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Original Research

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

Konstantinos Gkatzis, Jérémy Thalgott, Damien Dos-Santos-Luis, Sabrina Martin, Noël Lamandé, Marie France Carette, Frans Disch, Repke J. Snijder, Cornelius J. Westermann, Johannes J. Mager, S. Paul Oh, Lucile Miquerol, Helen M. Arthur, Christine L. Mummery, Franck Lebrin
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https://doi.org/10.1161/ATVBAHA.115.306719
Arteriosclerosis, Thrombosis, and Vascular Biology. 2016;ATVBAHA.115.306719
Originally published January 28, 2016
Konstantinos Gkatzis
From the Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands (K.G., C.L.M.); CNRS Unité mixte de recherche 7241/INSERM U1050, Center for Interdisciplinary Research in Biology, Collège de France, Paris cedex 05, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); MEMOLIFE Laboratory of Excellence, Paris Sciences et Lettres Research University, Paris, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); Department of Radiology, AP-HP, Tenon Hospital, Paris, France (M.F.C.); Sorbonne Universités, UPMC University, Paris, France (M.F.C.); St. Antonius Hospital, Nieuwegein, The Netherlands (F.D., R.J.S., C.J.W., J.J.M.); Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville (S.P.O.); Aix Marseille Université, CNRS IBDM UMR 7288, Marseille cedex 09, France (L.M.); and Institute of Genetic Medicine, Newcastle University, Newcastle, United Kingdom (C.L.M.).
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Jérémy Thalgott
From the Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands (K.G., C.L.M.); CNRS Unité mixte de recherche 7241/INSERM U1050, Center for Interdisciplinary Research in Biology, Collège de France, Paris cedex 05, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); MEMOLIFE Laboratory of Excellence, Paris Sciences et Lettres Research University, Paris, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); Department of Radiology, AP-HP, Tenon Hospital, Paris, France (M.F.C.); Sorbonne Universités, UPMC University, Paris, France (M.F.C.); St. Antonius Hospital, Nieuwegein, The Netherlands (F.D., R.J.S., C.J.W., J.J.M.); Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville (S.P.O.); Aix Marseille Université, CNRS IBDM UMR 7288, Marseille cedex 09, France (L.M.); and Institute of Genetic Medicine, Newcastle University, Newcastle, United Kingdom (C.L.M.).
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Damien Dos-Santos-Luis
From the Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands (K.G., C.L.M.); CNRS Unité mixte de recherche 7241/INSERM U1050, Center for Interdisciplinary Research in Biology, Collège de France, Paris cedex 05, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); MEMOLIFE Laboratory of Excellence, Paris Sciences et Lettres Research University, Paris, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); Department of Radiology, AP-HP, Tenon Hospital, Paris, France (M.F.C.); Sorbonne Universités, UPMC University, Paris, France (M.F.C.); St. Antonius Hospital, Nieuwegein, The Netherlands (F.D., R.J.S., C.J.W., J.J.M.); Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville (S.P.O.); Aix Marseille Université, CNRS IBDM UMR 7288, Marseille cedex 09, France (L.M.); and Institute of Genetic Medicine, Newcastle University, Newcastle, United Kingdom (C.L.M.).
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Sabrina Martin
From the Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands (K.G., C.L.M.); CNRS Unité mixte de recherche 7241/INSERM U1050, Center for Interdisciplinary Research in Biology, Collège de France, Paris cedex 05, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); MEMOLIFE Laboratory of Excellence, Paris Sciences et Lettres Research University, Paris, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); Department of Radiology, AP-HP, Tenon Hospital, Paris, France (M.F.C.); Sorbonne Universités, UPMC University, Paris, France (M.F.C.); St. Antonius Hospital, Nieuwegein, The Netherlands (F.D., R.J.S., C.J.W., J.J.M.); Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville (S.P.O.); Aix Marseille Université, CNRS IBDM UMR 7288, Marseille cedex 09, France (L.M.); and Institute of Genetic Medicine, Newcastle University, Newcastle, United Kingdom (C.L.M.).
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Noël Lamandé
From the Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands (K.G., C.L.M.); CNRS Unité mixte de recherche 7241/INSERM U1050, Center for Interdisciplinary Research in Biology, Collège de France, Paris cedex 05, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); MEMOLIFE Laboratory of Excellence, Paris Sciences et Lettres Research University, Paris, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); Department of Radiology, AP-HP, Tenon Hospital, Paris, France (M.F.C.); Sorbonne Universités, UPMC University, Paris, France (M.F.C.); St. Antonius Hospital, Nieuwegein, The Netherlands (F.D., R.J.S., C.J.W., J.J.M.); Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville (S.P.O.); Aix Marseille Université, CNRS IBDM UMR 7288, Marseille cedex 09, France (L.M.); and Institute of Genetic Medicine, Newcastle University, Newcastle, United Kingdom (C.L.M.).
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Marie France Carette
From the Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands (K.G., C.L.M.); CNRS Unité mixte de recherche 7241/INSERM U1050, Center for Interdisciplinary Research in Biology, Collège de France, Paris cedex 05, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); MEMOLIFE Laboratory of Excellence, Paris Sciences et Lettres Research University, Paris, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); Department of Radiology, AP-HP, Tenon Hospital, Paris, France (M.F.C.); Sorbonne Universités, UPMC University, Paris, France (M.F.C.); St. Antonius Hospital, Nieuwegein, The Netherlands (F.D., R.J.S., C.J.W., J.J.M.); Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville (S.P.O.); Aix Marseille Université, CNRS IBDM UMR 7288, Marseille cedex 09, France (L.M.); and Institute of Genetic Medicine, Newcastle University, Newcastle, United Kingdom (C.L.M.).
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Frans Disch
From the Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands (K.G., C.L.M.); CNRS Unité mixte de recherche 7241/INSERM U1050, Center for Interdisciplinary Research in Biology, Collège de France, Paris cedex 05, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); MEMOLIFE Laboratory of Excellence, Paris Sciences et Lettres Research University, Paris, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); Department of Radiology, AP-HP, Tenon Hospital, Paris, France (M.F.C.); Sorbonne Universités, UPMC University, Paris, France (M.F.C.); St. Antonius Hospital, Nieuwegein, The Netherlands (F.D., R.J.S., C.J.W., J.J.M.); Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville (S.P.O.); Aix Marseille Université, CNRS IBDM UMR 7288, Marseille cedex 09, France (L.M.); and Institute of Genetic Medicine, Newcastle University, Newcastle, United Kingdom (C.L.M.).
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Repke J. Snijder
