Synergy of a STING agonist and an IL-2 superkine in cancer immunotherapy against MHC I-deficient and MHC I+ tumors

Proc Natl Acad Sci U S A. 2022 May 31;119(22):e2200568119. doi: 10.1073/pnas.2200568119. Epub 2022 May 19.

Abstract

Cyclic dinucleotides (CDN) and Toll-like receptor (TLR) ligands mobilize antitumor responses by natural killer (NK) cells and T cells, potentially serving as complementary therapies to immune checkpoint therapy. In the clinic thus far, however, CDN therapy targeting stimulator of interferon genes (STING) protein has yielded mixed results, perhaps because it initiates responses potently but does not provide signals to sustain activation and proliferation of activated cytotoxic lymphocytes. To improve efficacy, we combined CDN with a half life-extended interleukin-2 (IL-2) superkine, H9-MSA (mouse serum albumin). CDN/H9-MSA therapy induced dramatic long-term remissions of the most difficult to treat major histocompatibility complex class I (MHC I)–deficient and MHC I+ tumor transplant models. H9-MSA combined with CpG oligonucleotide also induced potent responses. Mechanistically, tumor elimination required CD8 T cells and not NK cells in the case of MHC I+ tumors and NK cells but not CD8 T cells in the case of MHC-deficient tumors. Furthermore, combination therapy resulted in more prolonged and more intense NK cell activation, cytotoxicity, and expression of cytotoxic effector molecules in comparison with monotherapy. Remarkably, in a primary autochthonous sarcoma model that is refractory to PD-1 checkpoint therapy, the combination of CDN/H9-MSA with checkpoint therapy yielded long-term remissions in the majority of the animals, mediated by T cells and NK cells. This combination therapy has the potential to activate responses in tumors resistant to current therapies and prevent MHC I loss accompanying acquired resistance of tumors to checkpoint therapy.

Keywords: IL-2 superkine; NK cell; STING agonist; T cell; cancer immunotherapy.

Publication types

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

MeSH terms

  • Animals
  • Antineoplastic Combined Chemotherapy Protocols*
  • CD8-Positive T-Lymphocytes / immunology
  • Histocompatibility Antigens Class I* / genetics
  • Humans
  • Immunotherapy* / methods
  • Interleukin-2* / immunology
  • Killer Cells, Natural / immunology
  • Membrane Proteins* / agonists
  • Mice
  • Neoplasms* / genetics
  • Neoplasms* / therapy
  • Nucleotides, Cyclic* / therapeutic use
  • Oligodeoxyribonucleotides* / therapeutic use
  • Serum Albumin* / therapeutic use

Substances

  • Histocompatibility Antigens Class I
  • Interleukin-2
  • Membrane Proteins
  • Nucleotides, Cyclic
  • Oligodeoxyribonucleotides
  • STING1 protein, human
  • Serum Albumin