Adult-born neurons from the dorsal, intermediate, and ventral regions of the longitudinal axis of the hippocampus exhibit differential sensitivity to glucocorticoids.
Journal
Molecular psychiatry
ISSN: 1476-5578
Titre abrégé: Mol Psychiatry
Pays: England
ID NLM: 9607835
Informations de publication
Date de publication:
07 2021
07 2021
Historique:
received:
19
09
2018
accepted:
14
07
2020
revised:
06
07
2020
pubmed:
28
7
2020
medline:
27
1
2022
entrez:
26
7
2020
Statut:
ppublish
Résumé
Hippocampal neurogenesis has been shown to play roles in learning, memory, and stress responses. These diverse roles may be related to a functional segregation of the hippocampus along its longitudinal axis. Indeed, the dorsal hippocampus (dHi) plays a predominant role in spatial learning and memory, while the ventral hippocampus (vHi) is predominantly involved in the regulation of anxiety, a behaviour impacted by stress. Recent studies suggest that the area between them, the intermediate hippocampus (iHi) may also be functionally independent. In parallel, it has been reported that chronic stress reduces neurogenesis preferentially in the vHi rather the dHi. We thus aimed to determine whether such stress-induced changes in neurogenesis could be related to differential intrinsic sensitivity of neural progenitor cells (NPCs) from the dHi, iHi, or vHi to the stress hormone, corticosterone, or the glucocorticoid receptor (GR) agonist, dexamethasone. Long-term exposure of rat NPCs to corticosterone or dexamethasone decreased neuronal differentiation in the vHi but not the dHi, while iHi cultures showed an intermediate response. A similar gradient-like response on neuronal differentiation and maturation was observed with dexamethasone treatment. This gradient-like effect was also observed on GR nuclear translocation in response to corticosterone or dexamethasone. Long-term exposure to corticosterone or dexamethasone treatment also tended to induce a greater downregulation of GR-associated genes in vHi-derived neurons compared to those from the dHi and iHi. These data suggest that increased intrinsic sensitivity of vHi NPC-derived neurons to chronic glucocorticoid exposure may underlie the increased vulnerability of the vHi to chronic stress-induced reductions in neurogenesis.
Identifiants
pubmed: 32709996
doi: 10.1038/s41380-020-0848-8
pii: 10.1038/s41380-020-0848-8
doi:
Substances chimiques
Glucocorticoids
0
Receptors, Glucocorticoid
0
Corticosterone
W980KJ009P
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
3240-3252Informations de copyright
© 2020. The Author(s), under exclusive licence to Springer Nature Limited.
Références
Kempermann G, Wiskott L, Gage FH. Functional significance of adult neurogenesis. Curr Opin Neurobiol. 2004;14:186–91.
pubmed: 15082323
doi: 10.1016/j.conb.2004.03.001
Ming GL, Song H. Adult neurogenesis in the mammalian brain: significant answers and significant questions. Neuron. 2011;70:687–702.
pubmed: 21609825
pmcid: 3106107
doi: 10.1016/j.neuron.2011.05.001
Christie BR, Cameron HA. Neurogenesis in the adult hippocampus. Hippocampus. 2006;16:199–207.
pubmed: 16411231
doi: 10.1002/hipo.20151
Kempermann G, Kuhn HG, Gage FH. More hippocampal neurons in adult mice living in an enriched environment. Nature. 1997;386:493–5.
pubmed: 9087407
doi: 10.1038/386493a0
Malberg JE, Eisch AJ, Nestler EJ, Duman RS. Chronic antidepressant treatment increases neurogenesis in adult rat hippocampus. J Neurosci. 2000;20:9104–10.
pubmed: 11124987
pmcid: 6773038
doi: 10.1523/JNEUROSCI.20-24-09104.2000
Schloesser RJ, Lehmann M, Martinowich K, Manji HK, Herkenham M. Environmental enrichment requires adult neurogenesis to facilitate the recovery from psychosocial stress. Mol Psychiatry. 2010;15:1152–63.
pubmed: 20308988
pmcid: 2990187
doi: 10.1038/mp.2010.34
Simon M, Czeh B, Fuchs E. Age-dependent susceptibility of adult hippocampal cell proliferation to chronic psychosocial stress. Brain Res. 2005;1049:244–8.
