Long noncoding RNA H19X is a key mediator of TGF-β-driven fibrosis.


Journal

The Journal of clinical investigation
ISSN: 1558-8238
Titre abrégé: J Clin Invest
Pays: United States
ID NLM: 7802877

Informations de publication

Date de publication:
01 09 2020
Historique:
received: 09 12 2019
accepted: 17 06 2020
pubmed: 1 7 2020
medline: 9 2 2021
entrez: 1 7 2020
Statut: ppublish

Résumé

TGF-β is a master regulator of fibrosis, driving the differentiation of fibroblasts into apoptosis-resistant myofibroblasts and sustaining the production of extracellular matrix (ECM) components. Here, we identified the nuclear long noncoding RNA (lncRNA) H19X as a master regulator of TGF-β-driven tissue fibrosis. H19X was consistently upregulated in a wide variety of human fibrotic tissues and diseases and was strongly induced by TGF-β, particularly in fibroblasts and fibroblast-related cells. Functional experiments following H19X silencing revealed that H19X was an obligatory factor for TGF-β-induced ECM synthesis as well as differentiation and survival of ECM-producing myofibroblasts. We showed that H19X regulates DDIT4L gene expression, specifically interacting with a region upstream of the DDIT4L gene and changing the chromatin accessibility of a DDIT4L enhancer. These events resulted in transcriptional repression of DDIT4L and, in turn, in increased collagen expression and fibrosis. Our results shed light on key effectors of TGF-β-induced ECM remodeling and fibrosis.

Identifiants

pubmed: 32603313
pii: 135439
doi: 10.1172/JCI135439
pmc: PMC7456219
doi:
pii:

Substances chimiques

Adaptor Proteins, Signal Transducing 0
DDIT4L protein, human 0
Ddit4l protein, mouse 0
RNA, Long Noncoding 0
Transforming Growth Factor beta 0

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

4888-4905

Subventions

Organisme : NCATS NIH HHS
ID : KL2 TR003168
Pays : United States
Organisme : NIDDK NIH HHS
ID : P30 DK123704
Pays : United States

Références

Elife. 2013 Dec 31;2:e01749
pubmed: 24381249
Arthritis Rheum. 1996 Aug;39(8):1338-46
pubmed: 8702442
Ann Rheum Dis. 1994 Nov;53(11):763-7
pubmed: 7826139
Nat Rev Rheumatol. 2009 Apr;5(4):200-6
pubmed: 19337284
Arthritis Rheum. 2001 Jul;44(7):1667-76
pubmed: 11465719
Ann Rheum Dis. 2013 Nov;72(11):1747-55
pubmed: 24092682
Database (Oxford). 2017 Jan 1;2017:
pubmed: 28605766
J Cell Mol Med. 2019 Jul;23(7):4738-4745
pubmed: 31062436
Nucleic Acids Res. 2013 Feb 1;41(3):1450-63
pubmed: 23275551
EMBO Rep. 2012 Nov 6;13(11):971-83
pubmed: 23070366
Cell. 2014 Dec 18;159(7):1665-80
pubmed: 25497547
Arthritis Rheum. 2011 Jun;63(6):1707-17
pubmed: 21370225
Nat Rev Rheumatol. 2014 Dec;10(12):706-19
pubmed: 25136781
Nat Rev Nephrol. 2016 Jun;12(6):325-38
pubmed: 27108839
Circ Res. 2017 Aug 18;121(5):575-583
pubmed: 28630135
Nature. 2014 Jan 30;505(7485):635-40
pubmed: 24463510
J Clin Invest. 2007 Mar;117(3):557-67
pubmed: 17332883
Nucleic Acids Res. 2019 Jul 2;47(W1):W158-W165
pubmed: 31165883
FEBS J. 2016 Jun;283(12):2219-32
pubmed: 26807763
J Biol Chem. 2001 Jun 8;276(23):19945-53
pubmed: 11262418
Sci Transl Med. 2017 Dec 13;9(420):
pubmed: 29237758
Nat Rev Dis Primers. 2015 Apr 23;1:15002
pubmed: 27189141
Sci Rep. 2017 Feb 15;7:42657
pubmed: 28198439
Radiother Oncol. 2014 May;111(2):186-93
pubmed: 24835153
Biochemistry. 1975 Nov 18;14(23):5194-9
pubmed: 43
Cell Death Differ. 2015 Apr;22(4):612-25
pubmed: 25257176
Nat Commun. 2015 Jul 24;6:7743
pubmed: 26205790
Mol Biol Cell. 2003 Jun;14(6):2508-19
pubmed: 12808047
J Cell Physiol. 2004 Mar;198(3):350-8
pubmed: 14755540
Genome Biol. 2018 Oct 4;19(1):151
pubmed: 30286773
J Am Coll Cardiol. 2015 Nov 3;66(18):2005-2015
pubmed: 26516004
Arthritis Rheum. 2011 Mar;63(3):783-94
pubmed: 21360508
Nucleic Acids Res. 2014 Jan;42(Database issue):D749-55
pubmed: 24316576
Can J Gastroenterol. 2005 Sep;19 Suppl A:5A-36A
pubmed: 16151544
Nature. 2012 Sep 6;489(7414):57-74
pubmed: 22955616
Ann Intern Med. 2010 Feb 2;152(3):159-66
pubmed: 20124232
Sci Signal. 2017 Feb 28;10(468):
pubmed: 28246202
Nat Struct Mol Biol. 2014 Feb;21(2):198-206
pubmed: 24463464
Oncotarget. 2016 Aug 9;7(32):51473-51481
pubmed: 27391349
Curr Opin Rheumatol. 2014 Mar;26(2):131-7
pubmed: 24441644
Mol Cell. 2011 Nov 18;44(4):667-78
pubmed: 21963238
Arthritis Rheumatol. 2015 Nov;67(11):3016-26
pubmed: 26238292
Nat Cell Biol. 2012 Jun 10;14(7):659-65
pubmed: 22684254
J Cell Biochem. 2019 Jun;120(6):10821-10829
pubmed: 30672010
Cell. 2018 Jan 25;172(3):393-407
pubmed: 29373828
Wound Repair Regen. 2016 Mar;24(2):215-22
pubmed: 26704519
Nature. 2001 Feb 15;409(6822):860-921
pubmed: 11237011
Nat Med. 2015 Feb;21(2):150-8
pubmed: 25581517
Cell. 2014 Mar 27;157(1):77-94
pubmed: 24679528
Nucleic Acids Res. 2000 Jan 1;28(1):27-30
pubmed: 10592173
Theranostics. 2018 Apr 15;8(10):2814-2829
pubmed: 29774077
J Vis Exp. 2012 Mar 25;(61):
pubmed: 22472705
Int J Burns Trauma. 2012;2(1):18-28
pubmed: 22928164
Biochim Biophys Acta. 2014 Nov;1842(11):2204-15
pubmed: 25201080
Arthritis Rheumatol. 2014 Mar;66(3):714-25
pubmed: 24574232
Int J Dev Biol. 2000 Apr;44(3):253-65
pubmed: 10853822
Nat Struct Mol Biol. 2017 Mar 3;24(3):197-204
pubmed: 28257137
Int J Mol Sci. 2018 Aug 20;19(8):
pubmed: 30127261