From the Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands (K.G., C.L.M.); CNRS Unité mixte de recherche 7241/INSERM U1050, Center for Interdisciplinary Research in Biology, Collège de France, Paris cedex 05, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); MEMOLIFE Laboratory of Excellence, Paris Sciences et Lettres Research University, Paris, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); Department of Radiology, AP-HP, Tenon Hospital, Paris, France (M.F.C.); Sorbonne Universités, UPMC University, Paris, France (M.F.C.); St. Antonius Hospital, Nieuwegein, The Netherlands (F.D., R.J.S., C.J.W., J.J.M.); Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville (S.P.O.); Aix Marseille Université, CNRS IBDM UMR 7288, Marseille cedex 09, France (L.M.); and Institute of Genetic Medicine, Newcastle University, Newcastle, United Kingdom (C.L.M.).
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Cornelius J. Westermann
From the Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands (K.G., C.L.M.); CNRS Unité mixte de recherche 7241/INSERM U1050, Center for Interdisciplinary Research in Biology, Collège de France, Paris cedex 05, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); MEMOLIFE Laboratory of Excellence, Paris Sciences et Lettres Research University, Paris, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); Department of Radiology, AP-HP, Tenon Hospital, Paris, France (M.F.C.); Sorbonne Universités, UPMC University, Paris, France (M.F.C.); St. Antonius Hospital, Nieuwegein, The Netherlands (F.D., R.J.S., C.J.W., J.J.M.); Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville (S.P.O.); Aix Marseille Université, CNRS IBDM UMR 7288, Marseille cedex 09, France (L.M.); and Institute of Genetic Medicine, Newcastle University, Newcastle, United Kingdom (C.L.M.).
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Johannes J. Mager
From the Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands (K.G., C.L.M.); CNRS Unité mixte de recherche 7241/INSERM U1050, Center for Interdisciplinary Research in Biology, Collège de France, Paris cedex 05, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); MEMOLIFE Laboratory of Excellence, Paris Sciences et Lettres Research University, Paris, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); Department of Radiology, AP-HP, Tenon Hospital, Paris, France (M.F.C.); Sorbonne Universités, UPMC University, Paris, France (M.F.C.); St. Antonius Hospital, Nieuwegein, The Netherlands (F.D., R.J.S., C.J.W., J.J.M.); Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville (S.P.O.); Aix Marseille Université, CNRS IBDM UMR 7288, Marseille cedex 09, France (L.M.); and Institute of Genetic Medicine, Newcastle University, Newcastle, United Kingdom (C.L.M.).
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S. Paul Oh
From the Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands (K.G., C.L.M.); CNRS Unité mixte de recherche 7241/INSERM U1050, Center for Interdisciplinary Research in Biology, Collège de France, Paris cedex 05, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); MEMOLIFE Laboratory of Excellence, Paris Sciences et Lettres Research University, Paris, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); Department of Radiology, AP-HP, Tenon Hospital, Paris, France (M.F.C.); Sorbonne Universités, UPMC University, Paris, France (M.F.C.); St. Antonius Hospital, Nieuwegein, The Netherlands (F.D., R.J.S., C.J.W., J.J.M.); Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville (S.P.O.); Aix Marseille Université, CNRS IBDM UMR 7288, Marseille cedex 09, France (L.M.); and Institute of Genetic Medicine, Newcastle University, Newcastle, United Kingdom (C.L.M.).
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Lucile Miquerol
From the Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands (K.G., C.L.M.); CNRS Unité mixte de recherche 7241/INSERM U1050, Center for Interdisciplinary Research in Biology, Collège de France, Paris cedex 05, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); MEMOLIFE Laboratory of Excellence, Paris Sciences et Lettres Research University, Paris, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); Department of Radiology, AP-HP, Tenon Hospital, Paris, France (M.F.C.); Sorbonne Universités, UPMC University, Paris, France (M.F.C.); St. Antonius Hospital, Nieuwegein, The Netherlands (F.D., R.J.S., C.J.W., J.J.M.); Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville (S.P.O.); Aix Marseille Université, CNRS IBDM UMR 7288, Marseille cedex 09, France (L.M.); and Institute of Genetic Medicine, Newcastle University, Newcastle, United Kingdom (C.L.M.).
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Helen M. Arthur
From the Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands (K.G., C.L.M.); CNRS Unité mixte de recherche 7241/INSERM U1050, Center for Interdisciplinary Research in Biology, Collège de France, Paris cedex 05, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); MEMOLIFE Laboratory of Excellence, Paris Sciences et Lettres Research University, Paris, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); Department of Radiology, AP-HP, Tenon Hospital, Paris, France (M.F.C.); Sorbonne Universités, UPMC University, Paris, France (M.F.C.); St. Antonius Hospital, Nieuwegein, The Netherlands (F.D., R.J.S., C.J.W., J.J.M.); Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville (S.P.O.); Aix Marseille Université, CNRS IBDM UMR 7288, Marseille cedex 09, France (L.M.); and Institute of Genetic Medicine, Newcastle University, Newcastle, United Kingdom (C.L.M.).
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Christine L. Mummery
From the Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands (K.G., C.L.M.); CNRS Unité mixte de recherche 7241/INSERM U1050, Center for Interdisciplinary Research in Biology, Collège de France, Paris cedex 05, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); MEMOLIFE Laboratory of Excellence, Paris Sciences et Lettres Research University, Paris, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); Department of Radiology, AP-HP, Tenon Hospital, Paris, France (M.F.C.); Sorbonne Universités, UPMC University, Paris, France (M.F.C.); St. Antonius Hospital, Nieuwegein, The Netherlands (F.D., R.J.S., C.J.W., J.J.M.); Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville (S.P.O.); Aix Marseille Université, CNRS IBDM UMR 7288, Marseille cedex 09, France (L.M.); and Institute of Genetic Medicine, Newcastle University, Newcastle, United Kingdom (C.L.M.).
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Franck Lebrin
From the Department of Anatomy and Embryology, Leiden University Medical Center, Leiden, The Netherlands (K.G., C.L.M.); CNRS Unité mixte de recherche 7241/INSERM U1050, Center for Interdisciplinary Research in Biology, Collège de France, Paris cedex 05, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); MEMOLIFE Laboratory of Excellence, Paris Sciences et Lettres Research University, Paris, France (J.T., D.D.-S.-L., S.M., N.L., F.L.); Department of Radiology, AP-HP, Tenon Hospital, Paris, France (M.F.C.); Sorbonne Universités, UPMC University, Paris, France (M.F.C.); St. Antonius Hospital, Nieuwegein, The Netherlands (F.D., R.J.S., C.J.W., J.J.M.); Department of Physiology and Functional Genomics, College of Medicine, University of Florida, Gainesville (S.P.O.); Aix Marseille Université, CNRS IBDM UMR 7288, Marseille cedex 09, France (L.M.); and Institute of Genetic Medicine, Newcastle University, Newcastle, United Kingdom (C.L.M.).
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Abstract

