Cell-type-specific nuclei purification from whole animals for genome-wide expression and chromatin profiling
Open accessAbstract
An understanding of developmental processes requires knowledge of transcriptional and epigenetic landscapes at the level of tissues and ultimately individual cells. However, obtaining tissue- or cell-type-specific expression and chromatin profiles for animals has been challenging. Here we describe a method for purifying nuclei from specific cell types of animal models that allows simultaneous determination of both expression and chromatin profiles. The method is based on in vivo biotin-labeling of the nuclear envelope and subsequent affinity purification of nuclei. We describe the use of the method to isolate nuclei from muscle of adult Caenorhabditis elegans and from mesoderm of Drosophila melanogaster embryos. As a case study, we determined expression and nucleosome occupancy profiles for affinity-purified nuclei from C. elegans muscle. We identified hundreds of genes that are specifically expressed in muscle tissues and found that these genes are depleted of nucleosomes at promoters and gene bodies in muscle relative to other tissues. This method should be universally applicable to all model systems that allow transgenesis and will make it possible to determine epigenetic and expression profiles of different tissues and cell types.
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?
Purification of a homogeneous population of fluorescently tagged nuclei in animal models has demonstrated six-fold increased sensitivity for cell-type specific identification of down-regulated genes.
“Purification of a homogeneous population of fluorescently tagged nuclei in animal models has also demonstrated six-fold increased sensitivity for cell-type specific identification of down-regulated genes51.”
From Neuron Enriched Nuclear Proteome Isolated from Human Brain (2013) · cites this paper as [51]
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
Analysis of Relative Gene Expression Data Using Real-Time Quantitative PCR and the 2−ΔΔCT Method
Livak, K. J., & Schmittgen, T. D. (2001) · Methods · doi:10.1006/meth.2001.1262 · Cited by 180,860 · see citing works
Gene Ontology: tool for the unification of biology
Ashburner, M., Ball, C. A., Blake, J. A., Botstein, D., Butler, H., Cherry, J. M., Davis, A. P., Dolinski, K., Dwight, S. S., Eppig, J. T., et al. (2000) · Nature Genetics · doi:10.1038/75556 · Cited by 43,206 · see citing works
Targeted gene expression as a means of altering cell fates and generating dominant phenotypes
Brand, A. H., & Perrimon, N. (1993) · Development · doi:10.1242/dev.118.2.401 · Cited by 9,510 · see citing works
The embryonic cell lineage of the nematode Caenorhabditis elegans
Sulston, J. E., Schierenberg, E., White, J. G., & Thomson, J. N. (1983) · Developmental Biology · doi:10.1016/0012-1606(83)90201-4 · Cited by 4,199 · see citing works
Post-embryonic cell lineages of the nematode, Caenorhabditis elegans
Sulston, J. E., & Horvitz, H. R. (1977) · Developmental Biology · doi:10.1016/0012-1606(77)90158-0 · Cited by 3,479 · see citing works
The positive false discovery rate: a Bayesian interpretation and the q-value
Storey, J. D. (2003) · The Annals of Statistics · doi:10.1214/aos/1074290335 · Cited by 2,204 · see citing works
Baldi, P., & Long, A. D. (2001) · Bioinformatics · doi:10.1093/bioinformatics/17.6.509 · Cited by 1,622 · see citing works
Chromatin signatures of pluripotent cell lines
Azuara, V., Perry, P., Sauer, S., Spivakov, M., Jørgensen, H. F., John, R. M., Gouti, M., Casanova, M., Warnes, G., Merkenschlager, M., et al. (2006) · Nature Cell Biology · doi:10.1038/ncb1403 · Cited by 1,357 · see citing works
Mahajan, R. K., Delphin, C., Guan, T., Gerace, L., & Melchior, F. (1997) · Cell · doi:10.1016/s0092-8674(00)81862-0 · Cited by 1,258 · see citing works
A high-resolution atlas of nucleosome occupancy in yeast
Lee, W., Tillo, D., Bray, N., Morse, R. H., Davis, R. W., Hughes, T. R., & Nislow, C. (2007) · Nature Genetics · doi:10.1038/ng2117 · Cited by 829 · see citing works
Creation of Low-Copy Integrated Transgenic Lines in Caenorhabditis elegans
Praitis, V., Casey, E., Collar, D. C., & Austin, J. (2001) · Genetics · doi:10.1093/genetics/157.3.1217 · Cited by 817 · see citing works
Evidence for nucleosome depletion at active regulatory regions genome-wide
