A two-way communication between microglial cells and angiogenic sprouts regulates angiogenesis in aortic ring cultures

PLoS ONE

Volumn 6, Issue 1, 2011, Pages

  Rymo, Simin F ^a   Gerhardt, Holger ^b   Sand, Fredrik Wolfhagen ^c   Lang, Richard ^d   Uv, Anne ^a   Betsholtz, Christer ^e  

^a UNIVERSITY OF GOTHENBURG   (Sweden)

^b IMPERIAL CANCER RESEARCH FUND   (United Kingdom)

^c LUND UNIVERSITY   (Sweden)

^d UNIVERSITY OF CINCINNATI   (United States)

^e KAROLINSKA INSTITUTE   (Sweden)

Author keywords

[No Author keywords available]

Indexed keywords

VASCULOTROPIN A;

ANGIOGENESIS; ANIMAL CELL; ANIMAL TISSUE; ARTICLE; CELL COMMUNICATION; CELL CONTACT; CELL CULTURE; CELL MIGRATION; CELL STIMULATION; CELL STRUCTURE; CELLULAR DISTRIBUTION; CONTROLLED STUDY; CULTURE MEDIUM; ENDOTHELIUM; IN VITRO STUDY; IN VIVO STUDY; MICROGLIA; MOUSE; NONHUMAN; VASCULAR RING; AORTA; CELL SHAPE; CYTOLOGY; DRUG EFFECT; PHYSIOLOGY; PSEUDOPODIUM; RETINA; SECRETION; ULTRASTRUCTURE; VASCULAR ENDOTHELIUM;

MAMMALIA;

AORTA; CELL COMMUNICATION; CELL SHAPE; CELLS, CULTURED; CULTURE MEDIA, CONDITIONED; ENDOTHELIUM, VASCULAR; MICROGLIA; NEOVASCULARIZATION, PHYSIOLOGIC; PSEUDOPODIA; RETINA;

EID: 79251551934     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0015846     Document Type: Article

References (36)

