Single-Cell Profiles of Retinal Ganglion Cells Differing in Resilience to Injury Reveal Neuroprotective Genes
Open accessPublished version of a preprint
Abstract
Neuronal types in the central nervous system differ dramatically in their resilience to injury or other insults. Here we studied the selective resilience of mouse retinal ganglion cells (RGCs) following optic nerve crush (ONC), which severs their axons and leads to death of ∼80% of RGCs within 2 weeks. To identify expression programs associated with differential resilience, we first used single-cell RNA-seq (scRNA-seq) to generate a comprehensive molecular atlas of 46 RGC types in adult retina. We then tracked their survival after ONC; characterized transcriptomic, physiological, and morphological changes that preceded degeneration; and identified genes selectively expressed by each type. Finally, using loss- and gain-of-function assays in vivo, we showed that manipulating some of these genes improved neuronal survival and axon regeneration following ONC. This study provides a systematic framework for parsing type-specific responses to injury and demonstrates that differential gene expression can be used to reveal molecular targets for intervention.
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
The claims and statistics of this paper haven’t been checked yet.
Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
Prkaa1 expression is found in many RGC subtypes including αON sustained and transient, αOFF sustained and transient, melanopsin-positive (M1, M2 and M5), and ON-OFF direction selective RGCs (oo-DS).
“a comprehensive molecular atlas of 46 RGC subtypes in the adult retina generated by single-cell RNA-seq [58] shows that Prkaa1 expression is found in many RGC subtypes including αON sustained and transient, αOFF sustained and transient, melanopsin-positive (M1, M2 and M5), and ON-OFF direction selective RGCs (oo-DS).”
From AMPK hyperactivation promotes dendrite retraction, synaptic loss, and neuronal dysfunction in glaucoma (2021) · cites this paper as [58]
The Results section, “An atlas of molecularly defined RGC types,” confirms that the authors used single-cell RNA-seq to identify 46 RGC types in adult mouse retina. The subclass Results passages describe αRGCs, melanopsin-positive RGCs and ooDSGCs, but do not report Prkaa1 expression in the listed subtypes; searches for Prkaa1 and AMPK did not find that expression claim in our copy. (LLM, conf=0.86)
Experimental — accuracy not yet measured
Self-check
Percentages, sums and reported differences re-computed from the paper’s own numbers.
The self-check needs the paper’s full text.
Cites
Fiji: an open-source platform for biological-image analysis
Schindelin, J., Arganda-Carreras, I., Frise, E., Kaynig, V., Longair, M., Pietzsch, T., Preibisch, S., Rueden, C., Saalfeld, S., Schmid, B., et al. (2012) · Nature Methods · doi:10.1038/nmeth.2019 · Cited by 66,890 · see citing works
Fast gapped-read alignment with Bowtie 2
Langmead, B., & Salzberg, S. L. (2012) · Nature Methods · doi:10.1038/nmeth.1923 · Cited by 56,400 · see citing works
(2008) · Journal of Machine Learning Research · Cited by 33,051 · see citing works
RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome
Li, B., & Dewey, C. N. (2011) · BMC Bioinformatics · doi:10.1186/1471-2105-12-323 · Cited by 22,179 · see citing works
Fast unfolding of communities in large networks
Blondel, V. D., Guillaume, J.-L., Lambiotte, R., & Lefebvre, E. (2008) · Journal of Statistical Mechanics: Theory and Experiment · doi:10.1088/1742-5468/2008/10/p10008 · Cited by 21,424 · see citing works
Graph-based genome alignment and genotyping with HISAT2 and HISAT-genotype
Kim, D., Paggi, J. M., Park, C., Bennett, C., & Salzberg, S. L. (2019) · Nature Biotechnology · doi:10.1038/s41587-019-0201-4 · Cited by 15,022 · see citing works
Learning the parts of objects by non-negative matrix factorization
Lee, D. D., & Seung, H. S. (1999) · Nature · doi:10.1038/44565 · Cited by 13,898 · see citing works
Bioconductor: open software development for computational biology and bioinformatics
Gentleman, R., Carey, V., Bates, D., Bolstad, B., Dettling, M., Dudoit, S., Ellis, B., Gautier, L., Ge, Y., Gentry, J., et al. (2004) · Genome Biology · doi:10.1186/gb-2004-5-10-r80 · Cited by 13,133 · see citing works
Independent component analysis, A new concept?
Comon, P. (1994) · Signal Processing · doi:10.1016/0165-1684(94)90029-9 · Cited by 8,150 · see citing works
Highly parallel genome-wide expression profiling of individual cells using nanoliter droplets.