Lee, C.-K., Shibata, Y., Rao, B., Strahl, B. D., & Lieb, J. D. (2004) · Nature Genetics · doi:10.1038/ng1400 · Cited by 738 · see citing works
GENECODIS: a web-based tool for finding significant concurrent annotations in gene lists
Carmona‐Sáez, P., Chagoyen, M., Tirado, F., Carazo, J. M., & Pascual-Montano, A. (2007) · Genome biology · doi:10.1186/gb-2007-8-1-r3 · Cited by 591 · see citing works
Cell shape changes during gastrulation in Drosophila
Leptin, M., & Grunewald, B. (1990) · Development · doi:10.1242/dev.110.1.73 · Cited by 542 · see citing works
Genome-scale profiling of histone H3.3 replacement patterns
Mito, Y., Henikoff, J. G., & Henikoff, S. (2005) · Nature Genetics · doi:10.1038/ng1637 · Cited by 511 · see citing works
Self-citationThisse, B., Stoetzel, C., Thisse, C., & Perrin‐Schmitt, F. (1988) · The EMBO Journal · doi:10.1002/j.1460-2075.1988.tb03056.x · Cited by 470 · see citing works
Chromosomal clustering of muscle-expressed genes in Caenorhabditis elegans
Roy, P. J., Stuart, J. M., Lund, J., & Kim, S. K. (2002) · Nature · doi:10.1038/nature01012 · Cited by 439 · see citing works
Nogales‐Cadenas, R., Carmona‐Sáez, P., Vázquez, M., Vicente, C., Yang, X., Tirado, F., Carazo, J. M., & Pascual-Montano, A. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp416 · Cited by 438 · see citing works
Ultrastructural patterns of RNA synthesis during early embryogenesis of drosophila melanogaster
McKnight, S. L., & Miller Jr., O. L. (1976) · Cell · doi:10.1016/0092-8674(76)90014-3 · Cited by 400 · see citing works
Deal, R. B., & Henikoff, S. (2010) · Nature Protocols · doi:10.1038/nprot.2010.175 · Cited by 387 · see citing works
Self-citationA Simple Method for Gene Expression and Chromatin Profiling of Individual Cell Types within a Tissue
Deal, R. B., & Henikoff, S. (2010) · Developmental Cell · doi:10.1016/j.devcel.2010.05.013 · Cited by 379 · see citing works
Self-citationStructure, dynamics and function of nuclear pore complexes
D’Angelo, M. A., & Hetzer, M. W. (2008) · Trends in Cell Biology · doi:10.1016/j.tcb.2008.07.009 · Cited by 377 · see citing works
Global nucleosome occupancy in yeast
Bernstein, B., Liu, C. L., Humphrey, E. L., Perlstein, E. O., & Schreiber, S. L. (2004) · Genome biology · doi:10.1186/gb-2004-5-9-r62 · Cited by 356 · see citing works
McGhee, J. D. (2007) · WormBook · doi:10.1895/wormbook.1.133.1 · Cited by 344 · see citing works
Rapid, Transcription-Independent Loss of Nucleosomes over a Large Chromatin Domain at Hsp70 Loci
Petesch, S. J., & Lis, J. T. (2008) · Cell · doi:10.1016/j.cell.2008.05.029 · Cited by 319 · see citing works
Patterns of Gene Expression During Drosophila Mesoderm Development
Furlong, E., Andersen, E. C., Null, B. H., White, K., & Scott, M. (2001) · Science · doi:10.1126/science.1062660 · Cited by 286 · see citing works
Sequence-specific transactivation of the Drosophila twist gene by the dorsal gene product
Thisse, C., Perrin‐Schmitt, F., Stoetzel, C., & Thisse, B. (1991) · Cell · doi:10.1016/0092-8674(91)90014-p · Cited by 235 · see citing works
Genome-wide profiling of salt fractions maps physical properties of chromatinPreprint
Henikoff, S., Henikoff, J. G., Sakai, A., Loeb, G. B., & Ahmad, K. (2008) · Genome Research · doi:10.1101/gr.087619.108 · Cited by 227 · see citing works
Self-citationTU-tagging: cell type–specific RNA isolation from intact complex tissues
Miller, M. R., Robinson, K. J., Cleary, M. D., & Doe, C. Q. (2009) · Nature Methods · doi:10.1038/nmeth.1329 · Cited by 176 · see citing works
Epigenetic inheritance of cell differentiation status
Ng, R. K., & Gurdon, J. B. (2008) · Cell Cycle · doi:10.4161/cc.7.9.5791 · Cited by 166 · see citing works
Sarcomere assembly in C. elegans muscle
Moerman, D. (2006) · WormBook · doi:10.1895/wormbook.1.81.1 · Cited by 143 · see citing works
Stetina, S. E. V., Watson, J. D., Fox, R. M., Olszewski, K. L., Spencer, W. C., Roy, P. J., & Miller, D. M. (2007) · Genome biology · doi:10.1186/gb-2007-8-7-r135 · Cited by 124 · see citing works
Histone H3.3 Variant Dynamics in the Germline of Caenorhabditis elegans
Ooi, S. L., Priess, J. R., & Henikoff, S. (2006) · PLoS Genetics · doi:10.1371/journal.pgen.0020097 · Cited by 120 · see citing works
Self-citationWaterston, R. (1989) · The EMBO Journal · doi:10.1002/j.1460-2075.1989.tb08507.x · Cited by 118 · see citing works
The Nuclear Pore Protein AtTPR Is Required for RNA Homeostasis, Flowering Time, and Auxin Signaling
