Skip to main content
Top
Published in: Endocrine 1/2015

01-02-2015 | Original Article

IL-15 expression increased in response to treadmill running and inhibited endoplasmic reticulum stress in skeletal muscle in rats

Authors: Hong-Tao Yang, Li-Jie Luo, Wen-Jia Chen, Lei Zhao, Chao-Shu Tang, Yong-Fen Qi, Jing Zhang

Published in: Endocrine | Issue 1/2015

Login to get access

Abstract

Interleukin 15 (IL-15) has recently been proposed as a circulating myokine involved in glucose uptake and utilization in skeletal muscle. However, the role and mechanism of IL-15 in exercise improving insulin resistance (IR) is unclear. Here, we investigated the alteration in expression of IL-15 and IL-15 receptor α (IL-15Rα) in skeletal muscle during treadmill running in rats with IR induced by a high-fat diet (HFD) and elucidated the mechanism of the anti-IR effects of IL-15. At 20 weeks of HFD, rats showed severe IR, with increased levels of fasting blood sugar and plasma insulin, impaired glucose tolerance, and reduced glucose transport activity. IL-15 immunoreactivity and mRNA level in gastrocnemius muscle were decreased markedly as compared with controls. IL-15Rα protein and mRNA levels in both soleus and gastrocnemius muscle were significantly decreased, which might attenuate the signaling or secretion of IL-15 in muscle. Eight-week treadmill running completely ameliorated HFD-induced IR and reversed the downregulated level of IL-15 and IL-15Rα in skeletal muscle of HFD-fed rats. To investigate whether IL-15 exerts its anti-IR effects directly in muscle, we pre-incubated muscle strips with the endoplasmic reticulum stress (ERS) inducer dithiothreitol (DTT) or tunicamycin (Tm); IL-15 treatment markedly decreased the protein expression of the ERS markers 78-kDa glucose-regulated protein, 94-kDa glucose-regulated protein and C/EBP homologous protein and inhibited ERS induced by DTT or Tm. Therefore, treadmill running promoted skeletal IL-15 and IL-15Rα expression in HFD-induced IR in rats. The inhibitory effect of IL-15 on ERS may be involved in improved insulin sensitivity with exercise training.
Literature
1.
go back to reference M. Peppa, C. Koliaki, P. Nikolopoulos, S.A. Raptis, Skeletal muscle insulin resistance in endocrine disease. J. Biomed. Biotechnol. 2010, 527850 (2010)CrossRefPubMedCentralPubMed M. Peppa, C. Koliaki, P. Nikolopoulos, S.A. Raptis, Skeletal muscle insulin resistance in endocrine disease. J. Biomed. Biotechnol. 2010, 527850 (2010)CrossRefPubMedCentralPubMed
2.
go back to reference M.C. Venables, A.E. Jeukendrup, Physical inactivity and obesity: links with insulin resistance and type 2 diabetes mellitus. Diabetes Metab. Res. Rev. 5(Suppl 1), S18–S23 (2009)CrossRef M.C. Venables, A.E. Jeukendrup, Physical inactivity and obesity: links with insulin resistance and type 2 diabetes mellitus. Diabetes Metab. Res. Rev. 5(Suppl 1), S18–S23 (2009)CrossRef
3.
go back to reference M.A. Febbraio, N. Hiscock, M. Sacchetti, C.P. Fischer, B.K. Pedersen, Interleukin-6 is a novel factor mediating glucose homeostasis during skeletal muscle contraction. Diabetes 53, 1643–1648 (2004)CrossRefPubMed M.A. Febbraio, N. Hiscock, M. Sacchetti, C.P. Fischer, B.K. Pedersen, Interleukin-6 is a novel factor mediating glucose homeostasis during skeletal muscle contraction. Diabetes 53, 1643–1648 (2004)CrossRefPubMed
4.
go back to reference N.B. Ruderman, C. Keller, A.M. Richard, A.K. Saha, Z. Luo, X. Xiang, M. Giralt, V.B. Ritov, E.V. Menshikova, D.E. Kelley et al., 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–S54 (2006)CrossRefPubMed N.B. Ruderman, C. Keller, A.M. Richard, A.K. Saha, Z. Luo, X. Xiang, M. Giralt, V.B. Ritov, E.V. Menshikova, D.E. Kelley et al., 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–S54 (2006)CrossRefPubMed
5.
go back to reference B.K. Pedersen, M. Pedersen, K.S. Krabbe, H. Bruunsgaard, V.B. Matthews, M.A. Febbraio, Role of exercise-induced brain-derived neurotrophic factor production in the regulation of energy homeostasis in mammals. Exp. Physiol. 94, 1153–1160 (2009)CrossRefPubMed B.K. Pedersen, M. Pedersen, K.S. Krabbe, H. Bruunsgaard, V.B. Matthews, M.A. Febbraio, Role of exercise-induced brain-derived neurotrophic factor production in the regulation of energy homeostasis in mammals. Exp. Physiol. 94, 1153–1160 (2009)CrossRefPubMed
