Multi-omic Profiling Reveals Dynamics of the Phased Progression of Pluripotency
Open accessPublished version of a preprint
Abstract
Pluripotency is highly dynamic and progresses through a continuum of pluripotent stem cell states. The two states that bookend the pluripotency continuum, naive and primed, are well characterized, but our understanding of the intermediate states and transitions between them remains incomplete. Here, we dissect the dynamics of pluripotent state transitions underlying pre- to post-implantation epiblast differentiation. Through comprehensive mapping of the proteome, phosphoproteome, transcriptome, and epigenome of embryonic stem cells transitioning from naive to primed pluripotency, we find that rapid, acute, and widespread changes to the phosphoproteome precede ordered changes to the epigenome, transcriptome, and proteome. Reconstruction of the kinase-substrate networks reveals signaling cascades, dynamics, and crosstalk. Distinct waves of global proteomic changes mark discrete phases of pluripotency, with cell-state-specific surface markers tracking pluripotent state transitions. Our data provide new insights into multi-layered control of the phased progression of pluripotency and a foundation for modeling mechanisms regulating pluripotent state transitions (www.stemcellatlas.org).
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.
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
Moderated estimation of fold change and dispersion for RNA-seq data with DESeq2
Love, M. I., Huber, W., & Anders, S. (2014) · Genome Biology · doi:10.1186/s13059-014-0550-8 · Cited by 95,106 · see citing works
STAR: ultrafast universal RNA-seq aligner
Dobin, A., Davis, C. A., Schlesinger, F., Drenkow, J., Zaleski, C., Jha, S., Batut, P., Chaisson, M., & Gingeras, T. R. (2013) · Bioinformatics · doi:10.1093/bioinformatics/bts635 · Cited by 51,709 · see citing works
Robinson, M. D., McCarthy, D. J., & Smyth, G. K. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp616 · Cited by 41,364 · see citing works
limma powers differential expression analyses for RNA-sequencing and microarray studies
Ritchie, M. E., Phipson, B., Wu, D., Hu, Y., Law, C. W., Shi, W., & Smyth, G. K. (2015) · Nucleic Acids Research · doi:10.1093/nar/gkv007 · Cited by 40,458 · see citing works
Ultrafast and memory-efficient alignment of short DNA sequences to the human genome.
Langmead, B., Trapnell, C., Pop, M., & Salzberg, S. L. (2009) · Genome Biology · doi:10.1186/gb-2009-10-3-r25 · Cited by 21,849 · see citing works
HTSeq—a Python framework to work with high-throughput sequencing data
Anders, S., Pyl, P. T., & Huber, W. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btu638 · Cited by 21,464 · see citing works
Cox, J., & Mann, M. (2008) · Nature Biotechnology · doi:10.1038/nbt.1511 · Cited by 14,855 · see citing works
Self-citationIn silico prediction of protein-protein interactions in human macrophages
Souiai, O., Guerfali, F. Z., Miled, S. B., Brun, C., & Benkahla, A. (2014) · BMC Research Notes · doi:10.1186/1756-0500-7-157 · Cited by 10,785 · see citing works
Significance analysis of microarrays applied to the ionizing radiation response
Tusher, V. G., Tibshirani, R., & Chu, G. (2001) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.091062498 · Cited by 10,568 · see citing works
Adjusting batch effects in microarray expression data using empirical Bayes methods
Johnson, W. E., Li, C., & Rabinovic, A. (2007) · Biostatistics · doi:10.1093/biostatistics/kxj037 · Cited by 8,658 · see citing works
Global quantification of mammalian gene expression control
Schwanhäusser, B., Busse, D., Li, N., Dittmar, G., Schuchhardt, J., Wolf, J., Chen, W., & Selbach, M. (2011) · Nature · doi:10.1038/nature10098 · Cited by 6,566 · see citing works
The MaxQuant computational platform for mass spectrometry-based shotgun proteomics
Tyanova, S., Temu, T., & Cox, J. (2016) · Nature Protocols · doi:10.1038/nprot.2016.136 · Cited by 4,691 · see citing works
Gene Ontology Consortium: going forward
The Gene Ontology Consortium (2015) · Nucleic Acids Research · doi:10.1093/nar/gku1179 · Cited by 3,492 · see citing works
The ground state of embryonic stem cell self-renewal
Ying, Q.-L., Wray, J., Nichols, J., Batlle-Morera, L., Doble, B., Woodgett, J., Cohen, P., & Smith, A. (2008) · Nature · doi:10.1038/nature06968 · Cited by 3,442 · see citing works
Mass-spectrometric exploration of proteome structure and function
Aebersold, R., & Mann, M. (2016) · Nature · doi:10.1038/nature19949 · Cited by 2,334 · see citing works
Self-citationBioMart and Bioconductor: a powerful link between biological databases and microarray data analysis
Durinck, S., Moreau, Y., Kasprzyk, A., Davis, S. R., Moor, B. D., Brāzma, A., & Huber, W. K. (2005) · Computer applications in the biosciences · doi:10.1093/bioinformatics/bti525 · Cited by 2,327 · see citing works
BEDTools: The Swiss‐Army Tool for Genome Feature Analysis
Quinlan, A. R. (2014) · Current Protocols in Bioinformatics · doi:10.1002/0471250953.bi1112s47 · Cited by 2,286 · see citing works
New cell lines from mouse epiblast share defining features with human embryonic stem cells
Tesar, P. J., Chenoweth, J. G., Brook, F. A., Davies, T. J., Evans, E. P., Mack, D. L., Gardner, R. L., & McKay, R. D. G. (2007) · Nature · doi:10.1038/nature05972 · Cited by 2,153 · see citing works
The Fibroblast Growth Factor signaling pathway
Ornitz, D. M., & Itoh, N. (2015) · WIREs Developmental Biology · doi:10.1002/wdev.176 · Cited by 2,050 · see citing works
Derivation of pluripotent epiblast stem cells from mammalian embryos
Brons, I. G. M., Smithers, L. E., Trotter, M. W. B., Rugg‐Gunn, P. J., Sun, B., Lopes, S. M. C. D. S., Howlett, S., Clarkson, A., Ährlund‐Richter, L., Pedersen, R. A., et al. (2007) · Nature · doi:10.1038/nature05950 · Cited by 2,007 · see citing works
Naive and Primed Pluripotent States
Nichols, J., & Smith, A. G. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.05.015 · Cited by 1,835 · see citing works
The Ras-ERK and PI3K-mTOR pathways: cross-talk and compensation
Mendoza, M. C., Er, E. E., & Blenis, J. (2011) · Trends in Biochemical Sciences · doi:10.1016/j.tibs.2011.03.006 · Cited by 1,817 · see citing works
Single-cell RNA-Seq profiling of human preimplantation embryos and embryonic stem cells
Yan, L., Yang, M., Guo, H., Yang, L., Wu, J., Li, R., Liu, P., Lian, Y., Zheng, X., Yan, J., et al. (2013) · Nature Structural & Molecular Biology · doi:10.1038/nsmb.2660 · Cited by 1,740 · see citing works
Kulak, N. A., Pichler, G., Paron, I., Nagaraj, N., & Mann, M. (2014) · Nature Methods · doi:10.1038/nmeth.2834 · Cited by 1,719 · see citing works
Self-citationHornbeck, P. V., Kornhauser, J. M., Tkachev, S., Zhang, B., Skrzypek, E., Murray, B. W., Latham, V. M., & Sullivan, M. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr1122 · Cited by 1,636 · see citing works
Reconstitution of the mouse germ cell specification pathway in culture by pluripotent stem cells.