Macosko, E. Z., Basu, A., Satija, R., Nemesh, J., Shekhar, K., Goldman, M., Tirosh, I., Bialas, A. R., Kamitaki, N., Martersteck, E. M., et al. (2015) · Cell · doi:10.1016/j.cell.2015.05.002 · Cited by 7,110 · see citing works
Self-citationA robust and high-throughput Cre reporting and characterization system for the whole mouse brain
Madisen, L., Zwingman, T. A., Sunkin, S. M., Oh, S. W., Zariwala, H. A., Gu, H., Ng, L. L., Palmiter, R. D., Hawrylycz, M. J., Jones, A. R., et al. (2010) · Nature Neuroscience · doi:10.1038/nn.2467 · Cited by 6,907 · see citing works
Transcript-level expression analysis of RNA-seq experiments with HISAT, StringTie and Ballgown
Pertea, M., Kim, D., Pertea, G. M., Leek, J. T., & Salzberg, S. L. (2016) · Nature Protocols · doi:10.1038/nprot.2016.095 · Cited by 6,708 · see citing works
CellProfiler: image analysis software for identifying and quantifying cell phenotypes
Carpenter, A. E., Jones, T. R., Lamprecht, M. R., Clarke, C., Kang, I. H., Friman, O., Guertin, D. A., Chang, J. H., Lindquist, R. A., Moffat, J., et al. (2006) · Genome biology · doi:10.1186/gb-2006-7-10-r100 · Cited by 5,172 · see citing works
Maps of random walks on complex networks reveal community structure
Rosvall, M., & Bergstrom, C. T. (2008) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0706851105 · Cited by 4,583 · see citing works
Halko, N., Martinsson, P., & Tropp, J. A. (2011) · SIAM Review · doi:10.1137/090771806 · Cited by 4,038 · see citing works
Finak, G., McDavid, A., Yajima, M., Deng, J., Gersuk, V., Shalek, A. K., Slichter, C. K., Miller, H. W., McElrath, M. J., Prlic, M., et al. (2015) · Genome Biology · doi:10.1186/s13059-015-0844-5 · Cited by 3,159 · see citing works
Imaging Neuronal Subsets in Transgenic Mice Expressing Multiple Spectral Variants of GFP
Feng, G., Mellor, R. H., Bernstein, M., Keller-Peck, C., Nguyen, Q. T., Wallace, M., Nerbonne, J. M., Lichtman, J. W., & Sanes, J. R. (2000) · Neuron · doi:10.1016/s0896-6273(00)00084-2 · Cited by 3,042 · see citing works
Self-citationSmart-seq2 for sensitive full-length transcriptome profiling in single cells
Picelli, S., Björklund, Å. K., Faridani, O. R., Sagasser, S., Winberg, G., & Sandberg, R. (2013) · Nature Methods · doi:10.1038/nmeth.2639 · Cited by 2,358 · see citing works
Regev, A., Teichmann, S. A., Lander, E. S., Amit, I., Benoist, C., Birney, E., Bodenmiller, B., Campbell, P., Carninci, P., Clatworthy, M., et al. (2017) · eLife · doi:10.7554/elife.27041 · Cited by 2,232 · see citing works
Self-citationUnsupervised spike detection and sorting with wavelets and superparamagnetic clustering
Quiroga, R. Q., Nadasdy, Z., & Ben-Shaul, Y. (2004) · Neural Computation · doi:10.1162/089976604774201631 · Cited by 2,119 · see citing works
A resource of Cre driver lines for genetic targeting of GABAergic neurons in cerebral cortex
Taniguchi, H., He, M., Wu, P., Kim, S., Paik, R., Sugino, K., Kvitsani, D., Fu, Y., Lu, J., Lin, Y., et al. (2011) · Neuron · doi:10.1016/j.neuron.2011.07.026 · Cited by 1,828 · see citing works
Directed differentiation of embryonic stem cells into motor neurons.
