Precise Gene Editing Preserves Hematopoietic Stem Cell Function following Transient p53-Mediated DNA Damage Response.

DNA damage response DNA double strand breaks adeno-associated vector genome editing hematopoietic stem and progenitor cells p53 pathway programmable nucleases

Journal

Cell stem cell
ISSN: 1875-9777
Titre abrégé: Cell Stem Cell
Pays: United States
ID NLM: 101311472

Informations de publication

Date de publication:
04 04 2019
Historique:
received: 08 08 2018
revised: 21 12 2018
accepted: 26 02 2019
pubmed: 25 3 2019
medline: 19 5 2020
entrez: 26 3 2019
Statut: ppublish

Résumé

Precise gene editing in hematopoietic stem and progenitor cells (HSPCs) holds promise for treating genetic diseases. However, responses triggered by programmable nucleases in HSPCs are poorly characterized and may negatively impact HSPC engraftment and long-term repopulation capacity. Here, we induced either one or several DNA double-stranded breaks (DSBs) with optimized zinc-finger and CRISPR/Cas9 nucleases and monitored DNA damage response (DDR) foci induction, cell-cycle progression, and transcriptional responses in HSPC subpopulations, with up to single-cell resolution. p53-mediated DDR pathway activation was the predominant response to even single-nuclease-induced DSBs across all HSPC subtypes analyzed. Excess DSB load and/or adeno-associated virus (AAV)-mediated delivery of DNA repair templates induced cumulative p53 pathway activation, constraining proliferation, yield, and engraftment of edited HSPCs. However, functional impairment was reversible when DDR burden was low and could be overcome by transient p53 inhibition. These findings provide molecular and functional evidence for feasible and seamless gene editing in HSPCs.

Identifiants

pubmed: 30905619
pii: S1934-5909(19)30071-2
doi: 10.1016/j.stem.2019.02.019
pmc: PMC6458988
pii:
doi:

Substances chimiques

Tumor Suppressor Protein p53 0

Types de publication

Journal Article Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

551-565.e8

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2019 The Authors. Published by Elsevier Inc. All rights reserved.

Références

Nature. 2006 Nov 30;444(7119):638-42
pubmed: 17136094
Nat Biotechnol. 2015 Feb;33(2):187-197
pubmed: 25513782
Mol Cancer Ther. 2011 Jun;10(6):1046-58
pubmed: 21518729
Nat Biotechnol. 2015 Dec;33(12):1256-1263
pubmed: 26551060
Nat Biotechnol. 2013 Sep;31(9):827-32
pubmed: 23873081
Nat Rev Genet. 2016 May;17(5):300-12
pubmed: 27087594
Nucleic Acids Res. 2011 Nov;39(21):e142
pubmed: 21890902
Nat Methods. 2012 Mar 04;9(4):357-9
pubmed: 22388286
Cell Stem Cell. 2010 Aug 6;7(2):186-97
pubmed: 20619763
Nat Biotechnol. 2015 Sep;33(9):985-989
pubmed: 26121415
J Vis Exp. 2013 Feb 03;(72):e50087
pubmed: 23407477
BMC Genomics. 2017 May 15;18(1):379
pubmed: 28506212
EMBO J. 2010 Apr 21;29(8):1446-57
pubmed: 20360682
Nature. 2014 Aug 14;512(7513):198-202
pubmed: 25079315
Blood. 2017 Jun 22;129(25):3344-3351
pubmed: 28408459
EMBO Mol Med. 2017 Sep;9(9):1198-1211
pubmed: 28667090
Nat Rev Genet. 2014 May;15(5):321-34
pubmed: 24690881
N Engl J Med. 2006 Apr 27;354(17):1813-26
pubmed: 16641398
Nat Med. 2018 Jul;24(7):939-946
pubmed: 29892062
Nature. 2016 Nov 17;539(7629):384-389
pubmed: 27820943
Genes Dev. 2011 Mar 1;25(5):409-33
pubmed: 21363960
Cell Stem Cell. 2013 Oct 3;13(4):459-70
pubmed: 24094326
Nat Cell Biol. 2017 Apr;19(4):271-281
pubmed: 28319093
Genome Biol. 2003;4(10):R69
pubmed: 14519204
Cell Mol Immunol. 2015 Mar;12(2):139-53
pubmed: 25418469
J Virol. 2007 Dec;81(23):12936-45
pubmed: 17898048
Nucleic Acids Res. 2018 Jun 1;46(10):e58
pubmed: 29538768
Cell Rep. 2013 Feb 21;3(2):359-70
pubmed: 23416051
Nat Commun. 2017 May 31;8:15656
pubmed: 28561034
Nat Biotechnol. 2016 Apr;34(4):424-9
pubmed: 26950749
Nat Biotechnol. 2018 Jun;36(5):411-420
pubmed: 29608179
Nature. 2014 Jun 12;510(7504):235-240
pubmed: 24870228
Nat Commun. 2017 Jan 09;8:13905
pubmed: 28067217
Trends Mol Med. 2017 Dec;23(12):1067-1070
pubmed: 29133134
Curr Opin Hematol. 2017 Nov;24(6):481-488
pubmed: 28806273
Nat Biotechnol. 2016 Mar;34(3):339-44
pubmed: 26789497
Oncogene. 2017 Jul 13;36(28):3943-3956
pubmed: 28288132
Nature. 2018 Jan 11;553(7687):171-177
pubmed: 29323295
Sci Rep. 2018 Apr 17;8(1):6071
pubmed: 29666389
Nat Med. 2017 Apr 3;23(4):415-423
pubmed: 28388605
Nat Med. 2018 Jul;24(7):927-930
pubmed: 29892067
Sci Transl Med. 2017 Oct 11;9(411):
pubmed: 29021165
EMBO Mol Med. 2019 Mar;11(3):
pubmed: 30670463
Mol Cell. 2010 Oct 22;40(2):179-204
pubmed: 20965415
Cell Stem Cell. 2012 Feb 3;10(2):120-36
pubmed: 22305562
Nat Methods. 2011 Aug 21;8(10):861-9
pubmed: 21857672
Science. 2014 Nov 28;346(6213):1258096
pubmed: 25430774
Nat Methods. 2017 Sep;14(9):891-896
pubmed: 28737741
Genome Biol. 2015 Dec 10;16:278
pubmed: 26653891
Cell. 2006 Dec 29;127(7):1323-34
pubmed: 17182091
Genome Med. 2018 Aug 17;10(1):66
pubmed: 30119695
Cell Stem Cell. 2010 Aug 6;7(2):174-85
pubmed: 20619762
Bioinformatics. 2017 Sep 15;33(18):2941-2942
pubmed: 28541403
Nucleic Acids Res. 2014 Jul;42(13):8416-32
pubmed: 24957606
Blood. 2016 Aug 25;128(8):e20-31
pubmed: 27365425
Cell Stem Cell. 2014 Jul 3;15(1):37-50
pubmed: 24813857

