Adult Hippocampal Neurogenesis in Depression: Behavioral Implications and Regulation by the Stress System (original) (raw)
Altman J, Das GD (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J Comp Neurol 124:319–335 ArticleCASPubMed Google Scholar
Anacker C, Cattaneo A, Luoni A, Musaelyan K, Zunszain PA, Milanesi E, Rybka J, Berry A, Cirulli F, Thuret S, Price J, Riva MA, Gennarelli M, Pariante CM (2013a) Glucocorticoid-related molecular signaling pathways regulating hippocampal neurogenesis. Neuropsychopharmacology 38:872–883 ArticleCASPubMed CentralPubMed Google Scholar
Anacker C, Cattaneo A, Musaelyan K, Zunszain PA, Horowitz M, Molteni R, Luoni A, Calabrese F, Tansey K, Gennarelli M, Thuret S, Price J, Uher R, Riva MA, Pariante CM (2013b) Role for the kinase SGK1 in stress, depression, and glucocorticoid effects on hippocampal neurogenesis. Proc Natl Acad Sci USA 110:8708–8713 ArticleCASPubMed CentralPubMed Google Scholar
Anacker C, Pariante CM (2012a) Can adult neurogenesis buffer stress responses and depressive behaviour? Mol Psychiatry 17:9–10 ArticleCASPubMed Google Scholar
Anacker C, Pariante CM (2012b) New models to investigate complex glucocorticoid receptor functions. Front Behav Neurosci 6:90 Google Scholar
Anacker C, Zunszain PA, Carvalho LA, Pariante CM (2011a) The glucocorticoid receptor: pivot of depression and of antidepressant treatment? Psychoneuroendocrinology 36:415–425 ArticleCASPubMed CentralPubMed Google Scholar
Anacker C, Zunszain PA, Cattaneo A, Carvalho LA, Garabedian MJ, Thuret S, Price J, Pariante CM (2011b) Antidepressants increase human hippocampal neurogenesis by activating the glucocorticoid receptor. Mol Psychiatry 16:738–750 ArticleCASPubMed CentralPubMed Google Scholar
Appelhof BC, Huyser J, Verweij M, Brouwer JP, van Dyck R, Fliers E, Hoogendijk WJ, Tijssen JG, Wiersinga WM, Schene AH (2006) Glucocorticoids and relapse of major depression (dexamethasone/corticotropin-releasing hormone test in relation to relapse of major depression). Biol Psychiatry 59:696–701 ArticleCASPubMed Google Scholar
Banasr M, Soumier A, Hery M, Mocaer E, Daszuta A (2006) Agomelatine, a new antidepressant, induces regional changes in hippocampal neurogenesis. Biol Psychiatry 59:1087–1096 ArticleCASPubMed Google Scholar
Bessa JM, Ferreira D, Melo I, Marques F, Cerqueira JJ, Palha JA, Almeida OF, Sousa N (2009) The mood-improving actions of antidepressants do not depend on neurogenesis but are associated with neuronal remodeling. Mol Psychiatry 14:739, 764–773 Google Scholar
Boldrini M, Hen R, Underwood MD, Rosoklija GB, Dwork AJ, Mann JJ, Arango V (2012) Hippocampal angiogenesis and progenitor cell proliferation are increased with antidepressant use in major depression. Biol Psychiatry 72:562–571 ArticleCASPubMed CentralPubMed Google Scholar
Boldrini M, Underwood MD, Hen R, Rosoklija GB, Dwork AJ, John Mann J, Arango V (2009) Antidepressants increase neural progenitor cells in the human hippocampus. Neuropsychopharmacology 34:2376–2389 ArticleCASPubMed CentralPubMed Google Scholar
Boyle MP, Brewer JA, Funatsu M, Wozniak DF, Tsien JZ, Izumi Y, Muglia LJ (2005) Acquired deficit of forebrain glucocorticoid receptor produces depression-like changes in adrenal axis regulation and behavior. Proc Natl Acad Sci USA 102:473–478 ArticleCASPubMed CentralPubMed Google Scholar
