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

Author

Listed:
  • John TCHEN

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex)

  • Quentin SIMON

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex
    Inovarion)

  • Léa CHAPART

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex)

  • Morgane K. THAMINY

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex)

  • Shamila VIBHUSHAN

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex)

  • Loredana SAVEANU

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex)

  • Yasmine LAMRI

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex)

  • Fanny SAIDOUNE

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex)

  • Emeline PACREAU

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex)

  • Christophe PELLEFIGUES

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex)

  • Julie BEX-COUDRAT

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex)

  • Hajime KARASUYAMA

    (Tokyo Medical and Dental University (TMDU))

  • Kensuke MIYAKE

    (Tokyo Medical and Dental University (TMDU))

  • Juan HIDALGO

    (Bellaterra Campus)

  • Padraic G. FALLON

    (Trinity College Dublin)

  • Thomas PAPO

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex
    Hôpital Bichat, Assistance Publique – Hôpitaux de Paris)

  • Ulrich BLANK

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex)

  • Marc BENHAMOU

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex)

  • Guillaume HANOUNA

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex
    Hôpital Bichat, Assistance Publique – Hôpitaux de Paris)

  • Karim SACRE

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex
    Hôpital Bichat, Assistance Publique – Hôpitaux de Paris)

  • Eric DAUGAS

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex
    Hôpital Bichat, Assistance Publique – Hôpitaux de Paris)

  • Nicolas CHARLES

    (Faculté de Médecine site Bichat
    Laboratoire d’Excellence Inflamex)

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.

Suggested Citation

  • John TCHEN & Quentin SIMON & Léa CHAPART & Morgane K. THAMINY & Shamila VIBHUSHAN & Loredana SAVEANU & Yasmine LAMRI & Fanny SAIDOUNE & Emeline PACREAU & Christophe PELLEFIGUES & Julie BEX-COUDRAT & H, 2024. "PD-L1- and IL-4-expressing basophils promote pathogenic accumulation of T follicular helper cells in lupus," Nature Communications, Nature, vol. 15(1), pages 1-18, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-47691-w
    DOI: 10.1038/s41467-024-47691-w
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    References listed on IDEAS

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    1. Atsushi Otsuka & Saeko Nakajima & Masato Kubo & Gyohei Egawa & Tetsuya Honda & Akihiko Kitoh & Takashi Nomura & Sho Hanakawa & Catharina Sagita Moniaga & Bongju Kim & Satoshi Matsuoka & Takeshi Watana, 2013. "Basophils are required for the induction of Th2 immunity to haptens and peptide antigens," Nature Communications, Nature, vol. 4(1), pages 1-9, June.
    2. Alan Bénard & Anne Jacobsen & Maximilian Brunner & Christian Krautz & Bettina Klösch & Izabela Swierzy & Elisabeth Naschberger & Malgorzata J. Podolska & Dina Kouhestani & Paul David & Torsten Birkhol, 2021. "Interleukin-3 is a predictive marker for severity and outcome during SARS-CoV-2 infections," Nature Communications, Nature, vol. 12(1), pages 1-8, December.
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