Association of interleukin-6 signalling with the muscle stem cell response following muscle-lengthening contractions in humans

PLoS ONE

Volumn 4, Issue 6, 2009, Pages

  McKay, Bryon R ^a   De Lisio, Michael ^a   Johnston, Adam P W ^a   O'Reilly, Ciara E ^a   Phillips, Stuart M ^a   Tarnopolsky, Mark A ^a   Parise, Gianni ^a  

^a MCMASTER UNIVERSITY   (Canada)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIN D1; INTERLEUKIN 6; INTERLEUKIN 6 RECEPTOR ALPHA; JANUS KINASE 2; MESSENGER RNA; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TRANSCRIPTION FACTOR PAX7;

ADULT; ARTICLE; CELL COUNT; CELL CYCLE G1 PHASE; CELL CYCLE S PHASE; CELL PROLIFERATION; CELLULAR DISTRIBUTION; CONTROLLED STUDY; ENZYME LINKED IMMUNOSORBENT ASSAY; EXTENSOR MUSCLE; GENE EXPRESSION; GENE LOCATION; HUMAN; HUMAN CELL; HUMAN EXPERIMENT; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MUSCLE CONTRACTION; MUSCLE LENGTH; NORMAL HUMAN; PROTEIN BLOOD LEVEL; PROTEIN PHOSPHORYLATION; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; SKELETAL MUSCLE SATELLITE CELL; WESTERN BLOTTING; CYTOLOGY; HISTOLOGY; METABOLISM; ORGAN SIZE; PHYSIOLOGY; SKELETAL MUSCLE;

ANIMALIA;

HUMANS; INTERLEUKIN-6; JANUS KINASE 2; MALE; MUSCLE CONTRACTION; MUSCLE, SKELETAL; ORGAN SIZE; SATELLITE CELLS, SKELETAL MUSCLE; SIGNAL TRANSDUCTION; STAT3 TRANSCRIPTION FACTOR; YOUNG ADULT;

EID: 67650283899     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0006027     Document Type: Article

References (62)

