Lack of functional GABAB receptors alters GnRH physiology and sexual dimorphic expression of GnRH and GAD-67 in the brain

American Journal of Physiology - Endocrinology and Metabolism

Volumn 298, Issue 3, 2010, Pages

  Catalano, Paolo N ^a,b   Di Giorgio, Noelia ^a   Bonaventura, María M ^a   Bettler, Bernhard ^c   Libertun, Carlos ^a,b   Lux Lantos, Victoria A ^a  

^a Facultad de Ciencias Naturales e Instituto M Lillo   (Argentina)

^b UNIVERSIDAD DE BUENOS AIRES   (Argentina)

^c UNIVERSITY OF BASEL   (Switzerland)

Author keywords

Amino acid neurotransmitters; Gonadotropin releasing hormone pulsatility; Gonadotropins

Indexed keywords

4 AMINOBUTYRIC ACID; 4 AMINOBUTYRIC ACID B RECEPTOR; AMINO ACID RECEPTOR AFFECTING AGENT; FOLLITROPIN; GLUTAMATE DECARBOXYLASE 67; GLUTAMIC ACID; GONADORELIN; LUTEINIZING HORMONE; MESSENGER RNA; TAURINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTERIOR HYPOTHALAMUS; ARTICLE; BLOOD SAMPLING; BRAIN; CELL VIABILITY; CONTROLLED STUDY; FEMALE; FRONTAL CORTEX; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HYPOTHALAMUS; KNOCKOUT MOUSE; LUTEINIZING HORMONE RELEASE; MALE; MOUSE; NONHUMAN; OLFACTORY BULB; PARIETAL LOBE; PREOPTIC AREA; PRIORITY JOURNAL; PROTEIN EXPRESSION; RADIOIMMUNOASSAY; REAL TIME POLYMERASE CHAIN REACTION; SEX DIFFERENCE;

ANIMALS; BRAIN; FEMALE; GENE EXPRESSION; GLUTAMATE DECARBOXYLASE; GONADOTROPIN-RELEASING HORMONE; MALE; MICE; MICE, INBRED BALB C; MICE, KNOCKOUT; RECEPTORS, GABA-B; SEX CHARACTERISTICS; SIGNAL TRANSDUCTION; TISSUE DISTRIBUTION;

EID: 77349090172     PISSN: 01931849     EISSN: 15221555     Source Type: Journal    
DOI: 10.1152/ajpendo.00532.2009     Document Type: Article

References (100)

