Patterns of Pulsatile and Surge Modes of Follicle-Stimulating Hormone Treated with Different Progesterone Levels in Ovariectomized Goats

난소제거된 Shiba 염소에서 다른 농도의 Progesterone 처치에 의한 FSH Surge 및 Pulse 분비에 미치는 영향

  • Kim, Seung-Joon (Department of Veterinary Clinical Reproduction, College of Veterinary Medicine, Kyungpook National University) ;
  • Tanaka, Tomomi (Laboratory of Veterinary Reproduction, Tokyo University of Agriculture and Technology) ;
  • Kamomae, Hideo (Laboratory of Veterinary Reproduction, Tokyo University of Agriculture and Technology)
  • 김승준 (경북대학교 수의과대학 수의임상번식학교실) ;
  • ;
  • Accepted : 2011.04.07
  • Published : 2011.04.30

Abstract

The objective of the present study was to determine the progesterone levels that effects on the pulsatile and surge modes of FSH secretion. In previous studies we have shown that LH surge occurred in the follicular levels of progesterone, whereas there was no surge mode secretion of LH in either the sub luteal or luteal levels of progesterone. LH pulsatile frequencies were high in two groups such as follicular level and sub luteal level. But in the luteal level of progesterone the pulsatile pattern of LH were strongly suppressed. Namely, sub luteal levels of progesterone, around 1 ng/ml, completely suppressed the LH surge but did not affect the pulsatile frequency of LH secretion. Because of this we hypothesized that the two secretory patterns of FSH are similar to that of LH. Long-term ovariectomized Shiba goats that had received implants of estradiol capsules and three different progesterone silastic packet inducing follicular, subluteal and luteal levels of progesterone were divided into three groups such as non-P, low-P and high-P group. Blood samples were collected daily throughout the experiment for the analysis of gonadal steroid hormone levels and at 10-min intervals for 8 h on Days 0, 3, and 7 (Day 0: just before progesterone treatment) for analysis of the pulsatile frequency of FSH secretion. Then estradiol was infused into the jugular vein of all animals at a rate of 3 ${\mu}/h$ for 16 h on Day 8 to determine whether an FSH surge was induced. Blood samples were collected every 2 h from 4 h before the start of the estradiol infusion until 48 h after the start of the infusion. In each group, the mean ${\pm}$ SEM concentration after progesterone implant treatment was 3.3 ${\pm}$ 0.1 ng/ml for the high P group, 1.1 ${\pm}$ 0.1 ng/ml for the low P group, and < 0.1 ng/ml for the non-P group, concentrations similar to the luteal levels, subluteal levels, and follicular phase levels of the normal estrous cycle, respectively. The FSH pulse frequency was maintained highly in all groups on Day 0, Day 3 and Day 7. An FSH surge was induced in all 4 cases of the Non-P group. In the High P and Low P groups, the plasma concentrations of FSH remained low until 48 h after the start of estradiol infusion, and no occurrence of FSH surge was found in any of the animals. The results of this study not only confirm that the pulsatile patterns of FSH were not inhibited strongly relative to LH, they also suggest that some other mechanism and factor may be controlling the FSH secretion.

본 연구의 목적은 FSH 분비 조절에 있어서 각각 다른 progesterone (P) 농도가 Pulse 또는 Surge 형태의 분비 패턴에 어떤 영향을 미치는가를 탐구한다. 선행된 연구에서 LH surge는 난포기 (follicular phase)에서 보이는 P 농도에서만 발현되었고 황체기(luteal phase) 또는 아황체기(subluteal phase) P 농도에서는 완전히 억제되었다. 또한 LH pulse 분비는 황체기 P농도에서만 시간 의존적으로 감소되었으나 난포기 또는 아황체기 농도에서는 높은 빈도로 유지되었다. 즉 아황체기 P농도 (스트레스, 황체형성부전에서 발생)는 LH surge는 억제시키나 LH pulse 조절에는 아무런 영향을 마치지 않았다. 이 결과를 바탕으로 FSH surge 및 pulse 분비패턴을 알아보기 위해 난소가 제거된 Shiba 염소를 이용하여 인위적으로 난포기, 아황체기, 기능성황체기의 P 농도 및 estradiol(E) 농도를 유도하였다. 스테로이드 호르몬 농도의 변화를 알아보기 위해 매일 혈액을 채취하였으며, LH pulse 용 혈액은 10분 간격으로 8시간 동안 Day 0, Day 3, Day 7 (Day 0: P packet 이식 직전)에 연속채혈을 실시하고, LH surge 분비패턴은 Day 8에 16시간 estradiol를 3 ${\mu}g/h$ 농도로 주사하고, 52시간 동안 2시간 간격으로 채혈을 실시했다. 그 결과 유도된 P 농도는 염소의 정상적 발정주기에서 볼 수 있는 난포기(<0.1 ng/ml), 아황체기($1.1{\pm}0.1$ ng/ml), 황체기 ($3.3{\pm0.1}$ ng/ml) 수준의 농도로 유도되었다. FSH pulse 분비는 3그룹에서 모두 높은 빈도로 유지되었고, FSH surge는 LH surge와 같은 시간대에서 난포기 그룹에서만 확인되었다. 본 연구의 결과는 FSH pulse는 LH pulse에서 보이는 progesterone에 의한 억제 효과와 다르게 나타났으며, 이러한 결과는 FSH 분비 조절에 있어서 LH 분비와 다른 기전 및 요소들이 관여하는 것으로 판단되었다.

