Deficient leukemia inhibitory factor signaling in muscle precursor cells from patients with type 2 diabetes

American Journal of Physiology - Endocrinology and Metabolism

Volumn 303, Issue 2, 2012, Pages

  Broholm, Christa ^a   Brandt, Claus ^a   Schultz, Ninna S ^a   Nielsen, Anders R ^a   Pedersen, Bente K ^a   Scheele, Camilla ^a  

^a UNIVERSITY OF COPENHAGEN   (Denmark)

Author keywords

Cell culture; Cell proliferation; Cytokine; Satellite cell; Skeletal muscle

Indexed keywords

CYCLIN D1; LEUKEMIA INHIBITORY FACTOR; LEUKEMIA INHIBITORY FACTOR RECEPTOR; MESSENGER RNA; MYC PROTEIN; SMALL INTERFERING RNA; STAT1 PROTEIN; STAT3 PROTEIN; SUPPRESSOR OF CYTOKINE SIGNALING 3; TRANSCRIPTION FACTOR JUNB;

ADULT; ARTICLE; CELL PROLIFERATION; CLINICAL ARTICLE; CONTROLLED STUDY; DIABETIC PATIENT; FEMALE; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; MALE; MUSCLE BIOPSY; MUSCLE FUNCTION; MYOBLAST; NON INSULIN DEPENDENT DIABETES MELLITUS; POLYMERASE CHAIN REACTION; PRIORITY JOURNAL; PROTEIN DETERMINATION; PROTEIN INDUCTION; PROTEIN PHOSPHORYLATION; SIGNAL TRANSDUCTION; WESTERN BLOTTING;

ADULT; CELL PROLIFERATION; DIABETES MELLITUS, TYPE 2; FEMALE; HUMANS; LEUKEMIA INHIBITORY FACTOR; LEUKEMIA INHIBITORY FACTOR RECEPTOR ALPHA SUBUNIT; MALE; MIDDLE AGED; MYOBLASTS, SKELETAL; RNA, SMALL INTERFERING; SIGNAL TRANSDUCTION; STAT1 TRANSCRIPTION FACTOR; STAT3 TRANSCRIPTION FACTOR; SUPPRESSOR OF CYTOKINE SIGNALING PROTEINS;

EID: 84863919643     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00586.2011     Document Type: Article

References (41)

