Retinoic acid modulates intrahippocampal levels of corticosterone in middle-aged mice: Consequences on hippocampal plasticity and contextual memory

Frontiers in Aging Neuroscience

Volumn 6, Issue FEB, 2014, Pages

  Bonhomme, Damien ^a,b   Pallet, Véronique ^a,b   Dominguez, Gaelle ^c,d   Servant, Laure ^a,b   Henkous, Nadia ^c   Lafenêtre, Pauline ^a,b   Higueret, Paul ^a,b   Béracochéa, Daniel ^c   Touyarot, Katia ^a,b  

^a NutriNeuro Bordeaux University   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c UMR 5287   (France)

^d UNIVERSITÉ DE TOURS   (France)

Author keywords

Corticosterone; Hippocampal plasticity; Memory; Retinoic acid; Vitamin A

Indexed keywords

CORTICOSTERONE; RETINOIC ACID; RETINOIC ACID RECEPTOR ALPHA; RETINOIC ACID RECEPTOR BETA; RETINOL;

ADULT; AMNESIA; ANIMAL EXPERIMENT; ARTICLE; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; CORTICOSTERONE BLOOD LEVEL; DRUG MECHANISM; HIPPOCAMPAL PLASTICITY; HIPPOCAMPUS; MEMORY; MICRODIALYSIS; MIDDLE AGED; MOUSE; NONHUMAN; PLASTICITY; STRESS; VITAMIN SUPPLEMENTATION;

EID: 84895825262     PISSN: None     EISSN: 16634365     Source Type: Journal    
DOI: 10.3389/fnagi.2014.00006     Document Type: Article

References (64)