pubmed: 15950198
doi: 10.1016/j.brainres.2005.05.006
Surget A, Tanti A, Leonardo ED, Laugeray A, Rainer Q, Touma C, et al. Antidepressants recruit new neurons to improve stress response regulation. Mol Psychiatry. 2011;16:1177–88.
pubmed: 21537331
pmcid: 3223314
doi: 10.1038/mp.2011.48
Vivar C, van Praag H. Running changes the brain: the long and the short of it. Physiology. 2017;32:410–24.
pubmed: 29021361
pmcid: 6148340
doi: 10.1152/physiol.00017.2017
Dranovsky A, Hen R. Hippocampal neurogenesis: regulation by stress and antidepressants. Biol Psychiatry. 2006;59:1136–43.
pubmed: 16797263
pmcid: 7537828
doi: 10.1016/j.biopsych.2006.03.082
Jayatissa MN, Bisgaard C, Tingstrom A, Papp M, Wiborg O. Hippocampal cytogenesis correlates to escitalopram-mediated recovery in a chronic mild stress rat model of depression. Neuropsychopharmacology. 2006;31:2395–404.
pubmed: 16482085
doi: 10.1038/sj.npp.1301041
Jayatissa MN, Henningsen K, West MJ, Wiborg O. Decreased cell proliferation in the dentate gyrus does not associate with development of anhedonic-like symptoms in rats. Brain Res. 2009;1290:133–41.
pubmed: 19595674
doi: 10.1016/j.brainres.2009.07.001
Lehmann ML, Brachman RA, Martinowich K, Schloesser RJ, Herkenham M. Glucocorticoids orchestrate divergent effects on mood through adult neurogenesis. J Neurosci. 2013;33:2961–72.
pubmed: 23407954
pmcid: 3711562
doi: 10.1523/JNEUROSCI.3878-12.2013
Mitra R, Sundlass K, Parker KJ, Schatzberg AF, Lyons DM. Social stress-related behavior affects hippocampal cell proliferation in mice. Physiol Behav. 2006;89:123–7.
pubmed: 16837015
doi: 10.1016/j.physbeh.2006.05.047
Schoenfeld TJ, Gould EStress. stress hormones, and adult neurogenesis. Exp Neurol. 2012;233:12–21.
pubmed: 21281629
doi: 10.1016/j.expneurol.2011.01.008
David DJ, Samuels BA, Rainer Q, Wang JW, Marsteller D, Mendez I, et al. Neurogenesis-dependent and -independent effects of fluoxetine in an animal model of anxiety/depression. Neuron. 2009;62:479–93.
pubmed: 19477151
pmcid: 2759281
doi: 10.1016/j.neuron.2009.04.017
Brummelte S, Galea LA. Chronic high corticosterone reduces neurogenesis in the dentate gyrus of adult male and female rats. Neuroscience. 2010;168:680–90.
pubmed: 20406669
doi: 10.1016/j.neuroscience.2010.04.023
Ekstrand J, Hellsten J, Wennstrom M, Tingstrom A. Differential inhibition of neurogenesis and angiogenesis by corticosterone in rats stimulated with electroconvulsive seizures. Prog Neuropsychopharmacol Biol Psychiatry. 2008;32:1466–72.
pubmed: 18583010
doi: 10.1016/j.pnpbp.2008.05.012
Culig L, Surget A, Bourdey M, Khemissi W, Le Guisquet AM, Vogel E, et al. Increasing adult hippocampal neurogenesis in mice after exposure to unpredictable chronic mild stress may counteract some of the effects of stress. Neuropharmacology. 2017;126:179–89.
pubmed: 28890366
doi: 10.1016/j.neuropharm.2017.09.009
Snyder JS, Soumier A, Brewer M, Pickel J, Cameron HA. Adult hippocampal neurogenesis buffers stress responses and depressive behaviour. Nature. 2011;476:458–61.
pubmed: 21814201
pmcid: 3162077
doi: 10.1038/nature10287
Bannerman DM, Rawlins JN, McHugh SB, Deacon RM, Yee BK, Bast T, et al. Regional dissociations within the hippocampus–memory and anxiety. Neurosci Biobehav Rev. 2004;28:273–83.
pubmed: 15225971
doi: 10.1016/j.neubiorev.2004.03.004
Fanselow MS, Dong HW. Are the dorsal and ventral hippocampus functionally distinct structures? Neuron. 2010;65:7–19.
pubmed: 20152109
pmcid: 2822727
doi: 10.1016/j.neuron.2009.11.031
Levone BR, Cryan JF, O’Leary OF. Role of adult hippocampal neurogenesis in stress resilience. Neurobiol Stress. 2015;1:147–55.
