Effect of Treadmill Exercise on Interleukin-15 Expression and Glucose Tolerance in Zucker Diabetic Fatty Rats

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1 Originl Article Obesity nd Metbolic Syndrome pissn eissn DIABETES & METABOLISM JOURNAL Effect of Tredmill Exercise on Interleukin-15 Expression nd Glucose Tolernce in Zucker Dibetic Ftty Rts Hee-Je Kim 1, Je Young Prk 2, Seung Lyul Oh 1, Yong-An Kim 1, Byunghun So 1, Je Kyung Seong 3, Wook Song 1,4 1 Helth nd Exercise Science Lbortory, The Institute of Sports Science, Seoul Ntionl University, Seoul, 2 Deprtment of Sport, Kyungil University College of Arts nd Sports, Gyeongsn, 3 Deprtment of Antomy nd Cell Biology, Reserch Institute for Veterinry Science, Seoul Ntionl University College of Veterinry Medicine, Seoul, 4 Institute on Aging, Seoul Ntionl University College of Medicine, Seoul, Kore Bckground: Interleukin-15 (IL-15), well-known myokine, is highly expressed in skeletl muscle nd is involved in muscle-ft crosstlk. Recently, role of skeletl muscle-derived IL-15 in the improvement of glucose homeostsis nd insulin sensitivity hs been proposed. However, little is known regrding the influence of endurnce trining on IL-15 expression in type 2 dibetic skeletl muscles. We investigted the effect of endurnce exercise trining on glucose tolernce nd IL-15 expression in skeletl muscles using type 2 dibetic niml models. Methods: Mle Zucker dibetic ftty (ZDF) nd ZDF len control (ZLC) rts were rndomly divided into three groups: sedentry ZLC, sedentry ZDF (ZDF-Con), nd exercised ZDF (ZDF-Ex). The ZDF-Ex rts were forced to run motor-driven tredmill for 6 minutes once dy 5 times per week for 12 weeks. Intrperitonel glucose tolernce test (IPGTT) ws performed fter 12 weeks. Expression of IL-15 ws mesured using ELISA in extrcted soleus (SOL) nd gstrocnemius medil muscles. Results: After 12 weeks of tredmill trining, reduction of body weight ws observed in ZDF-Ex compred to ZDF-Con rts. Glucose tolernce using IPGTT in dibetic rts ws significntly improved in ZDF-Ex rts. Furthermore, the expression of IL-15 ws significntly incresed (P<.1) only in the SOL of ZDF-Ex rts compred to ZDF-Con. Additionlly, IL-15 expression in SOL muscles ws negtively correlted with chnge of body weight (R=-.424, P=.4). Conclusion: The present study results suggest tht 12 weeks of progressive endurnce trining significntly improved glucose tolernce with concomitnt increse of IL-15 expression in SOL muscles of type 2 dibetic rts. Keywords: Exercise; Glucose intolernce; Interleukin-15; Rts, Zucker; Tredmill INTRODUCTION Myokines, known s cytokines nd peptides, tht re produced, expressed, nd relesed by muscle fibers nd exertion of these substnces in either prcrine or endocrine fshion should be clssified [1]. Previously, reserchers hve serched for muscle contrction-induced hormonl fctor, n exercise fctor, which could medite some of the exercise-induced chnges in other orgns such s the liver nd dipose tissue [1]. Among vrious myokines, interleukin-15 (IL-15) hs been identified s n nbolic fctor, which is highly expressed in skeletl muscle [2]. Quinn et l. [3] hve proposed n importnt role of IL-15 in skeletl muscle by demonstrting tht IL- 15 cn stimulte differentited myocytes nd muscle fibers to ccumulte incresed mounts of contrctile proteins. The ction of IL-15 stimultes muscle-specific myosin hevy chin Corresponding uthor: Wook Song Helth nd Exercise