1. Arvy, N., Hamiani, R., Richard, E., Moisan, M. P., and Pallet, V. (2013). Vitamin A regulates HPA axis status in LOU/C rats. J. Endocrinol. 219, 21-27. doi: 10.1530/JOE-13-0062
2. 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. doi: 10.1210/en.2008-1618
3. Azais-Braesco, V., Moriniere, C., Guesne, B., Partier, A., Bellenand, P., Baguelin, D., et al. (1995). Vitamin A status in the institutionalized elderly. Critical analysis of four evaluation criteria: dietary vitamin A intake, serum retinol, relative dose-response test (RDR) and impression cytology with transfer (ICT). Int. J. Vitam. Nutr. Res. 65, 151-161.
4. Beique, J. C., Lin, D. T., Kang, M. G., Aizawa, H., Takamiya, K., and Huganir, R. L. (2006). Synapse-specific regulation of AMPA receptor function by PSD-95. Proc. Natl. Acad. Sci. U.S.A. 103, 19535-19540. doi: 10.1073/pnas.0608492103
5. Beracochea, D., Boucard, A., Trocme-Thibierge, C., and Morain, P. (2008a). Improvement of contextual memory by S 24795 in aged mice: comparison with memantine. Psychopharmacology (Berl.) 196, 555-564. doi: 10.1007/s00213-007-0987-5
6. Beracochea, D., Liscia, P., Tronche, C., Chauveau, F., Jouanin, J. C., and Pierard, C. (2008b). Stress modulation of the memory retrograde-enhancing effects of the awakening drug modafinil in mice. Psychopharmacology (Berl.) 196, 1-13. doi: 10.1007/s00213-007-0915-8
7. Beracochea, D., Tronche, C., Coutan, M., Dorey, R., Chauveau, F., and Pierard, C. (2011). Interaction between diazepam and hippocampal corticosterone after acute stress: impact on memory in middle-aged mice. Front. Behav. Neurosci. 5:14. doi: 10.3389/fnbeh.2011.00014
8. 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. doi: 10.1371/journal.pone.0003487
9. Born, J., Ditschuneit, I., Schreiber, M., Dodt, C., and Fehm, H. L. (1995). Effects of age and gender on pituitary-adrenocortical responsiveness in humans. Eur. J. Endocrinol. 132, 705-711. doi: 10.1530/eje.0.1320705
10. Brossaud, J., Roumes, H., Moisan, M. P., Pallet, V., Redonnet, A., and Corcuff, J. B. (2013). Retinoids and glucocorticoids target common genes in hippocampal HT22 cells. J. Neurochem. 125, 518-531. doi: 10.1111/jnc.12192
11. Cai, L., Yan, X. B., Chen, X. N., Meng, Q. Y., and Zhou, J. N. (2010). Chronic all-trans retinoic acid administration induced hyperactivity of HPA axis and behavioral changes in young rats. Eur. Neuropsychopharmacol. 20, 839-847. doi: 10.1016/j.euroneuro.2010.06.019
12. Cameron, H. A., and Gould, E. (1994). Adult neurogenesis is regulated by adrenal steroids in the dentate gyrus. Neuroscience 61, 203-209. doi: 10.1016/0306-4522(94)90224-0
13. Carlisle, H. J., Fink, A. E., Grant, S. G., and O'Dell, T. J. (2008). Opposing effects of PSD-93 and PSD-95 on long-term potentiation and spike timing-dependent plasticity. J. Physiol. 586, 5885-5900. doi: 10.1113/jphysiol.2008.163469
14. Celerier, A., Pierard, C., Rachbauer, D., Sarrieau, A., and Beracochea, D. (2004). Contextual and serial discriminations: a new learning paradigm to assess simultaneously the effects of acute stress on retrieval of flexible or stable information in mice. Learn. Mem. 11, 196-204. doi: 10.1101/lm.65604
15. Chauveau, F., Pierard, C., Corio, M., Celerier, A., Christophe, T., Vouimba, R. M., et al. (2009a). Mediodorsal thalamic lesions block the stress-induced inversion of serial memory retrieval pattern in mice. Behav. Brain Res. 203, 270-278. doi: 10.1016/j.bbr.2009.05.014
16. Chauveau, F., Pierard, C., Tronche, C., Coutan, M., Drouet, I., Liscia, P., et al. (2009b). The hippocampus and prefrontal cortex are differentially involved in serial memory retrieval in non-stress and stress conditions. Neurobiol. Learn. Mem. 91, 447-455. doi: 10.1016/j.nlm.2008.12.003
