Male effect pheromone tickles the gonadotrophin-releasing hormone pulse generator

Journal of Neuroendocrinology

Volumn 22, Issue 7, 2010, Pages 825-832

  Okamura, H ^a   Murata, K ^a,b   Sakamoto, K ^a,b   Wakabayashi, Y ^a,b   Ohkura, S ^c   Takeuchi, Y ^b   Mori, Y ^b  

^a NATIONAL INSTITUTE OF AGROBIOLOGICAL SCIENCES   (Japan)

^b UNIVERSITY OF TOKYO   (Japan)

^c NAGOYA UNIVERSITY   (Japan)

Author keywords

GnRH pulse generator; Goat; Kisspeptin; Male effect; Pheromone

Indexed keywords

DYNORPHIN; GONADORELIN; KISSPEPTIN; LUTEINIZING HORMONE; MESSENGER RNA; NEUROKININ 3 RECEPTOR; NEUROKININ B; OPIATE RECEPTOR; PHEROMONE RECEPTOR; SEX PHEROMONE; PHEROMONE;

ANIMAL EXPERIMENT; ARCUATE NUCLEUS; BIOASSAY; BIOLOGICAL ACTIVITY; ELECTROPHYSIOLOGY; GOAT; HYPOTHALAMUS NUCLEUS; IMMUNOHISTOCHEMISTRY; IMMUNOREACTIVITY; LUTEINIZING HORMONE RELEASE; MALE; MULTIPLE UNIT ACTIVITY; NERVE CELL; NONHUMAN; OLFACTORY SYSTEM; OPTIC TRACT; PRIORITY JOURNAL; PULSATILE HORMONE RELEASE; PULSE GENERATOR; PUTAMEN; PYRIFORM CORTEX; REVIEW; SHEEP; SIGNAL PROCESSING; SIGNAL TRANSDUCTION; ACTION POTENTIAL; ANIMAL; BIOLOGICAL RHYTHM; CYTOLOGY; DRUG EFFECT; FEMALE; HUMAN; METABOLISM; OVULATION; PERIODICITY; PHYSIOLOGY;

ACTION POTENTIALS; ANIMALS; ARCUATE NUCLEUS; BIOLOGICAL CLOCKS; DYNORPHINS; ELECTROPHYSIOLOGY; FEMALE; GONADOTROPIN-RELEASING HORMONE; HUMANS; MALE; NEUROKININ B; NEURONS; OVULATION; PERIODICITY; PHEROMONES; SIGNAL TRANSDUCTION;

EID: 77954161438     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2010.02037.x     Document Type: Review

References (84)

