CRISPR-Cas9-Mediated Glucocorticoid Resistance in Virus-Specific T Cells for Adoptive T Cell Therapy Posttransplantation

Mol Ther. 2020 Sep 2;28(9):1965-1973. doi: 10.1016/j.ymthe.2020.06.002. Epub 2020 Jun 11.

Abstract

Immunosuppression posttransplantation exposes patients to an increased risk for refractory viral infections as an important cause of morbidity and mortality. Protective T cell immunity can be restored by adoptive T cell transfer, but ongoing immunosuppression limits efficacy of T cell responses. In order to deliver protection against viral pathogens and allow at the same time necessary steroid therapy, we generated glucocorticoid-resistant T cells by CRISPR-Cas9-mediated knockout of the glucocorticoid receptor in primary human virus-specific T cell products. Characterization of the T cell product revealed high efficiency of glucocorticoid receptor knockout and high purity of virus-specific T cells. This tandem T cell engineering preserved protective T cell functionality, such as cytotoxicity, CD107a degranulation, proliferative capacity, and cytokine release patterns. Virus-specific T cells with glucocorticoid receptor knockout were resistant to the suppressive effect of dexamethasone treatment on lymphocyte proliferation and cytokine secretion (tumor necrosis factor alpha [TNF-α], interleukin-4 [IL-4], IL-6, and sFas). Additionally, glucocorticoid receptor knockout cells remained sensitive to cyclosporine A treatment, thereby providing a rescue approach for patients in case of safety issues. This novel approach provides a therapeutic option for the treatment of patients with viral infections after transplantation who are receiving glucocorticoid therapy.

Keywords: CRISPR/Cas9; T cell therapy; genetic engineering; glucocorticoid receptor; stem cell transplantation; virus-specific T cells.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer / methods*
  • CRISPR-Cas Systems*
  • Cell Engineering / methods*
  • Cell Proliferation / genetics
  • Cells, Cultured
  • Cyclosporine / pharmacology
  • Cytokines / metabolism
  • Drug Resistance / genetics*
  • Gene Knockout Techniques / methods
  • Glucocorticoids / therapeutic use*
  • Hematopoietic Stem Cell Transplantation / adverse effects*
  • Humans
  • Lymphocyte Activation / immunology
  • Receptors, Glucocorticoid / deficiency
  • Receptors, Glucocorticoid / genetics
  • T-Lymphocytes / drug effects
  • T-Lymphocytes / immunology*
  • T-Lymphocytes / metabolism
  • Viral Matrix Proteins / immunology
  • Virus Diseases / etiology*
  • Virus Diseases / immunology
  • Virus Diseases / therapy*

Substances

  • Cytokines
  • Glucocorticoids
  • Receptors, Glucocorticoid
  • Viral Matrix Proteins
  • cytomegalovirus matrix protein 65kDa
  • Cyclosporine