Engraftment of mesothelin chimeric antigen receptor using a hybrid Sleeping Beauty/minicircle vector into NK-92MI cells for treatment of pancreatic cancer

Surgery. 2019 Oct;166(4):503-508. doi: 10.1016/j.surg.2019.05.047. Epub 2019 Aug 13.

Abstract

Background: We have previously demonstrated in vitro cytotoxicity of mesothelin-chimeric antigen receptor autologous T cells against pancreatic cancer cells using lentiviral vectors, but these vectors pose safety concerns. Here, we incorporated Sleeping Beauty and minicircle design enhancements into interleukin-2-secreting natural NK-92MI cells to eliminate both bacterial and viral components and address inhibition by the tumor microenvironment.

Methods: Parental (conventional deoxyribonucleic acid)-mesothelin-chimeric antigen receptor and minicircle-mesothelin-chimeric antigen receptor vectors were electroporated into NK-92MI cells and engraftment was visualized by immunofluorescence analysis with protein-L staining. Interferon-γ and granzyme B secretion were measured by enzyme-linked immunosorbent assay from cocultures of parental-mesothelin-chimeric antigen receptors and minicircle-mesothelin-chimeric antigen receptors with human pancreatic cancer cells, and cytotoxicity of chimeric antigen receptor NK-92MI cells was tested against three pancreatic cancer cell lines.

Results: Cloning of mesothelin-chimeric antigen receptor Sleeping Beauty into a minicircle vector removed its bacterial backbone and reduced its size with improved electroporation efficiency. Chimeric antigen receptor engraftment, Interferon-γ and granzyme B secretion, and specific lysis against all three pancreatic cancer lines were significantly increased with minicircle-mesothelin-chimeric antigen receptor versus parental-mesothelin-chimeric antigen receptor NK-92MI cells.

Conclusion: We provide proof of concept that allogeneic mesothelin-chimeric antigen receptor NK-92MI cells with hybrid Sleeping Beauty and minicircle technologies provide increased engraftment and cytotoxicity in vitro with potential safety benefits when translated to the clinical arena.

Publication types

  • Research Support, Non-U.S. Gov't

MeSH terms

  • Cell Death / immunology*
  • Cell Line, Tumor
  • Electroporation / methods
  • Enzyme-Linked Immunosorbent Assay
  • GPI-Linked Proteins / pharmacology*
  • Humans
  • Immunotherapy, Adoptive / methods*
  • In Vitro Techniques
  • Killer Cells, Natural / drug effects
  • Killer Cells, Natural / immunology*
  • Mesothelin
  • Pancreatic Neoplasms / pathology*
  • Pancreatic Neoplasms / therapy
  • Receptors, Chimeric Antigen / immunology*
  • Sensitivity and Specificity
  • Tumor Microenvironment

Substances

  • GPI-Linked Proteins
  • Receptors, Chimeric Antigen
  • Mesothelin