Astrogenesis in the murine dentate gyrus is a life-long and dynamic process.


Journal

The EMBO journal
ISSN: 1460-2075
Titre abrégé: EMBO J
Pays: England
ID NLM: 8208664

Informations de publication

Date de publication:
01 06 2022
Historique:
revised: 25 03 2022
received: 10 12 2021
accepted: 30 03 2022
pubmed: 23 4 2022
medline: 3 6 2022
entrez: 22 4 2022
Statut: ppublish

Résumé

Astrocytes are highly abundant in the mammalian brain, and their functions are of vital importance for all aspects of development, adaption, and aging of the central nervous system (CNS). Mounting evidence indicates the important contributions of astrocytes to a wide range of neuropathies. Still, our understanding of astrocyte development significantly lags behind that of other CNS cells. We here combine immunohistochemical approaches with genetic fate-mapping, behavioural paradigms, single-cell transcriptomics, and in vivo two-photon imaging, to comprehensively assess the generation and the proliferation of astrocytes in the dentate gyrus (DG) across the life span of a mouse. Astrogenesis in the DG is initiated by radial glia-like neural stem cells giving rise to locally dividing astrocytes that enlarge the astrocyte compartment in an outside-in-pattern. Also in the adult DG, the vast majority of astrogenesis is mediated through the proliferation of local astrocytes. Interestingly, locally dividing astrocytes were able to adapt their proliferation to environmental and behavioral stimuli revealing an unexpected plasticity. Our study establishes astrocytes as enduring plastic elements in DG circuits, implicating a vital contribution of astrocyte dynamics to hippocampal plasticity.

Identifiants

pubmed: 35451150
doi: 10.15252/embj.2021110409
pmc: PMC9156974
doi:

Banques de données

GEO
['GSE190399']

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

e110409

Informations de copyright

© 2022 The Authors. Published under the terms of the CC BY NC ND 4.0 license.

