Coalescent angiogenesis-evidence for a novel concept of vascular network maturation.
Capillary mesh
Chorioallantoic membrane (CAM)
Coalescent angiogenesis
Intravital microscopy
Intussusception
Splitting angiogenesis
Sprouting angiogenesis
Tissue islands
Journal
Angiogenesis
ISSN: 1573-7209
Titre abrégé: Angiogenesis
Pays: Germany
ID NLM: 9814575
Informations de publication
Date de publication:
02 2022
02 2022
Historique:
received:
29
10
2021
accepted:
07
11
2021
pubmed:
15
12
2021
medline:
19
2
2022
entrez:
14
12
2021
Statut:
ppublish
Résumé
Angiogenesis describes the formation of new blood vessels from pre-existing vascular structures. While the most studied mode of angiogenesis is vascular sprouting, specific conditions or organs favor intussusception, i.e., the division or splitting of an existing vessel, as preferential mode of new vessel formation. In the present study, sustained (33-h) intravital microscopy of the vasculature in the chick chorioallantoic membrane (CAM) led to the hypothesis of a novel non-sprouting mode for vessel generation, which we termed "coalescent angiogenesis." In this process, preferential flow pathways evolve from isotropic capillary meshes enclosing tissue islands. These preferential flow pathways progressively enlarge by coalescence of capillaries and elimination of internal tissue pillars, in a process that is the reverse of intussusception. Concomitantly, less perfused segments regress. In this way, an initially mesh-like capillary network is remodeled into a tree structure, while conserving vascular wall components and maintaining blood flow. Coalescent angiogenesis, thus, describes the remodeling of an initial, hemodynamically inefficient mesh structure, into a hierarchical tree structure that provides efficient convective transport, allowing for the rapid expansion of the vasculature with maintained blood supply and function during development.
Identifiants
pubmed: 34905124
doi: 10.1007/s10456-021-09824-3
pii: 10.1007/s10456-021-09824-3
pmc: PMC8669669
doi:
Types de publication
Journal Article
Research Support, Non-U.S. Gov't
Langues
eng
Sous-ensembles de citation
IM
Pagination
35-45Informations de copyright
© 2021. The Author(s).
Références
Risau W (1997) Mechanisms of angiogenesis. Nature 386:671–674. https://doi.org/10.1038/386671a0
doi: 10.1038/386671a0
pubmed: 9109485
Patan S (2000) Vasculogenesis and angiogenesis as mechanisms of vascular network formation, growth and remodeling. J Neurooncol 50:1–15. https://doi.org/10.1023/A:1006493130855
doi: 10.1023/A:1006493130855
pubmed: 11245270
Zakrzewicz A, Secomb TW, Pries AR (2002) Angioadaptation: keeping the vascular system in shape. Physiology 17:197–201. https://doi.org/10.1152/nips.01395.2001
doi: 10.1152/nips.01395.2001
Betz C, Lenard A, Belting H-G, Affolter M (2016) Cell behaviors and dynamics during angiogenesis. Development 143:2249–2260. https://doi.org/10.1242/dev.135616
doi: 10.1242/dev.135616
pubmed: 27381223
Udan RS, Culver JC, Dickinson ME (2013) Understanding vascular development. Wiley Interdiscip Rev Dev Biol 2:327–346. https://doi.org/10.1002/wdev.91
doi: 10.1002/wdev.91
pubmed: 23799579
Adams RH, Eichmann A (2010) Axon guidance molecules in vascular patterning. Cold Spring Harb Perspect Biol 2:a001875. https://doi.org/10.1101/cshperspect.a001875
doi: 10.1101/cshperspect.a001875
pubmed: 20452960
pmcid: 2857165
Shibuya M (2001) Structure and dual function of vascular endothelial growth factor receptor-1 (Flt-1). Int J Biochem Cell Biol 33:409–420. https://doi.org/10.1016/S1357-2725(01)00026-7
doi: 10.1016/S1357-2725(01)00026-7
pubmed: 11312109
Burri PH, Tarek MR (1990) A novel mechanism of capillary growth in the rat pulmonary microcirculation. Anat Rec 228:35–45. https://doi.org/10.1002/ar.1092280107
doi: 10.1002/ar.1092280107
pubmed: 2240600