Science Lbortory, The Institute of Sports Science, Seoul Ntionl University, nd Institute on Aging, Seoul Ntionl University College of Medicine, 1 Gwnk-ro, Gwnk-gu, Seoul , Kore E-mil: songw3@snu.c.kr Received: Jn. 21, 213; Accepted: Apr. 3, 213 This is n Open Access rticle distributed under the terms of the Cretive Commons Attribution Non-Commercil License ( which permits unrestricted non-commercil use, distribution, nd reproduction in ny medium, provided the originl work is properly cited. Copyright 213 Koren Dibetes Assocition

2 Effect of tredmill exercise on IL-15 ccumultion by differentited myocytes nd muscle fibers in culture, suggesting role in skeletl muscle fiber growth in vivo [4]. In ddition, overexpression of IL-15 in mouse C2C12 cells leds to cler muscle hypertrophy [5]. Recently, the functionl role of IL-15 in regulting metbolic diseses, including obesity nd dibetes, hs been emphsized. Modultion of glucose uptke in incubted skeletl muscles nd muscle cell cultures by IL-15 implies tht cytokines my ply role in the inhibition of the development of dibetes [4]. Indeed, in vivo dministrtion of IL-15 results in n elevtion of 2-deoxyglucose uptke in skeletl muscle. Additionlly, in vitro tretment of IL-15 increses GLUT4 content in muscle cell cultures [6]. These findings suggest the possibility tht IL-15 cn serve s n importnt meditor of skeletl muscle fiber growth, hypertrophy, nd glucose uptke. One study demonstrted tht high intensity resistnce trining leds to trnsient increse in serum IL-15 concentrtion [7], while nother study reported tht plsm IL-15 concentrtion is not ltered by hevy resistnce trining [8]. Endurnce exercise did not increse IL-15 mrna content in skeletl muscle or circulting IL-15 concentrtion from 1 up to 6 hours fter exercise [9-12]. However, recent study implied tht endurnce exercise increses circulting IL-15 concentrtion 1 minutes fter the exercise [13]. These findings suggest tht exercise-induced IL-15 my medite the systemic s well s locl beneficil effects of endurnce exercise, including insulin-sensitizing, ntidipogenic effects, nd nbolic ctions in skeletl muscle [13]. Skeletl muscle is the principle site of glucose uptke under insulin-stimulted conditions nd strongly influences glucose intolernce [14]. Impired glucose trnsport in skeletl muscles leds to impired whole-body glucose uptke, nd fcilittes the development of type 2 dibetes. Subjects with glucose intolernce hve n incresed risk of type 2 dibetes, therefore improvement of glucose tolernce is considered importnt for the prevention of dibetes [15,16]. Collectively, the results of previous studies clerly indicte tht expression of IL-15 in skeletl muscles my regulte glucose metbolism in vrious metbolic diseses including dibetes. Although exercise is considered n importnt preventive mesure for ptients with dibetes, dt regrding the influence of endurnce trining on IL-15 expression in type 2 dibetic skeletl muscles by fiber types re lcking. Therefore, in the present study, we exmined the effect of endurnce exercise trining on glucose tolernce nd IL-15 expression in skeletl muscles using type 2 dibetic rts. METHODS Animls Mle nd femle Zucker dibetic ftty (ZDF, f/+) rts were purchsed from Genetic Models (Indinpolis, ME, USA) nd llowed to mte. They were housed in conventionl cges under dequte temperture (23 C) nd humidity (6%), control with 12-hour light/12-hour drk cycle, nd free ccess