Stress, glucocorticoid hormones, and hippocampal neural progenitor cells: Implications to mood disorders

Frontiers in Physiology

Volumn 6, Issue Aug, 2015, Pages 230-

  Kino, Tomoshige ^a  

^a SIDRA MEDICAL AND RESEARCH CENTER   (Qatar)

Author keywords

Dentate gyrus; Glucocorticoid receptor; Hippocampus; Major depression; Neural stem cells (NSCs)

Indexed keywords

GLUCOCORTICOID;

ADAPTATION; ASTROCYTE; BEHAVIOR; BRAIN FUNCTION; CELL FATE; CELL PROLIFERATION; CELL RENEWAL; COGNITION; HIPPOCAMPUS; HORMONE ACTION; HUMAN; HYPOTHALAMUS HYPOPHYSIS ADRENAL SYSTEM; MEMORY; MOOD; MOOD DISORDER; NERVE CELL; NERVE CELL DIFFERENTIATION; NEURAL STEM CELL; NONHUMAN; OLIGODENDROGLIA; PATHOPHYSIOLOGY; REVIEW; STRESS;

EID: 84940924570     PISSN: None     EISSN: 1664042X     Source Type: Journal    
DOI: 10.3389/fphys.2015.00230     Document Type: Review

References (67)

1. Anacker, C., Zunszain, P.A., Cattaneo, A., Carvalho, L.A., Garabedian, M.J., Thuret, S., et al. (2011). Antidepressants increase human hippocampal neurogenesis by activating the glucocorticoid receptor. Mol. Psychiatry 16, 738-750. doi: 10.1038/mp.2011.26.
2. Androutsellis-Theotokis, A., Chrousos, G.P., McKay, R.D., DeCherney, A.H., and Kino, T. (2013). Expression profiles of the nuclear receptors and their transcriptional coregulators during differentiation of neural stem cells. Horm. Metab. Res. 45, 159-168. doi: 10.1055/s-0032-1321789.
3. Androutsellis-Theotokis, A., Murase, S., Boyd, J.D., Park, D.M., Hoeppner, D.J., Ravin, R., et al. (2008a). Generating neurons from stem cells. Methods Mol. Biol. 438, 31-38. doi: 10.1007/978-1-59745-133-8_4.
4. Androutsellis-Theotokis, A., Rubin de Celis, M.F., Ehrhart-Bornstein, M., and Bornstein, S.R. (2012). Common features between chromaffin and neural progenitor cells. Mol. Psychiatry 17, 351. doi: 10.1038/mp.2012.18.
5. Androutsellis-Theotokis, A., Rueger, M.A., Mkhikian, H., Korb, E., and McKay, R.D. (2008b). Signaling pathways controlling neural stem cells slow progressive brain disease. Cold Spring Harb. Symp. Quant. Biol. 73, 403-410. doi: 10.1101/sqb.2008.73.018.
6. Androutsellis-Theotokis, A., Rueger, M.A., Park, D.M., Mkhikian, H., Korb, E., Poser, S.W., et al. (2009). Targeting neural precursors in the adult brain rescues injured dopamine neurons. Proc. Natl. Acad. Sci. U.S.A. 106, 13570-13575. doi: 10.1073/pnas.0905125106.
7. Aztiria, E., Capodieci, G., Arancio, L., and Leanza, G. (2007). Extensive training in a maze task reduces neurogenesis in the adult rat dentate gyrus probably as a result of stress. Neurosci. Lett. 416, 133-137. doi: 10.1016/j.neulet.2007.01.069.
8. Bessa, J.M., Ferreira, D., Melo, I., Marques, F., Cerqueira, J.J., Palha, J.A., et al. (2009). The mood-improving actions of antidepressants do not depend on neurogenesis but are associated with neuronal remodeling. Mol. Psychiatry 14, 764-773, 739. doi: 10.1038/mp.2008.119.
9. Boku, S., Nakagawa, S., Masuda, T., Nishikawa, H., Kato, A., Kitaichi, Y., et al. (2009). Glucocorticoids and lithium reciprocally regulate the proliferation of adult dentate gyrus-derived neural precursor cells through GSK-3b and b-catenin/TCF pathway. Neuropsychopharmacology 34, 805-815. doi: 10.1038/npp.2008.198.
