In Vitro and In Vivo Comparison of Lymphocytes Transduced with a Human CD16 or with a Chimeric Antigen Receptor Reveals Potential Off-Target Interactions due to the IgG2 CH2-CH3 CAR-Spacer

J Immunol Res. 2015:2015:482089. doi: 10.1155/2015/482089. Epub 2015 Nov 17.

Abstract

The present work was designed to compare two mechanisms of cellular recognition based on Ab specificity: firstly, when the anti-HER2 mAb trastuzumab bridges target cells and cytotoxic lymphocytes armed with a Fc receptor (ADCC) and, secondly, when HER2 positive target cells are directly recognized by cytotoxic lymphocytes armed with a chimeric antigen receptor (CAR). To compare these two mechanisms, we used the same cellular effector (NK-92) and the same signaling domain (FcεRIγ). The NK-92 cytotoxic cell line was transfected with either a FcγRIIIa-FcεRIγ (NK-92(CD16)) or a trastuzumab-based scFv-FcεRIγ chimeric receptor (NK-92(CAR)). In vitro, the cytotoxic activity against HER2 positive target cells after indirect recognition by NK-92(CD16) was always inferior to that observed after direct recognition by NK-92(CAR). In contrast, and somehow unexpectedly, in vivo, adoptive transfer of NK-92(CD16) + trastuzumab but not of NK-92(CAR) induced tumor regression. Analysis of the in vivo xenogeneic system suggested that the human CH2-CH3 IgG2 used as a spacer in our construct was able to interact with the FcR present at the cell surface of the few NSG-FcR+ remaining immune cells. This interaction, leading to blockage of the NK-92(CAR) in the periphery of the engrafted tumor cells, stresses the critical role of the composition of the spacer domain.

Publication types

  • Comparative Study
  • Research Support, Non-U.S. Gov't

MeSH terms

  • Adoptive Transfer
  • Animals
  • Antineoplastic Agents / chemistry
  • Antineoplastic Agents / pharmacology*
  • Cetuximab / chemistry
  • Cetuximab / pharmacology
  • Cytotoxicity, Immunologic / drug effects*
  • GPI-Linked Proteins / chemistry
  • GPI-Linked Proteins / genetics
  • GPI-Linked Proteins / immunology
  • Gene Expression
  • Humans
  • Immunoglobulin G / chemistry
  • Immunoglobulin G / genetics
  • Immunoglobulin G / immunology*
  • K562 Cells
  • Mice
  • Mice, Inbred NOD
  • Mice, SCID
  • Receptor, ErbB-2 / chemistry
  • Receptor, ErbB-2 / genetics
  • Receptor, ErbB-2 / immunology
  • Receptors, IgE / chemistry
  • Receptors, IgE / genetics
  • Receptors, IgE / immunology
  • Receptors, IgG / chemistry
  • Receptors, IgG / genetics
  • Receptors, IgG / immunology*
  • Recombinant Fusion Proteins / chemistry
  • Recombinant Fusion Proteins / genetics
  • Recombinant Fusion Proteins / immunology*
  • Single-Chain Antibodies / chemistry
  • Single-Chain Antibodies / genetics
  • Single-Chain Antibodies / immunology
  • T-Lymphocytes, Cytotoxic / cytology
  • T-Lymphocytes, Cytotoxic / immunology*
  • Transduction, Genetic
  • Trastuzumab / chemistry
  • Trastuzumab / pharmacology
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents
  • FCGR3A protein, human
  • FCGR3B protein, human
  • FcepsilonRI gamma-chain, human
  • GPI-Linked Proteins
  • Immunoglobulin G
  • Receptors, IgE
  • Receptors, IgG
  • Recombinant Fusion Proteins
  • Single-Chain Antibodies
  • ERBB2 protein, human
  • Receptor, ErbB-2
  • Trastuzumab
  • Cetuximab