to food nd wter. Purin 58 rodent diet (7.5% ft) ws provided s recommended by Genetic Models Co. (Purin, St. Louis, MO, USA). The f gene genotype ws determined using the strtegy described in our previous study [17]. Twenty-four mle len (ZDF len control, ZLC, +/+) nd dibetic (ZDF, f/f) Zucker rts (8-week-old) were seprted into three groups, len control (sedentry ZLC, ZLC-Con, n=8), dibetic control (sedentry ZDF, ZDF-Con, n=8), nd dibetic exercise-trined (exercised ZDF, ZDF-Ex, n=8). All nimls in the trining group hd tredmill dpttion period of 1 week. At 8 weeks (pre-exercise) nd 2 weeks (postexercise) of ge, body weight (mettle instrument AG CH- 866; Mettler Toledo, Greifensee, Switzerlnd) nd fsting plsm glucose level (Roche Dignostics Ltd., Mnnheim, Germny) were mesured in ll nimls. The hndling nd cring procedures for the nimls dhered to the guidelines in complince with the current interntionl lw nd policies (Ntionl Institutes of Helth [NIH] Guide for the Cre nd Use of Lbortory Animls, NIH Publiction No , 1985, revised 1996). All experiments were conducted to minimize the number of nimls used nd the suffering cused by the procedures in the present study. Progressive endurnce exercise trining The rts in the ZDF-Ex were forced to run motor-driven tredmill for 6 minutes once dy 5 times per week for 12 weeks. The ZDF-Ex rts were cclimted to the tredmill exercise before trining. The exercise intensity (running speed) ws set t the speed of 15 to 2 m/min t their lctte threshold [18]. The initil tredmill speed ws set to 15 nd 2 m/min ws dded every 2 weeks to simulte the intensity nd effect of exercise trining. The mximl tredmill speed ws limited to 2 m/min in the lst 2 weeks. Tissue collection Skeletl muscle tissue collection ws performed 2 dys fter the lst session of the exercise trining progrm. Rts were nesthe- 359

3 Kim HJ, et l. tized by Zoletil 5 (intrperitonel injection, 1 mg/kg; Vibc Lbortories, Crros, Frnce) nd scrificed. The tissues were collected from the soleus (SOL) nd the gstrocnemius medil (GM) muscles. The smples were quickly weighed, frozen with liquid nitrogen, nd then stored t -8 o C until used. Ech tissue ws homogenized in rdio immunoprecipittion ssy buffer. The homogenized tissues were then centrifuged t 14, rpm for 2 minutes t 4 o C, nd the totl protein concentrtion of the superntnt ws determined using the Brdford ssy. IL-15 protein nlysis Protein extrcts from the skeletl muscle were prepred by centrifugtion of the tissue homogentes ccording to the mnufcturer s specifictions (Rt IL-15 ELISA Kit; Cusbio Biotec Co., Ltd., Newrk, DE, USA). Detection rnge ws 1.56 to 1 pg/ml for ech ssy. All smples were ssyed in duplicte to gurntee the precision of the results, nd ll smples were run within the rnge of the stndrd curve. The results were expressed s concentrtion of IL-15 (pg/ml) red from stndrd curves. Intrperitonel glucose tolernce test Glucose tolernce ws ssessed using the intrperitonel glucose tolernce test (IPGTT) in rts during the lst week of the trining session. IPGTT ws performed by injecting glucose (2 g/kg in 2% solution) intrperitonelly in overnight-fsted rts. Blood smples were obtined by cutting the tile tip before nd, 15, 3, 6, 9, nd 12 minutes fter glucose dministrtion. Blood glucose concentrtion ws mesured using n Accu- Chek glucose nlyzer (Roche Dignostics Ltd., Mnnheim, Germny). Sttisticl nlysis Sttisticl nlysis ws performed using the Origin 