G-CSF supplementation with chemotherapy can promote revascularization and subsequent tumor regrowth: prevention by a CXCR4 antagonist

Blood. 2011 Sep 22;118(12):3426-35. doi: 10.1182/blood-2010-11-320812. Epub 2011 Jun 17.

Abstract

Recombinant granulocyte colony-stimulating factor (G-CSF) is used to accelerate recovery from chemotherapy-induced myelosuppression. G-CSF has been recently shown to stimulate angiogenesis mediated by several types of bone marrow-derived cell populations. To investigate whether G-CSF may alter tumor response to therapy, we studied Lewis lung and EMT/6 breast carcinomas in mice treated with paclitaxel (PTX) chemotherapy in combination with G-CSF. We compared the results obtained to mice treated with PTX and AMD3100, a small-molecule drug antagonist of CXCR4 which, like G-CSF, can be used to mobilize hematopoietic cells. We show that PTX combined with G-CSF treatment facilitates revascularization, leading to an improvement in blood perfusion in LLC tumors, and a decrease in hypoxia in EMT/6 tumors, thus enhancing tumor growth in comparison to PTX or PTX and AMD3100 therapies. We found that hemangiocytes but not Gr-1(+) CD11b(+) cells colonize EMT/6 tumors after treatment with PTX and G-CSF, but not PTX and AMD3100, and therefore may contribute to angiogenesis. However, increases in hemangiocyte colonization were not observed in LLC PTX and G-CSF-treated tumors, suggesting distinct mechanisms of tumor revascularization after G-CSF. Overall, our observations suggest that despite its known considerable clinical benefits, G-CSF might contribute to tumor revascularization by various mechanisms, and diminish the antitumor activity of chemotherapy, an effect that can be prevented by AMD3100.

Publication types

  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antineoplastic Agents / administration & dosage*
  • Benzylamines
  • Carcinoma, Lewis Lung / blood supply
  • Carcinoma, Lewis Lung / drug therapy*
  • Carcinoma, Lewis Lung / pathology
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cell Survival / drug effects
  • Cyclams
  • Drug Combinations
  • Female
  • Flow Cytometry
  • Granulocyte Colony-Stimulating Factor / administration & dosage
  • Granulocyte Colony-Stimulating Factor / adverse effects*
  • Granulocyte Colony-Stimulating Factor / therapeutic use
  • Heterocyclic Compounds* / administration & dosage
  • Heterocyclic Compounds* / therapeutic use
  • Humans
  • Immunohistochemistry
  • Inflammatory Breast Neoplasms / blood supply
  • Inflammatory Breast Neoplasms / drug therapy*
  • Inflammatory Breast Neoplasms / pathology
  • Injections, Intraperitoneal
  • Matrix Metalloproteinase 2 / analysis
  • Matrix Metalloproteinase 2 / biosynthesis
  • Mice
  • Mice, Knockout
  • Neovascularization, Pathologic* / drug therapy
  • Neovascularization, Pathologic* / prevention & control
  • Paclitaxel / administration & dosage*
  • Receptors, CXCR4 / antagonists & inhibitors*
  • Receptors, CXCR4 / metabolism
  • Vascular Endothelial Growth Factor A / analysis
  • Vascular Endothelial Growth Factor A / biosynthesis
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents
  • Benzylamines
  • Cyclams
  • Drug Combinations
  • Heterocyclic Compounds
  • Receptors, CXCR4
  • Vascular Endothelial Growth Factor A
  • Granulocyte Colony-Stimulating Factor
  • Matrix Metalloproteinase 2
  • Mmp2 protein, mouse
  • Paclitaxel
  • plerixafor