Oversecretion of interleukin-15 from skeletal muscle reduces adiposity

American Journal of Physiology - Endocrinology and Metabolism

Volumn 296, Issue 1, 2009, Pages

  Quinn, Lebris S ^a,b,c,f   Anderson, Barbara G ^a,c   Strait Bodey, Lena ^d   Stroud, Ashley M ^c,d   Argués, Josép M ^e  

^a Clinical Center   (Spain)

^b Puget Sound HC System   (United States)

^c UNIVERSITY OF WASHINGTON   (United States)

^d Seattle Institute for Biomedical and Clinical Research   (United States)

^e UNIVERSITY OF BARCELONA   (Spain)

^f VA PUGET SOUND HEALTH CARE SYSTEM   (United States)

Author keywords

Adipokines; Adipose tissue; Body composition; Bone; Cytokines; Interleukin 15; Myokines; Obesity; Skeletal muscle

Indexed keywords

INTERLEUKIN 15;

ADIPOSE TISSUE; ANIMAL EXPERIMENT; ARTICLE; BODY COMPOSITION; BODY FAT; BONE MINERAL; CONTROLLED STUDY; CYTOKINE PRODUCTION; LEAN BODY WEIGHT; LIPID DIET; MOUSE; NONHUMAN; OBESITY; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; SKELETAL MUSCLE; TRANSGENIC MOUSE;

ADIPOSITY; ANIMALS; BODY COMPOSITION; CROSSES, GENETIC; DIETARY FATS; FEMALE; INTERLEUKIN-15; MALE; MICE; MICE, INBRED C3H; MICE, INBRED C57BL; MICE, TRANSGENIC; MUSCLE, SKELETAL; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SPECIFIC PATHOGEN-FREE ORGANISMS;

EID: 58249096194     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.90506.2008     Document Type: Article

References (74)

