Differential gene expression in gonadotropin-releasing hormone neurons of male and metestrous female mice

Neuroendocrinology

Volumn 102, Issue 1-2, 2015, Pages 44-59

  Vastagh, Csaba ^a   Rodolosse, Annie ^d   Solymosi, Norbert ^b   Farkas, Imre ^a   Auer, Herbert ^e   Sárvári, Miklós ^a   Liposits, Zsolt ^a,c  

^a INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

^b SZENT ISTVÁN UNIVERSITY   (Hungary)

^c PÁZMÁNY PÉTER CATHOLIC UNIVERSITY   (Hungary)

^d INSTITUTE FOR RESEARCH IN BIOMEDICINE   (Spain)

^e Functional Genomics Consulting   (Spain)

Author keywords

Dimorphism; Gene expression; Gonadotropin releasing hormone; Laser capture microdissection; Microarray; Pico profiling; Real time PCR; Single cell qPCR

Indexed keywords

4 AMINOBUTYRIC ACID A RECEPTOR ALPHA3; 4 AMINOBUTYRIC ACID A RECEPTOR BETA3; 4 AMINOBUTYRIC ACID A RECEPTOR GAMMA2; ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; BETA CATENIN; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CANNABINOID 1 RECEPTOR; CHEMOKINE RECEPTOR CXCR4; CPLX1 PROTEIN; DOCKING PROTEIN; FATTY ACID AMIDASE; GLUTAMINASE; GONADORELIN; IMMUNOGLOBULIN LIKE DOMAIN CONTAINING RECEPTOR 2; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 1; NATRIURETIC PEPTIDE RECEPTOR 2; NERVE CELL ADHESION MOLECULE; NERVE CELL ADHESION MOLECULE 1; NICOTINIC ACETYLCHOLINE RECEPTOR BETA 4 SUBUNIT; POTASSIUM CHANNEL KCNQ2; RAB PROTEIN; STXBP1 PROTEIN; SYNAPTOTAGMIN I; TRANSCRIPTOME; TRANSFORMING GROWTH FACTOR BETA RECEPTOR 3; UNCLASSIFIED DRUG; UNCOUPLING PROTEIN 2; VESICULAR GLUTAMATE TRANSPORTER 2; VOLTAGE GATED CALCIUM CHANNEL; VOLTAGE GATED POTASSIUM CHANNEL; GREEN FLUORESCENT PROTEIN;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL ADHESION; CELL METABOLISM; CELL TRANSPORT; COMPARATIVE STUDY; CONTROLLED STUDY; ESTRUS CYCLE; FEMALE; GENE AMPLIFICATION; GENE CLUSTER; GENE EXPRESSION PROFILING; GLUTAMATERGIC SYNAPSE; HORMONAL REGULATION; LASER CAPTURE MICRODISSECTION; MALE; METESTRUS; MICROARRAY ANALYSIS; MOLECULAR DOCKING; MOUSE; NERVE CELL; NEUROTRANSMISSION; NONHUMAN; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; REPRODUCTION; SEX DIFFERENCE; SIGNAL TRANSDUCTION; TRANSGENIC MOUSE; ANIMAL; BRAIN; C57BL MOUSE; GENETICS; METABOLISM; SEXUAL DEVELOPMENT;

ANIMALS; BRAIN; FEMALE; GONADOTROPIN-RELEASING HORMONE; GREEN FLUORESCENT PROTEINS; MALE; METESTRUS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; NEURONS; SEX CHARACTERISTICS; TRANSCRIPTOME;

EID: 84942191451     PISSN: 00283835     EISSN: 14230194     Source Type: Journal    
DOI: 10.1159/000430818     Document Type: Article

References (118)