6.
go back to reference K.S. Krabbe, A.R. Nielsen, R. Krogh-Madsen, P. Plomgaard, P. Rasmussen, C. Erikstrup, D. Vyagova, V.N. Peneva, L. Aloe, Brain-derived neurotrophic factor (BDNF) and type 2 diabetes. Diabetologia 50, 431–438 (2007)CrossRefPubMed K.S. Krabbe, A.R. Nielsen, R. Krogh-Madsen, P. Plomgaard, P. Rasmussen, C. Erikstrup, D. Vyagova, V.N. Peneva, L. Aloe, Brain-derived neurotrophic factor (BDNF) and type 2 diabetes. Diabetologia 50, 431–438 (2007)CrossRefPubMed
7.
go back to reference J.M. Argilés, M. Orpí, S. Busquets, F.J. López-Soriano, Myostatin: more than just a regulator of muscle mass. Drug Discov. Today 17, 702–709 (2012)CrossRefPubMed J.M. Argilés, M. Orpí, S. Busquets, F.J. López-Soriano, Myostatin: more than just a regulator of muscle mass. Drug Discov. Today 17, 702–709 (2012)CrossRefPubMed
8.
go back to reference A. Di Sabatino, S.A. Calarota, F. Vidali, T.T. Macdonald, G.R. Corazza, Role of IL-15 in immune-mediated and infectious diseases. Cytokine Growth Factor Rev. 22, 19–33 (2011)CrossRefPubMed A. Di Sabatino, S.A. Calarota, F. Vidali, T.T. Macdonald, G.R. Corazza, Role of IL-15 in immune-mediated and infectious diseases. Cytokine Growth Factor Rev. 22, 19–33 (2011)CrossRefPubMed
9.
go back to reference L.S. Quinn, K.L. Haugk, K.H. Grabstein, Interleukin-15: a novel anabolic cytokine for skeletal muscle. Endocrinology 136, 3669–3672 (1995)PubMed L.S. Quinn, K.L. Haugk, K.H. Grabstein, Interleukin-15: a novel anabolic cytokine for skeletal muscle. Endocrinology 136, 3669–3672 (1995)PubMed
10.
go back to reference T. Sugiura, M. Harigai, Y. Kawaguchi, K. Takagi, C. Fukasawa, S. Ohsako-Higami, S. Ohta, M. Tanaka, M. Hara, N. Kamatani, Increased IL-15 production of muscle cells in polymyositis and dermatomyositis. Int. Immunol. 14, 917–924 (2002)CrossRefPubMed T. Sugiura, M. Harigai, Y. Kawaguchi, K. Takagi, C. Fukasawa, S. Ohsako-Higami, S. Ohta, M. Tanaka, M. Hara, N. Kamatani, Increased IL-15 production of muscle cells in polymyositis and dermatomyositis. Int. Immunol. 14, 917–924 (2002)CrossRefPubMed
11.
go back to reference L.S. Quinn, B.G. Anderson, R.H. Drivdahl, B. Alvarez, J.M. Argilés, Overexpression of interleukin-15 induces skeletal muscle hypertrophy in vitro: implications for treatment of muscle wasting disorders. Exp. Cell Res. 280, 55–63 (2002)CrossRefPubMed L.S. Quinn, B.G. Anderson, R.H. Drivdahl, B. Alvarez, J.M. Argilés, Overexpression of interleukin-15 induces skeletal muscle hypertrophy in vitro: implications for treatment of muscle wasting disorders. Exp. Cell Res. 280, 55–63 (2002)CrossRefPubMed
12.
go back to reference N. Carbó, J. López-Soriano, P. Costelli, S. Busquets, B. Alvarez, F.M. Baccino, L.S. Quinn, F.J. López-Soriano, J.M. Argilés, Interleukin-15 antagonizes muscle protein waste in tumour-bearing rats. Br. J. Cancer 83, 526–531 (2000)CrossRefPubMedCentralPubMed N. Carbó, J. López-Soriano, P. Costelli, S. Busquets, B. Alvarez, F.M. Baccino, L.S. Quinn, F.J. López-Soriano, J.M. Argilés, Interleukin-15 antagonizes muscle protein waste in tumour-bearing rats. Br. J. Cancer 83, 526–531 (2000)CrossRefPubMedCentralPubMed
13.
go back to reference G. Fuster, V. Almendro, C.C. Fontes-Oliveira, M. Toledo, P. Costelli, S. Busquets, F.J. López-Soriano, J.M. Argilés, Interleukin-15 affects differentiation and apoptosis in adipocytes: implications in obesity. Lipids 46, 1033–1042 (2011)CrossRefPubMed G. Fuster, V. Almendro, C.C. Fontes-Oliveira, M. Toledo, P. Costelli, S. Busquets, F.J. López-Soriano, J.M. Argilés, Interleukin-15 affects differentiation and apoptosis in adipocytes: implications in obesity. Lipids 46, 1033–1042 (2011)CrossRefPubMed
14.
go back to reference N.G. Barra, S. Reid, R. MacKenzie, G. Werstuck, B.L. Trigatti, C. Richards, A.C. Holloway, A.A. Ashkar, Interleukin-15 contributes to the regulation of murine adipose tissue and human adipocytes. Obesity (Silver Spring) 18, 1601–1607 (2010)CrossRef N.G. Barra, S. Reid, R. MacKenzie, G. Werstuck, B.L. Trigatti, C. Richards, A.C. Holloway, A.A. Ashkar, Interleukin-15 contributes to the regulation of murine adipose tissue and human adipocytes. Obesity (Silver Spring) 18, 1601–1607 (2010)CrossRef
