Comprehensive Classification of Retinal Bipolar Neurons by Single-Cell Transcriptomics

Cell - Tập 166 Số 5 - Trang 1308-1323.e30 - 2016
Karthik Shekhar1, Sylvain W. Lapan2,3, Irene E. Whitney4, Nicholas M. Tran4, Evan Z. Macosko2,5,6, Monika S. Kowalczyk1, Xian Adiconis1,6, Joshua Z. Levin1,6, James Nemesh2,5,6, Melissa Goldman2,6, Steven A. McCarroll2,5,6, Constance L. Cepko2,7,3, Aviv Regev1,8,3, Joshua R. Sanes4
1Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA
2Department of Genetics, Harvard Medical School, Boston, MA 02115 USA
3Howard Hughes Medical Institute, Chevy Chase, MD 20815 USA
4Center for Brain Science and Department of Molecular and Cellular Biology, Harvard University, Cambridge, MA 02130, USA
5Program in Medical and Population Genetics, Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA
6Stanley Center for Psychiatric Research, Broad Institute of Harvard and MIT, Cambridge, MA 02142, USA
7Department of Ophthalmology, Harvard Medical School, Boston, MA 02115 USA
8Department of Biology and Koch Institute, MIT, Cambridge, MA 02139, USA

Tóm tắt

Từ khóa


Tài liệu tham khảo

Baas, 2000, The subcellular localization of Otx2 is cell-type specific and developmentally regulated in the mouse retina, Brain Res. Mol. Brain Res., 78, 26, 10.1016/S0169-328X(00)00060-7

Berglund, 2006, Imaging synaptic inhibition in transgenic mice expressing the chloride indicator, Clomeleon, Brain Cell Biol., 35, 207, 10.1007/s11068-008-9019-6

Blondel, 2008, Fast unfolding of communities in large networks, J. Stat. Mech., 2008, P10008, 10.1088/1742-5468/2008/10/P10008

Borghuis, 2014, Kainate receptors mediate signaling in both transient and sustained OFF bipolar cell pathways in mouse retina, J. Neurosci., 34, 6128, 10.1523/JNEUROSCI.4941-13.2014

Breiman, 2001, Random forests, Mach. Learn., 45, 5, 10.1023/A:1010933404324

Breuninger, 2011, Chromatic bipolar cell pathways in the mouse retina, J. Neurosci., 31, 6504, 10.1523/JNEUROSCI.0616-11.2011

Buffelli, 2003, Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition, Nature, 424, 430, 10.1038/nature01844

Burmeister, 1996, Ocular retardation mouse caused by Chx10 homeobox null allele: impaired retinal progenitor proliferation and bipolar cell differentiation, Nat. Genet., 12, 376, 10.1038/ng0496-376

Cai, 2013, Improved tools for the Brainbow toolbox, Nat Methods, 10, 540, 10.1038/nmeth.2450

Chow, 2004, Control of late off-center cone bipolar cell differentiation and visual signaling by the homeobox gene Vsx1, Proc. Natl. Acad. Sci. USA, 101, 1754, 10.1073/pnas.0306520101

Darmanis, 2015, A survey of human brain transcriptome diversity at the single cell level, Proc. Natl. Acad. Sci. USA, 112, 7285, 10.1073/pnas.1507125112

Della Santina, 2016, Glutamatergic monopolar interneurons provide a novel pathway of excitation in the mouse retina, Curr. Biol., 10.1016/j.cub.2016.06.016

Dobin, 2013, STAR: ultrafast universal RNA-seq aligner, Bioinformatics, 29, 15, 10.1093/bioinformatics/bts635

Duan, 2014, Type II cadherins guide assembly of a direction-selective retinal circuit, Cell, 158, 793, 10.1016/j.cell.2014.06.047

Duan, 2015, Subtype-specific regeneration of retinal ganglion cells following axotomy: effects of osteopontin and mTOR signaling, Neuron, 85, 1244, 10.1016/j.neuron.2015.02.017

Elshatory, 2007, Expression of the LIM-homeodomain protein Isl1 in the developing and mature mouse retina, J. Comp. Neurol., 503, 182, 10.1002/cne.21390

Emerson, 2011, Identification of a retina-specific Otx2 enhancer element active in immature developing photoreceptors, Dev. Biol., 360, 241, 10.1016/j.ydbio.2011.09.012

Euler, 2014, Retinal bipolar cells: elementary building blocks of vision, Nat. Rev. Neurosci., 15, 507, 10.1038/nrn3783

Fortunato, 2010, Community detection in graphs, Phys. Rep., 486, 75, 10.1016/j.physrep.2009.11.002

Fox, 2007, Synaptotagmin I and II are present in distinct subsets of central synapses, J. Comp. Neurol., 503, 280, 10.1002/cne.21381