1. Austin L, Burgess AW. Stimulation of myoblast proliferation in culture by leukaemia inhibitory factor and other cytokines. J Neurol Sci 101: 193-197, 1991.
2. Barnard W, Bower J, Brown MA, Murphy M, Austin L. Leukemia inhibitory factor (LIF) infusion stimulates skeletal muscle regeneration after injury: injured muscle expresses lif mRNA. J Neurol Sci 123: 108-113, 1994.
3. Barres R, Osler ME, Yan J, Rune A, Fritz T, Caidahl K, Krook A, Zierath JR. Non-CpG methylation of the PGC-1alpha promoter through DNMT3B controls mitochondrial density. Cell Metab 10: 189-198, 2009.
4. Bergstrom J. Percutaneous needle biopsy of skeletal muscle in physiological and clinical research. Scand J Clin Lab Invest 35: 609-616, 1975.
5. Broholm C, Laye MJ, Brandt C, Vadalasetty R, Pilegaard H, Pedersen BK, Scheele C. LIF is a contraction-induced myokine stimulating human myocyte proliferation. J Appl Physiol 111: 251-259, 2011.
6. Chalaux E, Lopez-Rovira T, Rosa JL, Bartrons R, Ventura F. JunB is involved in the inhibition of myogenic differentiation by bone morphogenetic protein-2. J Biol Chem 273: 537-543, 1998.
7. Collins CA. Satellite cell self-renewal. Curr Opin Pharmacol 6: 301-306, 2006.
8. Diao Y, Wang X, Wu Z. SOCS1, SOCS3, and PIAS1 promote myogenic differentiation by inhibiting the leukemia inhibitory factor-induced JAK1/ STAT1/STAT3 pathway. Mol Cell Biol 29: 5084-5093, 2009.
9. Endo T, Nadal-Ginard B. Transcriptional and posttranscriptional control of c-myc during myogenesis: its mRNA remains inducible in differentiated cells and does not suppress the differentiated phenotype. Mol Cell Biol 6: 1412-1421, 1986.
10. Gallagher IJ, Scheele C, Keller P, Nielsen AR, Remenyi J, Fischer CP, Roder K, Babraj J, Wahlestedt C, Hutvagner G, Pedersen BK, Timmons JA. Integration of microRNA changes in vivo identifies novel molecular features of muscle insulin resistance in type 2 diabetes. Genome Med 2: 9, 2010.
11. Gaster M, Petersen I, Hojlund K, Poulsen P, Beck-Nielsen H. The diabetic phenotype is conserved in myotubes established from diabetic subjects: evidence for primary defects in glucose transport and glycogen synthase activity. Diabetes 51: 921-927, 2002.
12. Gaster M, Rustan AC, Aas V, Beck-Nielsen H. Reduced lipid oxidation in skeletal muscle from type 2 diabetic subjects may be of genetic origin: evidence from cultured myotubes. Diabetes 53: 542-548, 2004.
13. Giese B, Roderburg C, Sommerauer M, Wortmann SB, Metz S, Heinrich PC, Muller-Newen G. Dimerization of the cytokine receptors gp130 and LIFR analysed in single cells. J Cell Sci 118: 5129-5140, 2005.
14. Green CJ, Pedersen M, Pedersen BK, Scheele C. Elevated NF-(kappa)B activation is conserved in human myocytes cultured from obese type 2 diabetic patients and attenuated by AMP-activated protein kinase. Diabetes 60: 2810-2819, 2011.
15. Gregorevic P, Williams DA, Lynch GS. Effects of leukemia inhibitory factor on rat skeletal muscles are modulated by clenbuterol. Muscle Nerve 25: 194-201, 2002.
16. Hunt LC, Tudor EM, White JD. Leukemia inhibitory factor-dependent increase in myoblast cell number is associated with phosphotidylinositol 3-kinase-mediated inhibition of apoptosis and not mitosis. Exp Cell Res 316: 1002-1009, 2010.
17. Hunt LC, Upadhyay A, Jazayeri JA, Tudor EM, White JD. Caspase-3, myogenic transcription factors and cell cycle inhibitors are regulated by leukemia inhibitory factor to mediate inhibition of myogenic differentiation. Skelet Muscle 1: 17, 2011.
18. Jackson S, Bagstaff SM, Lynn S, Yeaman SJ, Turnbull DM, Walker M. Decreased insulin responsiveness of glucose uptake in cultured human skeletal muscle cells from insulin-resistant nondiabetic relatives of type 2 diabetic families. Diabetes 49: 1169-1177, 2000.
19. Kiuchi N, Nakajima K, Ichiba M, Fukada T, Narimatsu M, Mizuno K, Hibi M, Hirano T. STAT3 is required for the gp130-mediated full activation of the c-myc gene. J Exp Med 189: 63-73, 1999.
