Download PDF
Horm Metab Res 2007; 39(5): 377-383
DOI: 10.1055/s-2007-976542
Original Clinical

© Georg Thieme Verlag KG Stuttgart · New York

Plasma Adiponectin is Increased in Mice Selectively Bred for High Wheel-running Activity, but not by Wheel Running per sé

L. M. Vaanholt 1 , P. Meerlo 2 , T. Garland 3  Jr. , G. H. Visser 1 , 4 , G. van Dijk 5
  • 1University of Groningen, Department of Behavioural Biology, Haren, The Netherlands
  • 2University of Groningen, Molecular Neurobiology, Haren, The Netherlands
  • 3University of California, Riverside, Department of Biology, Riverside, USA
  • 4Centre for Isotope Research, Nijenborgh 4, Groningen, The Netherlands
  • 5University of Groningen, Neuroendocrinology, Haren, The Netherlands
Further Information

Publication History

received 4. 9. 2006

accepted 22. 12. 2006

Publication Date:
29 May 2007 (online)

Also available at
    Permissions and Reprints

Abstract

Mice selectively bred for high wheel-running activity (S) have decreased fat content compared to mice from randomly bred control (C) lines. We explored whether this difference was associated with alterations in levels of circulating hormones involved in regulation of food intake and energy balance, and whether alterations were caused by the presence of a running wheel. Plasma levels of leptin, adiponectin, and corticosterone as well as body composition were analyzed in male S mice housed with (+) and without (-) access to running wheels at ages of 10 and 18 months. These levels were compared to those found in C+ mice. Plasma corticosterone did not differ among groups. While plasma leptin levels tended to be lower in S+ mice as compared to S- or C+ mice, these differences were largely attributable to differences in fat content. Adiponectin levels were increased in S mice (+60%) compared to C mice, irrespective of wheel access. High levels of this hormone may be a trait co-segregated in mice bred for high wheel-running activity.

Key words

corticosterone - exercise - experimental evolution - leptin - metabolic rate - selective breeding

