PD-L1- and IL-4-expressing basophils promote pathogenic accumulation of T follicular helper cells in lupus

Nat Commun. 2024 Apr 22;15(1):3389. doi: 10.1038/s41467-024-47691-w.

Abstract

Systemic lupus erythematosus (SLE) is an autoimmune disease characterized by anti-nuclear autoantibodies whose production is promoted by autoreactive T follicular helper (TFH) cells. During SLE pathogenesis, basophils accumulate in secondary lymphoid organs (SLO), amplify autoantibody production and disease progression through mechanisms that remain to be defined. Here, we provide evidence for a direct functional relationship between TFH cells and basophils during lupus pathogenesis, both in humans and mice. PD-L1 upregulation on basophils and IL-4 production are associated with TFH and TFH2 cell expansions and with disease activity. Pathogenic TFH cell accumulation, maintenance, and function in SLO were dependent on PD-L1 and IL-4 in basophils, which induced a transcriptional program allowing TFH2 cell differentiation and function. Our study establishes a direct mechanistic link between basophils and TFH cells in SLE that promotes autoantibody production and lupus nephritis.

Publication types

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

MeSH terms

  • Adult
  • Animals
  • Autoantibodies / immunology
  • B7-H1 Antigen* / genetics
  • B7-H1 Antigen* / metabolism
  • Basophils* / immunology
  • Basophils* / metabolism
  • Cell Differentiation / immunology
  • Female
  • Humans
  • Interleukin-4* / immunology
  • Interleukin-4* / metabolism
  • Lupus Erythematosus, Systemic* / immunology
  • Lupus Erythematosus, Systemic* / metabolism
  • Lupus Erythematosus, Systemic* / pathology
  • Lupus Nephritis / immunology
  • Lupus Nephritis / metabolism
  • Lupus Nephritis / pathology
  • Male
  • Mice
  • Mice, Inbred C57BL
  • Middle Aged
  • T Follicular Helper Cells* / immunology
  • T Follicular Helper Cells* / metabolism
  • T-Lymphocytes, Helper-Inducer / immunology
  • T-Lymphocytes, Helper-Inducer / metabolism

Substances

  • Autoantibodies
  • B7-H1 Antigen
  • CD274 protein, human
  • Cd274 protein, mouse
  • Interleukin-4
  • IL4 protein, human
  • Il4 protein, mouse