Stress-induced inhibition of LH pulses in female rats: Role of GABA in arcuate nucleus

Journal of Molecular Endocrinology

Volumn 55, Issue 1, 2015, Pages 9-19

  Li, Xiao Feng ^a,b   Shao, Bei ^a   Lin, Cheng Cheng ^a   O’Byrne, Kevin T ^b   Lin, Yuan Shao ^a,b  

^a THE FIRST AFFILIATED HOSPITAL OF WENZHOU MEDICAL UNIVERSITY   (China)

^b KING'S COLLEGE LONDON   (United Kingdom)

Author keywords

Arcuate nucleus; Corticotrophin releasing factor; GABA; Luteinizing hormone; Stress

Indexed keywords

3 AMINOPROPYL(DIETHOXYMETHYL)PHOSPHINIC ACID; 4 AMINOBUTYRIC ACID; BICUCULLINE; CORTICOTROPIN RELEASING FACTOR; ESTRADIOL; GONADORELIN; LIPOPOLYSACCHARIDE; LUTEINIZING HORMONE; 4 AMINOBUTYRIC ACID RECEPTOR; GABA-C RECEPTOR; ORGANOPHOSPHORUS COMPOUND;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ARCUATE NUCLEUS; ARTICLE; BLOOD SAMPLING; CEREBROSPINAL FLUID; CONTROLLED STUDY; FEMALE; GABAERGIC TRANSMISSION; HEART CATHETER; HORMONE RELEASE; IMMOBILIZATION STRESS; LATERAL BRAIN VENTRICLE; LUTEINIZING HORMONE RELEASE; MENTAL STRESS; NONHUMAN; OVARIECTOMY; PRIORITY JOURNAL; PULSE GENERATOR; PULSE RATE; RAT; REPRODUCTION; SIGNAL TRANSDUCTION; ANIMAL; CEREBELLUM NUCLEUS; DRUG EFFECTS; METABOLISM; PHYSIOLOGICAL STRESS; PHYSIOLOGY; PROCEDURES;

ANIMALS; ARCUATE NUCLEUS OF HYPOTHALAMUS; BICUCULLINE; CEREBELLAR NUCLEI; CORTICOTROPIN-RELEASING HORMONE; ESTRADIOL; FEMALE; GAMMA-AMINOBUTYRIC ACID; GONADOTROPIN-RELEASING HORMONE; LUTEINIZING HORMONE; ORGANOPHOSPHORUS COMPOUNDS; PULSE; RATS; RECEPTORS, GABA; STRESS, PHYSIOLOGICAL;

EID: 84940389855     PISSN: 09525041     EISSN: 14796813     Source Type: Journal    
DOI: 10.1530/JME-15-0084     Document Type: Article

References (53)

