Bley Nadine, Rausch Alexander, Müller Simon, Simon Theresa, Glaß Markus, Misiak Danny, Schian Laura, Peters Lara Meret, Dipto Mohammad, Hmedat Ali, Busch Bianca, Schott Annekatrin, Lederer Marcell, Wedler Alice, Rolnik Robin Benedikt, Elrewany Hend, Ghazy Ehab, Sippl Wolfgang, Vetter Martina, Wallwiener Markus, Hüttelmaier Stefan
Institute of Molecular Medicine, Section for Molecular Cell Biology, Faculty of Medicine, Martin Luther University Halle-Wittenberg, Halle, Germany.
New York Genome Center, New York, NY, USA.
Signal Transduct Target Ther. 2025 Dec 25;10(1):419. doi: 10.1038/s41392-025-02515-1.
High-grade serous ovarian cancer (HGSC) accounts for more than 70% of ovarian cancer-related deaths, yet therapeutic progress remains stagnant. Among the four molecular subtypes reported for HGSC, the C5 subtype is distinguished by high proliferation and immune evasion with an unfavorable MHC-I/PD-L1 ratio. However, the molecular drivers of this immune desert state remain largely undefined. Here, we identify RNA-binding proteins (RBPs) as key regulators of immune evasion in C5-HGSC through integrated single-cell and bulk RNA sequencing. We perform a targeted loss-of-function screen in C5-like cell models and find IGF2BP1 as a central mediator of immune evasion in vitro and in vivo. Mechanistically, IGF2BP1 abrogates interferon-gamma signaling by accelerating IRF1 protein degradation, thereby suppressing MHC-I presentation. We also discover that IGF2BP1 decouples PD-L1 expression from IRF1-dependent transcription and reshapes the immune receptor landscape to limit immune cell infiltration and T cell activation. Therapeutically, the small-molecule BTYNB effectively inhibits IGF2BP1 and synergizes with PD-1 blockade to overcome immune evasion in vivo. Multi-spectral imaging confirms these findings in human HGSC tissues and highlights the role of oncofetal RBPs as molecular drivers of the C5-HGSC subtype. This subtype-wide survey uncovers a previously unrecognized RBP-interferon regulatory axis and establishes RBP inhibition as a therapeutic strategy to enhance immune checkpoint therapy in immunologically cold ovarian tumors.
高级别浆液性卵巢癌(HGSC)占卵巢癌相关死亡的70%以上,但治疗进展仍然停滞不前。在报道的HGSC的四种分子亚型中,C5亚型的特点是增殖率高和免疫逃逸,MHC-I/PD-L1比例不利。然而,这种免疫荒漠状态的分子驱动因素在很大程度上仍不明确。在这里,我们通过整合单细胞和批量RNA测序,确定RNA结合蛋白(RBP)是C5-HGSC免疫逃逸的关键调节因子。我们在C5样细胞模型中进行了靶向功能丧失筛选,发现IGF2BP1是体内外免疫逃逸的核心介质。从机制上讲,IGF2BP1通过加速IRF1蛋白降解来消除干扰素-γ信号,从而抑制MHC-I呈递。我们还发现,IGF2BP1使PD-L1表达与IRF1依赖性转录脱钩,并重塑免疫受体格局,以限制免疫细胞浸润和T细胞活化。在治疗方面,小分子BTYNB有效抑制IGF2BP1,并与PD-1阻断协同作用,以克服体内的免疫逃逸。多光谱成像在人类HGSC组织中证实了这些发现,并突出了癌胚RBP作为C5-HGSC亚型分子驱动因素的作用。这项全亚型调查揭示了一个以前未被认识的RBP-干扰素调节轴,并将RBP抑制确立为一种治疗策略,以增强免疫冷性卵巢肿瘤中的免疫检查点治疗。