1. Ajuwon KM, Spurlock ME. Direct regulation of lipolysis by interleukin-15 in primary pig adipocytes. Am J Physiol Regul Integr Comp Physiol 287: R608-R611, 2004.
2. 14C]-triolein load. Biochem Biophys Acta 1761: 37-42, 2006.
3. Alvarez B, Carbtó N, López-Soriano J, Drivdahl RH, Busquets S, López-Soriano FJ, Argilés JM, Quinn LS. Effects of interleukin-15 (IL-15) on adipose tissue mass in rodent obesity models: evidence for direct IL-15 action on adipose tissue. Biochem Biophys Acta 1570: 33-37, 2002.
4. Bergamaschi C, Rosati M, Jalah R, Valentin A, Kulkarni V, Alicea C, Zhang GM, Patel V, Felber BK, Pavlakis GN. Intracellular interaction of interleukin-15 with its receptor a during production leads to mutual stabilization and increased bioactivity. J Biol Chem 283: 4189-4199, 2008.
5. Brennan KJ, Hardeman EC. Quantitative analysis of the human α-skeletal actin gene in transgenic mice. J Biol Chem 268: 719 -725, 1993.
6. Budagian V, Bulanova E, Paus R, Bulfone-Paus S. IL-15/IL-15 receptor biology: a guided tour through an expanding universe. Cytokine Growth Factor Rev 17: 259-280, 2006.
7. Bulanova E, Budagian V, Duitman E, Orinska Z, Krause H, Ruckert R, Reiling N, Bulfone-Paus S. Soluble interleukin-15Ralpha is generated by alternative splicing or proteolytic cleavage and forms functional complexes with IL-15. J Biol Chem 282: 13167-13179, 2007.
8. Bulfone-Paus S, Bulanova E, Pohl T, Budagian V, Durkop H, Ruckert R, Kunzendorf U, Paus R, Krause H. Death deflected: IL-15 inhibits TNF-α-mediated apoptosis in fibroblasts by TRAF2 recruitment to the IL-15Ra chain. FASEB J 13: 1575-1585, 1999.
9. Busquets S, Figueras MT, Meijsing S, Carbó N, Quinn LS, Almendro V, Argilés JM, López-Soriano FJ. Interleukin-15 decreases proteolysis in skeletal muscle: A direct effect. Int J Mol Med 16: 471-476, 2005.
10. Busquets S, Figueras M, Almendro V, López-Soriano FJ, Argilés JM. Interleukin-15 increases glucose uptake in skeletal muscle. An antidiabetogenic effect of the cytokine. Biochem Biophys Acta 1760: 1613-1617, 2006.
11. CarbóN, López-Soriano J, Costelli P, Busquets S, Alvarez B, Baccino FM, Quinn LS, López-Soriano FJ, Argilés JM. Interleukin-15 antagonizes muscle protein waste in tumour-bearing rats. Br J Cancer 83: 526-531, 2000.
12. CarbóN, López-Soriano J, Costelli P, Alvarez B, Busquets S, Baccino FM, Quinn LS, López-Soriano FJ, Argilés JM. Interleukin-15 mediates reciprocal regulation of adipose and muscle mass: a potential role in body weight control. Biochem Biophys Acta 1526: 17-24, 2001.
13. Cauley JA, Danielson ME, Boudreau RM, Forest KYZ, Zmuda JM, Pahor M, Tylavsky FA, Cummings SR, Harris TB, Newman AB. Inflammatory markers and incident fracture risk in older men and women: the Health Aging and Body Composition study. J Bone Miner Res 22: 1088-1095, 2007.
14. Cesari M, Kritchevsky SB, Baumgartner RN, Atkinson HH, Penninx BWHJ, Lenchik L, Palla SL, Ambrosius WT, Tracy RP, Pahor M. Sarcopenia, obesity, and inflammation: results from the Trial of Angiotension Converting Enzyme Inhibition and Novel Cardiovascular Risk Factors study. Am J Clin Nutr 82: 428-434, 2005.
15. Crawford GE, Faulkner JA, Crosbie RH, Campbell KP, Froehner SC, Chamberlain JS. Assembly of the dystrophin-associated protein complex does not require the dystrophin COOH-terminal domain. J Cell Biol 150: 1399 -1410, 2000.
16. Di Renzo L, Bigioni M, Bottini FG, Del Grobbo V, Premrov MG, Cianci R, De Lorenzo A. Normal Weight Obese syndrome: role of single nucleotide polymorphism of IL-15Rα and MTHFR 677→T genes in the relationship between body composition and resting metabolic state. Eur Rev Med Pharm Sci 10: 235-245, 2006.
