Deficiency of miR-155 in Leukemic B-Cells Results in Cell Cycle Arrest and Deregulation of MIR155HG/TP53INP1/CDKN1A/CCND1 network

Arch Med Res. 2025 Apr;56(3):103124. doi: 10.1016/j.arcmed.2024.103124. Epub 2024 Nov 25.

Abstract

Background: Cell cycle progression and leukemia development are tightly regulated processes in which even a small imbalance in the expression of cell cycle regulatory molecules and microRNAs (miRNAs) can lead to an increased risk of cancer/leukemia development. Here, we focus on the study of a ubiquitous, multifunctional, and oncogenic miRNA-hsa-miR-155-5p (miR-155, MIR155HG), which is overexpressed in malignancies including chronic lymphocytic leukemia (CLL). Nonetheless, the precise mechanism of how miR-155 regulates the cell cycle in leukemic cells remains the subject of extensive research.

Methods: We edited the CLL cell line MEC-1 by CRISPR/Cas9 to introduce a short deletion within the MIR155HG gene. To describe changes at the transcriptome and miRNome level in miR-155-deficient cells, we performed mRNA-seq/miRNA-seq and validated changes by qRT-PCR. Flow cytometry was used to measure cell cycle kinetics. A WST-1 assay, hemocytometer, and Annexin V/PI staining assessed cell viability and proliferation.

Results: The limited but phenotypically robust miR-155 modification impaired cell proliferation, cell cycle, and cell ploidy. This was accompanied by overexpression of the negative cell cycle regulator p21/CDKN1A and Cyclin D1 (CCND1). We confirmed the overexpression of canonical miR-155 targets such as PU.1, FOS, SHIP-1, TP53INP1 and revealed new potential targets (FCRL5, ISG15, and MX1).

Conclusions: We demonstrate that miR-155 deficiency impairs cell proliferation, cell cycle, transcriptome, and miRNome via deregulation of the MIR155HG/TP53INP1/CDKN1A/CCND1 axis. Our CLL model is valuable for further studies to manipulate miRNA levels to revert highly aggressive leukemic cells to nearly benign or non-leukemic types.

Keywords: B-cells; CRISPR/Cas9; Cell cycle; Leukemia; miR-155.

MeSH terms

  • Carrier Proteins / genetics
  • Carrier Proteins / metabolism
  • Cell Cycle Checkpoints* / genetics
  • Cell Line, Tumor
  • Cell Proliferation / genetics
  • Cyclin D1 / genetics
  • Cyclin D1 / metabolism
  • Cyclin-Dependent Kinase Inhibitor p21* / genetics
  • Cyclin-Dependent Kinase Inhibitor p21* / metabolism
  • Gene Expression Regulation, Leukemic
  • Heat-Shock Proteins
  • Humans
  • Leukemia, Lymphocytic, Chronic, B-Cell* / genetics
  • Leukemia, Lymphocytic, Chronic, B-Cell* / pathology
  • MicroRNAs* / genetics
  • MicroRNAs* / metabolism

Substances

  • MicroRNAs
  • MIRN155 microRNA, human
  • TP53INP1 protein, human
  • Cyclin D1
  • Cyclin-Dependent Kinase Inhibitor p21
  • CCND1 protein, human
  • CDKN1A protein, human
  • Carrier Proteins
  • Heat-Shock Proteins