Institute of Genomic Medicine, College of Pharmacy, Jinan University, Guangzhou, 510632, China.
State Key Laboratory of Bioactive Molecules and Druggability Assessment, Jinan University, Guangzhou, 510632, China.
Acta Pharmacol Sin. 2023 Nov;44(11):2307-2321. doi: 10.1038/s41401-023-01116-4. Epub 2023 Jul 4.
Breast cancer is one of the most common malignant tumors with high mortality due to metastases. SCRIB, a scaffold protein mainly distributed in the cell membrane, is a potential tumor suppressor. Mislocalization and aberrant expression of SCRIB stimulate the EMT pathway and promote tumor cell metastasis. SCRIB has two isoforms (with or without exon 16) produced by alternative splicing. In this study we investigated the function of SCRIB isoforms in breast cancer metastasis and their regulatory mechanisms. We showed that in contrast to the full-length isoform (SCRIB-L), the truncated SCRIB isoform (SCRIB-S) was overexpressed in highly metastatic MDA-MB-231 cells that promoted breast cancer metastasis through activation of the ERK pathway. The affinity of SCRIB-S for the catalytic phosphatase subunit PPP1CA was lower than that of SCRIB-L and such difference might contribute to the different function of the two isoforms in cancer metastasis. By conducting CLIP, RIP and MS2-GFP-based experiments, we revealed that the heterogeneous nuclear ribonucleoprotein A1 (hnRNP A1) promoted SCRIB exon 16 skipping by binding to the "AG"-rich sequence "caggauggaggccccccgugccgag" on intron 15 of SCRIB. Transfection of MDA-MB-231 cells with a SCRIB antisense oligodeoxynucleotide (ASO-SCRIB) designed on the basis of this binding sequence, not only effectively inhibited the binding of hnRNP A1 to SCRIB pre-mRNA and suppressed the production of SCRIB-S, but also reversed the activation of the ERK pathway by hnRNP A1 and inhibited the metastasis of breast cancer. This study provides a new potential target and a candidate drug for treating breast cancer.
乳腺癌是一种常见的恶性肿瘤,由于转移导致死亡率较高。SCRIB 是一种主要分布在细胞膜上的支架蛋白,是一种潜在的肿瘤抑制因子。SCRIB 的定位错误和异常表达会刺激 EMT 通路,促进肿瘤细胞转移。SCRIB 有两种剪接异构体(含外显子 16 和不含外显子 16)。在本研究中,我们研究了 SCRIB 异构体在乳腺癌转移中的功能及其调控机制。我们发现,与全长异构体(SCRIB-L)相比,在高转移性 MDA-MB-231 细胞中截短的 SCRIB 异构体(SCRIB-S)过表达,通过激活 ERK 通路促进乳腺癌转移。SCRIB-S 与催化磷酸酶亚基 PPP1CA 的亲和力低于 SCRIB-L,这种差异可能导致两种异构体在癌症转移中的功能不同。通过进行 CLIP、RIP 和基于 MS2-GFP 的实验,我们揭示了异质核核糖核蛋白 A1(hnRNP A1)通过与 SCRIB 内含子 15 上的“AG”-富含序列“caggauggaggccccccgugccgag”结合,促进 SCRIB 外显子 16 跳跃。根据该结合序列设计的 SCRIB 反义寡核苷酸(ASO-SCRIB)转染 MDA-MB-231 细胞,不仅有效抑制了 hnRNP A1 与 SCRIB 前体 mRNA 的结合,抑制了 SCRIB-S 的产生,而且逆转了 hnRNP A1 对 ERK 通路的激活,抑制了乳腺癌的转移。本研究为治疗乳腺癌提供了一个新的潜在靶点和候选药物。