Combined quantification of intracellular (phospho-)proteins and transcriptomics from fixed single cells
Open accessPublished version of a preprint
Abstract
Environmental stimuli often lead to heterogeneous cellular responses and transcriptional output. We developed single-cell RNA and Immunodetection (RAID) to allow combined analysis of the transcriptome and intracellular (phospho-)proteins from fixed single cells. RAID successfully recapitulated differentiation-state changes at the protein and mRNA level in human keratinocytes. Furthermore, we show that differentiated keratinocytes that retain high phosphorylated FAK levels, a feature associated with stem cells, also express a selection of stem cell associated transcripts. Our data demonstrates that RAID allows investigation of heterogeneous cellular responses to environmental signals at the mRNA and phospho-proteome level.
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?
RAID enables correlation analysis of environmental stimuli with heterogeneous cellular responses.
“RNA and immunodetection (RAID), a method developed for immunodetection of intracellular proteins or phosphorylated proteins together with mRNA profiling, enables correlation analysis of environmental stimuli with heterogeneous cellular responses77.”
From The technological landscape and applications of single-cell multi-omics (2023) · cites this paper as [77]
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
Cox, J., & Mann, M. (2008) · Nature Biotechnology · doi:10.1038/nbt.1511 · Cited by 14,855 · see citing works
Integrating single-cell transcriptomic data across different conditions, technologies, and species
Butler, A., Hoffman, P., Smibert, P., Papalexi, E., & Satija, R. (2018) · Nature Biotechnology · doi:10.1038/nbt.4096 · Cited by 13,174 · see citing works
Trapnell, C., Cacchiarelli, D., Grimsby, J., Pokharel, P., Li, S., Morse, M., Lennon, N. J., Livak, K. J., Mikkelsen, T. S., & Rinn, J. L. (2014) · Nature Biotechnology · doi:10.1038/nbt.2859 · Cited by 7,314 · 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
Gene ontology analysis for RNA-seq: accounting for selection bias
Young, M. D., Wakefield, M. J., Smyth, G. K., & Oshlack, A. (2010) · Genome Biology · doi:10.1186/gb-2010-11-2-r14 · Cited by 7,107 · see citing works
Rappsilber, J., Mann, M., & Ishihama, Y. (2007) · Nature Protocols · doi:10.1038/nprot.2007.261 · Cited by 4,641 · see citing works
Droplet barcoding for single-cell transcriptomics applied to embryonic stem cells
Klein, A. M., Mazutis, L., Akartuna, I., Tallapragada, N., Veres, A., Li, V., Peshkin, L., Weitz, D. A., & Kirschner, M. W. (2015) · Cell · doi:10.1016/j.cell.2015.04.044 · Cited by 3,356 · see citing works
Simultaneous epitope and transcriptome measurement in single cells
Stoeckius, M., Hafemeister, C., Stephenson, W., Houck-Loomis, B., Chattopadhyay, P. K., Swerdlow, H., Satija, R., & Smibert, P. (2017) · Nature Methods · doi:10.1038/nmeth.4380 · Cited by 3,098 · 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
Massively parallel single-cell RNA-seq for marker-free decomposition of tissues into cell types
Jaitin, D. A., Kenigsberg, E., Keren-Shaul, H., Elefant, N., Paul, F., Zaretsky, I., Mildner, A., Cohen, N., Jung, S., Tanay, A., et al. (2014) · Science · doi:10.1126/science.1247651 · Cited by 1,795 · see citing works
The cornified envelope: a model of cell death in the skin
Candi, E., Schmidt, R., & Melino, G. (2005) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm1619 · Cited by 1,776 · see citing works
Tetrazine Ligation: Fast Bioconjugation Based on Inverse-Electron-Demand Diels−Alder Reactivity
Blackman, M. L., Royzen, M., & Fox, J. M. (2008) · Journal of the American Chemical Society · doi:10.1021/ja8053805 · Cited by 1,691 · see citing works
Regev, A., Teichmann, S. A., Lander, E. S., Amit, I., Benoist, C. O., Birney, E., Bodenmiller, B., & al, E. (2017) · Zurich Open Repository and Archive (University of Zurich) · doi:10.5167/uzh-162597 · Cited by 1,457 · see citing works
A Single-Cell Transcriptome Atlas of the Human Pancreas
Muraro, M. J., Dharmadhikari, G., Grün, D., Gröen, N., Dielen, T., Jansen, E., van Gurp, L., Engelse, M. A., Carlotti, F., de Koning, E. J. P., et al. (2016) · Cell Systems · doi:10.1016/j.cels.2016.09.002 · Cited by 1,288 · see citing works
