Levels of peripheral CD4(+)FoxP3(+) regulatory T cells are negatively associated with clinical response to adoptive immunotherapy of human cancer

Blood. 2012 Jun 14;119(24):5688-96. doi: 10.1182/blood-2011-10-386482. Epub 2012 May 3.

Abstract

CD4(+)FoxP3(+) regulatory T cells (Tregs) have been shown to suppress T cell-mediated host immune responses against self- and nonself-antigens; however, the impact of CD4(+) Tregs on human antitumor immune responses and their influence on cancer treatment are unknown. In the present study, we explored the factors that influence CD4(+) Treg reconstitution in patients receiving adoptive immunotherapy following conditioning regimens designed to enhance T-cell function and evaluated potential associations between CD4(+) Treg levels and clinical responses to therapy. The analysis of 4 trials employing nonmyeloablative chemotherapy with or without total body irradiation (TBI) before adoptive T-cell transfer revealed that the percentage and number of reconstituting CD4(+)FoxP3(+) Tregs observed in the peripheral blood was higher in nonresponders than in responders. The addition of TBI resulted in a further depletion of CD4(+) Tregs, and the degree of depletion was dependent on the TBI dose. The number of administered doses of IL-2 was found to be positively associated with peripheral Treg reconstitution. These observations provide strong evidence that endogenous CD4(+) Tregs have a negative impact on cancer therapy, and suggest that strategies reducing Treg levels may provide clinical benefit to cancer patients. All 5 clinical trials are registered at www.clinicaltrials.gov as NCT00001832, NCT00096382, NCT00335127, NCT00509496, and NCT00513604.

MeSH terms

  • CD4 Antigens / metabolism*
  • CD8-Positive T-Lymphocytes / immunology
  • Cells, Cultured
  • Dose-Response Relationship, Immunologic
  • Forkhead Transcription Factors / metabolism*
  • Humans
  • Immunotherapy, Adoptive / methods*
  • Interleukin-2 / administration & dosage
  • Interleukin-2 / immunology
  • Lymphocyte Count
  • Lymphocytes, Tumor-Infiltrating / immunology
  • Neoplasms / immunology*
  • Neoplasms / therapy*
  • Phenotype
  • T-Lymphocytes, Regulatory / immunology*
  • Treatment Outcome
  • Whole-Body Irradiation

Substances

  • CD4 Antigens
  • FOXP3 protein, human
  • Forkhead Transcription Factors
  • Interleukin-2

Associated data

  • ClinicalTrials.gov/NCT00001832
  • ClinicalTrials.gov/NCT00096382
  • ClinicalTrials.gov/NCT00335127
  • ClinicalTrials.gov/NCT00513604
  • ClinicalTrials.gov/NCT00509496