Hayashi, K., Ohta, H., Kurimoto, K., Aramaki, S., & Saitou, M. (2011) · Cell · doi:10.1016/j.cell.2011.06.052 · Cited by 1,324 · see citing works
Global signatures of protein and mRNA expression levels
de Sousa Abreu, R., Penalva, L. O., Marcotte, E. M., & Vogel, C. (2009) · Molecular BioSystems · doi:10.1039/b908315d · Cited by 1,248 · see citing works
Yu, J., & Cui, W. (2016) · Development · doi:10.1242/dev.137075 · Cited by 1,137 · see citing works
Single-Cell RNA-Seq Reveals Lineage and X Chromosome Dynamics in Human Preimplantation Embryos
Petropoulos, S., Edsgärd, D., Reinius, B., Deng, Q., Panula, S. P., Codeluppi, S., Plaza Reyes, A., Linnarsson, S., Sandberg, R., & Lanner, F. (2016) · Cell · doi:10.1016/j.cell.2016.03.023 · Cited by 1,063 · see citing works
Derivation of novel human ground state naive pluripotent stem cells
Gafni, O., Weinberger, L., Mansour, A. A., Manor, Y. S., Chomsky, E., Ben‐Yosef, D., Kalma, Y., Viukov, S. V., Maza, I., Zviran, A., et al. (2013) · Nature · doi:10.1038/nature12745 · Cited by 1,047 · see citing works
Resetting Transcription Factor Control Circuitry toward Ground-State Pluripotency in Human
Takashima, Y., Guo, G., Loos, R., Nichols, J., Ficz, G., Krueger, F., Oxley, D., Santos, F., Clarke, J., Mansfield, W., et al. (2014) · Cell · doi:10.1016/j.cell.2014.08.029 · Cited by 980 · see citing works
Sharma, K., D’Souza, R. C. J., Tyanova, S., Schaab, C., Wiśniewski, J. R., Cox, J., & Mann, M. (2014) · Cell Reports · doi:10.1016/j.celrep.2014.07.036 · Cited by 971 · see citing works
Self-citationA unique regulatory phase of DNA methylation in the early mammalian embryo
Smith, Z. D., Chan, M. M., Mikkelsen, T. S., Gu, H., Gnirke, A., Regev, A., & Meissner, A. (2012) · Nature · doi:10.1038/nature10960 · Cited by 964 · see citing works
Theunissen, T. W., Powell, B. E., Wang, H., Mitalipova, M., Faddah, D. A., Reddy, J., Fan, Z. P., Maetzel, D., Ganz, K., Shi, L., et al. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.07.002 · Cited by 888 · see citing works
The Transcriptional and Epigenomic Foundations of Ground State Pluripotency
Marks, H., Kalkan, T., Menafra, R., Denissov, S., Jones, K. A., Hofemeister, H., Nichols, J., Kranz, A., Stewart, A., Smith, A. G., et al. (2012) · Cell · doi:10.1016/j.cell.2012.03.026 · Cited by 881 · see citing works
A parallel circuit of LIF signalling pathways maintains pluripotency of mouse ES cells
Niwa, H., Ogawa, K., Shimosato, D., & Adachi, K. (2009) · Nature · doi:10.1038/nature08113 · Cited by 872 · see citing works
Deutsch, E. W., Csordás, A., Sun, Z., Jarnuczak, A. F., Pérez‐Riverol, Y., Ternent, T., Campbell, D. S., Llinares, M. B., Okuda, S., Kawano, S., et al. (2016) · Nucleic Acids Research · doi:10.1093/nar/gkw936 · Cited by 864 · see citing works
A Molecular Roadmap of Reprogramming Somatic Cells into iPS Cells
Polo, J. M., Anderssen, E., Walsh, R. M., Schwarz, B. A., Nefzger, C. M., Lim, S. M., Borkent, M., Apostolou, E., Alaei, S., Cloutier, J., et al. (2012) · Cell · doi:10.1016/j.cell.2012.11.039 · Cited by 861 · see citing works
Flicek, P., Amode, M. R., Barrell, D. G., Beal, K. M., Brent, S., Carvalho‐Silva, D., Clapham, P., Coates, G. M. P., Fairley, S., Fitzgerald, S. F., et al. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr991 · Cited by 818 · see citing works
Kunath, T., Saba-El-Leil, M. K., Almosailleakh, M., Wray, J. P., Meloche, S., & Smith, A. G. (2007) · Development · doi:10.1242/dev.02880 · Cited by 785 · see citing works
Next-generation proteomics: towards an integrative view of proteome dynamics
Altelaar, M. A. F., Muñoz, J., & Heck, A. J. R. (2012) · Nature Reviews Genetics · doi:10.1038/nrg3356 · Cited by 776 · see citing works
Improved visualization of protein consensus sequences by iceLogo
Colaert, N., Helsens, K., Martens, L., Vandekerckhove, J. S., & Gevaert, K. (2009) · Nature Methods · doi:10.1038/nmeth1109-786 · Cited by 746 · see citing works
Dynamic stem cell states: Naive to primed pluripotency in rodents and humans
Weinberger, L., Ayyash, M., Novershtern, N., & Hanna, J. H. (2016) · Nature Reviews Molecular Cell Biology · doi:10.1038/nrm.2015.28 · Cited by 622 · see citing works
Critical function of Prdm14 for the establishment of the germ cell lineage in mice
Yamaji, M., Seki, Y., Kurimoto, K., Yabuta, Y., Yuasa, M., Shigeta, M., Yamanaka, K., Ohinata, Y., & Saitou, M. (2008) · Nature Genetics · doi:10.1038/ng.186 · Cited by 592 · see citing works
Negative feedback regulation of the ERK1/2 MAPK pathway
Lake, D., Corrêa, S. A. L., & Müller, J. (2016) · Cellular and Molecular Life Sciences · doi:10.1007/s00018-016-2297-8 · Cited by 565 · see citing works
Cooperative Binding of Transcription Factors Orchestrates Reprogramming
Chronis, C., Fiziev, P., Papp, B., Butz, S., Bonora, G., Sabri, S., Ernst, J., & Plath, K. (2017) · Cell · doi:10.1016/j.cell.2016.12.016 · Cited by 555 · see citing works
Wiśniewski, J. R., Zougman, A., & Mann, M. (2009) · Journal of Proteome Research · doi:10.1021/pr900748n · Cited by 545 · see citing works
Self-citationDirect interaction between DNMT1 and G9a coordinates DNA and histone methylation during replicationPreprint
Estève, P., Chin, H. G., Smallwood, A., Feehery, G. R., Gangisetty, O., Karpf, A. R., Carey, M., & Pradhan, S. (2006) · Genes & Development · doi:10.1101/gad.1463706 · Cited by 539 · see citing works
Dual‐specificity MAP kinase phosphatases (MKPs): Shaping the outcome of MAP kinase signalling
Caunt, C. J., & Keyse, S. M. (2013) · The FEBS Journal · doi:10.1111/j.1742-4658.2012.08716.x · Cited by 535 · see citing works
Methylation of Histone H3 at Lys-9 Is an Early Mark on the X Chromosome during X Inactivation
Heard, É., Rougeulle, C., Arnaud, D., Avner, P. R., Allis, C. D., & Spector, D. L. (2001) · Cell · doi:10.1016/s0092-8674(01)00598-0 · Cited by 513 · see citing works
Reorganization of enhancer patterns in transition from naive to primed pluripotency
Buecker, C., Srinivasan, R., Wu, Z., Calo, E., Acampora, D., Faial, T., Simeone, A., Tan, M., Swigut, T., & Wysocka, J. (2014) · Cell Stem Cell · doi:10.1016/j.stem.2014.04.003 · Cited by 507 · see citing works
Genenames.org: the HGNC resources in 2015
Gray, K. A., Yates, B., Seal, R. L., Wright, M. W., & Bruford, E. A. (2014) · Nucleic Acids Research · doi:10.1093/nar/gku1071 · Cited by 493 · see citing works
Derivation of naïve human embryonic stem cells
Ware, C. B., Nelson, A. M., Mecham, B. H., Hesson, J., Zhou, W., Jonlin, E. C., Jiménez‐Caliani, A. J., Deng, X., Cavanaugh, C., Cook, S. M., et al. (2014) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.1319738111 · Cited by 470 · see citing works
Defining the three cell lineages of the human blastocyst by single-cell RNA-seq
