Kisspeptin signaling in the amygdala modulates reproductive hormone secretion

Brain Structure and Function

Volumn 221, Issue 4, 2016, Pages 2035-2047

  Comninos, Alexander N ^a   Anastasovska, Jelena ^a   Sahuri Arisoylu, Meliz ^a   Li, Xiaofeng ^b   Li, Shengyun ^b   Hu, Minghan ^b   Jayasena, Channa N ^a   Ghatei, Mohammad A ^a   Bloom, Stephen R ^a   Matthews, Paul M ^a   O’Byrne, Kevin T ^b   Bell, Jimmy D ^a   Dhillo, Waljit S ^a  

^a HAMMERSMITH HOSPITAL   (United Kingdom)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Amygdala; Gonadotropin releasing hormone neuron; Hypothalamus; Kisspeptin; Manganese enhanced MRI; Reproductive axis

Indexed keywords

GELATIN SUCCINATE; GONADOTROPIN; KISSPEPTIN; LUTEINIZING HORMONE; MANGANESE; METASTIN; CONTRAST MEDIUM; KISS1 PROTEIN, RAT;

ADENOHYPOPHYSIS; ADULT; AMYGDALA; ANIMAL EXPERIMENT; ARTICLE; FEMALE; GONADOTROPIN RELEASE; HYPOTHALAMUS; IMMUNOREACTIVITY; LUTEINIZING HORMONE BLOOD LEVEL; LUTEINIZING HORMONE RELEASE; MEDIAL AMYGDALA; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; RADIOIMMUNOASSAY; RAT; REPRODUCTION; SIGNAL TRANSDUCTION; ANIMAL; C57BL MOUSE; DRUG EFFECTS; METABOLISM; PHYSIOLOGY; SPRAGUE DAWLEY RAT;

AMYGDALA; ANIMALS; CONTRAST MEDIA; FEMALE; HYPOTHALAMUS; KISSPEPTINS; LUTEINIZING HORMONE; MAGNETIC RESONANCE IMAGING; MANGANESE; MICE, INBRED C57BL; RATS; RATS, SPRAGUE-DAWLEY; REPRODUCTION;

EID: 84924362748     PISSN: 18632653     EISSN: 18632661     Source Type: Journal    
DOI: 10.1007/s00429-015-1024-9     Document Type: Article

References (58)