8. nd SPSS version 18. softwre pckge (IBM Co., Armonk, NY, USA). Dt were nlyzed using two smples t-test to exmine the body weight, fsting glucose levels, IL-15 levels, nd re under the curve (AUC) of IPGTT. Dt were presented s men±stndrd error of men with significnce set t P<.5. Associtions of IL-15 expression in SOL with body weight nd fsting blood glucose were clculted with Person correltion coefficient. RESULTS As shown in Fig. 1A, the body weight of ZDF-Con rts ws mrkedly incresed (P<.5) compred to ZLC-Con rts t the end of exercise trining. After the 12-week tredmill exercise progrm, body weight ws lower (P<.5) in the ZDF-Ex group compred to ZDF-Con group. However, there ws no significnt chnge in body weight following the tredmill exercise in ZLC rts (dt not shown). The fsting blood glucose concentrtion in ZDF-Con rts (297.2±18.5 mg/dl) ws significntly higher (P<.5) thn in ZLC-Con rts (78.4±5.4 mg/dl). After the lst exercise session, the fsting blood glucose level ws lower in ZDF-Ex (178.2±12.9 mg/dl) thn in ZDF-Con rts (Fig. 1B). Body weight (g) Pretrining (bseline) Posttrining b Fsting blood glucose (mg/dl) Pretrining (bseline) Posttrining b ZLC-Con ZDF-Con ZDF-Ex A ZLC-Con ZDF-Con ZDF-Ex B Fig. 1. Effect of 12 weeks of (A) tredmill exercise on body weight nd (B) fsting blood glucose concentrtion. Vlues re men±stndrd error of men for n=8 in ech group. ZLC-Con, sedentry Zucker dibetic ftty len control; ZDF-Con, sedentry Zucker dibetic ftty; ZDF-Ex, exercised Zucker dibetic ftty. P<.5 compred with ZLC-Con group, b P<.5 compred with ZDF-Con group. 36

4 Effect of tredmill exercise on IL-15 Plsm glucose (ml/dl) ZDF-Con ZDF-Ex ZLC-Con AUC (mg/dlxmin) 5, 4, 3, 2, 1, Pretrining (bseline) Posttrining b Time (min) A ZLC-Con ZDF-Con ZDF-Ex B Fig. 2. Effect of 12 weeks of tredmill exercise on glucose tolernce in dibetic rts. (A) Blood glucose concentrtion ws mesured t vrious time points fter dextrose (2 g/kg) tretment. (B) Are under the curve (AUC) of intrperitonel glucose tolernce test ws clculted for quntified comprison. Vlues re men±stndrd error of men for n=8 in ech group. ZDF-Con, sedentry Zucker dibetic ftty; ZDF-Ex, exercised Zucker dibetic ftty; ZLC-Con, sedentry Zucker dibetic ftty len control. P<.5 compred with ZLC-Con group, b P<.5 compred with ZDF-Con group. IPGTT ws performed on every weekend to verify the improvement of glucose tolernce. The representtive result ws found t the lst mesurement, 2 dys fter the lst session of the exercise progrm. The significnt increse of blood glucose concentrtion ws found within 3 minutes fter dextrose injection (2 g/kg, intrperitonel) in ll experimentl groups (Fig. 2A). In ZLC-Con rts, the incresed blood glucose due to injection of dextrose ws grdully eliminted within 2 hours, wheres, the regultory cpcity of blood glucose ws significntly ttenuted in ZDF-Con rts (Fig. 2A). In prllel, the AUC vlues of blood glucose levels during IPGTT in ZDF-Con rts were incresed to pproximtely 2.8-fold compred to ZLC-Con rts (Fig. 2B). However, the blood glucose levels in ZDF-Ex rts were significntly reduced during IPGTT, nd the totl AUC for the glucose response ws mrkedly lower compred to ZDF-Con rts (Fig. 2B). The expressions of IL-15 in SOL nd GM muscles were mesured t the end of the 12-week endurnce trining. In SOL muscle, there ws no significnt chnge of IL-15 proteins between ZLC-Con nd ZDF-Con rts. In ddition, the expression of IL-15 in