Anti-interleukin-10R1 monoclonal antibody in combination with bacillus Calmette--Guérin is protective against bladder cancer metastasis in a murine orthotopic tumour model and demonstrates systemic specific anti-tumour immunity

Clin Exp Immunol. 2014 Jul;177(1):261-8. doi: 10.1111/cei.12315.

Abstract

Effective treatment of bladder cancer with bacillus Calmette-Guérin (BCG) depends on the induction of a T helper type (Th) 1 immune response. Interleukin (IL)-10 down-regulates the Th1 response and is associated with BCG failure. In this study, we investigated whether blocking IL-10 signalling could enhance the BCG-induced Th1 response and anti-tumour immunity in a murine orthotopic tumour model. Treatment with BCG and anti-IL-10 receptor 1 monoclonal antibody (anti-IL-10R1 mAb) increased the interferon (IFN)-γ to IL-10 ratio in both splenocyte cultures and urine. Mice bearing luciferase-expressing MB49 (MB49-Luc) tumours were treated and followed for tumour growth by bioluminescent imaging, bladder weight and histology. Mice treated with phosphate-buffered saline (PBS) (group 1), BCG plus control immunoglobulin (Ig)G1 (group 2) or BCG plus anti-IL-10R1 mAb (group 3) showed 0, 6 and 22% tumour regression, respectively. The mean bladder weight of group 3 mice was substantially lower than those of groups 1 and 2 mice. Remarkably, 36% of group 1 and 53% of group 2 mice but no group 3 mice developed lung metastasis (P = 0·02). To investigate the mechanisms underlying the effect of combination therapy, splenocytes were stimulated with S12 peptide (serine mutation at codon 12 of the K-ras oncogene) known to be expressed in MB49-Luc cells. Induction of ras mutation-specific IFN-γ and cytotoxicity was observed in mice treated with combination therapy. These observations indicate that BCG, in combination with anti-IL-10R1 mAb, induces enhanced anti-tumour immunity that is protective against lung metastasis. Anti-IL-10R1 mAb demonstrates systemic effects and may prove useful in clinical practice for treating bladder cancer in high-risk patients.

Keywords: BCG; IL-10; bladder cancer; immunotherapy.

MeSH terms

  • Animals
  • Antibodies, Monoclonal / therapeutic use*
  • Antigens, Neoplasm / immunology
  • Cell Line, Tumor
  • Cytotoxicity, Immunologic / drug effects
  • Disease Models, Animal
  • Female
  • Humans
  • Immunotherapy / methods*
  • Interferon-gamma / metabolism
  • Interleukin-10 / metabolism
  • Interleukin-10 Receptor alpha Subunit / immunology*
  • Lung Neoplasms / prevention & control*
  • Lung Neoplasms / secondary
  • Mice
  • Mice, Inbred C57BL
  • Mutation / genetics
  • Mycobacterium bovis / immunology*
  • Oncogene Protein p21(ras) / genetics
  • Oncogene Protein p21(ras) / immunology
  • Peptide Fragments / genetics
  • Peptide Fragments / immunology
  • Th1 Cells / immunology
  • Tumor Burden / drug effects
  • Urinary Bladder Neoplasms / pathology
  • Urinary Bladder Neoplasms / therapy*

Substances

  • Antibodies, Monoclonal
  • Antigens, Neoplasm
  • Interleukin-10 Receptor alpha Subunit
  • Peptide Fragments
  • Interleukin-10
  • Interferon-gamma
  • Oncogene Protein p21(ras)