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Heightened Immune Activation in Fetuses with Gastroschisis May Be Blocked by Targeting IL-5

Michela Frascoli, Cerine Jeanty, Shannon Fleck, Patriss W. Moradi, Sheila Keating, Aras N. Mattis, Qizhi Tang and Tippi C. MacKenzie
J Immunol May 13, 2016, 1502587; DOI: https://doi.org/10.4049/jimmunol.1502587
Michela Frascoli
*Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California San Francisco, San Francisco, CA 94143;
†Department of Surgery, University of California San Francisco, San Francisco, CA 94143;
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Cerine Jeanty
*Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California San Francisco, San Francisco, CA 94143;
†Department of Surgery, University of California San Francisco, San Francisco, CA 94143;
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Shannon Fleck
‡Department of Pediatrics, University of California San Francisco, San Francisco, CA 94143;
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Patriss W. Moradi
*Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California San Francisco, San Francisco, CA 94143;
†Department of Surgery, University of California San Francisco, San Francisco, CA 94143;
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Sheila Keating
§Blood Systems Research Institute, San Francisco, CA 94118; and
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Aras N. Mattis
*Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California San Francisco, San Francisco, CA 94143;
¶Department of Pathology, University of California San Francisco, San Francisco, CA 94143
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Qizhi Tang
†Department of Surgery, University of California San Francisco, San Francisco, CA 94143;
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Tippi C. MacKenzie
*Eli and Edythe Broad Center of Regeneration Medicine and Stem Cell Research, University of California San Francisco, San Francisco, CA 94143;
†Department of Surgery, University of California San Francisco, San Francisco, CA 94143;
‡Department of Pediatrics, University of California San Francisco, San Francisco, CA 94143;
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Abstract

The development of the fetal immune system during pregnancy is a well-orchestrated process with important consequences for fetal and neonatal health, but prenatal factors that affect immune activation are poorly understood. We hypothesized that chronic fetal inflammation may lead to alterations in development of the fetal immune system. To test this hypothesis, we examined neonates with gastroschisis, a congenital abdominal wall defect that leads to exposure of the fetal intestines to amniotic fluid, with resultant intestinal inflammation. We determined that patients with gastroschisis show high systemic levels of inflammatory cytokines and chemokines such as eotaxin, as well as earlier activation of CD4+ and CD8+ effector and memory T cells in the cord blood compared with controls. Additionally, increased numbers of T cells and eosinophils infiltrate the serosa and mucosa of the inflamed intestines. Using a mouse model of gastroschisis, we observed higher numbers of eosinophils and both type 2 and type 3 innate lymphoid cells (ILC2 and ILC3), specifically in the portion of organs exposed to the amniotic fluid. Given the role of IL-5 produced by ILC2 in regulating eosinophil development and survival, we determined that maternal or fetal administration of the anti–IL-5 neutralizing Ab, or a depleting Ab against ILCs, can both effectively reduce intestinal eosinophilia. Thus, a congenital anomaly causing chronic inflammation can alter the composition of circulating and tissue-resident fetal immune cells. Given the high rate of prenatal and neonatal complications in these patients, such changes have clinical significance and might become targets for fetal therapy.

Footnotes

  • This work was supported by grants from the March of Dimes (to T.C.M.), National Institutes of Health/National Institute of Allergy and Infectious Diseases Grant K08AI085042 (to T.C.M.), and by an American College of Surgeons resident research scholarship (to C.J.).

  • The online version of this article contains supplemental material.

  • Received December 15, 2015.
  • Accepted April 18, 2016.
  • Copyright © 2016 by The American Association of Immunologists, Inc.
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The Journal of Immunology: 206 (5)
The Journal of Immunology
Vol. 206, Issue 5
1 Mar 2021
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Heightened Immune Activation in Fetuses with Gastroschisis May Be Blocked by Targeting IL-5
Michela Frascoli, Cerine Jeanty, Shannon Fleck, Patriss W. Moradi, Sheila Keating, Aras N. Mattis, Qizhi Tang, Tippi C. MacKenzie
The Journal of Immunology May 13, 2016, 1502587; DOI: 10.4049/jimmunol.1502587

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Heightened Immune Activation in Fetuses with Gastroschisis May Be Blocked by Targeting IL-5
Michela Frascoli, Cerine Jeanty, Shannon Fleck, Patriss W. Moradi, Sheila Keating, Aras N. Mattis, Qizhi Tang, Tippi C. MacKenzie
The Journal of Immunology May 13, 2016, 1502587; DOI: 10.4049/jimmunol.1502587
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Print ISSN 0022-1767        Online ISSN 1550-6606