A rapid interference between glucocorticoids and cAMP-activated signalling in hypothalamic neurones prevents binding of phosphorylated cAMP response element binding protein and glucocorticoid receptor at the CRE-Like and composite GRE Sites of thyrotrophin-releasing hormone gene promoter

Journal of Neuroendocrinology

Volumn 22, Issue 4, 2010, Pages 282-293

  Diaz Gallardo M Y ^a   Cote Velez A ^a   Charli, J L ^a   Joseph Bravo, P ^a  

^a INSTITUTO DE BIOTECNOLOGÍA   (Mexico)

Author keywords

Composite GRE; Corticosterone BSA; CREB; Hypothalamus; Pro TRH

Indexed keywords

8 BROMO CYCLIC AMP; BOVINE SERUM ALBUMIN; CORTICOSTERONE; CYCLIC AMP; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; DEXAMETHASONE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; MEMBRANE RECEPTOR; MESSENGER RNA; NORADRENALIN; PHORBOL ESTER; PROTEIN C FOS; PROTEIN C JUN; PROTIRELIN; TRANSCRIPTION FACTOR; TRANSCRIPTION FACTOR AP 1; TRANSCRIPTION FACTOR SP1;

ANIMAL CELL; ANIMAL CELL CULTURE; ANIMAL TISSUE; ARTICLE; BINDING SITE; BRAIN NERVE CELL; CELL STIMULATION; CHROMATIN IMMUNOPRECIPITATION; CONTROLLED STUDY; EMBRYO; FEMALE; HYPOTHALAMUS; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN INTERACTION; RAT; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION;

ANIMALS; CELLS, CULTURED; CYCLIC AMP; CYCLIC AMP RESPONSE ELEMENT-BINDING PROTEIN; DRUG ANTAGONISM; FEMALE; GENE EXPRESSION REGULATION; GLUCOCORTICOIDS; HYPOTHALAMUS; NEURONS; PHOSPHORYLATION; PREGNANCY; PROMOTER REGIONS, GENETIC; PROTEIN BINDING; RATS; RATS, WISTAR; RECEPTORS, GLUCOCORTICOID; RESPONSE ELEMENTS; SIGNAL TRANSDUCTION; THYROTROPIN-RELEASING HORMONE; TIME FACTORS;

EID: 77952488508     PISSN: 09538194     EISSN: 13652826     Source Type: Journal    
DOI: 10.1111/j.1365-2826.2010.01966.x     Document Type: Article

References (47)

