Role of leptin in delayed embryonic development in the Indian short-nosed fruit bat, Cynopterus sphinx

General and Comparative Endocrinology

Volumn 168, Issue 1, 2010, Pages 36-45

  Banerjee, A ^a   Meenakumari, K J ^a   Krishna, A ^a  

^a BANARAS HINDU UNIVERSITY   (India)

Author keywords

Delayed embryonic development; Leptin; Leptin receptor (Ob R); Ovary; Progesterone

Indexed keywords

CYCLINE; INDUCIBLE NITRIC OXIDE SYNTHASE; LEPTIN; LEPTIN RECEPTOR; LUTEINIZING HORMONE RECEPTOR; PROGESTERONE; STAT3 PROTEIN; STEROIDOGENIC ACUTE REGULATORY PROTEIN;

ARTICLE; BAT; CELL PROLIFERATION; CONCENTRATION RESPONSE; CONTROLLED STUDY; CORPUS LUTEUM; CYNOPTERUS SPHINX; DEVELOPMENTAL DISORDER; EMBRYO; EMBRYO DEVELOPMENT; FEMALE; HORMONE INHIBITION; IN VITRO STUDY; LIPID STORAGE; NONHUMAN; PRIORITY JOURNAL; PROGESTERONE BLOOD LEVEL; PROGESTERONE SYNTHESIS; PROTEIN EXPRESSION; PROTEIN FUNCTION; SEASONAL VARIATION;

EID: 77953700404     PISSN: 00166480     EISSN: 10956840     Source Type: Journal    
DOI: 10.1016/j.ygcen.2010.04.002     Document Type: Article

References (75)

