Retinoids and glucocorticoids target common genes in hippocampal HT22 cells

Journal of Neurochemistry

Volumn 125, Issue 4, 2013, Pages 518-531

  Brossaud, Julie ^a,b   Roumes, Hélène ^a,b   Moisan, Marie Pierre ^a,b   Pallet, Véronique ^a,b   Redonnet, Anabelle ^a,b   Corcuff, Jean Benoît ^a,b  

^a NutriNeuro Bordeaux University   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

Author keywords

brain neurotrophic factor; glucocorticoids; hippocampus; retinoic acid; retinoic acid receptor; tissue transglutaminase 2

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DEXAMETHASONE; GLUCOCORTICOID; GLUCOCORTICOID RECEPTOR; MESSENGER RNA; PROTEIN GLUTAMINE GAMMA GLUTAMYLTRANSFERASE 2; RETINOIC ACID RECEPTOR BETA; RETINOID;

ANIMAL CELL; APOPTOSIS; ARTICLE; BRAIN CELL; BRAIN DERIVED NEUROTROPHIC FACTOR GENE; CELL VIABILITY; CONTROLLED STUDY; GENE EXPRESSION; GLUCOCORTICOID RECEPTOR GENE; HIPPOCAMPUS; MOLECULAR INTERACTION; MOUSE; NERVE CELL DIFFERENTIATION; NERVE CELL NECROSIS; NERVE CELL PLASTICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN SECRETION; RETINOIC ACID RECEPTOR BETA GENE; SIGNAL TRANSDUCTION; TISSUE TRANSGLUTAMINASE 2 GENE;

AGING; ANIMALS; APOPTOSIS; BRAIN-DERIVED NEUROTROPHIC FACTOR; CELL LINE, TRANSFORMED; CELL SURVIVAL; DEXAMETHASONE; DRUG SYNERGISM; GENE EXPRESSION; GLUCOCORTICOIDS; GTP-BINDING PROTEINS; HIPPOCAMPUS; MICE; NECROSIS; NEURAL STEM CELLS; NEURONAL PLASTICITY; RECEPTORS, GLUCOCORTICOID; RECEPTORS, RETINOIC ACID; RNA, MESSENGER; SIGNAL TRANSDUCTION; TRANSGLUTAMINASES; TRETINOIN;

EID: 84876785281     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/jnc.12192     Document Type: Article

References (74)