10. Bornstein, S.R., Ehrhart-Bornstein, M., Androutsellis-Theotokis, A., Eisenhofer, G., Vukicevic, V., Licinio, J., et al. (2012). Chromaffin cells: the peripheral brain. Mol. Psychiatry 17, 354-358. doi: 10.1038/mp.2011.176.
11. Brummelte, S., and Galea, L.A. (2010). Chronic high corticosterone reduces neurogenesis in the dentate gyrus of adult male and female rats. Neuroscience 168, 680-690. doi: 10.1016/j.neuroscience.2010.04.023.
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. Chen, G., Rajkowska, G., Du, F., Seraji-Bozorgzad, N., and Manji, H.K. (2000). Enhancement of hippocampal neurogenesis by lithium. J. Neurochem. 75, 1729-1734. doi: 10.1046/j.1471-4159.2000.0751729.x.
14. Chrousos, G.P., and Kino, T. (2005). Intracellular glucocorticoid signaling: a formerly simple system turns stochastic. Sci. STKE 2005:pe48. doi: 10.1126/stke.3042005pe48.
15. Chrousos, G.P., and Kino, T. (2007). Glucocorticoid action networks and complex psychiatric and/or somatic disorders. Stress 10, 213-219. doi: 10.1080/10253890701292119.
16. Chrousos, G.P. (2009). Stress and disorders of the stress system. Nat. Rev. Endocrinol. 5, 374-381. doi: 10.1038/nrendo.2009.106.
17. Crochemore, C., Lu, J., Wu, Y., Liposits, Z., Sousa, N., Holsboer, F., et al. (2005). Direct targeting of hippocampal neurons for apoptosis by glucocorticoids is reversible by mineralocorticoid receptor activation. Mol. Psychiatry 10, 790-798. doi: 10.1038/sj.mp.4001679.
18. Dupret, D., Fabre, A., Döbrössy, M.D., Panatier, A., Rodríguez, J.J., Lamarque, S., et al. (2007). Spatial learning depends on both the addition and removal of new hippocampal neurons. PLoS Biol. 5:e214. doi: 10.1371/journal.pbio.0050214.
19. Fischer, A.K., von Rosenstiel, P., Fuchs, E., Goula, D., Almeida, O.F., and Czéh, B. (2002). The prototypic mineralocorticoid receptor agonist aldosterone influences neurogenesis in the dentate gyrus of the adrenalectomized rat. Brain Res. 947, 290-293. doi: 10.1016/S0006-8993(02)03042-1.
20. Funato, H., Kobayashi, A., and Watanabe, Y. (2006). Differential effects of antidepressants on dexamethasone-induced nuclear translocation and expression of glucocorticoid receptor. Brain Res. 1117, 125-134. doi: 10.1016/j.brainres.2006.08.029.
21. Gold, P.W., and Chrousos, G.P. (2002). Organization of the stress system and its dysregulation in melancholic and atypical depression: high vs. low CRH/NE states. Mol. Psychiatry 7, 254-275. doi: 10.1038/sj.mp.4001032.
22. Gold, P.W., Goodwin, F.K., and Chrousos, G.P. (1988a). Clinical and biochemical manifestations of depression. Relation to the neurobiology of stress (2). N. Engl. J. Med. 319, 413-420.
23. Gold, P.W., Goodwin, F.K., and Chrousos, G.P. (1988b). Clinical and biochemical manifestations of depression. Relation to the neurobiology of stress (1). N. Engl. J. Med. 319, 348-353.
24. Gould, E., Beylin, A., Tanapat, P., Reeves, A., and Shors, T.J. (1999). Learning enhances adult neurogenesis in the hippocampal formation. Nat. Neurosci. 2, 260-265. doi: 10.1038/6365.
