Phasic synaptic incorporation of GluR2-lacking AMPA receptors at gonadotropin-releasing hormone neurons is involved in the generation of the luteinizing hormone surge in female rats

Neuroscience

Volumn 248, Issue , 2013, Pages 664-669

  Tada, H ^a   Kuroki, Y ^a   Funabashi, T ^a,b   Kamiya, Y ^c   Goto, T ^a   Suyama, K ^a   Sano, A ^a   Mitsushima, D ^a   Etgen, A M ^d   Takahashi, T ^a,d  

^a YOKOHAMA CITY UNIVERSITY GRADUATE SCHOOL OF MEDICINE   (Japan)

^b ST MARIANNA UNIVERSITY SCHOOL OF MEDICINE   (Japan)

^c NIIGATA UNIVERSITY GRADUATE SCHOOL OF MEDICAL AND DENTAL SCIENCES   (Japan)

^d ALBERT EINSTEIN COLLEGE OF MEDICINE   (United States)

Author keywords

CP AMPA receptor; Estrus cycle; GnRH; Synapse; Trafficking

Indexed keywords

AMPA RECEPTOR; ESTROGEN; GONADORELIN; LUTEINIZING HORMONE;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MIGRATION; CONTROLLED STUDY; FEMALE; HORMONAL REGULATION; JUVENILE ANIMAL; LUTEINIZING HORMONE RELEASE; MALE; NERVE CELL; NONHUMAN; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROESTRUS; RAT; RECEPTOR BLOCKING; STOICHIOMETRY;

1-NAPHTHYL ACETYL SPERMINE; 4-(2-HYDROXYETHYL)-1-PIPERAZINEETHANESULFONIC ACID; 6-CYANO-7-NITROQUINOXALINE-2,3-DIONE; ANALYSIS OF VARIANCE; ANOVA; CALCIUM PERMEABLE AMPA-TYPE GLUTAMATE RECEPTORS; CNQX; CP-AMPA RECEPTOR; CP-AMPARS; EGTA; ESTRUS CYCLE; ETHYLENE GLYCOL TETRAACETIC ACID; GFP; GNRH; GONADOTROPIN-RELEASING HORMONE; GREEN FLUORESCENT PROTEIN; HEPES; LH; LUTEINIZING HORMONE; MEPSCS; MINIATURE EXCITATORY POSTSYNAPTIC CURRENTS; NASPM; OVARIECTOMIZED; OVX; PAIRED-PULSE RATIO; PPR; SYNAPSE; TRAFFICKING;

ANIMALS; ESTROGENS; FEMALE; GONADOTROPIN-RELEASING HORMONE; LUTEINIZING HORMONE; NEURONS; RATS; RATS, WISTAR; RECEPTORS, AMPA; REPRODUCTION; SYNAPSES;

EID: 84881558281     PISSN: 03064522     EISSN: 18737544     Source Type: Journal    
DOI: 10.1016/j.neuroscience.2013.06.040     Document Type: Article

References (30)

