MicroRNA regulation of F-box proteins and its role in cancer

Jin, 2004, Systematic analysis and nomenclature of mammalian F-box proteins, Genes Dev., 18, 2573, 10.1101/gad.1255304 Skaar, 2009, SnapShot: F Box Proteins II, Cell, 137, 1358, 10.1016/j.cell.2009.05.039 Skaar, 2009, SnapShot: F box proteins I, Cell, 137, 1160, 10.1016/j.cell.2009.05.039 Bai, 1996, SKP1 connects cell cycle regulators to the ubiquitin proteolysis machinery through a novel motif, the F-box, Cell, 86, 263, 10.1016/S0092-8674(00)80098-7 Skaar, 2013, Mechanisms and function of substrate recruitment by F-box proteins, Nat. Rev. Mol. Cell Biol., 14, 369, 10.1038/nrm3582 Deshaies, 2009, RING domain E3 ubiquitin ligases, Annu. Rev. Biochem., 78, 399, 10.1146/annurev.biochem.78.101807.093809 Tan, 2013, adaptor capture proteomics reveals a role for SCFFBXL17 in NRF2 activation via BACH1 repressor turnover, Mol. Cell, 52, 9, 10.1016/j.molcel.2013.08.018 Vaites, 2011, The Fbx4 tumor suppressor regulates cyclin D1 accumulation and prevents neoplastic transformation, Mol. Cell. Biol., 31, 4513, 10.1128/MCB.05733-11 Duan, 2012, FBXO11 targets BCL6 for degradation and is inactivated in diffuse large B-cell lymphomas, Nature, 481, 90, 10.1038/nature10688 Santra, 2009, F-box protein FBXO31 mediates cyclin D1 degradation to induce G1 arrest after DNA damage, Nature, 459, 722, 10.1038/nature08011 Wang, 2014, Roles of F-box proteins in cancer, Nat. Rev. Cancer, 14, 233, 10.1038/nrc3700 Crusio, 2010, The ubiquitous nature of cancer: the role of the SCF(Fbw7) complex in development and transformation, Oncogene, 29, 4865, 10.1038/onc.2010.222 Akhoondi, 2007, FBXW7/hCDC4 is a general tumor suppressor in human cancer, Cancer Res., 67, 9006, 10.1158/0008-5472.CAN-07-1320 Maser, 2007, Chromosomally unstable mouse tumours have genomic alterations similar to diverse human cancers, Nature, 447, 966, 10.1038/nature05886 Onoyama, 2007, Conditional inactivation of Fbxw7 impairs cell-cycle exit during T cell differentiation and results in lymphomatogenesis, J. Exp. Med., 204, 2875, 10.1084/jem.20062299 Sancho, 2010, F-box and WD repeat domain-containing 7 regulates intestinal cell lineage commitment and is a haploinsufficient tumor suppressor, Gastroenterology, 139, 929, 10.1053/j.gastro.2010.05.078 Latres, 2001, Role of the F-box protein Skp2 in lymphomagenesis, Proc. Natl. Acad. Sci. U.S.A., 98, 2515, 10.1073/pnas.041475098 Umanskaya, 2007, Skp2B stimulates mammary gland development by inhibiting REA, the repressor of the estrogen receptor, Mol. Cell. Biol., 27, 7615, 10.1128/MCB.01239-07 Shim, 2003, Expression of the F-box protein SKP2 induces hyperplasia, dysplasia, and low-grade carcinoma in the mouse prostate, Cancer Res., 63, 1583 Seki, 2010, Prognostic significance of S-phase kinase-associated protein 2 and p27kip1 in patients with diffuse large B-cell lymphoma: effects of rituximab, Ann. Oncol., 21, 833, 10.1093/annonc/mdp481 Wang, 2012, Skp2: a novel potential therapeutic target for prostate cancer, Biochim. Biophys. Acta, 1825, 11 Rose, 2011, Clinical relevance of SKP2 alterations in metastatic melanoma, Pigm. Cell Melanoma Res., 24, 197, 10.1111/j.1755-148X.2010.00784.x Schuler, 2011, SKP2 confers resistance of pancreatic cancer cells towards