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

被引:276
作者
Lacar, Benjamin [1 ]
Linker, Sara B. [1 ]
Jaeger, Baptiste N. [1 ]
Krishnaswami, Suguna [2 ]
Barron, Jerika [1 ]
Kelder, Martijn [1 ]
Parylak, Sarah [1 ]
Paquola, Apua [1 ]
Venepally, Pratap [2 ]
Novotny, Mark [1 ]
O'Connor, Carolyn [1 ]
Fitzpatrick, Conor [1 ]
Erwin, Jennifer [1 ]
Hsu, Jonathan Y. [1 ]
Husband, David [1 ]
McConnell, Michael J. [3 ]
Lasken, Roger [2 ]
Gage, Fred H. [1 ]
机构
[1] Salk Inst Biol Studies, Genet Lab, 10010 N Torrey Pines Rd, La Jolla, CA 92037 USA
[2] J Craig Venter Inst, La Jolla, CA 92037 USA
[3] Univ Virginia, Sch Med, Dept Biochem & Mol Genet, Charlottesville, VA 22908 USA
来源
NATURE COMMUNICATIONS | 2016年 / 7卷
关键词
C-FOS; GENE-EXPRESSION; DENTATE GYRUS; MEMBRANE DEPOLARIZATION; DOUBLE DISSOCIATION; NERVOUS-SYSTEM; CELL; CALCIUM; PROTEIN; TRANSCRIPTOME;
D O I
10.1038/ncomms11022
中图分类号
O [数理科学和化学]; P [天文学、地球科学]; Q [生物科学]; N [自然科学总论];
学科分类号
07 ; 0710 ; 09 ;
摘要
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.
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页数:11
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共 68 条
[1]   Potential role for adult neurogenesis in the encoding of time in new memories [J].
Aimone, James B. ;
Wiles, Janet ;
Gage, Fred H. .
NATURE NEUROSCIENCE, 2006, 9 (06) :723-727
[2]   BASIC LOCAL ALIGNMENT SEARCH TOOL [J].
ALTSCHUL, SF ;
GISH, W ;
MILLER, W ;
MYERS, EW ;
LIPMAN, DJ .
JOURNAL OF MOLECULAR BIOLOGY, 1990, 215 (03) :403-410
[3]   GROWTH-FACTORS AND MEMBRANE DEPOLARIZATION ACTIVATE DISTINCT PROGRAMS OF EARLY RESPONSE GENE-EXPRESSION - DISSOCIATION OF FOS AND JUN INDUCTION [J].
BARTEL, DP ;
SHENG, M ;
LAU, LF ;
GREENBERG, ME .
GENES & DEVELOPMENT, 1989, 3 (03) :304-313
[4]   Quantitative Transcriptomics using Designed Primer-based Amplification [J].
Bhargava, Vipul ;
Ko, Pang ;
Willems, Erik ;
Mercola, Mark ;
Subramaniam, Shankar .
SCIENTIFIC REPORTS, 2013, 3
[5]   Sparse, environmentally selective expression of arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience [J].
Chawla, MK ;
Guzowski, JF ;
Ramirez-Amaya, V ;
Lipa, P ;
Hoffman, KL ;
Marriott, LK ;
Worley, PF ;
McNaughton, BL ;
Barnes, CA .
HIPPOCAMPUS, 2005, 15 (05) :579-586
[6]   Visualization of lymphatic vessels by Prox1-promoter directed GFP reporter in a bacterial artificial chromosome-based transgenic mouse [J].
Choi, Inho ;
Chung, Hee Kyoung ;
Ramu, Swapnika ;
Lee, Ha Neul ;
Kim, Kyu Eui ;
Lee, Sunju ;
Yoo, Jaehyuk ;
Choi, Dongwon ;
Lee, Yong Suk ;
Aguilar, Berenice ;
Hong, Young-Kwon .
BLOOD, 2011, 117 (01) :362-365
[7]   New technologies for examining the role of neuronal ensembles in drug addiction and fear [J].
Cruz, Fabio C. ;
Koya, Eisuke ;
Guez-Barber, Danielle H. ;
Bossert, Jennifer M. ;
Lupica, Carl R. ;
Shaham, Yavin ;
Hope, Bruce T. .
NATURE REVIEWS NEUROSCIENCE, 2013, 14 (11) :743-754
[8]   A survey of human brain transcriptome diversity at the single cell level [J].
Darmanis, Spyros ;
Sloan, Steven A. ;
Zhang, Ye ;
Enge, Martin ;
Caneda, Christine ;
Shuer, Lawrence M. ;
Gephart, Melanie G. Hayden ;
Barres, Ben A. ;
Quake, Stephen R. .
PROCEEDINGS OF THE NATIONAL ACADEMY OF SCIENCES OF THE UNITED STATES OF AMERICA, 2015, 112 (23) :7285-7290
[9]   Selection of distinct populations of dentate granule cells in response to inputs as a mechanism for pattern separation in mice [J].
Deng, Wei ;
Mayford, Mark ;
Gage, Fred H. .
ELIFE, 2013, 2
[10]   New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? [J].
Deng, Wei ;
Aimone, James B. ;
Gage, Fred H. .
NATURE REVIEWS NEUROSCIENCE, 2010, 11 (05) :339-350