SLIT3 deficiency attenuates pressure overload-induced cardiac fibrosis and remodeling.


Journal

JCI insight
ISSN: 2379-3708
Titre abrégé: JCI Insight
Pays: United States
ID NLM: 101676073

Informations de publication

Date de publication:
18 06 2020
Historique:
received: 13 02 2020
accepted: 06 05 2020
entrez: 10 7 2020
pubmed: 10 7 2020
medline: 9 6 2021
Statut: epublish

Résumé

In pulmonary hypertension and certain forms of congenital heart disease, ventricular pressure overload manifests at birth and is an obligate hemodynamic abnormality that stimulates myocardial fibrosis, which leads to ventricular dysfunction and poor clinical outcomes. Thus, an attractive strategy is to attenuate the myocardial fibrosis to help preserve ventricular function. Here, by analyzing RNA-sequencing databases and comparing the transcript and protein levels of fibrillar collagen in WT and global-knockout mice, we found that slit guidance ligand 3 (SLIT3) was present predominantly in fibrillar collagen-producing cells and that SLIT3 deficiency attenuated collagen production in the heart and other nonneuronal tissues. We then performed transverse aortic constriction or pulmonary artery banding to induce left and right ventricular pressure overload, respectively, in WT and knockout mice. We discovered that SLIT3 deficiency abrogated fibrotic and hypertrophic changes and promoted long-term ventricular function and overall survival in both left and right ventricular pressure overload. Furthermore, we found that SLIT3 stimulated fibroblast activity and fibrillar collagen production, which coincided with the transcription and nuclear localization of the mechanotransducer yes-associated protein 1. These results indicate that SLIT3 is important for regulating fibroblast activity and fibrillar collagen synthesis in an autocrine manner, making it a potential therapeutic target for fibrotic diseases, especially myocardial fibrosis and adverse remodeling induced by persistent afterload elevation.

Identifiants

pubmed: 32644051
pii: 136852
doi: 10.1172/jci.insight.136852
pmc: PMC7406261
doi:
pii:

Substances chimiques

Membrane Proteins 0
Slit3 protein, mouse 0
Collagen 9007-34-5

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

Subventions

Organisme : NHLBI NIH HHS
ID : K08 HL146351
Pays : United States
Organisme : NHLBI NIH HHS
ID : R35 HL144984
Pays : United States

