Li Kun, Zhang Dongbin, Zhai Shuiting, Wu Huilin, Liu Hongzhi
Department of Vascular and Endovascular Surgery, Henan Provincial People's Hospital, People's Hospital of Zhengzhou University, Zhengzhou, 450003, Henan, China.
Heart Center of Henan Provincial People's Hospital, Central China Fuwai Hospital, Fuwai Hospital of Zhengzhou University, No. 1 Fuwai Road, Zhengdong New District, Zhengzhou, 451464, Henan, China.
J Cell Commun Signal. 2023 Sep;17(3):897-914. doi: 10.1007/s12079-023-00737-y. Epub 2023 Mar 22.
Abdominal aortic aneurysms (AAA) have the highest incidence and rupture rate of all aortic aneurysms. The N6 methyladenosine (m6A) modification is closely associated with angiotensin (Ang II)-induced aortic diseases. This study aimed to identify whether the m6A writer METTL3/METTL4 regulates rip3 mRNA expression in AAA. To induce the mouse AAA model, apolipoprotein E-deficient (ApoE-/-) mice were subcutaneously infused with Ang II, and C57BL/6 mice were infused with type I elastase. Vascular smooth muscle cells (VSMCs) were induced with Ang II. Necroptosis was detected using an Annexin V-FITC/PI apoptosis detection kit, and ELISA assays measured inflammatory cytokines. The RNA immunoprecipitation-qPCR determined the methylated rip3 mRNA level. The increased expressions of inflammatory factors, aortic adventitia injury, degradation of elastin, and CD68-positive cells suggested the successful establishment of mouse AAA models. In AAA aorta wall tissues, the m6A modification level and the expression of METTL3/METTL14 were elevated. In Ang II-induced VSMCs, necroptosis and inflammatory cytokines in the supernatants were increased. RNA immunoprecipitation and co-immunoprecipitation assays confirmed the binding between the METTL3-METTL14 complex and rip3 mRNA, the interaction between YTHDF3 and rip3 mRNA, and between the METTL3-METTL14 complex and SMAD2/3. Interference with METTL3/METTL14 attenuated VSMC necroptosis, inflammatory response, and the AAA pathological process in vivo. The METTL3-METTL14 complex, which was increased by the activation of the SMAD2/3, elevated the m6A modification of rip3 mRNA by promoting the binding between YTHDF3 and rip3 mRNA, thus contributing to the progression of AAA. The activation of SMAD2/3 in VSMCs of abdominal aortic wall tissues is stimulated by Ang II. Subsequently, it promotes METTL3 METTL14 complex mediated m6A modification of rip3 mRNA. Meanwhile, the level of rip3 mRNA becomes more stable under the m6A reader of YTHDF3, which increases the protein level of RIP3 and further induces VSMC necroptosis. In addition, cell debris induces inflammatory factors in neighboring VSMCs and recruit monocytes/macrophages to the lesion.
腹主动脉瘤(AAA)在所有主动脉瘤中发病率和破裂率最高。N6甲基腺苷(m6A)修饰与血管紧张素(Ang II)诱导的主动脉疾病密切相关。本研究旨在确定m6A甲基转移酶METTL3/METTL4是否调节AAA中rip3 mRNA的表达。为诱导小鼠AAA模型,给载脂蛋白E缺陷(ApoE-/-)小鼠皮下注射Ang II,给C57BL/6小鼠注射I型弹性蛋白酶。用Ang II诱导血管平滑肌细胞(VSMC)。使用膜联蛋白V-FITC/PI凋亡检测试剂盒检测坏死性凋亡,ELISA法检测炎性细胞因子。RNA免疫沉淀-qPCR测定甲基化rip3 mRNA水平。炎性因子表达增加、主动脉外膜损伤、弹性蛋白降解以及CD68阳性细胞提示成功建立小鼠AAA模型。在AAA主动脉壁组织中,m6A修饰水平以及METTL3/METTL14的表达升高。在Ang II诱导的VSMC中,上清液中的坏死性凋亡和炎性细胞因子增加。RNA免疫沉淀和免疫共沉淀实验证实METTL3-METTL14复合物与rip3 mRNA结合、YTHDF3与rip3 mRNA相互作用以及METTL3-METTL14复合物与SMAD2/3相互作用。干扰METTL3/METTL14可减轻体内VSMC坏死性凋亡、炎性反应以及AAA病理过程。由SMAD2/3激活而增加的METTL3-METTL14复合物,通过促进YTHDF3与rip3 mRNA的结合提高rip3 mRNA的m6A修饰,从而促进AAA的进展。腹主动脉壁组织VSMC中SMAD2/3的激活由Ang II刺激。随后,它促进METTL3-METTL14复合物介导的rip3 mRNA的m6A修饰。同时,rip3 mRNA水平在YTHDF3这个m6A阅读蛋白作用下变得更稳定,这增加了RIP3蛋白水平并进一步诱导VSMC坏死性凋亡。此外,细胞碎片诱导邻近VSMC中的炎性因子,并将单核细胞/巨噬细胞募集到病变部位。