Auteurs

Elena Pachera (E)

Center of Experimental Rheumatology, Department of Rheumatology, University Hospital Zurich, Zurich, Switzerland.

Shervin Assassi (S)

Division of Rheumatology, Department of Internal Medicine, University of Texas Health Science Center at Houston, McGovern Medical School, Houston, Texas, USA.

Gloria A Salazar (GA)

Division of Rheumatology, Department of Internal Medicine, University of Texas Health Science Center at Houston, McGovern Medical School, Houston, Texas, USA.

Mara Stellato (M)

Center of Experimental Rheumatology, Department of Rheumatology, University Hospital Zurich, Zurich, Switzerland.

Florian Renoux (F)

Center of Experimental Rheumatology, Department of Rheumatology, University Hospital Zurich, Zurich, Switzerland.

Adam Wunderlin (A)

Center of Experimental Rheumatology, Department of Rheumatology, University Hospital Zurich, Zurich, Switzerland.

Przemyslaw Blyszczuk (P)

Center of Experimental Rheumatology, Department of Rheumatology, University Hospital Zurich, Zurich, Switzerland.

Robert Lafyatis (R)

Division of Rheumatology and Clinical Immunology, Department of Medicine, University of Pittsburgh, Pittsburgh, Pennsylvania, USA.

Fina Kurreeman (F)

Department of Rheumatology, Leiden University Medical Center, Leiden, Netherlands.

Jeska de Vries-Bouwstra (J)

Department of Rheumatology, Leiden University Medical Center, Leiden, Netherlands.

Tobias Messemaker (T)

Department of Rheumatology, Leiden University Medical Center, Leiden, Netherlands.

Carol A Feghali-Bostwick (CA)

Division of Rheumatology, Medical University of South Carolina, Charleston, South Carolina, USA.

Gerhard Rogler (G)

Department of Gastroenterology and Hepatology, University Hospital Zurich, Zurich, Switzerland.

Wouter T van Haaften (WT)

Department of Gastroenterology and Hepatology, University Medical Center Groningen, Groningen, Netherlands.

Gerard Dijkstra (G)

Department of Gastroenterology and Hepatology, University Medical Center Groningen, Groningen, Netherlands.

Fiona Oakley (F)

Newcastle Fibrosis Research Group, Institute of Cellular Medicine, Newcastle University, Newcastle upon Tyne, United Kingdom.

Maurizio Calcagni (M)

Department of Plastic Surgery and Hand Surgery, University Hospital Zurich, Zurich, Switzerland.

Janine Schniering (J)

Center of Experimental Rheumatology, Department of Rheumatology, University Hospital Zurich, Zurich, Switzerland.

Britta Maurer (B)

Center of Experimental Rheumatology, Department of Rheumatology, University Hospital Zurich, Zurich, Switzerland.

Jörg Hw Distler (JH)

Department of Internal Medicine 3, University of Erlangen, Erlangen, Germany.

Gabriela Kania (G)

Center of Experimental Rheumatology, Department of Rheumatology, University Hospital Zurich, Zurich, Switzerland.

Mojca Frank-Bertoncelj (M)

Center of Experimental Rheumatology, Department of Rheumatology, University Hospital Zurich, Zurich, Switzerland.

Oliver Distler (O)

Center of Experimental Rheumatology, Department of Rheumatology, University Hospital Zurich, Zurich, Switzerland.

Articles similaires

[Redispensing of expensive oral anticancer medicines: a practical application].

Lisanne N van Merendonk, Kübra Akgöl, Bastiaan Nuijen
1.00
Humans Antineoplastic Agents Administration, Oral Drug Costs Counterfeit Drugs

Smoking Cessation and Incident Cardiovascular Disease.

Jun Hwan Cho, Seung Yong Shin, Hoseob Kim et al.
1.00
Humans Male Smoking Cessation Cardiovascular Diseases Female
Humans United States Aged Cross-Sectional Studies Medicare Part C
1.00
Humans Yoga Low Back Pain Female Male

Classifications MeSH