1. Aeschlimann D., Kaupp O., and, Paulsson M., (1995) Transglutaminase- catalyzed matrix cross-linking in differentiating cartilage: identification of osteonectin as a major glutaminyl substrate. J. Cell Biol. 129, 881-892.
2. Akimov S. S., and, Belkin A. M., (2001) Cell surface tissue transglutaminase is involved in adhesion and migration of monocytic cells on fibronectin. Blood 98, 1567-1576.
3. Alfarez D. N., Wiegert O., Joels M., and, Krugers H. J., (2002) Corticosterone and stress reduce synaptic potentiation in mouse hippocampal slices with mild stimulation. Neuroscience 115, 1119-1126.
4. Alfos S., Higueret P., Pallet V., Higueret D., Garcin H., and, Jaffard R., (1996) Chronic ethanol consumption increases the amount of mRNA for retinoic acid and triiodothyronine receptors in mouse brain. Neurosci. Lett. 206, 73-76.
5. Aubry E. M., and, Odermatt A., (2009) Retinoic acid reduces glucocorticoid sensitivity in C2C12 myotubes by decreasing 11beta-hydroxysteroid dehydrogenase type 1 and glucocorticoid receptor activities. Endocrinology 150, 2700-2708.
6. Ballow M., Wang X., Xiang S., and, Allen C., (2003) Expression and regulation of nuclear retinoic acid receptors in human lymphoid cells. J. Clin. Immunol. 23, 46-54.
7. Bamberger C. M., Schulte H. M., and, Chrousos G. P., (1996) Molecular determinants of glucocorticoid receptor function and tissue sensitivity to glucocorticoids. Endocr. Rev. 17, 245-261.
8. Behl C., Lezoualc'h F., Trapp T., Widmann M., Skutella T., and, Holsboer F., (1997) Glucocorticoids enhance oxidative stress-induced cell death in hippocampal neurons in vitro. Endocrinology 138, 101-106.
9. Benz A. H., Shajari M., Peruzki N., Dehghani F., and, Maronde E., (2010) Early growth response-1 induction by fibroblast growth factor-1 via increase of mitogen-activated protein kinase and inhibition of protein kinase B in hippocampal neurons. Br. J. Pharmacol. 160, 1621-1630.
10. Boldizsar F., Talaber G., Szabo M., Bartis D., Palinkas L., Nemeth P., and, Berki T., (2010) Emerging pathways of non-genomic glucocorticoid (GC) signalling in T cells. Immunobiology 215, 521-526.
11. Bonnet E., Touyarot K., Alfos S., Pallet V., Higueret P., and, Abrous D. N., (2008) Retinoic acid restores adult hippocampal neurogenesis and reverses spatial memory deficit in vitamin A deprived rats. PLoS ONE 3, e3487.
12. Borrell-Pages M., Canals J. M., Cordelieres F. P., et al,. (2006) Cystamine and cysteamine increase brain levels of BDNF in Huntington disease via HSJ1b and transglutaminase. J. Clin. Invest. 116, 1410-1424.
13. Campisi A., Bramanti V., Caccamo D., et al,. (2008) Effect of growth factors and steroids on transglutaminase activity and expression in primary astroglial cell cultures. J. Neurosci. Res. 86, 1297-1305.
14. Chen J. S., and, Mehta K., (1999) Tissue transglutaminase: an enzyme with a split personality. Int. J. Biochem. Cell Biol. 31, 817-836.
15. Coste K., and, Labbe A., (2011) A study of the metabolic pathways of vitamin A in the fetal human lung. Rev. Mal. Respir. 28, 283-289.
16. De The H., Vivanco-Ruiz M. M., Tiollais P., Stunnenberg H., and, Dejean A., (1990) Identification of a retinoic acid responsive element in the retinoic acid receptor beta gene. Nature 343, 177-180.
17. Dey N., De P. K., Wang M., Zhang H., Dobrota E. A., Robertson K. A., and, Durden D. L., (2007) CSK controls retinoic acid receptor (RAR) signaling: a RAR-c-SRC signaling axis is required for neuritogenic differentiation. Mol. Cell. Biol. 27, 4179-4197.
18. Duman R. S., and, Monteggia L. M., (2006) A neurotrophic model for stress-related mood disorders. Biol. Psychiatry 59, 1116-1127.
19. Ernfors P., and, Bramham C. R., (2003) The coupling of a trkB tyrosine residue to LTP. Trends Neurosci. 26, 171-173.
20. Etchamendy N., Enderlin V., Marighetto A., Vouimba R. M., Pallet V., Jaffard R., and, Higueret P., (2001) Alleviation of a selective age-related relational memory deficit in mice by pharmacologically induced normalization of brain retinoid signaling. J. Neurosci. 21, 6423-6429.
