CD9 shapes glucocorticoid sensitivity in pediatric B-cell precursor acute lymphoblastic leukemia

Haematologica. 2024 Sep 1;109(9):2833-2845. doi: 10.3324/haematol.2023.282952.

Abstract

Resistance to glucocorticoids (GC), the common agents for remission induction in pediatric B-cell precursor acute lymphoblastic leukemia (BCP-ALL), poses a significant therapeutic hurdle. Therefore, dissecting the mechanisms shaping GC resistance could lead to new treatment modalities. Here, we showed that CD9- BCP-ALL cells were preferentially resistant to prednisone and dexamethasone over other standard cytotoxic agents. Concordantly, we identified significantly more poor responders to the prednisone prephase among BCP-ALL patients with a CD9- phenotype, especially for those with adverse presenting features including older age, higher white cell count and BCR-ABL1. Furthermore, gain- and loss-offunction experiments dictated a definitive functional linkage between CD9 expression and GC susceptibility, as demonstrated by the reversal and acquisition of relative GC resistance in CD9low and CD9high BCP-ALL cells, respectively. Despite physical binding to the GC receptor NR3C1, CD9 did not alter its expression, phosphorylation or nuclear translocation but potentiated the induction of GC-responsive genes in GC-resistant cells. Importantly, the MEK inhibitor trametinib exhibited higher synergy with GC against CD9- than CD9+ lymphoblasts to reverse drug resistance in vitro and in vivo. Collectively, our results elucidate a previously unrecognized regulatory function of CD9 in GC sensitivity, and inform new strategies for management of children with resistant BCP-ALL.

MeSH terms

  • Animals
  • Cell Line, Tumor
  • Child
  • Child, Preschool
  • Dexamethasone / pharmacology
  • Drug Resistance, Neoplasm* / genetics
  • Female
  • Glucocorticoids* / pharmacology
  • Glucocorticoids* / therapeutic use
  • Humans
  • Male
  • Mice
  • Precursor B-Cell Lymphoblastic Leukemia-Lymphoma* / drug therapy
  • Precursor B-Cell Lymphoblastic Leukemia-Lymphoma* / genetics
  • Precursor B-Cell Lymphoblastic Leukemia-Lymphoma* / metabolism
  • Precursor B-Cell Lymphoblastic Leukemia-Lymphoma* / pathology
  • Receptors, Glucocorticoid / genetics
  • Receptors, Glucocorticoid / metabolism
  • Tetraspanin 29* / genetics
  • Tetraspanin 29* / metabolism

Substances

  • Tetraspanin 29
  • Glucocorticoids
  • Receptors, Glucocorticoid
  • CD9 protein, human
  • Dexamethasone
  • NR3C1 protein, human

Grants and funding

Funding: This study was supported by the Bone Marrow Transplant Fund, Hong Kong (project no. 7105113); Children’s Cancer Foundation, Hong Kong (project no. 7104593); HOPE Research Seed Fund, The Chinese University of Hong Kong, Hong Kong (project no. HOPE-007); Sanming Project of Medicine, Shenzhen, China (project no. SZSM202011004); IdeaBooster Fund, The Chinese University of Hong Kong, Hong Kong (project no. IDBF23MED11); Ministry of Health, Czech Republic (AZV no. NU23-05-00353); and Direct Grant for Research, The Chinese University of Hong Kong, Hong Kong (project no. 4054491). The funding bodies were not involved in the study design, the collection, analysis, and interpretation of data, or the decision to submit the manuscript for publication.