Skibbens, R. V. et al. Cohesinopathies of a feather flock together. PLoS Genet 9, e1004036 (2013).Article
PubMed
PubMed Central
Google Scholar
Banerji, R., Skibbens, R. V. & Iovine, M. K. How many roads lead to cohesinopathies? Dev. Dyn. 246, 881–888 (2017).Article
CAS
PubMed
Google Scholar
McNairn, A. J. & Gerton, J. L. Cohesinopathies: one ring, many obligations. Mutat. Res–Fund. Mol. M. 647, 103–111 (2008).Article
CAS
Google Scholar
Piché, J., Van Vliet, P. P., Pucéat, M. & Andelfinger, G. The expanding phenotypes of cohesinopathies: one ring to rule them all! Cell Cycle 18, 2828–2848 (2019).Article
PubMed
PubMed Central
Google Scholar
Kantaputra, P. N. et al. Juberg-Hayward syndrome is a cohesinopathy, caused by mutation in ESCO2. Eur. J. Orthod. 43, 45–50 (2021).Article
PubMed
Google Scholar
Liu, J. & Krantz, I. D. Cornelia de Lange syndrome, cohesin, and beyond. Clin. Genet. 76, 303–314 (2009).Article
CAS
PubMed
PubMed Central
Google Scholar
Vega, H. et al. Roberts syndrome is caused by mutations in ESCO2, a human homolog of yeast ECO1 that is essential for the establishment of sister chromatid cohesion. Nat. Genet. 37, 468–470 (2005).Article
CAS
PubMed
Google Scholar
Schüle, B., Oviedo, A., Johnston, K., Pai, S. & Francke, U. Inactivating mutations in ESCO2 cause SC phocomelia and Roberts syndrome: no phenotype-genotype correlation. Am. J. Hum. Genet. 77, 1117–1128 (2005).Article
PubMed
PubMed Central
Google Scholar
Kantaputra, P. N. et al. Juberg-Hayward syndrome and Roberts syndrome are allelic, caused by mutations in ESCO2. Arch. Oral Biol. 119, 104918 (2020).Article
CAS
PubMed
Google Scholar
Gordillo, M. et al. The molecular mechanism underlying Roberts syndrome involves loss of ESCO2 acetyltransferase activity. Hum. Mol. Genet. 17, 2172–2180 (2008).Article
CAS
PubMed
Google Scholar
Robert, J. B. A child with double cleft of lip and palate, protrusion of the intermaxillary portion of the upper jaw and imperfect development of the bones of the four extremities. Ann. Surg. 70, 252–253 (1919).
Google Scholar
Goh, E. S. Y. et al. The Roberts syndrome/SC phocomelia spectrum—a case report of an adult with review of the literature. Am. J. Med. Genet. A. 152, 472–478 (2010).Article
Google Scholar
Lenz, W. D., Marquardt, E. & Weicker, H. Pseudothalidomide syndrome. Birth Defects Orig. Art. Ser. 11, 97–107 (1974).
Google Scholar
Vega, H. et al. Phenotypic variability in 49 cases of ESCO2 mutations, including novel missense and codon deletion in the acetyltransferase domain, correlates with ESCO2 expression and establishes the clinical criteria for Roberts syndrome. J. Med. Genet. 47, 30–37 (2010).Article
CAS
PubMed
Google Scholar
Sanchez, A. C., Thren, E. D., Iovine, M. K. & Skibbens, R. V. Esco2 and cohesin regulate CRL4 ubiquitin ligase ddb1 expression and thalidomide teratogenicity. Cell Cycle 21, 501–513 (2022).Article
CAS
PubMed
PubMed Central
Google Scholar
McBride, W. G. Thalidomide and congenital abnormalities. Lancet 2, 90927–90928 (1961).
