Role of the double luteinizing hormone peak, luteinizing follicles, and the secretion of inhibin for dominant follicle selection in asian elephants (Elephas maximus)

Biology of Reproduction

Volumn 85, Issue 4, 2011, Pages 714-720

  Lueders, Imke ^a   Taya, Kazuyoshi ^b,c   Watanabe, Gen ^b,c   Yamamoto, Yuki ^b,c   Yamamoto, Tatsuya ^b,c   Kaewmanee, Saroch ^b,c   Niemuller, Cheryl ^d   Gray, Charlie ^e   Streich, Wolf Jürgen ^a   Hildebrandt, Thomas B ^a  

^a LEIBNIZ INSTITUTE FOR ZOO AND WILDLIFE RESEARCH   (Germany)

^b TOKYO UNIVERSITY OF AGRICULTURE AND TECHNOLOGY   (Japan)

^c GIFU UNIVERSITY   (Japan)

^d Kingfisher International Inc   (Canada)

^e African Lion Safari   (Canada)

Author keywords

Corpus luteum; Estrous cycle; Follicle; Inhibin; Ovulation; Progesterone progesterone receptor

Indexed keywords

INHIBIN; LUTEINIZING HORMONE; PROGESTERONE;

ANOVULATION; ARTICLE; ECHOGRAPHY; ELEPHANT; ELEPHAS MAXIMUS; FEMALE; FOLLICULAR PHASE; GRANULOSA CELL; HORMONE BLOOD LEVEL; HORMONE RELEASE; LUTEAL PHASE; LUTEINIZATION; LUTEINIZING HORMONE RELEASE; NONHUMAN; OVARY FOLLICLE; OVARY FOLLICLE DEVELOPMENT; OVULATION; PRIORITY JOURNAL; PROGESTERONE RELEASE;

ANIMALS; CORPUS LUTEUM; ELEPHANTS; ESTROUS CYCLE; FEMALE; FOLLICULAR PHASE; GRANULOSA CELLS; INHIBINS; LUTEINIZATION; LUTEINIZING HORMONE; ORGAN SIZE; OVARIAN FOLLICLE; OVARY; OVULATION DETECTION; PROGESTERONE;

ELEPHANTIDAE; ELEPHAS MAXIMUS; MAMMALIA;

EID: 80955123830     PISSN: 00063363     EISSN: 15297268     Source Type: Journal    
DOI: 10.1095/biolreprod.110.090167     Document Type: Article

References (50)

