Targeting connexin37 alters angiogenesis and arteriovenous differentiation in the developing mouse retina.
Animals
Cell Differentiation
/ physiology
Cell Proliferation
/ physiology
Cells, Cultured
Connexins
/ metabolism
Endothelial Cells
/ metabolism
Endothelium, Vascular
/ metabolism
Female
Human Umbilical Vein Endothelial Cells
Humans
Male
Mice
Mice, Inbred C57BL
Neovascularization, Physiologic
/ physiology
Retina
/ metabolism
Signal Transduction
/ physiology
Gap Junction alpha-4 Protein
angiogenesis
connexin37
retina
vascular remodeling
Journal
FASEB journal : official publication of the Federation of American Societies for Experimental Biology
ISSN: 1530-6860
Titre abrégé: FASEB J
Pays: United States
ID NLM: 8804484
Informations de publication
Date de publication:
06 2020
06 2020
Historique:
received:
03
02
2020
revised:
20
03
2020
accepted:
06
04
2020
pubmed:
24
4
2020
medline:
16
1
2021
entrez:
24
4
2020
Statut:
ppublish
Résumé
Connexin37 (Cx37) forms intercellular channels between endothelial cells (EC), and contributes to coordinate the motor tone of vessels. We investigated the contribution of this protein during physiological angiogenesis. We show that, compared to WT littermates, mice lacking Cx37 (Cx37
Identifiants
pubmed: 32323401
doi: 10.1096/fj.202000257R
doi:
Substances chimiques
Connexins
0
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
8234-8249Informations de copyright
© 2020 Federation of American Societies for Experimental Biology.
Références
Chung AS, Ferrara N. Developmental and pathological angiogenesis. Annu Rev Cell Dev Biol. 2011;27:563-584.
Tahergorabi Z, Khazaei M. Imbalance of angiogenesis in diabetic complications: the mechanisms. Int J Prev Med. 2012;3:827-838.
Nohata N, Uchida Y, Stratman AN, et al. Temporal-specific roles of Rac1 during vascular development and retinal angiogenesis. Dev Biol. 2016;411:183-194.
Campochiaro PA. Molecular pathogenesis of retinal and choroidal vascular diseases. Prog Retin Eye Res. 2015;49:67-81.
Cabral T, Mello LGM, Lima LH, et al. Retinal and choroidal angiogenesis: a review of new targets. Int J Retina Vitreous. 2017;3:1-13.
Phng LK, Gerhardt H. Angiogenesis: a team effort coordinated by notch. Dev Cell. 2009;16:196-208.
Hellstrom M, Phng LK, Gerhardt H. VEGF and Notch signaling: the yin and yang of angiogenic sprouting. Cell Adh Migr. 2007;1:133-136.
Armulik A, Abramsson A, Betsholtz C. Endothelial/pericyte interactions. Circ Res. 2005;97:512-523.
Cuervo H, Pereira B, Nadeem T, et al. PDGFRbeta-P2A-CreER(T2) mice: a genetic tool to target pericytes in angiogenesis. Angiogenesis. 2017;20:655-662.
Shawber CJ, Kitajewski J. Notch function in the vasculature: insights from zebrafish, mouse and man. BioEssays. 2004;26:225-234.
Bosco D, Haefliger JA, Meda P. Connexins: key mediators of endocrine function. Physiol Rev. 2011;91:1393-1445.
Hamelin R, Allagnat F, Haefliger JA, Meda P. Connexins, diabetes and the metabolic syndrome. Curr Protein Pept Sci. 2009;10:18-29.
Meens MJ, Kwak BR, Duffy HS. Role of connexins and pannexins in cardiovascular physiology. Cell Mol Life Sci. 2015;72:2779-2792.
Meda P, Haefliger JA. Connexins and pannexins: from biology towards clinical targets. Swiss Med Wkly. 2016;146:w14365.
Simon AM, Goodenough DA, Li E, Paul DL. Female infertility in mice lacking connexin 37. Nature. 1997;385:525-529.
Meens MJ, Alonso F, Le Gal L, Kwak BR, Haefliger JA. Endothelial connexin37 and connexin40 participate in basal but not agonist-induced NO release. Cell Commun Signal. 2015;13:1-11.
Allagnat F, Dubuis C, Lambelet M, et al. Connexin37 reduces smooth muscle cell proliferation and intimal hyperplasia in a mouse model of carotid artery ligation. Cardiovasc Res. 2017;113:805-816.
Stahl A, Connor KM, Sapieha P, et al. The mouse retina as an angiogenesis model. Invest Ophthalmol Vis Sci. 2010;51:2813-2826.