Références

Am J Physiol Heart Circ Physiol. 2001 Sep;281(3):H1104-12
pubmed: 11514276
Genomics. 2006 Oct;88(4):480-8
pubmed: 16781840
Biochem Biophys Res Commun. 2018 Dec 2;506(4):847-853
pubmed: 30389141
Nat Cell Biol. 2013 Jun;15(6):637-46
pubmed: 23708000
Nat Cell Biol. 2018 Aug;20(8):888-899
pubmed: 30050119
Can J Cardiol. 2015 Apr;31(4):391-406
pubmed: 25840092
Mol Biol Cell. 2017 Jul 7;28(14):1871-1882
pubmed: 28468977
Mech Dev. 2003 Sep;120(9):1059-70
pubmed: 14550534
Cardiovasc Res. 2018 May 1;114(6):794-804
pubmed: 29538649
Circulation. 2018 Jan 30;137(5):508-518
pubmed: 29378757
J Biol Chem. 2019 Mar 8;294(10):3603-3617
pubmed: 30635403
Cell. 1999 Mar 19;96(6):795-806
pubmed: 10102268
Circ Res. 2016 Mar 18;118(6):1021-40
pubmed: 26987915
Nature. 2017 Dec 7;552(7683):110-115
pubmed: 29160304
Circ Res. 2002 Dec 13;91(12):1103-13
pubmed: 12480810
J Clin Invest. 2018 Apr 2;128(4):1429-1441
pubmed: 29504949
Cell Mol Life Sci. 2014 Feb;71(4):549-74
pubmed: 23649149
Circulation. 2004 Apr 6;109(13):1580-9
pubmed: 15066961
Circulation. 2013 Jul 23;128(4):388-400
pubmed: 23877061
Clin Sci (Lond). 2008 Aug;115(3):99-106
pubmed: 18248324
Eur Respir J. 2015 Jun;45(6):1603-12
pubmed: 25882798
Heart Fail Rev. 2016 Mar;21(2):199-211
pubmed: 26883434
Semin Fetal Neonatal Med. 2015 Aug;20(4):262-71
pubmed: 25843770
J Vis Exp. 2010 Oct 05;(44):
pubmed: 20972406
Biogerontology. 2002;3(6):325-35
pubmed: 12510171
Circulation. 2013 Oct 29;128(18):2016-25, 1-10
pubmed: 24056688
Science. 2000 Sep 1;289(5484):1501-4
pubmed: 10968779
Nat Rev Mol Cell Biol. 2017 Dec;18(12):758-770
pubmed: 28951564
J Mol Cell Cardiol. 2016 Feb;91:1-5
pubmed: 26748307
J Cardiovasc Dev Dis. 2019 Aug 20;6(3):
pubmed: 31434209
BMB Rep. 2018 Jun;51(6):263-264
pubmed: 29764562
Circ Res. 2005 Apr 15;96(7):748-55
pubmed: 15761199
Circ Genom Precis Med. 2019 Oct;12(10):442-451
pubmed: 31613678
Nat Protoc. 2013 Feb;8(2):302-9
pubmed: 23329003
Nature. 2011 Jun 08;474(7350):179-83
pubmed: 21654799
Circulation. 2002 Jan 1;105(1):85-92
pubmed: 11772881
J Clin Invest. 2011 Jun;121(6):2301-12
pubmed: 21537080
Circulation. 1997 Mar 18;95(6):1601-10
pubmed: 9118531
Science. 2011 Nov 25;334(6059):1074-5
pubmed: 22116874
Proc Natl Acad Sci U S A. 2012 Oct 23;109(43):17472-7
pubmed: 23047693
Annu Rev Physiol. 2003;65:45-79
pubmed: 12524460
Circulation. 2014 Mar 4;129(9):1033-44
pubmed: 24589696
Am J Respir Crit Care Med. 2019 Jun 15;199(12):1458-1459
pubmed: 30608865
Proc Natl Acad Sci U S A. 2003 Apr 29;100(9):5217-22
pubmed: 12702769
Am J Pathol. 2007 Jun;170(6):1807-16
pubmed: 17525249
JACC Cardiovasc Imaging. 2014 Nov;7(11):1081-3
pubmed: 25459588
Blood. 2009 Nov 5;114(19):4300-9
pubmed: 19741192
Dev Cell. 2013 Jan 14;24(1):52-63
pubmed: 23328398
J Clin Invest. 1999 Sep;104(6):709-19
pubmed: 10491406
Exp Biol Med (Maywood). 2002 May;227(5):301-14
pubmed: 11976400
Circulation. 2016 Oct 25;134(17):1293-1302
pubmed: 27777298
Arthritis Res Ther. 2010;12(2):R45
pubmed: 20298552
Nat Genet. 2013 Jun;45(6):580-5
pubmed: 23715323
Am J Respir Crit Care Med. 2014 Mar 1;189(5):603-6
pubmed: 24579837
Nat Commun. 2016 Jul 22;7:12260
pubmed: 27447449
Cold Spring Harb Perspect Biol. 2011 Jan 01;3(1):a004978
pubmed: 21421911
Cardiovasc J Afr. 2010 Jul-Aug;21(4):212-20
pubmed: 20838721
Lancet. 2009 Aug 15;374(9689):551-64
pubmed: 19683641
J Clin Invest. 1975 Jul;56(1):56-64
pubmed: 124746
Bone Res. 2020 Feb 19;8:11
pubmed: 32133214
Am J Physiol Lung Cell Mol Physiol. 2015 Feb 15;308(4):L344-57
pubmed: 25502501
Cardiovasc Res. 2015 Apr 1;106(1):55-66
pubmed: 25691540
Basic Res Cardiol. 2014;109(5):435
pubmed: 25168380
Science. 2001 Apr 27;292(5517):737-40
pubmed: 11326102
J Clin Invest. 2014 Jul;124(7):2921-34
pubmed: 24937432
Cell Stem Cell. 2015 Jan 8;16(1):51-66
pubmed: 25465115
Sci Data. 2017 Aug 29;4:170112
pubmed: 28850106
Organogenesis. 2015;11(1):1-15
pubmed: 25915734
Circ Res. 2019 Aug 16;125(5):552-566
pubmed: 31288631
Development. 2016 Feb 1;143(3):387-97
pubmed: 26839342
Cardiol Rev. 2009 Nov-Dec;17(6):293-9
pubmed: 19829180
Int J Mol Sci. 2010 Jan 28;11(2):407-26
pubmed: 20386646
Eur Respir J. 2015 Feb;45(2):449-62
pubmed: 25261325
Nature. 2010 Oct 14;467(7317):832-8
pubmed: 20881960
Expert Rev Cardiovasc Ther. 2017 Nov;15(11):813-823
pubmed: 28914109
J Clin Invest. 2010 Jan;120(1):254-65
pubmed: 20038803
J Mol Cell Cardiol. 2011 Oct;51(4):600-6
pubmed: 21059352
Nat Med. 2018 Jun;24(6):823-833
pubmed: 29785024
Circ Res. 2016 Sep 30;119(8):909-20
pubmed: 27502479
Nat Rev Mol Cell Biol. 2002 May;3(5):349-63
pubmed: 11988769
Herz. 2002 Mar;27(2):92-8
pubmed: 12025467
Brain Res Mol Brain Res. 1998 Nov 20;62(2):175-86
pubmed: 9813312
Neuron. 2002 Jan 17;33(2):233-48
pubmed: 11804571
Biophys J. 2007 Dec 15;93(12):4453-61
pubmed: 18045965
J Am Soc Nephrol. 2017 Nov;28(11):3278-3290
pubmed: 28768710
JCI Insight. 2017 Jul 6;2(13):
pubmed: 28679962
Mech Dev. 2000 Jun;94(1-2):213-7
pubmed: 10842075
Circulation. 2015 Apr 21;131(16):1435-47
pubmed: 25901069
Nature. 2018 Oct;562(7727):367-372
pubmed: 30283141
Wiley Interdiscip Rev Dev Biol. 2018 Mar;7(2):
pubmed: 29244903
Am J Cardiol. 1996 Apr 1;77(9):734-8
pubmed: 8651125
Circ Res. 2007 Aug 3;101(3):313-21
pubmed: 17569887
Biochem Soc Trans. 2008 Apr;36(Pt 2):251-6
pubmed: 18363568
Nat Rev Drug Discov. 2012 Oct;11(10):790-811
pubmed: 23000686
J Cardiovasc Transl Res. 2015 Apr;8(3):158-63
pubmed: 25788147
Neuron. 2002 Jan 17;33(2):219-32
pubmed: 11804570
Circulation. 2019 Jan 8;139(2):269-285
pubmed: 30615500
Cells. 2019 May 03;8(5):
pubmed: 31058846
Physiol Genomics. 2004 Feb 13;16(3):349-60
pubmed: 14679301
Circulation. 2000 Jun 20;101(24):2863-9
pubmed: 10859294
Circ Res. 2018 Jun 22;123(1):30-32
pubmed: 29929975
Circ Res. 2009 Nov 6;105(10):934-47
pubmed: 19893021
J Clin Invest. 1999 Sep;104(5):567-76
pubmed: 10487771
J Surg Res. 2018 Jan;221:35-42
pubmed: 29229150
Genes Dev. 2008 May 15;22(10):1276-312
pubmed: 18483217
Adv Drug Deliv Rev. 2003 Nov 28;55(12):1531-46
pubmed: 14623400

