Loss of Estrogen-Related Receptor Alpha Facilitates Angiogenesis in Endothelial Cells

REFERENCES

• Rodrigues SF, Granger DN. 2015. Blood cells and endothelial barrier function. Tissue Barriers 3:e978720. https://doi.org/10.4161/21688370.2014.978720.
   PubMed Web of Science ®Google Scholar
• Förstermann U, Sessa WC. 2012. Nitric oxide synthases: regulation and function. Eur Heart J 33:829–837. https://doi.org/10.1093/eurheartj/ehr304.
   PubMed Web of Science ®Google Scholar
• Pober JS, Sessa WC. 2007. Evolving functions of endothelial cells in inflammation. Nat Rev Immunol 7:803–815. https://doi.org/10.1038/nri2171.
   PubMed Web of Science ®Google Scholar
• Risau W. 1997. Mechanisms of angiogenesis. Nature 386:671–674. https://doi.org/10.1038/386671a0.
   PubMed Web of Science ®Google Scholar
• Blanco R, Gerhardt H. 2013. VEGF and Notch in tip and stalk cell selection. Cold Spring Harb Perspect Med 3:a006569. https://doi.org/10.1101/cshperspect.a006569.
   PubMed Web of Science ®Google Scholar
• Marcelo KL, Goldie LC, Hirschi KK. 2013. Regulation of endothelial cell differentiation and specification. Circ Res 112:1272–1287. https://doi.org/10.1161/CIRCRESAHA.113.300506.
   PubMed Web of Science ®Google Scholar
• Patel-Hett S, Damore PA. 2011. Signal transduction in vasculogenesis and developmental angiogenesis. Int J Dev Biol 55:353–363. https://doi.org/10.1387/ijdb.103213sp.
   PubMed Web of Science ®Google Scholar
• Ucuzian AA, Gassman AA, East AT, Greisler HP. 2010. Molecular mediators of angiogenesis. J Burn Care Res 31:158–175. https://doi.org/10.1097/BCR.0b013e3181c7ed82.
   PubMed Web of Science ®Google Scholar
• Potente M, Gerhardt H, Carmeliet P. 2011. Basic and therapeutic aspects of angiogenesis. Cell 146:873–887. https://doi.org/10.1016/j.cell.2011.08.039.
   PubMed Web of Science ®Google Scholar
• Jakobsson L, Bentley K, Gerhardt H. 2009. VEGFRs and Notch: a dynamic collaboration in vascular patterning. Biochem Soc Trans 37:1233–1236. https://doi.org/10.1042/BST0371233.
   PubMed Web of Science ®Google Scholar
• Park C, Kim TM, Malik AB. 2013. Transcriptional regulation of endothelial cell and vascular development. Circ Res 112:1380–1400. https://doi.org/10.1161/CIRCRESAHA.113.301078.
   PubMed Web of Science ®Google Scholar
• De Val S, Black BL. 2009. Transcriptional control of endothelial cell development. Dev Cell 16:180–195. https://doi.org/10.1016/j.devcel.2009.01.014.
   PubMed Web of Science ®Google Scholar
• Bautch VL. 2012. VEGF-directed blood vessel patterning: from cells to organism. Cold Spring Harb Perspect Med 2:a006452. https://doi.org/10.1101/cshperspect.a006452.
   PubMed Web of Science ®Google Scholar
• Jeltsch M, Leppanen VM, Saharinen P, Alitalo K. 2013. Receptor tyrosine kinase-mediated angiogenesis. Cold Spring Harb Perspect Biol 5:a009183. https://doi.org/10.1101/cshperspect.a009183.
   PubMed Web of Science ®Google Scholar
• Mangelsdorf DJ, Thummel C, Beato M, Herrlich P, Schutz G, Umesono K, Blumberg B, Kastner P, Mark M, Chambon P, Evans RM. 1995. The nuclear receptor superfamily: the second decade. Cell 83:835–839. https://doi.org/10.1016/0092-8674(95)90199-X.
   PubMed Web of Science ®Google Scholar
• Suzuki T, Nakamura Y, Moriya T, Sasano H. 2003. Effects of steroid hormones on vascular functions. Microsc Res Tech 60:76–84. https://doi.org/10.1002/jemt.10246.