1. Charge SB, Rudnicki MA (2004) Cellular and molecular regulation of muscle regeneration. Physiol Rev 84: 209-238.
2. Le GF, Rudnicki MA (2007) Skeletal muscle satellite cells and adult myogenesis. Curr Opin Cell Biol 19: 628-633.
3. Rando TA (2006) Stem cells, ageing and the quest for immortality. Nature 441: 1080-1086.
4. Gopinath SD, Rando TA (2008) Stem cell review series: aging of the skeletal muscle stem cell niche. Aging Cell 7: 590-598.
5. Zammit PS, Partridge TA, Yablonka-Reuveni Z (2006) The skeletal muscle satellite cell: the stem cell that came in from the cold. J Histochem Cytochem 54: 1177-1191.
6. Kuang S, Charge SB, Seale P, Huh M, Rudnicki MA (2006) Distinct roles for Pax7 and Pax3 in adult regenerative myogenesis. J Cell Biol 172: 103-113.
7. Olguin HC, Yang Z, Tapscott SJ, Olwin BB (2007) Reciprocal inhibition between Pax7 and muscle regulatory factors modulates myogenic cell fate determination. J Cell Biol 177: 769-779.
8. Seale P, Sabourin LA, Girgis-Gabardo A, Mansouri A, Gruss P, et al. (2000) Pax7 is required for the specification of myogenic satellite cells. Cell 102: 777-786.
9. McKinnell IW, Ishibashi J, Le Grand F, Punch VG, Addicks GC, et al. (2008) Pax7 activates myogenic genes by recruitment of a histone methyltransferase complex. Nat Cell Biol 10: 77-84.
10. Olguin HC, Olwin BB (2004) Pax-7 up-regulation inhibits myogenesis and cell cycle progression in satellite cells: a potential mechanism for self-renewal. Dev Biol 275: 375-388.
11. Oustanina S, Hause G, Braun T (2004) Pax7 directs postnatal renewal and propagation of myogenic satellite cells but not their specification. EMBO J 23: 3430-3439.
12. O'Reilly C, McKay B, Phillips S, Tarnopolsky M, Parise G (2008) Hepatocyte growth factor (HGF) and the satellite cell response following muscle lengthening contractions in humans. Muscle Nerve 38: 1434-1442.
13. Crameri RM, Langberg H, Magnusson P, Jensen CH, Schroder HD, et al. (2004) Changes in satellite cells in human skeletal muscle after a single bout of high intensity exercise. J Physiol 558: 333-340.
14. Dreyer HC, Blanco CE, Sattler FR, Schroeder ET, Wiswell RA (2006) Satellite cell numbers in young and older men 24 hours after eccentric exercise. Muscle Nerve 33: 242-253.
15. Chakravarthy MV, Abraha TW, Schwartz RJ, Fiorotto ML, Booth FW (2000) Insulin-like growth factor-I extends in vitro replicative life span of skeletal muscle satellite cells by enhancing G1/S cell cycle progression via the activation of phosphatidylinositol 3′-kinase/Akt signaling pathway. J Biol Chem 275: 35942-35952.
16. Mourkioti F, Rosenthal N (2005) IGF-1, inflammation and stem cells: interactions during muscle regeneration. Trends Immunol 26: 535-542.
17. Serrano AL, Baeza-Raja B, Perdiguero E, Jardi M, Munoz-Canoves P (2008) Interleukin-6 is an essential regulator of satellite cell-mediated skeletal muscle hypertrophy. Cell Metab 7: 33-44.
18. Spangenburg EE, Booth FW (2002) Multiple signaling pathways mediate LIF-induced skeletal muscle satellite cell proliferation. Am J Physiol Cell Physiol 283: C204-C211.
19. Allen RE, Sheehan SM, Taylor RG, Kendall TL, Rice GM (1995) Hepatocyte growth factor activates quiescent skeletal muscle satellite cells in vitro. J Cell Physiol 165: 307-312.
20. Horsley V, Jansen KM, Mills ST, Pavlath GK (2003) IL-4 acts as a myoblast recruitment factor during mammalian muscle growth. Cell 113: 483-494.
21. Kishimoto T (2005) Interleukin-6: from basic science to medicine-40 years in immunology. Annu Rev Immunol 23: 1-21.
22. Ershler WB, Keller ET (2000) Age-associated increased interleukin-6 gene expression, late-life diseases, and frailty. Annu Rev Med 51: 245-270.
23. Baltgalvis KA, Berger FG, Pena MM, Davis JM, Muga SJ, et al. (2008) Interleukin-6 and cachexia in ApcMin/+ mice. Am J Physiol Regul Integr Comp Physiol 294: R393-R401.
24. Haddad F, Zaldivar F, Cooper DM, Adams GR (2005) IL-6-induced skeletal muscle atrophy. J Appl Physiol 98: 911-917.
25. Steensberg A, van HG, Osada T, Sacchetti M, Saltin B, et al. (2000) Production of interleukin-6 in contracting human skeletal muscles can account for the exercise-induced increase in plasma interleukin-6. J Physiol 529 Pt 1: 237-242.
26. Pedersen BK, Febbraio MA (2008) Muscle as an endocrine organ: focus on muscle-derived interleukin-6. Physiol Rev 88: 1379-1406.
27. Keller P, Penkowa M, Keller C, Steensberg A, Fischer CP, et al. (2005) Interleukin-6 receptor expression in contracting human skeletal muscle: regulating role of IL-6. FASEB J 19: 1181-1183.
28. 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.
29. Weigert C, Dufer M, Simon P, Debre E, Runge H, et al. (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-C1147.
30. Keller C, Steensberg A, Pilegaard H, Osada T, Saltin B, et al. (2001) Transcriptional activation of the IL-6 gene in human contracting skeletal muscle: influence of muscle glycogen content. FASEB J 15: 2748-2750.
31. Tomiya A, Aizawa T, Nagatomi R, Sensui H, Kokubun S (2004) Myofibers express IL-6 after eccentric exercise. Am J Sports Med 32: 503-508.
32. Beaton LJ, Tarnopolsky MA, Phillips SM (2002) Contraction-induced muscle damage in humans following calcium channel blocker administration. J Physiol 544: 849-859.
33. Beaton LJ, Allan DA, Tarnopolsky MA, Tiidus PM, Phillips SM (2002) Contraction-induced muscle damage is unaffected by vitamin E supplementation. Med Sci Sports Exerc 34: 798-805.