1. Akema T, He D & Sugiyama H 2005 Lipopolysaccharide increases g-aminobutyric acid synthesis in medial preoptic neurones in association with inhibition of steroid-induced luteinising hormone surge in female rats. Journal of Neuroendocrinology 17 672-678. (doi:10.1111/j.1365-2826.2005.01358.x)
2. Anderson RA & Mitchell R 1986 Effects of g-aminobutyric acid receptor agonists on the secretion of growth hormone, luteinizing hormone, adrenocorticotrophic hormone and thyroid-stimulating hormone from the rat pituitary gland in vitro. Journal of Endocrinology 108 1-8. (doi:10.1677/joe.0.1080001)
3. Bowers G, Cullinan WE & Herman JP 1998 Region-specific regulation of glutamic acid decarboxylase (GAD) mRNA expression in central stress circuits. Journal of Neuroscience 18 5938-5947.
4. Cagampang FR, Maeda KI, Tsukamura H, Ohkura S & Ota K 1991 Involvement of ovarian steroids and endogenous opioids in the fastinginduced suppression of pulsatile LH release in ovariectomized rats. Journal of Endocrinology 129 321-328. (doi:10.1677/joe.0.1290321)
5. Campbell RE, Han SK & Herbison AE 2005 Biocytin filling of adult gonadotropin-releasing hormone neurons in situ reveals extensive, spiny, dendritic processes. Endocrinology 146 1163-1169. (doi:10.1210/en.2004-1369)
6. Castellano JM, Bentsen AH, Romero M, Pineda R, Ruiz-Pino F, Garcia-Galiano D, Sanchez-Garrido MA, Pinilla L, Mikkelsen JD & Tena-Sempere M 2010 Acute inflammation reduces kisspeptin immunoreactivity at the arcuate nucleus and decreases responsiveness to kisspeptin independently of its anorectic effects. American Journal of Physiology. Endocrinology and Metabolism 299 E54-E61. (doi:10.1152/ajpendo.00081.2010)
7. Decavel C & van den Pol AN 1990 GABA: a dominant neurotransmitter in the hypothalamus. Journal of Comparative Neurology 302 1019-1037. (doi:10.1002/cne.903020423)
8. Feleder C, Refojo D, Jarry H, Wuttke W & Moguilevsky JA 1996 Bacterial endotoxin inhibits LHRH secretion following the increased release of hypothalamic GABA levels. Different effects on amino acid neurotransmitter release. Neuroimmunomodulation 3 342-351. (doi:10.1159/000097294)
9. Ferreira SA, Scott CJ, Kuehl DE & Jackson GL 1996 Differential regulation of luteinizing hormone release by g-aminobutyric acid receptor subtypes in the arcuate-ventromedial region of the castrated ram. Endocrinology 137 3453-3460. (doi:10.1210/endo.137.8.8754774)
10. Ferreira SA, Hileman SM, Kuehl DE & Jackson GL 1998 Effects of dialyzing g-aminobutyric acid receptor antagonists into the medial preoptic and arcuate ventromedial region on luteinizing hormone release in male sheep. Biology of Reproduction 58 1038-1046. (doi:10.1095/biolreprod58.4.1038)
11. Goodman RL, Lehman MN, Smith JT, Coolen LM, de Oliveira CV, Jafarzadehshirazi MR, Pereira A, Iqbal J, Caraty A, Ciofi P et al. 2007 Kisspeptin neurons in the arcuate nucleus of the ewe express both dynorphin A and neurokinin B. Endocrinology 148 5752-5760. (doi:10.1210/en.2007-0961)
12. Hahn JD, Kalamatianos T & Coen CW 2003 Studies on the neuroanatomical basis for stress-induced oestrogen-potentiated suppression of reproductive function: evidence against direct corticotropin-releasing hormone projections to the vicinity of luteinizing hormone-releasing hormone cell bodies in female rats. Journal of Neuroendocrinology 15 732-742. (doi:10.1046/j.1365-2826.2003.01056.x)
