Corrigendum: Nuclear RNA-seq of single neurons reveals molecular signatures of activation (Nature Communications (2016) 7 (11022) DOI: 10.1038/ncomms11022);Nuclear RNA-seq of single neurons reveals molecular signatures of activation

Nature Communications

Volumn 7, Issue , 2016, Pages

  Lacar, Benjamin ^a   Linker, Sara B ^a   Jaeger, Baptiste N ^a   Krishnaswami, Suguna ^b   Barron, Jerika ^a   Kelder, Martijn ^a   Parylak, Sarah ^a   Paquola, Apuã ^a   Venepally, Pratap ^b   Novotny, Mark ^a   O'Connor, Carolyn ^a   Fitzpatrick, Conor ^a   Erwin, Jennifer ^a   Hsu, Jonathan Y ^a   Husband, David ^a   McConnell, Michael J ^c   Lasken, Roger ^b   Gage, Fred H ^a  

^a SALK INSTITUTE FOR BIOLOGICAL STUDIES   (United States)

^b J CRAIG VENTER INSTITUTE   (United States)

^c UNIVERSITY OF VIRGINIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ARC PROTEIN; EARLY GROWTH RESPONSE FACTOR 1; NUCLEAR RNA; PROTEIN; PROTEIN FOS; SMALL NUCLEAR RNA; UNCLASSIFIED DRUG; ACTIVITY REGULATED CYTOSKELETAL-ASSOCIATED PROTEIN; CYTOSKELETON PROTEIN; HOMEODOMAIN PROTEIN; IMMEDIATE EARLY PROTEIN; NERVE PROTEIN; PROSPERO-RELATED HOMEOBOX 1 PROTEIN; PROTEIN C FOS; TRANSCRIPTOME; TUMOR SUPPRESSOR PROTEIN;

BRAIN; CELLS AND CELL COMPONENTS; GENE EXPRESSION; HETEROGENEITY; NEUROLOGY; PROTEIN; RNA;

ADULT; ANIMAL EXPERIMENT; ARTICLE; COMPARATIVE STUDY; CONTROLLED STUDY; FEMALE; GENE EXPRESSION; HIPPOCAMPUS; IMMEDIATE EARLY GENE; IMMUNOHISTOCHEMISTRY; MOUSE; NERVE CELL; NONHUMAN; PROMOTER REGION; PROTEIN BINDING; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RNA SEQUENCE; ANIMAL; C57BL MOUSE; CELL NUCLEUS; CONFOCAL MICROSCOPY; CYTOLOGY; DENTATE GYRUS; GENE ONTOLOGY; GENETICS; METABOLISM; PROCEDURES; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS; SINGLE CELL ANALYSIS; TRANSGENIC MOUSE;

ANIMALS; CELL NUCLEUS; CYTOSKELETAL PROTEINS; DENTATE GYRUS; EARLY GROWTH RESPONSE PROTEIN 1; GENE ONTOLOGY; HOMEODOMAIN PROTEINS; IMMEDIATE-EARLY PROTEINS; IMMUNOHISTOCHEMISTRY; MICE, INBRED C57BL; MICE, TRANSGENIC; MICROSCOPY, CONFOCAL; NERVE TISSUE PROTEINS; NEURONS; PROTO-ONCOGENE PROTEINS C-FOS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; SEQUENCE ANALYSIS, RNA; SINGLE-CELL ANALYSIS; TRANSCRIPTOME; TUMOR SUPPRESSOR PROTEINS;

EID: 84973299445     PISSN: None     EISSN: 20411723     Source Type: Journal    
DOI: 10.1038/ncomms15047     Document Type: Erratum

References (69)

