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      Evidence for acute contraction-induced myokine secretion by C2C12 myotubes

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          Abstract

          Skeletal muscle is considered a secretory organ that produces bioactive proteins known as myokines, which are released in response to various stimuli. However, no experimental evidence exists regarding the mechanism by which acute muscle contraction regulates myokine secretion. Here, we present evidence that acute contractions induced myokine secretion from C2C12 myotubes. Changes in the cell culture medium unexpectedly triggered the release of large amounts of proteins from the myotubes, and these proteins obscured the contraction-induced myokine secretion. Once protein release was abolished, the secretion of interleukin-6 (IL-6), the best-known regulatory myokine, increased in response to a 1-hour contraction evoked by electrical stimulation. Using this experimental condition, intracellular calcium flux, rather than the contraction itself, triggered contraction-induced IL-6 secretion. This is the first report to show an evidence for acute contraction-induced myokine secretion by skeletal muscle cells.

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          Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin-6.

          1. Plasma interleukin (IL)-6 concentration is increased with exercise and it has been demonstrated that contracting muscles can produce IL-The question addressed in the present study was whether the IL-6 production by contracting skeletal muscle is of such a magnitude that it can account for the IL-6 accumulating in the blood. 2. This was studied in six healthy males, who performed one-legged dynamic knee extensor exercise for 5 h at 25 W, which represented 40% of peak power output (Wmax). Arterial-femoral venous (a-fv) differences over the exercising and the resting leg were obtained before and every hour during the exercise. Leg blood flow was measured in parallel by the ultrasound Doppler technique. IL-6 was measured by enzyme-linked immunosorbent assay (ELISA). 3. Arterial plasma concentrations for IL-6 increased 19-fold compared to rest. The a-fv difference for IL-6 over the exercising leg followed the same pattern as did the net IL-6 release. Over the resting leg, there was no significant a-fv difference or net IL-6 release. The work was produced by 2.5 kg of active muscle, which means that during the last 2 h of exercise, the median IL-6 production was 6.8 ng min-1 (kg active muscle)-1 (range, 3.96-9.69 ng min-1 kg-1). 4. The net IL-6 release from the muscle over the last 2 h of exercise was 17-fold higher than the elevation in arterial IL-6 concentration and at 5 h of exercise the net release during 1 min was half of the IL-6 content in the plasma. This indicates a very high turnover of IL-6 during muscular exercise. We suggest that IL-6 produced by skeletal contracting muscle contributes to the maintenance of glucose homeostasis during prolonged exercise.
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            Exercise is the real polypill.

            The concept of a "polypill" is receiving growing attention to prevent cardiovascular disease. Yet similar if not overall higher benefits are achievable with regular exercise, a drug-free intervention for which our genome has been haped over evolution. Compared with drugs, exercise is available at low cost and relatively free of adverse effects. We summarize epidemiological evidence on the preventive/therapeutic benefits of exercise and on the main biological mediators involved.
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              Interleukin-6 in acute exercise and training: what is the biological relevance?

              It is now recognized that contracting skeletal muscle may synthesize and release interleukin-6 (IL-6) into the interstitium as well as into the systemic circulation in response to a bout of exercise. Although several sources of IL-6 have been demonstrated, contracting muscles contributes to most of the IL-6 present in the circulation in response to exercise. The magnitude of the exercise-induced IL-6 response is dependent on intensity and especially duration of the exercise, while the mode of exercise has little effect. Several mechanisms may link muscle contractions to IL-6 synthesis: Changes in calcium homeostasis, impaired glucose availability, and increased formation of reactive oxygen species (ROS) are all capable of activating transcription factors known to regulate IL-6 synthesis. Via its effects on liver, adipose tissue, hypothalamic-pituitary-adrenal (HPA) axis and leukocytes, IL-6 may modulate the immunological and metabolic response to exercise. However, prolonged exercise involving a significant muscle mass in the contractile activity is necessary in order to produce a marked systemic IL-6 response. Furthermore, exercise training may reduce basal IL-6 production as well as the magnitude of the acute exercise IL-6 response by counteracting several potential stimuli of IL-6. Accordingly, a decreased plasma IL-6 concentration at rest as well as in response to exercise appears to characterize normal training adaptation.
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                Author and article information

