Ablation of C-type natriuretic peptide/cGMP signaling in fibroblasts exacerbates adverse cardiac remodeling in mice.


Journal

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

Informations de publication

Date de publication:
10 07 2023
Historique:
received: 22 03 2022
accepted: 23 05 2023
medline: 11 7 2023
pubmed: 25 5 2023
entrez: 25 5 2023
Statut: epublish

Résumé

Excessive activation of cardiac fibroblasts (CFs) in response to injury provokes cardiac fibrosis, stiffness, and failure. The local mediators counterregulating this response remain unclear. Exogenous C-type natriuretic peptide (CNP) exerts antifibrotic effects in preclinical models. To unravel the role of the endogenous hormone, we generated mice with fibroblast-restricted deletion (KO) of guanylyl cyclase-B (GC-B), the cGMP-synthesizing CNP receptor. CNP activated GC-B/cGMP signaling in human and murine CFs, preventing proliferative and promigratory effects of angiotensin II (Ang II) and TGF-β. Fibroblast-specific GC-B-KO mice showed enhanced fibrosis in response to Ang II infusions. Moreover, after 2 weeks of mild pressure overload induced by transverse aortic constriction (TAC), such KO mice had augmented cardiac fibrosis and hypertrophy, together with systolic and diastolic contractile dysfunction. This was associated with increased expression of the profibrotic genes encoding collagen I, III, and periostin. Notably, such responses to Ang II and TAC were greater in female as compared with male KO mice. Enhanced Ang II-induced CNP expression in female hearts and augmented GC-B expression and activity in female CFs may contribute to this sex disparity. The results show that paracrine CNP signaling in CFs has antifibrotic and antihypertrophic effects. The CNP/GC-B/cGMP pathway might be a target for therapies combating pathological cardiac remodeling.

Identifiants

pubmed: 37227779
pii: 160416
doi: 10.1172/jci.insight.160416
pmc: PMC10371345
doi:
pii:

Substances chimiques

Natriuretic Peptide, C-Type 127869-51-6
Vasodilator Agents 0
Angiotensin II 11128-99-7

