Altered myokine secretion is an intrinsic property of skeletal muscle in type 2 diabetes

PLoS ONE

Volumn 11, Issue 7, 2016, Pages

  Ciaraldi, Theodore P ^a,b   Ryan, Alexander J ^a,b,c   Mudaliar, Sunder R ^a,b   Henry, Robert R ^a,b  

^a VA SAN DIEGO HEALTHCARE SYSTEM   (United States)

^b UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^c UNIVERSITY OF MANCHESTER   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

FOLLISTATIN; GROWTH RELATED ONCOGENE ALPHA PROTEIN; I KAPPA B ALPHA; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 15; INTERLEUKIN 1BETA; INTERLEUKIN 6; INTERLEUKIN 8; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; MONOCYTE CHEMOTACTIC PROTEIN 1; MUSCLE PROTEIN; MYOKINE; STRESS ACTIVATED PROTEIN KINASE; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; VASCULOTROPIN; AUTACOID; BIOLOGICAL MARKER; CHEMOKINE; CONDITIONED MEDIUM; CYTOKINE; FATTY ACID; GLUCOSE;

ARTICLE; CLINICAL ARTICLE; CONTROLLED STUDY; ENZYME PHOSPHORYLATION; FEMALE; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HUMAN TISSUE; MALE; METABOLIC REGULATION; NON INSULIN DEPENDENT DIABETES MELLITUS; PROTEIN CONTENT; PROTEIN FUNCTION; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; PROTEIN SECRETION; SKELETAL MUSCLE; BLOOD; CASE CONTROL STUDY; CELL CULTURE; CONDITIONED MEDIUM; ENERGY METABOLISM; METABOLISM; MIDDLE AGED; OXIDATION REDUCTION REACTION; SECRETION (PROCESS); SIGNAL TRANSDUCTION; SKELETAL MUSCLE CELL;

BIOMARKERS; CASE-CONTROL STUDIES; CELLS, CULTURED; CHEMOKINES; CULTURE MEDIA, CONDITIONED; CYTOKINES; DIABETES MELLITUS, TYPE 2; ENERGY METABOLISM; FATTY ACIDS; FEMALE; GLUCOSE; HUMANS; INFLAMMATION MEDIATORS; MALE; MIDDLE AGED; MUSCLE FIBERS, SKELETAL; MUSCLE, SKELETAL; OXIDATION-REDUCTION; SIGNAL TRANSDUCTION;

EID: 84980320619     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0158209     Document Type: Article

References (62)

