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The Metabolic Cytokine Adiponectin Inhibits Inflammatory Lung Pathology in Invasive Aspergillosis

Nansalmaa Amarsaikhan, Angar Tsoggerel, Christopher Hug and Steven P. Templeton
J Immunol June 28, 2019, ji1900174; DOI: https://doi.org/10.4049/jimmunol.1900174
Nansalmaa Amarsaikhan
*Department of Microbiology and Immunology, Indiana University School of Medicine–Terre Haute, Terre Haute, IN 47809; and
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Angar Tsoggerel
*Department of Microbiology and Immunology, Indiana University School of Medicine–Terre Haute, Terre Haute, IN 47809; and
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Christopher Hug
†Boston Children’s Hospital, Boston, MA 02115
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Steven P. Templeton
*Department of Microbiology and Immunology, Indiana University School of Medicine–Terre Haute, Terre Haute, IN 47809; and
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Key Points

  • Adiponectin KO mice show increased pathology in a mouse model of IA.

  • KO mice show increased inflammatory and decreased anti-inflammatory phenotypes.

  • Increased lung inflammation in KO mice is independent of invasive fungal growth.

Abstract

Systemic immunity and metabolism are coregulated by soluble factors, including the insulin-regulating adipose tissue cytokine adiponectin. How these factors impact detrimental inflammatory responses during fungal infection remains unknown. In this study, we observed that mortality, fungal burden, and tissue histopathology were increased in adiponectin-deficient mice in a neutropenic model of invasive aspergillosis. Lung RNA sequencing, quantitative RT-PCR, and subsequent pathway analysis demonstrated activation of inflammatory cytokine pathways with upstream regulation by IL-1 and TNF in adiponectin-deficient mice with decreased/inhibited anti-inflammatory genes/pathways, suggesting broad cytokine-mediated pathology along with ineffective fungal clearance. Quantitative RT-PCR analysis confirmed increased transcription of IL-1a, IL-6, IL-12b, IL-17A/F, and TNF in adiponectin-deficient mice at early time points postinfection, with a specific increase in intracellular TNF in alveolar macrophages. Although eosinophil recruitment and activation were increased in adiponectin-deficient mice, mortality was delayed, but not decreased, in mice deficient in both adiponectin and eosinophils. Interestingly, neutrophil depletion was required for increased inflammation in adiponectin-deficient mice in response to swollen/fixed conidia, suggesting that immune suppression enhances detrimental inflammation, whereas invasive fungal growth is dispensable. Our results suggest that adiponectin inhibits excessive lung inflammation in invasive aspergillosis. Our study has therefore identified the adiponectin pathway as a potential source for novel therapeutics in immune-compromised patients with detrimental immunity to invasive fungal infection.

Footnotes

  • This work was supported in part by awards from the Indiana University School of Medicine and the Ralph W. and Grace M. Showalter Trust. The content is solely the responsibility of the authors and does not necessarily represent the official views of the Indiana University School of Medicine.

  • The RNA-sequencing data presented in this article have been submitted to Gene Expression Omnibus (https://www.ncbi.nlm.nih.gov/geo/) under accession number GSE130456.

  • The online version of this article contains supplemental material.

  • Received February 11, 2019.
  • Accepted June 12, 2019.
  • Copyright © 2019 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 206 (3)
The Journal of Immunology
Vol. 206, Issue 3
1 Feb 2021
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The Metabolic Cytokine Adiponectin Inhibits Inflammatory Lung Pathology in Invasive Aspergillosis
Nansalmaa Amarsaikhan, Angar Tsoggerel, Christopher Hug, Steven P. Templeton
The Journal of Immunology June 28, 2019, ji1900174; DOI: 10.4049/jimmunol.1900174

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The Metabolic Cytokine Adiponectin Inhibits Inflammatory Lung Pathology in Invasive Aspergillosis
Nansalmaa Amarsaikhan, Angar Tsoggerel, Christopher Hug, Steven P. Templeton
The Journal of Immunology June 28, 2019, ji1900174; DOI: 10.4049/jimmunol.1900174
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Print ISSN 0022-1767        Online ISSN 1550-6606