25. Gray, J.D., Milner, T.A., and McEwen, B.S. (2013). Dynamic plasticity: the role of glucocorticoids, brain-derived neurotrophic factor and other trophic factors. Neuroscience 239, 214-227. doi: 10.1016/j.neuroscience.2012.08.034.
26. Hill, A.S., Sahay, A., and Hen, R. (2015). Increasing adult hippocampal neurogenesis is sufficient to reduce anxiety and depression-like behaviors. Neuropsychopharmacology. doi: 10.1038/npp.2015.85. [Epub ahead of print].
27. Jessberger, S., Aigner, S., Clemenson, G.D. Jr., Toni, N., Lie, D.C., Karalay, O., et al. (2008). Cdk5 regulates accurate maturation of newborn granule cells in the adult hippocampus. PLoS Biol. 6:e272. doi: 10.1371/journal.pbio.0060272.
28. Joëls, M. (2008). Functional actions of corticosteroids in the hippocampus. Eur. J. Pharmacol. 583, 312-321. doi: 10.1016/j.ejphar.2007.11.064.
29. Jonas, P., and Lisman, J. (2014). Structure, function, and plasticity of hippocampal dentate gyrus microcircuits. Front. Neural Circuits 8:107. doi: 10.3389/fncir.2014.00107.
30. Kino, T. (2000). "Glucocorticoid receptor," in Endotext, eds L. J. De Groot, P. Beck-Peccoz, G. Chrousos, K. Dungan, A. Grossman, J.M. Hershman, et al. (South Dartmouth, MA: MDText.com, Inc.).
31. Kino, T. (2007). Tissue glucocorticoid sensitivity: beyond stochastic regulation on the diverse actions of glucocorticoids. Horm. Metab. Res. 39, 420-424. doi: 10.1055/s-2007-980193.
32. Kino, T. (2012). Circadian rhythms of glucocorticoid hormone actions in target tissues: potential clinical implications. Sci. Signal. 5, pt4. doi: 10.1126/scisignal.2003333.
33. Kino, T., and Chrousos, G.P. (2004a). "Glucocorticoid effect on gene expression," in Handbook on Stress and the Brain Part 1, eds T. Steckler, N.H. Kalin, J.M. Reul and H. M. Reul (Amsterdam: Elsevier BV), 295-312.
34. Kino, T., and Chrousos, G.P. (2004b). Glucocorticoid and mineralocorticoid receptors and associated diseases. Essays Biochem. 40, 137-155. doi: 10.1042/bse0400137.
35. Kino, T., and Chrousos, G.P. (2011). Acetylation-mediated epigenetic regulation of glucocorticoid receptor activity: circadian rhythm-associated alterations of glucocorticoid actions in target tissues. Mol. Cell. Endocrinol. 336, 23-30. doi: 10.1016/j.mce.2010.12.001.
36. Kino, T., De Martino, M.U., Charmandari, E., Mirani, M., and Chrousos, G.P. (2003). Tissue glucocorticoid resistance/hypersensitivity syndromes. J. Steroid Biochem. Mol. Biol. 85, 457-467. doi: 10.1016/S0960-0760(03)00218-8.
37. Kino, T., Ichijo, T., Amin, N.D., Kesavapany, S., Wang, Y., Kim, N., et al. (2007). Cyclin-dependent kinase 5 differentially regulates the transcriptional activity of the glucocorticoid receptor through phosphorylation: clinical implications for the nervous system response to glucocorticoids and stress. Mol. Endocrinol. 21, 1552-1568. doi: 10.1210/me.2006-0345.
38. Kino, T., Jaffe, H., Amin, N.D., Chakrabarti, M., Zheng, Y.L., Chrousos, G.P., et al. (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. doi: 10.1210/me.2009-0395.
39. Lau, W.M., Qiu, G., Helmeste, D.M., Lee, T.M., Tang, S.W., So, K.F., et al. (2007). Corticosteroid decreases subventricular zone cell proliferation, which could be reversed by paroxetine. Restor. Neurol. Neurosci. 25, 17-23.