Jacob, Y., Mongkolsiriwatana, C., Veley, K. M., Kim, S. Y., & Michaels, S. D. (2007) · PLANT PHYSIOLOGY · doi:10.1104/pp.107.100735 · Cited by 109 · see citing works
The morphogenesis of the zebrafish eye, including a fate map of the optic vesicle
Li, Z., Joseph, N. M., & Easter, S. S. (2000) · Developmental Dynamics · doi:10.1002/(sici)1097-0177(200005)218:1 · Cited by 106 · see citing works
Fukushige, T., Brodigan, T. M., Schriefer, L. A., Waterston, R., & Krause, M. (2006) · Genes & Development · doi:10.1101/gad.1481706 · Cited by 104 · see citing works
Introduction to C. elegansPreprint
Riddle, D. L., Blumenthal, T., Meyer, B. J., & Priess, J. R. (1997) · Cold Spring Harbor Monograph Archive · doi:10.1101/087969532.33.1 · Cited by 99 · see citing works
Large-scale sorting of C. elegans embryos reveals the dynamics of small RNA expression
Stoeckius, M., Maaskola, J., Colombo, T., Rahn, H.-P., Friedländer, M. R., Li, N., Chen, W., Piano, F., & Rajewsky, N. (2009) · Nature Methods · doi:10.1038/nmeth.1370 · Cited by 92 · see citing works
Barthelson, R. A., Lambert, G. M., Vanier, C. H., Lynch, R. M., & Galbraith, D. W. (2007) · BMC Genomics · doi:10.1186/1471-2164-8-340 · Cited by 91 · see citing works
The embryonic muscle transcriptome of Caenorhabditis elegans
Fox, R. M., Watson, J. D., Stetina, S. E. V., McDermott, J. B., Brodigan, T. M., Fukushige, T., Krause, M., & Miller, D. M. (2007) · Genome biology · doi:10.1186/gb-2007-8-9-r188 · Cited by 88 · see citing works
Nuclear Mislocalization of Enzymatically Active RanGAP Causes Segregation Distortion in Drosophila
Kusano, A., Staber, C. J., & Ganetzky, B. (2001) · Developmental Cell · doi:10.1016/s1534-5807(01)00042-9 · Cited by 79 · see citing works
Baugh, L. R., Wen, J. C., Hill, A. A. V., Slonim, D. K., Brown, E. L., & Hunter, C. P. (2005) · Genome biology · doi:10.1186/gb-2005-6-5-r45 · Cited by 66 · see citing works
A native chromatin purification system for epigenomic profiling in Caenorhabditis elegans
Ooi, S. L., Henikoff, J. G., & Henikoff, S. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkp1090 · Cited by 58 · see citing works
Self-citationHistone variants and epigenetic inheritance
Yuan, G., & Zhu, B. (2011) · Biochimica et Biophysica Acta (BBA) - Gene Regulatory Mechanisms · doi:10.1016/j.bbagrm.2011.06.007 · Cited by 44 · see citing works
A role for Phospholipase D in Drosophilaembryonic cellularization
LaLonde, M. M., Janssens, H., Yun, S., Crosby, J. A., Redina, O. E., Olive, V., Altshuller, Y. M., Choi, S., Du, G., Gergen, J. P., et al. (2006) · BMC Developmental Biology · doi:10.1186/1471-213x-6-60 · Cited by 32 · see citing works
Going green: plants' alternative way to position the Ran gradient
Meier, I., Xu, X., Brkljacić, J., Zhao, Q. L., & Wang, H.-J. (2008) · Journal of Microscopy · doi:10.1111/j.1365-2818.2008.02038.x · Cited by 16 · see citing works
Burgemeister, R. (2011) · Methods in molecular biology · doi:10.1007/978-1-61779-055-3_7 · Cited by 14 · see citing works
[24] Gene Discovery with laser Capture Microscopy
Neira, M., & Azen, E. A. (2002) · Methods in enzymology on CD-ROM/Methods in enzymology · doi:10.1016/s0076-6879(02)56941-x · Cited by 8 · see citing works
Baculovirus-encoded protein expression for epigenomic profiling in Drosophila cells
Bryson, T. D., Weber, C. M., & Henikoff, S. (2010) · Fly · doi:10.4161/fly.4.3.12177 · Cited by 6 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Transcriptional enhancers: from properties to genome-wide predictions
Shlyueva, D., Stampfel, G., & Stark, A. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3682 · Cited by 1,356 · see citing works
Epigenomic Signatures of Neuronal Diversity in the Mammalian Brain
Mo, A., Mukamel, E. A., Davis, F. P., Luo, C., Henry, G. L., Picard, S., Urich, M. A., Nery, J. R., Sejnowski, T. J., Lister, R., et al. (2015) · Neuron · doi:10.1016/j.neuron.2015.05.018 · Cited by 739 · see citing works
Chromatin accessibility profiling by ATAC-seq
Grandi, F. C., Modi, H., Kampman, L., & Corces, M. R. (2022) · Nature Protocols · doi:10.1038/s41596-022-00692-9 · Cited by 557 · see citing works
Site-Specific Biotinylation of Purified Proteins Using BirA
Fairhead, M., & Howarth, M. R. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-2272-7_12 · Cited by 405 · see citing works
The Drosophila embryo at single-cell transcriptome resolution