1. Aron C. Mechanisms of control of the reproductive function by olfactory stimuli in female mammals. Physiol Rev 1979, 59:229-284.
2. Booth WJ, Signoret JP. Olfaction and reproduction in ungulates. Oxf Rev Reprod Biol 1992, 14:263-301.
3. Vandenberg JG. Pheromones and mammalian reproduction. The Physiology of Reproduction 1994, 1621-1681. Knobil ENeill JD. eds, New York, NY, Raven Press
4. Brennan PA. The vomeronasal system. Cell Mol Life Sci 2001, 58:546-555.
5. Dulac C, Torello AT. Molecular detection of pheromone signals in mammals: from genes to behaviour. Nat Rev Neurosci 2003, 4:551-562.
6. Martin GB, Oldham CM, CogniÈ Y, Pearce DT. The physiological responses of anovulatory ewes to the introduction of rams -- A review. Livest Prod Sci 1986, 15:219-247.
7. Chemineau P. Possibilities for using bucks to stimulate ovarian and oestrous cycles in anovulatory goats - a review. Livest Prod Sci 1987, 17:135-147.
8. Gelez H, Fabre-Nys C. The " male effect" in sheep and goats: a review of the respective roles of the two olfactory systems. Horm Behav 2004, 46:257-271.
9. Delgadillo JA, Gelez H, Ungerfeld R, Hawken PA, Martin GB. The 'male effect' in sheep and goats - revisiting the dogmas. Behav Brain Res 2009, 200:304-314.
10. Signoret JP, Lindsay DR. The male effect in domestic mammals: effect on LH secretion and ovulation - importance of olfactory cues. Olfaction and Endocrine Regulation 1982, 63-70. Breiphol W, ed, London, IRL Press
11. Walkden-Brown SW, Restall BJ, Henniawati S. The male effect in the Australian cashmere goat. 2. Role of olfactory cues from the male. Anim Reprod Sci 1993, 32:55-67.
12. Knight TW, Lynch PR. Source of ram pheromones that stimulate ovulation in the ewe. Anim Reprod Sci 1980, 3:133-136.
13. Claus R, Over R, Dehnhard M. Effect of male odor on LH-secretion and the induction of ovulation in seasonally anestrous goats. Anim Reprod Sci 1990, 22:27-38.
14. Knobil E. The neuroendocrine control of the menstrual cycle. Recent Prog Horm Res 1980, 36:53-88.
15. Karsch FJ. The hypothalamus and anterior pituitary gland. Reproduction in mammals: 3 Hormonal Control of Reproduction 1984, 1-20. Austin CRShort RV. eds, 2nd edn, Cambridge, Cambridge University Press
16. Lincoln DW, Fraser HM, Lincoln GA, Martin GB, McNeilly AS. Hypothalamic pulse generators. Recent Prog Horm Res 1985, 41:369-419.
17. Murata K, Wakabayashi Y, Kitago M, Ohara H, Watanabe H, Tamogami S, Warita Y, Yamagishi K, Ichikawa M, Takeuchi Y, Okamura H, Mori Y. Modulation of gonadotrophin-releasing hormone pulse generator activity by the pheromone in small ruminants. J Neuroendocrinol 2009, 21:346-350.
18. Chen MD, O'Byrne KT, Chiappini SE, Hotchkiss J, Knobil E. Hypoglycemic 'stress' and gonadotropin-releasing hormone pulse generator activity in the rhesus monkey: role of the ovary. Neuroendocrinology 1992, 56:666-673.
19. O'Byrne K, Thalabard J, Chiappini S, Chen M, Hotchkiss J, Knobil E. Ambient light modifies gonadotropin-releasing hormone pulse generator frequency in the rhesus monkey. Endocrinology 1993, 133:1520-1524.
20. 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 Dev 1994, 40:183-188.
21. Ichimaru T, Mori Y, Okamura H. A possible role of neuropeptide Y as a mediator of undernutrition to the hypothalamic gonadotropin-releasing hormone pulse generator in goats. Endocrinology 2001, 142:2489-2498.
22. Hamada T, Nakajima M, Takeuchi Y, Mori Y. Pheromone-induced stimulation of hypothalamic gonadotropin-releasing hormone pulse generator in ovariectomized, estrogen-primed goats. Neuroendocrinology 1996, 64:313-319.
23. Chemineau P. Effect on oestrus and ovulation of exposing creole goats to the male at three times of the year. J Reprod Fertil 1983, 67:65-72.
24. Cohen-Tannoudji J, Einhorn J, Signoret JP. Ram sexual pheromone: first approach of chemical identification. Physiol Behav 1994, 56:955-961.