13. Herbison AE, Augood SJ, Simonian SX & Chapman C 1995 Regulation of GABA transporter activity and mRNA expression by estrogen in rat preoptic area. Journal of Neuroscience 15 8302-8309.
14. Herde MK, Iremonger KJ, Constantin S & Herbison AE 2013 GnRH neurons elaborate a long-range projection with shared axonal and dendritic functions. Journal of Neuroscience 33 12689-12697. (doi:10.1523/JNEUROSCI.0579-13.2013)
15. Hiruma H, Sano A & Kimura F 1994 Injection of bicuculline elicits firing of luteinizing hormone releasing hormone pulse generator in muscimoltreated ovariectomized rats. Brain Research 641 191-197. (doi:10.1016/0006-8993(94)90145-7)
16. Jackson GL & Kuehl D 2002 Gamma-aminobutyric acid (GABA) regulation of GnRH secretion in sheep. Reproduction. Supplement 59 15-24.
17. Kash TL & Winder DG 2006 Neuropeptide Y and corticotropin-releasing factor bi-directionally modulate inhibitory synaptic transmission in the bed nucleus of the stria terminalis. Neuropharmacology 51 1013-1022. (doi:10.1016/j.neuropharm.2006.06.011)
18. Kash SF, Tecott LH, Hodge C & Baekkeskov S 1999 Increased anxiety and altered responses to anxiolytics in mice deficient in the 65-kDa isoform of glutamic acid decarboxylase. PNAS 96 1698-1703. (doi:10.1073/pnas.96.4.1698)
19. Kawakami M, Uemura T & Hayashi R 1982 Electrophysiological correlates of pulsatile gonadotropin release in rats. Neuroendocrinology 35 63-67. (doi:10.1159/000123356)
20. Kimura F, Sano A, Hiruma H & Funabashi T 1993 Effects of g-aminobutyric acid-A receptor antagonist, bicuculline, on the electrical activity of luteinizing hormone-releasing hormone pulse generator in the ovariectomized rat. Neuroendocrinology 57 605-614. (doi:10.1159/000126414)
21. Kinsey-Jones JS, Li XF, Knox AM, Wilkinson ES, Zhu XL, Chaudhary AA, Milligan SR, Lightman SL & O’Byrne KT 2009 Down-regulation of hypothalamic kisspeptin and its receptor, Kiss1r, mRNA expression is associated with stress-induced suppression of luteinising hormone secretion in the female rat. Journal of Neuroendocrinology 21 20-29. (doi:10.1111/j.1365-2826.2008.01807.x)
22. Lee K, Porteous R, Campbell RE, Luscher B & Herbison AE 2010 Knockdown ofGABA(A) receptor signaling inGnRHneuronshasminimal effectsupon fertility. Endocrinology 151 4428-4436. (doi:10.1210/en.2010-0314)
23. Li XF, Kinsey-Jones JS, Cheng Y, Knox AM, Lin Y, Petrou NA, Roseweir A, Lightman SL, Milligan SR, Millar RP et al. 2009 Kisspeptin signalling in the hypothalamic arcuate nucleus regulates GnRH pulse generator frequency in the rat. PLoS ONE 4 e8334. (doi:10.1371/journal.pone.0008334)
24. Li XF, Knox AM & O’Byrne KT 2010 Corticotrophin-releasing factor and stress-induced inhibition of the gonadotrophin-releasing hormone pulse generator in the female. Brain Research 1364 153-163. (doi:10.1016/j.brainres.2010.08.036)
25. Li XF, Lin YS, Kinsey-Jones JS, Milligan SR, Lightman SL & O’Byrne KT 2011 The role of the bed nucleus of the stria terminalis in stress-induced inhibition of pulsatile luteinising hormone secretion in the female rat. Journal of Neuroendocrinology 23 3-11. (doi:10.1111/j.1365-2826.2010.02071.x)
26. Lin Y, Li X, Lupi M, Kinsey-Jones JS, Shao B, Lightman SL & O’Byrne KT 2011 The role of the medial and central amygdala in stress-induced suppression of pulsatile LH secretion in female rats. Endocrinology 152 545-555. (doi:10.1210/en.2010-1003)
27. Lin YS, Li XF, Shao B, Hu MH, Goundry AL, Jeyaram A, Lightman SL & O’Byrne KT 2012 The role of GABAergic signalling in stress-induced suppression of gonadotrophin-releasing hormone pulse generator frequency in female rats. Journal of Neuroendocrinology 24 477-488. (doi:10.1111/j.1365-2826.2011.02270.x)