1. Carmeliet P (2005) Angiogenesis in life, disease and medicine. Nature 438: 932-936.
2. Hellström M, Phng LK, Hofmann JJ, Wallgard E, Coultas L, et al. (2007) Dll4 signalling through Notch1 regulates formation of tip cells during angiogenesis. Nature 445: 776-780.
3. Siekmann AF, Lawson ND (2007) Notch signalling limits angiogenic cell behaviour in developing zebrafish arteries. Nature 445: 781-784.
4. Leslie JD, Ariza-McNaughton L, Bermange AL, McAdow R, Johnson SL, et al. (2007) Endothelial signalling by the Notch ligand Delta-like 4 restricts angiogenesis. Development 134: 839-844.
5. Suchting S, Freitas C, le Noble F, Benedito R, Bréant C, et al. (2007) The Notch ligand Delta-like 4 negatively regulates endothelial tip cell formation and vessel branching. Proc Natl Acad Sci USA 104: 3225-3230.
6. Lobov IB, Renard RA, Papadopoulos N, Gale NW, Thurston G, et al. (2007) Delta-like ligand 4 (Dll4) is induced by VEGF as a negative regulator of angiogenic sprouting. Proc Natl Acad Sci USA 104: 3219-3224.
7. Stone J, Dreher Z (1987) Relationship between astrocytes, ganglion cells and vasculature of the retina. J Comp Neurol 255: 35-49.
8. Gerhardt H, Golding M, Fruttiger M, Ruhrberg C, Lundkvist A, et al. (2003) VEGF guides angiogenic sprouting utilizing endothelial tip cell filopodia. J Cell Biol 161: 1163-1177.
9. Stone J, Itin A, Alon T, Pe'er J, Gnessin H, et al. (1995) Development of retinal vasculature is mediated by hypoxia-induced vascular endothelial growth factor (VEGF) expression by neuroglia. J Neurosci 15: 4738-4747.
10. Gerhardt H, Ruhrberg C, Abramsson A, Fujisawa H, Shima D, et al. (2004) Neuropilin-1 is required for endothelial tip cell guidance in the developing central nervous system. Dev Dyn 231: 503-509.
11. Eremina V, Sood M, Haigh J, Nagy A, Lajoie G, et al. (2003) Glomerularspecific alterations of VEGF-A expression lead to distinct congenital and acquired renal diseases. J Clin Invest 111: 707-716.
12. Luttun A, Tjwa M, Moons L, Wu Y, Angelillo-Scherrer A, et al. (2002) Revascularization of ischemic tissues by PlGF treatment, and inhibition of tumor angiogenesis, arthritis and atherosclerosis by anti-Flt1. Nat Med 8: 831-840.
13. Pipp F, Heil M, Issbrücker K, Ziegelhoeffer T, Martin S, et al. (2003) VEGFR-1-selective VEGF homologue PlGF is arteriogenic: evidence for a monocytemediated mechanism. Circ Res 92: 378-385.
14. Kubota Y, Takubo K, Shimizu T, Ohno H, Kishi K, et al. (2009) M-CSF inhibition selectively targets pathological angiogenesis and lymphangiogenesis. J Exp Med 206: 1089-1102.
15. Lin EY, Pollard JW (2007) Tumor-associated macrophages press the angiogenic switch in breast cancer. Cancer Res 67: 5064-5066.
16. Grunewald M, Avraham I, Dor Y, Bachar-Lustig E, Itin A, et al. (2006) VEGFinduced adult neovascularization: recruitment, retention, and role of accessory cells. Cell 124: 175-189.
17. Barron KD (1995) The microglial cell. A historical review. J Neurol Sci 134 Suppl: 57-68.
18. Jordan FL, Thomas WE (1988) Brain macrophages: questions of origin and interrelationship. Brain Res 472: 165-178.
19. Perry VH, Gordon S (1988) Macrophages and microglia in the nervous system. Trends Neurosci 11: 273-277.
20. Graeber MB, Streit WJ (2010) Microglia: biology and pathology. Acta Neuropathol 119: 89-105.
21. Perry VH, Hume DA, Gordon S (1985) Immunohistochemical localization of macrophages and microglia in the adult and developing mouse brain. Neuroscience 15: 313-326.
22. Checchin D, Sennlaub F, Levavasseur E, Leduc M, Chemtob S (2006) Potential role of microglia in retinal blood vessel formation. Invest Ophthalmol Vis Sci 47: 3595-3602.
23. Fantin A, Vieira JM, Gestri G, Denti L, Schwarz Q, et al. (2010) Tissue macrophages act as cellular chaperones for vascular anastomosis downstream of VEGF-mediated endothelial tip cell induction. Blood.
24. Espinosa-Heidmann DG, Suner IJ, Hernandez EP, Monroy D, Csaky KG, et al. (2003) Macrophage depletion diminishes lesion size and severity in experimental choroidal neovascularization. Invest Ophthalmol Vis Sci 44: 3586-3592.
25. Sakurai E, Anand A, Ambati BK, van Rooijen N, Ambati J (2003) Macrophage depletion inhibits experimental choroidal neovascularization. Invest Ophthalmol Vis Sci 44: 3578-3585.
26. Yoshida H, Hayashi S, Kunisada T, Ogawa M, Nishikawa S, et al. (1990) The murine mutation osteopetrosis is in the coding region of the macrophage colony stimulating factor gene. Nature 345: 442-444.
27. McKercher SR, Torbett BE, Anderson KL, Henkel GW, Vestal DJ, et al. (1996) Targeted disruption of the PU.1 gene results in multiple hematopoietic abnormalities. EMBO J 15: 5647-5658.
28. Anderson KL, Smith KA, Conners K, McKercher SR, Maki RA, et al. (1998) Myeloid development is selectively disrupted in PU.1 null mice. Blood 91: 3702-3710.
29. Nicosia RF, Ottinetti A (1990) Growth of microvessels in serum-free matrix culture of rat aorta. A quantitative assay of angiogenesis in vitro. Lab Invest 63: 115-122.
30. Stockmann C, Doedens A, Weidemann A, Zhang N, Takeda N, et al. (2008) Deletion of vascular endothelial growth factor in myeloid cells accelerates tumorigenesis. Nature 456: 814-818.
31. Mitchell P, Korobelnik JF, Lanzetta P, Holz FG, Prünte C, et al. (2010) Ranibizumab (Lucentis) in neovascular age-related macular degeneration: evidence from clinical trials. Br J Ophthalmol 94: 2-13.
32. Dixon JA, Oliver SC, Olson JL, Mandava N (2009) VEGF Trap-Eye for the treatment of neovascular age-related macular degeneration. Expert Opin Investig Drugs 18: 1573-1580.
33. Aplin AC, Fogel E, Zorzi P, Nicosia RF (2008) The aortic ring model of angiogenesis. Meth Enzymol 443: 119-136.
34. Nicosia RF (2009) The aortic ring model of angiogenesis: a quarter century of search and discovery. J Cell Mol Med 13: 4113-4136.
35. Gelati M, Aplin AC, Fogel E, Smith KD, Nicosia RF (2008) The angiogenic response of the aorta to injury and inflammatory cytokines requires macrophages. J Immunol 181: 5711-5719.
36. Zorzi P, Aplin AC, Smith KD, Nicosia RF (2010) Technical Advance: The rat aorta contains resident mononuclear phagocytes with proliferative capacity and proangiogenic properties. Journal of leukocyte biology.