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Research ArticleSystemic Lupus Erythematosus

High Systemic Type I Interferon Activity Is Associated With Active Class III/IV Lupus Nephritis

Taro Iwamoto, Jessica M. Dorschner, Shanmugapriya Selvaraj, Valeria Mezzano, Mark A. Jensen, Danielle Vsetecka, Shreyasee Amin, Ashima Makol, Thomas Osborn, Kevin Moder, Vaidehi R. Chowdhary, Peter Izmirly, H. Michael Belmont, Robert M. Clancy, Jill P. Buyon, Ming Wu, Cynthia A. Loomis and Timothy B. Niewold
The Journal of Rheumatology April 2022, 49 (4) 388-397; DOI: https://doi.org/10.3899/jrheum.210391
Taro Iwamoto
1T. Iwamoto, MD, PhD, Colton Center for Autoimmunity, New York University, New York, New York, USA, and Allergy and Clinical Immunology, Chiba University, Japan;
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  • ORCID record for Taro Iwamoto
Jessica M. Dorschner
2J.M. Dorschner, BS, D. Vsetecka, MPH, S. Amin, MD, A. Makol, MD, T. Osborn, MD, K. Moder, MD, V.R. Chowdhary, MD, Mayo Clinic College of Medicine, Rochester, Minnesota, USA;
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Shanmugapriya Selvaraj
3S. Selvaraj, MS, V. Mezzano, MD, PhD, M. Wu, MD, C.A. Loomis, MD, PhD, Department of Pathology, New York University, New York, New York, USA;
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Valeria Mezzano
3S. Selvaraj, MS, V. Mezzano, MD, PhD, M. Wu, MD, C.A. Loomis, MD, PhD, Department of Pathology, New York University, New York, New York, USA;
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Mark A. Jensen
4M.A. Jensen, PhD, R.M. Clancy, PhD, J.P. Buyon, MD, T.B. Niewold, MD, Colton Center for Autoimmunity, New York University, New York, New York, USA;
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Danielle Vsetecka
2J.M. Dorschner, BS, D. Vsetecka, MPH, S. Amin, MD, A. Makol, MD, T. Osborn, MD, K. Moder, MD, V.R. Chowdhary, MD, Mayo Clinic College of Medicine, Rochester, Minnesota, USA;
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Shreyasee Amin
2J.M. Dorschner, BS, D. Vsetecka, MPH, S. Amin, MD, A. Makol, MD, T. Osborn, MD, K. Moder, MD, V.R. Chowdhary, MD, Mayo Clinic College of Medicine, Rochester, Minnesota, USA;
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Ashima Makol
2J.M. Dorschner, BS, D. Vsetecka, MPH, S. Amin, MD, A. Makol, MD, T. Osborn, MD, K. Moder, MD, V.R. Chowdhary, MD, Mayo Clinic College of Medicine, Rochester, Minnesota, USA;
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Thomas Osborn
2J.M. Dorschner, BS, D. Vsetecka, MPH, S. Amin, MD, A. Makol, MD, T. Osborn, MD, K. Moder, MD, V.R. Chowdhary, MD, Mayo Clinic College of Medicine, Rochester, Minnesota, USA;
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Kevin Moder
2J.M. Dorschner, BS, D. Vsetecka, MPH, S. Amin, MD, A. Makol, MD, T. Osborn, MD, K. Moder, MD, V.R. Chowdhary, MD, Mayo Clinic College of Medicine, Rochester, Minnesota, USA;
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Vaidehi R. Chowdhary
2J.M. Dorschner, BS, D. Vsetecka, MPH, S. Amin, MD, A. Makol, MD, T. Osborn, MD, K. Moder, MD, V.R. Chowdhary, MD, Mayo Clinic College of Medicine, Rochester, Minnesota, USA;
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Peter Izmirly
5P. Izmirly, MD, H.M. Belmont, MD, Division of Rheumatology, New York University, New York, New York, USA.
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H. Michael Belmont
5P. Izmirly, MD, H.M. Belmont, MD, Division of Rheumatology, New York University, New York, New York, USA.
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Robert M. Clancy
4M.A. Jensen, PhD, R.M. Clancy, PhD, J.P. Buyon, MD, T.B. Niewold, MD, Colton Center for Autoimmunity, New York University, New York, New York, USA;
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Jill P. Buyon
4M.A. Jensen, PhD, R.M. Clancy, PhD, J.P. Buyon, MD, T.B. Niewold, MD, Colton Center for Autoimmunity, New York University, New York, New York, USA;
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Ming Wu
3S. Selvaraj, MS, V. Mezzano, MD, PhD, M. Wu, MD, C.A. Loomis, MD, PhD, Department of Pathology, New York University, New York, New York, USA;
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Cynthia A. Loomis
3S. Selvaraj, MS, V. Mezzano, MD, PhD, M. Wu, MD, C.A. Loomis, MD, PhD, Department of Pathology, New York University, New York, New York, USA;
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Timothy B. Niewold
4M.A. Jensen, PhD, R.M. Clancy, PhD, J.P. Buyon, MD, T.B. Niewold, MD, Colton Center for Autoimmunity, New York University, New York, New York, USA;
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  • For correspondence: Timothy.Niewold@nyulangone.org
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Abstract

