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Consensus guidelines for the use and interpretation of angiogenesis assays
Patrycja Nowak-Sliwinska, Kari Alitalo, Elizabeth Allen and 83 more
Angiogenesis · 2018 · Review
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Stainier DY, Fouquet B, Chen JN, Warren KS, Weinstein BM, Meiler SE, Mohideen MA, Neuhauss SC, Solnica-Krezel L, Schier AF, Zwartkruis F, Stemple DL, Malicki J, Driever W, Fishman MC. Mutations affecting the formation and function of the cardiovascular system in the zebrafish embryo. Development. 1996;123:285-292.
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Lawson ND, Scheer N, Pham VN, Kim CH, Chitnis AB, Campos-Ortega JA, Weinstein BM. Notch signaling is required for arterial-venous differentiation during embryonic vascular development. Development. 2001;128(19):3675-3683.
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Roman BL, Pham VN, Lawson ND, Kulik M, Childs S, Lekven AC, Garrity DM, Moon RT, Fishman MC, Lechleider RJ, Weinstein BM. Disruption of acvrl1 increases endothelial cell number in zebrafish cranial vessels. Development. 2002;129(12):3009-3019.
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Lawson ND, Mugford JW, Diamond BA, Weinstein BM. Phospholipase C gamma-1 is required downstream of vascular endothelial growth factor during arterial development. Genes Dev. 2003;17(11):1346-1351.
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Torres-Vazquez J, Gitler AD, Fraser SD, Berk JD, Van NP, Fishman MC, Childs S, Epstein JA, Weinstein BM. Semaphorin-plexin signaling guides patterning of the developing vasculature. Dev Cell. 2004;7(1):117-123.
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Shaw KM, Castranova DA, Pham VN, Kamei M, Kidd KR, Lo BD, Torres-Vasquez J, Ruby A, Weinstein BM. Fused-somites-like mutants exhibit defects in trunk vessel patterning. Dev Dyn. 2006;235(7):1753-1760.
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Pham VN, Lawson ND, Mugford JW, Dye L, Castranova D, Lo B, Weinstein BM. Combinatorial function of ETS transcription factors in the developing vasculature. Dev Biol. 2007;303(2):772-783.
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Gore AV, Swift MR, Cha YR, Lo B, McKinney MC, Li W, Castranova D, Davis A, Mukouyama YS, Weinstein BM. Rspo1/Wnt signaling promotes angiogenesis via Vegfc/Vegfr3. Development. 2011;138(22):4875-4886.
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Pan W, Pham VN, Stratman AN, Castranova D, Kamei M, Kidd KR, Lo BD, Shaw KM, Torres-Vazquez J, Mikelis CM, Gutkind JS, Davis GE, Weinstein BM. CDP-diacylglycerol synthetase-controlled phosphoinositide availability limits VEGFA signaling and vascular morphogenesis. Blood. 2012;120(2):489-498.
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Moens CB, Donn TM, Wolf-Saxon ER, Ma TP. Reverse genetics in zebrafish by TILLING. Brief Funct Genom Proteom. 2008;7(6):454-459.
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Varshney GK, Carrington B, Pei W, Bishop K, Chen Z, Fan C, Xu L, Jones M, LaFave MC, Ledin J, Sood R, Burgess SM. A high-throughput functional genomics workflow based on CRISPR/Cas9-mediated targeted mutagenesis in zebrafish. Nat Protoc. 2016;11(12):2357-2375.
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Won M, Ro H, Dawid IB. Lnx2 ubiquitin ligase is essential for exocrine cell differentiation in the early zebrafish pancreas. Proc Natl Acad Sci USA. 2015;112(40):12426-12431.
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Cha YR, Weinstein BM. Use of PCR template-derived probes prevents off-target whole mount in situ hybridization in transgenic zebrafish. Zebrafish. 2012;9(2):85-89.
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Hogan BM, Bos FL, Bussmann J, Witte M, Chi NC, Duckers HJ, Schulte-Merker S. Ccbe1 is required for embryonic lymphangiogenesis and venous sprouting. Nat Genet. 2009;41(4):396-398.