Greene, 2016, Analogous Convergence of Sustained and Transient Inputs in Parallel On and Off Pathways for Retinal Motion Computation, Cell Rep., 14, 1892, 10.1016/j.celrep.2016.02.001

Grün, 2015, Single-cell messenger RNA sequencing reveals rare intestinal cell types, Nature, 525, 251, 10.1038/nature14966

Haverkamp, 2003, Immunocytochemical description of five bipolar cell types of the mouse retina, J. Comp. Neurol., 455, 463, 10.1002/cne.10491

Haverkamp, 2005, The primordial, blue-cone color system of the mouse retina, J. Neurosci., 25, 5438, 10.1523/JNEUROSCI.1117-05.2005

Haverkamp, 2009, Expression analysis of green fluorescent protein in retinal neurons of four transgenic mouse lines, Neuroscience, 160, 126, 10.1016/j.neuroscience.2009.01.081

Heimberg, 2016, Low dimensionality in gene expression data enables the accurate extraction of transcriptional programs from shallow sequencing, Cell Syst., 2, 239, 10.1016/j.cels.2016.04.001

Hellmer, 2016, Morphological and physiological analysis of type-5 and other bipolar cells in the mouse retina, Neuroscience, 315, 246, 10.1016/j.neuroscience.2015.12.016

Helmstaedter, 2013, Connectomic reconstruction of the inner plexiform layer in the mouse retina, Nature, 500, 168, 10.1038/nature12346

Huang, 1999, Ggamma13 colocalizes with gustducin in taste receptor cells and mediates IP3 responses to bitter denatonium, Nat. Neurosci., 2, 1055, 10.1038/15981

Huang, 2003, G protein subunit G gamma 13 is coexpressed with G alpha o, G beta 3, and G beta 4 in retinal ON bipolar cells, J. Comp. Neurol., 455, 1, 10.1002/cne.10396

Ichinose, 2016, Differential signalling and glutamate receptor compositions in the OFF bipolar cell types in the mouse retina, J. Physiol., 594, 883, 10.1113/JP271458

Jaitin, 2014, Massively parallel single-cell RNA-seq for marker-free decomposition of tissues into cell types, Science, 343, 776, 10.1126/science.1247651

Jeon, 1998, The major cell populations of the mouse retina, J. Neurosci., 18, 8936, 10.1523/JNEUROSCI.18-21-08936.1998

Johnson, 2007, Adjusting batch effects in microarray expression data using empirical Bayes methods, Biostatistics, 8, 118, 10.1093/biostatistics/kxj037

Kay, 2011, Neurod6 expression defines new retinal amacrine cell subtypes and regulates their fate, Nat. Neurosci., 14, 965, 10.1038/nn.2859

Kay, 2012, MEGF10 and MEGF11 mediate homotypic interactions required for mosaic spacing of retinal neurons, Nature, 483, 465, 10.1038/nature10877

Kim, 2008, A core paired-type and POU homeodomain-containing transcription factor program drives retinal bipolar cell gene expression, J. Neurosci., 28, 7748, 10.1523/JNEUROSCI.0397-08.2008

Kim, 2008, Identification of molecular markers of bipolar cells in the murine retina, J. Comp. Neurol., 507, 1795, 10.1002/cne.21639

Kim, 2014, Space-time wiring specificity supports direction selectivity in the retina, Nature, 509, 331, 10.1038/nature13240

Koester, 1992, Functional classes of cortical projection neurons develop dendritic distinctions by class-specific sculpting of an early common pattern, J. Neurosci., 12, 1382, 10.1523/JNEUROSCI.12-04-01382.1992

Krishnaswamy, 2015, Sidekick 2 directs formation of a retinal circuit that detects differential motion, Nature, 524, 466, 10.1038/nature14682

Langmead, 2012, Fast gapped-read alignment with Bowtie 2, Nat. Methods, 9, 357, 10.1038/nmeth.1923

Levine, 2015, Data-driven phenotypic dissection of AML reveals progenitor-like cells that correlate with prognosis, Cell, 162, 184, 10.1016/j.cell.2015.05.047

Li, 2011, RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome, BMC Bioinformatics, 12, 323, 10.1186/1471-2105-12-323

Li, 2003, Aberrant responses to acoustic stimuli in mice deficient for neural recognition molecule NB-2, Eur. J. Neurosci., 17, 929, 10.1046/j.1460-9568.2003.02514.x

Lois, 2002, Germline transmission and tissue-specific expression of transgenes delivered by lentiviral vectors, Science, 295, 868, 10.1126/science.1067081

Macosko, 2015, Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets, Cell, 161, 1202, 10.1016/j.cell.2015.05.002

Madisen, 2010, A robust and high-throughput Cre reporting and characterization system for the whole mouse brain, Nat. Neurosci., 13, 133, 10.1038/nn.2467

Marchenko, 1967, Distribution of eigenvalues for some sets of random matrices, Matematicheskii Sbornik, 114, 507

Matutano, J.C., Unanue, R.M., and Avanzada, M.U.E.I. (2014). New clustering proposals for Twitter based on the Louvain algorithm, Master’s Thesis (Universidad Nacional de Educación a Distancia).