20. Kurek J, Bower J, Romanella M, Austin L. Leukaemia inhibitory factor treatment stimulates muscle regeneration in the mdx mouse. Neurosci Lett 212: 167-170, 1996.
21. Ling C, Groop L. Epigenetics: a molecular link between environmental factors and type 2 diabetes. Diabetes 58: 2718-2725, 2009.
22. Liu L, Li Y, Tollefsbol TO. Gene-environment interactions and epigenetic basis of human diseases. Curr Issues Mol Biol 10: 25-36, 2008.
23. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(+Delta Delta C(T) Method. Methods 25: 402-408, 2001.
24. Madi HA, Riches K, Warburton P, O'Regan DJ, Turner NA, Porter KE. Inherent differences in morphology, proliferation, and migration in saphenous vein smooth muscle cells cultured from nondiabetic and Type 2 diabetic patients. Am J Physiol Cell Physiol 297: C1307-C1317, 2009.
25. Masuda M, Suzui M, Yasumatu R, Nakashima T, Kuratomi Y, Azuma K, Tomita K, Komiyama S, Weinstein IB. 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, 2002.
26. Mauro A. Satellite cell of skeletal muscle fibers. J Biophys Biochem Cytol 9: 493-495, 1961.
27. Miner JH, Wold BJ. c-myc inhibition of MyoD and myogenin-initiated myogenic differentiation. Mol Cell Biol 11: 2842-2851, 1991.
28. Nielsen AR, Hojman P, Erikstrup C, Fischer CP, Plomgaard P, Mounier R, Mortensen OH, Broholm C, Taudorf S, Krogh-Madsen R, Lindegaard B, Petersen AM, Gehl J, Pedersen BK. Association between interleukin-15 and obesity: interleukin-15 as a potential regulator of fat mass. J Clin Endocrinol Metab 93: 4486-4493, 2008.
29. Plomgaard P, Nielsen AR, Fischer CP, Mortensen OH, Broholm C, Penkowa M, Krogh-Madsen R, Erikstrup C, Lindegaard B, Petersen AM, Taudorf S, Pedersen BK. Associations between insulin resistance and TNF-alpha in plasma, skeletal muscle and adipose tissue in humans with and without type 2 diabetes. Diabetologia 50: 2562-2571, 2007.
30. Ridderstrale M, Groop L. Genetic dissection of type 2 diabetes. Mol Cell Endocrinol 297: 10-17, 2009.
31. Rieusset J, Bouzakri K, Chevillotte E, Ricard N, Jacquet D, Bastard JP, Laville M, Vidal H. Suppressor of cytokine signaling 3 expression and insulin resistance in skeletal muscle of obese and type 2 diabetic patients. Diabetes 53: 2232-2241, 2004.
32. Shin JE, Park SH, Jang YK. Epigenetic up-regulation of leukemia inhibitory factor (LIF) gene during the progression to breast cancer. Mol Cell 31: 181-189, 2011.
33. Spangenburg EE, Booth FW. Multiple signaling pathways mediate LIF-induced skeletal muscle satellite cell proliferation. Am J Physiol Cell Physiol 283: C204-C211, 2002.
34. Spangenburg EE, Booth FW. Leukemia inhibitory factor restores the hypertrophic response to increased loading in the LIF(+/-) mouse. Cytokine 34: 125-130, 2006.
35. Sun L, Ma K, Wang H, Xiao F, Gao Y, Zhang W, Wang K, Gao X, Ip N, Wu Z. JAK1-STAT1-STAT3, a key pathway promoting proliferation and preventing premature differentiation of myoblasts. J Cell Biol 179: 129-138, 2007.
36. Thompson DB, Pratley R, Ossowski V. Human primary myoblast cell cultures from non-diabetic insulin resistant subjects retain defects in insulin action. J Clin Invest 98: 2346-2350, 1996.
37. Toledo-Corral CM, Banner LR. Early changes of LIFR and gp130 in sciatic nerve and muscle of diabetic mice. Acta Histochem 114: 159-165, 2011.
38. Villeneuve LM, Natarajan R. The role of epigenetics in the pathology of diabetic complications. Am J Physiol Renal Physiol 299: F14-F25, 2010.
39. Wagers AJ, Conboy IM. Cellular and molecular signatures of muscle regeneration: current concepts and controversies in adult myogenesis. Cell 122: 659-667, 2005.
40. Wei Q, Paterson BM. Regulation of MyoD function in the dividing myoblast. FEBS Lett 490: 171-178, 2001.
41. White JD, Bower JJ, Kurek JB, Austin L. Leukemia inhibitory factor enhances regeneration in skeletal muscles after myoblast transplantation. Muscle Nerve 24: 695-697, 2001.