Kim Heesoo, Shin Wonji, Lee Dongeun, Jeon Byunghoon, Kim Yongbo, Shin Donghyuk, Jeong Hyobin, Hong Jun Young, Lee Sungwook, Park Boyoun
Department of Systems Biology, College of Life Science and Biotechnology, Yonsei University, Seoul, 03722, South Korea.
Interdisciplinary Program of Integrated OMICS for Biomedical Science, Yonsei University, Seoul, 03722, South Korea.
EMBO Rep. 2025 Dec;26(23):5982-6014. doi: 10.1038/s44319-025-00616-0. Epub 2025 Oct 30.
Mammalian erythroid cells undergo extensive organelle and protein remodeling during erythropoiesis. The transcriptome and proteome of ubiquitin E3 ligases change dynamically during erythroid differentiation, yet mechanisms beyond E3 activity remain unclear. Here, we identify that tripartite motif-containing protein 10α (TRIM10α), an erythroid- and stage-specific E3 ligase, as crucial for stepwise erythroid maturation. TRIM10α self-association to localize on erythroblast surfaces, binding extracellular complement C1q, which facilitates pyrenocyte encapsulation and macrophage recognition. Surface C1q interacts with EpoR to promote lysosomal degradation, and its depletion prolongs Epo signaling. Notably, cytosolic TRIM10α enhances hemoglobin (Hb) maturation and sequesters Hb aggregates under oxidative conditions. Ultimately, TRIM10α self-ubiquitination and its binding to p62 are anticipated to lead to TRIM10α degradation, promoting the removal of Hb aggregates via autophagy. In contrast to TRIM10α, an alternatively spliced TRIM10β, which is barely expressed in human tissues and cells, forms deleterious aggregates, suggesting that evolutionary suppression of TRIM10β supports erythroid homeostasis. Our findings propose that aberrant TRIM10 expression drives erythroid-related diseases and highlight TRIM10 as a potential biomarker or therapeutic target.
哺乳动物红细胞在红细胞生成过程中经历广泛的细胞器和蛋白质重塑。泛素E3连接酶的转录组和蛋白质组在红细胞分化过程中动态变化,然而E3活性之外的机制仍不清楚。在这里,我们确定含三联基序蛋白10α(TRIM10α),一种红细胞特异性和阶段特异性E3连接酶,对红细胞的逐步成熟至关重要。TRIM10α通过自我缔合定位于成红细胞表面,结合细胞外补体C1q,这有助于红细胞的包裹和巨噬细胞识别。表面C1q与促红细胞生成素受体(EpoR)相互作用以促进溶酶体降解,其缺失会延长Epo信号传导。值得注意的是,胞质TRIM10α可促进血红蛋白(Hb)成熟,并在氧化条件下隔离Hb聚集体。最终,预计TRIM10α的自我泛素化及其与p62的结合会导致TRIM10α降解,通过自噬促进Hb聚集体的清除。与TRIM10α相反,另一种选择性剪接的TRIM10β在人类组织和细胞中几乎不表达,会形成有害聚集体,这表明对TRIM10β的进化抑制有助于维持红细胞内稳态。我们的研究结果表明,TRIM10的异常表达会引发红细胞相关疾病,并突出了TRIM10作为潜在生物标志物或治疗靶点的作用。