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Neuropilin-1 Expression on CD4 T Cells Is Atherogenic and Facilitates T Cell Migration to the Aorta in Atherosclerosis

Dalia E. Gaddis, Lindsey E. Padgett, Runpei Wu and Catherine C. Hedrick
J Immunol November 18, 2019, ji1900245; DOI: https://doi.org/10.4049/jimmunol.1900245
Dalia E. Gaddis
Division of Inflammation Biology, La Jolla Institute for Immunology, La Jolla, CA 92037
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  • ORCID record for Dalia E. Gaddis
Lindsey E. Padgett
Division of Inflammation Biology, La Jolla Institute for Immunology, La Jolla, CA 92037
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Runpei Wu
Division of Inflammation Biology, La Jolla Institute for Immunology, La Jolla, CA 92037
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Catherine C. Hedrick
Division of Inflammation Biology, La Jolla Institute for Immunology, La Jolla, CA 92037
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Key Points

  • Western diet feeding increases Nrp1 on Foxp3− CD4 T cells in ApoE−/− mice.

  • Nrp1+Foxp3− CD4 T cells are highly proliferative and atherogenic.

  • Nrp1+Foxp3− CD4 T cells preferentially migrate to the aorta and PaLN.

Abstract

Neuropilin 1 (Nrp1) is a type I transmembrane protein that plays important roles in axonal guidance, neuronal development, and angiogenesis. Nrp1 also helps migrate thymus-derived regulatory T cells to vascular endothelial growth factor (VEGF)-producing tumors. However, little is known about the role of Nrp1 on CD4 T cells in atherosclerosis. In ApoE−/− mice fed a Western diet for 15 wk, we found a 2-fold increase in Nrp1+Foxp3− CD4 T cells in their spleens, periaortic lymph nodes, and aortas, compared with chow-fed mice. Nrp1+Foxp3− CD4 T cells had higher proliferation potential, expressed higher levels of the memory marker CD44, and produced more IFN-γ when compared with Nrp1− CD4 T cells. Treatment of CD4 T cells with oxLDL increased Nrp1 expression. Furthermore, atherosclerosis-susceptible mice selectively deficient for Nrp1 expression on T cells developed less atherosclerosis than their Nrp1-sufficient counterparts. Mechanistically, we found that CD4 T cells that express Nrp1 have an increased capacity to migrate to the aorta and periaortic lymph nodes compared to Nrp1− T cells, suggesting that the expression of Nrp1 facilitates the recruitment of CD4 T cells into the aorta where they can be pathogenic. Thus, we have identified a novel role of Nrp1 on CD4 T cells in atherosclerosis. These results suggest that manipulation of Nrp1 expression on T cells can affect the outcome of atherosclerosis and lower disease incidence.

Footnotes

  • This work was supported by the American Heart Association (13POST16990031 to D.E.G. and 19POST34450020 to L.E.P.), the American Diabetes Association (7-12-MN-13 to D.E.G. and C.C.H.), and the National Institutes of Health (P01 HL055798 and P01 HL136275 to C.C.H., R01 HL112276 to C.C.H., T32 AI125279-01 Training in Immunological Mechanisms Training Grant to L.E.P., and S10 RR027366-01A1 to the La Jolla Institute for Immunology Flow Cytometry Core Facility).

  • The online version of this article contains supplemental material.

  • Received February 27, 2019.
  • Accepted October 21, 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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Neuropilin-1 Expression on CD4 T Cells Is Atherogenic and Facilitates T Cell Migration to the Aorta in Atherosclerosis
Dalia E. Gaddis, Lindsey E. Padgett, Runpei Wu, Catherine C. Hedrick
The Journal of Immunology November 18, 2019, ji1900245; DOI: 10.4049/jimmunol.1900245

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Neuropilin-1 Expression on CD4 T Cells Is Atherogenic and Facilitates T Cell Migration to the Aorta in Atherosclerosis
Dalia E. Gaddis, Lindsey E. Padgett, Runpei Wu, Catherine C. Hedrick
The Journal of Immunology November 18, 2019, ji1900245; DOI: 10.4049/jimmunol.1900245
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Print ISSN 0022-1767        Online ISSN 1550-6606