Estrogen permits vasopressin signaling in preoptic kisspeptin neurons in the female mouse

Journal of Neuroscience

Volumn 35, Issue 17, 2015, Pages 6881-6892

  Piet, Richard ^a   Fraissenon, Antoine ^a   Boehm, Ulrich ^b   Herbison, Allan E ^a  

^a UNIVERSITY OF OTAGO   (New Zealand)

^b SAARLAND UNIVERSITY   (Germany)

Author keywords

Circadian system; GnRH; Ovarian steroids; Ovulation

Indexed keywords

ESTROGEN; VASOPRESSIN; VOLTAGE GATED CALCIUM CHANNEL; AMINO ACID RECEPTOR BLOCKING AGENT; ARGIPRESSIN; CALCIUM; GREEN FLUORESCENT PROTEIN; KISSPEPTIN; SODIUM CHANNEL BLOCKING AGENT; TETRODOTOXIN;

ADULT; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BRAIN ELECTROPHYSIOLOGY; CIRCADIAN RHYTHM; ESTRUS CYCLE; FEMALE; MOUSE; NERVE CELL; NERVE CELL NETWORK; NERVE CELL PLASTICITY; NERVE EXCITABILITY; NONHUMAN; PREOPTIC KISSPEPTIN NEURON; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ACTION POTENTIAL; ANIMAL; CYTOLOGY; DRUG EFFECTS; GENETICS; METABOLISM; OVARIECTOMY; PHYSIOLOGY; PREOPTIC AREA; SUPRACHIASMATIC NUCLEUS; TRANSGENIC ANIMAL;

ACTION POTENTIALS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ARGININE VASOPRESSIN; CALCIUM; CIRCADIAN RHYTHM; ESTROGENS; ESTROUS CYCLE; EXCITATORY AMINO ACID ANTAGONISTS; FEMALE; GREEN FLUORESCENT PROTEINS; KISSPEPTINS; MICE; NERVE NET; NEURONS; OVARIECTOMY; PREOPTIC AREA; SIGNAL TRANSDUCTION; SODIUM CHANNEL BLOCKERS; SUPRACHIASMATIC NUCLEUS; TETRODOTOXIN;

EID: 84929378373     PISSN: 02706474     EISSN: 15292401     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.4587-14.2015     Document Type: Article

References (54)

