Live imaging of neurogenesis in the adult mouse hippocampus

Neural stem and progenitor cells (NSPCs) generate neurons throughout life in the mammalian hippocampus. We used chronic in vivo imaging and followed genetically labeled individual NSPCs and their progeny in the mouse hippocampus for up to 2 months. We show that NSPCs targeted by the endogenous Achae...

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Published in	Science (American Association for the Advancement of Science) Vol. 359; no. 6376; pp. 658 - 662
Main Authors	Pilz, Gregor-Alexander, Bottes, Sara, Betizeau, Marion, Jörg, David J., Carta, Stefano, April, Simon, Simons, Benjamin D., Helmchen, Fritjof, Jessberger, Sebastian
Format	Journal Article
Language	English
Published	United States The American Association for the Advancement of Science 09.02.2018
Subjects	Animals ASCL1 protein Basic Helix-Loop-Helix Transcription Factors - genetics Brain Cell Death Cell Division - genetics Cells (biology) Circuits Dentate gyrus Hippocampus Hippocampus - cytology Hippocampus - growth & development Homology Learning Memory Mice Nerve Net - cytology Nerve Net - growth & development Neural stem cells Neural Stem Cells - cytology Neurogenesis Neurogenesis - genetics Neuroglia - cytology Neuroimaging Neurons Neurons - cytology Progenitor cells Progeny Promoter Regions, Genetic Rodents
Online Access	Get full text
ISSN	0036-8075 1095-9203 1095-9203
DOI	10.1126/science.aao5056

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Abstract	Neural stem and progenitor cells (NSPCs) generate neurons throughout life in the mammalian hippocampus. We used chronic in vivo imaging and followed genetically labeled individual NSPCs and their progeny in the mouse hippocampus for up to 2 months. We show that NSPCs targeted by the endogenous Achaete-scute homolog 1 (Ascl1) promoter undergo limited rounds of symmetric and asymmetric divisions, eliciting a burst of neurogenic activity, after which they are lost. Further, our data reveal unexpected asymmetric divisions of nonradial glia-like NSPCs. Cell fates of Ascl1-labeled lineages suggest a developmental-like program involving a sequential transition from a proliferative to a neurogenic phase. By providing a comprehensive description of lineage relationships, from dividing NSPCs to newborn neurons integrating into the hippocampal circuitry, our data offer insight into how NSPCs support life-long hippocampal neurogenesis.
AbstractList	Neural stem and progenitor cells (NSPCs) generate neurons throughout life in the mammalian hippocampus. We used chronic in vivo imaging and followed genetically labeled individual NSPCs and their progeny in the mouse hippocampus for up to 2 months. We show that NSPCs targeted by the endogenous Achaete-scute homolog 1 (Ascl1) promoter undergo limited rounds of symmetric and asymmetric divisions, eliciting a burst of neurogenic activity, after which they are lost. Further, our data reveal unexpected asymmetric divisions of nonradial glia-like NSPCs. Cell fates of Ascl1-labeled lineages suggest a developmental-like program involving a sequential transition from a proliferative to a neurogenic phase. By providing a comprehensive description of lineage relationships, from dividing NSPCs to newborn neurons integrating into the hippocampal circuitry, our data offer insight into how NSPCs support life-long hippocampal neurogenesis. Neural stem and progenitor cells (NSPCs) generate neurons throughout life in the mammalian hippocampus. We used chronic in vivo imaging and followed genetically labeled individual NSPCs and their progeny in the mouse hippocampus for up to 2 months. We show that NSPCs targeted by the endogenous Achaete-scute homolog 1 (Ascl1) promoter undergo limited rounds of symmetric and asymmetric divisions, eliciting a burst of neurogenic activity, after which they are lost. Further, our data reveal unexpected asymmetric divisions of nonradial glia-like NSPCs. Cell fates of Ascl1-labeled lineages suggest a developmental-like program involving a sequential transition from a proliferative to a neurogenic phase. By providing a comprehensive description of lineage relationships, from dividing NSPCs to newborn neurons integrating into the hippocampal circuitry, our data offer insight into how NSPCs support life-long hippocampal neurogenesis.Neural stem and progenitor cells (NSPCs) generate neurons throughout life