Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction
Open accessAbstract
Blood vessel networks expand in a 2-step process that begins with vessel sprouting and is followed by vessel anastomosis. Vessel sprouting is induced by chemotactic gradients of the vascular endothelial growth factor (VEGF), which stimulates tip cell protrusion. Yet it is not known which factors promote the fusion of neighboring tip cells to add new circuits to the existing vessel network. By combining the analysis of mouse mutants defective in macrophage development or VEGF signaling with live imaging in zebrafish, we now show that macrophages promote tip cell fusion downstream of VEGF-mediated tip cell induction. Macrophages therefore play a hitherto unidentified and unexpected role as vascular fusion cells. Moreover, we show that there are striking molecular similarities between the pro-angiogenic tissue macrophages essential for vascular development and those that promote the angiogenic switch in cancer, including the expression of the cell-surface proteins TIE2 and NRP1. Our findings suggest that tissue macrophages are a target for antiangiogenic therapies, but that they could equally well be exploited to stimulate tissue vascularization in ischemic disease.
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Microglia associate with endothelial tip cells during embryonic brain and postnatal retinal angiogenesis.
“microglia associate with endothelial tip cells, as demonstrated during embryonic brain and postnatal retinal angiogenesis”
From The impact of microglial activation on blood-brain barrier in brain diseases (2014) · cites this paper as Fantin et al., 2010
Microglia play a role in CNS angiogenesis by serving as a bridge to promote tip cell fusion, vascular plexus growth following sprouting induction and tip cell migration by VEGF.
“the authors suggest that microglia play a role in CNS angiogenesis by serving as a bridge to promote tip cell fusion, vascular plexus growth following sprouting induction and tip cell migration by VEGF (Fantin et al., 2010).”
From The impact of microglial activation on blood-brain barrier in brain diseases (2014) · cites this paper as Fantin et al., 2010
Microglia are present in the embryonic CNS territory prior to endothelial invasion and participate in cerebrovasculature growth, placing microglia-endothelium interactions as a possible key mechanism in BBB formation and regulation.
“The fact that microglia are present in the embryonic CNS territory prior to endothelial invasion and that they participate in cerebrovasculature growth place the interactions between microglia and CNS endothelium as a possible key mechanism in BBB formation and regulation.”
From The impact of microglial activation on blood-brain barrier in brain diseases (2014) · cites this paper as Fantin et al., 2010
During embryonic stages of CNS vascularization, EC stabilization and fusion are mediated by resident microglial cells.
“Fantin and collaborators present in vivo data showing that during embryonic stages of CNS vascularization, EC stabilization and fusion are mediated by resident microglial cells (Fantin et al., 2010).”
From The impact of microglial activation on blood-brain barrier in brain diseases (2014) · cites this paper as Fantin et al., 2010
Microglia localize in tight physical association with microvascular structures.
“they localize in tight physical association with microvascular structures (Fantin et al., 2010; Figure 1)”
From The impact of microglial activation on blood-brain barrier in brain diseases (2014) · cites this paper as Fantin et al., 2010
Resident microglia in the brain parenchyma interact with CNS microvessels.
“recent in vivo studies present evidence that resident microglia in the brain parenchyma also interact with CNS microvessels”
From The impact of microglial activation on blood-brain barrier in brain diseases (2014) · cites this paper as Fantin et al., 2010
In macrophage-deficient models, angiogenesis is impaired.
“in macrophage-deficient models, angiogenesis is impaired [85].”
From Immunology of Wound Healing (2018) · cites this paper as [85]
Anti-inflammatory, pro-repair macrophages produce VEGF, which promotes vessel sprouting, and express two transmembrane proteins that promote vascular anastomosis.
“Not only do anti-inflammatory, pro-repair macrophages produce VEGF, which promotes vessel sprouting, they also express two transmembrane proteins that have been shown to promote vascular anastomosis [80, 85, 86].”
From Immunology of Wound Healing (2018) · cites this paper as [85]
Angiogenesis occurs in a two-step process: vessel sprouting, followed by vessel anastomosis.
“New blood vessel formation, referred to as angiogenesis, occurs in a two-step process: vessel sprouting, followed by vessel anastomosis [85].”
From Immunology of Wound Healing (2018) · cites this paper as [85]
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- Authors
- Fantin, A., Vieira, J. M., Gestri, G., Denti, L., Schwarz, Q., Prykhozhij, S., Peri, F., Wilson, S. W., & Ruhrberg, C.
- Affiliations
- University College London (GB)
- European Molecular Biology Laboratory (DE)
- Corresponding author
- Fantin, Alessandro
- Vieira, Joaquim M.
- ORCID
- Venue
- Blood
- Publisher
- American Society of Hematology
- Published
- 2010-08-05
- Volume
- 116
- Issue
- 5
- Pages
- 829-840
- ISSN
- 0006-4971 (ISSN-L)
- 1528-0020
- PMC
- PMC2938310
- OpenAlex
- W2072172632
- Cited by
- 1,153
- References
- 55
- Citations by year
- 2026: 31 · 2025: 55 · 2024: 112 · 2023: 82 · 2022: 78 · 2021: 91 · 2020: 72 · 2019: 76 · 2018: 86 · 2017: 82 · 2016: 66 · 2015: 52 · 2014: 71 · 2013: 66 · 2012: 64
- FWCI
- 25.81
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Blood (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion)
- Archivio Istituzionale della Ricerca (Universita Degli Studi Di Milano) (submittedVersion, other-oa)
- Adelaide Research & Scholarship (AR&S) (University of Adelaide) (submittedVersion)
- UCL Discovery (University College London) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion)
- Zurich Open Repository and Archive (University of Zurich)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Health Sciences › Medicine › Oncology › Lymphatic System and Diseases
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cell Biology › Zebrafish Biomedical Research Applications
- Keywords
- tissue macrophages, vascular anastomosis, VEGF signaling, endothelial tip cells, vessel sprouting, angiogenesis, Tie2, neuropilin-1, anti-angiogenic therapy, ischemic diseases, macrophage development
- MeSH terms
- Proto-Oncogene Protein Spi-1, Animals, Endothelium, Vascular, Female, Macrophages, Male, Proto-Oncogene Proteins, Retinal Vessels, Rhombencephalon, Yolk Sac, Zebrafish, Trans-Activators, Macrophage Colony-Stimulating Factor, Cell Polarity, Mice, Knockout, Neovascularization, Physiologic, Receptor Protein-Tyrosine Kinases, Neuropilin-1, Vascular Endothelial Growth Factor A, Endothelial Cells, Receptor, TIE-2, Mice, Gene Knock-In Techniques
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