1. Ahima R.S., Prabakaran D., Mantzoros C., Qu D., Lowell B., Maratos-Flier E., Flier J.S. Role of leptin in the neuroendocrine response to fasting. Nature 1996, 382:250-252.
2. Antczak M., Van Blerkom J. Oocyte influences on embryo development: the regulatory proteins leptin and STAT3 are polarized in mouse and human oocytes and differentially distributed within the cells of the pre-implantation stage embryo. Molecular Hum. Reprod. 1997, 3:1067-1086.
3. Banerjee A., Meenakumari K.J., Krishna A. Relationship between delayed embryonic development and metabolic factors and fat deposition in fruit bat Cynopterus sphinx. Reprod. Fertil. Dev. 2007, 19:626-633.
4. Banerjee A., Meenakumari K.J., Udin S., Krishna A. Melatonin regulates delayed embryonic development in the short-nosed fruit bat, Cynopterus sphinx. Reproduction 2009, 138:935-944.
5. Baratta M., Saleri R., Mainardi G.L., Valle D., Giustina A., Tamanini C. Leptin regulates growth hormone gene expression and secretion and nitric oxide production in pig pituitary cells. Endocrinology 2002, 143:551-557.
6. Barkan D., Jia H., Dantes A., Vardimon L., Amsterdam A., Rubinstein M. Leptin modulates the glucocorticoid-induced ovarian steroidogenesis. Endocrinology 1999, 140(4):1731-1738.
7. Baumann H., Morella K.K., White D.W., Dembski M., Bailon P.S., Kim H., Lai C.F., Tartaglia L.A. The full-length leptin receptor has signaling capabilities of interleukin 6-type cytokine receptors. Proc. Natl. Acad. Sci. USA 1996, 9:8374-8378.
8. Beltowski J., Wojcicka G., Borkowska E. Human leptin stimulates systemic nitric oxide production in the rat. Obes. Res. 2002, 10:939-946.
9. Bernard R.T.F., Bojarski C., Millar R.P. Plasma progesterone and luteinizing hormone concentrations and the role of the corpus luteum and LH gonadotrophs in the control of delayed implantation in Schreiber's long-fingered bat (Miniopterus schreibersii). J. Reprod. Fertil. 1991, 95:31-42.
10. Boelhauve M., Sinowatz F., Wolf E., Paula-Lopes F.F. Maturation of bovine oocytes in the presence of leptin improves development and reduces apoptosis of in vitro-produced blastocysts. Biol. Reprod. 2005, 73:737-744.
11. Bolli R., Dawn B., Xuan Y.T. Role of the JAK-STAT pathway in protection against myocardial ischemia/reperfusion injury. Trends Cardiovasc. Med. 2003, 13:72-79.
12. Bradshaw G.V.R. Reproductive cycle of the California leaf-nosed bat, Macrotus californicus. Science 1962, 136:645-646.
13. Brannian J.D., Zhao Y., McElroy M. Leptin inhibits gonadotrophin-stimulated granulosa cell progesterone production by antagonizing insulin action. Hum. Reprod. 1999, 14(6):1445-1448.
14. Brzechffa P.R., Jakimiuk A.J., Agarwal S.K., Weitsman S.R., Buyalos R.P., Magoffin D.A. Serum immunoreactive Leptin concentrations in Women with Polycystic Ovary Syndrome. J. Clin. Endocrinol. Metab. 1996, 81:4166-4169.
15. Burns J.M., Baker R.J., Bleier W.J. Hormonal control of " Delayed Development" in Macrotus waterhousii 1. Changes in plasma Thyroxine during pregnancy and lactation. Gen. Comp. Endocrinol. 1972, 18:54-58.
16. Burns J.M., Wallace W.E. Hormonal control of delayed development in Macrotus waterhousii. II. Radioimmunoassay of plasma estrone and estradiol 17β during pregnancy. Gen. Comp. Endocrinol. 1975, 25:529-533.
17. Cameo P., Bischof P., Calvo J.C. Effect of leptin on progesterone, human chorionic gonadotropin, and interleukin-6 secretion by human term trophoblast cells in culture biology of reproduction. Biol. Reprod. 2003, 8:472-477.
18. Clarke I.J., Henry B.A. Leptin and reproduction. Rev. Reprod. 1999, 4:48-55.
