Abstract
Leptin and adiponectin are proteins produced and secreted from white adipose tissue and are important regulators of energy balance and insulin sensitivity. Seasonal changes in leptin and adiponectin have not been investigated in mammalian hibernators in relationship to changes in fat cell and fat mass. We sought to determine the relationship between serum leptin and adiponectin levels with seasonal changes in lipid mass. We collected serum and tissue samples from marmots (Marmota flaviventris) in different seasons while measuring changes in fat mass, including fat-cell size. We found that leptin is positively associated with increasing fat mass and fat-cell size, while adiponectin is negatively associated with increasing lipid mass. These findings are consistent with the putative roles of these adipokines: leptin increases with fat mass and is involved in enhancing lipid oxidation while adiponectin appears to be higher in summer when hepatic insulin sensitivity should be maintained since the animals are eating. Our data suggest that during autumn/winter animals have switched from a lipogenic condition to a lipolytic state, which may include leptin resistance.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Ahima RS, Flier JS (2000) Leptin. Annu Rev Physiol 62:413–437
Ahima RS et al (1996) Role of leptin in the neuroendocrine response to fasting. Nature 382(6588):250–252
Baldini G et al (1992) Cloning of a Rab3 isotype predominantly expressed in adipocytes. Proc Natl Acad Sci USA 89(11):5049–5052
Berg AH et al (2001) The adipocyte-secreted protein Acrp30 enhances hepatic insulin action. Nat Med 7(8):947–953
Berg AH, Combs TP, Scherer PE (2002) ACRP30/adiponectin: an adipokine regulating glucose and lipid metabolism. Trends Endocrinol Metab 13(2):84–89
Boyer BB et al (1997) Leptin prevents posthibernation weight gain but does not reduce energy expenditure in arctic ground squirrels. Comp Biochem Physiol C Pharmacol Toxicol Endocrinol 118(3):405–412
Combs TP et al (2003) Sexual differentiation, pregnancy, calorie restriction, and aging affect the adipocyte-specific secretory protein adiponectin. Diabetes 52(2):268–276
Combs TP et al (2004) A transgenic mouse with a deletion in the collagenous domain of adiponectin displays elevated circulating adiponectin and improved insulin sensitivity. Endocrinology 145(1):367–383
Concannon P et al (2001) Seasonal changes in serum leptin, food intake, and body weight in photoentrained woodchucks. Am J Physiol Regul Integr Comp Physiol 281(3):R951–959
DiGirolamo M, Mendlinger S, Fertig JW (1971) A simple method to determine fat cell size and number in four mammalian species. Am J Physiol 221:850–858
Florant GL (1998) Lipid metabolism in hibernators: the importance of essential fatty acids. Am Zool 38:331–340
Florant GL et al (1985) Seasonal changes in pancreatic B-cell function in euthermic yellow-bellied marmots. Am J Physiol 249(2 Pt 2):R159–165
Florant GL et al (1990) Plasma and white adipose tissue lipid composition in marmots. Am J Physiol 258(5 Pt 2):R1123–1131
Fried SK, Moustaid-Moussa N (2001) Culture of adipose tissue and isolated adipocytes. Meth Mol Biol 155:197–212
Fruebis J et al (2001) 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 98(4):2005–2010
Goldrick RB (1967) Morphological changes in the adipocyte during fat deposition and mobilization. Am J Physiol 212:777–782
Havel PJ (2002) Control of energy homeostasis and insulin action by adipocyte hormones: leptin, acylation stimulating protein, and adiponectin. Curr Opin Lipidol 13(1):51–59
Hoehn KL, Hudachek SF, Summers SA, Florant GL (2004) Seasonal, tissue-specific regulation of Akt/protein kinase B and glycogen synthase in hibernators. Am J Physiol Regul Integr Comp Physiol 286(3):R498–504
