Drug-regulated CD33-targeted CAR T cells control AML using clinically optimized rapamycin dosing

J Clin Invest. 2024 Mar 19;134(9):e162593. doi: 10.1172/JCI162593.

Abstract

Chimeric antigen receptor (CAR) designs that incorporate pharmacologic control are desirable; however, designs suitable for clinical translation are needed. We designed a fully human, rapamycin-regulated drug product for targeting CD33+ tumors called dimerizaing agent-regulated immunoreceptor complex (DARIC33). T cell products demonstrated target-specific and rapamycin-dependent cytokine release, transcriptional responses, cytotoxicity, and in vivo antileukemic activity in the presence of as little as 1 nM rapamycin. Rapamycin withdrawal paused DARIC33-stimulated T cell effector functions, which were restored following reexposure to rapamycin, demonstrating reversible effector function control. While rapamycin-regulated DARIC33 T cells were highly sensitive to target antigen, CD34+ stem cell colony-forming capacity was not impacted. We benchmarked DARIC33 potency relative to CD19 CAR T cells to estimate a T cell dose for clinical testing. In addition, we integrated in vitro and preclinical in vivo drug concentration thresholds for off-on state transitions, as well as murine and human rapamycin pharmacokinetics, to estimate a clinically applicable rapamycin dosing schedule. A phase I DARIC33 trial has been initiated (PLAT-08, NCT05105152), with initial evidence of rapamycin-regulated T cell activation and antitumor impact. Our findings provide evidence that the DARIC platform exhibits sensitive regulation and potency needed for clinical application to other important immunotherapy targets.

Keywords: Cancer immunotherapy; Hematology; Leukemias; T cells; Therapeutics.

Publication types

  • Clinical Trial
  • Research Support, N.I.H., Extramural
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Animals
  • Female
  • Humans
  • Immunotherapy, Adoptive
  • Leukemia, Myeloid, Acute* / drug therapy
  • Leukemia, Myeloid, Acute* / immunology
  • Leukemia, Myeloid, Acute* / pathology
  • Leukemia, Myeloid, Acute* / therapy
  • Male
  • Mice
  • Receptors, Chimeric Antigen / immunology
  • Sialic Acid Binding Ig-like Lectin 3* / immunology
  • Sialic Acid Binding Ig-like Lectin 3* / metabolism
  • Sirolimus* / administration & dosage
  • Sirolimus* / pharmacology
  • T-Lymphocytes* / drug effects
  • T-Lymphocytes* / immunology
  • Xenograft Model Antitumor Assays

Substances

  • CD33 protein, human
  • Receptors, Chimeric Antigen
  • Sialic Acid Binding Ig-like Lectin 3
  • Sirolimus