Alternative splicing and allosteric regulation modulate the chromatin binding of UHRF1

Tauber, Maria; Kreuz, Sarah; Lemak, Alexander; Mandal, Papita; Yerkesh, Zhadyra; Veluchamy, Alaguraj; Al-Gashgari, Bothayna; Aljahani, Abrar; Cortés-Medina, Lorena V.; Azhibek, Dulat; Fan, Lixin; Ong, Michelle S.; Duan, Shili; Houliston, Scott; Arrowsmith, Cheryl H.; Fischle, Wolfgang

doi:10.1093/nar/gkaa520

Title: Alternative splicing and allosteric regulation modulate the chromatin binding of UHRF1

Journal Article · Wed Jul 01 00:00:00 EDT 2020 · Nucleic Acids Research

DOI:https://doi.org/10.1093/nar/gkaa520· OSTI ID:1635587

Tauber, Maria ^[1]; Kreuz, Sarah ^[2]; Lemak, Alexander ^[3]; Mandal, Papita ^[2]; Yerkesh, Zhadyra ^[2]; Veluchamy, Alaguraj ^[2]; Al-Gashgari, Bothayna ^[2]; Aljahani, Abrar ^[2]; Cortés-Medina, Lorena V. ^[2]; Azhibek, Dulat ^[2]; Fan, Lixin ^[4]; Ong, Michelle S. ^[5]; Duan, Shili ^[3]; Houliston, Scott ^[3]; Arrowsmith, Cheryl H. ^[6];

^[7]

Laboratory of Chromatin Biochemistry, Max Planck Institute for Biophysical Chemistry, 37077 Göttingen, Germany
Biological and Environmental Science and Engineering Division, Laboratory of Chromatin Biochemistry, King Abdullah University of Science and Technology, Thuwal 23955, Saudi Arabia
Princess Margaret Cancer Centre and Department of Medical Biophysics, University of Toronto, Toronto M5G 1L7, Canada
Basic Science Program, Frederick National Laboratory for Cancer Research, SAXS Core Facility of the National Cancer Institute, Frederick, MD 21702, USA
Structural Genomics Consortium, University of Toronto, Toronto M5G 1L7, Canada
Princess Margaret Cancer Centre and Department of Medical Biophysics, University of Toronto, Toronto M5G 1L7, Canada, Structural Genomics Consortium, University of Toronto, Toronto M5G 1L7, Canada
Laboratory of Chromatin Biochemistry, Max Planck Institute for Biophysical Chemistry, 37077 Göttingen, Germany, Biological and Environmental Science and Engineering Division, Laboratory of Chromatin Biochemistry, King Abdullah University of Science and Technology, Thuwal 23955, Saudi Arabia

UHRF1 is an important epigenetic regulator associated with apoptosis and tumour development. It is a multidomain protein that integrates readout of different histone modification states and DNA methylation with enzymatic histone ubiquitylation activity. Emerging evidence indicates that the chromatin-binding and enzymatic modules of UHRF1 do not act in isolation but interplay in a coordinated and regulated manner. Here, we compared two splicing variants (V1, V2) of murine UHRF1 (mUHRF1) with human UHRF1 (hUHRF1). We show that insertion of nine amino acids in a linker region connecting the different TTD and PHD histone modification-binding domains causes distinct H3K9me3-binding behaviour of mUHRF1 V1. Structural analysis suggests that in mUHRF1 V1, in contrast to V2 and hUHRF1, the linker is anchored in a surface groove of the TTD domain, resulting in creation of a coupled TTD-PHD module. This establishes multivalent, synergistic H3-tail binding causing distinct cellular localization and enhanced H3K9me3-nucleosome ubiquitylation activity. In contrast to hUHRF1, H3K9me3-binding of the murine proteins is not allosterically regulated by phosphatidylinositol 5-phosphate that interacts with a separate less-conserved polybasic linker region of the protein. Our results highlight the importance of flexible linkers in regulating multidomain chromatin binding proteins and point to divergent evolution of their regulation.

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Research Organization:: Argonne National Laboratory (ANL), Argonne, IL (United States). Advanced Photon Source (APS)

Sponsoring Organization:: Max Planck Society; German Research Foundation (DFG); King Abdullah University of Science and Technology; Natural Sciences and Engineering Research Council of Canada (NSERC); Abb-Vie; Bayer Pharma AG; Boehringer Ingelheim; Canada Foundation for Innovation (CFI); Eshelman Institute for Innovation; Ontario Genomics Institute; Innovative Medicines Initiative; Janssen; MerckKGaA; MSD; Novartis Pharma AG; Ontario Ministry of Research, Innovation and Science; Pfizer; São Paulo Research Foundation (FAPESP); Takeda; Wellcome; National Cancer Institute (NCI); National Institutes of Health (NIH); USDOE Office of Science (SC)

Grant/Contract Number:: FI1513/2-2; OSR-2015-CRG-2616; AC02-06CH11357

OSTI ID:: 1635587

Alternate ID(s):: OSTI ID: 1648350

Journal Information:: Nucleic Acids Research, Journal Name: Nucleic Acids Research Vol. 48 Journal Issue: 14; ISSN 0305-1048

Publisher:: Oxford University PressCopyright Statement

Country of Publication:: United Kingdom

Language:: English

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