Kisspeptin and the preovulatory gonadotrophin-releasing hormone/luteinising hormone surge in the ewe: Basic aspects and potential applications in the control of ovulation

Journal of Neuroendocrinology

Volumn 22, Issue 7, 2010, Pages 710-715

  Caraty, A ^a   Franceschini, I ^a   Hoffman, G E ^b  

^a UMR85 PHYSIOLOGIE DE LA REPRODUCTION ET DES COMPORTEMENTS   (France)

^b MORGAN STATE UNIVERSITY   (United States)

Author keywords

GnRH; Kisspeptin; LH surge; Oestrogen; Ovulation

Indexed keywords

ESTRADIOL; ESTROGEN; ESTROGEN RECEPTOR ALPHA; FOLLITROPIN; G PROTEIN COUPLED RECEPTOR; GONADORELIN; KISSPEPTIN; KISSPEPTIN 10; LUTEINIZING HORMONE; MESSENGER RNA; NEUROKININ; NEUROTRANSMITTER; PROGESTERONE; SOMATOSTATIN; TESTOSTERONE; TUMOR SUPPRESSOR PROTEIN;

ARCUATE NUCLEUS; ARTIFICIAL INSEMINATION; CELL ACTIVATION; DOWN REGULATION; ESTROGEN RELEASE; ESTRUS CYCLE; EWE; FEEDBACK SYSTEM; FEMALE; FOLLICULAR PHASE; GENE EXPRESSION; GONADORELIN RELEASE; HORMONAL REGULATION; HORMONE ACTION; HYPOTHALAMUS; LUTEINIZING HORMONE RELEASE; MENSTRUAL CYCLE; NEGATIVE FEEDBACK; NONHUMAN; OVARIECTOMY; OVULATION; OVULATION INDUCTION; PREOPTIC AREA; PRIORITY JOURNAL; PUBERTY; REPRODUCTION; REVIEW; STEROIDOGENESIS; TRANSCRIPTION INITIATION; ANIMAL; METABOLISM; PHYSIOLOGY; SECRETION; SHEEP;

ANIMALS; ESTROGENS; FEMALE; GONADOTROPIN-RELEASING HORMONE; LUTEINIZING HORMONE; OVULATION; SHEEP; TUMOR SUPPRESSOR PROTEINS;

EID: 77954149875     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2010.02022.x     Document Type: Review

References (51)

