In this episode of the Epigenetics Podcast, we caught up with Ben Delatte Research Scientist at Active Motif to talk about his work on Anchor Based Bisulfite Sequencing.

Whole Genome Bisulfite Sequencing (WGBS) is the current standard for DNA methylation profiling. However, this approach is costly as it requires sequencing coverage over the entire genome. Here we introduce Anchor-Based Bisulfite Sequencing (ABBS). ABBS captures accurate DNA methylation information in Escherichia coli and mammals, while requiring up to 10 times fewer sequencing reads than WGBS. ABBS interrogates the entire genome and is not restricted to the CpG islands assayed by methods like Reduced Representation Bisulfite Sequencing (RRBS). The ABBS protocol is simple and can be performed in a single day.

References

Chapin, N., Fernandez, J., Poole, J. et al. Anchor-based bisulfite sequencing determines genome-wide DNA methylation. Commun Biol 5, 596 (2022). https://doi.org/10.1038/s42003-022-03543-1

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In this episode of the Epigenetics Podcast, we caught up with Susanne Mandrup from the University of Southern Denmark to talk about her work on the role of enhancer communities in adipocyte differentiation.

The Laboratory of Susanne Mandrup focuses on the effect of enhancers and enhancer communities on the differentiation of mesenchymal stem cell into adipocytes and osteoblasts. The team has shown that there is significant cross-talk between enhancers and that these form communities of highly interconnected enhancers. Inactive enhancers are then activated by association with these pre-existing enhancer networks to facilitate gene expression in adipocyte differentiation.

References

Siersbæk R, Rabiee A, Nielsen R, Sidoli S, Traynor S, Loft A, Poulsen LC, Rogowska-Wrzesinska A, Jensen ON, Mandrup S. Transcription factor cooperativity in early adipogenic hotspots and super-enhancers. Cell Rep. 2014 Jun 12;7(5):1443-1455. doi: 10.1016/j.celrep.2014.04.042. Epub 2014 May 22. PMID: 24857652.

Siersbæk R, Baek S, Rabiee A, Nielsen R, Traynor S, Clark N, Sandelin A, Jensen ON, Sung MH, Hager GL, Mandrup S. Molecular architecture of transcription factor hotspots in early adipogenesis. Cell Rep. 2014 Jun 12;7(5):1434-1442. doi: 10.1016/j.celrep.2014.04.043. Epub 2014 May 22. PMID: 24857666; PMCID: PMC6360525.

Siersbæk R, Madsen JGS, Javierre BM, Nielsen R, Bagge EK, Cairns J, Wingett SW, Traynor S, Spivakov M, Fraser P, Mandrup S. Dynamic Rewiring of Promoter-Anchored Chromatin Loops during Adipocyte Differentiation. Mol Cell. 2017 May 4;66(3):420-435.e5. doi: 10.1016/j.molcel.2017.04.010. PMID: 28475875.

Rauch, A., Haakonsson, A.K., Madsen, J.G.S. et al. Osteogenesis depends on commissioning of a network of stem cell transcription factors that act as repressors of adipogenesis. Nat Genet 51, 716–727 (2019). https://doi.org/10.1038/s41588-019-0359-1

Madsen, J.G.S., Madsen, M.S., Rauch, A. et al. Highly interconnected enhancer communities control lineage-determining genes in human mesenchymal stem cells. Nat Genet 52, 1227–1238 (2020). https://doi.org/10.1038/s41588-020-0709-z

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In this episode of the Epigenetics Podcast, we caught up with Marco Trizzino from Thomas Jefferson University to talk about his work on transposable elements in gene regulation and evolution.

Marco Trizzino and his team focus on characterising transposable elements and how they affect gene regulation, evolution and ageing in primates. They could show that transposable elements that integrated into the genome turned into regulatory elements in the genome, like enhancers. They then contribute to regulation of processes like development or ageing, which could be among those factors that lead to increased brain development or longevity in great apes.

