T cells with chimeric antigen receptors have potent antitumor effects and can establish memory in patients with advanced leukemia

Sci Transl Med. 2011 Aug 10;3(95):95ra73. doi: 10.1126/scitranslmed.3002842.

Abstract

Tumor immunotherapy with T lymphocytes, which can recognize and destroy malignant cells, has been limited by the ability to isolate and expand T cells restricted to tumor-associated antigens. Chimeric antigen receptors (CARs) composed of antibody binding domains connected to domains that activate T cells could overcome tolerance by allowing T cells to respond to cell surface antigens; however, to date, lymphocytes engineered to express CARs have demonstrated minimal in vivo expansion and antitumor effects in clinical trials. We report that CAR T cells that target CD19 and contain a costimulatory domain from CD137 and the T cell receptor ζ chain have potent non-cross-resistant clinical activity after infusion in three of three patients treated with advanced chronic lymphocytic leukemia (CLL). The engineered T cells expanded >1000-fold in vivo, trafficked to bone marrow, and continued to express functional CARs at high levels for at least 6 months. Evidence for on-target toxicity included B cell aplasia as well as decreased numbers of plasma cells and hypogammaglobulinemia. On average, each infused CAR-expressing T cell was calculated to eradicate at least 1000 CLL cells. Furthermore, a CD19-specific immune response was demonstrated in the blood and bone marrow, accompanied by complete remission, in two of three patients. Moreover, a portion of these cells persisted as memory CAR(+) T cells and retained anti-CD19 effector functionality, indicating the potential of this major histocompatibility complex-independent approach for the effective treatment of B cell malignancies.

Publication types

  • Clinical Trial
  • Research Support, N.I.H., Extramural

MeSH terms

  • Aged
  • Antigens / immunology*
  • Antigens, CD19 / metabolism
  • Antineoplastic Agents / therapeutic use*
  • Bone Marrow / immunology
  • Bone Marrow / pathology
  • Cell Proliferation
  • Cytokines / blood
  • Gene Transfer Techniques
  • Genetic Vectors / genetics
  • Humans
  • Immunologic Memory / immunology*
  • Leukemia / blood
  • Leukemia / immunology*
  • Leukemia / pathology*
  • Male
  • Middle Aged
  • Neoplasm Staging
  • Plasma Cells / immunology
  • Plasma Cells / pathology
  • Receptors, Immunologic / immunology*
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / pathology
  • Treatment Outcome
  • Tumor Burden / immunology

Substances

  • Antigens
  • Antigens, CD19
  • Antineoplastic Agents
  • Cytokines
  • Receptors, Immunologic