Skip to main content

Advertisement

SpringerLink
Log in

Changes in body mass, serum leptin, and mRNA levels of leptin receptor isoforms during the premigratory period in Myotis lucifugus

  • Original Paper
  • Published:
Journal of Comparative Physiology B Aims and scope Submit manuscript

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.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  • Ahima RS, Osei SY (2004) Leptin signaling. Physiol Behav 81(2):223–241

    Article  PubMed  CAS  Google Scholar 

  • Anthony EL, Gustafson AW (1984) A quantitative study of pituitary colloid in the bat Myotis lucifugus lucifugus in relation to age, sex and season. Am J Anat 169(1):89–100

    Article  PubMed  CAS  Google Scholar 

  • Anthony EL, Weston PJ, Montvilo JA, Bruhn TO, Neel K, King JC (1989) Dynamic aspects on the LHRH system associated with ovulation in the little brown bat (Myotis lucifugus). J Reprod Fertil 87(2):671–686

    PubMed  CAS  Google Scholar 

  • Anthony EL, Bruhn TO, Weston PJ (1991) Immunocytochemical localization of growth hormone and growth hormone-releasing hormone immunoreactivity in the brain and pituitary of the little brown bat. Am J Anat 190(1):1–9

    Article  PubMed  CAS  Google Scholar 

  • Asikainen J, Mustonen AM, Hyvarinen H, Nieminen P (2004) Seasonal physiology of the wild raccoon dog (Nyctereutes procyonoides). Zool Sci 21(4):385–391

    Article  PubMed  Google Scholar 

  • Boado RJ, Golden PL, Levin N, Pardridge WM (1998) Up-regulation of blood-brain barrier short-form leptin receptor gene products in rats fed a high fat diet. J Neurochem 71(4):1761–1764

    Article  PubMed  CAS  Google Scholar 

  • Buchanan GD, YoungLai EV (1988) Plasma progesterone concentrations in female brown bats (Myotis lucifugus) during hibernation. J Reprod Fertil 83(1):59–65

    PubMed  CAS  Google Scholar 

  • Bullen JW Jr., Bluher S, Kelesidis T, Mantzoros CS (2007) Regulation of adiponectin and its receptors in response to development of diet-induced obesity in mice. Am J Physiol Endocrinol Metab 292(4):E1079–E1086

    Article  PubMed  CAS  Google Scholar 

  • Burnett CD, August PV (1981) Time and energy budgets for day roosting in a maternity colony of Myotis lucifugus. J Mammal 62:758–766

    Article  Google Scholar 

  • Cammisotto PG, Bendayan M (2007) Leptin secretion by white adipose tissue and gastric mucosa. Histol Histopathol 22(2):199–210

    PubMed  CAS  Google Scholar 

  • Chehab FF, Qui J, Mounzih K, Ewart-Toland A, Ogus S (2002) Leptin and reproduction. Nutr Rev 60(pt2):S39–S46

    Article  PubMed  Google Scholar 

  • Currie WB, Blake M, Wimsatt WA (1988) Fetal development and placental and maternal plasma concentrations of progesterone in the little brown bat (Myotis lucifugus). J Reprod Fertil 82(1):401–407

    Article  PubMed  CAS  Google Scholar 

  • Hector J, Schwarzloh B, Goehring J, Strate TG, Hess UF, Deuretzbacher G, Hansen-Algenstaedt N, Beil FU, Algenstaedt P (2007) TNF-α alters visfatin and adiponectin levels in human fat. Horm Metab Res 39(4):250–255

    Article  PubMed  CAS  Google Scholar 

  • Johnstone LE, Higuchi T (2001) Food intake and leptin during pregnancy and lactation. Prog Brain Res 133:215–227

    Article  PubMed  CAS  Google Scholar 

  • Kadowaki T, Yamauchi T (2005) Adiponectin and adiponectin receptors. Endocr Rev 26(3):439–451

    Article  PubMed  CAS  Google Scholar 

  • Klingenspor M, Niggemann H, Heldmaier G (2000) Modulation of leptin sensitivity by short photoperiod acclimation in the Djungarian hamster, Phodopus sungorus. J Comp Physiol B 170(1):37–43

    Article  PubMed  CAS  Google Scholar 

  • Kronfeld-Schor N, Richardson C, Silvia BA, Kunz TH, Widmaier EP (2000) Dissociation of leptin secretion and adiposity during prehibernatory fattening in little brown bats. Am J Physiol Regul Integr Comp Physiol 279(4):R1277–R1281

    PubMed  CAS  Google Scholar 

  • Kronfeld-Schor N, Zhao J, Silvia BA, Matthews PT, Zimmerman S, Widmaier EP, Kunz TH (2001) Hyperleptinemia in pregnant bats is characterized by increased placental leptin secretion in vitro. Endocrine 14(2):225–233

    Article  PubMed  CAS  Google Scholar 

  • Kunz TH (1980) Daily energy budgets of free-living bats. In: Wilson DE, Gardner AL (eds) Proceedings of the fifth international bat research conference. Texas Tech Press, Lubbock, pp 369–392

  • Kunz TH, Kurta A (1988) Methods of capturing and holding bats. In: Kunz TH (eds) Ecological and behavioral methods for the study of bats. Smithsonian Institution Press, Washington, DC. pp 1–30

