{"status":"ok","message-type":"work","message-version":"1.0.0","message":{"indexed":{"date-parts":[[2026,9,3]],"date-time":"2026-09-03T15:29:11Z","timestamp":1788449351566,"version":"build-2803163510"},"reference-count":50,"publisher":"Oxford University Press (OUP)","issue":"1","license":[{"start":{"date-parts":[[2023,3,17]],"date-time":"2023-03-17T00:00:00Z","timestamp":1679011200000},"content-version":"vor","delay-in-days":0,"URL":"https:\/\/academic.oup.com\/journals\/pages\/open_access\/funder_policies\/chorus\/standard_publication_model"}],"content-domain":{"domain":[],"crossmark-restriction":false},"short-container-title":[],"published-print":{"date-parts":[[2023,6,30]]},"abstract":"<jats:title>Abstract<\/jats:title>\n               <jats:p>Angiogenesis is a dynamic morphogenetic process that refers to the growth of new blood vessels from the pre-existing vessels and is critical for tissue repair during wound healing. In adult normal tissues, quiescent endothelial cells and pericytes maintain vascular integrity, whereas angiogenesis is immediately induced upon tissue injury, thereby forming neovascular networks to maintain homeostasis. However, impaired angiogenesis results in development of chronic and non-healing wounds in various diseases such as diabetes and peripheral artery diseases. Zebrafish are a vertebrate model organism widely used for studying many medical and life science fields. Indeed, the molecular and cellular mechanisms underlying regulation of wound angiogenesis have recently been studied by performing fluorescence-based live-imaging of adult zebrafish. In this review, we describe how endothelial cells and pericytes establish neovascular networks during wound angiogenesis and also introduce a novel role of blood flow-driven intraluminal pressure in regulating angiogenesis during wound healing.<\/jats:p>","DOI":"10.1093\/jb\/mvad024","type":"journal-article","created":{"date-parts":[[2023,3,17]],"date-time":"2023-03-17T23:39:16Z","timestamp":1679096356000},"page":"5-12","source":"Crossref","is-referenced-by-count":13,"title":["Novel regulatory mechanisms underlying angiogenesis during wound healing revealed by fluorescence-based live-imaging in zebrafish"],"prefix":"10.1093","volume":"174","author":[{"given":"Shinya","family":"Yuge","sequence":"first","affiliation":[{"name":"Institute for Advanced Medical Sciences, Nippon Medical School Department of Molecular Pathophysiology, , 1-1-5 Sendagi, Bunkyo-ku, Tokyo, 113-8602, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Tomohiro","family":"Ishii","sequence":"additional","affiliation":[{"name":"Institute for Advanced Medical Sciences, Nippon Medical School Department of Molecular Pathophysiology, , 1-1-5 Sendagi, Bunkyo-ku, Tokyo, 113-8602, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Chikage","family":"Noishiki","sequence":"additional","affiliation":[{"name":"Institute for Advanced Medical Sciences, Nippon Medical School Department of Molecular Pathophysiology, , 1-1-5 Sendagi, Bunkyo-ku, Tokyo, 113-8602, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]},{"given":"Shigetomo","family":"Fukuhara","sequence":"additional","affiliation":[{"name":"Institute for Advanced Medical Sciences, Nippon Medical School Department of Molecular Pathophysiology, , 1-1-5 Sendagi, Bunkyo-ku, Tokyo, 113-8602, Japan"}],"role":[{"vocabulary":"crossref","role":"author"}]}],"member":"286","published-online":{"date-parts":[[2023,3,17]]},"reference":[{"key":"2023070318410998400_ref1","doi-asserted-by":"crossref","first-page":"464","DOI":"10.1038\/nrm2183","article-title":"Molecular regulation of angiogenesis and lymphangiogenesis","volume":"8","author":"Adams","year":"2007","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2023070318410998400_ref2","doi-asserted-by":"crossref","first-page":"314","DOI":"10.1038\/nature07039","article-title":"Wound