References

  • 1 Holloszy JO. Exercise and longevity: studies on rats.  J Gerontol. 1988;  43 B149-B151
    PubMedGoogle Scholar
  • 2 Navarro A, Gomez C, Lopez-Cepero JM, Boveris A. Beneficial effects of moderate exercise on mice aging: survival, behavior, oxidative stress, and mitochondrial electron transfer.  Am J Physiol Regul Integr Comp Physiol. 2004;  286 R505-R511
    PubMedGoogle Scholar
  • 3 Novelli M, Pocai A, Skalicky M, Viidik A, Bergamini E, Masiello P. Effects of life-long exercise on circulating free fatty acids and muscle triglyceride content in ageing rats.  Exp Gerontol. 2004;  39 1333-1340
    CrossrefPubMedGoogle Scholar
  • 4 Carroll S, Dudfield M. What is the relationship between exercise and metabolic abnormalities? A review of the metabolic syndrome.  Sports Med. 2004;  34 371-418
    PubMedGoogle Scholar
  • 5 Boden G. Role of fatty acids in the pathogenesis of insulin resistance and NIDDM.  Diabetes. 1997;  46 3-10
    CrossrefPubMedGoogle Scholar
  • 6 McMurray RG, Hackney AC. Interactions of metabolic hormones, adipose tissue and exercise.  Sports Med. 2005;  35 393-412
    CrossrefPubMedGoogle Scholar
  • 7 Caro JF, Sinha MK, Kolaczynski JW, Zhang PL, Considine RV. Leptin: the tale of an obesity gene.  Diabetes. 1996;  45 1455-1462
    PubMedGoogle Scholar
  • 8 Halaas JL, Gajiwala KS, Maffei M, Cohen SL, Chait BT, Rabinowitz D, Lallone RL, Burley SK, Friedman JM. Weight-reducing effects of the plasma protein encoded by the obese gene.  Science. 1995;  269 543-546
    CrossrefPubMedGoogle Scholar
  • 9 Ryan AS, Berman DM, Nicklas BJ, Sinha M, Gingerich RL, Meneilly GS, Egan JM, Elahi D. Plasma adiponectin and leptin levels, body composition, and glucose utilization in adult women with wide ranges of age and obesity.  Diabetes Care. 2003;  26 2383-2388
    CrossrefPubMedGoogle Scholar
  • 10 Park KG, Park KS, Kim MJ, Kim HS, Suh YS, Ahn JD, Park KK, Chang YC, Lee IK. Relationship between serum adiponectin and leptin concentrations and body fat distribution.  Diabetes Res Clin Pract. 2004;  63 135-142
    CrossrefPubMedGoogle Scholar
  • 11 van Dijk G, Seeley RJ, Thiele TE, Friedman MI, Ji H, Wilkinson CW, Burn P, Campfield LA, Tenenbaum R, Baskin DG, Woods SC, Schwartz MW. Metabolic, gastrointestinal, and CNS neuropeptide effects of brain leptin administration in the rat.  Am J Physiol. 1999;  276 R1425-R1433
    PubMedGoogle Scholar
  • 12 Cnop M, Havel PJ, Utzschneider KM, Carr DB, Sinha MK, Boyko EJ, Retzlaff BM, Knopp RH, Brunzell JD, Kahn SE. Relationship of adiponectin to body fat distribution, insulin sensitivity and plasma lipoproteins: evidence for independent roles of age and sex.  Diabetologia. 2003;  46 459-469
    PubMedGoogle Scholar
  • 13 Ferguson MA, White LJ, McCoy S, Kim HW, Petty T, Wilsey J. Plasma adiponectin response to acute exercise in healthy subjects.  Eur J Appl Physiol. 2004;  91 324-329
    CrossrefPubMedGoogle Scholar
  • 14 Berg AH, Combs TP, Scherer PE. ACRP30/adiponectin: an adipokine regulating glucose and lipid metabolism.  Trends Endocrinol Metab. 2002;  13 84-89
    CrossrefPubMedGoogle Scholar
  • 15 Bruce CR, Mertz VA, Heigenhauser GJ, Dyck DJ. The stimulatory effect of globular adiponectin on insulin-stimulated glucose uptake and fatty acid oxidation is impaired in skeletal muscle from obese subjects.  Diabetes. 2005;  54 3154-3160
    PubMedGoogle Scholar
  • 16 Fruebis J, Tsao TS, Javorschi S, Ebbets-Reed D, Erickson MR, Yen FT, Bihain BE, Lodish HF. Proteolytic cleavage product of 30-kDa adipocyte complement-related protein increases fatty acid oxidation in muscle and causes weight loss in mice.  Proc Natl Acad Sci USA. 2001;  98 2005-2010
    CrossrefPubMedGoogle Scholar
  • 17 Yamauchi T, Kamon J, Minokoshi Y, Ito Y, Waki H, Uchida S, Yamashita S, Noda M, Kita S, Ueki K, Eto K, Akanuma Y, Froguel P, Foufelle F, Ferre P, Carling D, Kimura S, Nagai R, Kahn BB, Kadowaki T. Adiponectin stimulates glucose utilization and fatty-acid oxidation by activating AMP-activated protein kinase.  Nat Med. 2002;  8 1288-1295
    CrossrefPubMedGoogle Scholar
  • 18 Baratta R, Amato S, Degano C, Farina MG, Patane G, Vigneri R, Frittitta L. Adiponectin relationship with lipid metabolism is independent of body fat mass: evidence from both cross-sectional and intervention studies.  J Clin Endocrinol Metab. 2004;  89 2665-2671
    CrossrefPubMedGoogle Scholar
  • 19 Schondorf T, Maiworm A, Emmison N, Forst T, Pfutzner A. Biological background and role of adiponectin as marker for insulin resistance and cardiovascular risk.  Clin Lab. 2005;  51 489-494
    PubMedGoogle Scholar