Self-citationSingle-cell messenger RNA sequencing reveals rare intestinal cell types
Grün, D., Lyubimova, A., Kester, L., Wiebrands, K., Basak, O., Sasaki, N., Clevers, H., & van Oudenaarden, A. (2015) · Nature · doi:10.1038/nature14966 · Cited by 1,234 · see citing works
CEL-seq2: sensitive highly-multiplexed single-cell RNA-Seq
Hashimshony, T., Senderovich, N., Avital, G., Klochendler, A., de Leeuw, Y., Anavy, L., Gennert, D., Li, S., Livak, K. J., Rozenblatt-Rosen, O., et al. (2016) · Genome Biology · doi:10.1186/s13059-016-0938-8 · Cited by 1,125 · see citing works
Transcriptional Heterogeneity and Lineage Commitment in Myeloid Progenitors
Paul, F., Arkin, Y., Giladi, A., Jaitin, D. A., Kenigsberg, E., Keren-Shaul, H., Winter, D., Lara-Astiaso, D., Gury, M., Weiner, A., et al. (2015) · Cell · doi:10.1016/j.cell.2015.11.013 · Cited by 1,082 · see citing works
Epidermal Stem Cells of the Skin
Blanpain, C., & Fuchs, E. V. (2006) · Annual Review of Cell and Developmental Biology · doi:10.1146/annurev.cellbio.22.010305.104357 · Cited by 845 · see citing works
Multiplexed quantification of proteins and transcripts in single cells
Peterson, V. M., Zhang, K. X., Kumar, N., Wong, J., Li, L., Wilson, D. C., Moore, R., McClanahan, T. K., Sadekova, S., & Klappenbach, J. A. (2017) · Nature Biotechnology · doi:10.1038/nbt.3973 · Cited by 832 · see citing works
Role of integrins in regulating epidermal adhesion, growth and differentiation
Watt, F. M. (2002) · The EMBO Journal · doi:10.1093/emboj/cdf399 · Cited by 647 · see citing works
Emerging interactions between skin stem cells and their niches
Hsu, Y., Li, L., & Fuchs, E. V. (2014) · Nature Medicine · doi:10.1038/nm.3643 · Cited by 563 · see citing works
Multiple connections link FAK to cell motility and invasion
Schlaepfer, D. D., & Mitra, S. K. (2003) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2003.12.002 · Cited by 415 · see citing works
Highly multiplexed simultaneous detection of RNAs and proteins in single cells
Frei, A. P., Bava, F.-A., Zunder, E. R., Hsieh, E. W. Y., Chen, S.-Y., Nolan, G. P., & Gherardini, P. F. (2016) · Nature Methods · doi:10.1038/nmeth.3742 · Cited by 330 · see citing works
Wiśniewski, J. R., Ostasiewicz, P., & Mann, M. (2011) · Journal of Proteome Research · doi:10.1021/pr200019m · Cited by 290 · see citing works
Abseq: Ultrahigh-throughput single cell protein profiling with droplet microfluidic barcoding
Shahi, P., Kim, S., Haliburton, J. R., Gartner, Z. J., & Abate, A. R. (2017) · Scientific Reports · doi:10.1038/srep44447 · Cited by 258 · see citing works
A LncRNA-MAF:MAFB transcription factor network regulates epidermal differentiation
Lopez-Pajares, V., Qu, K., Zhang, J., Webster, D. E., Barajas, B. C., Siprashvili, Z., Zarnegar, B. J., Boxer, L. D., Rios, E. J., Tao, S., et al. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.01.028 · Cited by 194 · see citing works
Kolev, V. N., Mandinova, A., Guinea‐Viniegra, J., Hu, B., Lefort, K., Lambertini, C., Neel, V., Dummer, R., Wagner, E. F., & Dotto, G. P. (2008) · Nature Cell Biology · doi:10.1038/ncb1750 · Cited by 187 · see citing works
Digital Quantification of Proteins and mRNA in Single Mammalian Cells
Albayrak, C., Jordi, C. A., Zechner, C., Lin, J., Bichsel, C. A., Khammash, M., & Tay, S. (2016) · Molecular Cell · doi:10.1016/j.molcel.2016.02.030 · Cited by 176 · see citing works
Multiplexed, targeted profiling of single-cell proteomes and transcriptomes in a single reaction
Genshaft, A. S., Li, S., Gallant, C. J., Darmanis, S., Prakadan, S. M., Ziegler, C. G. K., Lundberg, M., Fredriksson, S., Hong, J., Regev, A., et al. (2016) · Genome Biology · doi:10.1186/s13059-016-1045-6 · Cited by 175 · see citing works
Diverse epigenetic strategies interact to control epidermal differentiation
Mulder, K. W., Wang, X., Escriu, C., Ito, Y., Schwarz, R. F., Gillis, J., Sirokmány, G., Donati, G., Uribe‐Lewis, S., Pavlidis, P., et al. (2012) · Nature Cell Biology · doi:10.1038/ncb2520 · Cited by 143 · see citing works
Self-citationMultiple tissue kallikrein mRNA and protein expression in normal skin and skin diseases
Komatsu, N., Saijoh, K., Toyama, T., Ohka, R., Otsuki, N., Hussack, G., Takehara, K., & Diamandis, E. P. (2005) · British Journal of Dermatology · doi:10.1111/j.1365-2133.2005.06754.x · Cited by 136 · see citing works
