Seasonal and cyclical change in the luteinizing hormone response to kisspeptin in the Ewe

Neuroendocrinology

Volumn 90, Issue 3, 2009, Pages 283-291

  Smith, Jeremy T ^a   Saleh, Sofie N H ^a   Clarke, Iain J ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

KiSS 1; Kiss1; Metastin; Reproduction

Indexed keywords

GONADORELIN; GROWTH HORMONE; HYDROCORTISONE; KISSPEPTIN 10; LUTEINIZING HORMONE; MESSENGER RNA; PROLACTIN;

ANIMAL EXPERIMENT; ARTICLE; BREEDING; CONTROLLED STUDY; ESTRUS CYCLE; EWE; FEMALE; FOLLICULAR PHASE; GONADOTROPIN RELEASE; HORMONE RESPONSE; HYPOTHALAMUS; LUTEAL PHASE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; SEASONAL VARIATION;

ANESTRUS; ANIMALS; ESTROUS CYCLE; FEMALE; FOLLICLE STIMULATING HORMONE; GONADOTROPIN-RELEASING HORMONE; GROWTH HORMONE; HYDROCORTISONE; LUTEINIZING HORMONE; MICE; OLIGOPEPTIDES; PERIODICITY; PROLACTIN; RADIOIMMUNOASSAY; SEASONS; SHEEP;

EID: 70350294317     PISSN: 00283835     EISSN: None     Source Type: Journal    
DOI: 10.1159/000227806     Document Type: Article

References (50)