References

Trizzino M, Park Y, Holsbach-Beltrame M, Aracena K, Mika K, Caliskan M, Perry GH, Lynch VJ, Brown CD. Transposable elements are the primary source of novelty in primate gene regulation. Genome Res. 2017 Oct;27(10):1623-1633. doi: 10.1101/gr.218149.116. Epub 2017 Aug 30. PMID: 28855262; PMCID: PMC5630026.

Pagliaroli L, Porazzi P, Curtis AT, Scopa C, Mikkers HMM, Freund C, Daxinger L, Deliard S, Welsh SA, Offley S, Ott CA, Calabretta B, Brugmann SA, Santen GWE, Trizzino M. Inability to switch from ARID1A-BAF to ARID1B-BAF impairs exit from pluripotency and commitment towards neural crest formation in ARID1B-related neurodevelopmental disorders. Nat Commun. 2021 Nov 9;12(1):6469. doi: 10.1038/s41467-021-26810-x. PMID: 34753942; PMCID: PMC8578637.

Tejada-Martinez D, Avelar RA, Lopes I, Zhang B, Novoa G, de Magalhães JP, Trizzino M. Positive Selection and Enhancer Evolution Shaped Lifespan and Body Mass in Great Apes. Mol Biol Evol. 2022 Feb 3;39(2):msab369. doi: 10.1093/molbev/msab369. PMID: 34971383; PMCID: PMC8837823.

Young transposable elements rewired gene regulatory networks in human and chimpanzee hippocampal intermediate progenitors. Sruti Patoori, Samantha M. Barnada, Christopher Large, John I. Murray, Marco Trizzino. bioRxiv 2021.11.24.469877; doi: https://doi.org/10.1101/2021.11.24.469877

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In this episode of the Epigenetics Podcast, we caught up with Marcela Sjöberg from the Pontificia Universidad Católica de Chile to talk about her work on the hydroxymethylation landscape in immune cells.

At the beginning of her career Marcela Sjöberg worked on Aurora B and Polycomb and how modifications placed by them modulate the binding of RNA Pol II. Later, her focus shifted to examine cytosine DNA methylation and hydroxymethylation changes in immune cells and how the epigenetic state of these marks varies between individuals and is reprogrammed for Metastable Epialleles in mouse. More recently, the laboratory is interested on how hydroxymethylation of transcription factor binding motifs influence binding and activity of the respective transcription factors in immune cells.

References

Sabbattini, P., Sjoberg, M., Nikic, S., Frangini, A., Holmqvist, P.-H., Kunowska, N., Carroll, T., Brookes, E., Arthur, S. J., Pombo, A., & Dillon, N. (2014). An H3K9/S10 methyl-phospho switch modulates Polycomb and Pol II binding at repressed genes during differentiation. Molecular Biology of the Cell, 25(6), 904–915. https://doi.org/10.1091/mbc.e13-10-0628

Kazachenka, A., Bertozzi, T. M., Sjoberg-Herrera, M. K., Walker, N., Gardner, J., Gunning, R., Pahita, E., Adams, S., Adams, D., & Ferguson-Smith, A. C. (2018). Identification, Characterization, and Heritability of Murine Metastable Epialleles: Implications for Non-genetic Inheritance. Cell, 175(5), 1259-1271.e13. https://doi.org/10.1016/j.cell.2018.09.043

Westoby, J., Herrera, M.S., Ferguson-Smith, A.C. et al. Simulation-based benchmarking of isoform quantification in single-cell RNA-seq. Genome Biol 19, 191 (2018). https://doi.org/10.1186/s13059-018-1571-5

Viner, C., Johnson, J., Walker, N., Shi, H., Sjöberg, M., Adams, D. J., Ferguson-Smith, A. C., Bailey, T. L., & Hoffman, M. M. (2016). Modeling methyl-sensitive transcription factor motifs with an expanded epigenetic alphabet [Preprint]. Bioinformatics. https://doi.org/10.1101/043794

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In this episode of the Epigenetics Podcast, we caught up with Tim Petros from the Eunice Kennedy Shriver National Institute of Child Health and Human Development at the NIH to talk about his work on Single Cell Epigenomics in Neuronal Development. 