SOL of ZDF-Ex rts ws higher compred to ZDF- Con rts (P<.5) (Fig. 3). However, no significnt effects of dibetes nd endurnce trining were detected in IL-15 expression in GM muscle. Additionlly, we found negtive correltion between expression of IL-15 in SOL muscle nd body weight (R=-.424, P=.4) (Fig. 4A), wheres, sttisticl correltion between IL-15 expression in SOL muscle nd concentrtion of fsting blood glucose ws not observed (R=-.328, IL-15 protein (pg/g pro.) P=.118) (Fig. 4B). DISCUSSION ZLC-Con ZDF-Con ZDF-Ex SOL GM Fig. 3. Effect of 12 weeks of tredmill exercise on expression of interleukin-15 (IL-15) in soleus (SOL) nd gstrocnemius medil (GM) muscles. Vlues re men±stndrd error of men for n=8 in ech group. ZLC-Con, sedentry Zucker dibetic ftty len control; ZDF-Con, sedentry Zucker dibetic ftty; ZDF-Ex, exercised Zucker dibetic ftty. P<.5 compred with ZDF-Con group. In the present study, we investigted whether 12 weeks of physicl exercise trining improves glucose tolernce nd expression of IL-15 in dibetic skeletl muscles. Our dt demonstrted tht body weight nd fsting blood glucose levels were positive- 361

5 Kim HJ, et l. 4 R=-.424 P=.4 4 R=-.328 P=.118 IL-15 in SOL (pg/g pro.) IL-15 in SOL (pg/g pro.) Body weight (g) A Fsting blood glucose (mg/dl) B Fig. 4. Assocition of interleukin-15 (IL-15) expression in soleus (SOL) with body weight nd fsting blood glucose levels. Person correltion coefficients of IL-15 expression in SOL with (A) body weight nd (B) concentrtion of fsting blood glucose re shown. Person correltion coefficients nd P vlues re shown in ech grph. ly chnged in trined dibetic rts. Additionlly, the glucose tolernce significntly improved following 12 weeks of tredmill exercise trining. The expression of IL-15 in skeletl muscles, especilly in the SOL muscle, significntly incresed fter tredmill exercise in dibetic nimls. To our knowledge, this is the first study to investigte the effect of exercise trining on the expression of IL-15 in skeletl muscles with concomitnt improvement of glucose tolernce in trnsgenic dibetic nimls. Our result demonstrted body weight reduction in ZDF- Ex rts. Bsed on our observtion, we could not find ny significnt differences in food nd wter intke between control nd exercise groups (dt not shown). Additionlly, there ws no visible symptom of under nutrition during the entire trining progrm. Although the chnge of body composition ws not mesured in our study, regulr physicl exercise is known to decrese body ft mss which leds to weight reduction. The results showing body weight reduction nd lower fsting blood glucose levels re typicl results obtined from exercise in type 2 dibetic models, indicting the trining progrm ws dequtely designed nd implemented. In previous IL-15 metbolism studies, IL-15 reportedly stimulted glucose uptke nd lipid oxidtion in muscle tissue [6,19]. Furthermore, systemic injection of IL-15 reduced ft deposition in norml nd obese rodents, which ws ssocited with inhibition of lipogenesis in the liver nd dipose tissues [2,21]. Additionlly, circulting IL-15 protein regulted body composition including dipose tissue deposition [22]. A recent study reported tht IL-15 improves glucose homeostsis nd insulin sensitivity in obese mice [23]. In the present study, we found the increse of IL-15 expression in SOL muscle with concomitnt improvement of glucose tolernce in dibetic rts fter trining. Systemic effect of