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Semaphorin 3E Regulates the Response of Macrophages to Lipopolysaccharide-Induced Systemic Inflammation

Ashfaque Mohammed, Ifeoma Okwor, Lianyu Shan, Chukwunonso Onyilagha, Jude E. Uzonna and Abdelilah S. Gounni
J Immunol November 27, 2019, ji1801514; DOI: https://doi.org/10.4049/jimmunol.1801514
Ashfaque Mohammed
Department of Immunology, Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Manitoba R3E 0T5, Canada
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Ifeoma Okwor
Department of Immunology, Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Manitoba R3E 0T5, Canada
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Lianyu Shan
Department of Immunology, Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Manitoba R3E 0T5, Canada
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Chukwunonso Onyilagha
Department of Immunology, Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Manitoba R3E 0T5, Canada
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Jude E. Uzonna
Department of Immunology, Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Manitoba R3E 0T5, Canada
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Abdelilah S. Gounni
Department of Immunology, Max Rady College of Medicine, Rady Faculty of Health Sciences, University of Manitoba, Winnipeg, Manitoba R3E 0T5, Canada
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Key Points

  • Mice deficient in Sema3E are more resistant to LPS-induced acute inflammation.

  • Sema3E regulates macrophage phenotype and function in response to LPS.

Abstract

Semaphorin 3E (Sema3E) is a secreted protein that was initially discovered as a neuronal guidance cue. Recent evidence showed that Sema3E plays an essential role in regulating the activities of various immune cells. However, the exact role of Sema3E in macrophage function, particularly during inflammation, is not fully understood. We studied the impact of Sema3E gene deletion on macrophage function during the LPS-induced acute inflammatory response. We found that Sema3E-deficient (Sema3e−/−) mice were better protected from LPS-induced acute inflammation as exemplified by their superior clinical score and effective temperature control compared with their wild-type littermates. This superior control of inflammatory response in Sema3e−/− mice was associated with significantly lower phosphorylation of ERK1/2, AKT, STAT3, and NF-κB, and a concomitant reduction in inducible NO synthase expression and production of TNF and IL-6 compared with their Sema3e+/+ littermates. Sema3e−/− mice also contained significantly higher numbers of activated macrophages compared with their Sema3e+/+ littermates at both baselines and after LPS challenge. In vivo–specific deletion of the Sema3E high-affinity receptor, plexinD1, on macrophages led to the improvement in clinical disease following exposure to a lethal dose of LPS. Collectively, our data show that Sema3E plays an essential role in dampening the early inflammatory response to LPS by regulating macrophage function, suggesting an essential role of this pathway in macrophage inflammatory response.

Footnotes

  • ↵1 A.M. and I.O. are cofirst authors.

  • This work was supported by the Manitoba Research Chair (to A.S.G.). A.M. was supported by a Children's Hospital Research Institute of Manitoba studentship. I.O. was supported by the International American Association of Immunologists Fellowship.

  • The online version of this article contains supplemental material.

  • Received December 21, 2018.
  • Accepted October 28, 2019.
  • Copyright © 2019 by The American Association of Immunologists, Inc.

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The Journal of Immunology: 203 (12)
The Journal of Immunology
Vol. 203, Issue 12
15 Dec 2019
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Semaphorin 3E Regulates the Response of Macrophages to Lipopolysaccharide-Induced Systemic Inflammation
Ashfaque Mohammed, Ifeoma Okwor, Lianyu Shan, Chukwunonso Onyilagha, Jude E. Uzonna, Abdelilah S. Gounni
The Journal of Immunology November 27, 2019, ji1801514; DOI: 10.4049/jimmunol.1801514

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Semaphorin 3E Regulates the Response of Macrophages to Lipopolysaccharide-Induced Systemic Inflammation
Ashfaque Mohammed, Ifeoma Okwor, Lianyu Shan, Chukwunonso Onyilagha, Jude E. Uzonna, Abdelilah S. Gounni
The Journal of Immunology November 27, 2019, ji1801514; DOI: 10.4049/jimmunol.1801514
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Print ISSN 0022-1767        Online ISSN 1550-6606