1. Neill JD, Plant TM, Pfaff DW, Challis JRG, de Kretser DM, Richards JS, Wassarman PM. Knobil and Neills Physiology of Reproduction, ed 3. Amsterdam, Elsevier, 2006.
2. Wray S, Grant P, Gainer H. Evidence that cells expressing luteinizing hormone-releasing hormone mRNA in the mouse are derived from progenitor cells in the olfactory placode. Proc Natl Acad Sci USA 1989; 86: 8132-8136.
3. Schwanzel-Fukuda M, Pfaff DW. Origin of luteinizing hormone-releasing hormone neurons. Nature 1989; 338: 161-164.
4. Schwanzel-Fukuda M, Zheng LM, Bergen H, Weesner G, Pfaff DW. LHRH neurons: functions and development. Prog Brain Res 1992; 93: 189-201, discussion 201-183.
5. Merchenthaler I, Kovacs G, Lavasz G, Setalo G. The preoptico-infundibular LH-RH tract of the rat. Brain Res 1980; 198: 63-74.
6. Carmel PW, Araki S, Ferin M. Pituitary stalk portal blood collection in rhesus monkeys: evidence for pulsatile release of gonadotropin-releasing hormone (GnRH). Endocrinology 1976; 99: 243-248.
7. Eskay RL, Mical RS, Porter JC. Relationship between luteinizing hormone releasing hormone concentration in hypophysial portal blood and luteinizing hormone release in intact, castrated, and electrochemically-stimulated rats. Endocrinology 1977; 100: 263-270.
8. Merchenthaler I, Gorcs T, Setalo G, Petrusz P, Flerko B. Gonadotropin-releasing hormone (GnRH) neurons and pathways in the rat brain. Cell Tissue Res 1984; 237: 15-29.
9. Sakuma Y. GnRH in the regulation of female rat sexual behavior. Prog Brain Res 2002; 141: 293-301.
10. Sakuma Y, Pfaff DW. LH-RH in the mesencephalic central grey can potentiate lordosis reflex of female rats. Nature 1980; 283: 566-567.
11. Herbison AE, Pape JR. New evidence for estrogen receptors in gonadotropin-releasing hormone neurons. Front Neuroendocrinol 2001; 22: 292-308.
12. Hrabovszky E, Liposits Z. Afferent neuronal control of type-I gonadotropin releasing hormone neurons in the human. Front Endocrinol 2013; 4: 130.
13. Adachi S, Fujioka H, Kakehashi C, Matsuwaki T, Nishihara M, Akema T. Possible involvement of microglia containing cyclooxygenase-1 in the accumulation of gonadotrophin-releasing hormone in the preoptic area in female rats. J Neuroendocrinol 2009; 21: 1029-1037.
14. Fujioka H, Kakehashi C, Funabashi T, Akema T. Immunohistochemical evidence for the relationship between microglia and GnRH neurons in the preoptic area of ovariectomized rats with and without steroid replacement. Endocr J 2013; 60: 191-196.
15. Voigt P, Ma YJ, Gonzalez D, Fahrenbach WH, Wetsel WC, Berg-von der Emde K, Hill DF, Taylor KG, Costa ME, Seidah NG, Ojeda SR. Neural and glial-mediated effects of growth factors acting via tyrosine kinase receptors on luteinizing hormone-releasing hormone neurons. Endocrinology 1996; 137: 2593-2605.
16. Prevot V, Dehouck B, Poulain P, Beauvillain JC, Buee-Scherrer V, Bouret S. Neuronal-glial-Endothelial interactions and cell plasticity in the postnatal hypothalamus: implications for the neuroendocrine control of reproduction. Psychoneuroendocrinology 2007; 32 (suppl 1):S46-S51.
17. Farkas I, Vastagh C, Sarvari M, Liposits Z. Ghrelin decreases firing activity of gonadotropin-releasing hormone (GnRH) neurons in an estrous cycle and endocannabinoid signaling dependent manner. PLoS One 2013; 8:e78178.
