IL-2 augments the therapeutic efficacy of adoptively transferred B cells which directly kill tumor cells via the CXCR4/CXCL12 and perforin pathways

Oncotarget. 2016 Sep 13;7(37):60461-60474. doi: 10.18632/oncotarget.11124.

Abstract

We previously reported that antitumor B cells directly kill tumor cells via the Fas/FasL pathway and are regulated by IL-10. In this study, we defined additional mechanisms involved in B cell antitumor immunity. Administration of IL-2 significantly augmented the therapeutic efficacy of adoptively transferred tumor-draining lymph node (TDLN) B cells which express IL- 2R. Culture supernatant of purified B splenocytes harvested from the mice that received adoptive transfer of 4T1 TDLN B cells plus IL-2 administration produced larger amounts of IgG which bound to 4T1, resulting in 4T1 lysis. Furthermore, we detected CXCR4 expression on 4T1 TDLN B cells, and 4T1 tumor cells produced its ligand CXCL12. Transwell experiments demonstrated the chemoattraction of CXCR4-expressing 4T1 TDLN B cells towards CXCL12- producing 4T1 cells. Blockade of CXCR4 using a CXCR4-specific inhibitor, AMD3100, significantly reduced the killing of 4T1 tumor cells by 4T1 TDLN B cells. Blockade of FasL and CXCR4 concurrently inhibited B cell-mediated direct killing of tumor cells in an additive manner, indicating that both Fas/FasL and CXCL12/CXCR4 pathways are involved in the direct killing of 4T1 cells by 4T1 TDLN B cells. TDLN B cells produced perforin. Additional transwell experiments showed that effector B cells could directly kill tumor cells in cell-cell contact via the Fas/FasL and CXCR4/CXCL12 pathways as well as perforin, while without cell contact, perforin secreted by B cells led to tumor cell cytotoxicity. These findings underscore the diversity of function by which B cells can play an important role in the host immune response to tumor.

Keywords: B cells; CXCR4/CXCL12; IL-2; adoptive immunotherapy; perforin.

MeSH terms

  • Animals
  • B-Lymphocytes / immunology*
  • B-Lymphocytes / transplantation
  • Benzylamines
  • Cell Line, Tumor
  • Chemokine CXCL12 / metabolism
  • Chemotaxis
  • Cyclams
  • Cytotoxicity, Immunologic
  • Female
  • Heterocyclic Compounds / administration & dosage
  • Humans
  • Immunity, Humoral
  • Immunotherapy, Adoptive / methods*
  • Interleukin-10 / metabolism
  • Interleukin-2 / therapeutic use*
  • Mammary Neoplasms, Animal / immunology
  • Mammary Neoplasms, Animal / therapy*
  • Mice
  • Perforin / immunology
  • Perforin / therapeutic use*
  • Receptors, CXCR4 / antagonists & inhibitors
  • Receptors, CXCR4 / metabolism
  • Receptors, Interleukin-2 / metabolism

Substances

  • Benzylamines
  • CXCL12 protein, human
  • CXCR4 protein, human
  • Chemokine CXCL12
  • Cyclams
  • Heterocyclic Compounds
  • Interleukin-2
  • Receptors, CXCR4
  • Receptors, Interleukin-2
  • Perforin
  • Interleukin-10
  • plerixafor