Keywords

References

  1. Araki K, Arai KY, Watanabe G, Taya K. Involvement of inhibin in the regulation of follicle-stimulating hormone secretion in the young adult male Shiba goat. Andrology 2000; 21: 558-565.
  2. Baird DT, Campbell BK, Mann GE, McNeilly AS. Inhibin and oestradiol in the control of FSH secretion in the sheep. J Reprod Fertil Suppl 1991; 43: 125-138.
  3. Baird DT, Swanston I, Scaramuzzi RJ. Pulsatile release of LH and secretion of ovarian steroids in sheep during the luteal phase of the estrous cycle. Endocrinology 1975; 98: 1490-1496.
  4. Clarke IJ, Cummins JT. The temporal relationship between gonadotropin releasing hormone (GnRH) and luteinizing hormone (LH secretion in ovariectomized ewes. Endocrinology 1982; 111: 1737-1739. https://doi.org/10.1210/endo-111-5-1737
  5. DePaolo LY. Hypersecretion of follicle-stimulating hormone (FSH) after ovariectomy of hypophysectomized, pituitary-grafted rats: implications for local regulatory control of FSH. Endocrinology 1991; 128: 1731-1740. https://doi.org/10.1210/endo-128-4-1731
  6. DePaolo L V, Bicsak TA, Erickson GF, Shimasaki S, Ling N. (1991). Follistatin and activin: a potential intrinsic regulatory system within diverse tissues. Proc Soc Exp Biol Med 1991; 198: 500-512.
  7. Dobson H. Plasma gonadotropins and oestradiol during oestrus in the cow. J Reprod Fertil 1978; 52: 51-53. https://doi.org/10.1530/jrf.0.0520051
  8. Evans AC, Komar CM, Wandji SA, Fortune JE. Changes in androgen secretion and luteinizing hormone pulse amplitude are associated with the recruitment and growth of ovarian follicles during the luteal phase of the bovine estrous cycle. Biol Reprod 1997; 57: 394-401 https://doi.org/10.1095/biolreprod57.2.394
  9. Gharib SD, Wierman ME, Shupnik MA, Chin WW. Molecular biology of the pituitary gonadotropins. Endocr Rev 1990; 11 177-199. https://doi.org/10.1210/edrv-11-1-177
  10. Goodman RL, Bittman EL, Foster DL, Karsch FJ. The endocrine basis of the synergistic suppression of luteinizing hormone by estradiol and progesterone. Endocrinology 1981; 109: 1414-1417. https://doi.org/10.1210/endo-109-5-1414
  11. Goodman RL, Karsch FJ. Pulsatile secretion of luteinizing hormone: Differential suppression by ovarian steroids. Endocrinology 1980; 107: 1286-1290. https://doi.org/10.1210/endo-107-5-1286
  12. Hall JE, Whitcomb RW, Rivier JE, Vale WW, Crowley WFJ. Differential regulation of luteinizing hormone, follicle-stimulating hormone, and free alpha-subunit secretion from the gonadotroph by gonadtropin-releasing hormone (GnRH): evidence from the use of two GnRH antagonists. J Clin Endocrinol Meta 1990; 70: 328-325. https://doi.org/10.1210/jcem-70-2-328
  13. Igarashi M, McCarm SM. A hypothalamic follicle stimulating hormone releasing factor. Endocrinology 1964; 74: 446-452. https://doi.org/10.1210/endo-74-3-446
  14. Imakawa K, Day ML, Zalesky DD, Garcia-Winder M, Kittok RJ, Kinder JE. (1986). Regulation of pulsatile LH secretion by ovarian steroids in the heifer. J Anim Sci 1986; 63: 162-168.
  15. Karsch FJ, Cummins JT, Thomas GB, Clarke IJ. Steroid feedback inhibition of pulsatile secretion of gonadotropin-releasing hormone in the ewe. Biol Reprod 1987; 36: 1207-1218. https://doi.org/10.1095/biolreprod36.5.1207
  16. Karsch FJ, Dahl GE, Evans NP, Manning JM, Mayfield KP, Moenter SM, Foster DL. Seasonal changes in gonadotropin-releasing hormone secretion in the ewe: alteration in response to the negative feedback action of estradiol. Biol Reprod 1993; 49: 1377-1383. https://doi.org/10.1095/biolreprod49.6.1377
