USP15 Deubiquitinase Safeguards Hematopoiesis and Genome Integrity in Hematopoietic Stem Cells and Leukemia Cells

Altering ubiquitination by disruption of deubiquitinating enzymes (DUBs) affects hematopoietic stem cell (HSC) maintenance. However, comprehensive knowledge of DUB function during hematopoiesis in vivo is lacking. Here, we systematically inactivate DUBs in mouse hematopoietic progenitors using in vi...

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Vydané v:Cell reports (Cambridge) Ročník 33; číslo 13; s. 108533
Hlavní autori: van den Berk, Paul, Lancini, Cesare, Company, Carlos, Serresi, Michela, Sanchez-Bailon, Maria Pilar, Hulsman, Danielle, Pritchard, Colin, Song, Ji-Ying, Schmitt, Matthias Jürgen, Tanger, Ellen, Popp, Oliver, Mertins, Philipp, Huijbers, Ivo J., Jacobs, Heinz, van Lohuizen, Maarten, Gargiulo, Gaetano, Citterio, Elisabetta
Médium: Journal Article
Jazyk:English
Vydavateľské údaje: United States Elsevier Inc 29.12.2020
Cell Press
Predmet:
deubiquitinase
deubiquitinating enzymes
DNA damage response
FUS
fused in sarcoma
genome integrity
hematopoietic stem cell
HSC
in vivo shRNA screen
leukemia
RNAi
USP15
leukemia
USP15
RNAi
DNA damage response
FUS
deubiquitinating enzymes
in vivo shRNA screen
hematopoietic stem cell
HSC
genome integrity
deubiquitinase
fused in sarcoma
ISSN:2211-1247, 2211-1247
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Abstract Altering ubiquitination by disruption of deubiquitinating enzymes (DUBs) affects hematopoietic stem cell (HSC) maintenance. However, comprehensive knowledge of DUB function during hematopoiesis in vivo is lacking. Here, we systematically inactivate DUBs in mouse hematopoietic progenitors using in vivo small hairpin RNA (shRNA) screens. We find that multiple DUBs may be individually required for hematopoiesis and identify ubiquitin-specific protease 15 (USP15) as essential for HSC maintenance in vitro and in transplantations and Usp15 knockout (KO) mice in vivo. USP15 is highly expressed in human hematopoietic tissues and leukemias. USP15 depletion in murine progenitors and leukemia cells impairs in vitro expansion and increases genotoxic stress. In leukemia cells, USP15 interacts with and stabilizes FUS (fused in sarcoma), a known DNA repair factor, directly linking USP15 to the DNA damage response (DDR). Our study underscores the importance of DUBs in preserving normal hematopoiesis and uncovers USP15 as a critical DUB in safeguarding genome integrity in HSCs and leukemia cells. [Display omitted] •In vivo shRNAs screens for deubiquitinases identify regulators of murine hematopoiesis•Usp15 deletion compromises HSC maintenance and reconstitution potential in vivo•USP15 loss affects genome integrity and growth of mHSPCs and human leukemia cells•In human leukemia cells, USP15 stabilizes its interactor, FUS, a DNA repair factor Van den Berk et al. use unbiased in vivo RNAi screens targeting deubiquitinases in mouse hematopoietic stem and progenitor cells. This study underscores the importance of deubiquitinases in hematopoietic stem cell function and reveals the role of USP15 in preserving genome integrity in normal and transformed hematopoietic cells.
AbstractList Altering ubiquitination by disruption of deubiquitinating enzymes (DUBs) affects hematopoietic stem cell (HSC) maintenance. However, comprehensive knowledge of DUB function during hematopoiesis in vivo is lacking. Here, we systematically inactivate DUBs in mouse hematopoietic progenitors using in vivo small hairpin RNA (shRNA) screens. We find that multiple DUBs may be individually required for hematopoiesis and identify ubiquitin-specific protease 15 (USP15) as essential for HSC maintenance in vitro and in transplantations and Usp15 knockout (KO) mice in vivo. USP15 is highly expressed in human hematopoietic tissues and leukemias. USP15 depletion in murine progenitors and leukemia cells impairs in vitro expansion and increases genotoxic stress. In leukemia cells, USP15 interacts with and stabilizes FUS (fused in sarcoma), a known DNA repair factor, directly linking USP15 to the DNA damage response (DDR). Our study underscores the importance of DUBs in preserving normal hematopoiesis and uncovers USP15 as a critical DUB in safeguarding genome integrity in HSCs and leukemia cells.