1. DeFronzo RA. Pathogenesis of type 2 (non-insulin-dependent) diabetes mellitus: a balanced overview. Diabetologia. 1992; 35:389-97. PMID: 1516769
2. Henry RR. Insulin resistance: from predisposing factor to therapeutic target in type 2 diabetes. Clin Ther. 2003; 25(Suppl. B):B47-B63. PMID: 14553866
3. Pedersen BK. Muscle as a Secretory Organ. Comp Physiol. 2013; 3:1337-62.
4. Munoz-Canoves P, Scheele C, Pedersen BK, Serrano AL. Interlukin-6 myokine signaling in skeletal muscle: a double-edged sword? FEBS Journal. 2013; 280:4131-48. doi: 10.1111/febs.12338 PMID: 23663276
5. Norheim F, Raastad T, Thiede B, Rustan AC, Drevon CA, Haugen F. Proteomic identification of secreted proteins in human skeletal muscle cells and expression in response to strength training. Am J Physiol Endocrinol Metab. 2011; 301:E1013-E21. doi: 10.1152/ajpendo.00326.2011 PMID: 21828336
6. Raschke S, Eckel J. Adipo-myokines: Two sides of the same coin-mediators of inflammation and mediators of exercise. Mediators of Inflammation. 2013; 2013:16.
7. McPherron AC. Metabolic functions of myostatin and GDF11. Immunol Endocr Metab Agents Med Chem. 2010; 10:217-31. PMID: 21197386
8. Le Bihan M- C, Bigot A, Jensen SS, Dennis JL, Rogowska-Wrzesinska A, Laine J, et al. In-depth analysis of the secretome identifies three major independent secretory pathways in diffetrentiating human myoblasts. j Proteomics. 2012; 77:344-56. doi: 10.1016/j.jprot.2012.09.008 PMID: 23000592
9. Scheler M, Irmler M, Lehr S, Hartwig S, Staiger H, Al-Hasani H, et al. Cytokine response of primary human myotubes in an in vitro exercise model. Am J Physiol Cell Physiol. 2013; 305:C877-C86. doi: 10.1152/ajpcell.00043.2013 PMID: 23926130
10. Nikolic N, Bakke SS, Kase ET, Rudberg I, Halle IF, Rustan AC, et al. Electrical pulse stimulation of cultured human skeletal muscle cells as an in vitro model of exercise. PLoS ONE. 2012; 7(3).
11. Bouzakri K, Plomgaard P, Berney T, Donath MY, Pedersen BK, Halban PA. Bimodal effect on pancreatic β-cells of secretory products from normal or insulin-resistant human skeletal muscle. Diabetes. 2011; 60:1111-21. doi: 10.2337/db10-1178 PMID: 21378173
12. Vandanmagsar B, Haynie KR, Wicks SE, Bermudez EM, Mendoza TM, Ribnicky D, et al. Artemisia dracunculuc L. extract ameloriates insulin sensitivity by attenuating inflammatory signaling in human skeletal muscle culture. Diabetes Obes Metab. 2014; 16:728-38. doi: 10.1111/dom.12274 PMID: 24521217
13. Saghizadeh M, Ong JM, Garvey WT, Henry RR, Kern PA. The expression of TNF alpha by human muscle. Relationship to insulin resistance. J Clin Invest. 1996; 97:1111-6. PMID: 8613535
14. Abdallah BM, Beck-Nielsen H, Gaster M. FA1 induces pro-inflammatory and anti-adipogenic pathways/ markers in human myotubes established from lean, obese, and type 2 diabetic subjects but not insulin resistance. Front Endo. 2013; 4:1-9.
15. de Sousa Abreu R, Penalva LO, Marcotte EM, Vogel C. Global signatures of protein and mRNA expression levels. Mol Biosyst. 2009; 5:1512-26. doi: 10.1039/b908315d PMID: 20023718
16. Aas V, Bakke SS, Feng YZ, Kase ET, Jensen J, Bajpeyi S, et al. Are cultured human myocytes far from home? Cell Tissue Res. 2013; 354:671-82. doi: 10.1007/s00441-013-1655-1 PMID: 23749200
17. Ciaraldi TP, Abrams L, Nikoulina S, Mudaliar S, Henry RR. Glucose transport in cultured human skeletal muscle cells. Regulation by insulin and glucose in nondiabetic and non-insulin-dependent diabetes mellitus subjects. J Clin Invest. 1995; 96:2820-7. PMID: 8675652