18. Ahima RS, Harlan RE. Glucocorticoid receptors in LHRH neurons. Neuroendocrinology 1992; 56: 845-850.
19. Klenke U, Taylor-Burds C, Wray S. Metabolic influences on reproduction: adiponectin attenuates GnRH neuronal activity in female mice. Endocrinology 2014; 155: 1851-1863.
20. Knobil E. The GnRH pulse generator. Am J Obstet Gynecol 1990; 163: 1721-1727.
21. Karsch FJ, Battaglia DF, Breen KM, Debus N, Harris TG. Mechanisms for ovarian cycle disruption by immune/inflammatory stress. Stress 2002; 5: 101-112.
22. Ordog T, Chen MD, OByrne KT, Goldsmith JR, Connaughton MA, Hotchkiss J, Knobil E. On the mechanism of lactational anovulation in the rhesus monkey. Am J Physiol 1998; 274:E665-E676.
23. Liu X, Brown RS, Herbison AE, Grattan DR. Lactational anovulation in mice results from a selective loss of kisspeptin input to GnRH neurons. Endocrinology 2014; 155: 193-203.
24. Knuth UA, Friesen HG. Starvation induced anoestrus: effect of chronic food restriction on body weight, its influence on oestrous cycle and gonadotrophin secretion in rats. Acta Endocrinol 1983; 104: 402-409.
25. Kallo I, Vida B, Bardoczi Z, Szilvasy-Szabo A, Rabi F, Molnar T, Farkas I, Caraty A, Mikkelsen J, Coen CW, Hrabovszky E, Liposits Z. Gonadotropin-releasing hormone neurones innervate kisspeptin neurones in the female mouse brain. Neuroendocrinology 2013; 98: 281-289.
26. Abraham IM, Herbison AE. Major sex differences in non-genomic estrogen actions on intracellular signaling in mouse brain in vivo. Neuroscience 2005; 131: 945-951.
27. Moenter SM, Chu Z. Rapid nongenomic effects of oestradiol on gonadotrophin-releasing hormone neurones. J Neuroendocrinol 2012; 24: 117-121.
28. Varju P, Chang KC, Hrabovszky E, Merchenthaler I, Liposits Z. Temporal profile of estrogen-Dependent gene expression in LHRHproducing GT1-7 cells. Neurochem Int 2009; 54: 119-134.
29. Hrabovszky E, Kallo I, Szlavik N, Keller E, Merchenthaler I, Liposits Z. Gonadotropinreleasing hormone neurons express estrogen receptor-beta. J Clin Endocrinol Metab 2007; 92: 2827-2830.
30. Hrabovszky E, Shughrue PJ, Merchenthaler I, Hajszan T, Carpenter CD, Liposits Z, Petersen SL. Detection of estrogen receptor-beta messenger ribonucleic acid and 125I-Estrogen binding sites in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 2000; 141: 3506-3509.
31. Hrabovszky E, Steinhauser A, Barabas K, Shughrue PJ, Petersen SL, Merchenthaler I, Liposits Z. Estrogen receptor-beta immunoreactivity in luteinizing hormone-releasing hormone neurons of the rat brain. Endocrinology 2001; 142: 3261-3264.
32. Noel SD, Kaiser UB. G protein-coupled receptors involved in GnRH regulation: molecular insights from human disease. Mol Cell Endocrinol 2011; 346: 91-101.
33. Bashour NM, Wray S. Progesterone directly and rapidly inhibits GnRH neuronal activity via progesterone receptor membrane component 1. Endocrinology 2012; 153: 4457-4469.
34. Wintermantel TM, Campbell RE, Porteous R, Bock D, Grone HJ, Todman MG, Korach KS, Greiner E, Perez CA, Schutz G, Herbison AE. Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility. Neuron 2006; 52: 271-280.
35. Simonian SX, Spratt DP, Herbison AE. Identification and characterization of estrogen receptor alpha-containing neurons projecting to the vicinity of the gonadotropin-releasing hormone perikarya in the rostral preoptic area of the rat. J Comp Neurol 1999; 411: 346-358.
