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Distinct transcriptomes and autocrine cytokines underpin maturation and survival of antibody-secreting cells in systemic lupus erythematosus

Author

Listed:
  • Weirong Chen

    (School of Medicine, Emory University)

  • So-Hee Hong

    (School of Medicine, Emory University
    Ewha Womans University)

  • Scott A. Jenks

    (School of Medicine, Emory University)

  • Fabliha A. Anam

    (School of Medicine, Emory University)

  • Christopher M. Tipton

    (School of Medicine, Emory University)

  • Matthew C. Woodruff

    (School of Medicine, Emory University)

  • Jennifer R. Hom

    (School of Medicine, Emory University)

  • Kevin S. Cashman

    (School of Medicine, Emory University)

  • Caterina Elisa Faliti

    (School of Medicine, Emory University)

  • Xiaoqian Wang

    (School of Medicine, Emory University)

  • Shuya Kyu

    (School of Medicine, Emory University)

  • Chungwen Wei

    (School of Medicine, Emory University)

  • Christopher D. Scharer

    (School of Medicine, Emory University)

  • Tian Mi

    (School of Medicine, Emory University)

  • Sakeenah Hicks

    (School of Medicine, Emory University)

  • Louise Hartson

    (School of Medicine, Emory University)

  • Doan C. Nguyen

    (School of Medicine, Emory University)

  • Arezou Khosroshahi

    (School of Medicine, Emory University)

  • Saeyun Lee

    (School of Medicine, Emory University)

  • Youliang Wang

    (School of Medicine, Emory University)

  • Regina Bugrovsky

    (School of Medicine, Emory University)

  • Yusho Ishii

    (School of Medicine, Emory University)

  • F. Eun-Hyung Lee

    (School of Medicine, Emory University)

  • Ignacio Sanz

    (School of Medicine, Emory University)

Abstract

Systemic lupus erythematosus (SLE) is an autoimmune disease characterized by multiple autoantibody types, some of which are produced by long-lived plasma cells (LLPC). Active SLE generates increased circulating antibody-secreting cells (ASC). Here, we examine the phenotypic, molecular, structural, and functional features of ASC in SLE. Relative to post-vaccination ASC in healthy controls, circulating blood ASC from patients with active SLE are enriched with newly generated mature CD19−CD138+ ASC, similar to bone marrow LLPC. ASC from patients with SLE displayed morphological features of premature maturation and a transcriptome epigenetically initiated in SLE B cells. ASC from patients with SLE exhibited elevated protein levels of CXCR4, CXCR3 and CD138, along with molecular programs that promote survival. Furthermore, they demonstrate autocrine production of APRIL and IL-10, which contributed to their prolonged in vitro survival. Our work provides insight into the mechanisms of generation, expansion, maturation and survival of SLE ASC.

Suggested Citation

  • Weirong Chen & So-Hee Hong & Scott A. Jenks & Fabliha A. Anam & Christopher M. Tipton & Matthew C. Woodruff & Jennifer R. Hom & Kevin S. Cashman & Caterina Elisa Faliti & Xiaoqian Wang & Shuya Kyu & C, 2024. "Distinct transcriptomes and autocrine cytokines underpin maturation and survival of antibody-secreting cells in systemic lupus erythematosus," Nature Communications, Nature, vol. 15(1), pages 1-17, December.
    • Handle: RePEc:nat:natcom:v:15:y:2024:i:1:d:10.1038_s41467-024-46053-w
    DOI: 10.1038/s41467-024-46053-w
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    References listed on IDEAS

    as
    1. Doan C. Nguyen & Swetha Garimalla & Haopeng Xiao & Shuya Kyu & Igor Albizua & Jacques Galipeau & Kuang-Yueh Chiang & Edmund K. Waller & Ronghu Wu & Greg Gibson & James Roberson & Frances E. Lund & Tro, 2018. "Factors of the bone marrow microniche that support human plasma cell survival and immunoglobulin secretion," Nature Communications, Nature, vol. 9(1), pages 1-12, December.
    2. Grant J. Brown & Pablo F. Cañete & Hao Wang & Arti Medhavy & Josiah Bones & Jonathan A. Roco & Yuke He & Yuting Qin & Jean Cappello & Julia I. Ellyard & Katharine Bassett & Qian Shen & Gaetan Burgio &, 2022. "TLR7 gain-of-function genetic variation causes human lupus," Nature, Nature, vol. 605(7909), pages 349-356, May.
    3. Matthew C. Woodruff & Richard P. Ramonell & Natalie S. Haddad & Fabliha A. Anam & Mark E. Rudolph & Tiffany A. Walker & Alexander D. Truong & Adviteeya N. Dixit & Jenny E. Han & Monica Cabrera-Mora & , 2022. "Dysregulated naive B cells and de novo autoreactivity in severe COVID-19," Nature, Nature, vol. 611(7934), pages 139-147, November.
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