Karaiskos, N., Wahle, P., Alles, J., Boltengagen, A., Ayoub, S., Kipar, C., Kocks, C., Rajewsky, N., & Zinzen, R. P. (2017) · Science · doi:10.1126/science.aan3235 · Cited by 371 · see citing works
Southall, T. D., Gold, K. S., Egger, B., Davidson, C. M., Caygill, E. E., Marshall, O. J., & Brand, A. H. (2013) · Developmental Cell · doi:10.1016/j.devcel.2013.05.020 · Cited by 257 · see citing works
An expanded auxin-inducible degron toolkit for Caenorhabditis elegans
Ashley, G. E., Duong, T., Levenson, M. T., Martinez, M. A. Q., Johnson, L. C., Hibshman, J. D., Saeger, H. N., Palmisano, N. J., Doonan, R., Martínez-Méndez, R., et al. (2021) · Genetics · doi:10.1093/genetics/iyab006 · Cited by 156 · see citing works
Marshall, O. J., Southall, T. D., Cheetham, S. W., & Brand, A. H. (2016) · Nature Protocols · doi:10.1038/nprot.2016.084 · Cited by 157 · see citing works
Roh, H. C., Tsai, L. T.-Y., Lyubetskaya, A., Tenen, D. E., Kumari, M., & Rosen, E. D. (2017) · Cell Reports · doi:10.1016/j.celrep.2016.12.087 · Cited by 150 · see citing works
Deciphering the functions and regulation of brain-enriched A-to-I RNA editing
Li, J. B., & Church, G. M. (2013) · Nature Neuroscience · doi:10.1038/nn.3539 · Cited by 141 · see citing works
Cell type–specific genomics of Drosophila neurons
Henry, G. L., Davis, F. P., Picard, S., & Eddy, S. R. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks671 · Cited by 139 · see citing works
High-resolution digital profiling of the epigenome
Zentner, G. E., & Henikoff, S. (2014) · Nature Reviews Genetics · doi:10.1038/nrg3798 · Cited by 125 · see citing works
Self-citationH3K27 modifications define segmental regulatory domains in the Drosophila bithorax complex
Bowman, S., Deaton, A. M., Domingues, H. G., Wang, P. I., Sadreyev, R. I., Kingston, R. E., & Bender, W. W. (2014) · eLife · doi:10.7554/elife.02833 · Cited by 122 · see citing works
Holocentromeres are dispersed point centromeres localized at transcription factor hotspots
Steiner, F. A., & Henikoff, S. (2014) · eLife · doi:10.7554/elife.02025 · Cited by 117 · see citing works
Self-citationRNA Polymerase II transcription elongation and Pol II CTD Ser2 phosphorylation
Bowman, E. A., & Kelly, W. G. (2014) · Nucleus · doi:10.4161/nucl.29347 · Cited by 108 · see citing works
Isolation of Specific Neurons from C. elegans Larvae for Gene Expression Profiling
Spencer, W. C., McWhirter, R. D., Miller‐Fleming, T. W., Strasbourger, P., Thompson, O. A., Hillier, L., Waterston, R., & Miller, D. M. (2014) · PLoS ONE · doi:10.1371/journal.pone.0112102 · Cited by 102 · see citing works
Chen, R. A.-J., Downand, T. A., Stempor, P., Chen, Q. B., Egelhofer, T. A., Hillier, L. W., Jeffers, T. E., & Ahringer, J. (2013) · Genome Research · doi:10.1101/gr.153668.112 · Cited by 93 · see citing works
Widiez, T., Symeonidi, A., Luo, C., Lam, E., Lawton, M., & Rensing, S. A. (2014) · The Plant Journal · doi:10.1111/tpj.12542 · Cited by 87 · see citing works
Cell type–specific chromatin immunoprecipitation from multicellular complex samples using BiTS-ChIP
Bonn, S., Zinzen, R. P., Perez‐Gonzalez, A., Riddell, A., Gavin, A., & Furlong, E. E. M. (2012) · Nature Protocols · doi:10.1038/nprot.2012.049 · Cited by 88 · see citing works
FACT Sets a Barrier for Cell Fate Reprogramming in Caenorhabditis elegans and Human Cells
Kolundžić, E., Ofenbauer, A., Bulut, S., Uyar, B., Baytek, G., Sommermeier, A., Seelk, S., He, M., Hirsekorn, A., Vučićević, D., et al. (2018) · Developmental Cell · doi:10.1016/j.devcel.2018.07.006 · Cited by 83 · see citing works
Hall, H., Medina, P., Cooper, D. A., Escobedo, S. E., Rounds, J., Brennan, K., Vincent, C., Miura, P., Doerge, R. W., & Weake, V. M. (2017) · BMC Genomics · doi:10.1186/s12864-017-4304-3 · Cited by 82 · see citing works
Blazie, S. M., Babb, C. S., Wilky, H., Rawls, A., Park, J. G., & Mangone, M. (2015) · BMC Biology · doi:10.1186/s12915-015-0116-6 · Cited by 79 · see citing works
Transcriptome dynamics revealed by a gene expression atlas of the early Arabidopsis embryo
Palovaara, J., Saiga, S., Wendrich, J. R., Hofland, N. V. ‘. W., van Schayck, J. P., Hater, F., Mutte, S. K., Sjollema, J., Boekschoten, M. V., Hooiveld, G. J. E. J., et al. (2017) · Nature Plants · doi:10.1038/s41477-017-0035-3 · Cited by 75 · see citing works