McDavid, 2013, Data exploration, quality control and testing in single-cell qPCR-based gene expression experiments, Bioinformatics, 29, 461, 10.1093/bioinformatics/bts714

Misgeld, 2007, Imaging axonal transport of mitochondria in vivo, Nat. Methods, 4, 559, 10.1038/nmeth1055

Picelli, 2014, Full-length RNA-seq from single cells using Smart-seq2, Nat. Protoc., 9, 171, 10.1038/nprot.2014.006

Pollen, 2014, Low-coverage single-cell mRNA sequencing reveals cellular heterogeneity and activated signaling pathways in developing cerebral cortex, Nat. Biotechnol., 32, 1053, 10.1038/nbt.2967

Preibisch, 2009, Globally optimal stitching of tiled 3D microscopic image acquisitions, Bioinformatics, 25, 1463, 10.1093/bioinformatics/btp184

Prince, 2013, Kirrel3 is required for the coalescence of vomeronasal sensory neuron axons into glomeruli and for male-male aggression, Development, 140, 2398, 10.1242/dev.087262

Puller, 2013, OFF bipolar cells express distinct types of dendritic glutamate receptors in the mouse retina, Neuroscience, 243, 136, 10.1016/j.neuroscience.2013.03.054

Puthussery, 2010, Localization of the calcium-binding protein secretagogin in cone bipolar cells of the mammalian retina, J. Comp. Neurol., 518, 513, 10.1002/cne.22234

Rosvall, 2008, Maps of random walks on complex networks reveal community structure, Proc. Natl. Acad. Sci. USA, 105, 1118, 10.1073/pnas.0706851105

Rowan, 2004, Genetic analysis of the homeodomain transcription factor Chx10 in the retina using a novel multifunctional BAC transgenic mouse reporter, Dev. Biol., 271, 388, 10.1016/j.ydbio.2004.03.039

Sanes, 2015, The types of retinal ganglion cells: current status and implications for neuronal classification, Annu. Rev. Neurosci., 38, 221, 10.1146/annurev-neuro-071714-034120

Schubert, 2008, Development of presynaptic inhibition onto retinal bipolar cell axon terminals is subclass-specific, J. Neurophysiol., 100, 304, 10.1152/jn.90202.2008

Seung, 2014, Neuronal cell types and connectivity: lessons from the retina, Neuron, 83, 1262, 10.1016/j.neuron.2014.08.054

Sharma, 1998, LIM homeodomain factors Lhx3 and Lhx4 assign subtype identities for motor neurons, Cell, 95, 817, 10.1016/S0092-8674(00)81704-3

Siegert, 2012, Transcriptional code and disease map for adult retinal cell types, Nat. Neurosci., 15, 487, 10.1038/nn.3032

Spitzer, 2015, Neurotransmitter switching? No surprise, Neuron, 86, 1131, 10.1016/j.neuron.2015.05.028

Taniguchi, 2011, A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex, Neuron, 71, 995, 10.1016/j.neuron.2011.07.026

Tasic, 2016, Adult mouse cortical cell taxonomy revealed by single cell transcriptomics, Nat. Neurosci., 19, 335, 10.1038/nn.4216

Taylor, 2012, The role of starburst amacrine cells in visual signal processing, Vis. Neurosci., 29, 73, 10.1017/S0952523811000393

Trimarchi, 2007, Molecular heterogeneity of developing retinal ganglion and amacrine cells revealed through single cell gene expression profiling, J. Comp. Neurol., 502, 1047, 10.1002/cne.21368

Ueda, 1997, The mGluR6 5′ upstream transgene sequence directs a cell-specific and developmentally regulated expression in retinal rod and ON-type cone bipolar cells, J. Neurosci., 17, 3014, 10.1523/JNEUROSCI.17-09-03014.1997

Usoskin, 2015, Unbiased classification of sensory neuron types by large-scale single-cell RNA sequencing, Nat. Neurosci., 18, 145, 10.1038/nn.3881

van der Maaten, 2008, Visualizing data using t-SNE, J. Mach. Learn. Res., 9, 2579

Wagner, 2015, GO-PCA: an unsupervised method to explore gene expression data using prior knowledge, PLoS ONE, 10, e0143196, 10.1371/journal.pone.0143196

Wässle, 2009, Cone contacts, mosaics, and territories of bipolar cells in the mouse retina, J. Neurosci., 29, 106, 10.1523/JNEUROSCI.4442-08.2009

Zeisel, 2015, Brain structure. Cell types in the mouse cortex and hippocampus revealed by single-cell RNA-seq, Science, 347, 1138, 10.1126/science.aaa1934