repair and regeneration","volume":"453","author":"Gurtner","year":"2008","journal-title":"Nature"},{"key":"2023070318410998400_ref3","doi-asserted-by":"crossref","first-page":"647","DOI":"10.1089\/wound.2013.0517","article-title":"Vascular endothelial growth factor and angiogenesis in the regulation of cutaneous wound repair","volume":"3","author":"Johnson","year":"2014","journal-title":"Adv. Wound Care (New Rochelle)"},{"key":"2023070318410998400_ref4","doi-asserted-by":"crossref","first-page":"1219","DOI":"10.1172\/JCI32169","article-title":"Cellular and molecular basis of wound healing in diabetes","volume":"117","author":"Brem","year":"2007","journal-title":"J. Clin. Invest."},{"key":"2023070318410998400_ref5","doi-asserted-by":"crossref","first-page":"551","DOI":"10.1038\/nrm3176","article-title":"Molecular control of endothelial cell behaviour during blood vessel morphogenesis","volume":"12","author":"Herbert","year":"2011","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2023070318410998400_ref6","doi-asserted-by":"crossref","first-page":"3835","DOI":"10.1158\/0008-5472.CAN-06-4056","article-title":"Systemic overexpression of angiopoietin-2 promotes tumor microvessel regression and inhibits angiogenesis and tumor growth","volume":"67","author":"Cao","year":"2007","journal-title":"Cancer Res."},{"key":"2023070318410998400_ref7","doi-asserted-by":"crossref","first-page":"99","DOI":"10.1160\/TH06-05-0277","article-title":"Impaired pericyte recruitment and abnormal retinal angiogenesis as a result of angiopoietin-2 overexpression","volume":"97","author":"Feng","year":"2007","journal-title":"Thromb. Haemost."},{"key":"2023070318410998400_ref8","doi-asserted-by":"crossref","first-page":"593","DOI":"10.1002\/ajh.21745","article-title":"Pericytes and vessel maturation during tumor angiogenesis and metastasis","volume":"85","author":"Raza","year":"2010","journal-title":"Am. J. Hematol."},{"key":"2023070318410998400_ref9","doi-asserted-by":"crossref","first-page":"298","DOI":"10.1038\/nature10144","article-title":"Molecular mechanisms and clinical applications of angiogenesis","volume":"473","author":"Carmeliet","year":"2011","journal-title":"Nature"},{"key":"2023070318410998400_ref10","doi-asserted-by":"crossref","first-page":"7968","DOI":"10.1073\/pnas.1310842111","article-title":"Fluid shear stress threshold regulates angiogenic sprouting","volume":"111","author":"Galie","year":"2014","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2023070318410998400_ref11","first-page":"4151","article-title":"Flow dynamics control the location of sprouting and direct elongation during developmental angiogenesis","volume":"142","author":"Ghaffari","year":"2015","journal-title":"Development"},{"key":"2023070318410998400_ref12","doi-asserted-by":"crossref","first-page":"15342","DOI":"10.1073\/pnas.1105316108","article-title":"Fluid forces control endothelial sprouting","volume":"108","author":"Song","year":"2011","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2023070318410998400_ref13","doi-asserted-by":"crossref","DOI":"10.1371\/journal.pbio.1001374","article-title":"Haemodynamics-driven developmental pruning of brain vasculature in zebrafish","volume":"10","author":"Chen","year":"2012","journal-title":"PLoS Biol."},{"key":"2023070318410998400_ref14","article-title":"Dynamic endothelial cell rearrangements drive developmental vessel regression","volume":"13","author":"Franco","year":"2015","journal-title":"PLoS Biol."},{"key":"2023070318410998400_ref15","doi-asserted-by":"crossref","first-page":"443","DOI":"10.1038\/ncb3320","article-title":"Blood flow drives lumen formation by inverse membrane blebbing during angiogenesis in vivo","volume":"18","author":"Gebala","year":"2016","journal-title":"Nat. Cell Biol."