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Le Guen L, Karpanen T, Schulte D, Harris NC, Koltowska K, Roukens G, Bower NI, van Impel A, Stacker SA, Achen MG, Schulte-Merker S, Hogan BM. Ccbe1 regulates Vegfc-mediated induction of Vegfr3 signaling during embryonic lymphangiogenesis. Development. 2014;141(6):1239-1249.
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Villefranc JA, Nicoli S, Bentley K, Jeltsch M, Zarkada G, Moore JC, Gerhardt H, Alitalo K, Lawson ND. A truncation allele in vascular endothelial growth factor c reveals distinct modes of signaling during lymphatic and vascular development. Development. 2013;140(7):1497-1506.
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Yaniv K, Isogai S, Castranova D, Dye L, Hitomi J, Weinstein BM. Live imaging of lymphatic development in the zebrafish. Nat Med. 2006;12(6):711-716.
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Isogai S, Hitomi J, Yaniv K, Weinstein BM. Zebrafish as a new animal model to study lymphangiogenesis. Anat Sci Int. 2009;84(3):102-111.
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Jung HM, Castranova D, Swift MR, Pham VN, Venero Galanternik MV, Isogai S, Butler MG, Mulligan TS, Weinstein BM. Development of the larval lymphatic system in the zebrafish. Development. 2017.
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Poelma C, Kloosterman A, Hierck BP, Westerweel J. Accurate blood flow measurements: are artificial tracers necessary? PLoS ONE. 2012;7(9):e45247.
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Vennemann P, Kiger KT, Lindken R, Groenendijk BC, Stekelenburg-de Vos S, ten Hagen TL, Ursem NT, Poelmann RE, Westerweel J, Hierck BP. In vivo micro particle image velocimetry measurements of blood-plasma in the embryonic avian heart. J Biomech. 2006;39(7):1191-1200.
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Zhou J, Zhang H, Wang H, Lutz AM, El Kaffas A, Tian L, Hristov D, Willmann JK. Early prediction of tumor response to bevacizumab treatment in murine colon cancer models using three-dimensional dynamic contrast-enhanced ultrasound imaging. Angiogenesis. 2017;20(4):547-555.
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Kwan KM, Fujimoto E, Grabher C, Mangum BD, Hardy ME, Campbell DS, Parant JM, Yost HJ, Kanki JP, Chien CB. The Tol2kit: a multisite gateway-based construction kit for Tol2 transposon transgenesis constructs. Dev Dyn. 2007;236(11):3088-3099.
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Kamei M, Isogai S, Pan W, Weinstein BM. Imaging blood vessels in the zebrafish. Methods Cell Biol. 2010;100:27-54.
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Isogai S, Horiguchi M, Weinstein BM. The vascular anatomy of the developing zebrafish: an atlas of embryonic and early larval development. Dev Biol. 2001;230(2):278-301.
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Lawson ND, Weinstein BM. In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol. 2002;248(2):307-318.
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Stratman AN, Pezoa SA, Farrelly OM, Castranova D, Dye LE, Butler MG, Sidik H, Talbot WS, Weinstein BM. Interactions between mural cells and endothelial cells stabilize the developing zebrafish dorsal aorta. Development. 2017;144(1):115-127.
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Choi WY, Gemberling M, Wang J, Holdway JE, Shen MC, Karlstrom RO, Poss KD. In vivo monitoring of cardiomyocyte proliferation to identify chemical modifiers of heart regeneration. Development. 2013;140(3):660-666.
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Jung HM, Isogai S, Kamei M, Castranova D, Gore AV, Weinstein BM. Imaging blood vessels and lymphatic vessels in the zebrafish. Methods Cell Biol. 2016;133:69-103.
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van Rooijen E, Voest EE, Logister I, Bussmann J, Korving J, van Eeden FJ, Giles RH, Schulte-Merker S. von Hippel–Lindau tumor suppressor mutants faithfully model pathological hypoxia-driven angiogenesis and vascular retinopathies in zebrafish. Dis Model Mech. 2010;3(5–6):343-353.
