Advertisement

Acta Biologica Hungarica

, Volume 59, Issue 1, pp 1–16 | Cite as

Changes in Serum Leptin, Insulin, Androstenedione and Luteinizing Hormone During Ovarian Cycle in the Bat, Taphozous Longimanus

  • U. P. SinghEmail author
  • A. Krishna
  • Kunwar P. BhatnagarEmail author
Article

Abstract

Detailed reproductive pattern and associated endocrine characteristics have been documented in only a few species of order Chiroptera. The aim of the present study was to examine the changes in body weight, serum insulin, leptin, androstenedione and luteinizing hormone (LH) concentrations during annual ovarian cycle in the sheath-tailed bat, Taphozous longimanus. Bats were sampled over three years. Leptin, a satiety hormone produced primarily by adipose tissue, provides information to feeding center of the brain about nutritional status, fat mass, appetite and energy expenditure. The circulating concentration of leptin begins to increase from October and attains a peak in December. The peak serum leptin concentration coincides with body weight in November before winter dormancy in December. The serum leptin levels dissociate from body weight during December. The other peaks of serum leptin levels coincide with late stages of the two successive pregnancies. The serum insulin concentration begins to increase from September and attains a peak during December. The insulin concentration remains low from January to August. The circulating androstenedione concentration begins to increase in October, reaching a peak in December. This increase in androstenedione concentration correlated with the period of heavy accumulation of abdominal fat and increase in body weight. There was a sharp decline in androstenedione concentration and body weight in January. The serum LH shows peaks, in November, coinciding with the peaked body weight, the other peaks in January and May, coinciding with ovulation for the two successive pregnancies. The high leptin and insulin levels might be responsible for the maintenance of reproductive response and gonadal function during adverse environmental condition in the winter, while high androstenedione, and associated body weight along with LH might be responsible for maintaining basal gonadal function. We conclude that high leptin, androstenedione and insulin serve, as signal for the reproductive functions in that sufficient body fat are available to meet the caloric demands and maintain normal function during adverse winter conditions.

Keywords

Androstenedione bats insulin leptin luteinizing hormone Taphozous longimanus 

Preview

Unable to display preview. Download preview PDF.

Unable to display preview. Download preview PDF.