Auteurs

Giulia Schiroli (G)

San Raffaele Telethon Institute for Gene Therapy (SR-Tiget), IRCCS San Raffaele Scientific Institute, 20132 Milan, Italy.

Anastasia Conti (A)

San Raffaele Telethon Institute for Gene Therapy (SR-Tiget), IRCCS San Raffaele Scientific Institute, 20132 Milan, Italy.

Samuele Ferrari (S)

San Raffaele Telethon Institute for Gene Therapy (SR-Tiget), IRCCS San Raffaele Scientific Institute, 20132 Milan, Italy; Vita-Salute San Raffaele University, 20132 Milan, Italy.

Lucrezia Della Volpe (L)

San Raffaele Telethon Institute for Gene Therapy (SR-Tiget), IRCCS San Raffaele Scientific Institute, 20132 Milan, Italy; Vita-Salute San Raffaele University, 20132 Milan, Italy.

Aurelien Jacob (A)

San Raffaele Telethon Institute for Gene Therapy (SR-Tiget), IRCCS San Raffaele Scientific Institute, 20132 Milan, Italy; Milano-Bicocca University, 20126 Milan, Italy.

Luisa Albano (L)

San Raffaele Telethon Institute for Gene Therapy (SR-Tiget), IRCCS San Raffaele Scientific Institute, 20132 Milan, Italy.

Stefano Beretta (S)

Milano-Bicocca University, 20126 Milan, Italy; Institute for Biomedical Technologies, National Research Council, 20090 Segrate, Italy.

Andrea Calabria (A)

San Raffaele Telethon Institute for Gene Therapy (SR-Tiget), IRCCS San Raffaele Scientific Institute, 20132 Milan, Italy.

Valentina Vavassori (V)

San Raffaele Telethon Institute for Gene Therapy (SR-Tiget), IRCCS San Raffaele Scientific Institute, 20132 Milan, Italy; Vita-Salute San Raffaele University, 20132 Milan, Italy.

Patrizia Gasparini (P)

Tumor Genomics Unit, Department of Experimental Oncology, Fondazione IRCCS Istituto Nazionale dei Tumori di Milano, 20133 Milan, Italy.

Eralda Salataj (E)

Inserm U1016, Institut Cochin, 75014 Paris, France; CNRS UMR8104, Paris, France; Université Paris Descartes, Sorbonne Paris Cité, France.

Delphine Ndiaye-Lobry (D)

Inserm U1016, Institut Cochin, 75014 Paris, France; CNRS UMR8104, Paris, France; Université Paris Descartes, Sorbonne Paris Cité, France.

Chiara Brombin (C)

CUSSB-University Center for Statistics in the Biomedical Sciences, Vita-Salute San Raffaele University, 20132 Milan, Italy.

Julie Chaumeil (J)

Inserm U1016, Institut Cochin, 75014 Paris, France; CNRS UMR8104, Paris, France; Université Paris Descartes, Sorbonne Paris Cité, France.

Eugenio Montini (E)

San Raffaele Telethon Institute for Gene Therapy (SR-Tiget), IRCCS San Raffaele Scientific Institute, 20132 Milan, Italy.

Ivan Merelli (I)

Institute for Biomedical Technologies, National Research Council, 20090 Segrate, Italy.

Pietro Genovese (P)

San Raffaele Telethon Institute for Gene Therapy (SR-Tiget), IRCCS San Raffaele Scientific Institute, 20132 Milan, Italy. Electronic address: genovese.pietro@hsr.it.

Luigi Naldini (L)

San Raffaele Telethon Institute for Gene Therapy (SR-Tiget), IRCCS San Raffaele Scientific Institute, 20132 Milan, Italy; Vita-Salute San Raffaele University, 20132 Milan, Italy. Electronic address: naldini.luigi@hsr.it.

Raffaella Di Micco (R)

San Raffaele Telethon Institute for Gene Therapy (SR-Tiget), IRCCS San Raffaele Scientific Institute, 20132 Milan, Italy. Electronic address: dimicco.raffaella@hsr.it.

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