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Ribatti D, Nico B, Vacca A, Roncali L, Burri PH, Djonov V. Chorioallantoic membrane capillary bed: a useful target for studying angiogenesis and anti-angiogenesis in vivo. Anat Rec. 2001;264(4):317-324.
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Ribatti D, Vacca A, Roncali L, Dammacco F. The chick embryo chorioallantoic membrane as a model for in vivo research on anti-angiogenesis. Curr Pharm Biotechnol. 2000;1(1):73-82.
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Adar Y, Stark M, Bram EE, Nowak-Sliwinska P, van den Bergh H, Szewczyk G, Sarna T, Skladanowski A, Griffioen AW, Assaraf YG. Imidazoacridinone-dependent lysosomal photodestruction: a pharmacological Trojan horse approach to eradicate multidrug-resistant cancers. Cell Death Dis. 2012;3:1-10.
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Valdes TI, Klueh U, Kreutzer D, Moussy F. Ex ova chick chorioallantoic membrane as a novel in vivo model for testing biosensors. J Biomed Mater Res Part A. 2003;67(1):215-223.
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Valdes TI, Kreutzer D, Moussy F. The chick chorioallantoic membrane as a novel in vivo model for the testing of biomaterials. J Biomed Mater Res. 2002;62(2):273-282.
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Weiss A, Bonvin D, Berndsen RH, Scherrer E, Wong TJ, Dyson PJ, Griffioen AW, Nowak-Sliwinska P. Angiostatic treatment prior to chemo- or photodynamic therapy improves anti-tumor efficacy. Sci Rep. 2015;5:8990.
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Lim SH, Nowak-Sliwinska P, Kamarulzaman FA, van den Bergh H, Wagnieres G, Lee HB. The neovessel occlusion efficacy of 15-hydroxypurpurin-7-lactone dimethyl ester induced with photodynamic therapy. Photochem Photobiol. 2010;86(2):397-402.
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West DC, Thompson WD, Sells PG, Burbridge MF. Angiogenesis assays using chick chorioallantoic membrane. Methods Mol Med. 2001;46:107-129.
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Dohle DS, Pasa SD, Gustmann S, Laub M, Wissler JH, Jennissen HP, Dunker N. Chick ex ovo culture and ex ovo CAM assay: how it really works. J Vis Exp. 2009.
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Nowak-Sliwinska P, Ballini JP, Wagnieres G, van den Bergh H. Processing of fluorescence angiograms for the quantification of vascular effects induced by anti-angiogenic agents in the CAM model. Microvasc Res. 2010;79(1):21-28.
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Cimpean AM, Seclaman E, Ceausu R, Gaje P, Feflea S, Anghel A, Raica M, Ribatti D. VEGF-A/HGF induce Prox-1 expression in the chick embryo chorioallantoic membrane lymphatic vasculature. Clin Exp Med. 2010;10(3):169-172.
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Clavel CM, Paunescu E, Nowak-Sliwinska P, Griffioen AW, Scopelliti R, Dyson PJ. Discovery of a highly tumor-selective organometallic ruthenium(II)-arene complex. J Med Chem. 2014;57(8):3546-3558.
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Nowak-Sliwinska P, Wagnieres G, van den Bergh H, Griffioen AW. Angiostasis-induced vascular normalization can improve photodynamic therapy. Cell Mol Life Sci. 2010;67(9):1559-1560.
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Kilarski WW, Petersson L, Fuchs PF, Zielinski MS, Gerwins P. An in vivo neovascularization assay for screening regulators of angiogenesis and assessing their effects on pre-existing vessels. Angiogenesis. 2012;15(4):643-655.
Not in our library10.1007/s10456-012-9287-8
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Weiss A, van Beijnum JR, Bonvin D, Jichlinski P, Dyson PJ, Griffioen AW, Nowak-Sliwinska P. Low-dose angiostatic tyrosine kinase inhibitors improve photodynamic therapy for cancer: lack of vascular normalization. J Cell Mol Med. 2014;18:480-491.