19. Crichton E.C., Hoyer P.B., Krutzsch P.H. Cellular composition and steroidogenic capacity of the ovary of Macrotus californicus (Chiroptera: Phyllostomatidae) during and after delayed embryonic development. Cell Tissue Res. 1990, 260:355-366.
20. Crichton E.C., Seamark R.F., Krutzsch P.H. The status of corpus luteum during pregnancy in Miniopterus schreibersii (Chiroptera: Vespertilionidae) with emphasis on its role in developmental delay. Cell Tissue Res. 1989, 258:183-201.
21. Duggal P.S., Van der Hoek K.H., Milner C.R., Ryan N.K., Armstrong D.T., Magoffin D.A., Norman R.J. The in vivo and in vitro effects of exogenous leptin on ovulation in the rat. Endocrinology 2000, 141:1971-1976.
22. Fedorcsák P., Storeng R., Dale P.O., Tanbo T., Åbyholm T. Obesity is associated with early pregnancy loss after IVF or ICSI. Acta Obstet. Gynecol. Scand. 2000, 79:43-48.
23. Fedorcsák P., Storeng R. Effects of leptin and leukemia inhibitory factor on preimplantation development and STAT3 signaling of mouse embryos in vitro. Biol. Reprod. 2003, 69(5):1531-1538.
24. Frühbeck G. Intracellular signalling pathways activated by leptin. Biochem. J. 2006, 393:7-20.
25. Ghilardi N., Ziegler S., Wiestner A., Stoffel A., Heim M.H., Skoda R.C. Defective STAT signaling by the leptin receptor in diabetic mice. Proc. Natl. Acad. Sci. USA 1996, 93:6231-6235.
26. Ghizzoni L., Barreca A., Mastorakos G., Furlini M., Vottero A., Ferrari B., Chrousos G.P., Bernasconi S. Leptin inhibits steroid biosynthesis by human granulosalutein cells. Horm. Metab. Res. 2001, 33:323-328.
27. Guo X., Chen S., Xing F. Effects of leptin on estradiol and progesterone production by human luteinized granulosa cells in vitro (in Chinese). Zhonghua Fu Chan Ke Za Zhi 2001, 36:95-97.
28. Heideman P.D. Delayed development in Fischer's pygmy fruit bat, Haplonycteris fischeri, in the Philippines. J. Reprod. Fertil. 1989, 85:363-382.
29. Henson M.C., Castracane V.D., Edwards D.E. Leptin: from satiety signal to reproductive regulator. Leptin and Reproduction 2003, 3-11. Kluwer Academic Press/Plenum Press Publishers, New York. M.C. Henson, V.D. Castracane (Eds.).
30. Herrid M., Nguyen V.L., Hinch G., McFarlane J.R. Leptin has concentration and stage-dependent effects on embryonic development in vitro. Reproduction 2006, 132:247-256.
31. Isenovic E.R., Meng Y., Divald A., Milivojevic N., Sowers J.R. Role of phosphatidylinositol 3-kinase/Akt pathway in angiotensin II and insulin-like growth factor-1 modulation of nitric oxide synthase in vascular smooth muscle cells. Endocrine 2002, 19:287-292.
32. Karlsson C., Lindell K., Svensson E., Bergh C., Lind P., Billig H., Carlsson L.M., Carlsson B. Expression of functional leptin receptors in the human ovary. J. Clin. Endocrinol. Metab. 1997, 82:4144-4148.
33. Karamouti M., Kollia P., Kallitsaris A., Vamvakopoulos N., Kollios G., Messinis I.E. Modulating effect of leptin on basal and follicle stimulating hormone stimulated steroidogenesis in cultured human lutein granulosa cells. J. Endocrinol. Invest. 2009, 32(5):415-419.
34. Kawamoto K. Endocrine control of the reproductive activity in hibernating bats. Zool. Sci. 2003, 20:1057-1069.
35. Kawamura K., Sato N., Fukuda J., Kodama H., Kumagai J., Tanikawa H., Nakamura A., Tanaka T. Leptin promotes the development of mouse preimplantation embryos in vitro. Endocrinology 2002, 143:1922-1931.
36. Kawamura K., Sato N., Fukuda J., Kodama H., Kumagai J., Tanikawa H., Murata M., Tanaka T. The role of leptin during the development of mouse preimplantation embryos. Mol. Cell. Endocrinol. 2003, 202:185-189.
37. Kikuchi N., Andoh K., Abe Y., Yamada K., Mizunuma H., Ibuki Y. Inhibitory action of leptin on early follicular growth differs in immature and adult female mice. Biol. Reprod. 2001, 65:66-71.
