Cytoreductive conditioning intensity predicts clonal diversity in ADA-SCID retroviral gene therapy patients

Blood. 2017 May 11;129(19):2624-2635. doi: 10.1182/blood-2016-12-756734. Epub 2017 Mar 28.

Abstract

Retroviral gene therapy has proved efficacious for multiple genetic diseases of the hematopoietic system, but roughly half of clinical gene therapy trial protocols using gammaretroviral vectors have reported leukemias in some of the patients treated. In dramatic contrast, 39 adenosine deaminase-deficient severe combined immunodeficiency (ADA-SCID) patients have been treated with 4 distinct gammaretroviral vectors without oncogenic consequence. We investigated clonal dynamics and diversity in a cohort of 15 ADA-SCID children treated with gammaretroviral vectors and found clear evidence of genotoxicity, indicated by numerous common integration sites near proto-oncogenes and by increased abundance of clones with integrations near MECOM and LMO2 These clones showed stable behavior over multiple years and never expanded to the point of dominance or dysplasia. One patient developed a benign clonal dominance that could not be attributed to insertional mutagenesis and instead likely resulted from expansion of a transduced natural killer clone in response to chronic Epstein-Barr virus viremia. Clonal diversity and T-cell repertoire, measured by vector integration site sequencing and T-cell receptor β-chain rearrangement sequencing, correlated significantly with the amount of busulfan preconditioning delivered to patients and to CD34+ cell dose. These data, in combination with results of other ADA-SCID gene therapy trials, suggest that disease background may be a crucial factor in leukemogenic potential of retroviral gene therapy and underscore the importance of cytoreductive conditioning in this type of gene therapy approach.

Publication types

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

MeSH terms

  • Adaptor Proteins, Signal Transducing / genetics
  • Adenosine Deaminase / deficiency*
  • Adenosine Deaminase / genetics
  • Agammaglobulinemia / genetics*
  • Agammaglobulinemia / pathology
  • Agammaglobulinemia / therapy*
  • Antineoplastic Agents, Alkylating / therapeutic use*
  • Busulfan / therapeutic use*
  • Child
  • DNA-Binding Proteins / genetics
  • Gammaretrovirus / genetics*
  • Genetic Therapy / methods*
  • Genetic Vectors / genetics
  • Genetic Vectors / therapeutic use*
  • Humans
  • LIM Domain Proteins / genetics
  • MDS1 and EVI1 Complex Locus Protein
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogenes / genetics
  • Severe Combined Immunodeficiency / genetics*
  • Severe Combined Immunodeficiency / pathology
  • Severe Combined Immunodeficiency / therapy*
  • T-Lymphocytes / cytology
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / metabolism
  • T-Lymphocytes / pathology
  • Transcription Factors / genetics

Substances

  • Adaptor Proteins, Signal Transducing
  • Antineoplastic Agents, Alkylating
  • DNA-Binding Proteins
  • LIM Domain Proteins
  • LMO2 protein, human
  • MDS1 and EVI1 Complex Locus Protein
  • MECOM protein, human
  • Proto-Oncogene Proteins
  • Transcription Factors
  • Adenosine Deaminase
  • Busulfan

Supplementary concepts

  • Severe combined immunodeficiency due to adenosine deaminase deficiency