Google Scholar
Bodera, P. & Stankiewicz, W. Immunomodulatory properties of thalidomide analogs: pomalidomide and lenalidomide, experimental and therapeutic applications. Recent Pat. Endocr. Metab. Immune Drug Discov. 5, 192–196 (2011).Article
CAS
PubMed
Google Scholar
Schwartz, M. P. et al. Human pluripotent stem cell-derived neural constructs for predicting neural toxicity. Proc. Natl. Acad. Sci. 112, 12516–12521 (2015).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Ulmke, P. A. et al. Molecular profiling reveals involvement of ESCO2 in intermediate progenitor cell maintenance in the developing mouse cortex. Stem Cell Rep 16, 968–984 (2021).Article
CAS
Google Scholar
Guo, X. B., Huang, B., Pan, Y. H., Su, S. G. & Li, Y. ESCO2 inhibits tumor metastasis via transcriptionally repressing MMP2 in colorectal cancer. Cancer Manag. Res. 10, 6157–6166 (2018).Article
CAS
PubMed
PubMed Central
Google Scholar
Ito, T. et al. Identification of a primary target of thalidomide teratogenicity. Science 327, 1345–1350 (2010).Article
ADS
CAS
PubMed
Google Scholar
Ito, T., Ando, H. & Handa, H. Teratogenic effects of thalidomide: molecular mechanisms. Cell. Mol. Life Sci. 68, 1569–1579 (2011).Article
CAS
PubMed
PubMed Central
Google Scholar
Banerji, R., Skibbens, R. V. & Iovine, M. K. Cohesin mediates Esco2-dependent transcriptional regulation in a zebrafish regenerating fin model of Roberts Syndrome. Biol. Open 6, 1802–1813 (2017).CAS
PubMed
PubMed Central
Google Scholar
Sun, H. et al. Cul4-Ddb1 ubiquitin ligases facilitate DNA replication-coupled sister chromatid cohesion through regulation of cohesin acetyltransferase Esco2. PLoS Genet. 15, e1007685 (2019).Article
CAS
PubMed
PubMed Central
Google Scholar
Minamino, M. et al. Temporal regulation of ESCO2 degradation by the MCM complex, the CUL4-DDB1-VPRBP complex, and the anaphase-promoting complex. Curr. Biol. 28, 2665–2672 (2018).Article
CAS
PubMed
Google Scholar
Skibbens, R. V., Corson, L. B., Koshland, D. & Hieter, P. Ctf7p is essential for sister chromatid cohesion and links mitotic chromosome structure to the DNA replication machinery. Genes Dev 13, 307–319 (1999).Article
CAS
PubMed
PubMed Central
Google Scholar
Tóth, A. et al. Yeast cohesin complex requires a conserved protein, Eco1p (Ctf7), to establish cohesion between sister chromatids during DNA replication. Genes Dev 13, 320–333 (1999).Article
PubMed
PubMed Central
Google Scholar
Bellows, A. M., Kenna, M. A., Cassimeris, L. & Skibbens, R. V. Human EFO1p exhibits acetyltransferase activity and is a unique combination of linker histone and Ctf7p/Eco1p chromatid cohesion establishment domains. Nucleic Acids Res. 31, 6334–6343 (2003).Article
CAS
PubMed
PubMed Central
Google Scholar
Peters, J. M., Tedeschi, A. & Schmitz, J. The cohesin complex and its roles in chromosome biology. Genes Dev 22, 3089–3114 (2008).Article
CAS
PubMed
Google Scholar
Michaelis, C., Ciosk, R. & Nasmyth, K. Cohesins: chromosomal proteins that prevent premature separation of sister chromatids. Cell 91, 35–45 (1997).Article
CAS
PubMed
Google Scholar
DiNardo, S., Voelkel, K. & Sternglanz, R. DNA topoisomerase II mutant of Saccharomyces cerevisiae: topoisomerase II is required for segregation of daughter molecules at the termination of DNA replication. Proc. Natl Acad. Sci. USA 81, 2616–2620 (1984).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Gassler, J. et al. A mechanism of cohesin‐dependent loop extrusion organizes zygotic genome architecture. EMBO J 36, 3600–3618 (2017).Article
CAS
PubMed
PubMed Central
Google Scholar
