Melanocortins may stimulate reproduction by activating orexin neurons in the dorsomedial hypothalamus and kisspeptin neurons in the preoptic area of the ewe

Endocrinology

Volumn 150, Issue 12, 2009, Pages 5488-5497

  Backholer, Kathryn ^a   Smith, Jeremy ^a   Clarke, Iain J ^a  

^a MONASH UNIVERSITY   (Australia)

Author keywords

[No Author keywords available]

Indexed keywords

KISSPEPTIN; LUTEINIZING HORMONE; MELANOCORTIN; MELANOCORTIN RECEPTOR AGONIST; OREXIN; PROOPIOMELANOCORTIN;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN NERVE CELL; CONTROLLED STUDY; FEMALE; GENE EXPRESSION REGULATION; HORMONE ACTION; HORMONE RESPONSE; HYPOTHALAMUS; LATERAL BRAIN VENTRICLE; LUTEAL PHASE; LUTEINIZING HORMONE RELEASE; NERVE PROJECTION; NONHUMAN; PREOPTIC AREA; PRIORITY JOURNAL; REPRODUCTION; SHEEP; UPREGULATION;

ALPHA-MSH; ANIMALS; ARCUATE NUCLEUS; ESTROUS CYCLE; FEMALE; GENE EXPRESSION; HYPOTHALAMUS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; LUTEINIZING HORMONE; MELANOCORTINS; NEURONS; NEUROPEPTIDES; PEPTIDES, CYCLIC; PREOPTIC AREA; RADIOIMMUNOASSAY; REPRODUCTION; RNA, MESSENGER; SHEEP; TUMOR SUPPRESSOR PROTEINS;

EID: 71949110404     PISSN: 00137227     EISSN: 00137227     Source Type: Journal    
DOI: 10.1210/en.2009-0604     Document Type: Article

References (64)