Ghosh, M. C., Grass, L., Soosaipillai, A. R., Sotiropoulou, G., & Diamandis, E. P. (2004) · Tumor Biology · doi:10.1159/000081102 · Cited by 122 · see citing works
van Buggenum, J. A. G. L., Gerlach, J. P., Eising, S., Schoonen, L., van Eijl, R. A. P. M., Tanis, S. E. J., Hogeweg, M., Hubner, N. C., van Hest, J. C., Bonger, K. M., et al. (2016) · Scientific Reports · doi:10.1038/srep22675 · Cited by 93 · see citing works
Self-citationA practical solution for preserving single cells for RNA sequencing
Attar, M., Sharma, E., Li, S., Bryer, C., Cubitt, L., Broxholme, J., Lockstone, H., Kinchen, J., Simmons, A., Piazza, P., et al. (2018) · Scientific Reports · doi:10.1038/s41598-018-20372-7 · Cited by 80 · see citing works
Immuno-detection by sequencing enables large-scale high-dimensional phenotyping in cells
van Buggenum, J. A. G. L., Gerlach, J. P., Tanis, S. E. J., Hogeweg, M., Jansen, P. W. T. C., Middelwijk, J., van der Steen, R., Vermeulen, M., Stunnenberg, H. G., Albers, C. A., et al. (2018) · Nature Communications · doi:10.1038/s41467-018-04761-0 · Cited by 22 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Methods and applications for single-cell and spatial multi-omics
Vandereyken, K., Sifrim, A., Thienpont, B., & Voet, T. (2023) · Nature Reviews Genetics · doi:10.1038/s41576-023-00580-2 · Cited by 1,244 · see citing works
The technological landscape and applications of single-cell multi-omics
Baysoy, A., Bai, Z., Satija, R., & Fan, R. (2023) · Nature Reviews Molecular Cell Biology · doi:10.1038/s41580-023-00615-w · Cited by 1,037 · see citing works
Mimitou, E. P., Lareau, C. A., Chen, K. Y., Zorzetto-Fernandes, A. L., Hao, Y., Takeshima, Y., Luo, W., Huang, T.-S., Yeung, B. Z., Papalexi, E., et al. (2021) · Nature Biotechnology · doi:10.1038/s41587-021-00927-2 · Cited by 529 · see citing works
Single-cell multiomics: technologies and data analysis methods
Lee, J., Hyeon, D. Y., & Hwang, D. (2020) · Experimental & Molecular Medicine · doi:10.1038/s12276-020-0420-2 · Cited by 524 · see citing works
Katzenelenbogen, Y., Sheban, F., Yalin, A., Yofe, I., Svetlichnyy, D., Jaitin, D. A., Bornstein, C., Moshe, A., Keren-Shaul, H., Cohen, M., et al. (2020) · Cell · doi:10.1016/j.cell.2020.06.032 · Cited by 498 · see citing works
Single-cell proteomics enabled by next-generation sequencing or mass spectrometry
Bennett, H. M., Stephenson, W., Rose, C. M., & Darmanis, S. (2023) · Nature Methods · doi:10.1038/s41592-023-01791-5 · Cited by 351 · see citing works
Advances in single-cell omics and multiomics for high-resolution molecular profiling
Lim, J., Park, C., Kim, M., Kim, H., Kim, J., & Lee, D.-S. (2024) · Experimental & Molecular Medicine · doi:10.1038/s12276-024-01186-2 · Cited by 193 · see citing works
Joint single-cell measurements of nuclear proteins and RNA in vivo
Chung, H., Parkhurst, C. N., Magee, E. M., Phillips, D., Habibi, E., Chen, F., Yeung, B. Z., Waldman, J., Artis, D., & Regev, A. (2021) · Nature Methods · doi:10.1038/s41592-021-01278-1 · Cited by 144 · see citing works
Chen, A. F., Parks, B., Kathiria, A. S., Ober-Reynolds, B., Goronzy, J. J., & Greenleaf, W. J. (2022) · Nature Methods · doi:10.1038/s41592-022-01461-y · Cited by 139 · see citing works
A combined approach for single-cell mRNA and intracellular protein expression analysis
Reimegård, J., Tarbier, M., Danielsson, M., Schuster, J., Baskaran, S., Panagiotou, S., Dahl, N., Friedländer, M. R., & Gallant, C. J. (2021) · Communications Biology · doi:10.1038/s42003-021-02142-w · Cited by 129 · see citing works
From bench to bedside: Single-cell analysis for cancer immunotherapy
Davis-Marcisak, E. F., Deshpande, A. M., Stein-O’Brien, G., Ho, W. J., Laheru, D. A., Jaffee, E. M., Fertig, E. J., & Kagohara, L. T. (2021) · Cancer Cell · doi:10.1016/j.ccell.2021.07.004 · Cited by 120 · see citing works
Trzupek, D., Dunstan, M., Cutler, A. J., Lee, M., Godfrey, L., Jarvis, L., Rainbow, D. B., Aschenbrenner, D., Jones, J. L., Uhlig, H. H., et al. (2020) · Genome Medicine · doi:10.1186/s13073-020-00756-z · Cited by 105 · see citing works
Le, J., Dian, Y., Zhao, D., Guo, Z., Luo, Z., Chen, X., Zeng, F., & Deng, G. (2025) · Molecular Cancer · doi:10.1186/s12943-025-02426-3 · Cited by 109 · see citing works
