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

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, Chungwen Wei, Christopher D. Scharer, Tian Mi, Sakeenah Hicks, Louise Hartson, Doan C. Nguyen, Arezou Khosroshahi, Saeyun Lee, Youliang Wang, Regina Bugrovsky, Yusho Ishii, F. Eun-Hyung Lee () and Ignacio Sanz ()
Additional contact information
Weirong Chen: School of Medicine, Emory University
So-Hee Hong: School of Medicine, Emory 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

Nature Communications, 2024, vol. 15, issue 1, 1-17

Abstract: 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.

Date: 2024
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DOI: 10.1038/s41467-024-46053-w

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