18. Nikoulina SE, Ciaraldi TP, Carter L, Mudaliar S, Park KS, Henry RR. Impaired muscle glycogen synthase in type 2 diabetes is associated with diminished phosphatidylinositol 3-kinase activation. J Clin Endocrinol Metab. 2001; 86(9):4307-14. PMID: 11549666
19. Cha B- S, Ciaraldi TP, Park K- S, Carter L, Mudaliar SR, Henry RR. Impaired fatty acid metabolism in type 2 diabetic skeletal muscle cells in reversed by PPARg agonists. Am J Physiol Endocrinol Metab. 2005; 289:E151-E9. PMID: 15727952
20. Koves TR, Ussher JR, Noland RC, Slentz D, Mosedale M, Ilkayeva O, et al. Mitochondrial overload and incomplete fatty acid oxidation contribute to skeletal muscle insulin resistance. Cell Metab. 2008; 7:45-56. doi: 10.1016/j.cmet.2007.10.013 PMID: 18177724
21. Henry RR, Abrams L, Nikoulina S, Ciaraldi TP. Insulin action and glucose metabolism in nondiabetic control and NIDDM subjects. Comparison using human skeletal muscle cell cultures. Diabetes. 1995; 44:936-46. PMID: 7622000
22. Sinha S, Perdomo G, Brown NF, O'Doherty RM. Fatty acid-induced insulin resistance in L6 myotubes is prevented by inhibition of activation and nuclear localization of nuclear factor kB. J Biol Chem. 2004; 279(40):41294-301. PMID: 15252018
23. Ciaraldi TP, Carter L, Seipke G, Mudaliar S, Henry RR. Effects of the long-acting insulin analog insulin glargine on cultured human skeletal muscle cells: comparisons to insulin and IGF-1. J Clin Endocrinol Metab. 2001; 86(12):5838-47. PMID: 11739448
24. Bradford MM. A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. AnalBiochem. 1976; 71:248-54.
25. Ciaraldi TP, Nikoulina SE, Bandukwala RA, Carter L, Henry RR. Role of GSK3alpha in insulin action in cultured human skeletal muscle cells. Endocrinology. 2007; 148:4393-9. PMID: 17569761
26. Kewalramani G, Fink LN, Asadi F, Klip A. Palmitate-activated macrophages confer insulin resistance to muscle cells by a mechanism involving protein kinase C theta and epsilon. PLoS One. 2011; 6:1-16.
27. Kewalramani G, Bilan PJ, Klip A. Muscle insulin resistance: assault by lipids, cytokines amd local macrophages. Curr Opin Clin Nutr Metabol Care. 2010; 13:382-90.
28. Park K- S, Ciaraldi TP, Lindgren K, Abrams-Carter L, Mudaliar S, Nikoulina S, et al. Troglitazone effects on gene expression in human skeletal muscle of type II diabetes involve up-regulation of peroxisome proliferator-activated receptor-gamma. J Clin Endocrinol Metab. 1998; 83:2830-5. PMID: 9709955
29. Henningsen J, Rigbolt KTG, Blagoev B, Pedersen BK, Kratchmarova I. Dynamics of the skeletal muscle secretome during myoblast differentiation. Mol Cell Prot. 2010; 9:2482-96.
30. Krook A, Bjornholm M, Galuska D, Jiang XJ, Fahlman R, Meyers MG, et al. Characterization of signal transduction and glucose transport in skeletal muscle from type 2 diabetic patients. Diabetes. 2000; 49 (2):284-92. PMID: 10868945
31. Al-Khalili L, de Castro Barbosa T, Ostling J, Massart J, Katayama M, Nystrom A- C, et al. Profiling of human myotubes reveals an intrinsic proteomic signature associated with type 2 diabetes. Translational Proteomics. 2014; 2:25-38.
32. Bartoccioni E, Michaelis D, Hohfeld R. Constitutive and cytokine-induced production of interlukin-6 by human myoblasts. Immunol Letts. 1994; 42:135-8.
33. Brown AE, Palsgaard J, Borup R, Avery P, Gunn DA, De Meyts P, et al. p38 MAPK activation upregulates proinflammatory pathways in skeletal muscle cells from insulin-resistant type 2 diabetic subjects. Am J Physiol Endocrinol Metab. 2015; 308:E63-E70. doi: 10.1152/ajpendo.00115.2014 PMID: 25370850