1. Hashimshony, T., Wagner, F., Sher, N. & Yanai, I. CEL-seq: single-cell RNA-Seq by multiplexed linear amplification. Cell Rep. 2, 666-673 (2012).
2. Picelli, S. et al. Full-length RNA-seq from single cells using Smart-seq2. Nat. Protoc.. 9, 171-181 (2014).
3. Tang, F. et al. mRNA-Seq whole-transcriptome analysis of a single cell. Nat. Methods 6, 377-382 (2009).
4. Bhargava, V., Ko, P., Willems, E., Mercola, M. & Subramaniam, S. Quantitative transcriptomics using designed primer-based amplification. Sci. Rep. 3, 1740 (2013).
5. Qiu, S. et al. Single-neuron RNA-Seq: Technical feasibility and reproducibility. Front. Genet. 3, 124 (2012).
6. Usoskin, D. et al. Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing. Nat. Neurosci. 18, 145-153 (2015).
7. Zeisel, A. et al. Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq. Science 347, 1138-1142 (2015).
8. Pollen, A. a. et al. Low-coverage single-cell mRNA sequencing reveals cellular heterogeneity and activated signaling pathways in developing cerebral cortex. Nat. Biotechnol. 32, 1053-1058 (2014).
9. Darmanis, S. et al. A survey of human brain transcriptome diversity at the single cell level. Proc. Natl Acad. Sci. USA 112, 7285-7290 (2015).
10. Deng, W., Mayford, M. & Gage, F. H. Selection of distinct populations of dentate granule cells in response to inputs as a mechanism for pattern separation in mice. Elife 2, e00312 (2013).
11. Bartel, D. P., Sheng, M., Lau, L. F. & Greenberg, M. E. Growth factors and membrane depolarization activate distinct programs of early response gene expression: dissociation of fos and jun induction. Genes Dev. 3, 304-313 (1989).
12. Müller, C. M., Vlachos, A. & Deller, T. Calcium homeostasis of acutely denervated and lesioned dentate gyrus in organotypic entorhino-hippocampal co-cultures. Cell Calcium 47, 242-252 (2010).
13. Grindberg, R. V et al. RNA-sequencing from single nuclei. Proc. Natl Acad. Sci. USA 110, 19802-19807 (2013).
14. Tschochner, H. & Hurt, E. Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol. 13, 255-263 (2003).
15. Dragunow, M. & Robertson, H. A. Kindling stimulation induces c-fos protein(s) in granule cells of the rat dentate gyrus. Nature 329, 441-442 (1987).
16. Mihály, A., Szakaćs, R., Bohata, C., Dobó, E. & Krisztin-Péva, B. Timedependent distribution and neuronal localization of c-fos protein in the rat hippocampus following 4-aminopyridine seizures. Epilepsy Res. 44, 97-108 (2001).
17. Lyford, G. L. et al. Arc, a growth factor and activity-regulated gene, encodes a novel cytoskeleton-associated protein that is enriched in neuronal dendrites. Neuron 14, 433-445 (1995).
18. Chawla, M. K. et al. Sparse, environmentally selective expression of Arc RNA in the upper blade of the rodent fascia dentata by brief spatial experience. Hippocampus 15, 579-586 (2005).
19. Worley, P. F. et al. Constitutive expression of zif268 in neocortex is regulated by synaptic activity. Proc. Natl Acad. Sci. USA 88, 5106-5110 (1991).
20. Deng, W., Aimone, J. B. & Gage, F. H. New neurons and new memories: how does adult hippocampal neurogenesis affect learning and memory? Nat. Rev. Neurosci. 11, 339-350 (2010).
21. Aimone, J. B., Wiles, J. & Gage, F. H. Potential role for adult neurogenesis in the encoding of time in new memories. Nat. Neurosci. 9, 723-727 (2006).
22. Lee, I. & Kesner, R. P. Encoding versus retrieval of spatial memory: Double dissociation between the dentate gyrus and the perforant path inputs into CA3 in the dorsal hippocampus. Hippocampus 14, 66-76 (2004).
23. Gilbert, P. E., Kesner, R. P. & Lee, I. Dissociating hippocampal subregions: A double dissociation between dentate gyrus and CA1. Hippocampus 11, 626-636 (2001).
