Mechanistic insights into immune checkpoint inhibitor-related hypophysitis: a form of paraneoplastic syndrome

Cancer Immunol Immunother. 2021 Dec;70(12):3669-3677. doi: 10.1007/s00262-021-02955-y. Epub 2021 May 11.

Abstract

Background: Immune checkpoint inhibitors (ICIs) as a cancer immunotherapy have emerged as a treatment for multiple advanced cancer types. Because of enhanced immune responses, immune-related adverse events (irAEs), including endocrinopathies such as hypophysitis, have been associated with the use of ICIs. Most underlying mechanisms of ICI-related hypophysitis remain unclear, especially for programmed cell death-1 (PD-1)/PD-1 ligand 1 (PD-L1) inhibitors. We hypothesized that ICI-related hypophysitis is associated with paraneoplastic syndrome caused by ectopic expression of pituitary-specific antigens.

Methods: Twenty consecutive patients with ICI-related hypophysitis between 2017 and 2019 at Kobe University Hospital were retrospectively analyzed. Circulating anti-pituitary antibodies were detected using immunofluorescence staining and immunoblotting. Ectopic expression of pituitary autoantigens in tumor specimens was also examined.

Results: Eighteen patients were treated with PD-1/PD-L1 inhibitors, and two were treated with a combination of cytotoxic T-lymphocyte antigen-4 (CTLA-4) and PD-1 inhibitors. All patients showed adrenocorticotropic hormone (ACTH) deficiency and additionally, three showed thyroid-stimulating hormone (TSH) deficiency, and one showed gonadotropin-releasing hormone (GnRH) deficiency. Among these patients, three exhibited anti-pituitary antibodies, two with anti-corticotroph antibody and one with anti-somatotroph antibody. Interestingly, the anti-corticotroph antibody recognized proopiomelanocortin (POMC) and those two patients exhibited ectopic ACTH expression in the tumor, while the patients without anti-corticotroph antibody did not.

Conclusions: We demonstrated 10% of PD-1/PD-L1 inhibitors-related hypophysitis were associated with the autoimmunity against corticotrophs and maybe caused as a form of paraneoplastic syndrome, in which ectopic expression of ACTH in the tumor was observed. It is also suggested that the pathophysiology is heterogenous in ICI-related hypophysitis.

Keywords: Autoimmunity; Hypophysitis; Hypopituitarism; Immune checkpoint inhibitor; Paraneoplastic syndrome.

MeSH terms

  • Adrenal Insufficiency / immunology
  • Adrenal Insufficiency / therapy
  • Adult
  • Aged
  • Aged, 80 and over
  • Animals
  • B7-H1 Antigen / immunology
  • CTLA-4 Antigen / immunology
  • Corticotrophs / immunology
  • Female
  • Humans
  • Hypophysitis / immunology*
  • Hypophysitis / therapy*
  • Immune Checkpoint Inhibitors / therapeutic use*
  • Immunotherapy / methods
  • Male
  • Mice
  • Middle Aged
  • Neoplasms / immunology
  • Neoplasms / therapy
  • Paraneoplastic Syndromes / immunology*
  • Paraneoplastic Syndromes / therapy*
  • Pro-Opiomelanocortin / immunology
  • Programmed Cell Death 1 Receptor / immunology
  • Retrospective Studies

Substances

  • B7-H1 Antigen
  • CTLA-4 Antigen
  • Immune Checkpoint Inhibitors
  • Programmed Cell Death 1 Receptor
  • Pro-Opiomelanocortin

Supplementary concepts

  • Adrenocorticotropic hormone deficiency