  • 20 Yamauchi T, Kamon J, Waki H, Terauchi Y, Kubota N, Hara K, Mori Y, Ide T, Murakami K, Tsuboyama-Kasaoka N, Ezaki O, Akanuma Y, Gavrilova O, Vinson C, Reitman ML, Kagechika H, Shudo K, Yoda M, Nakano Y, Tobe K, Nagai R, Kimura S, Tomita M, Froguel P, Kadowaki T. The fat-derived hormone adiponectin reverses insulin resistance associated with both lipoatrophy and obesity.  Nat Med. 2001;  7 941-946
    CrossrefPubMedGoogle Scholar
  • 21 Arita Y, Kihara S, Ouchi N, Takahashi M, Maeda K, Miyagawa JI, Hotta K, Shimomura I, Nakamura T, Miyaoka K. Paradoxical Decrease of an Adipose-Specific Protein, Adiponectin, in Obesity.  Biochem Biophys Res Commun. 1999;  257 79-83
    CrossrefPubMedGoogle Scholar
  • 22 Havel PJ. Peripheral Signals Conveying Metabolic Information to the Brain: Short-Term and Long-Term Regulation of Food Intake and Energy Homeostasis.  Exp Biol Med. 2001;  226 963-977
    PubMedGoogle Scholar
  • 23 Gil-Campos M, Canete R, Gil A. Adiponectin, the missing link in insulin resistance and obesity.  Clin Nutr. 2004;  23 963-974
    CrossrefPubMedGoogle Scholar
  • 24 Jurimae J, Purge P, Jurimae T. Adiponectin is altered after maximal exercise in highly trained male rowers.  Eur J Appl Physiol. 2005;  93 502-505
    PubMedGoogle Scholar
  • 25 Zoladz JA, Konturek SJ, Duda K, Majerczak J, Sliwowski Z, Grandys M, Bielanski W. Effect of moderate incremental exercise, performed in fed and fasted state on cardio-respiratory variables and leptin and ghrelin concentrations in young healthy men.  J Physiol Pharmacol. 2005;  56 63-85
    PubMedGoogle Scholar
  • 26 Coutinho AE, Fediuc S, Campbell JE, Riddell MC. Metabolic effects of voluntary wheel running in young and old Syrian golden hamsters.  Physiol Behav. 2006;  87 360-367
    CrossrefPubMedGoogle Scholar
  • 27 Swallow JG, Carter PA, Garland Jr T. Artificial selection for increased wheel running behavior in house mice.  Beh Gen. 1998;  28 227-237
    PubMedGoogle Scholar
  • 28 Swallow JG, Koteja P, Carter PA, Garland Jr T. Food consumption and body composition in mice selected for high wheel- running activity.  JComp Physiol [B]. 2001;  171 651-659
    PubMedGoogle Scholar
  • 29 Girard I, Garland Jr T. Plasma corticosterone response to acute and chronic voluntary exercise in female house mice.  J Appl Physiol. 2002;  92 1553-1561
    PubMedGoogle Scholar
  • 30 Malisch JL, Saltzman W, Gomes FR, Rezende EL, Jeske DR, Garland Jr T. Baseline and stress-induced plasma corticosterone concentrations of mice selectively bred for high voluntary wheel running.  Physiol Biochem Zool. 2006;  , in press
    PubMedGoogle Scholar
  • 31 Dumke CL, Rhodes JS, Garland Jr. T, Maslowski E, Swallow JG, Wetter AC, Cartee GD. Genetic selection of mice for high voluntary wheel running: effect on skeletal muscle glucose uptake.  J Appl Phys. 2001;  91 1289-1297
    PubMedGoogle Scholar
  • 32 Koteja P, Swallow JG, Carter PA, Garland Jr T. Energy cost of wheel running in house mice: implications for coadaptation of locomotion and energy budgets.  Physiol Biochem Zool. 1999;  72 238-249
    CrossrefPubMedGoogle Scholar
  • 33 Hickey MS, Israel RG, Gardiner SN, Considine RV, McCammon MR, Tyndall GL, Houmard JA, Marks RH, Caro JF. Gender differences in serum leptin levels in humans.  Biochem Mol Med. 1996;  59 1-6
    CrossrefPubMedGoogle Scholar
  • 34 Swallow JG, Koteja P, Carter PA, Garland T. Artificial selection for increased wheel-running activity in house mice results in decreased body mass at maturity.  J Exp Biol. 1999;  202 2513-2520
    PubMedGoogle Scholar
  • 35 Berg AH, Combs TP, Du X, Brownlee M, Scherer PE. The adipocyte-secreted protein Acrp30 enhances hepatic insulin action.  Nat Med. 2001;  7 947-953
    CrossrefPubMedGoogle Scholar
  • 36 Zhang Y, Lee TS, Kolb EM, Sun K, Lu X, Sladek FM, Kassab GS, Garland Jr. T, Shyy JY. AMP-activated protein kinase is involved in endothelial NO synthase activation in response to shear stress.  Arterioscler Thromb Vasc Biol. 2006;  26 1281-1287
    PubMedGoogle Scholar
  • 37 Droste SK, Gesing A, Ulbricht S, Muller MB, Linthorst AC, Reul JM. Effects of long-term voluntary exercise on the mouse hypothalamic-pituitary-adrenocortical axis.  Endocrinology. 2003;  144 3012-3023
    CrossrefPubMedGoogle Scholar
  • 38 Fallo F, Scarda A, Sonino N, Paoletta A, Boscaro M, Pagano C, Federspil G, Vettor R. Effect of glucocorticoids on adiponectin: a study in healthy subjects and in Cushing's syndrome.  Eur J Endocrinol. 2004;  150 339-344
    CrossrefPubMedGoogle Scholar
  • 39 van Dijk G, Donahey JC, Thiele TE, Scheurink AJ, Steffens AB, Wilkinson CW, Tenenbaum R, Campfield LA, Burn P, Seeley RJ, Woods SC. Central leptin stimulates corticosterone secretion at the onset of the dark phase.  Diabetes. 1997;  46 1911-1914
    PubMedGoogle Scholar

Correspondence

L. M. Vaanholt

Kerklaan 30

9751 NN Haren

The Netherlands

Phone: +31/50/363 20 51

Fax: +31/50/363 52 05

Email: l.m.vaanholt@rug.nl