21. Facchiano F., Deloye F., Doussau F., et al,. (2010) Transglutaminase participates in the blockade of neurotransmitter release by tetanus toxin: evidence for a novel biological function. Amino Acids 39, 257-269.
22. Fahey M., Mitton E., Muth E., and, Rosenthal A. K., (2009) Dexamethasone promotes calcium pyrophosphate dihydrate crystal formation by articular chondrocytes. J. Rheumatol. 36, 163-169.
23. Fok J. Y., Ekmekcioglu S., and, Mehta K., (2006) Implications of tissue transglutaminase expression in malignant melanoma. Mol. Cancer Ther. 5, 1493-1503.
24. Fukuda K., Kojiro M., and, Chiu J. F., (1994) Differential regulation of tissue transglutaminase in rat hepatoma cell lines McA-RH7777 and McA-RH8994: relation to growth rate and cell death. J. Cell. Biochem. 54, 67-77.
25. Galliher-Beckley A. J., Williams J. G., and, Cidlowski J. A., (2011) Ligand-independent phosphorylation of the glucocorticoid receptor integrates cellular stress pathways with nuclear receptor signaling. Mol. Cell. Biol. 31, 4663-4675.
26. Garabuczi E., Kiss B., Felszeghy S., Tsay G. J., Fesus L., and, Szondy Z., (2013) Retinoids produced by macrophages engulfing apoptotic cells contribute to the appearance of transglutaminase 2 in apoptotic thymocytes. Amino Acids 44, 235-244.
27. George T. N., Miakotina O. L., Goss K. L., and, Snyder J. M., (1998) Mechanism of all trans-retinoic acid and glucocorticoid regulation of surfactant protein mRNA. Am. J. Physiol. 274, L560-L566.
28. Grummer M. A., and, Zachman R. D., (1998) Retinoic acid and dexamethasone affect RAR-beta and surfactant protein C mRNA in the MLE lung cell line. Am. J. Physiol. 274, L1-L7.
29. Hodrea J., Majai G., Doro Z., Zahuczky G., Pap A., Rajnavolgyi E., and, Fesus L., (2012) The glucocorticoid dexamethasone programs human dendritic cells for enhanced phagocytosis of apoptotic neutrophils and inflammatory response. J. Leukoc. Biol. 91, 127-136.
30. Katsuki H., Kurimoto E., Takemori S., Kurauchi Y., Hisatsune A., Isohama Y., Izumi Y., Kume T., Shudo K., and, Akaike A., (2009) Retinoic acid receptor stimulation protects midbrain dopaminergic neurons from inflammatory degeneration via BDNF-mediated signaling. J. Neurochem. 110, 707-718.
31. Kino T., Jaffe H., Amin N. D., Chakrabarti M., Zheng Y. L., Chrousos G. P., and, Pant H. C., (2010) Cyclin-dependent kinase 5 modulates the transcriptional activity of the mineralocorticoid receptor and regulates expression of brain-derived neurotrophic factor. Mol. Endocrinol. 24, 941-952.
32. Korte M., Kang H., Bonhoeffer T., and, Schuman E., (1998) A role for BDNF in the late-phase of hippocampal long-term potentiation. Neuropharmacology 37, 553-559.
33. Krugers H. J., Goltstein P. M., van der Linden S., and, Joels M., (2006) Blockade of glucocorticoid receptors rapidly restores hippocampal CA1 synaptic plasticity after exposure to chronic stress. Eur. J. Neurosci. 23, 3051-3055.
34. Kurauchi Y., Hisatsune A., Isohama Y., Sawa T., Akaike T., Shudo K., and, Katsuki H., (2011) Midbrain dopaminergic neurons utilize nitric oxide/cyclic GMP signaling to recruit ERK that links retinoic acid receptor stimulation to up-regulation of BDNF. J. Neurochem. 116, 323-333.
35. Latasa M. J., and, Cosgaya J. M., (2011) Regulation of retinoid receptors by retinoic acid and axonal contact in Schwann cells. PLoS ONE 6, e17023.
36. Lefebvre O., Wouters D., Mereau-Richard C., Facon T., Zandecki M., Formstecher P., and, Belin M. T., (1999) Induction of apoptosis by all-trans retinoic acid in the human myeloma cell line RPMI 8226 and negative regulation of some of its typical morphological features by dexamethasone. Cell Death Differ. 6, 433-444.
37. Lendahl U., and, McKay R. D., (1990) The use of cell lines in neurobiology. Trends Neurosci. 13, 132-137.
38. Lindvall O., Kokaia Z., Bengzon J., Elmer E., and, Kokaia M., (1994) Neurotrophins and brain insults. Trends Neurosci. 17, 490-496.