24. Jung, M. W. & McNaughton, B. L. Spatial selectivity of unit activity in the hippocampal granular layer. Hippocampus 3, 165-182 (1993).
25. Morgan, J. I., Cohen, D. R., Hempstead, J. L. & Curran, T. Mapping patterns of c-fos expression in the central nervous system after seizure. Science 237, 192-197 (1987).
26. Lavado, A. & Oliver, G. Prox1 expression patterns in the developing and adult murine brain. Dev. Dyn. 236, 518-524 (2007).
27. Choi, I. et al. Visualization of lymphatic vessels by Prox1-promoter directed GFP reporter in a bacterial artificial chromosome-based transgenic mouse. Blood 117, 362-365 (2011).
28. Yount, G. L., Ponsalle, P. & White, J. D. Pentylenetetrazole-induced seizures stimulate transcription of early and late response genes. Brain Res. Mol. Brain Res. 21, 219-224 (1994).
29. Malik, A. N. et al. Genome-wide identification and characterization of functional neuronal activity-dependent enhancers. Nat. Neurosci. 17, 1330-1339 (2014).
30. Shinawi, M. et al. A small recurrent deletion within 15q13.3 is associated with a range of neurodevelopmental phenotypes. Nat. Genet. 41, 1269-1271 (2009).
31. Helbig, I. et al. 15q13.3 microdeletions increase risk of idiopathic generalized epilepsy. Nat. Genet. 41, 160-162 (2009).
32. Krishnaswami, S. R. et al. Using single nuclei for RNA-Seq to capture the transcriptome of postmortem neurons. Nat. Protoc. 11, 499-524 (2016).
33. Roux, P. et al. Nuclear localization of c-Fos, but not v-Fos proteins, is controlled by extracellular signals. Cell 63, 341-351 (1990).
34. Marinov, G. K. et al. From single-cell to cell-pool transcriptomes: Stochasticity in gene expression and RNA splicing. Genome Res. 24, 496-510 (2014).
35. Picelli, S. et al. Smart-seq2 for sensitive full-length transcriptome profiling in single cells. Nat. Methods 10, 1096-1098 (2013).
36. Madabhushi, R. et al. Activity-induced DNA breaks govern the expression of neuronal early-response genes. Cell 18, 1592-1605 (2015).
37. Yamane, K., Wu, X. & Chen, J. A DNA damage-regulated BRCT-containing protein , TopBP1 , is required for cell survival. Mol. Cell. Biol. 22, 555-566 (2002).
38. Yamane, K., Kawabata, M. & Tsuruo, T. A DNA-topoisomerase-II-binding protein with eight repeating regions similar to DNA-repair enzymes and to a cell-cycle regulator. Eur. J. Biochem. 250, 794-799 (1997).
39. Murai, J. et al. Tyrosyl-DNA phosphodiesterase 1 (TDP1) repairs DNA damage induced by topoisomerases I and II and base alkylation in vertebrate cells. J. Biol. Chem. 287, 12848-12857 (2012).
40. Hai, T., Wolfgang, C. D., Marsee, D. K., Allen, A. E. & Sivaprasad, U. ATF3 and stress responses. Gene Expr 7, 321-335 (1999).
41. Pavlovsky, A. A. et al. Psychological stress, cocaine and natural reward each induce endoplasmic reticulum stress genes in rat brain. Neuroscience 246, 160-169 (2013).
42. Guzowski, J. F., McNaughton, B. L., Barnes, C. A. & Worley, P. F. Environment-specific expression of the immediate-early gene Arc in hippocampal neuronal ensembles. Nat. Neurosci. 2, 1120-1124 (1999).
43. Reijmers, L. G., Perkins, B. L., Matsuo, N. & Mayford, M. Localization of a stable neural correlate of associative memory. Science 317, 1230-1233 (2007).
44. Shin, J. et al. Single-cell RNA-Seq with waterfall reveals molecular cascades underlying adult neurogenesis. Cell Stem Cell 17, 1-13 (2015).
45. Trapnell, C. et al. The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat. Biotechnol. 32, 381-386 (2014).
46. Hur, E.-M. M. et al. GSK3 controls axon growth via CLASP-mediated regulation of growth cone microtubules. Genes Dev. 25, 1968-1981 (2011).
47. Han, J.-H. et al. Neuronal competition and selection during memory formation. Science 316, 457-460 (2007).
