Abstract
Ubiquitination of histones plays a critical role in the regulation of several processes within the nucleus, including maintenance of genome stability and transcriptional regulation. The only known ubiquitination site on histones is represented by a conserved Lys residue located at the C terminus of the protein. Here, we describe a novel ubiquitin mark at the N-terminal tail of histone H2As consisting of two Lys residues at positions 13 and 15 (K13/K15). This "bidentate" site is a target of the DNA damage response (DDR) ubiquitin ligases RNF8 and RNF168. Histone mutants lacking the K13/K15 site impair RNF168- and DNA damage-dependent ubiquitination. Conversely, inactivation of the canonical C-terminal site prevents the constitutive monoubiquitination of histone H2As but does not abolish the ubiquitination induced by RNF168. A ubiquitination-defective mutant is obtained by inactivating both the N- and the C-terminal sites, suggesting that these are unique, non-redundant acceptors of ubiquitination on histone H2As. This unprecedented result implies that RNF168 generates a qualitatively different Ub mark on chromatin.
MeSH Terms
Amino Acid Sequence
Chromatin Assembly and Disassembly
DNA Repair
DNA-Binding Proteins/metabolism
HEK293 Cells
Histones/chemistry,genetics,metabolism
Humans
Molecular Sequence Data
Mutation
Protein Structure, Tertiary
Ubiquitin-Protein Ligases/metabolism
Ubiquitination
Chemicals
DNA-Binding Proteins
H2AX protein, human
Histones
RNF8 protein, human
RNF168 protein, human
Ubiquitin-Protein Ligases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Gatti Marco
Department of Pharmaceutical Sciences, University of Piemonte Orientale "A. Avogadro", Novara, Italy.
Pinato Sabrina
Maspero Elena
Soffientini Paolo
Polo Simona
Penengo Lorenza
References (22)
22 references, click to expand
-
Nonproteolytic functions of ubiquitin in cell signaling.
Mol Cell. 2009 Feb 13;33(3):275-86
PMID: 19217402
-
The ubiquitin- and SUMO-dependent signaling response to DNA double-strand breaks.
FEBS Lett. 2011 Sep 16;585(18):2914-9
PMID: 21664912
-
Regulation of chromatin by histone modifications.
Cell Res. 2011 Mar;21(3):381-95
PMID: 21321607
-
Protocol for micro-purification, enrichment, pre-fractionation and storage of peptides for proteomics using StageTips.
Nat Protoc. 2007;2(8):1896-906
PMID: 17703201
-
RNF8 ubiquitylates histones at DNA double-strand breaks and promotes assembly of repair proteins.
Cell. 2007 Nov 30;131(5):887-900
PMID: 18001824
-
Crystal structure of the ubiquitin binding domains of rabex-5 reveals two modes of interaction with ubiquitin.
Cell. 2006 Mar 24;124(6):1183-95
PMID: 16499958
-
RNF168 binds and amplifies ubiquitin conjugates on damaged chromosomes to allow accumulation of repair proteins.
Cell. 2009 Feb 6;136(3):435-46
PMID: 19203579
-
The ubiquitination code: a signalling problem.
Cell Div. 2007 Mar 13;2:11
PMID: 17355622
-
The RIDDLE syndrome protein mediates a ubiquitin-dependent signaling cascade at sites of DNA damage.
Cell. 2009 Feb 6;136(3):420-34
PMID: 19203578
-
BBAP monoubiquitylates histone H4 at lysine 91 and selectively modulates the DNA damage response.
Mol Cell. 2009 Oct 9;36(1):110-20
PMID: 19818714
-
Linkage-specific avidity defines the lysine 63-linked polyubiquitin-binding preference of rap80.
Mol Cell. 2009 Mar 27;33(6):775-83
PMID: 19328070
-
Abraxas and RAP80 form a BRCA1 protein complex required for the DNA damage response.
Science. 2007 May 25;316(5828):1194-8
PMID: 17525340
-
UMI, a novel RNF168 ubiquitin binding domain involved in the DNA damage signaling pathway.
Mol Cell Biol. 2011 Jan;31(1):118-26
PMID: 21041483
-
Histones: annotating chromatin.
Annu Rev Genet. 2009;43:559-99
PMID: 19886812
-
RNF168, a new RING finger, MIU-containing protein that modifies chromatin by ubiquitination of histones H2A and H2AX.
BMC Mol Biol. 2009 Jun 05;10:55
PMID: 19500350
-
Structural basis for the methylation state-specific recognition of histone H4-K20 by 53BP1 and Crb2 in DNA repair.
Cell. 2006 Dec 29;127(7):1361-73
PMID: 17190600
-
Histone ubiquitination: triggering gene activity.
Mol Cell. 2008 Mar 28;29(6):653-63
PMID: 18374642
-
RNF8 transduces the DNA-damage signal via histone ubiquitylation and checkpoint protein assembly.
Cell. 2007 Nov 30;131(5):901-14
PMID: 18001825
-
Structural basis for specific recognition of Lys 63-linked polyubiquitin chains by tandem UIMs of RAP80.
EMBO J. 2009 Aug 19;28(16):2461-8
PMID: 19536136
-
Orchestration of the DNA-damage response by the RNF8 ubiquitin ligase.
Science. 2007 Dec 7;318(5856):1637-40
PMID: 18006705
-
Methylated lysine 79 of histone H3 targets 53BP1 to DNA double-strand breaks.
Nature. 2004 Nov 18;432(7015):406-11
PMID: 15525939
-
Chromatin dynamics and the repair of DNA double strand breaks.
Cell Cycle. 2011 Jan 15;10(2):261-7
PMID: 21212734