Thomas Lord Department of Mechanical Engineering and Materials Science, Duke University, Durham, NC 27708.
Division of Rheumatology and Immunology, Duke University Medical Center, and Medical Research Service, Durham VA Medical Center, Durham, NC 27705.
Proc Natl Acad Sci U S A. 2024 Mar 12;121(11):e2319634121. doi: 10.1073/pnas.2319634121. Epub 2024 Mar 5.
Autoimmune and inflammatory diseases are highly complex, limiting treatment and the development of new therapies. Recent work has shown that cell-free DNA bound to biological microparticles is linked to systemic lupus erythematosus, a prototypic autoimmune disease. However, the heterogeneity and technical challenges associated with the study of biological particles have hindered a mechanistic understanding of their role. Our goal was to develop a well-controlled DNA-particle model system to understand how DNA-particle complexes affect cells. We first characterized the adsorption of DNA on the surface of polystyrene nanoparticles (200 nm and 2 µm) using transmission electron microscopy, dynamic light scattering, and colorimetric DNA concentration assays. We found that DNA adsorbed on the surface of nanoparticles was resistant to degradation by DNase 1. Macrophage cells incubated with the DNA-nanoparticle complexes had increased production of pro-inflammatory cytokines tumor necrosis factor alpha (TNF-α) and interleukin 6 (IL-6). We probed two intracellular DNA sensing pathways, toll-like receptor 9 (TLR9) and cyclic GMP-AMP synthase (cGAS)-stimulator of interferon genes (STING), to determine how cells sense the DNA-nanoparticle complexes. We found that the cGAS-STING pathway is the primary route for the interaction between DNA-nanoparticles and macrophages. These studies provide a molecular and cellular-level understanding of DNA-nanoparticle-macrophage interactions. In addition, this work provides the mechanistic information necessary for future in vivo experiments to elucidate the role of DNA-particle interactions in autoimmune diseases, providing a unique experimental framework to develop novel therapeutic approaches.
自身免疫和炎症性疾病非常复杂,限制了治疗方法的发展和新疗法的研发。最近的研究表明,与生物微粒结合的无细胞 DNA 与系统性红斑狼疮(一种典型的自身免疫性疾病)有关。然而,与生物颗粒研究相关的异质性和技术挑战阻碍了对其作用的机制理解。我们的目标是开发一种可控的 DNA-颗粒模型系统,以了解 DNA-颗粒复合物如何影响细胞。我们首先使用透射电子显微镜、动态光散射和比色 DNA 浓度测定法来表征 DNA 在聚苯乙烯纳米颗粒(200nm 和 2μm)表面的吸附。我们发现 DNA 吸附在纳米颗粒表面上对 DNase 1 的降解具有抗性。与 DNA-纳米颗粒复合物孵育的巨噬细胞细胞会增加促炎细胞因子肿瘤坏死因子-α(TNF-α)和白细胞介素 6(IL-6)的产生。我们探测了两种细胞内 DNA 感应途径,即 Toll 样受体 9(TLR9)和环鸟苷酸-腺苷酸合酶(cGAS)-干扰素基因刺激物(STING),以确定细胞如何感应 DNA-纳米颗粒复合物。我们发现 cGAS-STING 途径是 DNA-纳米颗粒与巨噬细胞相互作用的主要途径。这些研究提供了 DNA-纳米颗粒-巨噬细胞相互作用的分子和细胞水平的理解。此外,这项工作提供了未来体内实验阐明 DNA-颗粒相互作用在自身免疫性疾病中的作用所需的机制信息,为开发新的治疗方法提供了独特的实验框架。