   PubMed Web of Science ®Google Scholar
• Brouchet L, Krust A, Dupont S, Chambon P, Bayard F, Arnal JF. 2001. Estradiol accelerates reendothelialization in mouse carotid artery through estrogen receptor-alpha but not estrogen receptor-beta. Circulation 103:423–428. https://doi.org/10.1161/01.CIR.103.3.423.
   PubMed Web of Science ®Google Scholar
• Caulin-Glaser T, Farrell WJ, Pfau SE, Zaret B, Bunger K, Setaro JF, Brennan JJ, Bender JR, Cleman MW, Cabin HS, Remetz MS. 1998. Modulation of circulating cellular adhesion molecules in postmenopausal women with coronary artery disease. J Am Coll Cardiol 31:1555–1560. https://doi.org/10.1016/S0735-1097(98)00145-4.
   PubMed Web of Science ®Google Scholar
• Jun SS, Chen Z, Pace MC, Shaul PW. 1998. Estrogen upregulates cyclooxygenase-1 gene expression in ovine fetal pulmonary artery endothelium. J Clin Investig 102:176–183. https://doi.org/10.1172/JCI2034.
   PubMed Web of Science ®Google Scholar
• Losordo DW, Isner JM. 2001. Estrogen and angiogenesis: a review. Arterioscler Thromb Vasc Biol 21:6–12. https://doi.org/10.1161/01.ATV.21.1.6.
   PubMed Web of Science ®Google Scholar
• Morales DE, McGowan KA, Grant DS, Maheshwari S, Bhartiya D, Cid MC, Kleinman HK, Schnaper HW. 1995. Estrogen promotes angiogenic activity in human umbilical vein endothelial cells in vitro and in a murine model. Circulation 91:755–763. https://doi.org/10.1161/01.CIR.91.3.755.
   PubMed Web of Science ®Google Scholar
• Prabhushankar R, Krueger C, Manrique C. 2014. Membrane estrogen receptors: their role in blood pressure regulation and cardiovascular disease. Curr Hypertens Rep 16:013–0408.
   Web of Science ®Google Scholar
• Ingegno MD, Money SR, Thelmo W, Greene GL, Davidian M, Jaffe BM, Pertschuk LP. 1988. Progesterone receptors in the human heart and great vessels. Lab Investig 59:353–356.
   PubMed Web of Science ®Google Scholar
• Schnaper HW, McGuire J, Runyan C, Hubchak SC. 2000. Sex steroids and the endothelium. Curr Med Chem 7:519–531. https://doi.org/10.2174/0929867003374949.
   PubMed Web of Science ®Google Scholar
• Lee WS, Liu CW, Juan SH, Liang YC, Ho PY, Lee YH. 2003. Molecular mechanism of progesterone-induced antiproliferation in rat aortic smooth muscle cells. Endocrinology 144:2785–2790. https://doi.org/10.1210/en.2003-0045.
   PubMed Web of Science ®Google Scholar
• Wu J, Hadoke PWF, Takov K, Korczak A, Denvir MA, Smith LB. 2016. Influence of androgen receptor in vascular cells on reperfusion following hindlimb ischaemia. PLoS One 11:e0154987. https://doi.org/10.1371/journal.pone.0154987.
   Google Scholar
• Takov K, Wu J, Denvir MA, Smith LB, Hadoke PWF. 2018. The role of androgen receptors in atherosclerosis. Mol Cell Endocrinol 465:82–91. https://doi.org/10.1016/j.mce.2017.10.006.
   PubMed Web of Science ®Google Scholar
• Ullian ME. 1999. The role of corticosteriods in the regulation of vascular tone. Cardiovasc Res 41:55–64. https://doi.org/10.1016/S0008-6363(98)00230-2.
   PubMed Web of Science ®Google Scholar
• Logie JJ, Ali S, Marshall KM, Heck MMS, Walker BR, Hadoke PWF. 2010. Glucocorticoid-mediated inhibition of angiogenic changes in human endothelial cells is not caused by reductions in cell proliferation or migration. PLoS One 5:e14476. https://doi.org/10.1371/journal.pone.0014476.
   PubMed Web of Science ®Google Scholar
• Yano A, Fujii Y, Iwai A, Kageyama Y, Kihara K. 2006. Glucocorticoids suppress tumor angiogenesis and in vivo growth of prostate cancer cells. Clin Cancer Res 12:3003–3009. https://doi.org/10.1158/1078-0432.CCR-05-2085.
