Electric pulse stimulation of myotubes as an in vitro exercise model: Cell-mediated and non-cell-mediated effects

Scientific Reports

Volumn 5, Issue , 2015, Pages

  Evers Van Gogh, Inkie J A ^a   Alex, Sheril ^b   Stienstra, Rinke ^b,c   Brenkman, Arjan B ^a   Kersten, Sander ^b   Kalkhoven, Eric ^a  

^a UNIVERSITY MEDICAL CENTER UTRECHT   (Netherlands)

^b WAGENINGEN UNIVERSITY   (Netherlands)

^c RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

[No Author keywords available]

Indexed keywords

MUSCLE PROTEIN;

ANIMAL; CELL LINE; CYTOLOGY; ELECTROSTIMULATION; GENE EXPRESSION REGULATION; METABOLISM; MOUSE; MUSCLE CONTRACTION; RAT; SKELETAL MUSCLE CELL;

ANIMALS; CELL LINE; ELECTRIC STIMULATION; GENE EXPRESSION REGULATION; MICE; MUSCLE CONTRACTION; MUSCLE FIBERS, SKELETAL; MUSCLE PROTEINS; RATS;

EID: 84935006202     PISSN: None     EISSN: 20452322     Source Type: Journal    
DOI: 10.1038/srep10944     Document Type: Article

References (54)

