RNA-binding protein QKI-5 inhibits the proliferation of clear cell renal cell carcinoma via post-transcriptional stabilization of RASA1 mRNA

References

• Znaor A, Lortet-Tieulent J, Laversanne M, Jemal A, Bray F. International variations and trends in renal cell carcinoma incidence and mortality. Eur Urol 2015; 67(3):519-30; PMID:25449206; http://dx.doi.org/10.1016/j.eururo.2014.10.002
   PubMed Web of Science ®Google Scholar
• Linehan WM, Srinivasan R, Schmidt LS. The genetic basis of kidney cancer: a metabolic disease. Nat Rev Urol 2010; 7(5):277-85; PMID:20448661; http://dx.doi.org/10.1038/nrurol.2010.47
   PubMed Web of Science ®Google Scholar
• Qian CN. Hijacking the vasculature in ccRCC–co-option, remodelling and angiogenesis. Nat Rev Urol 2013; 10(5):300-4; PMID:23459032; http://dx.doi.org/10.1038/nrurol.2013.26
   PubMed Web of Science ®Google Scholar
• Qian CN, Tan MH, Yang JP, Cao Y. Revisiting tumor angiogenesis: vessel co-option, vessel remodeling, and cancer cell-derived vasculature formation. Chinese J Cancer 2016; 35(1):10.
   PubMed Web of Science ®Google Scholar
• Zhang ZL, Li YH, Xiong YH, Hou GL, Yao K, Dong P, Liu ZW, Han H, Qin ZK, Zhou FJ. Oncological outcome of surgical treatment in 336 patients with renal cell carcinoma. Chinese J Cancer 2010; 29(12):995-9; PMID:21114919; http://dx.doi.org/10.5732/cjc.010.10383
   PubMedGoogle Scholar
• Huang D, Ding Y, Luo WM, Bender S, Qian CN, Kort E, Zhang ZF, VandenBeldt K, Duesbery NS, Resau JH, et al. Inhibition of MAPK kinase signaling pathways suppressed renal cell carcinoma growth and angiogenesis in vivo. Cancer Res 2008; 68(1):81-88; PMID:18172299; http://dx.doi.org/10.1158/0008-5472.CAN-07-5311
   PubMed Web of Science ®Google Scholar
• Liang YY, Zheng LS, Wu YZ, Peng LX, Cao Y, Cao X, Xie P, Huang BJ, Qian CN. RASSF6 promotes p21(Cip1/Waf1)-dependent cell cycle arrest and apoptosis through activation of the JNK/SAPK pathway in clear cell renal cell carcinoma. Cell Cycle 2014; 13(9):1440-9; PMID:24626183; http://dx.doi.org/10.4161/cc.28416
   PubMed Web of Science ®Google Scholar
• Liu Y, Zhang M, Qian J, Bao M, Meng X, Zhang S, Zhang L, Zhao R, Li S, Cao Q, et al. miR-134 functions as a tumor suppressor in cell proliferation and epithelial-to-mesenchymal Transition by targeting KRAS in renal cell carcinoma cells. DNA Cell Biol 2015; 34(6):429-36; PMID:25811077; http://dx.doi.org/10.1089/dna.2014.2629
   PubMed Web of Science ®Google Scholar
• Salinas-Sanchez AS, Gimenez-Bachs JM, Serrano-Oviedo L, Nam Cha S, Sanchez-Prieto R. Role of mitogen-activated protein kinase (MAPK) in the sporadic renal cell carcinoma. Actas Urologicas Espanolas 2012; 36(2):99-103; PMID:21959062
   PubMed Web of Science ®Google Scholar
• Bos JL, Rehmann H, Wittinghofer A. GEFs and GAPs: critical elements in the control of small G proteins. Cell 2007; 129(5):865-77; PMID:17540168; http://dx.doi.org/10.1016/j.cell.2007.05.018
   PubMed Web of Science ®Google Scholar
• Kolfschoten IG, van Leeuwen B, Berns K, Mullenders J, Beijersbergen RL, Bernards R, Voorhoeve PM, Agami R. A genetic screen identifies PITX1 as a suppressor of RAS activity and tumorigenicity. Cell 2005; 121(6):849-58; PMID:15960973; http://dx.doi.org/10.1016/j.cell.2005.04.017
   PubMed Web of Science ®Google Scholar
