An enhancer-based gene-therapy strategy for spatiotemporal control of cargoes during tissue repair.


Journal

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

Informations de publication

Date de publication:
05 01 2023
Historique:
received: 27 02 2022
revised: 06 10 2022
accepted: 15 11 2022
pmc-release: 05 01 2024
pubmed: 15 12 2022
medline: 11 1 2023
entrez: 14 12 2022
Statut: ppublish

Résumé

The efficacy and safety of gene-therapy strategies for indications like tissue damage hinge on precision; yet, current methods afford little spatial or temporal control of payload delivery. Here, we find that tissue-regeneration enhancer elements (TREEs) isolated from zebrafish can direct targeted, injury-associated gene expression from viral DNA vectors delivered systemically in small and large adult mammalian species. When employed in combination with CRISPR-based epigenome editing tools in mice, zebrafish TREEs stimulated or repressed the expression of endogenous genes after ischemic myocardial infarction. Intravenously delivered recombinant AAV vectors designed with a TREE to direct a constitutively active YAP factor boosted indicators of cardiac regeneration in mice and improved the function of the injured heart. Our findings establish the application of contextual enhancer elements as a potential therapeutic platform for spatiotemporally controlled tissue regeneration in mammals.

Identifiants

pubmed: 36516837
pii: S1934-5909(22)00459-3
doi: 10.1016/j.stem.2022.11.012
pmc: PMC9830588
mid: NIHMS1858391
pii:
doi:

Types de publication

Journal Article Research Support, N.I.H., Extramural Research Support, Non-U.S. Gov't

Langues

eng

Sous-ensembles de citation

IM

Pagination

96-111.e6

Subventions

Organisme : NHLBI NIH HHS
ID : P01 HL146366
Pays : United States
Organisme : NHGRI NIH HHS
ID : UM1 HG012053
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL126524
Pays : United States
Organisme : NIAID NIH HHS
ID : U01 AI146356
Pays : United States
Organisme : NHLBI NIH HHS
ID : R35 HL150713
Pays : United States
Organisme : NIDDK NIH HHS
ID : R01 DK119621
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL151522
Pays : United States
Organisme : NHGRI NIH HHS
ID : RM1 HG011123
Pays : United States
Organisme : NIA NIH HHS
ID : P30 AG028716
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL136182
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL157277
Pays : United States
Organisme : American Heart Association-American Stroke Association
ID : 17SDG33660922
Pays : United States
Organisme : NHLBI NIH HHS
ID : R01 HL164013
Pays : United States
Organisme : NHLBI NIH HHS
ID : U01 HL134764
Pays : United States
Organisme : NIDA NIH HHS
ID : R33 DA041878
Pays : United States
Organisme : NIA NIH HHS
ID : R21 AG067245
Pays : United States
Organisme : American Heart Association-American Stroke Association
ID : 16SDG30020001
Pays : United States
Organisme : NHLBI NIH HHS
ID : F31 HL162460
Pays : United States

Commentaires et corrections

Type : CommentIn

Informations de copyright

Copyright © 2022 Elsevier Inc. All rights reserved.

Déclaration de conflit d'intérêts

Declaration of interests R.Y., J.K., J.A.G., V.C., and K.D.P. are listed as inventors on a patent application filed by Duke University on methods for enhancing tissue regeneration. C.A.G. is an inventor on patents and patent applications related to epigenome editing, is a co-founder/advisor of Tune Therapeutics and Locus Biosciences, and is an advisor to Sarepta Therapeutics.