1. Bronson FH (1981) The regulation of luteinizing hormone secretion by estrogen: relationships among negative feedback, surge potential, and male stimulation in juvenile, peripubertal, and adult female mice. Endocrinology 108:506-516. CrossRef Medline
2. Busnelli M, Bulgheroni E, Manning M, Kleinau G, Chini B (2013) Selective and potent agonists and antagonists for investigating the role of mouse oxytocin receptors. J Pharmacol Exp Ther 346:318-327. CrossRef Medline
3. Christian CA, Moenter SM (2008) Critical roles for fast synaptic transmission in mediating estradiol negative and positive feedback in the neural control of ovulation. Endocrinology 149:5500-5508. CrossRef Medline
4. Clarkson J, d'Anglemont de TassignyX, Moreno AS, Colledge WH, Herbison AE (2008) Kisspeptin-GPR54 signaling is essential for preovulatory gonadotropin-releasing hormone neuron activation and the luteinizing hormone surge. J Neurosci 28:8691-8697. CrossRef Medline
5. Constantin S, Jasoni CL, Wadas B, Herbison AE (2010) Gamma-aminobutyric acid and glutamate differentially regulate intracellular calcium concentrations in mouse gonadotropin-releasing hormone neurons. Endocrinology 151:262-270. CrossRef Medline
6. Dardente H, Menet JS, Challet E, Tournier BB, Pévet P, Masson-Pévet M (2004) Daily and circadian expression of neuropeptides in the suprachi-asmatic nuclei of nocturnal and diurnal rodents. Brain Res Mol Brain Res 124:143-151. CrossRef Medline
7. de Croft S, Piet R, Mayer C, Mai O, Boehm U, Herbison AE (2012) Spontaneous kisspeptin neuron firing in the adult mouse reveals marked sex and brain region differences but no support for a direct role in negative feedback. Endocrinology 153:5384-5393. CrossRef Medline
8. de la Iglesia HO, Schwartz WJ (2006) Minireview: timely ovulation: circadian regulation of the female hypothalamo-pituitary-gonadal axis. Endocrinology 147:1148-1153. CrossRef Medline
9. de la Iglesia HO, Blaustein JD, Bittman EL (1995) The suprachiasmatic area in the female hamster projects to neurons containing estrogen receptors and GnRH. Neuroreport 6:1715-1722. CrossRef Medline
10. Edelstein A, Amodaj N, Hoover K, Vale R, Stuurman N (2010) Computer control of microscopes using μManager. Curr Protoc Mol Biol Chapter 14:Unitl4.20. CrossRef Medline
11. Everett JW, Sawyer CH (1950) A 24-hour periodicity in the "LH-release apparatus" of female rats, disclosed by barbiturate sedation. Endocrinology 47:198-218. CrossRef Medline
12. Funabashi T, Aiba S, Sano A, Shinohara K, Kimura F (1999) Intracerebro-ventricular injection of arginine-vasopressin VI receptor antagonist attenuates the surge of luteinizing hormone and prolactin secretion in proestrous rats. Neurosci Lett 260:37-40. CrossRef Medline
13. Herbison AE (2008) Estrogen positive feedback to gonadotropin-releasing hormone (GnRH) neurons in the rodent: the case for the rostral periventricular area of the third ventricle (RP3V). Brain Res Rev 57:277-287. CrossRef Medline
14. Iremonger KJ, Herbison AE (2012) Initiation and propagation of action potentials in gonadotropin-releasing hormone neuron dendrites. J Neurosci 32:151-158. CrossRef Medline
15. Kalamatianos T, Kalló I, Goubillon ML, Coen CW (2004) Cellular expression of Via vasopressin receptor mRNA in the female rat preoptic area: effects of oestrogen. J Neuroendocrinol 16:525-533. CrossRef Medline
16. Kalsbeek A, Buijs RM, Engelmann M, Wotjak CT, Landgraf R (1995) In vivo measurement of a diurnal variation in vasopressin release in the rat suprachiasmatic nucleus. Brain Res 682:75-82. CrossRef Medline
17. Kriegsfeld LJ, Silver R (2006) The regulation of neuroendocrine function: timing is everything. Horm Behav 49:557-574. CrossRef Medline
18. Lee K, Duan W, Sneyd J, Herbison AE (2010) Two slow calcium-activated afterhyperpolarization currents control burst firing dynamics in gonadotropin-releasing hormone neurons. J Neurosci 30:6214-6224. CrossRef Medline
19. Legan SJ, Karsch FJ (1975) A daily signal for the LH surge in the rat. Endocrinology 96:57-62. CrossRef Medline