1. Knobil E. Discovery of the hypothalamic gonadotropin-releasing hormone pulse generator and of its physiologic significance. 1992. Am J Obstet Gynecol 2005, 193:1765-1766.
2. Sarkar DK, Chiappa SA, Fink G, Sherwood NM. Gonadotropin-releasing hormone surge in pro-oestrous rats. Nature 1976, 264:461-463.
3. Clarke IJ, Cummins JT, Jenkin M, Phillips DJ. The oestrogen-induced surge of LH requires a 'signal' pattern of gonadotrophin-releasing hormone input to the pituitary gland in the ewe. J Endocrinol 1989, 122:127-134.
4. Moenter SM, Caraty A, Locatelli A, Karsch FJ. Pattern of gonadotropin-releasing hormone (GnRH) secretion leading up to ovulation in the ewe: existence of a preovulatory GnRH surge. Endocrinology 1991, 129:1175-1182.
5. Xia L, Van Vugt D, Alston EJ, Luckhaus J, Ferin M. A surge of gonadotropin-releasing hormone accompanies the estradiol-induced gonadotropin surge in the rhesus monkey. Endocrinology 1992, 131:2812-2820.
6. Goodman RL, Karsch FJ. Pulsatile secretion of luteinizing hormone: differential suppression by ovarian steroids. Endocrinology 1980, 107:1286-1290.
7. Clarke IJ. GnRH and ovarian hormone feedback. Oxf Rev Reprod Biol 1987, 9:54-95. Review
8. Skinner DC, Caraty A, Allingham R. Unmasking the progesterone receptor in the preoptic area and hypothalamus of the ewe: no colocalization with gonadotropin-releasing neurons. Endocrinology 2001, 142:573-579.
9. Lehman MN, Ebling FJ, Moenter SM, Karsch FJ. Distribution of estrogen receptor-immunoreactive cells in the sheep brain. Endocrinology 1993, 133:876-886.
10. Evans NP, Dahl GE, Padmanabhan V, Thrun LA, Karsch FJ. Estradiol requirements for induction and maintenance of the gonadotropin-releasing hormone surge: implications for neuroendocrine processing of the estradiol signal. Endocrinology 1997, 138:5408-5414.
11. Blache D, Fabre-Nys CJ, Venier G. Ventromedial hypothalamus as a target for oestradiol action on proceptivity, receptivity and luteinizing hormone surge of the ewe. Brain Res 1991, 546:241-249.
12. Caraty A, Fabre-Nys C, Delaleu B, Locatelli A, Bruneau G, Karsch FJ, Herbison A. Evidence that the mediobasal hypothalamus is the primary site of action of estradiol in inducing the preovulatory gonadotropin releasing hormone surge in the ewe. Endocrinology 1998, 139:1752-1760.
13. Pillon D, Caraty A, Fabre-Nys C, Lomet D, Cateau M, Bruneau G. Regulation by estradiol of hypothalamic somatostatin gene expression: possible involvement of somatostatin in the control of luteinizing hormone secretion in the ewe. Biol Reprod 2004, 71:38-44.
14. Pillon D, Caraty A, Fabre-Nys C, Bruneau G. Early decrease of proopiomelanocortin but not neuropeptide Y mRNA expression in the mediobasal hypothalamus of the ewe, during the estradiol-induced preovulatory LH surge. Gen Comp Endocrinol 2004, 134:264-272.
15. Pillon D, Caraty A, Fabre-Nys C, Bruneau G. Short-term effect of oestradiol on neurokinin B mRNA expression in the infundibular nucleus of ewes. J Neuroendocrinol 2003, 15:749-753.
16. Richter TA, Robinson JE, Lozano JM, Evans NP. Progesterone can block the preovulatory gonadotropin-releasing hormone/luteinising hormone surge in the ewe by a direct inhibitory action on oestradiol-responsive cells within the hypothalamus. J Neuroendocrinol 2005, 17:161-169.
17. Clarke IJ, Pompolo S, Scott CJ, Rawson JA, Caddy D, Jakubowska AE, Pereira AM. Cells of the arcuate nucleus and ventromedial nucleus of the ovariectomized ewe that respond to oestrogen: a study using Fos immunohistochemistry. J Neuroendocrinol 2001, 13:934-941.
18. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E. Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA 2003, 100:10972-10976.
19. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS, Shagoury JK, Bo-Abbas Y, Kuohung W, Schwinof KM, Hendrick AG, Zahn D, Dixon J, Kaiser UB, Slaugenhaupt SA, Gusella JF, O'Rahilly S, Carlton MB, Crowley WF, Aparicio SA, Colledge WH. The GPR54 gene as a regulator of puberty. N Engl J Med 2003, 349:1614-1627.
20. Tena-Sempere M. GPR54 and kisspeptin in reproduction. Hum Reprod Update 2006, 12:631-639. Review
21. Messager S, Chatzidaki EE, Ma D, Hendrick AG, Zahn D, Dixon J, Thresher RR, Malinge I, Lomet D, Carlton MB, Colledge WH, Caraty A, Aparicio SA. Kisspeptin directly stimulates gonadotropin-releasing hormone release via G protein-coupled receptor 54. Proc Natl Acad Sci USA 2005, 102:1761-1766.
22. Oakley AE, Clifton DK, Steiner RA. Kisspeptin signaling in the brain. Endocr Rev 2009, 30:713-743.
23. Franceschini I, Lomet D, Cateau M, Delsol G, Tillet Y, Caraty A. Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor alpha. Neurosci Lett 2006, 401:225-230.
24. Smith JT, Cunningham MJ, Rissman EF, Clifton DK, Steiner RA. Regulation of Kiss1 gene expression in the brain of the female mouse. Endocrinology 2005, 146:3686-3692.
25. Lee DK, Nguyen T, O'Neill GP, Cheng R, Liu Y, Howard AD, Coulombe N, Tan CP, Tang-Nguyen AT, George SR, O'Dowd BF. Discovery of a receptor related to the galanin receptors. FEBS Lett 1999, 446:103-107.
26. Irwig MS, Fraley GS, Smith JT, Acohido BV, Popa SM, Cunningham MJ, Gottsch ML, Clifton DK, Steiner RA. Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 2004, 80:264-272.
27. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE. Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 2005, 25:11349-11356.