• Ohta M, Seto M, Ijichi H, Miyabayashi K, Kudo Y, Mohri D, Asaoka Y, Tada M, Tanaka Y, Ikenoue T, et al. Decreased expression of the RAS-GTPase activating protein RASAL1 is associated with colorectal tumor progression. Gastroenterology 2009; 136(1):206-16; PMID:18992247; http://dx.doi.org/10.1053/j.gastro.2008.09.063
   PubMed Web of Science ®Google Scholar
• McLaughlin SK, Olsen SN, Dake B, De Raedt T, Lim E, Bronson RT, Beroukhim R, Polyak K, Brown M, Kuperwasser C, et al. The RasGAP gene, RASAL2, is a tumor and metastasis suppressor. Cancer Cell 2013; 24(3):365-78; PMID:24029233; http://dx.doi.org/10.1016/j.ccr.2013.08.004
   PubMed Web of Science ®Google Scholar
• Yang XY, Guan M, Vigil D, Der CJ, Lowy DR, Popescu NC. p120Ras-GAP binds the DLC1 Rho-GAP tumor suppressor protein and inhibits its RhoA GTPase and growth-suppressing activities. Oncogene 2009; 28(11):1401-9; PMID:19151751; http://dx.doi.org/10.1038/onc.2008.498
   PubMed Web of Science ®Google Scholar
• Calvisi DF, Ladu S, Conner EA, Seo D, Hsieh JT, Factor VM, Thorgeirsson SS. Inactivation of Ras GTPase-activating proteins promotes unrestrained activity of wild-type Ras in human liver cancer. J Hepatol 2011; 54(2):311-9; PMID:21067840; http://dx.doi.org/10.1016/j.jhep.2010.06.036
   PubMed Web of Science ®Google Scholar
• Mai A, Veltel S, Pellinen T, Padzik A, Coffey E, Marjomaki V, Ivaska J. Competitive binding of Rab21 and p120RasGAP to integrins regulates receptor traffic and migration. J Cell Biol 2011; 194(2):291-306; PMID:21768288; http://dx.doi.org/10.1083/jcb.201012126
   PubMed Web of Science ®Google Scholar
• Sun D, Yu F, Ma Y, Zhao R, Chen X, Zhu J, Zhang CY, Chen J, Zhang J. MicroRNA-31 activates the RAS pathway and functions as an oncogenic MicroRNA in human colorectal cancer by repressing RAS p21 GTPase activating protein 1 (RASA1). J Biol Chem 2013; 288(13):9508-18; PMID:23322774; http://dx.doi.org/10.1074/jbc.M112.367763
   PubMed Web of Science ®Google Scholar
• Anand S, Majeti BK, Acevedo LM, Murphy EA, Mukthavaram R, Scheppke L, Huang M, Shields DJ, Lindquist JN, Lapinski PE, et al. MicroRNA-132-mediated loss of p120RasGAP activates the endothelium to facilitate pathological angiogenesis. Nat Med 2010; 16(8):909-14; PMID:20676106; http://dx.doi.org/10.1038/nm.2186
   PubMed Web of Science ®Google Scholar
• Organ SL, Hai J, Radulovich N, Marshall CB, Leung L, Sasazuki T, Shirasawa S, Zhu CQ, Navab R, Ikura M, et al. p120RasGAP is a mediator of rho pathway activation and tumorigenicity in the DLD1 colorectal cancer cell line. PloS One 2014; 9(1):e86103; PMID:24465899; http://dx.doi.org/10.1371/journal.pone.0086103
   PubMed Web of Science ®Google Scholar
• Sharma SB, Lin CC, Farrugia MK, McLaughlin SL, Ellis EJ, Brundage KM, Salkeni MA, Ruppert JM. MicroRNAs 206 and 21 cooperate to promote RAS-extracellular signal-regulated kinase signaling by suppressing the translation of RASA1 and SPRED1. Mol Cell Biol 2014; 34(22):4143-64; PMID:25202123; http://dx.doi.org/10.1128/MCB.00480-14
   PubMed Web of Science ®Google Scholar
• Liu Y, Liu T, Sun Q, Niu M, Jiang Y, Pang D. Downregulation of Ras GTPaseactivating protein 1 is associated with poor survival of breast invasive ductal carcinoma patients. Oncol Rep 2015; 33(1):119-24; PMID:25394563
   PubMed Web of Science ®Google Scholar