17. Dyck DJ, Heignehauser GJF, Bruce CR. The role of adipokines as regulators of skeletal muscle fatty acid metabolism and insulin sensitivity. Acta Physiol 186: 5-16, 2006.
18. Fehniger TA, Suzuki K, Ponnappan A, VanDeusen JB, Cooper MA, Florea SM, Freud AG, Robinison ML, Durbin J, Caliguiri MA. Fatal leukemia in interleukin 15 transgenic mice follows early expansions in natural killer and memory phenotype CD8+ T cells. J Exptl Med 193: 219-231, 2001.
19. Figueras M, Busquets S, Carbó N, Barreiro E, Almendro V, Argilés JM, López-Soriano FJ. Interleukin-15 is able to suppress the increased DNA fragmentation associated with muscle wasting in tumour-bearing rats. FEBS Lett 569: 201-206, 2004.
20. Frost RA, Lang CH. Skeletal muscle cytokines: regulation by pathogen-associated molecules and catabolic hormones. Curr Opin Clin Nutr Metab Care 8: 255-263, 2005.
21. Goodman MN. Interleukin-6 induces skeletal muscle protein breakdown in rats. Proc Soc Exp Biol Med 205: 182-185, 1994.
22. 2 synthesis in chrondrocytes. Arthr Rheum 58: 1399-1409, 2008.
23. Grabstein KH, Eisenman J, Shanebeck K, Rauch C, Srinivasan S, Fung V, Beers C, Richardson J, Schoenborn MA, Ahdieh M, Johnson L, Alderson MR, Watson JD, Anderson DM, Giri J. Cloning of a T cell growth factor that interacts with the beta chain of the interleukin-2 receptor. Science 264: 965-968, 1994.
24. Harcourt LJ, Holmes AG, Gregorevic P, Schertzer JD, Stupka N, Plant DR, Lynch GS. Interleukin-15 administration improves diaphragm muscle pathology and function in dystrophic mdx mice. Am J Pathol 166: 1131-1141, 2005.
25. Hill JA, Wyatt HR, Reed GW, Peters JC. Obesity and the environment: where do we go from here? Science 299: 853-855, 2003.
26. Hoene M, Weigert C. The role of inteleukin-6 in insulin resistance, body fat distribution and energy balance. Obes Rev 9: 20 -29, 2008.
27. Hotamisligil GS. Inflammation and metabolic disorders. Nature 444: 860-867, 2006.
28. Huising MO, Kruiswijk CP, Flik G. Phylogeny and evolution of class-I helical cytokines. J Endocrinol 189: 1-25, 2006.
29. Jacobi SK, Gabler NK, Ajuwon KM, Davis JE, Spurlock ME. Adipocytes, myofibers, and cytokine biology: new horizons in the regulation of growth and body composition. J Anim Sci 84: E140-E149, 2006.
30. Kahn SE, Hull RL, Utzschneider KM. Mechanisms linking obesity to insulin resistance and type 2 diabetes. Nature 444: 840-846, 2006.
31. Kelley KW, Weigent DA, Kooijman R. Protein hormones and immunity. Brain Behav Immun 21: 384-392, 2007.
32. Kennedy MK, Glaccum M, Brown SN, Butz EA, Viney JL, Embers M, Matsuki N, Charrier K, Sedger L, Willis CR, Brasel K, Morrissey PJ, Stocking K, Schuh JCL, Joyce S, Peschon JJ. Reversible defects in natural killer and memory CD8 T cell lineages in interleukin-15-deficient mice. J Exp Med 191: 771-780, 2000.
33. Klover PJ, Clementi AH, Mooney RA. Interleukin-6 depletion selectively improves hepatic insulin action in obesity. Endocrinol 146: 3417-3427, 2005.
34. Kubota T, Brown RA, Fang J, Krueger JM. Interleukin-15 and inter-leukin-2 enhance non-REM sleep in rabbits. Am J Physiol Regul Integr Comp Physiol 281: R1004-R10012, 2001.
35. Lai KMV, Gonzalez M, Poueymirou WT, Kline WO, Na E, Zlotchenko E, Stitt TN, Economides AR, Yancopoulos GD, Glass DJ. Conditional activation of Akt in adult skeletal muscle induces rapid hypertrophy. Molec Cell Biol 24: 9295-9304, 2004.
36. Lambert CP, Flynn MG, Sullivan DH, Evans WJ. Effects of megestrol acetate on circulating interleukin-15 and interleukin-18 concentrations in healthy elderly men. J Gerontol 59A: 855-858, 2004.
37. Landt M, Gingerich RL, Havel PJ, Mueller WM, Schoner B, Hale JE, Heiman ML. Radioimmunoassay of rat leptin: sexual dimorphism reversed from humans. Clin Chem 44: 565-570, 1998.
38. Lebrun CEI, van der Schouw YT, de Jong FH, Grobbee DE, Lamberts SW. Fat mass rather than muscle strength is the major determinant of physical function and disability in postmenopausal women younger than 75 years of age. Menopause 13: 474-481, 2006.
39. T method. Methods 25: 402-408, 2001.
40. Lollini PL, Palmieri G, De Giovanni C, Landuzzi L, Nicoletti G, Rossi I, Griffoni C, Frabetti F, Scotland K, Benini S, Baldini N, Santoni A, Nanni P. Expression of interleukin 15 (IL-15) in human rhabdomyosar-coma, osteosarcoma and Ewing's sarcoma. Intl J Cancer 71: 732-736, 1997.
41. Maynes JS, Watson GH. Direct effects of sex steroid hormones on adipose tissues and obesity. Obesity Rev 5: 197-216, 2004.
42. McPherron AC, Lawler AM, Lee SJ. Regulation of skeletal muscle mass in mice by a new TGF-β superfamily member. Nature 387: 83-90, 1997.
43. McPherron AC, Lee SJ. Double muscling in cattle due to mutations in the myostatin gene. Proc Natl Acad Sci USA 94: 12457-12461, 1997.
44. McPherron AC, Lee SJ. Suppression of body fat accumulation in myostatin-deficient mice. J Clin Invest 109: 595-601, 2002.
45. Nagy TR, Clair AL. Precision and accuracy of dual-enery X-ray absorptiometry for determining in vivo body composition of mice. Obes Res 8: 392-398, 2000.
46. Nielsen AR, Mounier R, Plomgaard P, Mortensen OH, Penkowa M, Speerschneider T, Pilegaard H, Pedersen BK. Expression of interleukin-15 in human skeletal muscle: effect of exercise and muscle fibre type composition. J Physiol 584: 305-312, 2007.
47. Nishimura H, Fujimoto A, Tamura N, Yajima T, Wajjwalku W, Yoshikai Y. A novel autoregulatory mechanism for transcriptional activation of the IL-15 gene by a nonsecretable isoform of IL-15 generated by alternative splicing. FASEB J 19: 19-28, 2005.
48. Otero M, Lago R, Lago F, Casanueva FF, Dieguez C, Gómez-Reino JJ, Gualillo O. Leptin, from fat to inflammation: old questions and new insights. FEBS Lett 579: 295-301, 2005.
49. Pedersen BK, Akerstrom TC, Nielsen AR, Fischer CP. Role of myokines in exercise and metabolism. J Appl Physiol 103: 1093-1098, 2007.
50. Pedersen BK, Fischer CP. Physiological roles of muscle-derived interleukin-6 in response to exercise. Curr Opin Clin Nutr Metab Care 10: 265-271, 2007.
51. Pischon T, Nothlings U, Boeing H. Obesity and cancer. Proc Nutr Soc 67: 128-145, 2008.
52. Pistilli EE, Devaney JM, Gordish-Dressman H, Bradbury MK, Seip RL, Thompson PD, Angelopoulos TJ, Clarkson PM, Moyna NM, Pescatello LS, Visich PS, Zoeller RF, Gordon PM, Hoffman EP. Interleukin-15 and insterleukin-15Ralpha SNPs and associations with muscle, bone, and predictors of the metabolic syndrome. Cytokine doi:10.1016/j.cyto.2008.04.008.PMID18514540.2008.
53. Prinz M, Hanisch UK, Kettenmann H, Kirchohoff F. Alternative splicing of mouse IL-15 is due to the use of an internal splice site in exon 5. Mol Brain Res 63: 155-162, 1998.
54. Quinn LS, Anderson BG, Drivdahl RH, Alvarez B, Argilés JM. Overexpression of interleukin-15 induces skeletal muscle hypertrophy in vitro: implications for treatment of muscle wasting disorders. Exp Cell Res 280: 55-63, 2002.
55. Quinn LS, Strait-Bodey L, Anderson BG, Argilés JM, Havel PJ. Interleukin-15 stimulates adiponectin secretion by 3T3-L1 adipocytes: evidence for a skeletal muscle-to-fat signaling pathway. Cell Biol Intl 29: 449-457, 2005.
56. Quinn LS. Interleukin-15: a muscle-derived cytokine regulating fat-to-lean body composition. J Anim Sci 86: E75-E83, 2008.
57. Reid MB, Li YP. Tumor necrosis factor-alpha and muscle wasting: a cellular perspective. Respir Res 2: 269 -272, 2001.
58. Riechman SE, Balasekaran G, Roth SM, Ferrell RE. Association of interleukin-15 protein and interleukin-15 receptor genetic variation with resistance exercise training responses. J Appl Physiol 97: 2214-2219, 2004.
59. Rosen C, Bouxsein ML. Mechanisms of disease: is osteoporosis the obesity of bone? Nat Clin Pract Rheumatol 2: 35-43, 2006.
60. Rosen ED, Spiegelman BM. Adipocytes as regulators of energy balance and glucose homeostasis. Nature 444: 847-853, 2006.
61. Schluns KS, Stoklasek T, Lefrançois L. The roles of interleukin-15 receptor α: trans-presentation, receptor component, or both? Intl J Biochem Cell Biol 37: 1567-1571, 2005.
62. Serrano AL, Baeza-Raja B, Perdiguero E, Jardí M, Munoz-Cánoves P. Interleukin-6 is an essential regulator of satellite cell-mediated skeletal muscle hypertrophy. Cell Metab 7: 33-44, 2008.
63. Sugiura T, Harigai M, Kawaguchi Y, Takagi K, Fukasawa C, Ohsako-Higami S, Ohta S, Tanaka M, Masako H, Kamatani N. Increased IL-15 production of muscle cells in polymyositis and dermatomyositis. Intl Immunol 14: 917-924, 2002.
64. Sun X, Zemel MB. Leucine and calcium regulate fat metabolism and energy partitioning in murine adipocytes and muscle cells. Lipids 42: 297-305, 2007.
65. Tagaya Y, Bamford RN, DeFilippis AP, Waldmann TA. IL-15: A pleiotropic cytokine with diverse receptor/signaling pathways whose expression is controlled at multiple levels. Immunity 4: 329 -336, 1996.
66. Tagaya Y, Kurys G, Thies TA, Losi JM, Azimi N, Hanover JA, Bamford RN, Waldmann TA. Generation of secretable and nonsecretable interleukin 15 isoforms through alternate usage of signal peptides. Proc Natl Acad Sci USA 94: 14444-14449, 1997.
67. Tinsley FC, Taicher GZ, Heiman ML. Evaluation of a quantitative magnetic resonance method for mouse whole body composition analysis. Obesity Res 12: 150-160, 2004.
68. Trujillo ME, Scherer PE. Adipose tissue-derived factors: impact on health and disease. Endocrine Rev 27: 762-778, 2006.
69. Tsujinaka T, Ebisui C, Fujita J, Kishibuchi M, Morimoto T, Ogawa A, Katsume A, Ohsugi Y, Kominami E, Monden M. Muscle undergoes atrophy in association with increase of lysosomal cathepsin activity in interleukin-6 transgenic mouse. Biochem Biophys Res Commun 207: 168-174, 1995.
70. Van Gaal LF, Mertens IL, De Block. Mechanisms linking obesity with cardiovascular disease. Nature 444: 875-880, 2006.
71. Weisberg SP, McCann D, Desai M, Rosenbaum M, Leibel RL, Ferrante AW. Obesity is associated with macrophage accumulation in adipose tissue. J Clin Invest 112: 1796-1808, 2003.
72. Xu H, Barnes GT, Yang Q, Tan G, Yang D, Chou Sole J CJ, Nichols A, Ross JS, Tartaglia LA, Chen H. Chronic inflammation in fat plays a crucial role in the development of obesity-related insulin resistance. J Clin Invest 112: 1821-1830, 2002.
73. Yang J, Zhao B. Postnatal expression of myostatin propeptide cDNA maintained high muscle growth and normal adipose tissue mass in transgenic mice fed a high-fat diet. Mol Reprod Dev 73: 462-469, 2006.
74. Zimmers TA, Davies MV, Koniaris LG, Haynes P, Esquela AF, Tomkinson KN, McPherron AC, Wolfman NM, Lee SJ. Induction of cachexia in mice by systemically administered myostatin. Science 296: 1486 -1488, 2002.