Contraction-induced interleukin-6 gene transcription in skeletal muscle is regulated by c-Jun terminal kinase/activator protein-1

Journal of Biological Chemistry

Volumn 287, Issue 14, 2012, Pages 10771-10779

  Whitham, Martin ^a   Chan, M H Stanley ^a   Pal, Martin ^b   Matthews, Vance B ^a   Prelovsek, Oja ^a   Lunke, Sebastian ^a   El Osta, Assam ^a   Broenneke, Hella ^c   Alber, Jens ^c   Brüning, Jens C ^b   Wunderlich, F Thomas ^b   Lancaster, Graeme I ^a   Febbraio, Mark A ^a  

^a BAKER IDI HEART AND DIABETES INSTITUTE   (Australia)

^b UNIVERSITY OF COLOGNE   (Germany)

^c UNIVERSITY OF COLOGNE   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

CYTOSOLIC; ELECTRICAL PULSE; EXERCISE CONDITION; GENE TRANSCRIPTIONS; INFLAMMATORY RESPONSE; INTERLEUKIN-6; JNK INHIBITION; MRNA EXPRESSION; MYOTUBES; PROTEIN EXPRESSIONS; REGULATORY PATHWAY; SKELETAL MUSCLE; TRANSCRIPTIONAL CONTROL;

GENES; MAMMALS; MUSCLE; PHOSPHORYLATION; TRANSCRIPTION; TRANSCRIPTION FACTORS;

IMMUNOLOGY;

ALKALINE PHOSPHATASE; CALCIMYCIN; CALCIUM ION; HYDROGEN PEROXIDE; I KAPPA B KINASE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 6; MESSENGER RNA; MITOGEN ACTIVATED PROTEIN KINASE P38; STRESS ACTIVATED PROTEIN KINASE; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR NFAT;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CALCIUM SIGNALING; CONCENTRATION RESPONSE; CONTROLLED STUDY; ELECTROSTIMULATION; ENZYME INHIBITION; ENZYME PHOSPHORYLATION; EXCITATION CONTRACTION COUPLING; GENE; GENE EXPRESSION; INFLAMMATION; INTERLEUKIN 6 GENE; MALE; MOUSE; MUSCLE CONTRACTION; MYOTUBE; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN SECRETION; TRANSCRIPTION REGULATION; TREADMILL EXERCISE;

ANIMALS; CALCIMYCIN; CELL LINE; ELECTRIC STIMULATION; INTERLEUKIN-6; JNK MITOGEN-ACTIVATED PROTEIN KINASES; MACROPHAGES; MALE; MICE; MICE, INBRED C57BL; MUSCLE CONTRACTION; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSCRIPTION FACTOR AP-1; TRANSCRIPTION, GENETIC;

MUS;

EID: 84859505189     PISSN: 00219258     EISSN: 1083351X     Source Type: Journal    
DOI: 10.1074/jbc.M111.310581     Document Type: Article

References (32)