},{"key":"2023070318410998400_ref16","doi-asserted-by":"crossref","first-page":"626","DOI":"10.1089\/wound.2013.0491","article-title":"Mechanoregulation of angiogenesis in wound healing","volume":"3","author":"Lancerotto","year":"2014","journal-title":"Adv Wound Care (New Rochelle)."},{"key":"2023070318410998400_ref17","doi-asserted-by":"crossref","first-page":"657","DOI":"10.1038\/nm.1985","article-title":"Biomechanical regulation of blood vessel growth during tissue vascularization","volume":"15","author":"Kilarski","year":"2009","journal-title":"Nat. Med."},{"key":"2023070318410998400_ref18","doi-asserted-by":"crossref","first-page":"979","DOI":"10.1189\/jlb.4MR0316-102R","article-title":"Angiogenesis and wound repair: when enough is enough","volume":"100","author":"DiPietro","year":"2016","journal-title":"J. Leukoc. Biol."},{"key":"2023070318410998400_ref19","doi-asserted-by":"crossref","DOI":"10.7554\/eLife.05635","article-title":"Advancing biology through a deeper understanding of zebrafish ecology and evolution","volume":"4","author":"Parichy","year":"2015","journal-title":"eLife"},{"key":"2023070318410998400_ref20","doi-asserted-by":"crossref","first-page":"353","DOI":"10.1038\/nrg2091","article-title":"Animal models of human disease: zebrafish swim into view","volume":"8","author":"Lieschke","year":"2007","journal-title":"Nat. Rev. Genet."},{"key":"2023070318410998400_ref21","doi-asserted-by":"crossref","first-page":"63","DOI":"10.1093\/jmicro\/dfs130","article-title":"Fluorescence imaging in the last two decades","volume":"62","author":"Miyawaki","year":"2013","journal-title":"Microscopy (Oxf)."},{"key":"2023070318410998400_ref22","doi-asserted-by":"crossref","first-page":"333","DOI":"10.1111\/dgd.12210","article-title":"Looking back and moving forward: recent advances in understanding of cardiovascular development by imaging of zebrafish","volume":"57","author":"Fukuhara","year":"2015","journal-title":"Develop. Growth Differ."},{"key":"2023070318410998400_ref23","doi-asserted-by":"crossref","DOI":"10.3389\/fphys.2020.00842","article-title":"Endothelial cell dynamics in vascular development: insights from live-imaging in zebrafish","volume":"11","author":"Okuda","year":"2020","journal-title":"Front. Physiol."},{"key":"2023070318410998400_ref24","doi-asserted-by":"crossref","first-page":"5758","DOI":"10.1038\/ncomms6758","article-title":"Arteries are formed by vein-derived endothelial tip cells","volume":"5","author":"Xu","year":"2014","journal-title":"Nat. Commun."},{"key":"2023070318410998400_ref25","doi-asserted-by":"crossref","first-page":"2064","DOI":"10.1038\/nprot.2015.130","article-title":"Intubation-based anesthesia for long-term time-lapse imaging of adult zebrafish","volume":"10","author":"Xu","year":"2015","journal-title":"Nat. Protoc."},{"key":"2023070318410998400_ref26","doi-asserted-by":"crossref","first-page":"341","DOI":"10.1007\/s10456-018-09660-y","article-title":"Live imaging of angiogenesis during cutaneous wound healing in adult zebrafish","volume":"22","author":"Noishiki","year":"2019","journal-title":"Angiogenesis"},{"key":"2023070318410998400_ref27","doi-asserted-by":"crossref","first-page":"41","DOI":"10.1007\/978-1-60327-019-9_3","article-title":"Transgenesis in zebrafish with the tol2 transposon system","volume":"561","author":"Suster","year":"2009","journal-title":"Methods Mol. Biol."},{"key":"2023070318410998400_ref28","doi-asserted-by":"crossref","first-page":"1655","DOI":"10.1038\/jid.2013.16","article-title":"Adult zebrafish as a model system for cutaneous wound-healing research","volume":"133","author":"Richardson","year":"2013","journal-title":"J. Invest. Dermatol."