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Hagedorn M, Javerzat S, Gilges D, Meyre A, de Lafarge B, Eichmann A, Bikfalvi A. Accessing key steps of human tumor progression in vivo by using an avian embryo model. Proc Natl Acad Sci USA. 2005;102(5):1643-1648.
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Dumartin L, Quemener C, Laklai H, Herbert J, Bicknell R, Bousquet C, Pyronnet S, Castronovo V, Schilling MK, Bikfalvi A, Hagedorn M. Netrin-1 mediates early events in pancreatic adenocarcinoma progression, acting on tumor and endothelial cells. Gastroenterology. 2010.
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Palmer TD, Lewis J, Zijlstra A. Quantitative analysis of cancer metastasis using an avian embryo model. J Vis Exp. 2011.
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Herbert JM, Stekel DJ, Mura M, Sychev M, Bicknell R. Bioinformatic methods for finding differentially expressed genes in cDNA libraries, applied to the identification of tumour vascular targets. Methods Mol Biol. 2011;729:99-119.
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Soulet F, Kilarski WW, Roux-Dalvai F, Herbert JM, Sacewicz I, Mouton-Barbosa E, Bicknell R, Lalor P, Monsarrat B, Bikfalvi A. Mapping the extracellular and membrane proteome associated with the vasculature and the stroma in the embryo. Mol Cell Proteom MCP. 2013;12(8):2293-2312.
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Kilarski WW, Herbert J, Bikfalvi A. Methods for mapping the extracellular and membrane proteome in the avian embryo, and identification of putative vascular targets or endothelial genes. Methods Mol Biol. 2018;1722:31-56.
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Sequence and comparative analysis of the chicken genome provide unique perspectives on vertebrate evolution. Nature. 2004;432(7018):695-716.
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Arora R, Papaioannou VE. The murine allantois: a model system for the study of blood vessel formation. Blood. 2012;120(13):2562-2572.
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Downs KM, Temkin R, Gifford S, McHugh J. Study of the murine allantois by allantoic explants. Dev Biol. 2001;233(2):347-364.
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Crosby CV, Fleming PA, Argraves WS, Corada M, Zanetta L, Dejana E, Drake CJ. VE-cadherin is not required for the formation of nascent blood vessels but acts to prevent their disassembly. Blood. 2005;105(7):2771-2776.
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Perryn ED, Czirok A, Little CD. Vascular sprout formation entails tissue deformations and VE-cadherin-dependent cell-autonomous motility. Dev Biol. 2008;313(2):545-555.
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Winderlich M, Keller L, Cagna G, Broermann A, Kamenyeva O, Kiefer F, Deutsch U, Nottebaum AF, Vestweber D. VE-PTP controls blood vessel development by balancing Tie-2 activity. J Cell Biol. 2009;185(4):657-671.
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Argraves KM, Wilkerson BA, Argraves WS. Sphingo-sine-1-phosphate signaling in vasculogenesis and angiogenesis. World J Biol Chem. 2010;1(10):291-297.
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Downs KM. In vitro methods for studying vascularization of the murine allantois and allantoic union with the chorion. Methods Mol Med. 2006;121:241-272.
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Downs KM, Gardner RL. An investigation into early placental ontogeny: allantoic attachment to the chorion is selective and developmentally regulated. Development. 1995;121(2):407-416.
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Gentile C, Fleming PA, Mironov V, Argraves KM, Argraves WS, Drake CJ. VEGF-mediated fusion in the generation of uniluminal vascular spheroids. Dev Dyn. 2008;237(10):2918-2925.
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Arora R, del Alcazar CM, Morrisey EE, Naiche LA, Papaioannou VE. Candidate gene approach identifies multiple genes and signaling pathways downstream of Tbx4 in the developing allantois. PLoS ONE. 2012;7(8):e43581.