Brown J, Cooper-Kuhn CM, Kempermann G, Van Praag H, Winkler J, Gage FH, Kuhn HG (2003) Enriched environment and physical activity stimulate hippocampal but not olfactory bulb neurogenesis. Eur J Neurosci 17:2042–2046 ArticlePubMed Google Scholar
Caldji C, Diorio J, Meaney MJ (2000) Variations in maternal care in infancy regulate the development of stress reactivity. Biol Psychiatry 48:1164–1174 ArticleCASPubMed Google Scholar
Cameron HA, McEwen BS, Gould E (1995) Regulation of adult neurogenesis by excitatory input and NMDA receptor activation in the dentate gyrus. J Neurosci 15:4687–4692 CASPubMed Google Scholar
Coe CL, Kramer M, Czeh B, Gould E, Reeves AJ, Kirschbaum C, Fuchs E (2003) Prenatal stress diminishes neurogenesis in the dentate gyrus of juvenile rhesus monkeys. Biol Psychiatry 54:1025–1034 ArticleCASPubMed Google Scholar
Dagyte G, Trentani A, Postema F, Luiten PG, Den Boer JA, Gabriel C, Mocaër E, Meerlo P, Van der Zee EA (2010) The novel antidepressant agomelatine normalizes hippocampal neuronal activity and promotes neurogenesis in chronically stressed rats. CNS Neurosci Ther 16:195–207 ArticleCASPubMed Google Scholar
David DJ, Samuels BA, Rainer Q, Wang JW, Marsteller D, Mendez I, Drew M, Craig DA, Guiard BP, Guilloux JP, Artymyshyn RP, Gardier AM, Gerald C, Antonijevic IA, Leonardo ED, Hen R (2009) Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron 62:479–493 ArticleCASPubMed CentralPubMed Google Scholar
Diamond DM, Bennett MC, Fleshner M, Rose GM (1992) Inverted-U relationship between the level of peripheral corticosterone and the magnitude of hippocampal primed burst potentiation. Hippocampus 2:421–430 ArticleCASPubMed Google Scholar
Duman RS (2004) Role of neurotrophic factors in the etiology and treatment of mood disorders. Neuromolecular Med 5:11–25 ArticleCASPubMed Google Scholar
Egeland M, Warner-Schmidt J, Greengard P, Svenningsson P (2010) Neurogenic effects of fluoxetine are attenuated in p11 (S100A10) knockout mice. Biol Psychiatry 67:1048–1056 ArticleCASPubMed Google Scholar
Eriksson PS, Perfilieva E, Bjork-Eriksson T, Alborn AM, Nordborg C, Peterson DA, Gage FH (1998) Neurogenesis in the adult human hippocampus. Nat Med 4:1313–1317 ArticleCASPubMed Google Scholar
Fitzsimons CP, van Hooijdonk LW, Schouten M, Zalachoras I, Brinks V, Zheng T, Schouten TG, Saaltink DJ, Dijkmans T, Steindler DA, Verhaagen J, Verbeek FJ, Lucassen PJ, de Kloet ER, Meijer OC, Karst H, Joels M, Oitzl MS, Vreugdenhil E (2013) Knockdown of the glucocorticoid receptor alters functional integration of newborn neurons in the adult hippocampus and impairs fear-motivated behavior. Mol Psychiatry 18:993–1005 Google Scholar
Gass P, Kretz O, Wolfer DP, Berger S, Tronche F, Reichardt HM, Kellendonk C, Lipp HP, Schmid W, Schutz G (2000) Genetic disruption of mineralocorticoid receptor leads to impaired neurogenesis and granule cell degeneration in the hippocampus of adult mice. EMBO Rep 1:447–451 ArticleCASPubMed CentralPubMed Google Scholar
Glasper ER, Schoenfeld TJ, Gould E (2012) Adult neurogenesis: optimizing hippocampal function to suit the environment. Behav Brain Res 14; 227(2):380–383 Google Scholar
Goritz C, Frisen J (2012) Neural stem cells and neurogenesis in the adult. Cell Stem Cell 10:657–659 ArticlePubMed Google Scholar
