Kisspeptin Signaling Is Required for the Luteinizing Hormone Response in Anestrous Ewes following the Introduction of Males

PLoS ONE

Volumn 8, Issue 2, 2013, Pages

  De Bond, Julie Ann P ^a   Li, Qun ^a   Millar, Robert P ^b,c,d   Clarke, Iain J ^a   Smith, Jeremy T ^a,e  

^a MONASH UNIVERSITY   (Australia)

^b UNIVERSITY OF PRETORIA   (South Africa)

^c UNIVERSITY OF CAPE TOWN   (South Africa)

^d UNIVERSITY OF EDINBURGH   (United Kingdom)

^e UNIVERSITY OF WESTERN AUSTRALIA   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

GONADORELIN; KISSPEPTIN; LUTEINIZING HORMONE; NEUROKININ B; PROTEIN FOS;

ANESTRUS; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HORMONE RELEASE; HORMONE RESPONSE; HYPOTHALAMUS; KISS1 GENE; LUTEINIZING HORMONE BLOOD LEVEL; MALE; NERVE CELL; NEUROKININ B GENE; NONHUMAN; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; SPECIES INTRODUCTION; STIMULUS RESPONSE;

ANIMALS; ARCUATE NUCLEUS; ESTROUS CYCLE; FEMALE; GENE EXPRESSION REGULATION; GONADOTROPIN-RELEASING HORMONE; KISSPEPTINS; LUTEINIZING HORMONE; MALE; NEURONS; PEPTIDES; PREOPTIC AREA; RNA, MESSENGER; SHEEP; SIGNAL TRANSDUCTION; TACHYKININS;

EID: 84874572420     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0057972     Document Type: Article

References (59)