in the mammalian hippocampus. We used chronic in vivo imaging and followed genetically labeled individual NSPCs and their progeny in the mouse hippocampus for up to 2 months. We show that NSPCs targeted by the endogenous Achaete-scute homolog 1 (Ascl1) promoter undergo limited rounds of symmetric and asymmetric divisions, eliciting a burst of neurogenic activity, after which they are lost. Further, our data reveal unexpected asymmetric divisions of nonradial glia-like NSPCs. Cell fates of Ascl1-labeled lineages suggest a developmental-like program involving a sequential transition from a proliferative to a neurogenic phase. By providing a comprehensive description of lineage relationships, from dividing NSPCs to newborn neurons integrating into the hippocampal circuitry, our data offer insight into how NSPCs support life-long hippocampal neurogenesis. Neural stem/progenitor cells (NSPCs) generate neurons throughout life in the mammalian hippocampus. We used chronic in vivo imaging and followed genetically labeled individual NSPCs and their progeny in the mouse hippocampus for up to 2 months. We show that NSPCs targeted by the endogenous Achaete-scute homolog 1 (Ascl1)-promoter undergo limited rounds of symmetric and asymmetric divisions, eliciting a burst of neurogenic activity, after which they are lost. Further, our data reveal unexpected asymmetric divisions of non-radial glia-like NSPCs. Cell fates of Ascl1-labeled lineages suggest a sequential transition from a proliferative to a neurogenic phase, reminiscent of a developmental-like program. By providing a comprehensive description of lineage-relationships, from dividing NSPCs to newborn neurons integrating into the hippocampal circuitry, our data provide insight into how NSPCs support life-long hippocampal neurogenesis. A window on hippocampal neurogenesisAddition of new neurons to the adult brain is key to the hippocampal functions of learning and memory. Pilz et al. labeled individual progenitor cells in the mouse hippocampus and watched them in situ for the next 2 months (see the Perspective by Götz). The results revealed the developmental progression as progenitor cells gave rise to mature cells of the dentate gyrus.Science, this issue p. 658; see also p. 639Neural stem and progenitor cells (NSPCs) generate neurons throughout life in the mammalian hippocampus. We used chronic in vivo imaging and followed genetically labeled individual NSPCs and their progeny in the mouse hippocampus for up to 2 months. We show that NSPCs targeted by the endogenous Achaete-scute homolog 1 (Ascl1) promoter undergo limited rounds of symmetric and asymmetric divisions, eliciting a burst of neurogenic activity, after which they are lost. Further, our data reveal unexpected asymmetric divisions of nonradial glia-like NSPCs. Cell fates of Ascl1-labeled lineages suggest a developmental-like program involving a sequential transition from a proliferative to a neurogenic phase. By providing a comprehensive description of lineage relationships, from dividing NSPCs to newborn neurons integrating into the hippocampal circuitry, our data offer insight into how NSPCs support life-long hippocampal neurogenesis.
Author	April, Simon Betizeau, Marion Pilz, Gregor-Alexander Jörg, David J. Carta, Stefano Jessberger, Sebastian Simons, Benjamin D. Bottes, Sara Helmchen, Fritjof
AuthorAffiliation	2 Laboratory of Neural Circuit Dynamics, Faculties of Medicine and Science, Brain Research Institute, University of Zurich, 8057 Zurich, Switzerland 3 Institute of Neuroinformatics, University of Zurich and Swiss Federal Institute of Technology (ETH) Zurich, 8057 Zurich, Switzerland 1 Laboratory of Neural Plasticity, Faculties of Medicine and Science, Brain Research Institute, University of Zurich, 8057 Zurich, Switzerland 4 Cavendish Laboratory, Department of Physics, University of Cambridge, Cambridge CB3 0HE, UK; Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge, Cambridge CB2 1QN, UK; Wellcome Trust-Medical Research Council Cambridge Stem Cell Institute, University of Cambridge, Cambridge CB2 1QR, UK