38. Kim H.S., Lee G.S., Kim J.H., Kang S.K., Lee B.C., Wang H. Expression of leptin ligand and receptor and effect of exogenous leptin supplement on in vitro development of porcine embryos. Theriogenology 2006, 65:831-844.
39. Kimura K., Takeda A., Uchida T.A. Changes in progesterone concentrations in the Japanese long-fingered bat, Miniopterus schreibersii fuliginosus. J. Reprod. Fertil. 1987, 80:59-63.
40. Krishna A. Reproductive delays in chiropterans. Topics in Endocrinology and Reproduction 1999, 410-421. Narosa Publishing House, India. K.P. Joy (Ed.).
41. Krishna A., Dominic C.J. Reproduction in the female short-nosed fruit bat Cynopterus sphinx (Vahl). Period. Biol. 1983, 85:23-30.
42. Krishna A., Abhilasha Proliferative activity of follicles and serum steroid concentration in Scotophilus heathi (vespertilionid bat) during periods of delayed ovulation. Can. J. Zool. 2000, 78:1301-1308.
43. Laughlin G.A., Morales A.J., Yen S.C. Serum leptin levels in women with Polycystic Ovary Syndrome: the role of insulin resistance/hyperinsulinemia. J. Clin. Endocrinol. Metab. 1997, 82:1692-1696.
44. Lin J., Barb C.R., Matteri R.L., Kraeling R.R., Chen X., Meinersmann R.J., Rampacek G.B. Long form leptin receptor mRNA expression in the brain, pituitary, and other tissues in the pig. Domest. Anim. Endocrinol. 2000, 19:53-61.
45. Lin Q., Poon S.L., Chen J., Cheng L., Yuen B.H., Leung P.C.K. Leptin interferes with 3',5'-Cyclic Adenosine Monophosphate (cAMP) signaling to inhibit steroidogenesis in human granulosa cells. Reprod. Biol. Endocrin. 2009, 7:115.
46. Lopes F.L., Desmarais J.A., Murphy B.D. Embryonic diapause and its regulation. Reproduction 2004, 128:669-678.
47. Maffei M., Halaas J., Ravussin E., Pratley R.E., Lee G.H., Zhang Y., Fei H., Kim S., Lallone R., Ranganathan S., Kern P.A., Friedman J.M. Leptin levels in human and rodent: measurement of plasma leptin and ob RNA in obese and weight-reduced subjects. Nat. Med. 1995, 1:1155-1161.
48. Matsuoka T., Tahara M., Yokoi T., Masumoto N., Takeda T., Yamaguchi M., Tasaka K., Kurachi H., Murata Y. Tyrosine phosphorylation of STAT3 by leptin through leptin receptor in mouse metaphase 2 stage oocyte. Biochem. Biophys. Res. Commun. 1999, 256:480-484.
49. Mathews M.B., Bernstein R.M., Franza B.R., Garrels J.I. Identity of the proliferating cell nuclear antigen and cyclin. Nature (Lond.) 1984, 303:374-376.
50. Mead R.A. Embryonic diapause in vertebrates. J. Exp. Zool. 1993, 266:629-641.
51. Meenakumari K.J., Krishna A. Delayed embryonic development in the Indian short-nosed fruit bat, Cynopterus sphinx. Zoology (Jena) 2005, 108(2):131-140.
52. Meenakumari K.J., Banerjee A., Krishna A. Luteal cell steroidogenesis in relation to delayed embryonic development in the Indian short-nosed fruit bat, Cynopterus sphinx. Zoology (Jena) 2009, 112:151-159.
53. Racey P.A. Ecology of bat reproduction. Ecology of Bats 1982, 57-104. Plenum press, New York and London. T.H. Kunz (Ed.).
54. Rasweiler J.J., Badwaik N.K. Delayed development in the short-tailed fruit bat, Carollia perspicillata. J. Reprod. Fertil. 1997, 109:7-20.
55. Rodríguez A., Fortuño A., Gómez-Ambrosi J., Zalba G., Díez J., Frühbeck G. The inhibitory effect of leptin on angiotensin ii-induced vasoconstriction in vascular smooth muscle cells is mediated via a nitric oxide-dependent mechanism endocrinology. Endocrinology 2007, 148(1):324-331.
56. Rosselli M., Keller P.J., Dubey R.K. Role of nitric oxide in the biology, physiology and pathophysiology of reproduction. Hum. Reprod. Update 1998, 4:3-24.
