Amino-biphosphonate-mediated MMP-9 inhibition breaks the tumor-bone marrow axis responsible for myeloid-derived suppressor cell expansion and macrophage infiltration in tumor stroma

Cancer Res. 2007 Dec 1;67(23):11438-46. doi: 10.1158/0008-5472.CAN-07-1882.

Abstract

BALB-neuT mice expressing an activated rat c-erbB-2/neu transgene under the mouse mammary tumor virus long terminal repeat show enhanced hematopoiesis with hyperproduction of myeloid-derived suppressor cells (MDSC) because of vascular endothelial growth factor (VEGF) secreted by the tumor. Here, we show that both tumor and stromal cells express matrix metalloproteinase-9 (MMP-9), thereby increasing the levels of pro-MMP-9 in the sera of tumor-bearing mice. Treatment with amino-biphosphonates impaired tumor growth, significantly decreased MMP-9 expression and the number of macrophages in tumor stroma, and reduced MDSC expansion both in bone marrow and peripheral blood by dropping serum pro-MMP-9 and VEGF. We dissected the role of tumor-derived MMP-9 from that secreted by stromal leukocytes by transplanting bone marrow from MMP-9 knockout mice into BALB-neuT mice. Although bone marrow progenitor-derived MMP-9 had a major role in driving MDSC expansion, amino-biphosphonate treatment of bone marrow chimeras further reduced both myelopoiesis and the supportive tumor stroma, thus enhancing tumor necrosis. Moreover, by reducing MDSC, amino-biphosphonates overcome the tumor-induced immune suppression and improved the generation and maintenance of antitumor immune response induced by immunization against the p185/HER-2. Our data reveal that suppression of MMP-9 activity breaks the vicious loop linking tumor growth and myeloid cell expansion, thus reducing immunosuppression. Amino-biphosphonates disclose a specific MMP-9 inhibitory activity that may broaden their application above their current usage.

Publication types

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

MeSH terms

  • Animals
  • Bone Marrow Cells / enzymology*
  • Bone Marrow Cells / pathology
  • Bone Marrow Transplantation
  • Colony-Forming Units Assay
  • Diphosphonates / pharmacology*
  • Female
  • Hematopoiesis
  • Imidazoles
  • Immune Tolerance
  • Immunotherapy
  • Macrophages / drug effects
  • Macrophages / metabolism
  • Macrophages / pathology*
  • Male
  • Mammary Neoplasms, Experimental / blood supply*
  • Mammary Neoplasms, Experimental / enzymology
  • Mammary Neoplasms, Experimental / pathology
  • Matrix Metalloproteinase 9 / biosynthesis*
  • Matrix Metalloproteinase 9 / deficiency
  • Matrix Metalloproteinase 9 / genetics
  • Mice
  • Mice, Inbred BALB C
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Myeloid Cells / drug effects
  • Myeloid Cells / metabolism
  • Myeloid Cells / pathology*
  • Neovascularization, Pathologic / enzymology*
  • Neovascularization, Pathologic / pathology
  • Receptor, ErbB-2 / metabolism
  • Stromal Cells / drug effects
  • Stromal Cells / metabolism
  • Stromal Cells / pathology*
  • Vascular Endothelial Growth Factor A
  • Zoledronic Acid

Substances

  • Diphosphonates
  • Imidazoles
  • Vascular Endothelial Growth Factor A
  • Zoledronic Acid
  • Receptor, ErbB-2
  • Matrix Metalloproteinase 9