Haenni, S., Ji, Z., Hoque, M., Rust, N., Sharpe, H., Eberhard, R., Browne, C., Hengartner, M. O., Mellor, J., Tian, B., et al. (2012) · Nucleic Acids Research · doi:10.1093/nar/gks282 · Cited by 71 · see citing works
Young genes have distinct gene structure, epigenetic profiles, and transcriptional regulationPreprint
Werner, M. S., Sieriebriennikov, B., Prabh, N., Loschko, T., Lanz, C., & Sommer, R. J. (2018) · Genome Research · doi:10.1101/gr.234872.118 · Cited by 67 · see citing works
Neuron Enriched Nuclear Proteome Isolated from Human Brain
Dammer, E. B., Duong, D. M., Diner, I., Gearing, M., Feng, Y., Lah, J. J., Levey, A. I., & Seyfried, N. T. (2013) · Journal of Proteome Research · doi:10.1021/pr400246t · Cited by 70 · see citing works
Combs, P. A., & Eisen, M. B. (2013) · PLoS ONE · doi:10.1371/journal.pone.0071820 · Cited by 65 · see citing works
Arabidopsis as a model for translational research
Yaschenko, A. E., Alonso, J. M., & Stepanova, A. N. (2024) · The Plant Cell · doi:10.1093/plcell/koae065 · Cited by 61 · see citing works
Extreme HOT regions are CpG-dense promoters in C. elegans and humansPreprint
Chen, R. A.-J., Stempor, P., Down, T. A., Zeiser, E., Feuer, S. K., & Ahringer, J. (2014) · Genome Research · doi:10.1101/gr.161992.113 · Cited by 58 · see citing works
Identification of sensory hair-cell transcripts by thiouracil-tagging in zebrafish
Erickson, T., & Nicolson, T. A. (2015) · BMC Genomics · doi:10.1186/s12864-015-2072-5 · Cited by 55 · see citing works
Genome-wide analysis links emerin to neuromuscular junction activity in Caenorhabditis elegans
González‐Aguilera, C., Ikegami, K., Ayuso, C., de Luis, A., Íñiguez, M., Cabello, J., Lieb, J. D., & Askjaer, P. (2014) · Genome biology · doi:10.1186/gb-2014-15-2-r21 · Cited by 54 · see citing works
Decoding neural transcriptomes and epigenomes via high-throughput sequencing
Shin, J., Ming, G., & Song, H. (2014) · Nature Neuroscience · doi:10.1038/nn.3814 · Cited by 52 · see citing works
Temporal transitions in the post-mitotic nervous system of Caenorhabditis elegans
Sun, H., & Hobert, O. (2021) · Nature · doi:10.1038/s41586-021-04071-4 · Cited by 52 · see citing works
Rapid Changes in the Translatome during the Conversion of Growth Cones to Synaptic Terminals
Zhang, K. X., Tan, L., Pellegrini, M. A., Zipursky, S. L., & McEwen, J. M. (2016) · Cell Reports · doi:10.1016/j.celrep.2015.12.102 · Cited by 51 · see citing works
Simple and Complex Centromeric Satellites in Drosophila Sibling Species
Talbert, P. B., Kasinathan, S., & Henikoff, S. (2018) · Genetics · doi:10.1534/genetics.117.300620 · Cited by 51 · see citing works
Self-citationProteomic profiling of cardiac tissue by isolation of nuclei tagged in specific cell types (INTACT)
Amin, N. M., Greco, T. M., Kuchenbrod, L. M., Rigney, M. M., Chung, M.-I., Wallingford, J. B., Cristea, I. M., & Conlon, F. L. (2014) · Development · doi:10.1242/dev.098327 · Cited by 50 · see citing works
Trinh, L. A., Chong-Morrison, V., Gavriouchkina, D., Hochgreb, T., Senanayake, U., Fraser, S. E., & Sauka‐Spengler, T. (2017) · Cell Reports · doi:10.1016/j.celrep.2017.03.045 · Cited by 43 · see citing works
RNA Expression Profiling from FACS‐Isolated Cells of the Drosophila Intestine
Dutta, D., Xiang, J., & Edgar, B. A. (2013) · Current Protocols in Stem Cell Biology · doi:10.1002/9780470151808.sc02f02s27 · Cited by 44 · see citing works
Microgenomics: Genome-Scale, Cell-Specific Monitoring of Multiple Gene Regulation Tiers
Bailey-Serres, J. N. (2013) · Annual Review of Plant Biology · doi:10.1146/annurev-arplant-050312-120035 · Cited by 42 · see citing works
Designing Cell-Type-Specific Genome-wide Experiments
Handley, A., Schauer, T., Ladurner, A. G., & Margulies, C. E. (2015) · Molecular Cell · doi:10.1016/j.molcel.2015.04.024 · Cited by 40 · see citing works
Surveying the epigenomic landscape, one base at a time
Zentner, G. E., & Henikoff, S. (2012) · Genome biology · doi:10.1186/gb-2012-13-10-250 · Cited by 40 · see citing works
Self-citationJones, S. G., Nixon, K. C. J., Chubak, M. C., & Kramer, J. M. (2018) · G3 Genes Genomes Genetics · doi:10.1534/g3.118.200560 · Cited by 38 · see citing works
Robust regulatory architecture of pan-neuronal gene expression
Leyva‐Díaz, E., & Hobert, O. (2022) · Current Biology · doi:10.1016/j.cub.2022.02.040 · Cited by 39 · see citing works