1. Adler BA, Crowley WR. Evidence for aminobutyric acid modulation of ovarian hormonal effects on luteinizing hormone secretion and hypothalamic catecholamine activity in female rats. Endocrinology 118: 91-97, 1986.
2. Akema T, Kimura F. Modulation of pulsatile LH secretion by baclofen, a selective GABA B receptor agonist, in ovariectomized rats. Neuroendocrinology 56: 141-147, 1992.
3. Apud JA, Masotto C, Racagni G. Effect of THIP and SL 76002, two clinically experimented GABA-mimetic compounds, on anterior pituitary GABA receptors and prolactin secretion in the rat. Life Sci 40: 871-881, 1987.
4. Arias P, Feleder C, Rodriguez M, Ginzburg M, Refojo D, Szwarcfarb B, Moguilevsky JA. Repeated intracerebroventricular administration of taurine lowers LH levels and postpones vaginal opening in peripubertal female rats. Brain Res Dev Brain Res 85: 137-139, 1995.
5. Bedecarrats GY, Kaiser UB. Differential regulation of gonadotropin subunit gene promoter activity by pulsatile gonadotropin-releasing hormone (GnRH) in perifused L beta T2 cells: role of GnRH receptor concentration. Endocrinology 144: 1802-1811, 2003.
6. B receptors mediate motility signals for migrating embryonic cortical cells. Cereb Cortex 11: 744-753, 2001.
7. Belluzzi O, Puopolo M, Benedusi M, Kratskin I. Selective neuroinhibitory effects of taurine in slices of rat main olfactory bulb. Neuroscience 124: 929-944, 2004.
8. B expression. Neuroendocrinology 80: 129-142, 2004.
9. Bianchi MS, Lux-Lantos VA, Bettler B, Libertun C. Expression of gamma-aminobutyric acid B receptor subunits in hypothalamus of male and female developing rats. Brain Res Dev Brain Res 160: 124-129, 2005.
10. B receptor subunits. Neuropharmacology 40: 185-192, 2001.
11. Bless EP, Westaway WA, Schwarting GA, Tobet SA. Effects of gamma-aminobutyric acid(A) receptor manipulation on migrating gonadotropin-releasing hormone neurons through the entire migratory route in vivo and in vitro. Endocrinology 141: 1254-1262, 2000.
12. B receptors: structure and function. Pharmacol Rev 54: 247-264, 2002.
13. Castelli MP, Ingianni A, Stefanini E, Gessa GL. Distribution of GABAB receptor mRNAs in the rat brain and peripheral organs. Life Sci 64: 1321-1328, 1999.
14. B1 knockout mice reveal alterations in prolactin levels, gonadotropic axis, and reproductive function. Neuroendocrinology 82: 294-305, 2005.
15. Chiappa SA, Fink G. Releasing factor and hormonal changes in the hypothalamic-pituitary-gonadotrophin and -adrenocorticotrophin systems before and after birth and puberty in male, female and androgenized female rats. J Endocrinol 72: 211-224, 1977.
16. Christian CA, Moenter SM. Estradiol induces diurnal shifts in GABA transmission to gonadotropin-releasing hormone neurons to provide a neural signal for ovulation. J Neurosci 27: 1913-1921, 2007.
17. Clarkson J, Herbison AE. Development of GABA and glutamate signaling at the GnRH neuron in relation to puberty. Mol Cell Endocrinol 254-255: 32-38, 2006.
18. Couse JF, Yates MM, Rodriguez KF, Johnson JA, Poirier D, Korach KS. The intraovarian actions of estrogen receptor-alpha are necessary to repress the formation of morphological and functional Leydig-like cells in the female gonad. Endocrinology 147: 3666-3678, 2006.
19. DeFazio RA, Heger S, Ojeda SR, Moenter SM. Activation of A-type gamma-aminobutyric acid receptors excites gonadotropin-releasing hormone neurons. Mol Endocrinol 16: 2872-2891, 2002.
20. Dellovade T, Schwanzel-Fukuda M, Gordan J, Pfaff D. Aspects of GnRH neurobiology conserved across vertebrate forms. Gen Comp Endocrinol 112: 276-282, 1998.
