Nardi Federica, Del Prete Rosita, Drago Roberta, Di Rita Anthea, Vallone Francesco Edoardo, Ciofini Sara, Malchiodi Margherita, Pezzella Laura, Tinti Laura, Cicaloni Vittoria, Salvini Laura, Licastro Danilo, Pezacki Aidan T, Chang Christopher J, Marotta Giuseppe, Naldini Antonella, Deaglio Silvia, Vaisitti Tiziana, Gozzetti Alessandro, Bocchia Monica, Kabanova Anna
Fondazione Toscana Life Sciences, Siena, Italy.
Department of Medicine, Surgery and Neuroscience, University of Siena, Siena, Italy.
Leukemia. 2025 Jan;39(1):122-133. doi: 10.1038/s41375-024-02442-0. Epub 2024 Oct 23.
Unraveling vulnerabilities in chronic lymphocytic leukemia (CLL) represents a key approach to understand molecular basis for its indolence and a path toward developing tailored therapeutic approaches. In this study, we found that CLL cells are particularly sensitive to the inhibitory action of abundant serum protein, apolipoprotein E (ApoE). Physiological concentrations of ApoE affect CLL cell viability and inhibit CD40-driven proliferation. Transcriptomics of ApoE-treated CLL cells revealed a signature of redox and metal disbalance which prompted us to explore the underlying mechanism of cell death. We discover, on one hand, that ApoE treatment of CLL cells induces lipid peroxidation and ferroptosis. On the other hand, we find that ApoE is a copper-binding protein and that intracellular copper regulates ApoE toxicity. ApoE regulation tends to be lost in aggressive CLL. CLL cells from patients with high leukocyte counts are less sensitive to ApoE inhibition, while resistance to ApoE is possible in transformed CLL cells from patients with Richter syndrome (RS). Nevertheless, both aggressive CLL and RS cells maintain sensitivity to drug-induced ferroptosis. Our findings suggest a natural suppression axis that mediates ferroptotic disruption of CLL cell proliferation, building up the rationale for choosing ferroptosis as a therapeutic target in CLL and RS.
揭示慢性淋巴细胞白血病(CLL)的脆弱性是理解其惰性分子基础的关键途径,也是开发定制化治疗方法的道路。在本研究中,我们发现CLL细胞对丰富的血清蛋白载脂蛋白E(ApoE)的抑制作用特别敏感。生理浓度的ApoE影响CLL细胞活力并抑制CD40驱动的增殖。经ApoE处理的CLL细胞的转录组学揭示了氧化还原和金属失衡的特征,这促使我们探索细胞死亡的潜在机制。一方面,我们发现用ApoE处理CLL细胞会诱导脂质过氧化和铁死亡。另一方面,我们发现ApoE是一种铜结合蛋白,细胞内铜调节ApoE的毒性。在侵袭性CLL中,ApoE调节往往丧失。白细胞计数高的患者的CLL细胞对ApoE抑制不太敏感,而里氏综合征(RS)患者的转化CLL细胞可能对ApoE产生抗性。然而,侵袭性CLL细胞和RS细胞对药物诱导的铁死亡均保持敏感。我们的研究结果表明存在一个天然抑制轴,可介导CLL细胞增殖的铁死亡破坏,为将铁死亡作为CLL和RS的治疗靶点提供了理论依据。