Glutamatergic innervation of growth hormone-releasing hormone-containing neurons in the hypothalamic arcuate nucleus and somatostatin-containing neurons in the anterior periventricular nucleus of the rat

Brain Research Bulletin

Volumn 70, Issue 4-6, 2006, Pages 278-288

  Kiss, József ^a   Csaba, Zsolt ^a   Csáki, Ágnes ^a   Halász, Béla ^a  

^a SEMMELWEIS UNIVERSITY   (Hungary)

Author keywords

Asymmetric synapse; Excitatory amino acids; Growth hormone regulation; Neuromorphology; SRIF; Vesicular glutamate transporter

Indexed keywords

BIOLOGICAL MARKER; GLUTAMIC ACID; GROWTH HORMONE RELEASING FACTOR; SOMATOSTATIN; VESICULAR GLUTAMATE TRANSPORTER 2;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARCUATE NUCLEUS; ARTICLE; BRAIN NUCLEUS; BRAIN VENTRICLE; CELL LABELING; CELL STRUCTURE; CONTROLLED STUDY; ELECTRON MICROSCOPE; ENZYME ACTIVITY; HORMONE RELEASE; HYPOPHYSIS; HYPOTHALAMUS; IMMUNOREACTIVITY; INNERVATION; MALE; NERVE CELL; NONHUMAN; OBSERVATION; PORTAL VEIN BLOOD; PRIORITY JOURNAL; RAT; SYNAPSE;

ANIMALS; ARCUATE NUCLEUS; GLUTAMIC ACID; GROWTH HORMONE-RELEASING HORMONE; IMMUNOHISTOCHEMISTRY; MALE; MICROSCOPY, CONFOCAL; MICROSCOPY, IMMUNOELECTRON; NEURONS; PARAVENTRICULAR HYPOTHALAMIC NUCLEUS; RATS; RATS, SPRAGUE-DAWLEY; SOMATOSTATIN; VESICULAR GLUTAMATE TRANSPORT PROTEIN 2;

EID: 33749259248     PISSN: 03619230     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainresbull.2006.05.006     Document Type: Article

References (60)