Objective Previous studies suggest a link between high serum type I interferon (IFN) and lupus nephritis (LN). We determined whether serum IFN activity is associated with subtypes of LN and studied renal tissues and cells to understand the effect of IFN in LN.

Methods Two hundred and twenty-one patients with systemic lupus erythematosus were studied. Serum IFN activity was measured by WISH bioassay. mRNA in situ hybridization was used in renal tissue to measure expression of the representative IFN-induced gene, IFN-induced protein with tetratricopeptide repeats-1 (IFIT1), and the plasmacytoid dendritic cell (pDC) marker gene C-type lectin domain family-4 member C (CLEC4C). Podocyte cell line gene expression was measured by real-time PCR.

Results Class III/IV LN prevalence was significantly increased in patients with high serum IFN compared with those with low IFN (odds ratio 5.40, P = 0.009). In multivariate regression models, type I IFN was a stronger predictor of class III/IV LN than complement C3 or anti-dsDNA antibody, and could account for the association of these variables with LN. IFIT1 expression was increased in all classes of LN, but most in the glomerular areas of active class III/IV LN kidneys. IFIT1 expression was not closely colocalized with pDCs. IFN directly activated podocyte cell lines to induce chemokines and proapoptotic molecules.

Conclusion Systemic high IFN is involved in the pathogenesis of severe LN. We did not find colocalization of pDCs with IFN signature in renal tissue, and instead observed the greatest intensity of the IFN signature in glomerular areas, which could suggest a blood source of IFN.

Key Indexing Terms:
  • interferon signature gene
  • lupus nephritis
  • podocyte injury type I interferon
  • Accepted for publication November 3, 2021.
  • Copyright © 2022 by the Journal of Rheumatology
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The Journal of Rheumatology
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1 Apr 2022
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High Systemic Type I Interferon Activity Is Associated With Active Class III/IV Lupus Nephritis
Taro Iwamoto, Jessica M. Dorschner, Shanmugapriya Selvaraj, Valeria Mezzano, Mark A. Jensen, Danielle Vsetecka, Shreyasee Amin, Ashima Makol, Thomas Osborn, Kevin Moder, Vaidehi R. Chowdhary, Peter Izmirly, H. Michael Belmont, Robert M. Clancy, Jill P. Buyon, Ming Wu, Cynthia A. Loomis, Timothy B. Niewold
The Journal of Rheumatology Apr 2022, 49 (4) 388-397; DOI: 10.3899/jrheum.210391

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High Systemic Type I Interferon Activity Is Associated With Active Class III/IV Lupus Nephritis
Taro Iwamoto, Jessica M. Dorschner, Shanmugapriya Selvaraj, Valeria Mezzano, Mark A. Jensen, Danielle Vsetecka, Shreyasee Amin, Ashima Makol, Thomas Osborn, Kevin Moder, Vaidehi R. Chowdhary, Peter Izmirly, H. Michael Belmont, Robert M. Clancy, Jill P. Buyon, Ming Wu, Cynthia A. Loomis, Timothy B. Niewold
The Journal of Rheumatology Apr 2022, 49 (4) 388-397; DOI: 10.3899/jrheum.210391
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Keywords

interferon signature gene
LUPUS NEPHRITIS
podocyte injury type I interferon

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Keywords

  • interferon signature gene
  • lupus nephritis
  • podocyte injury type I interferon

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