Mesenchymal stem cell-mediated, tumor stroma-targeted radioiodine therapy of metastatic colon cancer using the sodium iodide symporter as theranostic gene

J Nucl Med. 2015 Apr;56(4):600-6. doi: 10.2967/jnumed.114.146662. Epub 2015 Mar 5.

Abstract

The tumor-homing property of mesenchymal stem cells (MSCs) allows targeted delivery of therapeutic genes into the tumor microenvironment. The application of sodium iodide symporter (NIS) as a theranostic gene allows noninvasive imaging of MSC biodistribution and transgene expression before therapeutic radioiodine application. We have previously shown that linking therapeutic transgene expression to induction of the chemokine CCL5/RANTES allows a more focused expression within primary tumors, as the adoptively transferred MSC develop carcinoma-associated fibroblast-like characteristics. Although RANTES/CCL5-NIS targeting has shown efficacy in the treatment of primary tumors, it was not clear if it would also be effective in controlling the growth of metastatic disease.

Methods: To expand the potential range of tumor targets, we investigated the biodistribution and tumor recruitment of MSCs transfected with NIS under control of the RANTES/CCL5 promoter (RANTES-NIS-MSC) in a colon cancer liver metastasis mouse model established by intrasplenic injection of the human colon cancer cell line LS174t. RANTES-NIS-MSCs were injected intravenously, followed by (123)I scintigraphy, (124)I PET imaging, and (131)I therapy.

Results: Results show robust MSC recruitment with RANTES/CCL5-promoter activation within the stroma of liver metastases as evidenced by tumor-selective iodide accumulation, immunohistochemistry, and real-time polymerase chain reaction. Therapeutic application of (131)I in RANTES-NIS-MSC-treated mice resulted in a significant delay in tumor growth and improved overall survival.

Conclusion: This novel gene therapy approach opens the prospect of NIS-mediated radionuclide therapy of metastatic cancer after MSC-mediated gene delivery.

Keywords: RANTES; colon cancer; gene therapy; hepatic metastases; mesenchymal stem cells; sodium iodide symporter.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Chemokine CCL5 / metabolism
  • Colonic Neoplasms / radiotherapy*
  • Female
  • Fibroblasts / metabolism
  • Genetic Therapy / methods
  • Humans
  • Iodine Radioisotopes / therapeutic use*
  • Liver Neoplasms / radiotherapy
  • Magnetic Resonance Imaging
  • Mesenchymal Stem Cells / cytology*
  • Mice
  • Mice, Nude
  • Neoplasm Metastasis
  • Neoplasm Transplantation
  • Plasmids / metabolism
  • Positron-Emission Tomography
  • Radionuclide Imaging
  • Symporters / chemistry*
  • Symporters / genetics*
  • Transgenes
  • Tumor Microenvironment

Substances

  • CCL5 protein, human
  • Chemokine CCL5
  • Iodine Radioisotopes
  • Symporters
  • sodium-iodide symporter