The Korean Journal of Physiology and Pharmacology

The Korean Society of Pharmacology (대한약리학회)
권호 표지
DOI QR코드

DOI QR Code

Direct Corticosteroid Modulation of GABAergic Neurons in the Anterior Hypothalamic Area of GAD65-eGFP Mice

  • Shin, Seung-Yub (Laboratory of Veterinary Pharmacology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University) ;
  • Han, Tae-Hee (Laboratory of Veterinary Pharmacology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University) ;
  • Lee, So-Yeong (Laboratory of Veterinary Pharmacology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University) ;
  • Han, Seong-Kyu (Department of Oral Physiology and BK21 Program, School of Dentistry and Institute of Oral Bioscience, Chonbuk National University) ;
  • Park, Jin-Bong (Department of Physiology, School of Medicine, Chungnam National University) ;
  • Erdelyi, Ferenc (Laboratory of Molecular Biology and Genetics, Institute of Experimental Medicine) ;
  • Szabo, Gabor (Laboratory of Molecular Biology and Genetics, Institute of Experimental Medicine) ;
  • Ryu, Pan-Dong (Laboratory of Veterinary Pharmacology, College of Veterinary Medicine and Research Institute for Veterinary Science, Seoul National University)
  • Received : 2011.05.02
  • Accepted : 2011.06.15
  • Published : 2011.06.30
Download PDF
⟨ Previous Next ⟩

Abstract

Corticosterone is known to modulate GABAergic synaptic transmission in the hypothalamic paraventricular nucleus. However, the underlying receptor mechanisms are largely unknown. In the anterior hypothalamic area (AHA), the sympathoinhibitory center that project GABAergic neurons onto the PVN, we examined the expression of glucocorticoid receptor (GR) and mineralocorticoid receptor (MR) of GABAergic neurons using intact GAD65-eGFP transgenic mice, and the effects of corticosterone on the burst firing using adrenalectomized transgenic mice. GR or MR immunoreactivity was detected from the subpopulations of GABAergic neurons in the AHA. The AHA GABAergic neurons expressed mRNA of GR (42%), MR (38%) or both (8%). In addition, in brain slices incubated with corticosterone together with RU486 (MR-dominant group), the proportion of neurons showing a burst firing pattern was significantly higher than those in the slices incubated with vehicle, corticosterone, or corticosterone with spironolactone (GR-dominant group; 64 vs. 11~14%, p<0.01 by $x^2$-test). Taken together, the results show that the corticosteroid receptors are expressed on the GABAergic neurons in the AHA, and can mediate the corticosteroid-induced plasticity in the firing pattern of these neurons. This study newly provides the experimental evidence for the direct glucocorticoid modulation of GABAergic neurons in the AHA in the vicinity of the PVN.

