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Linyang Ju, Karl M. Glastad, Lihong Sheng, Janko Gospocic, Callum J. Kingwell, Shawn M. Davidson, Sarah D. Kocher, Roberto Bonasio, Shelley L. Berger. Hormonal gatekeeping via the blood-brain barrier governs caste-specific behavior in ants. Cell. September 7, 2023. DOI: https://doi.org/10.1016/j.cell.2023.08.002.
Summary
Here, we reveal an unanticipated role of the blood-brain barrier (BBB) in regulating complex social behavior in ants. Using scRNA-seq, we find localization in the BBB of a key hormone-degrading enzyme called juvenile hormone esterase (Jhe), and we show that this localization governs the level of juvenile hormone (JH3) entering the brain. Manipulation of the Jhe level reprograms the brain transcriptome between ant castes. Although ant Jhe is retained and functions intracellularly within the BBB, we show that Drosophila Jhe is naturally extracellular. Heterologous expression of ant Jhe into the Drosophila BBB alters behavior in fly to mimic what is seen in ants. Most strikingly, manipulation of Jhe levels in ants reprograms complex behavior between worker castes. Our study thus uncovers a remarkable, potentially conserved role of the BBB serving as a molecular gatekeeper for a neurohormonal pathway that regulates social behavior.
Phillip Wulfridge, Qingqing Yan, Nathaniel Rell, John Doherty, Skye Jacobson, Sarah Offley, Sandra Deliard, Kelly Feng, Jennifer E. Phillips-Cremins, Alessandro Gardini, Kavitha Sarma. G-quadruplexes associated with R-loops promote CTCF binding. Molecular Cell. Volume 82, Issue 17. P3064-3079.E5, August 7, 2023. DOI: https://doi.org/10.1016/j.molcel.2023.07.009
Summary
Alexandra M. Maldonado López, Eun Kyung Ko, Sijia Huang, Gina Pacella, Nina Kuprasertkul, Carina A. D’Souza, Raúl A. Reyes Hueros, Hui Shen, Julian Stoute, Heidi Elashal, Morgan Sinkfield, Amy Anderson, Stephen Pourty, Hua-Bing Li, John T. Seykora, Kathy Fange Liu, Brian C. Capell. Mettl3-catalyzed m6A regulates histone modifier and modification expression in self-renewing somatic tissue.Sci. Adv.9,eadg5234(2023).DOI:10.1126/sciadv.adg5234
Abstract
Abstract
Centromeres direct genetic inheritance but are not themselves genetically encoded. Instead, centromeres are defined epigenetically by the presence of a histone H3 variant, CENP-A.1 In cultured somatic cells, an established paradigm of cell-cycle-coupled propagation maintains centromere identity: CENP-A is partitioned between sisters during replication and replenished by new assembly, which is restricted to G1. The mammalian female germ line challenges this model because of the cell-cycle arrest between pre-meiotic S phase and the subsequent G1, which can last for the entire reproductive lifespan (months to decades). New CENP-A chromatin assembly maintains centromeres during prophase I in worm and starfish oocytes,2,3 suggesting that a similar process may be required for centromere inheritance in mammals. To test this hypothesis, we developed an oocyte-specific conditional knockout (cKO) mouse for Mis18α, an essential component of the assembly machinery. We find that embryos derived from Mis18α knockout oocytes fail to assemble CENP-A nucleosomes prior to zygotic genome activation (ZGA), validating the knockout model. We show that deletion of Mis18α in the female germ line at the time of birth has no impact on centromeric CENP-A nucleosome abundance, even after 6-8 months of aging. In addition, there is no detectable detriment to fertility. Thus, centromere chromatin is maintained long-term, independent of new assembly during the extended prophase I arrest in mouse oocytes.
Joint single-cell profiling resolves 5mC and 5hmC and reveals their distinct gene regulatory effects
Abstract
Oxidative modification of 5-methylcytosine (5mC) by ten-eleven translocation (TET) DNA dioxygenases generates 5-hydroxymethylcytosine (5hmC), the most abundant form of oxidized 5mC. Existing single-cell bisulfite sequencing methods cannot resolve 5mC and 5hmC, leaving the cell-type-specific regulatory mechanisms of TET and 5hmC largely unknown. Here, we present joint single-nucleus (hydroxy)methylcytosine sequencing (Joint-snhmC-seq), a scalable and quantitative approach that simultaneously profiles 5hmC and true 5mC in single cells by harnessing differential deaminase activity of APOBEC3A toward 5mC and chemically protected 5hmC. Joint-snhmC-seq profiling of single nuclei from mouse brains reveals an unprecedented level of epigenetic heterogeneity of both 5hmC and true 5mC at single-cell resolution. We show that cell-type-specific profiles of 5hmC or true 5mC improve multimodal single-cell data integration, enable accurate identification of neuronal subtypes and uncover context-specific regulatory effects on cell-type-specific genes by TET enzymes.