17. Chauveau, F., Tronche, C., Pierard, C., Liscia, P., Drouet, I., Coutan, M., et al. (2010). Rapid stress-induced corticosterone rise in the hippocampus reverses serial memory retrieval pattern. Hippocampus 20, 196-207. doi: 10.1002/hipo.20605
18. Chiang, M. Y., Misner, D., Kempermann, G., Schikorski, T., Giguere, V., Sucov, H. M., et al. (1998). An essential role for retinoid receptors RARbeta and RXRgamma in long-term potentiation and depression. Neuron 21, 1353-1361. doi: 10.1016/S0896-6273(00)80654-6
19. Cocco, S., Diaz, G., Stancampiano, R., Diana, A., Carta, M., Curreli, R., et al. (2002). Vitamin A deficiency produces spatial learning and memory impairment in rats. Neuroscience 115, 475-482. doi: 10.1016/S0306-4522(02)00423-2
20. Cohen, J. W., Louneva, N., Han, L. Y., Hodes, G. E., Wilson, R. S., Bennett, D. A., et al. (2011). Chronic corticosterone exposure alters postsynaptic protein levels of PSD-95, NR1, and synaptopodin in the mouse brain. Synapse 65, 763-770. doi: 10.1002/syn.20900
21. Delint-Ramirez, I., Salcedo-Tello, P., and Bermudez-Rattoni, F. (2008). Spatial memory formation induces recruitment of NMDA receptor and PSD-95 to synaptic lipid rafts. J. Neurochem. 106, 1658-1668. doi: 10.1111/j.1471-4159.2008.05523.x
22. de Quervain, D. J., Roozendaal, B., and Mcgaugh, J. L. (1998). Stress and glucocorticoids impair retrieval of long-term spatial memory. Nature 394, 787-790. doi: 10.1038/29542
23. Drapeau, E., Mayo, W., Aurousseau, C., Le Moal, M., Piazza, P. V., and Abrous, D. N. (2003). Spatial memory performances of aged rats in the water maze predict levels of hippocampal neurogenesis. Proc. Natl. Acad. Sci. U.S.A. 100, 14385-14390. doi: 10.1073/pnas.2334169100
24. Drapeau, E., Montaron, M. F., Aguerre, S., and Abrous, D. N. (2007). Learning-induced survival of new neurons depends on the cognitive status of aged rats. J. Neurosci. 27, 6037-6044. doi: 10.1523/JNEUROSCI.1031-07.2007
25. Dyall, S. C., Michael, G. J., and Michael-Titus, A. T. (2010). Omega-3 fatty acids reverse age-related decreases in nuclear receptors and increase neurogenesis in old rats. J. Neurosci. Res. 88, 2091-2102. doi: 10.1002/jnr.22390
26. Enderlin, V., Pallet, V., Alfos, S., Dargelos, E., Jaffard, R., Garcin, H., et al. (1997). Age-related decreases in mRNA for brain nuclear receptors and target genes are reversed by retinoic acid treatment. Neurosci. Lett. 229, 125-129. doi: 10.1016/S0304-3940(97)00424-2
27. Etchamendy, N., Enderlin, V., Marighetto, A., Pallet, V., Higueret, P., and Jaffard, R. (2003). Vitamin A deficiency and relational memory deficit in adult mice: relationships with changes in brain retinoid signalling. Behav. Brain Res. 145, 37-49. doi: 10.1016/S0166-4328(03)00099-8
28. Etchamendy, N., Enderlin, V., Marighetto, A., Vouimba, R. M., Pallet, V., Jaffard, R., et al. (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.
29. Feart, C., Mingaud, F., Enderlin, V., Husson, M., Alfos, S., Higueret, P., et al. (2005). Differential effect of retinoic acid and triiodothyronine on the age-related hypo-expression of neurogranin in rat. Neurobiol. Aging 26, 729-738. doi: 10.1016/j.neurobiolaging.2004.06.004
30. Frick, K. M., Baxter, M. G., Markowska, A. L., Olton, D. S., and Price, D. L. (1995). Age-related spatial reference and working memory deficits assessed in the water maze. Neurobiol. Aging 16, 149-160. doi: 10.1016/0197-4580(94)00155-3
31. Herman, J. P., Larson, B. R., Speert, D. B., and Seasholtz, A. F. (2001). Hypothalamo-pituitary-adrenocortical dysregulation in aging F344/Brown-Norway F1 hybrid rats. Neurobiol. Aging 22, 323-332. doi: 10.1016/S0197-4580(00)00242-6