15.
go back to reference N.G. Barra, M.V. Chew, A.C. Holloway, A.A. Ashkar, Interleukin-15 treatment improves glucose homeostasis and insulin sensitivity in obese mice. Diabetes Obes. Metab. 14, 190–193 (2012)CrossRefPubMed N.G. Barra, M.V. Chew, A.C. Holloway, A.A. Ashkar, Interleukin-15 treatment improves glucose homeostasis and insulin sensitivity in obese mice. Diabetes Obes. Metab. 14, 190–193 (2012)CrossRefPubMed
16.
go back to reference L.S. Quinn, B.G. Anderson, J.D. Conner, E.E. Pistilli, T. Wolden-Hanson, Overexpression of interleukin-15 in mice promotes resistance to diet-induced obesity, increased insulin sensitivity, and markers of oxidative skeletal muscle metabolism. Int. J. Interferon Cytokine Mediat. Res. 3, 29–42 (2011)CrossRef L.S. Quinn, B.G. Anderson, J.D. Conner, E.E. Pistilli, T. Wolden-Hanson, Overexpression of interleukin-15 in mice promotes resistance to diet-induced obesity, increased insulin sensitivity, and markers of oxidative skeletal muscle metabolism. Int. J. Interferon Cytokine Mediat. Res. 3, 29–42 (2011)CrossRef
17.
go back to reference L.S. Quinn, B.G. Anderson, L. Strait-Bodey, A.M. Stroud, J.M. Argilés, Oversecretion of interleukin-15 from skeletal muscle reduces adiposity. Am. J. Physiol. Endocrinol. Metab. 296, E191–E202 (2009)CrossRefPubMedCentralPubMed L.S. Quinn, B.G. Anderson, L. Strait-Bodey, A.M. Stroud, J.M. Argilés, Oversecretion of interleukin-15 from skeletal muscle reduces adiposity. Am. J. Physiol. Endocrinol. Metab. 296, E191–E202 (2009)CrossRefPubMedCentralPubMed
18.
go back to reference S. Busquets, M. Figueras, V. Almendro, F.J. Lopez-Soriano, J.M. Argiles, Interleukin-15 increases glucose uptake in skeletal muscle. An antidiabetogenic effect of the cytokine. Biochim. Biophys. Acta 1760, 1613–1617 (2006)CrossRefPubMed S. Busquets, M. Figueras, V. Almendro, F.J. Lopez-Soriano, J.M. Argiles, Interleukin-15 increases glucose uptake in skeletal muscle. An antidiabetogenic effect of the cytokine. Biochim. Biophys. Acta 1760, 1613–1617 (2006)CrossRefPubMed
19.
go back to reference S.R. Gray, T. Kamolrat, The effect of exercise induced cytokines on insulin stimulated glucose transport in C2C12 cells. Cytokine 55, 221–228 (2011)CrossRefPubMed S.R. Gray, T. Kamolrat, The effect of exercise induced cytokines on insulin stimulated glucose transport in C2C12 cells. Cytokine 55, 221–228 (2011)CrossRefPubMed
20.
go back to reference A.R. Nielsen, P. Hojman, C. Erikstrup, C.P. Fischer, P. Plomgaard, R. Mounier, O.H. Mortensen, C. Broholm, S. Taudorf, R. Krogh-Madsen et al., Association between interleukin-15 and obesity: interleukin-15 as a potential regulator of fat mass. J. Clin. Endocrinol. Metab. 93, 4486–4493 (2008)CrossRefPubMed A.R. Nielsen, P. Hojman, C. Erikstrup, C.P. Fischer, P. Plomgaard, R. Mounier, O.H. Mortensen, C. Broholm, S. Taudorf, R. Krogh-Madsen et al., Association between interleukin-15 and obesity: interleukin-15 as a potential regulator of fat mass. J. Clin. Endocrinol. Metab. 93, 4486–4493 (2008)CrossRefPubMed
21.
go back to reference A. Rinnov, C. Yfanti, S. Nielsen, T.C. Akerström, L. Peijs, A. Zankari, C.P. Fischer, B.K. Pedersen, Endurance training enhances skeletal muscle interleukin-15 in human male subjects. Endocrine 45, 271–278 (2014)CrossRefPubMed A. Rinnov, C. Yfanti, S. Nielsen, T.C. Akerström, L. Peijs, A. Zankari, C.P. Fischer, B.K. Pedersen, Endurance training enhances skeletal muscle interleukin-15 in human male subjects. Endocrine 45, 271–278 (2014)CrossRefPubMed
22.
go back to reference P. Boström, J. Wu, M.P. Jedrychowski, A. Korde, L. Ye, J.C. Lo, K.A. Rasbach, E.A. Boström, J.H. Choi, J.Z. Long et al., A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481, 463–468 (2012)CrossRefPubMedCentralPubMed P. Boström, J. Wu, M.P. Jedrychowski, A. Korde, L. Ye, J.C. Lo, K.A. Rasbach, E.A. Boström, J.H. Choi, J.Z. Long et al., A PGC1-α-dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481, 463–468 (2012)CrossRefPubMedCentralPubMed
