Activation of neurokinin 3 receptors stimulates GnRH release in a location-dependent but kisspeptin-independent manner in adult mice

Endocrinology

Volumn 154, Issue 11, 2013, Pages 3984-3989

  Gaskins, Garrett T ^a   Glanowska, Katarzyna M ^c   Moenter, Suzanne M ^a,b  

^a UNIVERSITY OF MICHIGAN MEDICAL SCHOOL   (United States)

^b UNIVERSITY OF MICHIGAN   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GONADORELIN; KISSPEPTIN; NEUROKININ 3 RECEPTOR; NEUROKININ B; SENKTIDE;

ANIMAL TISSUE; ARTICLE; GENE MUTATION; GONADORELIN RELEASE; HYPOGONADOTROPIC HYPOGONADISM; MALE; MEDIAN EMINENCE; MOUSE; NONHUMAN; PREOPTIC AREA; PRIORITY JOURNAL;

ANIMALS; FEMALE; GENE EXPRESSION REGULATION; GONADOTROPIN-RELEASING HORMONE; KISSPEPTINS; MALE; MEDIAN EMINENCE; MICE; MICE, KNOCKOUT; PEPTIDE FRAGMENTS; RECEPTORS, NEUROKININ-3; SUBSTANCE P;

EID: 84886473154     PISSN: 00137227     EISSN: 19457170     Source Type: Journal    
DOI: 10.1210/en.2013-1479     Document Type: Article

References (44)

