Olig2 defines a subset of neural stem cells that produce specific olfactory bulb interneuron subtypes in the subventricular zone of adult mice.


Journal

Development (Cambridge, England)
ISSN: 1477-9129
Titre abrégé: Development
Pays: England
ID NLM: 8701744

Informations de publication

Date de publication:
01 03 2022
Historique:
received: 21 07 2021
accepted: 24 01 2022
pubmed: 9 2 2022
medline: 9 3 2022
entrez: 8 2 2022
Statut: ppublish

Résumé

Distinct neural stem cells (NSCs) reside in different regions of the subventricular zone (SVZ) and generate multiple olfactory bulb (OB) interneuron subtypes in the adult brain. However, the molecular mechanisms underlying such NSC heterogeneity remain largely unknown. Here, we show that the basic helix-loop-helix transcription factor Olig2 defines a subset of NSCs in the early postnatal and adult SVZ. Olig2-expressing NSCs exist broadly but are most enriched in the ventral SVZ along the dorsoventral axis complementary to dorsally enriched Gsx2-expressing NSCs. Comparisons of Olig2-expressing NSCs from early embryonic to adult stages using single cell transcriptomics reveal stepwise developmental changes in their cell cycle and metabolic properties. Genetic studies further show that cross-repression contributes to the mutually exclusive expression of Olig2 and Gsx2 in NSCs/progenitors during embryogenesis, but that their expression is regulated independently from each other in adult NSCs. Finally, lineage-tracing and conditional inactivation studies demonstrate that Olig2 plays an important role in the specification of OB interneuron subtypes. Altogether, our study demonstrates that Olig2 defines a unique subset of adult NSCs enriched in the ventral aspect of the adult SVZ.

Identifiants

pubmed: 35132995
pii: 274286
doi: 10.1242/dev.200028
pmc: PMC8959153
pii:
doi:

Substances chimiques

Olig2 protein, mouse 0
Oligodendrocyte Transcription Factor 2 0

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, Non-P.H.S.

Langues

eng

Sous-ensembles de citation

IM

Subventions

Organisme : NINDS NIH HHS
ID : R01 NS069893
Pays : United States

Informations de copyright

© 2022. Published by The Company of Biologists Ltd.

Déclaration de conflit d'intérêts

Competing interests The authors declare no competing or financial interests.

Références

Proc Natl Acad Sci U S A. 2004 Mar 2;101(9):3196-201
pubmed: 14963232
J Neurosci. 2011 Mar 2;31(9):3407-22
pubmed: 21368052
J Neurosci. 2008 Apr 9;28(15):3966-75
pubmed: 18400896
Development. 1999 Feb;126(3):525-34
pubmed: 9876181
Neural Dev. 2017 Aug 16;12(1):13
pubmed: 28814342
Wiley Interdiscip Rev Dev Biol. 2020 May;9(3):e369
pubmed: 31825170
J Neurosci. 1995 Aug;15(8):5727-38
pubmed: 7643214
Neural Dev. 2009 Feb 10;4:5
pubmed: 19208224
Development. 1999 Feb;126(3):443-56
pubmed: 9876174
Curr Biol. 2002 Jul 9;12(13):1157-63
pubmed: 12121626
J Neurosci. 2007 Aug 1;27(31):8286-96
pubmed: 17670975
Proc Natl Acad Sci U S A. 2009 Apr 14;106(15):6387-92
pubmed: 19332781
J Comp Neurol. 2013 May 1;521(7):1561-84
pubmed: 23042297
Cell Rep. 2018 Nov 27;25(9):2457-2469.e8
pubmed: 30485812
Nat Neurosci. 2010 Jan;13(1):133-40
pubmed: 20023653
J Comp Neurol. 1999 May 10;407(3):404-14
pubmed: 10320220
J Neurosci. 2007 Jun 27;27(26):6878-91
pubmed: 17596436
Curr Opin Neurobiol. 2016 Aug;39:122-32
pubmed: 27258840
Cell Rep. 2019 Jan 8;26(2):394-406.e5
pubmed: 30625322
Development. 2001 Jan;128(2):193-205
pubmed: 11124115
Nat Cell Biol. 2013 Jun;15(6):602-13
pubmed: 23644466
Glia. 2006 Jul;54(1):21-34
pubmed: 16652340
J Neurosci. 2014 Apr 23;34(17):5788-99
pubmed: 24760839
Cold Spring Harb Perspect Biol. 2016 Jul 01;8(7):
pubmed: 27235475
Cell Rep. 2017 Jan 17;18(3):777-790
pubmed: 28099854
J Neurosci. 2005 Jul 27;25(30):6997-7003
pubmed: 16049175
Development. 2020 Apr 10;147(7):
pubmed: 32122989
Development. 2002 Nov;129(21):5029-40
pubmed: 12397111
J Neurosci. 2006 Jul 26;26(30):7907-18
pubmed: 16870736
Genes Dev. 2013 Jun 1;27(11):1272-87
pubmed: 23723414
Development. 2001 Dec;128(23):4769-80
pubmed: 11731457
Mol Cell Proteomics. 2020 Dec;19(12):2115-2125
pubmed: 32907876
Neuron. 2009 Aug 27;63(4):451-65
pubmed: 19709628
Cold Spring Harb Perspect Biol. 2015 Jul 01;7(9):a020461
pubmed: 26134004
Nat Neurosci. 2014 Feb;17(2):207-14
pubmed: 24362763
J Cell Sci. 2008 Sep 1;121(Pt 17):2783-93
pubmed: 18716282
Nat Biotechnol. 2018 Dec 03;:
pubmed: 30531897
J Neurosci. 2005 Jul 20;25(29):6816-25
pubmed: 16033891
Cell Rep. 2017 Dec 26;21(13):3970-3986
pubmed: 29281841
Dev Biol. 2018 Oct 1;442(1):115-126
pubmed: 29990475
Dev Biol. 2015 Nov 15;407(2):265-74
pubmed: 26387477
Neuron. 2002 Dec 19;36(6):1021-34
pubmed: 12495619
Nat Neurosci. 2012 Jun 24;15(8):1120-6
pubmed: 22729175
J Comp Neurol. 2007 Apr 20;501(6):825-36
pubmed: 17311323
Cold Spring Harb Perspect Biol. 2016 Aug 01;8(8):
pubmed: 27235474
J Neurosci. 2007 Mar 21;27(12):3230-43
pubmed: 17376983
Nat Neurosci. 2004 Feb;7(2):136-44
pubmed: 14703572
BMC Bioinformatics. 2013 Jan 16;14:7
pubmed: 23323831
Development. 2007 May;134(10):1887-99
pubmed: 17428828
J Neurosci. 2007 Jul 18;27(29):7786-98
pubmed: 17634372
Neuron. 2007 Aug 2;55(3):417-33
pubmed: 17678855
Development. 2000 Oct;127(20):4361-71
pubmed: 11003836
J Neurosci. 2003 Jan 1;23(1):167-74
pubmed: 12514213
Dev Biol. 2008 Aug 15;320(2):456-68
pubmed: 18582453
Mol Brain. 2021 Feb 17;14(1):36
pubmed: 33618751
Science. 2017 Jun 30;356(6345):1383-1386
pubmed: 28619719
Nat Neurosci. 2005 Jul;8(7):865-72
pubmed: 15951811
Science. 2007 Jul 20;317(5836):381-4
pubmed: 17615304
J Neurosci. 2008 Jun 18;28(25):6439-52
pubmed: 18562615
Cell. 2015 Jun 18;161(7):1644-55
pubmed: 26091041
J Comp Neurol. 2003 Jun 23;461(2):151-65
pubmed: 12724834
Proc Natl Acad Sci U S A. 2020 Dec 8;117(49):31448-31458
pubmed: 33229571
Elife. 2020 Aug 07;9:
pubmed: 32762844
Elife. 2021 Jul 14;10:
pubmed: 34259628
Nature. 2007 Nov 29;450(7170):717-20
pubmed: 18046410
J Neurosci. 2006 Jan 25;26(4):1275-80
pubmed: 16436615
Development. 2013 Jun;140(11):2289-98
pubmed: 23637331
Neuron. 2014 Sep 3;83(5):1085-97
pubmed: 25189209