23.
go back to reference N.H. Yeo, J. Woo, K.O. Shin, J.Y. Park, S. Kang, The effects of different exercise intensity on myokine and angiogenesis factors. J. Sports Med. Phys. Fit. 52, 48–54 (2012) N.H. Yeo, J. Woo, K.O. Shin, J.Y. Park, S. Kang, The effects of different exercise intensity on myokine and angiogenesis factors. J. Sports Med. Phys. Fit. 52, 48–54 (2012)
24.
go back to reference M. Wagner, D.D. Moore, Endoplasmic reticulum stress and glucose homeostasis. Curr. Opin. Clin. Nutr. Metab. Care 14, 367–373 (2011)CrossRefPubMed M. Wagner, D.D. Moore, Endoplasmic reticulum stress and glucose homeostasis. Curr. Opin. Clin. Nutr. Metab. Care 14, 367–373 (2011)CrossRefPubMed
25.
go back to reference S. Sundar Rajan, V. Srinivasan, M. Balasubramanyam, U. Tatu, Endoplasmic reticulum (ER) stress and diabetes. Indian J. Med. Res. 125, 411–424 (2007)PubMed S. Sundar Rajan, V. Srinivasan, M. Balasubramanyam, U. Tatu, Endoplasmic reticulum (ER) stress and diabetes. Indian J. Med. Res. 125, 411–424 (2007)PubMed
26.
go back to reference L. Deldicque, P. Hespel, M. Francaux, Endoplasmic reticulum stress in skeletal muscle: origin and metabolic consequences. Exerc. Sport Sci. Rev. 40, 43–49 (2012)CrossRefPubMed L. Deldicque, P. Hespel, M. Francaux, Endoplasmic reticulum stress in skeletal muscle: origin and metabolic consequences. Exerc. Sport Sci. Rev. 40, 43–49 (2012)CrossRefPubMed
27.
go back to reference S.L. Hwang, H.W. Chang, I.K. Lee, B.K. Yang, J. Magae, Y.C. Chang, Ascofuranone prevents ER stress-induced insulin resistance via activation of AMP-activated protein kinase in L6 myotube cells. Biochem. Biophys. Res. Commun. 396, 967–972 (2010)CrossRefPubMed S.L. Hwang, H.W. Chang, I.K. Lee, B.K. Yang, J. Magae, Y.C. Chang, Ascofuranone prevents ER stress-induced insulin resistance via activation of AMP-activated protein kinase in L6 myotube cells. Biochem. Biophys. Res. Commun. 396, 967–972 (2010)CrossRefPubMed
28.
go back to reference G.A. Raciti, C. Iadicicco, L. Ulianich, B.F. Vind, M. Gaster, F. Andreozzi, M. Longo, R. Teperino, P. Ungaro, B. Di Jeso et al., Glucosamine-induced endoplasmic reticulum stress affects GLUT4 expression via activating transcription factor 6 in rat and human skeletal muscle cells. Diabetologia 53, 955–965 (2010)CrossRefPubMed G.A. Raciti, C. Iadicicco, L. Ulianich, B.F. Vind, M. Gaster, F. Andreozzi, M. Longo, R. Teperino, P. Ungaro, B. Di Jeso et al., Glucosamine-induced endoplasmic reticulum stress affects GLUT4 expression via activating transcription factor 6 in rat and human skeletal muscle cells. Diabetologia 53, 955–965 (2010)CrossRefPubMed
29.
go back to reference E.K. Yoon, Y.T. Jeong, X. Li, Song-Cui, D.C. Park, Y.H. Kim, Y.D. Kim, H.W. Chang, S.H. Lee, S.L. Hwang, Glyceollin improves endoplasmic reticulum stress-induced insulin resistance through CaMKK–AMPK pathway in L6 myotubes. J. Nutr. Biochem. 24, 1053–1061 (2013)CrossRefPubMed E.K. Yoon, Y.T. Jeong, X. Li, Song-Cui, D.C. Park, Y.H. Kim, Y.D. Kim, H.W. Chang, S.H. Lee, S.L. Hwang, Glyceollin improves endoplasmic reticulum stress-induced insulin resistance through CaMKK–AMPK pathway in L6 myotubes. J. Nutr. Biochem. 24, 1053–1061 (2013)CrossRefPubMed
30.
go back to reference S.L. Hwang, Y.T. Jeong, X. Li, Y.D. Kim, Y. Lu, Y.C. Chang, I.K. Lee, H.W. Chang, Inhibitory cross-talk between the AMPK and ERK pathways mediates endoplasmic reticulum stress-induced insulin resistance in skeletal muscle. Br. J. Pharmacol. 169, 69–81 (2013)CrossRefPubMedCentralPubMed S.L. Hwang, Y.T. Jeong, X. Li, Y.D. Kim, Y. Lu, Y.C. Chang, I.K. Lee, H.W. Chang, Inhibitory cross-talk between the AMPK and ERK pathways mediates endoplasmic reticulum stress-induced insulin resistance in skeletal muscle. Br. J. Pharmacol. 169, 69–81 (2013)CrossRefPubMedCentralPubMed
31.
32.
go back to reference M.S. Gauthier, K. Couturier, A. Charbonneau, J.M. Lavoie, Effects of introducing physical training in the course of a 16-week high-fat diet regimen on hepatic steatosis, adipose tissue fat accumulation, and plasma lipid profile. Int. J. Obes. Relat. Metab. Disord. 28, 1064–1071 (2004)CrossRefPubMed M.S. Gauthier, K. Couturier, A. Charbonneau, J.M. Lavoie, Effects of introducing physical training in the course of a 16-week high-fat diet regimen on hepatic steatosis, adipose tissue fat accumulation, and plasma lipid profile. Int. J. Obes. Relat. Metab. Disord. 28, 1064–1071 (2004)CrossRefPubMed