1. Crown A, Clifton DK, Steiner RA, (2007) Neuropeptide signaling in the integration of metabolism and reproduction. Neuroendocrinology 86: 175-182.
2. Clarke IJ, (2011) Control of GnRH secretion: one step back. Front Neuroendocrinol 32: 367-375.
3. Schnickel PG, (1954) The effect of the ram on the incidence and occurrence of oestrus in ewes. The Australian Veterinary Journal 30: 189-195.
4. Jansen HT, Iwamoto GA, Jackson GL, (1998) Central connections of the ovine olfactory bulb formation identified using wheat germ agglutinin-conjugated horseradish peroxidase. Brain Res Bull 45: 27-39.
5. Keller M, Baum MJ, Brock O, Brennan PA, Bakker J, (2009) The main and the accessory olfactory systems interact in the control of mate recognition and sexual behavior. Behav Brain Res 200: 268-276.
6. Delgadillo JA, Gelez H, Ungerfeld R, Hawken PA, Martin GB, (2009) The 'male effect' in sheep and goats-revisiting the dogmas. Behav Brain Res 200: 304-314.
7. Gelez H, Fabre-Nys C, (2006) Neural pathways involved in the endocrine response of anestrous ewes to the male or its odor. Neuroscience 140: 791-800.
8. Murata K, Wakabayashi Y, Sakamoto K, Tanaka T, Takeuchi Y, et al. (2011) Effects of brief exposure of male pheromone on multiple-unit activity at close proximity to kisspeptin neurons in the goat arcuate nucleus. J Reprod Dev 57: 197-202.
9. Okamura H, Murata K, Sakamoto K, Wakabayashi Y, Ohkura S, et al. (2010) Male effect pheromone tickles the gonadotrophin-releasing hormone pulse generator. J Neuroendocrinol 22: 825-832.
10. Ohkura S, Takase K, Matsuyama S, Mogi K, Ichimaru T, et al. (2009) Gonadotrophin-releasing hormone pulse generator activity in the hypothalamus of the goat. J Neuroendocrinol 21: 813-821.
11. Wakabayashi Y, Nakada T, Murata K, Ohkura S, Mogi K, et al. (2010) 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 30: 3124-3132.
12. Bakker J, Pierman S, Gonzalez-Martinez D, (2010) Effects of aromatase mutation (ArKO) on the sexual differentiation of kisspeptin neuronal numbers and their activation by same versus opposite sex urinary pheromones. Horm Behav 57: 390-395.
13. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, et al. (2003) Hypogonadotropic hypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci U S A 100: 10972-10976.
14. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, Acierno JS Jr, et al. (2003) The GPR54 gene as a regulator of puberty. N Engl J Med 349: 1614-1627.
15. Gottsch ML, Cunningham MJ, Smith JT, Popa SM, Acohido BV, et al. (2004) A role for kisspeptins in the regulation of gonadotropin secretion in the mouse. Endocrinology 145: 4073-4077.
16. Smith JT, Li Q, Yap KS, Shahab M, Roseweir AK, et al. (2011) Kisspeptin is essential for the full preovulatory LH surge and stimulates GnRH release from the isolated ovine median eminence. Endocrinology 152: 1001-1012.
17. Estrada KM, Clay CM, Pompolo S, Smith JT, Clarke IJ, (2006) 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 18: 806-809.
18. Franceschini I, Lomet D, Cateau M, Delsol G, Tillet Y, et al. (2006) Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor alpha. Neurosci Lett 401: 225-230.
19. Smith JT, Clay CM, Caraty A, Clarke IJ, (2007) KiSS-1 messenger ribonucleic acid expression in the hypothalamus of the ewe is regulated by sex steroids and season. Endocrinology 148: 1150-1157.
20. Smith JT, Coolen LM, Kriegsfeld LJ, Sari IP, Jaafarzadehshirazi MR, et al. (2008) Variation in kisspeptin and RFamide-related peptide (RFRP) expression and terminal connections to gonadotropin-releasing hormone neurons in the brain: a novel medium for seasonal breeding in the sheep. Endocrinology 149: 5770-5782.
21. Smith JT, Li Q, Pereira A, Clarke IJ, (2009) Kisspeptin neurons in the ovine arcuate nucleus and preoptic area are involved in the preovulatory luteinizing hormone surge. Endocrinology 150: 5530-5538.
22. Smith JT, (2008) Kisspeptin signalling in the brain: steroid regulation in the rodent and ewe. Brain Res Rev 57: 288-298.
23. Smith JT, (2009) Sex steroid control of hypothalamic Kiss1 expression in sheep and rodents: comparative aspects. Peptides 30: 94-102.
24. Clarke IJ, Smith JT, Caraty A, Goodman RL, Lehman MN, (2009) Kisspeptin and seasonality in sheep. Peptides 30: 154-163.
25. Wagner GC, Johnston JD, Clarke IJ, Lincoln GA, Hazlerigg DG, (2008) Redefining the limits of day length responsiveness in a seasonal mammal. Endocrinology 149: 32-39.
26. Caraty A, Smith JT, Lomet D, Ben Said S, Morrissey A, et al. (2007) Kisspeptin synchronizes preovulatory surges in cyclical ewes and causes ovulation in seasonally acyclic ewes. Endocrinology 148: 5258-5267.
27. Li Q, Roa A, Clarke IJ, Smith JT (2012) Seasonal Variation in the Gonadotropin-Releasing Hormone Response to Kisspeptin in Sheep: Possible Kisspeptin Regulation of the Kisspeptin Receptor. Neuroendocrinology.
28. Goodman RL, Lehman MN, Smith JT, Coolen LM, de Oliveira CV, et al. (2007) Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B. Endocrinology 148: 5752-5760.
29. Lehman MN, Coolen LM, Goodman RL, (2010) Minireview: kisspeptin/neurokinin B/dynorphin (KNDy) cells of the arcuate nucleus: a central node in the control of gonadotropin-releasing hormone secretion. Endocrinology 151: 3479-3489.
30. Roseweir AK, Kauffman AS, Smith JT, Guerriero KA, Morgan K, et al. (2009) Discovery of potent kisspeptin antagonists delineate physiological mechanisms of gonadotropin regulation. J Neurosci 29: 3920-3929.
31. Pineda R, Garcia-Galiano D, Roseweir A, Romero M, Sanchez-Garrido MA, et al. (2010) Critical roles of kisspeptins in female puberty and preovulatory gonadotropin surges as revealed by a novel antagonist. Endocrinology 151: 722-730.
32. Lee VW, Cumming IA, de Kretser DM, Findlay JK, Hudson B, et al. (1976) Regulation of gonadotrophin secretion in rams from birth to sexual maturity. I. Plasma LH, FSH and testosterone levels. J Reprod Fertil 46: 1-6.