36. Fekete CS, Strutton PH, Cagampang FR, Hrabovszky E, Kallo I, Shughrue PJ, Dobo E, Mihaly E, Baranyi L, Okada H, Panula P, Merchenthaler I, Coen CW, Liposits ZS. Estrogen receptor immunoreactivity is present in the majority of central histaminergic neurons: evidence for a new neuroendocrine pathway associated with luteinizing hormone-releasing hormone-synthesizing neurons in rats and humans. Endocrinology 1999; 140: 4335-4341.
37. Karsch FJ, Dierschke DK, Weick RF, Yamaji T, Hotchkiss J, Knobil E. Positive and negative feedback control by estrogen of luteinizing hormone secretion in the rhesus monkey. Endocrinology 1973; 92: 799-804.
38. Karsch FJ, Weick RF, Butler WR, Dierschke DJ, Krey LC, Weiss G, Hotchkiss J, Yamaji T, Knobil E. Induced LH surges in the rhesus monkey: strength-Duration characteristics of the estrogen stimulus. Endocrinology 1973; 92: 1740-1747.
39. Gorski RA. Hypothalamic imprinting by gonadal steroid hormones. Adv Exp Med Biol 2002; 511: 57-70, discussion 70-53.
40. Dorsa DM, Smith ER. Facilitation of mounting behavior in male rats by intracranial injections of luteinizing hormone-releasing hormone. Regul Pept 1980; 1: 147-155.
41. Suter KJ, Song WJ, Sampson TL, Wuarin JP, Saunders JT, Dudek FE, Moenter SM. Genetic targeting of green fluorescent protein to gonadotropin-releasing hormone neurons: characterization of whole-cell electrophysiological properties and morphology. Endocrinology 2000; 141: 412-419.
42. Parkening TA, Collins TJ, Smith ER. Plasma and pituitary concentrations of LH, FSH, and prolactin in aging C57BL/6 mice at various times of the estrous cycle. Neurobiol Aging 1982; 3: 31-35.
43. Walmer DK, Wrona MA, Hughes CL, Nelson KG. Lactoferrin expression in the mouse reproductive tract during the natural estrous cycle: correlation with circulating estradiol and progesterone. Endocrinology 1992; 131: 1458-1466.
44. Nelson JF, Felicio LS, Randall PK, Sims C, Finch CE. A longitudinal study of estrous cyclicity in aging C57BL/6J mice. I. Cycle frequency, length and vaginal cytology. Biol Reprod 1982; 27: 327-339.
45. Byers SL, Wiles MV, Dunn SL, Taft RA. Mouse estrous cycle identification tool and images. PLoS One 2012; 7:e35538.
46. Khodosevich K, Inta D, Seeburg PH, Monyer H. Gene expression analysis of in vivo fluorescent cells. PLoS One 2007; 2:e1151.
47. Paxinos G, Franklin K. The Mouse Brain in Stereotaxic Coordinates, ed 2. San Diego, Academic Press, 2001.
48. Jasoni CL, Todman MG, Han SK, Herbison AE. Expression of mRNAs encoding receptors that mediate stress signals in gonadotropin-releasing hormone neurons of the mouse. Neuroendocrinology 2005; 82: 320-328.
49. Zhang C, Bosch MA, Levine JE, Ronnekleiv OK, Kelly MJ. Gonadotropin-releasing hormone neurons express K(ATP) channels that are regulated by estrogen and responsive to glucose and metabolic inhibition. J Neurosci 2007; 27: 10153-10164.
50. Parman C, Halling C, Gentleman R. QC Report Generation for affyBatch Objects. R package version 1.42.0., 2014.
51. Irizarry RA, Hobbs B, Collin F, Beazer-Barclay YD, Antonellis KJ, Scherf U, Speed TP. Exploration, normalization, and summaries of high density oligonucleotide array probe level data. Biostatistics 2003; 4: 249-264.
52. Smyth GK. Linear models and empirical Bayes methods for assessing differential expression in microarray experiments. Stat Appl Genet Mol Biol 2004; 3:article 3.