28. Lohman RJ, Liu L, Morris M & O’Brien TJ 2005 Validation of a method for localised microinjection of drugs into thalamic subregions in rats for epilepsy pharmacological studies. Journal of Neuroscience Methods 146 191-197. (doi:10.1016/j.jneumeth.2005.02.008)
29. MacLusky NJ, Naftolin F & Leranth C 1988 Immunocytochemical evidence for direct synaptic connections between corticotrophin-releasing factor (CRF) and gonadotrophin-releasing hormone (GnRH)-containing neurons in the preoptic area of the rat. Brain Research 439 391-395. (doi:10.1016/0006-8993(88)91501-6)
30. Mansky T, Mestres-Ventura P & Wuttke W 1982 Involvement of GABA in the feedback action of estradiol on gonadotropin and prolactin release: hypothalamic GABA and catecholamine turnover rates. Brain Research 231 353-364. (doi:10.1016/0006-8993(82)90372-9)
31. Masotto C, Wisniewski G & Negro-Vilar A 1989 Different g-aminobutyric acid receptor subtypes are involved in the regulation of opiatedependent and independent luteinizing hormone-releasing hormone secretion. Endocrinology 125 548-553. (doi:10.1210/endo-125-1-548)
32. Merchenthaler I, Thomas CR & Arimura A 1984 Immunocytochemical localization of growth hormone releasing factor (GHRF)-containing structures in the rat brain using anti-rat GHRF serum. Peptides 5 1071-1075. (doi:10.1016/0196-9781(84)90173-6)
33. Mitsushima D, Tin-Tin WS & Kimura F 2003 Sexual dimorphism in the GABAergic control of gonadotropin release in intact rats. Neuroscience Research 46 399-405. (doi:10.1016/S0168-0102(03)00099-3)
34. Moore AM, Prescott M, Marshall CJ, Yip SH & Campbell RE 2015 Enhancement of a robust arcuate GABAergic input to gonadotropinreleasing hormone neurons in a model of polycystic ovarian syndrome. PNAS 112 596-601. (doi:10.1073/pnas.1415038112)
35. Muroya S, Funahashi H, Uramura K, Shioda S & Yada T 2005 Gamma aminobutyric acid regulates glucosensitive neuropeptide Y neurons in arcuate nucleus via A/B receptors. Neuroreport 16 897-901. (doi:10.1097/00001756-200506210-00005)
36. Nakagawa Y, Ishima T, Ishibashi Y, Yoshii T & Takashima T 1996 Involvement of GABA(B) receptor systems in action of antidepressants: baclofen but not bicuculline attenuates the effects of antidepressants on the forced swim test in rats. Brain Research 709 215-220. (doi:10.1016/0006-8993(95)01273-7)
37. Nishihara M & Kimura F 1987 Roles of g-aminobutyric acid and serotonin in the arcuate nucleus in the control of prolactin and luteinizing hormone secretion. Japanese Journal of Physiology 37 955-961. (doi:10.2170/jjphysiol.37.955)
38. Nowak G, Partyka A, Palucha A, Szewczyk B, Wieronska JM, Dybala M, Metz M, Librowski T, Froestl W, Papp M et al. 2006 Antidepressant-like activity of CGP 36742 and CGP 51176, selective GABAB receptor antagonists, in rodents. British Journal of Pharmacology 149 581-590. (doi:10.1038/sj.bjp.0706845)
39. Ohkura S, Tsukamura H & Maeda K 1991 Effects of various types of hypothalamic deafferentation on luteinizing hormone pulses in ovariectomized rats. Journal of Neuroendocrinology 3 503-508. (doi:10.1111/j.1365-2826.1991.tb00310.x)
40. Paxinos G & Watson C 1998 Stereotaxic reference system. In The Rat Brain in Stereotaxic Coordinates, 4 edn, pp 30-36. Eds G Paxinos & C Watson. London, UK: Academic Press.
