Giuliano M, Lauricella M, Calvaruso G, Carabillò M, Emanuele S, Vento R, Tesoriere G
Institute of Biological Chemistry, University of Palermo, Italy.
Cancer Res. 1999 Nov 1;59(21):5586-95.
This study deals with the apoptotic effect exerted on human retinoblastoma Y79 cells by both sodium butyrate and an inhibitor of 26S proteasome [z-Leu-Leu-Leu-CHO (MG132)] and their synergistic effect. Exposure to sodium butyrate (1-4 mM) induced an accumulation of cells in the G2-M phase that was already visible after 24 h of treatment, when morphological and biochemical signs of apoptosis appeared only in a small number of cells (5-10%). Thereafter, the apoptotic effects increased progressively with slow kinetics, reaching a maximum after 72 h of exposure, when they concerned a large fraction of cells (>75% with 4 mM sodium butyrate). Sodium butyrate stimulated the conversion of procaspase-3 into caspase-3 and also induced the cleavage of poly-(ADP-ribose) polymerase and lamin B, two hallmarks of apoptosis. All of the apoptotic signals were suppressed by benzyloxy carbonyl-Val-Ala-Asp-fluoromethylketone (a general inhibitor of caspase activities), whereas acetyl-Asp-Glu-Val-Asp aldehyde, a specific inhibitor of caspase-3 activity, only induced a partial reversion of the apoptotic effects. Sodium butyrate also decreased the Bcl-2 level, whereas it increased the Bax level and stimulated the release of cytochrome c from the mitochondria, an event that was most likely responsible for the activation of caspase-3. Finally, sodium butyrate activated 26S proteasome, the major extralysosomal degradative machinery, which is responsible for the degradation of short-lived proteins. Consequently, the levels of p53, N-myc, and IkappaBalpha (factors that play regulatory roles in apoptosis) diminished, whereas the nuclear level of nuclear factor kappaB concomitantly increased. Treatment of Y79 cells with MG132 induced apoptosis with more rapid kinetics than with sodium butyrate. The effects appeared after 8 h of incubation, reaching a maximum at 24 h, and they were accompanied by increased levels of N-myc, p53, and IkappaBalpha. MG132 also favored the release of cytochrome c from the mitochondria and increased the activity of caspase-3. When Y79 cells were exposed to combinations of sodium butyrate and MG132, the latter compound suppressed the decreasing effect induced by sodium butyrate on the levels of p53, N-myc, and IkappaBalpha and the increasing effect on the nuclear level of nuclear factor kappaB. Moreover, an increase in the level of Bax and an enhancement in the release of cytochrome c from the mitochondria were observed. Clear synergistic effects concerning the activation of both caspase-3 and apoptosis were induced by a combination of suboptimal doses of sodium butyrate and MG132. The results support the conclusion that MG132 potentiates the apoptotic effect of sodium butyrate by suppressing its stimulatory effect on 26S proteasome activity. Synergistic interactions between butyrate and inhibitors of proteasome could represent a new important tool in tumor therapy and, in particular, the treatment of retinoblastoma.
本研究探讨丁酸钠和26S蛋白酶体抑制剂[z-亮氨酰-亮氨酰-亮氨酰-醛(MG132)]对人视网膜母细胞瘤Y79细胞的凋亡作用及其协同效应。暴露于丁酸钠(1 - 4 mM)会导致细胞在G2 - M期积累,处理24小时后即可观察到,此时凋亡的形态学和生化迹象仅出现在少数细胞(5 - 10%)中。此后,凋亡效应随时间缓慢增加,暴露72小时后达到最大值,此时大部分细胞(4 mM丁酸钠处理时>75%)出现凋亡。丁酸钠刺激procaspase - 3转化为caspase - 3,还诱导聚(ADP - 核糖)聚合酶和核纤层蛋白B的裂解,这是凋亡的两个标志。所有凋亡信号均被苄氧羰基 - 缬氨酰 - 丙氨酰 - 天冬氨酸 - 氟甲基酮(一种半胱天冬酶活性的通用抑制剂)抑制,而乙酰 - 天冬氨酸 - 谷氨酸 - 缬氨酸 - 天冬氨酸醛(一种caspase - 3活性的特异性抑制剂)仅能部分逆转凋亡效应。丁酸钠还降低了Bcl - 2水平,同时增加了Bax水平,并刺激细胞色素c从线粒体释放,这一事件很可能是caspase - 3激活的原因。最后,丁酸钠激活了26S蛋白酶体,这是主要的溶酶体外降解机制,负责降解短命蛋白。因此,p53、N - myc和IkappaBalpha(在凋亡中起调节作用的因子)水平降低,而核因子kappaB的核水平相应增加。用MG132处理Y79细胞诱导凋亡的动力学比丁酸钠更快。处理8小时后出现效应,24小时达到最大值,同时N - myc、p53和IkappaBalpha水平升高。MG132还促进细胞色素c从线粒体释放并增加caspase - 3的活性。当Y79细胞暴露于丁酸钠和MG132的组合时,后者抑制了丁酸钠对p53、N - myc和IkappaBalpha水平的降低作用以及对核因子kappaB核水平的增加作用。此外,观察到Bax水平升高以及细胞色素c从线粒体释放增加。次优剂量的丁酸钠和MG132组合诱导了caspase - 3激活和凋亡的明显协同效应。结果支持以下结论:MG132通过抑制丁酸钠对26S蛋白酶体活性的刺激作用来增强其凋亡效应。丁酸盐与蛋白酶体抑制剂之间的协同相互作用可能代表肿瘤治疗尤其是视网膜母细胞瘤治疗中的一种新的重要工具。