1. Hotamisligil, G. S. (2006) Inflammation and metabolic disorders. Nature 444, 860-867
2. Pedersen, B. K., and Febbraio, M. A. (2008) Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol. Rev. 88, 1379-1406
3. de Waal Malefyt, R., Abrams, J., Bennett, B., Figdor, C. G., and de Vries, J. E. (1991) Interleukin-10 (IL-10) inhibits cytokine synthesis by human monocytes: an autoregulatory role of IL-10 produced by monocytes. J. Exp. Med. 174, 1209-1220
4. Kreutz, M., Ackermann, U., Hauschildt, S., Krause, S. W., Riedel, D., Bessler, W., and Andreesen, R. (1997) A comparative analysis of cytokine production and tolerance induction by bacterial lipopeptides, lipopolysaccharides and Staphylococcus aureus in human monocytes. Immunology 92, 396-401 (Pubitemid 27488153)
5. Guha, M., and Mackman, N. (2001) LPS induction of gene expression in human monocytes. Cell. Signal. 13, 85-94 (Pubitemid 32222977)
6. Donath, M. Y., and Shoelson, S. E. (2011) Type 2 diabetes as an inflammatory disease. Nat. Rev. Immunol. 11, 98-107
7. Carey, A. L., Bruce, C. R., Sacchetti, M., Anderson, M. J., Olsen, D. B., Saltin, B., Hawley, J. A., and Febbraio, M. A. (2004) Interleukin-6 and tumor necrosis factor-α are not increased in patients with type 2 diabetes: evidence that plasma interleukin-6 is related to fat mass and not insulin responsiveness. Diabetologia 47, 1029-1037 (Pubitemid 38918162)
8. Balon, T. W., and Nadler, J. L. (1994) Nitric oxide release is present from incubated skeletal muscle preparations. J. Appl. Physiol. 77, 2519-2521
9. Steensberg, A., Keller, C., Hillig, T., Frøsig, C., Wojtaszewski, J. F., Pedersen, B. K., Pilegaard, H., and Sander, M. (2007) Nitric oxide production is a proximal signaling event controlling exercise-induced mRNA expression in human skeletal muscle. FASEB J. 21, 2683-2694 (Pubitemid 47372736)
10. Holmes, A. G., Watt, M. J., Carey, A. L., and Febbraio, M. A. (2004) Ionomycin, but not physiologic doses of epinephrine, stimulates skeletal muscle interleukin-6 mRNA expression and protein release. Metabolism 53, 1492-1495 (Pubitemid 39410392)
11. Keller, C., Hellsten, Y., Steensberg, A., and Pedersen, B. K. (2006) Differential regulation of IL-6 and TNF-α via calcineurin in human skeletal muscle cells. Cytokine 36, 141-147
12. Allen, D. L., Uyenishi, J. J., Cleary, A. S., Mehan, R. S., Lindsay, S. F., and Reed, J. M. (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-R210
13. Dolmetsch, R. E., Xu, K., and Lewis, R. S. (1998) Calcium oscillations increase the efficiency and specificity of gene expression. Nature 392, 933-936 (Pubitemid 28232066)
14. Chan, M. H., McGee, S. L., Watt, M. J., Hargreaves, M., and Febbraio, M. A. (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 (Pubitemid 39561684)
15. Noguchi, H., Matsushita, M., Okitsu, T., Moriwaki, A., Tomizawa, K., Kang, S., Li, S. T., Kobayashi, N., Matsumoto, S., Tanaka, K., Tanaka, N., and Matsui, H. (2004) A new cell-permeable peptide allows successful allogeneic islet transplantation in mice. Nat. Med. 10, 305-309 (Pubitemid 38667623)
16. Matthews, V. B., Aström, M. B., Chan, M. H., Bruce, C. R., Krabbe, K. S., Prelovsek, O., Akerström, T., Yfanti, C., Broholm, C., Mortensen, O. H., Penkowa, M., Hojman, P., Zankari, A., Watt, M. J., Bruunsgaard, H., Pedersen, B. K., and Febbraio, M. A. (2009) Brain-derived neurotrophic factor is produced by skeletal muscle cells in response to contraction and enhances fat oxidation via activation of AMP-activated protein kinase. Diabetologia 52, 1409-1418
17. Nedachi, T., Fujita, H., and Kanzaki, M. (2008) Contractile C2C12 myotube model for studying exercise-inducible responses in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 295, E1191-E1204
18. Belgardt, B. F., Mauer, J., Wunderlich, F. T., Ernst, M. B., Pal, M., Spohn, G., Brönneke, H. S., Brodesser, S., Hampel, B., Schauss, A. C., and Brüning, J. C. (2010) Hypothalamic and pituitary c-Jun N-terminal kinase 1 signaling coordinately regulates glucose metabolism. Proc. Natl. Acad. Sci. U.S.A. 107, 6028-6033
19. Frost, R. A., Nystrom, G. J., and Lang, C. H. (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-R1164 (Pubitemid 37296368)
20. Sabio, G., Das, M., Mora, A., Zhang, Z., Jun, J. Y., Ko, H. J., Barrett, T., Kim, J. K., and Davis, R. J. (2008) A stress signaling pathway in adipose tissue regulates hepatic insulin resistance. Science 322, 1539-1543
21. Nedachi, T., Hatakeyama, H., Kono, T., Sato, M., and Kanzaki, M. (2009) Characterization of contraction-inducible CXC chemokines and their roles in C2C12 myocytes. Am. J. Physiol. Endocrinol. Metab. 297, E866-E878
22. Dendorfer, U., Oettgen, P., and Libermann, T. A. (1994) Multiple regulatory elements in the interleukin-6 gene mediate induction by prostaglandins, cyclic AMP, and lipopolysaccharide. Mol. Cell. Biol. 14, 4443-4454 (Pubitemid 24196793)
23. Kramer, H. F., and Goodyear, L. J. (2007) Exercise, MAPK, and NFκB signaling in skeletal muscle. J. Appl. Physiol. 103, 388-395 (Pubitemid 47092316)
24. Tantiwong, P., Shanmugasundaram, K., Monroy, A., Ghosh, S., Li, M., DeFronzo, R. A., Cersosimo, E., Sriwijitkamol, A., Mohan, S., and Musi, N. (2010) NFκB activity in muscle from obese and type 2 diabetic subjects under basal and exercise-stimulated conditions. Am. J. Physiol. Endocrinol. Metab. 299, E794-E801
25. 2-terminal kinase pathway in rat skeletal muscle. J. Biol. Chem. 272, 25636-25640
26. 2 kinase activity and c-Jun transcriptional activity in human skeletal muscle. Biochem. Biophys. Res. Commun. 251, 106-110
27. Petersen, A. C., McKenna, M. J., Medved, I., Murphy, K. T., Brown, M. J., Della Gatta, P., and Cameron-Smith, D. (2012) Infusion with the antioxidant N-acetylcysteine attenuates early adaptive responses to exercise in human skeletal muscle. Acta Physiol. Scand. 204, 382-392
28. Shaulian, E., and Karin, M. (2002) AP-1 as a regulator of cell life and death. Nat. Cell Biol. 4, E131-E136 (Pubitemid 34521026)
29. Eickelberg, O., Pansky, A., Mussmann, R., Bihl, M., Tamm, M., Hildebrand, P., Perruchoud, A. P., and Roth, M. (1999) Transforming growth factor-β1 induces interleukin-6 expression via activating protein-1 consisting of JunD homodimers in primary human lung fibroblasts. J. Biol. Chem. 274, 12933-12938
30. Rohrbach, S., Engelhardt, S., Lohse, M. J., Werdan, K., Holtz, J., and Muller-Werdan, U. (2007) Activation of AP-1 contributes to the β-adrenoceptor-mediated myocardial induction of interleukin-6. Mol. Med. 13, 605-614 (Pubitemid 350228721)
31. Banzet, S., Koulmann, N., Simler, N., Birot, O., Sanchez, H., Chapot, R., Peinnequin, A., and Bigard, X. (2005) Fiber-type specificity of interleukin- 6 gene transcription during muscle contraction in rat: association with calcineurin activity. J. Physiol. 566, 839-847 (Pubitemid 41122665)
32. McGee, S. L., Sparling, D., Olson, A. L., and Hargreaves, M. (2006) Exercise increases MEF2- and GEF DNA-binding activity in human skeletal muscle. FASEB J. 20, 348-349 (Pubitemid 46671167)