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Author_xml	– sequence: 1 givenname: Gregor-Alexander orcidid: 0000-0002-6161-4976 surname: Pilz fullname: Pilz, Gregor-Alexander organization: Laboratory of Neural Plasticity, Faculties of Medicine and Science, Brain Research Institute, University of Zurich, 8057 Zurich, Switzerland – sequence: 2 givenname: Sara orcidid: 0000-0003-1801-9247 surname: Bottes fullname: Bottes, Sara organization: Laboratory of Neural Plasticity, Faculties of Medicine and Science, Brain Research Institute, University of Zurich, 8057 Zurich, Switzerland – sequence: 3 givenname: Marion orcidid: 0000-0002-0851-292X surname: Betizeau fullname: Betizeau, Marion organization: Laboratory of Neural Plasticity, Faculties of Medicine and Science, Brain Research Institute, University of Zurich, 8057 Zurich, Switzerland., Institute of Neuroinformatics, University of Zurich and Swiss Federal Institute of Technology (ETH) Zurich, 8057 Zurich, Switzerland – sequence: 4 givenname: David J. orcidid: 0000-0001-5960-0260 surname: Jörg fullname: Jörg, David J. organization: Cavendish Laboratory, Department of Physics, University of Cambridge, Cambridge CB3 0HE, UK., Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge, Cambridge CB2 1QN, UK – sequence: 5 givenname: Stefano orcidid: 0000-0001-7691-7550 surname: Carta fullname: Carta, Stefano organization: Laboratory of Neural Plasticity, Faculties of Medicine and Science, Brain Research Institute, University of Zurich, 8057 Zurich, Switzerland., Laboratory of Neural Circuit Dynamics, Faculties of Medicine and Science, Brain Research Institute, University of Zurich, 8057 Zurich, Switzerland – sequence: 6 givenname: Simon orcidid: 0000-0002-8941-7990 surname: April fullname: April, Simon organization: Laboratory of Neural Plasticity, Faculties of Medicine and Science, Brain Research Institute, University of Zurich, 8057 Zurich, Switzerland – sequence: 7 givenname: Benjamin D. orcidid: 0000-0002-3875-7071 surname: Simons fullname: Simons, Benjamin D. organization: Cavendish Laboratory, Department of Physics, University of Cambridge, Cambridge CB3 0HE, UK., Wellcome Trust/Cancer Research UK Gurdon Institute, University of Cambridge, Cambridge CB2 1QN, UK., Wellcome Trust–Medical Research Council Cambridge Stem Cell Institute, University of Cambridge, Cambridge CB2 1QR, UK – sequence: 8 givenname: Fritjof orcidid: 0000-0002-8867-9569 surname: Helmchen fullname: Helmchen, Fritjof organization: Laboratory of Neural Circuit Dynamics, Faculties of Medicine and Science, Brain Research Institute, University of Zurich, 8057 Zurich, Switzerland – sequence: 9 givenname: Sebastian orcidid: 0000-0002-0056-8275 surname: Jessberger fullname: Jessberger, Sebastian organization: Laboratory of Neural Plasticity, Faculties of Medicine and Science, Brain Research Institute, University of Zurich, 8057 Zurich, Switzerland
BackLink	https://www.ncbi.nlm.nih.gov/pubmed/29439238$$D View this record in MEDLINE/PubMed
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ContentType	Journal Article
Copyright	Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works
Copyright_xml	– notice: Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works. – notice: Copyright © 2018 The Authors, some rights reserved; exclusive licensee American Association for the Advancement of Science. No claim to original U.S. Government Works
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DOI	10.1126/science.aao5056
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Snippet	Neural stem and progenitor cells (NSPCs) generate neurons throughout life in the mammalian hippocampus. We used chronic in vivo imaging and followed... A window on hippocampal neurogenesisAddition of new neurons to the adult brain is key to the hippocampal functions of learning and memory. Pilz et al. labeled... Neural stem/progenitor cells (NSPCs) generate neurons throughout life in the mammalian hippocampus. We used chronic in vivo imaging and followed genetically...
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SubjectTerms	Animals ASCL1 protein Basic Helix-Loop-Helix Transcription Factors - genetics Brain Cell Death Cell Division - genetics Cells (biology) Circuits Dentate gyrus Hippocampus Hippocampus - cytology Hippocampus - growth & development Homology Learning Memory Mice Nerve Net - cytology Nerve Net - growth & development Neural stem cells Neural Stem Cells - cytology Neurogenesis Neurogenesis - genetics Neuroglia - cytology Neuroimaging Neurons Neurons - cytology Progenitor cells Progeny Promoter Regions, Genetic Rodents
Title	Live imaging of neurogenesis in the adult mouse hippocampus
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