1. Bailey J.D., Centers A., Jennes L. Expression of AMPA receptor subunits (GluR1-GluR4) in gonadotrophin-releasing hormone neurones of young and middle-aged persistently oestrous rats during the steroid-induced luteinising hormone surge. J Neuroendocrinol 2006, 18:1-12.
2. Blaustein J.D. The year in neuroendocrinology. Mol Endocrinol 2010, 24:252-260.
3. Bowie D., Mayer M.L. Inward rectification of both AMPA and kainate subtype glutamate receptors generated by polyamine-mediated ion channel block. Neuron 1995, 15:453-462.
4. Brann D.W., Mahesh V.B. Endogenous excitatory amino acid involvement in the preovulatory and steroid-induced surge of gonadotropins in the female rat. Endocrinology 1991, 128:1541-1547.
5. Butcher R.L., Collins W.E., Fugo N.W. Plasma concentration of LH, FSH, prolactin, progesterone and estradiol-17b throughout the 4-day estrous cycle of the rat. Endocrinology 1974, 94:1704-1708.
6. Campbell R.E., Suter K.J. Redefining the gonadotrophin-releasing hormone neurone dendrite. J Neuroendocrinol 2010, 22:650-658.
7. Clem R.L., Barth A. Pathway-specific trafficking of native AMPARs by in vivo experience. Neuron 2006, 49:663-670.
8. Conrad K.L., Tseng K.Y., Uejima J.L., Reimers J.M., Heng L.J., Shaham Y., Marinelli M., Wolf M.E. Formation of accumbens GluR2-lacking AMPA receptors mediates incubation of cocaine craving. Nature 2008, 454:118-121.
9. 2+-permeable AMPA receptors: synaptic plasticity and beyond. Curr Opin Neurobiol 2006, 16:288-297.
10. Iremonger K.J., Constantin S., Liu X., Herbison A.E. Glutamate regulation of GnRH neuron excitability. Brain Res 2010, 1364:35-43.
11. Isaac J.T., Ashby M., McBain C.J. The role of the GluR2 subunit in AMPA receptor function and synaptic plasticity. Neuron 2007, 54:859-871.
12. Jarry H., Leonhardt S., Schwarze T., Wuttke W. Preoptic rather than mediobasal hypothalamic amino acid neurotransmitter release regulates GnRH secretion during the estrogen-induced LH surge in the ovariectomized rat. Neuroendocrinology 1995, 62:479-486.
13. Jitsuki S., Takemoto K., Kawasaki T., Tada H., Takahashi A., Becamel C., Sano A., Yuzaki M., Zukin R.S., Ziff E.B., Kessels H.W., Takahashi T. Serotonin mediates cross-modal reorganization of cortical circuits. Neuron 2011, 69:780-792.
14. Kalra S.P. Mandatory neuropeptide-steroid signaling for the preovulatory luteinizing hormone-releasing hormone discharge. Endocr Rev 1993, 14:507-538.
15. Kato M., Ui-Tei K., Watanabe M., Sakuma Y. Characterization of voltage-gated calcium currents in gonadotropin-releasing hormone neurons tagged with green fluorescent protein in rats. Endocrinology 2003, 144:5118-5125.
16. Kessels H.W., Malinow R. Synaptic AMPA receptor plasticity and behavior. Neuron 2009, 61:340-350.
17. Khan M., De Sevilla L., Mahesh V.B., Brann D.W. Enhanced glutamatergic and decreased GABAergic synaptic appositions to GnRH neurons on proestrus in the rat: modulatory effect of aging. PLoS One 2010, 5:e10172.
18. Kiss J., Kocsis K., Csaki A., Halasz B. Evidence for vesicular glutamate transporter synapses onto gonadotropin-releasing hormone and other neurons in the rat medial preoptic area. Eur J Neurosci 2003, 18:3267-3278.
19. 2+-permeable AMPA receptors in synaptic plasticity and neuronal death. Trends Neurosci 2007, 30:126-134.
20. Mitsushima D., Ishihara K., Sano A., Kessels H.W., Takahashi T. Contextual learning requires synaptic AMPA receptor delivery in the hippocampus. Proc Natl Acad Sci U S A 2011, 108:12503-12508.
21. Miyazaki T., Kunii M., Jitsuki S., Sano A., Kuroiwa Y., Takahashi T. Social isolation perturbs experience-driven synaptic glutamate receptor subunit 4 delivery in the developing rat barrel cortex. Eur J Neurosci 2013, 37:1602-1609.
22. Miyazaki T., Kunii M., Tada H., Sano A., Kuroiwa Y., Goto T., Malinow R., Takahashi T. Developmental AMPA receptor subunit specificity during experience-driven synaptic plasticity in the rat barrel cortex. Brain Res 2012, 1435:1-7.
23. Miyazaki T., Takase K., Nakajima W., Tada H., Ohya D., Sano A., Goto T., Hirase H., Malinow R., Takahashi T. Disrupted cortical function underlies behavior dysfunction due to social isolation. J Clin Invest 2012, 122:2690-2701.
24. Nishihara M., Sano A., Kimura F. Cessation of the electrical activity of gonadotropin-releasing hormone pulse generator during the steroid-induced surge of luteinizing hormone in the rat. Neuroendocrinology 1994, 59:513-519.
25. Ping L., Mahesh V.B., Bhat G.K., Brann D.W. Regulation of gonadotropin-releasing hormone and luteinizing hormone secretion by AMPA receptors. Evidence for a physiological role of AMPA receptors in the steroid-induced luteinizing hormone surge. Neuroendocrinology 1997, 66:246-253.
26. Plant K., Pelkey K.A., Bortolotto Z.A., Morita D., Terashima A., McBain C.J., Collingridge G.L., Isaac J.T. Transient incorporation of native GluR2-lacking AMPA receptors during hippocampal long-term potentiation. Nat Neurosci 2006, 9:602-604.
27. Rumpel S., LeDoux J., Zador A., Malinow R. Postsynaptic receptor trafficking underlying a form of associative learning. Science 2005, 308:83-88.
28. Takahashi T., Svoboda K., Malinow R. Experience strengthening transmission by driving AMPA receptors into synapses. Science 2003, 299:1585-1588.
29. Tsubokawa H., Oguro K., Masuzawa T., Nakaima T., Kawai N. Effects of a spider toxin and its analogue on glutamate-activated currents in the hippocampal CA1 neuron after ischemia. J Neurophysiol 1995, 74:218-225.
30. Witkin J.W., O'Sullivan H., Silverman A.J. Novel associations among gonadotropin-releasing hormone neurons. Endocrinology 1995, 136:4323-4330.