40. Le Menuet, D., and Lombés, M. (2014). The neuronal mineralocorticoid receptor: from cell survival to neurogenesis. Steroids 91, 11-19. doi: 10.1016/j.steroids.2014.05.018.
41. Lemaire, V., Koehl, M., Le Moal, M., and Abrous, D.N. (2000). Prenatal stress produces learning deficits associated with an inhibition of neurogenesis in the hippocampus. Proc. Natl. Acad. Sci. U.S.A. 97, 11032-11037. doi: 10.1073/pnas.97.20.11032.
42. Leuner, B., Mendolia-Loffredo, S., Kozorovitskiy, Y., Samburg, D., Gould, E., and Shors, T.J. (2004). Learning enhances the survival of new neurons beyond the time when the hippocampus is required for memory. J. Neurosci. 24, 7477-7481. doi: 10.1523/JNEUROSCI. 0204-04.2004.
43. Malberg, J.E., Eisch, A.J., Nestler, E.J., and Duman, R.S. (2000). Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J. Neurosci. 20, 9104-9110.
44. Nader, N., Chrousos, G.P., and Kino, T. (2010). Interactions of the circadian CLOCK system and the HPA axis. Trends Endocrinol. Metab. 21, 277-286. doi: 10.1016/j.tem.2009.12.011.
45. Nicolaides, N.C., Charmandari, E., Chrousos, G.P., and Kino, T. (2014). Circadian endocrine rhythms: the hypothalamic-pituitary-adrenal axis and its actions. Ann. N.Y. Acad. Sci. 1318, 71-80. doi: 10.1111/nyas.12464.
46. Papadopoulou, A., Siamatras, T., Delgado-Morales, R.N., Amin, D.S. V., Zheng, Y.L., Pant, H.C., et al. (2015). Acute and chronic stress differentially regulate cyclin-dependent kinase 5 in mouse brain: implications to glucocorticoid actions and major depression. Trans. Psychiatry 5, e578. doi: 10.1038/tp.2015.72.
47. Pariante, C.M., Pearce, B.D., Pisell, T.L., Owens, M.J., and Miller, A.H. (1997). Steroid-independent translocation of the glucocorticoid receptor by the antidepressant desipramine. Mol. Pharmacol. 52, 571-581. doi: 10.1016/s0924-977x(97)88604-x.
48. Sahay, A., Scobie, K.N., Hill, A.S., O'Carroll, C.M., Kheirbek, M.A., Burghardt, N.S., et al. (2011). Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472, 466-470. doi: 10.1038/nature09817.
49. Schoenfeld, T.J., and Gould, E. (2013). Differential effects of stress and glucocorticoids on adult neurogenesis. Curr. Top. Behav. Neurosci. 15, 139-164. doi: 10.1007/7854_2012_233.
50. Sheline, Y.I., Wang, P.W., Gado, M.H., Csernansky, J.G., and Vannier, M.W. (1996). Hippocampal atrophy in recurrent major depression. Proc. Natl. Acad. Sci. U.S.A. 93, 3908-3913. doi: 10.1073/pnas.93.9.3908.
51. Shors, T.J. (2008). From stem cells to grandmother cells: how neurogenesis relates to learning and memory. Cell Stem Cell 3, 253-258. doi: 10.1016/j.stem.2008.08.010.
52. Smith, D.M., and Bulkin, D.A. (2014). The form and function of hippocampal context representations. Neurosci. Biobehav. Rev. 40, 52-61. doi: 10.1016/j.neubiorev.2014.01.005.
53. Snyder, J.S., Soumier, A., Brewer, M., Pickel, J., and Cameron, H.A. (2011). Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 476, 458-461. doi: 10.1038/nature10287.