25. Over R, Cohen-Tannoudji J, Dehnhard M, Claus R, Signoret JP. Effect of pheromones from male goats on LH-secretion in anoestrous ewes. Physiol Behav 1990, 48:665-668.
26. Mori Y, Nishihara M, Tanaka T, Shimizu T, Yamaguchi M, Takeuchi Y, Hoshino K. Chronic recording of electrophysiological manifestation of the hypothalamic gonadotropin-releasing hormone pulse generator activity in the goat. Neuroendocrinology 1991, 53:392-395.
27. Mori Y, Tanaka T. Electrophysiological approach to the hypothalamic GnRH pulse-generator. J Reprod Fertil 1995, 49:231-243.
28. Knobil E. Patterns of hypophysiotropic signals and gonadotropin secretion in the rhesus monkey. Biol Reprod 1981, 24:44-49.
29. O'Byrne KT, Knobil E. Electrophysiological analysis of GnRH pulse generator activity in the rhesus monkey. Methods in Neurosciences 20 1994, 114-126. Levine JE, ed, San Diego, CA, Academic Press
30. O'Byrne KT, Thalabard JC, Grosser PM, Wilson RC, Williams CL, Chen MD, Ladendorf D, Hotchkiss J, Knobil E. Radiotelemetric monitoring of hypothalamic gonadotropin-releasing hormone pulse generator activity throughout the menstrual cycle of the rhesus monkey. Endocrinology 1991, 129:1207-1214.
31. Kimura F, Nishihara M, Hiruma H, Funabashi T. Naloxone increases the frequency of the electrical activity of luteinizing hormone-releasing hormone pulse generator in long-term ovariectomized rats. Neuroendocrinology 1991, 53:97-102.
32. Nishihara M, Hiruma H, Kimura F. Interactions between the noradrenergic and opioid peptidergic systems in controlling the electrical activity of luteinizing hormone-releasing hormone pulse generator in ovariectomized rats. Neuroendocrinology 1991, 54:321-326.
33. Ichimaru T, Takeuchi Y, Mori Y. Stimulation of the GnRH pulse generator activity by continuous exposure to the male pheromones in the female goat. J Reprod Dev 1999, 45:243-248.
34. Iwata E, Wakabayashi Y, Kakuma Y, Kikusui T, Takeuchi Y, Mori Y. Testosterone-dependent primer pheromone production in the sebaceous gland of male goat. Biol Reprod 2000, 62:806-810.
35. Wakabayashi Y, Iwata E, Kikusui T, Takeuchi Y, Mori Y. Regional differences of pheromone production in the sebaceous glands of castrated goats treated with testosterone. J Vet Med Sci 2000, 62:1067-1072.
36. Iwata E, Wakabayashi Y, Matsuse S, Kikusui T, Takeuchi Y, Mori Y. Induction of primer pheromone production by dihydrotestosterone in the male goat. J Vet Med Sci 2001, 63:347-348.
37. Momozawa Y, Takeuchi Y, Kitago M, Masuda K, Kakuma Y, Hashizume C, Ichimaru T, Mogi K, Yonezawa T, Kikusui T, Okamura H, Mori Y. Gene expression profiles linked to the hormonal induction of male-effect pheromone synthesis in goats (Capra hircus). Biol Reprod 2007, 77:102-107.
38. Kitago M, Momozawa Y, Masuda K, Wakabayashi Y, Date-Ito A, Hagino-Yamagishi K, Kikusui T, Takeuchi Y, Mori Y. Localization of the candidate genes ELOVL5 and SCD1 for 'male effect' pheromone synthesis in goats (Capra hircus). J Reprod Dev 2007, 53:1329-1333.
39. Ichimaru T, Mogi K, Ohkura S, Mori Y, Okamura H. Exposure to ram wool stimulates gonadotropin-releasing hormone pulse generator activity in the female goat. Anim Reprod Sci 2008, 106:361-368.
40. Ohara H, Nikaido M, Date-Ito A, Mogi K, Okamura H, Okada N, Takeuchi Y, Mori Y, Hagino-Yamagishi K. Conserved repertoire of orthologous vomeronasal type 1 receptor genes in ruminant species. BMC Evol Biol 2009, 9:233.
41. Keverne EB. Pheromonal influences on the endocrine regulation of reproduction. Trends Neurosci 1983, 6:381-384.
42. Firestein S. How the olfactory system makes sense of scents. Nature 2001, 413:211-218.
43. Stowers L, Marton TF. What is a pheromone? Mammalian pheromones reconsidered. Neuron 2005, 46:699-702.
44. Wyatt TD. Fifty years of pheromones. Nature 2009, 457:262-263.
45. Dulac C, Axel R. A novel family of genes encoding putative pheromone receptors in mammals. Cell 1995, 83:195-206.