Klebes, A., Ates, H. C., Verboket, R. D., Urban, G. A., von Stetten, F., Dincer, C., & Früh, S. M. (2023) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2023.115800 · Cited by 90 · see citing works
Into the multiverse: advances in single-cell multiomic profiling
Ogbeide, S., Giannese, F., Mincarelli, L., & Macaulay, I. C. (2022) · Trends in Genetics · doi:10.1016/j.tig.2022.03.015 · Cited by 82 · see citing works
Ge, S., Sun, S., Xu, H., Cheng, Q. S., & Ren, Z. (2025) · Briefings in Bioinformatics · doi:10.1093/bib/bbaf136 · Cited by 89 · see citing works
Single-cell omics: experimental workflow, data analyses and applications
Sun, F., Li, H., Sun, D., Fu, S., Gu, L., Shao, X., Wang, Q., Dong, X., Duan, B., Xing, F., et al. (2024) · Science China Life Sciences · doi:10.1007/s11427-023-2561-0 · Cited by 81 · see citing works
Time-resolved single-cell RNA-seq using metabolic RNA labelling
Erhard, F., Saliba, A.-E., Lusser, A., Toussaint, C., Hennig, T., Prusty, B. K., Kirschenbaum, D., Abadie, K., Miska, E. A., Friedel, C. C., et al. (2022) · Nature Reviews Methods Primers · doi:10.1038/s43586-022-00157-z · Cited by 73 · see citing works
Advances and applications in single-cell and spatial genomics
Wang, J., Ye, F., Chai, H., Jiang, Y., Wang, T., Ran, X., Xia, Q., Xu, Z., Fu, Y., Zhang, G., et al. (2024) · Science China Life Sciences · doi:10.1007/s11427-024-2770-x · Cited by 69 · see citing works
Gene regulatory network inference in single-cell biology
Akers, K., & Murali, T. M. (2021) · Current Opinion in Systems Biology · doi:10.1016/j.coisb.2021.04.007 · Cited by 63 · see citing works
SCITO-seq: single-cell combinatorial indexed cytometry sequencing
Hwang, B., Lee, D. S., Tamaki, W., Sun, Y., Ogorodnikov, A., Hartoularos, G. C., Winters, A. F., Yeung, B. Z., Nazor, K. L., Song, Y. S., et al. (2021) · Nature Methods · doi:10.1038/s41592-021-01222-3 · Cited by 63 · see citing works
Single‐Cell Sequencing Methodologies: From Transcriptome to Multi‐Dimensional Measurement
Chen, Y., Song, J. T., Ruan, Q., Zeng, X., Wu, L., Cai, L., Wang, X., & Yang, C. J. (2021) · Small Methods · doi:10.1002/smtd.202100111 · Cited by 59 · see citing works
Signalling dynamics in embryonic development
Sonnen, K. F., & Janda, C. Y. (2021) · Biochemical Journal · doi:10.1042/bcj20210043 · Cited by 56 · see citing works
Integrated multi-omics with machine learning to uncover the intricacies of kidney disease
Liu, X., Shi, J., Jiao, Y., An, J., Tian, J., Yang, Y., & Zhuo, L. (2024) · Briefings in Bioinformatics · doi:10.1093/bib/bbae364 · Cited by 58 · see citing works
Neurodegeneration cell per cell
Balusu, S., Praschberger, R., Lauwers, E., Strooper, B. D., & Verstreken, P. (2023) · Neuron · doi:10.1016/j.neuron.2023.01.016 · Cited by 51 · see citing works
Vlahos, A., Mansell, T., Saffery, R., & Novakovic, B. (2019) · PLoS Genetics · doi:10.1371/journal.pgen.1008236 · Cited by 52 · see citing works
van Kuijk, K., Kuppe, C., Betsholtz, C., Vanlandewijck, M., Kramann, R., & Sluimer, J. C. (2019) · Cardiovascular Research · doi:10.1093/cvr/cvz185 · Cited by 52 · see citing works
Single-cell intracellular epitope and transcript detection reveals signal transduction dynamics
Rivello, F., van Buijtenen, E., Matuła, K., van Buggenum, J. A. G. L., Vink, P. M., van Eenennaam, H., Mulder, K. W., & Huck, W. T. S. (2021) · Cell Reports Methods · doi:10.1016/j.crmeth.2021.100070 · Cited by 46 · see citing works
Self-citationProgress in single-cell multimodal sequencing and multi-omics data integration
Wang, X. J., Wu, X., Hong, N., & Jin, W. (2023) · Biophysical Reviews · doi:10.1007/s12551-023-01092-3 · Cited by 43 · see citing works
Huang, A. C., Hsieh, T.-H. S., Zhu, J., Michuda, J., Teng, A., Kim, S., Rumsey, E. M., Lam, S. K., Anigbogu, I., Wright, P., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.06.11.659105 · Cited by 50 · see citing works
Computational Methods for Single-Cell Imaging and Omics Data Integration
Watson, E. R., Fard, A. T., & Mar, J. C. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2021.768106 · Cited by 41 · see citing works
Single-Cell Multi-Omics: Insights into Therapeutic Innovations to Advance Treatment in Cancer
Guan, A., & Quek, C. Y. J. (2025) · International Journal of Molecular Sciences · doi:10.3390/ijms26062447 · Cited by 32 · see citing works
Gene expression and protein abundance: Just how associated are these molecular traits?