1. Bagga N, Chhina GS, Kumar VM, Singh B (1984) Cholinergic activation of medial preoptic area by amygdala for ovulation in rat. Physiol Behav 32:45–48
2. Bar-Sela M, Critchlow V (1966) Delayed puberty following electrical stimulation of amygdala in female rats. Am J Physiol 211:1103–1107
3. Bellefontaine N, Chachlaki K, Parkash J, Vanacker C, Colledge W, d’Anglemont de Tassigny X, Garthwaite J, Bouret SG, Prevot V (2014) Leptin-dependent neuronal NO signaling in the preoptic hypothalamus facilitates reproduction. J Clin Invest 124(6):2550–2559
4. Beltramino C, Taleisnik S (1978) Facilitatory and inhibitory effects of electrochemical stimulation of the amygdala on the release of luteinizing hormone. Brain Res 144:95–107
5. Cagampang FR, Maeda KI, Tsukamura H, Ohkura S, Ota K (1991) Involvement of ovarian steroids and endogenous opioids in the fasting-induced suppression of pulsatile LH release in ovariectomized rats. J Endocrinol 129:321–328
6. Canteras NS, Simerly RB, Swanson LW (1995) Organization of projections from the medial nucleus of the amygdala: a PHAL study in the rat. J Comp Neurol 360:213–245
7. Chand D, Lovejoy DA (2011) Stress and reproduction: controversies and challenges. Gen Comp Endocrinol 171(3):253–257
8. Chaudhri OB, Parkinson JR, Kuo YT, Druce MR, Herlihy AH, Bell JD, Dhillo WS, Stanley SA, Ghatei MA, Bloom SR (2006) Differential hypothalamic neuronal activation following peripheral injection of GLP-1 and oxyntomodulin in mice detected by manganese-enhanced magnetic resonance imaging. Biochem Biophys Res Commun 350(2):298–306
9. Clarkson J, d’Anglemont de Tassigny X, Colledge WH, Caraty A, Herbison AE (2009) Distribution of kisspeptin neurones in the adult female mouse brain. J Neuroendocrinol 21:673–682
10. Clasadonte J, Poulain P, Beauvillain JC, Prevot V (2008) Activation of neuronal nitric oxide release inhibits spontaneous firing in adult gonadotropin-releasing hormone neurons: a possible local synchronizing signal. Endocrinology 149(2):587–596
11. Curtis AE, Cooke JH, Baxter JE, Parkinson JR, Bataveljic A, Ghatei MA, Bloom SR, Murphy KG (2010) A kisspeptin-10 analog with greater in vivo bioactivity than kisspeptin-10. Am J Physiol Endocrinol Metab 298:E296–E303
12. d’Anglemont de Tassigny X, Ackroyd KJ, Chatzidaki EE, Colledge WH (2010) Kisspeptin signaling is required for peripheral but not central stimulation of gonadotropin-releasing hormone neurons by NMDA. J Neurosci 30:8581–8590
13. de Roux N, Genin E, Carel JC, Matsuda F, Chaussain JL, Milgrom E (2003) Hypogonadotropichypogonadism due to loss of function of the KiSS1-derived peptide receptor GPR54. Proc Natl Acad Sci USA 100:10972–10976
14. 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
15. Di Giorgio NP, Semaan SJ, Kim J, Lopez PV, Bettler B, Libertun C, Lux-Lantos VA, Kauffman AS (2014) Impaired GABAB receptor signaling dramatically up-regulates Kiss1 expression selectively in nonhypothalamic brain regions of adult but not prepubertal mice. Endocrinology 155:1033–1044
16. Garcia-Galiano D, Pineda R, Roa J, Ruiz-Pino F, Sanchez-Garrido MA, Castellano JM, Aguilar E, Navarro VM, Pinilla L, Tena-Sempere M (2012) Differential modulation of gonadotropin responses to kisspeptin by aminoacidergic, peptidergic, and nitric oxide neurotransmission. Am J Physiol Endocrinol Metab 303:E1252–E1263
17. Grossman AB, Rossmanith WG, Kabigting EB, Cadd G, Clifton D, Steiner RA (1994) The distribution of hypothalamic nitric oxide synthase mRNA in relation to gonadotrophin-releasing hormone neurons. J Endocrinol 140:R5–R8
18. Hahn JD, Kalamatianos T, Coen CW (2003) Studies on the neuroanatomical basis for stress-induced oestrogen-potentiated suppression of reproductive function: evidence against direct corticotropin-releasing hormone projections to the vicinity of luteinizing hormone-releasing hormone cell bodies in female rats. J Neuroendocrinol 15:732–742