33. Li Q, Rao A, Pereira A, Clarke IJ, Smith JT, (2011) Kisspeptin cells in the ovine arcuate nucleus express prolactin receptor but not melatonin receptor. J Neuroendocrinol 23: 871-882.
34. Martin GB, Scaramuzzi RJ, Oldham CM, Lindsay DR, (1983) Effects of progesterone on the responses of Merino ewes to the introduction of rams during anoestrus. Aust J Biol Sci 36: 369-378.
35. Cohen-Tannoudji J, Einhorn J, Signoret JP, (1994) Ram sexual pheromone: first approach of chemical identification. Physiol Behav 56: 955-961.
36. Hawken PA, Esmaili T, Scanlan V, Blache D, Martin GB, (2009) Can audio-visual or visual stimuli from a prospective mate stimulate a reproductive neuroendocrine response in sheep? Animal 3: 690-696.
37. Jorre de St Jorre T, Hawken PA, Martin GB, (2012) Role of male novelty and familiarity in male-induced LH secretion in female sheep. Reprod Fertil Dev 24: 523-530.
38. Chanvallon A, Blache D, Chadwick A, Esmaili T, Hawken PA, et al. (2010) Sexual experience and temperament affect the response of Merino ewes to the ram effect during the anoestrous season. Anim Reprod Sci 119: 205-211.
39. Buck LB, (2000) The molecular architecture of odor and pheromone sensing in mammals. Cell 100: 611-618.
40. Brennan PA, Keverne EB, (2004) Something in the air? New insights into mammalian pheromones. Curr Biol 14: R81-89.
41. Hawken PA, Martin GB, (2012) Sociosexual stimuli and gonadotropin-releasing hormone/luteinizing hormone secretion in sheep and goats. Domest Anim Endocrinol 43: 85-94.
42. Hawken PA, Jorre TJ, Rodger J, Esmaili T, Blache D, et al. (2009) Rapid induction of cell proliferation in the adult female ungulate brain (Ovis aries) associated with activation of the reproductive axis by exposure to unfamiliar males. Biol Reprod 80: 1146-1151.
43. d'Anglemont de Tassigny X, Fagg LA, Carlton MB, Colledge WH, (2008) Kisspeptin can stimulate gonadotropin-releasing hormone (GnRH) release by a direct action at GnRH nerve terminals. Endocrinology 149: 3926-3932.
44. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, et al. (2005) Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 25: 11349-11356.
45. Herbison AE, de Tassigny X, Doran J, Colledge WH, (2010) Distribution and postnatal development of Gpr54 gene expression in mouse brain and gonadotropin-releasing hormone neurons. Endocrinology 151: 312-321.
46. Scott CJ, Tilbrook AJ, Simmons DM, Rawson JA, Chu S, et al. (2000) The distribution of cells containing estrogen receptor-alpha (ERalpha) and ERbeta messenger ribonucleic acid in the preoptic area and hypothalamus of the sheep: comparison of males and females. Endocrinology 141: 2951-2962.
47. Navarro VM, Gottsch ML, Chavkin C, Okamura H, Clifton DK, et al. (2009) Regulation of gonadotropin-releasing hormone secretion by kisspeptin/dynorphin/neurokinin B neurons in the arcuate nucleus of the mouse. J Neurosci 29: 11859-11866.
48. Sakamoto K, Murata K, Wakabayashi Y, Yayou KI, Ohkura S,et al. (2012) Central Administration of Neurokinin B Activates Kisspeptin/NKB Neurons in the Arcuate Nucleus and Stimulates Luteinizing Hormone Secretion in Ewes During the Non-Breeding Season. J Reprod Dev.
49. Billings HJ, Connors JM, Altman SN, Hileman SM, Holaskova I, et al. (2010) Neurokinin B acts via the neurokinin-3 receptor in the retrochiasmatic area to stimulate luteinizing hormone secretion in sheep. Endocrinology 151: 3836-3846.
50. Grachev P, Li XF, Kinsey-Jones JS, di Domenico AL, Millar RP, et al. (2012) Suppression of the GnRH Pulse Generator by Neurokinin B Involves a kappa-Opioid Receptor-Dependent Mechanism. Endocrinology 153: 4894-4904.
51. Kinsey-Jones JS, Grachev P, Li XF, Lin YS, Milligan SR, et al. (2012) The inhibitory effects of neurokinin B on GnRH pulse generator frequency in the female rat. Endocrinology 153: 307-315.
52. Hrabovszky E, Sipos MT, Molnar CS, Ciofi P, Borsay BA, et al. (2012) Low Degree of Overlap Between Kisspeptin, Neurokinin B, and Dynorphin Immunoreactivities in the Infundibular Nucleus of Young Male Human Subjects Challenges the KNDy Neuron Concept. Endocrinology 153: 4978-4989.
53. Ruiz-Pino F, Navarro VM, Bentsen AH, Garcia-Galiano D, Sanchez-Garrido MA, et al. (2012) Neurokinin B and the control of the gonadotropic axis in the rat: developmental changes, sexual dimorphism, and regulation by gonadal steroids. Endocrinology 153: 4818-4829.
54. Hoffman GE, Le WW, Franceschini I, Caraty A, Advis JP, (2011) Expression of fos and in vivo median eminence release of LHRH identifies an active role for preoptic area kisspeptin neurons in synchronized surges of LH and LHRH in the ewe. Endocrinology 152: 214-222.
55. Lindsay DR, Cognie Y, Pelletier J, Signoret JP, (1975) Influence of the presence of rams on the timing of ovulation and discharge of LH in ewes. Physiol Behav 15: 423-426.
56. Sebert ME, Lomet D, Said SB, Monget P, Briant C, et al. (2010) 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 38: 289-298.
57. Lehman MN, Robinson JE, Karsch FJ, Silverman AJ, (1986) Immunocytochemical localization of luteinizing hormone-releasing hormone (LHRH) pathways in the sheep brain during anestrus and the mid-luteal phase of the estrous cycle. J Comp Neurol 244: 19-35.
58. Polkowska J, Dubois MP, Domanski E, (1980) Immunocytochemistry of luteinizing hormone releasing hormone (LHRH) in the sheep hypothalamus during variuos reproductive stages: correlation with the gonadotropic hormones of the pituitary. Cell Tissue Res 208: 327-341.
59. Boukhliq R, Goodman RL, Berriman SJ, Adrian B, Lehman MN, (1999) A subset of gonadotropin-releasing hormone neurons in the ovine medial basal hypothalamus is activated during increased pulsatile luteinizing hormone secretion. Endocrinology 140: 5929-5936.