose metabolism in biopsy-derived cultured human myotubes, showing that training in vivo are able to induce changes in human myotubes that are discernible in vitro. Physical activity has preventive as well as therapeutic benefits for overweight subjects. In this study we aimed to examine effects of in vivo exercise on in vitro metabolic adaptations by studying energy metabolism in cultured myotubes isolated from biopsies taken before and after 12 weeks of extensive endurance and strength training, from healthy sedentary normal weight and overweight men. Healthy sedentary men, aged 40-62 years, with normal weight (body mass index (BMI) < 25 kg/m.sup.2) or overweight (BMI [greater than or equal to] 25 kg/m.sup.2) were included. Fatty acid and glucose metabolism were studied in myotubes using [.sup.14 C]oleic acid and [.sup.14 C]glucose, respectively. Gene and protein expressions, as well as DNA methylation were measured for selected genes. The 12-week training intervention improved endurance, strength and insulin sensitivity in vivo, and reduced the participants' body weight. Biopsy-derived cultured human myotubes after exercise showed increased total cellular oleic acid uptake (30%), oxidation (46%) and lipid accumulation (34%), as well as increased fractional glucose oxidation (14%) compared to cultures established prior to exercise. Most of these exercise-induced increases were significant in the overweight group, whereas the normal weight group showed no change in oleic acid or glucose metabolism. 12 weeks of combined endurance and strength training promoted increased lipid and glucose metabolism in biopsy-derived cultured human myotubes, showing that training in vivo are able to induce changes in human myotubes that are discernible in vitro. Physical activity has preventive as well as therapeutic benefits for overweight subjects. In this study we aimed to examine effects of in vivo exercise on in vitro metabolic adaptations by studying energy metabolism in cultured myotubes isolated from biopsies taken before and after 12 weeks of extensive endurance and strength training, from healthy sedentary normal weight and overweight men.BACKGROUND AND AIMSPhysical activity has preventive as well as therapeutic benefits for overweight subjects. In this study we aimed to examine effects of in vivo exercise on in vitro metabolic adaptations by studying energy metabolism in cultured myotubes isolated from biopsies taken before and after 12 weeks of extensive endurance and strength training, from healthy sedentary normal weight and overweight men.Healthy sedentary men, aged 40-62 years, with normal weight (body mass index (BMI) < 25 kg/m2) or overweight (BMI ≥ 25 kg/m2) were included. Fatty acid and glucose metabolism were studied in myotubes using [14C]oleic acid and [14C]glucose, respectively. Gene and protein expressions, as well as DNA methylation were measured for selected genes.METHODSHealthy sedentary men, aged 40-62 years, with normal weight (body mass index (BMI) < 25 kg/m2) or overweight (BMI ≥ 25 kg/m2) were included. Fatty acid and glucose metabolism were studied in myotubes using [14C]oleic acid and [14C]glucose, respectively. Gene and protein expressions, as well as DNA methylation were measured for selected genes.The 12-week training intervention improved endurance, strength and insulin sensitivity in vivo, and reduced the participants' body weight. Biopsy-derived cultured human myotubes after exercise showed increased total cellular oleic acid uptake (30%), oxidation (46%) and lipid accumulation (34%), as well as increased fractional glucose oxidation (14%) compared to cultures established prior to exercise. Most of these exercise-induced increases were significant in the overweight group, whereas the normal weight group showed no change in oleic acid or glucose metabolism.RESULTSThe 12-week training intervention improved endurance, strength and insulin sensitivity in vivo, and reduced the participants' body weight. Biopsy-derived cultured human myotubes after exercise showed increased total cellular oleic acid uptake (30%), oxidation (46%) and lipid accumulation (34%), as well as increased fractional glucose oxidation (14%) compared to cultures established prior to exercise. Most of these exercise-induced increases were significant in the overweight group, whereas the normal weight group showed no change in oleic acid or glucose metabolism.12 weeks of combined endurance and strength training promoted increased lipid and glucose metabolism in biopsy-derived cultured human myotubes, showing that training in vivo are able to induce changes in human myotubes that are discernible in vitro.CONCLUSIONS12 weeks of combined endurance and strength training promoted increased lipid and glucose metabolism in biopsy-derived cultured human myotubes, showing that training in vivo are able to induce changes in human myotubes that are discernible in vitro. |
| Audience | Academic |
| Author | Birkeland, Kåre I. Langleite, Torgrim Mikal Stensrud, Camilla Løvsletten, Nils Gunnar Johansen, Egil Ivar Thoresen, G. Hege Lund, Jenny Krook, Anna Kase, Eili Tranheim Mudry, Jonathan M. Brubak, Mari G Drevon, Christian A Kolnes, Kristoffer Jensen Jensen, Jørgen Rustan, Arild Feng, Yuan Zeng Tangen, Daniel S. Stadheim, Hans Kristian Gulseth, Hanne Løvdal |