32. Holmes, M. C., Carter, R. N., Noble, J., Chitnis, S., Dutia, A., Paterson, J. M., et al. (2010). 11beta-hydroxysteroid dehydrogenase type 1 expression is increased in the aged mouse hippocampus and parietal cortex and causes memory impairments. J. Neurosci. 30, 6916-6920. doi: 10.1523/JNEUROSCI.0731-10.2010
33. Holmes, M. C., Yau, J. L., Kotelevtsev, Y., Mullins, J. J., and Seckl, J. R. (2003). 11 Beta-hydroxysteroid dehydrogenases in the brain: two enzymes two roles. Ann. N. Y. Acad. Sci. 1007, 357-366. doi: 10.1196/annals.1286.035
34. Hu, P., Liu, J., Zhao, J., Qi, X. R., Qi, C. C., Lucassen, P. J., et al. (2013). All-trans retinoic acid-induced hypothalamus-pituitary-adrenal hyperactivity involves glucocorticoid receptor dysregulation. Transl. Psychiatry 3, e336. doi: 10.1038/tp.2013.98
35. Joels, M. (2008). Functional actions of corticosteroids in the hippocampus. Eur. J. Pharmacol. 583, 312-321. doi: 10.1016/j.ejphar.2007.11.064
36. Kaczorowski, C. C., and Disterhoft, J. F. (2009). Memory deficits are associated with impaired ability to modulate neuronal excitability in middle-aged mice. Learn. Mem. 16, 362-366. doi: 10.1101/lm.1365609
37. Kadish, I., Thibault, O., Blalock, E. M., Chen, K. C., Gant, J. C., Porter, N. M., et al. (2009). Hippocampal and cognitive aging across the lifespan: a bioenergetic shift precedes and increased cholesterol trafficking parallels memory impairment. J. Neurosci. 29, 1805-1816. doi: 10.1523/JNEUROSCI.4599-08.2009
38. Lane, M. A., and Bailey, S. J. (2005). Role of retinoid signalling in the adult brain. Prog. Neurobiol. 75, 275-293. doi: 10.1016/j.pneurobio.2005.03.002
39. Lupien, S. J., De Leon, M., De Santi, S., Convit, A., Tarshish, C., Nair, N. P., et al. (1998). Cortisol levels during human aging predict hippocampal atrophy and memory deficits. Nat. Neurosci. 1, 69-73. doi: 10.1038/271
40. Marill, J., Idres, N., Capron, C. C., Nguyen, E., and Chabot, G. G. (2003). Retinoic acid metabolism and mechanism of action: a review. Curr. Drug Metab. 4, 1-10. doi: 10.2174/1389200033336900
41. Markowska, A. L., and Breckler, S. J. (1999). Behavioral biomarkers of aging: illustration of a multivariate approach for detecting age-related behavioral changes. J. Gerontol. A Biol. Sci. Med. Sci. 54, B549-B566. doi: 10.1093/gerona/54.12.B549
42. McCaffery, P., Zhang, J., and Crandall, J. E. (2006). Retinoic acid signaling and function in the adult hippocampus. J. Neurobiol. 66, 780-791. doi: 10.1002/neu.20237
43. Migaud, M., Charlesworth, P., Dempster, M., Webster, L. C., Watabe, A. M., Makhinson, M., et al. (1998). Enhanced long-term potentiation and impaired learning in mice with mutant postsynaptic density-95 protein. Nature 396, 433-439. doi: 10.1038/24790
44. Mingaud, F., Mormede, C., Etchamendy, N., Mons, N., Niedergang, B., Wietrzych, M., 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. doi: 10.1523/JNEUROSCI.4065-07.2008
45. Mizoguchi, K., Ikeda, R., Shoji, H., Tanaka, Y., Maruyama, W., and Tabira, T. (2009). Aging attenuates glucocorticoid negative feedback in rat brain. Neuroscience 159, 259-270. doi: 10.1016/j.neuroscience.2008.12.020
46. Nyffeler, M., Zhang, W. N., Feldon, J., and Knuesel, I. (2007). Differential expression of PSD proteins in age-related spatial learning impairments. Neurobiol. Aging 28, 143-155. doi: 10.1016/j.neurobiolaging.2005.11.003
47. Oitzl, M. S., and de Kloet, E. R. (1992). Selective corticosteroid antagonists modulate specific aspects of spatial orientation learning. Behav. Neurosci. 106, 62-71. doi: 10.1037/0735-7044.106.1.62
