Manni Sabrina, Fregnani Anna, Quotti Tubi Laura, Spinello Zaira, Carraro Marco, Scapinello Greta, Visentin Andrea, Barilà Gregorio, Pizzi Marco, Dei Tos Angelo Paolo, Vianello Fabrizio, Zambello Renato, Gurrieri Carmela, Semenzato Gianpietro, Trentin Livio, Piazza Francesco
Department of Medicine-DIMED, Hematology and Clinical Immunology Section, University of Padova, Padova, Italy.
Laboratory of Myeloma and Lymphoma Pathobiology, Veneto Institute of Molecular Medicine, Padova, Italy.
Front Oncol. 2021 Oct 14;11:733848. doi: 10.3389/fonc.2021.733848. eCollection 2021.
Mantle Cell Lymphoma (MCL) is still an incurable B-cell malignancy characterized by poor prognosis and frequent relapses. B Cell Receptor (BCR) signaling inhibitors, in particular of the kinases BTK and PI3Kγ/δ, have demonstrated clinically meaningful anti-proliferative effects in B cell tumors. However, refractoriness to these drugs may develop, portending a dismal prognosis. Protein kinase CK1α is an emerging pro-growth enzyme in B cell malignancies. In multiple myeloma, this kinase sustains β-catenin and AKT-dependent survival and is involved in the activation of NF-κB in B cells. In this study, we analyzed the role of CK1α on MCL cell survival and proliferation, on the regulation of BCR-related BTK, NF-κB, PI3K/AKT signaling cascades and the effects of CK1α chemical inhibition or gene silencing in association with the BTK inhibitor Ibrutinib or the PI3Kγ/δ inhibitor Duvelisib. CK1α was found highly expressed in MCL cells as compared to normal B cells. The inactivation/loss of CK1α caused MCL cell apoptosis and proliferation arrest. CK1α sustained BCR signaling, in particular the NF-κB, AKT and BTK pathways by modulating the phosphorylation of Ser 652 on CARD11, Ser 536 p65 on NF-κB, Ser 473 on AKT, Tyr 223 on BTK, as well as the protein levels. We also provided evidence that CK1α-mediated regulation of CARD11 and BTK likely implicates a physical interaction. The combination of CK1α inhibition with Ibrutinib or Duvelisib synergistically increased cytotoxicity, leading to a further decrease of the activation of BCR signaling pathways. Therefore, CK1α sustains MCL growth through the regulation of BCR-linked survival signaling cascades and protects from Ibrutinib/Duvelisib-induced apoptosis. Thus, CK1α could be considered as a rational molecular target for the treatment of MCL, in association with novel agents.
套细胞淋巴瘤(MCL)仍然是一种无法治愈的B细胞恶性肿瘤,其特点是预后不良且频繁复发。B细胞受体(BCR)信号抑制剂,特别是激酶BTK和PI3Kγ/δ的抑制剂,已在B细胞肿瘤中显示出具有临床意义的抗增殖作用。然而,对这些药物可能会产生耐药性,这预示着预后不佳。蛋白激酶CK1α是B细胞恶性肿瘤中一种新出现的促进生长的酶。在多发性骨髓瘤中,这种激酶维持β-连环蛋白和AKT依赖的生存,并参与B细胞中NF-κB的激活。在本研究中,我们分析了CK1α在MCL细胞存活和增殖中的作用,在BCR相关的BTK、NF-κB、PI3K/AKT信号级联调节中的作用,以及CK1α化学抑制或基因沉默与BTK抑制剂伊布替尼或PI3Kγ/δ抑制剂度维利西布联合使用的效果。与正常B细胞相比,发现CK1α在MCL细胞中高表达。CK1α的失活/缺失导致MCL细胞凋亡和增殖停滞。CK1α通过调节CARD11上的Ser 652、NF-κB上的Ser 536 p65、AKT上的Ser 473、BTK上的Tyr 223的磷酸化以及蛋白水平来维持BCR信号,特别是NF-κB、AKT和BTK途径。我们还提供了证据表明CK1α介导的CARD11和BTK调节可能涉及物理相互作用。CK1α抑制与伊布替尼或度维利西布联合使用可协同增加细胞毒性,导致BCR信号通路的激活进一步降低。因此,CK1α通过调节与BCR相关的生存信号级联来维持MCL的生长,并保护细胞免受伊布替尼/度维利西布诱导的凋亡。因此,与新型药物联合使用时,CK1α可被视为治疗MCL的合理分子靶点。