Tetanus toxoid and CCL3 improve dendritic cell vaccines in mice and glioblastoma patients

Nature. 2015 Mar 19;519(7543):366-9. doi: 10.1038/nature14320. Epub 2015 Mar 11.

Abstract

After stimulation, dendritic cells (DCs) mature and migrate to draining lymph nodes to induce immune responses. As such, autologous DCs generated ex vivo have been pulsed with tumour antigens and injected back into patients as immunotherapy. While DC vaccines have shown limited promise in the treatment of patients with advanced cancers including glioblastoma, the factors dictating DC vaccine efficacy remain poorly understood. Here we show that pre-conditioning the vaccine site with a potent recall antigen such as tetanus/diphtheria (Td) toxoid can significantly improve the lymph node homing and efficacy of tumour-antigen-specific DCs. To assess the effect of vaccine site pre-conditioning in humans, we randomized patients with glioblastoma to pre-conditioning with either mature DCs or Td unilaterally before bilateral vaccination with DCs pulsed with Cytomegalovirus phosphoprotein 65 (pp65) RNA. We and other laboratories have shown that pp65 is expressed in more than 90% of glioblastoma specimens but not in surrounding normal brain, providing an unparalleled opportunity to subvert this viral protein as a tumour-specific target. Patients given Td had enhanced DC migration bilaterally and significantly improved survival. In mice, Td pre-conditioning also enhanced bilateral DC migration and suppressed tumour growth in a manner dependent on the chemokine CCL3. Our clinical studies and corroborating investigations in mice suggest that pre-conditioning with a potent recall antigen may represent a viable strategy to improve anti-tumour immunotherapy.

Publication types

  • Randomized Controlled Trial
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Antigens, Neoplasm / immunology
  • CD4-Positive T-Lymphocytes / drug effects
  • CD4-Positive T-Lymphocytes / immunology
  • Cancer Vaccines / administration & dosage
  • Cancer Vaccines / immunology*
  • Cancer Vaccines / therapeutic use
  • Cell Movement / drug effects
  • Chemokine CCL3 / immunology*
  • Dendritic Cells / cytology
  • Dendritic Cells / drug effects*
  • Dendritic Cells / immunology
  • Female
  • Glioblastoma / drug therapy
  • Glioblastoma / immunology*
  • Glioblastoma / pathology
  • Glioblastoma / therapy*
  • Humans
  • Immunotherapy / methods
  • Lymph Nodes / cytology
  • Lymph Nodes / drug effects
  • Lymph Nodes / immunology
  • Mice
  • Mice, Inbred C57BL
  • Phosphoproteins / chemistry
  • Phosphoproteins / genetics
  • Phosphoproteins / immunology
  • Substrate Specificity
  • Survival Rate
  • Tetanus Toxoid / administration & dosage*
  • Tetanus Toxoid / pharmacology*
  • Tetanus Toxoid / therapeutic use
  • Treatment Outcome
  • Viral Matrix Proteins / chemistry
  • Viral Matrix Proteins / genetics
  • Viral Matrix Proteins / immunology

Substances

  • Antigens, Neoplasm
  • CCL3 protein, human
  • Cancer Vaccines
  • Ccl3 protein, mouse
  • Chemokine CCL3
  • Phosphoproteins
  • Tetanus Toxoid
  • Viral Matrix Proteins
  • cytomegalovirus matrix protein 65kDa