Gould E, McEwen BS, Tanapat P, Galea LA, Fuchs E (1997) Neurogenesis in the dentate gyrus of the adult tree shrew is regulated by psychosocial stress and NMDA receptor activation. J Neurosci 17:2492–2498 CASPubMed Google Scholar
Guidotti G, Calabrese F, Anacker C, Racagni G, Pariante CM, Riva MA (2013) Glucocorticoid receptor and FKBP5 expression is altered following exposure to chronic stress: modulation by antidepressant treatment. Neuropsychopharmacology 38:616–627 ArticleCASPubMed CentralPubMed Google Scholar
Henke PG (1990) Hippocampal pathway to the amygdala and stress ulcer development. Brain Res Bull 25:691–695 ArticleCASPubMed Google Scholar
Hoglinger GU, Rizk P, Muriel MP, Duyckaerts C, Oertel WH, Caille I, Hirsch EC (2004) Dopamine depletion impairs precursor cell proliferation in Parkinson disease. Nat Neurosci 7:726–735 ArticlePubMed Google Scholar
Holick KA, Lee DC, Hen R, Dulawa SC (2008) Behavioral effects of chronic fluoxetine in BALB/cJ mice do not require adult hippocampal neurogenesis or the serotonin 1A receptor. Neuropsychopharmacology 33:406–417 ArticleCASPubMed Google Scholar
Holsboer F (2000) The corticosteroid receptor hypothesis of depression. Neuropsychopharmacology 23:477–501 ArticleCASPubMed Google Scholar
Holsboer F, Von Bardeleben U, Gerken A, Stalla GK, Muller OA (1984) Blunted corticotropin and normal cortisol response to human corticotropin-releasing factor in depression. N Engl J Med 311:1127 CASPubMed Google Scholar
Hu P, Oomen C, van Dam AM, Wester J, Zhou JN, Joëls M, Lucassen PJ (2012) A single-day treatment with mifepristone is sufficient to normalize chronic glucocorticoid induced suppression of hippocampal cell proliferation. PLoS ONE 7:e46224 ArticleCASPubMed CentralPubMed Google Scholar
Huang GJ, Herbert J (2006) Stimulation of neurogenesis in the hippocampus of the adult rat by fluoxetine requires rhythmic change in corticosterone. Biol Psychiatry 59:619–624 ArticleCASPubMed Google Scholar
Jacobson L, Sapolsky R (1991) The role of the hippocampus in feedback regulation of the hypothalamic-pituitary-adrenocortical axis. Endocr Rev 12:118–134 ArticleCASPubMed Google Scholar
Juruena MF, Cleare AJ, Papadopoulos AS, Poon L, Lightman S, Pariante CM (2006) Different responses to dexamethasone and prednisolone in the same depressed patients. Psychopharmacology 189:225–235 ArticleCASPubMed Google Scholar
Kaplan MS, Hinds JW (1977) Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197:1092–1094 ArticleCASPubMed Google Scholar
Kheirbek MA, Drew LJ, Burghardt NS, Costantini DO, Tannenholz L, Ahmari SE, Zeng H, Fenton AA, Hen R (2013) Differential control of learning and anxiety along the dorsoventral axis of the dentate gyrus. Neuron 77:955–968 ArticleCASPubMed CentralPubMed Google Scholar
Koehl M, van der Veen R, Gonzales D, Piazza PV, Abrous DN (2012) Interplay of maternal care and genetic influences in programming adult hippocampal neurogenesis. Biol Psychiatry 72:282–289 ArticlePubMed Google Scholar
Kronenberg G, Kirste I, Inta D, Chourbaji S, Heuser I, Endres M, Gass P (2009) Reduced hippocampal neurogenesis in the GR(±) genetic mouse model of depression. Eur Arch Psychiatry Clin Neurosci 259(8):499–504 Google Scholar
Lehmann ML, Brachman RA, Martinowich K, Schloesser RJ, Herkenham M (2013) Glucocorticoids orchestrate divergent effects on mood through adult neurogenesis. J Neurosci 33:2961–2972 ArticleCASPubMed CentralPubMed Google Scholar