1. Acs Z., Lonart G., and Makara G.B. Role of hypothalamic factors (growth-hormone-releasing hormone and gamma-aminobutyric acid) in the regulation of growth hormone secretion in the neonatal and adult rat. J. Neuroendocrinol. 52 (1990) 156-160
2. Alonso G., Tapia-Arancibia L., and Assenmacher I. Electron microscopic immunocytochemical study of somatostatin neurons in the periventricular nucleus of the rat hypothalamus with special reference to their relationships with homologous neuronal processes. Neuroscience 16 (1985) 297-306
3. Bassant M.H., Simon A., Poindessous-Jazat F., Csaba Z., Epelbaum J., and Dournaud P. Medial septal GABAergic neurons express the somatostatin sst2A receptor: functional consequences on unit firing and hippocampal theta. J. Neurosci. 25 (2005) 2032-2041
4. Behnke O., Ammitzboll T., Jessen H., Klokker M., Nilausen K., Tranumjenssen K., and Olsson L. Nonspecific-binding of protein-stabilized gold sols as a source of error in immunocytochemistry. Eur. J. Cell. Biol. 41 (1986) 326-338
5. Bellocchio E.E., Reimer R.J., Fremeau R.T., and Edwards R.H. Uptake of glutamate into synaptic vesicles by an inorganic phosphate transporter. Science 289 (2000) 957-960
6. Brann D.W., and Mahesh V.B. Excitatory amino acids: evidence for a role in the control of reproduction and anterior pituitary hormone secretion. Endocr. Rev. 18 (1997) 678-700
7. Chautard T., Boudouresque F., Guillaume V., and Oliver C. Effect of excitatory amino acid on the hypothalamo-pituitary-adrenal axis in the rat during the stress-hyporesponsive period. Neuroendocrinology 57 (1993) 70-80
8. Cocchi D., and Cattaneo L. Role of excitatory amino acids in the regulation of growth hormone secretion. In: Brann D.W., and Mahesh V.B. (Eds). Excitatory Amino Acids: Their Role in Neuroendocrine Regulation (1996), CRC Press, Boca Raton, FL 187-203
9. Cocilovo L., Colonna V., Zoli M., Biagini G., Settembrini B.P., Muller E.E., and Cocchi D. Central mechanisms subserving the impaired growth hormone secretion induced by persistent blockade of NMDA receptors in immature male rats. Neuroendocrinology 55 (1992) 416-421
10. Collin M., Bäckberg M., Ovesjö M.-L., Fisone G., Edwards R.H., Fujiyama F., and Meister B. Plasma membrane and vesicular glutamate transporter mRNAs/proteins in hypothalamic neurons that regulate body weight. Eur. J. Neurosci. 18 (2003) 1265-1278
11. Csaba Z., Pirker S., Lelouvier B., Simon A., Videau C., Epelbaum J., Czech T., Baumgartner C., Sperk G., and Dournaud P. Somatostatin receptor type 2 undergoes plastic changes in the human epileptic dentate gyrus. J. Neuropathol. Exp. Neurol. 64 (2005) 956-969
12. Daikoku S., Hisano S., Kawano H., Chikamori-Aoyama M., Kagotani Y., Zhang R.J., and Chihara K. Ultrastructural evidence for neuronal regulation of growth hormone secretion. Neuroendocrinology 47 (1988) 405-415
13. Estienne M.J., Schillo K.K., Gree M.A., Hileman S.M., and Boling J.A. N-Methyl-d-l-aspartate stimulates growth hormone but not luteinizing hormone secretion in the sheep. Life Sci. 44 (1989) 1527-1533
14. Eyigor O., Centers A., and Jennes L. Distribution of ionotropic glutamate receptor subunit mRNAs in the rat hypothalamus. J. Comp. Neurol. 434 (2001) 101-124
15. Fremeau Jr. R.T., Troyer M.D., Pahner I., Nygaard G.O., Tran C.H., Reimer R.J., Bellocchio E.E., Fortin D., Storm-Mathisen J., and Edwards R.H. The expression of vesicular glutamate transporters defines two classes of excitatory synapse. Neuron 31 (2001) 247-260
16. Gay V.L., and Plant T.M. N-Methyl-d-l-aspartate elicits hypothalamic gonadotropin-releasing hormone release in prepubertal male rhesus monkeys. Endocrinology 120 (1987) 2289-2296
17. Gaykema R.P., and Zaborszky L. Direct catecholaminergic-cholinergic interactions in the basal forebrain. Part II. Substantia nigra-ventral tegmental area projections to cholinergic neurons. J. Comp. Neurol. 374 (1996) 555-577
18. Ghosh P.K., Baskaran N., and van den Pol A.N. Developmentally regulated gene expression of all eight metabotropic glutamate receptors in hypothalamic suprachiasmatic and arcuate nuclei - a PCR analysis. Dev. Brain Res. 102 (1997) 1-12
19. Gras C., Herzog E., Bellenchi G.C., Bernard V., Ravassard P., Pohl M., Gasnier B., Giros B., and El Mestikawy S. A third vesicular glutamate transporter expressed by cholinergic and serotoninergic neurons. J. Neurosci. 22 (2002) 5442-5451