pubmed: 27589664
doi: 10.1016/j.ynstr.2014.11.003
O’Leary OF, Cryan JF. A ventral view on antidepressant action: roles for adult hippocampal neurogenesis along the dorsoventral axis. Trends Pharm Sci. 2014;35:675–87.
pubmed: 25455365
doi: 10.1016/j.tips.2014.09.011
Tanti A, Belzung C. Neurogenesis along the septo-temporal axis of the hippocampus: are depression and the action of antidepressants region-specific? Neuroscience. 2013;252:234–52.
pubmed: 23973415
doi: 10.1016/j.neuroscience.2013.08.017
Winocur G, Wojtowicz JM, Sekeres M, Snyder JS, Wang S. Inhibition of neurogenesis interferes with hippocampus-dependent memory function. Hippocampus. 2006;16:296–304.
pubmed: 16411241
doi: 10.1002/hipo.20163
Wu MV, Hen R. Functional dissociation of adult-born neurons along the dorsoventral axis of the dentate gyrus. Hippocampus. 2014;24:751–61.
pubmed: 24550158
pmcid: 4222246
doi: 10.1002/hipo.22265
Ambrogini P, Cuppini R, Cuppini C, Ciaroni S, Cecchini T, Ferri P, et al. Spatial learning affects immature granule cell survival in adult rat dentate gyrus. Neurosci Lett. 2000;286:21–4.
pubmed: 10822143
doi: 10.1016/S0304-3940(00)01074-0
Dalla C, Papachristos EB, Whetstone AS, Shors TJ. Female rats learn trace memories better than male rats and consequently retain a greater proportion of new neurons in their hippocampi. Proc Natl Acad Sci USA. 2009;106:2927–32.
pubmed: 19188598
pmcid: 2650367
doi: 10.1073/pnas.0809650106
O’Leary OF, O’Connor RM, Cryan JF. Lithium-induced effects on adult hippocampal neurogenesis are topographically segregated along the dorso-ventral axis of stressed mice. Neuropharmacology. 2012;62:247–55.
pubmed: 21803056
doi: 10.1016/j.neuropharm.2011.07.015
Tanti A, Rainer Q, Minier F, Surget A, Belzung C. Differential environmental regulation of neurogenesis along the septo-temporal axis of the hippocampus. Neuropharmacology. 2012;63:374–84.
pubmed: 22561281
doi: 10.1016/j.neuropharm.2012.04.022
Hawley DF, Leasure JL. Region-specific response of the hippocampus to chronic unpredictable stress. Hippocampus. 2012;22:1338–49.
pubmed: 21805528
doi: 10.1002/hipo.20970
Perera TD, Dwork AJ, Keegan KA, Thirumangalakudi L, Lipira CM, Joyce N, et al. Necessity of hippocampal neurogenesis for the therapeutic action of antidepressants in adult nonhuman primates. PLoS ONE. 2011;6:e17600.
pubmed: 21525974
pmcid: 3078107
doi: 10.1371/journal.pone.0017600
Bast T. Toward an integrative perspective on hippocampal function: from the rapid encoding of experience to adaptive behavior. Rev Neurosci. 2007;18:253–81.
pubmed: 18019609
doi: 10.1515/REVNEURO.2007.18.3-4.253
Bast T, Wilson IA, Witter MP, Morris RG. From rapid place learning to behavioral performance: a key role for the intermediate hippocampus. PLoS Biol. 2009;7:e1000089.
pubmed: 19385719
pmcid: 2671558
doi: 10.1371/journal.pbio.1000089
Strange BA, Witter MP, Lein ES, Moser EI. Functional organization of the hippocampal longitudinal axis. Nat Rev Neurosci. 2014;15:655–69.
pubmed: 25234264
doi: 10.1038/nrn3785
Thompson CL, Pathak SD, Jeromin A, Ng LL, MacPherson CR, Mortrud MT, et al. Genomic anatomy of the hippocampus. Neuron. 2008;60:1010–21.
pubmed: 19109908
doi: 10.1016/j.neuron.2008.12.008
Cembrowski MS, Wang L, Sugino K, Shields BC, Spruston N. Hipposeq: a comprehensive RNA-seq database of gene expression in hippocampal principal neurons. Elife. 2016;5:e14997.