},{"key":"2023070318410998400_ref29","first-page":"1328","article-title":"Clarification of mural cell coverage of vascular endothelial cells by live imaging of zebrafish","volume":"143","author":"Ando","year":"2016","journal-title":"Development"},{"key":"2023070318410998400_ref30","doi-asserted-by":"crossref","first-page":"223","DOI":"10.1016\/B978-0-12-381320-6.00009-6","volume-title":"Methods in Cell Biology The Zebrafish: Disease Models and Chemical Screens","author":"Karpanen","year":"2011"},{"key":"2023070318410998400_ref31","doi-asserted-by":"crossref","first-page":"165","DOI":"10.1038\/nrm2639","article-title":"Control of vascular morphogenesis and homeostasis through the angiopoietin-tie system","volume":"10","author":"Augustin","year":"2009","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2023070318410998400_ref32","doi-asserted-by":"crossref","first-page":"563","DOI":"10.1146\/annurev-cellbio-092910-154002","article-title":"Developmental and pathological angiogenesis","volume":"27","author":"Chung","year":"2011","journal-title":"Annu. Rev. Cell Dev. Biol."},{"key":"2023070318410998400_ref33","doi-asserted-by":"crossref","first-page":"2182","DOI":"10.1182\/blood-2012-04-396846","article-title":"Eyeing central neurons in vascular growth and reparative angiogenesis","volume":"120","author":"Sapieha","year":"2012","journal-title":"Blood"},{"key":"2023070318410998400_ref34","doi-asserted-by":"crossref","first-page":"310","DOI":"10.1161\/CIRCRESAHA.120.316851","article-title":"Basic and therapeutic aspects of angiogenesis updated","volume":"127","author":"Eelen","year":"2020","journal-title":"Circ. Res."},{"key":"2023070318410998400_ref35","doi-asserted-by":"crossref","first-page":"2594","DOI":"10.1038\/s41467-022-30197-8","article-title":"Mechanical loading of intraluminal pressure mediates wound angiogenesis by regulating the TOCA family of F-BAR proteins","volume":"13","author":"Yuge","year":"2022","journal-title":"Nat. Commun."},{"key":"2023070318410998400_ref36","doi-asserted-by":"crossref","first-page":"782","DOI":"10.1161\/01.RES.0000259593.07661.1e","article-title":"Endothelial cell migration during angiogenesis","volume":"100","author":"Lamalice","year":"2007","journal-title":"Circ. Res."},{"key":"2023070318410998400_ref37","doi-asserted-by":"crossref","first-page":"97","DOI":"10.1038\/nrm.2015.14","article-title":"The front and rear of collective cell migration","volume":"17","author":"Mayor","year":"2016","journal-title":"Nat. Rev. Mol. Cell Biol."},{"key":"2023070318410998400_ref38","doi-asserted-by":"crossref","first-page":"11429","DOI":"10.1073\/pnas.1010481108","article-title":"Membrane tension regulates motility by controlling lamellipodium organization","volume":"108","author":"Batchelder","year":"2011","journal-title":"Proc. Natl. Acad. Sci. U. S. A."},{"key":"2023070318410998400_ref39","doi-asserted-by":"crossref","first-page":"175","DOI":"10.1016\/j.cell.2011.10.050","article-title":"Membrane tension maintains cell polarity by confining signals to the leading edge during neutrophil migration","volume":"148","author":"Houk","year":"2012","journal-title":"Cell"},{"key":"2023070318410998400_ref40","doi-asserted-by":"crossref","first-page":"1409","DOI":"10.1016\/j.cub.2013.05.063","article-title":"Membrane tension in rapidly moving cells is determined by cytoskeletal forces","volume":"23","author":"Lieber","year":"2013","journal-title":"Curr. Biol."},{"key":"2023070318410998400_ref41","doi-asserted-by":"crossref","first-page":"20170145","DOI":"10.1098\/rstb.2017.0145","article-title":"Joining forces: crosstalk between biochemical signalling and physical forces orchestrates cellular polarity and dynamics","volume":"373","author":"Saha","year":"2018","journal-title":"Philos. Trans. R. Soc. Lond. Ser. B Biol. Sci."},{"key":"2023070318410998400_ref42","doi-asserted-by":"crossref","first-page":"11","DOI":"10.1016\/j.ceb.2020.04.001","article-title":"Pay attention to membrane tension: Mechanobiology of the cell surface","volume":"66","author":"Sitarska","year":"2020","journal-title":"Curr. Opin. Cell Biol."