Pessino Greta, Lonati Leonardo, Scotti Claudia, Calandra Silvia, Cazzalini Ornella, Iaria Ombretta, Previtali Andrea, Baiocco Giorgio, Perucca Paola, Tricarico Anna, Vetro Martina, Stivala Lucia Anna, Ganini Carlo, Cancelliere Marta, Zucchetti Massimo, Guardamagna Isabella, Maggi Maristella
Unit of Immunology and General Pathology, Department of Molecular Medicine, University of Pavia, 27100 Pavia, Italy.
Laboratory of Radiation Biophysics and Radiobiology, Department of Physics, University of Pavia, 27100 Pavia, Italy.
Heliyon. 2024 Aug 3;10(15):e35789. doi: 10.1016/j.heliyon.2024.e35789. eCollection 2024 Aug 15.
Asparagine and glutamine depletion operated by the drug Asparaginase (ASNase) has revolutionized therapy in pediatric patients affected by Acute Lymphoblastic Leukemia (ALL), bringing remissions to a remarkable 90 % of cases. However, the knowledge of the proproliferative role of asparagine in adult and solid tumors is still limited. We have here analyzed the effect of ASNase on three adenocarcinoma cell lines (A549, lung adenocarcinoma, MCF-7, breast cancer, and 786-O, kidney cancer). In contrast to MCF-7 cells, 786-O and A549 cells proved to be a relevant target for cell cycle perturbation by asparagine and glutamine shortage. Indeed, when the cell-cycle was analyzed by flow cytometry, A549 showed a canonical response to asparaginase, 786-O cells, instead, showed a reduction of the percentage of cells in the G1 phase and an increase of those in the S-phase. Despite an increased number of PCNA and RPA70 positive nuclear foci, BrdU and EdU incorporation was absent or strongly delayed in treated 786-O cells, thus indicating a readiness of replication forks unmatched by DNA synthesis. In 786-O asparagine synthetase was reduced following treatment and glutamine synthetase was totally absent. Interestingly, DNA synthesis could be recovered by adding Gln to the medium. MCF-7 cells showed no significant changes in the cell cycle phases, in DNA-bound PCNA and in total PCNA, but a significant increase in ASNS and GS mRNA and protein expression. The collected data suggest that the effect observed on 786-O cells following ASNase treatment could rely on mechanisms which differ from those well-known and described for leukemic blasts, consisting of a complete block in the G1/S transition in proliferating cells and on an increase on non-proliferative (G0) blasts.
天冬酰胺酶(ASNase)导致的天冬酰胺和谷氨酰胺耗竭彻底改变了急性淋巴细胞白血病(ALL)患儿的治疗方法,使约90%的病例实现缓解。然而,关于天冬酰胺在成人肿瘤和实体瘤中的促增殖作用的认识仍然有限。我们在此分析了ASNase对三种腺癌细胞系(A549,肺腺癌;MCF-7,乳腺癌;以及786-O,肾癌)的影响。与MCF-7细胞不同,786-O和A549细胞被证明是天冬酰胺和谷氨酰胺短缺导致细胞周期紊乱的相关靶点。事实上,通过流式细胞术分析细胞周期时,A549对天冬酰胺酶表现出典型反应,而786-O细胞则显示G1期细胞百分比降低,S期细胞百分比增加。尽管增殖细胞核抗原(PCNA)和复制蛋白A70(RPA70)阳性核灶数量增加,但在处理后的786-O细胞中,5-溴脱氧尿嘧啶核苷(BrdU)和5-乙炔基-2'-脱氧尿苷(EdU)掺入缺失或严重延迟,这表明复制叉准备就绪,但DNA合成未跟上。在786-O细胞中,处理后天冬酰胺合成酶减少,谷氨酰胺合成酶完全缺失。有趣的是,向培养基中添加谷氨酰胺可恢复DNA合成。MCF-7细胞在细胞周期阶段、DNA结合的PCNA和总PCNA方面无显著变化,但天冬酰胺合成酶(ASNS)和谷氨酰胺合成酶(GS)的mRNA和蛋白表达显著增加。收集的数据表明,ASNase处理后在786-O细胞上观察到的效应可能依赖于与白血病母细胞中已知和描述的机制不同的机制,白血病母细胞中的机制包括增殖细胞在G1/S期转变完全受阻以及非增殖(G0)母细胞增加。