Keywords

References

  1. De Kloet ER, Vreugdenhil E, Oitzl MS, Joels M. Brain corticosteroid receptor balance in health and disease. Endocr Rev. 1998;19:269-301. https://doi.org/10.1210/er.19.3.269
  2. de Kloet ER, Joels M, Holsboer F. Stress and the brain: from adaptation to disease. Nat Rev Neurosci. 2005;6:463-475. https://doi.org/10.1038/nrn1683
  3. Karst H, Berger S, Turiault M, Tronche F, Schutz G, Joels M. Mineralocorticoid receptors are indispensable for nongenomic modulation of hippocampal glutamate transmission by corticosterone. Proc Natl Acad Sci USA. 2005;102:19204-19207. https://doi.org/10.1073/pnas.0507572102
  4. Di S, Malcher-Lopes R, Halmos KC, Tasker JG. Nongenomic glucocorticoid inhibition via endocannabinoid release in the hypothalamus: a fast feedback mechanism. J Neurosci. 2003;23:4850-4857.
  5. Herman JP, Cullinan WE, Ziegler DR, Tasker JG. Role of the paraventricular nucleus microenvironment in stress integration. Eur J Neurosci. 2002;16:381-385. https://doi.org/10.1046/j.1460-9568.2002.02133.x
  6. Cullinan WE, Ziegler DR, Herman JP. Functional role of local GABAergic influences on the HPA axis. Brain Struct Funct. 2008;213:63-72. https://doi.org/10.1007/s00429-008-0192-2
  7. Roland BL, Sawchenko PE. Local origins of some GABAergic projections to the paraventricular and supraoptic nuclei of the hypothalamus in the rat. J Comp Neurol. 1993;332:123-143. https://doi.org/10.1002/cne.903320109
  8. Cullinan WE, Herman JP, Watson SJ. Ventral subicular interaction with the hypothalamic paraventricular nucleus: evidence for a relay in the bed nucleus of the stria terminalis. J Comp Neurol. 1993;332:1-20. https://doi.org/10.1002/cne.903320102
  9. Miklos IH, Kovacs KJ. GABAergic innervation of corticotropin-releasing hormone (CRH)-secreting parvocellular neurons and its plasticity as demonstrated by quantitative immunoelectron microscopy. Neuroscience. 2002;113:581-592. https://doi.org/10.1016/S0306-4522(02)00147-1
  10. Yang JH, Li LH, Lee S, Jo IH, Lee SY, Ryu PD. Effects of adrenalectomy on the excitability of neurosecretory parvocellular neurones in the hypothalamic paraventricular nucleus. J Neuroendocrinol. 2007;19:293-301. https://doi.org/10.1111/j.1365-2826.2007.01531.x
  11. Yang JH, Li LH, Shin SY, Lee S, Lee SY, Han SK, Ryu PD. Adrenalectomy potentiates noradrenergic suppression of GABAergic transmission in parvocellular neurosecretory neurons of hypothalamic paraventricular nucleus. J Neurophysiol. 2008;99:514-523. https://doi.org/10.1152/jn.00568.2007
  12. Verkuyl JM, Joels M. Effect of adrenalectomy on miniature inhibitory postsynaptic currents in the paraventricular nucleus of the hypothalamus. J Neurophysiol. 2003;89:237-245. https://doi.org/10.1152/jn.00401.2002
  13. Verkuyl JM, Karst H, Joels M. GABAergic transmission in the rat paraventricular nucleus of the hypothalamus is suppressed by corticosterone and stress. Eur J Neurosci. 2005;21:113-121. https://doi.org/10.1111/j.1460-9568.2004.03846.x
  14. Verkuyl JM, Hemby SE, Joels M. Chronic stress attenuates GABAergic inhibition and alters gene expression of parvocellular neurons in rat hypothalamus. Eur J Neurosci. 2004;20:1665-1673. https://doi.org/10.1111/j.1460-9568.2004.03568.x
  15. Bali B, Erdelyi F, Szabo G, Kovacs KJ. Visualization of stress-responsive inhibitory circuits in the GAD65-eGFP transgenic mice. Neurosci Lett. 2005;380:60-65. https://doi.org/10.1016/j.neulet.2005.01.014
  16. Shin SY, Yang JH, Lee H, Erdelyi F, Szabo G, Lee SY, Ryu PD. Identification of the adrenoceptor subtypes expressed on GABAergic neurons in the anterior hypothalamic area and rostral zona incerta of GAD65-eGFP transgenic mice. Neurosci Lett. 2007;422:153-157. https://doi.org/10.1016/j.neulet.2007.05.060
  17. Oparil S, Chen YF, Peng N, Wyss JM. Anterior hypothalamic norepinephrine, atrial natriuretic peptide, and hypertension. Front Neuroendocrinol. 1996;17:212-246. https://doi.org/10.1006/frne.1996.0006
  18. Kim E, Seo S, Chung H, Park S. Role of glucocorticoids in fasting-induced changes in hypothalamic and pituitary components of the growth hormone (GH)-axis. Korean J Physiol Pharmacol. 2008;12:217-223. https://doi.org/10.4196/kjpp.2008.12.5.217
  19. Han TH, Lee K, Park JB, Ahn D, Park JH, Kim DY, Stern JE, Lee SY, Ryu PD. Reduction in synaptic GABA release contributes to target-selective elevation of PVN neuronal activity in rats with myocardial infarction. Am J Physiol Regul Integr Comp Physiol. 2010;299:R129-139. https://doi.org/10.1152/ajpregu.00391.2009
  20. Krugers HJ, Alfarez DN, Karst H, Parashkouhi K, van Gemert N, Joels M. Corticosterone shifts different forms of synaptic potentiation in opposite directions. Hippocampus. 2005;15:697-703. https://doi.org/10.1002/hipo.20092
  21. Goldberg JH, Lacefield CO, Yuste R. Global dendritic calcium spikes in mouse layer 5 low threshold spiking interneurones: implications for control of pyramidal cell bursting. J Physiol. 2004;558:465-478. https://doi.org/10.1113/jphysiol.2004.064519
  22. Kawaguchi Y, Shindou T. Noradrenergic excitation and inhibition of GABAergic cell types in rat frontal cortex. J Neurosci. 1998;18:6963-6976.
  23. Kim D, Song I, Keum S, Lee T, Jeong MJ, Kim SS, McEnery MW, Shin HS. Lack of the burst firing of thalamocortical relay neurons and resistance to absence seizures in mice lacking alpha(1G) T-type Ca(2+) channels. Neuron. 2001;31:35-45. https://doi.org/10.1016/S0896-6273(01)00343-9