References

  1. 1.
    Abhilasha, Krishna A. (1997) Adiposity and androstenedione production in relation to delayed ovulation in the Indian bat, Scotophilus heathi. Comp. Biochem. Physiol. 116, 97–101.Google Scholar
  2. 2.
    Ahima R. S., Prabakaran D., Mantzoros C., Qu D., Lowell B., Marato-flier E., Flier J. S. (1996) Role of leptin in the neuroendocrine response to fasting. Nature 382, 250–252.Google Scholar
  3. 3.
    Ahima R. S., Flier J. S. (2000) Leptin. Ann. Rev. Physiol. 62, 413–437.Google Scholar
  4. 4.
    Auwerx J., Staels B. (1998) Leptin. Lancet. 351, 737–742.PubMedGoogle Scholar
  5. 5.
    Barash I. A., Cheung C. C., Weigle D. S., Ren H., Kabigting E. B., Kuijper J. L., Clifton D. K., Steiner R. A. (1996) Leptin is metabolic signal to the reproductive system. Endocrinol. 137, 3144–3147.Google Scholar
  6. 6.
    Barbieri R. L., Hornstein M. D. (1988) Hyperinsulenemia and ovarian hyperandrogenism: Cause and effect. Endocrinol. Metab. Clin. North Amer 17, 685–703.Google Scholar
  7. 7.
    Bernard R. T. F., Bojarski C., Millar R. R. (1991) Plasma progesterone and luteinizing hormone concentrations and the role of the corpus luteum and LH gonadotropes in the control of delayed implantation in Schreiber’s long-fingered bat (Miniopterus schreibersii). J. Reprod Fert. 93, 34–42.Google Scholar
  8. 8.
    Budak E., Fernandez Sanchez M., Bellver J., Cervero A., Simon C., Pellicer A. (2006) Interactions of the hormones leptin, ghrelin, adiponectin, resistin, and PYY336 with the reproductive system. Fertil. Steril. 85, 1563–1581.PubMedGoogle Scholar
  9. 9.
    Butte N. F., Hopkinson J. M., Nicolson M. A. (1997) Leptin in human reproduction; serum leptin levels in pregnant and lactating women. J. Clin. Endocrinol. Metab. 82, 585–589.PubMedGoogle Scholar
  10. 10.
    Campfield L. A., Smith F. J., Guisez Y., Devos R., Burn B. (1995) Recombinant mouse OB protein; evidence for a peripheral signal linking adiposity and central neural networks. Science 269, 546–549.PubMedGoogle Scholar
  11. 11.
    Chehab F. F., Lim M. R., Lu R. (1996) Correction of the sterility defect in homozygous obese female mice by treatment with human recombinant leptin. Nature (Genetics) 12, 318–320.Google Scholar
  12. 12.
    Considine R. V., Sinha M. K., Heiman M. L., Kriauciunas A., Stephens T. W., Nyce M. R., Ohannesian J. P., Marco C. C., Mckee L. J., Bauer T. L. et al. (1996) Serum immunoreactive leptin concentration in normal weight and obese humans. N. Engl. J. Med. 334, 292–295.PubMedGoogle Scholar
  13. 13.
    Conway G. S., Jacobs H. S. (1993) Clinical implications of hyperinsulenemia in women. Clin. Endocrinol. 39, 623–632.Google Scholar
  14. 14.
    Dagogo-Jack S., Fanelli C., Paramore D., Brothers J., Landt M. (1996) Plasma leptin and insulin relationship in obese and non-obese humans. Diabetes 45, 695–698.PubMedGoogle Scholar
  15. 15.
    Dominic C. J., Krishna A. (1989) Reproductive cycle of mammals. Chiroptera and Insectivore. In: S. K. Saidapur (ed.) Reproductive Cycle of Indian Vertebrates. Allied Publishers Ltd., New Delhi, pp. 311–346.Google Scholar
  16. 16.
    Drazen D. L., Kriegsfeld L. J., Schneider J. R., Nelson R. J. (2000) Leptin, but not immune function is linked to reproductive responsiveness to photoperiod. Am. J. Physiol. 278, 1401–1407.Google Scholar
  17. 17.
    Dunaif A., Mandeli J., Fluhr F. L., Dobrjansky A. (1988) The impact of obesity and chronic hyperinsulenemia on gonadotrophin release and gonadal steroids secretion in the polycystic ovary syndrome. J. Clin. Endocrinol. Metab. 66, 131–139.PubMedGoogle Scholar
  18. 18.
    Feist D., Florant G., Greenwood M. R. C., Feist C. (1986) Regulation of energy stores in arctic ground squirrels. Brown fat thermogenic capacity, lipoprotein lipase and pancreatic hormone during fat deposition. In: H. C. Hellet X. J. Musacchia L. C. H. Wang (eds) Living in the Cold: Physiological and Biochemical Adaptations. Elsevier, New York, pp. 281–285.Google Scholar
  19. 19.
    Ferreira-Dias G., Claudino F., Carvalho H., Agricola R., Alpoim-Moreira J., Robalo Silva J. (2005) Seasonal reproduction in the mare: possible role of plasma leptin, body weight and immune status. Domest. Anim. Endocrinol. 29, 203–213.PubMedGoogle Scholar
  20. 20.
    Fitzgerald B. P., McManus C. J. (2000) Photoperiodic versus metabolic signals as determinants of seasonal anestrous in the mare. Biol. Reprod. 63, 335–340.PubMedGoogle Scholar
  21. 21.
    Florant G. L., Lawrence A. K., Williams K., Bauman W. A. (1985) Seasonal changes in pancreatic (3-cell function in euthermic yellow bellied marmots. Am. J. Physiol. 249, 159–165.Google Scholar
  22. 22.
