Transfusion independence and HMGA2 activation after gene therapy of human β-thalassaemia

Nature. 2010 Sep 16;467(7313):318-22. doi: 10.1038/nature09328.

Abstract

The β-haemoglobinopathies are the most prevalent inherited disorders worldwide. Gene therapy of β-thalassaemia is particularly challenging given the requirement for massive haemoglobin production in a lineage-specific manner and the lack of selective advantage for corrected haematopoietic stem cells. Compound β(E)/β(0)-thalassaemia is the most common form of severe thalassaemia in southeast Asian countries and their diasporas. The β(E)-globin allele bears a point mutation that causes alternative splicing. The abnormally spliced form is non-coding, whereas the correctly spliced messenger RNA expresses a mutated β(E)-globin with partial instability. When this is compounded with a non-functional β(0) allele, a profound decrease in β-globin synthesis results, and approximately half of β(E)/β(0)-thalassaemia patients are transfusion-dependent. The only available curative therapy is allogeneic haematopoietic stem cell transplantation, although most patients do not have a human-leukocyte-antigen-matched, geno-identical donor, and those who do still risk rejection or graft-versus-host disease. Here we show that, 33 months after lentiviral β-globin gene transfer, an adult patient with severe β(E)/β(0)-thalassaemia dependent on monthly transfusions since early childhood has become transfusion independent for the past 21 months. Blood haemoglobin is maintained between 9 and 10 g dl(-1), of which one-third contains vector-encoded β-globin. Most of the therapeutic benefit results from a dominant, myeloid-biased cell clone, in which the integrated vector causes transcriptional activation of HMGA2 in erythroid cells with further increased expression of a truncated HMGA2 mRNA insensitive to degradation by let-7 microRNAs. The clonal dominance that accompanies therapeutic efficacy may be coincidental and stochastic or result from a hitherto benign cell expansion caused by dysregulation of the HMGA2 gene in stem/progenitor cells.

Publication types

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

MeSH terms

  • Adolescent
  • Blood Cells / cytology
  • Blood Cells / metabolism
  • Blood Transfusion*
  • Bone Marrow Cells / cytology
  • Bone Marrow Cells / metabolism
  • Child, Preschool
  • Clone Cells / metabolism
  • Gene Expression
  • Genetic Therapy*
  • Genetic Vectors / genetics
  • HMGA2 Protein / genetics
  • HMGA2 Protein / metabolism*
  • Homeostasis
  • Humans
  • Lentivirus / genetics
  • Male
  • MicroRNAs / genetics
  • Organ Specificity
  • RNA, Messenger / analysis
  • RNA, Messenger / genetics
  • Time Factors
  • Transcriptional Activation
  • Young Adult
  • beta-Globins / genetics*
  • beta-Globins / metabolism*
  • beta-Thalassemia / genetics*
  • beta-Thalassemia / metabolism
  • beta-Thalassemia / therapy*

Substances

  • HMGA2 Protein
  • MicroRNAs
  • RNA, Messenger
  • beta-Globins
  • mirnlet7 microRNA, human