                Contributors
                Role: Data curationRole: InvestigationRole: ValidationRole: VisualizationRole: Writing – original draftRole: Writing – review & editing
                Role: Funding acquisitionRole: InvestigationRole: Writing – review & editing
                Role: Data curationRole: Investigation
                Role: Data curationRole: Investigation
                Role: ConceptualizationRole: Funding acquisitionRole: InvestigationRole: Project administrationRole: Writing – review & editing
                Role: Editor
                Journal
                PLoS One
                PLoS ONE
                plos
                plosone
                PLoS ONE
                Public Library of Science (San Francisco, CA USA )
                1932-6203
                24 October 2018
                2018
                : 13
                : 10
                : e0206146
                Affiliations
                [001]Department of Health Promotion Sciences, Graduate School of Human Health Sciences, Tokyo Metropolitan University, Tokyo, Japan
                University of Minnesota Medical Center, UNITED STATES
                Author notes

                Competing Interests: The authors have declared that no competing interests exist.

                Author information
                http://orcid.org/0000-0002-0974-3033
                Article
                PONE-D-18-16795
                10.1371/journal.pone.0206146
                6200277
                30356272
                39be32d0-57a5-4730-96db-1469d1bdcbf7
                © 2018 Furuichi et al

                This is an open access article distributed under the terms of the Creative Commons Attribution License, which permits unrestricted use, distribution, and reproduction in any medium, provided the original author and source are credited.

                History
                : 5 June 2018
                : 8 October 2018
                Page count
                Figures: 6, Tables: 0, Pages: 15
                Funding
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: KAKENHI 15K16489
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: KAKENHI 24700700
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100001691, Japan Society for the Promotion of Science;
                Award ID: KAKENHI 26242068
                Award Recipient :
                Funded by: funder-id http://dx.doi.org/10.13039/501100009539, Council for Science and Technology Policy;
                Award ID: LS102
                Award Recipient :
                This work was supported by grants from the Japan Society for the Promotion of Science (KAKENHI 15K16489 to Y.F., KAKENHI 24700700 to Y.M., KAKENHI 26242068 to N.L.F) and by a grant-in-aid by the Funding Program for World-Leading Innovative R&D on Science and Technology (#LS102) from the Council for Science and Technology Policy to N.L.F. The funder’s website can be found at https://www.jsps.go.jp/english/index.html. The funders had no role in the study design, data collection and analysis, decision to publish, or preparation of the manuscript.
                Categories
                Research Article
                Biology and Life Sciences
                Physiology
                Muscle Physiology
                Muscle Contraction
                Medicine and Health Sciences
                Physiology
                Muscle Physiology
                Muscle Contraction
                Biology and Life Sciences
                Physiology
                Physiological Processes
                Secretion
                Medicine and Health Sciences
                Physiology
                Physiological Processes
                Secretion
                Biology and Life Sciences
                Anatomy
                Musculoskeletal System
                Muscles
                Skeletal Muscles
                Medicine and Health Sciences
                Anatomy
                Musculoskeletal System
                Muscles
                Skeletal Muscles
                Medicine and Health Sciences
                Surgical and Invasive Medical Procedures
                Functional Electrical Stimulation
                Biology and Life Sciences
                Cell Biology
                Cell Processes
                Protein Transport
                Protein Secretion
                Biology and Life Sciences
                Biochemistry
                Proteins
                Protein Transport
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                Bacterial Physiology
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                Microbial Physiology
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                Medicine and Health Sciences
                Pathology and Laboratory Medicine
                Pathogens
                Virulence Factors
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                Biology and Life Sciences
                Cell Biology
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                Animal Cells
                Muscle Cells
                Biology and Life Sciences
                Anatomy
                Biological Tissue
                Muscle Tissue
                Muscle Cells
                Medicine and Health Sciences
                Anatomy
                Biological Tissue
                Muscle Tissue
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                Research and Analysis Methods
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