46. Matsunami H, Buck LB. A multigene family encoding a diverse array of putative pheromone receptors in mammals. Cell 1997, 90:775-784.
47. Takigami S, Mori Y, Tanioka Y, Ichikawa M. Morphological evidence for two types of mammalian vomeronasal system. Chem Senses 2004, 29:301-310.
48. Grus WE, Shi P, Zhang Y-p, Zhang J. Dramatic variation of the vomeronasal pheromone receptor gene repertoire among five orders of placental and marsupial mammals. Proc Natl Acad Sci USA 2005, 102:5767-5772.
49. Wakabayashi Y, Mori Y, Ichikawa M, Yazaki K, Hagino-Yamagishi K. A putative pheromone receptor gene is expressed in two distinct olfactory organs in goats. Chem Senses 2002, 27:207-213.
50. Gelez H, Fabre-Nys C. Neural pathways involved in the endocrine response of anestrous ewes to the male or its odor. Neuroscience 2006, 140:791-800.
51. Cohen-Tannoudji J, Lavenet C, Locatelli A, Tillet Y, Signoret JP. Non-involvement of the accessory olfactory system in the LH response of anoestrous ewes to male odour. J Reprod Fertil 1989, 86:135-144.
52. Li CS, Kaba H, Saito H, Seto K. Neural mechanisms underlying the action of primer pheromones in mice. Neuroscience 1990, 36:773-778.
53. Wakabayashi Y, Mogi K, Nakada T, Murata K, Ohkura S, Mori Y, Maeda KI, Okamura H. Kisspeptin neurons in the arcuate nucleus of goats receive neural projections from the medial nucleus of amygdala, a key nucleus for the pheromone signaling pathway. 2008, First World Conference on Kisspeptin Signaling in the Brain, Cordoba
54. Yoon H, Enquist LW, Dulac C. Olfactory inputs to hypothalamic neurons controlling reproduction and fertility. Cell 2005, 123:669-682.
55. Boehm U, Zou Z, Buck LB. Feedback loops link odor and pheromone signaling with reproduction. Cell 2005, 123:683-695.
56. Moss RL, McCann SM. Action of luteinizing hormone-releasing factor (LRF) in the initiation of lordosis behavior in the estrone-primed ovariectomized female rat. Neuroendocrinology 1975, 17:309-318.
57. Sakuma Y, Pfaff DW. Modulation of the lordosis reflex of female rats by LHRH, its antiserum and analogs in the mesencephalic central gray. Neuroendocrinology 1983, 36:218-224.
58. 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.
59. 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 MBL, Crowley WF, Aparicio SAJR, Colledge WH. The GPR54 gene as a regulator of puberty. N Engl J Med 2003, 349:1614-1627.
60. de Roux N, Genin E, Carel J-C, Matsuda F, Chaussain J-L, 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.
61. Maeda K-I, Adachi S, Inoue K, Ohkura S, Tsukamura H. Metastin/kisspeptin and control of estrous cycle in rats. Rev Endocr Metab Disord 2007, 8:21-29.
62. Oakley AE, Clifton DK, Steiner RA. Kisspeptin signaling in the brain. Endocr Rev 2009, 30:713-743.
63. Ohkura S, Uenoyama Y, Yamada S, Homma T, Takase K, Inoue N, Maeda K-i, Tsukamura H. Physiological role of metastin/kisspeptin in regulating gonadotropin-releasing hormone (GnRH) secretion in female rats. Peptides 2009, 30:49-56.
64. 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.
65. Adachi S, Yamada S, Takatsu Y, Matsui H, Kinoshita M, Takase K, Sugiura H, Ohtaki T, Matsumoto H, Uenoyama Y, Tsukamura H, Inoue K, Maeda K-I. Involvement of anteroventral periventricular metastin/kisspeptin neurons in estrogen positive feedback action on luteinizing hormone release in female rats. J Reprod Dev 2007, 53:367-378.
66. 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.
67. Smith J, Clarke I. Kisspeptin expression in the brain: catalyst for the initiation of puberty. Rev Endocr Metab Disord 2007, 8:1-9.
68. Navarro VM, Castellano JM, Fernandez-Fernandez R, Barreiro ML, Roa J, Sanchez-Criado JE, Aguilar E, Dieguez C, Pinilla L, Tena-Sempere M. Developmental and hormonally regulated messenger ribonucleic acid expression of KiSS-1 and Its putative receptor, GPR54, in rat hypothalamus and potent luteinizing hormone-releasing activity of KiSS-1 peptide. Endocrinology 2004, 145:4565-4574.
