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Opposing Roles of Dendritic Cell Subsets in Experimental GN

Sebastian Brähler, Bernd H. Zinselmeyer, Saravanan Raju, Maximilian Nitschke, Hani Suleiman, Brian T. Saunders, Michael W. Johnson, Alexander M.C. Böhner, Susanne F. Viehmann, Derek J. Theisen, Nicole M. Kretzer, Carlos G. Briseño, Konstantin Zaitsev, Olga Ornatsky, Qing Chang, Javier A. Carrero, Jeffrey B. Kopp, Maxim N. Artyomov, Christian Kurts, Kenneth M. Murphy, Jeffrey H. Miner and Andrey S. Shaw
JASN January 2018, 29 (1) 138-154; DOI: https://doi.org/10.1681/ASN.2017030270
Sebastian Brähler
1Department of Pathology and Immunology,
2Division of Nephrology, Department of Medicine, and
3Department II of Internal Medicine and
4Center for Molecular Medicine Cologne, University of Cologne, Cologne, Germany;
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Bernd H. Zinselmeyer
1Department of Pathology and Immunology,
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Saravanan Raju
1Department of Pathology and Immunology,
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Maximilian Nitschke
5Research Biology, Genentech, South San Francisco, California;
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Hani Suleiman
2Division of Nephrology, Department of Medicine, and
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Brian T. Saunders
1Department of Pathology and Immunology,
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Michael W. Johnson
1Department of Pathology and Immunology,
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Alexander M.C. Böhner
6Institute of Experimental Immunology, University Clinic of the Rheinische Friedrich Wilhelms Universität, Bonn, Germany;
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Susanne F. Viehmann
6Institute of Experimental Immunology, University Clinic of the Rheinische Friedrich Wilhelms Universität, Bonn, Germany;
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Derek J. Theisen
1Department of Pathology and Immunology,
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Nicole M. Kretzer
1Department of Pathology and Immunology,
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Carlos G. Briseño
1Department of Pathology and Immunology,
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Konstantin Zaitsev
7Computer Technologies Department, ITMO University, St. Petersburg, Russia;
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Olga Ornatsky
8Fluidigm Inc., Markham, Ontario, Canada; and
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Qing Chang
8Fluidigm Inc., Markham, Ontario, Canada; and
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Javier A. Carrero
1Department of Pathology and Immunology,
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Jeffrey B. Kopp
9Kidney Diseases Branch, National Institute of Diabetes and Digestive and Kidney Diseases, National Institutes of Health, Bethesda, Maryland
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Maxim N. Artyomov
1Department of Pathology and Immunology,
7Computer Technologies Department, ITMO University, St. Petersburg, Russia;
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Christian Kurts
6Institute of Experimental Immunology, University Clinic of the Rheinische Friedrich Wilhelms Universität, Bonn, Germany;
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Kenneth M. Murphy
1Department of Pathology and Immunology,
10Howard Hughes Medical Institute, Washington University School of Medicine, St. Louis, Missouri;
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Jeffrey H. Miner
2Division of Nephrology, Department of Medicine, and
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Andrey S. Shaw
5Research Biology, Genentech, South San Francisco, California;
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Abstract

Dendritic cells (DCs) are thought to form a dendritic network across barrier surfaces and throughout organs, including the kidney, to perform an important sentinel function. However, previous studies of DC function used markers, such as CD11c or CX3CR1, that are not unique to DCs. Here, we evaluated the role of DCs in renal inflammation using a CD11c reporter mouse line and two mouse lines with DC-specific reporters, Zbtb46-GFP and Snx22-GFP. Multiphoton microscopy of kidney sections confirmed that most of the dendritically shaped CD11c+ cells forming a network throughout the renal interstitium expressed macrophage-specific markers. In contrast, DCs marked by Zbtb46-GFP or Snx22-GFP were less abundant, concentrated around blood vessels, and round in shape. We confirmed this pattern of localization using imaging mass cytometry. Motility measurements showed that resident macrophages were sessile, whereas DCs were motile before and after inflammation. Although uninflamed glomeruli rarely contained DCs, injury with nephrotoxic antibodies resulted in accumulation of ZBTB46+ cells in the periglomerular region. ZBTB46 identifies all classic DCs, which can be categorized into two functional subsets that express either CD103 or CD11b. Depletion of ZBTB46+ cells attenuated the antibody-induced kidney injury, whereas deficiency of the CD103+ subset accelerated injury through a mechanism that involved increased neutrophil infiltration. RNA sequencing 7 days after nephrotoxic antibody injection showed that CD11b+ DCs expressed the neutrophil-attracting cytokine CXCL2, whereas CD103+ DCs expressed high levels of several anti-inflammatory genes. These results provide new insights into the distinct functions of the two major DC subsets in glomerular inflammation.

  • immunology
  • glomerulonephritis
  • glomerular disease
  • Copyright © 2018 by the American Society of Nephrology
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Journal of the American Society of Nephrology: 29 (1)
Journal of the American Society of Nephrology
Vol. 29, Issue 1
January 2018
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Opposing Roles of Dendritic Cell Subsets in Experimental GN
Sebastian Brähler, Bernd H. Zinselmeyer, Saravanan Raju, Maximilian Nitschke, Hani Suleiman, Brian T. Saunders, Michael W. Johnson, Alexander M.C. Böhner, Susanne F. Viehmann, Derek J. Theisen, Nicole M. Kretzer, Carlos G. Briseño, Konstantin Zaitsev, Olga Ornatsky, Qing Chang, Javier A. Carrero, Jeffrey B. Kopp, Maxim N. Artyomov, Christian Kurts, Kenneth M. Murphy, Jeffrey H. Miner, Andrey S. Shaw
JASN Jan 2018, 29 (1) 138-154; DOI: 10.1681/ASN.2017030270

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Opposing Roles of Dendritic Cell Subsets in Experimental GN
Sebastian Brähler, Bernd H. Zinselmeyer, Saravanan Raju, Maximilian Nitschke, Hani Suleiman, Brian T. Saunders, Michael W. Johnson, Alexander M.C. Böhner, Susanne F. Viehmann, Derek J. Theisen, Nicole M. Kretzer, Carlos G. Briseño, Konstantin Zaitsev, Olga Ornatsky, Qing Chang, Javier A. Carrero, Jeffrey B. Kopp, Maxim N. Artyomov, Christian Kurts, Kenneth M. Murphy, Jeffrey H. Miner, Andrey S. Shaw
JASN Jan 2018, 29 (1) 138-154; DOI: 10.1681/ASN.2017030270
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  • glomerulonephritis
  • glomerular disease

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