Vitamin A status regulates glucocorticoid availability in Wistar rats: Consequences on cognitive functions and hippocampal neurogenesis?

Frontiers in Behavioral Neuroscience

Volumn 8, Issue FEB, 2014, Pages

  Bonhomme, Damien ^a,b   Minni, Amandine M ^a,b   Alfos, Serge ^a,b   Roux, Pascale ^a,b   Richard, Emmanuel ^c   Higueret, Paul ^a,b   Moisan, Marie Pierre ^a,b   Pallet, Véronique ^a,b   Touyarot, Katia ^a,b  

^a NutriNeuro Bordeaux University   (France)

^b UNIVERSITÉ DE BORDEAUX   (France)

^c INSERM   (France)

Author keywords

11beta Hydrosteroid dehydrogenase type 1; Anxiety like behavior; Corticosteroid binding globulin; Glucocorticoid; Hippocampal neurogenesis; Retinoic acid; Spatial memory; Vitamin A status

Indexed keywords

EID: 84893618016     PISSN: 16625153     EISSN: None     Source Type: Journal    
DOI: 10.3389/fnbeh.2014.00020     Document Type: Article

References (69)

1. Alliot, J., Boghossian, S., Jourdan, D., Veyrat-Durebex, C., Pickering, G., Meynial-Denis, D., et al. (2002). The LOU/c/jall rat as an animal model of healthy aging? J. Gerontol. A Biol. Sci. Med. Sci. 57, B312-B320. doi: 10.1093/gerona/57.8.B312
2. Arfaoui, A., Lobo, M. V., Boulbaroud, S., Ouichou, A., Mesfioui, A., and Arenas, M. I. (2013). Expression of retinoic acid receptors and retinoid X receptors in normal and vitamin A deficient adult rat brain. Ann. Anat. 195, 111-121. doi: 10.1016/j.aanat.2012.06.006
3. 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
4. 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
5. Biesalski, H. K., Ehrenthal, W., Gross, M., Hafner, G., and Harth, O. (1983). Rapid determination of retinol (vitamin A) in serum by high pressure liquid chromatography (HPLC). Int. J. Vitam. Nutr. Res. 53, 130-137.
6. Bloem, M. W., Kiess, L., and Moench-Pfanner, R. (2002). Process indicators for monitoring and evaluating vitamin A programs. J. Nutr. 132, 2934S-2939S.
7. 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
8. Breuner, C. W., and Orchinik, M. (2002). Plasma binding proteins as mediators of corticosteroid action in vertebrates. J. Endocrinol. 175, 99-112. doi: 10.1677/joe.0.1750099
9. 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
10. 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
11. 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
12. 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
13. Crandall, J., Sakai, Y., Zhang, J., Koul, O., Mineur, Y., Crusio, W. E., et al. (2004). 13-cis-retinoic acid suppresses hippocampal cell division and hippocampal-dependent learning in mice. Proc. Natl. Acad. Sci. U.S.A. 101, 5111-5116. doi: 10.1073/pnas.0306336101
14. de Kloet, E. R., Joels, M., and Holsboer, F. (2005). Stress and the brain: from adaptation to disease. Nat. Rev. Neurosci. 6, 463-475. doi: 10.1038/nrn1683
15. Duman, R. S., and Monteggia, L. M. (2006). A neurotrophic model for stress-related mood disorders. Biol. Psychiatry 59, 1116-1127. doi: 10.1016/j.biopsych.2006.02.013
16. Eichenbaum, H. (2004). Hippocampus: cognitive processes and neural representations that underlie declarative memory. Neuron 44, 109-120. doi: 10.1016/j.neuron.2004.08.028
17. Eichenbaum, H., Dudchenko, P., Wood, E., Shapiro, M., and Tanila, H. (1999). The hippocampus, memory, and place cells: is it spatial memory or a memory space? Neuron 23, 209-226. doi: 10.1016/S0896-6273(00)80773-4
18. 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
19. 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.
20. Goodman, T., Crandall, J. E., Nanescu, S. E., Quadro, L., Shearer, K., Ross, A., et al. (2012). Patterning of retinoic acid signaling and cell proliferation in the hippocampus. Hippocampus 22, 2171-2183. doi: 10.1002/hipo.22037
21. Gould, E., and Tanapat, P. (1999). Stress and hippocampal neurogenesis. Biol. Psychiatry 46, 1472-1479. doi: 10.1016/S0006-3223(99)00247-4
22. 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
23. 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
24. Hunter, R. G., Bellani, R., Bloss, E., Costa, A., McCarthy, K., and McEwen, B. S. (2009). Regulation of kainate receptor subunit mRNA by stress and corticosteroids in the rat hippocampus. PLoS ONE 4:e4328. doi: 10.1371/journal.pone.0004328