21. Donoso AO, Seltzer AM, Navarro CE, Cabrera RJ, Lopez FJ, Negro-Vilar A. Regulation of luteinizing hormone-releasing hormone and luteinizing hormone secretion by hypothalamic amino acids. Braz J Med Biol Res 27: 921-932, 1994.
22. Feleder C, Ginzburg M, Wuttke W, Moguilevsky JA, Arias P. GABAergic activation inhibits the hypothalamic-pituitary-ovaric axis and sexual development in the immature female rat. Associated changes in hypothalamic glutamatergic and taurinergic systems. Brain Res Dev Brain Res 116: 151-157, 1999.
23. Fernandez MO, Bianchi MS, Lux-Lantos VA, Libertun C. Neonatal exposure to bisphenol a alters reproductive parameters and gonadotropin releasing hormone signaling in female rats. Environ Health Perspect 117: 757-762, 2009.
24. Fiszer de Plazas S, Becu D, Mitridate de Novara A, Libertun C. GABA receptors in anterior pituitary and brain areas after median eminence lesions. Endocrinology 111: 1974-1978, 1982.
25. Freeman ME. The ovarian cycle of the rat. In: The Physiology of Reproduction, edited by Knobil E, Neill JD. New York: Raven, 1986, p. 2323-2349.
26. Fujioka H, Yamanouchi K, Akema T, Nishihara M. The effects of GABA on embryonic gonadotropin-releasing hormone neurons in rat hypothalamic primary culture. J Reprod Dev 53: 323-331, 2007.
27. B receptors expressed by undifferentiated neural progenitor cells isolated from fetal mouse brain. J Cell Physiol 216: 507-519, 2008.
28. Gamel-Didelon K, Corsi C, Pepeu G, Jung H, Gratzl M, Mayerhofer A. An autocrine role for pituitary GABA: activation of GABA-B receptors and regulation of growth hormone levels. Neuroendocrinology 76: 170-177, 2002.
29. Gamel-Didelon K, Kunz L, Föhr J, Gratzl M, Mayerhofer A. Molecular and physiological evidence for functional gamma-aminobutyric acid (GABA)-C receptors in growth hormone-secreting cells. J Biol Chem 278: 20192-20195, 2003.
30. Garyfallou VT, Lemos D, Urbanski HF. Expression profiling of genes encoding glutamate and GABA receptor subunits in three immortalized GnRH cell lines. Brain Res 1086: 50-54, 2006.
31. Gautron JP, Pattou E, Kordon C. Occurrence of higher molecular forms of LHRH in fractionated extracts from rat hypothalamus, cortex and placenta. Mol Cell Endocrinol 24: 1-15, 1981.
32. Geigerseder C, Doepner R, Thalhammer A, Frungieri MB, Gamel-Didelon K, Calandra RS, Kohn FM, Mayerhofer A. Evidence for a GABAergic system in rodent and human testis: local GABA production and GABA receptors. Neuroendocrinology 77: 314-323, 2003.
33. Gonzalez IA, Diaz-Torga G, Piroli G, Achaval-Zaia R, De Nicola AF, Libertun C, Becu-Villalobos D. Bromocriptine restores angiotensin II response in pituitary hyperplasia. Mol Cell Endocrinol 165: 67-74, 2000.
34. 2 and db-cAMP in rats. Physiol Behav 96: 606-612, 2009.
35. Gore AC. Gonadotropin-releasing hormone (GnRH) neurons: gene expression and neuroanatomical studies. Prog Brain Res 141: 193-208, 2002.
36. Gore AC, Roberts JL, Gibson MJ. Mechanisms for the regulation of gonadotropin-releasing hormone gene expression in the developing mouse. Endocrinology 140: 2280-2287, 1999.
37. Grattan DR, Jasoni CL, Liu X, Anderson GM, Herbison AE. Prolactin regulation of gonadotropin-releasing hormone neurons to suppress luteinizing hormone secretion in mice. Endocrinology 148: 4344-4351, 2007.
38. Grattan DR, Selmanoff M. Sex differences in the activity of gammaaminobutyric acidergic neurons in the rat hypothalamus. Brain Res 775: 244-249, 1997.
39. Grove-Strawser D, Jimenez-Linan M, Rubin BS. Middle-aged female rats lack the dynamic changes in GAD(67) mRNA levels observed in young females on the day of a luteinising hormone surge. J Neuroendocrinol 19: 708-716, 2007.