1. Ng, M. et al. Global, regional, and national prevalence of overweight and obesity in children and adults during 1980-2013: a systematic analysis for the Global Burden of Disease Study 2013. Lancet 384, 766-781 (2014).
2. Charakida, M. et al. Lifelong patterns of BMI and cardiovascular phenotype in individuals aged 60-64 years in the 1946 British birth cohort study: an epidemiological study. Lancet Diabetes Endocrinol. 2, 648-654 (2014).
3. Thompson, P. D. et al. Exercise and physical activity in the prevention and treatment of atherosclerotic cardiovascular disease: a statement from the Council on Clinical Cardiology (Subcommittee on Exercise, Rehabilitation, and Prevention) and the Council on Nutrition, Physical Activity, and Metabolism (Subcommittee on Physical Activity). Circulation 107, 3109-3116 (2003).
4. Knowler, W. C. et al. Reduction in the incidence of type 2 diabetes with lifestyle intervention or metformin. N. Engl. J. Med. 346, 393-403 (2002).
5. Gibbons, R. J. et al. ACC/AHA 2002 guideline update for exercise testing: summary article: a report of the American College of Cardiology/American Heart Association Task Force on Practice Guidelines (Committee to Update the 1997 Exercise Testing Guidelines). Circulation 106, 1883-1892 (2002).
6. Heinonen, I. et al. Organ-Specific Physiological Responses to Acute Physical Exercise and Long-Term Training in Humans. Physiology (Bethesda) 29, 421-436 (2014).
7. Pedersen, B. K. & Febbraio, M. A. Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat. Rev. Endocrinol. 8, 457-465 (2012).
8. Bostrom, P. et al. A PGC1-alpha-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481, 463-468 (2012).
9. Rao, R. R. et al. Meteorin-like is a hormone that regulates immune-adipose interactions to increase beige fat thermogenesis. Cell 157, 1279-1291 (2014).
10. Catoire, M. et al. Pronounced effects of acute endurance exercise on gene expression in resting and exercising human skeletal muscle. PLoS ONE 7, e51066 (2012).
11. Catoire, M., Mensink, M., Kalkhoven, E., Schrauwen, P. & Kersten, S. Identification of human exercise-induced myokines using secretome analysis. Physiol. Genomics 46, 256-267 (2014).
12. Raschke, S., Eckardt, K., Bjorklund Holven, K., Jensen, J. & Eckel, J. Identification and validation of novel contraction-regulated myokines released from primary human skeletal muscle cells. PLoS ONE 8, e62008 (2013).
13. Nieman, D. C. et al. Muscle cytokine mRNA changes after 2.5 h of cycling: influence of carbohydrate. Med. Sci. Sports Exerc. 37, 1283-1290 (2005).
14. Broholm, C. et al. Exercise induces expression of leukaemia inhibitory factor in human skeletal muscle. J. Physiol. 586, 2195-2201 (2008).
15. Lewis, G. D. et al. Metabolic signatures of exercise in human plasma. Sci. Transl. Med. 2, 33ra37 (2010).
16. Roberts, L. D. et al. beta-Aminoisobutyric acid induces browning of white fat and hepatic beta-oxidation and is inversely correlated with cardiometabolic risk factors. Cell Metab. 19, 96-108 (2014).
17. Hartwig, S. et al. Secretome profiling of primary human skeletal muscle cells. Biochim. Biophys. Acta 1844, 1011-1017 (2014).
18. Weigert, C., Lehmann, R., Hartwig, S. & Lehr, S. The secretome of the working human skeletal muscle-a promising opportunity to combat the metabolic disaster? Proteomics Clin. Appl. 8, 5-18 (2014).
19. Bortoluzzi, S., Scannapieco, P., Cestaro, A., Danieli, G. A. & Schiaffino, S. Computational reconstruction of the human skeletal muscle secretome. Proteins 62, 776-792 (2006).
20. Henningsen, J., Rigbolt, K. T., Blagoev, B., Pedersen, B. K. & Kratchmarova, I. Dynamics of the skeletal muscle secretome during myoblast differentiation. Mol. Cell. Proteomics 9, 2482-2496 (2010).
21. Norheim, F. et al. Proteomic identification of secreted proteins from human skeletal muscle cells and expression in response to strength training. Am. J. Physiol. Endocrinol. Metab. 301, E1013-1021 (2011).
22. Yoon, J. H. et al. Comparative proteomic analysis of the insulin-induced L6 myotube secretome. Proteomics 9, 51-60 (2009).
23. Seglen, P. O. Preparation of isolated rat liver cells. Methods Cell Biol. 13, 29-83 (1976).
24. Lambernd, S. et al. Contractile activity of human skeletal muscle cells prevents insulin resistance by inhibiting pro-inflammatory signalling pathways. Diabetologia 55, 1128-1139 (2012).
25. Gentleman, R. C. et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol. 5, R80 (2004).
26. Irizarry, R. A. et al. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 4, 249-264 (2003).
27. Ruijter, J. M. et al. Amplification efficiency: linking baseline and bias in the analysis of quantitative PCR data. Nucleic Acids Res. 37, e45 (2009).
28. Pfaffl, M. W. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res. 29, e45 (2001).
