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Review

The importance of regulatory ubiquitination in cancer and metastasis

, &
Pages 634-648 | Received 09 Dec 2016, Accepted 24 Jan 2017, Published online: 28 Feb 2017

References

  • Emmerich CH, Ordureau A, Strickson S, Arthur JS, Pedrioli PG, Komander D, Cohen P. Activation of the canonical IKK complex by K63/M1-linked hybrid ubiquitin chains. Proc Natl Acad Sci U S A 2013; 110:15247-52; PMID:23986494; http://dx.doi.org/10.1073/pnas.1314715110
  • Chen J, Chen ZJ. Regulation of NF-kappaB by ubiquitination. Curr Opin Immunol 2013; 25:4-12; PMID:23312890; http://dx.doi.org/10.1016/j.coi.2012.12.005
  • Messick TE, Greenberg RA. The ubiquitin landscape at DNA double-strand breaks. J Cell Biol 2009; 187:319-26; PMID:19948475; http://dx.doi.org/10.1083/jcb.200908074
  • Ori D, Kato H, Sanjo H, Tartey S, Mino T, Akira S, Takeuchi O. Essential roles of K63-linked polyubiquitin-binding proteins TAB2 and TAB3 in B cell activation via MAPKs. J Immunol 2013; 190:4037-45; PMID:23509369; http://dx.doi.org/10.4049/jimmunol.1300173
  • Cheung KJ, Ewald AJ. A collective route to metastasis: Seeding by tumor cell clusters. Science 2016; 352:167-9; PMID:27124449; http://dx.doi.org/10.1126/science.aaf6546
  • Clague MJ, Heride C, Urbe S. The demographics of the ubiquitin system. Trends Cell Biol 2015; 25:417-26; PMID:25906909; http://dx.doi.org/10.1016/j.tcb.2015.03.002
  • Wu X, Zhang W, Font-Burgada J, Palmer T, Hamil AS, Biswas SK, Poidinger M, Borcherding N, Xie Q, Ellies LG, et al. Ubiquitin-conjugating enzyme Ubc13 controls breast cancer metastasis through a TAK1-p38 MAP kinase cascade. Proc Natl Acad Sci U S A 2014; 111:13870-5; PMID:25189770; http://dx.doi.org/10.1073/pnas.1414358111
  • Wu Z, Shen S, Zhang Z, Zhang W, Xiao W. Ubiquitin-conjugating enzyme complex Uev1A-Ubc13 promotes breast cancer metastasis through nuclear factor-small ka, CyrillicB mediated matrix metalloproteinase-1 gene regulation. Breast Cancer Res 2014; 16:R75; PMID:25022892; http://dx.doi.org/10.1186/bcr3692
  • Deryugina EI, Quigley JP. Matrix metalloproteinases and tumor metastasis. Cancer Metastasis Rev 2006; 25:9-34; PMID:16680569; http://dx.doi.org/10.1007/s10555-006-7886-9
  • Fujita T, Ikeda H, Kawasaki K, Taira N, Ogasawara Y, Nakagawara A, Doihara H. Clinicopathological relevance of UbcH10 in breast cancer. Cancer Sci 2009; 100:238-48; PMID:19038004; http://dx.doi.org/10.1111/j.1349-7006.2008.01026.x
  • van Ree JH, Jeganathan KB, Malureanu L, van Deursen JM. Overexpression of the E2 ubiquitin-conjugating enzyme UbcH10 causes chromosome missegregation and tumor formation. J Cell Biol 2010; 188:83-100; PMID:20065091; http://dx.doi.org/10.1083/jcb.200906147
  • Narayan G, Bourdon V, Chaganti S, Arias-Pulido H, Nandula SV, Rao PH, Gissmann L, Durst M, Schneider A, Pothuri B, et al. Gene dosage alterations revealed by cDNA microarray analysis in cervical cancer: identification of candidate amplified and overexpressed genes. Genes Chromosomes Cancer 2007; 46:373-84; PMID:17243165; http://dx.doi.org/10.1002/gcc.20418
  • Tzelepi V, Zhang J, Lu JF, Kleb B, Wu G, Wan X, Hoang A, Efstathiou E, Sircar K, Navone NM, et al. Modeling a lethal prostate cancer variant with small-cell carcinoma features. Clin Cancer Res 2012; 18:666-77; PMID:22156612; http://dx.doi.org/10.1158/1078-0432.CCR-11-1867
  • Takahashi Y, Ishii Y, Nishida Y, Ikarashi M, Nagata T, Nakamura T, Yamamori S, Asai S. Detection of aberrations of ubiquitin-conjugating enzyme E2C gene (UBE2C) in advanced colon cancer with liver metastases by DNA microarray and two-color FISH. Cancer Genet Cytogenet 2006; 168:30-5; PMID:16772118; http://dx.doi.org/10.1016/j.cancergencyto.2005.12.011
  • Jung CR, Hwang KS, Yoo J, Cho WK, Kim JM, Kim WH, Im DS. E2-EPF UCP targets pVHL for degradation and associates with tumor growth and metastasis. Nat Med 2006; 12:809-16; PMID:16819549; http://dx.doi.org/10.1038/nm1440
  • Rankin EB, Giaccia AJ. Hypoxic control of metastasis. Science 2016; 352:175-80; PMID:27124451; http://dx.doi.org/10.1126/science.aaf4405
  • Witkiewicz AK, McMillan EA, Balaji U, Baek G, Lin WC, Mansour J, Mollaee M, Wagner KU, Koduru P, Yopp A, et al. Whole-exome sequencing of pancreatic cancer defines genetic diversity and therapeutic targets. Nat Commun 2015; 6:6744; PMID:25855536; http://dx.doi.org/10.1038/ncomms7744
  • Beltran H, Prandi D, Mosquera JM, Benelli M, