Exercise-stimulated interleukin-15 is controlled by AMPK and regulates skin metabolism and aging

Aging Cell

Volumn 14, Issue 4, 2015, Pages 625-634

  Crane, Justin D ^a   Macneil, Lauren G ^a   Lally, James S ^a   Ford, Rebecca J ^a   Bujak, Adam L ^a   Brar, Ikdip K ^a   Kemp, Bruce E ^b   Raha, Sandeep ^a   Steinberg, Gregory R ^a   Tarnopolsky, Mark A ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b UNIVERSITY OF MELBOURNE   (Australia)

Author keywords

Aging; Exercise; Metabolism; Mitochondria; Muscle; Skin

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; CYTOCHROME B; CYTOCHROME C OXIDASE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; INTERLEUKIN 10; INTERLEUKIN 15; LYMPHOTOXIN; MESSENGER RNA; MITOCHONDRIAL PROTEIN; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA COACTIVATOR 1ALPHA; RECOMBINANT INTERLEUKIN 15; UBIQUINOL CYTOCHROME C REDUCTASE; COX7B PROTEIN, HUMAN; NADH DEHYDROGENASE SUBUNIT 1, HUMAN; PPARGC1A PROTEIN, HUMAN; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; TRANSCRIPTION FACTOR;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CHEEK CELL; CONTROLLED STUDY; CROSS-SECTIONAL STUDY; ENDURANCE TRAINING; ENERGY METABOLISM; EXERCISE; GLUCOSE TRANSPORT; GRIP STRENGTH; HUMAN; HUMAN CELL; METABOLISM; MITOCHONDRIAL BIOGENESIS; MITOCHONDRIAL RESPIRATION; MOUSE; MUSCLE MASS; MUSCLE MITOCHONDRION; MUSCLE STRENGTH; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; SEDENTARY LIFESTYLE; SKELETAL MUSCLE; SKIN FIBROBLAST; SKIN FUNCTION; SKIN STRUCTURE; SKINFOLD THICKNESS; STRATUM CORNEUM; TREADMILL EXERCISE; ADULT; AGED; ANIMAL; C57BL MOUSE; FEMALE; GENE EXPRESSION REGULATION; GENETICS; MALE; MIDDLE AGED; MITOCHONDRION; PATHOLOGY; SIGNAL TRANSDUCTION; SKIN; VERY ELDERLY;

ADULT; AGED; AGED, 80 AND OVER; AGING; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ELECTRON TRANSPORT COMPLEX IV; EXERCISE; FEMALE; GENE EXPRESSION REGULATION; HUMANS; INTERLEUKIN-15; MALE; MICE; MICE, INBRED C57BL; MIDDLE AGED; MITOCHONDRIA; MUSCLE, SKELETAL; NADH DEHYDROGENASE; PEROXISOME PROLIFERATOR-ACTIVATED RECEPTOR GAMMA COACTIVATOR 1-ALPHA; PHYSICAL CONDITIONING, ANIMAL; RNA, MESSENGER; SIGNAL TRANSDUCTION; SKIN; TRANSCRIPTION FACTORS;

EID: 84928348920     PISSN: 14749718     EISSN: 14749726     Source Type: Journal    
DOI: 10.1111/acel.12341     Document Type: Article

References (45)

1. Anderson DM, Kumaki S, Ahdieh M, Bertles J, Tometsko M, Loomis A, Giri J, Copeland NG, Gilbert DJ, Jenkins NA (1995) Functional characterization of the human interleukin-15 receptor alpha chain and close linkage of IL15RA and IL2RA genes. J. Biol. Chem. 270, 29862-29869.
2. Bamford RN, DeFilippis AP, Azimi N, Kurys G, Waldmann TA (1998) The 5’ untranslated region, signal peptide, and the coding sequence of the carboxyl terminus of IL-15 participate in its multifaceted translational control. J. Immunol. 160, 4418-4426.
3. Boström P, Wu J, Jedrychowski MP, Korde A, Ye L, Lo JC, Rasbach KA, Bostrom EA, Choi JH, Long JZ, Kajimura S, Zingaretti MC, Vind BF, Tu H, Cinti S, Hojlund K, Gygi SP, Spiegelman BM (2012) A PGC1-a- dependent myokine that drives brown-fat-like development of white fat and thermogenesis. Nature 481:7382, 463-468.
4. Chakravarty EF, Hubert HB, Lingala VB, Fries JF (2008) Reduced disability and mortality among aging runners: a 21-year longitudinal study. Arch. Intern. Med. 168, 1638-1646.
5. Chen J, Feigenbaum L, Awasthi P, Butcher DO, Anver MR, Golubeva YG, Bamford R, Zhang X, St Claire MB, Thomas CJ, Discepolo V, Jabri B, Waldmann TA (2013) Insulin-dependent diabetes induced by pancreatic beta cell expression of IL-15 and IL-15Ra. Proc. Natl Acad. Sci. USA 110, 13534-13539.
6. Coppé J-P, Patil CK, Rodier F, Sun Y, Muñoz DP, Goldstein J, Nelson PS, Desprez P, Campisi J (2008) Senescence- associated secretory phenotypes reveal cellnonautonomous functions of oncogenic RAS and the p53 tumor suppressor. PLoS Biol. 6, 2853-2868.
7. Crane JD, Abadi A, Hettinga BP, Ogborn DI, Macneil LG, Steinberg GR, Tarnopolsky MA (2013a) Elevated mitochondrial oxidative stress impairs metabolic adaptations to exercise in skeletal muscle. PLoS One 8, e81879.
8. Crane JD, Macneil LG, Tarnopolsky MA (2013b) Long-term aerobic exercise is associated with greater muscle strength throughout the life span. J. Gerontol. A Biol. Sci. Med. Sci. 68, 631-638.
9. Dai X, Sayama K, Shirakata Y, Hanakawa Y, Yamasaki K, Tokumaru S, Yang L, Wang X, Hirakawa S, Tohyama M, Yamauchi T, Takashi K, Kagechika H, Hashimoto K (2007) STAT5a/PPARgamma pathway regulates involucrin expression in keratinocyte differentiation. J. Invest. Dermatol. 127, 1728-1735.
10. Dillon LM, Hida A, Garcia S, Prolla TA, Moraes CT (2012) Long-term bezafibrate treatment improves skin and spleen phenotypes of the mtDNA mutator mouse. PLoS One 7, e44335.
11. Fehniger TA, Suzuki K, Ponnappan A, VanDeusen JB, Cooper MA, Florea SM, Freud AG, Robinson ML, Durbin J, Caligiuri MA (2001) Fatal leukemia in interleukin 15 transgenic mice follows early expansions in natural killer and memory phenotype CD8 + T cells. J. Exp. Med. 193, 219-231.
12. Fisher GJ, Kang S, Varani J, Bata-Csorgo Z, Wan Y, Datta S, Voorhees JJ (2002) Mechanisms of photoaging and chronological skin aging. Arch. Dermatol. 138, 1462-1470.
13. Giri JG, Ahdieh M, Eisenman J, Shanebeck K, Grabstein K, Kumaki S, Namen A, Park LS, Cosman D, Anderson D (1994) Utilization of the beta and gamma chains of the IL-2 receptor by the novel cytokine IL-15. EMBO J. 13, 2822-2830.
14. Green DR, Galluzzi L, Kroemer G (2011) Mitochondria and the autophagyinflammation- cell death axis in organismal aging. Science 333, 1109-1112.
15. Ham SA, Kim HJ, Kim HJ, Kang ES, Eun SY, Kim GH, Park MH, Woo IS, Kim HJ, Chang KC, Lee JH, Seo HG (2010) PPARdelta promotes wound healing by upregulating TGF-beta1-dependent or -independent expression of extracellular matrix proteins. J. Cell Mol. Med. 14, 1747-1759.
16. Harman D (1972) The biologic clock: the mitochondria? J. Am. Geriatr. Soc. 20, 145-147.
17. Isobe K, Ito S, Hosaka H, Iwamura Y, Kondo H, Kagawa Y, Hayashi JI (1998) Nuclear- recessive mutations of factors involved in mitochondrial translation are responsible for age-related respiration deficiency of human skin fibroblasts. J. Biol. Chem. 273, 4601-4606.
18. Katsimpardi L, Litterman NK, Schein PA, Miller CM, Loffredo FS, Wojtkiewicz GR, Chen JW, Lee RT, Wagers AJ, Rubin LL (2014) Vascular and neurogenic rejuvenation of the aging mouse brain by young systemic factors. Science 344:6184, 630-634.
19. Kim M-S, Song HJ, Lee SH, Lee CK (2014) Comparative study of various growth factors and cytokines on type I collagen and hyaluronan production in human dermal fibroblasts. J. Cosmet. Dermatol. 13, 44-51.
20. Lanza IR, Short DK, Short KR, Raghavakaimal S, Basu R, Joyner MJ, McConnell JP, Nair KS (2008) Endurance exercise as a countermeasure for aging. Diabetes 57, 2933-2942.
21. Lu CY, Lee HC, Fahn HJ, Wei YH (1999) Oxidative damage elicited by imbalance of free radical scavenging enzymes is associated with large-scale mtDNA deletions in aging human skin. Mutat. Res. 423, 11-21.
22. Munger W, DeJoy SQ, Jeyaseelan R, Torley LW, Grabstein KH, Eisenmann J, Paxton R, Cox T, Wick MM, Kerwar SS (1995) Studies evaluating the antitumor activity and toxicity of interleukin-15, a new T cell growth factor: comparison with interleukin-2. Cell. Immunol. 165, 289-293.
23. Nielsen AR, Mounier R, Plomgaard P, Mortensen OH, Penkowa M, Speerschneider T, Pilegaard H, Pedersen BK (2007) Expression of interleukin-15 in human skeletal muscle effect of exercise and muscle fibre type composition. J. Physiol. 584, 305-312.
24. Ogborn DI, Smith KJ, Crane JD, Safdar A, Hettinga BP, Tupler R, Tarnopolsky MA (2012) Effects of creatine and exercise on skeletal muscle of FRG1-transgenic mice. Can. J. Neurol. Sci. 39, 225-231.
25. O’Neill HM, Maarbjerg SJ, Crane JD, Jeppesen J, Jørgensen SB, Schertzer JD, Shyroka O, Kiens B, van Denderen BJ, Tarnopolsky MA, Kemp BE, Richter EA, Steinberg GR (2011) AMP-activated protein kinase (AMPK) {beta}1{beta}2 muscle null mice reveal an essential role for AMPK in maintaining mitochondrial content and glucose uptake during exercise. Proc. Natl Acad. Sci. USA 108, 16092-16097.
26. O’Neill HM, Holloway GP, Steinberg GR (2013) AMPK regulation of fatty acid metabolism and mitochondrial biogenesis: implications for obesity. Mol. Cell. Endocrinol. 366, 135-151.
27. Pedersen BK, Febbraio MA (2012) Muscles, exercise and obesity: skeletal muscle as a secretory organ. Nat. Rev. Endocrinol. 8, 457-465.
28. Quinn LS, Anderson BG, Strait-Bodey L, Stroud AM, Argilés JM (2009) Oversecretion of interleukin-15 from skeletal muscle reduces adiposity. Am. J. Physiol. Endocrinol. Metab. 296, E191-E202.
29. Ruas JL, White JP, Rao RR, Kleiner S, Brannan KT, Harrison BC, Greene NP, Wu J, Estall JL, Irving BA, Lanza IR, Rasbach KA, Okutsu M, Nair KS, Yan Z, Leinwand LA, Spiegelman BM (2012) A PGC-1a isoform induced by resistance training regulates skeletal muscle hypertrophy. Cell 151, 1319-1331.
30. Safdar A, Bourgeois JM, Ogborn DI, Little JP, Hettinga BP, Akhtar M, Thompson JE, Melov S, Mocellin NJ, Kujoth GC, Prolla TA, Tarnopolsky MA (2011) Endurance exercise rescues progeroid aging and induces systemic mitochondrial rejuvenation in mtDNA mutator mice. Proc. Natl Acad. Sci. USA 108, 4135-4140.
31. Sahin E, Depinho RA (2010) Linking functional decline of telomeres, mitochondria and stem cells during ageing. Nature 464, 520-528.
