Guangdong Province Key Laboratory of Pharmaceutical Functional Genes, MOE Key Laboratory of Gene Function and Regulation, State Key Laboratory of Biocontrol, School of Life Sciences, Sun Yat-sen University, Guangzhou, China.
Institute of Precision Medicine, Department of Critical Care Medicine, the First Affiliated Hospital, Sun Yat-sen University, Guangzhou, China.
EMBO J. 2024 Nov;43(21):5057-5084. doi: 10.1038/s44318-024-00232-z. Epub 2024 Sep 16.
ER-phagy, a selective form of autophagic degradation of endoplasmic reticulum (ER) fragments, plays an essential role in governing ER homeostasis. Dysregulation of ER-phagy is associated with the unfolded protein response (UPR), which is a major clue for evoking inflammatory diseases. However, the molecular mechanism underpinning the connection between ER-phagy and disease remains poorly defined. Here, we identified ubiquitin-associated domain-containing protein 2 (UBAC2) as a receptor for ER-phagy, while at the same time being a negative regulator of inflammatory responses. UBAC2 harbors a canonical LC3-interacting region (LIR) in its cytoplasmic domain, which binds to autophagosomal GABARAP. Upon ER-stress or autophagy activation, microtubule affinity-regulating kinase 2 (MARK2) phosphorylates UBAC2 at serine (S) 223, promoting its dimerization. Dimerized UBAC2 interacts more strongly with GABARAP, thus facilitating selective degradation of the ER. Moreover, by affecting ER-phagy, UBAC2 restrains inflammatory responses and acute ulcerative colitis (UC) in mice. Our findings indicate that ER-phagy directed by a MARK2-UBAC2 axis may provide targets for the treatment of inflammatory disease.
内质网吞噬(ER-phagy)是内质网(ER)片段的一种选择性自噬降解形式,在调节 ER 稳态方面发挥着重要作用。ER-phagy 的失调与未折叠蛋白反应(UPR)有关,UPR 是引发炎症性疾病的主要线索。然而,ER-phagy 与疾病之间的联系的分子机制仍未得到明确界定。在这里,我们确定泛素相关结构域蛋白 2(UBAC2)是 ER-phagy 的受体,同时也是炎症反应的负调节剂。UBAC2 的细胞质结构域中含有一个典型的 LC3 相互作用区域(LIR),与自噬体 GABARAP 结合。在内质网应激或自噬激活时,微管亲和力调节激酶 2(MARK2)在丝氨酸(S)223 处磷酸化 UBAC2,促进其二聚化。二聚化的 UBAC2 与 GABARAP 结合更紧密,从而促进 ER 的选择性降解。此外,通过影响 ER-phagy,UBAC2 可抑制小鼠的炎症反应和急性溃疡性结肠炎(UC)。我们的研究结果表明,由 MARK2-UBAC2 轴指导的 ER-phagy 可能为炎症性疾病的治疗提供靶点。