• Li Z, Li D, Zhang G, Xiong J, Jie Z, Cheng H, Cao Y, Jiang M, Lin L, Le Z, et al. Methylation-associated silencing of MicroRNA-335 contributes tumor cell invasion and migration by interacting with RASA1 in gastric cancer. Am J Cancer Res 2014; 4(6):648-62; PMID:25520857
   PubMed Web of Science ®Google Scholar
• Cancer Genome Atlas Research N. Comprehensive molecular characterization of clear cell renal cell carcinoma. Nature 2013; 499(7456):43-9; PMID:23792563; http://dx.doi.org/10.1038/nature12222
   PubMed Web of Science ®Google Scholar
• Galarneau A, Richard S. Target RNA motif and target mRNAs of the Quaking STAR protein. Nat Structural Mol Biol 2005; 12(8):691-8; PMID:16041388; http://dx.doi.org/10.1038/nsmb963
   PubMed Web of Science ®Google Scholar
• Chenard CA, Richard S. New implications for the QUAKING RNA binding protein in human disease. J Neurosci Res 2008; 86(2):233-42; PMID:17787018; http://dx.doi.org/10.1002/jnr.21485
   PubMed Web of Science ®Google Scholar
• Biedermann B, Hotz HR, Ciosk R. The Quaking family of RNA-binding proteins: coordinators of the cell cycle and differentiation. Cell Cycle 2010; 9(10):1929-33; PMID:20495365; http://dx.doi.org/10.4161/cc.9.10.11533
   PubMed Web of Science ®Google Scholar
• Hafner M, Landthaler M, Burger L, Khorshid M, Hausser J, Berninger P, Rothballer A, Ascano M, Jr, Jungkamp AC, Munschauer M, et al. Transcriptome-wide identification of RNA-binding protein and microRNA target sites by PAR-CLIP. Cell 2010; 141(1):129-41; PMID:20371350; http://dx.doi.org/10.1016/j.cell.2010.03.009
   PubMed Web of Science ®Google Scholar
• Darbelli L, Richard S. Emerging functions of the Quaking RNA-binding proteins and link to human diseases. Wiley Interdisciplinary Rev RNA 2016; 7(3):399-412.
   PubMed Web of Science ®Google Scholar
• Bandopadhayay P, Ramkissoon LA, Jain P, Bergthold G, Wala J, Zeid R, Schumacher SE, Urbanski L, O'Rourke R, Gibson WJ, et al. MYB-QKI rearrangements in angiocentric glioma drive tumorigenicity through a tripartite mechanism. Nature Genetics 2016; 48(3):273-82; PMID:26829751
   PubMed Web of Science ®Google Scholar
• Chen AJ, Paik JH, Zhang H, Shukla SA, Mortensen R, Hu J, Ying H, Hu B, Hurt J, Farny N, et al. STAR RNA-binding protein Quaking suppresses cancer via stabilization of specific miRNA. Genes Dev 2012; 26(13):1459-72; PMID:22751500; http://dx.doi.org/10.1101/gad.189001.112
   PubMed Web of Science ®Google Scholar
• Zhao Y, Zhang G, Wei M, Lu X, Fu H, Feng F, Wang S, Lu W, Wu N, Lu Z, et al. The tumor suppressing effects of QKI-5 in prostate cancer: a novel diagnostic and prognostic protein. Cancer Biol Ther 2014; 15(1):108-8; PMID:24153116; http://dx.doi.org/10.4161/cbt.26722
   PubMed Web of Science ®Google Scholar
• Yang G, Fu H, Zhang J, Lu X, Yu F, Jin L, Bai L, Huang B, Shen L, Feng Y, et al. RNA-binding protein quaking, a critical regulator of colon epithelial differentiation and a suppressor of colon cancer. Gastroenterology 2010; 138(1):231-40 e231-235; http://dx.doi.org/10.1053/j.gastro.2009.08.001
   PubMed Web of Science ®Google Scholar
• Zong FY, Fu X, Wei WJ, Luo YG, Heiner M, Cao LJ, Fang Z, Fang R, Lu D, Ji H, et al. The RNA-binding protein QKI suppresses cancer-associated aberrant splicing. PLoS Genetics 2014; 10(4):e1004289; PMID:24722255; http://dx.doi.org/10.1371/journal.pgen.1004289
   PubMed Web of Science ®Google Scholar