  24. Perez-Reyes E. Molecular physiology of low-voltage-activated t-type calcium channels. Physiol Rev. 2003;83:117-161. https://doi.org/10.1152/physrev.00018.2002
  25. Lee S, Han TH, Sonner PM, Stern JE, Ryu PD, Lee SY. Molecular characterization of T-type Ca(2+) channels responsible for low threshold spikes in hypothalamic paraventricular nucleus neurons. Neuroscience. 2008;155:1195-1203. https://doi.org/10.1016/j.neuroscience.2008.06.055
  26. Lalevee N, Rebsamen MC, Barrere-Lemaire S, Perrier E, Nargeot J, Benitah JP, Rossier MF. Aldosterone increases T-type calcium channel expression and in vitro beating frequency in neonatal rat cardiomyocytes. Cardiovasc Res. 2005;67:216-224. https://doi.org/10.1016/j.cardiores.2005.05.009
  27. Lesouhaitier O, Chiappe A, Rossier MF. Aldosterone increases T-type calcium currents in human adrenocarcinoma (H295R) cells by inducing channel expression. Endocrinology. 2001;142:4320-4330. https://doi.org/10.1210/en.142.10.4320
  28. Rossier MF, Lesouhaitier O, Perrier E, Bockhorn L, Chiappe A, Lalevee N. Aldosterone regulation of T-type calcium channels. J Steroid Biochem Mol Biol. 2003;85:383-388. https://doi.org/10.1016/S0960-0760(03)00201-2
  29. Beurrier C, Congar P, Bioulac B, Hammond C. Subthalamic nucleus neurons switch from single-spike activity to burstfiring mode. J Neurosci. 1999;19:599-609.
  30. Zhan XJ, Cox CL, Rinzel J, Sherman SM. Current clamp and modeling studies of low-threshold calcium spikes in cells of the cat's lateral geniculate nucleus. J Neurophysiol. 1999;81:2360-2373. https://doi.org/10.1152/jn.1999.81.5.2360
  31. Bessaih T, Leresche N, Lambert RC. T current potentiation increases the occurrence and temporal fidelity of synaptically evoked burst firing in sensory thalamic neurons. Proc Natl Acad Sci USA. 2008;105:11376-11381. https://doi.org/10.1073/pnas.0801484105
  32. Herman JP, Tasker JG, Ziegler DR, Cullinan WE. Local circuit regulation of paraventricular nucleus stress integration: glutamate-GABA connections. Pharmacol Biochem Behav. 2002;71:457-468. https://doi.org/10.1016/S0091-3057(01)00681-5
  33. Borkowski KR, Finch L. Cardiovascular changes in anaesthetised rats after the intra-hypothalamic administration of adrenaline. Clin Exp Hypertens. 1978;1:279-291. https://doi.org/10.3109/10641967809068609
  34. Pitts DK, Beuthin FC, Commissaris RL. Cardiovascular effects of perfusion of the rostral rat hypothalamus with clonidine: differential interactions with prazosin and yohimbine. Eur J Pharmacol. 1986;124:67-74. https://doi.org/10.1016/0014-2999(86)90125-1
  35. Poole S. Cardiovascular responses of rats to intrahypothalamic injection of carbachol and noradrenaline. Br J Pharmacol. 1983;79:693-700. https://doi.org/10.1111/j.1476-5381.1983.tb10006.x
  36. Wyss JM, Chen YF, Jin H, Gist R, Oparil S. Spontaneously hypertensive rats exhibit reduced hypothalamic noradrenergic input after NaCl loading. Hypertension. 1987;10:313-320. https://doi.org/10.1161/01.HYP.10.3.313
  37. Chen YF, Meng QC, Wyss JM, Jin H, Oparil S. High NaCl diet reduces hypothalamic norepinephrine turnover in hypertensive rats. Hypertension. 1988;11:55-62. https://doi.org/10.1161/01.HYP.11.1.55
  38. Yang RH, Jin H, Chen SJ, Wyss JM, Oparil S. Blocking hypothalamic AT1 receptors lowers blood pressure in saltsensitive rats. Hypertension. 1992;20:755-762. https://doi.org/10.1161/01.HYP.20.6.755
  39. Oparil S, Yang RH, Jin HG, Chen SJ, Meng QC, Berecek KH, Wyss JM. Role of anterior hypothalamic angiotensin II in the pathogenesis of salt sensitive hypertension in the spontaneously hypertensive rat. Am J Med Sci. 1994;307 Suppl 1:S26-37.
  40. Kubo T, Yamaguchi H, Tsujimura M, Hagiwara Y, Fukumori R. An angiotensin system in the anterior hypothalamic area anterior is involved in the maintenance of hypertension in spontaneously hypertensive rats. Brain Res Bull. 2000;52:291-296. https://doi.org/10.1016/S0361-9230(00)00266-5
  41. Kvetnansky R, Pacak K, Fukuhara K, Viskupic E, Hiremagalur B, Nankova B, Goldstein DS, Sabban EL, Kopin IJ. Sympathoadrenal system in stress. Interaction with the hypothalamicpituitary- adrenocortical system. Ann N Y Acad Sci. 1995;771:131-158. https://doi.org/10.1111/j.1749-6632.1995.tb44676.x
  42. Usuku T, Nishi M, Morimoto M, Brewer JA, Muglia LJ, Sugimoto T, Kawata M. Visualization of glucocorticoid receptor in the brain of green fluorescent protein-glucocorticoid receptor knockin mice. Neuroscience. 2005;135:1119-1128. https://doi.org/10.1016/j.neuroscience.2005.06.071
  43. Ito T, Morita N, Nishi M, Kawata M. In vitro and in vivo immunocytochemistry for the distribution of mineralocorticoid receptor with the use of specific antibody. Neurosci Res. 2000;37:173-182. https://doi.org/10.1016/S0168-0102(00)00112-7
  44. Han F, Ozawa H, Matsuda K, Nishi M, Kawata M. Colocalization of mineralocorticoid receptor and glucocorticoid receptor in the hippocampus and hypothalamus. Neurosci Res. 2005;51:371-381. https://doi.org/10.1016/j.neures.2004.12.013
  45. Sarabdjitsingh RA, Meijer OC, de Kloet ER. Specificity of glucocorticoid receptor primary antibodies for analysis of receptor localization patterns in cultured cells and rat hippocampus. Brain Res. 2010;1331:1-11. https://doi.org/10.1016/j.brainres.2010.03.052