TRAIL-induced apoptosis, Int. J. Oncol., 38, 219 Radke, 2005, Differential expression of the F-box proteins Skp2 and Skp2B in breast cancer, Oncogene, 24, 3448, 10.1038/sj.onc.1208328 Winston, 1999, The SCFbeta-TRCP-ubiquitin ligase complex associates specifically with phosphorylated destruction motifs in IkappaBalpha and beta-catenin and stimulates IkappaBalpha ubiquitination in vitro, Genes Dev., 13, 270, 10.1101/gad.13.3.270 Yaron, 1998, Identification of the receptor component of the IkappaBalpha-ubiquitin ligase, Nature, 396, 590, 10.1038/25159 Hart, 1999, The F-box protein beta-TrCP associates with phosphorylated beta-catenin and regulates its activity in the cell, Curr. Biol.: CB, 9, 207, 10.1016/S0960-9822(99)80091-8 Kitagawa, 1999, An F-box protein, FWD1, mediates ubiquitin-dependent proteolysis of beta-catenin, EMBO J., 18, 2401, 10.1093/emboj/18.9.2401 Hatakeyama, 1999, Ubiquitin-dependent degradation of IkappaBalpha is mediated by a ubiquitin ligase Skp1/Cul 1/F-box protein FWD1, Proc. Natl. Acad. Sci. U.S.A., 96, 3859, 10.1073/pnas.96.7.3859 Tan, 1999, Recruitment of a ROC1-CUL1 ubiquitin ligase by Skp1 and HOS to catalyze the ubiquitination of I kappa B alpha, Mol. Cell, 3, 527, 10.1016/S1097-2765(00)80481-5 Ougolkov, 2004, Associations among beta-TrCP, an E3 ubiquitin ligase receptor, beta-catenin, and NF-kappaB in colorectal cancer, J. Natl. Cancer Inst., 96, 1161, 10.1093/jnci/djh219 Muerkoster, 2005, Increased expression of the E3-ubiquitin ligase receptor subunit betaTRCP1 relates to constitutive nuclear factor-kappaB activation and chemoresistance in pancreatic carcinoma cells, Cancer Res., 65, 1316, 10.1158/0008-5472.CAN-04-1626 Fuchs, 2004, The many faces of beta-TrCP E3 ubiquitin ligases: reflections in the magic mirror of cancer, Oncogene, 23, 2028, 10.1038/sj.onc.1207389 Kim, 2007, Somatic mutations of the beta-TrCP gene in gastric cancer, APMIS: Acta Pathol. Microbiol. Immunol. Scand., 115, 127, 10.1111/j.1600-0463.2007.apm_562.x Saitoh, 2001, Expression profiles of betaTRCP1 and betaTRCP2, and mutation analysis of betaTRCP2 in gastric cancer, Int. J. Oncol., 18, 959 Skaar, 2014, SCF ubiquitin ligase-targeted therapies, Nat. Rev. Drug Discovery, 13, 889, 10.1038/nrd4432 Bartel, 2009, MicroRNAs: target recognition and regulatory functions, Cell, 136, 215, 10.1016/j.cell.2009.01.002 Bartel, 2004, MicroRNAs: genomics, biogenesis, mechanism, and function, Cell, 116, 281, 10.1016/S0092-8674(04)00045-5 Lee, 2003, The nuclear RNase III Drosha initiates microRNA processing, Nature, 425, 415, 10.1038/nature01957 Ha, 2014, Regulation of microRNA biogenesis, Nat. Rev. Mol. Cell Biol., 15, 509, 10.1038/nrm3838 Lytle, 2007, Target mRNAs are repressed as efficiently by microRNA-binding sites in the 5’ UTR as in the 3′ UTR, Proc. Natl. Acad. Sci. U.S.A., 104, 9667, 10.1073/pnas.0703820104 Niu, 2015, Induction of miRNA-181a by genotoxic treatments promotes chemotherapeutic resistance and metastasis in breast cancer, Oncogene Calin, 2006, MicroRNA signatures in human cancers, Nat. Rev. Cancer, 6, 857, 10.1038/nrc1997 Xu, 2010, MicroRNA-223 regulates cyclin E activity by modulating expression of F-box and WD-40 domain protein 7, J. Biol. Chem., 285, 34439, 10.1074/jbc.M110.152306 Jahid, 2012, miR-23a