20. Hisano S., and Daikoku S. Existence of mutual synaptic relations between corticotropin-releasing factor-containing and somatostatin-containing neurons in the rat hypothalamus. Brain Res. 545 (1991) 265-275
21. Hisano S., Tsuruo Y., Kagotani Y., Daikoku S., and Chihara K. Immunohistochemical evidence for synaptic connections between neuropeptide Y-containing axons and periventricular somatostatin neurons in the anterior hypothalamus in rats. Brain Res. 520 (1990) 170-177
22. Horváth S., and Palkovits M. Synaptic interactions among growth hormone-releasing hormone (GHRH)-containing neurons in the arcuate nucleus of the rat hypothalamus. Neuroendocrinology 48 (1988) 471-476
23. Hrabovszky E., Turi G.F., Kallo I., and Liposits Zs. Expression of vesicular glutamate transporter-2 in gonadotropin-releasing hormone neurons of the adult male rat. Endocrinology 145 (2004) 4018-4021
24. Hrabovszky E., Turi G.F., and Liposits Zs. Presence of vesicular glutamate transporter-2 in hypophysiotropic somatostatin but not growth hormone-releasing hormone neurons of the male rat. Eur. J. Neurosci. 21 (2005) 2120-2126
25. Hrabovszky E., Wittmann G., Turi G.F., Liposits Zs., and Fekete C. Hypophysiotropic thyrotropin-releasing hormone and corticotropin-releasing hormone neurons of the rat contain vesicular glutamate transporter-2. Endocrinology 146 (2005) 346-347
26. Kakucska I., Tappaz M.L., Gaal Gy., Stoeckel M.E., and Makara G.B. GABAergic innervation of somatostatin-containing neurosecretory cells of the anterior periventricular hypothalamic area: a light and electron microscopy double immunolabelling study. Neuroscience 25 (1988) 585-593
27. Kaneko T., Fujiyama F., and Hioki H. Immunohistochemical localization of candidates for vesicular glutamate transporters in the rat brain. J. Comp. Neurol. 444 (2002) 39-62
28. Kiss J., Kocsis K., Csáki A., Görcs T.J., and Halász B. Metabotropic glutamate receptor in GHRH and β-endorphin neurones of the hypothalamic arcuate nucleus. NeuroReport 8 (1997) 3703-3707
29. Kiss J., Kocsis K., Csáki A., and Halász B. Evidence for vesicular glutamate transporter synapses onto gonadotropin-releasing hormone and other neurons in the rat medial preoptic area. Eur. J. Neurosci. 18 (2003) 3267-3278
30. Kiss J., Csaba Zs., Csáki A., and Halász B. Glutamatergic innervation of neuropeptide Y and pro-opiomelanocortin-containing neurons in the hypothalamic arcuate nucleus of the rat. Eur. J. Neurosci. 21 (2005) 2111-2119
31. Kosaka T., Nagatsu I., Wu J.-H., and Hama K. Use of high concentrations of glutaraldehyde for immunocytochemistry of transmitter synthesizing enzymes in the central nervous system. Neuroscience 18 (1986) 975-990
32. Lin W., McKinney K., Liu L., Lakhlani S., and Jennes L. Distribution of vesicular glutamate transporter-2 messenger ribonucleic acid and protein in the septum-hypothalamus of the rat. Endocrinology 144 (2003) 662-670
33. Lindstrom P., and Ohlsson L. Effect of N-methyl-d-aspartate on isolated rat somatotropes. Endocrinology 131 (1992) 1903-1907
34. Liposits Zs., Merchenthaler I., Paull W.K., and Flerkó B. Synaptic communication between somatostatinergic axons and growth hormone-releasing factor (GRF) synthesizing neurons in the arcuate nucleus of the rat. Histochemistry 89 (1988) 247-252
35. Login I.S. Direct stimulation of pituitary prolactin release by glutamate. Life Sci. 47 (1990) 2269-2275
36. Mason G.A., Bissette G., and Nemeroff C.B. Effects of excitotoxic amino acids on pituitary hormone secretion in the rat. Brain. Res. 289 (1983) 366-369
37. Merchenthaler I., Csontos Cs., Kallo I., and Arimura A. The hypothalamo-infundibular growth hormone-releasing hormone (GHRH) system of the rat. Brain Res. 378 (1986) 297-302
38. Merchenthaler I., Sétáló Gy., Csontos Cs., Petrusz P., Flerkó B., and Negro-Vilar A. Combined retrograde tracing and immunocytochemical identification of luteinizing hormone-releasing hormone- and somatostatin-containing neurons projecting to the median eminence of the rat. Endocrinology 125 (1989) 2812-2821
39. Merchenthaler I., Thomas C.R., and Arimura A. Immunocytochemical localization of growth hormone releasing factor (GHRF)-containing structures in the rat brain using anti-rat GHRF serum. Peptides 5 (1984) 1071-1075