Davidson, I. F. et al. DNA loop extrusion by human cohesin. Science 366, 1338–1345 (2019).Article
ADS
CAS
PubMed
Google Scholar
Kim, Y., Shi, Z., Zhang, H., Finkelstein, I. J. & Yu, H. Human cohesin compacts DNA by loop extrusion. Science 366, 1345–1349 (2019).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Golfier, S., Quail, T., Kimura, H. & Brugués, J. Cohesin and condensin extrude DNA loops in a cell cycle-dependent manner. eLife 9, e53885 (2020).Article
PubMed
PubMed Central
Google Scholar
Wutz, G. et al. Topologically associating domains and chromatin loops depend on cohesin and are regulated by CTCF, WAPL, and PDS5 proteins. EMBO J 36, 3573–3599 (2017).Article
CAS
PubMed
PubMed Central
Google Scholar
Ball, A. R. Jr & Yokomori, K. Damage‐induced reactivation of cohesin in postreplicative DNA repair. Bioessays 30, 5–9 (2008).Article
CAS
PubMed
PubMed Central
Google Scholar
Covo, S., Westmoreland, J. W., Gordenin, D. A. & Resnick, M. A. Cohesin is limiting for the suppression of DNA damage–induced recombination between homologous chromosomes. PLoS Genet 6, e1001006 (2010).Article
PubMed
PubMed Central
Google Scholar
Watrin, E. & Peters, J. M. The cohesin complex is required for the DNA damage‐induced G2/M checkpoint in mammalian cells. EMBO J 28, 2625–2635 (2009).Article
CAS
PubMed
PubMed Central
Google Scholar
Kim, S. T., Xu, B. & Kastan, M. B. Involvement of the cohesin protein, Smc1, in Atm-dependent and independent responses to DNA damage. Genes Dev 16, 560–570 (2002).Article
CAS
PubMed
PubMed Central
Google Scholar
Ünal, E. et al. DNA damage response pathway uses histone modification to assemble a double-strand break-specific cohesin domain. Mol. Cell. 16, 991–1002 (2004).Article
PubMed
Google Scholar
Mönnich, M., Kuriger, Z., Print, C. G. & Horsfield, J. A. A zebrafish model of Roberts syndrome reveals that Esco2 depletion interferes with development by disrupting the cell cycle. PloS One 6, e20051 (2011).Article
ADS
PubMed
PubMed Central
Google Scholar
Whelan, G. et al. Cohesin acetyltransferase Esco2 is a cell viability factor and is required for cohesion in pericentric heterochromatin. EMBO J 31, 71–82 (2012).Article
CAS
PubMed
Google Scholar
Percival, S. M. et al. Variations in dysfunction of sister chromatid cohesion in esco2 mutant zebrafish reflect the phenotypic diversity of Roberts syndrome. Dis. Model Mech. 8, 941–955 (2015).CAS
PubMed
PubMed Central
Google Scholar
Jabs, E. W., Tuck-Muller, C. M., Cusano, R. & Rattner, J. B. Centromere separation and aneuploidy in human mitotic mutants: Roberts syndrome. Prog. Clin. Biol. Res. 318, 111–118 (1989).CAS
PubMed
Google Scholar
Tomkins, D. J. & Sisken, J. E. Abnormalities in the cell-division cycle in Roberts syndrome fibroblasts: a cellular basis for the phenotypic characteristics? Am. J. Hum. Genet. 36, 1332 (1984).CAS
PubMed
PubMed Central
Google Scholar
Burns, M. A. & Tomkins, D. J. Hypersensitivity to mitomycin C cell-killing in Roberts syndrome fibroblasts with, but not without, the heterochromatin abnormality. Mutat. Res., Sect. Environ. Mutagen. Relat. Subj 216, 243–249 (1989).CAS
Google Scholar
van der Lelij, P. et al. The cellular phenotype of Roberts syndrome fibroblasts as revealed by ectopic expression of ESCO2. PloS One 4, e6936 (2009).Article
ADS
PubMed
PubMed Central
Google Scholar
Van Den Berg, D. J. & Francke, U. Sensitivity of Roberts syndrome cells to gamma radiation, mitomycin C, and protein synthesis inhibitors. Somat. Cell Mol. Genet. 19, 377–392 (1993).Article
PubMed
Google Scholar