Wichterle, H., Lieberam, I., Porter, J. A., & Jessell, T. (2002) · Cell · doi:10.1016/s0092-8674(02)00835-8 · Cited by 1,792 · see citing works
Promoting Axon Regeneration in the Adult CNS by Modulation of the PTEN/mTOR Pathway
Park, K. K., Liu, K., Hu, Y., Smith, P. D., Wang, C., Cai, B., Xu, B., Connolly, L., Kramvis, I., Sahin, M., et al. (2008) · Science · doi:10.1126/science.1161566 · Cited by 1,686 · see citing works
Self-citationLeptin Action on GABAergic Neurons Prevents Obesity and Reduces Inhibitory Tone to POMC Neurons
Vong, L., Ye, C., Yang, Z., Choi, B. J., Chua, S. C., & Lowell, B. B. (2011) · Neuron · doi:10.1016/j.neuron.2011.05.028 · Cited by 1,238 · see citing works
Single-Cell Multi-omic Integration Compares and Contrasts Features of Brain Cell Identity
Welch, J. D., Kozareva, V., Ferreira, A., Vanderburg, C., Martin, C., & Macosko, E. Z. (2019) · Cell · doi:10.1016/j.cell.2019.05.006 · Cited by 1,193 · see citing works
Comprehensive Classification of Retinal Bipolar Neurons by Single-Cell Transcriptomics
Shekhar, K., Lapan, S. W., Whitney, I. E., Tran, N. M., Macosko, E. Z., Kowalczyk, M., Adiconis, X., Levin, J. Z., Nemesh, J., Goldman, M., et al. (2016) · Cell · doi:10.1016/j.cell.2016.07.054 · Cited by 1,176 · see citing works
Self-citationThe functional diversity of retinal ganglion cells in the mouse
Baden, T., Berens, P., Franke, K., Román Rosón, M., Bethge, M., & Euler, T. (2016) · Nature · doi:10.1038/nature16468 · Cited by 999 · see citing works
Longair, M., Baker, D. A., & Armstrong, J. D. (2011) · Bioinformatics · doi:10.1093/bioinformatics/btr390 · Cited by 939 · see citing works
The Types of Retinal Ganglion Cells: Current Status and Implications for Neuronal Classification
Sanes, J. R., & Masland, R. H. (2015) · Annual Review of Neuroscience · doi:10.1146/annurev-neuro-071714-034120 · Cited by 789 · see citing works
Self-citationEcker, J. L., Dumitrescu, O. N., Wong, K. Y., Alam, N. M., Chen, S., LeGates, T. A., Renna, J. M., Prusky, G. T., Berson, D. M., & Hattar, S. S. (2010) · Neuron · doi:10.1016/j.neuron.2010.05.023 · Cited by 669 · see citing works
Pun, S., Santos, A. F., Saxena, S., Xu, L., & Caroni, P. (2006) · Nature Neuroscience · doi:10.1038/nn1653 · Cited by 659 · see citing works
Selective vulnerability in neurodegenerative diseases
Fu, H., Hardy, J., & Duff, K. E. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0221-2 · Cited by 585 · see citing works
Saxena, S., & Caroni, P. (2011) · Neuron · doi:10.1016/j.neuron.2011.06.031 · Cited by 561 · see citing works
Duan, X., Qiao, M., Bei, F., Kim, I.-J., He, Z., & Sanes, J. R. (2015) · Neuron · doi:10.1016/j.neuron.2015.02.017 · Cited by 527 · see citing works
Self-citationFast interpolation-based t-SNE for improved visualization of single-cell RNA-seq data
Linderman, G. C., Rachh, M., Hoskins, J. G., Steinerberger, S., & Kluger, Y. (2019) · Nature Methods · doi:10.1038/s41592-018-0308-4 · Cited by 521 · see citing works
Single-cell analysis of experience-dependent transcriptomic states in the mouse visual cortex
Hrvatin, S., Hochbaum, D. R., Nagy, M. A., Cicconet, M., Robertson, K., Cheadle, L., Zilionis, R., Ratner, A., Borges-Monroy, R., Klein, A. M., et al. (2018) · Nature Neuroscience · doi:10.1038/s41593-017-0029-5 · Cited by 497 · see citing works
Molecular Classification and Comparative Taxonomics of Foveal and Peripheral Cells in Primate Retina
Peng, Y., Shekhar, K., Yan, W., Herrmann, D., Sappington, A., Bryman, G. S., van Zyl, T. A., Do, M. T. H., Regev, A., & Sanes, J. R. (2019) · Cell · doi:10.1016/j.cell.2019.01.004 · Cited by 465 · see citing works