33.
go back to reference D.R. Matthews, J.P. Hosker, A.S. Rudenski, B.A. Naylor, D.F. Treacher, R.C. Turner, Homeostasis model assessment: insulin resistance and b-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412–419 (1985)CrossRefPubMed D.R. Matthews, J.P. Hosker, A.S. Rudenski, B.A. Naylor, D.F. Treacher, R.C. Turner, Homeostasis model assessment: insulin resistance and b-cell function from fasting plasma glucose and insulin concentrations in man. Diabetologia 28, 412–419 (1985)CrossRefPubMed
34.
go back to reference M.C. Blendea, D. Jacobs, C.S. Stump, S.I. McFarlane, C. Ogrin, G. Bahtyiar, S. Stas, P. Kumar, Q. Sha, C.M. Ferrario et al., Abrogation of oxidative stress improves insulin sensitivity in the Ren-2 rat model of tissue angiotensin II overexpression. Am. J. Physiol. Endocrinol. Metab. 288, E353–E359 (2005)CrossRefPubMed M.C. Blendea, D. Jacobs, C.S. Stump, S.I. McFarlane, C. Ogrin, G. Bahtyiar, S. Stas, P. Kumar, Q. Sha, C.M. Ferrario et al., Abrogation of oxidative stress improves insulin sensitivity in the Ren-2 rat model of tissue angiotensin II overexpression. Am. J. Physiol. Endocrinol. Metab. 288, E353–E359 (2005)CrossRefPubMed
35.
go back to reference E.E. Pistilli, J.M. Devaney, H. Gordish-Dressman, M.K. Bradbury, R.L. Seip, P.D. Thompson, T.J. Angelopoulos, P.M. Clarkson, N.M. Moyna, L.S. Pescatello et al., Interleukin-15 and interleukin-15R alpha SNPs and associations with muscle, bone, and predictors of the metabolic syndrome. Cytokine 43, 45–53 (2008)CrossRefPubMedCentralPubMed E.E. Pistilli, J.M. Devaney, H. Gordish-Dressman, M.K. Bradbury, R.L. Seip, P.D. Thompson, T.J. Angelopoulos, P.M. Clarkson, N.M. Moyna, L.S. Pescatello et al., Interleukin-15 and interleukin-15R alpha SNPs and associations with muscle, bone, and predictors of the metabolic syndrome. Cytokine 43, 45–53 (2008)CrossRefPubMedCentralPubMed
36.
go back to reference A.R. Nielsen, P. Hojman, C. Erikstrup, C.P. Fischer, P. Plomgaard, R. Mounier, O.H. Mortensen, C. Broholm, S. Taudorf, R. Krogh-Madsen et al., Association between interleukin-15 and obesity: interleukin-15 as a potential regulator of fat mass. J. Clin. Endocrinol. Metab. 93, 4486–4493 (2008)CrossRefPubMed A.R. Nielsen, P. Hojman, C. Erikstrup, C.P. Fischer, P. Plomgaard, R. Mounier, O.H. Mortensen, C. Broholm, S. Taudorf, R. Krogh-Madsen et al., Association between interleukin-15 and obesity: interleukin-15 as a potential regulator of fat mass. J. Clin. Endocrinol. Metab. 93, 4486–4493 (2008)CrossRefPubMed
37.
go back to reference H.J. Kim, J.Y. Park, S.L. Oh, Y.A. Kim, B. So, J.K. Seong, W. Song, Effect of treadmill exercise on interleukin-15 expression and glucose tolerance in zucker diabetic fatty rats. Diabetes Metab. J. 37, 358–364 (2013)CrossRefPubMedCentralPubMed H.J. Kim, J.Y. Park, S.L. Oh, Y.A. Kim, B. So, J.K. Seong, W. Song, Effect of treadmill exercise on interleukin-15 expression and glucose tolerance in zucker diabetic fatty rats. Diabetes Metab. J. 37, 358–364 (2013)CrossRefPubMedCentralPubMed
38.
go back to reference M. Molanouri Shamsi, Z.H. Hassan, R. Gharakhanlou, L.S. Quinn, K. Azadmanesh, L. Baghersad, A. Isanejad, M. Mahdavi, Expression of interleukin-15 and inflammatory cytokines in skeletal muscles of STZ-induced diabetic rats: effect of resistance exercise training. Endocrine (2013). doi:10.1007/s12020-013-0038-4 PubMed M. Molanouri Shamsi, Z.H. Hassan, R. Gharakhanlou, L.S. Quinn, K. Azadmanesh, L. Baghersad, A. Isanejad, M. Mahdavi, Expression of interleukin-15 and inflammatory cytokines in skeletal muscles of STZ-induced diabetic rats: effect of resistance exercise training. Endocrine (2013). doi:10.​1007/​s12020-013-0038-4 PubMed
39.