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Gambardella L, Hemberger M, Hughes B, Zudaire E, Andrews S, Vermeren S. PI3 K signaling through the dual GTPase-activating protein ARAP3 is essential for developmental angiogenesis. Sci Signal. 2010;3(145):ra76.
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Passaniti A, Taylor RM, Pili R, Guo Y, Long PV, Haney JA, Pauly RR, Grant DS, Martin GR. A simple, quantitative method for assessing angiogenesis and antiangiogenic agents using reconstituted basement membrane, heparin, and fibroblast growth factor. Lab Investig J Tech Methods Pathol. 1992;67(4):519-528.
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Malinda KM. In vivo matrigel migration and angiogenesis assay. Methods Mol Biol. 2009;467:287-294.
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Kibbey MC, Corcoran MC, Wahl LM, Kleinman HK. Laminin SIKVAV peptide induced angiogeneses in vivo is potentiated by neutrophils. J Cell Physiol. 1994;160:185-193.
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Salcedo R, Ponce ML, Young HA, Wasserman K, Ward JM, Kleinman HK, Oppenheim JJ, Murphy WJ. Human endothelial cells express CCR2 and respond to MCP-1: direct role of MCP-1 in angiogenesis and tumor progression. Blood. 2000;96(1):34-40.
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Johns A, Freay AD, Fraser W, Korach KS, Rubanyi GM. Disruption of estrogen receptor gene prevents 17 beta estradiol-induced angiogenesis in transgenic mice. Endocrinology. 1996;137(10):4511-4513.
Not in our library10.1210/endo.137.10.8828515
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Ferber S, Tiram G, Satchi-Fainaro R. Monitoring functionality and morphology of vasculature recruited by factors secreted by fast-growing tumor-generating cells. J Vis Exp. 2014;93:e51525.
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Kleinman HK, Martin GR. Matrigel: basement membrane matrix with biological activity. Semin Cancer Biol. 2005;15(5):378-386.
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Benton G, Arnaoutova I, George J, Kleinman HK, Koblinski J. Matrigel: from discovery and ECM mimicry to assays and models for cancer research. Adv Drug Deliv Rev. 2014;79–80:3-18.
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Thijssen VL, Brandwijk RJ, Dings RP, Griffioen AW. Angiogenesis gene expression profiling in xenograft models to study cellular interactions. Exp Cell Res. 2004;299(2):286-293.
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Guedez L, Rivera AM, Salloum R, Miller ML, Diegmueller JJ, Bungay PM, Stetler-Stevenson WG. Quantitative assessment of angiogenic responses by the directed in vivo angiogenesis assay. Am J Pathol. 2003;162(5):1431-1439.
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Melero-Martin JM, Khan ZA, Picard A, Wu X, Paruchuri S, Bischoff J. In vivo vasculogenic potential of human blood-derived endothelial progenitor cells. Blood. 2007;109(11):4761-4768.
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Masaki I, Yonemitsu Y, Yamashita A, Sata S, Tanii M, Komori K, Nakagawa K, Hou X, Nagai Y, Hasegawa M, Sugimachi K, Sueishi K. Angiogenic gene therapy for experimental critical limb ischemia: acceleration of limb loss by overexpression of vascular endothelial growth factor 165 but not of fibroblast growth factor-2. Circ Res. 2002;90(9):966-973.
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Bastiaansen AJ, Ewing MM, de Boer HC, van der Pouw Kraan TC, de Vries MR, Peters EA, Welten SM, Arens R, Moore SM, Faber JE, Jukema JW, Hamming JF, Nossent AY, Quax PH. Lysine acetyltransferase PCAF is a key regulator of arteriogenesis. Arterioscler Thromb Vasc Biol. 2013;33(8):1902-1910.
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Chalothorn D, Faber JE. Strain-dependent variation in collateral circulatory function in mouse hindlimb. Physiol Genom. 2010;42(3):469-479.