1. Lueders I, Niemuller C, Gray C, Rich P, Hildebrandt TB. Luteogenesis during the estrous cycle in Asian elephants (Elephas maximus). Reproduction 2010; 140:777-786.
2. Plotka ED, Sael US, Zarembka FR, Simmons LG, Teare A, Phillips LG, Hinshaw KC. Ovarian function in the elephant: luteinizing hormone and progesterone cycles in African and Asian elephants. Biol Reprod 1988; 38:309-314.
3. Brown JL, Schmitt DJ, Bellem A, Graham LH, Lehnhardt J. Hormone secretion in the Asian elephant (Elephas maximus): characterization of ovulatory and anovulatory luteinizing hormone surges. Biol Reprod 1999; 61:1294-1299.
4. Brown JL, Citino SB, Bush M, Lehnhardt J, Phillips LG. Cyclic patterns of luteinizing hormone, follicle-stimulating hormone, inhibin, and progesterone secretion in the Asian elephant (Elephas maximus). J Zoo Wildl Med 1991; 22:49-57.
5. Czekala NM, MacDonald EA, Steinman K, Walker S, Garrigues NW II, Olson D, Brown JL. Estrogen and LH dynamics during the follicular phase of the estrous cycle in the Asian elephant. Zoo Biol 2003; 22:443-454.
6. Kapustin N, Critser JK, Olson D, Malven PV. Nonluteal estrous cycles of 3-week duration are initiated by anovulatory luteinizing hormone peaks in African elephants. Biol Reprod 1996; 55:1147-1154.
7. Hermes R, Olson D, Goeritz F, Brown JL, Schmitt DL, Hagan D, Peterson JS, Fritsch G, Hildebrandt TB. Ultrasonography of the sexual cycle in female African elephants (Loxodonta africana). Zoo Biol 2000; 19:369-382.
8. Hildebrandt TB, Goeritz F, Hermes R, Reid C, Dehnhard M, Brown JL. Aspects of the reproductive biology and breeding management of Asian and African elephants Elephas maximus and Loxodonta africana. International Zoo Yearbook 2006; 40:20-40.
9. Knight PG, Glister C. Potential local regulatory functions of inhibins, activins and follistatin in the ovary. Reproduction 2001; 121:503-512.
10. Knight PG. Roles of inhibins, activins and follistatin in the female reproductive system. Front Neuroendocrinol 1996; 17:476-509.
11. Mather JP, Moore A, Li RH. Activins, inhibins and follistatins: further thoughts on a growing family of regulators. Proc Soc Exp Biol Med 1997; 215:209-222.
12. Brown JL. Reproductive endocrine monitoring of elephants: an essential tool for assisting captive management. Zoo Biol 2000; 19:347-367.
13. Kaewmanee S, Watanabe G, Kishimoto M, Jin WZ, Yamamoto Y, Yamamoto T, Arushima E, Komiya T, Taya K. Secretion of inhibin during the estrous cycle in the female Asian elephant (Elephas maximus). J Vet Med Sci 2011; 73:77-82.
14. Nambo Y, Nagaoka K, Tanaka Y, Nagamine N, Shinbo H, Nagata S, Yoshihara T, Watanabe G, Groome NP, Taya K. Mechanisms responsible for increase in circulating inhibin levels at the time of ovulation in mares. Theriogenology 2002; 57:1707-1717.
15. Medan MS, Nambo Y, Nagamine N, Shinbo H, Watanabe G, Groome N, Taya K. Plasma concentrations of ir-inhibin, inhibin A, inhibin proalphaC, FSH, and estradiol-17β during the estrous cycle in mares and their relationship with follicular growth. Endocrine 2004; 25:7-14.
16. Kaneko H, Noguchi J, Kikuchi K, Todoroki J, Hasegawa Y. Alterations in peripheral concentrations of inhibin A in cattle studied using a time- resolved immunofluorometric assay: relationship with estradiol and follicle-stimulating hormone in various reproductive conditions. Biol Reprod 2002; 67:38-45.
17. Watanabe G, Taya K, Sasamoto S. Dynamics of ovarian inhibin secretion during the estrous cycle of the rat. J Endocrinol 1990; 126:151-157.
18. Tsonis CG, Baird DT, Campbell BK, Leask R, Scaramuzzi RJ. The sheep corpus luteum secretes inhibin. J Endocrinol 1988; 116:R3-R5.
19. Shimizu K, Kojima C, Kondo M, Jin WZ, Ito M, Watanabe G, Groome NP, Taya K. Circulating inhibin A and inhibin B in normal menstrual cycle during breeding seasons of Japanese monkeys. J Reprod Dev 2002; 48:355-361.
20. Groome NP, Illingworth PJ, O'Brien M, Pai R, Rodger FE, Mather JP, McNeilly AS. Measurement of dimeric inhibin B throughout the human menstrual cycle. J Clin Endocrinol Metab 1996; 81:1401-1405.
21. Taya K. Secretion of gonadal inhibin and steroid hormones in the elephant. In: EU-Asia Link Project Symposium, 2007: Managing the Health and Reproduction of Elephant Populations in Asia. Bangkok, Thailand: Faculty of Veterinary Medicine, Kasetsart University; 2007:106-113.
22. Hildebrandt TB, Goeritz F, Pratt NC, Brown JL, Montali RJ, Schmitt DL, Fritsch G, Hermes R. Ultrasonography of the urogenital tract in elephants (Loxodonta africana and Elephas maximus): an important tool for assessing female reproductive function. Zoo Biol 2000; 19:321-332.
23. Graham L, Schwarzenberger F, Moestl E, Galama W, Savage A. A versatile enzyme immunoassay for the determination of progestogens in feces and serum. Zoo Biol 2001; 20:227-236.
24. Szdzuy K, Dehnhard M, Strauss G, Eulenberger K, Hofer H. Behavioral and endocrinological parameters of female African and Asian elephants (Loxodonta africana and Elephas maximus) in the peripartal period. International Zoo Yearbook 2006; 40:41-50.
25. Dahl NJ, Olson D, Schmitt DL, Blasko DR, Kristipati RS, Roser JF. Development of an enzyme-linked immunosorbent assay (ELISA) for luteinizing hormone (LH) in the elephant (Loxodonta africana and Elephas maximus). Zoo Biol 2004; 23:65-78.
26. Matteri RL, Roser JF, Baldwin DM, Lipovetsky V, Papkoff H. Characterization of a monclonal antibody, which detects luteinizing hormone from diverse mammalian species. Domest Anim Endocrinol 1987; 4:157-165.
27. Hamada T, Watanabe G, Kokuho T, Taya K, Sasamoto S, Hasegawa Y, Miyamoto K, Igarashi M. Radioimmunoassay of inhibin in various mammals. J Endocrinol 1989; 122:697-704.
28. Taya K. Roles of inhibin in regulation of FSH secretion and folliculogenesis in mammals. Curr Trends Exp Endocrinol 1993; 1:97-116.
29. Taya K, Watanabe G. Inhibin as a key hormone in determining species- specific ovulation rates in mammals. In: Kwon HB, Joss JMP, Ishii S (eds.), Recent Progress in Molecular and Comparative Endocrinology. Kwangju, Korea: Hormone Research Center, Chonman National University; 1999:134-143
30. Kishi H, Ohshima K, Itoh M, Tsukada J, Arai KY, Nakano S, Watanabe G, Taya K. Changes in expression of inhibin subunits in the cyclic golden hamster (Mesocricetus auratus) and the regulation of inhibin α subunit production by luteinizing hormone. Zool Sci 2002; 19:225-232.
31. Kenny HA, Woodruff TK. Follicle size class contributes to distinct secretion patterns of inhibin isoforms during the rat estrous cycle. Endocrinology 2006; 147:51-60.
32. Bernard DJ, Woodruff TK. Inhibin binding protein in rats: alternative transcripts and regulation in the pituitary across the estrous cycle. Mol Endocrinol 2001; 15:654-667.
33. Arai KY, Ohshima K, Watanabe G, Arai K, Uehara K, Taya K. Dynamics of messenger RNAs encoding inhibin/activin subunits and follistatin in the ovary during the rat estrous cycle. Biol Reprod 2002; 66:1119-1126.
34. Kastelic JP, Bergfelt DR, Ginther OJ. Relationship between ultrasonic assessment of the corpus luteum and plasma progesterone concentrations in heifers. Theriogenology 1990; 33:1269-1278.
35. de Bulnes G, Moreno JS, Brunet AG, Sebastian AL. Relationship between ultrasonographic assessment of the corpus luteum and plasma progesterone concentration during the estrous cycle in monovular ewes. Reprod Domest Anim 2000; 35:65-68.
36. Lueders I, Hildebrandt, TB, Pootoolal J, Rich P, Gray C, Niemuller C. Ovarian ultrasonography correlated with fecal progestins and estradiol during the estrous cycle and early pregnancy in giraffes (Giraffa camelopardalis rothschildi). Biol Reprod 2009; 81:989-995.
37. Ginther OJ, Gastal EL, Gastal MO, Utt MD, Beg MA. Luteal blood flow and progesterone production in mares. Anim Reprod Sci 2007; 99:213-220.
38. Hunter MG. Characteristics and causes of the inadequate corpus luteum. J Reprod Fertil Suppl 1991; 43:91-99.
39. Lueders I, Niemuller C, Pootoolal J, Rich P, Gray C, Streich WJ, Hildebrandt TB. Sonomorphology of the reproductive tract in male and pregnant and nonpregnant female Rothschild's giraffe (Giraffa camelopardis rotschildi). Theriogenology 2009; 72:22-31.
40. Mais V, Cetel NS, Muse KN, Quigley ME, Reid RL, Yen SSC. Hormonal dynamics during luteal-follicular transition. J Clin Endocrinol Metab 1987; 64:1109-1114.
41. Hodges KJ, Heistermann M, Beard A, van Aarde RJ. Concentrations of progesterone and the 5α-reduced progestins, 5α-pregnane-3, 20-dione and 3a-hydroxy-5α -pregnan-20-one, in luteal tissue and circulating blood and their relationship to luteal function in the African elephant, Loxodonta africana. Biol Reprod 1997; 56:640-646.
42. Campbell BK, McNeilly AS, Mann GE, Baird DT. The effect of stage of estrous cycle and follicular maturation on ovarian inhibin production in sheep. Biol Reprod 1991; 44:483-490.
43. Mann GE, McNeilly AS, Baird DT. Hormone production in vivo and in vitro from follicles at different stages of the estrous cycle in the sheep. Int J Endocrinol 1992; 132:225-234.
44. Thitaram C, Pongsopawijit P, Chansitthiwet S, Brown JL, Nimtragul K, Boonprasert K, Homkong P, Mahasawangkul A, Rojanasthien R, Colenbrander B, van der Weijden GC, van Eerdenburg FJCM. Induction of the ovulatory LH surge in Asian elephants (Elephas maximus): a novel aid in captive breeding management of an endangered species. Reprod Fertil Dev 2009; 21:672-678.
45. Hanks J, Short RV. The formation and function of the corpus luteum in the African elephant (Loxodonta africana). J Reprod Fertil 1972; 29:79-89.
46. Allen WR. Ovulation, pregnancy, placentation and husbandry in the African elephant (Loxodonta africana). Philos Trans R Soc Lond B Biol Sci 2006; 361:821-834.
47. Bernard DJ, Chapman SC, Woodruff TK. Mechanisms of inhibin signal transduction. Recent Prog Horm Res 2001; 56:417-450.
48. Schwall R, Schmelzer CH, Matsuyama E, Mason AJ. Multiple actions of recombinant activin-A in vivo. Endocrinology 1989; 125:1420-1423.
49. Nakamura M, Minegishi T, Hasegawa Y, Nakamura K, Igarashi S, Ito I, Shinozaki H, Miyamoto K, Eto Y, Ibuki Y. Effect of an activin A on follicle-stimulating hormone (FSH) receptor messenger ribonucleic acid levels and FSH receptor expression in cultured rat granulosa cells. Endocrinology 1993; 133:538-544.
50. Woodruff TK, D'Agostino J, Schwartz NB, Mayo KE. Dynamic changes in inhibin messenger RNAs in rat ovarian follicles during the reproductive cycle. Science 1988; 239:1296-1299.