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Chromatin structure undergoes global and local reorganization during murine dendritic cell development and activation

Kurotaki, Daisuke ; Kikuchi, Kenta ; Cui, Kairong ; Kawase, Wataru ; Saeki, Keita ; Fukumoto, Junpei ; Nishiyama, Akira ; Nagamune, Kisaburo ; Zhao, Keji ; Ozato, Keiko ; Rocha, Pedro P ; Tamura, Tomohiko

Proceedings of the National Academy of Sciences - PNAS, 2022-08, Vol.119 (34), p.e2207009119-e2207009119 [Periódico revisado por pares]

United States: National Academy of Sciences

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  • Título:
    Chromatin structure undergoes global and local reorganization during murine dendritic cell development and activation
  • Autor: Kurotaki, Daisuke ; Kikuchi, Kenta ; Cui, Kairong ; Kawase, Wataru ; Saeki, Keita ; Fukumoto, Junpei ; Nishiyama, Akira ; Nagamune, Kisaburo ; Zhao, Keji ; Ozato, Keiko ; Rocha, Pedro P ; Tamura, Tomohiko
  • Assuntos: Animals ; Biological Sciences ; CDC gene ; Cell activation ; Cell differentiation ; Cell Differentiation - genetics ; Chemokines ; Chromatin ; Chromatin - genetics ; Chromatin - metabolism ; Chromatin Assembly and Disassembly ; Compartments ; Cytokines ; Dendritic cells ; Dendritic Cells - cytology ; Differentiation ; Gene expression ; Gene Expression Regulation ; Gene loci ; Gene regulation ; Hematopoietic Stem Cells ; Infections ; Mice ; Monocytes ; Progenitor cells ; Stem cell transplantation ; Stem cells ; Subpopulations
  • É parte de: Proceedings of the National Academy of Sciences - PNAS, 2022-08, Vol.119 (34), p.e2207009119-e2207009119
  • Notas: ObjectType-Article-1
    SourceType-Scholarly Journals-1
    ObjectType-Feature-2
    content type line 23
    1D.K. and K.K. contributed equally to this work.
    Author contributions: D.K., P.P.R., and T.T. designed research; D.K., K.C., W.K., K.S., J.F., A.N., and K.N. performed research;  D.K., K.K., and T.T. analyzed data; D.K., K.K., K.O., P.P.R., and T.T. wrote the paper; D.K. and T.T. supervised the project; K.N., K.Z., K.O., and P.P.R. provided key materials; and K.Z., K.O., and P.P.R. provided critical suggestions.
    Edited by Kenneth Murphy, Washington University in St. Louis School of Medicine, St. Louis, MO; received April 23, 2022; accepted July 15, 2022
  • Descrição: Classical dendritic cells (cDCs) are essential for immune responses and differentiate from hematopoietic stem cells via intermediate progenitors, such as monocyte-DC progenitors (MDPs) and common DC progenitors (CDPs). Upon infection, cDCs are activated and rapidly express host defense-related genes, such as those encoding cytokines and chemokines. Chromatin structures, including nuclear compartments and topologically associating domains (TADs), have been implicated in gene regulation. However, the extent and dynamics of their reorganization during cDC development and activation remain unknown. In this study, we comprehensively determined higher-order chromatin structures by Hi-C in DC progenitors and cDC subpopulations. During cDC differentiation, chromatin activation was initially induced at the MDP stage. Subsequently, a shift from inactive to active nuclear compartments occurred at the cDC gene loci in CDPs, which was followed by increased intra-TAD interactions and loop formation. Mechanistically, the transcription factor IRF8, indispensable for cDC differentiation, mediated chromatin activation and changes into the active compartments in DC progenitors, thereby possibly leading to cDC-specific gene induction. Using an infection model, we found that the chromatin structures of host defense-related gene loci were preestablished in unstimulated cDCs, indicating that the formation of higher-order chromatin structures prior to infection may contribute to the rapid responses to pathogens. Overall, these results suggest that chromatin structure reorganization is closely related to the establishment of cDC-specific gene expression and immune functions. This study advances the fundamental understanding of chromatin reorganization in cDC differentiation and activation.
  • Editor: United States: National Academy of Sciences
  • Idioma: Inglês
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  • Realização: ABCD-USP USP   Logos de Redes Sociais: Freepik

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