41. Plant TM, Krey LC, Moossy J, McCormack JT, Hess DL & Knobil E 1978 The arcuate nucleus and the control of gonadotropin and prolactin secretion in the female rhesus monkey (Macaca mulatta). Endocrinology 102 52-62. (doi:10.1210/endo-102-1-52)
42. Pompolo S, Ischenko O, Pereira A, Iqbal J & Clarke IJ 2005 Evidence that projections from the bed nucleus of the stria terminalis and from the lateral and medial regions of the preoptic area provide input to gonadotropin releasing hormone (GNRH) neurons in the female sheep brain. Neuroscience 132 421-436. (doi:10.1016/j.neuroscience.2004.12.042)
43. Ramaswamy S, Guerriero KA, Gibbs RB & Plant TM 2008 Structural interactions between kisspeptin and GnRH neurons in the mediobasal hypothalamus of the male rhesus monkey (Macaca mulatta) as revealed by double immunofluorescence and confocal microscopy. Endocrinology 149 4387-4395. (doi:10.1210/en.2008-0438)
44. Rivier C & Vale W 1985 Effects of corticotropin-releasing factor, neurohypophyseal peptides, and catecholamines on pituitary function. Federation Proceedings 44 189-195.
45. Roberto M, Cruz MT, Gilpin NW, Sabino V, Schweitzer P, Bajo M, Cottone P, Madamba SG, Stouffer DG, Zorrilla EP et al. 2010 Corticotropin releasing factor-induced amygdala g-aminobutyric acid release plays a key role in alcohol dependence. Biological Psychiatry 67 831-839. (doi:10.1016/j.biopsych.2009.11.007)
46. Roozendaal MM, De Kruijf HF, Reuling RJ, Threels A, Swarts JJ, Wiegant VM & Mattheij JA 1997 Inhibition of the LH surge by restraint stress in cyclic rats: studies on the role of GABAA and GABAB receptors. Stress 1 241-248. (doi:10.3109/10253899709013744)
47. Scott CJ & Clarke IJ 1993a Inhibition of luteinizing hormone secretion in ovariectomized ewes during the breeding season by gamma-aminobutyric acid (GABA) is mediated by GABA-A receptors, but not GABA-B receptors. Endocrinology 132 1789-1796. (doi:10.1210/endo.132.4.8384997)
48. Scott CJ & Clarke IJ 1993b Evidence that changes in the function of the subtypes of the receptors for g-amino butyric acid may be involved in the seasonal changes in the negative-feedback effects of estrogen on gonadotropin-releasing hormone secretion and plasma luteinizing hormone levels in the ewe. Endocrinology 133 2904-2912. (doi:10.1210/endo.133.6.8243318)
49. Sirivelu MP, Burnett R, Shin AC, Kim C, MohanKumar PS & MohanKumar SM 2009 Interaction between GABA and norepinephrine in interleukin-1b-induced suppression of the luteinizing hormone surge. Brain Research 1248 107-114. (doi:10.1016/j.brainres.2008.10.057)
50. Terasawa E, Kurian JR, Guerriero KA, Kenealy BP, Hutz ED & Keen KL 2010 Recent discoveries on the control of gonadotrophin-releasing hormone neurones in nonhuman primates. Journal of Neuroendocrinology 22 630-638. (doi:10.1111/j.1365-2826.2010.02027.x)
51. Van Cauter E 1988 Estimating false-positive and false-negative errors in analyses of hormonal pulsatility. American Journal of Physiology 254 E786-E794.
52. Wagner EJ, Bosch MA, Kelly MJ & Ronnekleiv OK 1999 A powerful GABA(B) receptor-mediated inhibition of GABAergic neurons in arcuate nucleus. Neuroreport 10 2681-2687. (doi:10.1097/00001756-199908200-00045)
53. Wintermantel TM, Campbell RE, Porteous R, Bock D, Grone HJ, Todman MG, Korach KS, Greiner E, Perez CA, Schutz G et al. 2006 Definition of estrogen receptor pathway critical for estrogen positive feedback to gonadotropin-releasing hormone neurons and fertility. Neuron 52 271-280. (doi:10.1016/j.neuron.2006.07.023)