29. Canto, C. et al. AMPK regulates energy expenditure by modulating NAD+ metabolism and SIRT1 activity. Nature 458, 1056-1060 (2009).
30. Blau, H. M., Chiu, C. P. & Webster, C. Cytoplasmic activation of human nuclear genes in stable heterocaryons. Cell 32, 1171-1180 (1983).
31. Burch, N. et al. Electric pulse stimulation of cultured murine muscle cells reproduces gene expression changes of trained mouse muscle. PLoS ONE 5, e10970 (2010).
32. Winder, W. W. & Hardie, D. G. Inactivation of acetyl-CoA carboxylase and activation of AMP-activated protein kinase in muscle during exercise. Am. J. Physiol. 270, E299-304 (1996).
33. Hutber, C. A., Hardie, D. G. & Winder, W. W. Electrical stimulation inactivates muscle acetyl-CoA carboxylase and increases AMP-activated protein kinase. Am. J. Physiol. 272, E262-266 (1997).
34. Fukada, T. & Kambe, T. Molecular and genetic features of zinc transporters in physiology and pathogenesis. Metallomics 3, 662-674 (2011).
35. Patten, C. J., Peterson, L. A. & Murphy, S. E. Evidence for metabolic activation of N'-nitrosonornicotine and N-nitrosobenzylmethylamine by a rat nasal coumarin hydroxylase. Drug Metab. Dispos. 26, 177-180 (1998).
36. Robottom-Ferreira, A. B., Aquino, S. R., Queiroga, R., Albano, R. M. & Ribeiro Pinto, L. F. Expression of CYP2A3 mRNA and its regulation by 3-methylcholanthrene, pyrazole, and beta-ionone in rat tissues. Braz. J. Med. Biol. Res. 36, 839-844 (2003).
37. Muller, P. et al. Gene expression profiling of liver cells after copper overload in vivo and in vitro reveals new copper-regulated genes. J. Biol. Inorg. Chem. 12, 495-507 (2007).
38. Liuzzi, J. P., Blanchard, R. K. & Cousins, R. J. Differential regulation of zinc transporter 1, 2, and 4 mRNA expression by dietary zinc in rats. J. Nutr. 131, 46-52 (2001).
39. Pinto, L. F. et al. Rat oesophageal cytochrome P450 (CYP) monooxygenase system: comparison to the liver and relevance in N-nitrosodiethylamine carcinogenesis. Carcinogenesis 22, 1877-1883 (2001).
40. Lee, K. Y. et al. Effect of exercise on hepatic gene expression in an obese mouse model using cDNA microarrays. Obesity (Silver Spring) 14, 1294-1302 (2006).
41. Shinogi, M., Sakaridani, M. & Yokoyama, I. Metallothionein induction in rat liver by dietary restriction or exercise and reduction of exercise-induced hepatic lipid peroxidation. Biol. Pharm. Bull. 22, 132-136 (1999).
42. Rosen, P. et al. The role of oxidative stress in the onset and progression of diabetes and its complications: a summary of a Congress Series sponsored by UNESCO-MCBN, the American Diabetes Association and the German Diabetes Society. Diabetes Metab. Res. Rev. 17, 189-212 (2001).
43. Cai, L. Metallothionein as an adaptive protein prevents diabetes and its toxicity. Nonlinearity Biol. Toxicol. Med. 2, 89-103 (2004).
44. Grungreiff, K. & Reinhold, D. Liver cirrhosis and "liver" diabetes mellitus are linked by zinc deficiency. Med. Hypotheses 64, 316-317 (2005).
45. Jayawardena, R. et al. Effects of zinc supplementation on diabetes mellitus: a systematic review and meta-analysis. Diabetol. Metab. Syndr. 4, 13 (2012).
46. Ye, G., Metreveli, N. S., Ren, J. & Epstein, P. N. Metallothionein prevents diabetes-induced deficits in cardiomyocytes by inhibiting reactive oxygen species production. Diabetes 52, 777-783 (2003).
47. Wang, X., Li, H., Fan, Z. & Liu, Y. Effect of zinc supplementation on type 2 diabetes parameters and liver metallothionein expressions in Wistar rats. J. Physiol. Biochem. 68, 563-572 (2012).
48. Chen, M. L. & Failla, M. L. Metallothionein metabolism in the liver and kidney of the streptozotocin-diabetic rat. Comp. Biochem. Physiol. B 90, 439-445 (1988).
49. Cai, L. Diabetic cardiomyopathy and its prevention by metallothionein: experimental evidence, possible mechanisms and clinical implications. Curr. Med. Chem. 14, 2193-2203 (2007).
50. Jiang, Y. & Kang, Y. J. Metallothionein gene therapy for chemical-induced liver fibrosis in mice. Mol. Ther. 10, 1130-1139 (2004).
51. Wang, Y., Cheng, M., Zhang, B., Nie, F. & Jiang, H. Dietary supplementation of blueberry juice enhances hepatic expression of metallothionein and attenuates liver fibrosis in rats. PLoS ONE 8, e58659 (2013).
52. Wang, Y. et al. Inactivation of GSK-3beta by metallothionein prevents diabetes-related changes in cardiac energy metabolism, inflammation, nitrosative damage, and remodeling. Diabetes 58, 1391-1402 (2009).
53. Patel, S. et al. Tissue-specific role of glycogen synthase kinase 3beta in glucose homeostasis and insulin action. Mol. Cell. Biol. 28, 6314-6328 (2008).
54. Cline, G. W. et al. Effects of a novel glycogen synthase kinase-3 inhibitor on insulin-stimulated glucose metabolism in Zucker diabetic fatty (fa/fa) rats. Diabetes 51, 2903-2910 (2002).