Glucocorticoid negative feedback selectively targets vasopressin transcription in parvocellular neurosecretory neurons

Journal of Neuroscience

Volumn 20, Issue 10, 2000, Pages 3843-3852

  Kovács, Krisztina J ^a,b   Földes, Anna ^b   Sawchenko, Paul E ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b INSTITUTE OF EXPERIMENTAL MEDICINE   (Hungary)

Author keywords

Arginine vasopressin; Corticosterone; Corticotropin releasing factor; CREB; Fos; Glucocorticoids; Negative feedback; Neurosecretory neurons; Paraventricular nucleus

Indexed keywords

VASOPRESSIN;

ANIMAL TISSUE; ARTICLE; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MALE; NEGATIVE FEEDBACK; NEUROENDOCRINE SYSTEM; NEUROSECRETION; NONHUMAN; PRIORITY JOURNAL; RAT; STRESS; TRANSCRIPTION REGULATION;

EID: 0343091962     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/jneurosci.20-10-03843.2000     Document Type: Article

References (62)

1. Akana SF, Cascio CS, Shinsako J, Dallman MF (1985) Corticosterone: narrow range required for normal body and thymus weight and ACTH. Am J Physiol 249:R527-R532.
2. Akana SF, Jacobson L, Cascio CS, Shinsako J, Dallman MF (1988) Constant corticosterone replacement normalizes basal adrenocorticotropin (ACTH) but permits sustained ACTH hypersecretion after stress in adrenalectomized rats. Endocrinology 122:1337-1342.
3. Akerblom IE, Slater EP, Beato M, Baxter JD, Mellon PE (1988) Negative regulation by glucocorticoids through interference with cAMP responsive enhancer. Science 241:350-353.
4. Antoni FA (1986) Hypothalamic control of adrenocorticotropin secretion: advances since the discovery of 41-residue corticotropin-releasing factor. Endocr Rev 7:351-378.
5. Antoni FA (1993) Vasopressinergic control of pituitary adrenocorticotropin secretion comes of age. Front Neuroendocrinol 14:76-122.
6. Armstrong RC, Montminy MM (1993) Transsynaptic control of gene expression. Annu Rev Neurosci 16:17-29.
7. Bradbury MJ, Akana SF, Dallman MF (1994) Roles of type I and II corticosteroid receptors in regulation of basal activity in the hypothalamo-pituitary-adrenal axis during the diurnal trough and the peak: evidence for a nonadditive effect of combined receptor occupation. Endocrinology 134:1286-1296.
8. Burke ZD, Ho MY, Morgan H, Smith M, Murphy D, Carter D (1997) Repression of vasopressin gene expression by glucocorticoids in transgenic mice: evidence of a direct mechanism mediated by proximal 5′ flanking sequence. Neuroscience 78:1177-1185.
9. Cairns C, Cairns W, Okret S (1993) Inhibition of gene expression by steroid hormone receptors via negative glucocorticoid response element: evidence for the involvement of DNA-binding and agonistic effects of the antiglucocorticoid/antiprogestin RU486. DNA Cell Biol 12:695-702.
10. Ceccatelli S, Villar MJ, Goldstein M, Hökfelt T (1989) Expression of c-fos immunoreactivity in transmitter-characterized neurons after stress. Proc Natl Acad Sci USA 86:9569-9573.
11. Chan RKW, Brown ER, Ericsson A, Kovács KJ, Sawchenko PE (1993) A comparison of two immediate-early genes, c-fos and NGFI-B, as markers for functional activation in stress-related neuroendocrine circuitry. J Neurosci 13:5126-5138.
12. Dallman MF, Akana SF, Cascio CS, Darlington DN, Jacobson L, Levine N (1987) Regulation of ACTH secretion: variation on a theme B. Recent Prog Horm Res 43:113-167.
13. Diamond MI, Miner JN, Yashinaga SK, Yamamoto KR (1990) Transcription factor interactions: selectors of positive or negative regulation from a single DNA element. Science 249:1266-1272.
