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Leptin induces vascular permeability and synergistically stimulates angiogenesis with FGF-2 and VEGF
Open accessAbstract
Most endocrine hormones are produced in tissues and organs with permeable microvessels that may provide an excess of hormones to be transported by the blood circulation to the distal target organ. Here, we investigate whether leptin, an endocrine hormone, induces the formation of vascular fenestrations and permeability, and we characterize its angiogenic property in the presence of other angiogenic factors. We provide evidence that leptin-induced new blood vessels are fenestrated. Under physiological conditions, capillary fenestrations are found in the leptin-producing adipose tissue in lean mice. In contrast, no vascular fenestrations were detected in the adipose tissue of leptin-deficient ob/ob mice. Thus, leptin plays a critical role in the maintenance and regulation of vascular fenestrations in the adipose tissue. Leptin induces a rapid vascular permeability response when administrated intradermally. Further, leptin synergistically stimulates angiogenesis with fibroblast growth factor (FGF)-2 and vascular endothelial growth factor (VEGF), the two most potent and commonly expressed angiogenic factors. These findings demonstrate that leptin has another new function—the increase of vascular permeability.
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“In addition to authentic angiogenic factors, AT secretes several important adipokines and endogenous angiogenesis inhibitors to modulate the balance of new blood vessel formation, including adiponectin (36,37), leptin (34), resistin (38), visfatin/thrombospondin 1 (39), and plasminogen activator inhibitor (40).”
From The ominous triad of adipose tissue dysfunction: inflammation, fibrosis, and impaired angiogenesis. (2017) · cites this paper as [34]
Citations
Cites
Leptin and the regulation of body weight in mammals
Friedman, J. M., & Halaas, J. L. (1998) · Nature · doi:10.1038/27376 · Cited by 5,405
Tumor Cells Secrete a Vascular Permeability Factor That Promotes Accumulation of Ascites Fluid
Senger, D. R., Galli, S. J., Dvořàk, A. M., Perruzzi, C. A., Harvey, V. S., & Dvorak, H. F. (1983) · Science · doi:10.1126/science.6823562 · Cited by 3,969
Abnormal splicing of the leptin receptor in diabetic mice
Lee, G.-H., Proenca, R., Montez, J. M., Carroll, K. M., Darvishzadeh, J. G., Lee, J. I., & Friedman, J. M. (1996) · Nature · doi:10.1038/379632a0 · Cited by 2,327
Biological Action of Leptin as an Angiogenic Factor
Sierra-Honigmann, M. R., Nath, A. K., Murakami, C., García‐Cardeña, G., Papapetropoulos, A., Sessa, W. C., Madge, L. A., Schechner, J. S., Schwabb, M. B., Polverini, P. J., et al. (1998) · Science · doi:10.1126/science.281.5383.1683 · Cited by 1,385
Nonadipose tissue production of leptin: Leptin as a novel placenta-derived hormone in humans
Masuzaki, H., Ogawa, Y., Sagawa, N., Hosoda, K., Matsumoto, T., Mise, H., Nishimura, H., Yoshimasa, Y., Tanaka, I., Mori, T., et al. (1997) · Nature Medicine · doi:10.1038/nm0997-1029 · Cited by 1,277
Roberts, W. G., & Palade, G. E. (1995) · Journal of Cell Science · doi:10.1242/jcs.108.6.2369 · Cited by 1,039
Clinical applications of angiogenic growth factors and their inhibitors
Ferrara, N., & Alitalo, K. (1999) · Nature Medicine · doi:10.1038/70928 · Cited by 1,004
Divergent Signaling Capacities of the Long and Short Isoforms of the Leptin Receptor
Bjørbæk, C., Uotani, S., da Silva, B., & Flier, J. S. (1997) · Journal of Biological Chemistry · doi:10.1074/jbc.272.51.32686 · Cited by 890
Dvorak, H. F., Nagy, J. A., Feng, D., Brown, L. F., & Dvorak, A. M. (1999) · Current Topics in Microbiology and Immunology · doi:10.1007/978-3-642-59953-8_6 · Cited by 743
Leptin, the Product of Ob Gene, Promotes Angiogenesis
Bouloumié, A., Drexler, H. C. A., Lafontan, M., & Busse, R. (1998) · Circulation Research · doi:10.1161/01.res.83.10.1059 · Cited by 715
Research works printed but not linked: 4
- H F Dvorak, J A Nagy, D Feng, L F Brown, A M Dvorak Curr Top Microbiol Immunol 237, 97–132 (1999).
- B M Kenyon, E E Voest, C C Chen, E Flynn, J Folkman, R J D'Amato Invest Ophthalmol Visual Sci 37, 1625–1632 (1996).
- E T Wei, J G Kiang, P Buchan, T W Smith J Pharmacol Exp Ther 238, 783–787 (1986).
- H Yoshiji, S Kuriyama, D K Ways, J Yoshii, Y Miyamoto, M Kawata, Y Ikenaka, H Tsujinoue, T Nakatani, M Shibuya, H Fukui Cancer Res 59, 4413–4418 (1999).
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Metadata
- Authors
- Cao, R., Brakenhielm, E., Wahlestedt, C., Thyberg, J., & Cao, Y.
- Affiliations
- Karolinska Institutet (SE)
- Laboratory of Angiogenesis Research, Microbiology and Tumor Biology Center, Center for Genomic Research, Department of Cell and Molecular Biology, Karolinska Institute, S-171 77 Stockholm, Sweden
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2001-05-08
- Volume
- 98
- Issue
- 11
- Pages
- 6390-6395
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC33478
- OpenAlex
- W2111796479
- Cited by
- 446
- References
- 29
- Citations by year
- 2026: 5 · 2025: 10 · 2024: 7 · 2023: 12 · 2022: 22 · 2021: 17 · 2020: 19 · 2019: 19 · 2018: 14 · 2017: 23 · 2016: 17 · 2015: 17 · 2014: 18 · 2013: 40 · 2012: 24
- FWCI
- 6.17
- Type
- journal article
- Language
- en
- Open access
- green
- europepmc.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Angiogenesis and VEGF in Cancer
- Life Sciences › Neuroscience › Neurology › Barrier Structure and Function Studies
- Health Sciences › Medicine › Endocrinology, Diabetes and Metabolism › Adipokines, Inflammation, and Metabolic Diseases
- Keywords
- leptin, vascular permeability, angiogenesis, FGF2, vascular endothelial growth factor, adipose tissue, ob/ob mice, hormone transport
- MeSH terms
- Adipose Tissue, Animals, Capillaries, Capillary Permeability, Cattle, Cell Division, Cells, Cultured, Cornea, Drug Synergism, Endothelium, Vascular, Female, Humans, Lymphokines, Male, Mice, Inbred BALB C, Mice, Inbred C57BL, Mice, Obese, Fibroblast Growth Factor 2, Endothelial Growth Factors, Corneal Neovascularization, Neovascularization, Physiologic, Leptin, Vascular Endothelial Growth Factors, Vascular Endothelial Growth Factor A, Mice
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