53. Benjamini Y, Hochberg Y. Controlling the false discovery rate: a practical and powerful approach to multiple testing. J Royal Stat Soc Ser B 1995; 57: 289-300.
54. R Core Team: R. A Language and Environment for Statistical Computing. Vienna, The R Foundation for Statistical Computing, 2013.
55. Gentleman RC, Carey VJ, Bates DM, et al. Bioconductor: open software development for computational biology and bioinformatics. Genome Biol 2004; 5:R80.
56. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009; 4: 44-57.
57. Huang da W, Sherman BT, Lempicki RA. Bioinformatics enrichment tools: paths toward the comprehensive functional analysis of large gene lists. Nucleic Acids Res 2009; 37: 1-13.
58. Gonzalez-Roca E, Garcia-Albeniz X, Rodriguez-Mulero S, Gomis RR, Kornacker K, Auer H. Accurate expression profiling of very small cell populations. PLoS One 2010; 5: e14418.
59. Jensen LJ, Kuhn M, Stark M, Chaffron S, Creevey C, Muller J, Doerks T, Julien P, Roth A, Simonovic M, Bork P, von Mering C. String 8-A global view on proteins and their functional interactions in 630 organisms. Nucleic Acids Res 2009; 37:D412-D416.
60. Herbison AE, Moenter SM. Depolarising and hyperpolarising actions of GABA(A) receptor activation on gonadotrophin-releasing hormone neurones: towards an emerging consensus. J Neuroendocrinol 2011; 23: 557-569.
61. Iremonger KJ, Constantin S, Liu X, Herbison AE. Glutamate regulation of GnRH neuron excitability. Brain Res 2010; 1364: 35-43.
62. Decavel C, Van den Pol AN. GABA: a dominant neurotransmitter in the hypothalamus. J Compar Neurol 1990; 302: 1019-1037.
63. van den Pol AN. Glutamate and aspartate immunoreactivity in hypothalamic presynaptic axons. J Neurosci 1991; 11: 2087-2101.
64. Donoso AO, Lopez FJ, Negro-Vilar A. Crosstalk between excitatory and inhibitory amino acids in the regulation of luteinizing hormone-releasing hormone secretion. Endocrinology 1992; 131: 1559-1561.
65. Nikolarakis KE, Loeffler JP, Almeida OF, Herz A. Pre-And postsynaptic actions of GABA on the release of hypothalamic gonadotropin-releasing hormone (GnRH). Brain Res Bull 1988; 21: 677-683.
66. Bosma MM. Ion channel properties and episodic activity in isolated immortalized gonadotropin-releasing hormone (GnRH) neurons. J Membr Biol 1993; 136: 85-96.
67. Favit A, Wetsel WC, Negro-Vilar A. Differential expression of gamma-Aminobutyric acid receptors in immortalized luteinizing hormone-releasing hormone neurons. Endocrinology 1993; 133: 1983-1989.
68. Jarry H, Leonhardt S, Wuttke W. Gammaaminobutyric acid neurons in the preoptic/anterior hypothalamic area synchronize the phasic activity of the gonadotropin-releasing hormone pulse generator in ovariectomized rats. Neuroendocrinology 1991; 53: 261-267.
69. 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.
70. Spergel DJ, Kruth U, Hanley DF, Sprengel R, Seeburg PH. GABA-And glutamate-Activated channels in green fluorescent protein-Tagged gonadotropin-releasing hormone neurons in transgenic mice. J Neurosci 1999; 19: 2037-2050.
71. Kuehl-Kovarik MC, Pouliot WA, Halterman GL, Handa RJ, Dudek FE, Partin KM. Episodic bursting activity and response to excitatory amino acids in acutely dissociated gonadotropin-releasing hormone neurons genetically targeted with green fluorescent protein. J Neurosci 2002; 22: 2313-2322.
