Center for Excellence in Post-Harvest Technologies, North Carolina Agricultural and Technical State University, North Carolina Research Campus, 500 Laureate Way, Kannapolis, North Carolina 28081, USA.
Chem Res Toxicol. 2013 Jun 17;26(6):976-85. doi: 10.1021/tx4001286. Epub 2013 May 15.
Shogaols, a series of major constituents in dried ginger (Zingiber officinale), show high anticancer potencies. Previously, we reported that a major metabolite resulting from the mercapturic acid pathway, 5-cysteinyl-[6]-shogaol (M2), showed comparable growth inhibitory effects toward cancer cells to [6]-shogaol (6S). Here, we probe the mechanism by which M2 exerts its bioactivity. We utilized a series of chemical stability tests in conjunction with bioassays to show that thiol-conjugates display chemopreventative potency by acting as carriers of active ginger component 6S. M2 chemical degradation to 6S was observed in an environment most resembling physiological conditions, with a pH of 7.4 at 37 °C. The metabolic profiles of M2 in cancer cells HCT-116 and H-1299 resembled those of 6S, indicating that its biotransformation route was initiated by deconjugation. Further, the presence of excess glutathione significantly delayed 6S and M2 metabolism and counteracted cell death induced by 6S and M2, suggesting that increasing available free thiols exogenously both promoted the formation of 5-glutathionyl-[6]-shogaol (M13) and inhibited the production of free 6S from M2 deconjugation, resulting in delayed 6S cell entry and bioactivity. Given the chemopreventative properties of M2 and our observations in vitro, we investigated its metabolism in mice. M2 and 6S showed similar metabolic profiles in mouse urine and fecal samples. Six new thiol-conjugated metabolites (M16-M21), together with previously reported ones, were identified by LC/MS. In particular, the increase of 5-N-acetylcystenyl-[6]-shogaol (M5) and its 3'-demethylated product (M16) abundance in mouse feces after treatment with M2 indicates that in addition to acting as a carrier of 6S, M2 is also directly acetylated to M5, which is further demethylated to M16 in vivo. In conclusion, the cysteine-conjugated metabolite of [6]-shogaol M2 exerts its bioactivity by acting as a carrier of 6S in both cancer cells and in mice.
姜辣素是干姜(Zingiber officinale)中的主要成分之一,具有很强的抗癌活性。之前,我们报道了一种主要的代谢产物,即通过硫醚氨酸途径生成的 5-半胱氨酸-[6]-姜辣素(M2),对癌细胞的生长抑制作用与 [6]-姜辣素(6S)相当。在这里,我们探究了 M2 发挥其生物活性的机制。我们利用一系列化学稳定性测试与生物测定相结合,表明硫醚结合物通过充当活性姜成分 6S 的载体来发挥化学预防作用。在最接近生理条件的环境中,即 pH 值为 7.4、37°C 的条件下,观察到 M2 化学降解为 6S。M2 在癌细胞 HCT-116 和 H-1299 中的代谢谱与 6S 相似,表明其生物转化途径是由去结合引发的。此外,过量谷胱甘肽的存在显著延迟了 6S 和 M2 的代谢,并抵消了 6S 和 M2 诱导的细胞死亡,这表明外源性增加可用游离巯基既促进了 5-谷胱甘肽基-[6]-姜辣素(M13)的形成,又抑制了 M2 去结合产生游离 6S,从而延迟了 6S 进入细胞并发挥生物活性。鉴于 M2 的化学预防特性以及我们在体外的观察结果,我们研究了其在小鼠体内的代谢情况。M2 和 6S 在小鼠尿液和粪便样本中的代谢谱相似。通过 LC/MS 鉴定出 6 种新的硫醚结合代谢物(M16-M21),以及之前报道的代谢物。特别是 M2 处理后,小鼠粪便中 5-N-乙酰半胱氨酸基-[6]-姜辣素(M5)及其 3'-去甲基产物(M16)的含量增加,表明 M2 不仅可以作为 6S 的载体,还可以直接乙酰化为 M5,然后在体内进一步去甲基化为 M16。总之,[6]-姜辣素 M2 的半胱氨酸结合代谢物通过在癌细胞和小鼠中充当 6S 的载体发挥其生物活性。