Références

Nat Genet. 2017 Sep;49(9):1346-1353
pubmed: 28783163
Nat Biotechnol. 2015 May;33(5):510-7
pubmed: 25849900
Methods Mol Biol. 2021;2189:65-69
pubmed: 33180293
Genome Res. 2018 Dec;28(12):1852-1866
pubmed: 30459214
Science. 2021 Sep 24;373(6562):1537-1540
pubmed: 34554778
Mol Ther Methods Clin Dev. 2020 Sep 01;19:120-138
pubmed: 33209958
Nature. 2017 Oct 12;550(7675):260-264
pubmed: 28976966
Dev Cell. 2017 Feb 27;40(4):392-404.e5
pubmed: 28245924
Sci Signal. 2015 May 05;8(375):ra41
pubmed: 25943351
Development. 2013 Dec;140(23):4683-90
pubmed: 24255096
Cell. 2018 Mar 22;173(1):104-116.e12
pubmed: 29502971
J Hand Surg Br. 1995 Feb;20(1):63-71
pubmed: 7759939
Science. 2002 Dec 13;298(5601):2188-90
pubmed: 12481136
Nat Med. 2019 Mar;25(3):427-432
pubmed: 30778238
Proc Natl Acad Sci U S A. 2013 Aug 20;110(34):13839-44
pubmed: 23918388
Bone. 2015 Aug;77:31-41
pubmed: 25886903
Methods Mol Biol. 2021;2158:3-21
pubmed: 32857361
Elife. 2016 Feb 03;5:
pubmed: 26840050
Development. 2011 Aug;138(16):3421-30
pubmed: 21752928
Dev Dyn. 2021 Sep;250(9):1330-1339
pubmed: 33064344
Cardiovasc Res. 2008 Apr 1;78(1):18-25
pubmed: 18079102
Expert Opin Biol Ther. 2022 Sep;22(9):1117-1135
pubmed: 35428407
Circ Res. 2014 Jul 18;115(3):354-63
pubmed: 24833660
Development. 2022 Feb 15;149(4):
pubmed: 35179181
Proc Natl Acad Sci U S A. 2019 Sep 10;116(37):18455-18465
pubmed: 31451669
Development. 2020 Jul 30;147(14):
pubmed: 32665240
Nature. 2020 Nov;587(7835):613-618
pubmed: 33029008
Nat Methods. 2021 Aug;18(8):965-974
pubmed: 34341582
Science. 2011 Apr 22;332(6028):458-61
pubmed: 21512031
Dev Cell. 2017 May 22;41(4):382-391.e5
pubmed: 28535373
Nat Rev Genet. 2020 Apr;21(4):255-272
pubmed: 32042148
Science. 2011 Feb 25;331(6020):1078-80
pubmed: 21350179
Theranostics. 2019 Aug 14;9(21):6099-6111
pubmed: 31534539
Hum Gene Ther. 2011 Sep;22(9):1143-53
pubmed: 21476867
Circulation. 2021 Jun;143(22):2143-2154
pubmed: 33820424
Nat Methods. 2015 Dec;12(12):1143-9
pubmed: 26501517
Nature. 2017 Jul 13;547(7662):179-184
pubmed: 28581497
Nature. 2016 Apr 14;532(7598):201-6
pubmed: 27049946
Am J Physiol Heart Circ Physiol. 2006 Oct;291(4):H1754-60
pubmed: 16699071
Elife. 2020 Jun 03;9:
pubmed: 32490812
Annu Rev Med. 2022 Sep 14;:
pubmed: 36103998
Nat Commun. 2021 Oct 29;12(1):6239
pubmed: 34716331
Science. 2020 Sep 4;369(6508):
pubmed: 32883834
Circulation. 2021 Apr 6;143(14):1343-1358
pubmed: 33478245
Nat Methods. 2012 Jun 28;9(7):676-82
pubmed: 22743772
Gene Ther. 2008 Nov;15(22):1489-99
pubmed: 18563184
Mol Ther. 2006 Jul;14(1):45-53
pubmed: 16713360
Nat Rev Genet. 2020 Sep;21(9):511-525
pubmed: 32504079
Nat Rev Drug Discov. 2021 Mar;20(3):173-174
pubmed: 33495615
Mech Dev. 2003 Sep;120(9):1021-32
pubmed: 14550531
Cell. 2013 Jul 18;154(2):442-51
pubmed: 23849981
Methods Mol Biol. 2016;1382:81-91
pubmed: 26611580
Nature. 2010 Mar 25;464(7288):601-5
pubmed: 20336144
Front Cardiovasc Med. 2022 Feb 10;9:833335
pubmed: 35224061
Science. 2019 Apr 12;364(6436):184-188
pubmed: 30846611
Cell. 2014 Apr 24;157(3):565-79
pubmed: 24766806
Science. 2016 Sep 9;353(6304):1123-9
pubmed: 27609886
Dev Cell. 2019 Mar 25;48(6):765-779.e7
pubmed: 30773489
Am J Physiol. 1996 Nov;271(5 Pt 2):H2183-9
pubmed: 8945939
Nat Cell Biol. 2015 May;17(5):627-38
pubmed: 25848746
J Pediatr Surg. 1974 Dec;9(6):853-58
pubmed: 4473530
Nature. 2012 Dec 20;492(7429):376-81
pubmed: 23222520
J Biol Chem. 2005 Sep 23;280(38):32602-8
pubmed: 16043490
Nat Cell Biol. 2020 Nov;22(11):1346-1356
pubmed: 33046882
J Hand Surg Br. 1993 Apr;18(2):230-3
pubmed: 8501382
Dev Cell. 2011 Mar 15;20(3):397-404
pubmed: 21397850
Dev Cell. 2014 Jul 28;30(2):137-50
pubmed: 25043473
Neurobiol Dis. 2021 Feb;149:105235
pubmed: 33383186
Genome Biol. 2020 Feb 27;21(1):52
pubmed: 32106888
J Orthop Res. 2014 Apr;32(4):581-6
pubmed: 24347536
Science. 2019 Mar 15;363(6432):
pubmed: 30872491
Cell. 2017 Dec 14;171(7):1495-1507.e15
pubmed: 29224783

Auteurs

Ruorong Yan (R)

Duke Regeneration Center, Duke University, Durham, NC, USA; Department of Cell Biology, Duke University Medical School, Durham, NC, USA.

