Interaction between ALK1 Signaling and Connexin40 in the Development of Arteriovenous Malformations

Document Type

Article

Abstract

© 2016 American Heart Association, Inc. Objective - To determine the role of Gja5 that encodes for the gap junction protein connexin40 in the generation of arteriovenous malformations in the hereditary hemorrhagic telangiectasia type 2 (HHT2) mouse model. Approach and Results - We identified GJA5 as a target gene of the bone morphogenetic protein-9/activin receptor-like kinase 1 signaling pathway in human aortic endothelial cells and importantly found that connexin40 levels were particularly low in a small group of patients with HHT2. We next took advantage of the Acvrl1+/- mutant mice that develop lesions similar to those in patients with HHT2 and generated Acvrl1+/-; Gja5EGFP/+ mice. Gja5 haploinsufficiency led to vasodilation of the arteries and rarefaction of the capillary bed in Acvrl1+/- mice. At the molecular level, we found that reduced Gja5 in Acvrl1+/- mice stimulated the production of reactive oxygen species, an important mediator of vessel remodeling. To normalize the altered hemodynamic forces in Acvrl1+/-; Gja5EGFP/+ mice, capillaries formed transient arteriovenous shunts that could develop into large malformations when exposed to environmental insults. Conclusions - We identified GJA5 as a potential modifier gene for HHT2. Our findings demonstrate that Acvrl1 haploinsufficiency combined with the effects of modifier genes that regulate vessel caliber is responsible for the heterogeneity and severity of the disease. The mouse models of HHT have led to the proposal that 3 events - heterozygosity, loss of heterozygosity, and angiogenic stimulation - are necessary for arteriovenous malformation formation. Here, we present a novel 3-step model in which pathological vessel caliber and consequent altered blood flow are necessary events for arteriovenous malformation development.

Keywords

alpha-smooth muscle actin, mouse, arteriovenous malformations, connexin 40, erythrocyte, hereditary hemorrhagic telangiectasia

Publication Date

4-1-2016

Publication Title

Arteriosclerosis, Thrombosis, and Vascular Biology

ISSN

10795642

E-ISSN

15244636

Volume

36

Issue

4

First Page

707

Last Page

717

PubMed ID

26821948

Digital Object Identifier (DOI)

10.1161/ATVBAHA.115.306719

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