19. Han SK, Gottsch ML, Lee KJ, Popa SM, Smith JT, Jakawich SK, Clifton DK, Steiner RA, Herbison AE (2005) Activation of gonadotropin-releasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci 25:11349–11356
20. Hanchate NK, Parkash J, Bellefontaine N, Mazur D, Colledge WH, d’Anglemont de Tassigny X, Prevot V (2012) Kisspeptin-GPR54 signaling in mouse NO-synthesizing neurons participates in the hypothalamic control of ovulation. J Neurosci 32(3):932–945
21. Hankir MK, Parkinson JR, Bloom SR, Bell JD (2012) The effects of glutamate receptor agonists and antagonists on mouse hypothalamic and hippocampal neuronal activity shown through manganese enhanced MRI. Neuroimage 59:968–978
22. 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
23. Herde MK, Geist K, Campbell RE, Herbison AE (2011) Gonadotropin-releasing hormone neurons extend complex highly branched dendritic trees outside the blood–brain barrier. Endocrinology 152:3832–3841
24. 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
25. Jayasena CN, Nijher GM, Comninos AN, Abbara A, Januszewki A, Vaal ML, Sriskandarajah L, Murphy KG, Farzad Z, Ghatei MA, Bloom SR, Dhillo WS (2011) The effects of kisspeptin-10 on reproductive hormone release show sexual dimorphism in humans. J Clin Endocrinol Metab 96:E1963–E1972
26. Kauffman AS, Park JH, McPhie-Lalmansingh AA, Gottsch ML, Bodo C, Hohmann JG, Pavlova MN, Rohde AD, Clifton DK, Steiner RA, Rissman EF (2007) The kisspeptin receptor GPR54 is required for sexual differentiation of the brain and behavior. J Neurosci 27:8826–8835
27. Keshavarzi S, Sullivan RK, Ianno DJ, Sah P (2014) Functional properties and projections of neurons in the medial amygdala. J Neurosci 34(26):8699–8715
28. Kim J, Semaan SJ, Clifton DK, Steiner RA, Dhamija S, Kauffman AS (2011) Regulation of Kiss1 expression by sex steroids in the amygdala of the rat and mouse. Endocrinology 152:2020–2030
29. Kluver H, Bucy PC (1997) Preliminary analysis of functions of the temporal lobes in monkeys. J Neuropsychiatry Clin Neurosci 9:606–620
30. Kuo YT, Herlihy AH, So PW, Bell JD (2006) Manganese-enhanced magnetic resonance imaging (MEMRI) without compromise of the blood–brain barrier detects hypothalamic neuronal activity in vivo. NMR Biomed 19(8):1028–1034
31. Kuo YT, Parkinson JR, Chaudhri OB, Herlihy AH, So PW, Dhillo WS, Small CJ, Bloom SR, Bell JD (2007) The temporal sequence of gut peptide CNS interactions tracked in vivo by magnetic resonance imaging. J Neurosci 27:12341–12348
32. Kuo YT, So PW, Parkinson JR, Yu WS, Hankir M, Herlihy AH, Goldstone AP, Frost GS, Wasserfall C, Bell JD (2010) The combined effects on neuronal activation and blood–brain barrier permeability of time and n-3 polyunsaturated fatty acids in mice, as measured in vivo using MEMRI. Neuroimage 50:1384–1391
33. Lawton IE, Sawyer CH (1970) Role of amygdala in regulating LH secretion in the adult female rat. Am J Physiol 218:622–626
34. 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 (1999) Discovery of a receptor related to the galanin receptors. FEBS Lett 446:103–107
35. Li XF, Kinsey-Jones JS, Cheng Y, Knox AM, Lin Y, Petrou NA, Roseweir A, Lightman SL, Milligan SR, Millar RP, O’Byrne KT (2009) Kisspeptin signaling in the hypothalamic arcuate nucleus regulates GnRH pulse generator frequency in the rat. PLoS ONE 4:e8334
36. Lin Y, Li X, Lupi M, Kinsey-Jones JS, Shao B, Lightman SL, O’Byrne KT (2011) The role of the medial and central amygdala in stress-induced suppression of pulsatile LH secretion in female rats. Endocrinology 152:545–555
37. Martin C, Navarro VM, Simavli S, Vong L, Carroll RS, Lowell BB, Kaiser UB (2014) Leptin-responsive GABAergic neurons regulate fertility through pathways that result in reduced kisspeptinergic tone. J Neurosci 34(17):6047–6056