Altering ubiquitination by disruption of deubiquitinating enzymes (DUBs) affects hematopoietic stem cell (HSC) maintenance. However, comprehensive knowledge of DUB function during hematopoiesis in vivo is lacking. Here, we systematically inactivate DUBs in mouse hematopoietic progenitors using in vivo small hairpin RNA (shRNA) screens. We find that multiple DUBs may be individually required for hematopoiesis and identify ubiquitin-specific protease 15 (USP15) as essential for HSC maintenance in vitro and in transplantations and Usp15 knockout (KO) mice in vivo. USP15 is highly expressed in human hematopoietic tissues and leukemias. USP15 depletion in murine progenitors and leukemia cells impairs in vitro expansion and increases genotoxic stress. In leukemia cells, USP15 interacts with and stabilizes FUS (fused in sarcoma), a known DNA repair factor, directly linking USP15 to the DNA damage response (DDR). Our study underscores the importance of DUBs in preserving normal hematopoiesis and uncovers USP15 as a critical DUB in safeguarding genome integrity in HSCs and leukemia cells.Altering ubiquitination by disruption of deubiquitinating enzymes (DUBs) affects hematopoietic stem cell (HSC) maintenance. However, comprehensive knowledge of DUB function during hematopoiesis in vivo is lacking. Here, we systematically inactivate DUBs in mouse hematopoietic progenitors using in vivo small hairpin RNA (shRNA) screens. We find that multiple DUBs may be individually required for hematopoiesis and identify ubiquitin-specific protease 15 (USP15) as essential for HSC maintenance in vitro and in transplantations and Usp15 knockout (KO) mice in vivo. USP15 is highly expressed in human hematopoietic tissues and leukemias. USP15 depletion in murine progenitors and leukemia cells impairs in vitro expansion and increases genotoxic stress. In leukemia cells, USP15 interacts with and stabilizes FUS (fused in sarcoma), a known DNA repair factor, directly linking USP15 to the DNA damage response (DDR). Our study underscores the importance of DUBs in preserving normal hematopoiesis and uncovers USP15 as a critical DUB in safeguarding genome integrity in HSCs and leukemia cells.
Altering ubiquitination by disruption of deubiquitinating enzymes (DUBs) affects hematopoietic stem cell (HSC) maintenance. However, comprehensive knowledge of DUB function during hematopoiesis in vivo is lacking. Here, we systematically inactivate DUBs in mouse hematopoietic progenitors using in vivo small hairpin RNA (shRNA) screens. We find that multiple DUBs may be individually required for hematopoiesis and identify ubiquitin-specific protease 15 (USP15) as essential for HSC maintenance in vitro and in transplantations and Usp15 knockout (KO) mice in vivo. USP15 is highly expressed in human hematopoietic tissues and leukemias. USP15 depletion in murine progenitors and leukemia cells impairs in vitro expansion and increases genotoxic stress. In leukemia cells, USP15 interacts with and stabilizes FUS (fused in sarcoma), a known DNA repair factor, directly linking USP15 to the DNA damage response (DDR). Our study underscores the importance of DUBs in preserving normal hematopoiesis and uncovers USP15 as a critical DUB in safeguarding genome integrity in HSCs and leukemia cells. [Display omitted] •In vivo shRNAs screens for deubiquitinases identify regulators of murine hematopoiesis•Usp15 deletion compromises HSC maintenance and reconstitution potential in vivo•USP15 loss affects genome integrity and growth of mHSPCs and human leukemia cells•In human leukemia cells, USP15 stabilizes its interactor, FUS, a DNA repair factor Van den Berk et al. use unbiased in vivo RNAi screens targeting deubiquitinases in mouse hematopoietic stem and progenitor cells. This study underscores the importance of deubiquitinases in hematopoietic stem cell function and reveals the role of USP15 in preserving genome integrity in normal and transformed hematopoietic cells.
