Improved outcome following allogeneic stem cell transplantation in chronic myeloid leukemia is associated with higher expression of BMI-1 and immune responses to BMI-1 protein

Leukemia. 2011 Apr;25(4):629-37. doi: 10.1038/leu.2010.325. Epub 2011 Jan 21.

Abstract

BMI-1 and EZH2 are polycomb group (PcG) proteins that maintain self-renewal of stem cells, and are overexpressed in leukemia. To investigate the potential of PcG proteins as leukemia-associated antigens, and as targets for graft-versus-leukemia (GVL) effects, we studied cells obtained from 86 patients with chronic myeloid leukemia (CML) and 25 human leukocyte antigen (HLA)-A*0201(+) sibling donors collected before allogeneic stem cell transplantation (SCT). Although BMI-1 overexpression in CD34(+) cells of CML patients treated with pharmacotherapy is associated with poor prognosis, we found, conversely, that in CML patients treated with SCT, a higher expression of BMI-1, and correspondingly a lower expression of its target for repression, CDKN2A, is associated with improved leukemia-free survival. Cytotoxic T-lymphocyte (CTL) responses to the BMI-1 peptide were detected in 5 of 25 (20%) donors, and in 8 of 19 (42%) HLA-A*0201(+) CML patients. BMI-1 generated more total and high-avidity immune responses, and was more immunogenic than EZH2. PcG-specific CTLs had a memory phenotype, were readily expanded in short-term cultures and were detected after SCT in recipients of PcG-specific CTL-positive donors. A higher BMI-1 expression in CML CD34(+) progenitors was associated with native BMI-1 immune responses. These immune responses to PcG proteins may target leukemia stem cells and have relevance for disease control by GVL.

Publication types

  • Research Support, N.I.H., Intramural

MeSH terms

  • Antigens, CD34 / metabolism
  • Cohort Studies
  • DNA-Binding Proteins / genetics
  • DNA-Binding Proteins / metabolism
  • Enhancer of Zeste Homolog 2 Protein
  • Enzyme-Linked Immunosorbent Assay
  • Graft vs Host Disease / prevention & control*
  • HLA-A Antigens
  • HLA-A2 Antigen
  • Humans
  • Immunophenotyping
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / immunology*
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / metabolism
  • Leukemia, Myelogenous, Chronic, BCR-ABL Positive / therapy*
  • Nuclear Proteins / genetics
  • Nuclear Proteins / immunology*
  • Nuclear Proteins / metabolism*
  • Peptide Fragments / immunology
  • Peptide Fragments / metabolism
  • Polycomb Repressive Complex 1
  • Polycomb Repressive Complex 2
  • Proto-Oncogene Proteins / genetics
  • Proto-Oncogene Proteins / immunology*
  • Proto-Oncogene Proteins / metabolism*
  • RNA, Messenger / genetics
  • Repressor Proteins / genetics
  • Repressor Proteins / immunology*
  • Repressor Proteins / metabolism*
  • Reverse Transcriptase Polymerase Chain Reaction
  • Stem Cell Transplantation*
  • Survival Rate
  • T-Lymphocytes, Cytotoxic / immunology*
  • Transcription Factors / genetics
  • Transcription Factors / metabolism
  • Transplantation, Homologous
  • Treatment Outcome

Substances

  • Antigens, CD34
  • BMI1 protein, human
  • DNA-Binding Proteins
  • HLA-A Antigens
  • HLA-A*02:01 antigen
  • HLA-A2 Antigen
  • Nuclear Proteins
  • Peptide Fragments
  • Proto-Oncogene Proteins
  • RNA, Messenger
  • Repressor Proteins
  • Transcription Factors
  • EZH2 protein, human
  • Enhancer of Zeste Homolog 2 Protein
  • Polycomb Repressive Complex 2
  • Polycomb Repressive Complex 1