Decade-long safety and function of retroviral-modified chimeric antigen receptor T cells

Sci Transl Med. 2012 May 2;4(132):132ra53. doi: 10.1126/scitranslmed.3003761.

Abstract

The success of adoptive T cell gene transfer for treatment of cancer and HIV is predicated on generating a response that is both durable and safe. We report long-term results from three clinical trials to evaluate gammaretroviral vector-engineered T cells for HIV. The vector encoded a chimeric antigen receptor (CAR) composed of CD4 linked to the CD3ζ signaling chain (CD4ζ). CAR T cells were detected in 98% of samples tested for at least 11 years after infusion at frequencies that exceeded average T cell levels after most vaccine approaches. The CD4ζ transgene retained expression and function. There was no evidence of vector-induced immortalization of cells; integration site distributions showed no evidence of persistent clonal expansion or enrichment for integration sites near genes implicated in growth control or transformation. The CD4ζ T cells had stable levels of engraftment, with decay half-lives that exceeded 16 years, in marked contrast to previous trials testing engineered T cells. These findings indicate that host immunosuppression before T cell transfer is not required to achieve long-term persistence of gene-modified T cells. Further, our results emphasize the safety of T cells modified by retroviral gene transfer in clinical application, as measured in >500 patient-years of follow-up. Thus, previous safety issues with integrating viral vectors are hematopoietic stem cell or transgene intrinsic, and not a general feature of retroviral vectors. Engineered T cells are a promising form of synthetic biology for long-term delivery of protein-based therapeutics. These results provide a framework to guide the therapy of a wide spectrum of human diseases.

Publication types

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

MeSH terms

  • Adoptive Transfer / adverse effects*
  • CD3 Complex / metabolism
  • CD4 Antigens / metabolism
  • Cohort Studies
  • Epigenesis, Genetic
  • Follow-Up Studies
  • Gene Transfer Techniques*
  • Genetic Vectors / genetics
  • Genomics
  • Half-Life
  • Humans
  • Interleukin-2 / administration & dosage
  • Interleukin-2 / immunology
  • Mutagenesis, Insertional / genetics
  • Receptors, Antigen, T-Cell / genetics
  • Receptors, Antigen, T-Cell / immunology*
  • Recombinant Proteins / genetics
  • Recombinant Proteins / immunology*
  • Retroviridae / genetics*
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism
  • T-Lymphocytes / transplantation*
  • Time Factors
  • Transcription, Genetic
  • Transgenes / genetics

Substances

  • CD3 Complex
  • CD4 Antigens
  • Interleukin-2
  • Receptors, Antigen, T-Cell
  • Recombinant Proteins