14. Drouin J, Trifiro MA, Plante RK, Nemer M, Eriksson P, Wrange O (1989) Glucocorticoid receptor binding to a specific DNA sequence is required for hormone-dependent repression of pro-opiomelanocortin gene expression. Mol Cell Biol 9:5305-5314.
15. Gonzalez GA, Montminy MR (1989) Cyclic AMP stimulates somatostatin gene transcription by phosphorylation of CREB at serine 133. Cell 59:675-680.
16. Guardiola-Diaz HM, Boswell C, Seasholtz AF (1994) The cAMP-responsive element in the corticotropin-releasing hormone gene mediates transcriptional regulation by depolarization. J Biol Chem 269:14784-14791.
17. Guardiola-Diaz HM, Kolinske JS, Gates LH, Seasholtz AF (1996) Negative glucocorticoid regulation of cyclic adenosine 3′5′-monophosphate-stimulated corticotropin-releasing hormone-reporter expression in AtT-20 cells. Mol Endocrinol 10:317-329.
18. Hagiwara M, Brindle P, Harootunian A, Armstrong R, Rivier J, Vale W, Tsien R, Montminy MR (1993) Coupling of hormonal stimulation and transcription via the cyclic AMP-responsive factor CREB is rate limited by nuclear entry of protein kinase A. Mol Cell Biol 13:4852-4859.
19. Herman JP (1995) In situ hybridization analysis of vasopressin gene transcription in the paraventricular and supraoptic nuclei of the rat: regulation by stress and glucocorticoids. J Comp Neurol 363:15-27.
20. Herman JP, Schafer MK-H, Watson SJ, Sherman TG (1991) In situ hybridization analysis of arginine vasopressin gene transcription using intron-specific probes. Mol Endocrinol 5:1447-1456.
21. Herman JP, Schafer MK-H, Thompson RC, Watson SJ (1992) Rapid regulation of corticotropin-releasing hormone gene transcription in vivo. Mol Endocrinol 6:1061-1069.
22. Herman JP, Cullinan WE, Morano MI, Akil H, Watson SJ (1995) Contribution of the ventral subiculum to inhibitory regulation of the hypothalamo-pituitary-adrenocortical axis. J Neuroendocrinol 7:475-482.
23. Jingami H, Matsukura S, Numa S, Imura H (1985) Effects of adrenalectomy and dexamethasone administration on the level of preprocorticotropin-releasing factor messenger rihonucleic acid (mRNA) in the hypothalamus and adrenocorticotropin/β-lipotropin precursor mRNA in the pituitary in rats. Endocrinology 117:1314-1320.
24. Keller-Wood ME, Dallman MF (1984) Corticosteroid inhibition of ACTH secretion. Endocr Rev 5:1-24.
25. Kiss JZ, Mezey É, Skirboll L (1984) Corticotropin-releasing factor-immunoreactive neurons of the paraventricular nucleus become vasopressin positive after adrenalectomy. Proc Natl Acad Sci USA 81:1854-1858.
26. Kovács KJ (1998) c-Fos as a transcription factor: a stressful review from a functional map. Neurochem Int 33:287-297.
27. Kovács K, Mezey É (1987) Dexamethasone inhibits corticotropin-releasing factor gene expression in the rat paraventricular nucleus. Neuroendocrinology 46:365-368.
28. Kovács KJ, Sawchenko PE (1996) Sequence of stress-induced alterations in indices of synaptic and transcriptional activation in parvocellular neurosecretory neurons. J Neurosci 16:262-273.
29. Kovács KJ, Sawchenko PE (1997) Glucocorticoid negative feedback is exerted selectively on vasopressin gene transcription in parvocellular neurosecretory neurons. Soc Neurosci Abstr 23:797.8.
30. Kovács K, Kiss JZ, Makara GB (1986) Glucocorticoid implants around the hypothalamic paraventricular nucleus prevent the increase of corticotropin-releasing factor and arginine vasopressin immunostaining induced by adrenalectomy. Neuroendocrinology 44:229-234.
