Secretory IgM Exacerbates Tumor Progression by Inducing Accumulations of MDSCs in Mice

Cancer Immunol Res. 2018 Jun;6(6):696-710. doi: 10.1158/2326-6066.CIR-17-0582. Epub 2018 Apr 12.

Abstract

Chronic lymphocytic leukemia (CLL) cells can secrete immunoglobulin M. However, it is not clear whether secretory IgM (sIgM) plays a role in disease progression. We crossed the Eμ-TCL1 mouse model of CLL, in which the expression of human TCL1 oncogene was driven by the V(H) promoter-Ig(H)-Eμ enhancer, with MD4 mice whose B cells produced B-cell receptor (membrane-bound IgM) and sIgM with specificity for hen egg lysozyme (HEL). CLL cells that developed in these MD4/Eμ-TCL1 mice reactivated a parental Ig gene allele and secreted IgM, and did not recognize HEL. The MD4/Eμ-TCL1 mice had reduced survival, increased myeloid-derived suppressor cells (MDSC), and decreased numbers of T cells. We tested whether sIgM could contribute to the accumulation of MDSCs by crossing μS-/- mice, which could not produce sIgM, with Eμ-TCL1 mice. The μS-/-/Eμ-TCL1 mice survived longer than Eμ-TCL1 mice and developed decreased numbers of MDSCs which were less able to suppress proliferation of T cells. We targeted the synthesis of sIgM by deleting the function of XBP-1s and showed that targeting XBP-1s genetically or pharmacologically could lead to decreased sIgM, accompanied by decreased numbers and reduced functions of MDSCs in MD4/Eμ-TCL1 mice. Additionally, MDSCs from μS-/- mice grafted with Lewis lung carcinoma were inefficient suppressors of T cells, resulting in slower tumor growth. These results demonstrate that sIgM produced by B cells can upregulate the functions of MDSCs in tumor-bearing mice to aggravate cancer progression. In a mouse model of CLL, production of secretory IgM led to more MDSCs, fewer T cells, and shorter survival times for the mice. Thus, secretory IgM may aggravate the progression of this cancer. Cancer Immunol Res; 6(6); 696-710. ©2018 AACR.

Publication types

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

MeSH terms

  • Animals
  • B-Lymphocytes / immunology
  • B-Lymphocytes / metabolism
  • Biomarkers
  • Cell Line, Tumor
  • Disease Models, Animal
  • Disease Progression
  • Granulocytes / immunology
  • Granulocytes / metabolism
  • Immunoglobulin M / immunology*
  • Immunophenotyping
  • Lymphocyte Activation / immunology
  • Mice
  • Mice, Knockout
  • Myeloid-Derived Suppressor Cells / immunology*
  • Myeloid-Derived Suppressor Cells / metabolism
  • Myeloid-Derived Suppressor Cells / pathology
  • Neoplasms / immunology*
  • Neoplasms / metabolism
  • Neoplasms / pathology*
  • Receptors, Antigen, B-Cell / metabolism
  • Signal Transduction
  • Spleen / immunology
  • Spleen / metabolism
  • Spleen / pathology
  • T-Lymphocyte Subsets / immunology
  • T-Lymphocyte Subsets / metabolism
  • Tumor Microenvironment / immunology

Substances

  • Biomarkers
  • Immunoglobulin M
  • Receptors, Antigen, B-Cell
  • secretory IgM