The DOI matches its Crossref record; 64 of the 64 references it cites were found in a registry or an index.
Angiogenic Role of LYVE-1–Positive Macrophages in Adipose Tissue
Open accessAbstract
Here we report the discovery of a characteristic dense vascular network (DVN) in the tip portion of epididymal adipose tissue in adult mice. The DVN is formed by angiogenesis rather than by vasculogenesis, and has functional blood circulation. This DVN and its subsequent branching may provide a new functional route for adipogenesis. The recruitment, infiltration, and accumulation of bone marrow-derived LYVE-1 + macrophages in the tip region are crucial for the formation of the DVN. Matrix metalloproteinases (MMPs) and the VEGF-VEGFR2 system are responsible not only for the formation of the DVN, but also for the recruitment and infiltration of LYVE-1 + macrophages into the epididymal adipose tissue tip region. SDF-1, but not the MCP-1-CCR2 system, is a critical factor in recruitment and ongoing retention of macrophages in this area. We also demonstrate that the tip region of epididymal adipose tissue is highly hypoxic, and thus provides a microenvironment conducive to the high expression and enhanced activities of VEGF, VEGFR2, MMPs, and SDF-1 in autocrine and paracrine manners, to create an ideal niche for the recruitment, retention, and angiogenic action of macrophages. These findings shed light on the complex interplay between macrophage infiltration, angiogenesis, and adipogenesis in the tip region of adult epididymal adipose tissue, and provide novel insight into the regulation of alternative outgrowth of adipose tissue.
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In the citing paper
“The hypoxic regions at the tip of the mouse epididymal fat pad have been shown to promote infiltration of a specific species of macrophage expressing the lymphatic endothelial marker LYVE-1.”
From The ominous triad of adipose tissue dysfunction: inflammation, fibrosis, and impaired angiogenesis. (2017) · cites this paper as [52]
In the citing paper
“This new vasculature provides the framework for adipogenesis and growth of the fat pad (52).”
From The ominous triad of adipose tissue dysfunction: inflammation, fibrosis, and impaired angiogenesis. (2017) · cites this paper as [52]
In the citing paper
“These LYVE-1 + macrophages promote angiogenesis through secretion of MMP-9, -12, and -7 to remodel the ECM and angiogenic factors like VEGF to stimulate the growth of a dense vascular network.”
From The ominous triad of adipose tissue dysfunction: inflammation, fibrosis, and impaired angiogenesis. (2017) · cites this paper as [52]
Citations
Cites
Obesity is associated with macrophage accumulation in adipose tissue
Weisberg, S. P., McCann, D., Desai, M., Rosenbaum, M., Leibel, R. L., & Ferrante, A. W. (2003) · Journal of Clinical Investigation · doi:10.1172/jci200319246 · Cited by 10,041
The biology of VEGF and its receptors
Ferrara, N., Gerber, H.-P., & LeCouter, J. (2003) · Nature Medicine · doi:10.1038/nm0603-669 · Cited by 9,591
Human Adipose Tissue Is a Source of Multipotent Stem Cells
Zuk, P. A., Zhu, M., Ashjian, P. H., Ugarte, D. A. D., Huang, J. I., Mizuno, H., Alfonso, Z. C., Fraser, J. K., Benhaim, P., & Hedrick, M. H. (2002) · Molecular Biology of the Cell · doi:10.1091/mbc.e02-02-0105 · Cited by 6,762
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Risau, W. (1997) · Nature · doi:10.1038/386671a0 · Cited by 5,727
Angiogenesis in life, disease and medicine
Carmeliet, P. (2005) · Nature · doi:10.1038/nature04478 · Cited by 3,551
Tumour-educated macrophages promote tumour progression and metastasis
Pollard, J. W. (2004) · Nature reviews. Cancer · doi:10.1038/nrc1256 · Cited by 3,414
VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia
Gerhardt, H., Golding, M., Fruttiger, M., Ruhrberg, C., Lundkvist, A., Abramsson, A., Jeltsch, M., Mitchell, C., Alitalo, K., Shima, D., et al. (2003) · The Journal of Cell Biology · doi:10.1083/jcb.200302047 · Cited by 2,894
Matrix metalloproteinase-9 triggers the angiogenic switch during carcinogenesis
Bergers, G., Brekken, R., McMahon, G., Vu, T. H., Itoh, T., Tamaki, K., Tanzawa, K., Thorpe, P., Itohara, S., Werb, Z., et al. (2000) · Nature Cell Biology · doi:10.1038/35036374 · Cited by 2,797
Self-citationKanda, H. (2006) · Journal of Clinical Investigation · doi:10.1172/jci26498 · Cited by 2,682
Research works printed but not linked: 2
- 10.1172/JCI20514 · DOI · Paper page
- 10.1093/ansci/82.3.925 · DOI
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Askia, H. (2022) · theses.fr (ABES) · doi:10.70675/0d09beffzcdaez4950za6c0z29a0dd68a41b
IRF5 and the metabolic adaptations of adipose tissue macrophages upon metabolic stress
Orliaguet, L. (2022) · theses.fr (ABES) · doi:10.70675/145b35eazd61az4b32zacc7z422afeae6061
An emerging role for eosinophils as pro-angiogenic drivers of adipose tissue beiging
Valentini, T. J., Spek, A. C., & Quinlan, K. G. R. (2026) · Clinical Science · doi:10.1042/cs20250051
The role of adipose tissue macrophages in adipose tissue fibrosis
Zhang, D., & Wu, N. (2026) · Metabolism · doi:10.1016/j.metabol.2026.156752
L’angiogenèse dans le tissu adipeux
Bouloumié, A., & Galitzky, J. (2013) · Springer eBooks · doi:10.1007/978-2-8178-0332-6_3
Metadata
- Authors
- Cho, C.-H., Jun Koh, Y., Han, J., Sung, H.-K., Jong Lee, H., Morisada, T., Schwendener, R. A., Brekken, R. A., Kang, G., Oike, Y., Choi, T.-S., Suda, T., Yoo, O.-J., & Koh, G. Y.
- Affiliations
- Korea Advanced Institute of Science and Technology (KR)
- From the National Research Laboratory of Vascular Biology and Department of Biological Sciences (C-H.C., Y.J.K., J.H., H-K. S., H.J.L., O-J.Y., G.Y.K.), Korea Advanced Institute of Science and Technology, Daejeon, Korea; Department of Cell Differentiation (T.M.,Y.O., T.S.), The Sakaguchi Laboratory, Keio University Internal Medicine, Tokyo, Japan; Laboratory of Liposome Research (R.A.S.), Institute of Molecular Cancer Research, University of Zurich, Switzerland; Departments of Surgery and...
- ORCID
- Venue
- Circulation Research
- Published
- 2007-03-02
- Volume
- 100
- Issue
- 4
- Pages
- e47-57
- ISSN
- 0009-7330 (ISSN-L)
- 1524-4571
- OpenAlex
- W2150586369
- Cited by
- 309
- References
- 64
- Citations by year
- 2026: 8 · 2025: 14 · 2024: 30 · 2023: 13 · 2022: 19 · 2021: 19 · 2020: 13 · 2019: 12 · 2018: 19 · 2017: 7 · 2016: 12 · 2015: 10 · 2014: 14 · 2013: 27 · 2012: 14
- FWCI
- 7.81
- Type
- journal article
- Language
- en
- Open access
- green
- www.zora.uzh.ch
- Licence
- other-oa
- Locations
- Circulation Research (publishedVersion)
- PubMed (publishedVersion)
- Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich) (submittedVersion, other-oa)
- Zurich Open Repository and Archive (University of Zurich)
- Funders
- Korea Advanced Institute of Science and Technology
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiovascular Disease and Adiposity
- Keywords
- adipose tissue angiogenesis, epididymal adipose tissue, adipogenesis, macrophage recruitment, CXCL12, VEGF/VEGFR2 signaling, matrix metalloproteinases, hypoxia, bone marrow-derived macrophages
- MeSH terms
- Adipose Tissue, Animals, Cell Movement, Epididymis, Glycoproteins, Macrophages, Male, Mice, Inbred C57BL, Mice, Knockout, Gene Expression Regulation, Developmental, Neovascularization, Physiologic, Membrane Transport Proteins, Adipogenesis, Mice
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