34. Green CJ, Pedersen M, Pedersen BK, Scheele C. Elevated NFkB activation is conserved in human myocytes cultured from obese type 2 diabetic patients and attenuated by AMP-activated protein kinase. Diabetes. 2011; 60:2810-9. doi: 10.2337/db11-0263 PMID: 21911750
35. Jiang LQ, Duque-Guimaraes DE, Machado UF, Zierath JR, Krook A. Altered response of skeletal muscle to IL-6 in type 2 diabetic patients. Diabetes. 2013; 62:355-61. doi: 10.2337/db11-1790 PMID: 23086036
36. Patsouris D, Cao J- J, Vial G, Bravard A, Lefai E, Durand A, et al. Insuloin resistance is associated with MCP1-mediated macrophage accumulation in skeletal muscle in mice and humans. PLOS One. 2014.
37. Gray SR, Kamolrat T. The effect of exercise induced cytokines on insulin-stimulated glucose transport in C2C12 cells. Cytokine. 2011; 55:221-8. doi: 10.1016/j.cyto.2011.04.019 PMID: 21600784
38. Jiang LQ, Franck N, Egan B, Sjogren RJO, Katayama M, Duque-Guimaraes DE, et al. Autocrine role of interlukin-13 on skeletal muscle glucose metabolism in type 2 diabetic ptients involves mircoRNA let-7. Am J Physiol Endocrinol Metab. 2013; 305:E1359-E66. doi: 10.1152/ajpendo.00236.2013 PMID: 24105413
39. Begum N, Ragolia L, Srinivasan M. Effect of tumor necrosis factor-alpha on insulin -stimulated mitogen-activated protein kinase cascade in cultured rat skeletal muscle cells. EurJBiochem. 1996; 238:214-20.
40. Snel M, van Diepen JA, Stijnen T, Pijl H, Romjin JA, Meinders AE, et al. Immediate and long-term effects of addition of exercise to a 16-week very low calorie diet on low-grade inflammation in obese, insulin-dependent type 2 diabetic patients. Food Chem Toxicol. 2011; 49:3104-11. doi: 10.1016/j.fct. 2011.09.032 PMID: 22001172
41. Sajadi SM, Khoramdelazad H, Hassanshahi G, Rafatpanah H, Hosseini J, Mahmoodi M, et al. Plasma levels of CXCL1 (GRO-alpha) and CXCL10 (IP-10) are elevated in type 2 diabetic patients: evidence for the involvement of inflammation and angiogenesis/angiostasis in this disease state. Clin Lab. 2013; 59:133-7. PMID: 23505918
42. Hansen J, Rinnov A, Krough-Madsen R, Fischer CP, Andreasen AS, Berg RM, et al. Plasma follistatin is elevated in patients with type 2 diabetes: relationship to hyperglycemia, hyperinsulinemia, and systemic low-grade inflammation. Diabetes Metab Res Rev. 2013; 29:463-72. doi: 10.1002/dmrr.2415 PMID: 23564759
43. Hansen JS, Rutti S, Arous C, Clemmesen JO, Secher NH, Drescher A, et al. Circulating follistatin is liver-derived and regulated by the glucagon-to-insulin ratio. J Clin Endocrinol Metab. 2015.
44. Gregor MF, Hotamisligil GS. Inflammatiory mechanisms in obesity. Annu Rev Immunol. 2011; 29:415-45. doi: 10.1146/annurev-immunol-031210-101322 PMID: 21219177
45. Khan IM, Dai Perrard XY, Brunner G, Liui H, Sparks LM, Smith SR, et al. Intermusclular and perimuscular fat expansion in obesity correlated with skeletal muscle T cell and macrophage infiltration and insulin resistance. Int J Obes. 2015.
46. Poelkens F, Lammers G, Pardoel EM, Tack CJ, Hopman MTE. Upregulation of skeletal muscle inflammatory genes links inflammation with insulin resistance in women with the metabolic syndrome. Exp Physiol. 2013; 98:1485-94. doi: 10.1113/expphysiol.2013.072710 PMID: 23771909
47. Amouzou C, Breuker C, Fabre O, Bourret A, LAmbert K, Birot O, et al. Skeletal muscle insulin resistance and absence of inflammation characterize insulin-resistant grade 1 obese women. PLoS One. 2016; 11(4):e154119.
48. Tam CS, Sparks LM, Johannsen DL, Covington JD, Church TS, Ravussin E. Low macrophage accumulation in skeletal muscle of obese type 2 diabetics and elderly subjects. Obesity. 2012; 20:1530-3.doi: 10.1038/oby.2012.24 PMID: 22314623