31. Kovács KJ, Arias C, Sawchenko PE (1998) Protein synthesis blockade differentially affects the stress-induced transcriptional activation of neuropeptide genes in parvocellular neurosecretory neurons. Mol Brain Res 54:85-91.
32. Legradi G, Holzer D, Kapcala LP, Lechan RM (1997) Glucocorticoids inhibit stress-induced phosphorylation of CREB in corticotropin-releasing hormone neurons of the hypothalamic paraventricular nucleus. Neuroendocrinology 66:86-97.
33. Lightman SL, Young III WS (1988) Corticotropin-releasing factor, vasopressin and pro-opiomelanocortin mRNA responses to stress and opiates in the rats. J Physiol (Lond) 403:511-523.
34. Ma X-M, Levy A, Lightman SL (1997a) Emergence of an isolated arginine vasopressin (AVP) response to stress after repeated restraint: a study of both AVP and corticotropin-releasing hormone messenger ribonucleic acid (RNA) and heteronuclear RNA. Endocrinology 138:4351-4357.
35. Ma X-M, Levy A, Lightman SL (1997b) Rapid changes of heteronuclear RNA for arginine vasopressin but not for corticotropin releasing hormone in response to acute corticosterone administration. J Neuroendocrinol 9:723-728.
36. Makino S, Smith MA, Gold PW (1995) Increased expression of corticotropin-releasing hormone and vasopressin messenger ribonucleic acid (mRNA) in the hypothalamic paraventricular nucleus during repeated stress: association with reduction in glucocorticoid receptor mRNA levels. Endocrinology 136:3299-3309.
37. Morgan JI, Curran T (1991) Stimulus-transcription coupling in the nervous system: involvement of inducible proto-oncogenes fos and jun. Annu Rev Neurosci 14:421-451.
38. Pardy K, Adan RAH, Carter DA, Seah V, Burbach JPH, Murphy D (1992) The identification of a cis-acting element involved in cyclic 3′,5′-adenosine monophosphate regulation of bovine vasopressin gene expression. J Biol Chem 267:21746-21752.
39. Pearce D, Yamamoto KR (1993) Mineralocorticoid and glucocorticoid receptor activities distinguished by nonreceptor factors at a composite response element. Science 259:1161-1165.
40. Reul JM, de Kloet ER (1985) Two receptor systems for corticosterone in rat brain: microdistribution and differential occupation. Endocrinology 117:2505-2511.
41. Roberts JL, Budarf ML, Baxter JD, Herbert E (1979) Selective reduction of proadenocorticotropin/endorphin proteins and mRNA activity in mouse pituitary tumor cells by glucocorticoids. Biochemistry 18:4907-4915.
42. Roche PJ, Crawford RJ, Fernley RT, Tregear GW, Coghlan JP (1988) Nucleotide sequence of the gene coding for ovine corticotropin-releasing factor and regulation its mRNA level by glucocorticoids. Gene 71:421-431.
43. Rosen LB, Majzoub JA, Adler GK (1992) Effects of glucocorticoid on corticotropin-releasing hormone gene regulation by second messenger pathways in NPLC and AtT-20 cells. Endocrinology 130:2237-2244.
44. Sassone-Corsi P, Visvader J, Ferland L, Mellon PL, Verma IM (1988) Induction of proto-oncogene fos transcription through the adenylatecyclase pathway: characterization of a cAMP-responsive element. Genes Dev 2:1529-1538.
45. Sawchenko PE, Swanson LW, Vale WW (1984) Co-expression of corticotropin-releasing factor and vasopressin immunoreactivity in parvocellular neurosecretory neurons of the adrenalectomized rat. Proc Natl Acad Sci USA 81:1883-1887.
