Recruitment of myeloid but not endothelial precursor cells facilitates tumor regrowth after local irradiation

Cancer Res. 2010 Jul 15;70(14):5679-85. doi: 10.1158/0008-5472.CAN-09-4446. Epub 2010 Jul 14.

Abstract

Tumor neovascularization and growth might be promoted by the recruitment of bone marrow-derived cells (BMDC), which include endothelial precursor cells and "vascular modulatory" myelomonocytic (CD11b+) cells. BMDCs may also drive tumor regrowth after certain chemotherapeutic and vascular disruption treatments. In this study, we evaluated the role of BMDC recruitment in breast and lung carcinoma xenograft models after local irradiation (LI). We depleted the bone marrow by including whole-body irradiation (WBI) of 6 Gy as part of a total tumor dose of 21 Gy, and compared the growth delay with the one achieved after LI of 21 Gy. In both models, the inclusion of WBI induced longer tumor growth delays. Moreover, WBI increased lung tumor control probability by LI. Exogenous delivery of BMDCs from radiation-naïve donors partially abrogated the WBI effect. Myeloid BMDCs, primarily macrophages, rapidly accumulated in tumors after LI. Intratumoral expression of stromal-derived factor 1alpha (SDF-1alpha), a chemokine that promotes tissue retention of BMDCs, was noted 2 days after LI. Conversely, treatment with an inhibitor of SDF-1alpha receptor CXCR4 (AMD3100) with LI significantly delayed tumor regrowth. However, when administered starting from 5 days post-LI, AMD3100 treatment was ineffective. Lastly, with restorative bone marrow transplantation of Tie2-GFP-labeled BMDC population, we observed an increased number of monocytes but not endothelial precursor cells in tumors that recurred following LI. Our results suggest that an increase in intratumoral SDF-1alpha triggered by LI recruits myelomonocytes/macrophages which promotes tumor regrowth.

Publication types

  • Research Support, N.I.H., Extramural

MeSH terms

  • Animals
  • Bone Marrow Cells / pathology
  • Cell Growth Processes / radiation effects
  • Chemokine CXCL12 / biosynthesis
  • Chemokine CXCL12 / genetics
  • Endothelial Cells / pathology
  • Female
  • Humans
  • Lung Neoplasms / blood supply
  • Lung Neoplasms / pathology*
  • Lung Neoplasms / radiotherapy
  • Male
  • Mammary Neoplasms, Experimental / blood supply
  • Mammary Neoplasms, Experimental / pathology*
  • Mammary Neoplasms, Experimental / radiotherapy
  • Mice
  • Mice, Nude
  • Myeloid Cells / pathology
  • Neovascularization, Pathologic / pathology
  • Receptors, CXCR4 / antagonists & inhibitors
  • Receptors, CXCR4 / metabolism
  • Stem Cells / pathology*
  • Transplantation, Heterologous
  • Up-Regulation / radiation effects
  • Whole-Body Irradiation

Substances

  • CXCR4 protein, mouse
  • Chemokine CXCL12
  • Receptors, CXCR4

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