54. Sousa, N., and Almeida, O.F. (2002). Corticosteroids: sculptors of the hippocampal formation. Rev. Neurosci. 13, 59-84. doi: 10.1515/revneuro.2002.13.1.59.
55. Spiers, H.J., and Bendor, D. (2014). Enhance, delete, incept: manipulating hippocampus-dependent memories. Brain Res. Bull. 105, 2-7. doi: 10.1016/j.brainresbull.2013.12.011.
56. Starkman, M.N., Gebarski, S.S., Berent, S., and Schteingart, D.E. (1992). Hippocampal formation volume, memory dysfunction, and cortisol levels in patients with Cushing's syndrome. Biol. Psychiatry 32, 756-765. doi: 10.1016/0006-3223(92)90079-F.
57. Sundberg, M., Savola, S., Hienola, A., Korhonen, L., and Lindholm, D. (2006). Glucocorticoid hormones decrease proliferation of embryonic neural stem cells through ubiquitin-mediated degradation of cyclin D1. J. Neurosci. 26, 5402-5410. doi: 10.1523/JNEUROSCI. 4906-05.2006.
58. Surget, A., Tanti, A., Leonardo, E.D., Laugeray, A., Rainer, Q., Touma, C., et al. (2011). Antidepressants recruit new neurons to improve stress response regulation. Mol. Psychiatry 16, 1177-1188. doi: 10.1038/mp.2011.48.
59. Tanapat, P., Hastings, N.B., Rydel, T.A., Galea, L.A., and Gould, E. (2001). Exposure to fox odor inhibits cell proliferation in the hippocampus of adult rats via an adrenal hormone-dependent mechanism. J. Comp. Neurol. 437, 496-504. doi: 10.1002/cne.1297.
60. Thomas, R.M., Hotsenpiller, G., and Peterson, D.A. (2007). Acute psychosocial stress reduces cell survival in adult hippocampal neurogenesis without altering proliferation. J. Neurosci. 27, 2734-2743. doi: 10.1523/JNEUROSCI. 3849-06.2007.
61. Wang, J., Lu, J., Bond, M.C., Chen, M., Ren, X.R., Lyerly, H.K., et al. (2010). Identification of select glucocorticoids as Smoothened agonists: potential utility for regenerative medicine. Proc. Natl. Acad. Sci. U.S.A. 107, 9323-9328. doi: 10.1073/pnas.0910712107.
62. Wong, E.Y., and Herbert, J. (2006). Raised circulating corticosterone inhibits neuronal differentiation of progenitor cells in the adult hippocampus. Neuroscience 137, 83-92. doi: 10.1016/j.neuroscience.2005.08.073.
63. Woolley, C.S., Gould, E., Sakai, R.R., Spencer, R.L., and McEwen, B.S. (1991). Effects of aldosterone or RU28362 treatment on adrenalectomy-induced cell death in the dentate gyrus of the adult rat. Brain Res. 554, 312-315. doi: 10.1016/0006-8993(91)90207-C.
64. Wyrwoll, C.S., Holmes, M.C., and Seckl, J.R. (2011). 11b-hydroxysteroid dehydrogenases and the brain: from zero to hero, a decade of progress. Front. Neuroendocrinol. 32, 265-286. doi: 10.1016/j.yfrne.2010.12.001.
65. Xi, G., Zhang, X., Zhang, L., Sui, Y., Hui, J., Liu, S., et al. (2011). Fluoxetine attenuates the inhibitory effect of glucocorticoid hormones on neurogenesis in vitro via a two-pore domain potassium channel, TREK-1. Psychopharmacology 214, 747-759. doi: 10.1007/s00213-010-2077-3.
66. Yu, S., Patchev, A.V., Wu, Y., Lu, J., Holsboer, F., Zhang, J.Z., et al. (2010). Depletion of the neural precursor cell pool by glucocorticoids. Ann. Neurol. 67, 21-30. doi: 10.1002/ana.21812.
67. Zhao, C., Deng, W., and Gage, F.H. (2008). Mechanisms and functional implications of adult neurogenesis. Cell 132, 645-660. doi: 10.1016/j.cell.2008.01.033.