39. Liu J., Li L., and, Suo W. Z., (2009a) HT22 hippocampal neuronal cell line possesses functional cholinergic properties. Life Sci. 84, 267-271.
40. Liu J., Zhou R., He Q., Li W. I., Zhang T., Niu B., Zheng X., and, Xie J., (2009b) Calmodulin kinase II activation of mitogen-activated protein kinase in PC12 cell following all-trans retinoic acid treatment. Neurotoxicology 30, 599-604.
41. Maden M., (2007) Retinoic acid in the development, regeneration and maintenance of the nervous system. Nat. Rev. Neurosci. 8, 755-765.
42. Masia S., Alvarez S., de Lera A. R., and, Barettino D., (2007) Rapid, nongenomic actions of retinoic acid on phosphatidylinositol-3-kinase signaling pathway mediated by the retinoic acid receptor. Mol. Endocrinol. 21, 2391-2402.
43. Mikkonen L., Pihlajamaa P., Sahu B., Zhang F. P., and, Janne O. A., (2010) Androgen receptor and androgen-dependent gene expression in lung. Mol. Cell. Endocrinol. 317, 14-24.
44. Mingam R., De Smedt V., Amedee T., Bluthe R. M., Kelley K. W., Dantzer R., and, Laye S., (2008) In vitro and in vivo evidence for a role of the P2X7 receptor in the release of IL-1 beta in the murine brain. Brain Behav. Immun. 22, 234-244.
45. Mingaud F., Mormede C., Etchamendy N., et al,. (2008) Retinoid hyposignaling contributes to aging-related decline in hippocampal function in short-term/working memory organization and long-term declarative memory encoding in mice. J. Neurosci. 28, 279-291.
46. Murakami S., Imbe H., Morikawa Y., Kubo C., and, Senba E., (2005) Chronic stress, as well as acute stress, reduces BDNF mRNA expression in the rat hippocampus but less robustly. Neurosci. Res. 53, 129-139.
47. Nagahara A. H., Merrill D. A., Coppola G., et al,. (2009) Neuroprotective effects of brain-derived neurotrophic factor in rodent and primate models of Alzheimer's disease. Nat. Med. 15, 331-337.
48. Numakawa T., Kumamaru E., Adachi N., Yagasaki Y., Izumi A., and, Kunugi H., (2009) Glucocorticoid receptor interaction with TrkB promotes BDNF-triggered PLC-gamma signaling for glutamate release via a glutamate transporter. Proc. Natl Acad. Sci. USA 106, 647-652.
49. Ohashi E., Kogai T., Kagechika H., and, Brent G. A., (2009) Activation of the PI3 kinase pathway by retinoic acid mediates sodium/iodide symporter induction and iodide transport in MCF-7 breast cancer cells. Cancer Res. 69, 3443-3450.
50. Okamoto S., Krainc D., Sherman K., and, Lipton S. A., (2000) Antiapoptotic role of the p38 mitogen-activated protein kinase-myocyte enhancer factor 2 transcription factor pathway during neuronal differentiation. Proc. Natl Acad. Sci. USA 97, 7561-7566.
51. Oliveira M., Bessa J. M., Mesquita A., et al,. (2006) Induction of a hyperanxious state by antenatal dexamethasone: a case for less detrimental natural corticosteroids. Biol. Psychiatry 59, 844-852.
52. Ou H., Haendeler J., Aebly M. R., Kelly L. A., Cholewa B. C., Koike G., Kwitek-Black A., Jacob H. J., Berk B. C., and, Miano J. M., (2000) Retinoic acid-induced tissue transglutaminase and apoptosis in vascular smooth muscle cells. Circ. Res. 87, 881-887.
53. Park J. J., and, Loh Y. P., (2011) Visualization of peptide secretory vesicles in living nerve cells. Methods Mol. Biol. 789, 137-145.
54. Pasquali D., Rossi V., Prezioso D., Gentile V., Colantuoni V., Lotti T., Bellastella A., and, Sinisi A. A., (1999) Changes in tissue transglutaminase activity and expression during retinoic acid-induced growth arrest and apoptosis in primary cultures of human epithelial prostate cells. J. Clin. Endocrinol. Metab. 84, 1463-1469.
55. Piacentini M., Sartori C., Beninati S., Bargagli A. M., and, Ceru-Argento M. P., (1986) Ornithine decarboxylase, transglutaminase, diamine oxidase and total diamines and polyamines in maternal liver and kidney throughout rat pregnancy. Biochem. J. 234, 435-440.
56. Reul J. M., Pearce P. T., Funder J. W., and, Krozowski Z. S,. (1989) Type I and type II corticosteroid receptor gene expression in the rat: effect of adrenalectomy and dexamethasone administration. Mol. Endocrinol. 3, 1674-1680.