   PubMed Web of Science ®Google Scholar
• Lother A, Moser M, Bode C, Feldman RD, Hein L. 2015. Mineralocorticoids in the heart and vasculature: new insights for old hormones. Annu Rev Pharmacol Toxicol 55:289–312. https://doi.org/10.1146/annurev-pharmtox-010814-124302.
   PubMed Web of Science ®Google Scholar
• Giguere V. 1999. Orphan nuclear receptors: from gene to function. Endocr Rev 20:689–725. https://doi.org/10.1210/er.20.5.689.
   PubMed Web of Science ®Google Scholar
• Mullican SE, DiSpirito JR, Lazar MA. 2013. The orphan nuclear receptors at their 25th year reunion. J Mol Endocrinol 51:T115–T140. https://doi.org/10.1530/JME-13-0212.
   PubMed Web of Science ®Google Scholar
• Kotlinowski J, Jozkowicz A. 2016. PPAR gamma and angiogenesis: endothelial cells perspective. J Diabetes Res 2016:8492353. https://doi.org/10.1155/2016/8492353.
   PubMed Web of Science ®Google Scholar
• Hong HK, Cho YM, Park KH, Lee CT, Lee HK, Park KS. 2003. Peroxisome proliferator-activated receptor gamma mediated inhibition of plasminogen activator inhibitor type 1 production and proliferation of human umbilical vein endothelial cells. Diabetes Res Clin Pract 62:1–8. https://doi.org/10.1016/S0168-8227(03)00142-6.
   PubMed Web of Science ®Google Scholar
• Zhao Y, Bruemmer D. 2010. NR4A orphan nuclear receptors: transcriptional regulators of gene expression in metabolism and vascular biology. Arterioscler Thromb Vasc Biol 30:1535–1541. https://doi.org/10.1161/ATVBAHA.109.191163.
   PubMed Web of Science ®Google Scholar
• Pereira FA, Qiu Y, Zhou G, Tsai MJ, Tsai SY. 1999. The orphan nuclear receptor COUP-TFII is required for angiogenesis and heart development. Genes Dev 13:1037–1049. https://doi.org/10.1101/gad.13.8.1037.
   PubMed Web of Science ®Google Scholar
• Giguere V. 2008. Transcriptional control of energy homeostasis by the estrogen-related receptors. Endocr Rev 29:677–696. https://doi.org/10.1210/er.2008-0017.
   PubMed Web of Science ®Google Scholar
• Giguere V, Yang N, Segui P, Evans RM. 1988. Identification of a new class of steroid hormone receptors. Nature 331:91–94. https://doi.org/10.1038/331091a0.
   PubMed Web of Science ®Google Scholar
• Dufour CR, Wilson BJ, Huss JM, Kelly DP, Alaynick WA, Downes M, Evans RM, Blanchette M, Giguere V. 2007. Genome-wide orchestration of cardiac functions by the orphan nuclear receptors ERRalpha and gamma. Cell Metab 5:345–356. https://doi.org/10.1016/j.cmet.2007.03.007.
   PubMed Web of Science ®Google Scholar
• Audet-Walsh É, Giguére V. 2015. The multiple universes of estrogen-related receptor alpha and gamma in metabolic control and related diseases. Acta Pharmacol Sin 36:51–61. https://doi.org/10.1038/aps.2014.121.
   PubMed Web of Science ®Google Scholar
• Huss JM, Kopp RP, Kelly DP. 2002. Peroxisome proliferator-activated receptor coactivator-1alpha (PGC-1alpha) coactivates the cardiac-enriched nuclear receptors estrogen-related receptor-alpha and -gamma. Identification of novel leucine-rich interaction motif within PGC-1alpha. J Biol Chem 277:40265–40274. https://doi.org/10.1074/jbc.M206324200.
   PubMed Web of Science ®Google Scholar
• Kamei Y, Ohizumi H, Fujitani Y, Nemoto T, Tanaka T, Takahashi N, Kawada T, Miyoshi M, Ezaki O, Kakizuka A. 2003. PPARgamma coactivator 1beta/ERR ligand 1 is an ERR protein ligand, whose expression induces a high-energy expenditure and antagonizes obesity. Proc Natl Acad Sci U S A 100:12378–12383. https://doi.org/10.1073/pnas.2135217100.