    Google Scholar 

  • Kunz TH, Wrazen JA, Burnett CD (1998) Changes in body mass and body composition in pre-hibernating little brown bats (Myotis lucifugus). Ecoscience 5:8–17

    Google Scholar 

  • Kunz TH, Bicer E, Hood WR, Axtell MJ, Harrington WR, Silvia BA, Widmaier EP (1999) Plasma leptin decreases during lactation in insectivorous bats. J Comp Physiol B 169(1): 61–66

    Article  PubMed  CAS  Google Scholar 

  • Ladyman SR, Grattan DR (2004) 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 145(8):3704–3711

    Article  PubMed  CAS  Google Scholar 

  • Lecklin A, Dube MG, Torto RN, Kalra PS, Kalra SP (2005) Perigestational suppression of weight gain with central leptin gene therapy results in lower weight FI generation. Peptides 26(7):1176–1187

    Article  PubMed  CAS  Google Scholar 

  • Livak KJ, Schmittgen TD (2001) Analysis of relative gene expression data using real-time quantitative PCR and the 2−ΔΔCt Method. Methods 25(4):402–408

    Article  PubMed  CAS  Google Scholar 

  • Martin L, Bernard RTF (2000) Endocrine regulation of reproduction in bats: the role of circulating gonadal hormones. In: Crichton EG, Krutzsch PH (eds) Reproductive biology of bats. Academic, San Diego, pp 27–64

    Google Scholar 

  • Ormseth OA, Nicolson M, Pelleymounter MA, Boyer BB (1996) Leptin inhibits prehibernation hyperphagia and reduces body weight in ground squirrels. Am J Physiol 271(6 pt 2):R1775–R1779

    PubMed  CAS  Google Scholar 

  • Rousseau K, Atcha Z, Cagampang FR, Le Rouzic P, Stirland JA, Ivanov TR, Ebling FJ, Klingenspor M, Loudon AS (2002) Photoperiodic regulation of leptin resistance in the seasonally breeding Siberian hamster (Phodopus sangorus). Endocrinology 143(8):3083–3095

    Article  PubMed  CAS  Google Scholar 

  • Rousseau K, Atcha Z, Lousdon AS (2003) Leptin and seasonal mammals. J Neuroendocrinol 15(4):4091414

    Article  PubMed  CAS  Google Scholar 

  • Sahu A (2004) Minireview: a hypothalamic role in energy balance with special emphasis on leptin. Endocrinology 145(6):2613–2620

    Article  PubMed  CAS  Google Scholar 

  • Schulz LC, Widmaier EP (2006) Leptin receptors. In: Henson MC, Castracane VD (eds) Leptin. Endocrinology update series, Springer, Heidelberg, pp 11–31

  • Schulz LC, Townsend K, Kunz TH, Widmaier EP (2007) Inhibition of trophoblast invasiveness in vitro by immunoneutralization of leptin in the bat, Myotis lucifugus (Chiroptera). Gen Comp Endocrinol 150(1):59–65

    Article  PubMed  CAS  Google Scholar 

  • Speakman JR, Thomas DW (2003) Physiological ecology and energetics of bats. In: Kunz TH, Fenton M (eds) Bat ecology, University of Chicago Press, Chicago, pp 430–490

    Google Scholar 

  • Tups A, Ellis C, Moar KM, Logie TJ, Adam CL, Mercer JG, Klingenspor M (2004) 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 145(3):1185–1193

    Article  PubMed  CAS  Google Scholar 

  • Widmaier EP, Long J, Cadigan B, Gurgel S, Kunz TH (1997) Leptin, corticotropin-releasing hormone (CRH), and neuropeptide Y (NPY) in free-ranging pregnant bats. Endocrine 7(2):145–150

    Article  PubMed  CAS  Google Scholar 

  • Yamashita T, Murakami T, Otani S, Kuwajima M, Shima K (1998) Leptin receptor signal transduction: OBRa and OBRb of fa type. Biochem Biophys Res Commun 246(3):752–759

    Article  PubMed  CAS  Google Scholar 

  • Zhao J, Kunz TH, Tumba N, Schulz LC, Li C, Reeves M, Widmaier EP (2003) Comparative analysis of expression and secretion of placental leptin in mammals. Am J Physiol Regul Integr Comp Physiol 285(2):R438–R446

    PubMed  CAS  Google Scholar 

  • Zhang Y, Proenca R, Maffei M, Barone M, Leopold L, Friedman JM (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372(6505):425-432

    Article  PubMed  Google Scholar 

Download references

Acknowledgments

This work was supported in part by NSF grant IBN (IOS)0446057 to EPW and THK, NSF DDIG grant IOB 0507914 to KLT, and American Association of University Women Doctoral Dissertation grant to KLT.

Author information

Authors and Affiliations

  1. Department of Biology, Boston University, 5 Cummington Street, Boston, MA, 02215, USA

    Kristy L. Townsend, Thomas H. Kunz & Eric P. Widmaier

Authors
  1. Kristy L. Townsend
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Thomas H. Kunz
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Eric P. Widmaier
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Eric P. Widmaier.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Townsend, K.L., Kunz, T.H. & Widmaier, E.P. Changes in body mass, serum leptin, and mRNA levels of leptin receptor isoforms during the premigratory period in Myotis lucifugus . J Comp Physiol B 178, 217–223 (2008). https://doi.org/10.1007/s00360-007-0215-y

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-007-0215-y

Keywords

Search

Navigation