Flow-dependent regulation of endothelial Tie2 by GATA3 in vivo.

Blood flow Capillary leakage Hypotension Permeability Shock Vascular leakage

Journal

Intensive care medicine experimental
ISSN: 2197-425X
Titre abrégé: Intensive Care Med Exp
Pays: Germany
ID NLM: 101645149

Informations de publication

Date de publication:
02 Aug 2021
Historique:
received: 09 04 2021
accepted: 24 06 2021
entrez: 2 8 2021
pubmed: 3 8 2021
medline: 3 8 2021
Statut: epublish

Résumé

Reduced endothelial Tie2 expression occurs in diverse experimental models of critical illness, and experimental Tie2 suppression is sufficient to increase spontaneous vascular permeability. Looking for a common denominator among different critical illnesses that could drive the same Tie2 suppressive (thereby leak inducing) phenotype, we identified "circulatory shock" as a shared feature and postulated a flow-dependency of Tie2 gene expression in a GATA3 dependent manner. Here, we analyzed if this mechanism of flow-regulation of gene expression exists in vivo in the absence of inflammation. To experimentally mimic a shock-like situation, we developed a murine model of clonidine-induced hypotension by targeting a reduced mean arterial pressure (MAP) of approximately 50% over 4 h. We found that hypotension-induced reduction of flow in the absence of confounding disease factors (i.e., inflammation, injury, among others) is sufficient to suppress GATA3 and Tie2 transcription. Conditional endothelial-specific GATA3 knockdown (B6-Gata3 The data suggest that the GATA3-Tie2 signaling pathway might play a pivotal role in controlling vascular barrier function and that it is affected in diverse critical illnesses with shock as a consequence of a flow-regulated gene response. Targeting this novel mechanism might offer therapeutic opportunities to treat vascular leakage of diverse etiologies.

Sections du résumé

BACKGROUND BACKGROUND
Reduced endothelial Tie2 expression occurs in diverse experimental models of critical illness, and experimental Tie2 suppression is sufficient to increase spontaneous vascular permeability. Looking for a common denominator among different critical illnesses that could drive the same Tie2 suppressive (thereby leak inducing) phenotype, we identified "circulatory shock" as a shared feature and postulated a flow-dependency of Tie2 gene expression in a GATA3 dependent manner. Here, we analyzed if this mechanism of flow-regulation of gene expression exists in vivo in the absence of inflammation.
RESULTS RESULTS
To experimentally mimic a shock-like situation, we developed a murine model of clonidine-induced hypotension by targeting a reduced mean arterial pressure (MAP) of approximately 50% over 4 h. We found that hypotension-induced reduction of flow in the absence of confounding disease factors (i.e., inflammation, injury, among others) is sufficient to suppress GATA3 and Tie2 transcription. Conditional endothelial-specific GATA3 knockdown (B6-Gata3
CONCLUSIONS CONCLUSIONS
The data suggest that the GATA3-Tie2 signaling pathway might play a pivotal role in controlling vascular barrier function and that it is affected in diverse critical illnesses with shock as a consequence of a flow-regulated gene response. Targeting this novel mechanism might offer therapeutic opportunities to treat vascular leakage of diverse etiologies.

Identifiants

pubmed: 34337671
doi: 10.1186/s40635-021-00402-x
pii: 10.1186/s40635-021-00402-x
pmc: PMC8326239
doi:

Types de publication

Journal Article

Langues

eng

Pagination

38

Subventions

Organisme : Deutsche Forschungsgemeinschaft
ID : DA 1209/4-3

Informations de copyright

© 2021. The Author(s).

Références

BMC Bioinformatics. 2017 Nov 29;18(1):529
pubmed: 29187165
Am J Physiol Renal Physiol. 2009 Aug;297(2):F272-81
pubmed: 19515812
Proc Natl Acad Sci U S A. 2012 Jun 19;109(25):10024-9
pubmed: 22665799
Pflugers Arch. 2020 Apr;472(4):419-433
pubmed: 32239285
Proc Natl Acad Sci U S A. 2018 Feb 6;115(6):1298-1303
pubmed: 29358379
Br J Anaesth. 2018 Nov;121(5):1041-1051
pubmed: 30336848
J Biol Chem. 2009 Oct 16;284(42):29109-24
pubmed: 19674970
Biol Pharm Bull. 2015;38(9):1320-7
pubmed: 26328487
Arch Biochem Biophys. 2016 Feb 1;591:111-31
pubmed: 26686737
J Am Soc Nephrol. 2017 Jul;28(7):1973-1982
pubmed: 28465380
Shock. 2019 Jun;51(6):757-769
pubmed: 30520765
Physiol Rev. 2011 Jan;91(1):327-87
pubmed: 21248169
Shock. 2016 Mar;45(3):259-70
pubmed: 26871664
Elife. 2018 Dec 28;7:
pubmed: 30592462
N Engl J Med. 2015 May 21;372(21):1987-95
pubmed: 25981191
Int J Cancer. 2016 May 15;138(10):2466-76
pubmed: 26704560
Blood. 2002 Sep 1;100(5):1689-98
pubmed: 12176889
JAMA. 2016 Feb 23;315(8):801-10
pubmed: 26903338
Elife. 2020 Aug 24;9:
pubmed: 32838837
Immunity. 2003 Jul;19(1):83-94
pubmed: 12871641
Dev Cell. 2006 Dec;11(6):845-57
pubmed: 17141159
Annu Rev Biomed Eng. 2014 Jul 11;16:505-32
pubmed: 24905872
Br J Pharmacol. 1999 Mar;126(6):1522-30
pubmed: 10217548
Proc Natl Acad Sci U S A. 2016 Mar 1;113(9):2472-7
pubmed: 26884170
J Cell Sci. 2012 Jul 1;125(Pt 13):3061-73
pubmed: 22797927
Crit Care Med. 2018 Sep;46(9):e928-e936
pubmed: 29979219
Antioxid Redox Signal. 2016 Sep 1;25(7):373-88
pubmed: 27027326
J Vis Exp. 2010 Dec 14;(46):
pubmed: 21178973
Nat Immunol. 2004 Nov;5(11):1157-65
pubmed: 15475959

Auteurs

Temitayo O Idowu (TO)

Department of Nephrology and Hypertension, Hannover Medical School, Hannover, Germany.

Valerie Etzrodt (V)

Department of Nephrology and Hypertension, Hannover Medical School, Hannover, Germany.

Thorben Pape (T)

Department of Nephrology and Hypertension, Hannover Medical School, Hannover, Germany.

Joerg Heineke (J)

Department of Cardiovascular Physiology, European Center for Angioscience, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany.
German Center for Cardiovascular Research (DZHK), Partner Site Heidelberg, Mannheim, Germany.

Klaus Stahl (K)

Department of Gastroenterology, Hepatology and Endocrinology, Hannover Medical School, Hannover, Germany.

Hermann Haller (H)

Department of Nephrology and Hypertension, Hannover Medical School, Hannover, Germany.

Sascha David (S)

Department of Nephrology and Hypertension, Hannover Medical School, Hannover, Germany. sascha.david@usz.ch.
Institute of Intensive Care Medicine, University Hospital Zurich, Rämistrasse 100, 8091, Zurich, Switzerland. sascha.david@usz.ch.

Classifications MeSH