The Petros lab focuses on “interneurons”, their diversity and how environmental signals interact to generate this diversity. This subgroup of neurons comprise about 20% of neutrons in the brain, however, they are the primary source of inhibition. Furthermore, interneurons are critical components in modulating information flow throughout the nervous system. The Petros lab seeks to uncover the genetic programs that lead to the incredible diversity in interneurons, as well as how the local environment influences this process. 

To lay a foundation for this and to provide a data-base for other researchers the Petros lab generated an epigenome atlas of neural progenitor cells of the mouse brain. This data includes scRNA-Seq, snATAC-Seq, CUT&Tag (H3K4me3, H3K27me3), CUT&RUN (H3K27ac), Hi-C and Capture-C. This data can be downloaded at the link below:  

https://www.nichd.nih.gov/research/atNICHD/Investigators/petros/data-sharing 

References

Datasets: https://www.nichd.nih.gov/research/atNICHD/Investigators/petros/data-sharing

Quattrocolo G, Fishell G, Petros TJ. Heterotopic Transplantations Reveal Environmental Influences on Interneuron Diversity and Maturation. Cell Rep. 2017 Oct 17;21(3):721-731. doi: 10.1016/j.celrep.2017.09.075. PMID: 29045839; PMCID: PMC5662128.

Dongjin R Lee, Christopher Rhodes, Apratim Mitra, Yajun Zhang, Dragan Maric, Ryan K Dale, Timothy J Petros (2022) Transcriptional heterogeneity of ventricular zone cells in the ganglionic eminences of the mouse forebrain eLife 11:e71864 https://doi.org/10.7554/eLife.71864

Rhodes, C. T., Thompson, J. J., Mitra, A., Asokumar, D., Lee, D. R., Lee, D. J., Zhang, Y., Jason, E., Dale, R. K., Rocha, P. P., & Petros, T. J. (2022). An epigenome atlas of neural progenitors within the embryonic mouse forebrain. Nature communications, 13(1), 4196. https://doi.org/10.1038/s41467-022-31793-4

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In this episode of the Epigenetics Podcast, we caught up with Nada Jabado from McGill University to talk about her work on oncohistones as drivers of Pediatric Brain Tumors.

Nada Jabado and her team were amongst the first to identify mutations in Histone 3.3 Tails which lead to differentially remodeled chromatin in pediatric glioblastoma. Mutations that occur include the Lysine at position 27 and the Glycine at position 34. If those residues are mutated it will influence the equilibrium of chromatin associated proteins like the Polycomb Repressive Complex (PRC) and hence domains of heterochromatin will be shifted. This, in turn, will lead to differential gene expression and development of developmental disorders or cancer.

References

Schwartzentruber, J., Korshunov, A., Liu, X. Y., Jones, D. T., Pfaff, E., Jacob, K., Sturm, D., Fontebasso, A. M., Quang, D. A., Tönjes, M., Hovestadt, V., Albrecht, S., Kool, M., Nantel, A., Konermann, C., Lindroth, A., Jäger, N., Rausch, T., Ryzhova, M., Korbel, J. O., … Jabado, N. (2012). Driver mutations in histone H3.3 and chromatin remodelling genes in paediatric glioblastoma. Nature, 482(7384), 226–231. https://doi.org/10.1038/nature10833

Kleinman, C. L., Gerges, N., Papillon-Cavanagh, S., Sin-Chan, P., Pramatarova, A., Quang, D. A., Adoue, V., Busche, S., Caron, M., Djambazian, H., Bemmo, A., Fontebasso, A. M., Spence, T., Schwartzentruber, J., Albrecht, S., Hauser, P., Garami, M., Klekner, A., Bognar, L., Montes, J. L., … Jabado, N. (2014). Fusion of TTYH1 with the C19MC microRNA cluster drives expression of a brain-specific DNMT3B isoform in the embryonal brain tumor ETMR. Nature genetics, 46(1), 39–44. https://doi.org/10.1038/ng.2849

