Hasegawa Tatsuya, Noguchi Saori, Nakashima Masaya, Miyai Masashi, Goto Makiko, Matsumoto Yuko, Torii Satoru, Honda Shinya, Shimizu Shigeomi
Shiseido Global Innovation Center, Yokohama, Japan.
Department of Pathological Cell Biology, Medical Research Institute, Tokyo Medical and Dental University, Tokyo, Japan.
J Biol Chem. 2024 Apr;300(4):107173. doi: 10.1016/j.jbc.2024.107173. Epub 2024 Mar 17.
Sunlight exposure results in an inflammatory reaction of the skin commonly known as sunburn, which increases skin cancer risk. In particular, the ultraviolet B (UVB) component of sunlight induces inflammasome activation in keratinocytes to instigate the cutaneous inflammatory responses. Here, we explore the intracellular machinery that maintains skin homeostasis by suppressing UVB-induced inflammasome activation in human keratinocytes. We found that pharmacological inhibition of autophagy promoted UVB-induced NLRP3 inflammasome activation. Unexpectedly, however, gene silencing of Atg5 or Atg7, which are critical for conventional autophagy, had no effect, whereas gene silencing of Beclin1, which is essential not only for conventional autophagy but also for Atg5/Atg7-independent alternative autophagy, promoted UVB-induced inflammasome activation, indicating an involvement of alternative autophagy. We found that damaged mitochondria were highly accumulated in UVB-irradiated keratinocytes when alternative autophagy was inhibited, and they appear to be recognized by NLRP3. Overall, our findings indicate that alternative autophagy, rather than conventional autophagy, suppresses UVB-induced NLRP3 inflammasome activation through the clearance of damaged mitochondria in human keratinocytes and illustrate a previously unknown involvement of alternative autophagy in inflammation. Alternative autophagy may be a new therapeutic target for sunburn and associated cutaneous disorders.
暴露于阳光会导致皮肤发生炎症反应,即通常所说的晒伤,这会增加患皮肤癌的风险。特别是,阳光中的紫外线B(UVB)成分会诱导角质形成细胞中的炎性小体激活,从而引发皮肤炎症反应。在此,我们探索了通过抑制人角质形成细胞中UVB诱导的炎性小体激活来维持皮肤稳态的细胞内机制。我们发现,自噬的药理学抑制促进了UVB诱导的NLRP3炎性小体激活。然而,出乎意料的是,对传统自噬至关重要的Atg5或Atg7的基因沉默没有效果,而对传统自噬以及对不依赖Atg5/Atg7的替代性自噬都必不可少的Beclin1的基因沉默则促进了UVB诱导的炎性小体激活,这表明替代性自噬参与其中。我们发现,当替代性自噬受到抑制时,受损的线粒体在UVB照射的角质形成细胞中高度积累,并且它们似乎被NLRP3识别。总体而言,我们的研究结果表明,替代性自噬而非传统自噬通过清除人角质形成细胞中受损的线粒体来抑制UVB诱导的NLRP3炎性小体激活,并阐明了替代性自噬在炎症中以前未知的作用。替代性自噬可能是晒伤及相关皮肤疾病的一个新的治疗靶点。