CD38-Mediated Immunosuppression as a Mechanism of Tumor Cell Escape from PD-1/PD-L1 Blockade

Cancer Discov. 2018 Sep;8(9):1156-1175. doi: 10.1158/2159-8290.CD-17-1033. Epub 2018 Jul 16.

Abstract

Although treatment with immune checkpoint inhibitors provides promising benefit for patients with cancer, optimal use is encumbered by high resistance rates and requires a thorough understanding of resistance mechanisms. We observed that tumors treated with PD-1/PD-L1 blocking antibodies develop resistance through the upregulation of CD38, which is induced by all-trans retinoic acid and IFNβ in the tumor microenvironment. In vitro and in vivo studies demonstrate that CD38 inhibits CD8+ T-cell function via adenosine receptor signaling and that CD38 or adenosine receptor blockade are effective strategies to overcome the resistance. Large data sets of human tumors reveal expression of CD38 in a subset of tumors with high levels of basal or treatment-induced T-cell infiltration, where immune checkpoint therapies are thought to be most effective. These findings provide a novel mechanism of acquired resistance to immune checkpoint therapy and an opportunity to expand their efficacy in cancer treatment.Significance: CD38 is a major mechanism of acquired resistance to PD-1/PD-L1 blockade, causing CD8+ T-cell suppression. Coinhibition of CD38 and PD-L1 improves antitumor immune response. Biomarker assessment in patient cohorts suggests that a combination strategy is applicable to a large percentage of patients in whom PD-1/PD-L1 blockade is currently indicated. Cancer Discov; 8(9); 1156-75. ©2018 AACR.See related commentary by Mittal et al., p. 1066This article is highlighted in the In This Issue feature, p. 1047.

Publication types

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

MeSH terms

  • ADP-ribosyl Cyclase 1 / antagonists & inhibitors
  • ADP-ribosyl Cyclase 1 / metabolism*
  • Animals
  • Antineoplastic Agents, Immunological / administration & dosage*
  • Antineoplastic Agents, Immunological / pharmacology
  • B7-H1 Antigen / antagonists & inhibitors
  • CD8-Positive T-Lymphocytes / drug effects
  • CD8-Positive T-Lymphocytes / immunology
  • Carcinoma, Non-Small-Cell Lung / drug therapy*
  • Carcinoma, Non-Small-Cell Lung / immunology
  • Cell Line, Tumor
  • Drug Resistance, Neoplasm / drug effects*
  • Drug Synergism
  • Gene Expression Regulation, Neoplastic / drug effects
  • Humans
  • Interferon-gamma / metabolism
  • Lung Neoplasms / drug therapy*
  • Lung Neoplasms / immunology
  • Melanoma / drug therapy*
  • Melanoma / genetics
  • Melanoma / immunology
  • Membrane Glycoproteins / antagonists & inhibitors
  • Membrane Glycoproteins / metabolism*
  • Mice
  • Programmed Cell Death 1 Receptor / antagonists & inhibitors
  • Receptors, Purinergic P1 / metabolism
  • Signal Transduction / drug effects
  • Tretinoin / metabolism
  • Tumor Microenvironment / drug effects
  • Up-Regulation / drug effects
  • Xenograft Model Antitumor Assays

Substances

  • Antineoplastic Agents, Immunological
  • B7-H1 Antigen
  • CD274 protein, human
  • Membrane Glycoproteins
  • PDCD1 protein, human
  • Programmed Cell Death 1 Receptor
  • Receptors, Purinergic P1
  • Tretinoin
  • Interferon-gamma
  • CD38 protein, human
  • ADP-ribosyl Cyclase 1