Blakeley, P., Fogarty, N. M. E., del Valle, I., Wamaitha, S. E., Hu, T. X., Elder, K. T., Snell, P., Christie, L., Robson, P., & Niakan, K. K. (2015) · Development · doi:10.1242/dev.123547 · Cited by 466 · see citing works
High-throughput phosphoproteomics reveals in vivo insulin signaling dynamics
Humphrey, S. J., Azimifar, S. B., & Mann, M. (2015) · Nature Biotechnology · doi:10.1038/nbt.3327 · Cited by 460 · see citing works
Self-citationRigbolt, K. T. G., Prokhorova, T. A., Akimov, V., Henningsen, J., Johansen, P. T., Kratchmarova, I., Kassem, M., Mann, M., Olsen, J. V., & Blagoev, B. (2011) · Science Signaling · doi:10.1126/scisignal.2001570 · Cited by 451 · see citing works
Self-citationFormative pluripotency: the executive phase in a developmental continuum
Smith, A. G. (2017) · Development · doi:10.1242/dev.142679 · Cited by 449 · see citing works
Boroviak, T., Loos, R., Bertone, P., Smith, A. G., & Nichols, J. (2014) · Nature Cell Biology · doi:10.1038/ncb2965 · Cited by 440 · see citing works
G9a/GLP complexes independently mediate H3K9 and DNA methylation to silence transcription
Tachibana, M., Matsumura, Y., Fukuda, M., Kimura, H., & Shinkai, Y. (2008) · The EMBO Journal · doi:10.1038/emboj.2008.192 · Cited by 431 · see citing works
Boroviak, T., Loos, R., Lombard, P., Okahara, J., Behr, R., Sasaki, E., Nichols, J., Smith, A. G., & Bertone, P. (2015) · Developmental Cell · doi:10.1016/j.devcel.2015.10.011 · Cited by 421 · see citing works
The role of FGF/Erk signaling in pluripotent cells
Lanner, F., & Rossant, J. (2010) · Development · doi:10.1242/dev.050146 · Cited by 404 · see citing works
Regulatory Principles of Pluripotency: From the Ground State Up
Hackett, J. A., & Surani, M. A. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.09.015 · Cited by 404 · see citing works
Chan, Y.-S., Göke, J., Ng, J.-H., Lu, X., Gonzales, K. A. U., Tan, C.-P., Tng, W. J., Hong, Z.-Z., Lim, Y. S., & Ng, H. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.11.015 · Cited by 392 · see citing works
Angeles, A. D. L., Ferrari, F., Xi, R., Fujiwara, Y., Benvenisty, N., Deng, H., Hochedlinger, K., Jaenisch, R., Lee, S., Leitch, H. G., et al. (2015) · Nature · doi:10.1038/nature15515 · Cited by 390 · see citing works
High-throughput and high-sensitivity phosphoproteomics with the EasyPhos platform
Humphrey, S. J., Karayel, Ö., James, D. E., & Mann, M. (2018) · Nature Protocols · doi:10.1038/s41596-018-0014-9 · Cited by 359 · see citing works
Self-citationPhosphorylation Is a Central Mechanism for Circadian Control of Metabolism and Physiology
Robles, M. S., Humphrey, S. J., & Mann, M. (2016) · Cell Metabolism · doi:10.1016/j.cmet.2016.10.004 · Cited by 355 · see citing works
Self-citationBetschinger, J., Nichols, J., Dietmann, S., Corrin, P. D., Paddison, P. J., & Smith, A. G. (2013) · Cell · doi:10.1016/j.cell.2013.03.012 · Cited by 335 · see citing works
Phosphorylation Dynamics during Early Differentiation of Human Embryonic Stem Cells
Hoof, D. V., Muñoz, J., Braam, S. R., Pinkse, M. W. H., Linding, R., Heck, A. J. R., Mummery, C. L., & Krijgsveld, J. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.05.021 · Cited by 323 · see citing works
Illuminating the dark phosphoproteome
Needham, E. J., Parker, B. L., Burykin, T., James, D. E., & Humphrey, S. J. (2019) · Science Signaling · doi:10.1126/scisignal.aau8645 · Cited by 322 · see citing works
Self-citationKojima, Y., Kaufman‐Francis, K., Studdert, J. B., Steiner, K. A., Power, M., Loebel, D. A. F., Jones, V. J., Hor, A. C. C., de Alencastro, G., Logan, G. J., et al. (2013) · Cell stem cell · doi:10.1016/j.stem.2013.09.014 · Cited by 303 · see citing works
AnimalTFDB: a comprehensive animal transcription factor database
Zhang, H., Chen, H., Liu, W., Liu, H., Gong, J., Wang, H., & Guo, A.-Y. (2011) · Nucleic Acids Research · doi:10.1093/nar/gkr965 · Cited by 301 · see citing works
Yamaji, M., Ueda, J., Hayashi, K., Ohta, H., Yabuta, Y., Kurimoto, K., Nakato, R., Yamada, Y., Shirahige, K., & Saitou, M. (2013) · Cell stem cell · doi:10.1016/j.stem.2012.12.012 · Cited by 294 · see citing works
Ishihama, Y., Rappsilber, J., & Mann, M. (2006) · Journal of Proteome Research · doi:10.1021/pr050385q · Cited by 285 · see citing works
Self-citationPastor, W. A., Chen, D., Liu, W., Kim, R., Sahakyan, A., Lukianchikov, A., Plath, K., Jacobsen, S. E., & Clark, A. T. (2016) · Cell stem cell · doi:10.1016/j.stem.2016.01.019 · Cited by 284 · see citing works
Inhibition of mTOR induces a paused pluripotent state
Bulut-Karslioglu, A., Biechele, S., Jin, H., Macrae, T. A., Hejna, M., Gertsenstein, M., Song, J. S., & Ramalho-Santos, M. (2016) · Nature · doi:10.1038/nature20578 · Cited by 283 · see citing works
Tracking the embryonic stem cell transition from ground state pluripotency
Kalkan, T., Olova, N. N., Roode, M., Mulas, C., Lee, H. J., Nett, I. R. E., Marks, H., Walker, R. V., Stunnenberg, H. G., Lilley, K. S., et al. (2017) · Development · doi:10.1242/dev.142711 · Cited by 281 · see citing works
Prolonged Mek1/2 suppression impairs the developmental potential of embryonic stem cells
Choi, J., Huebner, A. J., Clement, K., Walsh, R. M., Savol, A. J., Lin, K., Gu, H., Stefano, B. D., Brumbaugh, J., Kim, S. Y., et al. (2017) · Nature · doi:10.1038/nature23274 · Cited by 272 · see citing works
Phosphoproteomics in the Age of Rapid and Deep Proteome Profiling
Riley, N. M., & Coon, J. J. (2016) · Analytical Chemistry · doi:10.1021/acs.analchem.5b04123 · Cited by 265 · see citing works
New Insights into Early Human Development: Lessons for Stem Cell Derivation and Differentiation
Rossant, J., & Tam, P. (2017) · Cell stem cell · doi:10.1016/j.stem.2016.12.004 · Cited by 251 · see citing works
Pluripotent state transitions coordinate morphogenesis in mouse and human embryos
Shahbazi, M. N., Scialdone, A., Skorupska, N., Weberling, A., Recher, G., Zhu, M., Jędrusik, A., Devito, L., Noli, L., Macaulay, I. C., et al. (2017) · Nature · doi:10.1038/nature24675 · Cited by 249 · see citing works
Integrative Analyses of Human Reprogramming Reveal Dynamic Nature of Induced Pluripotency
Cacchiarelli, D., Trapnell, C., Ziller, M. J., Soumillon, M., Cesana, M., Karnik, R., Donaghey, J., Smith, Z. D., Ratanasirintrawoot, S., Zhang, X., et al. (2015) · Cell · doi:10.1016/j.cell.2015.06.016 · Cited by 228 · see citing works
A draft map of the mouse pluripotent stem cell spatial proteome
Christoforou, A., Mulvey, C. M., Breckels, L. M., Geladaki, A., Hurrell, T., Hayward, P. C., Naake, T., Gatto, L., Viner, R., Arias, A. M., et al. (2016) · Nature Communications · doi:10.1038/ncomms9992 · Cited by 221 · see citing works
Oldfield, A., Yang, P., Conway, A. E., Cinghu, S., Freudenberg, J., Yellaboina, S., & Jothi, R. (2014) · Molecular Cell · doi:10.1016/j.molcel.2014.07.005 · Cited by 216 · see citing works
Self-citationEpiblast Stem Cell Subpopulations Represent Mouse Embryos of Distinct Pregastrulation Stages