  17. Kim S, Tanaka T, Kamomae H. Different effects of subnormal levels of progesterone on the pulsatile and surge mode secretion of luteinizing hormone in ovariectomized goats. Biol Reprod 2003; 69: 141-145. https://doi.org/10.1095/biolreprod.102.013532
  18. Kimura F, Funabashi T. Two subgroups of gonadotropin releasing hormone neurons control gonadotropin secretion in rats. News Physiol Sci 1998; 13: 225-231.
  19. Lamperti A, HiII L. The effects of anterior hypothalamic deafferentation on FSH-releasing activity in the intact female hamster. Exp Brain Res 1987: 68: 189-194.
  20. Lumpkin MD, McCann SM. Effect of destruction of the dorsal anterior hypothalamus on follicle-stimulating hormone secretion in the rat. Endocrinology 1984; 115: 2473-2480. https://doi.org/10.1210/endo-115-6-2473
  21. Lumpkin MD, McDonald JK, Samson WK, McCann SM. Destruction of the dorsal anterior hypothalamic region suppresses pulsatile release of follicle stimulating hormone but not luteinizing hormone. Neuroendocrinology 1989; 50: 229-235. https://doi.org/10.1159/000125227
  22. Martin GB, Price CA, Thiery JC, Webb R. lnteractions between inhibin, estradiol and progesterone in the control of gonadotropin secretion in the ewe. J Reprod Fertil 1988; 82: 319-328. https://doi.org/10.1530/jrf.0.0820319
  23. Mizunuma H, Samson WK, Lumpkin MD, McCann SM. Evidence for an FSH-releasing factor in the posterior portion of the rat median eminence. Life Sci 1983; 33: 2003-2009. https://doi.org/10.1016/0024-3205(83)90739-7
  24. Mori Y, Kano Y. Changes in plasma concentrations of LH, progesterone and oestradiol in relation to the occurrence of luteolysis, oestrous and time of ovulation in the Shiba goat (Capra hircus). J Reprod Fertil 1984; 72: 223-230. https://doi.org/10.1530/jrf.0.0720223
  25. Kano Y, Mori Y. The Shia goat. In: Suzuki Y (eds.), Mammalian Reproductive Physiology: Aspects of Its Animal Experimentation [in Japanese]. Tolyo: Soft Science Co; 1982: 367-379.
  26. Nanda AS, Ward WR, Dobson H. Effect of endogenous and exogenous progesterone on the oestradiol-induced LH surge in dairy cows. J Reprod Fertil 1988; 84: 367-371. https://doi.org/10.1530/jrf.0.0840367
  27. Nishihara M, Takeuchi Y, Tanaka T, Mori Y. Electrophy-siological correlates of pulsatile and surge gonadotropin secretion. Rev Reprod 1999; 4: 110-116. https://doi.org/10.1530/ror.0.0040110
  28. Orita J, Tanaka T, Kamomae H, Kaneda Y. Utrasonographic observation of follicular and luteal dynamics during the estrous cycle in Shiba goats. J Reprod Dev 2000; 46: 31-37. https://doi.org/10.1262/jrd.46.31
  29. Padmanabhan V, Battaglia D, Brown MB, Karsch FJ, Lee JS, Pan W, Phillips DJ, Cleeff J V. Neuroendocrine control of follicle-stimulating hormone (FSH) secretion: II. Is follistatin-induced suppression of FSH secretion mediated via changes in activin availability and does it involve changes in gonadotropin-releasing hormone secretion? Biol Reprod 2002; 66: 1395-1402. https://doi.org/10.1095/biolreprod66.5.1395
  30. Padmanabhan V, Mcfadden K, Mauger D T, Karsch FJ, Midgley ARJ. Neuroendocrine control of follicle-stimulating hormone (FSH) secretion. I. Direct evidence for separate episodic and basal components of FSH secretion. Endocrinology 1997; 138: 424-432. https://doi.org/10.1210/en.138.1.424
  31. Padmanabhan V, McNeilly AS. Is there an FSH-releasing factor? Reproduction 2001; 121: 21-30. https://doi.org/10.1530/rep.0.1210021
  32. Padmanabhan V, Sharma TP. Neuroendocrine vs. paracrine control of follicle-stimulating hormone. Arch Med Res 2001; 32: 533-543. https://doi.org/10.1016/S0188-4409(01)00318-6
  33. Pincus S M, Padmanabhan V, Lemon W, Randolph J, Midgley AR. Follicle-stimulating hormone is secreted more irregularly than luteinizing hormone in both human and sheep. J Clin Invest 1998: 101: 1318-1324. https://doi.org/10.1172/JCI985
