Appleton Allison A, Lester Barry M, Armstrong David A, Lesseur Corina, Marsit Carmen J
Department of Epidemiology and Biostatistics, University at Albany School of Public Health, State University of New York, Rensselaer, NY, USA.
Department of Psychiatry and Department of Pediatrics, Brown Center for the Study of Children at Risk, Alpert Medical School of Brown University and Women and Infants Hospital, Providence, RI, USA.
Psychoneuroendocrinology. 2015 Feb;52:32-42. doi: 10.1016/j.psyneuen.2014.11.004. Epub 2014 Nov 10.
Infant neurobehavior, a potential sentinel of future mental and behavioral morbidity characterized in part by reflex symmetry, excitability and habituation to stimuli, is influenced by aspects of the intrauterine environment partially through epigenetic alterations of genes involved in the stress response. DNA methylation of two related cortisol response genes, the glucocorticoid receptor (NR3C1), a nuclear receptor to which cortisol binds, and 11-beta hydroxysteroid dehydrogenase (HSD11B2), the enzyme responsible for conversion of cortisol into inactive cortisone, independently associate with infant neurobehavior. Although these factors are part of a common cortisol regulation pathway, the combined effect of DNA methylation of these factors on infant neurobehavior has not been characterized. Therefore, we conducted an examination of the joint contribution of NR3C1 and HSD11B2 DNA methylation on infant neurobehavior. Among 372 healthy term newborns, we tested the interaction between placental NR3C1 and HSD11B2 DNA methylation in association with neurobehavior as assessed with the validated NICU Network Neurobehavioral Scales. Controlling for confounders, interactions between DNA methylation of these genes were detected for distinct domains of neurobehavior (habituation, excitability, asymmetrical reflexes). Moreover, different patterns of DNA methylation across the cortisol regulation pathway associated with different neurobehavioral phenotypes. Those with low NR3C1 methylation but high HSD11B2 methylation had lower excitability scores; those with high NR3C1 methylation but low HSD11B2 methylation had more asymmetrical reflexes; those with high DNA methylation across the entire pathway had higher habituation scores. These results suggest that epigenetic alterations across the cortisol regulation pathway may contribute to different neurobehavioral phenotypes, likely though varying degrees of glucocorticoid exposure during gestation. While the postnatal environment may continue to affect neurobehavioral risk, this study provides novel insights into the molecular basis for fetal origins of mental conditions.
婴儿神经行为是未来心理和行为疾病的一个潜在预警指标,部分特征表现为反射对称性、兴奋性和对刺激的习惯化,它受到子宫内环境因素的影响,部分是通过参与应激反应的基因的表观遗传改变实现的。两个相关的皮质醇反应基因的DNA甲基化,即糖皮质激素受体(NR3C1)(皮质醇与之结合的核受体)和11-β-羟基类固醇脱氢酶(HSD11B2)(负责将皮质醇转化为无活性可的松的酶),分别与婴儿神经行为相关。尽管这些因素是常见皮质醇调节途径的一部分,但这些因素的DNA甲基化对婴儿神经行为的综合影响尚未得到明确。因此,我们对NR3C1和HSD11B2的DNA甲基化对婴儿神经行为的联合作用进行了研究。在372名健康足月新生儿中,我们测试了胎盘NR3C1和HSD11B2的DNA甲基化与神经行为之间的相互作用,神经行为是通过经过验证的新生儿重症监护病房网络神经行为量表进行评估的。在控制混杂因素后,检测到这些基因的DNA甲基化之间在神经行为的不同领域(习惯化、兴奋性、不对称反射)存在相互作用。此外,皮质醇调节途径中不同的DNA甲基化模式与不同的神经行为表型相关。NR3C1甲基化低但HSD11B2甲基化高的婴儿兴奋性得分较低;NR3C1甲基化高但HSD11B2甲基化低的婴儿不对称反射较多;整个途径中DNA甲基化高的婴儿习惯化得分较高。这些结果表明,皮质醇调节途径中的表观遗传改变可能导致不同的神经行为表型,可能是通过孕期不同程度的糖皮质激素暴露实现的。虽然出生后的环境可能继续影响神经行为风险,但这项研究为精神疾病的胎儿起源的分子基础提供了新的见解。