go back to reference A.R. Nielsen, R. Mounier, P. Plomgaard, O.H. Mortensen, M. Penkowa, T. Speerschneider, H. Pilegaard, B.K. Pedersen, Expression of interleukin-15 in human skeletal muscle effect of exercise and muscle fibre type composition. J. Physiol. 584, 305–312 (2007)CrossRefPubMedCentralPubMed A.R. Nielsen, R. Mounier, P. Plomgaard, O.H. Mortensen, M. Penkowa, T. Speerschneider, H. Pilegaard, B.K. Pedersen, Expression of interleukin-15 in human skeletal muscle effect of exercise and muscle fibre type composition. J. Physiol. 584, 305–312 (2007)CrossRefPubMedCentralPubMed
40.
go back to reference E.E. Pistilli, L.S. Quinn, From anabolic to oxidative: reconsidering the roles of IL-15 and IL-15Rα in skeletal muscle. Exerc. Sport Sci. Rev. 41, 100–106 (2013)CrossRefPubMed E.E. Pistilli, L.S. Quinn, From anabolic to oxidative: reconsidering the roles of IL-15 and IL-15Rα in skeletal muscle. Exerc. Sport Sci. Rev. 41, 100–106 (2013)CrossRefPubMed
41.
go back to reference L. Deldicque, P.D. Cani, A. Philp, J.M. Raymackers, P.J. Meakin, M.L. Ashford, N.M. Delzenne, M. Francaux, K. Baar, The unfolded protein response is activated in skeletal muscle by high-fat feeding: potential role in the down-regulation of protein synthesis. Am. J. Physiol. Endocrinol. Metab. 299, E695–E705 (2010)CrossRefPubMed L. Deldicque, P.D. Cani, A. Philp, J.M. Raymackers, P.J. Meakin, M.L. Ashford, N.M. Delzenne, M. Francaux, K. Baar, The unfolded protein response is activated in skeletal muscle by high-fat feeding: potential role in the down-regulation of protein synthesis. Am. J. Physiol. Endocrinol. Metab. 299, E695–E705 (2010)CrossRefPubMed
42.
go back to reference M. Boyce, J. Yuan, Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ. 13, 363–373 (2006)CrossRefPubMed M. Boyce, J. Yuan, Cellular response to endoplasmic reticulum stress: a matter of life or death. Cell Death Differ. 13, 363–373 (2006)CrossRefPubMed
43.
go back to reference G. Peng, L. Li, Y. Liu, J. Pu, S. Zhang, J. Yu, J. Zhao, P. Liu, Oleate blocks palmitate-induced abnormal lipid distribution, endoplasmic reticulum expansion and stress, and insulin resistance in skeletal muscle. Endocrinology 152, 2206–2218 (2011)CrossRefPubMed G. Peng, L. Li, Y. Liu, J. Pu, S. Zhang, J. Yu, J. Zhao, P. Liu, Oleate blocks palmitate-induced abnormal lipid distribution, endoplasmic reticulum expansion and stress, and insulin resistance in skeletal muscle. Endocrinology 152, 2206–2218 (2011)CrossRefPubMed
44.
go back to reference U. Ozcan, E. Yilmaz, L. Ozcan, M. Furuhashi, E. Vaillancourt, R.O. Smith, C.Z. Görgün, G.S. Hotamisligil, Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313, 1137–1140 (2006)CrossRefPubMed U. Ozcan, E. Yilmaz, L. Ozcan, M. Furuhashi, E. Vaillancourt, R.O. Smith, C.Z. Görgün, G.S. Hotamisligil, Chemical chaperones reduce ER stress and restore glucose homeostasis in a mouse model of type 2 diabetes. Science 313, 1137–1140 (2006)CrossRefPubMed
46.
go back to reference G. da Luz, M.J. Frederico, S. da Silva, M.F. Vitto, P.A. Cesconetto, R.A. de Pinho, J.R. Pauli, A.S. Silva, D.E. Cintra, E.R. Ropelle et al., Endurance exercise training ameliorates insulin resistance and reticulum stress in adipose and hepatic tissue in obese rats. Eur. J. Appl. Physiol. 111, 2015–2023 (2011)CrossRefPubMed G. da Luz, M.J. Frederico, S. da Silva, M.F. Vitto, P.A. Cesconetto, R.A. de Pinho, J.R. Pauli, A.S. Silva, D.E. Cintra, E.R. Ropelle et al., Endurance exercise training ameliorates insulin resistance and reticulum stress in adipose and hepatic tissue in obese rats. Eur. J. Appl. Physiol. 111, 2015–2023 (2011)CrossRefPubMed
47.
go back to reference J. Wu, J.L. Ruas, J.L. Estall, K.A. Rasbach, J.H. Choi, L. Ye, P. Boström, H.M. Tyra, R.W. Crawford, K.P. Campbell et al., The unfolded protein response mediates adaptation to exercise in skeletal muscle through a PGC-1alpha/ATF6alpha complex. Cell Metab. 13, 160Y9 (2011)CrossRef J. Wu, J.L. Ruas, J.L. Estall, K.A. Rasbach, J.H. Choi, L. Ye, P. Boström, H.M. Tyra, R.W. Crawford, K.P. Campbell et al., The unfolded protein response mediates adaptation to exercise in skeletal muscle through a PGC-1alpha/ATF6alpha complex. Cell Metab. 13, 160Y9 (2011)CrossRef
48.
49.