Self-citationDetecting Activated Cell Populations Using Single-Cell RNA-Seq
Wu, Y. E., Pan, L., Zuo, Y., Li, X., & Hong, W. (2017) · Neuron · doi:10.1016/j.neuron.2017.09.026 · Cited by 438 · see citing works
Axon Regeneration in the Peripheral and Central Nervous Systems
Huebner, E. A., & Strittmatter, S. M. (2009) · Results and problems in cell differentiation · doi:10.1007/400_2009_19 · Cited by 420 · see citing works
Single cell transcriptome profiling of retinal ganglion cells identifies cellular subtypes
Rheaume, B. A., Jereen, A., Bolisetty, M. T., Sajid, M. S., Yang, Y. J., Renna, K., Sun, L., Robson, P., & Trakhtenberg, E. F. (2018) · Nature Communications · doi:10.1038/s41467-018-05134-3 · Cited by 401 · see citing works
Molecular identification of a retinal cell type that responds to upward motion
Kim, I.-J., Zhang, Y., Yamagata, M., Meister, M., & Sanes, J. R. (2008) · Nature · doi:10.1038/nature06739 · Cited by 397 · see citing works
Self-citationKay, J. N., la Huerta, I. D., Kim, I.-J., Zhang, Y., Yamagata, M., Chu, M. W., Meister, M., & Sanes, J. R. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.0907-11.2011 · Cited by 351 · see citing works
Self-citationAdult neurogenesis and brain regeneration in zebrafish
Kızıl, Ç., Kaslin, J., Kroehne, V., & Brand, M. (2011) · Developmental Neurobiology · doi:10.1002/dneu.20918 · Cited by 346 · see citing works
Hannibal, J., Hindersson, P., Knudsen, S. M., Georg, B., & Fahrenkrug, J. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-01-j0002.2002 · Cited by 339 · see citing works
Genetic evidence that relative synaptic efficacy biases the outcome of synaptic competition
Buffelli, M., Burgess, R. W., Feng, G., Lobe, C. G., Lichtman, J. W., & Sanes, J. R. (2003) · Nature · doi:10.1038/nature01844 · Cited by 332 · see citing works
Self-citationDirection selectivity in the retina: symmetry and asymmetry in structure and function
Vaney, D. I., Sivyer, B., & Taylor, W. R. (2012) · Nature reviews. Neuroscience · doi:10.1038/nrn3165 · Cited by 330 · see citing works
Watkins, T. A., Wang, B., Huntwork, S., Yang, J. H., Jiang, Z., Eastham‐Anderson, J., Modrusan, Z. D., Kaminker, J. S., Tessier‐Lavigne, M., & Lewcock, J. W. (2013) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1211074110 · Cited by 330 · see citing works
Stable long-term chronic brain mapping at the single-neuron level
Tian-ming Fu, B., Hong, G., Zhou, T., Schuhmann, T. G., Viveros, R. D., & Lieber, C. M. (2016) · Nature Methods · doi:10.1038/nmeth.3969 · Cited by 326 · see citing works
Self-citationThe most numerous ganglion cell type of the mouse retina is a selective feature detector
Zhang, Y., Kim, I.-J., Sanes, J. R., & Meister, M. (2012) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1211547109 · Cited by 316 · see citing works
Self-citationNeuronal Matrix Metalloproteinase-9 Is a Determinant of Selective Neurodegeneration
Kaplan, A., Spiller, K. J., Towne, C. L., Kanning, K. C., Choe, G. T., Geber, A. B., Akay, T., Aebischer, P., & Henderson, C. E. (2014) · Neuron · doi:10.1016/j.neuron.2013.12.009 · Cited by 309 · see citing works
Kim, I.-J., Zhang, Y., Meister, M., & Sanes, J. R. (2010) · Journal of Neuroscience · doi:10.1523/jneurosci.4779-09.2010 · Cited by 282 · see citing works
Self-citationDigital Museum of Retinal Ganglion Cells with Dense Anatomy and Physiology
Bae, J. A., Mu, S., Kim, J. S., Turner, N. L., Tartavull, I., Kemnitz, N., Jordan, C. S., Norton, A. D., Silversmith, W. M., Prentki, R., et al. (2018) · Cell · doi:10.1016/j.cell.2018.04.040 · Cited by 263 · see citing works