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von Degenfeld G, Raake P, Kupatt C, Lebherz C, Hinkel R, Gildehaus FJ, Munzing W, Kranz A, Waltenberger J, Simoes M, Schwaiger M, Thein E, Boekstegers P. Selective pressure-regulated retroinfusion of fibroblast growth factor-2 into the coronary vein enhances regional myocardial blood flow and function in pigs with chronic myocardial ischemia. J Am Coll Cardiol. 2003;42(6):1120-1128.
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Wisenbaugh T, Allen P, Gt C, Holzgrefe H, Beller G, Carabello B. Contractile function, myosin ATPase activity and isozymes in the hypertrophied pig left ventricle after a chronic progressive pressure overload. Circ Res. 1983;53(3):332-341.
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Poltorak A, He X, Smirnova I, Liu MY, Van Huffel C, Du X, Birdwell D, Alejos E, Silva M, Galanos C, Freudenberg M, Ricciardi-Castagnoli P, Layton B, Beutler B. Defective LPS signaling in C3H/HeJ and C57BL/10ScCr mice: mutations in Tlr4 gene. Science. 1998;282(5396):2085-2088.
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Harmey JH, Bucana CD, Lu W, Byrne AM, McDonnell S, Lynch C, Bouchier-Hayes D, Dong Z. Lipopolysaccharide-induced metastatic growth is associated with increased angiogenesis, vascular permeability and tumor cell invasion. Int J Cancer. 2002;101(5):415-422.
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Lundin JI, Checkoway H. Endotoxin and cancer. Environ Health Perspect. 2009;117(9):1344-1350.
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Haricharan S, Brown P. TLR4 has a TP53-dependent dual role in regulating breast cancer cell growth. Proc Natl Acad Sci USA. 2015;112(25):E3216-E3225.
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Singh M, Couto SS, Forrest WF, Lima A, Cheng JH, Molina R, Long JE, Hamilton P, McNutt A, Kasman I, Nannini MA, Reslan HB, Cao TC, Ho CC, Barck KH, Carano RA, Foreman O, Eastham-Anderson J, Jubb AM, Ferrara N, Johnson L. Anti-VEGF antibody therapy does not promote metastasis in genetically engineered mouse tumour models. J Pathol. 2012;227(4):417-430.
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Prewett M, Huber J, Li Y, Santiago A, O’Connor W, King K, Overholser J, Hooper A, Pytowski B, Witte L, Bohlen P, Hicklin DJ. Antivascular endothelial growth factor receptor (fetal liver kinase 1) monoclonal antibody inhibits tumor angiogenesis. Cancer Res. 1999;59:5209-5218.
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Clark HF, Gurney AL, Abaya E, Baker K, Baldwin D, Brush J, Chen J, Chow B, Chui C, Crowley C, Currell B, Deuel B, Dowd P, Eaton D, Foster J, Grimaldi C, Gu Q, Hass PE, Heldens S, Huang A, Kim HS, Klimowski L, Jin Y, Johnson S, Lee J, Lewis L, Liao D, Mark M, Robbie E, Sanchez C, Schoenfeld J, Seshagiri S, Simmons L, Singh J, Smith V, Stinson J, Vagts A, Vandlen R, Watanabe C, Wieand D, Woods K, Xie MH, Yansura D, Yi S, Yu G, Yuan J, Zhang M, Zhang Z, Goddard A, Wood WI, Godowski P, Gray A. The secreted protein discovery initiative (SPDI), a large-scale effort to identify novel human secreted and transmembrane proteins: a bioinformatics assessment. Genome Res. 2003;13(10):2265-2270.
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LeCouter J, Kowalski J, Foster J, Hass P, Zhang Z, Dillard-Telm L, Frantz G, Rangell L, DeGuzman L, Keller G-A, Peale F, Gurney A, Hillan KJ, Ferrara N. Identification of an angiogenic mitogen selective for endocrine gland endothelium. Nature. 2001;412:877-884.
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Eswarappa SM, Potdar AA, Koch WJ, Fan Y, Vasu K, Lindner D, Willard B, Graham LM, DiCorleto PE, Fox PL. Programmed translational readthrough generates antiangiogenic VEGF-Ax. Cell. 2014;157(7):1605-1618.