Papillon-Cavanagh, S., Lu, C., Gayden, T., Mikael, L. G., Bechet, D., Karamboulas, C., Ailles, L., Karamchandani, J., Marchione, D. M., Garcia, B. A., Weinreb, I., Goldstein, D., Lewis, P. W., Dancu, O. M., Dhaliwal, S., Stecho, W., Howlett, C. J., Mymryk, J. S., Barrett, J. W., Nichols, A. C., … Jabado, N. (2017). Impaired H3K36 methylation defines a subset of head and neck squamous cell carcinomas. Nature genetics, 49(2), 180–185. https://doi.org/10.1038/ng.3757

Chen, C., Deshmukh, S., Jessa, S., Hadjadj, D., Lisi, V., Andrade, A. F., Faury, D., Jawhar, W., Dali, R., Suzuki, H., Pathania, M., A, D., Dubois, F., Woodward, E., Hébert, S., Coutelier, M., Karamchandani, J., Albrecht, S., Brandner, S., De Jay, N., … Jabado, N. (2020). Histone H3.3G34-Mutant Interneuron Progenitors Co-opt PDGFRA for Gliomagenesis. Cell, 183(6), 1617–1633.e22. https://doi.org/10.1016/j.cell.2020.11.012

Chaouch, A., Berlandi, J., Chen, C., Frey, F., Badini, S., Harutyunyan, A. S., Chen, X., Krug, B., Hébert, S., Jeibmann, A., Lu, C., Kleinman, C. L., Hasselblatt, M., Lasko, P., Shirinian, M., & Jabado, N. (2021). Histone H3.3 K27M and K36M mutations de-repress transposable elements through perturbation of antagonistic chromatin marks. Molecular cell, 81(23), 4876–4890.e7. https://doi.org/10.1016/j.molcel.2021.10.008

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In this episode of the Epigenetics Podcast, we caught up with Goncalo Castelo-Branco from the Karolinska Institute to talk about his work on the characterization of epigenetic states in the Oligodendrocyte Lineage.

The group from Gonçalo Castelo-Branco’s lab focuses on characterizing epigenetic states of oligodendrocytes, with the aim to understand their contribution to diseases like multiple sclerosis. To do this the group used single-cell RNA-Seq to identify sub-populations of oligodendrocytes. Furthermore, the team pioneered improvements in CUT&Tag and applied it to the single-cell space, as well as developing spatial CUT&Tag. More recently they used nanobodies in an optimised version of single cell CUT&Tag that allows simultaneous probing of three epigenomic modalities at single-cell resolution, using nanobody-Tn5 fusion proteins. The three modalities encompass chromatin accessibility as measured via ATAC-Seq and two histone post-transcriptional modifications.

References

Deng Y, Bartosovic M, Kukanja P, Zhang D, Liu Y, Su G, Enninful A, Bai Z, Castelo-Branco G, Fan R. Spatial-CUT&Tag: Spatially resolved chromatin modification profiling at the cellular level. Science. 2022 Feb 11;375(6581):681-686. doi: 10.1126/science.abg7216. Epub 2022 Feb 10. PMID: 35143307.

Winick-Ng W, Kukalev A, Harabula I, Zea-Redondo L, Szabó D, Meijer M, Serebreni L, Zhang Y, Bianco S, Chiariello AM, Irastorza-Azcarate I, Thieme CJ, Sparks TM, Carvalho S, Fiorillo L, Musella F, Irani E, Torlai Triglia E, Kolodziejczyk AA, Abentung A, Apostolova G, Paul EJ, Franke V, Kempfer R, Akalin A, Teichmann SA, Dechant G, Ungless MA, Nicodemi M, Welch L, Castelo-Branco G, Pombo A. Cell-type specialization is encoded by specific chromatin topologies. Nature. 2021 Nov;599(7886):684-691. doi: 10.1038/s41586-021-04081-2. Epub 2021 Nov 17. PMID: 34789882; PMCID: PMC8612935.

