Hydroxyurea-induced senescent peripheral blood mesenchymal stromal cells inhibit bystander cell proliferation of JAK2V617F-positive human erythroleukemia cells

FEBS J. 2019 Sep;286(18):3647-3663. doi: 10.1111/febs.14927. Epub 2019 May 23.

Abstract

Hydroxyurea (HU) is a nonalkylating antineoplastic agent used in the treatment of hematological malignancies. HU is a DNA replication stress inducer, and as such, it may induce a premature senescence-like cell phenotype; however, its repercussion on bystander cell proliferation has not been revealed so far. Our results indicate that HU strongly inhibited peripheral blood mesenchymal stromal cells (PBMSC) proliferation by cell cycle arrest in S phase, and that, consequently, PBMSC acquire senescence-related phenotypical changes. HU-treated PBMSC display increased senescence-associated β-galactosidase levels and p16INK4 expression, as well as DNA damage response and genotoxic effects, evidenced by expression of γH2A.X and micronuclei. Moreover, HU-induced PBMSC senescence is mediated by increased reactive oxygen species (ROS) levels, as demonstrated by the inhibition of senescence markers in the presence of ROS scavenger N-acetylcysteine and NADPH oxidase inhibitor Apocynin. To determine the HU-induced bystander effect, we used the JAK2V617F-positive human erythroleukemia 92.1.7 (HEL) cells. Co-culture with HU-induced senescent PBMSC (HU-S-PBMSC) strongly inhibited bystander HEL cell proliferation, and this effect is mediated by both ROS and transforming growth factor (TGF)-β expression. Besides induction of premature senescence, HU educates PBMSC toward an inhibitory phenotype of HEL cell proliferation. Finally, our study contributes to the understanding of the role of HU-induced PBMSC senescence as a potential adjuvant in hematological malignancy therapies.

Keywords: bystander effects; hydroxyurea; peripheral blood mesenchymal stem cells; proliferation; reactive oxygen species; senescence.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Bystander Effect / genetics
  • Cell Cycle Checkpoints / drug effects
  • Cell Line, Tumor
  • Cell Proliferation / drug effects
  • Cellular Senescence / drug effects*
  • DNA Damage / drug effects
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Hydroxyurea / pharmacology*
  • Janus Kinase 2 / genetics*
  • Leukemia, Erythroblastic, Acute / drug therapy*
  • Leukemia, Erythroblastic, Acute / genetics
  • Leukemia, Erythroblastic, Acute / pathology
  • Mesenchymal Stem Cells / drug effects
  • Peripheral Blood Stem Cells / drug effects
  • Reactive Oxygen Species / metabolism
  • Transforming Growth Factor beta / genetics*

Substances

  • Reactive Oxygen Species
  • Transforming Growth Factor beta
  • JAK2 protein, human
  • Janus Kinase 2
  • Hydroxyurea