40. Grumbach MM. The neuroendocrinology of human puberty revisited. Horm Res 57, Suppl 2: 2-14, 2002.
41. Hartman RD, He JR, Barraclough CA. Gamma-aminobutyric acid A and B receptor antagonist increase luteinizing hormone-releasing hormone neuronal responsiveness to intracerebroventricular norepinephrine in ovariectomized estrogen-treated rats. Endocrinology 127: 1336-1345, 1990.
42. He X, Zhang Y, Yan Y, Li Y, Koide SS. Identification of GABABR2 in rat testis and sperm. J Reprod Dev 49: 397-402, 2003.
43. Heger S, Seney M, Bless E, Schwarting GA, Bilger M, Mungenast A, Ojeda SR, Tobet SA. Overexpression of glutamic acid decarboxylase-67 (GAD-67) in gonadotropin-releasing hormone neurons disrupts migratory fate and female reproductive function in mice. Endocrinology 144: 2566-2579, 2003.
44. Hu JH, Zhang JF, Ma YH, Jiang J, Yang N, Li XB, Yu Chi ZG, Fei J, Guo LH. Impaired reproduction in transgenic mice overexpressing gamma-aminobutyric acid transporter I (GAT1). Cell Res 14: 54-59, 2004.
45. Kalra SP, Kalra PS. Neural regulation of luteinizing hormone secretion in the rat. Endocr Rev 4: 311-351, 1981.
46. Kang SH, Seong JY, Cho S, Cho H, Kim K. Acute increase of GABAergic neurotransmission exerts a stimulatory effect on GnRH gene expression in the preoptic/anterior hypothalamic area of ovariectomized, estrogen- and progesterone-treated adult female rats. Neuroendocrinology 61: 486-492, 1995.
47. Karpuk N, Hayar A. Activation of postsynaptic GABAB receptors modulates the bursting pattern and synaptic activity of olfactory bulb juxtaglomerular neurons. J Neurophysiol 99: 308-319, 2008.
48. Kaupmann K, Malitschek B, Schuler B, Heid J, Froestl W, Beck P, Mosbacher J, Bischoff S, Kulik A, Shigemoto R, Karschin A, Bettler B. GABA B receptor subtypes assemble into functional heteromeric complexes. Nature 396: 683-687, 1998.
49. Keller M, Pierman S, Douhard Q, Baum MJ, Bakker J. The vomeronasal organ is required for the expression of lordosis behaviour, but not sex discrimination in female mice. Eur J Neurosci 23: 521-530, 2006.
50. Knobil E. The GnRH pulse generator. Am J Obstet Gynecol 163: 1721-1727, 1990.
51. Lagrange AH, Wagner EJ, Ronnekleiv OK, Kelly MJ. Estrogen rapidly attenuates a GABAB response in hypothalamic neurons. Neuroendocrinology 64: 114-123, 1996.
52. Lee VH, Lee LT, Chow BK. Gonadotropin-releasing hormone: regulation of the GnRH gene. FEBS J 275: 5458-5478, 2008.
53. Leranth C, Maclusky NJ, Sakamoto H, Shanabrough M, Naftolin F. Glutamic acid decarboxylase-containing axons synapse on LHRH neurons in the rat medial preoptic area. Neuroendocrinology 40: 536-539, 1985.
54. Lux-Lantos V, Becu-Villalobos D, Bianchi M, Rey-Roldán EB, Chamson-Reig A, Pignataro O, Libertun C. GABAB receptors in anterior pituitary cells. Mechanism of action coupled to endocrine effects. Neuroendocrinology 73: 334-343, 2001.
55. B receptors in neuroendocrine regulation. Cell Mol Neurobiol 28: 803-817, 2008.
56. Lux-Lantos VAR, Rey EB, Libertun C. Activation of GABA B receptors in the anterior pituitary inhibits prolactin and luteinizing hormone secretion. Neuroendocrinology 56: 687-693, 1992.
57. Maffucci JA, Gore AC. Chapter 2: hypothalamic neural systems controlling the female reproductive life cycle gonadotropin-releasing hormone, glutamate, and GABA. Int Rev Cell Mol Biol 274: 69-127, 2009.
58. Mahesh VB, Brann DW. Regulatory role of excitatory amino acids in reproduction. Endocrine 28: 271-280, 2005.