exercise-induced IL-15 on improvement of glucose metbolism is unknown, nd IL-15 my be potent meditor to elucidte the beneficil effect of exercise on metbolic diseses such s obesity or type 2 dibetes. Previous studies showed inconsistent results regrding the effects of exercise on IL-15 expression in skeletl muscle nd plsm [24]. Niemn et l. [12] reported no chnges in muscle IL-15 mrna following 2 hours of intensive strength trining. Similrly, Ostrowski et l. [11] observed no chnges in plsm IL-15 following 2 hours of tredmill running. In contrst, plsm IL-15 levels incresed following resistnce exercise [8,25] nd tredmill running in helthy young men [13]. To dte, however, most of the previous reserch subjects were norml individuls, nd ltertion of IL-15 expression in dibetic skeletl muscle ws not found. Only one study reported tht tredmill exercise promotes IL-15 expression in skeletl muscle of high-ft induced obese rts [26]. In our results, IL-15 expression ws incresed in skeletl muscle following exercise trining especilly in the SOL muscle when using trnsgenic dibetic model. Hving n importnt role in the determintion of crbohydrte nd lipid metbolism, skeletl muscle is ffected by insulin resistnce in dibetic conditions. In ptients nd nimls with type 2 dibetes, skeletl muscles showed lower oxidtive enzyme ctivity thn norml subjects [27-29]. Additionlly, the ltertion of muscle fiber types nd fiber specific oxidtive enzyme ctivities in skeletl muscles of ptients with type 2 di- 362

6 Effect of tredmill exercise on IL-15 betes hve been reported [3]. In vrious type 2 dibetic nimls including Otsuk Long Evns Tokushim Ftty, Goto- Kkizki, nd ZDF rts, skeletl muscle hd lower percentge of type IIA fibers compred to ge-mtched nondibetic rts [31,32]. Additionlly, Ysud et l. [33] reported the SOL muscle in ZDF rts hs lower percentge of type IIA fibers thn len controls. Due to different metbolic properties of the muscle fiber clssifiction, type I (slow-twitch, oxidtive) nd type II (fst-twitch, glycolytic) skeletl muscles re differently ffected by dibetes. In the present study, IL-15 expression ws mrkedly incresed in SOL (mostly type I fiber) but not in GM (type II dominnt) muscles. Bsed on our results, in dibetic skeletl muscle, response of type I muscle fibers my be more sensitive to IL-15 expression thn type II muscle fibers following exercise trining. Although this study investigtes new perspective of exercise-induced improvement in type 2 dibetes, severl limittions in the experimentl design nd vribles remin. IL-15 expression should hve been mesured in both skeletl muscle nd circulting plsm following exercise trining. However, not enough plsm ws obtined to nlyze insulin nd plsm IL-15 levels in this experiment. In conclusion, our dt showed tht 12 weeks of tredmill exercise induced n increse of IL-15 expression in SOL muscle with concomitnt improvement of glucose tolernce. Bsed on the current knowledge, including our own findings, incresed IL-15 following endurnce exercise might be potent meditor of glucose regultion in type 2 dibetes. Further studies will be required to investigte the mechnisms by which different expressions of IL-15 re regulted by different muscle fiber types under dibetic conditions, nd how the incresed expression of IL-15 exerts preventive effects including improvement of glucose tolernce in dibetic models. CONFLICTS OF INTEREST No potentil conflict of interest relevnt