pubmed: 27113915
pmcid: 4846374
doi: 10.7554/eLife.14997
Ge R, Torres I, Brown JJ, Gregory E, McLellan E, Downar JH, et al. Functional disconnectivity of the hippocampal network and neural correlates of memory impairment in treatment-resistant depression. J Affect Disord. 2019;253:248–56.
pubmed: 31060011
doi: 10.1016/j.jad.2019.04.096
Zhou QG, Lee D, Ro EJ, Suh H. Regional-specific effect of fluoxetine on rapidly dividing progenitors along the dorsoventral axis of the hippocampus. Sci Rep. 2016;6:35572.
pubmed: 27759049
pmcid: 5069667
doi: 10.1038/srep35572
Faul F, Erdfelder E, Lang AG, Buchner A. G*Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav Res Methods. 2007;39:175–91.
pubmed: 17695343
doi: 10.3758/BF03193146
Anacker C, Zunszain PA, Cattaneo A, Carvalho LA, Garabedian MJ, Thuret S, et al. Antidepressants increase human hippocampal neurogenesis by activating the glucocorticoid receptor. Mol Psychiatry. 2011;16:738–50.
pubmed: 21483429
pmcid: 3121947
doi: 10.1038/mp.2011.26
Saaltink DJ, Vreugdenhil E. Stress, glucocorticoid receptors, and adult neurogenesis: a balance between excitation and inhibition? Cell Mol Life Sci. 2014;71:2499–515.
pubmed: 24522255
pmcid: 4055840
doi: 10.1007/s00018-014-1568-5
Falconer EM, Galea LA. Sex differences in cell proliferation, cell death and defensive behavior following acute predator odor stress in adult rats. Brain Res. 2003;975:22–36.
pubmed: 12763590
doi: 10.1016/S0006-8993(03)02542-3
Heine VM, Maslam S, Zareno J, Joels M, Lucassen PJ. Suppressed proliferation and apoptotic changes in the rat dentate gyrus after acute and chronic stress are reversible. Eur J Neurosci. 2004;19:131–44.
pubmed: 14750971
doi: 10.1046/j.1460-9568.2003.03100.x
Anacker C, Cattaneo A, Luoni A, Musaelyan K, Zunszain PA, Milanesi E, et al. Glucocorticoid-related molecular signaling pathways regulating hippocampal neurogenesis. Neuropsychopharmacology. 2013;38:872–83.
pubmed: 23303060
pmcid: 3672002
doi: 10.1038/npp.2012.253
Boku S, Nakagawa S, Masuda T, Nishikawa H, Kato A, Kitaichi Y, et al. Glucocorticoids and lithium reciprocally regulate the proliferation of adult dentate gyrus-derived neural precursor cells through GSK-3beta and beta-catenin/TCF pathway. Neuropsychopharmacology. 2009;34:805–15.
pubmed: 19005466
doi: 10.1038/npp.2008.198
Kim SJ, Lee KJ, Shin YC, Choi SH, Do E, Kim S, et al. Stress-induced decrease of granule cell proliferation in adult rat hippocampus: assessment of granule cell proliferation using high doses of bromodeoxyuridine before and after restraint stress. Mol Cells. 2005;19:74–80.
pubmed: 15750343
Hawley DF, Morch K, Christie BR, Leasure JL. Differential response of hippocampal subregions to stress and learning. PLoS ONE. 2012;7:e53126.
pubmed: 23285257
pmcid: 3532167
doi: 10.1371/journal.pone.0053126
Morley-Fletcher S, Mairesse J, Soumier A, Banasr M, Fagioli F, Gabriel C, et al. Chronic agomelatine treatment corrects behavioral, cellular, and biochemical abnormalities induced by prenatal stress in rats. Psychopharmacology. 2011;217:301–13.
pubmed: 21503609
doi: 10.1007/s00213-011-2280-x
Zuena AR, Mairesse J, Casolini P, Cinque C, Alema GS, Morley-Fletcher S, et al. Prenatal restraint stress generates two distinct behavioral and neurochemical profiles in male and female rats. PLoS ONE. 2008;3:e2170.
pubmed: 18478112
pmcid: 2366064
doi: 10.1371/journal.pone.0002170
Pinto V, Costa JC, Morgado P, Mota C, Miranda A, Bravo FV, et al. Differential impact of chronic stress along the hippocampal dorsal-ventral axis. Brain Struct Funct. 2015;220:1205–12.
