Changes in Body Mass, Serum Leptin, and MRNA Levels of Leptin Receptor Isoforms During the Premigratory Period in Myotis Lucifugus

Overview

Journal J Comp Physiol B

Specialties Biochemistry
Endocrinology
Physiology

Date 2007 Oct 27

PMID 17962952

Citations 9

Authors

Kristy L Townsend

Thomas H Kunz

Eric P Widmaier

Affiliations

Soon will be listed here.

Abstract

Migration and hibernation in mammals may be preceded by a period of leptin resistance, which may in part account for the increasing adiposity and body mass that occurs during these periods. We hypothesized that hypothalamic expression of leptin receptor mRNA would decrease during the premigration (PM) period in the little brown myotis, Myotis lucifugus. Body mass of M. lucifugus increased during the PM period, but serum leptin levels did not change during that time. Hypothalamic mRNA levels for both the short (ObRa) and fully active long (ObRb) forms of the leptin receptor increased during PM, but the relative increase in ObRa was larger and occurred sooner than ObRb. mRNA levels of an inhibitor of leptin signaling (protein inhibitor of activated STAT3: PIAS3) increased in hypothalami during the PM period in bats. Adiponectin is an adipokine that has been linked to obesity in rodents; normally, serum levels of adiponectin decrease in obesity. In M. lucifugus, adiponectin mRNA levels decreased in adipose tissue during the period of mass gain, but circulating adiponectin levels did not change. We conclude that the relative changes in leptin receptor isoform expression during the PM fattening period may favor binding of leptin to the less active short isoform. Coupled with increased expression of PIAS3 and the dissociation of serum leptin levels from body mass and adiposity, these changes could account in part for the adaptive fattening during the PM period. In addition, the adipokine profiles of M. lucifugus during the PM period and that of obesity in non-hibernating mammals are strikingly dissimilar.

Citing Articles

Active season body mass patterns of little brown and northern myotis bats.

Balzer E, Grottoli A, Burns L, Broders H Ecol Evol. 2024; 12(8):e9230.

PMID: 39411583 PMC: 11476244. DOI: 10.1002/ece3.9230.

Body fat and circulating leptin levels in the captive short-beaked echidna (Tachyglossus aculeatus).

Dutton-Regester K, Roser A, Meer H, Hill A, Pyne M, Al-Najjar A J Comp Physiol B. 2024; 194(4):457-471.

PMID: 38748188 PMC: 11316712. DOI: 10.1007/s00360-024-01559-z.

Plasma mammalian leptin analogue predicts reproductive phenology, but not reproductive output in a capital-income breeding seaduck.

Hennin H, Legagneux P, Gilchrist H, Bety J, McMurtry J, Love O Ecol Evol. 2019; 9(3):1512-1522.

PMID: 30805178 PMC: 6374671. DOI: 10.1002/ece3.4873.

Beyond thermoregulation: metabolic function of cetacean blubber in migrating bowhead and beluga whales.

Ball H, Londraville R, Prokop J, George J, Suydam R, Vinyard C J Comp Physiol B. 2016; 187(1):235-252.

PMID: 27573204 PMC: 5535305. DOI: 10.1007/s00360-016-1029-6.

Endocrine regulation of bone and energy metabolism in hibernating mammals.

Doherty A, Florant G, Donahue S Integr Comp Biol. 2014; 54(3):463-83.

PMID: 24556365 PMC: 4184349. DOI: 10.1093/icb/icu001.

References

Klingenspor M, Niggemann H, Heldmaier G . Modulation of leptin sensitivity by short photoperiod acclimation in the Djungarian hamster, Phodopus sungorus. J Comp Physiol B. 2000; 170(1):37-43. DOI: 10.1007/s003600050005. View

Rousseau K, Atcha Z, Cagampang F, Le Rouzic P, Stirland J, Ivanov T . Photoperiodic regulation of leptin resistance in the seasonally breeding Siberian hamster (Phodopus sungorus). Endocrinology. 2002; 143(8):3083-95. DOI: 10.1210/endo.143.8.8967. View

Anthony E, Gustafson A . A quantitative study of pituitary colloid in the bat Myotis lucifugus lucifugus in relation to age, sex, and season. Am J Anat. 1984; 169(1):89-100. DOI: 10.1002/aja.1001690108. View