• Bian Y, Wang L, Lu H, Yang G, Zhang Z, Fu H, Lu X, Wei M, Sun J, Zhao Q, et al. Downregulation of tumor suppressor QKI in gastric cancer and its implication in cancer prognosis. Biochem Biophys Res Commun 2012; 422(1):187-93; PMID:22569043; http://dx.doi.org/10.1016/j.bbrc.2012.04.138
   PubMed Web of Science ®Google Scholar
• Pilotte J, Larocque D, Richard S. Nuclear translocation controlled by alternatively spliced isoforms inactivates the QUAKING apoptotic inducer. Genes Dev 2001; 15(7):845-58; PMID:11297509; http://dx.doi.org/10.1101/gad.860301
   PubMed Web of Science ®Google Scholar
• Wang L, Ma L, Wang X, Li B, Guo S, Qiao Q. Therapeutic effects and associated adverse events of first-line treatments of advanced renal cell carcinoma (RCC): a meta-analysis. Int Urol Nephrol 2015; 47(4):617-24; PMID:25686740; http://dx.doi.org/10.1007/s11255-015-0932-1
   PubMed Web of Science ®Google Scholar
• Gudas LJ, Fu L, Minton DR, Mongan NP, Nanus DM. The role of HIF1alpha in renal cell carcinoma tumorigenesis. J Mol Med 2014; 92(8):825-36; PMID:24916472; http://dx.doi.org/10.1007/s00109-014-1180-z
   PubMed Web of Science ®Google Scholar
• Novikov L, Park JW, Chen H, Klerman H, Jalloh AS, Gamble MJ. QKI-mediated alternative splicing of the histone variant MacroH2A1 regulates cancer cell proliferation. Mol Cell Biol 2011; 31(20):4244-55; PMID:21844227; http://dx.doi.org/10.1128/MCB.05244-11
   PubMed Web of Science ®Google Scholar
• Teplova M, Hafner M, Teplov D, Essig K, Tuschl T, Patel DJ. Structure-function studies of STAR family Quaking proteins bound to their in vivo RNA target sites. Genes Dev 2013; 27(8):928-40; http://dx.doi.org/10.1101/gad.216531.113
   PubMed Web of Science ®Google Scholar
• Donovan S, Shannon KM, Bollag G. GTPase activating proteins: critical regulators of intracellular signaling. Biochim Et Biophys Acta 2002; 1602(1):23-45; PMID:11960693
   PubMed Web of Science ®Google Scholar
• Buday L, Downward J. Many faces of Ras activation. Biochim Et Biophys Acta 2008; 1786(2):178-87; PMID:18541156
   PubMed Web of Science ®Google Scholar
• Yang G, Lu X, Wang L, Bian Y, Fu H, Wei M, Pu J, Jin L, Yao L, Lu Z. E2F1 and RNA binding protein QKI comprise a negative feedback in the cell cycle regulation. Cell Cycle 2014; 10(16):2703-13; http://dx.doi.org/10.4161/cc.10.16.15928
   Web of Science ®Google Scholar
• Fu X, Feng Y. QKI-5 suppresses cyclin D1 expression and proliferation of oral squamous cell carcinoma cells via MAPK signalling pathway. Int J Oral Maxillofacial Surg 2015; 44(5):562-7; PMID:25457822; http://dx.doi.org/10.1016/j.ijom.2014.10.001
   PubMed Web of Science ®Google Scholar
• Li XJ, Peng LX, Shao JY, Lu WH, Zhang JX, Chen S, Chen ZY, Xiang YQ, Bao YN, Zheng FJ, et al. As an independent unfavorable prognostic factor, IL-8 promotes metastasis of nasopharyngeal carcinoma through induction of epithelial-mesenchymal transition and activation of AKT signaling. Carcinogenesis 2012; 33(7):1302-9; PMID:22610073; http://dx.doi.org/10.1093/carcin/bgs181
   PubMed Web of Science ®Google Scholar
• Luo LL, Zhao L, Xi M, He LR, Shen JX, Li QQ, Liu SL, Zhang P, Xie D, Liu MZ. Association of insulin-like growth factor-binding protein-3 with radiotherapy response and prognosis of esophageal squamous cell carcinoma. Chinese J Cancer 2015; 34(11):514-21; PMID:26370590
   PubMedGoogle Scholar