Samih, A., Ferreira, M. A. D. M., & Nikoloski, Z. (2025) · Biotechnology Advances · doi:10.1016/j.biotechadv.2025.108720 · Cited by 34 · see citing works
Microfluidics-based single cell analysis: from transcriptomics to spatiotemporal multi-omics
Cao, J., Chen, X., Huang, S., Shi, W., Fan, Q., Gong, Y., Peng, Y., Wu, L., & Yang, C. J. (2022) · TrAC Trends in Analytical Chemistry · doi:10.1016/j.trac.2022.116868 · Cited by 29 · see citing works
Epigenetic Regulations in Mammalian Cells: Roles and Profiling Techniques
Kim, U., & Lee, D.-S. (2023) · Molecules and Cells · doi:10.14348/molcells.2023.0013 · Cited by 26 · see citing works
FixNCut: single-cell genomics through reversible tissue fixation and dissociation
Jiménez-Gracia, L., Marchese, D., Nieto, J. C., Caratù, G., Melón-Ardanaz, E., Gudiño, V., Roth, S., Wise, K., Ryan, N. K., Jensen, K. B., et al. (2024) · Genome biology · doi:10.1186/s13059-024-03219-5 · Cited by 24 · see citing works
scTrends: A living review of commercial single-cell and spatial 'omic technologies
Jonghe, J. D., Opzoomer, J. W., Vilas‐Zornoza, A., Nilges, B. S., Crane, P., Vicari, M., Lee, H., Lara‐Astiaso, D., Groß, T., Morf, J., et al. (2024) · Cell Genomics · doi:10.1016/j.xgen.2024.100723 · Cited by 25 · see citing works
Xu, X., Zhang, M.-X., Zhang, X., Liu, Y., Cai, L.-F., Zhang, Q., Chen, Q., Lin, L., Lin, S., Song, Y.-L., et al. (2022) · Analytical Chemistry · doi:10.1021/acs.analchem.1c05312 · Cited by 21 · see citing works
Microfluidic single‐cell multiomics analysis
Xu, X., Zhang, Q., Li, M., Lin, S., Liang, S., Cai, L., Zhu, H., Su, R. J., & Yang, C. J. (2022) · Open Research (University of Surrey) · doi:10.1002/viw.20220034 · Cited by 23 · see citing works
Kaur, H., Jha, P., Ochatt, S., & Kumar, V. (2023) · Critical Reviews in Biotechnology · doi:10.1080/07388551.2023.2165900 · Cited by 22 · see citing works
Epigenetically regulated RNA-binding proteins signify malaria hypnozoite dormancy
Toenhake, C. G., der Wel, A. V.-V., Wu, H., Kanyal, A., Nieuwenhuis, I. G., van der Werff, N., Hofman, S., Zeeman, A., Kocken, C. H. M., & Bártfai, R. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.112727 · Cited by 21 · see citing works
The role of single-cell genomics in human genetics
Sreenivasan, V. K. A., Balachandran, S., & Spielmann, M. (2022) · Journal of Medical Genetics · doi:10.1136/jmedgenet-2022-108588 · Cited by 18 · see citing works
Velez, M. V. L., Neikes, H. K., Snabel, R. R., Quint, Y. M., Chen, Q., Martens, A., Veenstra, G. J. C., Freeman, M. R., van Heeringen, S. J., & Vermeulen, M. (2022) · Nucleic Acids Research · doi:10.1093/nar/gkac1236 · Cited by 19 · see citing works
Chen, M., Jiang, J., & Hou, J. (2023) · Biomarker Research · doi:10.1186/s40364-023-00502-8 · Cited by 19 · see citing works
Scalable, multimodal profiling of chromatin accessibility and protein levels in single cellsPreprint
Mimitou, E. P., Lareau, C. A., Chen, K. Y., Zorzetto-Fernandes, A. L., Takeshima, Y., Luo, W., Huang, T.-S., Yeung, B. Z., Thakore, P. I., Wing, J. B., et al. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.09.08.286914 · Cited by 18 · see citing works
Nesterenko, P. A., McLaughlin, J., Cheng, D., Bangayan, N. J., Sojo, G. B., Seet, C. S., Yu, Q., Mao, Z., Obusan, M. B., Phillips, J. W., et al. (2021) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2021190118 · Cited by 16 · see citing works
Integration of single‐cell transcriptome and proteome technologies: Toward spatial resolution levels
He, L., Wang, W., Dang, K., Ge, Q., & Zhao, X. (2023) · Open Research (University of Surrey) · doi:10.1002/viw.20230040 · Cited by 16 · see citing works
Key Considerations on CITE‐Seq for Single‐Cell Multiomics
Song, H.-W., Martin, J., Shi, X., & Tyznik, A. J. (2025) · PROTEOMICS · doi:10.1002/pmic.202400011 · Cited by 18 · see citing works
Advanced sequencing-based high-throughput and long-read single-cell transcriptome analysis
Huang, S., Shi, W., Li, S., Fan, Q., Yang, C. J., Cao, J., & Wu, L. (2024) · Lab on a Chip · doi:10.1039/d4lc00105b · Cited by 14 · see citing works
Advances in Single Cell Technologies in Immunology