Burri PH, Hlushchuk R, Djonov V (2004) Intussusceptive angiogenesis: its emergence, its characteristics, and its significance. Dev Dyn 231:474–488. https://doi.org/10.1002/dvdy.20184
doi: 10.1002/dvdy.20184
pubmed: 15376313
De Spiegelaere W, Casteleyn C, Van den Broeck W et al (2012) Intussusceptive angiogenesis: a biologically relevant form of angiogenesis. J Vasc Res 49:390–404. https://doi.org/10.1159/000338278
doi: 10.1159/000338278
pubmed: 22739226
Lee GS, Filipovic N, Miele LF et al (2010) Blood flow shapes intravascular pillar geometry in the chick chorioallantoic membrane. J Angiogenes Res 2:11. https://doi.org/10.1186/2040-2384-2-11
doi: 10.1186/2040-2384-2-11
pubmed: 20609245
pmcid: 2911408
Eldridge L, Wagner EM (2019) Angiogenesis in the lung. J Physiol 597:1023–1032. https://doi.org/10.1113/JP275860
doi: 10.1113/JP275860
pubmed: 30022479
Mentzer SJ, Konerding MA (2014) Intussusceptive angiogenesis: expansion and remodeling of microvascular networks. Angiogenesis 17:499–509. https://doi.org/10.1007/s10456-014-9428-3
doi: 10.1007/s10456-014-9428-3
pubmed: 24668225
pmcid: 4063884
Ackermann M, Mentzer SJ, Kolb M, Jonigk D (2020) Inflammation and intussusceptive angiogenesis in COVID-19: everything in and out of flow. Eur Respir J. https://doi.org/10.1183/13993003.03147-2020
doi: 10.1183/13993003.03147-2020
pubmed: 33008942
pmcid: 7530910
Dimova I, Karthik S, Makanya A et al (2019) SDF-1/CXCR4 signalling is involved in blood vessel growth and remodelling by intussusception. J Cell Mol Med. https://doi.org/10.1111/jcmm.14269
doi: 10.1111/jcmm.14269
pubmed: 30950188
pmcid: 6533523
Djonov V, Baum O, Burri PH (2003) Vascular remodeling by intussusceptive angiogenesis. Cell Tissue Res 314:107–117. https://doi.org/10.1007/s00441-003-0784-3
doi: 10.1007/s00441-003-0784-3
pubmed: 14574551
Logothetidou A, De Spiegelaere W, Vandecasteele T et al (2018) Intussusceptive pillar formation in developing porcine glomeruli. JVR 55:278–286. https://doi.org/10.1159/000490905
doi: 10.1159/000490905
Uccelli A, Wolff T, Valente P et al (2019) Vascular endothelial growth factor biology for regenerative angiogenesis. Swiss Med Wkly. https://doi.org/10.4414/smw.2019.20011
doi: 10.4414/smw.2019.20011
pubmed: 30685867
Noden DM (1990) Origins and assembly of avian embryonic blood vessels. Ann N Y Acad Sci 588:236–249. https://doi.org/10.1111/j.1749-6632.1990.tb13214.x
doi: 10.1111/j.1749-6632.1990.tb13214.x
pubmed: 2192642
Caolo V, Peacock HM, Kasaai B et al (2018) Shear Stress and VE-Cadherin. Arterioscler Thromb Vasc Biol 38:2174–2183. https://doi.org/10.1161/ATVBAHA.118.310823
doi: 10.1161/ATVBAHA.118.310823
pubmed: 29930007
Drake CJ, Little CD (1999) VEGF and vascular fusion: implications for normal and pathological vessels. J Histochem Cytochem 47:1351–1356. https://doi.org/10.1177/002215549904701101
doi: 10.1177/002215549904701101
pubmed: 10544208
Karthik S, Djukic T, Kim J-D et al (2018) Synergistic interaction of sprouting and intussusceptive angiogenesis during zebrafish caudal vein plexus development. Sci Rep 8:9840. https://doi.org/10.1038/s41598-018-27791-6
doi: 10.1038/s41598-018-27791-6
pubmed: 29959335
pmcid: 6026200
Kolte D, McClung JA, Aronow WS (2016) Chapter 6 - Vasculogenesis and Angiogenesis. In: Aronow WS, McClung JA (eds) Translational Research in Coronary Artery Disease. Academic Press, Boston, pp 49–65
doi: 10.1016/B978-0-12-802385-3.00006-1
Makanya AN, Hlushchuk R, Baum O et al (2007) Microvascular endowment in the developing chicken embryo lung. Am J Physiol-Lung Cell Mol Physiol. https://doi.org/10.1152/ajplung.00371.2006
doi: 10.1152/ajplung.00371.2006
pubmed: 17244646
Pries AR, Secomb TW (2014) Making microvascular networks work: angiogenesis, remodeling, and pruning. Physiology (Bethesda) 29:446–455. https://doi.org/10.1152/physiol.00012.2014
doi: 10.1152/physiol.00012.2014
