Department of Biomedical Sciences, Colorado State University, Fort Collins, Colorado, USA.
Department of Psychiatry, Mass General Hospital, Harvard Medical School, Boston, Massachusetts, USA.
J Neuroendocrinol. 2024 Aug;36(8):e13417. doi: 10.1111/jne.13417. Epub 2024 Jun 1.
Infections during pregnancy are associated with increased risk for adult neuropsychiatric disease, such as major depressive disorder, schizophrenia, and autism spectrum disorder. In mouse models of maternal immune activation (MIA), different toll-like receptors (TLRs) are stimulated to initiate inflammatory responses in mother and fetus. The goal of this study was to determine sex-dependent aspects of MIA using a TLR7/8 agonist, Resiquimod (RQ), on neurodevelopment. RQ was administered to timed-pregnant mice on embryonic day (E) 12.5. At E15, maternal/fetal plasma cytokines were measured by enzyme-linked immunosorbent assay (ELISA). Maternal cytokines interleukin (IL)-6 and IL-10 were higher while tumor necrosis factor (TNF)-α and IL-17 were lower in pregnant dams exposed to RQ. Fetal cytokines (E15) were altered at the same timepoint with fetal plasma IL-6 and IL-17 greater after RQ compared to vehicle, while IL-10 and TNF-α were higher in male fetuses but not female. Other timed-pregnant dams were allowed to give birth. MIA with RQ did not alter the female to male ratio of offspring born per litter. Body weights were reduced significantly in both sexes at birth, and over the next 5 weeks. Offspring from RQ-injected mothers opened their eyes 5 days later than controls. Similarly, female offspring from RQ-injected mothers exhibited pubertal delay based on vaginal opening 2-3 days later than control females. On the behavioral side, juvenile and adult male and female MIA offspring exhibited less social-like behavior in a social interaction test. Anhedonia-like behavior was greater in MIA adult female mice. This study provides support for sex-dependent influences of fetal antecedents for altered brain development and behavioral outputs that could be indicative of increased susceptibility for adult disorders through immune mechanisms. Future studies are needed to determine neural cellular and molecular mechanisms for such programming effects.
孕期感染与成人神经精神疾病的风险增加有关,例如重度抑郁症、精神分裂症和自闭症谱系障碍。在母体免疫激活 (MIA) 的小鼠模型中,不同的 toll 样受体 (TLR) 被刺激以引发母体和胎儿的炎症反应。本研究的目的是使用 TLR7/8 激动剂瑞喹莫德 (RQ) 确定 MIA 的性别依赖性方面对神经发育的影响。RQ 在胚胎期 (E) 12.5 时给予定时怀孕的小鼠。在 E15 时,通过酶联免疫吸附试验 (ELISA) 测量母胎血浆细胞因子。暴露于 RQ 的孕鼠母体/胎儿白细胞介素 (IL)-6 和 IL-10 更高,而肿瘤坏死因子 (TNF)-α 和 IL-17 更低。同时改变了胎儿细胞因子(E15),与载体相比,RQ 后胎儿血浆 IL-6 和 IL-17 更高,而 IL-10 和 TNF-α 在雄性胎儿中更高,但在雌性胎儿中则不然。其他定时怀孕的母鼠允许分娩。MIA 用 RQ 并没有改变每窝出生的雌雄比例。出生时,雌雄后代的体重均明显减轻,并且在接下来的 5 周内持续减轻。来自 RQ 注射母亲的后代比对照晚 5 天睁开眼睛。同样,来自 RQ 注射母亲的雌性后代的青春期延迟比对照雌性晚 2-3 天。在行为方面,幼年和成年雄性和雌性 MIA 后代在社交互动测试中表现出较少的社交行为。MIA 成年雌性小鼠的快感缺失样行为更多。这项研究为改变大脑发育和行为结果的胎儿前因的性别依赖性影响提供了支持,这些影响可能通过免疫机制表明成年疾病的易感性增加。需要进一步的研究来确定这种编程效应的神经细胞和分子机制。