25. Husson, M., Enderlin, V., Alfos, S., Boucheron, C., Pallet, V., and Higueret, P. (2004). Expression of neurogranin and neuromodulin is affected in the striatum of vitamin A-deprived rats. Brain Res. Mol. Brain Res. 123, 7-17. doi: 10.1016/j.molbrainres.2003.12.012
26. Husson, M., Enderlin, V., Alfos, S., Feart, C., Higueret, P., and Pallet, V. (2003). Triiodothyronine administration reverses vitamin A deficiency-related hypo-expression of retinoic acid and triiodothyronine nuclear receptors and of neurogranin in rat brain. Br. J. Nutr. 90, 191-198. doi: 10.1079/BJN2003877
27. Issa, A. M., Rowe, W., Gauthier, S., and Meaney, M. J. (1990). Hypothalamic-pituitary-adrenal activity in aged, cognitively impaired and cognitively unimpaired rats. J. Neurosci. 10, 3247-3254.
28. Jacobs, S., Lie, D. C., Decicco, K. L., Shi, Y., Deluca, L. M., Gage, F. H., et al. (2006). Retinoic acid is required early during adult neurogenesis in the dentate gyrus. Proc. Natl. Acad. Sci. U.S.A. 103, 3902-3907. doi: 10.1073/pnas.0511294103
29. Jiang, W., Yu, Q., Gong, M., Chen, L., Wen, E. Y., Bi, Y., et al. (2012). Vitamin A deficiency impairs postnatal cognitive function via inhibition of neuronal calcium excitability in hippocampus. J. Neurochem. 121, 932-943. doi: 10.1111/j.1471-4159.2012.07697.x
30. Joels, M., Karst, H., Alfarez, D., Heine, V. M., Qin, Y., van Riel, E., et al. (2004). Effects of chronic stress on structure and cell function in rat hippocampus and hypothalamus. Stress 7, 221-231. doi: 10.1080/10253890500070005
31. Joels, M., and Krugers, H. J. (2007). LTP after stress: up or down? Neural Plast. 2007, 93202. doi: 10.1155/2007/93202
32. Klempin, F., and Kempermann, G. (2007). Adult hippocampal neurogenesis and aging. Eur. Arch. Psychiatry Clin. Neurosci. 257, 271-280. doi: 10.1007/s00406-007-0731-5
33. Krugers, H. J., Lucassen, P. J., Karst, H., and Joels, M. (2010). Chronic stress effects on hippocampal structure and synaptic function: relevance for depression and normalization by anti-glucocorticoid treatment. Front. Synaptic Neurosci. 2:24. doi: 10.3389/fnsyn.2010.00024
34. 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
35. Lemaire, V., Lamarque, S., Le Moal, M., Piazza, P. V., and Abrous, D. N. (2006). Postnatal stimulation of the pups counteracts prenatal stress-induced deficits in hippocampal neurogenesis. Biol. Psychiatry 59, 786-792. doi: 10.1016/j.biopsych.2005.11.009
36. 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
37. Magarinos, A. M., and McEwen, B. S. (1995). Stress-induced atrophy of apical dendrites of hippocampal CA3c neurons: involvement of glucocorticoid secretion and excitatory amino acid receptors. Neuroscience 69, 89-98. doi: 10.1016/0306-4522(95)00259-L
38. 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
39. 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
40. McEwen, B. S. (1999). Stress and hippocampal plasticity. Annu. Rev. Neurosci. 22, 105-122. doi: 10.1146/annurev.neuro.22.1.105
41. 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
42. Minni, A. M., Dorey, R., Pierard, C., Dominguez, G., Helbling, J. C., Foury, A., et al. (2012). Critical role of plasma corticosteroid-binding-globulin during stress to promote glucocorticoid delivery to the brain: impact on memory retrieval. Endocrinology 153, 4766-4774. doi: 10.1210/en.2012-1485
43. Misner, D. L., Jacobs, S., Shimizu, Y., de Urquiza, A. M., Solomin, L., Perlmann, T., et al. (2001). Vitamin A deprivation results in reversible loss of hippocampal long-term synaptic plasticity. Proc. Natl. Acad. Sci. U.S.A. 98, 11714-11719. doi: 10.1073/pnas.191369798
44. 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
45. Mohler, E. G., Browman, K. E., Roderwald, V. A., Cronin, E. A., Markosyan, S., Scott Bitner, R., et al. (2011). Acute inhibition of 11beta-hydroxysteroid dehydrogenase type-1 improves memory in rodent models of cognition. J. Neurosci. 31, 5406-5413. doi: 10.1523/JNEUROSCI.4046-10.2011
46. Moisan, M. P. (2010). Genotype-phenotype associations in understanding the role of corticosteroid-binding globulin in health and disease animal models. Mol. Cell. Endocrinol. 316, 35-41. doi: 10.1016/j.mce.2009.07.017