Waaijers, S., Muñoz, J., Berends, C. W. H., Ramalho, J. J., Goerdayal, S. S., Low, T. Y., Zoumaro-Djayoon, A. D., Hoffmann, M., Koorman, T., Tas, R. P., et al. (2016) · BMC Biology · doi:10.1186/s12915-016-0286-x · Cited by 33 · see citing works
Modern techniques for the analysis of chromatin and nuclear organization in C. elegans
Askjaer, P. (2014) · WormBook · doi:10.1895/wormbook.1.169.1 · Cited by 38 · see citing works
Surveying the epigenomic landscape, one base at a time
Zentner, G. E., & Henikoff, S. (2012) · Genome biology · doi:10.1186/gb4051 · Cited by 38 · see citing works
Self-citationHan, M., Wei, G., McManus, C. E., Hillier, L., & Reinke, V. (2019) · BMC Genomics · doi:10.1186/s12864-019-5893-9 · Cited by 36 · see citing works
The Genetic Analysis of Functional Connectomics in Drosophila
Meinertzhagen, I. A., & Lee, C. (2012) · Advances in genetics · doi:10.1016/b978-0-12-404742-6.00003-x · Cited by 35 · see citing works
miR-1 sustains muscle physiology by controlling V-ATPase complex assembly
Gutiérrez‐Pérez, P., Santillán, E. M., Lendl, T., Wang, J., Schrempf, A., Steinacker, T. L., Asparuhova, M., Brandstetter, M., Haselbach, D., & Cochella, L. (2021) · Science Advances · doi:10.1126/sciadv.abh1434 · Cited by 34 · see citing works
Dutta, D., Buchon, N., Xiang, J., & Edgar, B. A. (2015) · Current Protocols in Stem Cell Biology · doi:10.1002/9780470151808.sc02f02s34 · Cited by 33 · see citing works
CAST-ChIP Maps Cell-Type-Specific Chromatin States in the Drosophila Central Nervous System
Schauer, T., Schwalie, P. C., Handley, A., Margulies, C. E., Flicek, P., & Ladurner, A. G. (2013) · Cell Reports · doi:10.1016/j.celrep.2013.09.001 · Cited by 31 · see citing works
Agrawal, P., Chung, P., Heberlein, U., & Kent, C. F. (2019) · BMC Biology · doi:10.1186/s12915-019-0646-4 · Cited by 29 · see citing works
Repression of somatic cell fate in the germline
Robert, V. J. P., Garvis, S., & Palladino, F. (2015) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-015-1942-y · Cited by 30 · see citing works
Endosperm-specific transcriptome analysis by applying the INTACT system
León, G. D. T.-D., & Köhler, C. (2018) · Plant Reproduction · doi:10.1007/s00497-018-00356-3 · Cited by 29 · see citing works
Kubik, S., Bruzzone, M. J., & Shore, D. (2017) · BioEssays · doi:10.1002/bies.201600237 · Cited by 29 · see citing works
Epigenome Profiling of Specific Plant Cell Types Using a Streamlined INTACT Protocol and ChIP-seq
Wang, D., & Deal, R. B. (2015) · Methods in molecular biology · doi:10.1007/978-1-4939-2444-8_1 · Cited by 26 · see citing works
Self-citationDomsch, K., Carnesecchi, J., Disela, V., Friedrich, J., Trost, N., Ermakova, O. V., Polychronidou, M., & Lohmann, I. (2019) · eLife · doi:10.7554/elife.42675 · Cited by 26 · see citing works
Tissue-Specific Transcription Footprinting Using RNA PoI DamID (RAPID) in Caenorhabditis elegans
Gómez-Saldívar, G., Osuna-Luque, J., Semple, J. I., Glauser, D. A., Jarriault, S., & Meister, P. (2020) · Genetics · doi:10.1534/genetics.120.303774 · Cited by 24 · see citing works
The Importance of Detailed Epigenomic Profiling of Different Cell Types within Organs
Stueve, T. R., Marconett, C. N., Zhou, B., Borok, Z., & Laird‐Offringa, I. A. (2016) · Epigenomics · doi:10.2217/epi-2016-0005 · Cited by 24 · see citing works
Affinity-based Isolation of Tagged Nuclei from Drosophila Tissues for Gene Expression Analysis
Ma, J., & Weake, V. M. (2014) · Journal of Visualized Experiments · doi:10.3791/51418 · Cited by 23 · see citing works
Chemical Tools for Temporally and Spatially Resolved Mass Spectrometry-Based Proteomics
Yuet, K. P., & Tirrell, D. A. (2013) · Annals of Biomedical Engineering · doi:10.1007/s10439-013-0878-3 · Cited by 24 · see citing works
Marion‐Poll, L., Montalban, E., Munier, A., Hervé, D., & Girault, J. (2014) · European Journal of Neuroscience · doi:10.1111/ejn.12506 · Cited by 22 · see citing works
Ye, Y., Li, M., Gu, L., Chen, X., Shi, J., Zhang, X., & Jiang, C. (2016) · Cell Death and Differentiation · doi:10.1038/cdd.2016.135 · Cited by 23 · see citing works
Nuclei on the Rise: When Nuclei-Based Methods Meet Next-Generation Sequencing
Butto, T., Mungikar, K., Baumann, P., Winter, J., Lutz, B., & Gerber, S. (2023) · Cells · doi:10.3390/cells12071051 · Cited by 21 · see citing works
Gene expression profiling of epidermal cell types in C. elegans using Targeted DamID
Katsanos, D., Ferrando-Marco, M., Razzaq, I., Aughey, G., Southall, T. D., & Barkoulas, M. (2021) · Development · doi:10.1242/dev.199452 · Cited by 20 · see citing works