Altering ubiquitination by disruption of deubiquitinating enzymes (DUBs) affects hematopoietic stem cell (HSC) maintenance. However, comprehensive knowledge of DUB function during hematopoiesis in vivo is lacking. Here, we systematically inactivate DUBs in mouse hematopoietic progenitors using in vivo small hairpin RNA (shRNA) screens. We find that multiple DUBs may be individually required for hematopoiesis and identify ubiquitin-specific protease 15 (USP15) as essential for HSC maintenance in vitro and in transplantations and Usp15 knockout (KO) mice in vivo. USP15 is highly expressed in human hematopoietic tissues and leukemias. USP15 depletion in murine progenitors and leukemia cells impairs in vitro expansion and increases genotoxic stress. In leukemia cells, USP15 interacts with and stabilizes FUS (fused in sarcoma), a known DNA repair factor, directly linking USP15 to the DNA damage response (DDR). Our study underscores the importance of DUBs in preserving normal hematopoiesis and uncovers USP15 as a critical DUB in safeguarding genome integrity in HSCs and leukemia cells. • In vivo shRNAs screens for deubiquitinases identify regulators of murine hematopoiesis • Usp15 deletion compromises HSC maintenance and reconstitution potential in vivo • USP15 loss affects genome integrity and growth of mHSPCs and human leukemia cells • In human leukemia cells, USP15 stabilizes its interactor, FUS, a DNA repair factor Van den Berk et al. use unbiased in vivo RNAi screens targeting deubiquitinases in mouse hematopoietic stem and progenitor cells. This study underscores the importance of deubiquitinases in hematopoietic stem cell function and reveals the role of USP15 in preserving genome integrity in normal and transformed hematopoietic cells.
ArticleNumber 108533
Author Sanchez-Bailon, Maria Pilar
van Lohuizen, Maarten
Pritchard, Colin
Gargiulo, Gaetano
Schmitt, Matthias Jürgen
Popp, Oliver
Mertins, Philipp
Company, Carlos
van den Berk, Paul
Hulsman, Danielle
Jacobs, Heinz
Tanger, Ellen
Song, Ji-Ying
Huijbers, Ivo J.
Citterio, Elisabetta
Lancini, Cesare
Serresi, Michela
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  surname: Company
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  organization: Max-Delbrück-Center for Molecular Medicine (MDC), Robert-Rössle-Str. 10, 13092 Berlin, Germany
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  givenname: Ji-Ying
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  organization: Division of Experimental Animal Pathology, the Netherlands Cancer Institute, Plesmanlaan 121, Amsterdam 1066 CX, the Netherlands
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  organization: Division of Molecular Genetics, the Netherlands Cancer Institute, Plesmanlaan 121, Amsterdam 1066 CX, the Netherlands
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  surname: Popp
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  organization: Proteomics Platform, Max Delbrück Center for Molecular Medicine in the Helmholtz Association and Berlin Institute of Health, Robert Rössle Strasse 10, 13125 Berlin, Germany
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  surname: Huijbers
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  surname: Gargiulo
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  orcidid: 0000-0003-2347-3495
  surname: Citterio
  fullname: Citterio, Elisabetta
  email: elisabetta.citterio@gmail.com
  organization: Division of Molecular Genetics, the Netherlands Cancer Institute, Plesmanlaan 121, Amsterdam 1066 CX, the Netherlands
BackLink https://www.ncbi.nlm.nih.gov/pubmed/33378683$$D View this record in MEDLINE/PubMed
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Issue 13
Keywords leukemia
USP15
RNAi
DNA damage response
FUS
deubiquitinating enzymes
in vivo shRNA screen
hematopoietic stem cell
HSC
genome integrity
deubiquitinase
fused in sarcoma
Language English
License This is an open access article under the CC BY license.
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Snippet Altering ubiquitination by disruption of deubiquitinating enzymes (DUBs) affects hematopoietic stem cell (HSC) maintenance. However, comprehensive knowledge of...
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SubjectTerms deubiquitinase
deubiquitinating enzymes
DNA damage response
FUS
fused in sarcoma
genome integrity
hematopoietic stem cell
HSC
in vivo shRNA screen
leukemia
RNAi
USP15
Title USP15 Deubiquitinase Safeguards Hematopoiesis and Genome Integrity in Hematopoietic Stem Cells and Leukemia Cells
URI https://dx.doi.org/10.1016/j.celrep.2020.108533
https://www.ncbi.nlm.nih.gov/pubmed/33378683
https://www.proquest.com/docview/2474498312
https://pubmed.ncbi.nlm.nih.gov/PMC7788286
Volume 33
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