1. Kotani M, Detheux M, Vandenbogaerde A, Communi D, Vanderwinden JM, Le Poul E, Brezillon S, Tyldesley R, Suarez-Huerta N, Vandeput F, Blanpain C, Schiffmann SN, Vassart G, Parmentier M: The metastasis suppressor gene KiSS-1 encodes kisspeptins, the natural ligands of the orphan G proteincoupled receptor GPR54. J Biol Chem 2001; 276: 34631-34636.
2. Muir AI, Chamberlain L, Elshourbagy NA, Michalovich D, Moore DJ, Calamari A, Szekeres PG, Sarau HM, Chambers JK, Murdock P, Steplewski K, Shabon U, Miller JE, Middleton SE, Darker JG, Larminie CG, Wilson S, Bergsma DJ, Emson P, Faull R, Philpott KL, Harrison DC: AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. J Biol Chem 2001; 276: 28969-28975.
3. Ohtaki T, Shintani Y, Honda S, Matsumoto H, Hori A, Kanehashi K, Terao Y, Kumano S, Takatsu Y, Masuda Y, Ishibashi Y, Watanabe T, Asada M, Yamada T, Suenaga M, Kitada C, Usuki S, Kurokawa T, Onda H, Nishimura O, Fujino M: Metastasis suppressor gene KiSS-1 encodes peptide ligand of a G-protein-coupled receptor. Nature 2001; 411: 613-617.
4. 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.
5. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS Jr, 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 Jr, Aparicio SA, Colledge WH: The GPR54 gene as a regulator of puberty. N Engl J Med 2003; 349: 1614-1627.
6. Dhillo WS, Chaudhri OB, Patterson M, Thompson EL, Murphy KG, Badman MK, McGowan BM, Amber V, Patel S, Ghatei MA, Bloom SR: Kisspeptin-54 stimulates the hypothalamic-pituitary gonadal axis in human males. J Clin Endocrinol Metab 2005; 90: 6609-6615.
7. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, Crowley WF, Seminara S, Clifton DK, Steiner RA: A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 2004; 145: 4073-4077.
8. 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.
9. 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.
10. Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM: Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci USA 2005; 102: 2129-2134.
11. 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.
12. Arreguin-Arevalo JA, Lents CA, Farmerie TA, Nett TM, Clay CM: KiSS-1 peptide induces release of LH by a direct effect on the hypothalamus of ovariectomized ewes. Anim Reprod Sci 2007; 101: 265-275.
13. Smith JT, Rao A, Pereira A, Caraty A, Millar RP, Clarke IJ: Kisspeptin is present in ovine hypophysial portal blood but does not increase during the preovulatory luteinizing hormone surge: evidence that gonadotropes are not direct targets of kisspeptin in vivo. Endocrinology 2008; 149: 1951-1959.
14. Karsch FJ, Robinson JE, Woodfill CJ, Brown MB: Circannual cycles of luteinizing hormone and prolactin secretion in ewes during prolonged exposure to a fixed photoperiod: evidence for an endogenous reproductive rhythm. Biol Reprod 1989; 41: 1034-1046.
15. 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.
16. 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.
17. Smith JT, Clarke IJ: Kisspeptin expression in the brain: catalyst for the initiation of puberty. Rev Endocr Metab Disord 2007; 8: 1-9.
18. Gutierrez-Pascual E, Martinez-Fuentes AJ, Pinilla L, Tena-Sempere M, Malagon MM, Castano JP: Direct pituitary effects of kisspeptin: activation of gonadotrophs and somatotrophs and stimulation of luteinising hormone and growth hormone secretion. J Neuroendocrinol 2007; 19: 521-530.
19. Kadokawa H, Matsui M, Hayashi K, Matsunaga N, Kawashima C, Shimizu T, Kida K, Miyamoto A: Peripheral administration of kisspeptin-10 increases plasma concentrations of growth hormone as well as luteinizing hormone in prepubertal Holstein heifers. J Endocrinol 2008; 196: 331-334.
20. Cumming IA, Brown JM, Goding JR, Bryant GD, Greenwood FC: Secretion of prolactin and luteinizing hormone at oestrus in the ewe. J Endocrinol 1972; 54: 207-213.
21. Estrada KM, Pompolo S, Morris MJ, Tilbrook AJ, Clarke IJ: Neuropeptide Y (NPY) delays the oestrogen-induced luteinizing hormone (LH) surge in the ovariectomized ewe: further evidence that NPY has a predominant negative effect on LH secretion in the ewe. J Neuroendocrinol 2003; 15: 1011-1020.
22. Lee VW, Cumming IA, de Kretser DM, Findlay JK, Hudson B, Keogh EJ: Regulation of gonadotrophin secretion in rams from birth to sexual maturity. I. Plasma LH, FSH and testosterone levels. J Reprod Fertil 1976; 46: 1-6.
23. Burger HG, Lee VW, Rennie GC: A generalized computer program for the treatment of data from competitive protein-binding assays including radioimmunoassays. J Lab Clin Med 1972; 80: 302-312.
24. Thomas GB, Mercer JE, Karalis T, Rao A, Cummins JT, Clarke IJ: Effect of restricted feeding on the concentrations of growth hormone (GH), gonadotropins, and prolactin (PRL) in plasma, and on the amounts of messenger ribonucleic acid for GH, gonadotropin subunits, and PRL in the pituitary glands of adult ovariectomized ewes. Endocrinology 1990; 126: 1361-1367.
25. Bocking AD, McMillen IC, Harding R, Thorburn GD: Effect of reduced uterine blood flow on fetal and maternal cortisol. J Dev Physiol 1986; 8: 237-245.
26. 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.