Logan, M. et al. Expression of Cre recombinase in the developing mouse limb bud driven by a Prxl enhancer. Genesis 33, 77–80 (2002).Article
CAS
PubMed
Google Scholar
Martin, J. F. & Olson, E. N. Identification of a prx1 limb enhancer. Genesis 26, 225–229 (2000).Article
CAS
PubMed
Google Scholar
Durland, J. L., Sferlazzo, M., Logan, M. & Burke, A. C. Visualizing the lateral somitic frontier in the Prx1Cre transgenic mouse. J. Anat. 212, 590–602 (2008).Article
CAS
PubMed
PubMed Central
Google Scholar
Yin, M. & Pacifici, M. Vascular regression is required for mesenchymal condensation and chondrogenesis in the developing limb. Dev. Dyn. 222, 522–533 (2001).Article
CAS
PubMed
Google Scholar
Eshkar-Oren, I. et al. The forming limb skeleton serves as a signaling center for limb vasculature patterning via regulation of Vegf. Development 136, 1263–1272 (2009).Article
CAS
PubMed
Google Scholar
Komarov, P. G. et al. A chemical inhibitor of p53 that protects mice from the side effects of cancer therapy. Science 285, 1733–1737 (1999).Article
CAS
PubMed
Google Scholar
Jones, N. C. et al. Prevention of the neurocristopathy Treacher Collins syndrome through inhibition of p53 function. Nat. Med. 14, 125–133 (2008).Article
CAS
PubMed
PubMed Central
Google Scholar
Zhou, X., Wang, M., Katsyv, I., Irie, H. & Zhang, B. EMUDRA: ensemble of multiple drug repositioning approaches to improve prediction accuracy. Bioinformatics 34, 3151–3159 (2018).Article
CAS
PubMed
PubMed Central
Google Scholar
Mfarej, M. G. & Skibbens, R. V. An ever-changing landscape in Roberts syndrome biology: implications for macromolecular damage. PLoS Genet 16, e1009219 (2020).Article
CAS
PubMed
PubMed Central
Google Scholar
Salmon, T. B., Evert, B. A., Song, B. & Doetsch, P. W. Biological consequences of oxidative stress-induced DNA damage in Saccharomyces cerevisiae. Nucleic Acids Res. 32, 3712–3723 (2004).Article
CAS
PubMed
PubMed Central
Google Scholar
Rowe, L. A., Degtyareva, N. & Doetsch, P. W. DNA damage-induced reactive oxygen species (ROS) stress response in Saccharomyces cerevisiae. Free Radic. Biol. Med. 45, 1167–1177 (2008).Article
CAS
PubMed
PubMed Central
Google Scholar
Kang, M. et al. DNA damage induces reactive oxygen species generation through the H2AX-Nox1/Rac1 pathway. Cell Death Dis. 3, e249 (2012).Article
CAS
PubMed
PubMed Central
Google Scholar
Xu, B., Lee, K. K., Zhang, L. & Gerton, J. L. Stimulation of mTORC1 with L-leucine rescues defects associated with Roberts syndrome. PLoS Genet. 9, e1003857 (2013).Article
PubMed
PubMed Central
Google Scholar
Xu, B., Gogol, M., Gaudenz, K. & Gerton, J. L. Improved transcription and translation with L-leucine stimulation of mTORC1 in Roberts syndrome. BMC Genom. 17, 1–18 (2016).Article
Google Scholar
McKay, M. J. et al. A Roberts syndrome individual with differential genotoxin sensitivity and a DNA damage response defect. Int. J. Radiat. Oncol. Biol. Phys. 103, 1194–1202 (2019).Article
PubMed
Google Scholar
Ren, Q., Yang, H., Gao, B. & Zhang, Z. Global transcriptional analysis of yeast cell death induced by mutation of sister chromatid cohesin. Compar. Funct. Genom. 2008, e634283 (2008).Article
Google Scholar
Perkins, A. T., Das, T. M., Panzera, L. C. & Bickel, S. E. Oxidative stress in oocytes during midprophase induces premature loss of cohesion and chromosome segregation errors. Proc. Natl Acad. Sci. USA 113, 6823–6830 (2016).Article
ADS
Google Scholar
Polyak, K., Xia, Y., Zweier, J. L., Kinzler, K. W. & Vogelstein, B. A model for p53-induced apoptosis. Nature 389, 300–305 (1997).Article