   PubMed Web of Science ®Google Scholar
• Schreiber SN, Emter R, Hock MB, Knutti D, Cardenas J, Podvinec M, Oakeley EJ, Kralli A. 2004. The estrogen-related receptor alpha (ERRalpha) functions in PPARgamma coactivator 1alpha (PGC-1alpha)-induced mitochondrial biogenesis. Proc Natl Acad Sci U S A 101:6472–6477. https://doi.org/10.1073/pnas.0308686101.
   PubMed Web of Science ®Google Scholar
• Perry MC, Dufour CR, Tam IS, B'Chir W, Giguere V. 2014. Estrogen-related receptor-alpha coordinates transcriptional programs essential for exercise tolerance and muscle fitness. Mol Endocrinol 28:2060–2071. https://doi.org/10.1210/me.2014-1281.
   PubMed Web of Science ®Google Scholar
• Narkar VA, Fan W, Downes M, Yu RT, Jonker JW, Alaynick WA, Banayo E, Karunasiri MS, Lorca S, Evans RM. 2011. Exercise and PGC-1alpha-independent synchronization of type I muscle metabolism and vasculature by ERRgamma. Cell Metab 13:283–293. https://doi.org/10.1016/j.cmet.2011.01.019.
   PubMed Web of Science ®Google Scholar
• Luo J, Sladek R, Carrier J, Bader JA, Richard D, Giguere V. 2003. Reduced fat mass in mice lacking orphan nuclear receptor estrogen-related receptor alpha. Mol Cell Biol 23:7947–7956. https://doi.org/10.1128/MCB.23.22.7947-7956.2003.
   PubMed Web of Science ®Google Scholar
• Powelka AM, Seth A, Virbasius JV, Kiskinis E, Nicoloro SM, Guilherme A, Tang X, Straubhaar J, Cherniack AD, Parker MG, Czech MP. 2006. Suppression of oxidative metabolism and mitochondrial biogenesis by the transcriptional corepressor RIP140 in mouse adipocytes. J Clin Investig 116:125–136.
   PubMed Web of Science ®Google Scholar
• Villena JA, Hock MB, Chang WY, Barcas JE, Giguere V, Kralli A. 2007. Orphan nuclear receptor estrogen-related receptor alpha is essential for adaptive thermogenesis. Proc Natl Acad Sci U S A 104:1418–1423. https://doi.org/10.1073/pnas.0607696104.
   PubMed Web of Science ®Google Scholar
• Huss JM, Garbacz WG, Xie W. 2015. Constitutive activities of estrogen-related receptors: transcriptional regulation of metabolism by the ERR pathways in health and disease. Biochim Biophys Acta 9:24.
   Google Scholar
• Sonoda J, Laganiere J, Mehl IR, Barish GD, Chong LW, Li X, Scheffler IE, Mock DC, Bataille AR, Robert F, Lee CH, Giguere V, Evans RM. 2007. Nuclear receptor ERR alpha and coactivator PGC-1 beta are effectors of IFN-gamma-induced host defense. Genes Dev 21:1909–1920. https://doi.org/10.1101/gad.1553007.
   PubMed Web of Science ®Google Scholar
• Michalek RD, Gerriets VA, Nichols AG, Inoue M, Kazmin D, Chang CY, Dwyer MA, Nelson ER, Pollizzi KN, Ilkayeva O, Giguere V, Zuercher WJ, Powell JD, Shinohara ML, McDonnell DP, Rathmell JC. 2011. Estrogen-related receptor-alpha is a metabolic regulator of effector T-cell activation and differentiation. Proc Natl Acad Sci U S A 108:18348–18353. https://doi.org/10.1073/pnas.1108856108.
   PubMed Web of Science ®Google Scholar
• Matsakas A, Yadav V, Lorca S, Evans RM, Narkar VA. 2012. Revascularization of ischemic skeletal muscle by estrogen-related receptor-gamma. Circ Res 110:1087–1096. https://doi.org/10.1161/CIRCRESAHA.112.266478.
   PubMed Web of Science ®Google Scholar
• Stein RA, Gaillard S, McDonnell DP. 2009. Estrogen-related receptor alpha induces the expression of vascular endothelial growth factor in breast cancer cells. J Steroid Biochem Mol Biol 114:106–112. https://doi.org/10.1016/j.jsbmb.2009.02.010.