Chávez MN, Aedo G, Fierro FA et al (2016) Zebrafish as an emerging model organism to study angiogenesis in development and regeneration. Front Physiol. https://doi.org/10.3389/fphys.2016.00056
doi: 10.3389/fphys.2016.00056
pubmed: 27014075
pmcid: 4781882
Vimalraj S, Pichu S, Pankajam T et al (2019) Nitric oxide regulates intussusceptive-like angiogenesis in wound repair in chicken embryo and transgenic zebrafish models. Nitric Oxide 82:48–58. https://doi.org/10.1016/j.niox.2018.11.001
doi: 10.1016/j.niox.2018.11.001
pubmed: 30439561
Geudens I, Gerhardt H (2011) Coordinating cell behaviour during blood vessel formation. Development 138:4569–4583. https://doi.org/10.1242/dev.062323
doi: 10.1242/dev.062323
pubmed: 21965610
Okuda KS, Hogan BM (2020) Endothelial cell dynamics in vascular development: insights from live-imaging in zebrafish. Front Physiol 11:842. https://doi.org/10.3389/fphys.2020.00842
doi: 10.3389/fphys.2020.00842
pubmed: 32792978
pmcid: 7387577
Richard S, Brun A, Tedesco A et al (2018) Direct imaging of capillaries reveals the mechanism of arteriovenous interlacing in the chick chorioallantoic membrane. Commun Biol 1:235. https://doi.org/10.1038/s42003-018-0229-x
doi: 10.1038/s42003-018-0229-x
pubmed: 30588514
pmcid: 6303259
McFerrin HE, Olson SD, Gutschow MV et al (2014) Rapidly self-renewing human multipotent marrow stromal cells (hMSC) express sialyl Lewis X and actively adhere to arterial endothelium in a chick embryo model system. PLoS ONE 9:e105411. https://doi.org/10.1371/journal.pone.0105411
doi: 10.1371/journal.pone.0105411
pubmed: 25144321
pmcid: 4140774
Nowak-Sliwinska P, Segura T, Iruela-Arispe ML (2014) The chicken chorioallantoic membrane model in biology, medicine and bioengineering. Angiogenesis 17:779–804. https://doi.org/10.1007/s10456-014-9440-7
doi: 10.1007/s10456-014-9440-7
pubmed: 25138280
pmcid: 4583126
Rahn H, Paganelli CV, Ar A (1974) The avian egg: air-cell gas tension, metabolism and incubation time. Respir Physiol 22:297–309
doi: 10.1016/0034-5687(74)90079-6
Dusseau JW, Hutchins PM (1988) Hypoxia-induced angiogenesis in chick chorioallantoic membranes: a role for adenosine. Respir Physiol 71:33–44
doi: 10.1016/0034-5687(88)90113-2
Xiang W, Reglin B, Nitzsche B et al (2017) Dynamic remodeling of arteriolar collaterals after acute occlusion in chick chorioallantoic membrane. Microcirculation. https://doi.org/10.1111/micc.12351
doi: 10.1111/micc.12351
pubmed: 28075525
Pries AR (1988) A versatile video image analysis system for microcirculatory research. Int J Microcirc Clin Exp 7:327–345
pubmed: 3220679
Pries AR, Eriksson SE, Jepsen H (1990) Real-time oriented image analysis in microcirculatory research. In: Medtech ’89: Medical Imaging. International Society for Optics and Photonics, pp 257–263
Lee T-C, Kashyap RL, Chu C-N (1994) Building skeleton models via 3-D medial surface/axis thinning algorithms. CVGIP: Graph Models Image Process 56:462–478. https://doi.org/10.1006/cgip.1994.1042
doi: 10.1006/cgip.1994.1042
le Noble F, Moyon D, Pardanaud L et al (2004) Flow regulates arterial-venous differentiation in the chick embryo yolk sac. Development 131:361–375. https://doi.org/10.1242/dev.00929
doi: 10.1242/dev.00929
pubmed: 14681188
Belle J, Ysasi A, Bennett RD et al (2014) Stretch-induced intussuceptive and sprouting angiogenesis in the chick chorioallantoic membrane. Microvasc Res 95:60–67. https://doi.org/10.1016/j.mvr.2014.06.009
doi: 10.1016/j.mvr.2014.06.009
pubmed: 24984292
pmcid: 4188740
Makanya AN, Dimova I, Koller T et al (2016) Dynamics of the developing chick chorioallantoic membrane assessed by stereology, allometry. Immunohistochemistry and Molecular Analysis PLOS ONE 11:e0152821. https://doi.org/10.1371/journal.pone.0152821
doi: 10.1371/journal.pone.0152821
pubmed: 27046154
Wild R, Klems A, Takamiya M et al (2017) Neuronal sFlt1 and Vegfaa determine venous sprouting and spinal cord vascularization. Nat Commun. https://doi.org/10.1038/ncomms13991