Choi, J. R. (2020) · BioTechniques · doi:10.2144/btn-2020-0047 · Cited by 15 · see citing works
Single‐Cell and Spatial Omics: Methods and Applications
Cen, X., Huang, X., Deng, E., Gong, X., Tan, N., Ye, J. T., Wang, Y., Eils, R., Luo, Q., Li, Y., et al. (2026) · MedComm · doi:10.1002/mco2.70713 · Cited by 13 · see citing works
Single-cell epigenomics and proteomics methods integrated in multiomics
Bi, H., & Weng, X. (2024) · Fundamental Research · doi:10.1016/j.fmre.2023.11.014 · Cited by 12 · see citing works
Large-scale datasets uncovering cell signalling networks in cancer: context matters
Sharma, S., & Petsalaki, E. (2019) · Current Opinion in Genetics & Development · doi:10.1016/j.gde.2019.05.001 · Cited by 10 · see citing works
The Application of Single-Cell Technologies in Cardiovascular Research
Chen, Y., Liu, Y., & Gao, X. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.751371 · Cited by 11 · see citing works
Single-Cell Molecular Barcoding to Decode Multimodal Information Defining Cell States
Kim, I. S. (2023) · Molecules and Cells · doi:10.14348/molcells.2023.2168 · Cited by 11 · see citing works
Lindeman, I., & Sollid, L. M. (2021) · Mucosal Immunology · doi:10.1038/s41385-021-00452-0 · Cited by 11 · see citing works
Heuts, B. M. H., Arza-Apalategi, S., Alkema, S. G., Tijchon, E. J. H., Jussen, L., Bergevoet, S. M., van der Reijden, B. A., & Martens, J. H. A. (2023) · Cells · doi:10.3390/cells12081195 · Cited by 10 · see citing works
Self-citationDecoding Human Biology and Disease Using Single-Cell Omics Technologies
Shi, Q., Chen, X., & Zhang, Z. (2023) · Genomics Proteomics & Bioinformatics · doi:10.1016/j.gpb.2023.06.003 · Cited by 10 · see citing works
Multimodal detection of protein isoforms and nucleic acids from mouse pre-implantation embryos
Rosàs, E., Modzelewski, A. J., Geldert, A., He, L., & Herr, A. E. (2021) · Nature Protocols · doi:10.1038/s41596-020-00449-2 · Cited by 8 · see citing works
Caprioli, C., Nazari, I., Milovanovic, S., & Pelicci, P. G. (2022) · Frontiers in Oncology · doi:10.3389/fonc.2021.796477 · Cited by 9 · see citing works
Healy, Z. R., Weinhold, K. J., & Murdoch, D. M. (2020) · Frontiers in Immunology · doi:10.3389/fimmu.2020.01859 · Cited by 9 · see citing works
van Buijtenen, E., Janssen, W., Vink, P. M., Habraken, M., Wingens, L., van Elsas, A., Huck, W. T. S., van Buggenum, J. A. G. L., & van Eenennaam, H. (2023) · Molecular & Cellular Proteomics · doi:10.1016/j.mcpro.2023.100492 · Cited by 9 · see citing works
Self-citationPregizer, S. K., Vreven, T., Mathur, M., & Robinson, L. N. (2023) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2023.1176856 · Cited by 8 · see citing works
Reverse Phase Protein Arrays in cancer stem cells
Signore, M., & Manganelli, V. (2022) · Methods in cell biology · doi:10.1016/bs.mcb.2022.04.004 · Cited by 8 · see citing works
Mutisheva, I., Robatel, S., Bäriswyl, L., & Schenk, M. (2022) · International Journal of Molecular Sciences · doi:10.3390/ijms231810233 · Cited by 8 · see citing works
SIGNAL-seq: Multimodal Single-cell Inter- and Intra-cellular Signalling AnalysisPreprint
Opzoomer, J. W., O’Sullivan, R., Sufi, J., Madsen, R. R., Qin, X., Basiarz, E., & Tape, C. J. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.02.23.581433 · Cited by 8 · see citing works
Mircea, M., & Semrau, S. (2021) · Biochemical Society Transactions · doi:10.1042/bst20210135 · Cited by 7 · see citing works
Single-cell RNA-Sequencing in Neuroscience
Mayer, S., Khakipoor, S., Droemer, M. A., & Cozetto, D. A. (2019) · e-Neuroforum · doi:10.1515/nf-2019-0021 · Cited by 6 · see citing works
Combined mRNA and protein single cell analysis in a dynamic cellular system using SPARCPreprint
Reimegård, J., Danielsson, M., Tarbier, M., Schuster, J., Baskaran, S., Panagiotou, S., Dahl, N., Friedländer, M. R., & Gallant, C. J. (2019) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/749473 · Cited by 6 · see citing works
Multiplexed multimodal single-cell technologies: From observation to perturbation analysis
Lee, S.-H., Park, J., & Hwang, B. (2024) · Molecules and Cells · doi:10.1016/j.mocell.2024.100147 · Cited by 4 · see citing works