BUCHANAN G, Younglai E . Plasma progesterone concentrations in female little brown bats (Myotis lucifugus) during hibernation. J Reprod Fertil. 1988; 83(1):59-65. DOI: 10.1530/jrf.0.0830059. View

Chehab F, Qiu J, Mounzih K, Ewart-Toland A, Ogus S . Leptin and reproduction. Nutr Rev. 2002; 60(10 Pt 2):S39-46; discussion S68-84, 85-7. DOI: 10.1301/002966402320634823. View

Tups A, Ellis C, Moar K, Logie T, Adam C, Mercer J . Photoperiodic regulation of leptin sensitivity in the Siberian hamster, Phodopus sungorus, is reflected in arcuate nucleus SOCS-3 (suppressor of cytokine signaling) gene expression. Endocrinology. 2003; 145(3):1185-93. DOI: 10.1210/en.2003-1382. View

Lecklin A, Dube M, Torto R, Kalra P, Kalra S . Perigestational suppression of weight gain with central leptin gene therapy results in lower weight F1 generation. Peptides. 2005; 26(7):1176-87. DOI: 10.1016/j.peptides.2005.01.021. View

Ahima R, Osei S . Leptin signaling. Physiol Behav. 2004; 81(2):223-41. DOI: 10.1016/j.physbeh.2004.02.014. View

Livak K, Schmittgen T . Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods. 2002; 25(4):402-8. DOI: 10.1006/meth.2001.1262. View

10.

Ladyman S, Grattan D . Region-specific reduction in leptin-induced phosphorylation of signal transducer and activator of transcription-3 (STAT3) in the rat hypothalamus is associated with leptin resistance during pregnancy. Endocrinology. 2004; 145(8):3704-11. DOI: 10.1210/en.2004-0338. View

11.

Bullen Jr J, Bluher S, Kelesidis T, Mantzoros C . Regulation of adiponectin and its receptors in response to development of diet-induced obesity in mice. Am J Physiol Endocrinol Metab. 2006; 292(4):E1079-86. DOI: 10.1152/ajpendo.00245.2006. View

12.

Anthony E, Weston P, Montvilo J, Bruhn T, Neel K, King J . Dynamic aspects of the LHRH system associated with ovulation in the little brown bat (Myotis lucifugus). J Reprod Fertil. 1989; 87(2):671-86. DOI: 10.1530/jrf.0.0870671. View

13.

Sahu A . Minireview: A hypothalamic role in energy balance with special emphasis on leptin. Endocrinology. 2004; 145(6):2613-20. DOI: 10.1210/en.2004-0032. View

14.

Widmaier E, Long J, Cadigan B, Gurgel S, Kunz T . Leptin, corticotropin-releasing hormone (CRH), and neuropeptide Y (NPY)in free-ranging pregnant bats. Endocrine. 1998; 7(2):145-50. DOI: 10.1007/BF02778135. View

15.

Boado R, Golden P, Levin N, Pardridge W . Up-regulation of blood-brain barrier short-form leptin receptor gene products in rats fed a high fat diet. J Neurochem. 1998; 71(4):1761-4. DOI: 10.1046/j.1471-4159.1998.71041761.x. View

16.

Kadowaki T, Yamauchi T . Adiponectin and adiponectin receptors. Endocr Rev. 2005; 26(3):439-51. DOI: 10.1210/er.2005-0005. View

17.

Yamashita T, Murakami T, Otani S, Kuwajima M, Shima K . Leptin receptor signal transduction: OBRa and OBRb of fa type. Biochem Biophys Res Commun. 1998; 246(3):752-9. DOI: 10.1006/bbrc.1998.8689. View

18.

Johnstone L, Higuchi T . Food intake and leptin during pregnancy and lactation. Prog Brain Res. 2001; 133:215-27. DOI: 10.1016/s0079-6123(01)33016-9. View

19.

Ormseth O, Nicolson M, Pelleymounter M, Boyer B . Leptin inhibits prehibernation hyperphagia and reduces body weight in arctic ground squirrels. Am J Physiol. 1996; 271(6 Pt 2):R1775-9. DOI: 10.1152/ajpregu.1996.271.6.R1775. View

20.

Kronfeld-Schor N, Zhao J, Silvia B, Mathews P, Zimmerman S, Widmaier E . Hyperleptinemia in pregnant bats is characterized by increased placental leptin secretion in vitro. Endocrine. 2001; 14(2):225-33. DOI: 10.1385/ENDO:14:2:225. View