{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,29]],"date-time":"2026-09-29T14:15:52Z","timestamp":1790691352587,"version":"4.1.0"},"reference-count":50,"publisher":"Impact Journals, LLC","issue":"27","content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":["Oncotarget"],"published-print":{"date-parts":[[2017,7,4]]},"DOI":"10.18632\/oncotarget.17267","type":"journal-article","created":{"date-parts":[[2017,5,17]],"date-time":"2017-05-17T20:44:05Z","timestamp":1495053845000},"page":"44732-44748","source":"Crossref","is-referenced-by-count":41,"title":["Catecholamines facilitate VEGF-dependent angiogenesis via \u03b22-adrenoceptor-induced Epac1 and PKA activation"],"prefix":"10.18632","volume":"8","author":[{"given":"Jaspal","family":"Garg","sequence":"first","affiliation":[{"name":"Institute of Experimental and Clinical Pharmacology and Toxicology, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Yu-Xi","family":"Feng","sequence":"additional","affiliation":[{"name":"Institute of Experimental and Clinical Pharmacology and Toxicology, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Sepp R.","family":"Jansen","sequence":"additional","affiliation":[{"name":"Institute of Experimental and Clinical Pharmacology and Toxicology, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Julian","family":"Friedrich","sequence":"additional","affiliation":[{"name":"5th Medical Clinic, University Hospital Mannheim, Heidelberg University, Mannheim, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Frank","family":"Lezoualc'h","sequence":"additional","affiliation":[{"name":"Institute of Cardiovascular and Metabolic Diseases, Inserm UMR-1048, Universit\u00e9 Toulouse -Paul Sabatier, Toulouse, France"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Martina","family":"Schmidt","sequence":"additional","affiliation":[{"name":"Department of Molecular Pharmacology, Center of Pharmacy, University of Groningen, Groningen, The Netherlands"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Thomas","family":"Wieland","sequence":"additional","affiliation":[{"name":"Institute of Experimental and Clinical Pharmacology and Toxicology, Medical Faculty Mannheim, Heidelberg University, Mannheim, Germany"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"7892","published-online":{"date-parts":[[2017,4,20]]},"reference":[{"key":"1","doi-asserted-by":"publisher","first-page":"653","DOI":"10.1038\/nm0603-653","article-title":"Angiogenesis in health and disease","volume":"9","author":"Carmeliet","year":"2003","journal-title":"Nat Med"},{"key":"2","doi-asserted-by":"publisher","first-page":"1909","DOI":"10.1158\/0008-5472.can-11-3406","article-title":"Anti-VEGF\/VEGFR Therapy for Cancer: Reassessing the Target","volume":"72","author":"Dvorak","year":"2012","journal-title":"Cancer Research"},{"key":"3","doi-asserted-by":"publisher","first-page":"1201","DOI":"10.1158\/1078-0432.ccr-11-0641","article-title":"Molecular pathways: beta-adrenergic signaling in cancer","volume":"18","author":"Sood","year":"2012","journal-title":"Clin Cancer Res"},{"key":"4","doi-asserted-by":"publisher","first-page":"1863","DOI":"10.2217\/fon.10.142","article-title":"Impact of stress on cancer metastasis","volume":"6","author":"Sood","year":"2010","journal-title":"Future Oncol"},{"key":"5","doi-asserted-by":"publisher","first-page":"438","DOI":"10.1161\/01.RES.0000088358.99466.04","article-title":"Angiotensin II type 2 receptor inhibits vascular endothelial growth factor-induced migration and in vitro tube formation of human endothelial cells","volume":"93","author":"Wieland","year":"2003","journal-title":"Circ Res"},{"key":"6","doi-asserted-by":"publisher","first-page":"1261","DOI":"10.1016\/j.cellsig.2012.02.005","article-title":"Angiotensin II modulates VEGF-driven angiogenesis by opposing effects of type 1 and type 2 receptor stimulation in the microvascular endothelium","volume":"24","author":"Wieland","year":"2012","journal-title":"Cell Signal"},{"key":"7","doi-asserted-by":"publisher","first-page":"2478","DOI":"10.1016\/j.cellsig.2013.08.017","article-title":"The activation of RhoC in vascular endothelial cells is required for the S1P receptor type 2-induced inhibition of angiogenesis","volume":"25","author":"Wieland","year":"2013","journal-title":"Cell Signal"},{"key":"8","first-page":"1251","article-title":"Characterization of beta-adrenergic receptors in cultured human and bovine endothelial cells","volume":"65","author":"Levine","year":"1985","journal-title":"J Appl Physiol"},{"key":"9","doi-asserted-by":"publisher","first-page":"118","DOI":"10.1111\/j.1549-8719.2010.00072.x","article-title":"Beta-adrenergic stimulation contributes to maintenance of endothelial barrier functions under baseline conditions","volume":"18","author":"Waschke","year":"2011","journal-title":"Microcirculation"},{"key":"10","doi-asserted-by":"publisher","first-page":"103","DOI":"10.1016\/j.preteyeres.2014.06.001","article-title":"The beta-adrenergic system as a possible new target for pharmacologic treatment of neovascular retinal diseases","volume":"42","author":"Bagnoli","year":"2014","journal-title":"Prog Retin Eye Res"},{"key":"11","doi-asserted-by":"publisher","first-page":"27","DOI":"10.1016\/j.exer.2013.03.013","article-title":"Eye drop propranolol administration promotes the recovery of oxygen-induced retinopathy in mice","volume":"111","author":"Bagnoli","year":"2013","journal-title":"Exp Eye Res"},{"key":"12","doi-asserted-by":"publisher","first-page":"1570","DOI":"10.1016\/j.jpeds.2013.07.049","article-title":"Oral propranolol for retinopathy of prematurity: risks, safety concerns, and perspectives","volume":"163","author":"Fortunato","year":"2013","journal-title":"J Pediatr"},{"key":"13","doi-asserted-by":"publisher","first-page":"1317","DOI":"10.1111\/j.1471-4159.2011.07530.x","article-title":"Antiangiogenic effects of beta2 -adrenergic receptor blockade in a mouse model of oxygen-induced retinopathy","volume":"119","author":"Bagnoli","year":"2011","journal-title":"J Neurochem"},{"key":"14","doi-asserted-by":"publisher","first-page":"155","DOI":"10.1167\/iovs.10-5536","article-title":"Role of the adrenergic system in a mouse model of oxygen-induced retinopathy: antiangiogenic effects of beta-adrenoreceptor blockade","volume":"52","author":"Bagnoli","year":"2011","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"15","doi-asserted-by":"publisher","first-page":"765","DOI":"10.1007\/s00418-008-0422-y","article-title":"cAMP induced Rac 1-mediated cytoskeletal reorganization in microvascular endothelium","volume":"129","author":"Waschke","year":"2008","journal-title":"Histochem Cell Biol"},{"key":"16","doi-asserted-by":"publisher","first-page":"4966","DOI":"10.1016\/j.febslet.2005.07.080","article-title":"Epac1 regulates integrity of endothelial cell junctions through VE-cadherin","volume":"579","author":"Bos","year":"2005","journal-title":"FEBS Lett"},{"key":"17","doi-asserted-by":"crossref","first-page":"906","DOI":"10.1016\/j.cellsig.2009.01.038","article-title":"Forskolin increases angiogenesis through the coordinated cross-talk of PKA-dependent VEGF expression and Epac-mediated PI3K\/Akt\/eNOS signaling","volume":"21","author":"Kim","year":"2009","journal-title":"Cell