go back to reference G. Fuster, S. Busquets, M. Figueras, E. Ametller, C.C. Fontes de Oliveira, M. Oliván, P.A. Grimaldi, J.M. Argilés, F.J. López-Soriano, PPARdelta mediates IL15 metabolic actions in myotubes: effects of hyperthermia. Int. J. Mol. Med. 24, 63–68 (2009)PubMed G. Fuster, S. Busquets, M. Figueras, E. Ametller, C.C. Fontes de Oliveira, M. Oliván, P.A. Grimaldi, J.M. Argilés, F.J. López-Soriano, PPARdelta mediates IL15 metabolic actions in myotubes: effects of hyperthermia. Int. J. Mol. Med. 24, 63–68 (2009)PubMed
50.
go back to reference L.S. Quinn, B.G. Anderson, J.D. Conner, T. Wolden-Hanson, IL-15 overexpression promotes endurance, oxidative energy metabolism, and muscle PPARδ, SIRT1, PGC-1α, and PGC-1β expression in male mice. Endocrinology 154, 232–245 (2013)CrossRefPubMedCentralPubMed L.S. Quinn, B.G. Anderson, J.D. Conner, T. Wolden-Hanson, IL-15 overexpression promotes endurance, oxidative energy metabolism, and muscle PPARδ, SIRT1, PGC-1α, and PGC-1β expression in male mice. Endocrinology 154, 232–245 (2013)CrossRefPubMedCentralPubMed
51.
go back to reference L.S. Quinn, B.G. Anderson, J.D. Conner, T. Wolden-Hanson, T.J. Marcell, IL-15 is required for postexercise induction of the pro-oxidative mediators PPARδ and SIRT1 in male mice. Endocrinology 155, 143–155 (2014)CrossRefPubMed L.S. Quinn, B.G. Anderson, J.D. Conner, T. Wolden-Hanson, T.J. Marcell, IL-15 is required for postexercise induction of the pro-oxidative mediators PPARδ and SIRT1 in male mice. Endocrinology 155, 143–155 (2014)CrossRefPubMed
52.
go back to reference M. Cao, Y. Tong, Q. Lv, X. Chen, Y. Long, L. Jiang, J. Wan, Y. Zhang, F. Zhang, N. Tong, PPARδ activation rescues pancreatic β-cell line INS-1E from palmitate-induced endoplasmic reticulum stress through enhanced fatty acid oxidation. PPAR Res. 2012, 680684 (2012)CrossRefPubMedCentralPubMed M. Cao, Y. Tong, Q. Lv, X. Chen, Y. Long, L. Jiang, J. Wan, Y. Zhang, F. Zhang, N. Tong, PPARδ activation rescues pancreatic β-cell line INS-1E from palmitate-induced endoplasmic reticulum stress through enhanced fatty acid oxidation. PPAR Res. 2012, 680684 (2012)CrossRefPubMedCentralPubMed
53.
go back to reference T. Ramirez, M. Tong, W.C. Chen, Q.G. Nguyen, J.R. Wands, S.M. de la Monte, Chronic alcohol-induced hepatic insulin resistance and endoplasmic reticulum stress ameliorated by peroxisome-proliferator activated receptor-δ agonist treatment. J. Gastroenterol. Hepatol. 28, 179–187 (2013)CrossRefPubMed T. Ramirez, M. Tong, W.C. Chen, Q.G. Nguyen, J.R. Wands, S.M. de la Monte, Chronic alcohol-induced hepatic insulin resistance and endoplasmic reticulum stress ameliorated by peroxisome-proliferator activated receptor-δ agonist treatment. J. Gastroenterol. Hepatol. 28, 179–187 (2013)CrossRefPubMed
54.
go back to reference T.W. Jung, K.T. Lee, M.W. Lee, K.H. Ka, SIRT1 attenuates palmitate-induced endoplasmic reticulum stress and insulin resistance in HepG2 cells via induction of oxygen-regulated protein 150. Biochem. Biophys. Res. Commun. 422, 229–232 (2012)CrossRefPubMed T.W. Jung, K.T. Lee, M.W. Lee, K.H. Ka, SIRT1 attenuates palmitate-induced endoplasmic reticulum stress and insulin resistance in HepG2 cells via induction of oxygen-regulated protein 150. Biochem. Biophys. Res. Commun. 422, 229–232 (2012)CrossRefPubMed
55.
go back to reference Y. Li, S. Xu, A. Giles, K. Nakamura, J.W. Lee, X. Hou, G. Donmez, J. Li, Z. Luo, K. Walsh, Hepatic overexpression of SIRT1 in mice attenuates endoplasmic reticulum stress and insulin resistance in the liver. FASEB J. 25, 1664–1679 (2011)CrossRefPubMedCentralPubMed Y. Li, S. Xu, A. Giles, K. Nakamura, J.W. Lee, X. Hou, G. Donmez, J. Li, Z. Luo, K. Walsh, Hepatic overexpression of SIRT1 in mice attenuates endoplasmic reticulum stress and insulin resistance in the liver. FASEB J. 25, 1664–1679 (2011)CrossRefPubMedCentralPubMed
Metadata
Title
IL-15 expression increased in response to treadmill running and inhibited endoplasmic reticulum stress in skeletal muscle in rats
Authors
Hong-Tao Yang
Li-Jie Luo
Wen-Jia Chen
Lei Zhao
Chao-Shu Tang
Yong-Fen Qi
Jing Zhang
Publication date
01-02-2015
Publisher
Springer US
Published in
Endocrine / Issue 1/2015
Print ISSN: 1355-008X
Electronic ISSN: 1559-0100
DOI
https://doi.org/10.1007/s12020-014-0233-y

