Characterization of contraction-induced IL-6 up-regulation using contractile C2C12 myotubes

Endocrine Journal

Volumn 60, Issue 2, 2013, Pages 137-147

  Farmawati, Arta ^a,e   Kitajima, Yasuo ^a   Nedachi, Taku ^b   Sato, Masaaki ^c   Kanzaki, Makoto ^c,d   Nagatomi, Ryoichi ^a,c  

^a TOHOKU UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b TOYO UNIVERSITY   (Japan)

^c TOHOKU UNIVERSITY   (Japan)

^d JAPAN SCIENCE AND TECHNOLOGY AGENCY   (Japan)

^e GADJAH MADA UNIVERSITY   (Indonesia)

Author keywords

Exercise; Glycogen; IL 6; Insulin; Myokine

Indexed keywords

ALPHA CHEMOKINE; CALCINEURIN; CXCL1 CHEMOKINE; CYCLOSPORIN A; GLUCOSE; GLYCOGEN; INSULIN; INTERLEUKIN 6; MESSENGER RNA;

ANIMAL CELL; ARTICLE; BIOACCUMULATION; CELL LEVEL; CONTROLLED STUDY; CYTOKINE PRODUCTION; EVOKED RESPONSE; IN VITRO STUDY; INSULIN RESPONSE; INTRACELLULAR SIGNALING; MOUSE; MUSCLE CONTRACTION; MYOTUBE; NONHUMAN; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; PROTEIN FUNCTION; UPREGULATION;

ANIMALS; CALCINEURIN; CALCIUM SIGNALING; CELL LINE; CHEMOKINES, CXC; ELECTRIC STIMULATION; GLUCOSE; GLYCOGEN; HYPERGLYCEMIA; HYPOGLYCEMIC AGENTS; IMMUNOSUPPRESSIVE AGENTS; INSULIN; INSULIN RESISTANCE; INTERLEUKIN-6; KINETICS; MICE; MUSCLE CONTRACTION; MUSCLE FIBERS, SKELETAL; RNA, MESSENGER; UP-REGULATION;

EID: 84874592546     PISSN: 09188959     EISSN: 13484540     Source Type: Journal    
DOI: 10.1507/endocrj.EJ12-0316     Document Type: Article

References (45)