Références

Front Cell Neurosci. 2014 Nov 21;8:393
pubmed: 25484855
PLoS One. 2013 Dec 20;8(12):e83797
pubmed: 24376750
Sci Rep. 2019 Dec 3;9(1):18194
pubmed: 31796832
Development. 2011 Feb;138(4):745-53
pubmed: 21266410
Eur J Neurosci. 2002 Jul;16(1):129-36
pubmed: 12153537
Brain Plast. 2017 Nov 9;3(1):73-87
pubmed: 29765861
Nat Protoc. 2011 Nov 17;6(12):1981-9
pubmed: 22094733
Cell Stem Cell. 2015 Oct 1;17(4):385-95
pubmed: 26431181
Cold Spring Harb Perspect Biol. 2015 Oct 01;7(10):a018879
pubmed: 26430216
Stem Cell Reports. 2020 Oct 13;15(4):883-897
pubmed: 32976762
Exp Neurol Suppl. 1965 Oct;:Suppl 2:1-70
pubmed: 5838955
Front Neuroanat. 2015 May 07;9:53
pubmed: 25999820
Physiol Rev. 2018 Jan 1;98(1):239-389
pubmed: 29351512
J Neurosci. 2000 Aug 15;20(16):6095-105
pubmed: 10934259
Cell Stem Cell. 2011 May 6;8(5):566-79
pubmed: 21549330
Neurobiol Aging. 2004 Mar;25(3):361-75
pubmed: 15123342
Nat Neurosci. 1999 Mar;2(3):266-70
pubmed: 10195220
EMBO J. 2021 Nov 2;40(21):e107532
pubmed: 34549820
Cell Stem Cell. 2019 Jun 6;24(6):974-982.e3
pubmed: 31130513
Neurobiol Aging. 2011 Oct;32(10):1906-14
pubmed: 20006411
Nature. 2008 May 15;453(7193):345-51
pubmed: 18480816
Neurobiol Aging. 2010 Jan;31(1):151-61
pubmed: 18455269
Nat Commun. 2020 Mar 5;11(1):1220
pubmed: 32139688
Neuron. 2007 May 3;54(3):357-69
pubmed: 17481390
Neuron. 2022 Feb 2;110(3):452-469.e14
pubmed: 34798047
J Vis Exp. 2019 Jun 19;(148):
pubmed: 31282875
Front Cell Neurosci. 2014 Nov 27;8:396
pubmed: 25505873
Neuromolecular Med. 2008;10(2):128-40
pubmed: 18286389
Stem Cells. 2014 Jul;32(7):1968-82
pubmed: 24604711
Neuron. 2008 Nov 6;60(3):430-40
pubmed: 18995817
Neurobiol Dis. 2016 Jan;85:254-261
pubmed: 25843667
Glia. 2019 Nov;67(11):2153-2165
pubmed: 31038810
Nature. 2010 Nov 11;468(7321):232-43
pubmed: 21068832
Nature. 2002 May 2;417(6884):39-44
pubmed: 11986659
Methods Mol Biol. 2020;2150:183-194
pubmed: 31020634
Behav Brain Res. 2012 Feb 14;227(2):497-507
pubmed: 22024433
J Comp Neurol. 1974 Nov 1;158(1):55-79
pubmed: 4430737
J Comp Neurol. 2007 Apr 1;501(4):659-67
pubmed: 17278139
Neurobiol Aging. 2004 Mar;25(3):333-40
pubmed: 15123339
J Neurosci. 2007 Nov 14;27(46):12623-9
pubmed: 18003841
J Neurosci. 2015 Jul 1;35(26):9764-81
pubmed: 26134658
Cell Stem Cell. 2018 Apr 5;22(4):589-599.e5
pubmed: 29625071
Glia. 2005 Aug 15;51(3):173-86
pubmed: 15800930
Cold Spring Harb Perspect Biol. 2017 Jan 3;9(1):
pubmed: 27836834
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Cell Stem Cell. 2021 May 6;28(5):863-876.e6
pubmed: 33581058
J Comp Neurol. 2003 Jun 9;460(4):563-72
pubmed: 12717714
Front Neurosci. 2016 Mar 07;10:78
pubmed: 27013941
Exp Brain Res. 1986;62(3):541-8
pubmed: 3720883
Proc Natl Acad Sci U S A. 1999 Nov 9;96(23):13427-31
pubmed: 10557337
Cell. 2011 Mar 4;144(5):810-23
pubmed: 21376239
Front Neuroanat. 2018 Oct 23;12:83
pubmed: 30405363
Neurobiol Dis. 2004 Jun;16(1):1-13
pubmed: 15207256
Cell. 2019 Apr 18;177(3):654-668.e15
pubmed: 30929900
Development. 2012 Jul;139(14):2477-87
pubmed: 22675209
Glia. 2010 Oct;58(13):1553-69
pubmed: 20549747
Cell Stem Cell. 2007 Nov;1(5):515-28
pubmed: 18371391
Brain Struct Funct. 2015 Jan;220(1):361-83
pubmed: 24178679
Neuron. 2011 May 26;70(4):687-702
pubmed: 21609825
J Comp Neurol. 1975 Jan 15;159(2):149-75
pubmed: 1112911
Methods Mol Biol. 2019;1938:19-33
pubmed: 30617970