Abstract
In development, pioneer transcription factors access silent chromatin to reveal lineage-specific gene programs. The structured DNA-binding domains of pioneer factors have been well characterized, but whether and how intrinsically disordered regions affect chromatin and control cell fate is unclear. Here, we report that deletion of an intrinsically disordered region of the pioneer factor TCF-1 (termed L1) leads to an early developmental block in T cells. The few T cells that develop from progenitors expressing TCF-1 lacking L1 exhibit lineage infidelity distinct from the lineage diversion of TCF-1-deficient cells. Mechanistically, L1 is required for activation of T cell genes and repression of GATA2-driven genes, normally reserved to the mast cell and dendritic cell lineages. Underlying this lineage diversion, L1 mediates binding of TCF-1 to its earliest target genes, which are subject to repression as T cells develop. These data suggest that the intrinsically disordered N terminus of TCF-1 maintains T cell lineage fidelity.
Abstract
The human genome functions as a three-dimensional chromatin polymer, driven by a complex collection of chromosome interactions. Although the molecular rules governing these interactions are being quickly elucidated, relatively few proteins regulating this process have been identified. Here, to address this gap, we developed high-throughput DNA or RNA labelling with optimized Oligopaints (HiDRO)—an automated imaging pipeline that enables the quantitative measurement of chromatin interactions in single cells across thousands of samples. By screening the human druggable genome, we identified more than 300 factors that influence genome folding during interphase. Among these, 43 genes were validated as either increasing or decreasing interactions between topologically associating domains. Our findings show that genetic or chemical inhibition of the ubiquitous kinase GSK3A leads to increased long-range chromatin looping interactions in a genome-wide and cohesin-dependent manner. These results demonstrate the importance of GSK3A signalling in nuclear architecture and the use of HiDRO for identifying mechanisms of spatial genome organization.
Mutant NPM1 hijacks transcriptional hub to maintain pathogenic gene programs in acute myeloid leukemia.Wang X*, Fan D*, Han Q*, Liu Y*, Miao H, Wang X, Li Q, Chen D, Gore H, Himadewi P, Pfeifer GP, Cierpicki T, Grembecka J, Su J, Chong S#, Wan L#, Zhang X#. Cancer Discovery https://doi.org/10.1158/2159-8290.CD-22-0424. (*co-first; #co-corresponding)
A pioneer factor locally opens compacted chromatin to enable targeted ATP-dependent nucleosome remodeling Frederick MA, Williamson KE, Garcia MF, Ferretti MB, McCarthy RL, Donahue G, Monteiro EL, Takenaka N, Reynaga J, Kadoch C, Zaret KS. Nat Struct Mol Biol. 2022 Dec 19; doi: 10.1038/s41594-022-00886-5
CTCF blocks antisense transcription initiation at divergent promoters.
Luan J, Vermunt MW, Syrett CM, Coté A, Tome JM, Zhang H, Huang A, Luppino JM, Keller CA, Giardine BM, Zhang S, Dunagin MC, Zhang Z, Joyce EF, Lis JT, Raj A, Hardison RC, Blobel GA. Nat Struct Mol Biol. 2022 Nov;29(11):1136-1144. doi: 10.1038/s41594-022-00855-y. Epub 2022 Nov 11. PMID: 36369346
Hotspot mutations in the structured ENL YEATS domain link aberrant transcriptional condensates and cancer. Song L*, Yao X*, Li H, Peng B, Boka AP, Liu Y, Chen G, Liu Z, Mathias KM, Xia L, Li Q, Mir M, Li Y#, Li H#, Wan L#. Molecular Cell, 2022 Nov 3;82(21):4080-4098.e12. (featured in cover) PMID:36272410 (*co-first;#co-corresponding)
Small-molecule inhibition of the acyl-lysine reader ENL as a strategy against acute myeloid leukemia
Small-molecule inhibition of the acyl-lysine reader ENL as a strategy against acute myeloid leukemia. Liu Y, Li H, Alikarami F, Barrett DR, Khan TA, Michino M, Hill C, Mahdavi L, Song L, Tang S, Yang L, Li Y, Pokharel SP, Li Q, Stamford AW, Liverton N, Renzetti LM, Taylor S, Watt GF, Ladduwahetty T, Kargman S, Meinke PT, Foley MA, Shi J, Li H, Chen CW, Gardini A, Huggins DJ, Bernt KM#, Wan L#. Cancer Discovery, September 2022.
Quantitative sub-cellular acyl-CoA analysis reveals distinct nuclear metabolism and isoleucine-dependent histone propionylation. Trefely S, Huber K, Liu J Noji M, Stransky S, Singh J, Doan MT, Lovell CD,von Krusenstiern E, Jiang H, Bostwick A, Pepper HL, Izzo L, Zhao Z, Xu JP, Bedi Jr KC, Rame JE, Bogner-Strauss J, Mesaros C, Sidoli S, Wellen KE*,Snyder NW*. Mol Cell, Jan 20;82(2):447-462 *co-corresponding authors
Neuronal YY1 in the prefrontal cortex regulates transcriptional and behavioral responses to chronic stress. Kwon DY, Xu B#, Hu P#, Zhao Y-T, Beagan JA, Nofziger JH, Cui Y, Phillips-Cremins JE, Blendy JA, Wu H, Zhou Z*. Nature Communications 13: 55. doi.org/10.1038/s41467-021-27571-3, 2022.