   PubMed Web of Science ®Google Scholar
• Liang J, Han F, Chen Y. 2013. Transcriptional regulation of VEGF expression by estrogen-related receptor γ. Acta Pharmaceutica Sinica B 3:373–380. https://doi.org/10.1016/j.apsb.2013.09.001.
   Web of Science ®Google Scholar
• Sobczak M, Dargatz J, Chrzanowska-Wodnicka M. 2010. Isolation and culture of pulmonary endothelial cells from neonatal mice. J Vis Exp 14:2316.
   Google Scholar
• Korff T, Augustin HG. 1999. Tensional forces in fibrillar extracellular matrices control directional capillary sprouting. J Cell Sci 112:3249–3258.
   PubMed Web of Science ®Google Scholar
• Pfisterer L, Korff T. 2016. Spheroid-based in vitro angiogenesis model, p 167–177. In Martin SG, Hewett PW (ed), Angiogenesis protocols. Springer New York, New York, NY. https://doi.org/10.1007/978-1-4939-3628-1_11.
   Google Scholar
• Rangwala SM, Wang X, Calvo JA, Lindsley L, Zhang Y, Deyneko G, Beaulieu V, Gao J, Turner G, Markovits J. 2010. Estrogen-related receptor gamma is a key regulator of muscle mitochondrial activity and oxidative capacity. J Biol Chem 285:22619–22629. https://doi.org/10.1074/jbc.M110.125401.
   PubMed Web of Science ®Google Scholar
• Alaynick WA, Kondo RP, Xie W, He W, Dufour CR, Downes M, Jonker JW, Giles W, Naviaux RK, Giguere V, Evans RM. 2007. ERRgamma directs and maintains the transition to oxidative metabolism in the postnatal heart. Cell Metab 6:13–24. https://doi.org/10.1016/j.cmet.2007.06.007.
   PubMed Web of Science ®Google Scholar
• Vega RB, Kelly DP. 1997. A role for estrogen-related receptor alpha in the control of mitochondrial fatty acid beta-oxidation during brown adipocyte differentiation. J Biol Chem 272:31693–31699. https://doi.org/10.1074/jbc.272.50.31693.
   PubMed Web of Science ®Google Scholar
• Cruys B, Wong BW, Kuchnio A, Verdegem D, Cantelmo AR, Conradi LC, Vandekeere S, Bouche A, Cornelissen I, Vinckier S, Merks RM, Dejana E, Gerhardt H, Dewerchin M, Bentley K, Carmeliet P. 2016. Glycolytic regulation of cell rearrangement in angiogenesis. Nat Commun 7:12240. https://doi.org/10.1038/ncomms12240.
   PubMed Web of Science ®Google Scholar
• De Bock K, Georgiadou M, Carmeliet P. 2013. Role of endothelial cell metabolism in vessel sprouting. Cell Metab 18:634–647. https://doi.org/10.1016/j.cmet.2013.08.001.
   PubMed Web of Science ®Google Scholar
• Treps L, Conradi LC, Harjes U, Carmeliet P. 2016. Manipulating angiogenesis by targeting endothelial metabolism: hitting the engine rather than the drivers-a new perspective? Pharmacol Rev 68:872–887. https://doi.org/10.1124/pr.116.012492.
   PubMed Web of Science ®Google Scholar
• Rothhammer T, Bataille F, Spruss T, Eissner G, Bosserhoff AK. 2007. Functional implication of BMP4 expression on angiogenesis in malignant melanoma. Oncogene 26:4158–4170. https://doi.org/10.1038/sj.onc.1210182.
   PubMed Web of Science ®Google Scholar
• Yadav SS, Narayan G. 2014. Role of ROBO4 signalling in developmental and pathological angiogenesis. Biomed Res Int 2014:683025. https://doi.org/10.1155/2014/683025.
   PubMed Web of Science ®Google Scholar
• Zhou Y, Williams J, Smallwood PM, Nathans J. 2015. Sox7, Sox17, and Sox18 cooperatively regulate vascular development in the mouse retina. PLoS One 10:e0143650. https://doi.org/10.1371/journal.pone.0143650.
   PubMed Web of Science ®Google Scholar
• Fukumura D, Gohongi T, Kadambi A, Izumi Y, Ang J, Yun CO, Buerk DG, Huang PL, Jain RK. 2001. Predominant role of endothelial nitric oxide synthase in vascular endothelial growth factor-induced angiogenesis and vascular permeability. Proc Natl Acad Sci U S A 98:2604–2609. https://doi.org/10.1073/pnas.041359198.