ADS
CAS
PubMed
Google Scholar
Norbury, C. J. & Zhivotovsky, B. DNA damage-induced apoptosis. Oncogene 23, 2797–2808 (2004).Article
CAS
PubMed
Google Scholar
Shen, H. M. & Liu, Z. G. JNK signaling pathway is a key modulator in cell death mediated by reactive oxygen and nitrogen species. Free Radic. Biol. Med. 40, 928–939 (2006).Article
CAS
PubMed
Google Scholar
Madesh, M. & Hajnóczky, G. VDAC-dependent permeabilization of the outer mitochondrial membrane by superoxide induces rapid and massive cytochrome c release. J. Cell Biol. 155, 1003–1016 (2001).Article
CAS
PubMed
PubMed Central
Google Scholar
Simon, H. U., Haj-Yehia, A. & Levi-Schaffer, F. Role of reactive oxygen species (ROS) in apoptosis induction. Apoptosis 5, 415–418 (2000).Article
CAS
PubMed
Google Scholar
Gotoh, Y. & Cooper, J. A. Reactive oxygen species-and dimerization-induced activation of apoptosis signal-regulating kinase 1 in tumor necrosis factor-α signal transduction. J. Biol. Chem. 273, 17477–17482 (1998).Article
CAS
PubMed
Google Scholar
Lopez, K. E. & Bouchier-Hayes, L. Lethal and non-lethal functions of caspases in the DNA damage response. Cells 11, e1887 (2022).Article
Google Scholar
Schaub, F. J. et al. Fas/FADD-mediated activation of a specific program of inflammatory gene expression in vascular smooth muscle cells. Nat. Med. 6, 790–796 (2000).Article
CAS
PubMed
Google Scholar
Lauber, K. et al. Apoptotic cells induce migration of phagocytes via caspase-3-mediated release of a lipid attraction signal. Cell 113, 717–730 (2003).Article
CAS
PubMed
Google Scholar
Horsfield, J. A. et al. Cohesin-dependent regulation of Runx genes. Development 134, 2639–2649 (2007).Article
CAS
PubMed
Google Scholar
Kim, B. J. et al. Esco2 is a novel corepressor that associates with various chromatin modifying enzymes. Biochem. Biophys. Res. Commun. 372, 298–304 (2008).Article
CAS
PubMed
Google Scholar
Rhodes, J. M., McEwan, M. & Horsfield, J. A. Gene regulation by cohesin in cancer: is the ring an unexpected party to proliferation? Mol. Cancer Res. 9, 1587–1607 (2011).Article
CAS
PubMed
Google Scholar
Mehta, G. D., Rizvi, S. M. A. & Ghosh, S. K. Cohesin: a guardian of genome integrity. Biochim. Biophys. Acta. Mol. Cell. Res. 1823, 1324–1342 (2012).Article
CAS
Google Scholar
Skibbens, R. V., Marzillier, J. & Eastman, L. Cohesins coordinate gene transcriptions of related function within Saccharomyces cerevisiae. Cell Cycle 9, 1601–1606 (2010).Article
CAS
PubMed
Google Scholar
Waldman, T. Emerging themes in cohesin cancer biology. Nat. Rev. Cancer 20, 504–515 (2020).Article
CAS
PubMed
Google Scholar
Vargesson, N. The teratogenic effects of thalidomide on limbs. J Hand Surg Eur Vol. 44, 88–95 (2019).Article
PubMed
Google Scholar
Vargesson, N. & Hootnick, D. Arterial dysgenesis and limb defects: clinical and experimental examples. Reprod. Toxicol. 70, 21–29 (2017).Article
CAS
PubMed
Google Scholar
Meganathan, K. et al. Identification of thalidomide-specific transcriptomics and proteomics signatures during differentiation of human embryonic stem cells. PloS One 7, e44228 (2012).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Bean, C. J., Hunt, P. A., Millie, E. A. & Hassold, T. J. Analysis of a malsegregating mouse Y chromosome: evidence that the earliest cleavage divisions of the mammalian embryo are non-disjunction-prone. Hum. Mol. Genet. 10, 963–972 (2001).Article
CAS
PubMed
Google Scholar
Wang, Y. et al. Activation of p38 MAPK pathway in the skull abnormalities of Apert syndrome Fgfr2+ P253R mice. BMC Dev. Bio. 10, 1–20 (2010).
