Frascoli Michela, Jeanty Cerine, Fleck Shannon, Moradi Patriss W, Keating Sheila, Mattis Aras N, Tang Qizhi, MacKenzie Tippi C
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;
J Immunol. 2016 Jun 15;196(12):4957-66. doi: 10.4049/jimmunol.1502587. Epub 2016 May 13.
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.
孕期胎儿免疫系统的发育是一个精心编排的过程,对胎儿和新生儿健康具有重要影响,但影响免疫激活的产前因素却知之甚少。我们推测慢性胎儿炎症可能导致胎儿免疫系统发育的改变。为验证这一假设,我们研究了患有腹裂的新生儿,腹裂是一种先天性腹壁缺陷,会导致胎儿肠道暴露于羊水中,进而引发肠道炎症。我们发现,与对照组相比,腹裂患者全身炎症细胞因子和趋化因子(如嗜酸性粒细胞趋化因子)水平较高,脐带血中CD4(+)和CD8(+)效应及记忆T细胞的激活也更早。此外,更多的T细胞和嗜酸性粒细胞浸润到发炎肠道的浆膜和黏膜中。利用腹裂小鼠模型,我们观察到嗜酸性粒细胞以及2型和3型固有淋巴细胞(ILC2和ILC3)数量增加,特别是在暴露于羊水的器官部分。鉴于ILC2产生的IL-5在调节嗜酸性粒细胞发育和存活中的作用,我们确定母体或胎儿给予抗IL-5中和抗体或针对ILC的耗竭性抗体,均可有效减少肠道嗜酸性粒细胞增多。因此,一种导致慢性炎症的先天性异常可改变循环和组织驻留胎儿免疫细胞的组成。鉴于这些患者产前和新生儿并发症的发生率较高,这种变化具有临床意义,可能成为胎儿治疗的靶点。