Schultz Michelle A, Diaz Andrew M, Smite Sharon, Lay Anna R, DeCant Brian, McKinney Ronald, Mascarinas Windel E, Xia Yinglin, Neumann Carola, Bentrem David, Dawson David W, Grippo Paul J
Division of Gastroenterology, Department of Medicine, University of Illinois-Chicago, Chicago IL 60612, USA.
Department of Surgery, Northwestern University Feinberg School of Medicine, Chicago IL 60611, USA.
Oncotarget. 2017 Oct 4;8(54):92667-92681. doi: 10.18632/oncotarget.21539. eCollection 2017 Nov 3.
Peroxiredoxin-1 (Prdx1), a member of the thioredoxin (Txn) system, is overexpressed and correlates with poor prognosis in pancreatic cancer patients and can suppress Kras signaling through redox-mediated inhibition of ERK and AKT in lung and breast cancer. Its redox function is maintained by Txn and sulfiredoxin (Srxn), and its tumor promoting functions are activated by post-translational modification. We studied the role of the Txn system in pancreatic neoplasia and cancer by determining how it regulates the phosphorylation of Kras effectors and by determining its association with patient survival. We found that elevated Prdx1 nuclear localization significantly correlated with better patient survival. Our data also demonstrate that the expression of the Txn system is dysregulated, with elevated Prdx1 expression and significantly decreased Txn and Srxn expression in pancreatic lesions of targeted mutant Kras mouse models. This correlated with distinct differences in the interconversion of Prdx1 oligomers that affect its ability to regulate ERK and AKT phosphorylation. Our data also suggest that Prdx1 post-translational modification and oligomerization suppress Prdx1 mediated redox regulation of ERK phosphorylation. We observed distinct differences in Txn expression and in the ability of pTyr-Prdx1 to bind to pERK in a PanIN model of pancreatic neoplasia as compared to an IPMN model, indicating a distinct difference in the function of post-translationally modified Prdx1 in cells with less Txn expression. Modified Txn system function and post-translational regulation may therefore play a significant role in pancreatic tumorigenesis by altering Kras effector phosphorylation and inhibiting the tumor suppressive redox functions of Prdx1.
过氧化物酶1(Prdx1)是硫氧还蛋白(Txn)系统的成员之一,在胰腺癌患者中过表达且与预后不良相关,在肺癌和乳腺癌中它可通过氧化还原介导的ERK和AKT抑制作用来抑制Kras信号传导。其氧化还原功能由Txn和硫氧还蛋白还原酶(Srxn)维持,其肿瘤促进功能通过翻译后修饰激活。我们通过确定Txn系统如何调节Kras效应子的磷酸化以及其与患者生存的关系,研究了Txn系统在胰腺肿瘤形成和癌症中的作用。我们发现Prdx1核定位升高与患者更好的生存显著相关。我们的数据还表明,在靶向突变Kras小鼠模型的胰腺病变中,Txn系统的表达失调,Prdx1表达升高,而Txn和Srxn表达显著降低。这与Prdx1寡聚体相互转化的明显差异相关,这种差异影响其调节ERK和AKT磷酸化的能力。我们的数据还表明,Prdx1的翻译后修饰和寡聚化抑制了Prdx1介导的ERK磷酸化的氧化还原调节。与胰腺导管内乳头状黏液性肿瘤(IPMN)模型相比,我们在胰腺肿瘤形成的胰腺上皮内瘤变(PanIN)模型中观察到Txn表达以及磷酸化酪氨酸Prdx1与磷酸化ERK结合能力的明显差异,这表明在Txn表达较低的细胞中,翻译后修饰的Prdx1功能存在明显差异。因此,修饰后的Txn系统功能和翻译后调控可能通过改变Kras效应子磷酸化并抑制Prdx1的肿瘤抑制氧化还原功能,在胰腺肿瘤发生中发挥重要作用。