pubmed: 24500370
doi: 10.1007/s00429-014-0713-0
Garcia A, Steiner B, Kronenberg G, Bick-Sander A, Kempermann G. Age-dependent expression of glucocorticoid- and mineralocorticoid receptors on neural precursor cell populations in the adult murine hippocampus. Aging Cell. 2004;3:363–71.
pubmed: 15569353
doi: 10.1111/j.1474-9728.2004.00130.x
Wong EY, Herbert J. Roles of mineralocorticoid and glucocorticoid receptors in the regulation of progenitor proliferation in the adult hippocampus. Eur J Neurosci. 2005;22:785–92.
pubmed: 16115202
pmcid: 1592225
doi: 10.1111/j.1460-9568.2005.04277.x
Egeland M, Zunszain PA, Pariante CM. Molecular mechanisms in the regulation of adult neurogenesis during stress. Nat Rev Neurosci. 2015;16:189–200.
pubmed: 25790864
doi: 10.1038/nrn3855
Zhang TY, Keown CL, Wen X, Li J, Vousden DA, Anacker C, et al. Environmental enrichment increases transcriptional and epigenetic differentiation between mouse dorsal and ventral dentate gyrus. Nat Commun. 2018;9:298.
pubmed: 29352183
pmcid: 5775256
doi: 10.1038/s41467-017-02748-x
Piatti VC, Davies-Sala MG, Esposito MS, Mongiat LA, Trinchero MF, Schinder AF. The timing for neuronal maturation in the adult hippocampus is modulated by local network activity. J Neurosci. 2011;31:7715–28.
pubmed: 21613484
pmcid: 3701257
doi: 10.1523/JNEUROSCI.1380-11.2011
Snyder JS, Ferrante SC, Cameron HA. Late maturation of adult-born neurons in the temporal dentate gyrus. PLoS ONE. 2012;7:e48757.
pubmed: 23144957
pmcid: 3492442
doi: 10.1371/journal.pone.0048757
Li G, Fang L, Fernandez G, Pleasure SJ. The ventral hippocampus is the embryonic origin for adult neural stem cells in the dentate gyrus. Neuron. 2013;78:658–72.
pubmed: 23643936
pmcid: 3669230
doi: 10.1016/j.neuron.2013.03.019
Anacker C, Cattaneo A, Musaelyan K, Zunszain PA, Horowitz M, Molteni R, et al. Role for the kinase SGK1 in stress, depression, and glucocorticoid effects on hippocampal neurogenesis. Proc Natl Acad Sci USA. 2013;110:8708–13.
pubmed: 23650397
pmcid: 3666742
doi: 10.1073/pnas.1300886110
Banerjee SB, Rajendran R, Dias BG, Ladiwala U, Tole S, Vaidya VA. Recruitment of the Sonic hedgehog signalling cascade in electroconvulsive seizure-mediated regulation of adult rat hippocampal neurogenesis. Eur J Neurosci. 2005;22:1570–80.
pubmed: 16197497
pmcid: 4820647
doi: 10.1111/j.1460-9568.2005.04317.x
Han YG, Spassky N, Romaguera-Ros M, Garcia-Verdugo JM, Aguilar A, Schneider-Maunoury S, et al. Hedgehog signaling and primary cilia are required for the formation of adult neural stem cells. Nat Neurosci. 2008;11:277–84.
pubmed: 18297065
doi: 10.1038/nn2059
Cembrowski MS, Bachman JL, Wang L, Sugino K, Shields BC, Spruston N. Spatial gene-expression gradients underlie prominent heterogeneity of CA1 pyramidal neurons. Neuron. 2016;89:351–68.
pubmed: 26777276
doi: 10.1016/j.neuron.2015.12.013
Bienkowski MS, Bowman I, Song MY, Gou L, Ard T, Cotter K, et al. Integration of gene expression and brain-wide connectivity reveals the multiscale organization of mouse hippocampal networks. Nat Neurosci. 2018;21:1628–43.
pubmed: 30297807
pmcid: 6398347
doi: 10.1038/s41593-018-0241-y
Vogel JW, La Joie R, Grothe MJ, Diaz-Papkovich A, Doyle A, Vachon-Presseau E, et al. A molecular gradient along the longitudinal axis of the human hippocampus informs large-scale behavioral systems. Nat Commun. 2020;11:960.
pubmed: 32075960
pmcid: 7031290
doi: 10.1038/s41467-020-14518-3