Han, D., Tàpia, N., Joo, J. Y., Greber, B., Araúzo-Bravo, M. J., Bernemann, C., Ko, K., Wu, G., Stehling, M., Tae, J., et al. (2010) · Cell · doi:10.1016/j.cell.2010.10.015 · Cited by 203 · see citing works
Swaney, D. L., Wenger, C. D., Thomson, J. A., & Coon, J. J. (2009) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0811964106 · Cited by 192 · see citing works
Phosphoproteomic Analysis of Human Embryonic Stem Cells
Brill, L. M., Xiong, W., Lee, K., Ficarro, S. B., Crain, A., Xu, Y., Terskikh, A. V., Snyder, E. Y., & Ding, S. (2009) · Cell stem cell · doi:10.1016/j.stem.2009.06.002 · Cited by 189 · see citing works
In Vivo Differentiation Potential of Epiblast Stem Cells Revealed by Chimeric Embryo Formation
Huang, Y., Osorno, R., Tsakiridis, A., & Wilson, V. A. (2012) · Cell Reports · doi:10.1016/j.celrep.2012.10.022 · Cited by 184 · see citing works
Kurimoto, K., Yabuta, Y., Hayashi, K., Ohta, H., Kiyonari, H., Mitani, T., Moritoki, Y., Kohri, K., Kimura, H., Yamamoto, T., et al. (2015) · Cell Stem Cell · doi:10.1016/j.stem.2015.03.002 · Cited by 182 · see citing works
Collier, A. J., Panula, S., Schell, J. P., Chovanec, P., Reyes, Á. P., Sophie Petropoulos, A., Corcoran, A. E., Walker, R. V., Douagi, I., Lanner, F., et al. (2017) · Cell stem cell · doi:10.1016/j.stem.2017.02.014 · Cited by 178 · see citing works
Beck, S., Michalski, A., Raether, O., Lubeck, M., Kaspar, S., Goedecke, N., Baessmann, C., Hornburg, D., Meier, F., Paron, I., et al. (2015) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m114.047407 · Cited by 176 · see citing works
Self-citationDynamic Pluripotent Stem Cell States and Their Applications
Wu, J., & Belmonte, J. C. I. (2015) · Cell stem cell · doi:10.1016/j.stem.2015.10.009 · Cited by 163 · see citing works
Factor, D. C., Corradin, O., Zentner, G. E., Saiakhova, A., Song, L., Chenoweth, J. G., McKay, R. D. G., Crawford, G. E., Scacheri, P. C., & Tesar, P. J. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.05.005 · Cited by 159 · see citing works
The pluripotent state in mouse and human
Davidson, K. C., Mason, E. A., & Pera, M. F. (2015) · Development · doi:10.1242/dev.116061 · Cited by 155 · see citing works
Huang, K. Y., Maruyama, T., & Fan, G. (2014) · Cell stem cell · doi:10.1016/j.stem.2014.09.014 · Cited by 149 · see citing works
Shirane, K., Kurimoto, K., Yabuta, Y., Yamaji, M., Satoh, J., Ito, S., Watanabe, A., Hayashi, K., Saitou, M., & Sasaki, H. (2016) · Developmental Cell · doi:10.1016/j.devcel.2016.08.008 · Cited by 120 · see citing works
Chen, A. F., Liu, A. J., Krishnakumar, R., Freimer, J. W., DeVeale, B., & Blelloch, R. H. (2018) · Cell stem cell · doi:10.1016/j.stem.2018.06.005 · Cited by 95 · see citing works
Large‐scale identification of proteins expressed in mouse embryonic stem cells
Nagano, K., Taoka, M., Yamauchi, Y., Itagaki, C., Shinkawa, T., Nunomura, K., Okamura, N., Takahashi, N., Izumi, T., & Isobe, T. (2005) · PROTEOMICS · doi:10.1002/pmic.200400990 · Cited by 89 · see citing works
Tsanov, K. M., Pearson, D. S., Wu, Z., Han, A., Triboulet, R., Seligson, M. T., Powers, J. T., Osborne, J. K., Kane, S., Gygi, S. P., et al. (2016) · Nature Cell Biology · doi:10.1038/ncb3453 · Cited by 78 · see citing works
Prospective Isolation of Rare Poised iPSC Intermediates Reveals Principles of Cellular Reprogramming
Schwarz, B. A., Çetinbas, M., Clement, K., Walsh, R. M., Cheloufi, S., Gu, H., Langkabel, J., Kamiya, A., Schorle, H., Meissner, A., et al. (2018) · Cell Stem Cell · doi:10.1016/j.stem.2018.06.013 · Cited by 69 · see citing works
Cripto is essential to capture mouse epiblast stem cell and human embryonic stem cell pluripotency
Fiorenzano, A., Pascale, E., D’Aniello, C., Acampora, D., Bassalert, C., Russo, F., Andolfi, G., Biffoni, M., Francescangeli, F., Zeuner, A., et al. (2016) · Nature Communications · doi:10.1038/ncomms12589 · Cited by 64 · see citing works
Pines, A., Kelstrup, C. D., Vrouwe, M. G., Puigvert, J. C., Typas, D., Mišovic, B., de Groot, A., von Stechow, L., van de Water, B., Danen, E. H. J., et al. (2011) · Molecular and Cellular Biology · doi:10.1128/mcb.05258-11 · Cited by 61 · see citing works
Pluripotency and Nuclear Reprogramming
Déjosez, M., & Zwaka, T. P. (2012) · Annual Review of Biochemistry · doi:10.1146/annurev-biochem-052709-104948 · Cited by 44 · see citing works
Knowledge-Based Analysis for Detecting Key Signaling Events from Time-Series Phosphoproteomics Data
Yang, P., Zheng, X., Jayaswal, V., Hu, G., Yang, J. Y. H., & Jothi, R. (2015) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1004403 · Cited by 39 · see citing works
Self-citationYang, P., Humphrey, S. J., James, D. E., Yang, J. Y. H., & Jothi, R. (2015) · Bioinformatics · doi:10.1093/bioinformatics/btv550 · Cited by 38 · see citing works
Self-citationNegative feedback via RSK modulates Erk‐dependent progression from naïve pluripotency
Nett, I. R. E., Mulas, C., Gatto, L., Lilley, K. S., & Smith, A. G. (2018) · EMBO Reports · doi:10.15252/embr.201745642 · Cited by 34 · see citing works
KinasePA: Phosphoproteomics data annotation using hypothesis driven kinase perturbation analysis
Yang, P., Patrick, E., Humphrey, S. J., Ghazanfar, S., James, D. E., Jothi, R., & Yang, J. Y. H. (2016) · PROTEOMICS · doi:10.1002/pmic.201600068 · Cited by 33 · see citing works
Self-citationVeillard, A.-C., Marks, H., Bernardo, A. S., Jouneau, L., Laloë, D., Boulanger, L., Kaan, A., Brochard, V., Tosolini, M., Pedersen, R. A., et al. (2014) · Stem Cells and Development · doi:10.1089/scd.2013.0639 · Cited by 33 · see citing works
Large Scale Phosphoproteome Profiles Comprehensive Features of Mouse Embryonic Stem Cells
Li, Q., Xing, X., Chen, T., Li, R.-X., Dai, J., Sheng, Q., Xin, S., Zhu, L., Jin, Y., Pei, G., et al. (2010) · Molecular & Cellular Proteomics · doi:10.1074/mcp.m110.001750 · Cited by 32 · see citing works
Yang, P., Patrick, E., Tan, S., Fazakerley, D. J., Burchfield, J. G., Gribben, C., Prior, M. J., James, D. E., & Yang, J. Y. H. (2013) · Bioinformatics · doi:10.1093/bioinformatics/btt616 · Cited by 30 · see citing works
Self-citation
Flagged first, then by citations
Cited by
Sorted by citations
Ensemble deep learning in bioinformatics
Cao, Y., Geddes, T. A., Yang, J. Y. H., & Yang, P. (2020) · Nature Machine Intelligence · doi:10.1038/s42256-020-0217-y · Cited by 357 · see citing works
Self-citationH3K18 lactylation marks tissue-specific active enhancers
Galle, E., Wong, C.-W., Ghosh, A., Desgeorges, T., Melrose, K., Hinte, L. C., Castellano‐Castillo, D., Engl, M., de Sousa, J. A., Ruiz‐Ojeda, F. J., et al. (2022) · Genome biology · doi:10.1186/s13059-022-02775-y · Cited by 242 · see citing works
Derivation of Intermediate Pluripotent Stem Cells Amenable to Primordial Germ Cell Specification.