38. Muir AI et al (2001) AXOR12, a novel human G protein-coupled receptor, activated by the peptide KiSS-1. J Biol Chem 276:28969–28975
39. Murray EA (2007) The amygdala, reward and emotion. Trends Cogn Sci 11:489–497
40. Neal-Perry G, Lebesgue D, Lederman M, Shu J, Zeevalk GD, Etgen AM (2009) The excitatory peptide kisspeptin restores the luteinizing hormone surge and modulates amino acid neurotransmission in the medial preoptic area of middle-aged rats. Endocrinology 150:3699–3708
41. Paxinos G, Franklin KBJ (2001) The mouse brain in stereotaxic coordinates. Academic, London
42. Paxinos G, Watson C (1986) The rat brain in stereotactic coordinates. Academic, London
43. Pheng V, Uenoyama Y, Homma T, Inamoto Y, Takase K, Yoshizawa-Kumagaye K, Isaka S, Watanabe TX, Ohkura S, Tomikawa J, Maeda K, Tsukamura H (2009) Potencies of centrally- or peripherally-injected full-length kisspeptin or its C-terminal decapeptide on LH release in intact male rats. J Reprod Dev. 55(4):378–382
44. Pinilla L, Aguilar E, Dieguez C, Millar RP, Tena-Sempere M (2012) Kisspeptins and reproduction: physiological roles and regulatory mechanisms. Physiol Rev 92:1235–1316
45. Scott V, Brown CH (2011) Kisspeptin activation of supraoptic nucleus neurons in vivo. Endocrinology 152(10):3862–3870
46. Seminara SB, Messager S, Chatzidaki EE, Thresher RR, AciernoJS 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 (2003) The GPR54 gene as a regulator of puberty. N Engl J Med 349:1614–1627
47. Silva AC, Bock NA (2008) Manganese-enhanced MRI: an exceptional tool in translational neuroimaging. Schizophr Bull 34(4):595–604
48. Silva AC, Lee JH, Aoki I, Koretsky AP (2004) Manganese-enhanced magnetic resonance imaging (MEMRI): methodological and practical considerations. NMR Biomed 17(8):532–543
49. Silveira LG, Noel SD, Silveira-Neto AP, Abreu AP, Brito VN, Santos MG, Bianco SD, Kuohung W, Xu S, Gryngarten M, Escobar ME, Arnhold IJ, Mendonca BB, Kaiser UB, Latronico AC (2010) Mutations of the KISS1 gene in disorders of puberty. J Clin Endocrinol Metab 95:2276–2280
50. Teles MG, Bianco SD, Brito VN, Trarbach EB, Kuohung W, Xu S, Seminara SB, Mendonca BB, Kaiser UB, Latronico AC (2008) A GPR54-activating mutation in a patient with central precocious puberty. N Engl J Med 358:709–715
51. Thompson EL, Patterson M, Murphy KG, Smith KL, Dhillo WS, Todd JF, Ghatei MA, Bloom SR (2004) Central and peripheral administration of kisspeptin-10 stimulates the hypothalamic-pituitary-gonadal axis. J Neuroendocrinol 16(10):850–858
52. Topaloglu AK, Tello JA, Kotan LD, Ozbek MN, Yilmaz MB, Erdogan S, Gurbuz F, Temiz F, Millar RP, Yuksel B (2012) Inactivating KISS1 mutation and hypogonadotropic hypogonadism. N Engl J Med 366:629–635
53. Van Cauter E (1988) Estimating false-positive and false-negative errors in analyses of hormonal pulsatility. Am J Physiol 254:E786–E794
54. Veinante P, Stoeckel ME, Freund-Mercier MJ (1997) GABA- and peptide-immunoreactivities co-localize in the rat central extended amygdala. NeuroReport 8:2985–2989
55. Xu Z, Kaga S, Mochiduki A, Tsubomizu J, Adachi S, Sakai T, Inoue K, Adachi AA (2012) Immunocytochemical localization of kisspeptin neurons in the rat forebrain with special reference to sexual dimorphism and interaction with GnRH neurons. Endocr J 59:161–171
56. Zeger SL, Liang KY (1986) Longitudinal data analysis for discrete and continuous outcomes. Biometrics 42:121–130
57. Zhang C, Bosch MA, Rønnekleiv OK, Kelly MJ (2009) Gamma-aminobutyric acid B receptor mediated inhibition of gonadotropin-releasing hormone neurons is suppressed by kisspeptin-G protein-coupled receptor 54 signaling. Endocrinology 150(5):2388–2394
58. Zuure WA, Roberts A, Quennell JH, Anderson GM (2013) Leptin signaling in GABA neurons, but not glutamate neurons, is required for reproductive function. J Neurosci 33(45):17874–17883