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Carbon ion radiation inhibits glioma and endothelial cell migration induced by secreted VEGF.

Liu Y, Liu Y, Sun C, Gan L, Zhang L, Mao A, Du Y, Zhou R, Zhang H - PLoS ONE (2014)

Bottom Line: Exposure to X-ray radiation-conditioned medium induced dose-dependent increases in cell migration and tube formation, which were accompanied by an upregulation of vascular endothelial growth factor (VEGF) and matrix metalloproteinase (MMP)-2 and -9 expression.However, glioma cells treated with conditioned medium of cells irradiated at a carbon ion dose of 4.0 Gy showed a marked decrease in migratory potential and VEGF secretion relative to non-irradiated cells.Taken together, these findings indicate that carbon ion may be superior to X-ray radiation for inhibiting tumorigenesis and angiogenesis through modulation of VEGF level in the glioma microenvironment.

View Article: PubMed Central - PubMed

Affiliation: Department of Radiation Medicine, Institute of Modern physics, Chinese Academy of Sciences, Lanzhou, China; Key Laboratory of Heavy Ion Radiation Biology and Medicine of Chinese Academy of Sciences, Lanzhou, China; Key Laboratory of Heavy Ion Radiation Medicine of Gansu Province, Lanzhou, China.

ABSTRACT
This study evaluated the effects of carbon ion and X-ray radiation and the tumor microenvironment on the migration of glioma and endothelial cells, a key process in tumorigenesis and angiogenesis during cancer progression. C6 glioma and human microvascular endothelial cells were treated with conditioned medium from cultures of glioma cells irradiated at a range of doses and the migration of both cell types, tube formation by endothelial cells, as well as the expression and secretion of migration-related proteins were evaluated. Exposure to X-ray radiation-conditioned medium induced dose-dependent increases in cell migration and tube formation, which were accompanied by an upregulation of vascular endothelial growth factor (VEGF) and matrix metalloproteinase (MMP)-2 and -9 expression. However, glioma cells treated with conditioned medium of cells irradiated at a carbon ion dose of 4.0 Gy showed a marked decrease in migratory potential and VEGF secretion relative to non-irradiated cells. The application of recombinant VEGF165 stimulated migration in glioma and endothelial cells, which was associated with increased FAK phosphorylation at Tyr861, suggesting that the suppression of cell migration by carbon ion radiation could be via VEGF-activated FAK signaling. Taken together, these findings indicate that carbon ion may be superior to X-ray radiation for inhibiting tumorigenesis and angiogenesis through modulation of VEGF level in the glioma microenvironment.

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Effect of radiation on endothelial cell migration as assessed by the Boyden chamber migration assay.Representative images are shown of migrating HMEC-1 cells exposed to conditioned medium from cultures of A. unirradiated or heavy ion-irradiated, or B. unirradiated or X ray-irradiated glioma cells. C. Quantification of the number of migratory endothelial cells is expressed as means ± standard error of the mean from three independent experiments, in which treatments were performed in triplicate. *P<0.05, ***P<0.001 vs. controls (0 Gy).
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pone-0098448-g002: Effect of radiation on endothelial cell migration as assessed by the Boyden chamber migration assay.Representative images are shown of migrating HMEC-1 cells exposed to conditioned medium from cultures of A. unirradiated or heavy ion-irradiated, or B. unirradiated or X ray-irradiated glioma cells. C. Quantification of the number of migratory endothelial cells is expressed as means ± standard error of the mean from three independent experiments, in which treatments were performed in triplicate. *P<0.05, ***P<0.001 vs. controls (0 Gy).

Mentions: Endothelial cell migration is essential for angiogenesis, a process that is closely associated with tumorigenesis and cancer progression. HMEC-1 cells incubated with conditioned media from carbon ion-irradiated cultures showed a decrease in migration at 4.0 Gy compared to controls (Fig. 2A, C), while in cells incubated with media from X-ray-irradiated cultures, a dose-dependent increase in migration was observed compared to control cells (Fig. 2B).