   PubMed Web of Science ®Google Scholar
• Lamalice L, Le Boeuf F, Huot J. 2007. Endothelial cell migration during angiogenesis. Circ Res 100:782–794. https://doi.org/10.1161/01.RES.0000259593.07661.1e.
   PubMed Web of Science ®Google Scholar
• Cao G, O'Brien CD, Zhou Z, Sanders SM, Greenbaum JN, Makrigiannakis A, DeLisser HM. 2002. Involvement of human PECAM-1 in angiogenesis and in vitro endothelial cell migration. Am J Physiol Cell Physiol 282:C1181–C1190. https://doi.org/10.1152/ajpcell.00524.2001.
   PubMed Web of Science ®Google Scholar
• van Hinsbergh VW, Koolwijk P. 2008. Endothelial sprouting and angiogenesis: matrix metalloproteinases in the lead. Cardiovasc Res 78:203–212. https://doi.org/10.1093/cvr/cvm102.
   PubMed Web of Science ®Google Scholar
• Ishida T, Kundu RK, Yang E, Hirata K, Ho YD, Quertermous T. 2003. Targeted disruption of endothelial cell-selective adhesion molecule inhibits angiogenic processes in vitro and in vivo. J Biol Chem 278:34598–34604. https://doi.org/10.1074/jbc.M304890200.
   PubMed Web of Science ®Google Scholar
• Yang H, Zhang H, Ge S, Ning T, Bai M, Li J, Li S, Sun W, Deng T, Zhang L, Ying G, Ba Y. 2018. Exosome-derived miR-130a activates angiogenesis in gastric cancer by targeting C-MYB in vascular endothelial cells. Mol Ther 26:2466–2475. https://doi.org/10.1016/j.ymthe.2018.07.023.
   PubMed Web of Science ®Google Scholar
• ENCODE Project Consortium. 2012. An integrated encyclopedia of DNA elements in the human genome. Nature 489:57–74. https://doi.org/10.1038/nature11247.
   PubMed Web of Science ®Google Scholar
• Audet-Walsh É, Papadopoli DJ, Gravel S-P, Yee T, Bridon G, Caron M, Bourque G, Giguère V, St-Pierre J. 2016. The PGC-1alpha/ERRalpha axis represses one-carbon metabolism and promotes sensitivity to anti-folate therapy in breast cancer. Cell Rep 14:920–931. https://doi.org/10.1016/j.celrep.2015.12.086.
   PubMed Web of Science ®Google Scholar
• Potente M, Carmeliet P. 2017. The link between angiogenesis and endothelial metabolism. Annu Rev Physiol 79:43–66. https://doi.org/10.1146/annurev-physiol-021115-105134.
   PubMed Web of Science ®Google Scholar
• Xu Y, An X, Guo X, Habtetsion TG, Wang Y, Xu X, Kandala S, Li Q, Li H, Zhang C, Caldwell RB, Fulton DJ, Su Y, Hoda MN, Zhou G, Wu C, Huo Y. 2014. Endothelial PFKFB3 plays a critical role in angiogenesis. Arterioscler Thromb Vasc Biol 34:1231–1239. https://doi.org/10.1161/ATVBAHA.113.303041.
   PubMed Web of Science ®Google Scholar
• Schoors S, Bruning U, Missiaen R, Queiroz KC, Borgers G, Elia I, Zecchin A, Cantelmo AR, Christen S, Goveia J, Heggermont W, Godde L, Vinckier S, Van Veldhoven PP, Eelen G, Schoonjans L, Gerhardt H, Dewerchin M, Baes M, De Bock K, Ghesquiere B, Lunt SY, Fendt SM, Carmeliet P. 2015. Fatty acid carbon is essential for dNTP synthesis in endothelial cells. Nature 520:192–197. https://doi.org/10.1038/nature14362.