59. B receptors in the rat central nervous system. J Comp Neurol 405: 299-321, 1999.
60. Marshall JC, Eagleson CA. Neuroendocrine aspects of polycystic ovary syndrome. Endocrinol Metab Clin North Am 28: 295-324, 1999.
61. Martin C, Jacobi JS, Nava G, Jeziorski MC, Clapp C, Martinez de la Escalera G. GABA inhibition of cyclic AMP production in immortalized GnRH neurons is mediated by calcineurin-dependent dephosphorylation of adenylyl cyclase 9. Neuroendocrinology 85: 257-266, 2007.
62. Martinez de la Escalera G, Choi AL, Weiner RI. Generation and synchronization of gonadotropin-releasing hormone (GnRH) pulses: intrinsic properties of the GT1-1 GnRH neuronal cell line. Proc Natl Acad Sci USA 89: 1852-1855, 1992.
63. Martinez de la Escalera G, Choi AL, Weiner RI. Biphasic GABAergic regulation of GnRH secretion in GT1 cell lines. Neuroendocrinology 59: 420-425, 1994.
64. B receptors role in cell migration and positioning within the ventromedial nucleus of the hypothalamus. Neuroscience 151: 1119-1131, 2008.
65. Mitsushima D, Tin-Tin WS, Kimura F. Sexual dimorphism in the GABAergic control of gonadotropin release in intact rats. Neurosci Res 46: 399-405, 2003.
66. Moenter SM, Chu Z, Christian CA. Neurobiological mechanisms underlying oestradiol negative and positive feedback regulation of gonadotrophin-releasing hormone neurones. J Neuroendocrinol 21: 327-333, 2009.
67. Moenter SM, DeFazio AR, Pitts GR, Nunemaker CS. Mechanisms underlying episodic gonadotropin-releasing hormone secretion. Front Neuroendocrinol 24: 79-93, 2003.
68. Moenter SM, DeFazio RA. Endogenous gamma-aminobutyric acid can excite gonadotropin-releasing hormone neurons. Endocrinology 146: 5374-5379, 2005.
69. Mongiat LA, Lux-Lantos VA, Libertun C. Evidences for different gonadotropin-releasing hormone response sites in rat ovarian and pituitary cells. Biol Reprod 71: 464-469, 2004.
70. Naftolin F, Garcia-Segura LM, Horvath TL, Zsarnovszky A, Demir N, Fadiel A, Leranth C, Vondracek-Klepper S, Lewis C, Chang A, Parducz A. Estrogen-induced hypothalamic synaptic plasticity and pituitary sensitization in the control of the estrogen-induced gonadotrophin surge. Reprod Sci 14: 101-116, 2007.
71. Ojeda SR, Prevot V, Heger S, Lomniczi A, Dziedzic B, Mungenast A. The neurobiology of female puberty. Horm Res 60, Suppl 3: 15-20, 2003.
72. Parhar IS. Cell migration and evolutionary significance of GnRH subtypes. Prog Brain Res 141: 3-17, 2002.
73. Petersen SL, Ottem EN, Carpenter CD. Direct and indirect regulation of gonadotropin-releasing hormone neurons by estradiol. Biol Reprod 69: 1771-1778, 2003.
74. Pfaffl MW. A new mathematical model for relative quantification in real-time RT-PCR. Nucleic Acids Res 29: e45, 2001.
75. Pleau JM, Esling A, Geutkens S, Dardenne M, Homo-Delarche F. Pancreatic hormone and glutamic acid decarboxylase expression in the mouse thymus: a real-time PCR study. Biochem Biophys Res Commun 283: 843-848, 2001.
76. Quintanar JL, Salinas E, Gonzalez R. Expression of gonadotropinreleasing hormone receptor in cerebral cortical neurons of embryos and adult rats. Neurosci Lett 411: 22-25, 2007.
77. Richter TA, Terasawa E. Neural mechanisms underlying the pubertal increase in LHRH release in the rhesus monkey. Trends Endocrinol Metab 12: 353-359, 2001.
78. Roberts JL, Mani SK, Woller MJ, Glucksman MJ, Wu TJ. LHRH-(1-5): a bioactive peptide regulating reproduction. Trends Endocrinol Metab 18: 386-392, 2007.
79. B1. Neuron 31: 47-58, 2001.
80. Schwanzel-Fukuda M. Origin and migration of luteinizing hormonereleasing hormone neurons in mammals. Microsc Res Tech 44: 2-10, 1999.