Valentina Cigliola (V)

Duke Regeneration Center, Duke University, Durham, NC, USA; Department of Cell Biology, Duke University Medical School, Durham, NC, USA.

Kelsey A Oonk (KA)

Duke Regeneration Center, Duke University, Durham, NC, USA; Department of Cell Biology, Duke University Medical School, Durham, NC, USA.

Zachary Petrover (Z)

Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, Israel.

Sophia DeLuca (S)

Department of Cell Biology, Duke University Medical School, Durham, NC, USA; Department of Biomedical Engineering, Duke University, Durham, NC, USA.

David W Wolfson (DW)

Duke Regeneration Center, Duke University, Durham, NC, USA; Department of Cell Biology, Duke University Medical School, Durham, NC, USA; Department of Surgery, Duke University School of Medicine, Durham, NC, USA; Center for Advanced Genomic Technologies, Duke University, Durham, NC, USA.

Andrew Vekstein (A)

Department of Surgery, Duke University School of Medicine, Durham, NC, USA.

Michelle A Mendiola (MA)

Department of Surgery, Duke University School of Medicine, Durham, NC, USA.

Garth Devlin (G)

Department of Surgery, Duke University School of Medicine, Durham, NC, USA.

Muath Bishawi (M)

Department of Biomedical Engineering, Duke University, Durham, NC, USA; Department of Surgery, Duke University School of Medicine, Durham, NC, USA.

Matthew P Gemberling (MP)

Department of Biomedical Engineering, Duke University, Durham, NC, USA; Center for Advanced Genomic Technologies, Duke University, Durham, NC, USA.

Tanvi Sinha (T)

Cardiovascular Research Institute, University of California, San Francisco, San Francisco, CA, USA.

Michelle A Sargent (MA)

Department of Pediatrics, Cincinnati Children's Hospital Medical Center, University of Cincinnati, Cincinnati, OH, USA.

Allen J York (AJ)

Department of Pediatrics, Cincinnati Children's Hospital Medical Center, University of Cincinnati, Cincinnati, OH, USA.

Avraham Shakked (A)

Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, Israel.

Paige DeBenedittis (P)

Department of Medicine, Duke University Medical Center, Durham, NC, USA.

David C Wendell (DC)

Duke Cardiovascular Magnetic Resonance Center, Duke University Medical Center, Durham, NC, USA.

Jianhong Ou (J)

Duke Regeneration Center, Duke University, Durham, NC, USA.

Junsu Kang (J)

Department of Cell and Regenerative Biology, School of Medicine and Public Health, University of Wisconsin-Madison, Madison, WI, USA.

Joseph A Goldman (JA)

Department of Biological Chemistry and Pharmacology, Ohio State University, Columbus, OH, USA.

Gurpreet S Baht (GS)

Duke Molecular Physiology Institute, Duke University School of Medicine, Durham, NC, USA; Department of Orthopaedic Surgery, Duke University School of Medicine, Durham, NC, USA.

Ravi Karra (R)

Department of Medicine, Duke University Medical Center, Durham, NC, USA.

Adam R Williams (AR)

Department of Surgery, Duke University School of Medicine, Durham, NC, USA.

Dawn E Bowles (DE)

Department of Surgery, Duke University School of Medicine, Durham, NC, USA.

Aravind Asokan (A)

Duke Regeneration Center, Duke University, Durham, NC, USA; Department of Biomedical Engineering, Duke University, Durham, NC, USA; Department of Surgery, Duke University School of Medicine, Durham, NC, USA; Center for Advanced Genomic Technologies, Duke University, Durham, NC, USA.

Eldad Tzahor (E)

Department of Molecular Cell Biology, Weizmann Institute of Science, Rehovot, Israel.

Charles A Gersbach (CA)

Duke Regeneration Center, Duke University, Durham, NC, USA; Department of Cell Biology, Duke University Medical School, Durham, NC, USA; Department of Biomedical Engineering, Duke University, Durham, NC, USA; Department of Surgery, Duke University School of Medicine, Durham, NC, USA; Center for Advanced Genomic Technologies, Duke University, Durham, NC, USA; Department of Orthopaedic Surgery, Duke University School of Medicine, Durham, NC, USA.

Jeffery D Molkentin (JD)

Department of Pediatrics, Cincinnati Children's Hospital Medical Center, University of Cincinnati, Cincinnati, OH, USA.

Nenad Bursac (N)

Department of Biomedical Engineering, Duke University, Durham, NC, USA.

Brian L Black (BL)

Cardiovascular Research Institute, University of California, San Francisco, San Francisco, CA, USA.

Kenneth D Poss (KD)

Duke Regeneration Center, Duke University, Durham, NC, USA; Department of Cell Biology, Duke University Medical School, Durham, NC, USA; Center for Advanced Genomic Technologies, Duke University, Durham, NC, USA. Electronic address: ken.poss@duke.edu.

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