1. Pedersen BK, Febbraio MA (2012) Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat Rev Endocrinol 8: 457-465.
2. Nielsen AR, Pedersen BK (2007) The biological roles of exercise-induced cytokines: IL-6, IL-8, and IL-15. Appl Physiol Nutr Metab 32: 833-839.
3. Croisier JL, Camus G, Venneman I, Deby-Dupont G, Juchmes-Ferir A, Lamy M, Crielaard JM, Deby C, Duchateau J (1999) Effects of training on exercise-induced muscle damage and interleukin 6 production. Muscle Nerve 22: 208-212.
4. Ostrowski K, Rohde T, Zacho M, Asp S, Pedersen BK (1998) Evidence that interleukin-6 is produced in human skeletal muscle during prolonged running. J Physiol 508: 949-953.
5. Jonsdottir IH, Schjerling P, Ostrowski K, Asp S, Richter EA, Pedersen BK (2000) Muscle contractions induce interleukin-6 mRNA production in rat skeletal muscles. J Physiol 528: 157-163.
6. Hiscock N, Chan MH, Bisucci T, Darby IA, Febbraio MA (2004) Skeletal myocytes are a source of interleukin-6 mRNA expression and protein release during contraction: evidence of fiber type specificity. FASEB J 18: 992-994.
7. Febbraio MA, Hiscock N, Sacchetti M, Fischer CP, Pedersen BK (2004) Interleukin-6 is a novel factor mediating glucose homeostasis during skeletal muscle contraction. Diabetes 53: 1643-1648.
8. Ruderman NB, Keller C, Richard AM, Saha AK, Luo Z, Xiang X, Giralt M, Ritov VB, Menshikova EV, Kelley DE, Hidalgo J, Pedersen BK, Kelly M (2006) Interleukin-6 regulation of AMP-activated protein kinase. Potential role in the systemic response to exercise and prevention of the metabolic syndrome. Diabetes 55: S48-54.
9. Pedersen BK, Akerstrom TC, Nielsen AR, Fischer CP (2007) Role of myokines in exercise and metabolism. J Appl Physiol 103: 1093-1098.
10. Nehlsen-Cannarella SL, Fagoaga OR, Nieman DC, Henson DA, Butterworth DE, Schmitt RL, Bailey EM, Warren BJ, Utter A, Davis JM (1997) Carbohydrate and the cytokine response to 2.5 h of running. J Appl Physiol 82: 1662-1667.
11. Nieman DC, Nehlsen-Cannarella SL, Fagoaga OR, Henson DA, Utter A, Davis JM, Williams F, Butterworth DE (1998) Influence of mode and carbohydrate on the cytokine response to heavy exertion. Med Sci Sports Exerc 30: 671-678.
12. Febbraio MA, Steensberg A, Keller C, Starkie RL, Nielsen HB, Krustrup P, Ott P, Secher NH, Pedersen BK (2003) Glucose ingestion attenuates interleukin-6 release from contracting skeletal muscle in humans. J Physiol 549: 607-612.
13. Keller C, Steensberg A, Pilegaard H, Osada T, Saltin B, Pedersen BK, Neufer PD (2001) Transcriptional activation of the IL-6 gene in human contracting skeletal muscle: influence of muscle glycogen content. FASEB J 15: 2748-2750.
14. Steensberg A, Febbraio MA, Osada T, Schjerling P, van Hall G, Saltin B, Pedersen BK (2001) Interleukin-6 production in contracting human skeletal muscle is influenced by pre-exercise muscle glycogen content. J Physiol 537: 633-639.
15. Keller P, Keller C, Carey AL, Jauffred S, Fischer CP, Steensberg A, Pedersen BK (2003) Interleukin-6 production by contracting human skeletal muscle: autocrine regulation by IL-6. Biochem Biophys Res Commun 310: 550-554.
16. Weigert C, Dufer M, Simon P, Debre E, Runge H, Brodbeck K, Haring HU, Schleicher ED (2007) Upregulation of IL-6 mRNA by IL-6 in skeletal muscle cells: role of IL-6 mRNA stabilization and Ca2+-dependent mechanisms. Am J Physiol Cell Physiol 293: C1139-1147.
17. Nedachi T, Fujita H, Kanzaki M (2008) Contractile C2C12 myotube model for studying exercise-inducible responses in skeletal muscle. Am J Physiol Endocrinol Metab 295: E1191-1204.
18. Nedachi T, Hatakeyama H, Kono T, Sato M, Kanzaki M (2009) Characterization of contraction-inducible CXC chemokines and their roles in C2C12 myocytes. Am J Physiol Endocrinol Metab 297: E866-878.
19. Yaffe D, Saxel O (1977) Serial passaging and differentiation of myogenic cells isolated from dystrophic mouse muscle. Nature 270: 725-727.
20. Nedachi T, Kanzaki M (2006) Regulation of glucose transporters by insulin and extracellular glucose in C2C12 myotubes. Am J Physiol Endocrinol Metab 291: E817-828.
21. Fujita H, Nedachi T, Kanzaki M (2007) Accelerated de novo sarcomere assembly by electric pulse stimulation in C2C12 myotubes. Exp Cell Res 313: 1853-1865.
22. Kruszynska YT, Ciaraldi TP, Henry RR (2011) Regulation of Glucose Metabolism in Skeletal Muscle. Compr Physiol 2011, Supplement 21: Handbook of Physiology, The Endocrine System, The Endocrine Pancreas and Regulation of Metabolism 579-607.
23. Banzet S, Koulmann N, Simler N, Birot O, Sanchez H, Chapot R, Peinnequin A, Bigard X (2005) Fibre-type specificity of interleukin-6 gene transcription during muscle contraction in rat: association with calcineurin activity. J Physiol 566: 839-847.
24. Burch N, Arnold AS, Item F, Summermatter S, Brochmann Santana Santos G, Christe M, Boutellier U, Toigo M, Handschin C (2010) Electric pulse stimulation of cultured murine muscle cells reproduces gene expression changes of trained mouse muscle. PLoS One 5: e10970.