72. Ottem EN, Godwin JG, Petersen SL. Glutamatergic signaling through the n-methyl-Daspartate receptor directly activates medial subpopulations of luteinizing hormone-releasing hormone (LHRH) neurons, but does not appear to mediate the effects of estradiol on LHRH gene expression. Endocrinology 2002; 143: 4837-4845.
73. DeFazio RA, Heger S, Ojeda SR, Moenter SM. Activation of A-Type gamma-Aminobutyric acid receptors excites gonadotropin-releasing hormone neurons. Mol Endocrinol 2002; 16: 2872-2891.
74. Moenter SM, DeFazio RA. Endogenous gamma-Aminobutyric acid can excite gonadotropin-releasing hormone neurons. Endocrinology 2005; 146: 5374-5379.
75. Yin C, Ishii H, Tanaka N, Sakuma Y, Kato M. Activation of A-Type gamma-Amino butyric acid receptors excites gonadotrophin-releasing hormone neurones isolated from adult rats. J Neuroendocrinol 2008; 20: 566-575.
76. Christian CA, Moenter SM. The neurobiology of preovulatory and estradiol-induced gonadotropin-releasing hormone surges. Endocr Rev 2010; 31: 544-577.
77. Pape JR, Skynner MJ, Sim JA, Herbison AE. Profiling gamma-Aminobutyric acid (GABA(A)) receptor subunit mRNA expression in postnatal gonadotropin-releasing hormone (GNRH) neurons of the male mouse with single cell RT-PCR. Neuroendocrinology 2001; 74: 300-308.
78. Lee K, Porteous R, Campbell RE, Luscher B, Herbison AE. Knockdown of GABA(A) receptor signaling in GnRH neurons has minimal effects upon fertility. Endocrinology 2010; 151: 4428-4436.
79. Liu X, Herbison AE. Estrous cycle-And sexdependent changes in pre-And postsynaptic GABA B control of GnRH neuron excitability. Endocrinology 2011; 152: 4856-4864.
80. Christian CA, Pielecka-Fortuna J, Moenter SM. Estradiol suppresses glutamatergic transmission to gonadotropin-releasing hormone neurons in a model of negative feedback in mice. Biol Reprod 2009; 80: 1128-1135.
81. Constantin S, Jasoni CL, Wadas B, Herbison AE. Gamma-Aminobutyric acid and glutamate differentially regulate intracellular calcium concentrations in mouse gonadotropinreleasing hormone neurons. Endocrinology 2010; 151: 262-270.
82. Ottem EN, Godwin JG, Krishnan S, Petersen SL. Dual-phenotype GABA/glutamate neurons in adult preoptic area: sexual dimorphism and function. J Neurosci 2004; 24: 8097-8105.
83. Krsmanovic LZ, Mores N, Navarro CE, Saeed SA, Arora KK, Catt KJ. Muscarinic regulation of intracellular signaling and neurosecretion in gonadotropin-releasing hormone neurons. Endocrinology 1998; 139: 4037-4043.
84. Morales A, Diaz M, Ropero AB, Nadal A, Alonso R. Estradiol modulates acetylcholineinduced Ca 2+ signals in LHRH-releasing GT1-7 cells through a membrane binding site. Eur J Neurosci 2003; 18: 2505-2514.
85. Turi GF, Liposits Z, Hrabovszky E. Cholinergic afferents to gonadotropin-releasing hormone neurons of the rat. Neurochem Int 2008; 52: 723-728.
86. Todman MG, Han SK, Herbison AE. Profiling neurotransmitter receptor expression in mouse gonadotropin-releasing hormone neurons using green fluorescent protein-promoter transgenics and microarrays. Neuroscience 2005; 132: 703-712.
87. Nunemaker CS, DeFazio RA, Moenter SM. Calcium current subtypes in GnRH neurons. Biol Reprod 2003; 69: 1914-1922.
