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SUMOylation differentially regulates SMCHD1 complex formation and function in a genomic context-specific manner

Goossens, R.; Tihaya, M. S.; Willemsen, I. M.; Straasheijm, K. R.; van der Vliet, P. J.; Gonzalez-Prieto, R.; Vertegaal, A. C. O.; Tapscott, S. J.; Balog, J.; van der Maarel, S. M.

2024-10-13 molecular biology
10.1101/2024.10.13.618066 bioRxiv
Show abstract

Structural Maintenance of Chromosomes Hinge Domain Containing 1 (SMCHD1) is a chromatin repressor regulating gene expression and chromatin architecture of distinct autosomal and X-chromosomal loci. SMCHD1 mutations cause derepression of the D4Z4 macrosatellite repeat-embedded DUX4 gene in skeletal muscle of facioscapulohumeral muscular dystrophy (FSHD) patients Little is known about the regulation and post-translational modification of SMCHD1. Here we report the SUMOylation dynamics of SMCHD1 and its impact on autosomal single copy and repetitive loci, and the inactive X chromosome (Xi). We identify that SMCHD1 is SUMOylated primarily at lysine 1374, uncover factors regulating SMCHD1 SUMOylation, and demonstrate that SMCHD1 interacts with chromatin repressors TRIM28, HNRNPK and SETDB1 in a SUMO-dependent manner. We find that SUMOylation impacts Xi engagement of SMCHD1, maintenance of a repressive D4Z4 chromatin structure preventing DUX4 expression, and regulation of LRIF1 promoter activity. The rapid, SUMO-dependent upregulation of DUX4 could explain the bursts of DUX4 expression typical for FSHD muscle.

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