Crist AM, Young C, Meadows SM. Characterization of arteriovenous identity in the developing neonate mouse retina. Gene Expr Patterns. 2017;23-24:22-31.
Scheppke L, Murphy EA, Zarpellon A, et al. Notch promotes vascular maturation by inducing integrin-mediated smooth muscle cell adhesion to the endothelial basement membrane. Blood. 2012;119:2149-2158.
Ehling M, Adams S, Benedito R, Adams RH. Notch controls retinal blood vessel maturation and quiescence. Development. 2013;140:3051-3061.
Pitulescu ME, Schmidt I, Benedito R, Adams RH. Inducible gene targeting in the neonatal vasculature and analysis of retinal angiogenesis in mice. Nat Protoc. 2010;5:1518-1534.
Haefliger JA, Allagnat F, Hamard L, et al. Targeting Cx40 (CONNexin40) expression or function reduces angiogenesis in the developing mouse retina. Arterioscler Thromb Vasc Biol. 2017;37:2136-2146.
Benton RL, Maddie MA, Minnillo DR, Hagg T, Whittemore SR. Griffonia simplicifolia isolectin B4 identifies a specific subpopulation of angiogenic blood vessels following contusive spinal cord injury in the adult mouse. J Comp Neurol. 2008;507:1031-1052.
Simon AM, Chen H, Jackson CL. Cx37 and Cx43 localize to zona pellucida in mouse ovarian follicles. Cell Commun Adhes. 2006;13:61-77.
Fang JS, Coon BG, Gillis N, et al. Shear-induced Notch-Cx37-p27 axis arrests endothelial cell cycle to enable arterial specification. Nat Commun. 2017;8:1-14.
Sakabe M, Fan J, Odaka Y, et al. YAP/TAZ-CDC42 signaling regulates vascular tip cell migration. Proc Natl Acad Sci U S A. 2017;114:10918-10923.
Le Gal L, Pellegrin M, Santoro T, et al. Connexin37-dependent mechanisms selectively contribute to modulate Angiotensin II-mediated hypertension. J Am Heart Assoc. 2019;8:e010823.
Peghaire C, Dufton NP, Lang M, et al. The transcription factor ERG regulates a low shear stress-induced anti-thrombotic pathway in the microvasculature. Nat Commun. 2019;10:1-17.
Kalna V, Yang Y, Peghaire CR, et al. The transcription factor ERG regulates super-enhancers associated with an endothelial-specific gene expression program. Circ Res. 2019;124:1337-1349.
Sarrazin S, Adam E, Lyon M, et al. Endocan or endothelial cell specific molecule-1 (ESM-1): a potential novel endothelial cell marker and a new target for cancer therapy. Biochim Biophys Acta. 2006;1765:25-37.
Yang D, Jin C, Ma H, et al. EphrinB2/EphB4 pathway in postnatal angiogenesis: a potential therapeutic target for ischemic cardiovascular disease. Angiogenesis. 2016;19:297-309.
Le Gal L, Alonso F, Mazzolai L, Meda P, Haefliger JA. Interplay between connexin40 and nitric oxide signaling during hypertension. Hypertension. 2015;65:910-915.
Le Gal L, Alonso F, Wagner C, et al. Restoration of connexin 40 (Cx40) in renin-producing cells reduces the hypertension of Cx40 null mice. Hypertension. 2014;63:1198-1204.
Fang JS, Coon BG, Gillis N, et al. Addendum: shear-induced Notch-Cx37-p27 axis arrests endothelial cell cycle to enable arterial specification. Nat Commun. 2018;9:1.
Li Z, Zhang S, Cao L, et al. Tanshinone IIA and Astragaloside IV promote the angiogenesis of mesenchymal stem cell-derived endothelial cell-like cells via upregulation of Cx37, Cx40 and Cx43. Exp Ther Med. 2018;15:1847-1854.
Ivanova E, Kovacs-Oller T, Sagdullaev BT. Domain-specific distribution of gap junctions defines cellular coupling to establish a vascular relay in the retina. J Compar Neurol. 2019;527:2675-2693.
Okamoto T, Usuda H, Tanaka T, Wada K, Shimaoka M. The functional implications of endothelial gap junctions and cellular mechanics in vascular angiogenesis. Cancers. 2019;11:237.
Fang JS, Angelov SN, Simon AM, Burt JM. Cx37 deletion enhances vascular growth and facilitates ischemic limb recovery. Am J Physiol Heart Circ Physiol. 2011;301:H1872-H1881.
