TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chromosomes

Histone ubiquitylation is a prominent response to DNA double-strand breaks (DSBs), but how these modifications are confined to DNA lesions is not understood. Here, we show that TRIP12 and UBR5, two HECT domain ubiquitin E3 ligases, control accumulation of RNF168, a rate-limiting component of a pathw...

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Published in:	Cell Vol. 150; no. 4; p. 697
Main Authors:	Gudjonsson, Thorkell, Altmeyer, Matthias, Savic, Velibor, Toledo, Luis, Dinant, Christoffel, Grøfte, Merete, Bartkova, Jirina, Poulsen, Maria, Oka, Yasuyoshi, Bekker-Jensen, Simon, Mailand, Niels, Neumann, Beate, Heriche, Jean-Karim, Shearer, Robert, Saunders, Darren, Bartek, Jiri, Lukas, Jiri, Lukas, Claudia
Format:	Journal Article
Language:	English
Published:	United States 17.08.2012
Subjects:	Alphapapillomavirus Carrier Proteins - metabolism Cell Line Cell Line, Tumor Chromatin - metabolism DNA Breaks, Double-Stranded DNA Repair Gene Silencing Humans Intracellular Signaling Peptides and Proteins - metabolism Neoplasms - metabolism Neoplasms - pathology Neoplasms - virology Papillomavirus Infections - metabolism Papillomavirus Infections - pathology Transcription, Genetic Tumor Suppressor p53-Binding Protein 1 Ubiquitin-Protein Ligases - metabolism Ubiquitination
ISSN:	1097-4172, 1097-4172
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Abstract	Histone ubiquitylation is a prominent response to DNA double-strand breaks (DSBs), but how these modifications are confined to DNA lesions is not understood. Here, we show that TRIP12 and UBR5, two HECT domain ubiquitin E3 ligases, control accumulation of RNF168, a rate-limiting component of a pathway that ubiquitylates histones after DNA breakage. We find that RNF168 can be saturated by increasing amounts of DSBs. Depletion of TRIP12 and UBR5 allows accumulation of RNF168 to supraphysiological levels, followed by massive spreading of ubiquitin conjugates and hyperaccumulation of ubiquitin-regulated genome caretakers such as 53BP1 and BRCA1. Thus, regulatory and proteolytic ubiquitylations are wired in a self-limiting circuit that promotes histone ubiquitylation near the DNA lesions but at the same time counteracts its excessive spreading to undamaged chromosomes. We provide evidence that this mechanism is vital for the homeostasis of ubiquitin-controlled events after DNA breakage and can be subverted during tumorigenesis.
AbstractList	Histone ubiquitylation is a prominent response to DNA double-strand breaks (DSBs), but how these modifications are confined to DNA lesions is not understood. Here, we show that TRIP12 and UBR5, two HECT domain ubiquitin E3 ligases, control accumulation of RNF168, a rate-limiting component of a pathway that ubiquitylates histones after DNA breakage. We find that RNF168 can be saturated by increasing amounts of DSBs. Depletion of TRIP12 and UBR5 allows accumulation of RNF168 to supraphysiological levels, followed by massive spreading of ubiquitin conjugates and hyperaccumulation of ubiquitin-regulated genome caretakers such as 53BP1 and BRCA1. Thus, regulatory and proteolytic ubiquitylations are wired in a self-limiting circuit that promotes histone ubiquitylation near the DNA lesions but at the same time counteracts its excessive spreading to undamaged chromosomes. We provide evidence that this mechanism is vital for the homeostasis of ubiquitin-controlled events after DNA breakage and can be subverted during tumorigenesis. Histone ubiquitylation is a prominent response to DNA double-strand breaks (DSBs), but how these modifications are confined to DNA lesions is not understood. Here, we show that TRIP12 and UBR5, two HECT domain ubiquitin E3 ligases, control accumulation of RNF168, a rate-limiting component of a pathway that ubiquitylates histones after DNA breakage. We find that RNF168 can be saturated by increasing amounts of DSBs. Depletion of TRIP12 and UBR5 allows accumulation of RNF168 to supraphysiological levels, followed by massive spreading of ubiquitin conjugates and hyperaccumulation of ubiquitin-regulated genome caretakers such as 53BP1 and BRCA1. Thus, regulatory and proteolytic ubiquitylations are wired in a self-limiting circuit that promotes histone ubiquitylation near the DNA lesions but at the same time counteracts its excessive spreading to undamaged chromosomes. We provide evidence that this mechanism is vital for the homeostasis of ubiquitin-controlled events after DNA breakage and can be subverted during tumorigenesis.Histone ubiquitylation is a prominent response to DNA double-strand breaks (DSBs), but how these modifications are confined to DNA lesions is not understood. Here, we show that TRIP12 and UBR5, two HECT domain ubiquitin E3 ligases, control accumulation of RNF168, a rate-limiting component of a pathway that ubiquitylates histones after DNA breakage. We find that RNF168 can be saturated by increasing amounts of DSBs. Depletion of TRIP12 and UBR5 allows accumulation of RNF168 to supraphysiological levels, followed by massive spreading of ubiquitin conjugates and hyperaccumulation of ubiquitin-regulated genome caretakers such as 53BP1 and BRCA1. Thus, regulatory and proteolytic ubiquitylations are wired in a self-limiting circuit that promotes histone ubiquitylation near the DNA lesions but at the same time counteracts its excessive spreading to undamaged chromosomes. We provide evidence that this mechanism is vital for the homeostasis of ubiquitin-controlled events after DNA breakage and can be subverted during tumorigenesis.