Google Scholar
Schindelin, J. et al. Fiji: an open-source platform for biological-image analysis. Nat. Methods 9, 676–682 (2012).Article
CAS
PubMed
Google Scholar
Bernsen, J. Dynamic thresholding of grey-level images fcV. Proceeding of the 8 International Conference O11 Pattern Recognition, 1251–1255 (1986).Martin, M. Cutadapt removes adapter sequences from high-throughput sequencing reads. EMBnet J 17, 10–12 (2011).Article
Google Scholar
Dobin, A. et al. STAR: ultrafast universal RNA-seq aligner. Bioinformatics 29, 15–21 (2013).Article
CAS
PubMed
Google Scholar
Liao, Y., Smyth, G. K. & Shi, W. FeatureCounts: an efficient general purpose program for assigning sequence reads to genomic features. Bioinformatics 30, 923–930 (2014).Article
CAS
PubMed
Google Scholar
Ritchie, M. E. et al. Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43, e47 (2015).Article
PubMed
PubMed Central
Google Scholar
Li, B. & Dewey, C. N. RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC Bioinform 12, 1–16 (2011).Article
Google Scholar
Law, C. W., Chen, Y., Shi, W. & Smyth, G. K. Voom: Precision weights unlock linear model analysis tools for RNA-seq read counts. Genome Biol. 15, 1–17 (2014).Article
Google Scholar
Reimand, J., Kull, M., Peterson, H., Hansen, J. & Vilo, J. g: Profiler—a web-based toolset for functional profiling of gene lists from large-scale experiments. Nucleic Acids Res. 35, W193–W200 (2007).Article
PubMed
PubMed Central
Google Scholar
Butler, A., Hoffman, P., Smibert, P., Papalexi, E. & Satija, R. Integrating single-cell transcriptomic data across different conditions, technologies, and species. Nat. Biotechnol. 36, 411–420 (2018).Article
CAS
PubMed
PubMed Central
Google Scholar
Stuart, T. et al. Comprehensive integration of single-cell data. Cell 177, 1888–1902 (2019).Article
CAS
PubMed
PubMed Central
Google Scholar
Hafemeister, C. & Satija, R. Normalization and variance stabilization of single-cell RNA-seq data using regularized negative binomial regression. Genome Biol. 20, 296 (2019).Article
CAS
PubMed
PubMed Central
Google Scholar
Trapnell, C. et al. The dynamics and regulators of cell fate decisions are revealed by pseudotemporal ordering of single cells. Nat. Biotechnol. 32, 381–386 (2014).Article
CAS
PubMed
PubMed Central
Google Scholar
La Manno, G. et al. RNA velocity of single cells. Nature 560, 494–498 (2018).Article
ADS
PubMed
PubMed Central
Google Scholar
RDevelopment, C.O.R.E. TEAM 2009: R: a language and environment for statistical computing. Internet: http://www.R-project.org (2012).Song, W. M. & Zhang, B. Multiscale embedded gene co-expression network analysis. PLoS Comput. Biol. 11, e1004574 (2015).Article
PubMed
PubMed Central
Google Scholar
Subramanian, A. et al. Gene set enrichment analysis: a knowledge-based approach for interpreting genome-wide expression profiles. Proc. Natl Acad. Sci. USA 102, 15545–15550 (2005).Article
ADS
CAS
PubMed
PubMed Central
Google Scholar
Shannon, P. et al. Cytoscape: a software environment for integrated models of biomolecular interaction networks. Genome Res. 13, 2498–2504 (2003).Article
CAS
PubMed
PubMed Central
Google Scholar