Cargando…

Nuclear RNA-seq of single neurons reveals molecular signatures of activation

Single-cell sequencing methods have emerged as powerful tools for identification of heterogeneous cell types within defined brain regions. Application of single-cell techniques to study the transcriptome of activated neurons can offer insight into molecular dynamics associated with differential neur...

Descripción completa

Detalles Bibliográficos
Autores principales: Lacar, Benjamin, Linker, Sara B., Jaeger, Baptiste N., Krishnaswami, Suguna, Barron, Jerika, Kelder, Martijn, Parylak, Sarah, Paquola, Apuã, Venepally, Pratap, Novotny, Mark, O'Connor, Carolyn, Fitzpatrick, Conor, Erwin, Jennifer, Hsu, Jonathan Y., Husband, David, McConnell, Michael J., Lasken, Roger, Gage, Fred H.
Formato: Online Artículo Texto
Lenguaje:English
Publicado: Nature Publishing Group 2016
Materias:
Acceso en línea:https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4838832/
https://www.ncbi.nlm.nih.gov/pubmed/27090946
http://dx.doi.org/10.1038/ncomms11022
_version_ 1782428041316663296
author Lacar, Benjamin
Linker, Sara B.
Jaeger, Baptiste N.
Krishnaswami, Suguna
Barron, Jerika
Kelder, Martijn
Parylak, Sarah
Paquola, Apuã
Venepally, Pratap
Novotny, Mark
O'Connor, Carolyn
Fitzpatrick, Conor
Erwin, Jennifer
Hsu, Jonathan Y.
Husband, David
McConnell, Michael J.
Lasken, Roger
Gage, Fred H.
author_facet Lacar, Benjamin
Linker, Sara B.
Jaeger, Baptiste N.
Krishnaswami, Suguna
Barron, Jerika
Kelder, Martijn
Parylak, Sarah
Paquola, Apuã
Venepally, Pratap
Novotny, Mark
O'Connor, Carolyn
Fitzpatrick, Conor
Erwin, Jennifer
Hsu, Jonathan Y.
Husband, David
McConnell, Michael J.
Lasken, Roger
Gage, Fred H.
author_sort Lacar, Benjamin
collection PubMed
description Single-cell sequencing methods have emerged as powerful tools for identification of heterogeneous cell types within defined brain regions. Application of single-cell techniques to study the transcriptome of activated neurons can offer insight into molecular dynamics associated with differential neuronal responses to a given experience. Through evaluation of common whole-cell and single-nuclei RNA-sequencing (snRNA-seq) methods, here we show that snRNA-seq faithfully recapitulates transcriptional patterns associated with experience-driven induction of activity, including immediate early genes (IEGs) such as Fos, Arc and Egr1. SnRNA-seq of mouse dentate granule cells reveals large-scale changes in the activated neuronal transcriptome after brief novel environment exposure, including induction of MAPK pathway genes. In addition, we observe a continuum of activation states, revealing a pseudotemporal pattern of activation from gene expression alone. In summary, snRNA-seq of activated neurons enables the examination of gene expression beyond IEGs, allowing for novel insights into neuronal activation patterns in vivo.
format Online
Article
Text
id pubmed-4838832
institution National Center for Biotechnology Information
language English
publishDate 2016
publisher Nature Publishing Group
record_format MEDLINE/PubMed
spelling pubmed-48388322016-05-04 Nuclear RNA-seq of single neurons reveals molecular signatures of activation Lacar, Benjamin Linker, Sara B. Jaeger, Baptiste N. Krishnaswami, Suguna Barron, Jerika Kelder, Martijn Parylak, Sarah Paquola, Apuã Venepally, Pratap Novotny, Mark O'Connor, Carolyn Fitzpatrick, Conor Erwin, Jennifer Hsu, Jonathan Y. Husband, David McConnell, Michael J. Lasken, Roger Gage, Fred H. Nat Commun Article Single-cell sequencing methods have emerged as powerful tools for identification of heterogeneous cell types within defined brain regions. Application of single-cell techniques to study the transcriptome of activated neurons can offer insight into molecular dynamics associated with differential neuronal responses to a given experience. Through evaluation of common whole-cell and single-nuclei RNA-sequencing (snRNA-seq) methods, here we show that snRNA-seq faithfully recapitulates transcriptional patterns associated with experience-driven induction of activity, including immediate early genes (IEGs) such as Fos, Arc and Egr1. SnRNA-seq of mouse dentate granule cells reveals large-scale changes in the activated neuronal transcriptome after brief novel environment exposure, including induction of MAPK pathway genes. In addition, we observe a continuum of activation states, revealing a pseudotemporal pattern of activation from gene expression alone. In summary, snRNA-seq of activated neurons enables the examination of gene expression beyond IEGs, allowing for novel insights into neuronal activation patterns in vivo. Nature Publishing Group 2016-04-19 /pmc/articles/PMC4838832/ /pubmed/27090946 http://dx.doi.org/10.1038/ncomms11022 Text en Copyright © 2016, Nature Publishing Group, a division of Macmillan Publishers Limited. All Rights Reserved. http://creativecommons.org/licenses/by/4.0/ This work is licensed under a Creative Commons Attribution 4.0 International License. The images or other third party material in this article are included in the article's Creative Commons license, unless indicated otherwise in the credit line; if the material is not included under the Creative Commons license, users will need to obtain permission from the license holder to reproduce the material. To view a copy of this license, visit http://creativecommons.org/licenses/by/4.0/
spellingShingle Article
Lacar, Benjamin
Linker, Sara B.
Jaeger, Baptiste N.
Krishnaswami, Suguna
Barron, Jerika
Kelder, Martijn
Parylak, Sarah
Paquola, Apuã
Venepally, Pratap
Novotny, Mark
O'Connor, Carolyn
Fitzpatrick, Conor
Erwin, Jennifer
Hsu, Jonathan Y.
Husband, David
McConnell, Michael J.
Lasken, Roger
Gage, Fred H.
Nuclear RNA-seq of single neurons reveals molecular signatures of activation
title Nuclear RNA-seq of single neurons reveals molecular signatures of activation
title_full Nuclear RNA-seq of single neurons reveals molecular signatures of activation
title_fullStr Nuclear RNA-seq of single neurons reveals molecular signatures of activation
title_full_unstemmed Nuclear RNA-seq of single neurons reveals molecular signatures of activation
title_short Nuclear RNA-seq of single neurons reveals molecular signatures of activation
title_sort nuclear rna-seq of single neurons reveals molecular signatures of activation
topic Article
url https://www.ncbi.nlm.nih.gov/pmc/articles/PMC4838832/
https://www.ncbi.nlm.nih.gov/pubmed/27090946
http://dx.doi.org/10.1038/ncomms11022
work_keys_str_mv AT lacarbenjamin nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation
AT linkersarab nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation
AT jaegerbaptisten nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation
AT krishnaswamisuguna nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation
AT barronjerika nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation
AT keldermartijn nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation
AT parylaksarah nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation
AT paquolaapua nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation
AT venepallypratap nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation
AT novotnymark nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation
AT oconnorcarolyn nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation
AT fitzpatrickconor nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation
AT erwinjennifer nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation
AT hsujonathany nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation
AT husbanddavid nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation
AT mcconnellmichaelj nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation
AT laskenroger nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation
AT gagefredh nuclearrnaseqofsingleneuronsrevealsmolecularsignaturesofactivation