47. Moisan, M. P., Seckl, J. R., and Edwards, C. R. (1990). 11 beta-hydroxysteroid dehydrogenase bioactivity and messenger RNA expression in rat forebrain: localization in hypothalamus, hippocampus, and cortex. Endocrinology 127, 1450-1455. doi: 10.1210/endo-127-3-1450
48. Montaron, M. F., Drapeau, E., Dupret, D., Kitchener, P., Aurousseau, C., Le Moal, M., et al. (2006). Lifelong corticosterone level determines age-related decline in neurogenesis and memory. Neurobiol. Aging 27, 645-654. doi: 10.1016/j.neurobiolaging.2005.02.014
49. 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
50. 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
51. 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
52. Richard, E. M., Helbling, J. C., Tridon, C., Desmedt, A., Minni, A. M., Cador, M., et al. (2010). Plasma transcortin influences endocrine and behavioral stress responses in mice. Endocrinology 151, 649-659. doi: 10.1210/en.2009-0862
53. Ross, A. C., Russell, R. M., Miller, S. A., Munro, I. C., Rodricks, J. V., Yetley, E. A., et al. (2009). Application of a key events dose-response analysis to nutrients: a case study with vitamin A (retinol). Crit. Rev. Food Sci. Nutr. 49, 708-717. doi: 10.1080/10408390903098749
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. Sandi, C. (2003). [Glucocorticoid involvement in memory consolidation]. Rev. Neurol. 37, 843-848.
56. Sandi, C., Cordero, M. I., Merino, J. J., Kruyt, N. D., Regan, C. M., and Murphy, K. J. (2004). Neurobiological and endocrine correlates of individual differences in spatial learning ability. Learn. Mem. 11, 244-252. doi: 10.1101/lm.73904
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. Sooy, K., Webster, S. P., Noble, J., Binnie, M., Walker, B. R., Seckl, J. R., et al. (2010). Partial deficiency or short-term inhibition of 11beta-hydroxysteroid dehydrogenase type 1 improves cognitive function in aging mice. J. Neurosci. 30, 13867-13872. doi: 10.1523/JNEUROSCI.2783-10.2010
59. Souganidis, E., Laillou, A., Leyvraz, M., and Moench-Pfanner, R. (2013). A comparison of retinyl palmitate and red palm oil beta-carotene as strategies to address Vitamin A deficiency. Nutrients 5, 3257-3271. doi: 10.3390/nu5083257
60. Sousa, N., Lukoyanov, N. V., Madeira, M. D., Almeida, O. F., and Paula-Barbosa, M. M. (2000). Reorganization of the morphology of hippocampal neurites and synapses after stress-induced damage correlates with behavioral improvement. Neuroscience 97, 253-266. doi: 10.1016/S0306-4522(00)00050-6
61. 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
62. Walf, A. A., and Frye, C. A. (2007). The use of the elevated plus maze as an assay of anxiety-related behavior in rodents. Nat. Protoc. 2, 322-328. doi: 10.1038/nprot.2007.44
63. Yau, J. L., McNair, K. M., Noble, J., Brownstein, D., Hibberd, C., Morton, N., et al. (2007). Enhanced hippocampal long-term potentiation and spatial learning in aged 11beta-hydroxysteroid dehydrogenase type 1 knock-out mice. J. Neurosci. 27, 10487-10496. doi: 10.1523/JNEUROSCI.2190-07.2007
64. 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
65. Yau, J. L., Noble, J., and Seckl, J. R. (2011). 11beta-hydroxysteroid dehydrogenase type 1 deficiency prevents memory deficits with aging by switching from glucocorticoid receptor to mineralocorticoid receptor-mediated cognitive control. J. Neurosci. 31, 4188-4193. doi: 10.1523/JNEUROSCI.6145-10.2011
66. Yau, J. L., Olsson, T., Morris, R. G., Meaney, M. J., and Seckl, J. R. (1995). Glucocorticoids, hippocampal corticosteroid receptor gene expression and antidepressant treatment: relationship with spatial learning in young and aged rats. Neuroscience 66, 571-581. doi: 10.1016/0306-4522(94)00612-9
67. 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
68. Yau, S. Y., Lau, B. W., Zhang, E. D., Lee, J. C., Li, A., Lee, T. M., et al. (2012). Effects of voluntary running on plasma levels of neurotrophins, hippocampal cell proliferation and learning and memory in stressed rats. Neuroscience 222, 289-301. doi: 10.1016/j.neuroscience.2012.07.019
69. Zhang, M., Huang, K., Zhang, Z., Ji, B., Zhu, H., Zhou, K., et al. (2011). Proteome alterations of cortex and hippocampus tissues in mice subjected to vitamin A depletion. J. Nutr. Biochem. 22, 1003-1008. doi: 10.1016/j.jnutbio.2010.08.012