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/ALK1 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 a proangiogenic—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.

  • α-smooth muscle actin, mouse
  • arteriovenous malformations
  • connexin 40
  • red blood cell
  • telangiectasia, hereditary hemorrhagic
  • Received October 13, 2015.
  • Accepted January 20, 2016.
  • © 2016 American Heart Association, Inc.
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    Interaction Between ALK1 Signaling and Connexin40 in the Development of Arteriovenous Malformations
    Konstantinos Gkatzis, Jérémy Thalgott, Damien Dos-Santos-Luis, Sabrina Martin, Noël Lamandé, Marie France Carette, Frans Disch, Repke J. Snijder, Cornelius J. Westermann, Johannes J. Mager, S. Paul Oh, Lucile Miquerol, Helen M. Arthur, Christine L. Mummery and Franck Lebrin
    Arteriosclerosis, Thrombosis, and Vascular Biology. 2016;ATVBAHA.115.306719, originally published January 28, 2016
    https://doi.org/10.1161/ATVBAHA.115.306719

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    Interaction Between ALK1 Signaling and Connexin40 in the Development of Arteriovenous Malformations
    Konstantinos Gkatzis, Jérémy Thalgott, Damien Dos-Santos-Luis, Sabrina Martin, Noël Lamandé, Marie France Carette, Frans Disch, Repke J. Snijder, Cornelius J. Westermann, Johannes J. Mager, S. Paul Oh, Lucile Miquerol, Helen M. Arthur, Christine L. Mummery and Franck Lebrin
    Arteriosclerosis, Thrombosis, and Vascular Biology. 2016;ATVBAHA.115.306719, originally published January 28, 2016
    https://doi.org/10.1161/ATVBAHA.115.306719
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