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Iwai and Honjo: tumours use PD-L1 to escape T cells, and blocking it restores attack

A decade after Honjo's group cloned PD-1 (1992), this study showed that tumour cells expressing PD-L1 resist killing by cytotoxic T cells in mice, and that anti-PD-L1 antibody or PD-1 deficiency restores tumour rejection, the foundation of PD-1/PD-L1 therapy.

Tasuku Honjo's group discovered PD-1 in 1992 (Ishida et al., EMBO J) as a gene induced during programmed cell death in T-cell lines, and later showed PD-1-deficient mice develop autoimmunity, identifying it as an inhibitory receptor. PD-L1 (B7-H1) was identified as its ligand by Freeman, Honjo and colleagues in 2000.

In this paper, P815 mastocytoma cells transfected with PD-L1 were less susceptible to lysis by cytotoxic T lymphocytes in vitro and grew more aggressively in vivo; anti-PD-L1 antibody reversed this. Myeloma cells naturally expressing PD-L1 grew in wild-type mice but were rejected in PD-1-deficient mice. In parallel, Dong and Chen (Nature Medicine 2002) showed that PD-L1 expressed on human tumours induced T-cell apoptosis.

These data motivated the development of nivolumab (Ono/Medarex) and other PD-1 and PD-L1 antibodies, now the most widely used cancer drugs in the world. Honjo shared the 2018 Nobel Prize with James Allison.

Basic scienceHas not changed practice yet
Authors
Iwai Y, Ishida M, Tanaka Y, Okazaki T, Honjo T, Minato N
Published
PNAS, 2002
What it found
  • PD-L1 expression on tumour cells reduced cytotoxic T-cell killing in vitro and enhanced tumour growth in mice
  • Anti-PD-L1 antibody suppressed growth of PD-L1-expressing tumours
  • Naturally PD-L1-positive myeloma cells were rejected in PD-1-deficient mice but not in wild-type mice
  • Together with Ishida 1992 and Freeman 2000, defined the PD-1/PD-L1 axis as a tumour immune-escape mechanism
What it means

Tumours hide from T cells by displaying PD-L1; blocking that interaction lets the immune system attack. This is the mechanism of pembrolizumab, nivolumab, atezolizumab and their relatives, which now treat more than 20 cancer types.

Be careful
  • Mouse tumour models overexpressing PD-L1 exaggerate a mechanism that is only one of many in human tumours
  • PD-L1 expression on tumour cells is an imperfect biomarker of response in patients
  • Most patients do not respond to PD-1 blockade, and mechanisms of primary resistance remain incompletely understood
  • Clinical translation took another decade and depended on industry (Ono, Medarex, BMS, Merck) investment

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