Santina, L. D., Inman, D. M., Lupien, C. B., Horner, P. J., & Wong, R. (2013) · Journal of Neuroscience · doi:10.1523/jneurosci.5461-12.2013 · Cited by 260 · see citing works
Matrix metalloproteinases and their endogenous inhibitors in neuronal physiology of the adult brain
Dzwonek, J., Rylski, M., & Kaczmarek, L. (2004) · FEBS Letters · doi:10.1016/j.febslet.2004.03.070 · Cited by 256 · see citing works
Melanopsin-Positive Intrinsically Photosensitive Retinal Ganglion Cells: From Form to Function
Schmidt, T. M., Do, M. T. H., Dacey, D. M., Lucas, R. J., Hattar, S. S., & Matynia, A. (2011) · Journal of Neuroscience · doi:10.1523/jneurosci.4132-11.2011 · Cited by 255 · see citing works
Injury-Induced Decline of Intrinsic Regenerative Ability Revealed by Quantitative Proteomics
Belin, S., Nawabi, H., Wang, C., Tang, S., Latrémolière, A., Warren, P. G., Schorle, H., Uncu, C., Woolf, C. J., He, Z., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.03.060 · Cited by 250 · see citing works
Self-citationBleckert, A., Schwartz, G. W., Turner, M. H., Rieke, F., & Wong, R. O. L. (2014) · Current Biology · doi:10.1016/j.cub.2013.12.020 · Cited by 244 · see citing works
Four alpha ganglion cell types in mouse retina: Function, structure, and molecular signatures
Krieger, B. M., Qiao, M., Rousso, D. L., Sanes, J. R., & Meister, M. (2017) · PLoS ONE · doi:10.1371/journal.pone.0180091 · Cited by 242 · see citing works
Self-citationReaching the brain: Advances in optic nerve regeneration
Benowitz, L. I., He, Z., & Goldberg, J. L. (2015) · Experimental Neurology · doi:10.1016/j.expneurol.2015.12.015 · Cited by 223 · see citing works
Self-citationSox11 Expression Promotes Regeneration of Some Retinal Ganglion Cell Types but Kills Others
Norsworthy, M. W., Bei, F., Kawaguchi, R., Wang, Q., Tran, N. M., Li, Y., Brommer, B., Zhang, Y., Wang, C., Sanes, J. R., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.05.035 · Cited by 215 · see citing works
Self-citationAn Adverse Role for Matrix Metalloproteinase 12 after Spinal Cord Injury in Mice
Wells, J. E. A., Rice, T. K., Nuttall, R. K., Edwards, D. R., Zekki, H., Rivest, S., & Yong, V. W. (2003) · Journal of Neuroscience · doi:10.1523/jneurosci.23-31-10107.2003 · Cited by 203 · see citing works
Aguayo, A. J., Rasminsky, M., Bray, G. M., et al. (1991) · Philosophical Transactions of the Royal Society B Biological Sciences · doi:10.1098/rstb.1991.0025 · Cited by 197 · see citing works
Age-related alterations in neurons of the mouse retina
Samuel, M. A., Zhang, Y., Meister, M., & Sanes, J. R. (2011) · The Journal of Neuroscience · doi:10.1523/jneurosci.3580-11.2011 · Cited by 184 · see citing works
Self-citationCorticotropin-releasing hormone-binding protein: biochemistry and function from fishes to mammals
Af, S., Valverde, R., & Denver, R. J. (2002) · Journal of Endocrinology · doi:10.1677/joe.0.1750089 · Cited by 174 · see citing works
Rousso, D. L., Qiao, M., Kagan, R. D., Yamagata, M., Palmiter, R. D., & Sanes, J. R. (2016) · Cell Reports · doi:10.1016/j.celrep.2016.04.069 · Cited by 172 · see citing works
Self-citationA method for single-neuron chronic recording from the retina in awake mice
Hong, G., Tian-ming Fu, B., Qiao, M., Viveros, R. D., Yang, X., Zhou, T., Lee, J. M., Park, H., Sanes, J. R., & Lieber, C. M. (2018) · Science · doi:10.1126/science.aas9160 · Cited by 172 · see citing works
Self-citationSidekick 2 directs formation of a retinal circuit that detects differential motion
Krishnaswamy, A., Yamagata, M., Duan, X., Hong, Y. K., & Sanes, J. R. (2015) · Nature · doi:10.1038/nature14682 · Cited by 162 · see citing works