promotes the transition from indolent to invasive colorectal cancer, Cancer Discovery, 2, 540, 10.1158/2159-8290.CD-11-0267 Wang, 2011, Upregulation of miR-27a contributes to the malignant transformation of human bronchial epithelial cells induced by SV40 small T antigen, Oncogene, 30, 3875, 10.1038/onc.2011.103 Lerner, 2011, MiRNA-27a controls FBW7/hCDC4-dependent cyclin E degradation and cell cycle progression, Cell Cycle, 10, 2172, 10.4161/cc.10.13.16248 Li, 2012, MicroRNA-223 functions as an oncogene in human gastric cancer by targeting FBXW7/hCdc4, J. Cancer Res. Clin. Oncol., 138, 763, 10.1007/s00432-012-1154-x Mavrakis, 2011, A cooperative microRNA-tumor suppressor gene network in acute T-cell lymphoblastic leukemia (T-ALL), Nat. Genet., 43, 673, 10.1038/ng.858 Kurashige, 2012, Overexpression of microRNA-223 regulates the ubiquitin ligase FBXW7 in oesophageal squamous cell carcinoma, Br. J. Cancer, 106, 182, 10.1038/bjc.2011.509 Haneklaus, 2013, miR-223: infection, inflammation and cancer, J. Int. Med., 274, 215, 10.1111/joim.12099 Mansour, 2013, The TAL1 complex targets the FBXW7 tumor suppressor by activating miR-223 in human T cell acute lymphoblastic leukemia, J. Exp. Med., 210, 1545, 10.1084/jem.20122516 Kumar, 2014, Notch and NF-kB signaling pathways regulate miR-223/FBXW7 axis in T-cell acute lymphoblastic leukemia, Leukemia, 28, 2324, 10.1038/leu.2014.133 Eto, 2015, The sensitivity of gastric cancer to trastuzumab is regulated by the miR-223/FBXW7 pathway, Int. J. Cancer, 136, 1537, 10.1002/ijc.29168 Zhou, 2015, MiR-223 promotes the cisplatin resistance of human gastric cancer cells via regulating cell cycle by targeting FBXW7, J. Exp. Clin. Cancer Res.: CR, 34, 28, 10.1186/s13046-015-0145-6 Ma, 2013, Genistein down-regulates miR-223 expression in pancreatic cancer cells, Curr. Drug Targets, 14, 1150, 10.2174/13894501113149990187 Zhou, 2015, miR-92a is upregulated in cervical cancer and promotes cell proliferation and invasion by targeting FBXW7, Biochem. Biophys. Res. Commun., 458, 63, 10.1016/j.bbrc.2015.01.066 Li, 2014, Sequential expression of miR-182 and miR-503 cooperatively targets FBXW7, contributing to the malignant transformation of colon adenoma to adenocarcinoma, J. Pathol., 234, 488, 10.1002/path.4407 Jeon, 2013, An SREBP-responsive microRNA operon contributes to a regulatory loop for intracellular lipid homeostasis, Cell Metab., 18, 51, 10.1016/j.cmet.2013.06.010 Gong, 2015, MicroRNA-25 promotes gastric cancer proliferation, invasion, and migration by directly targeting F-box and WD-40 Domain Protein 7, FBXW7, Tumour Biol.: J. Int. Soc. Oncodev. Biol. Med., 10.1007/s13277-015-3510-3 Li, 2015, p53 mutation directs AURKA overexpression via miR-25 and FBXW7 in prostatic small cell neuroendocrine carcinoma, Mol. Cancer Res.: MCR, 13, 584, 10.1158/1541-7786.MCR-14-0277-T Lu, 2012, MiR-25 regulates Wwp2 and Fbxw7 and promotes reprogramming of mouse fibroblast cells to iPSCs, PLoS ONE, 7, e 40938, 10.1371/journal.pone.0040938 Zhang, 2012, MiR-25 regulates apoptosis by targeting Bim in human ovarian cancer, Oncol. Rep., 27, 594 Xu, 2012, MicroRNA-25 promotes cell migration and invasion in esophageal squamous cell carcinoma, Biochem. Biophys. Res. Commun., 421, 640, 10.1016/j.bbrc.2012.03.048 