88. Herbison AE, Pape JR, Simonian SX, Skynner MJ, Sim JA. Molecular and cellular properties of GnRH neurons revealed through transgenics in the mouse. Mol Cell Endocrinol 2001; 185: 185-194.
89. Hemond PJ, OBoyle MP, Roberts CB, Delgado-Reyes A, Hemond Z, Suter KJ. Simulated GABA synaptic input and l-Type calcium channels form functional microdomains in hypothalamic gonadotropin-releasing hormone neurons. J Neurosci 2012; 32: 8756-8766.
90. Watanabe M, Sakuma Y, Kato M. High expression of the r-Type voltage-gated Ca 2+channel and its involvement in Ca 2+-Dependent gonadotropin-releasing hormone release in GT1-7 cells. Endocrinology 2004; 145: 2375-2383.
91. Bosch MA, Tonsfeldt KJ, Ronnekleiv OK: mRNA expression of ion channels in GnRH neurons: subtype-specific regulation by 17beta-Estradiol. Mol Cell Endocrinol 2013; 367: 85-97.
92. Xu C, Roepke TA, Zhang C, Ronnekleiv OK, Kelly MJ. Gonadotropin-releasing hormone (GnRH) activates the m-current in GnRH neurons: an autoregulatory negative feedback mechanism? Endocrinology 2008; 149: 2459-2466.
93. Ankarberg C, Norjavaara E. Diurnal rhythm of testosterone secretion before and throughout puberty in healthy girls: correlation with 17beta-Estradiol and dehydroepiandrosterone sulfate. J Clin Endocrinol Metab 1999; 84: 975-984.
94. Blank SK, McCartney CR, Chhabra S, Helm KD, Eagleson CA, Chang RJ, Marshall JC. Modulation of gonadotropin-releasing hormone pulse generator sensitivity to progesterone inhibition in hyperandrogenic adolescent girls-implications for regulation of pubertal maturation. J Clin Endocrinol Metab 2009; 94: 2360-2366.
95. Pastor CL, Griffin-Korf ML, Aloi JA, Evans WS, Marshall JC. Polycystic ovary syndrome: evidence for reduced sensitivity of the gonadotropin-releasing hormone pulse generator to inhibition by estradiol and progesterone. J Clin Endocrinol Metab 1998; 83: 582-590.
96. Bhattarai JP, Kaszas A, Park SA, Yin H, Park SJ, Herbison AE, Han SK, Abraham IM. Somatostatin inhibition of gonadotropin-releasing hormone neurons in female and male mice. Endocrinology 2010; 151: 3258-3266.
97. Koyama M, Yin C, Ishii H, Sakuma Y, Kato M. Somatostatin inhibition of GnRH neuronal activity and the morphological relationship between GnRH and somatostatin neurons in rats. Endocrinology 2012; 153: 806-814.
98. Olcese J, Middendorff R, Munker M, Schmidt C, McArdle CA. Natriuretic peptides stimulate cyclic GMP production in an immortalized LHRH neuronal cell line. J Neuroendocrinol 1994; 6: 127-130.
99. Middendorff R, Paust HJ, Davidoff MS, Olcese J. Synthesis of C-Type natriuretic peptide (CNP) by immortalized LHRH cells. J Neuroendocrinol 1997; 9: 177-182.
100. Schwarting GA, Henion TR, Nugent JD, Caplan B, Tobet S. Stromal cell-Derived factor-1 (chemokine C-X-C motif ligand 12) and chemokine C-X-C motif receptor 4 are required for migration of gonadotropin-releasing hormone neurons to the forebrain. J Soc Neurosci 2006; 26: 6834-6840.
101. Toba Y, Tiong JD, Ma Q, Wray S. CXCR4/SDF-1 system modulates development of GnRH-1 neurons and the olfactory system. Dev Neurobiol 2008; 68: 487-503.
102. Casoni F, Hutchins BI, Donohue D, Fornaro M, Condie BG, Wray S. SDF and GABA interact to regulate axophilic migration of GnRH neurons. J Cell Sci 2012; 125: 5015-5025.
103. Bovolin P, Cottone E, Pomatto V, Fasano S, Pierantoni R, Cobellis G, Meccariello R. Endocannabinoids are involved in male vertebrate reproduction: regulatory mechanisms at central and gonadal level. Front Endocrinol 2014; 5: 54.