Bartosovic M, Kabbe M, Castelo-Branco G. Single-cell CUT&Tag profiles histone modifications and transcription factors in complex tissues. Nat Biotechnol. 2021 Jul;39(7):825-835. doi: 10.1038/s41587-021-00869-9. Epub 2021 Apr 12. PMID: 33846645; PMCID: PMC7611252.

Marek Bartosovic, Gonçalo Castelo-Branco. Multimodal chromatin profiling using nanobody-based single-cell CUT&Tag. bioRxiv. 2022.03.08.483459; doi: https://doi.org/10.1101/2022.03.08.483459

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In this episode of the Epigenetics Podcast, we caught up with Active Motif’s own Yuan Xue to talk about some of the challenges of performing ATAC-Seq.

ATAC-Seq stands for Assay for Transposase-Accessible Chromatin with high-throughput sequencing and was initially described by Jason Buenrostro in 2013. The ATAC-Seq method relies on next-generation sequencing (NGS) library construction using the hyperactive transposase Tn5. NGS adapters are loaded onto the transposase, which allows simultaneous fragmentation of chromatin and integration of those adapters into open chromatin regions. ATAC-Seq is an attractive method to start your epigenetic journey. Whether you want to analyze the state of the chromatin in your sample or compare the chromatin state before and after a special treatment, ATAC-Seq allows you to investigate genome-wide chromatin changes and can offer guidelines about which epigenetic modification or transcription factor should be studied next in the follow-up experiments and which method should be used to study them.

In this Episode we go through the Protocol in detail and discuss potential challenges and points to pay attention to when starting your first ATAC-Seq experiment.

References

ATAC-Seq Resource Center

Complete Guide to Understanding and Using ATAC-Seq

Beginner’s Guide to Understanding Single-Cell ATAC-Seq

Buenrostro, J. D., Giresi, P. G., Zaba, L. C., Chang, H. Y., & Greenleaf, W. J. (2013). Transposition of native chromatin for fast and sensitive epigenomic profiling of open chromatin, DNA-binding proteins and nucleosome position. Nature methods, 10(12), 1213–1218. https://doi.org/10.1038/nmeth.2688

Buenrostro, J. D., Wu, B., Litzenburger, U. M., Ruff, D., Gonzales, M. L., Snyder, M. P., Chang, H. Y., & Greenleaf, W. J. (2015). Single-cell chromatin accessibility reveals principles of regulatory variation. Nature, 523(7561), 486–490. https://doi.org/10.1038/nature14590

Cusanovich, D. A., Daza, R., Adey, A., Pliner, H. A., Christiansen, L., Gunderson, K. L., Steemers, F. J., Trapnell, C., & Shendure, J. (2015). Multiplex single cell profiling of chromatin accessibility by combinatorial cellular indexing. Science (New York, N.Y.), 348(6237), 910–914. https://doi.org/10.1126/science.aab1601

Podcast: ATAC-Seq, scATAC-Seq and Chromatin Dynamics in Single-Cells (Jason Buenrostro)

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In this episode of the Epigenetics Podcast, we caught up with John Rinn from the University of Colorado in Boulder to talk about his work on the role of lncRNAs in gene expression and nuclear organization.

The Rinn Lab pioneered the approach of screening the human genome for long noncoding RNAs (lncRNAs). More recently, the lab has shifted focus from measuring the number of lncRNAs to finding lncRNAs that have a distinct biological function in human health and disease. One example of such a lncRNA is FIRRE, which is present in all animals, however the sequence is not conserved, except for in primates. FIRRE contains many interesting features, such as repeat sequences and CTCF binding sites. In absence of FIRRE, defects in the immune system can be observed and also some brain defects may also be observed.