Self-citationGalindo‐Romero, C., Avilés‐Trigueros, M., Jiménez-López, M., Valiente‐Soriano, F. J., Salinas‐Navarro, M., Nadal-Nicolás, F. M., Villegas‐Pérez, M. P., Vidal‐Sanz, M., & Agudo‐Barriuso, M. (2011) · Experimental Eye Research · doi:10.1016/j.exer.2011.02.008 · Cited by 156 · see citing works
Thrombospondin-1 Mediates Axon Regeneration in Retinal Ganglion Cells
Bray, E. R., Yungher, B. J., Levay, K., Ribeiro, M., Dvoryanchikov, G. A., Ayupe, A. C., Thakor, K., Marks, V. S., Randolph, M. J., Danzi, M. C., et al. (2019) · Neuron · doi:10.1016/j.neuron.2019.05.044 · Cited by 156 · see citing works
The M6 cell: A small‐field bistratified photosensitive retinal ganglion cell
Quattrochi, L. E., Stabio, M. E., Kim, I., Ilardi, M. C., Fogerson, P. M., Leyrer, M. L., & Berson, D. M. (2018) · The Journal of Comparative Neurology · doi:10.1002/cne.24556 · Cited by 154 · see citing works
Thompson, M. A., & Ziff, E. B. (1989) · Neuron · doi:10.1016/0896-6273(89)90228-6 · Cited by 144 · see citing works
Pandey, S., Shekhar, K., Regev, A., & Schier, A. F. (2018) · Current Biology · doi:10.1016/j.cub.2018.02.040 · Cited by 144 · see citing works
Self-citationBhlhb5 and Prdm8 form a repressor complex involved in neuronal circuit assembly
Ross, S. E., McCord, A. E., Jung, C., Atan, D., Mok, S. I., Hemberg, M., Kim, T.-K., Salogiannis, J., Hu, L., Cohen, S., et al. (2012) · Neuron · doi:10.1016/j.neuron.2011.09.035 · Cited by 137 · see citing works
Pedersen, W. A., Wan, R., Zhang, P., & Mattson, M. P. (2002) · Journal of Neuroscience · doi:10.1523/jneurosci.22-02-00404.2002 · Cited by 135 · see citing works
Elevating Growth Factor Responsiveness and Axon Regeneration by Modulating Presynaptic Inputs
Zhang, Y., Williams, P. R., Jacobi, A., Wang, C., Goel, A., Hirano, A. A., Brecha, N. C., Kerschensteiner, D., & He, Z. (2019) · Neuron · doi:10.1016/j.neuron.2019.04.033 · Cited by 130 · see citing works
Self-citationPromoting axon regeneration in the adult CNS by modulation of the melanopsin/GPCR signaling
Li, S., Yang, C., Zhang, L., Gao, X., Wang, X., Liu, W., Wang, Y., Jiang, S., Wong, Y. H., Zhang, Y., et al. (2016) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1523645113 · Cited by 129 · see citing works
Hong, G., Tian-ming Fu, B., Zhou, T., Schuhmann, T. G., Huang, J., & Lieber, C. M. (2015) · Nano Letters · doi:10.1021/acs.nanolett.5b02987 · Cited by 128 · see citing works
Self-citationAAV-mediated CRISPR/cas gene editing of retinal cells in vivo
Hung, S. S. C., Chrysostomou, V., Li, F., Lim, J. K. H., Wang, J.-H., Powell, J. E., Tu, L., Daniszewski, M., Lo, C., Wong, R. C., et al. (2016) · Investigative Opthalmology & Visual Science · doi:10.1167/iovs.16-19316 · Cited by 125 · see citing works
Agostinone, J., Alarcon-Martinez, L., Gamlin, C., Yu, W.-Q., Wong, R. O. L., & Di Polo, A. (2018) · Brain · doi:10.1093/brain/awy142 · Cited by 124 · see citing works
The M5 Cell: A Color-Opponent Intrinsically Photosensitive Retinal Ganglion Cell
Stabio, M. E., Sabbah, S., Quattrochi, L. E., Ilardi, M. C., Fogerson, P. M., Leyrer, M. L., Kim, M. T., Kim, I., Schiel, M., Renna, J. M., et al. (2017) · Neuron · doi:10.1016/j.neuron.2017.11.030 · Cited by 120 · see citing works
Systematic comparative analysis of single cell RNA-sequencing methodsPreprint
Ding, J., Adiconis, X., Simmons, S., Kowalczyk, M. S., Hession, C. C., Marjanovic, N. D., Hughes, T. K., Wadsworth, M. H., Burks, T., Nguyễn, L., et al. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/632216 · Cited by 106 · see citing works