Author	Savic, Velibor Grøfte, Merete Bartek, Jiri Gudjonsson, Thorkell Dinant, Christoffel Bekker-Jensen, Simon Toledo, Luis Heriche, Jean-Karim Mailand, Niels Lukas, Jiri Oka, Yasuyoshi Lukas, Claudia Neumann, Beate Shearer, Robert Saunders, Darren Bartkova, Jirina Poulsen, Maria Altmeyer, Matthias
Author_xml	– sequence: 1 givenname: Thorkell surname: Gudjonsson fullname: Gudjonsson, Thorkell organization: Chromosome Biology Unit, Danish Cancer Society Research Center and Center for Genotoxic Stress Research, Strandboulevarden 49, DK-2100 Copenhagen, Denmark – sequence: 2 givenname: Matthias surname: Altmeyer fullname: Altmeyer, Matthias – sequence: 3 givenname: Velibor surname: Savic fullname: Savic, Velibor – sequence: 4 givenname: Luis surname: Toledo fullname: Toledo, Luis – sequence: 5 givenname: Christoffel surname: Dinant fullname: Dinant, Christoffel – sequence: 6 givenname: Merete surname: Grøfte fullname: Grøfte, Merete – sequence: 7 givenname: Jirina surname: Bartkova fullname: Bartkova, Jirina – sequence: 8 givenname: Maria surname: Poulsen fullname: Poulsen, Maria – sequence: 9 givenname: Yasuyoshi surname: Oka fullname: Oka, Yasuyoshi – sequence: 10 givenname: Simon surname: Bekker-Jensen fullname: Bekker-Jensen, Simon – sequence: 11 givenname: Niels surname: Mailand fullname: Mailand, Niels – sequence: 12 givenname: Beate surname: Neumann fullname: Neumann, Beate – sequence: 13 givenname: Jean-Karim surname: Heriche fullname: Heriche, Jean-Karim – sequence: 14 givenname: Robert surname: Shearer fullname: Shearer, Robert – sequence: 15 givenname: Darren surname: Saunders fullname: Saunders, Darren – sequence: 16 givenname: Jiri surname: Bartek fullname: Bartek, Jiri – sequence: 17 givenname: Jiri surname: Lukas fullname: Lukas, Jiri – sequence: 18 givenname: Claudia surname: Lukas fullname: Lukas, Claudia
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SubjectTerms	Alphapapillomavirus Carrier Proteins - metabolism Cell Line Cell Line, Tumor Chromatin - metabolism DNA Breaks, Double-Stranded DNA Repair Gene Silencing Humans Intracellular Signaling Peptides and Proteins - metabolism Neoplasms - metabolism Neoplasms - pathology Neoplasms - virology Papillomavirus Infections - metabolism Papillomavirus Infections - pathology Transcription, Genetic Tumor Suppressor p53-Binding Protein 1 Ubiquitin-Protein Ligases - metabolism Ubiquitination
Title	TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chromosomes
URI	https://www.ncbi.nlm.nih.gov/pubmed/22884692 https://www.proquest.com/docview/1034516041
Volume	150
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