Types de publication

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

Langues

eng

Sous-ensembles de citation

IM

Références

Physiol Rev. 2016 Apr;96(2):751-804
pubmed: 27030537
Circulation. 2014 Jul 29;130(5):419-30
pubmed: 24899689
J Biol Chem. 1999 Aug 20;274(34):23761-9
pubmed: 10446136
Br J Pharmacol. 2019 Dec;176(24):4696-4707
pubmed: 31423565
Nat Commun. 2022 Jan 10;13(1):149
pubmed: 35013221
Circ Res. 2016 Jun 10;118(12):1906-17
pubmed: 27140435
Clin Endocrinol (Oxf). 2013 May;78(5):783-9
pubmed: 22963390
J Renin Angiotensin Aldosterone Syst. 2001 Jun;2(2):117-22
pubmed: 11881110
Hypertension. 2011 Feb;57(2):201-7
pubmed: 21189408
J Invest Dermatol. 2009 Jan;129(1):194-204
pubmed: 18563179
Circ Heart Fail. 2019 Apr;12(4):e005565
pubmed: 30998392
MethodsX. 2015 Feb 21;2:124-34
pubmed: 26150980
Circ Res. 2018 Mar 2;122(5):742-751
pubmed: 29326144
J Am Coll Cardiol. 2005 Feb 15;45(4):608-16
pubmed: 15708711
Kidney Int. 1998 May;53(5):1143-51
pubmed: 9573528
EMBO J. 2012 Jan 18;31(2):429-42
pubmed: 22085926
Am J Physiol Lung Cell Mol Physiol. 2004 Dec;287(6):L1172-7
pubmed: 15285999
Circulation. 2018 Jul 31;138(5):494-508
pubmed: 29626067
Eur Heart J. 2020 Mar 1;41(9):1006-1020
pubmed: 30903134
Circulation. 2020 Oct 13;142(15):1448-1463
pubmed: 32795101
J Clin Invest. 2014 Sep;124(9):4039-51
pubmed: 25105365
J Endocrinol. 2008 Dec;199(3):481-7
pubmed: 18784186
Am J Physiol. 1997 Dec;273(6):H2672-7
pubmed: 9435603
Eur Heart J. 2013 Apr;34(16):1233-44
pubmed: 22199120
Steroids. 2014 Sep;87:1-5
pubmed: 24880122
Sci Rep. 2015 May 27;5:10554
pubmed: 26014585
Circ Res. 2021 May 14;128(10):1451-1467
pubmed: 33983831
FASEB J. 2018 Sep;32(9):4941-4954
pubmed: 29601781
Circulation. 2020 Jan 21;141(3):217-233
pubmed: 31801360
Proc Natl Acad Sci U S A. 1999 Jun 22;96(13):7403-8
pubmed: 10377427
PLoS One. 2015 Dec 21;10(12):e0144824
pubmed: 26691397
Cardiovasc Res. 2021 May 25;117(6):1450-1488
pubmed: 33135058
JCI Insight. 2019 Aug 08;4(15):e128722
pubmed: 31393098
Proc Natl Acad Sci U S A. 2021 Feb 2;118(5):
pubmed: 33500351
Proc Natl Acad Sci U S A. 2004 Dec 7;101(49):17300-5
pubmed: 15572448
JCI Insight. 2020 Nov 19;5(22):
pubmed: 33055420
J Clin Invest. 2010 Jan;120(1):254-65
pubmed: 20038803
J Clin Invest. 2017 Oct 2;127(10):3770-3783
pubmed: 28891814
J Mol Cell Cardiol. 2014 Oct;75:199-205
pubmed: 25117468
Nature. 2014 Oct 30;514(7524):585-90
pubmed: 25317562

Auteurs

Franziska Werner (F)

Institute of Physiology, University of Würzburg, Würzburg, Germany.

Estefania Prentki Santos (E)

Institute of Physiology, University of Würzburg, Würzburg, Germany.

Konstanze Michel (K)

Institute of Physiology, University of Würzburg, Würzburg, Germany.

Hanna Schrader (H)

Institute of Physiology, University of Würzburg, Würzburg, Germany.

Katharina Völker (K)

Institute of Physiology, University of Würzburg, Würzburg, Germany.

Tamara Potapenko (T)

Institute of Physiology, University of Würzburg, Würzburg, Germany.

Lisa Krebes (L)

Institute of Physiology, University of Würzburg, Würzburg, Germany.

Marco Abeßer (M)

Institute of Physiology, University of Würzburg, Würzburg, Germany.

Dorothe Möllmann (D)

Institute of Pathology, University Hospital Essen, University Duisburg-Essen, Duisburg, Germany.

Martin Schlattjan (M)

Institute of Pathology, University Hospital Essen, University Duisburg-Essen, Duisburg, Germany.

Hannes Schmidt (H)

Interfaculty Institute of Biochemistry, University of Tübingen, Tübingen, Germany.

Boris V Skryabin (BV)

Core Facility Transgenic Animal and Genetic Engineering Models, University of Münster, Münster, Germany.

Katarina Špiranec Spes (K)

Institute of Physiology, University of Würzburg, Würzburg, Germany.

Kai Schuh (K)

Institute of Physiology, University of Würzburg, Würzburg, Germany.

Christopher P Denton (CP)

UCL Centre for Rheumatology and Connective Tissue Diseases, Royal Free Hospital, London, United Kingdom.

Hideo A Baba (HA)

Institute of Pathology, University Hospital Essen, University Duisburg-Essen, Duisburg, Germany.

Michaela Kuhn (M)

Institute of Physiology, University of Würzburg, Würzburg, Germany.

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Classifications MeSH