Cited by

  1. The reciprocal regulation of stress hormones and GABA A receptors vol.6, pp.None, 2012, https://doi.org/10.3389/fncel.2012.00004
  2. Stress-induced plasticity of GABAergic inhibition vol.8, pp.None, 2011, https://doi.org/10.3389/fncel.2014.00157
  3. Expression of mineralocorticoid and glucocorticoid receptors in preautonomic neurons of the rat paraventricular nucleus vol.306, pp.5, 2011, https://doi.org/10.1152/ajpregu.00506.2013
  4. Characteristics of GABAergic and cholinergic neurons in perinuclear zone of mouse supraoptic nucleus vol.113, pp.3, 2015, https://doi.org/10.1152/jn.00561.2014
  5. Stress and Sucrose Intake Modulate Neuronal Activity in the Anterior Hypothalamic Area in Rats vol.11, pp.5, 2011, https://doi.org/10.1371/journal.pone.0156563
  6. Neuroactive Steroids and GABAergic Involvement in the Neuroendocrine Dysfunction Associated With Major Depressive Disorder and Postpartum Depression vol.13, pp.None, 2011, https://doi.org/10.3389/fncel.2019.00083
  7. Hypothalamic-pituitary-adrenal axis targets for the treatment of epilepsy vol.746, pp.None, 2021, https://doi.org/10.1016/j.neulet.2020.135618