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Xin H, Zhong C, Nudleman E, Ferrara N. Evidence for pro-angiogenic functions of VEGF-Ax. Cell. 2016;167(1):275-284.
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Lopez XM, Debeir O, Maris C, Rorive S, Roland I, Saerens M, Salmon I, Decaestecker C. Clustering methods applied in the detection of Ki67 hot-spots in whole tumor slide images: an efficient way to characterize heterogeneous tissue-based biomarkers. Cytom A. 2012;81(9):765-775.
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Hlushchuk R, Barré S, Djonov V. Morphological aspects of tumor angiogenesis. Methods Mol Biol. 2016;1464:13-24.
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Hlushchuk R, Bronnimann D, Correa Shokiche C, Schaad L, Triet R, Jazwinska A, Tschanz SA, Djonov V. Zebrafish Caudal Fin angiogenesis assay-advanced quantitative assessment including 3-way correlative microscopy. PLoS ONE. 2016;11(3):e0149281.
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Fujita M, Cha YR, Pham VN, Sakurai A, Roman BL, Gutkind JS, Weinstein BM. Assembly and patterning of the vascular network of the vertebrate hindbrain. Development. 2011;138(9):1705-1715.
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Isogai S, Lawson ND, Torrealday S, Horiguchi M, Weinstein BM. Angiogenic network formation in the developing vertebrate trunk. Development. 2003;130(21):5281-5290.
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Ribatti D, Bertossi M, Nico B, Vacca A, Ria R, Riva A, Roncali L, Presta M. Role of basic fibroblast growth factor in the formation of the capillary plexus in the chick embryo chorioallantoic membrane. An in situ hybridization, immunohistochemical and ultrastructural study. J Submicrosc Cytol Pathol. 1998;30(1):127-136.
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Ribatti D, Nico B, Pezzolo A, Vacca A, Meazza R, Cinti R, Carlini B, Parodi F, Pistoia V, Corrias MV. Angiogenesis in a human neuroblastoma xenograft model: mechanisms and inhibition by tumour-derived interferon-gamma. Br J Cancer. 2006;94(12):1845-1852.
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Nurro J, Halonen PJ, Kuivanen A, Tarkia M, Saraste A, Honkonen K, Lahteenvuo J, Rissanen TT, Knuuti J, Yla-Herttuala S. AdVEGF-B186 and AdVEGF-DDeltaNDeltaC induce angiogenesis and increase perfusion in porcine myocardium. Heart. 2016;102(21):1716-1720.
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Ausprunk DH, Knighton DR, Folkman J. Differentiation of vascular endothelium in the chick chorioallantois: a structural and autoradiographic study. Dev Biol. 1974;38(2):237-248.
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Lei Y, Rahim M, Ng Q, Segura T. Hyaluronic acid and fibrin hydrogels with concentrated DNA/PEI polyplexes for local gene delivery. J Control Release. 2011;153(3):255-261.
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Forough R, Wang X, Martinez-Lemus LA, Thomas D, Sun Z, Motamed K, Parker JL, Meininger GA. Cell-based and direct gene transfer-induced angiogenesis via a secreted chimeric fibroblast growth factor-1 (sp-FGF-1) in the chick chorioallantoic membrane (CAM). Angiogenesis. 2003;6(1):47-54.
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Javerzat S, Franco M, Herbert J, Platonova N, Peille AL, Pantesco V, De Vos J, Assou S, Bicknell R, Bikfalvi A, Hagedorn M. Correlating global gene regulation to angiogenesis in the developing chick extra-embryonic vascular system. PLoS ONE. 2009;4(11):e7856.
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Cavill R, Sidhu JK, Kilarski W, Javerzat S, Hagedorn M, Ebbels TM, Bikfalvi A, Keun HC. A combined metabonomic and transcriptomic approach to investigate metabolism during development in the chick chorioallantoic membrane. J Proteome Res. 2010;9(6):3126-3134.
Not in our library10.1021/pr100033t
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