Other articles of this Issue 1/2015

Endocrine 1/2015 Go to the issue
Live Webinar | 27-06-2024 | 18:00 (CEST)

Keynote webinar | Spotlight on medication adherence

Live: Thursday 27th June 2024, 18:00-19:30 (CEST)

WHO estimates that half of all patients worldwide are non-adherent to their prescribed medication. The consequences of poor adherence can be catastrophic, on both the individual and population level.

Join our expert panel to discover why you need to understand the drivers of non-adherence in your patients, and how you can optimize medication adherence in your clinics to drastically improve patient outcomes.

Prof. Kevin Dolgin
Prof. Florian Limbourg
Prof. Anoop Chauhan
Developed by: Springer Medicine
Obesity Clinical Trial Summary

At a glance: The STEP trials

A round-up of the STEP phase 3 clinical trials evaluating semaglutide for weight loss in people with overweight or obesity.

Developed by: Springer Medicine

Highlights from the ACC 2024 Congress

Year in Review: Pediatric cardiology

Watch Dr. Anne Marie Valente present the last year's highlights in pediatric and congenital heart disease in the official ACC.24 Year in Review session.

Year in Review: Pulmonary vascular disease

The last year's highlights in pulmonary vascular disease are presented by Dr. Jane Leopold in this official video from ACC.24.

Year in Review: Valvular heart disease

Watch Prof. William Zoghbi present the last year's highlights in valvular heart disease from the official ACC.24 Year in Review session.

Year in Review: Heart failure and cardiomyopathies

Watch this official video from ACC.24. Dr. Biykem Bozkurt discusses last year's major advances in heart failure and cardiomyopathies.