Auteurs

Lianghui Gong (L)

Section of Pediatric Cardiovascular Surgery, Department of Cardiac Surgery, Michigan Medicine, University of Michigan, Ann Arbor, Michigan, USA.
Department of Cardiovascular Surgery, The Second Xiangya Hospital of Central South University, Changsha, China.

Shuyun Wang (S)

Section of Pediatric Cardiovascular Surgery, Department of Cardiac Surgery, Michigan Medicine, University of Michigan, Ann Arbor, Michigan, USA.

Li Shen (L)

Section of Pediatric Cardiovascular Surgery, Department of Cardiac Surgery, Michigan Medicine, University of Michigan, Ann Arbor, Michigan, USA.

Catherine Liu (C)

Section of Pediatric Cardiovascular Surgery, Department of Cardiac Surgery, Michigan Medicine, University of Michigan, Ann Arbor, Michigan, USA.

Mena Shenouda (M)

Section of Pediatric Cardiovascular Surgery, Department of Cardiac Surgery, Michigan Medicine, University of Michigan, Ann Arbor, Michigan, USA.

Baolei Li (B)

Section of Pediatric Cardiovascular Surgery, Department of Cardiac Surgery, Michigan Medicine, University of Michigan, Ann Arbor, Michigan, USA.

Xiaoxiao Liu (X)

Section of Pediatric Cardiovascular Surgery, Department of Cardiac Surgery, Michigan Medicine, University of Michigan, Ann Arbor, Michigan, USA.

John A Shaw (JA)

Department of Aerospace Engineering and.

Alan L Wineman (AL)

Department of Mechanical Engineering, University of Michigan, Ann Arbor, Michigan, USA.

Yifeng Yang (Y)

Department of Cardiovascular Surgery, The Second Xiangya Hospital of Central South University, Changsha, China.

Dingding Xiong (D)

Section of Pediatric Cardiovascular Surgery, Department of Cardiac Surgery, Michigan Medicine, University of Michigan, Ann Arbor, Michigan, USA.

Anne Eichmann (A)

Yale Cardiovascular Research Center, Department of Internal Medicine, Yale University School of Medicine, New Haven, Connecticut, USA.
Paris Cardiovascular Research Center, INSERM U970, Paris, France.
Department of Cellular and Molecular Physiology, Yale University School of Medicine, New Haven, Connecticut, USA.

Sylvia M Evans (SM)

Skaggs School of Pharmacy and Pharmaceutical Sciences.
Department of Medicine, and.
Department of Pharmacology, UCSD, La Jolla, California, USA.

Stephen J Weiss (SJ)

Division of Genetic Medicine.
Department of Internal Medicine.
Life Sciences Institute.
Cellular and Molecular Biology Graduate Program, and.
Rogel Cancer Center, Michigan Medicine, University of Michigan, Ann Arbor, Michigan, USA.

Ming-Sing Si (MS)

Section of Pediatric Cardiovascular Surgery, Department of Cardiac Surgery, Michigan Medicine, University of Michigan, Ann Arbor, Michigan, USA.

Articles similaires

Robotic Surgical Procedures Animals Humans Telemedicine Models, Animal

Odour generalisation and detection dog training.

Lyn Caldicott, Thomas W Pike, Helen E Zulch et al.
1.00
Animals Odorants Dogs Generalization, Psychological Smell
Animals TOR Serine-Threonine Kinases Colorectal Neoplasms Colitis Mice
Animals Tail Swine Behavior, Animal Animal Husbandry

Classifications MeSH