    Gore-Langton R. E., Armstrong D. T. (1988) Follicular steroidogenesis and its control. In: E. Knobil, J. Neil (eds) Physiology of Reproduction. Raven Press, New York. pp. 331–386.Google Scholar
  23. 23.
    Heideman P. D. (1989) Delayed development in Fischer’s pygmy fruit bat, Haplonycteris fischeri, in the Philippines. J. Reprod. Fertil. 85, 363–382.PubMedGoogle Scholar
  24. 24.
    King B. M. (1988) Glucocorticoids and hypothalamic obesity. Neurosci. Biobehav. Rev. 12, 29–37.PubMedGoogle Scholar
  25. 25.
    Krishna A., Dominic C. J. (1982) Differential rates of fetal growth in two successive pregnancies in the emballonurid bat, Taphozous longimanus Hardwicke. Biol. Reprod. 27, 351–353.PubMedGoogle Scholar
  26. 26.
    Krishna A., Singh K., Doval J., Chanda D. (1998) Changes in circulating insulin and corticos-terone concentration during different reproductive phases and their relationship to body weight and androstenedione concentration of male Scotophilus heathi. J. Exp. Zool. 281, 201–206.PubMedGoogle Scholar
  27. 27.
    Kronfeld-Schor N., Richardson, C, Silvia B. A., Kunz T. H., Widmaier E. P. (2000) Dissociation of leptin secretion and adiposity during pre-hibernatory fattening in little brown bats. AJP-Reg. Int. Comp. Physiol. 279, 1277–1281.Google Scholar
  28. 28.
    Laughlin G. A., Morales A. J., Yen S. S. (1997) Serum leptin levels in women with polycystic ovary syndrome: the role of insulin resistance/hyperinsulenemia. J. Clin. Endocrinol. Metab. 82, 1692–1696.PubMedGoogle Scholar
  29. 29.
    Lee G. H., Proenca R., Montez J. M., Caroll K. M., Darvishzadeh J. G., Lee J. I., Friedman J. M. (1996) Abnormal splicing of the leptin receptor in diabetic mice. Nature 379, 632–635.PubMedGoogle Scholar
  30. 30.
    Lindheim S. R., Sauer M. V., Carmina E., Chang, P. L, Zimmerman R., Lobo R. A. (2000) Circulating leptin levels during ovulation induction: relation to adiposity and ovarian morphology. Fertil. Steril. 73, 493–498.PubMedGoogle Scholar
  31. 31.
    Masuzaki H., Ogawa Y., Sagawa N., Hosada K., Matsumoto T., Mise H., Nishimura H., Yoshimasa, Y., Tanaka, Y., Mori T., Nakao K. (1997) Nonadipose tissue production of leptin: leptin as a novel placenta-derived hormone in humans. Nat. Med. 3, 1029–1033.PubMedGoogle Scholar
  32. 32.
    Meenakumari K. J., Krishna A. (2005) Delayed embryonic development in the Indian short-nosed fruit bat, Cynopterus sphinx. Zoology 108, 131–140.PubMedGoogle Scholar
  33. 33.
    Racey P. A. (1982) Ecology of bat reproduction. In: T. Kunz (ed.) Ecology of Bats. Plenum Press, New York, pp. 57–164.Google Scholar
  34. 34.
    Schwartz, M. W., Woods S. C., Porte, D. Jr., Seeley R. J., Baskin D. G. (2000) Central nervous system control food intake. Nature 404, 661–671.PubMedGoogle Scholar
  35. 35.
    Singh U. P., Krishna A. (1996) Immunocytochemical studies on the pituitary pars distalis of the tropical Vespertilionid bat, Scotophilus heathi, in reference to ovarian cycle. Acta Anat. 155, 104–112.PubMedGoogle Scholar
  36. 36.
    Singh U. P., Krishna A. (1997) A mini review on the female chiropteran reproduction. J. Endocrinol. Reprod. 1, 1–19.Google Scholar
  37. 37.
    Singh U. P., Krishna A. (2002) Seasonal changes in circulating steroid concentration and their correlation with the ovarian activity in the female Indian sheath tailed bat, Taphozous longimanus. J. Exp. Zool. 292, 384–392.PubMedGoogle Scholar
  38. 38.
    Tokuyama K., Galantino H. L., Green R., Florant G. L. (1991) Seasonal glucose uptake in marmots (Marmota flaviventris); the role of pancreatic hormones. Comp. Biochem. Physiol. A 100, 925–930.PubMedGoogle Scholar
  39. 39.
    Van der Spuy Z. M. (1985) Nutrition and reproduction. Clinical Obstet. Gynecol. 12, 579–604.Google Scholar
  40. 40.
    Vogel G. (1996) Leptin: a trigger for puberty. Science 274, 1466–1467.PubMedGoogle Scholar
  41. 41.
    Widmaier E. P., Long J. K., Cadigan B., Gurgel S., Kunz T. H. (1997) Leptin, corticotropin-releas-ing hormone (CRH), and neuropeptide Y (NPY) in free ranging pregnant bats. Endocrine 7, 145–150.PubMedGoogle Scholar
  42. 42.
    Zhang Y., Proenca R., Maffei M., Barone M., Leopold L., Friedman J. M. (1994) Positional cloning of the mouse obese gene and its human homologue. Nature 372, 425–432.PubMedPubMedCentralGoogle Scholar

Copyright information

© Akadémiai Kiadó, Budapest 2008

This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made.

Authors and Affiliations

  1. 1.Department of Pathology, Microbiology and ImmunologyUniversity of South CarolinaColumbiaUSA
  2. 2.Department of ZoologyBanaras Hindu UniversityVaranasiIndia
  3. 3.Department of Anatomical Sciences & NeurobiologyUniversity of Louisville School of MedicineLouisvilleUSA

Personalised recommendations