Lemaire V, Koehl M, Le Moal M, Abrous DN (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 ArticleCASPubMed CentralPubMed Google Scholar
Leuner B, Caponiti JM, Gould E (2012) Oxytocin stimulates adult neurogenesis even under conditions of stress and elevated glucocorticoids. Hippocampus 22:861–868 ArticleCASPubMed Google Scholar
Leuner B, Glasper ER, Gould E (2010) Sexual experience promotes adult neurogenesis in the hippocampus despite an initial elevation in stress hormones. PLoS ONE 5:e11597 ArticlePubMed CentralPubMed Google Scholar
Liu D, Diorio J, Day JC, Francis DD, Meaney MJ (2000) Maternal care, hippocampal synaptogenesis and cognitive development in rats. Nat Neurosci 3:799–806 ArticleCASPubMed Google Scholar
Lucassen PJ, Stumpel MW, Wang Q, Aronica E (2010) Decreased numbers of progenitor cells but no response to antidepressant drugs in the hippocampus of elderly depressed patients. Neuropharmacology 58:940–949 ArticleCASPubMed Google Scholar
Malberg JE, Eisch AJ, Nestler EJ, Duman RS (2000) Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci 20:9104–9110 CASPubMed Google Scholar
Mateus-Pinheiro A, Pinto L, Bessa JM, Morais M, Alves ND, Monteiro S, Patrício P, Almeida OF, Sousa N (2013) Sustained remission from depressive-like behavior depends on hippocampal neurogenesis. Transl Psychiatry 3:e210 ArticleCASPubMed CentralPubMed Google Scholar
Mayer JL, Klumpers L, Maslam S, de Kloet ER, Joels M, Lucassen PJ (2006) Brief treatment with the glucocorticoid receptor antagonist mifepristone normalises the corticosterone-induced reduction of adult hippocampal neurogenesis. J Neuroendocrinol 18:629–631 ArticleCASPubMed Google Scholar
Meaney MJ, O’Donnell D, Rowe W, Tannenbaum B, Steverman A, Walker M, Nair NP, Lupien S (1995) Individual differences in hypothalamic-pituitary-adrenal activity in later life and hippocampal aging. Exp Gerontol 30:229–251 ArticleCASPubMed Google Scholar
Miller AH, Vogt GJ, Pearce BD (2002) The phosphodiesterase type 4 inhibitor, rolipram, enhances glucocorticoid receptor function. Neuropsychopharmacology 27:939–948 ArticleCASPubMed Google Scholar
Mirescu C, Peters JD, Gould E (2004) Early life experience alters response of adult neurogenesis to stress. Nat Neurosci 7:841–846 ArticleCASPubMed Google Scholar
Murray F, Smith DW, Hutson PH (2008) Chronic low dose corticosterone exposure decreased hippocampal cell proliferation, volume and induced anxiety and depression like behaviours in mice. Eur J Pharmacol 583:115–127 ArticleCASPubMed Google Scholar
Nemeroff CB, Krishnan KR, Reed D, Leder R, Beam C, Dunnick NR (1992) Adrenal gland enlargement in major depression. A computed tomographic study: Arch Gen Psychiatry 49:384–387 CASPubMed Google Scholar
Oomen CA, Mayer JL, de Kloet ER, Joels M, Lucassen PJ (2007) Brief treatment with the glucocorticoid receptor antagonist mifepristone normalizes the reduction in neurogenesis after chronic stress. Eur J Neurosci 26:3395–3401 ArticlePubMed Google Scholar
Pariante CM (2006) The glucocorticoid receptor: part of the solution or part of the problem? J Psychopharmacol 20:79–84 ArticlePubMed Google Scholar
Pariante CM, Lightman SL (2008) The HPA axis in major depression: classical theories and new developments. Trends Neurosci 31:464–468 ArticleCASPubMed Google Scholar