1. Pritchard LE, Turnbull AV, White A 2002 Pro-opiomelanocortin processing in the hypothalamus: impact on melanocortin signalling and obesity. J Endocrinol 172:411-421 (Pubitemid 34232683)
2. Walsh JP, Rao A, Simmons DM, Clarke IJ 1998 Proopiomelanocortin mRNA levels in ovine hypothalamus are not reduced at the time of the preovulatory luteinising hormone surge. J Neuroendocrinol 10:803-808 (Pubitemid 28446151)
3. Wise PM, Scarbrough K, Weiland NG, Larson GH 1990 Diurnal pattern of proopiomelanocortin gene expression in the arcuate nucleus of proestrous, ovariectomized, and steroid-treated rats: a possible role in cyclic luteinizing hormone secretion. Mol Endocrinol 4:886-892 (Pubitemid 20351997)
4. Bohler Jr HC, Tracer H, Merriam GR, Petersen SL 1991 Changes in proopiomelanocortin messenger ribonucleic acid levels in the rostral periarcuate region of the female rat during the estrous cycle. Endocrinology 128:1265-1269
5. Tong Y, Zhao HF, Labrie F, Pelletier G 1990 Regulation of proopiomelanocortin messenger ribonucleic acid content by sex steroids in the arcuate nucleus of the female rat brain. Neurosci Lett 112:104-108 (Pubitemid 20120635)
6. Wilcox JN, Roberts JL 1985 Estrogen decreases rat hypothalamic proopiomelanocortin messenger ribonucleic acid levels. Endocrinology 117:2392-2396 (Pubitemid 16194066)
7. Petersen SL, Keller ML, Carder SA, McCrone S 1993 Differential effects of estrogen and progesterone on levels of POMC mRNA levels in the arcuate nucleus: relationship to the timing of LH surge release. J Neuroendocrinol 5:643-648 (Pubitemid 24013367)
8. Schiöth HB, Watanobe H 2002 Melanocortins and reproduction. Brain Res Brain Res Rev 38:340-350
9. Alde S, Celis ME 1980 Influence of α-melanotropin on LH release in the rat. Neuroendocrinology 31:116-120
10. Watanobe H, Schiöth HB, Wikberg JE, Suda T 1999 The melanocortin 4 receptor mediates leptin stimulation of luteinizing hormone and prolactin surges in steroid-primed ovariectomized rats. Biochem Biophys Res Commun 257:860-864 (Pubitemid 29301532)
11. Limone P, Calvelli P, Altare F, Ajmone-Catt P, Lima T, Molinatti GM 1997 Evidence for an interaction between α-MSH and opioids in the regulation of gonadotropin secretion in man. J Endocrinol Invest 20:207-210 (Pubitemid 27289380)
12. Stanley SA, Davies S, Small CJ, Gardiner JV, Ghatei MA, Smith DM, Bloom SR 2003 γ-MSH increases intracellular cAMP accumulation and GnRH release in vitro and LH release in vivo. FEBS Lett 543:66-70 (Pubitemid 36577229)
13. Backholer K, Bowden M, Gamber K, Bjorbaek C, Iqbal J, Clarke IJ Propiomelanocortin, melanocortin, and reproductive function in lean body condition. Program of the 90th Annual Meeting of The Endocrine Society, San Francisco, CA, 2008 (Abstract P1-690)
14. Mizuno TM, Kleopoulos SP, Bergen HT, Roberts JL, Priest CA, Mobbs CV 1998 Hypothalamic pro-opiomelanocortin mRNA is reduced by fasting and [corrected] in ob/ob and db/db mice, but is stimulated by leptin. Diabetes 47:294-297 (Pubitemid 28079992)
15. McShane TM, Petersen SL, McCrone S, Keisler DH 1993 Influence of food restriction on neuropeptide-Y, proopiomelanocortin, and luteinizing hormone-releasing hormone gene expression in sheep hypothalami. Biol Reprod 49:831-839 (Pubitemid 23276944)
16. Pompolo S, Rawson JA, Clarke IJ 2001 Projections from the arcuate/ventromedial region of the hypothalamus to the preoptic area and bed nucleus of stria terminalis in the brain of the ewe; lack of direct input to gonadotropin-releasing hormone neurons. Brain Res 904:1-12 (Pubitemid 32545349)
17. Goubillon M, Delaleu B, Tillet Y, Caraty A, Herbison AE 1999 Localization of estrogen-receptive neurons projecting to the GnRH neuron-containing rostral preoptic area of the ewe. Neuroendocrinology 70:228-236 (Pubitemid 29481659)
18. Goubillon ML, Caraty A, Herbison AE 2002 Evidence in favour of a direct input from the ventromedial nucleus to gonadotropin-releasing hormone neurones in the ewe: an anterograde tracing study. J Neuroendocrinol 14:95-100
19. Pu S, Jain MR, Kalra PS, Kalra SP 1998 Orexins, a novel family of hypothalamic neuropeptides, modulate pituitary luteinizing hormone secretion in an ovarian steroid-dependent manner. Regul Pept 78:133-136 (Pubitemid 28564515)
20. Irwig MS, Fraley GS, Smith JT, Acohido BV, Popa SM, Cunningham MJ, Gottsch ML, Clifton DK, Steiner RA 2004 Kisspeptin activation of gonadotropin releasing hormone neurons and regulation of KiSS-1 mRNA in the male rat. Neuroendocrinology 80:264-272
21. Smith JT, Clifton DK, Steiner RA 2006 Regulation of the neuroendocrine reproductive axis by kisspeptin-GPR54 signaling. Reproduction 131:623-630
