Griesmann Heidi, Mühl Sebastian, Riedel Jan, Theuerkorn Katharina, Sipos Bence, Esposito Irene, Vanden Heuvel Gregory B, Michl Patrick
Department of Internal Medicine I, Martin Luther University Halle-Wittenberg, D06120 Halle/Saale, Germany.
Department of Gastroenterology, Endocrinology and Metabolism, Philipps University Marburg, D35043 Marburg, Germany.
Cancers (Basel). 2021 May 18;13(10):2462. doi: 10.3390/cancers13102462.
The transcription factor CUX1 has been implicated in either tumor suppression or progression, depending on the cancer entity and the prevalent CUX1 isoform. Previously, we could show that CUX1 acts as an important mediator of tumor cell proliferation and resistance to apoptosis in pancreatic cancer cell lines. However, in vivo evidence for its impact on pancreatic carcinogenesis, isoform-specific effects and downstream signaling cascades are missing. We crossbred two different CUX1 isoform mouse models (p200 CUX1 and p110 CUX1) with KC (KrasLSL-G12D/+; Ptf1aCre/+) mice, a genetic model for pancreatic precursor lesions (PanIN). In the context of oncogenic KRASs, both mice KCCux1p200 and KCCux1p110 led to increased PanIN formation and development of invasive pancreatic ductal adenocarcinomata (PDAC). In KCCux1p110 mice, tumor development was dramatically more accelerated, leading to formation of invasive PDAC within 4 weeks. In vitro and in vivo, we could show that CUX1 enhanced proliferation by activating MEK-ERK signaling via an upstream increase of ADAM17 protein, which in turn led to an activation of EGFR. Additionally, CUX1 further enhanced MEK-ERK activation through upregulation of the serine/threonine kinase MOS, phosphorylating MEK in a KRAS-independent manner. We identified p110 CUX1 as major driver of pancreatic cancer formation in the context of mutant KRAS. These results provide the first in vivo evidence for the importance of CUX1 in the development of pancreatic cancer, and highlight the importance of CUX1-dependent signaling pathways as potential therapeutic targets.
转录因子CUX1与肿瘤抑制或进展有关,具体取决于癌症类型和普遍存在的CUX1亚型。此前,我们发现CUX1在胰腺癌细胞系中是肿瘤细胞增殖和抗凋亡的重要调节因子。然而,关于其对胰腺癌发生、亚型特异性效应和下游信号级联反应影响的体内证据尚缺失。我们将两种不同的CUX1亚型小鼠模型(p200 CUX1和p110 CUX1)与KC(KrasLSL-G12D/+; Ptf1aCre/+)小鼠杂交,KC小鼠是胰腺前驱病变(胰腺上皮内瘤变,PanIN)的遗传模型。在致癌KRAS的背景下,KCCux1p200和KCCux1p110小鼠均导致PanIN形成增加和侵袭性胰腺导管腺癌(PDAC)的发展。在KCCux1p110小鼠中,肿瘤发展显著加速,在4周内形成侵袭性PDAC。在体外和体内,我们发现CUX1通过上游增加ADAM17蛋白激活MEK-ERK信号,从而增强增殖,这反过来又导致EGFR激活。此外,CUX1通过上调丝氨酸/苏氨酸激酶MOS进一步增强MEK-ERK激活,以KRAS非依赖的方式磷酸化MEK。我们确定p110 CUX1是突变KRAS背景下胰腺癌形成的主要驱动因素。这些结果首次提供了体内证据,证明CUX1在胰腺癌发展中的重要性,并强调了CUX1依赖性信号通路作为潜在治疗靶点的重要性。