   PubMed Web of Science ®Google Scholar
• Kalucka J, Bierhansl L, Conchinha NV, Missiaen R, Elia I, Bruning U, Scheinok S, Treps L, Cantelmo AR, Dubois C, de Zeeuw P, Goveia J, Zecchin A, Taverna F, Morales-Rodriguez F, Brajic A, Conradi LC, Schoors S, Harjes U, Vriens K, Pilz GA, Chen R, Cubbon R, Thienpont B, Cruys B, Wong BW, Ghesquiere B, Dewerchin M, De Bock K, Sagaert X, Jessberger S, Jones EAV, Gallez B, Lambrechts D, Mazzone M, Eelen G, Li X, Fendt SM, Carmeliet P. 2018. Quiescent endothelial cells upregulate fatty acid beta-oxidation for vasculoprotection via redox homeostasis. Cell Metab 28:881–894. https://doi.org/10.1016/j.cmet.2018.07.016.
   PubMed Web of Science ®Google Scholar
• National Research Council. 2011. Guide for the care and use of laboratory animals, 8th ed. National Academies Press, Washington, DC.
   Google Scholar
• Yu G, Wang LG, Han Y, He QY. 2012. clusterProfiler: an R package for comparing biological themes among gene clusters. Omics 16:284–287. https://doi.org/10.1089/omi.2011.0118.
   PubMed Web of Science ®Google Scholar
• Eglinger J, Karsjens H, Lammert E. 2017. Quantitative assessment of angiogenesis and pericyte coverage in human cell-derived vascular sprouts. Inflamm Regen 37:016–0033.
   PubMedGoogle Scholar
• Carpentier GMM, Courty J, Cascone I. 2012. Angiogenesis analyzer for ImageJ, p 198–201. 4th ImageJ User and Developer Conference Proceedings. Centre de Recherche Henri Tudor, Luxembourg, Belgium.
   Google Scholar
• Tual-Chalot S, Allinson KR, Fruttiger M, Arthur HM. 2013. Whole mount immunofluorescent staining of the neonatal mouse retina to investigate angiogenesis in vivo. J Vis Exp 9:50546.
   Google Scholar
• Zudaire E, Gambardella L, Kurcz C, Vermeren S. 2011. A computational tool for quantitative analysis of vascular networks. PLoS One 6:e27385. https://doi.org/10.1371/journal.pone.0027385.
   PubMed Web of Science ®Google Scholar
• Langmead B, Salzberg SL. 2012. Fast gapped-read alignment with Bowtie 2. Nat Methods 9:357–359. https://doi.org/10.1038/nmeth.1923.
   PubMed Web of Science ®Google Scholar
• Zhang Y, Liu T, Meyer CA, Eeckhoute J, Johnson DS, Bernstein BE, Nusbaum C, Myers RM, Brown M, Li W, Liu XS. 2008. Model-based analysis of ChIP-Seq (MACS). Genome Biol 9:2008–2009.
   Web of Science ®Google Scholar
• Li QB, James B, Huang H, Bickel PJ. 2011. Measuring reproducibility of high-throughput experiments. Ann Appl Stat 5:1752–1779. https://doi.org/10.1214/11-AOAS466.
   Web of Science ®Google Scholar
• Heinz S, Benner C, Spann N, Bertolino E, Lin YC, Laslo P, Cheng JX, Murre C, Singh H, Glass CK. 2010. Simple combinations of lineage-determining transcription factors prime cis-regulatory elements required for macrophage and B cell identities. Mol Cell 38:576–589. https://doi.org/10.1016/j.molcel.2010.05.004.
   PubMed Web of Science ®Google Scholar
• Wang J, Zhuang J, Iyer S, Lin X, Whitfield TW, Greven MC, Pierce BG, Dong X, Kundaje A, Cheng Y, Rando OJ, Birney E, Myers RM, Noble WS, Snyder M, Weng Z. 2012. Sequence features and chromatin structure around the genomic regions bound by 119 human transcription factors. Genome Res 22:1798–1812. https://doi.org/10.1101/gr.139105.112.
   PubMed Web of Science ®Google Scholar
• Ramirez F, Ryan DP, Gruning B, Bhardwaj V, Kilpert F, Richter AS, Heyne S, Dundar F, Manke T. 2016. deepTools2: a next generation web server for deep-sequencing data analysis. Nucleic Acids Res 44:13.
   Web of Science ®Google Scholar
• Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, Harris MA, Hill DP, Issel-Tarver L, Kasarskis A, Lewis S, Matese JC, Richardson JE, Ringwald M, Rubin GM, Sherlock G. 2000. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet 25:25–29. https://doi.org/10.1038/75556.
   PubMed Web of Science ®Google Scholar