22. Shahab M, Mastronardi C, Seminara SB, Crowley WF, Ojeda SR, Plant TM 2005 Increased hypothalamic GPR54 signaling: a potential mechanism for initiation of puberty in primates. Proc Natl Acad Sci USA 102:2129-2134 (Pubitemid 40262023)
23. Dhillo WS, Chaudhri OB, Patterson M, Thompson EL, Murphy KG, Badman MK, McGowan BM, Amber V, Patel S, Ghatei MA, Bloom SR 2005 Kisspeptin-54 stimulates the hypothalamic-pituitary gonadal axis in human males. J Clin Endocrinol Metab 90:6609-6615 (Pubitemid 41759323)
24. Iqbal J, Pompolo S, Sakurai T, Clarke IJ 2001 Evidence that orexin-containing neurones provide direct input to gonadotropin-releasing hormone neurones in the ovine hypothalamus. J Neuroendocrinol 13:1033-1041 (Pubitemid 33100220)
25. Smith JT, Coolen LM, Kriegsfeld LJ, Sari IP, Jaafarzadehshirazi MR, Maltby M, Bateman K, Goodman RL, Tilbrook AJ, Ubuka T, Bentley GE, Clarke IJ, Lehman MN 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
26. Campbell RE, Grove KL, Smith MS 2003 Gonadotropin-releasing hormone neurons coexpress orexin 1 receptor immunoreactivity and receive direct contacts by orexin fibers. Endocrinology 144:1542-1548
27. Karsch FJ, Cummins JT, Thomas GB, Clarke IJ 1987 Steroid feedback inhibition of pulsatile secretion of gonadotropin-releasing hormone in the ewe. Biol Reprod 36:1207-1218 (Pubitemid 17107333)
28. Henry BA, Dunshea FR, Gould M, Clarke IJ 2008 Profiling postprandial thermogenesis in muscle and fat of sheep and the central effect of leptin administration. Endocrinology 149:2019-2026
29. Scott CJ, Pereira AM, Tilbrook AJ, Rawson JA, Clarke IJ 2001 Changes in preoptic and hypothalamic levels of progesterone receptor mRNA across the oestrous cycle of the ewe. J Neuroendocrinol 13:401-406
30. 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
31. Qi Y, Iqbal J, Oldfield BJ, Clarke IJ 2008 Neural connectivity in the mediobasal hypothalamus of the sheep brain. Neuroendocrinology 87:91-112 (Pubitemid 351301280)
32. Henry BA, Rao A, Ikenasio BA, Mountjoy KG, Tilbrook AJ, Clarke IJ 2001 Differential expression of cocaine- and amphetamine-regulated transcript and agouti related-protein in chronically food-restricted sheep. Brain Res 918:40-50 (Pubitemid 33001487)
33. Caraty A, Skinner DC 1999 Progesterone priming is essential for the full expression of the positive feedback effect of estradiol in inducing the preovulatory gonadotropin-releasing hormone surge in the ewe. Endocrinology 140:165-170 (Pubitemid 29011156)
34. Goodman RL, Lehman MN, Smith JT, Coolen LM, de Oliveira CV, Jafarzadehshirazi MR, Pereira A, Iqbal J, Caraty A, Ciofi P, Clarke IJ 2007 Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B. Endocrinology 148:5752-5760 (Pubitemid 350146171)
35. Franceschini I, Lomet D, Cateau M, Delsol G, Tillet Y, Caraty A 2006 Kisspeptin immunoreactive cells of the ovine preoptic area and arcuate nucleus co-express estrogen receptor α. Neurosci Lett 401:225-230 (Pubitemid 43729526)
36. Simmons DMAJ, Swanson LW 1989 A complete protocol for in situ hybridization of messenger RNAs in brain and other tissues with radio-labelled single-stranded RNA probes. J Histotechnol 12:169-181
37. Scott CJ, Pereira AM, Rawson JA, Simmons DM, Rossmanith WG, Ing NH, Clarke IJ 2000 The distribution of progesterone receptor immunoreactivity and mRNA in the preoptic area and hypothalamus of the ewe: upregulation of progesterone receptor mRNA in the mediobasal hypothalamus by oestrogen. J Neuroendocrinol 12:565-575
38. Sambrook J, Fritsch E, Maniatis T 1989 Molecular cloning, a laboratory manual. 2nd ed. Cold Spring Harbor, NY: Cold Sping Harbor Laboratory Press
39. Lee VW, Cumming IA, de Kretser DM, Findlay JK, Hudson B, Keogh EJ 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
40. Clarke IJ, Cummins JT 1985 Increased gonadotropin-releasing hormone pulse frequency associated with estrogen-induced luteinizing hormone surges in ovariectomized ewes. Endocrinology 116:2376-2383
41. Deayton JM, Young IR, Thorburn GD 1993 Early hypophysectomy of sheep fetuses: effects on growth, placental steroidogenesis and prostaglandin production. J Reprod Fertil 97:513-520
42. Yin W, Mendenhall JM, Bratton SB, Oung T, Janssen WG, Morrison JH, Gore AC 2007 Novel localization of NMDA receptors within neuroendocrine gonadotropin-releasing hormone terminals. Exp Biol Med (Maywood) 232:662-673 (Pubitemid 46683392)
43. Clarke IJ, Thomas GB, Yao B, Cummins JT 1987 GnRH secretion throughout the ovine estrous cycle. Neuroendocrinology 46:82-88 (Pubitemid 17098299)