Single-Cell Transcriptome Sequencing Using Microfluidics
Chen, Y., Jung, S., Choi, Y., & Yoon, E. (2021) · Springer eBooks · doi:10.1007/978-981-10-8953-4_42 · Cited by 4 · see citing works
Kim, H., Choi, S., Heo, H., Cho, S. H., Lee, Y., Kim, D., Jung, K. O., & Rhee, S. (2024) · International Journal of Stem Cells · doi:10.15283/ijsc23183 · Cited by 3 · see citing works
Single-Cell Transcriptomics and Computational Frameworks for Target Discovery in Cancer
Tarozzi, M. E., Derus, N. R., Polizzi, S., Sala, C., & Castellani, G. (2026) · Targets · doi:10.3390/targets4010006 · Cited by 3 · see citing works
Cell-State-Specific Drug Responses are Associated With Differences in Signaling Network Wiring
Krämer, N., van Eijl, R. A. P. M., Stohn, T., Tanis, S. E. J., Wessels, L. F. A., Bosdriesz, E., & Mulder, K. W. (2026) · Molecular & Cellular Proteomics · doi:10.1016/j.mcpro.2026.101529 · Cited by 3 · see citing works
Self-citationThe role of single-cell sequencing in studying tumour evolution
Mossner, M., Baker, A., & Graham, T. A. (2021) · Faculty Reviews · doi:10.12703/r/10-49 · Cited by 3 · see citing works
Wong, M. H., Kosman, C., Takahashi, L., & Ramalingam, N. (2021) · Methods in molecular biology · doi:10.1007/978-1-0716-1771-7_15 · Cited by 3 · see citing works
Brain-wide monosynaptic single-neuron connectivity with ROInet-seqPreprint
Lin, Z., Ophir, O., Trimbuch, T., Brokowski, B., Tibi, M., Schmidt, H., Rosenmund, C., Hochgerner, H., & Zeisel, A. (2024) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2024.04.04.588058 · Cited by 3 · see citing works
Sequencing-based methods for single-cell multi-omics studies
Qin, S., Liu, S., & Weng, X. (2023) · Science China Chemistry · doi:10.1007/s11426-023-1793-7 · Cited by 2 · see citing works
Recent progress in co-detection of single-cell transcripts and proteins
Huang, S., Fan, Q., Wang, Y., Huang, Z., Shi, W., Gong, Y., Yang, T., Wang, J., Wu, L., & Yang, C. J. (2023) · Nano Research · doi:10.1007/s12274-023-5924-3 · Cited by 2 · see citing works
Li, Y., Li, W., Chen, J., Qiu, S., Liu, Y., Xu, L., Tian, T., & Li, J. P. (2023) · Bioorganic Chemistry · doi:10.1016/j.bioorg.2023.106987 · Cited by 2 · see citing works
Total-mRNA-Aware Analysis for Droplet-Based Single Cell SequencingPreprint
Lian, Q., Ma, J., Hua, K., Rong, Z., Cai, J., Jiang, X., Zhou, J., Xu, J., Zhang, Z., Fan, L., et al. (2022) · Research Square · doi:10.21203/rs.3.rs-2211167/v1 · Cited by 2 · see citing works
Signalling-state dependent drug-tolerance in head and neck squamous cell carcinomaPreprint
Karjosukarso, D. W., Dini, A., Wingens, L., Liu, R., Joosten, L. A. B., Bussink, J., & Mulder, K. W. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.12.05.570063 · Cited by 2 · see citing works
Self-citationStochastic variation in the FOXM1 transcription program mediates replication stress tolerance
Segeren, H. A., Wierenga, K. A., Riemers, F. M., van Liere, E. A., & Westendorp, B. (2025) · Molecular Oncology · doi:10.1002/1878-0261.13819 · Cited by 1 · see citing works
van Oosterom, F., Gankema, A. A. F., Rojas-Rodríguez, F., Hoogendijk, A. J., & Kuijpers, T. W. (2026) · Frontiers in Immunology · doi:10.3389/fimmu.2026.1814355 · Cited by 1 · see citing works
Understanding developing kidneys and Wilms tumors one cell at a time
Pop, N. S., Dolt, K. S., & Hohenstein, P. (2025) · Current topics in developmental biology/Current Topics in Developmental Biology · doi:10.1016/bs.ctdb.2024.11.005 · Cited by 1 · see citing works
Xue, Y., Qi, J., Xie, G., Wang, M., Xu, W., Ma, C., Xu, X., Yang, Y., He, Y., Guo, Y. L., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.05.26.653374 · Cited by 1 · see citing works
Single-Cell Transcriptome Sequencing Using Microfluidics
Chen, Y., Jung, S., Choi, Y., & Yoon, E. (2020) · Springer eBooks · doi:10.1007/978-981-10-4857-9_42-1
Single Cell Sequencing, Its Application and Future Challenges
Saleem, M., Alam, S., Kainat, I., Iftikhar, R., & Ijaz, A. (2021) · Current Trends in OMICS · doi:10.32350/cto.11.05
Bouwers, E. G. (2011) · PUB – Publications at Bielefeld University (Bielefeld University)