104. Gammon CM, Freeman GM Jr, Xie W, Petersen SL, Wetsel WC. Regulation of gonadotropin-releasing hormone secretion by cannabinoids. Endocrinology 2005; 146: 4491-4499.
105. Scorticati C, Fernandez-Solari J, De Laurentiis A, Mohn C, Prestifilippo JP, Lasaga M, Seilicovich A, Billi S, Franchi A, McCann SM, Rettori V. The inhibitory effect of anandamide on luteinizing hormone-releasing hormone secretion is reversed by estrogen. Proc Natl Acad Sci USA 2004; 101: 11891-11896.
106. Wittmann G, Deli L, Kallo I, Hrabovszky E, Watanabe M, Liposits Z, Fekete C. Distribution of type 1 cannabinoid receptor (CB1)-immunoreactive axons in the mouse hypothalamus. J Comp Neurology 2007; 503: 270-279.
107. Perera AD, Lagenaur CF, Plant TM. Postnatal expression of polysialic acid-neural cell adhesion molecule in the hypothalamus of the male rhesus monkey (Macaca mulatta) . Endocrinology 1993; 133: 2729-2735.
108. Franceschini I, Desroziers E, Caraty A, Duittoz A. The intimate relationship of gonadotropin-releasing hormone neurons with the polysialylated neural cell adhesion molecule revisited across development and adult plasticity. Eur J Neurosci 2010; 32: 2031-2041.
109. Parkash J, Kaur G. Neuronal-glial plasticity in gonadotropin-releasing hormone release in adult female rats: role of the polysialylated form of the neural cell adhesion molecule. J Endocrinol 2005; 186: 397-409.
110. Okamoto M, Sudhof TC. Mints, Munc18-interacting proteins in synaptic vesicle exocytosis. J Biol Chem 1997; 272: 31459-31464.
111. Schiavo G, Stenbeck G, Rothman JE, Sollner TH. Binding of the synaptic vesicle v-SNARE, synaptotagmin, to the plasma membrane t-SNARE, SNAP-25, can explain docked vesicles at neurotoxin-Treated synapses. Proc Natl Acad Sci USA 1997; 94: 997-1001.
112. Tang J, Maximov A, Shin OH, Dai H, Rizo J, Sudhof TC. A complexin/synaptotagmin 1 switch controls fast synaptic vesicle exocytosis. Cell 2006; 126: 1175-1187.
113. Brose N, Petrenko AG, Sudhof TC, Jahn R. Synaptotagmin: a calcium sensor on the synaptic vesicle surface. Science 1992; 256: 1021-1025.
114. Luan X, Luo L, Cao Z, Li R, Liu D, Gao M, Liu M, Wang L. Molecular cloning and expression analysis of the synaptotagmin-1 gene in the hypothalamus and pituitary of Huoyan goose during different stages of the egg-laying cycle. Reprod Biol Endocrinol 2014; 12: 83.
115. Auger AP, Hexter DP, McCarthy MM. Sex difference in the phosphorylation of camp response element binding protein (CREB) in neonatal rat brain. Brain Res 2001; 890: 110-117.
116. Abraham IM, Han SK, Todman MG, Korach KS, Herbison AE. Estrogen receptor beta mediates rapid estrogen actions on gonadotropin-releasing hormone neurons in vivo. J Neurosci 2003; 23: 5771-5777.
117. Kwakowsky A, Cheong RY, Herbison AE, Abraham IM. Non-classical effects of estradiol on camp responsive element binding protein phosphorylation in gonadotropinreleasing hormone neurons: mechanisms and role. Front Neuroendocrinol 2014; 35: 31-41.
118. Peterson MP, Rosvall KA, Choi JH, Ziegenfus C, Tang H, Colbourne JK, Ketterson ED. Testosterone affects neural gene expression differently in male and female juncos: a role for hormones in mediating sexual dimorphism and conflict. PLoS One 2013; 8: e61784.