Stuart Scott A, Houel Stephane, Lee Thomas, Wang Nan, Old William M, Ahn Natalie G
From the ‡Department of Chemistry and Biochemistry.
From the ‡Department of Chemistry and Biochemistry, §BioFrontiers Institute, University of Colorado, Boulder, Colorado 80309
Mol Cell Proteomics. 2015 Jun;14(6):1599-615. doi: 10.1074/mcp.M114.047233. Epub 2015 Apr 7.
Inhibitors of oncogenic B-RAF(V600E) and MKK1/2 have yielded remarkable responses in B-RAF(V600E)-positive melanoma patients. However, the efficacy of these inhibitors is limited by the inevitable onset of resistance. Despite the fact that these inhibitors target the same pathway, combination treatment with B-RAF(V600E) and MKK1/2 inhibitors has been shown to improve both response rates and progression-free survival in B-RAF(V600E) melanoma patients. To provide insight into the molecular nature of the combinatorial response, we used quantitative mass spectrometry to characterize the inhibitor-dependent phosphoproteome of human melanoma cells treated with the B-RAF(V600E) inhibitor PLX4032 (vemurafenib) or the MKK1/2 inhibitor AZD6244 (selumetinib). In three replicate experiments, we quantified changes at a total of 23,986 phosphosites on 4784 proteins. This included 1317 phosphosites that reproducibly decreased in response to at least one inhibitor. Phosphosites that responded to both inhibitors grouped into networks that included the nuclear pore complex, growth factor signaling, and transcriptional regulators. Although the majority of phosphosites were responsive to both inhibitors, we identified 16 sites that decreased only in response to PLX4032, suggesting rare instances where oncogenic B-RAF signaling occurs in an MKK1/2-independent manner. Only two phosphosites were identified that appeared to be uniquely responsive to AZD6244. When cells were treated with the combination of AZD6244 and PLX4032 at subsaturating concentrations (30 nm), responses at nearly all phosphosites were additive. We conclude that AZD6244 does not substantially widen the range of phosphosites inhibited by PLX4032 and that the benefit of the drug combination is best explained by their additive effects on suppressing ERK1/2 signaling. Comparison of our results to another recent ERK1/2 phosphoproteomics study revealed a surprising degree of variability in the sensitivity of phosphosites to MKK1/2 inhibitors in human cell lines, revealing unexpected cell specificity in the molecular responses to pathway activation.
致癌性B-RAF(V600E)和MKK1/2抑制剂已在B-RAF(V600E)阳性黑色素瘤患者中产生了显著疗效。然而,这些抑制剂的疗效受到不可避免的耐药性出现的限制。尽管这些抑制剂靶向相同的信号通路,但B-RAF(V600E)和MKK1/2抑制剂联合治疗已显示可提高B-RAF(V600E)黑色素瘤患者的缓解率和无进展生存期。为深入了解联合治疗反应的分子本质,我们使用定量质谱法对用B-RAF(V600E)抑制剂PLX4032(维莫非尼)或MKK1/2抑制剂AZD6244(司美替尼)处理的人黑色素瘤细胞的抑制剂依赖性磷酸化蛋白质组进行了表征。在三个重复实验中,我们对4784种蛋白质上总共23986个磷酸化位点的变化进行了定量。这包括1317个磷酸化位点,它们对至少一种抑制剂有可重复的减少反应。对两种抑制剂都有反应的磷酸化位点聚集在包括核孔复合体、生长因子信号传导和转录调节因子的网络中。尽管大多数磷酸化位点对两种抑制剂都有反应,但我们鉴定出16个仅对PLX4032有反应而减少的位点,表明致癌性B-RAF信号以MKK1/2非依赖性方式发生的罕见情况。仅鉴定出两个似乎对AZD6244有独特反应的磷酸化位点。当细胞用亚饱和浓度(30 nM)的AZD6244和PLX4032联合处理时,几乎所有磷酸化位点的反应都是相加的。我们得出结论,AZD6244不会显著拓宽PLX4032抑制的磷酸化位点范围,药物联合的益处最好通过它们对抑制ERK1/2信号传导的相加作用来解释。将我们的结果与另一项最近的ERK1/2磷酸化蛋白质组学研究进行比较,发现人细胞系中磷酸化位点对MKK1/2抑制剂的敏感性存在惊人程度的变异性,揭示了对信号通路激活的分子反应中意想不到的细胞特异性。