Li, 2013, MicroRNA-25 functions as a potential tumor suppressor in colon cancer by targeting Smad7, Cancer Lett., 335, 168, 10.1016/j.canlet.2013.02.029 Esposito, 2012, Down-regulation of the miR-25 and miR-30d contributes to the development of anaplastic thyroid carcinoma targeting the polycomb protein EZH2, J. Clin. Endocrinol. Metab., 97, E710, 10.1210/jc.2011-3068 Yang, 2015, The oncogenic microRNA-21 inhibits the tumor suppressive activity of FBXO11 to promote tumorigenesis, J. Biol. Chem., 290, 6037, 10.1074/jbc.M114.632125 Pfeffer, 2015, The role of miR-21 in cancer, Drug Dev. Res., 10.1002/ddr.21257 Abbas, 2013, CRL1-FBXO11 promotes Cdt2 ubiquitylation and degradation and regulates Pr-Set7/Set8-mediated cellular migration, Mol. Cell, 49, 1147, 10.1016/j.molcel.2013.02.003 Rossi, 2013, Regulation of the CRL4Cdt2 ubiquitin ligase and cell-cycle exit by the SCFFbxo11 ubiquitin ligase, Mol. Cell, 49, 1159, 10.1016/j.molcel.2013.02.004 Yang, 2012, SET8 promotes epithelial-mesenchymal transition and confers TWIST dual transcriptional activities, EMBO J., 31, 110, 10.1038/emboj.2011.364 Xue, 2015, MiRNA-621 sensitizes breast cancer to chemotherapy by suppressing FBXO11 and enhancing p53 activity, Oncogene Abida, 2007, FBXO11 promotes the Neddylation of p53 and inhibits its transcriptional activity, J. Biol. Chem., 282, 1797, 10.1074/jbc.M609001200 Zheng, 2014, PKD1 phosphorylation-dependent degradation of SNAIL by SCF-FBXO11 regulates epithelial-mesenchymal transition and metastasis, Cancer Cell, 26, 358, 10.1016/j.ccr.2014.07.022 Jackson, 2013, Rapid and widespread suppression of self-renewal by microRNA-203 during epidermal differentiation, Development, 140, 1882, 10.1242/dev.089649 Yu, 1998, Human CUL-1 associates with the SKP1/SKP2 complex and regulates p21(CIP1/WAF1) and cyclin D proteins, Proc. Natl. Acad. Sci. U.S.A., 95, 11324, 10.1073/pnas.95.19.11324 Carrano, 1999, SKP2 is required for ubiquitin-mediated degradation of the CDK inhibitor p27, Nat. Cell Biol., 1, 193, 10.1038/12013 Sanchez, 2013, MiR-7 triggers cell cycle arrest at the G1/S transition by targeting multiple genes including Skp2 and Psme3, PLoS ONE, 8, e65671, 10.1371/journal.pone.0065671 Fernandez, 2015, miR-340 inhibits tumor cell proliferation and induces apoptosis by targeting multiple negative regulators of p27 in non-small cell lung cancer, Oncogene, 34, 3240, 10.1038/onc.2014.267 Osoegawa, 2004, Regulation of p27 by S-phase kinase-associated protein 2 is associated with aggressiveness in non-small-cell lung cancer, J. Clin. Oncol., 22, 4165, 10.1200/JCO.2004.01.035 Qi, 2015, The miR-30 family inhibits pulmonary vascular hyperpermeability in the premetastatic phase by direct targeting of Skp2, Clin. Cancer Res., 21, 3071, 10.1158/1078-0432.CCR-14-2785 Garzon, 2010, Targeting microRNAs in cancer: rationale, strategies and challenges, Nat. Rev. Drug Discovery, 9, 775, 10.1038/nrd3179 Liu, 2012, Suppression of Akt/Foxp3-mediated miR-183 expression blocks Sp1-mediated ADAM17 expression and TNFalpha-mediated NFkappaB activation in piceatannol-treated human leukemia U937 cells, Biochem. Pharmacol., 84, 670, 10.1016/j.bcp.2012.06.007 Lin, 2013, MicroRNA-135b promotes lung cancer metastasis by regulating multiple targets in the