Signal"},{"key":"18","doi-asserted-by":"publisher","first-page":"4592","DOI":"10.1182\/blood-2009-04-217042","article-title":"A novel interplay between Epac\/Rap1 and mitogen-activated protein kinase kinase 5\/extracellular signal-regulated kinase 5 (MEK5\/ERK5) regulates thrombospondin to control angiogenesis","volume":"114","author":"Rosner","year":"2009","journal-title":"Blood"},{"key":"19","doi-asserted-by":"publisher","first-page":"356","DOI":"10.1002\/jcp.24716","article-title":"Beta-Adrenoceptor Activation Reduces Both Dermal Microvascular Endothelial Cell Migration via a cAMP-Dependent Mechanism and Wound Angiogenesis","volume":"230","author":"Pullar","year":"2015","journal-title":"J Cell Physiol"},{"key":"20","first-page":"101","article-title":"Oxygen-induced retinopathy in the mouse","volume":"35","author":"D'Amore","year":"1994","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"21","first-page":"416","article-title":"Oxygen-induced retinopathy: a model for vascular pathology in the retina","volume":"24","author":"Fruttiger","year":"2009","journal-title":"Eye"},{"key":"22","doi-asserted-by":"publisher","first-page":"2813","DOI":"10.1167\/iovs.10-5176","article-title":"The mouse retina as an angiogenesis model","volume":"51","author":"Hellstrom","year":"2010","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"23","doi-asserted-by":"publisher","first-page":"55","DOI":"10.1093\/cvr\/cvu242","article-title":"Exchange protein directly activated by cAMP 1 promotes autophagy during cardiomyocyte hypertrophy","volume":"105","author":"Lezoualc'h","year":"2015","journal-title":"Cardiovasc Res"},{"key":"24","doi-asserted-by":"publisher","first-page":"2181","DOI":"10.1167\/iovs.11-9408","article-title":"Beta-adrenoreceptor agonism influences retinal responses to hypoxia in a model of retinopathy of prematurity","volume":"53","author":"Bagnoli","year":"2012","journal-title":"Invest Ophthalmol Vis Sci"},{"key":"25","doi-asserted-by":"publisher","first-page":"2292","DOI":"10.1161\/ATVBAHA.114.304239","article-title":"Nucleoside diphosphate kinase B regulates angiogenesis through modulation of vascular endothelial growth factor receptor type 2 and endothelial adherens junction proteins","volume":"34","author":"Wieland","year":"2014","journal-title":"Arterioscler Thromb Vasc Biol"},{"key":"26","doi-asserted-by":"publisher","first-page":"4041","DOI":"10.1074\/jbc.M111.319970","article-title":"Induction of Intracellular Calcium Concentration by Environmental Benzo(a)pyrene Involves a \u03b22-Adrenergic Receptor\/Adenylyl Cyclase\/Epac-1\/Inositol 1,4,5-Trisphosphate Pathway in Endothelial Cells","volume":"287","author":"Le Ferrec","year":"2012","journal-title":"Journal of Biological Chemistry"},{"key":"27","doi-asserted-by":"publisher","first-page":"1551","DOI":"10.1158\/1535-7163.mct-07-0428","article-title":"Fasudil-induced hypoxia-inducible factor-1\u03b1 degradation disrupts a hypoxia-driven vascular endothelial growth factor autocrine mechanism in endothelial cells","volume":"7","author":"Kurachi","year":"2008","journal-title":"American Association for Cancer Research"},{"key":"28","doi-asserted-by":"publisher","first-page":"54","DOI":"10.1016\/j.ejphar.2006.09.048","article-title":"Effect of norepinephrine on RhoA, MAP kinase, proliferation and VEGF expression in human umbilical vein endothelial cells","volume":"553","author":"Takekoshi","year":"2006","journal-title":"European Journal of Pharmacology"},{"key":"29","doi-asserted-by":"crossref","first-page":"32521","DOI":"10.1074\/jbc.272.51.32521","article-title":"The vascular endothelial growth factor receptor KDR activates multiple