Lippincott Michael J, Tomkinson Jenna, Bunten Dave, Mohammadi Milad, Kastl Johanna, Knop Johannes, Schwandner Ralf, Huang Jiamin, Ongo Grant, Robichaud Nathaniel, Dagher Milad, Mansilla-Soto Andrés, Saravia-Estrada Cynthia, Tsuboi Masafumi, Basualto-Alarcón Carla, Way Gregory P
Department of Biomedical Informatics, University of Colorado School of Medicine, Aurora, CO 80045.
Assay.Works GmbH, Regensburg, Germany 93053.
Mol Biol Cell. 2025 Jun 1;36(6):ar63. doi: 10.1091/mbc.E25-03-0119. Epub 2025 Apr 9.
Pyroptosis represents one type of programmed cell death. It is a form of inflammatory cell death that is canonically defined by caspase-1 cleavage and Gasdermin-mediated membrane pore formation. Caspase-1 initiates the inflammatory response (through IL-1β processing), and the N-terminal cleaved fragment of Gasdermin D polymerizes at the cell periphery forming pores to secrete proinflammatory markers. Cell morphology also changes in pyroptosis, with nuclear condensation and membrane rupture. However, recent research challenges canon, revealing a more complex secretome and morphological response in pyroptosis, including overlapping molecular characterization with other forms of cell death, such as apoptosis. Here, we take a multimodal, systems biology approach to characterize pyroptosis. We treated human peripheral blood mononuclear cells (PBMCs) with 36 different combinations of stimuli to induce pyroptosis or apoptosis. We applied both secretome profiling (nELISA) and high-content fluorescence microscopy (Cell Painting). To differentiate apoptotic, pyroptotic, and control cells, we used canonical secretome markers and modified our Cell Painting assay to mark the N-terminus of Gasdermin D. We trained hundreds of machine learning (ML) models to reveal intricate morphology signatures of pyroptosis that implicate changes across many different organelles and predict levels of many proinflammatory markers. Overall, our analysis provides a detailed map of pyroptosis which includes overlapping and distinct connections with apoptosis revealed through a mechanistic link between cell morphology and cell secretome.
细胞焦亡是程序性细胞死亡的一种类型。它是一种炎症性细胞死亡形式,典型地由半胱天冬酶-1切割和Gasdermin介导的膜孔形成来定义。半胱天冬酶-1引发炎症反应(通过白细胞介素-1β加工),Gasdermin D的N端切割片段在细胞周边聚合形成孔,以分泌促炎标志物。细胞焦亡时细胞形态也会发生变化,出现核浓缩和膜破裂。然而,最近的研究对传统观点提出了挑战,揭示了细胞焦亡中更复杂的分泌组和形态学反应,包括与其他形式的细胞死亡(如凋亡)的分子特征重叠。在这里,我们采用多模态系统生物学方法来表征细胞焦亡。我们用36种不同的刺激组合处理人外周血单核细胞(PBMC)以诱导细胞焦亡或凋亡。我们应用了分泌组分析(nELISA)和高内涵荧光显微镜技术(细胞成像)。为了区分凋亡细胞、细胞焦亡细胞和对照细胞,我们使用了传统的分泌组标志物,并改进了我们的细胞成像分析方法来标记Gasdermin D的N端。我们训练了数百个机器学习(ML)模型,以揭示细胞焦亡复杂的形态学特征,这些特征涉及许多不同细胞器的变化,并预测许多促炎标志物的水平。总体而言,我们的分析提供了一张细胞焦亡的详细图谱,其中包括通过细胞形态和细胞分泌组之间的机制联系揭示的与凋亡的重叠和不同联系。