Self-citationMüller, L. P. D. S., Sargoy, A., Rodriguez, A. R., & Brecha, N. C. (2014) · PLoS ONE · doi:10.1371/journal.pone.0093274 · Cited by 98 · see citing works
Dupraz, S., Grassi, D., Karnas, D., Guil, A. F. N., Hicks, D., & Quiroga, S. (2013) · PLoS ONE · doi:10.1371/journal.pone.0054462 · Cited by 78 · see citing works
Dendritic changes in visual pathways in glaucoma and other neurodegenerative conditions
Liu, M., Duggan, J., Salt, T. E., & Cordeiro, M. F. (2011) · Experimental Eye Research · doi:10.1016/j.exer.2011.01.014 · Cited by 78 · see citing works
Welin, D., Novikova, L. N., Wiberg, M., et al. (2007) · Experimental Brain Research · doi:10.1007/s00221-007-1232-5 · Cited by 74 · see citing works
Kuang, X., Zhao, X., Xu, H.-F., et al. (2010) · BMC Neuroscience · doi:10.1186/1471-2202-11-137 · Cited by 74 · see citing works
Tbr1 instructs laminar patterning of retinal ganglion cell dendrites
Liu, J., Reggiani, J. D. S., Laboulaye, M. A., Pandey, S., Chen, B., Rubenstein, J. L. R., Krishnaswamy, A., & Sanes, J. R. (2018) · Nature Neuroscience · doi:10.1038/s41593-018-0127-z · Cited by 71 · see citing works
Self-citationHicks, D. (2011) · Graefe s Archive for Clinical and Experimental Ophthalmology · doi:10.1007/s00417-011-1631-y · Cited by 68 · see citing works
Ambidextrous binding of cell and membrane bilayers by soluble matrix metalloproteinase-12
Koppisetti, R. K., Fulcher, Y. G., Jurkevich, A., Prior, S. H., Xu, J., Lenoir, M., Overduin, M., & Doren, S. R. V. (2014) · Nature Communications · doi:10.1038/ncomms6552 · Cited by 55 · see citing works
Laboulaye, M. A., Duan, X., Qiao, M., Whitney, I. E., & Sanes, J. R. (2018) · Frontiers in Molecular Neuroscience · doi:10.3389/fnmol.2018.00385 · Cited by 53 · see citing works
Self-citationMagnoni, S., Baker, A. H., Thomson, S. R., et al. (2007) · Gene Therapy · doi:10.1038/sj.gt.3302894 · Cited by 42 · see citing works
Abuirmeileh, A. N., Lever, R., Kingsbury, A. E., Lees, A. J., Locke, I. C., Knight, R. A., Chowdrey, H. S., Biggs, C. S., & Whitton, P. S. (2007) · European Journal of Neuroscience · doi:10.1111/j.1460-9568.2007.05653.x · Cited by 39 · see citing works
Transcriptomic Signatures of Postnatal and Adult Intrinsically Photosensitive Ganglion Cells
Berg, D. J., Kartheiser, K., Leyrer, M. L., Saali, A., & Berson, D. M. (2019) · eNeuro · doi:10.1523/eneuro.0022-19.2019 · Cited by 30 · see citing works
Steencken, A. C., Smirnov, I., & Stelzner, D. J. (2011) · Neuroscience · doi:10.1016/j.neuroscience.2011.05.052 · Cited by 24 · see citing works
Huang, H., Lin, S., Chen, W.-F., Li, K.-W., Kuo, J., & Wang, M.-J. (2009) · Neurobiology of Aging · doi:10.1016/j.neurobiolaging.2009.09.010 · Cited by 19 · see citing works
MacLaren, R. E., & Taylor, J. S. H. (1997) · Progress in Neurobiology · doi:10.1016/s0301-0082(97)00041-5 · Cited by 17 · see citing works
Vinet, J., Costa, A., Salinas‐Navarro, M., Leo, G., Moons, L., Arckens, L., & Biagini, G. (2018) · International Journal of Molecular Sciences · doi:10.3390/ijms19082178 · Cited by 16 · see citing works
McLean, J. R., Smith, G. A., Rocha, E. M., Osborn, T. M., Dib, S., Hayes, M. A., Beagan, J. A., Brown, T. B., Lawson, T., Hallett, P. J., et al. (2014) · Experimental Neurology · doi:10.1016/j.expneurol.2014.05.024 · Cited by 10 · see citing works
Flagged first, then by citations
Research works printed but not linked: 1
- Chen T, and Guestrin C (2016). Xgboost: A scalable tree boosting system. Paper presented at: Proceedings of the 22nd acm sigkdd international conference on knowledge discovery and data mining (ACM).