20. Legan SJ, Coon GA, Karsch FJ (1975) Role of estrogen as initiator of daily LH surges in the ovariectomized rat. Endocrinology 96:50-56. CrossRef Medline
21. Li JD, Hu WP, Zhou QY (2012) The circadian output signals from the suprachiasmatic nuclei. Prog Brain Res 199:119-127. CrossRef Medline
22. Liu X, Porteous R, d'Anglemont de Tassigny X, Colledge WH, Millar R, Petersen SL, Herbison AE (2011) Frequency-dependent recruitment of fast amino acid and slow neuropeptide neurotransmitter release controls gonadotropin-releasing hormone neuron excitability. J Neurosci 31: 2421-2430. CrossRef Medline
23. Lowbridge J, Manning M, Haidar J, Sawyer WH (1977) Synthesis and some pharmacological properties of [4-threonine, 7-glycine]oxytocin, [ l-(L-2-hydroxy-3-mercaptopropanoic acid), 4-threonine, 7-glycine] oxytocin (hydroxy[Thr4, Gly7]oxytocin), and [7-glycine]oxytocin, peptides with high oxytocic-antidiuretic selectivity. J Med Chem 20:120-123. CrossRef Medline
24. Manning M, Misicka A, Olma A, Bankowski K, Stoev S, Chini B, Durroux T, Mouillac B, Corbani M, Guillon G (2012) Oxytocin and vasopressin agonists and antagonists as research tools and potential therapeutics. J Neuroendocrinol 24:609-628. CrossRef Medline
25. Mayer C, Acosta-Martinez M, Dubois SL, Wolfe A, Radovick S, Boehm U, Levine JE (2010) Timing and completion of puberty in female mice depend on estrogen receptor alpha-signaling in kisspeptin neurons. Proc Natl Acad Sci U S A 107:22693-22698. CrossRef Medline
26. Miller BH, Olson SL, Turek FW, Levine JE, Horton TH, Takahashi JS (2004) Circadian clock mutation disrupts estrous cyclicity and maintenance of pregnancy. Curr Biol 14:1367-1373. CrossRef Medline
27. Miller BH, Olson SL, Levine JE, Turek FW, Horton TH, Takahashi JS (2006) Vasopressin regulation of the proestrous luteinizing hormone surge in wild-type and Clock mutant mice. Biol Reprod 75:778-784. CrossRef Medline
28. Moore RY, Eichler VB (1972) Loss of a circadian adrenal corticosterone rhythm following suprachiasmatic lesions in the rat. Brain Res 42:201-206. CrossRef Medline
29. Owen BM, Bookout AL, Ding X, Lin VY, Atkin SD, Gautron L, Kliewer SA, Mangelsdorf DJ (2013) FGF21 contributes to neuroendocrine control of female reproduction. Nat Med 19:1153-1156. CrossRef Medline
30. Palm IF, Van Der Beek EM, Wiegant VM, Buijs RM, Kalsbeek A (1999) Vasopressin induces a luteinizing hormone surge in ovariectomized, estradiol-treated rats with lesions of the suprachiasmatic nucleus. Neuroscience 93:659-666. CrossRef Medline
31. Palm IF, van der Beek EM, Wiegant VM, Buijs RM, Kalsbeek A (2001) The stimulatory effect of vasopressin on the luteinizing hormone surge in ovariectomized, estradiol-treated rats is time-dependent. Brain Res 901: 109-116. CrossRef Medline
32. Partch CL, Green CB, Takahashi JS (2014) Molecular architecture of the mammalian circadian clock. Trends Cell Biol 24:90-99. CrossRef Medline
33. Piet R, Boehm U, Herbison AE (2013) Estrous cycle plasticity in the hyperpolarization-activated current Ih is mediated by circulating 17β-estradiol in preoptic area kisspeptin neurons. J Neurosci 33:10828-10839. CrossRef Medline
34. Piet R, de Croft S, Liu X, Herbison AE (2015) Electrical properties of kisspeptin neurons and their regulation of GnRH neurons. Front Neuroendocrinol 36C: 15-27. CrossRef Medline
35. Robertson JL, Clifton DK, de la Iglesia HO, Steiner RA, Kauffman AS (2009) Circadian regulation of Kissl neurons: implications for timing the preovulatory gonadotropin-releasing hormone/luteinizing hormone surge. Endocrinology 150:3664-3671. CrossRef Medline
36. Sabatier N, Richard P, Dayanithi G (1997) L-, N-and T-but neither P-nor Q-type Ca2+ channels control vasopressin-induced Ca2+ influx in mag-nocellular vasopressin neurones isolated from the rat supraoptic nucleus. J Physiol 503:253-268. CrossRef Medline
37. Schneider CA, Rasband WS, Eliceiri KW (2012) NIH Image to ImageJ: 25 years of image analysis. Nat Methods 9:671-675. CrossRef Medline
38. Smarr BL, Morris E, de la Iglesia HO (2012) The dorsomedial suprachiasmatic nucleus times circadian expression of Kissl and the luteinizing hormone surge. Endocrinology 153:2839-2850. CrossRef Medline