57. Ruiz-Cortés Z.T., Martel-Kennes Y., Gevery N.Y., Downey B.R., Palin M.F., Murphy B.D. Biphasic effects of leptin in porcine granulosa cells. Biol. Reprod. 2003, 68:789-796.
58. Ruiz-Cortés Z.T., Men T., Palin M.F., Downey B.R., Lacroix D.A., Murphy B.D. Porcine leptin receptor: molecular structure and expression in the ovary. Mol. Reprod. Dev. 2000, 56:465-474.
59. Salzmann C., Otis M., Long H., Roberge C., Gallo-Payet N., Walker C.D. Inhibition of steroidogenic response to adrenocorticotropin by leptin: implications for the adrenal response to maternal separation in neonatal rats. Endocrinology 2004, 145:1810-1822.
60. Sastry K.V.H., Moudgal R.P., Mohan J., Tyagi J.S., Rao G.S. Spectrophotometric determination of serum nitrite and nitrate by copper-cadmium alloy. Anal. Biochem. 2002, 306:79-82.
61. Schulz L.C., Widmaier E.P. The effect of leptin on mouse trophoblast cell invasion. Biol. Reprod. 2004, 71:1963-1967.
62. Singh U.P., Krishna A., Bhatnagar K.P. Changes in serum leptin, insulin, androstenedione and luteinizing hormone during ovarian cycle in bat, Taphozous longimanus. Acta Biol. Hung. 2008, 59:1-16.
63. Spicer L.J., Chamberlain C.S., Francisco C.C. Ovarian action of leptin: effects on insulin-like growth factor-I-stimulated function of granulosa and thecal cells. Endocrine 2000, 12:53-59.
64. Spicer L.J., Francisco C.C. Adipose obese gene product, leptin, inhibits bovine ovarian thecal cell steroidogenesis. Biol. Reprod. 1998, 58:207-212.
65. Srivastava R.K., Krishna A. Adiposity associated rise in leptin impairs ovarian activity during winter dormancy in Vespertilionid bat, Scotophilus heathi. Reproduction 2007, 133:165-176.
66. Swain J.E., Dunn R.L., McConnell D., Martinez J.G., Smith G.D. Direct effects of leptin on mouse reproductive function: regulation of follicular, oocyte and embryo development. Biol. Reprod. 2004, 71:1446-1452.
67. Tamanini C., Basini G., Grasselli F., Tirelli M. Nitric oxide and the ovary. J. Anim. Sci. 2003, 81:E1-E7.
68. van der Merwe M., van Aarde R.J. Plasma progesterone concentrations in the female Natal clinging bat (Miniopterus schreibersii). J. Reprod. Fertil. 1989, 87:665-669.
69. Wade-Smith J., Richmond M.E., Mead R.A., Taylor M. Hormonal and gestational evidence for delayed implantation in the striped skunk, Mephitis mephitis. Gen. Comp. Endocrinol. 1980, 42:509-515.
70. Wang Y., Kuropatwinski K.K., White D.W., Hawley T.S., Hawley R.G., Tartaglia L.A., Baumann H. Leptin receptor action in hepatic cells. J. Biol. Chem. 1997, 272:16216-16223.
71. Zachow R.J., Magoffin D.A. Direct intraovarian effects of leptin: impairment of the synergistic action of insulin-like growth factor-I on follicle-stimulating hormone-dependent estradiol-17 beta production by rat ovarian granulosa cells. Endocrinology 1997, 138:847-850.
72. Zachow R.J., Weitsman S.R., Magoffin D.A. Leptin impairs the synergistic stimulation by transforming growth factor-ß of follicle-stimulating hormone-dependent aromatase activity and messenger ribonucleic acid expression in rat ovarian granulosa cells. Biol. Reprod. 1999, 61:1104-1109.
73. Zamorano P.L., Mahesh V.B., De Sevilla L.M., Chorich L.P., Bhat G.K., Brann D.W. Expression and localization of the leptin receptor in endocrine and neuroendocrine tissues of the rat. Neuroendocrinology 1997, 65:223-228.
74. Zerani M., Boiti C., Zampini D., Brecchia G., Dall'Aglio C., Ceccarelli P., Gobbetti A. Ob receptor in rabbit ovary and leptin in vitro regulation of corpora lutea. J. Endocrinol. 2004, 183:279-288.
75. Zhang Y., Proenca R., Maffei M., Barone M., Leopold L., Friedman J.M. Positional cloning of the mouse obese gene and its human homologue. Nature 1994, 372:425-432.