Stromal cells engineered to express T cell factors induce robust CLL cell proliferation in vitro and in PDX co-transplantations allowing the identification of RAF inhibitors as anti-proliferative drugs

Leukemia. 2024 Aug;38(8):1699-1711. doi: 10.1038/s41375-024-02284-w. Epub 2024 Jun 14.

Abstract

Several in vitro models have been developed to mimic chronic lymphocytic leukemia (CLL) proliferation in immune niches; however, they typically do not induce robust proliferation. We prepared a novel model based on mimicking T-cell signals in vitro and in patient-derived xenografts (PDXs). Six supportive cell lines were prepared by engineering HS5 stromal cells with stable expression of human CD40L, IL4, IL21, and their combinations. Co-culture with HS5 expressing CD40L and IL4 in combination led to mild CLL cell proliferation (median 7% at day 7), while the HS5 expressing CD40L, IL4, and IL21 led to unprecedented proliferation rate (median 44%). The co-cultures mimicked the gene expression fingerprint of lymph node CLL cells (MYC, NFκB, and E2F signatures) and revealed novel vulnerabilities in CLL-T-cell-induced proliferation. Drug testing in co-cultures revealed for the first time that pan-RAF inhibitors fully block CLL proliferation. The co-culture model can be downscaled to five microliter volume for large drug screening purposes or upscaled to CLL PDXs by HS5-CD40L-IL4 ± IL21 co-transplantation. Co-transplanting NSG mice with purified CLL cells and HS5-CD40L-IL4 or HS5-CD40L-IL4-IL21 cells on collagen-based scaffold led to 47% or 82% engraftment efficacy, respectively, with ~20% of PDXs being clonally related to CLL, potentially overcoming the need to co-transplant autologous T-cells in PDXs.

MeSH terms

  • Animals
  • CD40 Ligand* / genetics
  • CD40 Ligand* / metabolism
  • Cell Proliferation*
  • Coculture Techniques*
  • Humans
  • Interleukins / genetics
  • Interleukins / metabolism
  • Leukemia, Lymphocytic, Chronic, B-Cell* / drug therapy
  • Leukemia, Lymphocytic, Chronic, B-Cell* / genetics
  • Leukemia, Lymphocytic, Chronic, B-Cell* / pathology
  • Mice
  • Protein Kinase Inhibitors / pharmacology
  • Stromal Cells* / metabolism
  • Stromal Cells* / pathology
  • T-Lymphocytes / immunology
  • T-Lymphocytes / metabolism
  • Xenograft Model Antitumor Assays

Substances

  • CD40 Ligand
  • interleukin-21
  • Interleukins
  • Protein Kinase Inhibitors