28. Kinoshita M, Tsukamura H, Adachi S, Matsui H, Uenoyama Y, Iwata K, Yamada S, Inoue K, Ohtaki T, Matsumoto H, Maeda K. Involvement of central metastin in the regulation of preovulatory luteinizing hormone surge and estrous cyclicity in female rats. Endocrinology 2005, 146:4431-4436.
29. Clarkson J, Herbison AE. Postnatal development of kisspeptin neurons in mouse hypothalamus; sexual dimorphism and projections to gonadotropin-releasing hormone neurons. Endocrinology 2006, 147:5817-5825.
30. Smith JT. Sex steroid control of hypothalamic Kiss1 expression in sheep and rodents: comparative aspects. Peptides 2009, 30:94-102.
31. Smith JT, Popa SM, Clifton DK, Hoffman GE, Steiner RA. Kiss1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge. J Neurosci 2006, 26:6687-6694.
32. Herbison AE. Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: the case for the rostral periventricular area of the third ventricle (RP3V). Brain Res Rev 2008, 57:277-287.
33. Gottsch ML, Clifton DK, Steiner RA. Kisspeptin-GPR54 signaling in the neuroendocrine reproductive axis. Mol Cell Endocrinol 2006, 255:91-96.
34. Kauffman AS, Gottsch ML, Roa J, Byquist AC, Crown A, Clifton DK, Hoffman GE, Steiner RA, Tena-Sempere M. Sexual differentiation of Kiss1 gene expression in the brain of the rat. Endocrinology 2007, 148:1774-1783.
35. Pompolo S, Pereira A, Estrada KM, Clarke IJ. Colocalization of kisspeptin and gonadotropin-releasing hormone in the ovine brain. Endocrinology 2006, 147:804-810.
36. Smith JT, Clay CM, Caraty A, Clarke IJ. KiSS-1 messenger ribonucleic acid expression in the hypothalamus of the ewe is regulated by sex steroids and season. Endocrinology 2007, 148:1150-1157.
37. Estrada KM, Clay CM, Pompolo S, Smith JT, Clarke IJ. Elevated KiSS-1 expression in the arcuate nucleus prior to the cyclic preovulatory gonadotropin-releasing hormone/luteinising hormone surge in the ewe suggests a stimulatory role for kisspeptin in oestrogen-positive feedback. J Neuroendocrinol 2006, 18:139-149.
38. Smith JT, Li Q, Pereira A, Clarke IJ. Kisspeptin neurons in the ovine arcuate nucleus and preoptic area are involved in the preovulatory luteinizing hormone surge. Endocrinology 2009, 150:5530-5538.
39. Conover CD, Kuljis RO, Rabii J, Advis JP. Beta-endorphin regulation of luteinizing hormone-releasing hormone release at the median eminence in ewes: immunocytochemical and physiological evidence. Neuroendocrinology 1993, 57:1182-1195.
40. Moenter SM, Karsch FJ, Lehman MN. Fos expression during the estradiol-induced gonadotropin-releasing hormone (GnRH) surge of the ewe: induction in GnRH and other neurons. Endocrinology 1993, 133:896-903.
41. Cheng G, Coolen LM, Padmanabhan V, Goodman RL, Lehman MN. The kisspeptin/neurokinin B/dynorphin (KNDy) cell population of the arcuate nucleus: sex differences and effects of prenatal testosterone in sheep. Endocrinology 2010, 151:301-311.
42. Matsui H, Takatsu Y, Kumano S, Matsumoto H, Ohtaki T. Peripheral administration of metastin induces marked gonadotropin release and ovulation in the rat. Biochem Biophys Res Commun 2004, 320:383-388.
43. Ritar AJ, Maxwell WM, Salamon S. Ovulation and LH secretion in the goat after intravaginal progestagen sponge-PMSG treatment. J Reprod Fertil 1984, 72:559-563.
44. Caraty A, Smith JT, Lomet D, Ben Said S, Morrissey A, Cognie J, Doughton B, Baril G, Briant C, Clarke IJ. Kisspeptin synchronizes preovulatory surges in cyclical ewes and causes ovulation in seasonally acyclic ewes. Endocrinology 2007, 148:5258-5267.
45. Dhillo WS, Chaudhri OB, Thompson EL, Murphy KG, Patterson M, Ramachandran R, Nijher GK, Amber V, Kokkinos A, Donaldson M, Ghatei MA, Bloom SR. Kisspeptin-54 stimulates gonadotropin release most potently during the preovulatory phase of the menstrual cycle in women. J Clin Endocrinol Metab 2007, 92:3958-3966.
46. Sébert ME, Lomet D, Saïd SB, Monget P, Briant C, Scaramuzzi RJ, Caraty A. Insights into the mechanism by which kisspeptin stimulates a preovulatory LH surge and ovulation in seasonally acyclic ewes: potential role of estradiol. Domest Anim Endocrinol 2010, 38:289-298.
47. Richard N, Galmiche G, Corvaisier S, Caraty A, Kottler ML. KiSS-1 and GPR54 genes are co-expressed in rat gonadotrophs and differentially regulated in vivo by oestradiol and gonadotrophin-releasing hormone. J Neuroendocrinol 2008, 20:381-393.
48. Ben Said S, Lomet D, Chesneau D, Lardic L, Canepa S, Guillaume D, Briant C, Fabre-Nys C, Caraty A. Differential estradiol requirement for the induction of estrus behaviour and the luteinizing hormone surge in two breeds of sheep. Biol Reprod 2007, 76:673-680.
49. Lahlou-Kassi A, Schams D, Glatzel P. Plasma gonadotrophin concentrations during the oestrous cycle and after ovariectomy in two breeds of sheep with low and high fecundity. J Reprod Fertil 1984, 70:165-173.
50. Castellano JM, Gaytan M, Roa J, Vigo E, Navarro VM, Bellido C, Dieguez C, Aguilar E, Sánchez-Criado JE, Pellicer A, Pinilla L, Gaytan F, Tena-Sempere M. Expression of KiSS-1 in rat ovary: putative local regulator of ovulation? Endocrinology 2006, 147:4852-4862.
51. Wakabayashi Y, Nakada T, Murata K, Ohkura S, Mogi K, Navarro VM, Clifton DK, Mori Y, Tsukamura H, Maeda K, Steiner RA, Okamura H. Neurokinin B and dynorphin A in kisspeptin neurons of the arcuate nucleus participate in generation of periodic oscillation of neural activity driving pulsatile gonadotropin-releasing hormone secretion in the goat. J Neurosci 2010, 24:3124-3132.