signal transduction pathways in porcine aortic endothelial cells","volume":"272","author":"Waltenberger","year":"1997","journal-title":"J Biol Chem"},{"key":"30","doi-asserted-by":"crossref","first-page":"1","DOI":"10.3109\/15419060109080703","article-title":"Rac regulates vascular endothelial growth factor stimulated motility","volume":"8","author":"Hruska","year":"2001","journal-title":"Cell Commun Adhes"},{"key":"31","doi-asserted-by":"publisher","first-page":"863","DOI":"10.1111\/j.1600-0625.2009.00867.x","article-title":"Inhibition of Rac1 GTPase downregulates vascular endothelial growth factor receptor-2 expression by suppressing Sp1-dependent DNA binding in human endothelial cells","volume":"18","author":"Gille","year":"2009","journal-title":"Exp Dermatol"},{"key":"32","doi-asserted-by":"publisher","DOI":"10.14814\/phy2.12175","article-title":"cAMP controls the restoration of endothelial barrier function after thrombin-induced hyperpermeability via Rac1 activation","volume":"2","author":"Gunduz","year":"2014","journal-title":"Physiol Rep"},{"key":"33","doi-asserted-by":"publisher","first-page":"24713","DOI":"10.1074\/jbc.M111.321976","article-title":"The Epac-Rap1 signaling pathway controls cAMP-mediated exocytosis of Weibel-Palade bodies in endothelial cells","volume":"287","author":"Bierings","year":"2012","journal-title":"J Biol Chem"},{"key":"34","doi-asserted-by":"crossref","first-page":"23","DOI":"10.1177\/229255031302100103","article-title":"Beta-blockers for the treatment of problematic hemangiomas","volume":"21","author":"Harrop","year":"2013","journal-title":"Can J Plast Surg"},{"key":"35","doi-asserted-by":"publisher","first-page":"499","DOI":"10.1515\/jpm-2015-0357","article-title":"Oral propranolol in early stages of retinopathy of prematurity","volume":"44","author":"Pena","year":"2016","journal-title":"J Perinat Med"},{"key":"36","doi-asserted-by":"publisher","first-page":"545","DOI":"10.1161\/ATVBAHA.115.307011","article-title":"Induction of Angiogenesis by a Type III Phosphodiesterase Inhibitor, Cilostazol, Through Activation of Peroxisome Proliferator-Activated Receptor-gamma and cAMP Pathways in Vascular Cells","volume":"36","author":"Morishita","year":"2016","journal-title":"Arterioscler Thromb Vasc Biol"},{"key":"37","doi-asserted-by":"publisher","first-page":"34871","DOI":"10.1074\/jbc.M114.571000","article-title":"GPR126 protein regulates developmental and pathological angiogenesis through modulation of VEGFR2 receptor signaling","volume":"289","author":"Liu","year":"2014","journal-title":"J Biol Chem"},{"key":"38","doi-asserted-by":"publisher","first-page":"443","DOI":"10.1016\/j.bbrc.2013.09.107","article-title":"The (R)-enantiomer of CE3F4 is a preferential inhibitor of human exchange protein directly activated by cyclic AMP isoform 1 (Epac1)","volume":"440","author":"Blondeau","year":"2013","journal-title":"Biochem Biophys Res Commun"},{"key":"39","doi-asserted-by":"publisher","first-page":"9344","DOI":"10.1038\/srep09344","article-title":"Biochemical and pharmacological characterizations of ESI-09 based EPAC inhibitors: defining the ESI-09 \u201ctherapeutic window\u201d","volume":"5","author":"Cheng","year":"2015","journal-title":"Sci Rep"},{"key":"40","doi-asserted-by":"publisher","first-page":"2744","DOI":"10.1002\/ijc.21723","article-title":"The norepinephrine-driven metastasis development of PC-3 human prostate cancer cells in BALB\/c nude mice is inhibited by beta-blockers","volume":"118","author":"Entschladen","year":"2006","journal-title":"Int J Cancer"},{"key":"41","doi-asserted-by":"publisher","first-page":"939","DOI":"10.1038\/nm1447","article-title":"Chronic