Hippo pathway and LZTS1, Nat. Commun., 4, 1877, 10.1038/ncomms2876 Shi, 2014, MicroRNA-218 inhibits the proliferation of human choriocarcinoma JEG-3 cell line by targeting Fbxw8, Biochem. Biophys. Res. Commun., 450, 1241, 10.1016/j.bbrc.2014.06.094 Lin, 2011, Fbxw8 is involved in the proliferation of human choriocarcinoma JEG-3 cells, Mol. Biol. Rep., 38, 1741, 10.1007/s11033-010-0288-7 Eisfeld, 2012, miR-3151 interplays with its host gene BAALC and independently affects outcome of patients with cytogenetically normal acute myeloid leukemia, Blood, 120, 249, 10.1182/blood-2012-02-408492 Xiao, 2015, FBXL20-mediated Vps34 ubiquitination as a p53 controlled checkpoint in regulating autophagy and receptor degradation, Genes Dev., 29, 184, 10.1101/gad.252528.114 Eisfeld, 2014, Intronic miR-3151 within BAALC drives leukemogenesis by deregulating the TP53 pathway, Sci. Signaling, 7, ra36, 10.1126/scisignal.2004762 Lichner, 2011, The miR-290–295 cluster promotes pluripotency maintenance by regulating cell cycle phase distribution in mouse embryonic stem cells, Differentiation Res. Biol. Divers., 81, 11, 10.1016/j.diff.2010.08.002 Zheng, 2011, A latent pro-survival function for the mir-290-295 cluster in mouse embryonic stem cells, PLoS Genet., 7, e1002054, 10.1371/journal.pgen.1002054 Dragoi, 2014, Novel strategies to enforce an epithelial phenotype in mesenchymal cells, Cancer Res., 74, 3659, 10.1158/0008-5472.CAN-13-3231 Vinas-Castells, 2014, Nuclear ubiquitination by FBXL5 modulates Snail1 DNA binding and stability, Nucleic Acids Res., 42, 1079, 10.1093/nar/gkt935 Tan, 2007, Pharmacologic disruption of Polycomb-repressive complex 2-mediated gene repression selectively induces apoptosis in cancer cells, Genes Dev., 21, 1050, 10.1101/gad.1524107 Gomes, 2001, Atrogin-1, a muscle-specific F-box protein highly expressed during muscle atrophy, Proc. Natl. Acad. Sci. U.S.A., 98, 14440, 10.1073/pnas.251541198 Guo, 2014, Aberrant methylation and decreased expression of the TGF-beta/Smad target gene FBXO32 in esophageal squamous cell carcinoma, Cancer, 120, 2412, 10.1002/cncr.28764 Chou, 2010, Promoter hypermethylation of FBXO32, a novel TGF-beta/SMAD4 target gene and tumor suppressor, is associated with poor prognosis in human ovarian cancer, Lab. Invest. J. Tech. Methods Pathol., 90, 414, 10.1038/labinvest.2009.138 Song, 2014, The miR-19a/b family positively regulates cardiomyocyte hypertrophy by targeting atrogin-1 and MuRF-1, Biochem. J., 457, 151, 10.1042/BJ20130833 Olive, 2013, mir-17-92: a polycistronic oncomir with pleiotropic functions, Immunol. Rev., 253, 158, 10.1111/imr.12054 He, 2008, The H3K36 demethylase Jhdm1b/Kdm2b regulates cell proliferation and senescence through p15(Ink4b), Nat. Struct. Mol. Biol., 15, 1169, 10.1038/nsmb.1499 Frescas, 2007, JHDM1B/FBXL10 is a nucleolar protein that represses transcription of ribosomal RNA genes, Nature, 450, 309, 10.1038/nature06255 Tzatsos, 2011, Lysine-specific demethylase 2B (KDM2B)-let-7-enhancer of zester homolog 2 (EZH2) pathway regulates cell cycle progression and senescence in primary cells, J. Biol. Chem., 286, 33061, 10.1074/jbc.M111.257667 Gantier, 2012, A miR-19 regulon that controls NF-kappaB signaling, Nucleic Acids Res., 40, 8048, 10.1093/nar/gks521