Palovaara, J., & Weijers, D. (2018) · Plant Reproduction · doi:10.1007/s00497-018-0347-0 · Cited by 20 · see citing works
Analysis ofC. elegansmuscle transcriptome using trans-splicing-based RNA tagging (SRT)
Ma, X., Zhan, G., Sleumer, M. C., Chen, S., Liu, W., Zhang, M. Q., & Liu, X. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw734 · Cited by 19 · see citing works
TRAP-rc, Translating Ribosome Affinity Purification from Rare Cell Populations of Drosophila Embryos
Bertin, B., Renaud, Y., Aradhya, R., Jagla, K., & Junion, G. (2015) · Journal of Visualized Experiments · doi:10.3791/52985 · Cited by 18 · see citing works
PAN-INTACT enables direct isolation of lineage-specific nuclei from fibrous tissues
Bhattacharyya, S., Sathe, A. A., Bhakta, M., Xing, C., & Munshi, N. V. (2019) · PLoS ONE · doi:10.1371/journal.pone.0214677 · Cited by 18 · see citing works
Chongtham, M. C., Butto, T., Mungikar, K., Gerber, S., & Winter, J. (2021) · International Journal of Molecular Sciences · doi:10.3390/ijms22105335 · Cited by 18 · see citing works
Seyres, D., Röder, L., & Perrin, L. (2012) · Briefings in Functional Genomics · doi:10.1093/bfgp/els028 · Cited by 15 · see citing works
Quantitative analyses of EGFR localization and trafficking dynamics in the follicular epithelium
Revaitis, N. T., Niepielko, M. G., Marmion, R. A., Klein, E. A., Piccoli, B., & Yakoby, N. (2020) · Development · doi:10.1242/dev.183210 · Cited by 15 · see citing works
A platform utilizing Drosophila ovulation for nonhormonal contraceptive screening
Jiang, K., Zhang, J., Huang, Y., Wang, Y., Xiao, S., Hadden, M. K., Woodruff, T. K., & Sun, J. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2026403118 · Cited by 15 · see citing works
Discovering enhancers by mapping chromatin features in primary tissue
Bowman, S. (2015) · Genomics · doi:10.1016/j.ygeno.2015.06.006 · Cited by 15 · see citing works
Domsch, K., Schröder, J., Janeschik, M., Schaub, C., & Lohmann, I. (2021) · Cell Reports · doi:10.1016/j.celrep.2020.108577 · Cited by 14 · see citing works
Fragoso-Luna, A., Romero-Bueno, R., Eibl, M., Ayuso, C., Muñoz-Jiménez, C. M., Beneš, V., Cases, I., & Askjaer, P. (2022) · Genetics · doi:10.1093/genetics/iyac166 · Cited by 12 · see citing works
Tracking context‐specific transcription factors regulating hox activity
Merabet, S., & Dard, A. (2013) · Developmental Dynamics · doi:10.1002/dvdy.24002 · Cited by 13 · see citing works
Temporally and Spatially Restricted Gene Expression Profiling
Tallafuß, A., Washbourne, P., & Postlethwait, J. H. (2014) · Current Genomics · doi:10.2174/1389202915666140602230106 · Cited by 13 · see citing works
McClure, C. D., & Southall, T. D. (2015) · Advances in genetics · doi:10.1016/bs.adgen.2015.06.003 · Cited by 12 · see citing works
Wuest, S. E., Schmid, M. W., & Grossniklaus, U. (2012) · Current Opinion in Plant Biology · doi:10.1016/j.pbi.2012.12.001 · Cited by 11 · see citing works
Emerging Roles for Chromo Domain Proteins in Genome Organization and Cell Fate in C. elegans
DasGupta, A., Lee, T. L., Li, C., & Saltzman, A. L. (2020) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2020.590195 · Cited by 11 · see citing works
Chromatin remodeling during the in vivo glial differentiation in early Drosophila embryos
Ye, Y., Gu, L., Chen, X., Shi, J., Zhang, X., & Jiang, C. (2016) · Scientific Reports · doi:10.1038/srep33422 · Cited by 10 · see citing works
Fortezza, M. L., Grigolon, G., Cosolo, A., Pindyurin, A. V., Breimann, L., Blum, H., van Steensel, B., & Classen, A.-K. (2018) · Epigenetics & Chromatin · doi:10.1186/s13072-018-0196-y · Cited by 10 · see citing works
Freedom of expression: cell‐type‐specific gene profiling
Otsuki, L., Cheetham, S. W., & Brand, A. H. (2014) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.149 · Cited by 9 · see citing works
Cell Type-Specific Affinity Purification of Nuclei for Chromatin Profiling in Whole Animals
Steiner, F. A., & Henikoff, S. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-1680-1_1 · Cited by 9 · see citing works
Self-citationCell Type-Specific Profiling of Chromatin Modifications and Associated Proteins
Morao, A. K., Caillieux, E., Colot, V., & Roudier, F. (2017) · Methods in molecular biology · doi:10.1007/978-1-4939-7318-7_8 · Cited by 8 · see citing works