Auteurs

Ángela Del Águila (Á)

Division of Developmental Biology, Cincinnati Children's Hospital Research Foundation, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA.

Mike Adam (M)

Division of Developmental Biology, Cincinnati Children's Hospital Research Foundation, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA.

Kristy Ullom (K)

Division of Developmental Biology, Cincinnati Children's Hospital Research Foundation, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA.

Nicholas Shaw (N)

Division of Developmental Biology, Cincinnati Children's Hospital Research Foundation, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA.
Department of Medical Science, University of Cincinnati College of Medicine, 3125 Eden Avenue, Cincinnati, OH 45267-0521, USA.

Shenyue Qin (S)

Division of Developmental Biology, Cincinnati Children's Hospital Research Foundation, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA.

Jacqueline Ehrman (J)

Division of Developmental Biology, Cincinnati Children's Hospital Research Foundation, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA.

Diana Nardini (D)

Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Research Foundation, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA.

Joseph Salomone (J)

Division of Developmental Biology, Cincinnati Children's Hospital Research Foundation, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA.

Brian Gebelein (B)

Division of Developmental Biology, Cincinnati Children's Hospital Research Foundation, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA.

Q Richard Lu (QR)

Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Research Foundation, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA.
Department of Pediatrics, University of Cincinnati College of Medicine, 3125 Eden Avenue, Cincinnati, OH 45267-0521, USA.

Steven S Potter (SS)

Division of Developmental Biology, Cincinnati Children's Hospital Research Foundation, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA.
Department of Pediatrics, University of Cincinnati College of Medicine, 3125 Eden Avenue, Cincinnati, OH 45267-0521, USA.

Ronald Waclaw (R)

Division of Developmental Biology, Cincinnati Children's Hospital Research Foundation, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA.
Division of Experimental Hematology and Cancer Biology, Cincinnati Children's Hospital Research Foundation, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA.
Department of Pediatrics, University of Cincinnati College of Medicine, 3125 Eden Avenue, Cincinnati, OH 45267-0521, USA.

Kenneth Campbell (K)

Division of Developmental Biology, Cincinnati Children's Hospital Research Foundation, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA.
Department of Pediatrics, University of Cincinnati College of Medicine, 3125 Eden Avenue, Cincinnati, OH 45267-0521, USA.
Division of Neurosurgery, Cincinnati Children's Hospital Research Foundation, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA.

Masato Nakafuku (M)

Division of Developmental Biology, Cincinnati Children's Hospital Research Foundation, 3333 Burnet Avenue, Cincinnati, OH 45229-3039, USA.
Department of Pediatrics, University of Cincinnati College of Medicine, 3125 Eden Avenue, Cincinnati, OH 45267-0521, USA.
Department of Neurosurgery, University of Cincinnati College of Medicine, 3125 Eden Avenue, Cincinnati, OH 45267-0521, USA.

Articles similaires

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male
Humans Meals Time Factors Female Adult

Classifications MeSH