  34. Price CA, Wcbb R. Steroid control of gonadotropin secretion and ovarian function in heifers. Endocrinology 1998; 122: 2222-2231.
  35. Roche JF, lreland JJ. The differential effect of progesterone on concentrations of luteinizing hormone and follicle-stimulating hormone in heifers. Endocrinology 1981: 108: 568-572. https://doi.org/10.1210/endo-108-2-568
  36. Skinner DC, Evans NP, Delaleu B, Goodman RL, Bouchard P, Caraty A. The negative feedback actions of progesterone on gonadotropin-releasing hormone secretion are transduced by the classical progesterone receptor. Proc Natl Acad Sci 1998; 95: 10978-10983. https://doi.org/10.1073/pnas.95.18.10978
  37. Strobl FJ, Levine JE. Estrogen inhibits luteinizing hormone (LH), but not follicle-stimulating hormone secretion in hypophysectomized pituitary-grafted rats receiving pulsatile LH-releasing hormone infusions. Endocrinology 1988; 123: 622-630. https://doi.org/10.1210/endo-123-1-622
  38. Stumpf TT, Day ML, Wolfe MW, Clutter AC, Stotts JA, Wolfe PL, Kittok RJ, Kinder JE. Effect of estradiol on secretion of luteinizing hormone during the follicular phase of the bovine estrous cycle. Biol Reprod 1989; 40: 91-97.
  39. Tanaka, T, Akaboshi N, Inoue Y, Kamomae H, Kaneda Y. Fasting-induced suppression of pulsatile luteinizing hormone secretion is related to body energy status in ovariectomized goats. Anim Reprod Sci 2002; 72: 185-196. https://doi.org/10.1016/S0378-4320(02)00091-X
  40. Tanaka T, Mori Y, Hoshino K. Hypothalamic GnRH pulse generator activity during the estradiol-induced LH surge in ovariectomized goats. Neuroendocrinology 1992; 56: 641-645. https://doi.org/10.1159/000126287
  41. Tanaka T, Mori Y, Hoshino K. Long-term recording of hypothalamic GnRH pulse generator activity during programmed administration of progesterone and estradiol in the ovariectomized goat. J Reprod Fertil 1994; 40: 183-188.
  42. Tanaka T, Ozawa T, Hoshino K, Mori Y. Changes in the gonadotropin-releasing hormone pulse generator activity during the estrous cycle in the goat. Neuroendocrinology 1995; 62: 553-591 https://doi.org/10.1159/000127051
  43. Taya K, Watanabe G, Sasamoto S. Radioimmunoassay for progesterone, testosterone and estradiol-17 beta using 125I-iodohistamine radioligands [in Japanese]. Jpn J Anim Reprod 1985; 31: 186-196. https://doi.org/10.1262/jrd1977.31.186
  44. Veldhuis JD, Johnson ML. Cluster analysis: a simple, versatile, and robust algorithm for endocrine pulse detection. Am J Physiol; 250: E 486-493.
  45. Walters DL, Schallenberger E. Pulsatile secretion of gonadotrophins, ovarian steroids and ovarian oxytocin during the periovulatory phase of the oestrous cycle in the cow. J Reprod Fertil 1984; 71: 503-512. https://doi.org/10.1530/jrf.0.0710503
  46. Walters D L, Schams D, Schallenberger E. Pulsatile secretion of gonadotrophins, ovarian steroids and ovarian oxytocin during the luteal phase of the oestrous cycle in the cow. J Reprod Fertil 1984; 71: 479-491. https://doi.org/10.1530/jrf.0.0710479
  47. Wu FCW, Irby DC, Clarke IJ, Cummins JT, de Kretser DM. Effects of gonadotropin-releasing hormone pulse-frequency modulation on luteinizing hormone, follicle-stimulating hormone and testosterone secretion in hypothalamo/pituitary-disconnected rams. Biol Reprod 1987; 37: 501-510. https://doi.org/10.1095/biolreprod37.3.501
  48. Ying SY. Inhibins, actvins, and follistatins: gonadal proteins modulating the secretion of follicle-stimulating hormone. Endocr Rev 1988; 9: 267-293. https://doi.org/10.1210/edrv-9-2-267