to this rticle ws reported. ACKNOWLEDGMENTS This reserch ws supported by Bsic Science Reserch Progrm through the Ntionl Reserch Foundtion of Kore (NRF) funded by Ministry of Eduction, Science nd Technology ( ), MEST , nd lso supported by the grnts from KGEMC ( ). REFERENCES 1. Pedersen BK, Akerstrom TC, Nielsen AR, Fischer CP. Role of myokines in exercise nd metbolism. J Appl Physiol 27; 13: Grbstein KH, Eisenmn J, Shnebeck K, Ruch C, Srinivsn S, Fung V, Beers C, Richrdson J, Schoenborn MA, Ahdieh M, Johnson L, Alderson MR, Wtson JD, Anderson DM, Giri JG. Cloning of T cell growth fctor tht intercts with the bet chin of the interleukin-2 receptor. Science 1994;264: Quinn LS, Hugk KL, Grbstein KH. Interleukin-15: novel nbolic cytokine for skeletl muscle. Endocrinology 1995; 136: Argiles JM, Lopez-Sorino FJ, Busquets S. Therpeutic potentil of interleukin-15: myokine involved in muscle wsting nd diposity. Drug Discov Tody 29;14: Quinn LS, Anderson BG, Drivdhl RH, Alvrez B, Argiles JM. Overexpression of interleukin-15 induces skeletl muscle hypertrophy in vitro: implictions for tretment of muscle wsting disorders. Exp Cell Res 22;28: Busquets S, Figuers M, Almendro V, Lopez-Sorino FJ, Argiles JM. Interleukin-15 increses glucose uptke in skeletl muscle. An ntidibetogenic effect of the cytokine. Biochim Biophys Act 26;176: Argiles JM, Busquets S, Felipe A, Lopez-Sorino FJ. Muscle wsting in cncer nd geing: cchexi versus srcopeni. Adv Gerontol 26;18: Riechmn SE, Blsekrn G, Roth SM, Ferrell RE. Assocition of interleukin-15 protein nd interleukin-15 receptor genetic vrition with resistnce exercise trining responses. J Appl Physiol 24;97: Nielsen AR, Mounier R, Plomgrd P, Mortensen OH, Penkow M, Speerschneider T, Pilegrd H, Pedersen BK. Expression of interleukin-15 in humn skeletl muscle effect of exercise nd muscle fibre type composition. J Physiol 27;584(Pt 1): Chn MH, Crey AL, Wtt MJ, Febbrio MA. Cytokine gene expression in humn skeletl muscle during concentric contrction: evidence tht IL-8, like IL-6, is influenced by glycogen vilbility. Am J Physiol Regul Integr Comp Physiol 24; 287:R Ostrowski K, Hermnn C, Bngsh A, Schjerling P, Nielsen JN, Pedersen BK. A trum-like elevtion of plsm cytokines in humns in response to tredmill running. J Physiol 1998; 363

7 Kim HJ, et l. 513(Pt 3): Niemn DC, Dvis JM, Brown VA, Henson DA, Dumke CL, Utter AC, Vinci DM, Downs MF, Smith JC, Crson J, Brown A, McAnulty SR, McAnulty LS. Influence of crbohydrte ingestion on immune chnges fter 2 h of intensive resistnce trining. J Appl Physiol 24;96: Tmur Y, Wtnbe K, Kntni T, Hyshi J, Ishid N, Kneki M. Upregultion of circulting IL-15 by tredmill running in helthy individuls: is IL-15 n endocrine meditor of the beneficil effects of endurnce exercise? Endocr J 211;58: DeFronzo RA, Bondonn RC, Ferrnnini E. Pthogenesis of NIDDM. A blnced overview. Dibetes Cre 1992;15: Bergmn RN, Finegood DT, Ader M. Assessment of insulin sensitivity in vivo. Endocr Rev 1985;6: Tuomilehto J, Lindstrom J, Eriksson JG, Vlle TT, Hmlinen H, Ilnne-Prikk P, Keinnen-Kiuknniemi S, Lkso M, Louhernt A, Rsts M, Slminen V, Uusitup M; Finnish Dibetes Prevention Study Group. Prevention of type 2 dibetes mellitus by chnges in lifestyle mong subjects with impired glucose tolernce. N Engl J Med 21;344: Hwng IK, Yi SS, Kim YN, Kim IY, Lee IS, Yoon YS, Seong JK. Reduced hippocmpl cell differentition in the subgrnulr zone of the dentte gyrus