1. de Kloet ER, Joels M, Holsboer F. Stress and the brain: from adaptation to disease. Nat Rev Neurosci 2005, 6:463-475.
2. Lechan RM, Fekete C. The TRH neuron: a hypothalamic integrator of energy metabolism. Prog Brain Res 2006, 153:209-235.
3. Aguilera G, Kiss A, Liu Y, Kamitakahara A. Negative regulation of corticotropin releasing factor expression and limitation of stress response. Stress 2007, 10:153-161.
4. Uribe RM, Redondo JL, Charli JL, Joseph-Bravo P. Suckling and cold stress rapidly and transiently increase TRH mRNA in the paraventricular nucleus. Neuroendocrinology 1993, 58:140-145.
5. Sánchez E, Uribe RM, Corkidi G, Zoeller RT, Cisneros M, Zacarias M, Morales-Chapa C, Charli JL, Joseph-Bravo P. Differential responses of thyrotropin-releasing hormone (TRH) neurons to cold exposure or suckling indicate functional heterogeneity of the TRH system in the paraventricular nucleus of the rat hypothalamus. Neuroendocrinology 2001, 74:407-422.
6. Cizza G, Brady LS, Esclapes M, Blackman MR, Gold PW, Chrousos GP. Age and gender influence basal and stress-modulated hypothalamic-pituitary-thyroidal function in Fischer 344/N rats. Neuroendocrinology 1996, 64:440-448.
7. Kakucska I, Qi Y, Lechan RM. Changes in adrenal status affect hypothalamic thyrotropin-releasing hormone gene expression in parallel with corticotropin-releasing hormone. Endocrinology 1995, 136:2795-2802.
8. Aguilar-Valles A, Sanchez E, de Gortari P, Balderas I, Ramirez-Amaya V, Bermudez-Rattoni F, Joseph-Bravo P. Analysis of the stress response in rats trained in the water-maze: differential expression of corticotropin-releasing hormone, CRH-R1, glucocorticoid receptors and brain-derived neurotrophic factor in limbic regions. Neuroendocrinology 2005, 82:306-319.
9. Aguilar-Valles A, Sanchez E, de Gortari P, Garcia-Vazquez AI, Ramirez-Amaya V, Bermudez-Rattoni F, Joseph-Bravo P. The expression of TRH, its receptors and degrading enzyme is differentially modulated in the rat limbic system during training in the Morris water maze. Neurochem Int 2007, 50:404-417.
10. Gutiérrez-Mariscal M, de Gortari P, López-Rubalcava C, Martínez A, Joseph-Bravo P. Analysis of the anxiolytic-like effect of TRH and the response of amygdalar TRHergic neurons in anxiety. Psychoneuroendocrinology 2008, 33:198-213.
11. Pérez-Martínez L, Carréon-Rodríguez A, González-Alzati ME, Morales C, Charli JL, Joseph-Bravo P. Dexamethasone rapidly regulates TRH mRNA levels in hypothalamic cell cultures: interaction with the cAMP pathway. Neuroendocrinology 1998, 68:345-354.
12. Cote-Vélez A, Pérez-Martínez L, Díaz-Gallardo MY, Pérez-Monter C, Carréon-Rodríguez A, Charli JL, Joseph-Bravo P. Dexamethasone represses cAMP rapid upregulation of TRH gene transcription: identification of a composite glucocorticoid response element and a cAMP response element in TRH promoter. J Mol Endocrinol 2005, 34:177-197.
13. Uribe RM, Pérez-Martínez L, Covarrubias ML, Gómez OB, Covarrubias L, Charli JL, Joseph-Bravo P. Phorbol ester or cAMP enhance thyrotropin releasing hormone mRNA in primary cultures of hypothalamic cells. Neurosci Lett 1995, 201:41-44.
14. Maroder M, Farina AR, Vacca A, Felli MP, Meco D, Screpanti I, Frati L, Gulino A. Cell-specific bifunctional role of Jun oncogene family members on glucocorticoid receptor-dependent transcription. Mol Endocrinol 1993, 7:570-784.
15. Lee SL, Stewart K, Goodman RH. Structure of the gene encoding rat thyrotropin releasing hormone. J Biol Chem 1988, 263:16604-16609.
16. Harris M, Aschkenasi C, Elias CF, Chandrankunnel A, Nillni EA, Bjorbaek C, Elmquist JK, Flier JS, Hollenberg AN. Transcriptional regulation of the thyrotropin-releasing hormone gene by leptin and melanocortin signaling. J Clin Invest 2001, 107:111-120.
17. Díaz-Gallardo M, Cote-Vélez A, Carreón-Rodríguez A, Charli JL, Joseph-Bravo P. Phosphorylated cyclic-AMP- and thyroid hormone receptor have independent response elements in the rat thyrotropin-releasing hormone promoter; an analysis in hypothalamic cells. Neuroendocrinology 2010, 91:64-76.
18. Kaczynski J, Cook T, Urrutia R. Sp1-and Kruppel-like transcription factors. Genome Biol 2003, 4:206.
19. Hollenberg AN, Monden T, Flynn TR, Borres ME, Cohen O, Wondisford FE. The human thyrotropin-releasing hormone gene is regulated by thyroid-hormone through 2 distinct classes of negative thyroid-hormone response elements. Mol Endocrinol 1995, 9:540-550.
20. Lee GC, Yang IM, Kim BJ, Woo JT, Kim SW, Kim JW, Kim YS, Choi YK. Identification of glucocorticoid response element of the rat TRH gene. Korean J Intern Med 1996, 11:138-144.
21. Cote-Vélez A, Pérez-Martínez L, Charli JL, Joseph-Bravo P. The PKC and ERK/MAPK pathways regulate glucocorticoid action on TRH transcription. Neurochem Res 2008, 33:1582-1591.
22. Haller J, Mikics E, Makara GB. The effects of non-genomic glucocorticoid mechanisms on bodily functions and the central nervous system. A critical evaluation of findings. J Neuroendocrinol 2008, 29:273-291.
23. Joseph-Bravo P, Pérez-Martínez L, Lezama L, Morales-Chapa C, Charli JL. An improved method for the expression of TRH in serum-supplemented primary cultures of foetal hypothalamic cells. Brain Res Brain Res Protoc 2002, 9:93-104.