Kronfeld-Schor N et al (2000) Dissociation of leptin secretion and adiposity during prehibernatory fattening in little brown bats. Am J Physiol Regul Integr Comp Physiol 279(4):R1277–1281
Le Lay S et al (2001) Cholesterol, a cell size-dependent signal that regulates glucose metabolism and gene expression in adipocytes. J Biol Chem 276(20):16904–16910
Margues B, Hausman DB, Martin RJ (1998) Association of fat cell size and paracrine growth factors in development of hyperplastic obesity. Am J Physiol 275(6 Pt 2):R1898–1908
Niswender KD, Schwartz MW (2003) Insulin and leptin revisited: adiposity signals with overlapping physiological and intracellular signaling capabilities. Front Neuroendocrinol 24(1):1–10
Ormseth OA et al (1996) Leptin inhibits prehibernation hyperphagia and reduces body weight in arctic ground squirrels. Am J Physiol 271(6 Pt. 2):R1775–1779
Pulawa LK, Florant GL (2000) The effects of caloric restriction on the body composition and hibernation of the golden-mantled ground squirrel (Spermophilus lateralis). Physiol Biochem Zool 73(5):538–546
Qi Y et al (2004) Adiponectin acts in the brain to decrease body weight. Nat Med 10:524–529
Rajala MW, Scherer P (2003) The adipocyte: at the crossroads of energy homeostasis, inflammation, and atherosclerosis. Endocrinology 144(9):3765–3773
Rajala MW et al (2002) Cell type-specific expression and coregulation of murine resistin and resistin-like molecule-alpha in adipose tissue. Mol Endocrinol 16(8):1920–1930
Rajala MW et al (2004) Regulation of resistin expression and circulating levels in obesity, diabetes, and fasting. Diabetes 53(7):1671–1679
Rodbell M (1964) Metabolism of isolated fat cells. I. Effects of hormones on glucose metabolism and lipolysis. J Biol Chem 239(2):375–380
Rousseau K, Atcha Z, Loudon AS (2003) Leptin and seasonal mammals. J Neuroendocrinol 15(4):409–414
Scherer PE et al (1994) Induction of caveolin during adipogenesis and association of GLUT4 with caveolin-rich vesicles. J Cell Biol 127(5):1233–1243
Tsao TS et al (2002a) Oligomerization state-dependent activation of NF-kappa B signaling pathway by adipocyte complement-related protein of 30 kDa (Acrp30). J Biol Chem 277(33):29359–29362
Tsao TS, Lodish HF, Fruebis J (2002b) ACRP30, a new hormone controlling fat and glucose metabolism. Eur J Pharmacol 440(2–3):213–221
Walsberg GE (1988) Evaluation of a nondestructive method for determining fat stores in small birds and mammals. Physiol Zool 61:153–159
Wang P et al (1997) Seasonal changes in enzymes of lipogenesis and triacylglycerol synthesis in the golden-mantled ground squirrel (Spermophilus lateralis). Comp Biochem Physiol B Biochem Mol Biol 118(2):261–267
Acknowledgements
We thank Dr. Robert Handa’s lab at CSU for assistance with the leptin RIA kit; Dr. Susan Fried for technical assistance with the isolation of the fat cells; and Dr. Ying Lin, and Ann Marie Gage for outstanding technical assistance. This research was supported by a Grant from the American Heart Association (#5-35669) awarded to S.A.S., a NIH grant # DK60676-01 to G.L.F., a NIHMST program grant T32-GM07288 to M.R., and a NIH grant DK55758 to P.E.S.
Author information
Authors and Affiliations
Corresponding author
Additional information
Communicated by I.D. Hume
Rights and permissions
About this article
Cite this article
Florant, G.L., Porst, H., Peiffer, A. et al. Fat-cell mass, serum leptin and adiponectin changes during weight gain and loss in yellow-bellied marmots (Marmota flaviventris). J Comp Physiol B 174, 633–639 (2004). https://doi.org/10.1007/s00360-004-0454-0
Accepted:
Published:
Issue Date:
DOI: https://doi.org/10.1007/s00360-004-0454-0