Fang JS, Angelov SN, Simon AM, Burt JM. Cx40 is required for, and cx37 limits, postischemic hindlimb perfusion, survival and recovery. J Vasc Res. 2012;49:2-12.
Selbonne S, Francois D, Raoul W, et al. Protease nexin-1 regulates retinal vascular development. Cell Mol Life Sci. 2015;72:3999-4011.
Weinl C, Wasylyk C, Garcia Garrido M, et al. Elk3 deficiency causes transient impairment in post-natal retinal vascular development and formation of tortuous arteries in adult murine retinae. PLoS ONE. 2014;9:e107048.
Dhein S, Gaertner C, Georgieff C, Salameh A, Schlegel F, Mohr FW. Effects of isoprenaline on endothelial connexins and angiogenesis in a human endothelial cell culture system. Naunyn Schmiedebergs Arch Pharmacol. 2015;388:101-108.
Gartner C, Ziegelhoffer B, Kostelka M, Stepan H, Mohr FW, Dhein S. Knock-down of endothelial connexins impairs angiogenesis. Pharmacol Res. 2012;65:347-357.
Burt JM, Nelson TK, Simon AM, Fang JS. Connexin 37 profoundly slows cell cycle progression in rat insulinoma cells. Am J Physiol Cell Physiol. 2008;295:C1103-C1112.
Simon AM, McWhorter AR. Vascular abnormalities in mice lacking the endothelial gap junction proteins connexin37 and connexin40. Dev Biol. 2002;251:206-220.
Pfenniger A, Derouette JP, Verma V, et al. Gap junction protein Cx37 interacts with endothelial nitric oxide synthase in endothelial cells. Arterioscler Thromb Vasc Biol. 2010;30:827-834.
Alonso F, Boittin FX, Beny JL, Haefliger JA. Loss of connexin40 is associated with decreased endothelium-dependent relaxations and eNOS levels in the mouse aorta. Am J Physiol Heart Circ Physiol. 2010;299:H1365-H1373.
Alonso F, Krattinger N, Mazzolai L, et al. An angiotensin II- and NF-kappaB-dependent mechanism increases connexin 43 in murine arteries targeted by renin-dependent hypertension. Cardiovasc Res. 2010;87:166-176.
Alonso F, Domingos-Pereira S, Le Gal L, et al. Targeting endothelial connexin40 inhibits tumor growth by reducing angiogenesis and improving vessel perfusion. Oncotarget. 2016;7:14015-14028.
Slavi N, Toychiev AH, Kosmidis S, et al. Suppression of connexin 43 phosphorylation promotes astrocyte survival and vascular regeneration in proliferative retinopathy. Proc Natl Acad Sci U S A. 2018;115:E5934-E5943.
Park HJ, Zhang Y, Georgescu SP, Johnson KL, Kong D, Galper JB. Human umbilical vein endothelial cells and human dermal microvascular endothelial cells offer new insights into the relationship between lipid metabolism and angiogenesis. Stem Cell Rev. 2006;2:93-102.
Cossutta M, Darche M, Carpentier G, et al. Weibel-Palade bodies orchestrate pericytes during angiogenesis. Arterioscler Thromb Vasc Biol. 2019;39:1843-1858.
Gaengel K, Genove G, Armulik A, Betsholtz C. Endothelial-mural cell signaling in vascular development and angiogenesis. Arterioscler Thromb Vasc Biol. 2009;29:630-638.
Cai J, Kehoe O, Smith GM, Hykin P, Boulton ME. The angiopoietin/Tie-2 system regulates pericyte survival and recruitment in diabetic retinopathy. Invest Ophthalmol Vis Sci. 2008;49:2163-2171.
Meda P. Gap junction proteins are key drivers of endocrine function. Biochim Biophys Acta. 2018;1860:124-140.
Gridley T. Notch signaling in vascular development and physiology. Development. 2007;134:2709-2718.
Hellstrom M, Phng LK, Hofmann JJ, et al. Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature. 2007;445:776-780.
Kuijper S, Turner CJ, Adams RH. Regulation of angiogenesis by Eph-ephrin interactions. Trends Cardiovasc Med. 2007;17:145-151.
Lackmann M, Boyd AW. Eph, a protein family coming of age: more confusion, insight, or complexity? Sci Signal. 2008;1:re2.
Klein R. Eph/ephrin signalling during development. Development. 2012;139:4105-4109.
Wolf K, Hu H, Isaji T, Dardik A. Molecular identity of arteries, veins, and lymphatics. J Vasc Surg. 2019;69:253-262.