Hijacking antibody-induced CTLA-4 lysosomal degradation for safer and more effective cancer immunotherapy

Cell Res. 2019 Aug;29(8):609-627. doi: 10.1038/s41422-019-0184-1. Epub 2019 Jul 2.

Abstract

It remains unclear why the clinically used anti-CTLA-4 antibodies, popularly called checkpoint inhibitors, have severe immunotherapy-related adverse effects (irAEs) and yet suboptimal cancer immunotherapeutic effects (CITE). Here we report that while irAE-prone Ipilimumab and TremeIgG1 rapidly direct cell surface CTLA-4 for lysosomal degradation, the non-irAE-prone antibodies we generated, HL12 or HL32, dissociate from CTLA-4 after endocytosis and allow CTLA-4 recycling to cell surface by the LRBA-dependent mechanism. Disrupting CTLA-4 recycling results in robust CTLA-4 downregulation by all anti-CTLA-4 antibodies and confers toxicity to a non-irAE-prone anti-CTLA-4 mAb. Conversely, increasing the pH sensitivity of TremeIgG1 by introducing designed tyrosine-to-histidine mutations prevents antibody-triggered lysosomal CTLA-4 downregulation and dramatically attenuates irAE. Surprisingly, by avoiding CTLA-4 downregulation and due to their increased bioavailability, pH-sensitive anti-CTLA-4 antibodies are more effective in intratumor regulatory T-cell depletion and rejection of large established tumors. Our data establish a new paradigm for cancer research that allows for abrogating irAE while increasing CITE of anti-CTLA-4 antibodies.

Publication types

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

MeSH terms

  • Animals
  • Antineoplastic Agents, Immunological / adverse effects
  • Antineoplastic Agents, Immunological / pharmacology
  • Antineoplastic Agents, Immunological / therapeutic use*
  • CHO Cells
  • CTLA-4 Antigen / genetics
  • CTLA-4 Antigen / immunology
  • CTLA-4 Antigen / metabolism*
  • Cricetulus
  • Gene Knock-In Techniques
  • HEK293 Cells
  • Humans
  • Hydrogen-Ion Concentration
  • Immunoglobulin G / pharmacology
  • Immunoglobulin G / therapeutic use
  • Immunotherapy / adverse effects*
  • Ipilimumab / adverse effects
  • Ipilimumab / pharmacology
  • Ipilimumab / therapeutic use*
  • Lysosomes / metabolism*
  • Mice
  • Mice, Inbred C57BL
  • Mice, Transgenic
  • Neoplasms / therapy*
  • Proteolysis / drug effects*
  • T-Lymphocytes, Regulatory / immunology
  • Transfection

Substances

  • Antineoplastic Agents, Immunological
  • CTLA-4 Antigen
  • CTLA4 protein, human
  • Immunoglobulin G
  • Ipilimumab