48. Morgan, J. I. & Curran, T. Stimulus-transcription coupling in the nervous system: involvement of the inducible proto-oncogenes fos and jun. Annu. Rev. Neurosci. 14, 421-451 (1991).
49. Sheng, M., McFadden, G. & Greenberg, M. E. Membrane depolarization and calcium induce c-fos transcription via phosphorylation of transcription factor CREB. Neuron 4, 571-582 (1990).
50. Hardingham, G. E., Chawla, S., Johnson, C. M. & Bading, H. Distinct functions of nuclear and cytoplasmic calcium in the control of gene expression. Nature 385, 260-265 (1997).
51. Valjent, E. et al. d9-tetrahydrocannabinol-induced MAPK/ERK and Elk-1 activation in vivo depends on dopaminergic transmission. Eur. J. Neurosci. 14, 342-352 (2001).
52. Thomas, G. M. & Huganir, R. L. MAPK cascade signalling and synaptic plasticity. Nat. Rev. Neurosci. 5, 173-183 (2004).
53. Pierrat, B., Correia, J. S., Mary, J. L., Tomás-Zuber, M. & Lesslauer, W. RSK-B, a novel ribosomal S6 kinase family member, is a CREB kinase under dominant control of p38alpha mitogen-activated protein kinase (p38alphaMAPK). J. Biol. Chem. 273, 29661-29671 (1998).
54. Cruz, F. C. et al. New technologies for examining the role of neuronal ensembles in drug addiction and fear. Nat. Rev. Neurosci. 14, 743-754 (2013).
55. Simms, B. a. & Zamponi, G. W. Neuronal voltage-gated calcium channels: structure, function, and dysfunction. Neuron 82, 24-45 (2014).
56. Gorter, J. a., Borgdorff, A. J., Van Vliet, E. a., Lopes da Silva, F. H. & Wadman, W. J. Differential and long-lasting alterations of high-voltage activated calcium currents in CA1 and dentate granule neurons after status epilepticus. Eur. J. Neurosci. 16, 701-712 (2002).
57. Martinello, K. et al. Cholinergic afferent stimulation induces axonal function plasticity in adult hippocampal granule cells. Neuron 85, 346-363 (2015).
58. Knapska, E., Radwanska, K., Werka, T. & Kaczmarek, L. Functional internal complexity of amygdala: focus on gene activity mapping after behavioral training and drugs of abuse. Physiol. Rev. 87, 1113-1173 (2007).
59. Lin, D. et al. Functional identification of an aggression locus in the mouse hypothalamus. Nature 470, 221-226 (2011).
60. Lee, H. et al. Scalable control of mounting and attack by Esr1+ neurons in the ventromedial hypothalamus. Nature 509, 627-632 (2014).
61. Yassin, L. et al. An Embedded Subnetwork of Highly Active Neurons in the Neocortex. Neuron 68, 1043-1050 (2010).
62. Guez-Barber, D. et al. FACS identifies unique cocaine-induced gene regulation in selectively activated adult striatal neurons. J. Neurosci. 31, 4251-4259 (2011).
63. Robinson, M. D., McCarthy, D. J. & Smyth, G. K. edgeR: A Bioconductor package for differential expression analysis of digital gene expression data. Bioinformatics 26, 139-140 (2010).
64. Faul, F., Erdfelder, E., Lang, A.-G. & Buchner, A. G∗Power 3: a flexible statistical power analysis program for the social, behavioral, and biomedical sciences. Behav. Res. Methods 39, 175-191 (2007).
65. Smit, Afa, Hubley, R & Green, P. RepeatMasker Open-4.0. Available at http://www.repeatmasker.org. Accessed on 25 April 2014.
66. Altschul, S. F., Gish, W., Miller, W., Myers, E. W. & Lipman, D. J. Basic local alignment search tool. J. Mol. Biol. 215, 403-410 (1990).
67. Rosenbloom, K. R. et al. ENCODE Data in the UCSC Genome Browser: Year 5 update. Nucleic Acids Res. 41, D56-D63 (2013).
68. Smoot, M. E., Ono, K., Ruscheinski, J., Wang, P. L. & Ideker, T. Cytoscape 2.8: New features for data integration and network visualization. Bioinformatics 27, 431-432 (2011).
69. Huang, D. W., Lempicki, R. A. & Sherman, B. T. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat. Protoc. 4, 44-57 (2009).