Nat Biotechnol. 2018 Jun;36(5):411-420
pubmed: 29608179
J Comp Neurol. 1980 Mar 1;190(1):87-114
pubmed: 7381056
J Neurosci. 1996 Mar 15;16(6):2027-33
pubmed: 8604047
J Neurosci Res. 2002 Nov 1;70(3):327-34
pubmed: 12391592
Neuroreport. 2000 Jun 26;11(9):1991-6
pubmed: 10884058
Cell Rep. 2018 Jan 2;22(1):269-285
pubmed: 29298427
Circ Res. 2006 Jun 23;98(12):1547-54
pubmed: 16709902
Science. 2007 Aug 24;317(5841):1083-6
pubmed: 17717185
J Vis Exp. 2017 Dec 16;(130):
pubmed: 29286427
Development. 2011 Mar;138(6):1057-68
pubmed: 21343361
Brain Sci. 2020 Nov 26;10(12):
pubmed: 33255945
Stem Cell Reports. 2014 Feb 06;2(2):153-62
pubmed: 24527389
Neurobiol Aging. 2021 Apr;100:59-71
pubmed: 33493951
Cereb Cortex. 2018 Jul 1;28(7):2458-2478
pubmed: 29722804
EMBO J. 2022 Jun 1;41(11):e110409
pubmed: 35451150
Proc Natl Acad Sci U S A. 2016 Sep 6;113(36):10186-91
pubmed: 27559087
Cell. 2013 Jun 6;153(6):1219-1227
pubmed: 23746839
Cold Spring Harb Perspect Biol. 2015 Sep 01;7(9):a018812
pubmed: 26330519
Brain Res Brain Res Protoc. 2004 Nov;14(1):45-57
pubmed: 15519951
Cell. 2011 Jun 24;145(7):1142-55
pubmed: 21664664
Glia. 2013 Aug;61(8):1347-63
pubmed: 23828756
Brain Behav Immun. 2012 Mar;26(3):500-10
pubmed: 22281279
Nat Protoc. 2019 Mar;14(3):703-721
pubmed: 30804569
Nat Med. 2019 Apr;25(4):554-560
pubmed: 30911133
Neuron. 2012 Sep 20;75(6):1035-50
pubmed: 22998872
Nat Biotechnol. 2016 Jul 12;34(7):703-6
pubmed: 27404877
Nat Methods. 2017 Sep 29;14(10):935-936
pubmed: 28960196
BMC Dev Biol. 2001;1:4
pubmed: 11299042
Cell Rep. 2021 Mar 16;34(11):108853
pubmed: 33730566
Nature. 2018 Mar 15;555(7696):377-381
pubmed: 29513649
J Neurosci. 1998 May 1;18(9):3206-12
pubmed: 9547229
J Neurosci. 1997 Jun 1;17(11):4112-20
pubmed: 9151728
Proc Natl Acad Sci U S A. 1958 May;44(5):476-83
pubmed: 16590224
Cell. 2019 Jun 13;177(7):1888-1902.e21
pubmed: 31178118
Front Cell Neurosci. 2020 Mar 18;14:57
pubmed: 32256319
Science. 2018 Feb 9;359(6376):658-662
pubmed: 29439238
Aging Cell. 2004 Dec;3(6):363-71
pubmed: 15569353
Glia. 2001 Jan;33(1):72-86
pubmed: 11169793
Neuron. 2014 Feb 19;81(4):728-39
pubmed: 24559669
J Comp Neurol. 2010 Nov 15;518(22):4479-90
pubmed: 20886617
Proc Natl Acad Sci U S A. 2009 Aug 18;106(33):14108-13
pubmed: 19666520
J Neurosci. 2001 Sep 15;21(18):7153-60
pubmed: 11549726
J Neurosci. 2014 Oct 15;34(42):13948-53
pubmed: 25319691
Proc Natl Acad Sci U S A. 1997 Sep 16;94(19):10409-14
pubmed: 9294224
Nature. 2005 Oct 27;437(7063):1370-5
pubmed: 16251967
Nature. 2010 Nov 11;468(7321):223-31
pubmed: 21068831
Nat Neurosci. 2021 Feb;24(2):225-233
pubmed: 33349709
Stem Cell Res. 2015 Nov;15(3):514-521
pubmed: 26448270
Neuron. 2004 Mar 4;41(5):683-6
pubmed: 15003168
Dev Neurobiol. 2012 Jul;72(7):1032-43
pubmed: 22354697
Neuron. 2015 Dec 2;88(5):957-972
pubmed: 26606999
Genome Biol. 2015 Dec 10;16:278
pubmed: 26653891
J Neurosci. 2005 Sep 21;25(38):8680-5
pubmed: 16177036
Nat Commun. 2019 Oct 25;10(1):4884
pubmed: 31653848
Cell Stem Cell. 2010 Jul 2;7(1):78-89
pubmed: 20621052
Nature. 2012 Mar 28;484(7394):376-80
pubmed: 22456708
Methods Mol Biol. 2013;1052:1-11
pubmed: 23640252
J Comp Neurol. 1987 Oct 22;264(4):449-79
pubmed: 3680638
Front Neurosci. 2014 Jun 12;8:145
pubmed: 24971048
Sci Rep. 2018 Apr 25;8(1):6521
pubmed: 29695820
Glia. 2014 Sep;62(9):1377-91
pubmed: 24807023
Mol Cell Neurosci. 2005 Nov;30(3):291-303
pubmed: 16169246