44. Khorram O, Bedran de Castro JC, McCann SM 1985 The effect of the estrous cycle and estrogen on the release of immunoreactive α-melanocyte- stimulating hormone. Peptides 6:503-508 (Pubitemid 16255664)
45. Abbott CR, Rossi M, Kim M, AlAhmed SH, Taylor GM, Ghatei MA, Smith DM, Bloom SR 2000 Investigation of the melanocyte stimulating hormones on food intake. Lack of evidence to support a role for the melanocortin-3-receptor. Brain Res 869:203-210
46. Tsujii S, Bray GA 1989 Acetylation alters the feeding response to MSH and β-endorphin. Brain Res Bull 23:165-169 (Pubitemid 19277653)
47. Mauri A, Martellotta MC, Melis MR, Caminiti F, Serri F, FrattaW 1990 Plasma α-melanocyte-stimulating hormone during the menstrual cycle in women. Horm Res 34:66-70
48. Harrold JA, Widdowson PS, Williams G 2003 β-MSH: a functional ligand that regulated energy homeostasis via hypothalamic MC4-R? Peptides 24:397-405
49. Gantz I, Konda Y, Tashiro T, Shimoto Y, Miwa H, Munzert G, Watson SJ, DelValle J, Yamada T 1993 Molecular cloning of a novel melanocortin receptor. J Biol Chem 268:8246-8250 (Pubitemid 23120413)
50. Pompolo S, Ischenko O, Pereira A, Iqbal J, Clarke IJ 2005 Evidence that projections from the bed nucleus of the stria terminalis and from the lateral and medial regions of the preoptic area provide input to gonadotropin releasing hormone (GNRH) neurons in the female sheep brain. Neuroscience 132:421-436 (Pubitemid 40417915)
51. Jacobowitz DM, O'Donohue TL 1978 α-Melanocyte stimulating hormone: immunohistochemical identification and mapping in neurons of rat brain. Proc Natl Acad Sci USA 75:6300-6304
52. Homma A, Li HP, Hayashi K, Kawano Y, Kawano H 2006 Differential response of arcuate proopiomelanocortin- and neuropeptide Y-containing neurons to the lesion produced by gold thioglucose administration. J Comp Neurol 499:120-131 (Pubitemid 44423699)
53. Iqbal J, Pompolo S, Dumont LM,WuCS, Mountjoy KG, Henry BA, Clarke IJ 2001 Long-term alterations in body weight do not affect the expression of melanocortin receptor-3 and -4 mRNA in the ovine hypothalamus. Neuroscience 105:931-940 (Pubitemid 32786806)
54. Sartin JL, Dyer C, Matteri R, Buxton D, Buonomo F, Shores M, Baker J, Osborne JA, Braden T, Steele B 2001 Effect of intracerebroventricular orexin-B on food intake in sheep. J Anim Sci 79:1573-1577 (Pubitemid 33620435)
55. Fan W, Boston BA, Kesterson RA, Hruby VJ, Cone RD 1997 Role of melanocortinergic neurons in feeding and the agouti obesity syndrome. Nature 385:165-168 (Pubitemid 27034218)
56. 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 (Pubitemid 46272806)
57. Smith JT 2009 Sex steroid control of hypothalamic Kiss1 expression in sheep and rodents: comparative aspects. Peptides 30:94-102
58. Legan SJ, Karsch FJ, Foster DL 1977 The endocrin control of seasonal reproductive function in the ewe: a marked change in response to the negative feedback action of estradiol on luteinizing hormone secretion. Endocrinology 101:818-824
59. Clarke IJ, Scott CJ, Rao A, Pompolo S, Barker-Gibb ML 2000 Seasonal changes in the expression of neuropeptide Y and pro-opiomelanocortin mRNA in the arcuate nucleus of the ovariectomized ewe: relationship to the seasonal appetite and breeding cycles. J Neuroendocrinol 12:1105-1111 (Pubitemid 30795760)
60. Anukulkitch C, Rao A, Dunshea FR, Blache D, Lincoln GA, Clarke IJ 2007 Influence of photoperiod and gonadal status on food intake, adiposity, and gene expression of hypothalamic appetite regulators in a seasonal mammal. Am J Physiol Regul Integr Comp Physiol 292:R242-R252 (Pubitemid 46091601)
61. Ramaswamy S, Guerriero KA, Gibbs RB, Plant TM 2008 Structural interactions between kisspeptin and GnRH neurons in the mediobasal hypothalamus of the male rhesus monkey (Macaca mulatta) as revealed by double immunofluorescence and confocal microscopy. Endocrinology 149:4387-4395
62. Conover CD, Kuljis RO, Rabii J, Advis JP 1993 β-Endorphin regulation of luteinizing hormone-releasing hormone release at the median eminence in ewes: immunocytochemical and physiological evidence. Neuroendocrinology 57:1182-1195 (Pubitemid 23260797)
63. Kawakami S, Ichikawa M, Murahashi K, Hirunagi K, Tsukamura H, Maeda K 1998 Excitatory amino acids act on the median eminence nerve terminals to induce gonadotropin-releasing hormone release in female rats. Gen Comp Endocrinol 112:372-382 (Pubitemid 29003994)
64. Durrant AR, PlantTM 1999 A study of the gonadotropin releasing hormone neuronal network in the median eminence of the rhesus monkey (Macaca mulatta) using a post-embedding immunolabelling procedure. J Neuroendocrinol 11:813-821