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Pericyte involvement in capillary sprouting during angiogenesis in situ

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Summary

To investigate the participation of microvascular pericytes in the process of capillary sprouting, we examined whole-mount preparations of the rat mesentery by use of a double immunofluorescence approach. Angiogenesis was induced by intraperitoneal injections of either the mast cell-degranulating substance compound 48/80 or tumor cell-conditioned medium. Capillary sprouts were visualized by staining with rhodaminconjugated phalloidin and pericytes were simultaneosly stained by an antibody to the intermediate filament protein desmin. Developing pericytes were negative for the smooth-muscle isoform of α-actin, bbut were clearly reactive for desmin. Pericytes appear to be involved in the carliest stages of capillary sprouting. Pericytes were regularly found lying at and in front of the advancing tips of endothelial sprouts. At many sites pericytes were seen to bridge the gap between the leading edges of opposing endothelial sprouts, which were apparently preparing to merge, suggesting that pericytic processes may serve as guiding structures aiding outgrowth of endothelial cells.

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References

  • Antonelli-Orlidge A, Saunders KB, Smith SR, D'Amore PA (1989) An activated form of transforming growth factor β is produced by cocultures of endothelial cells and pericytes. Proc Natl Acad Sci USA 86:4544–4548

    Google Scholar 

  • Ashton A, DeOliveira F (1966) Nomenclature of pericytes. Intramural and extramural. Br J Ophthalmol 50:119–123

    Google Scholar 

  • Bär Th, Wolff JR (1972) The formation of capillary basement membranes during internal vascularization of the rat's cerebral cortex. Z Zellforsch 133:231–248

    Google Scholar 

  • Blood CH, Zetter BR (1990) Tumor interactions with the vasculature: angiogenesis and tumor metastasis. Biochem Biophys Acta 1032:89–118

    Google Scholar 

  • Crocker DJ, Murad TM, Geer JC (1970) Role of the pericyte in wound healing. An ultrastructural study. Exp Mol Pathol 13:51–65

    Google Scholar 

  • Diaz-Flores L, Gutiérrez R, Varela H, Rancel N, Valladares F (1991) Microvascular pericytes: a review of their morphological and functional characteristics. Histol Histopathol 6:269–286

    Google Scholar 

  • Drenckhahn D, Franz H (1986) Identification of actin, α-actinin, and vinculin-containing plaques at the lateral membrane of epithelial cells. J Cell Biol 102:1843–1852

    Google Scholar 

  • Drenckhahn D, Frotscher M, Kaiser HW (1984) Concentration of F-actin in synaptic formations of the hippocampus as visualized by staining with fluorescent phalloidin. Brain Res 300:381–384

    Google Scholar 

  • Folkman J, Haudenschild C (1980) Angiogenesis in vitro. Nature 288:551–556

    Google Scholar 

  • Folkman J, Klagsbrun M (1987) Angiogenic factors. Science 235:442–447

    Google Scholar 

  • Fujimoto T, Singer SJ (1987) Immunocytochemical studies of desmin and vimentin in pericapillary cells of chicken. J Histochem Cytochem 35:1105–1115

    Google Scholar 

  • Herman IM, D'Amore PA (1985) Microvascular pericytes contain muscle and non-muscle actins. J Cell Biol 101:43–52

    Google Scholar 

  • Joyce NC, DeCamilli P, Boyles J (1984) Pericytes, like vascular smooth muscle cells, are immunocytochemically positive for cyclic GMP-dependent protein kinase. Microvasc Res 28:206–219

    Google Scholar 

  • Joyce NC, Haire MF, Palade GE (1985) Contractile proteins in pericytes. II. Immunocytochemical evidence for the presence of two isomyosins in graded concentrations. J Cell Biol 100:1387–1395

    Google Scholar 

  • Nakayasu K (1988) Origin of pericytes in neovascularization of rat cornea. Jpn J Ophthalmol 32:105–112

    Google Scholar 

  • Nehls V, Drenckhahn D (1991a) Heterogeneity of microvascular pericytes for smooth muscle type alpha-actin. J Cell Biol 113:147–154

    Google Scholar 

  • Nehls V, Drenckhahn D (1991b) Demonstration of actin filament stress fibers in microvascular endothelial cells in situ. Microvasc Res 42:103–112

    Google Scholar 

  • Norrby K, Jakobsson A, Sörbo J (1986) Mast cell-mediated angiogenesis: a novel experimental model using the rat mesentery. Virchows Arch [B] 52:195–206

    Google Scholar 

  • Orlidge A, D'Amore PA (1987) Inhibition of capillary endothelial cell growth by pericytes and smooth muscle cells. J Cell Biol 105:1455–1462

    Google Scholar 

  • Paku S, Paweletz N (1991) First steps of tumor-related angiogenesis. Lab Invest 65:334–346

    Google Scholar 

  • Paweletz N, Knierim M (1989) Tumor-related angiogenesis. Crit Rev Oncol/Hematol 9:197–242

    Google Scholar 

  • Pepper MS, Belin D, Montesano R, Orci L, Vassalli J-D (1990) Transforming growth factor-beta 1 modulates basic fibroblast growth factor-induced proteolytic and angiogenic properties of endothelial cells in vitro. J Cell Biol 111:743–755

    Google Scholar 

  • Rhodin JAG, Fujita H (1989) Capillary growth in the mesentery of normal young rats. Intravital video and electron microscope analyses. J Submicrosc Cytol Pathol 21:1–34

    Google Scholar 

  • Sappino AP, Schürch W, Gabbiani G (1990) Biology of disease. Differentiation repertoire of fibroblastic cells: Expression of cytoskeletal proteins as marker of phenotypic modulations. Lab Invest 63:144–161

    Google Scholar 

  • Schlingemann RO, Rietveld FJR, Kwaspen F, Kerkhof PCM van de, Waal RMW de, Ruiter DJ (1991) Differential expression of markers for endothelial cells, pericytes, and basal lamina in the microvasculature of tumors and granulation tissue. Am J Pathol 138:1335–1347

    Google Scholar 

  • Sims DE (1986) The pericyte — a review. Tissue Cell 18:153–174

    Google Scholar 

  • Skalli O, Ropraz P, Trzeciak A, Benzonana G, Gillessen D, Gabbiani G (1986) A mAb against alpha-smooth muscle actin: A new probe for smooth muscle differentiation. J Cell Biol 103:2787–2796

    Google Scholar 

  • Skalli O, Pelte M-F, Peclet M-C, Gabbiani G, Gugliotta P, Bussolati G, Ravazzola M, Orci L (1989) Alpha-smooth muscle actin, a differentiation marker of smooth muscle cells, is present in microfilamentous bundles of pericytes. J Histochem Cytochem 37:315–321

    Google Scholar 

  • Verhoeven D, Buyssens N (1988) Desmin-positive stellate cells associated with angiogenesis in a tumour and non-tumour system. Virchows Arch [B] 54:263–272

    Google Scholar 

  • Wakui S (1988) Two- and three-dimensional ultrastructural observation of two cell angiogenesis in human granulation tissue. Virch Arch [B] 56:127–139

    Google Scholar 

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Nehls, V., Denzer, K. & Drenckhahn, D. Pericyte involvement in capillary sprouting during angiogenesis in situ. Cell Tissue Res. 270, 469–474 (1992). https://doi.org/10.1007/BF00645048

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  • DOI: https://doi.org/10.1007/BF00645048

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