Auteurs

Julia Schneider (J)

Institute of Biochemistry, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Johannes Weigel (J)

Institute of Biochemistry, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Marie-Theres Wittmann (MT)

Institute of Biochemistry, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.
Institute of Human Genetics, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Pavel Svehla (P)

Institute of Clinical Neuroimmunology, Klinikum der Universität München, Ludwig-Maximilians University Munich, Munich, Germany.
Graduate School of Systemic Neurosciences, Ludwig-Maximilians University Munich, Munich, Germany.
Medical Faculty, BioMedical Center, Ludwig-Maximilians University Munich, Munich, Germany.

Sebastian Ehrt (S)

Institute of Clinical Neuroimmunology, Klinikum der Universität München, Ludwig-Maximilians University Munich, Munich, Germany.
Medical Faculty, BioMedical Center, Ludwig-Maximilians University Munich, Munich, Germany.

Fang Zheng (F)

Institute of Physiology and Pathophysiology, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Tarek Elmzzahi (T)

Institute of Biochemistry, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.
Department of Molecular Immunology in Neurodegeneration, German Centre for Neurodegenerative Diseases Bonn, Bonn, Germany.

Julian Karpf (J)

Institute of Biochemistry, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Lucía Paniagua-Herranz (L)

Department of Molecular Biology, Universidad Complutense de Madrid, Madrid, Spain.
Instituto Universitario de Investigación en Neuroquímica (IUIN), Madrid, Spain.
Instituto de Investigación Sanitaria San Carlos (IdISSC), Spain.

Onur Basak (O)

Department of Translational Neuroscience, University Medical Centre Utrecht (UMCU), Utrecht, Netherlands.

Arif Ekici (A)

Institute of Human Genetics, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Andre Reis (A)

Institute of Human Genetics, University Hospital Erlangen, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Christian Alzheimer (C)

Institute of Physiology and Pathophysiology, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Felipe Ortega de la O (F)

Department of Molecular Biology, Universidad Complutense de Madrid, Madrid, Spain.
Instituto Universitario de Investigación en Neuroquímica (IUIN), Madrid, Spain.
Instituto de Investigación Sanitaria San Carlos (IdISSC), Spain.

Sabine Liebscher (S)

Institute of Clinical Neuroimmunology, Klinikum der Universität München, Ludwig-Maximilians University Munich, Munich, Germany.
Graduate School of Systemic Neurosciences, Ludwig-Maximilians University Munich, Munich, Germany.
Medical Faculty, BioMedical Center, Ludwig-Maximilians University Munich, Munich, Germany.
Munich Cluster for Systems Neurology (SyNergy), Munich, Germany.

Ruth Beckervordersandforth (R)

Institute of Biochemistry, Friedrich-Alexander-Universität Erlangen-Nürnberg, Erlangen, Germany.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH