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Erschienen in: Angiogenesis 2/2019

04.01.2019 | Original Paper

Live imaging of angiogenesis during cutaneous wound healing in adult zebrafish

verfasst von: Chikage Noishiki, Shinya Yuge, Koji Ando, Yuki Wakayama, Naoki Mochizuki, Rei Ogawa, Shigetomo Fukuhara

Erschienen in: Angiogenesis | Ausgabe 2/2019

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Abstract

Angiogenesis, the growth of new blood vessels from pre-existing vessels, is critical for cutaneous wound healing. However, it remains elusive how endothelial cells (ECs) and pericytes (PCs) establish new blood vessels during cutaneous angiogenesis. We set up a live-imaging system to analyze cutaneous angiogenesis in adult zebrafish. First, we characterized basic structures of cutaneous vasculature. In normal skin tissues, ECs and PCs remained dormant to maintain quiescent blood vessels, whereas cutaneous injury immediately induced angiogenesis through the vascular endothelial growth factor signaling pathway. Tortuous and disorganized vessel networks formed within a few weeks after the injury and subsequently normalized through vessel regression in a few months. Analyses of the repair process of injured single blood vessels revealed that severed vessels elongated upon injury and anastomosed with each other. Thereafter, repaired vessels and adjacent uninjured vessels became tortuous by increasing the number of ECs. In parallel, PCs divided and migrated to cover the tortuous blood vessels. ECs sprouted from the PC-covered tortuous vessels, suggesting that EC sprouting does not require PC detachment from the vessel wall. Thus, live imaging of cutaneous angiogenesis in adult zebrafish enables us to clarify how ECs and PCs develop new blood vessels during cutaneous angiogenesis.
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Literatur
3.
Zurück zum Zitat Richardson R, Slanchev K, Kraus C, Knyphausen P, Eming S, Hammerschmidt M (2013) Adult zebrafish as a model system for cutaneous wound-healing research. J Invest Dermatol 133(6):1655–1665CrossRefPubMedPubMedCentral Richardson R, Slanchev K, Kraus C, Knyphausen P, Eming S, Hammerschmidt M (2013) Adult zebrafish as a model system for cutaneous wound-healing research. J Invest Dermatol 133(6):1655–1665CrossRefPubMedPubMedCentral
4.
5.
Zurück zum Zitat Larrivee B, Freitas C, Suchting S, Brunet I, Eichmann A (2009) Guidance of vascular development. Circ Res 104(4):428–441CrossRefPubMed Larrivee B, Freitas C, Suchting S, Brunet I, Eichmann A (2009) Guidance of vascular development. Circ Res 104(4):428–441CrossRefPubMed
6.
Zurück zum Zitat Chung AS, Ferrara N (2011) Developmental and pathological angiogenesis. Annu Rev Cell Dev Biol 27:563–584CrossRefPubMed Chung AS, Ferrara N (2011) Developmental and pathological angiogenesis. Annu Rev Cell Dev Biol 27:563–584CrossRefPubMed
7.
Zurück zum Zitat Augustin HG, Koh GY, Thurston G, Alitalo K (2009) Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol 10(3):165–177CrossRefPubMed Augustin HG, Koh GY, Thurston G, Alitalo K (2009) Control of vascular morphogenesis and homeostasis through the angiopoietin-Tie system. Nat Rev Mol Cell Biol 10(3):165–177CrossRefPubMed
15.
Zurück zum Zitat Fukuhara S, Zhang J, Yuge S, Ando K, Wakayama Y, Sakaue-Sawano A, Miyawaki A, Mochizuki N (2014) Visualizing the cell-cycle progression of endothelial cells in zebrafish. Dev Biol 393(1):10–23CrossRefPubMed Fukuhara S, Zhang J, Yuge S, Ando K, Wakayama Y, Sakaue-Sawano A, Miyawaki A, Mochizuki N (2014) Visualizing the cell-cycle progression of endothelial cells in zebrafish. Dev Biol 393(1):10–23CrossRefPubMed
16.
Zurück zum Zitat Kawakami K, Takeda H, Kawakami N, Kobayashi M, Matsuda N, Mishina M (2004) A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev Cell 7(1):133–144CrossRefPubMed Kawakami K, Takeda H, Kawakami N, Kobayashi M, Matsuda N, Mishina M (2004) A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish. Dev Cell 7(1):133–144CrossRefPubMed
18.
Zurück zum Zitat Kwon HB, Fukuhara S, Asakawa K, Ando K, Kashiwada T, Kawakami K, Hibi M, Kwon YG, Kim KW, Alitalo K, Mochizuki N (2013) The parallel growth of motoneuron axons with the dorsal aorta depends on Vegfc/Vegfr3 signaling in zebrafish. Development 140(19):4081–4090CrossRefPubMedPubMedCentral Kwon HB, Fukuhara S, Asakawa K, Ando K, Kashiwada T, Kawakami K, Hibi M, Kwon YG, Kim KW, Alitalo K, Mochizuki N (2013) The parallel growth of motoneuron axons with the dorsal aorta depends on Vegfc/Vegfr3 signaling in zebrafish. Development 140(19):4081–4090CrossRefPubMedPubMedCentral
20.
Zurück zum Zitat Xu C, Volkery S, Siekmann AF (2015) Intubation-based anesthesia for long-term time-lapse imaging of adult zebrafish. Nat Protoc 10(12):2064–2073CrossRefPubMed Xu C, Volkery S, Siekmann AF (2015) Intubation-based anesthesia for long-term time-lapse imaging of adult zebrafish. Nat Protoc 10(12):2064–2073CrossRefPubMed
22.
Zurück zum Zitat Olson KR (1996) Secondary circulation in fish: anatomical organization and physiological significance. J Exp Zool 275:172–185CrossRef Olson KR (1996) Secondary circulation in fish: anatomical organization and physiological significance. J Exp Zool 275:172–185CrossRef
28.
Zurück zum Zitat Saaristo A, Veikkola T, Enholm B, Hytonen M, Arola J, Pajusola K, Turunen P, Jeltsch M, Karkkainen MJ, Kerjaschki D, Bueler H, Yla-Herttuala S, Alitalo K (2002) Adenoviral VEGF-C overexpression induces blood vessel enlargement, tortuosity, and leakiness but no sprouting angiogenesis in the skin or mucous membranes. FASEB J 16(9):1041–1049. https://doi.org/10.1096/fj.01-1042com CrossRefPubMed Saaristo A, Veikkola T, Enholm B, Hytonen M, Arola J, Pajusola K, Turunen P, Jeltsch M, Karkkainen MJ, Kerjaschki D, Bueler H, Yla-Herttuala S, Alitalo K (2002) Adenoviral VEGF-C overexpression induces blood vessel enlargement, tortuosity, and leakiness but no sprouting angiogenesis in the skin or mucous membranes. FASEB J 16(9):1041–1049. https://​doi.​org/​10.​1096/​fj.​01-1042com CrossRefPubMed
31.
Zurück zum Zitat Sweeney MD, Ayyadurai S, Zlokovic BV (2016) Pericytes of the neurovascular unit: key functions and signaling pathways. Nat Neurosci 19(6):771–783CrossRefPubMedPubMedCentral Sweeney MD, Ayyadurai S, Zlokovic BV (2016) Pericytes of the neurovascular unit: key functions and signaling pathways. Nat Neurosci 19(6):771–783CrossRefPubMedPubMedCentral
33.
Zurück zum Zitat Cogan DG, Toussaint D, Kuwabara T (1961) Retinal vascular patterns. IV. Diabetic retinopathy. Arch Ophthalmol 66(3):366–378CrossRefPubMed Cogan DG, Toussaint D, Kuwabara T (1961) Retinal vascular patterns. IV. Diabetic retinopathy. Arch Ophthalmol 66(3):366–378CrossRefPubMed
38.
Zurück zum Zitat Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, Jeltsch M, Mitchell C, Alitalo K, Shima D, Betsholtz C (2003) VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161(6):1163–1177CrossRefPubMedPubMedCentral Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, Abramsson A, Jeltsch M, Mitchell C, Alitalo K, Shima D, Betsholtz C (2003) VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161(6):1163–1177CrossRefPubMedPubMedCentral
40.
Zurück zum Zitat Hellstrom M, Kalen M, Lindahl P, Abramsson A, Betsholtz C (1999) Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126(14):3047–3055PubMed Hellstrom M, Kalen M, Lindahl P, Abramsson A, Betsholtz C (1999) Role of PDGF-B and PDGFR-beta in recruitment of vascular smooth muscle cells and pericytes during embryonic blood vessel formation in the mouse. Development 126(14):3047–3055PubMed
Metadaten
Titel
Live imaging of angiogenesis during cutaneous wound healing in adult zebrafish
verfasst von
Chikage Noishiki
Shinya Yuge
Koji Ando
Yuki Wakayama
Naoki Mochizuki
Rei Ogawa
Shigetomo Fukuhara
Publikationsdatum
04.01.2019
Verlag
Springer Netherlands
Erschienen in
Angiogenesis / Ausgabe 2/2019
Print ISSN: 0969-6970
Elektronische ISSN: 1573-7209
DOI
https://doi.org/10.1007/s10456-018-09660-y

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