Domínguez-Cáceres María Aurora, García-Martínez José Manuel, Calcabrini Annarica, González Lorena, Porque Pedro González, León Javier, Martín-Pérez Jorge
Instituto de Investigaciones Biomédicas, CSIC, Calle Arturo Duperier, 4, Madrid 28029, Spain.
Oncogene. 2004 Sep 23;23(44):7378-90. doi: 10.1038/sj.onc.1208002.
Stimulation of resting W53 cells (lymphoid murine cells expressing prolactin (PRL) receptor) by PRL induced expression of growth-related immediate-early genes (IEG), and proliferation through activation of the Src kinases. Since IEG are essential for cell cycle progression, we have studied how PRL controls expression of c-Myc mRNA and c-Fos. Stimulation of W53 cell proliferation by PRL required activation of MAPK, as the Mek1/2 inhibitor PD184352 eliminated Erk1/2 stimulation, cell proliferation, and expression of c-Fos mRNA. In contrast, PD184352 did not alter PRL activation of c-Myc mRNA expression or stimulation of p70S6K, Akt, and the Jak2/Stat5 pathway. Activation of the PI3K by PRL was necessary for the expression of c-MycmRNA and W53 cell proliferation, as the PI3K inhibitor LY294002 abolished them. However, it did not modify PRL stimulation of c-Fos mRNA expression or activation of Erk1/2 and Stat5. Furthermore, rapamycin, an inhibitor of mTOR and consequently of p70S6K, did not alter PRL stimulation of c-Myc and c-Fos mRNA expression and it had a very minor inhibitory effect on PRL stimulation of W53 cell proliferation. In addition, rapamycin did not affect PRL stimulation of Akt or Stat5. However, it reinforced PRL activation of Erk1/2. Overexpression of a constitutively activated Akt (myristoylated Akt) in W53 cells overcame the inhibitory effect of LY294002 on c-Myc expression, as well as cell death upon PRL deprivation. Consistently, inducible expression of Akt-CAAX Box in W53 cells caused inhibition of c-Myc expression. PRL stimulation of W53 cells resulted in Akt translocation to the nucleus, phosphorylation of FKHRL1 transcription factor, and its nuclear exclusion. In contrast, induced expression of Akt-CAAX Box caused inhibition of FKHRL1 phosphorylation. Furthermore, transient expression of nonphosphorylatable FKHRL1-A3 mutant impaired PRL-induced activation of the c-Myc promoter. Akt activation also resulted in phosphorylation and inhibition of glycogen synthetase kinase 3 (GSK3), which in turn promoted c-Myc stability. Consistently, treatment of W53 with selective inhibitors of GSK3 such as SB415286 and lithium salts resulted in increased levels of c-Myc. Also, overexpression of c-Myc in W53 cells overcame the decrease in cell proliferation induced by LY294002. These findings defined a PRL-signalling cascade in W53 cells, involving Src kinases/PI3K/Akt/FKHRL1-GSK3, that mediates stimulation of c-Myc expression.
催乳素(PRL)刺激静止的W53细胞(表达催乳素受体的小鼠淋巴细胞)可诱导生长相关即早基因(IEG)的表达,并通过Src激酶的激活促进细胞增殖。由于IEG对细胞周期进程至关重要,我们研究了PRL如何控制c-Myc mRNA和c-Fos的表达。PRL刺激W53细胞增殖需要激活丝裂原活化蛋白激酶(MAPK),因为Mek1/2抑制剂PD184352可消除细胞外信号调节激酶1/2(Erk1/2)的刺激、细胞增殖以及c-Fos mRNA的表达。相比之下,PD184352并未改变PRL对c-Myc mRNA表达的激活作用,也未改变对p70核糖体蛋白S6激酶(p70S6K)、蛋白激酶B(Akt)和Jak2/信号转导及转录激活因子5(Stat5)途径的刺激。PRL对磷脂酰肌醇-3激酶(PI3K)的激活对于c-Myc mRNA的表达和W53细胞增殖是必需的,因为PI3K抑制剂LY294002可消除这些作用。然而,它并未改变PRL对c-Fos mRNA表达的刺激作用,也未改变对Erk1/2和Stat5的激活作用。此外,雷帕霉素是一种哺乳动物雷帕霉素靶蛋白(mTOR)抑制剂,因此也是p70S6K的抑制剂,它并未改变PRL对c-Myc和c-Fos mRNA表达的刺激作用,并且对PRL刺激W53细胞增殖的抑制作用非常小。此外,雷帕霉素并不影响PRL对Akt或Stat5的刺激作用。然而,它增强了PRL对Erk1/2的激活作用。在W53细胞中过表达组成型激活的Akt(肉豆蔻酰化Akt)可克服LY294002对c-Myc表达的抑制作用,以及PRL剥夺后的细胞死亡。同样,在W53细胞中诱导表达Akt-CAAX盒可导致c-Myc表达受到抑制。PRL刺激W53细胞导致Akt转位至细胞核、叉头框蛋白O1(FKHRL1)转录因子磷酸化并使其核输出。相比之下,诱导表达Akt-CAAX盒可导致FKHRL1磷酸化受到抑制。此外,不可磷酸化的FKHRL1-A3突变体的瞬时表达会损害PRL诱导的c-Myc启动子激活。Akt激活还导致糖原合成酶激酶3(GSK3)磷酸化并受到抑制,这反过来又促进了c-Myc的稳定性。同样,用GSK3的选择性抑制剂如SB415286和锂盐处理W53细胞会导致c-Myc水平升高。此外,在W53细胞中过表达c-Myc可克服LYS294002诱导的细胞增殖减少。这些发现确定了W53细胞中的一种PRL信号级联反应,涉及Src激酶/PI3K/Akt/FKHRL1-GSK3,该级联反应介导对c-Myc表达的刺激。