Pariante CM, Makoff A, Lovestone S, Feroli S, Heyden A, Miller AH, Kerwin RW (2001) Antidepressants enhance glucocorticoid receptor function in vitro by modulating the membrane steroid transporters. Br J Pharmacol 134:1335–1343 ArticleCASPubMed CentralPubMed Google Scholar
Pariante CM, Miller AH (2001) Glucocorticoid receptors in major depression: relevance to pathophysiology and treatment. Biol Psychiatry 49:391–404 ArticleCASPubMed Google Scholar
Pariante CM, Pearce BD, Pisell TL, Owens MJ, Miller AH (1997) Steroid-independent translocation of the glucocorticoid receptor by the antidepressant desipramine. Mol Pharmacol 52:571–581 CASPubMed Google Scholar
Pascual-Leone A, Amedi A, Fregni F, Merabet LB (2005) The plastic human brain cortex. Annu Rev Neurosci 28:377–401 ArticleCASPubMed Google Scholar
Perera TD, Coplan JD, Lisanby SH, Lipira CM, Arif M, Carpio C, Spitzer G, Santarelli L, Scharf B, Hen R, Rosoklija G, Sackeim HA, Dwork AJ (2007) Antidepressant-induced neurogenesis in the hippocampus of adult nonhuman primates. J Neurosci 27:4894–4901 ArticleCASPubMed Google Scholar
Perera TD, Dwork AJ, Keegan KA, Thirumangalakudi L, Lipira CM, Joyce N, Lange C, Higley JD, Rosoklija G, Hen R, Sackeim HA, Coplan JD (2011) Necessity of hippocampal neurogenesis for the therapeutic action of antidepressants in adult nonhuman primates. PLoS ONE 6:e17600 ArticleCASPubMed CentralPubMed Google Scholar
Ramon y Cajal S (1928) Degeneration and regeneration of the nervous system. Oxford University Press, London Google Scholar
Reif A, Fritzen S, Finger M, Strobel A, Lauer M, Schmitt A, Lesch KP (2006) Neural stem cell proliferation is decreased in schizophrenia, but not in depression. Mol Psychiatry 11:514–522 ArticleCASPubMed Google Scholar
Revest JM, Dupret D, Koehl M, Funk-Reiter C, Grosjean N, Piazza PV, Abrous DN (2009) Adult hippocampal neurogenesis is involved in anxiety-related behaviors. Mol Psychiatry 14:959–967 ArticlePubMed Google Scholar
Sahay A, Scobie KN, Hill AS, O’Carroll CM, Kheirbek MA, Burghardt NS, Fenton AA, Dranovsky A, Hen R (2011) Increasing adult hippocampal neurogenesis is sufficient to improve pattern separation. Nature 472:466–470 ArticleCASPubMed CentralPubMed Google Scholar
Santarelli L, Saxe M, Gross C, Surget A, Battaglia F, Dulawa S, Weisstaub N, Lee J, Duman R, Arancio O, Belzung C, Hen R (2003) Requirement of hippocampal neurogenesis for the behavioral effects of antidepressants. Science 301:805–809 ArticleCASPubMed Google Scholar
Sapolsky RM, Meaney MJ, McEwen BS (1985) The development of the glucocorticoid receptor system in the rat limbic brain: III. Negative-feedback regulation. Brain Res 350:169–173 ArticleCASPubMed Google Scholar
Schloesser RJ, Manji HK, Martinowich K (2009) Suppression of adult neurogenesis leads to an increased hypothalamo-pituitary-adrenal axis response. NeuroReport 20:553–557 ArticleCASPubMed CentralPubMed Google Scholar
Sheline YI, Wang PW, Gado MH, Csernansky JG, Vannier MW (1996) Hippocampal atrophy in recurrent major depression. Proc Natl Acad Sci USA 93:3908–3913 ArticleCASPubMed CentralPubMed Google Scholar
Snyder JS, Soumier A, Brewer M, Pickel J, Cameron HA (2011) Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature 476:458–461 Google Scholar
