Rituximab-induced HMGB1 release is associated with inhibition of STAT3 activity in human diffuse large B-cell lymphoma

Oncotarget. 2015 Sep 29;6(29):27816-31. doi: 10.18632/oncotarget.4816.

Abstract

Treatment with rituximab plus cyclophosphamide, doxorubicin, vincristine, and prednisone (R-CHOP) has greatly improved clinical outcomes in patients with diffuse large B-cell lymphoma (DLBCL) compared with CHOP. The mechanism of rituximab-induced cell death is poorly understood. We found that rituximab does not enhance the directly killing efficacy of CHOP, as tested on a panel of DLBCL cell lines. Rituximab induced a rapid release of HMGB1 (High mobility group protein B 1). This release is independent of cell death but significantly correlated with an inhibition on STAT3 activity. In the resting state, HMGB1 co-localizes and interacts with STAT3 in the nucleus of DLBCL cells. Treatment with rituximab breaks this binding and triggers HMGB1 release. Treatment with R-CHOP but not CHOP significantly increased plasma HMGB1 and decreased IL-10 concentrations in DLBCL patients compared with controls. The conditioned medium from rituximab-treated DLBCL cells is able to trigger dendritic cell maturation, phagocytosis, and IFN-γ secretion by cytotoxic T cells. In conclusion, our results demonstrate that rituximab induces an inhibition on STAT3 activity, leading to increased HMGB1 release and decreased IL-10 secretion, which elicits immune responses, suggesting that indirect effects on the immune system rather than direct killing contribute to elimination of DLBCL.

Keywords: DLBCL; HMGB1; STAT3; immunogenic cell death; rituximab.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Antibodies, Monoclonal, Murine-Derived
  • Antineoplastic Agents / pharmacology*
  • Antineoplastic Combined Chemotherapy Protocols
  • Apoptosis / drug effects
  • Blotting, Western
  • Cell Line, Tumor
  • Cyclophosphamide
  • Doxorubicin
  • Enzyme-Linked Immunosorbent Assay
  • Flow Cytometry
  • HMGB1 Protein / metabolism*
  • Humans
  • Immunohistochemistry
  • Immunoprecipitation
  • Lymphoma, Large B-Cell, Diffuse / immunology
  • Lymphoma, Large B-Cell, Diffuse / metabolism*
  • Prednisone
  • Rituximab / pharmacology*
  • STAT3 Transcription Factor / drug effects*
  • STAT3 Transcription Factor / metabolism
  • Tumor Cells, Cultured
  • Vincristine

Substances

  • Antibodies, Monoclonal, Murine-Derived
  • Antineoplastic Agents
  • HMGB1 Protein
  • HMGB1 protein, human
  • R-CHOP protocol
  • STAT3 Transcription Factor
  • STAT3 protein, human
  • Rituximab
  • Vincristine
  • Doxorubicin
  • Cyclophosphamide
  • Prednisone