1. Silverman AJ. The gonadotropin-releasing hormone (GnRH) neuron. In: Knobil E, Neill JD, ed. The Physiology of Reproduction. New York: Raven Press; 1994;1683-1709.
2. Moenter SM, Brand RM, Midgley AR, Karsch FJ. Dynamics of gonadotropin-releasing hormone release during a pulse. Endocrinology. 1992;130: 503-510.
3. Glanowska KM, Venton BJ, Moenter SM. Fast scan cyclic voltammetry as a novel method for detection of real-time gonadotropinreleasing hormone release in mouse brain slices. J Neurosci. 2012; 32: 14664-14669.
4. Fuenzalida LC, Keen KL, Terasawa E. Colocalization of FM1-43, Bassoon, and GnRH-1: GnRH-1 release from cell bodies and their neuroprocesses. Endocrinology. 2011;152: 4310-4321.
5. Guran T, Tolhurst G, Bereket A, et al. Hypogonadotropic hypogonadism due to a novel missense mutation in the first extracellular loop of the neurokinin B receptor. J Clin Endocrinol Metab. 2009; 94: 3633-3639.
6. Topaloglu AK, Reimann F, Guclu M, et al. 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.
7. Navarro VM, Tena-Sempere M. Kisspeptins and the neuroendocrine control of reproduction. Front Biosci. 2011;3: 267-275.
8. Rance NE, Krajewski SJ, Smith MA, Cholanian M, Dacks PA. Neurokinin B and the hypothalamic regulation of reproduction. Brain Res. 2010;1364: 116-128.
9. Krajewski SJ, Anderson MJ, Iles-Shih L, Chen KJ, Urbanski HF, Rance NE. Morphologic evidence that neurokinin B modulates gonadotropin- releasing hormone secretion via neurokinin 3 receptors in the rat median eminence. J Comp Neurol. 2005;489: 372-386.
10. Lucas LR, Hurley DL, Krause JE, Harlan RE. Localization of the tachykinin neurokinin B precursor peptide in rat brain by immunocytochemistry and in situ hybridization. Neuroscience. 1992;51: 317-345.
11. Navarro VM, Gottsch ML, Wu M, et al. Regulation of NKB pathways and their roles in the control of Kiss1 neurons in the arcuate nucleus of the male mouse. Endocrinology. 2011;152: 4265-4275.
12. Ruka KA, Burger LL, Moenter SM. Regulation of arcuate neurons coexpressing kisspeptin, neurokinin B, and dynorphin by modulators of neurokinin 3 and κ-opioid receptors in adult male mice. Endocrinology. 2013;154: 2761-2771.
13. Oakley AE, Clifton DK, Steiner RA. Kisspeptin signaling in the brain. Endocr Rev. 2009;30: 713-743.
14. Lehman MN, Coolen LM, Goodman RL. Minireview: kisspeptin/ neurokinin B/dynorphin (KNDy) cells of the arcuate nucleus: a central node in the control of gonadotropin-releasing hormone secretion. Endocrinology. 2010;151: 3479-3489.
15. 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.
16. Han SK, Gottsch ML, Lee KJ, et al. Activation of gonadotropinreleasing hormone neurons by kisspeptin as a neuroendocrine switch for the onset of puberty. J Neurosci. 2005;25: 11349-11356.
17. Pielecka-Fortuna J, Chu Z, Moenter SM. Kisspeptin acts directly and indirectly to increase gonadotropin-releasing hormone neuron activity and its effects are modulated by estradiol. Endocrinology. 2008;149: 1979-1986.
18. Messager S, Chatzidaki EE, Ma D, et al. Kisspeptin directly stimulates gonadotropin-releasing hormone release viaGprotein-coupled receptor 54. Proc Natl Acad Sci USA. 2005;102: 1761-1766.
19. Suter KJ, Song WJ, Sampson TL, et al. Genetic targeting of green fluorescent protein to gonadotropin-releasing hormone neurons: characterization of whole-cell electrophysiological properties and morphology. Endocrinology. 2000;141: 412-419.
20. Chan YM, Broder-Fingert S, Wong KM, Seminara SB. Kisspeptin/ Gpr54-independent gonadotrophin-releasing hormone activity in Kiss1 and Gpr54 mutant mice. J Neuroendocrinol. 2009;21: 1015-1023.
21. Lapatto R, Pallais JC, Zhang D, et al. Kiss1-/- mice exhibit more variable hypogonadism than Gpr54-/- mice. Endocrinology. 2007;148: 4927-4936.
22. Chu Z, Moenter SM. Endogenous activation of metabotropic glutamate receptors modulates GABAergic transmission to gonadotropin- releasing hormone neurons and alters their firing rate: a possible local feedback circuit. J Neurosci. 2005;25: 5740-5749.
23. Nunemaker CS, DeFazio RA, Moenter SM. A targeted extracellular approach for recording long-term firing patterns of excitable cells: a practical guide. Biol Proced Online. 2003;5: 53-62.
24. Kinsey-Jones JS, Grachev P, Li XF, et al. The inhibitory effects of neurokinin B on GnRH pulse generator frequency in the female rat. Endocrinology. 2012;153: 307-315.
25. Navarro VM, Castellano JM, McConkey SM, et al. Interactions between kisspeptin and neurokinin B in the control of GnRH secretion in the female rat. Am J Physiol Endocrinol Metab. 2011;300: E202-E210.
26. Sandoval-Guzmán 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.
27. Grachev P, Li XF, Kinsey-Jones JS, et al. Suppression of the GnRH pulse generator by neurokinin B involves a κ-opioid receptor-dependent mechanism. Endocrinology. 2012;153: 4894-4904.
28. Corander MP, Challis BG, Thompson EL, et al. The effects of neurokinin B upon gonadotrophin release in male rodents. J Neuroendocrinol. 2010;22: 181-187.
29. Caraty A, Locatelli A, Martin GB. Biphasic response in the secretion of gonadotrophin-releasing hormone in ovariectomized ewes injected with oestradiol. J Endocrinol. 1989;123: 375-382.
30. Clarke IJ, Cummins JT. Direct pituitary effects of estrogen and progesterone on gonadotropin secretion in the ovariectomized ewe. Neuroendocrinology. 1984;39: 267-274.
31. Grachev P, Li XF, Lin YS, et al. GPR54-dependent stimulation of luteinizing hormone secretion by neurokinin B in prepubertal rats. PLoS One. 2012;7:e44344.
32. Billings HJ, Connors JM, Altman SN, et al. NeurokininBacts via the neurokinin-3 receptor in the retrochiasmatic area to stimulate luteinizing hormone secretion in sheep. Endocrinology. 2010;151: 3836-3846.
33. Navarro VM, Ruiz-Pino F, Sánchez-Garrido MA, et al. Role of neurokinin B in the control of female puberty and its modulation by metabolic status. J Neurosci. 2012;32: 2388-2397.
34. Ramaswamy S, Seminara SB, Ali B, Ciofi P, Amin NA, Plant TM. Neurokinin B stimulatesGnRHrelease in the male monkey (Macaca mulatta) and is colocalized with kisspeptin in the arcuate nucleus. Endocrinology. 2010;151: 4494-4503.
35. RamaswamyS, Seminara SB, PlantTM.Evidence from the agonadal juvenile male rhesus monkey (Macaca mulatta) for the view that the action of neurokinin B to trigger gonadotropin-releasing hormone release is upstream from the kisspeptin receptor. Neuroendocrinology. 2011;94: 237-245.
36. García-Galiano D, van Ingen Schenau D, Leon S, et al. Kisspeptin signaling is indispensable for neurokinin B, but not glutamate, stimulation of gonadotropin secretion in mice. Endocrinology. 2012; 153: 316-328.
37. Smith JT. Sex steroid regulation of kisspeptin circuits. Adv Exp Med Biol. 2013;784: 275-295.
38. Blache D, Fabre-Nys CJ, Venier G. Ventromedial hypothalamus as a target for oestradiol action on proceptivity, receptivity and luteinizing hormone surge of the ewe. Brain Res. 1991;546: 241-249.
39. Caraty A, Fabre-Nys C, Delaleu B, et al. Evidence that the mediobasal hypothalamus is the primary site of action of estradiol in inducing the preovulatory gonadotropin releasing hormone surge in the ewe. Endocrinology. 1998;139: 1752-1760.
40. Kim W, Jessen HM, Auger AP, Terasawa E. Postmenopausal increase in KiSS-1, GPR54, and luteinizing hormone releasing hormone (LHRH-1)mRNAin the basal hypothalamus of female rhesus monkeys. Peptides. 2009;30: 103-110.
41. Shibata M, Friedman RL, Ramaswamy S, Plant TM. Evidence that down regulation of hypothalamic KiSS-1 expression is involved in the negative feedback action of testosterone to regulate luteinising hormone secretion in the adult male rhesus monkey (Macaca mulatta). J Neuroendocrinol. 2007;19: 432-438.
42. Smith JT, Shahab M, Pereira A, Pau KY, Clarke IJ. Hypothalamic expression of KISS1 and gonadotropin inhibitory hormone genes during the menstrual cycle of a non-human primate. Biol Reprod. 2010;83: 568-577.
43. d'Anglemont de Tassigny X, Fagg LA, Carlton MB, Colledge WH. Kisspeptin can stimulate gonadotropin-releasing hormone (GnRH) release by a direct action at GnRH nerve terminals. Endocrinology. 2008;149: 3926-3932.
44. Tsutsui K, Ubuka T, Bentley GE, Kriegsfeld LJ. Gonadotropininhibitory hormone (GnIH): discovery, progress and prospect. Gen Comp Endocrinol. 2012;177: 305-314.