Four-dimensional chromosome reconstruction elucidates the spatiotemporal reorganization of the mammalian X chromosome.

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Abstrakt

Tytuł:: Four-dimensional chromosome reconstruction elucidates the spatiotemporal reorganization of the mammalian X chromosome.
Autorzy:: Lappala A; Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545.; Department of Molecular Biology, Massachusetts General Hospital, Boston, MA 02114.; Department of Genetics, The Blavatnik Institute, Harvard Medical School, Boston, MA 02114.
Wang CY; Department of Molecular Biology, Massachusetts General Hospital, Boston, MA 02114.; Department of Genetics, The Blavatnik Institute, Harvard Medical School, Boston, MA 02114.
Kriz A; Department of Molecular Biology, Massachusetts General Hospital, Boston, MA 02114.; Department of Genetics, The Blavatnik Institute, Harvard Medical School, Boston, MA 02114.
Michalk H; Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545.
Tan K; Department of Molecular Biology, Massachusetts General Hospital, Boston, MA 02114.; Department of Genetics, The Blavatnik Institute, Harvard Medical School, Boston, MA 02114.
Lee JT; Department of Molecular Biology, Massachusetts General Hospital, Boston, MA 02114; .; Department of Genetics, The Blavatnik Institute, Harvard Medical School, Boston, MA 02114.
Sanbonmatsu KY; Theoretical Biology and Biophysics, Los Alamos National Laboratory, Los Alamos, NM 87545; .; New Mexico Consortium, Los Alamos, NM 87545.
Źródło:: Proceedings of the National Academy of Sciences of the United States of America [Proc Natl Acad Sci U S A] 2021 Oct 19; Vol. 118 (42).
Typ publikacji:: Journal Article; Research Support, N.I.H., Extramural; Research Support, Non-U.S. Gov't
Język:: English
Imprint Name(s):: Original Publication: Washington, DC : National Academy of Sciences
MeSH Terms:: X Chromosome*
Mammals/*genetics
Animals ; X Chromosome Inactivation
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Grant Information:: F31 HD100109 United States HD NICHD NIH HHS; R01 HD097665 United States HD NICHD NIH HHS
Contributed Indexing:: Keywords: 3D modeling; SMCHD1; X chromosome inactivation; Xist RNA; chromosome structure
Entry Date(s):: Date Created: 20211014 Date Completed: 20211220 Latest Revision: 20220414
Update Code:: 20240104
PubMed Central ID:: PMC8594586
DOI:: 10.1073/pnas.2107092118
PMID:: 34645712
: Czasopismo naukowe

Chromosomes are segmented into domains and compartments, but how these structures are spatially related in three dimensions (3D) is unclear. Here, we developed tools that directly extract 3D information from Hi-C experiments and integrate the data across time. With our "4DHiC" method, we use X chromosome inactivation (XCI) as a model to examine the time evolution of 3D chromosome architecture during large-scale changes in gene expression. Our modeling resulted in several insights. Both A/B and S1/S2 compartments divide the X chromosome into hemisphere-like structures suggestive of a spatial phase-separation. During the XCI, the X chromosome transits through A/B, S1/S2, and megadomain structures by undergoing only partial mixing to assume new structures. Interestingly, when an active X chromosome (Xa) is reorganized into an inactive X chromosome (Xi), original underlying compartment structures are not fully eliminated within the Xi superstructure. Our study affirms slow mixing dynamics in the inner chromosome core and faster dynamics near the surface where escapees reside. Once established, the Xa and Xi resemble glassy polymers where mixing no longer occurs. Finally, Xist RNA molecules initially reside within the A compartment but transition to the interface between the A and B hemispheres and then spread between hemispheres via both surface and core to establish the Xi.
Competing Interests: Competing interest statement: J.T.L. is a cofounder of Translate Bio and Fulcrum, and is an advisor to Skyhawk Therapeutics.

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