46. Sawchenko PE, Cunningham Jr ET, Mortrud MT, Pfeiffer SW, Gerfen CR (1990) Phaseolus vulgaris-leucoagglutinin (PHA-L) anterograde axonal transport technique. Methods Neurosci 3:247-260.
47. Schule R, Rangarajan P, Kliewer S, Ransone LJ, Bolado J, Yang N, Verma IM, Evans RM (1990) Functional antagonism between oncoprotein c-jun and the glucocorticoid receptor. Cell 62:1217-1226.
48. Seasholtz AF, Thompson RC, Douglas JO (1988) Identification of a cyclic adenosine monophosphate-responsive element in the rat corticotropin-releasing hormone gene. Mol Endocrinol 2:1311-1319.
49. Sheng M, McFadden G, Greenberg ME (1990) Membrane depolarization and calcium induce c-fos via phosphorylation of transcription factor CREB. Neuron 4:571-582.
50. Simmons DM, Arriza JL, Swanson LW (1989) A complete protocol for in situ hybridization of messenger RNAs in brain and other tissues with radiolabeled single-stranded RNA probes. J Histotechnol 12:169-181.
51. Stauber C, Altschmeid J, Akerblom IE, Marron JL, Mellon PL (1990) Mutual cross-interference between glucocorticoid receptor and CREB inhibits transactivation in placental cells. New Biol 4:527-540.
52. Swanson LW, Kuypers HGJM (1980) The paraventricular nucleus of the hypothalamus: cytoarchitectonic subdivisions and the organization of projections to the pituitary, dorsal vagal complex and spinal cord as demonstrated by retrograde fluorescence double labeling methods. J Comp Neurol 194:555-570.
53. Swanson LW, Simmons DM (1989) Differential steroid hormone and neural influences on peptide mRNA levels in CRH cells of the paraventricular nucleus: hybridization histochemical study in the rat. J Comp Neurol 285:413-435.
54. Swanson LW, Sawchenko PE, Rivier J, Vale WW (1983) Organization of ovine corticotropin-releasing factor immunoreactive cells and fibers in the rat brain: an immunohistochemical study. Neuroendocrinology 36:165-186.
55. Uht RM, McKelvy JF, Harrison RW, Bohn MC (1988) Demonstration of glucocorticoid receptor-like immunoreactivity in glucocorticoid-sensitive vasopressin and corticotropin-releasing factor neurons in the hypothalamic paraventricular nucleus. J Neurosci Res 19:405-411.
56. Unlap T, Jope RS (1994) Dexamethasone attenuates kainate-induced AP-1 activation in rat brain. Mol Brain Res 24:275-282.
57. Vale W, Spiess J, Rivier C, Rivier J (1981) Characterization of a 41-residue ovine hypothalamic peptide that stimulates secretion of corticotropin and β-endorphin. Science 213:1394-1397.
58. Verbeeck MAE, Adan RAH, Burbach JPH (1990) Vasopressin gene expression is stimulated by cyclic AMP in homologous and heterologous expression systems. FEBS Lett 272:89-93.
59. Wolfson B, Manning RW, Davis LG, Arentzen R, Baldino Jr F (1985) Co-localization of corticotropin-releasing factor and vasopressin mRNA in neurons after adrenalectomy. Nature 315:59-61.
60. Yang-Yen H-F, Chambard J-C, Sun Y-L, Smeal T, Schmidt TJ, Drouin J, Karin M (1990) Transcriptional interference between c-Jun and the glucocorticoid receptor: mutual inhibition of DNA binding due to direct protein-protein interaction. Cell 62:1205-1215.
61. Young III WS, Mezey É, Siegel RE (1986a) Vasopressin and oxytocin mRNAs in adrenalectomized and Brattleboro rats: analysis by quantitative in situ hybridization histochemistry. Mol Brain Res 1:231-241.
62. Young III WS, Mezey É, Siegel RE (1986b) Quantitative in situ hybridization histochemistry reveals increased levels of corticotropin-releasing factor mRNA after adrenalectomy in rats. Neurosci Lett 70:198-203.