Spalding KL, Bergmann O, Alkass K, Bernard S, Salehpour M, Huttner HB, Boström E, Westerlund I, Vial C, Buchholz BA, Possnert G, Mash DC, Druid H, Frisén J (2013) Dynamics of hippocampal neurogenesis in adult humans. Cell 153:1219–1227 ArticleCASPubMed Google Scholar
Surget A, Saxe M, Leman S, Ibarguen-Vargas Y, Chalon S, Griebel G, Hen R, Belzung C (2008) Drug-dependent requirement of hippocampal neurogenesis in a model of depression and of antidepressant reversal. Biol Psychiatry 64:293–301 ArticleCASPubMed Google Scholar
Surget A, Tanti A, Leonardo ED, Laugeray A, Rainer Q, Touma C, Palme R, Griebel G, Ibarguen-Vargas Y, Hen R, Belzung C (2011) Antidepressants recruit new neurons to improve stress response regulation. Mol Psychiatry 16:1177–1188 Google Scholar
Tanapat P, Galea LA, Gould E (1998) Stress inhibits the proliferation of granule cell precursors in the developing dentate gyrus. Int J Dev Neurosci 16:235–239 ArticleCASPubMed Google Scholar
Tanti A, Rainer Q, Minier F, Surget A, Belzung C (2012) Differential environmental regulation of neurogenesis along the septo-temporal axis of the hippocampus. Neuropharmacology 63:374–384 Google Scholar
Tronche F, Kellendonk C, Kretz O, Gass P, Anlag K, Orban PC, Bock R, Klein R, Schutz G (1999) Disruption of the glucocorticoid receptor gene in the nervous system results in reduced anxiety. Nat Genet 23:99–103 ArticleCASPubMed Google Scholar
van Praag H, Christie BR, Sejnowski TJ, Gage FH (1999) Running enhances neurogenesis, learning, and long-term potentiation in mice. Proc Natl Acad Sci USA 96:13427–13431 ArticlePubMed CentralPubMed Google Scholar
Watanabe Y, Gould E, Daniels DC, Cameron H, McEwen BS (1992) Tianeptine attenuates stress-induced morphological changes in the hippocampus. Eur J Pharmacol 222:157–162 ArticleCASPubMed Google Scholar
Weaver IC, Meaney MJ, Szyf M (2006) Maternal care effects on the hippocampal transcriptome and anxiety-mediated behaviors in the offspring that are reversible in adulthood. Proc Natl Acad Sci USA 103:3480–3485 ArticleCASPubMed CentralPubMed Google Scholar
Willner P (2005) Chronic mild stress (CMS) revisited: consistency and behavioural-neurobiological concordance in the effects of CMS. Neuropsychobiology 52:90–110 ArticleCASPubMed Google Scholar
Woolley CS, Gould E, McEwen BS (1990) Exposure to excess glucocorticoids alters dendritic morphology of adult hippocampal pyramidal neurons. Brain Res 531:225–231 ArticleCASPubMed Google Scholar
Young EA, Haskett RF, Murphy-Weinberg V, Watson SJ, Akil H (1991) Loss of glucocorticoid fast feedback in depression. Arch Gen Psychiatry 48:693–699 ArticleCASPubMed Google Scholar
Zobel AW, Nickel T, Sonntag A, Uhr M, Holsboer F, Ising M (2001) Cortisol response in the combined dexamethasone/CRH test as predictor of relapse in patients with remitted depression: a prospective study. J Psychiatr Res 35:83–94 ArticleCASPubMed Google Scholar
Zunszain PA, Anacker C, Cattaneo A, Carvalho LA, Pariante CM (2011) Glucocorticoids, cytokines and brain abnormalities in depression. Prog Neuropsychopharmacol Biol Psychiatry 35:722–729 ArticleCASPubMed CentralPubMed Google Scholar
Zunszain PA, Anacker C, Cattaneo A, Choudhury S, Musaelyan K, Myint AM, Thuret S, Price J, Pariante CM (2012) Interleukin-1β: a new regulator of the kynurenine pathway affecting human hippocampal neurogenesis. Neuropsychopharmacology 37:939–949 ArticleCASPubMed CentralPubMed Google Scholar