32. Schroeder P, Gremmel T, Berneburg M, Krutmann J (2008) Partial depletion of mitochondrial DNA from human skin fibroblasts induces a gene expression profile reminiscent of photoaged skin. J. Invest. Dermatol. 128, 2297-2303.
33. Seals DR, Walker AE, Pierce GL, Lesniewski LA (2009) Habitual exercise and vascular ageing. J. Physiol. 587, 5541-5549.
34. Sinha M, Jang YC, Oh J, Khong D, Wu EY, Manohar R, Miller C, Regalado SG, Loffredo FS, Pancoast JR, Hirshman MF, Lebowitz J, Shadrach JL, Cerletti M, Kim M, Serwold T, Goodyear LJ, Rosner B, Lee RT, Wagers AJ (2014) Restoring systemic GDF11 levels reverses age-related dysfunction in mouse skeletal muscle. Science 344, 6184, 649-52.
35. Steinberg GR, Jørgensen SB (2007) The AMP-activated protein kinase: role in regulation of skeletal muscle metabolism and insulin sensitivity. Mini Rev. Med. Chem. 7, 519-526.
36. Suzuki A, McCall S, Choi SS, Sicklick JK, Huang J, Qi Y, Zdanowicz M, Camp T, Li Y, Diehl AM (2006) Interleukin-15 increases hepatic regenerative activity. J. Hepatol. 45, 410-418.
37. Tamura Y, Watanabe K, Kantani T, Hayashi J, Ishida N, Kaneki M (2011) Upregulation of circulating IL-15 by treadmill running in healthy individuals: is IL-15 an endocrine mediator of the beneficial effects of endurance exercise? Endocr. J. 58, 211-215.
38. Treiber N, Maity P, Singh K, Kohn M, Keist AF, Ferchiu F, Sante L, Frese S, Bloch W, Kreppel F, Kochanek S, Sindrilaru A, Iben S, Hogel J, Ohnmacht M, Claes LE, Ignatius A, Chung JH, Lee MJ, Kamenisch Y, Berneburg M, Nikolaus T, Braunstein K, Sperfeld A, Ludolph AC, Briviba K, Wlaschek M, Florin L, Angel P, Scharffetter-Kochanek K (2011) Accelerated aging phenotype in mice with conditional deficiency for mitochondrial superoxide dismutase in the connective tissue. Aging Cell 10, 239-254.
39. Trifunovic A, Wredenberg A, Falkenberg M, Spelbrink JN, Rovio AT, Bruder CE, Bohlooly-Y M, Gidlof S, Oldfors A, Wibom R, Tornell J, Jacobs HT, Larsson N (2004) Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature 429, 417-423.
40. Velarde MC, Flynn JM, Day NU, Melov S, Campisi J (2012) Mitochondrial oxidative stress caused by Sod2 deficiency promotes cellular senescence and aging phenotypes in the skin. Aging (Albany NY) 4, 3-12.
41. Villeda SA, Luo J, Mosher KI, Zou B, Britschgi M, Bieri G, Stan TM, Fainberg N, Ding Z, Eggel A, Lucin KM, Czirr E, Park J, Couillard-Despres S, Aigner L, Li G, Peskind ER, Kaye JA, Quinn JF, Galasko DR, Xie XS, Rando TA, Wyss-Coray T (2011) The ageing systemic milieu negatively regulates neurogenesis and cognitive function. Nature 477, 90-94.
42. Villegas J, McPhaul M (2005). Establishment and culture of human skin fibroblasts. In: Current Protocols in Molecular Biology (Frederick M. Ausubel et al., ed.). Hoboken, NJ, USA: John Wiley & Sons, Inc, pp. 71:28.3:28.3.1-28.3.9.
43. Waldmann TA (2006) The biology of interleukin-2 and interleukin-15: implications for cancer therapy and vaccine design. Nat. Rev. Immunol. 6, 595-601.
44. Waldmann TA, Lugli E, Roederer M, Perera LP, Smedley JV, Macallister RP, Godlman CK, Bryant BR, Decker JM, Fleisher TA, Lane HC, Sneller MC, Kurlander RJ, Kleiner DE, Pletcher JM, Figg WD, Yovandich JL, Creekmore SP (2011) Safety (toxicity), pharmacokinetics, immunogenicity, and impact on elements of the normal immune system of recombinant human IL-15 in rhesus macaques. Blood 117, 4787-4795.
45. Zouboulis CC, Makrantonaki E (2012) Hormonal therapy of intrinsic aging. Rejuvenation Res. 15, 302-312.