57. Rhinn M., and, Dolle P., (2012) Retinoic acid signalling during development. Development 139, 843-858.
58. Rochette-Egly C., (2005) Dynamic combinatorial networks in nuclear receptor-mediated transcription. J. Biol. Chem. 280, 32565-32568.
59. Rochette-Egly C., and, Germain P., (2009) Dynamic and combinatorial control of gene expression by nuclear retinoic acid receptors (RARs). Nucl. Recept. Signal. 7, e005.
60. Sarabdjitsingh R. A., Meijer O. C., and, de Kloet E. R., (2010) Specificity of glucocorticoid receptor primary antibodies for analysis of receptor localization patterns in cultured cells and rat hippocampus. Brain Res. 1331, 1-11.
61. Scarpellini A., Germack R., Lortat-Jacob H., Muramatsu T., Billett E., Johnson T., and, Verderio E. A., (2009) Heparan sulfate proteoglycans are receptors for the cell-surface trafficking and biological activity of transglutaminase-2. J. Biol. Chem. 284, 18411-18423.
62. Shearer K. D., Stoney P. N., Morgan P. J., and, McCaffery P. J., (2012) A vitamin for the brain. Trends Neurosci. 35, 733-741.
63. Sommer K. M., Chen L. I., Treuting P. M., Smith L. T., and, Swisshelm K., (1999) Elevated retinoic acid receptor beta(4) protein in human breast tumor cells with nuclear and cytoplasmic localization. Proc. Natl Acad. Sci. USA 96, 8651-8656.
64. Sousa N., Cerqueira J. J., and, Almeida O. F., (2008) Corticosteroid receptors and neuroplasticity. Brain Res. Rev. 57, 561-570.
65. Tang S., Machaalani R., and, Waters K. A., (2010) Immunolocalization of pro- and mature-brain derived neurotrophic factor (BDNF) and receptor TrkB in the human brainstem and hippocampus. Brain Res. 1354, 1-14.
66. Toth K., Sarang Z., Scholtz B., Brazda P., Ghyselinck N., Chambon P., Fesus L., and, Szondy Z., (2011) Retinoids enhance glucocorticoid-induced apoptosis of T cells by facilitating glucocorticoid receptor-mediated transcription. Cell Death Differ. 18, 783-792.
67. Verma A., Wang H., Manavathi B., Fok J. Y., Mann A. P., Kumar R., and, Mehta K., (2006) Increased expression of tissue transglutaminase in pancreatic ductal adenocarcinoma and its implications in drug resistance and metastasis. Cancer Res. 66, 10525-10533.
68. Wang X., and, DeFranco D. B., (2005) Alternative effects of the ubiquitin-proteasome pathway on glucocorticoid receptor down-regulation and transactivation are mediated by CHIP, an E3 ligase. Mol. Endocrinol. 19, 1474-1482.
69. Wang X., Pongrac J. L., and, DeFranco D. B., (2002) Glucocorticoid receptors in hippocampal neurons that do not engage proteasomes escape from hormone-dependent down-regulation but maintain transactivation activity. Mol. Endocrinol. 16, 1987-1998.
70. Wang X. L., Herzog B., Waltner-Law M., Hall R. K., Shiota M., and, Granner D. K., (2004) The synergistic effect of dexamethasone and all-trans-retinoic acid on hepatic phosphoenolpyruvate carboxykinase gene expression involves the coactivator p300. J. Biol. Chem. 279, 34191-34200.
71. Wei S., Xu H., Xia D., and, Zhao R., (2010) Curcumin attenuates the effects of transport stress on serum cortisol concentration, hippocampal NO production, and BDNF expression in the pig. Domest. Anim. Endocrinol. 39, 231-239.
72. Yamaguchi S., Murata Y., Nagaya T., Hayashi Y., Ohmori S., Nimura Y., and, Seo H., (1999) Glucocorticoids increase retinoid-X receptor alpha (RXRalpha) expression and enhance thyroid hormone action in primary cultured rat hepatocytes. J. Mol. Endocrinol. 22, 81-90.
73. Yuan L., Siegel M., Choi K., Khosla C., Miller C. R., Jackson E. N., Piwnica-Worms D., and, Rich K. M., (2007) Transglutaminase 2 inhibitor, KCC009, disrupts fibronectin assembly in the extracellular matrix and sensitizes orthotopic glioblastomas to chemotherapy. Oncogene 26, 2563-2573.
74. Yulug B., Ozan E., Gonul A. S., and, Kilic E., (2009) Brain-derived neurotrophic factor, stress and depression: a minireview. Brain Res. Bull. 78, 267-269.