Carbon ion radiation inhibits glioma and endothelial cell migration induced by secreted VEGF.

Liu Y, Liu Y, Sun C, Gan L, Zhang L, Mao A, Du Y, Zhou R, Zhang H - PLoS ONE (2014)

Effect of radiation on endothelial cell migration as assessed by the Boyden chamber migration assay.Representative images are shown of migrating HMEC-1 cells exposed to conditioned medium from cultures of A. unirradiated or heavy ion-irradiated, or B. unirradiated or X ray-irradiated glioma cells. C. Quantification of the number of migratory endothelial cells is expressed as means ± standard error of the mean from three independent experiments, in which treatments were performed in triplicate. *P<0.05, ***P<0.001 vs. controls (0 Gy).
© Copyright Policy
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4043910&req=5

pone-0098448-g002: Effect of radiation on endothelial cell migration as assessed by the Boyden chamber migration assay.Representative images are shown of migrating HMEC-1 cells exposed to conditioned medium from cultures of A. unirradiated or heavy ion-irradiated, or B. unirradiated or X ray-irradiated glioma cells. C. Quantification of the number of migratory endothelial cells is expressed as means ± standard error of the mean from three independent experiments, in which treatments were performed in triplicate. *P<0.05, ***P<0.001 vs. controls (0 Gy).
Mentions: Endothelial cell migration is essential for angiogenesis, a process that is closely associated with tumorigenesis and cancer progression. HMEC-1 cells incubated with conditioned media from carbon ion-irradiated cultures showed a decrease in migration at 4.0 Gy compared to controls (Fig. 2A, C), while in cells incubated with media from X-ray-irradiated cultures, a dose-dependent increase in migration was observed compared to control cells (Fig. 2B).

Bottom Line: Exposure to X-ray radiation-conditioned medium induced dose-dependent increases in cell migration and tube formation, which were accompanied by an upregulation of vascular endothelial growth factor (VEGF) and matrix metalloproteinase (MMP)-2 and -9 expression.However, glioma cells treated with conditioned medium of cells irradiated at a carbon ion dose of 4.0 Gy showed a marked decrease in migratory potential and VEGF secretion relative to non-irradiated cells.Taken together, these findings indicate that carbon ion may be superior to X-ray radiation for inhibiting tumorigenesis and angiogenesis through modulation of VEGF level in the glioma microenvironment.

View Article: PubMed Central - PubMed

Affiliation: Department of Radiation Medicine, Institute of Modern physics, Chinese Academy of Sciences, Lanzhou, China; Key Laboratory of Heavy Ion Radiation Biology and Medicine of Chinese Academy of Sciences, Lanzhou, China; Key Laboratory of Heavy Ion Radiation Medicine of Gansu Province, Lanzhou, China.

ABSTRACT
This study evaluated the effects of carbon ion and X-ray radiation and the tumor microenvironment on the migration of glioma and endothelial cells, a key process in tumorigenesis and angiogenesis during cancer progression. C6 glioma and human microvascular endothelial cells were treated with conditioned medium from cultures of glioma cells irradiated at a range of doses and the migration of both cell types, tube formation by endothelial cells, as well as the expression and secretion of migration-related proteins were evaluated. Exposure to X-ray radiation-conditioned medium induced dose-dependent increases in cell migration and tube formation, which were accompanied by an upregulation of vascular endothelial growth factor (VEGF) and matrix metalloproteinase (MMP)-2 and -9 expression. However, glioma cells treated with conditioned medium of cells irradiated at a carbon ion dose of 4.0 Gy showed a marked decrease in migratory potential and VEGF secretion relative to non-irradiated cells. The application of recombinant VEGF165 stimulated migration in glioma and endothelial cells, which was associated with increased FAK phosphorylation at Tyr861, suggesting that the suppression of cell migration by carbon ion radiation could be via VEGF-activated FAK signaling. Taken together, these findings indicate that carbon ion may be superior to X-ray radiation for inhibiting tumorigenesis and angiogenesis through modulation of VEGF level in the glioma microenvironment.

Show MeSH
Related in: MedlinePlus