Korotev Sophia C, Cheng Jason X, Haribabu Yogameenakshi, Strauss Joshua, Dominguez Salina, Koppayi Ashwin, Perpich Melody, Pies Madeline, Moma Luke, Kim Aelin, Basdag Hatice, Rodgers Courtnee, Kosuri Satyajit, Saiki Ryunosuke, Makishima Hideki, Tawde Sanjukta, Galasinski Shelly, Kandikatla Priscilla, Subramanian Hari Prasanna, Ren Kehan, Bi Honghao, Mohammadhosseini Mona, Ogawa Seishi, Ji Peng, Agarwal Anupriya, Das Soma, Godley Lucy A
Division of Hematology/Oncology, Department of Medicine, Robert H. Lurie Comprehensive Cancer Center, Northwestern University, Chicago, IL 60611.
Section of Hematopathology, Department of Pathology, The University of Chicago, Chicago, IL 60637.
Haematologica. 2025 Sep 1;110(9):2076-2090. doi: 10.3324/haematol.2024.286887. Epub 2025 Feb 13.
Germline loss-of-function (LoF) DDX41 variants predispose to late-onset hematopoietic malignancies (HM), predominantly of myeloid lineage. Among 43 families with germline DDX41LoF variants, bone marrow (BM) biopsies in those without (N=8) or with malignancies (N=21) revealed mild dysplasia in peripheral blood (57%) and BM (88%), long before the average age of DDX41-related HM onset. Therefore, we recommend baseline BM biopsies in people with germline DDX41LoF alleles to avoid over-diagnosis of myelodysplastic syndromes. A variety of solid tumors were also observed in our cohort, with 24% penetrance by age 75. Although acquired DDX41 mutations are common in HM, we failed to identify such alleles in solid tumors arising in those with germline DDX41LoF variants (N=15), suggesting an alternative mechanism driving solid tumor development. Furthermore, 33% of pedigrees in which ≥15% of first-degree relatives including the proband were diagnosed with a solid tumor had second germline deleterious variants in other cancer-predisposition genes, likely serving as primary cancer drivers. Finally, both lymphoblastoid cell lines and primary peripheral blood from individuals with germline DDX41LoF variants exhibited differential levels of inflammation-associated proteins. These data provide evidence of inflammatory dysfunction mediated by germline DDX41LoF alleles that may contribute to solid tumor growth in the context of additional germline cancer- associated variants. For those with HM and personal/family histories of solid tumors, we recommend broad germline testing. DDX41 may be an indirect modifier of solid tumor pathogenesis compared to its tumor suppressor function within hematopoietic tissues, a hypothesis that can be addressed in future work.
种系功能丧失(LoF)的DDX41变异易导致迟发性血液系统恶性肿瘤(HM),主要为髓系。在43个携带种系DDX41 LoF变异的家族中,对未患恶性肿瘤(N = 8)或患有恶性肿瘤(N = 21)的家族进行骨髓(BM)活检发现,在外周血(57%)和骨髓(88%)中存在轻度发育异常,这远早于DDX41相关HM发病的平均年龄。因此,我们建议对携带种系DDX41 LoF等位基因的人群进行基线BM活检,以避免骨髓增生异常综合征的过度诊断。在我们的队列中还观察到多种实体瘤,到75岁时的外显率为24%。虽然获得性DDX41突变在HM中很常见,但我们未能在携带种系DDX41 LoF变异的个体所患实体瘤中鉴定出此类等位基因(N = 15),这表明存在驱动实体瘤发展的另一种机制。此外,在≥15%的一级亲属(包括先证者)被诊断患有实体瘤的家系中,33%在其他癌症易感基因中存在第二个种系有害变异,这些变异可能是原发性癌症驱动因素。最后,携带种系DDX41 LoF变异个体的淋巴母细胞系和外周血原代细胞均表现出不同水平的炎症相关蛋白。这些数据提供了由种系DDX41 LoF等位基因介导的炎症功能障碍的证据,在存在其他种系癌症相关变异的情况下,这种炎症功能障碍可能促进实体瘤生长。对于患有HM且有实体瘤个人/家族史的患者,我们建议进行广泛的种系检测。与DDX41在造血组织中的肿瘤抑制功能相比,它可能是实体瘤发病机制的间接调节因子,这一假设可在未来的研究中得到验证。