School of Arts & Sciences, Health Psychology Program, Massachusetts College of Pharmacy and Health Sciences, Boston, MA, 02115, USA.
Department of Psychiatry, University of Pittsburgh, 450 Technology Drive, Pittsburgh, PA, 15219, USA.
Neuropsychopharmacology. 2024 Jun;49(7):1078-1090. doi: 10.1038/s41386-023-01771-5. Epub 2023 Nov 25.
Maternal immune activation (MIA) puts offspring at greater risk for neurodevelopmental disorders associated with impaired social behavior. While it is known that immune signaling through maternal, placental, and fetal compartments contributes to these phenotypical changes, it is unknown to what extent the stress response to illness is involved and how it can be harnessed for potential interventions. To this end, on gestational day 15, pregnant rat dams were administered the bacterial mimetic lipopolysaccharide (LPS; to induce MIA) alongside metyrapone, a clinically available 11β-hydroxylase (11βHSD) inhibitor used to treat hypercortisolism in pregnant, lactating, and neonatal populations. Maternal, placental, and fetal brain levels of corticosterone and placental 11βHSD enzymes type 1 and 2 were measured 3-hrs post treatment. Offspring social behaviors were evaluated across critical phases of development. MIA was associated with increased maternal, placental, and fetal brain corticosterone concentrations that were diminished with metyrapone exposure. Metyrapone protected against reductions in placental 11βHSD2 in males only, suggesting that less corticosterone was inactivated in female placentas. Behaviorally, metyrapone-exposure attenuated MIA-induced social disruptions in juvenile, adolescent, and adult males, while females were unaffected or performed worse. Metyrapone-exposure reversed MIA-induced transcriptional changes in monoamine-, glutamate-, and GABA-related genes in adult male ventral hippocampus, but not in females. Taken together, these findings illustrate that MIA-induced HPA responses act alongside the immune system to produce behavioral deficits. As a clinically available drug, the sex-specific benefits and constraints of metyrapone should be investigated further as a potential means of reducing neurodevelopmental risks due to gestational MIA.
母体免疫激活(MIA)使后代患与社交行为受损相关的神经发育障碍的风险增加。虽然已知母体、胎盘和胎儿部位的免疫信号传递导致这些表型变化,但尚不清楚疾病应激反应在多大程度上涉及其中,以及如何利用它进行潜在干预。为此,在妊娠第 15 天,给怀孕的大鼠母体注射细菌模拟物脂多糖(LPS;诱导 MIA),同时注射米替拉酮,一种临床上可用的 11β-羟化酶(11βHSD)抑制剂,用于治疗孕妇、哺乳期和新生儿人群的皮质醇过多症。在治疗后 3 小时测量母本、胎盘和胎脑皮质酮水平以及胎盘 11βHSD 酶 1 型和 2 型。在关键发育阶段评估后代的社交行为。MIA 与母体、胎盘和胎脑皮质酮浓度增加有关,米替拉酮暴露可降低皮质酮浓度。米替拉酮可防止雄性胎盘 11βHSD2 减少,表明雌性胎盘的皮质酮失活较少。行为上,米替拉酮暴露可减轻 MIA 诱导的幼鼠、青少年和成年雄性的社交障碍,但对雌性没有影响或表现更差。米替拉酮暴露可逆转 MIA 诱导的成年雄性腹侧海马中与单胺、谷氨酸和 GABA 相关基因的转录变化,但对雌性没有影响。综上所述,这些发现表明,MIA 诱导的 HPA 反应与免疫系统一起产生行为缺陷。作为一种临床可用的药物,米替拉酮的性别特异性益处和限制应进一步研究,作为降低因妊娠期 MIA 而导致的神经发育风险的潜在手段。