Anti-PD-1 synergizes with cyclophosphamide to induce potent anti-tumor vaccine effects through novel mechanisms

Eur J Immunol. 2011 Oct;41(10):2977-86. doi: 10.1002/eji.201141639. Epub 2011 Aug 17.

Abstract

Programmed death-1 receptor (PD-1) is expressed on T cells following TCR activation. Binding of this receptor to its cognate ligands, programmed death ligand (PDL)-1 and PDL-2, down-regulates signals by the TCR, promoting T-cell anergy and apoptosis, thus leading to immune suppression. Here, we find that using an anti-PD-1 antibody (CT-011) with Treg-cell depletion by low-dose cyclophosphamide (CPM), combined with a tumor vaccine, induces synergistic antigen-specific immune responses and reveals novel activities of each agent in this combination. This strategy led to complete regression of established tumors in a significant percentage of treated animals, with survival prolongation. We show for the first time that combining CT-011 and CPM significantly increases the number of vaccine-induced tumor-infiltrating CD8(+) T cells, with simultaneous decrease in infiltrating Treg cells. Interestingly, we find that CT-011 prolongs Treg-cell inhibition induced by CPM, leading to a sustainable significant synergistic decrease of splenic and tumor-infiltrated Treg cells. Surprisingly, we find that the anti-tumor effect elicited by the combination of CT-011 and CPM is dependent on both CD8(+) and CD4(+) T-cell responses, although the antigen we used is a class I MHC-restricted peptide. Thus, we describe a novel and effective therapeutic approach by combining multiple strategies to target several tumor-mediated immune inhibitory mechanisms.

Publication types

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

MeSH terms

  • Animals
  • Antibodies, Monoclonal / administration & dosage
  • Antibodies, Monoclonal / immunology
  • Apoptosis
  • Apoptosis Regulatory Proteins / metabolism*
  • B7-H1 Antigen / immunology*
  • B7-H1 Antigen / metabolism
  • CD4-Positive T-Lymphocytes / immunology
  • CD8-Positive T-Lymphocytes / drug effects
  • CD8-Positive T-Lymphocytes / immunology
  • Cancer Vaccines / immunology
  • Cyclophosphamide / administration & dosage
  • Cyclophosphamide / pharmacology*
  • Female
  • Lymphocyte Activation
  • Mice
  • Mice, Inbred C57BL
  • Neoplasms, Experimental / immunology
  • Neoplasms, Experimental / therapy*
  • Papillomavirus E7 Proteins / administration & dosage
  • Papillomavirus E7 Proteins / immunology
  • Programmed Cell Death 1 Ligand 2 Protein / immunology*
  • Programmed Cell Death 1 Ligand 2 Protein / metabolism
  • Receptors, Antigen, T-Cell
  • T-Lymphocytes, Regulatory / drug effects
  • T-Lymphocytes, Regulatory / immunology
  • T-Lymphocytes, Regulatory / metabolism

Substances

  • Antibodies, Monoclonal
  • Apoptosis Regulatory Proteins
  • B7-H1 Antigen
  • Cancer Vaccines
  • Cd274 protein, mouse
  • Papillomavirus E7 Proteins
  • Pdcd1lg2 protein, mouse
  • Programmed Cell Death 1 Ligand 2 Protein
  • Receptors, Antigen, T-Cell
  • oncogene protein E7, Human papillomavirus type 16
  • Cyclophosphamide