Song Lili, Zhang Rui, Pan Liya, Mi Qiang, Yang Yi, Wang Xiang, Ma Yani, Shen Shuhong, Li Benshang, Li Yanxin, Hong Li
Department of Clinical Nutrition, Shanghai Children's Medical Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
Department of Hematology & Oncology, Key Laboratory of Pediatric Hematology and Oncology Ministry of Health, Shanghai Children's Medical Center, Shanghai Jiao Tong University School of Medicine, Shanghai, China.
Int J Cancer. 2025 Aug 1;157(3):559-572. doi: 10.1002/ijc.35418. Epub 2025 Apr 26.
Relapse and disease progression are the primary causes of treatment failure and subsequent mortality in children with B-cell acute lymphocytic leukemia (B-ALL). At diagnosis and during treatment, dyslipidemia and the bone marrow adipose microenvironment are commonly observed in pediatric leukemia. However, the intricate connection between these factors and disease progression remains largely unexplored. We found that abnormal triglyceride accumulation increased the risk of death. Further investigation into the adipogenic potential of BM-MSCs revealed a correlation between higher adipogenicity and elevated serum TG levels, which subsequently led to the rapid proliferation of leukemia cells and heightened the risk of post-relapse mortality. Through RNA sequencing, Gremlin1 (GREM1) was identified as an important factor affecting adipogenicity. Silencing of GREM1 in BM-MSCs induced adipogenic differentiation, partly through the BMP/SMAD signaling pathway. In an in vitro co-culture model, shGREM1-MSCs promoted B-ALL cell proliferation and induced drug resistance to dexamethasone, while increasing sensitivity to L-asparaginase. Furthermore, GREM1-deficient BM-MSCs promoted B-ALL disease progression in xenograft models. This study provides new insights into overcoming drug resistance, relapse, and death by elucidating the novel mechanism by which GREM1 deficiency induces adipogenic differentiation of BM-MSCs and promotes B-ALL disease progression.
复发和疾病进展是B细胞急性淋巴细胞白血病(B-ALL)患儿治疗失败及随后死亡的主要原因。在诊断和治疗期间,小儿白血病患者中常出现血脂异常和骨髓脂肪微环境。然而,这些因素与疾病进展之间的复杂联系在很大程度上仍未得到探索。我们发现异常的甘油三酯积累会增加死亡风险。对骨髓间充质干细胞(BM-MSCs)成脂潜能的进一步研究揭示了较高的成脂性与血清甘油三酯水平升高之间的相关性,这随后导致白血病细胞快速增殖并增加复发后死亡风险。通过RNA测序,Gremlin1(GREM1)被确定为影响成脂性的一个重要因素。BM-MSCs中GREM1的沉默诱导了成脂分化,部分是通过骨形态发生蛋白/信号转导分子(BMP/SMAD)信号通路。在体外共培养模型中,shGREM1-MSCs促进B-ALL细胞增殖并诱导对地塞米松的耐药性,同时增加对L-天冬酰胺酶的敏感性。此外,GREM1缺陷的BM-MSCs在异种移植模型中促进了B-ALL疾病进展。本研究通过阐明GREM1缺陷诱导BM-MSCs成脂分化并促进B-ALL疾病进展的新机制,为克服耐药性、复发和死亡提供了新见解。