27. Roa J, Vigo E, Castellano JM, Navarro VM, Fernandez-Fernandez R, Casanueva FF, Dieguez C, Aguilar E, Pinilla L, Tena-Sempere M: Hypothalamic expression of KiSS-1 system and gonadotropin-releasing effects of kisspeptin in different reproductive states of the female rat. Endocrinology 2006; 147: 2864-2878.
28. de Kretser DM, Burger HG, Dumpys R: Patterns of serum LH and FSH in response to 4-hour infusions of luteinizing hormone releasing hormone in normal women during menstrual cycle, on oral contraceptives, and in postmenopausal state. J Clin Endocrinol Metab 1978; 46: 227-235.
29. Jewelewicz R, Dyrenfurth I, Ferin M, Bogumil J, Vande Wiele RL: Gonadotropin, estrogen and progesterone response to long term gonadotropin-releasing hormone infusion at various stages of the menstrual cycle. J Clin Endocrinol Metab 1977; 45: 662-667.
30. Wollesen F, Swerdloff RS, Odell WD: LH and FSH responses to luteinizing releasing hormone in normal fertile women. Metabolism 1976; 25: 1275-1285.
31. Clarke IJ: Evidence that the switch from negative to positive feedback at the level of the pituitary gland is an important timing event for the onset of the preovulatory surge in LH in the ewe. J Endocrinol 1995; 145: 271-282.
32. Brooks J, Taylor PL, Saunders PT, Eidne KA, Struthers WJ, McNeilly AS: Cloning and sequencing of the sheep pituitary gonadotropin- releasing hormone receptor and changes in expression of its mRNA during the estrous cycle. Mol Cell Endocrinol 1993; 94:R23-R27.
33. Clarke IJ, Cummins JT: Direct pituitary effects of estrogen and progesterone on gonadotropin secretion in the ovariectomized ewe. Neuroendocrinology 1984; 39: 267-274.
34. Clarke IJ: Effects of tamoxifen on concentrations of luteinizing hormone and folliclestimulating hormone in the plasma of ovariectomized ewes. J Endocrinol 1983; 99: 23-29.
35. Radford HM, Wheatley IS, Wallace AL: The effects of oestradiol benzoate and progesterone on secretion of luteinizing hormone in the ovariectomized ewe. J Endocrinol 1969; 44: 135-136.
36. Clarke IJ: Variable patterns of gonadotropinreleasing hormone secretion during the estrogen- induced luteinizing hormone surge in ovariectomized ewes. Endocrinology 1993; 133: 1624-1632.
37. Clarke IJ, Thomas GB, Yao B, Cummins JT: GnRH secretion throughout the ovine estrous cycle. Neuroendocrinology 1987; 46: 82-88.
38. Estrada KM, Clay CM, Pompolo S, Smith JT, Clarke IJ: Elevated KiSS-1 expression in the arcuate nucleus prior to the cyclic preovulatory gonadotrophin-releasing hormone/lutenising hormone surge in the ewe suggests a stimulatory role for kisspeptin in oestrogen- positive feedback. J Neuroendocrinol 2006; 18: 806-809.
39. 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.
40. Stackpole CA, Turner AI, Clarke IJ, Lambert GW, Tilbrook AJ: Seasonal differences in the effect of isolation and restraint stress on the luteinizing hormone response to gonadotropin- releasing hormone in hypothalamopituitary disconnected, gonadectomized rams and ewes. Biol Reprod 2003; 69: 1158-1164.
41. Clarke IJ, Cummins JT: GnRH pulse frequency determines LH pulse amplitude by altering the amount of releasable LH in the pituitary glands of ewes. J Reprod Fertil 1985; 73: 425-431.
42. Lents CA, Heidorn NL, Barb CR, Ford JJ: Central and peripheral administration of kisspeptin activates gonadotropin but not somatotropin secretion in prepubertal gilts. Reproduction 2008; 135: 879-887.
43. Clarke IJ, Pompolo S: Synthesis and secretion of GnRH. Anim Reprod Sci 2005; 88: 29-55.
44. Navarro VM, Castellano JM, Fernandez-Fernandez R, Tovar S, Roa J, Mayen A, Barreiro ML, Casanueva FF, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M: Effects of KiSS-1 peptide, the natural ligand of GPR54, on follicle-stimulating hormone secretion in the rat. Endocrinology 2005; 146: 1689-1697.
45. Navarro VM, Castellano JM, Fernandez-Fernandez R, Tovar S, Roa J, Mayen A, Nogueiras R, Vazquez MJ, Barreiro ML, Magni P, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M: Characterization of the potent luteinizing hormone-releasing activity of KiSS-1 peptide, the natural ligand of GPR54. Endocrinology 2005; 146: 156-163.
46. Thompson EL, Patterson M, Murphy KG, Smith KL, Dhillo WS, Todd JF, Ghatei MA, Bloom SR: Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic- pituitary-gonadal axis. J Neuroendocrinol 2004; 16: 850-858.
47. Suzuki S, Kadokawa H, Hashizume T: Direct kisspeptin-10 stimulation on luteinizing hormone secretion from bovine and porcine anterior pituitary cells. Anim Reprod Sci 2007; 103: 360-365.
48. Kadokawa H, Suzuki S, Hashizume T: Kisspeptin-10 stimulates the secretion of growth hormone and prolactin directly from cultured bovine anterior pituitary cells. Anim Reprod Sci 2008; 105: 404-408.
49. Clarke IJ, Cummins JT, Findlay JK, Burman KJ, Doughton BW: Effects on plasma luteinizing hormone and follicle-stimulating hormone of varying the frequency and amplitude of gonadotropin-releasing hormone pulses in ovariectomized ewes with hypothalamo- pituitary disconnection. Neuroendocrinology 1984; 39: 214-221.
50. Wu FC, 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.