40. Miles R., Tóth K., Gulyás A.I., Hájos N., and Freund T.F. Differences between somatic and dendritic inhibition in the hippocampus. Neuron 16 (1996) 815-823
41. Nemeroff C.B., Mason G.A., Bissette G., Parks D.A., and Schwarcz R. Effects of intra-hypothalamic-injection of quinolinic acid on anterior pituitary hormone secretion in the unanesthetized rat. Neuroendocrinology 41 (1985) 332-337
42. Niimi M., Sato M., Murao K., Takahara J., and Kawanishi K. Effect of excitatory amino acid receptor agonists on secretion of growth hormone as assessed by the reverse hemolytic plaque assay. Neuroendocrinology 60 (1994) 173-178
43. Niimi M., Takahata J., Sato M., and Kawanishi K. Sites of origin of growth hormone-releasing factor-containing neurons projecting to the stalk-median eminence of the rat. Peptides 10 (1989) 605-608
44. Ondo J.G., Pass K.A., and Baldwin R. The effects of neurally active amino acids on pituitary gonadotropin secretion. Neuroendocrinology 21 (1976) 79-87
45. Onishi H., Alazawa C., Shigemoto R., Nakanishi S., and Mizuno N. Distributions of the mRNAs for l-2-amino-4-phosphonobutyrate-sensitive metabotropic glutamate receptors, mGluR4 and mGluR7, in the rat brain. J. Comp. Neurol. 360 (1995) 555-570
46. Petralia R.S., Wang Y.X., and Wenthold R.J. Histological and ultrastructural localization of the kainate receptor subunits KA2 and GluR6/7 in the rat nervous system using selective antipeptide antibodies. J. Comp. Neurol. 349 (1994) 85-110
47. Petralia R.S., Wang Y.X., and Wenthold R.J. The NMDA receptor subunits NR2A and NR2B show histological and ultrastructural localization patterns similar to those of NR1. J. Neurosci. 14 (1994) 6102-6120
48. Petralia R.S., and Wenthold R.J. Light and electron immunocytochemicl localization of AMPA-selective glutamate receptors in the rat brain. J. Comp. Neurol. 318 (1992) 329-354
49. Petralia R.S., Yokotani N., and Wenthold R.J. Light and electron microscope distribution of the NMDA receptor subunit NMDAR1 in the rat nervous system using a selective anti-peptide antibody. J. Neurosci. 14 (1994) 667-696
50. Sato A., Shioda S., and Nakai Y. Catecholaminergic innervation of GRF-containing neurons in the rat hypothalamus revealed by electron-microscopic cytochemistry. Cell Tissue Res. 257 (1989) 31-34
51. Shahab M., Nusser K.D., Griel L.C., and Deaver D.R. Effect of a single intravenous injection of N-methyl-d-l-aspartic acid on secretion of luteinizing hormone and growth hormone in holstein bull calves. J. Neuroendocrinol. 5 (1993) 469-473
52. Shioda S., Kohara H., and Nakai Y. TRH axon terminals in synapsis with GRF neurons in the arcuate nucleus of the rat hypothalamus as revealed by double labeling immunocytochemistry. Brain Res. 402 (1987) 355-358
53. Takamori S., Rhee J.S., Rosenmund C., and Jahn R. Identification of a vesicular glutamate transporter that defines a glutamatergic phenotype in neurons. Nature 407 (2000) 189-194
54. Tal J., Price M.T., and Olney J.W. Neuroactive amino acids influence gonadotropin output by a suprapituitary mechanism in either rodents or primates. Brain Res. 273 (1983) 179-182
55. van den Pol A.N. Glutamate and aspartate immunoreactivity in hypothalamic presynaptic axons. J. Neurosci. 11 (1991) 2087-2101
56. van den Pol A.N., Hermans-Borgmeyer I., Hofer M., Ghosh P., and Heinemann S. Ionotropic glutamate-receptor gene expression in hypothalamus: localization of AMPA, kainate and NMDA receptor RNA with in situ hybridization. J. Comp. Neurol. 338 (1994) 377-390
57. van den Pol A.N., and Trombley P.Q. Glutamate neurons in hypothalamus regulate excitatory transmission. J. Neurosci. 13 (1993) 2829-2836
58. van den Pol A.N., Wuarin J.-P., and Dudek F.E. Glutamate, the dominant excitatory transmitter in neuroendocrine regulation. Science 250 (1990) 1276-1278
59. Willoughby J.O., Beroukas D., and Blessing W.W. Ultrastructural evidence for gamma aminobutyric acid-immunoreactive synapses on somatostatin-immunoreactive perikarya in the periventricular anterior hypothalamus. Neuroendocrinology 46 (1987) 268-272
60. Willoughby J.O., Brogan M., and Kapoor R. Hypothalamic interconnections of somatostatin and growth hormone releasing factor neurons. Neuroendocrinology 50 (1989) 584-591