24. Guerra-Crespo M, Ubieta R, Joseph-Bravo P, Charli JL, Pérez-Martínez L. BDNF increases the early expression of TRH mRNA in fetal TrkB+ hypothalamic neurons in primary culture. Eur J Neurosci 2001, 14:483-494.
25. Balkan W, Tavianini MA, Gkonos PJ, Roos BA. Expression of rat thyrotropin-releasing hormone (TRH) gene in TRH-producing tissues of transgenic mice requires sequences located in Exon 1. Endocrinology 1998, 139:252-259.
26. Bonecini-Almeida MG, Ho JL, Boechat N, Huard RC, Chitale S, Doo H, Geng J, Rego L, Lazzarini LCO, Kritski AL, Jonson WD, McCaffrey TA, Silva JRL. Down-modulation of lung immune responses by interleukin-10 and transforming growth factor beta (TGF-beta) and analysis of TGF-beta receptors I and II in active tuberculosis. Infect Immun 2004, 72:2628-2634.
27. Schöfl C, Waring M, Bergwitz C, Arseniev L, von zur Mühlen A, Bravant G. Cyclic-adenosine 3′,5′monophosphate-stimulated c-fos gene transcription involves distinct calcium pathways in single β-cells. Mol Cell Endocrinol 2002, 186:121-131.
28. Ren Y, Satoh T, Yamada M, Hashimoto K, Konaka S, Iwasaki T, Mori M. Stimulation of the preprothyrotropin-releasing hormone gene by epidermal growth factor. Endocrinology 1998, 139:195-203.
29. Nichols M, Weih F, Wolfgang S, DeVack C, Kowenz-Leutz E, Kuckow B, Boshart M, GünTHer Schthomampersan. Phosphorylation of CREB affects its binding to high and low affinity sites: implications for cAMP induced gene transcription. EMBO J 1992, 11:3337-3346.
30. Rohlff C, Ahmad S, Borellini F, Lei J, Glazer RI. Modulation of transcription factor Sp1 by cAMP-dependent protein kinase. J Biol Chem 1997, 272:21137-21141.
31. Haas MJ, Pitot HC. Glucocorticoids stimulate CREB binding to a cyclic-AMP response element in the rat serine dehydratase gene. Arch Biochem Biophys 1999, 362:317-324.
32. Marinovic AC, Zheng B, Match WE, Price SR. Tissue-specific regulation of ubiquitin (UbC) transcription by glucocorticoids: in vivo and in vitro analyses. Am J Physiol Renal Physiol 2007, 292:F660-F666.
33. Ubieta R, Uribe RM, González JA, García-Vázquez A, Pérez-Monter C, Pérez-Martínez L, Joseph-Bravo P, Charli JL. BDNF upregulates pre-proTRH mRNA in the foetal/neonatal paraventricular nucleus of the hypothalamus. Properties of the transduction pathway. Brain Res 2007, 1174:28-38.
34. Mayr BM, Guzmán E, Montminy M. Glutamine rich and basic region/leucine zipper (bZip) domains stabilize cAMP-response element-bincing protein (CREB) binding to chromatin. J Biol Chem 2005, 15:15103-15110.
35. Mahapatra NR, Mahata M, Ghosh S, Gayen JR, O′Connor DT, Mahata SK. Molecular basis of neuroendocrine cell type-specific expression of the chromogranin B gene: crucial role of the transcription factors CREB, AP-2, Egr-1 and Sp1. J Neurochem 2006, 99:119-133.
36. Chinemov Y, Kerppola TK. Close encounters of many kinds: Fos-Jun interactions that mediate transcription regulatory specificity. Oncogene 2001, 20:2438-2452.
37. Rangarajan RN, Umesono K, Evans RM. Modulation of glucocorticoid receptor function by protein kinase A. Mol Endocrinol 1992, 6:1451-1457.
38. Kassel O, Herrlich P. Crosstalk between the glucocorticoid receptor and other transcription factors: molecular aspects. Mol Cell Endocrinol 2007, 275:13-29.
39. Gerits N, Kostenko S, Shiryaev A, Johannessen M, Moens U. Relations between the mitogen-activated protein kinase and the cAMP-dependent protein kinase pathways: comradeship and hostility. Cell Signal 2008, 20:1592-1607.
40. Yao M, Denver RJ. Regulation of vertebrate corticotrophin-releasing factor genes. Gen Comp Endocrinol 2007, 153:200-216.
41. Yamamori E, Iwasaki Y, Taguchi T, Nishiyama M, Yoshida M, Asai M, Oiso Y, Itoi K, Kambayashi M, Hashimoto K. Molecular mechanisms for corticotropin-releasing hormone gene repression by glucocorticoid in BE(2)C neuronal cell line. Mol Cell Endocrinol 2007, 264:142-148.
42. Doucas V, Shi Y, Miyamoto S, West A, Verma I, Evans RM. Cytoplasmic catalytic subunit of protein kinase A mediates cross-repression by NF-kappa B and the glucocorticoid receptor. Proc Natl Acad Sci USA 2000, 97:11893-11898.
43. van der Laan S, Lachize SB, Vreugendhil E, de Kloet ER, Meijer OC. Nuclear receptor coregulators differentially modulate CREB-mediated induction and glucocorticoid receptor mediated repression of the CRH gene. Endocrinology 2008, 149:725-732.
44. Cintra A, Fuxe K, Solfrini V, Agnati LF, Tinner B, Wikström AC, Staines W, Okret S, Gustafsson JA. Central peptidergic neurons as targets of glucocorticoid action. Evidence for the presence of glucocorticoid receptor immunoreactivity in various types of classes of peptidergic neurons. J Steroid Biochem Mol Biol 1991, 40:93-103.
45. Joseph-Bravo P, Cote-Vélez A, Pérez-Martínez L. Integration of neuroendocrine signals that regulate the activity of hypophysiotropic peptides. Molecular Endocrinology 2006, 1-24. http://trnres.com/ebook.php, Joseph-Bravo P, In, ed, Kerala, Research Signpost, [.]
46. van der Laan S, de Kloet ER, Meijer OC. Timing is critical for effective glucocorticoid receptor mediated repression of the cAMP-induced CRH gene. PLoS ONE 2009, 4:e4327.
47. Jaimes-Hoy L, Joseph-Bravo P, de Gortari P. Differential response of the TRHergic neurons of the hypothalamic paraventricular nucleus (PVN) in animals submitted to food-restriction or dehydration-induced anorexia and cold exposure. Horm Behav 2007, 56:366-377.