Yu, L., Wei, Y., Sun, H., Mahdi, A. K., Pinzon-Arteaga, C., Sakurai, M., Schmitz, D. A., Zheng, C.-B., Ballard, E. D., Li, J., et al. (2020) · Cell Stem Cell · doi:10.1016/j.stem.2020.11.003 · Cited by 166 · see citing works
Applications of transformer-based language models in bioinformatics: a survey
Zhang, S., Fan, R., Liu, Y., Chen, S., Liu, Q., & Zeng, W. (2023) · Bioinformatics Advances · doi:10.1093/bioadv/vbad001 · Cited by 176 · see citing works
Decoding the function of bivalent chromatin in development and cancerPreprint
Kumar, D., Cinghu, S., Oldfield, A., Yang, P., & Jothi, R. (2021) · Genome Research · doi:10.1101/gr.275736.121 · Cited by 139 · see citing works
Self-citationPhosR Enables Processing and Functional Analysis of Phosphoproteomic Data
Kim, H. J., Kim, T.-Y., Hoffman, N. J., Xiao, D., James, D. E., Humphrey, S. J., & Yang, P. (2020) · Cell Reports · doi:10.1016/j.celrep.2021.108771 · Cited by 120 · see citing works
Self-citationFormative pluripotent stem cells show features of epiblast cells poised for gastrulation
Wang, X., Xiang, Y., Yu, Y., Wang, R., Zhang, Y., Xu, Q., Sun, H., Zhao, Z., Jiang, X., Wang, X., et al. (2021) · Cell Research · doi:10.1038/s41422-021-00477-x · Cited by 101 · see citing works
Thomas, H. F., Kotova, E., Jayaram, S., Pilz, A., Romeike, M., Lackner, A., Penz, T., Bock, C., Leeb, M., Halbritter, F., et al. (2021) · Molecular Cell · doi:10.1016/j.molcel.2020.12.047 · Cited by 98 · see citing works
Personalized phosphoproteomics identifies functional signaling
Needham, E. J., Hingst, J. R., Parker, B. L., Morrison, K. R., Yang, G., Onslev, J., Kristensen, J. M., Højlund, K., Ling, N. X. Y., Oakhill, J. S., et al. (2021) · Nature Biotechnology · doi:10.1038/s41587-021-01099-9 · Cited by 98 · see citing works
Self-citationFazakerley, D. J., van Gerwen, J., Cooke, K. C., Duan, X., Needham, E. J., Díaz‐Vegas, A., Madsen, S., Norris, D. M., Shun-Shion, A. S., Krycer, J. R., et al. (2023) · Nature Communications · doi:10.1038/s41467-023-36549-2 · Cited by 80 · see citing works
Self-citationAbscission Couples Cell Division to Embryonic Stem Cell Fate
Chaigne, A., Labouesse, C., White, I. J., Agnew, M., Hannezo, É., Chalut, K. J., & Paluch, E. K. (2020) · Developmental Cell · doi:10.1016/j.devcel.2020.09.001 · Cited by 67 · see citing works
Glancy, E., Wang, C., Tuck, E., Healy, E., Amato, S., Neikes, H. K., Mariani, A., Mucha, M., Vermeulen, M., Pasini, D., et al. (2023) · Molecular Cell · doi:10.1016/j.molcel.2023.03.018 · Cited by 71 · see citing works
Enhancer cooperativity can compensate for loss of activity over large genomic distances
Antonović, M., Feng, S., Haslhofer, F., Huber, M., Gallardo, M. G., Loubiere, V., Vanina, D., Pitasi, M., Stark, A., & Buecker, C. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.11.008 · Cited by 50 · see citing works
Global phosphoproteomics reveals DYRK1A regulates CDK1 activity in glioblastoma cells
Recasens, A., Humphrey, S. J., Ellis, M., Hoque, M., Abbassi, R. H., Chen, B., Longworth, M., Needham, E. J., James, D. E., Johns, T. G., et al. (2021) · Cell Death Discovery · doi:10.1038/s41420-021-00456-6 · Cited by 52 · see citing works
Self-citationEnhancer-associated H3K4 methylation safeguards in vitro germline competence
Bleckwehl, T., Crispatzu, G., Schaaf, K., Respuela, P., Bartusel, M., Benson, L., Clark, S. J., Dorighi, K. M., Barral, A., Laugsch, M., et al. (2021) · Nature Communications · doi:10.1038/s41467-021-26065-6 · Cited by 39 · see citing works
Multi-omics profiling visualizes dynamics of cardiac development and functions
Gu, Y., Zhou, Y., Ju, S., Liu, X., Zhang, Z., Guo, J., Gao, J., Zang, J., Sun, H., Chen, Q., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.111891 · Cited by 49 · see citing works
Fine-tuning of gene expression through the Mettl3-Mettl14-Dnmt1 axis controls ESC differentiation
Quarto, G., Li Greci, A., Bizet, M., Penning, A., Primac, I., Murisier, F., Garcia-Martinez, L., Borges, R. L., Gao, Q., Cingaram, P. K. R., et al. (2025) · Cell · doi:10.1016/j.cell.2024.12.009 · Cited by 50 · see citing works
Luque, A. V., Savill, R. G., López-Anguita, N., Bolondi, A., Garai, S., Gassaloglu, S. I., Rouatbi, R., Schmeißer, K., Poddar, A., Bauer, L., et al. (2025) · Cell stem cell · doi:10.1016/j.stem.2025.03.012 · Cited by 48 · see citing works
noisyR : enhancing biological signal in sequencing datasets by characterizing random technical noise
Moutsopoulos, I., Maischak, L., Lauzikaite, E., Urbina, S. A. V., Williams, E. C., Drost, H., & Mohorianu, I. I. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab433 · Cited by 45 · see citing works
Esrrb guides naive pluripotent cells through the formative transcriptional programme
Carbognin, E., Carlini, V., Panariello, F., Chieregato, M., Guerzoni, E., Benvegnù, D., Perrera, V., Malucelli, C., Cesana, M., Grimaldi, A., et al. (2023) · Nature Cell Biology · doi:10.1038/s41556-023-01131-x · Cited by 37 · see citing works
Chromatin and Epigenetic Rearrangements in Embryonic Stem Cell Fate Transitions
Sun, L., Fu, X., Ma, G., & Hutchins, A. P. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.637309 · Cited by 38 · see citing works
Zhang, H., Ji, S., Zhang, K., Chen, Y., Ming, J., Kong, F., Wang, L., Wang, S., Zou, Z., Xiong, Z., et al. (2023) · Genome biology · doi:10.1186/s13059-023-02997-8 · Cited by 38 · see citing works
The Key Role of MicroRNAs in Self-Renewal and Differentiation of Embryonic Stem Cells
Divisato, G., Passaro, F., Russo, T., & Parisi, S. (2020) · International Journal of Molecular Sciences · doi:10.3390/ijms21176285 · Cited by 37 · see citing works
Computational Stem Cell Biology: Open Questions and Guiding Principles
Cahan, P., Cacchiarelli, D., Dunn, S.-J., Hemberg, M., Lopes, S. M. C. D. S., Morris, S. A., Rackham, O. J. L., del Sol, A., & Wells, C. A. (2021) · Cell stem cell · doi:10.1016/j.stem.2020.12.012 · Cited by 36 · see citing works
RNA polymerase II pausing in development: orchestrating transcription
Abuhashem, A., Garg, V., & Hadjantonakis, A. (2022) · Open Biology · doi:10.1098/rsob.210220 · Cited by 36 · see citing works
Needham, E. J., Humphrey, S. J., Cooke, K. C., Fazakerley, D. J., Duan, X., Parker, B. L., & James, D. E. (2019) · Cell Reports · doi:10.1016/j.celrep.2019.10.001 · Cited by 33 · see citing works
Self-citationINO80 promotes H2A.Z occupancy to regulate cell fate transition in pluripotent stem cells