stress promotes tumor growth and angiogenesis in a mouse model of ovarian carcinoma","volume":"12","author":"Mangala","year":"2006","journal-title":"Nat Med"},{"key":"42","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/S0169-5002(00)00168-9","article-title":"Prostaglandin E2 and vasoactive intestinal peptide increase vascular endothelial cell growth factor mRNAs in lung cancer cells","volume":"31","author":"Moody","year":"2001","journal-title":"Lung Cancer"},{"key":"43","doi-asserted-by":"publisher","first-page":"46354","DOI":"10.18632\/oncotarget.10128","article-title":"Epac1 links prostaglandin E2 to beta-catenin-dependent transcription during epithelial-to-mesenchymal transition","volume":"7","author":"Schmidt","year":"2016","journal-title":"Oncotarget"},{"key":"44","doi-asserted-by":"publisher","first-page":"1312","DOI":"10.1093\/annonc\/mds616","article-title":"Improved survival outcomes with the incidental use of beta-blockers among patients with non-small-cell lung cancer treated with definitive radiation therapy","volume":"24","author":"Gomez","year":"2013","journal-title":"Ann Oncol"},{"key":"45","doi-asserted-by":"publisher","first-page":"2635","DOI":"10.1200\/JCO.2010.33.5422","article-title":"Beta blockers and breast cancer mortality: a population- based study","volume":"29","author":"Visvanathan","year":"2011","journal-title":"J Clin Oncol"},{"key":"46","doi-asserted-by":"publisher","first-page":"1768","DOI":"10.2353\/ajpath.2009.090171","article-title":"Vascular permeability and pathological angiogenesis in caveolin-1-null mice","volume":"175","author":"Dvorak","year":"2009","journal-title":"Am J Pathol"},{"key":"47","doi-asserted-by":"publisher","first-page":"481","DOI":"10.1038\/nprot.2007.54","article-title":"A protocol for isolation and culture of human umbilical vein endothelial cells","volume":"2","author":"Vaubourdolle","year":"2007","journal-title":"Nat Protoc"},{"key":"48","doi-asserted-by":"publisher","first-page":"670","DOI":"10.1124\/pr.110.003707","article-title":"Exchange protein directly activated by cAMP (epac): a multidomain cAMP mediator in the regulation of diverse biological functions","volume":"65","author":"Maarsingh","year":"2013","journal-title":"Pharmacol Rev"},{"key":"49","doi-asserted-by":"crossref","first-page":"1341","DOI":"10.1083\/jcb.143.5.1341","article-title":"Integration of endothelial cells in multicellular spheroids prevents apoptosis and induces differentiation","volume":"143","author":"Augustin","year":"1998","journal-title":"J Cell Biol"},{"key":"50","doi-asserted-by":"crossref","first-page":"329","DOI":"10.1038\/nprot.2007.30","article-title":"In vitro scratch assay: a convenient and inexpensive method for analysis of cell migration in vitro","volume":"2","author":"Guan","year":"2007","journal-title":"Nat Protocols"}],"container-title":["Oncotarget"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/www.oncotarget.com\/lookup\/doi\/10.18632\/oncotarget.17267","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2020,8,6]],"date-time":"2020-08-06T15:14:42Z","timestamp":1596726882000},"score":1,"resource":{"primary":{"URL":"https:\/\/www.oncotarget.com\/lookup\/doi\/10.18632\/oncotarget.17267"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2017,4,20]]},"references-count":50,"journal-issue":{"issue":"27","published-print":{"date-parts":[[2017,7,4]]}},"alternative-id":["17267","28512254"],"URL":"https:\/\/doi.org\/10.18632\/oncotarget.17267","relation":{},"ISSN":["1949-2553"],"issn-type":[{"value":"1949-2553","type":"electronic"}],"subject":[],"published":{"date-parts":[[2017,4,20]]}}}