van Buijtenen, E., Janssen, W., Vink, P. M., Habraken, M., Wingens, L. J. A., van Elsas, A., Huck, W. T. S., van Buggenum, J. A. G. L., & van Eenennaam, H. (2022) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2022.03.31.486501
Self-citationSingle-Cell Technologies: Advances in Single-Cell Migration and Multi-Omics
Moarefian, M., Capossela, A. M., Eom, R., & Aran, K. (2022) · GEN Biotechnology · doi:10.1089/genbio.2022.0014
Liakh, I., Durnyak, B., & Babichev, S. A. (2021) · Printing and Publishing · doi:10.32403/0554-4866-2021-2-82-92-103
Tools for Kidney Tissue Analysis
Melk, A. (2023) · Springer eBooks · doi:10.1007/978-3-031-11665-0_5
Assessing the Influence of Selected Permeabilization Methods on Lymphocyte Single-Cell Multi-Omics
Ding, S., Lu, N., & Abolhassani, H. (2025) · Antibodies · doi:10.3390/antib14010015
Hu, J., Park, J. S., Lei, H., Akarapipad, P., Sun, J., Park, D. J., Cui, W., & Wang, T. (2025) · medRxiv · doi:10.1101/2025.08.31.25334810
Jiménez-Gracia, L., Marchese, D., Nieto, J. C., Caratù, G., Melón-Ardanaz, E., Gudiño, V., Roth, S., Wise, K., Ryan, N. K., Jensen, K. B., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26699438
Jiménez-Gracia, L., Marchese, D., Nieto, J. C., Caratù, G., Melón-Ardanaz, E., Gudiño, V., Roth, S., Wise, K., Ryan, N. K., Jensen, K. B., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26699426
Jiménez-Gracia, L., Marchese, D., Nieto, J. C., Caratù, G., Melón-Ardanaz, E., Gudiño, V., Roth, S., Wise, K., Ryan, N. K., Jensen, K. B., et al. (2024) · Figshare · doi:10.6084/m9.figshare.25511855
Jiménez-Gracia, L., Marchese, D., Nieto, J. C., Caratù, G., Melón-Ardanaz, E., Gudiño, V., Roth, S., Wise, K., Ryan, N. K., Jensen, K. B., et al. (2024) · Figshare · doi:10.6084/m9.figshare.26699444
- Authors
- Gerlach, J. P., van Buggenum, J. A. G., Tanis, S. E. J., Hogeweg, M., Heuts, B. M. H., Muraro, M. J., Elze, L., Rivello, F., Rakszewska, A., van Oudenaarden, A., Huck, W. T. S., Stunnenberg, H. G., & Mulder, K. W.
- Affiliations
- Radboud University Nijmegen (NL)
- Royal Netherlands Academy of Arts and Sciences (NL)
- Corresponding author
- Mulder, Klaas W.
- ORCID
- Venue
- Scientific Reports
- Published
- 2019-02-06
- Volume
- 9
- Issue
- 1
- Pages
- 1469-1469
- ISSN
- 2045-2322 (ISSN-L)
- PMC
- PMC6365588
- OpenAlex
- W2810689242
- Cited by
- 104
- References
- 35
- Citations by year
- 2026: 10 · 2025: 11 · 2024: 13 · 2023: 21 · 2022: 15 · 2021: 20 · 2020: 8 · 2019: 5
- FWCI
- 3.97
- Type
- journal article
- Language
- en
- Open access
- gold
- doi.org
- Locations
- Scientific Reports (publishedVersion, cc-by)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion)
- Europe PMC (PubMed Central) (publishedVersion, other-oa)
- PubMed Central (publishedVersion, cc-by)
- PubMed (publishedVersion)
- KNAW research portal (Royal Academy of Art and Sciences (KNAW)) (publishedVersion, other-oa)
- Data Archiving and Networked Services (DANS) (submittedVersion, other-oa)
- DOAJ (DOAJ: Directory of Open Access Journals) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion)
- Radboud Repository (Radboud University) (submittedVersion, other-oa)
- Funders
- EC | European Research Council (339431)
- Nederlandse Organisatie voor Wetenschappelijk Onderzoek (864.12.010)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Single-cell and spatial transcriptomics
- Physical Sciences › Chemistry › Spectroscopy › Advanced Proteomics Techniques and Applications
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Molecular Biology Techniques and Applications
- Keywords
- single-cell proteomics, phosphoproteomics, transcriptome, protein expression, keratinocytes, keratinocyte differentiation, focal adhesion kinase phosphorylation, stem cell markers, cellular heterogeneity, environmental stimuli
- MeSH terms
- Cell Differentiation, Cells, Cultured, Gene Expression Regulation, Humans, Phosphorylation, Quinazolines, Keratinocytes, Tissue Fixation, Tyrphostins, Gene Expression Profiling, Proteomics, Focal Adhesion Kinase 1, Single-Cell Analysis
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