Hollingsworth John W, Maruoka Shuichiro, Boon Kathy, Garantziotis Stavros, Li Zhuowei, Tomfohr John, Bailey Nathaniel, Potts Erin N, Whitehead Gregory, Brass David M, Schwartz David A
Division of Pulmonary, Allergy and Critical Care Medicine, Department of Medicine, Duke University Medical Center, Durham, North Carolina 27710, USA.
J Clin Invest. 2008 Oct;118(10):3462-9. doi: 10.1172/JCI34378.
Asthma is a complex heritable disease that is increasing in prevalence and severity, particularly in developed countries such as the United States, where 11% of the population is affected. The contribution of environmental and genetic factors to this growing epidemic is currently not well understood. We developed the hypothesis, based on previous literature, that changes in DNA methylation resulting in aberrant gene transcription may enhance the risk of developing allergic airway disease. Our findings indicate that in mice, a maternal diet supplemented with methyl donors enhanced the severity of allergic airway disease that was inherited transgenerationally. Using a genomic approach, we discovered 82 gene-associated loci that were differentially methylated after in utero supplementation with a methyl-rich diet. These methylation changes were associated with decreased transcriptional activity and increased disease severity. Runt-related transcription factor 3 (Runx3), a gene known to negatively regulate allergic airway disease, was found to be excessively methylated, and Runx3 mRNA and protein levels were suppressed in progeny exposed in utero to a high-methylation diet. Moreover, treatment with a demethylating agent increased Runx3 gene transcription, further supporting our claim that a methyl-rich diet can affect methylation status and consequent transcriptional regulation. Our findings indicate that dietary factors can modify the heritable risk of allergic airway disease through epigenetic mechanisms during a vulnerable period of fetal development in mice.
哮喘是一种复杂的遗传性疾病,其患病率和严重程度正在上升,尤其是在美国等发达国家,该国11%的人口受其影响。目前,环境和遗传因素对这一日益严重的疾病流行的作用尚不清楚。基于之前的文献,我们提出了一个假设,即DNA甲基化的改变导致异常的基因转录可能会增加患过敏性气道疾病的风险。我们的研究结果表明,在小鼠中,母体饮食中添加甲基供体可加重遗传性过敏性气道疾病的严重程度。通过基因组学方法,我们发现了82个与基因相关的位点,在子宫内补充富含甲基的饮食后,这些位点的甲基化存在差异。这些甲基化变化与转录活性降低和疾病严重程度增加有关。已知对过敏性气道疾病起负调控作用的基因—— runt相关转录因子3(Runx3)被发现甲基化过度,在子宫内暴露于高甲基化饮食的后代中,Runx3 mRNA和蛋白质水平受到抑制。此外,用去甲基化剂处理可增加Runx3基因转录,进一步支持了我们的观点,即富含甲基的饮食可影响甲基化状态及随之而来的转录调控。我们的研究结果表明,在小鼠胎儿发育的脆弱期,饮食因素可通过表观遗传机制改变过敏性气道疾病的遗传风险。