Caenorhabditis elegans Small RNA Pathways Make Their Mark on Chromatin
Claycomb, J. M. (2012) · DNA and Cell Biology · doi:10.1089/dna.2012.1611 · Cited by 8 · see citing works
Technologies to measure and modulate protein subcellular localization
Leineweber, W. D., Tei, R., Mäkiniemi, A., Ting, A. Y., & Lundberg, E. K. (2026) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-026-00957-1 · Cited by 7 · see citing works
Murray, J. I. (2018) · Wiley Interdisciplinary Reviews Developmental Biology · doi:10.1002/wdev.314 · Cited by 8 · see citing works
Defaye, A., & Perrin, L. (2014) · Methods in molecular biology · doi:10.1007/978-1-4939-1242-1_11 · Cited by 7 · see citing works
Detecting gene expression in Caenorhabditis elegans
Calarco, J. A., Taylor, S. R., & Miller, D. M. (2024) · Genetics · doi:10.1093/genetics/iyae167 · Cited by 6 · see citing works
Zibetti, C. (2022) · Cells · doi:10.3390/cells11050806 · Cited by 6 · see citing works
Seyres, D., Ghavi-Helm, Y., Junion, G., Taghli-Lamallem, O., Guichard, C., Röder, L., Girardot, C., Furlong, E. E. M., & Perrin, L. (2016) · Development · doi:10.1242/dev.140822 · Cited by 6 · see citing works
Cell-type specificcis-regulatory networks
Polychronidou, M., & Lohmann, I. (2013) · Fly · doi:10.4161/fly.22939 · Cited by 5 · see citing works
INTACT Proteomics in XenopusPreprint
Wasson, L. K., Amin, N. M., & Conlon, F. L. (2018) · Cold Spring Harbor Protocols · doi:10.1101/pdb.prot098384 · Cited by 5 · see citing works
An Evolutionary Perspective on Hox Binding Site Preferences in Two Different Tissues
Folkendt, L., Lohmann, I., & Domsch, K. (2021) · Journal of Developmental Biology · doi:10.3390/jdb9040057 · Cited by 4 · see citing works
Decoding the role of chromatin architecture in development: coming closer to the end of the tunnel
Luo, C., Dong, J., Zhang, Y., & Lam, E. (2014) · Frontiers in Plant Science · doi:10.3389/fpls.2014.00374 · Cited by 3 · see citing works
Cell type‐specific epigenome profiling using affinity‐purified nuclei
Chitikova, Z., & Steiner, F. A. (2016) · genesis · doi:10.1002/dvg.22919 · Cited by 3 · see citing works
Self-citationTrinh, L. A., Chong-Morrison, V., & Sauka‐Spengler, T. (2018) · Methods · doi:10.1016/j.ymeth.2018.07.011 · Cited by 3 · see citing works
Deconvolution of gene expression from cell populations across the C. eleganslineage
Burdick, J. T., & Murray, J. I. (2013) · BMC Bioinformatics · doi:10.1186/1471-2105-14-204 · Cited by 3 · see citing works
- Authors
- Steiner, F. A., Talbert, P. B., Kasinathan, S., Deal, R. B., & Henikoff, S.
- Affiliations
- Fred Hutch Cancer Center (US)
- Howard Hughes Medical Institute (US)
- Venue
- Genome Research
- Publisher
- Cold Spring Harbor Laboratory
- Published
- 2012-01-04
- Volume
- 22
- Issue
- 4
- Pages
- 766-777
- ISSN
- 1088-9051 (ISSN-L)
- PMC
- PMC3317158
- OpenAlex
- W2163482547
- Cited by
- 123
- References
- 50
- Citations by year
- 2026: 3 · 2025: 2 · 2024: 2 · 2023: 1 · 2022: 7 · 2021: 8 · 2020: 5 · 2019: 4 · 2018: 12 · 2017: 10 · 2016: 11 · 2015: 13 · 2014: 22 · 2013: 13 · 2012: 10
- Type
- posted content
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- other-oa
- Locations
- Genome Research (publishedVersion, other-oa)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- HighWire Press Open Archive (submittedVersion)
- Archive ouverte UNIGE (University of Geneva) (submittedVersion, cc-by-nc)
- Funders
- National Science Foundation
- Howard Hughes Medical Institute
- Fred Hutchinson Cancer Research Center
- Schweizerischer Nationalfonds zur Förderung der Wissenschaftlichen Forschung
- National Institutes of Health
- National Human Genome Research Institute
- National Institute of General Medical Sciences (T32GM007266)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Chromatin Dynamics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Genomics and Phylogenetic Studies
- Keywords
- nucleosome occupancy, chromatin profiling, tissue-specific gene expression, epigenetics, transgenic animals
- MeSH terms
- Animals, Cell Nucleus, Chromatin, Drosophila melanogaster, Embryo, Nonmammalian, Luminescent Proteins, Mesoderm, Microscopy, Fluorescence, Muscles, Nucleosomes, Helminth Proteins, Genome, Caenorhabditis elegans, Gene Expression Regulation, Developmental, Gene Expression Profiling, Muscle Development, Drosophila Proteins, Animals, Genetically Modified
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