The histone methyltransferase MLL1 complex inhibits expression of fetal hemoglobin

J Biol Chem. 2025 Dec;301(12):110863. doi: 10.1016/j.jbc.2025.110863. Epub 2025 Oct 27.

Abstract

Increasing fetal-type hemoglobin expression in adult erythroid cells holds promise in the treatment of sickle cell disease (SCD) and β-thalassemia. We have identified the MLL1 complex as a critical regulator of fetal and embryonic hemoglobin repression. Knockdowns of MEN1 and KMT2A, encoding essential components of the complex, caused a significant downregulation of BCL11A expression and a substantial increase in γ- and ε-globin mRNA levels in HUDEP-2 cells. Significant binding of MEN1 and KMT2A was readily detected at the promoter and a critical enhancer of BCL11A in HUDEP-2 cells, suggesting that BCL11A is a direct transcriptional target of the MLL1 complex. Consistent with these results, MEN1 or KMT2A knockdown in normal human CD34+ hematopoietic stem and progenitor cells induced to undergo erythroid differentiation also significantly decreased their BCL11A expression and increased their γ- and ε-globin expression and the production of F cells in the culture. Treatment of these cells with MENIN inhibitors yielded similar results and promoted erythroid differentiation with minimal effects on their growth. Moreover, treatment of CD34+ hematopoietic stem and progenitor cells from SCD patients with MENIN inhibitors substantially increased γ-globin expression in their erythroid progenies. These findings underscore a critical role of the MLL1 complex in regulating fetal and embryonic hemoglobin expression and suggest that MENIN inhibitors could offer a promising therapeutic approach for SCD and β-thalassemia.

Keywords: MEN1; chromatin regulation; differentiation; hemoglobin; transcription regulation.

MeSH terms

  • Anemia, Sickle Cell / genetics
  • Anemia, Sickle Cell / metabolism
  • Anemia, Sickle Cell / pathology
  • Antigens, CD34 / metabolism
  • Carrier Proteins* / genetics
  • Carrier Proteins* / metabolism
  • Cell Differentiation
  • Erythroid Cells / metabolism
  • Fetal Hemoglobin* / biosynthesis
  • Fetal Hemoglobin* / genetics
  • Fetal Hemoglobin* / metabolism
  • Gene Expression Regulation*
  • Gene Knockdown Techniques
  • Hematopoietic Stem Cells / cytology
  • Hematopoietic Stem Cells / metabolism
  • Histone-Lysine N-Methyltransferase* / genetics
  • Histone-Lysine N-Methyltransferase* / metabolism
  • Humans
  • Myeloid-Lymphoid Leukemia Protein* / genetics
  • Myeloid-Lymphoid Leukemia Protein* / metabolism
  • Nuclear Proteins* / genetics
  • Nuclear Proteins* / metabolism
  • Proto-Oncogene Proteins* / antagonists & inhibitors
  • Proto-Oncogene Proteins* / genetics
  • Proto-Oncogene Proteins* / metabolism
  • Repressor Proteins
  • beta-Thalassemia / genetics
  • beta-Thalassemia / metabolism
  • gamma-Globins / biosynthesis
  • gamma-Globins / genetics

Substances

  • Histone-Lysine N-Methyltransferase
  • Fetal Hemoglobin
  • Myeloid-Lymphoid Leukemia Protein
  • KMT2A protein, human
  • Proto-Oncogene Proteins
  • BCL11A protein, human
  • MEN1 protein, human
  • Nuclear Proteins
  • Carrier Proteins
  • gamma-Globins
  • Repressor Proteins
  • Antigens, CD34