49. Perry BD, Caldow MK, Brennan-Speranzam TC, Sbaraglia M, Jerums G, Garnham A, et al. Muscle atrophy in patients with Type 2 Diabetes Mellitus: roles of inflammatory pathways, physical activity and exercise. Exerc Immunol Rev. 2016; 22:94-108. PMID: 26859514
50. Fink LN, Oberbach A, Costford SR, Chan KL, Sams A, Bluher M, et al. Expression of anti-inflammatory macrophage genes within skeletal muscle correlated with insulin sensitivity in human obesity and type 2 diabetes. Diabetologia. 2013; 56:1623-8. doi: 10.1007/s00125-013-2897-x PMID: 23595247
51. Patsouris D, Cao J- J, Vial G, Bravard A, Lefal E, Durand A, et al. Insulin resistance is associated with MCP1-mediated macrophage accumulation in skeletal muscle in mice and humans. PLoS ONE. 2014; 9(10).
52. Brown AE, Palsgaard J, Borup R, Avery P, Gunn DA, De Meyts P, et al. p38 MAPK activation upregulates proinflammatory pathways in skeletal muscle cells from insulin-resistant type 2 diabetic patients. Am J Physiol Endocrinol Metab. 2015; 308:E63-E70. doi: 10.1152/ajpendo.00115.2014 PMID: 25370850
53. Chan KL, Pillon NJ, Sivaloganthan DM, Costfors SR, Liu Z, Theret M, et al. Palmitoleate reverses high fat-induced proinflammatory macrophage ploarization via AMP-activated protein kinase (AMPK). J Biol Chem. 2015; 290:16979-88. doi: 10.1074/jbc.M115.646992 PMID: 25987561
54. Kim CS, Park HS, Kawada T, Kim JH, Lim D, Hubbard NE, et al. Circulating levels of MCP-1 anf IL-8 are elevated in human obese subjects and associated with obesity-related parameters. Int J Obes. 2006; 30:1347-55.
55. Maury E, Brichard SM, Pataky Z, Carpentier A, Golay A, Bobbioni-Harsch E. Effect of obesity on growth-related oncogene factor-alpha, thrombopoietin, and tissue inhibitor metalloproteinase-1 serum levels. Obesity. 2010; 18:1503-9. doi: 10.1038/oby.2009.464 PMID: 20035279
56. Akerstrom T, Steensberg A, Keller P, Keller C, Penkowa M, Pedersen BK. Exercise induces interlukin-8 expression in human skeletal muscle. J Physiol. 2005; 563.2:507-16.
57. Garcia JJ, Bote E, Hinchado MD, Ortega E. A single session of intense exercise improves the inflammatory response in healthy sedentary women. J Physiol Biochem. 2011; 67:87-94. doi: 10.1007/ s13105-010-0052-4 PMID: 20936392
58. Rosenkilde MM, Schwartz TW. The chemikone system-a major regulator of angiogenesis in health and disease. APMIS. 2004; 112:481-95. PMID: 15563311
59. Quinn LS, Anderson BG, Strait-Bodey L, Stroud AM, Argiles JM. Oversecretion of interlukin-15 from skeletal muscle reduces adiposity. Am J Physiol Endocrinol Metab. 2009; 296:E191-E202. doi: 10. 1152/ajpendo.90506.2008 PMID: 19001550
60. Pedersen L, Olsen CH, Pedersen BK, Hojman P. Muscle-derived expression of the chemokine CXCL1 attenuates diet-induced obesity and improves fatty acid oxidation in muscle. Am J Physiol Endocrinol Metab. 2012; 302:E831-E40. doi: 10.1152/ajpendo.00339.2011 PMID: 22275756
61. Pierce JR, Maples JM, Hickner RC. IL-15 concentrations in skeletal muscle and subcutaneous adipose tissue in lean and obese humans: local effects of IL-15 on adipose tissue lipolysis. Am J Physiol Endocrinol Metab. 2015; 308:E1131-E9. doi: 10.1152/ajpendo.00575.2014 PMID: 25921578
62. Amir Levy Y, Ciaraldi TP, Mudaliar SR, Phillips SA, Henry RR. Excessive secretion of IL-8 by skeletal muscle in type 2 diabetes impairs tube growth: potential role of PI3K and the Tie2 receptor. Am J Physiol Endocrinol Metab. 2015; 309:E22-34. doi: 10.1152/ajpendo.00513.2014 PMID: 25944879