Yu, H., Wang, J., Lackford, B. L., Bennett, B. D., Li, J., & Hu, G. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab476 · Cited by 34 · see citing works
Boileau, R. M., Chen, K. X., & Blelloch, R. H. (2023) · Genome biology · doi:10.1186/s13059-023-02883-3 · Cited by 33 · see citing works
A proteome signature for acute incisional pain in dorsal root ganglia of mice
Pogatzki-Zahn, E. M., Gómez‐Varela, D., Erdmann, G., Kaschube, K., Segelcke, D., & Schmidt, M. (2021) · Pain · doi:10.1097/j.pain.0000000000002207 · Cited by 30 · see citing works
Cardiopoietic stem cell therapy restores infarction-altered cardiac proteome
Arrell, D. K., Rosenow, C. S., Yamada, S., Behfar, A., & Terzic, A. (2020) · npj Regenerative Medicine · doi:10.1038/s41536-020-0091-6 · Cited by 30 · see citing works
Stirred suspension bioreactors maintain naïve pluripotency of human pluripotent stem cells
Rohani, L., Borys, B. S., Razian, G., Naghsh, P., Liu, S., Johnson, A. A., Machiraju, P., Holland, H., Lewis, I. A., Groves, R. A., et al. (2020) · Communications Biology · doi:10.1038/s42003-020-01218-3 · Cited by 31 · see citing works
Dissection of two routes to naïve pluripotency using different kinase inhibitors
Martínez‐Val, A., Lynch, C. J., Calvo, I., Ximénez‐Embún, P., Garcı́a, F., Zarzuela, E., Serrano, M., & Muñoz, J. (2021) · Nature Communications · doi:10.1038/s41467-021-22181-5 · Cited by 26 · see citing works
Trafficking regulator of GLUT4-1 (TRARG1) is a GSK3 substrate
Duan, X., Norris, D. M., Humphrey, S. J., Yang, P., Cooke, K. C., Bultitude, W. P., Parker, B. L., Conway, O. J., Burchfield, J. G., Krycer, J. R., et al. (2022) · Biochemical Journal · doi:10.1042/bcj20220153 · Cited by 22 · see citing works
Self-citationMolecular versatility during pluripotency progression
Furlan, G., Huyghe, A., Combémorel, N., & Lavial, F. (2023) · Nature Communications · doi:10.1038/s41467-022-35775-4 · Cited by 18 · see citing works
Norris, D. M., Yang, P., Shin, S., Kearney, A. L., Kim, H. J., Geddes, T. A., Senior, A. M., Fazakerley, D. J., Nguyen, L. K., James, D. E., et al. (2021) · iScience · doi:10.1016/j.isci.2021.102118 · Cited by 19 · see citing works
Self-citationRNA Pol II pausing facilitates phased pluripotency transitions by buffering transcriptionPreprint
Abuhashem, A., Chivu, A. G., Zhao, Y., Rice, E. J., Siepel, A. C., Danko, C. G., & Hadjantonakis, A. (2022) · Genes & Development · doi:10.1101/gad.349565.122 · Cited by 22 · see citing works
FoxO transcription factors actuate the formative pluripotency specific gene expression programme
Santini, L., Kowald, S., Cerron-Alvan, L. M., Huth, M., Fabing, A. P., Sestini, G., Rivron, N. C., & Leeb, M. (2024) · Nature Communications · doi:10.1038/s41467-024-51794-9 · Cited by 21 · see citing works
Arekatla, G., Trenzinger, C., Reimann, A., Loeffler, D., Kull, T., & Schroeder, T. (2023) · Developmental Cell · doi:10.1016/j.devcel.2023.04.013 · Cited by 21 · see citing works
Impact of eIF2α phosphorylation on the translational landscape of mouse embryonic stem cells
Amiri, M., Kiniry, S. J., Possemato, A., Mahmood, N., Basiri, T., Dufour, C., Tabatabaei, N., Deng, Q., Bellucci, M. A., Harwalkar, K., et al. (2023) · Cell Reports · doi:10.1016/j.celrep.2023.113615 · Cited by 13 · see citing works
Sangokoya, C., & Blelloch, R. H. (2020) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.2002750117 · Cited by 20 · see citing works
Moutsopoulos, I., Williams, E. C., & Mohorianu, I. I. (2022) · Briefings in Bioinformatics · doi:10.1093/bib/bbac591 · Cited by 19 · see citing works
Three-dimensional geometry controls division symmetry in stem cell colonies
Chaigne, A., Smith, M. B., Cavestany, R. L., Hannezo, É., Chalut, K. J., & Paluch, E. K. (2021) · Journal of Cell Science · doi:10.1242/jcs.255018 · Cited by 17 · see citing works
Progression of the pluripotent epiblast depends upon the NMD factor UPF2
Chousal, J. N., Sohni, A., Vitting‐Seerup, K., Cho, K., Kim, M., Tan, K., Porse, B. T., Wilkinson, M., & Cook‐Andersen, H. (2022) · Development · doi:10.1242/dev.200764 · Cited by 18 · see citing works
A high-content endogenous GLUT4 trafficking assay reveals new aspects of adipocyte biology
Díaz‐Vegas, A., Norris, D. M., Jall-Rogg, S., Cooke, K. C., Conway, O. J., Shun-Shion, A. S., Duan, X., Potter, M., van Gerwen, J., Baird, H. J. M., et al. (2022) · Life Science Alliance · doi:10.26508/lsa.202201585 · Cited by 17 · see citing works
Self-citationThe application of cell surface markers to demarcate distinct human pluripotent states
Goodwin, J., Laslett, A. L., & Rugg‐Gunn, P. J. (2019) · Experimental Cell Research · doi:10.1016/j.yexcr.2019.111749 · Cited by 18 · see citing works
Qin, W., Ugur, E., Mulholland, C. B., Bultmann, S., Solovei, I. V., Modic, M., Smets, M., Wierer, M., Forné, I., Imhof, A., et al. (2021) · Nucleic Acids Research · doi:10.1093/nar/gkab548 · Cited by 18 · see citing works
Kim, H. J., Osteil, P., Humphrey, S. J., Cinghu, S., Oldfield, A., Patrick, E., Wilkie, E. E., Peng, G., Suo, S., Jothi, R., et al. (2019) · Nucleic Acids Research · doi:10.1093/nar/gkz1179 · Cited by 17 · see citing works
Self-citationTemporal ordering of omics and multiomic events inferred from time-series data
Kaur, S., Peters, T. J., Yang, P., Luu, L. D. W., Vuong, J., Krycer, J. R., & O’Donoghue, S. I. (2020) · npj Systems Biology and Applications · doi:10.1038/s41540-020-0141-0 · Cited by 15 · see citing works
Self-citationMetabolic characterization of a paused-like pluripotent state
Sousa, M. I., Correia, B., Rodrigues, A. S., & Ramalho‐Santos, J. (2020) · Biochimica et Biophysica Acta (BBA) - General Subjects · doi:10.1016/j.bbagen.2020.129612 · Cited by 16 · see citing works
Pecori, F., Yokota, I., Hanamatsu, H., Miura, T., Ogura, C., Ota, H., Furukawa, J., Oki, S., Yamamoto, K., Yoshie, O., et al. (2021) · Scientific Reports · doi:10.1038/s41598-020-79666-4 · Cited by 17 · see citing works
Unraveling the Spatiotemporal Human Pluripotency in Embryonic Development
Ávila‐González, D., Portillo, W., Garcı́a-López, G., Molina‐Hernández, A., Diaz-Martinez, N. E., & Díaz, N. F. (2021) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2021.676998 · Cited by 15 · see citing works
Krumm, J., Sekine, K., Samaras, P., Brazovskaja, A., Breunig, M., Yasui, R., Kleger, A., Taniguchi, H., Wilhelm, M., Treutlein, B., et al. (2022) · Cell Reports · doi:10.1016/j.celrep.2022.110604 · Cited by 15 · see citing works
