Seaman J E, Julien O, Lee P S, Rettenmaier T J, Thomsen N D, Wells J A
Department of Pharmaceutical Chemistry and Cellular and Molecular Pharmacology, University of California, San Francisco, CA, USA.
Cell Death Differ. 2016 Oct;23(10):1717-26. doi: 10.1038/cdd.2016.62. Epub 2016 Jul 1.
Caspases are a family of proteases found in all metazoans, including a dozen in humans, that drive the terminal stages of apoptosis as well as other cellular remodeling and inflammatory events. Caspases are named because they are cysteine class enzymes shown to cleave after aspartate residues. In the past decade, we and others have developed unbiased proteomic methods that collectively identified ~2000 native proteins cleaved during apoptosis after the signature aspartate residues. Here, we explore non-aspartate cleavage events and identify 100s of substrates cleaved after glutamate in both human and murine apoptotic samples. The extended consensus sequence patterns are virtually identical for the aspartate and glutamate cleavage sites suggesting they are cleaved by the same caspases. Detailed kinetic analyses of the dominant apoptotic executioner caspases-3 and -7 show that synthetic substrates containing DEVD↓ are cleaved only twofold faster than DEVE↓, which is well within the 500-fold range of rates that natural proteins are cut. X-ray crystallography studies confirm that the two acidic substrates bind in virtually the same way to either caspases-3 or -7 with minimal adjustments to accommodate the larger glutamate. Lastly, during apoptosis we found 121 proteins cleaved after serine residues that have been previously annotated to be phosphorylation sites. We found that caspase-3, but not caspase-7, can cleave peptides containing DEVpS↓ at only threefold slower rate than DEVD↓, but does not cleave the unphosphorylated serine peptide. There are only a handful of previously reported examples of proteins cleaved after glutamate and none after phosphorserine. Our studies reveal a much greater promiscuity for cleaving after acidic residues and the name 'cacidase' could aptly reflect this broader specificity.
半胱天冬酶是一类在所有后生动物中都能找到的蛋白酶家族,人类中有十几种,它们驱动细胞凋亡的终末阶段以及其他细胞重塑和炎症事件。半胱天冬酶之所以得名,是因为它们是半胱氨酸类酶,显示在天冬氨酸残基之后进行切割。在过去十年中,我们和其他人开发了无偏向性蛋白质组学方法,这些方法共同鉴定出约2000种在凋亡过程中在标志性天冬氨酸残基之后被切割的天然蛋白质。在这里,我们探索非天冬氨酸切割事件,并在人和小鼠凋亡样本中鉴定出数百种在谷氨酸之后被切割的底物。天冬氨酸和谷氨酸切割位点的扩展共有序列模式几乎相同,这表明它们是由相同的半胱天冬酶切割的。对主要的凋亡执行者半胱天冬酶-3和-7的详细动力学分析表明,含有DEVD↓的合成底物的切割速度仅比DEVE↓快两倍,这完全在天然蛋白质切割速度的500倍范围内。X射线晶体学研究证实,这两种酸性底物以几乎相同的方式与半胱天冬酶-3或-7结合,只需进行最小的调整以容纳更大的谷氨酸。最后,在细胞凋亡过程中,我们发现121种蛋白质在丝氨酸残基之后被切割,这些丝氨酸残基先前已被注释为磷酸化位点。我们发现半胱天冬酶-3而非半胱天冬酶-7能够切割含有DEVpS↓的肽段,其速度仅比DEVD↓慢三倍,但不能切割未磷酸化的丝氨酸肽段。以前报道的在谷氨酸之后被切割的蛋白质例子很少,在磷酸化丝氨酸之后被切割的则没有。我们的研究揭示了在酸性残基之后进行切割的更大的混杂性,“cacidase”这个名字可以恰当地反映这种更广泛的特异性。