in rt model of type II dibetes. Neurochem Res 28;33: Chng H, Prk JY, Suk MH, Lee HJ, Kng HJ, Choi KM, Song W. Comprison of lctte threshold, glucose, nd insulin levels between OLETF nd LETO rts fter ll-out exercise. J Sports Sci Med 29;8: Almendro V, Busquets S, Ametller E, Crbo N, Figuers M, Fuster G, Argiles JM, Lopez-Sorino FJ. Effects of interleukin-15 on lipid oxidtion: disposl of n orl [(14)C]-triolein lod. Biochim Biophys Act 26;1761: Alvrez B, Crbo N, Lopez-Sorino J, Drivdhl RH, Busquets S, Lopez-Sorino FJ, Argiles JM, Quinn LS. Effects of interleukin-15 (IL-15) on dipose tissue mss in rodent obesity models: evidence for direct IL-15 ction on dipose tissue. Biochim Biophys Act 22;157: Crbo N, Lopez-Sorino J, Costelli P, Alvrez B, Busquets S, Bccino FM, Quinn LS, Lopez-Sorino FJ, Argiles JM. Interleukin-15 medites reciprocl regultion of dipose nd muscle mss: potentil role in body weight control. Biochim Biophys Act 21;1526: Quinn LS, Anderson BG, Strit-Bodey L, Stroud AM, Argiles JM. Oversecretion of interleukin-15 from skeletl muscle reduces diposity. Am J Physiol Endocrinol Metb 29;296: E Brr NG, Chew MV, Hollowy AC, Ashkr AA. Interleukin-15 tretment improves glucose homeostsis nd insulin sensitivity in obese mice. Dibetes Obes Metb 212;14: Quinn LS, Anderson BG. Interleukin-15, IL-15 receptor-lph, nd obesity: Concordnce of Lbortory Animl nd Humn Genetic Studies. J Obes 211;211: Lmbert CP, Flynn MG, Sullivn DH, Evns WJ. Effects of megestrol cette on circulting interleukin-15 nd interleukin-18 concentrtions in helthy elderly men. J Gerontol A Biol Sci Med Sci 24;59: Yng H, Chng J, Chen W, Zho L, Qu B, Tng C, Qi Y, Zhng J. Tredmill exercise promotes interleukin 15 expression in skeletl muscle nd interleukin 15 receptor lph expression in dipose tissue of high-ft diet rts. Endocrine 213;43: Mrin P, Andersson B, Krotkiewski M, Bjorntorp P. Muscle fiber composition nd cpillry density in women nd men with NIDDM. Dibetes Cre 1994;17: Hickey MS, Crey JO, Azevedo JL, Houmrd JA, Pories WJ, Isrel RG, Dohm GL. Skeletl muscle fiber composition is relted to diposity nd in vitro glucose trnsport rte in humns. Am J Physiol 1995;268(3 Pt 1):E Nyholm B, Qu Z, Kl A, Pedersen SB, Grvholt CH, Andersen JL, Sltin B, Schmitz O. Evidence of n incresed number of type IIb muscle fibers in insulin-resistnt first-degree reltives of ptients with NIDDM. Dibetes 1997;46: Oberbch A, Bossenz Y, Lehmnn S, Niebuer J, Adms V, Pschke R, Schon MR, Bluher M, Punkt K. Altered fiber distribution nd fiber-specific glycolytic nd oxidtive enzyme ctivity in skeletl muscle of ptients with type 2 dibetes. Dibetes Cre 26;29: Ysud K, Adchi T, Kikuchi N, Tsujimoto G, Aoki N, Tsud K, Ishihr A. Effects of running exercise on fibre-type distribution of soleus nd plntris muscles in dibetic Otsuk Long-Evns Tokushim ftty rts. Dibetes Obes Metb 26;8: Ysud K, Nishikw W, Iwnk N, Nkmur E, Seino Y, Tsud K, Ishihr A. Abnormlity in fibre type distribution of soleus nd plntris muscles in non-obese dibetic Goto-Kkizki rts. Clin Exp Phrmcol Physiol 22;29: Adchi T, Kikuchi N, Ysud K, Anhr R, Gu N, Mtsung T, Ymmur T, Mori C, Tsujimoto G, Tsud K, Ishihr A. Fibre type distribution nd gene expression levels of both succinte dehydrogense nd peroxisome prolifertor-ctivted receptor-gmm coctivtor-1lph of fibres in the soleus muscle of Zucker dibetic ftty rts. Exp Physiol 27;92:

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