Nanog regulates Pou3f1 expression at the exit from pluripotency during gastrulation
Barral, A., Rollan, I., Sánchez-Iranzo, H., Jawaid, W., Badía-Careaga, C., Menchero, S., Gómez, M., Torroja, C., Sánchez-Cabo, F., Göttgens, B., et al. (2019) · Biology Open · doi:10.1242/bio.046367 · Cited by 14 · see citing works
Ugur, E., de la Porte, A., Qin, W., Bultmann, S., Ivanova, A., Drukker, M., Mann, M., Wierer, M., & Leonhardt, H. (2023) · Nucleic Acids Research · doi:10.1093/nar/gkad058 · Cited by 13 · see citing works
Self-citationLyu, X., Cui, Y., Kong, Y., Yang, M., Shen, H., Liao, S., Li, S., An, C., Wang, H., Zhang, Z., et al. (2024) · Molecular Cell · doi:10.1016/j.molcel.2024.06.005 · Cited by 13 · see citing works
Yuan, F., Yang, J.-H., Ma, F., Hu, Z., Malik, V., Zang, R., Li, D., Shi, X., Huang, X., Zhou, H.-W., et al. (2025) · Nature Communications · doi:10.1038/s41467-025-57165-2 · Cited by 12 · see citing works
Self-citationXiao, Y., Sosa, F., Ross, P. J., Diffenderfer, K. E., & Hansen, P. J. (2021) · Biology Open · doi:10.1242/bio.058669 · Cited by 13 · see citing works
Computational systems approach towards phosphoproteomics and their downstream regulation
Xiao, D., Chen, C., & Yang, P. (2022) · PROTEOMICS · doi:10.1002/pmic.202200068 · Cited by 12 · see citing works
Self-citationSharaireh, A. M., FitzPatrick, L. M., Ward, C. M., McKay, T. R., & Unwin, R. D. (2020) · Stem Cells · doi:10.1002/stem.3249 · Cited by 11 · see citing works
Luu, L. D. W., Zhong, L., Kaur, S., Raftery, M. J., & Lan, R. (2021) · Frontiers in Cellular and Infection Microbiology · doi:10.3389/fcimb.2021.660280 · Cited by 11 · see citing works
Matsuzaki, F., Uda, S., Yamauchi, Y., Matsumoto, M., Soga, T., Maehara, K., Ohkawa, Y., Nakayama, K. I., Kuroda, S., & Kubota, H. (2021) · Cell Reports · doi:10.1016/j.celrep.2021.109569 · Cited by 11 · see citing works
Poised PABP–RNA hubs implement signal-dependent mRNA decay in development
Modic, M., Kuret, K., Steinhauser, S., Faraway, R., van Genderen, E., Mozos, I. R. D. L., Novljan, J., Vičič, Ž., Lee, F. C. Y., ten Berge, D., et al. (2024) · Nature Structural & Molecular Biology · doi:10.1038/s41594-024-01363-x · Cited by 11 · see citing works
Transcriptional and epigenetic control of germline competence and specification.
Bleckwehl, T., & Rada-Iglesias, Á. (2019) · Current Opinion in Cell Biology · doi:10.1016/j.ceb.2019.05.006 · Cited by 10 · see citing works
Combinatorial metabolism drives the naive to primed pluripotent chromatin landscape
Ehnes, D. D., Hussein, A. M., Ware, C. B., Mathieu, J., & Ruohola‐Baker, H. (2020) · Experimental Cell Research · doi:10.1016/j.yexcr.2020.111913 · Cited by 10 · see citing works
Aurora B controls microtubule stability to regulate abscission dynamics in stem cells
Kodba, S., Öztop, A., van Berkum, E., Katrukha, E. A., Iwanski, M. K., Nijenhuis, W., Kapitein, L. C., & Chaigne, A. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.115238 · Cited by 10 · see citing works
Gökbuget, D., Goehring, L. J., Boileau, R. M., Lenshoek, K., Huang, T. T., & Blelloch, R. H. (2025) · Cell Reports · doi:10.1016/j.celrep.2025.115272 · Cited by 9 · see citing works
A systems view of cellular heterogeneity: Unlocking the “wheel of fate”
Movasat, H., Giacopino, E., Shahdoost, A., Nokoorani, Y. D., Abrbekouh, A. H., Tahamtani, Y., & Shakiba, N. (2025) · Cell Systems · doi:10.1016/j.cels.2025.101300 · Cited by 14 · see citing works
A Review of Complex Systems Approaches to Cancer Networks
Uthamacumaran, A. (2020) · Complex Systems · doi:10.25088/complexsystems.29.4.779 · Cited by 9 · see citing works
Functional analysis of the stable phosphoproteome reveals cancer vulnerabilities
Xiao, D., Kim, H. J., Pang, C. N. I., & Yang, P. (2022) · Bioinformatics · doi:10.1093/bioinformatics/btac015 · Cited by 9 · see citing works
Self-citationModeling the early development of a primate embryo
Tam, P. (2019) · Science · doi:10.1126/science.aaz6976 · Cited by 9 · see citing works
Epigenetics as “conductor” in “orchestra” of pluripotent states
Baral, I., Varghese, P. C., & Dutta, D. (2022) · Cell and Tissue Research · doi:10.1007/s00441-022-03667-0 · Cited by 9 · see citing works
Waisman, A., Sevlever, F., Saulnier, D., Francia, M. G., Blanco, R., Amín, G., Lombardi, A., Biani, C., Palma, M. B., Scarafía, A., et al. (2024) · Scientific Reports · doi:10.1038/s41598-024-59247-5 · Cited by 8 · see citing works
Enhancer-associated H3K4 methylation safeguards in vitro germline competence
Bleckwehl, T., Crispatzu, G., Schaaf, K., Respuela, P., Bartusel, M., Benson, L. J., Clark, S. J., Dorighi, K. M., Barral, A., Laugsch, M., et al. (2020) · Kölner Universitäts PublikationsServer (Universität zu Köln) · doi:10.17863/cam.76317 · Cited by 8 · see citing works
Xiao, D., Caldow, M. K., Kim, H. J., Blazev, R., Koopman, R., Manandi, D., Parker, B. L., & Yang, P. (2022) · iScience · doi:10.1016/j.isci.2022.104489 · Cited by 8 · see citing works
Self-citationOrganelle biogenesis: ribosomes as organizer and performer
Wang, Q., Wang, Y., Li, S., Zhou, A., & Qin, Y. (2022) · 中国科学通报:英文版 · doi:10.1016/j.scib.2022.07.023 · Cited by 8 · see citing works
Integrative analysis reveals histone demethylase LSD1 promotes RNA polymerase II pausing
Kim, H. J., Li, P., Kim, T.-Y., Oldfield, A., Zheng, X., & Yang, P. (2022) · iScience · doi:10.1016/j.isci.2022.105049 · Cited by 7 · see citing works
Self-citationQuantitative Proteomics and Phosphoproteomics Analysis of Patient-Derived Ovarian Cancer Stem Cells
Franciosa, G., Nieddu, V., Battistini, C., Caffarini, M., Lupia, M., Colombo, N., Fusco, N., Olsen, J. V., & Cavallaro, U. (2025) · Molecular & Cellular Proteomics · doi:10.1016/j.mcpro.2025.100965 · Cited by 7 · see citing works
Vega-Sendino, M., Olbrich, T., Tillo, D., Tran, A. D., Domingo, C. N., Franco, M., FitzGerald, P. C., Kruhlak, M. J., & Ruiz, S. (2021) · Science Advances · doi:10.1126/sciadv.abg8306 · Cited by 7 · see citing works
Culture of Neurospheres Derived from the Neurogenic Niches in Adult Prairie Voles
Ávila‐González, D., Young, L. J., Camacho, F., Paredes, R. G., Díaz, N. F., & Portillo, W. (2020) · Journal of Visualized Experiments · doi:10.3791/61402 · Cited by 7 · see citing works
SRRM2 splicing factor modulates cell fate in early development
Carvalho, S., Zea-Redondo, L., Tang, T. C. C., Stachel-Braum, P., Miller, D. C., Caldas, P., Kukalev, A., Diecke, S., Grosswendt, S., Grosso, A. R., et al. (2024) · Biology Open · doi:10.1242/bio.060415 · Cited by 6 · see citing works