69. Takase K, Uenoyama Y, Inoue N, Matsui H, Yamada S, Shimizu M, Homma T, Tomikawa J, Kanda S, Matsumoto H, Oka Y, Tsukamura H, Maeda K-I. Possible role of oestrogen in pubertal increase of Kiss1/kisspeptin expression in discrete hypothalamic areas of female rats. J Neuroendocrinol 2009, 21:527-537.
70. 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.
71. Yamada S, Uenoyama Y, Kinoshita M, Iwata K, Takase K, Matsui H, Adachi S, Inoue K, Maeda K-I, Tsukamura H. Inhibition of metastin (kisspeptin-54)-GPR54 signaling in the arcuate nucleus-median eminence region during lactation in rats. Endocrinology 2007, 148:2226-2232.
72. Keen KL, Wegner FH, Bloom SR, Ghatei MA, Terasawa E. An Increase in kisspeptin-54 release occurs with the pubertal increase in LHRH-1 release in the stalk-median eminence of female rhesus monkeys in vivo. Endocrinology 2008, 149:4151-4157.
73. Roseweir AK, Kauffman AS, Smith JT, Guerriero KA, Morgan K, Pielecka-Fortuna J, Pineda R, Gottsch ML, Tena-Sempere M, Moenter SM, Terasawa E, Clarke IJ, Steiner RA, Millar RP. Discovery of potent kisspeptin antagonists delineate physiological mechanisms of gonadotropin regulation. J Neurosci 2009, 29:3920-3929.
74. Ohkura S, Takase K, Matsuyama S, Mogi K, Ichimaru T, Wakabayashi Y, Uenoyama Y, Mori Y, Steiner RA, Tsukamura H, Maeda KI, Okamura H. Gonadotrophin-releasing hormone pulse generator activity in the hypothalamus of the goat. J Neuroendocrinol 2009, 21:813-821.
75. Wakabayashi Y, Nakada T, Murata K, Ohkura S, Mogi K, Navarro VM, Clifton DK, Mori Y, Tsukamura H, Maeda K-I, 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, 30:3124-3132.
76. Goodman RL, Lehman MN, Smith JT, Coolen LM, de Oliveira CVR, Jafarzadehshirazi MR, Pereira A, Iqbal J, Caraty A, Ciofi P, Clarke IJ. Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B. Endocrinology 2007, 148:5752-5760.
77. Navarro VM, Gottsch ML, Chavkin C, Okamura H, Clifton DK, Steiner RA. Regulation of gonadotropin-releasing hormone secretion by kisspeptin/dynorphin/neurokinin B neurons in the arcuate nucleus of the mouse. J Neurosci 2009, 29:11859-11866.
78. Amstalden M, Coolen LM, Hemmerle AM, Billings HJ, Connors JM, Goodman RL, Lehman MN. Neurokinin 3 receptor immunoreactivity in the septal region, preoptic area and hypothalamus of the female sheep: colocalisation in neurokinin B cells of the arcuate nucleus but not in gonadotrophin-releasing hormone neurones. J Neuroendocrinol 2010, 22:1-12.
79. Topaloglu AK, Reimann F, Guclu M, Yalin AS, Kotan LD, Porter KM, Serin A, Mungan NO, Cook JR, Ozbek MN, Imamoglu S, Akalin NS, Yuksel B, O'Rahilly S, Semple RK. TAC3 and TACR3 mutations in familial hypogonadotropic hypogonadism reveal a key role for Neurokinin B in the central control of reproduction. Nat Genet 2009, 41:354-358.
80. Sandoval-Guzman T, Rance NE. Central injection of senktide, an NK3 receptor agonist, or neuropeptide Y inhibits LH secretion and induces different patterns of Fos expression in the rat hypothalamus. Brain Res 2004, 1026:307-312.
81. Gallo RV. Kappa-opioid receptor involvement in the regulation of pulsatile luteinizing hormone release during early pregnancy in the rat. J Neuroendocrinol 1990, 2:685-691.
82. Goodman RL, Coolen LM, Anderson GM, Hardy SL, Valent M, Connors JM, Fitzgerald ME, Lehman MN. Evidence that dynorphin plays a major role in mediating progesterone negative feedback on gonadotropin-releasing hormone neurons in sheep. Endocrinology 2004, 145:2959-2967.
83. Kinsey-Jones JS, Li XF, Luckman SM, O'Byrne KT. Effects of kisspeptin-10 on the electrophysiological manifestation of gonadotropin-releasing hormone pulse generator activity in the female rat. Endocrinology 2008, 149:1004-1008.
84. Oldham CM, Pearce DT. The ram effect in the breeding season. Proc Aust Soc Reprod Biol 1983, 15:72.