25. Lambernd S, Taube A, Schober A, Platzbecker B, Gorgens SW, Schlich R, Jeruschke K, Weiss J, Eckardt K, Eckel J (2012) Contractile activity of human skeletal muscle cells prevents insulin resistance by inhibiting pro-inflammatory signalling pathways. Diabetologia 55: 1128-1139.
26. Whitham M, Chan MH, Pal M, Matthews VB, Prelovsek O, Lunke S, El-Osta A, Broenneke H, Alber J, Bruning JC, Wunderlich FT, Lancaster GI, Febbraio MA (2012) Contraction-induced IL-6 gene transcription in skeletal muscle is regulated by c-jun terminal kinase/Activator protein-1. J Biol Chem 287: 10771-10779.
27. Nikolic N, Skaret Bakke S, Tranheim Kase E, Rudberg I, Flo Halle I, Rustan AC, Thoresen GH, Aas V (2012) Electrical pulse stimulation of cultured human skeletal muscle cells as an in vitro model of exercise. PLoS One 7, e33203.
28. Banzet S, Koulmann N, Sanchez H, Serrurier B, Peinnequin A, Alonso A, Bigard X (2007) Contractioninduced interleukin-6 transcription in rat slow-type muscle is partly dependent on calcineurin activation. J Cell Physiol 210: 596-601.
29. Allen DL, Uyenishi JJ, Cleary AS, Mehan RS, Lindsay SF, Reed JM (2010) Calcineurin activates interleukin-6 transcription in mouse skeletal muscle in vivo and in C2C12 myotubes in vitro. Am J Physiol Regul Integr Comp Physiol 298: R198-210.
30. Chan MH, McGee SL, Watt MJ, Hargreaves M, Febbraio MA (2004) Altering dietary nutrient intake that reduces glycogen content leads to phosphorylation of nuclear p38 MAP kinase in human skeletal muscle: association with IL-6 gene transcription during contraction. FASEB J 18: 1785-1787.
31. Gallucci S, Provenzano C, Mazzarelli P, Scuderi F, Bartoccioni E (1998) Myoblasts produce IL-6 in response to inflammatory stimuli. Int Immunol 10: 267-273.
32. Frost RA, Nystrom GJ, Lang CH (2003) Lipopolysaccharide and proinflammatory cytokines stimulate interleukin-6 expression in C2C12 myoblasts: role of the Jun NH2-terminal kinase. Am J Physiol Regul Integr Comp Physiol 285: R1153-1164.
33. Frost RA, Nystrom GJ, Lang CH (2006) Multiple Tolllike receptor ligands induce an IL-6 transcriptional response in skeletal myocytes. Am J Physiol Regul Integr Comp Physiol 290: R773-784.
34. Luo G, Hershko DD, Robb BW, Wray CJ, Hasselgren PO (2003) IL-1beta stimulates IL-6 production in cultured skeletal muscle cells through activation of MAP kinase signaling pathway and NF-kappa B. Am J Physiol Regul Integr Comp Physiol 284: R1249-1254.
35. Kosmidou I, Vassilakopoulos T, Xagorari A, Zakynthinos S, Papapetropoulos A, Roussos C (2002) Production of interleukin-6 by skeletal myotubes: role of reactive oxygen species. Am J Respir Cell Mol Biol 26: 587-593.
36. Frost RA, Nystrom GJ, Lang CH (2004) Epinephrine stimulates IL-6 expression in skeletal muscle and C2C12 myoblasts: role of c-Jun NH2-terminal kinase and histone deacetylase activity. Am J Physiol Endocrinol Metab 286: E809-817.
37. Owens DM, Keyse SM (2007) Differential regulation of MAP kinase signalling by dual-specificity protein phosphatases. Oncogene 26: 3203-3213.
38. Coyle EF, Coggan AR, Hemmert MK, Ivy JL (1986) Muscle glycogen utilization during prolonged strenuous exercise when fed carbohydrate. J Appl Physiol 61: 165-172.
39. Goodyear LJ, Hirshman MF, Valyou PM, Horton ES (1992) Glucose transporter number, function, and subcellular distribution in rat skeletal muscle after exercise training. Diabetes 41: 1091-1099.
40. Ivy JL, Kuo CH (1998) Regulation of GLUT4 protein and glycogen synthase during muscle glycogen synthesis after exercise. Acta Physiol Scand 162: 295-304.
41. Franch J, Aslesen R, Jensen J (1999) Regulation of glycogen synthesis in rat skeletal muscle after glycogendepleting contractile activity: effects of adrenaline on glycogen synthesis and activation of glycogen synthase and glycogen phosphorylase. Biochem J 344: 231-235.
42. Nedachi T, Kadotani A, Ariga M, Katagiri H, Kanzaki M (2008) Ambient Glucose Levels Qualify the Potency of Insulin Myogenic Actions by Regulating SIRT1 and FoxO3a in C2C12 myocytes. Am J Physiol Endocrinol Metab 294: E668-678.
43. Bouskila M, Hunter RW, Ibrahim AF, Delattre L, Peggie M, van Diepen JA, Voshol PJ, Jensen J, Sakamoto K (2010) Allosteric regulation of glycogen synthase controls glycogen synthesis in muscle. Cell Metab 12: 456-466.
44. Weigert C, Hennige AM, Brodbeck K, Haring HU, Schleicher ED (2005) Interleukin-6 acts as insulin sensitizer on glycogen synthesis in human skeletal muscle cells by phosphorylation of Ser473 of Akt. Am J Physiol Endocrinol Metab 289: E251-257.
45. Glund S, Deshmukh A, Long YC, Moller T, Koistinen HA, Caidahl K, Zierath JR, Krook A (2007) Interleukin-6 directly increases glucose metabolism in resting human skeletal muscle. Diabetes 56: 1630-1637.