Lee, U., Laguillo-Diego, A., Magliulo, D., Wong, W., Kasliwal, K., Ni, Z., Cheng, L., Li, J., Pelham‐Webb, B., Pertsinidis, A., et al. (2026) · Nature Genetics · doi:10.1038/s41588-026-02556-4 · Cited by 9 · see citing works
Xiao, D., Lin, M., Liu, C., Geddes, T. A., Burchfield, J. G., Parker, B. L., Humphrey, S. J., & Yang, P. (2023) · NAR Genomics and Bioinformatics · doi:10.1093/nargab/lqad099 · Cited by 5 · see citing works
Self-citationSun, L., Yin, Y., Cao, Y., Chen, C., Guo, Y., Cai, Z., Wu, J., & Li, Q. (2024) · Biophysics Reports · doi:10.52601/bpr.2024.240045 · Cited by 5 · see citing works
AMPK activation by glycogen expenditure primes the exit of naïve pluripotency
Kim, S.-M., Kwon, E., Oh, J., Kim, H. S., Park, S., Jang, G., Tae, J., Kim, K.-T., & Cha, H. (2025) · EMBO Reports · doi:10.1038/s44319-025-00384-x · Cited by 6 · see citing works
Bivalent chromatin protects reversibly repressed genes from irreversible silencingPreprint
Kumar, D., & Jothi, R. (2020) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2020.12.02.406751 · Cited by 6 · see citing works
Self-citationMLL3/MLL4 enzymatic activity shapes DNA replication timingPreprint
Gökbuget, D., Boileau, R. M., Lenshoek, K., & Blelloch, R. H. (2023) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2023.12.07.569680 · Cited by 5 · see citing works
Steindel, M., Davis, O., Neumann, K., Agsu, G. G., Mao, L., Kranz, A., Pirvan, L., Adhya, D., Morf, J., Zhang, Z., et al. (2025) · bioRxiv (Cold Spring Harbor Laboratory) · doi:10.1101/2025.02.21.639010 · Cited by 5 · see citing works
RNA Degradation in Pluripotent Stem Cells: Mechanisms, Crosstalk, and Fate Regulation
Jeong, S., Oh, M., Han, J., & Kim, S.-K. (2025) · Cells · doi:10.3390/cells14201634 · Cited by 4 · see citing works
Oses, C., Francia, M. G., Verneri, P., Echegaray, C. V., Guberman, A., & Levi, V. (2023) · Frontiers in Cell and Developmental Biology · doi:10.3389/fcell.2023.1125015 · Cited by 4 · see citing works
TASOR expression in naive embryonic stem cells safeguards their developmental potential
Pinzón-Arteaga, C. A., O’Hara, R. A., Mazzagatti, A., Ballard, E. B., Hu, Y., Pan, A., Schmitz, D. A., Wei, Y., Sakurai, M., Ly, P., et al. (2024) · Cell Reports · doi:10.1016/j.celrep.2024.114887 · Cited by 4 · see citing works
Ávila‐González, D., Portillo, W., Barragán-Álvarez, C. P., Hernández‐Montes, G., Flores-Garza, E., Molina‐Hernández, A., Diaz-Martinez, N. E., & Díaz, N. F. (2022) · eLife · doi:10.7554/elife.68035 · Cited by 4 · see citing works
Wu, Y., Sun, H., Qin, L., Zhang, X., Zhou, H., Wang, Y., Wang, L., Li, M., Liu, J., & Zhang, J. (2023) · Frontiers in Pharmacology · doi:10.3389/fphar.2023.1149659 · Cited by 4 · see citing works
Dong, M., Zhang, Z., Li, Z., Yan, T., Henawy, A. R., Meng, Y., Li, Y. H., Li, M., Huang, F., Cai, M., et al. (2025) · Journal of Advanced Research · doi:10.1016/j.jare.2025.12.018 · Cited by 4 · see citing works
The FIRE biosensor illuminates iron regulatory protein activity and cellular iron homeostasis
Sangokoya, C. (2025) · Cell Reports Methods · doi:10.1016/j.crmeth.2024.100960 · Cited by 3 · see citing works
Soliman, S. S., Shah, D. H., El‐Samad, H., & Weinberg, Z. Y. (2025) · Development · doi:10.1242/dev.204505 · Cited by 3 · see citing works
Ubiquitin Dynamics in Stem Cell Biology: Current Challenges and Perspectives
de Dieuleveult, M., & Miotto, B. (2020) · BioEssays · doi:10.1002/bies.201900129 · Cited by 2 · see citing works
Guo, G., Yang, J., Guo, W., Deng, H., Yu, H., Bai, S., Li, G., Tang, Y., Ping, Z., Xu, Y., et al. (2023) · Stroke and Vascular Neurology · doi:10.1136/svn-2022-002165 · Cited by 3 · see citing works
Self-citationWang, J., Zhang, C., Huang, Y., Ruan, Y., Yan, H., Wang, J., Wang, F., Yu, M., Xu, Y., Liu, L., et al. (2023) · Stem Cells and Development · doi:10.1089/scd.2023.0053 · Cited by 3 · see citing works
AKT1 induces Nanog promoter in a SUMOylation-dependent manner in different pluripotent contexts
Francia, M. G., Verneri, P., Oses, C., Echegaray, C. V., García, M. R., Toro, A. R., Levi, V., & Guberman, A. (2023) · BMC Research Notes · doi:10.1186/s13104-023-06598-3 · Cited by 3 · see citing works
Dehghanian, F., Bovio, P. P., Gather, F., Probst, S., Nilchi, A. N., & Vogel, T. (2024) · Biochimica et Biophysica Acta (BBA) - Molecular Cell Research · doi:10.1016/j.bbamcr.2024.119686 · Cited by 3 · see citing works
- Authors
- Yang, P., Humphrey, S. J., Cinghu, S., Pathania, R., Oldfield, A. J., Kumar, D., Perera, D., Yang, J. Y. H., James, D. E., Mann, M., & Jothi, R.
- Affiliations
- The University of Sydney (AU)
- National Institutes of Health (US)
- Max Planck Institute of Biochemistry (DE)
- Corresponding author
- Yang, Pengyi
- Humphrey, Sean J.
- Jothi, Raja
- ORCID
- Venue
- Cell Systems
- Publisher
- Elsevier BV
- Published
- 2019-05
- Volume
- 8
- Issue
- 5
- Pages
- 427-445.e10
- ISSN
- 2405-4712 (ISSN-L)
- PMC
- PMC6544180
- OpenAlex
- W2950402574
- Cited by
- 146
- References
- 109
- Citations by year
- 2026: 6 · 2025: 21 · 2024: 14 · 2023: 28 · 2022: 25 · 2021: 26 · 2020: 20 · 2019: 6
- FWCI
- 6.37
- Type
- journal article
- Language
- en
- Open access
- hybrid
- doi.org
- Licence
- Locations
- Cell Systems (publishedVersion, cc-by-nc-nd)
- bioRxiv (Cold Spring Harbor Laboratory) (acceptedVersion, cc-by-nc-nd)
- PubMed (publishedVersion)
- PubMed Central (acceptedVersion)
- HAL (submittedVersion, cc-by-nc-nd)
- MPG.PuRe (Max Planck Society) (submittedVersion, other-oa)
- Funders
- Max Planck Institute for Dynamics of Complex Technical Systems Magdeburg
- Australian Research Council
- National Institutes of Health
- European Molecular Biology Organization
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Pluripotent Stem Cells Research
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Developmental Biology and Gene Regulation
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Epigenetics and DNA Methylation
- Keywords
- pluripotency, naive pluripotency, primed pluripotency, embryonic stem cells, phosphoproteome, proteome, transcriptome, epigenome, signaling pathways
- MeSH terms
- Epigenome, Animals, Cell Differentiation, Germ Layers, Humans, Signal Transduction, Gene Expression Regulation, Developmental, Cell Lineage, Proteome, Pluripotent Stem Cells, Embryonic Stem Cells, Transcriptome
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