Berríos KN, Evitt NH, DeWeerd RA, Ren D, Luo M, Barka A, Wang T, Bartman CR, Lan Y, Green AM, Shi J, Kohli RM. Controllable genome editing with split-engineered base editors. Nat Chem Biol. 2021 Oct 18. doi: 10.1038/s41589-021-00880-w. Epub ahead of print. PMID: 34663942.
Temporal manipulation of Cdkl5 reveals essential post-developmental functions and reversible CDKL5 deficiency disorder-related deficits. Terzic B, Davatolhagh MF, Ho Y, Tang S, Liu Y-T, Xia Z, Cui Y, Fuccillo MV and Zhou Z*. Journal of Clinical Investigation 131(20): e143655, 2021.
Temporal manipulation of Cdkl5 reveals essential post-developmental functions and reversible CDKL5 deficiency disorder-related deficits. Terzic B, Davatolhagh MF, Ho Y, Tang S, Liu Y-T, Xia Z, Cui Y, Fuccillo MV and Zhou Z*. Journal of Clinical Investigation 131(20): e143655, 2021.
Linares-Saldana R, Kim W, Bolar NA, Zhang H, Koch-Bojalad BA, Yoon S, Shah PP, Karnay A, Park DS, Luppino JM, Nguyen SC, Padmanabhan A, Smith CL, Poleshko A, Wang Q, Li L, Srivastava D, Vahedi G, Eom GH, Blobel GA, Joyce EF, Jain R. BRD4 orchestrates genome folding to promote neural crest differentiation. Nat Genet. 2021 Oct;53(10):1480-1492. doi: 10.1038/s41588-021-00934-8. Epub 2021 Oct 5. PMID: 34611363.
Glastad KM, Ju L, Berger SL. PLoS Genet. 2021 Sep 22;17(9):e1009801. doi: 10.1371/journal.pgen.1009801. PMID: 34550980; PMCID: PMC8489709.
Mellis IA, Edelstein HI, Truitt R, Goyal Y, Beck LE, Symmons O, Dunagin MC, Linares Saldana RA, Shah PP, Pérez-Bermejo JA, Padmanabhan A, Yang W, Jain R, Raj A. Cell Syst. 2021 Sep 22;12(9):885-899.e8. doi: 10.1016/j.cels.2021.07.003. Epub 2021 Aug 4. PMID: 34352221.
Single-molecule tracking technologies for quantifying the dynamics of gene regulation in cells, tissue, and embryos.
A.P. Boka, A. Mukherjee, M. Mir. Development 148(18): dev199744, September 2021.
Blobel GA, Higgs DR, Mitchell JA, Notani D, Young RA. Testing the super-enhancer concept. Nat Rev Genet. 2021 Sep 3. doi: 10.1038/s41576-021-00398-w. Epub ahead of print. PMID: 34480110.
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Aleman JR, Kuhn TM, Pascual-Garcia P, Gospocic J, Lan Y, Bonasio R, Little SC, Capelson M. Cell Rep. 2021 Jun 15;35(11):109236. doi: 10.1016/j.celrep.2021.109236. PMID: 34133927.
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Chemically Linked Vemurafenib Inhibitors Promote an Inactive BRAFV600E Conformation. Grasso M, Estrada MA, Ventocilla C, Samanta M, Maksimoska J, Villanueva J, Winkler JD, Marmorstein R. ACS Chem Biol. 2016 Oct 21;11(10):2876-2888. Epub 2016 Sep 6.
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A Novel Quantitative Mass Spectrometry Platform for Determining Protein O-GlcNAcylation Dynamics. Wang X, Yuan ZF, Fan J, Karch KR, Ball LE, Denu JM, Garcia BA. Mol Cell Proteomics. 2016 Jul;15(7):2462-75. doi: 10.1074/mcp.O115.049627. Epub 2016 Apr 25.
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The Pioneer Transcription Factor FoxA Maintains an Accessible Nucleosome Configuration at Enhancers for Tissue-Specific Gene Activation. Iwafuchi-Doi M, Donahue G, Kakumanu A, Watts JA, Mahony S, Pugh BF, Lee D, Kaestner KH, Zaret KS. Mol Cell. 2016 Apr 7;62(1):79-91. doi: 10.1016/j.molcel.2016.03.001.
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AINTEGUMENTA and AINTEGUMENTA-LIKE6/PLETHORA3 Induce LEAFY Expression in Response to Auxin to Promote the Onset of Flower Formation in Arabidopsis. Yamaguchi N, Jeong CW, Nole-Wilson S, Krizek BA, Wagner D. Plant Physiol. 2016 Jan;170(1):283-93. doi: 10.1104/pp.15.00969. Epub 2015 Nov 4.
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