References

Carter, T., Singh, M., Dumbovic, G., Chobirko, J. D., Rinn, J. L., & Feschotte, C. (2022). Mosaic cis-regulatory evolution drives transcriptional partitioning of HERVH endogenous retrovirus in the human embryo. eLife, 11, e76257. Advance online publication. https://doi.org/10.7554/eLife.76257

Long, Y., Hwang, T., Gooding, A. R., Goodrich, K. J., Rinn, J. L., & Cech, T. R. (2020). RNA is essential for PRC2 chromatin occupancy and function in human pluripotent stem cells. Nature Genetics, 52(9), 931–938. https://doi.org/10.1038/s41588-020-0662-x

Kelley, D., & Rinn, J. (2012). Transposable elements reveal a stem cell-specific class of long noncoding RNAs. Genome biology, 13(11), R107. https://doi.org/10.1186/gb-2012-13-11-r107

Khalil, A. M., Guttman, M., Huarte, M., Garber, M., Raj, A., Rivea Morales, D., Thomas, K., Presser, A., Bernstein, B. E., van Oudenaarden, A., Regev, A., Lander, E. S., & Rinn, J. L. (2009). Many human large intergenic noncoding RNAs associate with chromatin-modifying complexes and affect gene expression. Proceedings of the National Academy of Sciences, 106(28), 11667–11672. https://doi.org/10.1073/pnas.0904715106

Guttman, M., Amit, I., Garber, M., French, C., Lin, M. F., Feldser, D., Huarte, M., Zuk, O., Carey, B. W., Cassady, J. P., Cabili, M. N., Jaenisch, R., Mikkelsen, T. S., Jacks, T., Hacohen, N., Bernstein, B. E., Kellis, M., Regev, A., Rinn, J. L., & Lander, E. S. (2009). Chromatin signature reveals over a thousand highly conserved large non-coding RNAs in mammals. Nature, 458(7235), 223–227. https://doi.org/10.1038/nature07672

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 In this episode of the Epigenetics Podcast, we caught up with Morgan Levine from Altos lab to talk about her work on Epigenetic Clocks and Biomarkers of Ageing.

The Levine Lab focuses on deciphering mechanisms that lead to epigenetic ageing, which can be measured by epigenetic clocks. Epigenetic clocks were first described in 2011 by Bocklandt et al.. Later-on, the Horvath and the Hannum clock were described by using a combination of CpGs to calculate biological/epigenetic age in contrast to chronological age.

The Levine Lab themselves worked on generating an advanced version of an Epigenetic clock, called "DNAm PhenoAge" that will now be used, and not only in human samples. The team now moves to mouse models and to cells in a dish and using those models to investigate the mechanisms behind epigenetic aging.

References

Liu, Z., Leung, D., Thrush, K., Zhao, W., Ratliff, S., Tanaka, T., Schmitz, L. L., Smith, J. A., Ferrucci, L., & Levine, M. E. (2020). Underlying features of epigenetic aging clocks in vivo and in vitro. Aging cell, 19(10), e13229. https://doi.org/10.1111/acel.13229

Levine, M. E., Lu, A. T., Quach, A., Chen, B. H., Assimes, T. L., Bandinelli, S., Hou, L., Baccarelli, A. A., Stewart, J. D., Li, Y., Whitsel, E. A., Wilson, J. G., Reiner, A. P., Aviv, A., Lohman, K., Liu, Y., Ferrucci, L., & Horvath, S. (2018). An epigenetic biomarker of aging for lifespan and healthspan. Aging, 10(4), 573–591. https://doi.org/10.18632/aging.101414

Levine, M., McDevitt, R. A., Meer, M., Perdue, K., Di Francesco, A., Meade, T., Farrell, C., Thrush, K., Wang, M., Dunn, C., Pellegrini, M., de Cabo, R., & Ferrucci, L. (2020). A rat epigenetic clock recapitulates phenotypic aging and co-localizes with heterochromatin. eLife, 9, e59201. https://doi.org/10.7554/eLife.59201

Kuo, C. L., Pilling, L. C., Atkins, J. C., Masoli, J., Delgado, J., Tignanelli, C., Kuchel, G., Melzer, D., Beckman, K. B., & Levine, M. (2020). COVID-19 severity is predicted by earlier evidence of accelerated aging. medRxiv : the preprint server for health sciences, 2020.07.10.20147777. https://doi.org/10.1101/2020.07.10.20147777

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