},{"key":"2023070318410998400_ref43","doi-asserted-by":"crossref","first-page":"8347","DOI":"10.1158\/0008-5472.CAN-09-4149","article-title":"Cdc42-interacting protein 4 promotes breast cancer cell invasion and formation of invadopodia through activation of N-WASp","volume":"70","author":"Pichot","year":"2010","journal-title":"Cancer Res."},{"key":"2023070318410998400_ref44","doi-asserted-by":"crossref","first-page":"3080","DOI":"10.1038\/onc.2012.317","article-title":"Transducer of Cdc42-dependent actin assembly promotes breast cancer invasion and metastasis","volume":"32","author":"Chander","year":"2013","journal-title":"Oncogene"},{"key":"2023070318410998400_ref45","doi-asserted-by":"crossref","first-page":"203","DOI":"10.1016\/j.cell.2004.06.027","article-title":"Toca-1 mediates Cdc42-dependent actin nucleation by activating the N-WASP-WIP complex","volume":"118","author":"Ho","year":"2004","journal-title":"Cell"},{"key":"2023070318410998400_ref46","doi-asserted-by":"crossref","first-page":"749","DOI":"10.1038\/ncb3162","article-title":"Feedback regulation between plasma membrane tension and membrane-bending proteins organizes cell polarity during leading edge formation","volume":"17","author":"Tsujita","year":"2015","journal-title":"Nat. Cell Biol."},{"key":"2023070318410998400_ref47","doi-asserted-by":"crossref","first-page":"72","DOI":"10.1016\/j.mvr.2007.05.003","article-title":"Tumor microvasculature and microenvironment: targets for anti-angiogenesis and normalization","volume":"74","author":"Fukumura","year":"2007","journal-title":"Microvasc. Res."},{"key":"2023070318410998400_ref48","first-page":"4264","article-title":"Tumor angiogenesis and interstitial hypertension","volume":"56","author":"Boucher","year":"1996","journal-title":"Cancer Res."},{"key":"2023070318410998400_ref49","doi-asserted-by":"crossref","first-page":"2943","DOI":"10.1158\/0008-5472.CAN-12-4354","article-title":"Vascular normalization as an emerging strategy to enhance cancer immunotherapy","volume":"73","author":"Huang","year":"2013","journal-title":"Cancer Res."},{"key":"2023070318410998400_ref50","doi-asserted-by":"crossref","first-page":"6607","DOI":"10.1158\/0008-5472.CAN-18-0498","article-title":"LPA4-mediated vascular network formation increases the efficacy of anti-PD-1 therapy against brain tumors","volume":"78","author":"Eino","year":"2018","journal-title":"Cancer Res."}],"container-title":["The Journal of Biochemistry"],"original-title":[],"language":"en","link":[{"URL":"https:\/\/academic.oup.com\/jb\/advance-article-pdf\/doi\/10.1093\/jb\/mvad024\/49806203\/mvad024.pdf","content-type":"application\/pdf","content-version":"am","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jb\/article-pdf\/174\/1\/5\/50790554\/mvad024.pdf","content-type":"application\/pdf","content-version":"vor","intended-application":"syndication"},{"URL":"https:\/\/academic.oup.com\/jb\/article-pdf\/174\/1\/5\/50790554\/mvad024.pdf","content-type":"unspecified","content-version":"vor","intended-application":"similarity-checking"}],"deposited":{"date-parts":[[2023,7,3]],"date-time":"2023-07-03T19:08:08Z","timestamp":1688411288000},"score":1,"resource":{"primary":{"URL":"https:\/\/academic.oup.com\/jb\/article\/174\/1\/5\/7080125"}},"subtitle":[],"short-title":[],"issued":{"date-parts":[[2023,3,17]]},"references-count":50,"journal-issue":{"issue":"1","published-online":{"date-parts":[[2023,3,17]]},"published-print":{"date-parts":[[2023,6,30]]}},"URL":"https:\/\/doi.org\/10.1093\/jb\/mvad024","relation":{},"ISSN":["0021-924X","1756-2651"],"issn-type":[{"value":"0021-924X","type":"print"},{"value":"1756-2651","type":"electronic"}],"subject":[],"published-other":{"date-parts":[[2023,7]]},"published":{"date-parts":[[2023,3,17]]}}}