34. Mahoney DJ, Safdar A, Parise G, Melov S, Fu M, et al. (2008) Gene expression profiling in human skeletal muscle during recovery from eccentric exercise. Am J Physiol Regul Integr Comp Physiol 294: R1901-R1910.
35. Leslie K, Lang C, Devgan G, Azare J, Berishaj M, et al. (2006) Cyclin D1 is transcriptionally regulated by and required for transformation by activated signal transducer and activator of transcription 3. Cancer Res 66: 2544-2552.
36. Bromberg JF, Wrzeszczynska MH, Devgan G, Zhao Y, Pestell RG, et al. (1999) Stat3 as an oncogene. Cell 98: 295-303.
37. Bamman MM, Shipp JR, Jiang J, Gower BA, Hunter GR, et al. (2001) Mechanical load increases muscle IGF-I and androgen receptor mRNA concentrations in humans. Am J Physiol Endocrinol Metab 280: E383-E390.
38. Yang SY, Goldspink G (2002) Different roles of the IGF-I Ec peptide (MGF) and mature IGF-I in myoblast proliferation and differentiation. FEBS Lett 522: 156-160.
39. McKay BR, O'Reilly CE, Phillips SM, Tarnopolsky MA, Parise G (2008) Co-expression of IGF-1 family members with myogenic regulatory factors following acute damaging muscle-lengthening contractions in humans. J Physiol 586: 5549-5560.
40. Cantini M, Massimino ML, Rapizzi E, Rossini K, Catani C, et al. (1995) Human satellite cell proliferation in vitro is regulated by autocrine secretion of IL-6 stimulated by a soluble factor(s) released by activated monocytes. Biochem Biophys Res Commun 216: 49-53.
41. Trenerry MK, Carey KA, Ward AC, Cameron-Smith D (2007) STAT3 signaling is activated in human skeletal muscle following acute resistance exercise. J Appl Physiol 102: 1483-1489.
42. Helge JW, Stallknecht B, Pedersen BK, Galbo H, Kiens B, et al. (2003) The effect of graded exercise on IL-6 release and glucose uptake in human skeletal muscle. J Physiol 546: 299-305.
43. Ullum H, Haahr PM, Diamant M, Palmo J, Halkjaer-Kristensen J, et al. (1994) Bicycle exercise enhances plasma IL-6 but does not change IL-1 alpha, IL-1 beta, IL-6, or TNF-alpha pre-mRNA in BMNC. J Appl Physiol 77: 93-97.
44. Hiscock N, Fischer CP, Sacchetti M, van HG, Febbraio MA, et al. (2005) Recombinant human interleukin-6 infusion during low-intensity exercise does not enhance whole body lipolysis or fat oxidation in humans. Am J Physiol Endocrinol Metab 289: E2-E7.
45. Bruunsgaard H, Galbo H, Halkjaer-Kristensen J, Johansen TL, MacLean DA, et al. (1997) Exercise-induced increase in serum interleukin-6 in humans is related to muscle damage. J Physiol 499(Pt 3): 833-841.
46. Ostrowski K, Rohde T, Asp S, Schjerling P, Pedersen BK (1999) Pro- and anti-inflammatory cytokine balance in strenuous exercise in humans. J Physiol 515(Pt 1): 287-291.
47. Keller C, Steensberg A, Hansen AK, Fischer CP, Plomgaard P, et al. (2005) Effect of exercise, training, and glycogen availability on IL-6 receptor expression in human skeletal muscle. J Appl Physiol 99: 2075-2079.
48. Cahill CM, Rogers JT (2008) Interleukin (IL) 1beta induction of IL-6 is mediated by a novel phosphatidylinositol 3-kinase-dependent AKT/IkappaB kinase alpha pathway targeting activator protein-1. J Biol Chem 283: 25900-25912.
49. Yu Y, Ge N, Xie M, Sun W, Burlingame S, et al. (2008) Phosphorylation of Thr-178 and Thr-184 in the TAK1 T-loop is required for interleukin (IL)-1-mediated optimal NFkappaB and AP-1 activation as well as IL-6 gene expression. J Biol Chem 283: 24497-24505.
50. Rawlings JS, Rosler KM, Harrison DA (2004) The JAK/STAT signaling pathway. J Cell Sci 117: 1281-1283.
51. Wang X, Wu H, Zhang Z, Liu S, Yang J, et al. (2008) Effects of interleukin-6, leukemia inhibitory factor, and ciliary neurotrophic factor on the proliferation and differentiation of adult human myoblasts. Cell Mol Neurobiol 28: 113-124.
52. Masuda M, Suzui M, Yasumatu R, Nakashima T, Kuratomi Y, et al. (2002) Constitutive activation of signal transducers and activators of transcription 3 correlates with cyclin D1 overexpression and may provide a novel prognostic marker in head and neck squamous cell carcinoma. Cancer Res 62: 3351-3355.
53. Wei Q, Paterson BM (2001) Regulation of MyoD function in the dividing myoblast. FEBS Lett 490: 171-178.
54. Kiuchi N, Nakajima K, Ichiba M, Fukada T, Narimatsu M, et al. (1999) STAT3 is required for the gp130-mediated full activation of the c-myc gene. J Exp Med 189: 63-73.
55. Kami K, Senba E (2002) In vivo activation of STAT3 signaling in satellite cells and myofibers in regenerating rat skeletal muscles. J Histochem Cytochem 50: 1579-1589.
56. Bienvenu F, Gascan H, Coqueret O (2001) Cyclin D1 represses STAT3 activation through a Cdk4-independent mechanism. J Biol Chem 276: 16840-16847.
57. Snyder M, Huang XY, Zhang JJ (2008) Identification of novel direct Stat3 target genes for control of growth and differentiation. J Biol Chem 283: 3791-3798.
58. Naka T, Fujimoto M, Kishimoto T (1999) Negative regulation of cytokine signaling: STAT-induced STAT inhibitor. Trends Biochem Sci 24: 394-398.
59. Chen XP, Losman JA, Rothman P (2000) SOCS proteins, regulators of intracellular signaling. Immunity 13: 287-290.
60. Hennessey JV, Chromiak JA, Della VS, Guertin J, MacLean DB (1997) Increase in percutaneous muscle biopsy yield with a suction-enhancement technique. J Appl Physiol 82: 1739-1742.
61. Bergstrom J (1975) Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 35: 609-616.
62. Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 25: 402-408.