81. Schwarting GA, Raitcheva D, Bless EP, Ackerman SL, Tobet S. Netrin 1-mediated chemoattraction regulates the migratory pathway of LHRH neurons. Eur J Neurosci 19: 11-20, 2004.
82. Schwarz JM, McCarthy MM. Steroid-induced sexual differentiation of the developing brain: multiple pathways, one goal. J Neurochem 105: 1561-1572, 2008.
83. Schwarz JM, McCarthy MM. The role of neonatal NMDA receptor activation in defeminization and masculinization of sex behavior in the rat. Horm Behav 54: 662-668, 2008.
84. 67) mRNA in the rat hypothalamus. Brain Res 878: 11-19, 2000.
85. Silveyra P, Catalano PN, Lux-Lantos V, Libertun C. Impact of proestrous milieu on expression of orexin receptors and prepro-orexin in rat hypothalamus and hypophysis: actions of Cetrorelix and Nembutal. Am J Physiol Endocrinol Metab 292: E820-E828, 2007.
86. Sliwowska JH, Billings HJ, Goodman RL, Lehman MN. Immunocytochemical colocalization of GABA-B receptor subunits in gonadotropin-releasing hormone neurons of the sheep. Neuroscience 141: 311-319, 2006.
87. Sorianello EM, Fernandez MO, Catalano PN, Mongiat LA, Somoza GM, Libertun C, Lux-Lantos VA. Differential gonadotropin releasing hormone (GnRH) expression, autoregulation and effects in two models of rat luteinized ovarian cells. Life Sci 77: 2141-2155, 2005.
88. Stojilkovic SS, Krsmanovic LZ, Spergel DJ, Catt KJ. Gonadotropinreleasing hormone neurons. Intrinsic pulsatility and receptor mediated regulation. Trends Endocrinol Metab 5: 201-208, 1994.
89. Terasawa E. Control of luteinizing hormone-releasing hormone pulse generation in nonhuman primates. Cell Mol Neurobiol 15: 141-164, 1995.
90. Tobet S, Knoll JG, Hartshorn C, Aurand E, Stratton M, Kumar P, Searcy B, McClellan K. Brain sex differences and hormone influences: a moving experience? J Neuroendocrinol 21: 387-392, 2009.
91. Tobet SA, Bless EP, Schwarting GA. Developmental aspect of the gonadotropin-releasing hormone system. Mol Cell Endocrinol 185: 173-184, 2001.
92. Tobet SA, Schwarting GA. Minireview: recent progress in gonadotropin-releasing hormone neuronal migration. Endocrinology 147: 1159-1165, 2006.
93. Veldhuis JD, Johnson ML. Cluster analysis: a simple, versatile, and robust algorithm for endocrine pulse detection. Am J Physiol Endocrinol Metab 250: E486-E493, 1986.
94. Vincent SR, Hokfelt T, Wu JY. GABA neuron systems in hypothalamus and the pituitary gland. Neuroendocrinology 34: 117-125, 1982.
95. Wierman ME, Pawlowski JE, Allen MP, Xu M, Linseman DA, Nielsen-Preiss S. Molecular mechanisms of gonadotropin-releasing hormone neuronal migration. Trends Endocrinol Metab 15: 96-102, 2004.
96. Wildt L, Hausler A, Marshall G, Hutchinson J, Plant T, Belchetz P, Knobil E. Frequency and amplitude of gonadotropin-releasing hormone stimulation and gonadotropin secretion in the Rhesus monkey. Endocrinology 109: 376-385, 1981.
97. Wilson AC, Salamat MS, Haasl RJ, Roche KM, Karande A, Meethal SV, Terasawa E, Bowen RL, Atwood CS. Human neurons express type I GnRH receptor and respond to GnRH I by increasing luteinizing hormone expression. J Endocrinol 191: 651-663, 2006.
98. Wirsig-Wiechmann CR, Wiechmann AF. The prairie vole vomeronasal organ is a target for gonadotropin-releasing hormone. Chem Senses 26: 1193-1202, 2001.
99. Wolfe CA, Van Doren M, Walker HJ, Seney ML, McClellan KM, Tobet SA. Sex differences in the location of immunochemically defined cell populations in the mouse preoptic area/anterior hypothalamus. Brain Res Dev Brain Res 157: 34-41, 2005.
100. Wray S. Development of luteinizing hormone releasing hormone neurones. J Neuroendocrinol 13: 3-11, 2001.