Cited by
Sorted by citations
Confronting false discoveries in single-cell differential expression
Squair, J. W., Gautier, M., Kathe, C., Anderson, M. A., James, N. D., Hutson, T. H., Hudelle, R., Qaiser, T., Matson, K. J. E., Barraud, Q., et al. (2021) · doi:10.1101/2021.03.12.435024 · Cited by 1,017 · see citing works
Neurotoxic Reactive Astrocytes Drive Neuronal Death after Retinal Injury
Guttenplan, K. A., Stafford, B. K., El-Danaf, R. N., Adler, D. I., Münch, A. E., Weigel, M. K., Huberman, A. D., & Liddelow, S. A. (2020) · Cell Reports · doi:10.1016/j.celrep.2020.107776 · Cited by 221 · see citing works
Analytic Pearson residuals for normalization of single-cell RNA-seq UMI data
Lause, J., Berens, P., & Kobak, D. (2021) · Genome Biology · doi:10.1186/s13059-021-02451-7 · Cited by 195 · see citing works
Intrinsically photosensitive retinal ganglion cells of the human retina
Mure, L. S. (2021) · Frontiers in Neurology · doi:10.3389/fneur.2021.636330 · Cited by 151 · see citing works
Belforte, N., Agostinone, J., Alarcon-Martinez, L., Villafranca-Baughman, D., Dotigny, F., Cueva Vargas, J. L., & Di Polo, A. (2021) · Molecular Neurodegeneration · doi:10.1186/s13024-021-00466-z · Cited by 67 · see citing works
“Of interest, a comprehensive molecular atlas of 46 RGC subtypes in the adult retina generated by single-cell RNA-seq [58] shows that Prkaa1 expression is found in many RGC subtypes including αON sustained and transient, αOFF sustained and transient, melanopsin-positive (M1, M2 and M5), and ON-OFF direction selective R…”
BackgroundShekhar, K., Whitney, I. E., Butrus, S., Peng, Y.-R., & Sanes, J. R. (2022) · eLife · doi:10.7554/elife.73809 · Cited by 68 · see citing works
Human retinal model systems: Strengths, weaknesses, and future directions
Eldred, K. C., & Reh, T. A. (2021) · Developmental Biology · doi:10.1016/j.ydbio.2021.09.001 · Cited by 41 · see citing works
Violet Light Modulates the Central Nervous System to Regulate Memory and Mood
Sasaki, N., Gusain, P., Hayano, M., Sugaya, T., Tonegawa, N., Hatanaka, Y., Tamura, R., Okuyama, K., Osada, H., Ban, N., et al. (2021) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2021.11.02.466604 · Cited by 5 · see citing works
Progress in single-cell sequencing of retinal vein occlusion or ischemic hypoxic retinopathy
Feng, Y., Wu, Y., Zhu, Y., He, Y., & Weng, W. (2025) · Experimental Eye Research · doi:10.1016/j.exer.2025.110436 · Cited by 3 · see citing works
- Authors
- Tran, N. M., Shekhar, K., Whitney, I. E., Jacobi, A., Benhar, I., Hong, G., Yan, W., Adiconis, X., Arnold, M. E., Lee, J. M., Levin, J. Z., Lin, D., Wang, C., Lieber, C. M., Regev, A., He, Z., & Sanes, J. R.
- Affiliations
- Harvard University (US)
- Broad Institute (US)
- Boston Children's Hospital (US)
- Corresponding author
- Sanes, Joshua R.
- ORCID
- Venue
- Neuron
- Publisher
- Elsevier BV
- Published
- 2019-12
- Volume
- 104
- Issue
- 6
- Pages
- 1039-1055.e12
- ISSN
- 0896-6273 (ISSN-L)
- PMC
- PMC6923571
- OpenAlex
- W2990382732
- Cited by
- 627
- References
- 98
- Citations by year
- 2026: 79 · 2025: 92 · 2024: 96 · 2023: 105 · 2022: 101 · 2021: 101 · 2020: 47 · 2019: 4
- FWCI
- 62.07
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Licence
- Locations
- Neuron (publishedVersion)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- DSpace@MIT (Massachusetts Institute of Technology) (submittedVersion, cc-by-nc-nd)
- eScholarship (California Digital Library) (submittedVersion, cc-by-nc-nd)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- Biogen
- National Institutes of Health
- Topics
- Health Sciences › Medicine › Ophthalmology › Glaucoma and retinal disorders
- Life Sciences › Neuroscience › Cellular and Molecular Neuroscience › Nerve injury and regeneration
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Keywords
- retinal ganglion cells, optic nerve crush, neuroprotection, axon regeneration, single-cell transcriptomics, neurodegeneration
- MeSH terms
- Neuroprotection, Animals, Cell Survival, Female, Male, Nerve Crush, Nerve Regeneration, Retinal Ganglion Cells, Mice
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review
