Université Nice Sophia Antipolis, CNRS-UMR 7275, Institut de Pharmacologie Moléculaire et Cellulaire, Sophia Antipolis, Valbonne, France.
Mol Cancer Res. 2012 Nov;10(11):1496-508. doi: 10.1158/1541-7786.MCR-11-0578. Epub 2012 Jul 2.
Most anticancer drugs fail to eradicate tumors, leading to the development of drug resistance and disease recurrence. The Hedgehog signaling plays a crucial role during embryonic development, but is also involved in cancer development, progression, and metastasis. The Hedgehog receptor Patched (Ptc) is a Hedgehog signaling target gene that is overexpressed in many cancer cells. Here, we show a link between Ptc and resistance to chemotherapy, and provide new insight into Ptc function. Ptc is cleared from the plasma membrane upon interaction with its ligand Hedgehog, or upon treatment of cells with the Hedgehog signaling antagonist cyclopamine. In both cases, after incubation of cells with doxorubicin, a chemotherapeutic agent that is used for the clinical management of recurrent cancers, we observed an inhibition of the efflux of doxorubicin from Hedgehog-responding fibroblasts, and an increase of doxorubicin accumulation in two different cancer cell lines that are known to express aberrant levels of Hedgehog signaling components. Using heterologous expression system, we stringently showed that the expression of human Ptc conferred resistance to growth inhibition by several drugs from which chemotherapeutic agents such as doxorubicin, methotrexate, temozolomide, and 5-fluorouracil. Resistance to doxorubicin correlated with Ptc function, as shown using mutations from Gorlin's syndrome patients in which the Ptc-mediated effect on Hedgehog signaling is lost. Our results show that Ptc is involved in drug efflux and multidrug resistance, and suggest that Ptc contributes to chemotherapy resistance of cancer cells.
大多数抗癌药物都无法彻底消除肿瘤,导致耐药性的产生和疾病的复发。Hedgehog 信号通路在胚胎发育过程中起着至关重要的作用,但也与癌症的发生、发展和转移有关。Hedgehog 受体 Patched(Ptc)是 Hedgehog 信号通路的靶基因,在许多癌细胞中过度表达。在这里,我们发现 Ptc 与化疗耐药性之间存在关联,并为 Ptc 功能提供了新的见解。Ptc 在与配体 Hedgehog 相互作用或用 Hedgehog 信号通路拮抗剂环巴胺处理细胞时,会从质膜上清除。在这两种情况下,在用多柔比星(一种用于治疗复发性癌症的临床管理的化疗药物)孵育细胞后,我们观察到 Hedgehog 反应性成纤维细胞中多柔比星的外排被抑制,并且两种不同的癌细胞系中多柔比星的积累增加,这两种癌细胞系已知表达异常水平的 Hedgehog 信号通路成分。使用异源表达系统,我们严格证明了人 Ptc 的表达赋予了对几种药物的生长抑制的耐药性,其中包括多柔比星、甲氨蝶呤、替莫唑胺和 5-氟尿嘧啶等化疗药物。多柔比星耐药性与 Ptc 功能相关,如 Gorlin 综合征患者中的突变所示,其中 Ptc 介导的 Hedgehog 信号通路的作用丧失。我们的结果表明 Ptc 参与药物外排和多药耐药性,并提示 Ptc 有助于癌细胞的化疗耐药性。