48. Olson, C. R., and Mello, C. V. (2010). Significance of vitamin A to brain function, behavior and learning. Mol. Nutr. Food Res. 54, 489-495. doi: 10.1002/mnfr.200900246
49. Paez-Pereda, M., Kovalovsky, D., Hopfner, U., Theodoropoulou, M., Pagotto, U., Uhl, E., et al. (2001). Retinoic acid prevents experimental Cushing syndrome. J. Clin. Invest. 108, 1123-1131. doi: 10.1172/JCI11098
50. Paxinos, G., and Franklin, K. B. J. (2001). The Mouse Brain in Stereotaxic Coordinates, 2nd Edn. San Diego: Academic Press.
51. Penniston, K. L., and Tanumihardjo, S. A. (2006). The acute and chronic toxic effects of vitamin A. Am. J. Clin. Nutr. 83, 191-201.
52. Pepeu, G. (2004). Mild cognitive impairment: animal models. Dialogues Clin. Neurosci. 6, 369-377.
53. Pierard, C., Tronche, C., Liscia, P., Chauveau, F., and Beracochea, D. (2009). Combined effects of acute stress and amphetamine on serial memory retrieval pattern in mice. Psychopharmacology (Berl.) 203, 463-473. doi: 10.1007/s00213-008-1391-5
54. Sakamuri, V. P., Ananthathmakula, P., Veettil, G. N., and Ayyalasomayajula, V. (2011). Vitamin A decreases pre-receptor amplification of glucocorticoids in obesity: study on the effect of vitamin A on 11beta-hydroxysteroid dehydrogenase type 1 activity in liver and visceral fat of WNIN/Ob obese rats. Nutr. J. 10, 70. doi: 10.1186/1475-2891-10-70
55. Salehi, B., Cordero, M. I., and Sandi, C. (2010). Learning under stress: the inverted-U-shape function revisited. Learn. Mem. 17, 522-530. doi: 10.1101/lm.1914110
56. Sandi, C., and Pinelo-Nava, M. T. (2007). Stress and memory: behavioral effects and neurobiological mechanisms. Neural Plast. 2007, 78970. doi: 10.1155/2007/78970
57. Seckl, J. R. (1997). 11beta-Hydroxysteroid dehydrogenase in the brain: a novel regulator of glucocorticoid action? Front. Neuroendocrinol. 18, 49-99. doi: 10.1006/frne.1996.0143
58. Touyarot, K., Bonhomme, D., Roux, P., Alfos, S., Lafenetre, P., Richard, E., et al. (2013). A mid-life vitamin A supplementation prevents age-related spatial memory deficits and hippocampal neurogenesis alterations through CRABP-I. PLoS ONE 8:e72101. doi: 10.1371/journal.pone.0072101
59. Tronche, C., Pierard, C., Coutan, M., Chauveau, F., Liscia, P., and Beracochea, D. (2010). Increased stress-induced intra-hippocampus corticosterone rise associated with memory impairments in middle-aged mice. Neurobiol. Learn. Mem. 93, 343-351. doi: 10.1016/j.nlm.2009.11.009
60. VanGuilder, H. D., Farley, J. A., Yan, H., Van Kirk, C. A., Mitschelen, M., Sonntag, W. E., et al. (2011). Hippocampal dysregulation of synaptic plasticity-associated proteins with age-related cognitive decline. Neurobiol. Dis. 43, 201-212. doi: 10.1016/j.nbd.2011.03.012
61. Vickers, C. A., Stephens, B., Bowen, J., Arbuthnott, G. W., Grant, S. G., and Ingham, C. A. (2006). Neurone specific regulation of dendritic spines in vivo by post synaptic density 95 protein (PSD-95). Brain Res. 1090, 89-98. doi: 10.1016/j.brainres.2006.03.075
62. Wietrzych, M., Meziane, H., Sutter, A., Ghyselinck, N., Chapman, P. F., Chambon, P., et al. (2005). Working memory deficits in retinoid X receptor gamma-deficient mice. Learn. Mem. 12, 318-326. doi: 10.1101/lm.89805
63. Yau, J. L., Noble, J., Kenyon, C. J., Hibberd, C., Kotelevtsev, Y., Mullins, J. J., et al. (2001). Lack of tissue glucocorticoid reactivation in 11beta-hydroxysteroid dehydrogenase type 1 knockout mice ameliorates age-related learning impairments. Proc. Natl. Acad. Sci. U.S.A. 98, 4716-4721. doi: 10.1073/pnas.071562698
64. Yau, J. L., and Seckl, J. R. (2012). Local amplification of glucocorticoids in the aging brain and impaired spatial memory. Front. Aging Neurosci. 4:24. doi: 10.3389/fnagi.2012.00024