doi: 10.1038/ncomms13991
pubmed: 29133867
pmcid: 5684212
Persson AB, Buschmann IR (2011) Vascular growth in health and disease. Front Mol Neurosci. https://doi.org/10.3389/fnmol.2011.00014
doi: 10.3389/fnmol.2011.00014
pubmed: 21904523
pmcid: 3160751
Prior BM, Yang HT, Terjung RL (2004) What makes vessels grow with exercise training? J Appl Physiol 97:1119–1128. https://doi.org/10.1152/japplphysiol.00035.2004
doi: 10.1152/japplphysiol.00035.2004
pubmed: 15333630
Jones EAV, le Noble F, Eichmann A (2006) What determines blood vessel structure? Genetic prespecification vs hemodynamics Physiology (Bethesda) 21:388–395. https://doi.org/10.1152/physiol.00020.2006
doi: 10.1152/physiol.00020.2006
Santamaría R, González-Álvarez M, Delgado R et al (2020) Remodeling of the microvasculature: may the blood flow be with you. Front Physiol 11:586852. https://doi.org/10.3389/fphys.2020.586852
doi: 10.3389/fphys.2020.586852
pubmed: 33178049
pmcid: 7593767
Makanya AN, Hlushchuk R, Djonov VG (2009) Intussusceptive angiogenesis and its role in vascular morphogenesis, patterning, and remodeling. Angiogenesis 12:113. https://doi.org/10.1007/s10456-009-9129-5
doi: 10.1007/s10456-009-9129-5
pubmed: 19194777
Gifre-Renom L, Jones EAV (2021) Vessel enlargement in development and pathophysiology. Front Physiol 12:639645. https://doi.org/10.3389/fphys.2021.639645
doi: 10.3389/fphys.2021.639645
pubmed: 33716786
pmcid: 7947306
Kuebler WM, Parthasarathi K, Lindert J (1985) Bhattacharya J (2007) Real-time lung microscopy. J Appl Physiol 102:1255–1264. https://doi.org/10.1152/japplphysiol.00786.2006
doi: 10.1152/japplphysiol.00786.2006
Tabuchi A, Mertens M, Kuppe H et al (1985) (2008) Intravital microscopy of the murine pulmonary microcirculation. J Appl Physiol 104:338–346. https://doi.org/10.1152/japplphysiol.00348.2007
doi: 10.1152/japplphysiol.00348.2007
Haas G, Fan S, Ghadimi M et al (2021) Different forms of tumor vascularization and their clinical implications focusing on vessel co-option in colorectal cancer liver metastases. Front Cell Dev Biol. https://doi.org/10.3389/fcell.2021.612774
doi: 10.3389/fcell.2021.612774
pubmed: 34422788
pmcid: 8373647
Pezzella F, Pastorino U, Tagliabue E et al (1997) Non-small-cell lung carcinoma tumor growth without morphological evidence of neo-angiogenesis. Am J Pathol 151:1417–1423
pubmed: 9358768
pmcid: 1858069
Majidpoor J, Mortezaee K (2021) Angiogenesis as a hallmark of solid tumors - clinical perspectives. Cell Oncol (Dordr). https://doi.org/10.1007/s13402-021-00602-3
doi: 10.1007/s13402-021-00602-3
Kuczynski EA, Vermeulen PB, Pezzella F et al (2019) Vessel co-option in cancer. Nat Rev Clin Oncol 16:469–493. https://doi.org/10.1038/s41571-019-0181-9
doi: 10.1038/s41571-019-0181-9
pubmed: 30816337
Bridgeman VL, Vermeulen PB, Foo S et al (2017) Vessel co-option is common in human lung metastases and mediates resistance to anti-angiogenic therapy in preclinical lung metastasis models. J Pathol 241:362–374. https://doi.org/10.1002/path.4845
doi: 10.1002/path.4845
pubmed: 27859259
Seano G, Jain RK (2020) Vessel co-option in glioblastoma: emerging insights and opportunities. Angiogenesis 23:9–16. https://doi.org/10.1007/s10456-019-09691-z
doi: 10.1007/s10456-019-09691-z
pubmed: 31679081
Deryugina EI, Quigley JP (2008) Chapter 2. Chick embryo chorioallantoic membrane models to quantify angiogenesis induced by inflammatory and tumor cells or purified effector molecules. Meth Enzymol 444:21–41. https://doi.org/10.1016/S0076-6879(08)02802-4
doi: 10.1016/S0076-6879(08)02802-4
Pawlikowska P, Tayoun T, Oulhen M et al (2020) Exploitation of the chick embryo chorioallantoic membrane (CAM) as a platform for anti-metastatic drug testing. Sci Rep 10:16876. https://doi.org/10.1038/s41598-020-73632-w
doi: 10.1038/s41598-020-73632-w
pubmed: 33037240
pmcid: 7547099