| AuthorAffiliation | 5 Department of Physical Performance, Norwegian School of Sport Sciences, Oslo, Norway 3 Department of Nutrition, Institute of Basic Medical Sciences, University of Oslo, Oslo, Norway 1 Department of Pharmaceutical Biosciences, School of Pharmacy, University of Oslo, Oslo, Norway 4 Department of Endocrinology, Morbid Obesity and Preventive Medicine, Oslo, University Hospital and Institute of Clinical Medicine, University of Oslo, Oslo, Norway 6 Department of Pharmacology, Institute of Clinical Medicine, University of Oslo, Oslo, Norway 2 Integrative Physiology, Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden Tohoku University, JAPAN |
| AuthorAffiliation_xml | – name: Tohoku University, JAPAN – name: 1 Department of Pharmaceutical Biosciences, School of Pharmacy, University of Oslo, Oslo, Norway – name: 2 Integrative Physiology, Department of Physiology and Pharmacology, Karolinska Institutet, Stockholm, Sweden – name: 5 Department of Physical Performance, Norwegian School of Sport Sciences, Oslo, Norway – name: 6 Department of Pharmacology, Institute of Clinical Medicine, University of Oslo, Oslo, Norway – name: 3 Department of Nutrition, Institute of Basic Medical Sciences, University of Oslo, Oslo, Norway – name: 4 Department of Endocrinology, Morbid Obesity and Preventive Medicine, Oslo, University Hospital and Institute of Clinical Medicine, University of Oslo, Oslo, Norway |
| Author_xml | – sequence: 1 fullname: Lund, Jenny – sequence: 2 fullname: Rustan, Arild – sequence: 3 fullname: Løvsletten, Nils Gunnar – sequence: 4 fullname: Mudry, Jonathan M. – sequence: 5 fullname: Langleite, Torgrim Mikal – sequence: 6 fullname: Feng, Yuan Zeng – sequence: 7 fullname: Stensrud, Camilla – sequence: 8 fullname: Brubak, Mari G – sequence: 9 fullname: Drevon, Christian A – sequence: 10 fullname: Birkeland, Kåre I. – sequence: 11 orcidid: 0000-0001-8824-5173 fullname: Kolnes, Kristoffer Jensen – sequence: 12 fullname: Johansen, Egil Ivar – sequence: 13 fullname: Tangen, Daniel S. – sequence: 14 fullname: Stadheim, Hans Kristian – sequence: 15 fullname: Gulseth, Hanne Løvdal – sequence: 16 fullname: Krook, Anna – sequence: 17 fullname: Kase, Eili Tranheim – sequence: 18 fullname: Jensen, Jørgen – sequence: 19 fullname: Thoresen, G. Hege |
| BackLink | https://cir.nii.ac.jp/crid/1871991017445353984$$DView record in CiNii https://www.ncbi.nlm.nih.gov/pubmed/28403174$$D View this record in MEDLINE/PubMed http://kipublications.ki.se/Default.aspx?queryparsed=id:135739479$$DView record from Swedish Publication Index |
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| Copyright | COPYRIGHT 2017 Public Library of Science 2017 Lund et al. This is an open access article distributed under the terms of the Creative Commons Attribution License: http://creativecommons.org/licenses/by/4.0/ (the “License”), which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited. Notwithstanding the ProQuest Terms and Conditions, you may use this content in accordance with the terms of the License. info:eu-repo/semantics/openAccess 2017 Lund et al 2017 Lund et al |
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| Notes | ObjectType-Article-1 SourceType-Scholarly Journals-1 ObjectType-Feature-2 content type line 14 content type line 23 Jenny Lund (2017) Regulation of energy metabolism in cultured skeletal muscle cells: Effects of exercise, donor differences and perilipin 2. Studies in human and mouse myotubes. Doctoral thesis http://urn.nb.no/URN:NBN:no-61296 Competing Interests: The authors report no conflicts of interests. Conceptualization: JL ACR TML CAD KIB KJK EIJ DST HKS HLG JJ GHT.Formal analysis: JL.Funding acquisition: JL ACR CAD KIB AK JJ GHT.Investigation: JL NGL JMM TML YZF CS MGB KJK EIJ DST HKS HLG.Methodology: JL ACR AK ETK GHT.Project administration: JL.Resources: ACR KIB HLG AK JJ GHT.Supervision: JL ACR ETK GHT.Validation: JL ACR ETK GHT.Visualization: JL.Writing – original draft: JL.Writing – review & editing: JL ACR JMM CAD KIB HLG AK ETK JJ GHT. |
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| SubjectTerms | Adenylate Kinase Adenylate Kinase - genetics Adenylate Kinase - metabolism Bioaccumulation Biology and Life Sciences Body size Body weight Cells, Cultured DNA Methylation Epigenesis, Genetic Exercise Fatigue tests Fatty Acids Fatty Acids - metabolism Glucose Glucose - metabolism Health aspects Humans In vitro methods and tests In vivo methods and tests Insulin Insulin - physiology Insulin Receptor Substrate Proteins Insulin Receptor Substrate Proteins - genetics Insulin Receptor Substrate Proteins - metabolism Insulin resistance Lipid Metabolism Lipids Male Medicine Medicine and Health Sciences Metabolism Middle Aged Mitochondria, Muscle Mitochondria, Muscle - metabolism Mitochondrial Proteins Mitochondrial Proteins - metabolism Muscle Fibers, Skeletal Muscle Fibers, Skeletal - metabolism Obesity Oleic acid Oxidation Phosphorylation Physical Sciences Physical training Preventive medicine Protein Processing, Post-Translational Q R Research and Analysis Methods Research Article Resistance Training Science Training Transcriptome |
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| Title | Exercise in vivo marks human myotubes in vitro: Training-induced increase in lipid metabolism |
| URI | https://cir.nii.ac.jp/crid/1871991017445353984 https://www.ncbi.nlm.nih.gov/pubmed/28403174 https://www.proquest.com/docview/1887001581 https://www.proquest.com/docview/1887427806 http://hdl.handle.net/10852/59036 https://pubmed.ncbi.nlm.nih.gov/PMC5389842 http://kipublications.ki.se/Default.aspx?queryparsed=id:135739479 https://journals.plos.org/plosone/article/file?id=10.1371/journal.pone.0175441&type=printable https://doaj.org/article/65fc36c8c0624d4b98bee9d90c7fbbda http://dx.doi.org/10.1371/journal.pone.0175441 |
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