39. Smarr BL, Gile JJ, de la Iglesia HO (2013) Oestrogen-independent circadian clock gene expression in the anteroventral periventricular nucleus in female rats: possible role as an integrator for circadian and ovarian signals timing the luteinising hormone surge. J Neuroendocrinol 25:1273-1279. CrossRef Medline
40. Smith JT, Popa SM, Clifton DK, Hoffman GE, Steiner RA (2006) Kiss 1 neurons in the forebrain as central processors for generating the preovulatory luteinizing hormone surge. J Neurosci 26:6687-6694. CrossRef Medline
41. Stephan FK, Zucker I (1972) Circadian rhythms in drinking behavior and locomotor activity of rats are eliminated by hypothalamic lesions. Proc Natl Acad Sci U S A 69:1583-1586. CrossRef Medline
42. Stetson MH, Watson-Whitmyre M (1976) Nucleus suprachiasmaticus: the biological clock in the hamster? Science 191:197-199. CrossRef Medline
43. Terasawa E, Rodriguez JS, Bridson WE, Wiegand SJ (1979) Factors influencing the positive feedback action of estrogen upon the luteinizing hormone surge in the ovariectomized guinea pig. Endocrinology 104:680-686. CrossRef Medline
44. Tian L, Hires SA, Mao T, Huber D, Chiappe ME, Chalasani SH, Petreanu L, Akerboom J, McKinney SA, Schreiter ER, Bargmann Cl, Jayaraman V, Svoboda K, Looger LL (2009) Imaging neural activity in worms, flies and mice with improved GCaMP calcium indicators. Nat Methods 6:875-881. CrossRef Medline
45. Uhl GR, Reppert SM (1986) Suprachiasmatic nucleus vasopressin messenger RNA: circadian variation in normal and Brattleboro rats. Science 232:390-393. CrossRef Medline
46. Van der Beek EM, Horvath TL, Wiegant VM, Van den Hurk R, Buijs RM (1997) Evidence for a direct neuronal pathway from the suprachiasmatic nucleus to the gonadotropin-releasing hormone system: combined tracing and light and electron microscopic immunocytochemical studies. J Comp Neurol 384:569-579. CrossRef Medline
47. Vida B, Deli L, Hrabovszky E, Kalamatianos T, Caraty A, Coen CW, Liposits Z, Kalló I (2010) Evidence for suprachiasmatic vasopressin neurones innervating kisspeptin neurones in the rostral periventricular area of the mouse brain: regulation by oestrogen. J Neuroendocrinol 22:1032-1039. CrossRef Medline
48. Watson RE Jr, Langub MC Jr, Engle MG, Maley BE (1995) Estrogen-receptive neurons in the anteroventral periventricular nucleus are synaptic targets of the suprachiasmatic nucleus and peri-suprachiasmatic region. Brain Res 689:254-264. CrossRef Medline
49. Wiegand SJ, Terasawa E, Bridson WE, Goy RW (1980) Effects of discrete lesions of preoptic and suprachiasmatic structures in the female rat. Alterations in the feedback regulation of gonadotropin secretion. Neuroendocrinology 31:147-157. CrossRef Medline
50. Williams WP 3rd, Jarjisian SG, Mikkelsen JD, Kriegsfeld LJ (2011) Circadian control of kisspeptin and a gated GnRH response mediate the preovulatory luteinizing hormone surge. Endocrinology 152:595-606. CrossRef Medline
51. Wintermantel TM, Campbell RE, Porteous R, Bock D, Gröne HJ, Todman MG, Korach KS, Greiner E, Pérez CA, Schütz G, Herbison AE (2006) Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility. Neuron 52:271-280. CrossRef Medline
52. Xu Z, Kaga S, Tsubomizu J, Fujisaki J, Mochiduki A, Sakai T, Tsukamura H, Maeda K, Inoue K, Adachi AA (2011) Circadian transcriptional factor DBP regulates expression of Kissl in the anteroventral periventricular nucleus. Mol Cell Endocrinol 339:90-97. CrossRef Medline
53. Zariwala HA, Borghuis BG, Hoogland TM, Madisen L, Tian L, De Zeeuw Cl, Zeng H, Looger LL, Svoboda K, Chen TW (2012) A Cre-dependent GCaMP3 reporter mouse for neuronal imaging in vivo. J Neurosci 32: 3131-3141. CrossRef Medline
54. Zhang C, Tonsfeldt KJ, Qiu J, Bosch MA, Kobayashi K, Steiner RA, Kelly MJ, Rønnekleiv OK (2013) Molecular mechanisms that drive estradiol-dependent burst firing of Kissl neurons in the rostral periventricular preoptic area. Am J Physiol Endocrinol Me tab 305: E1384-E1397. CrossRef Medline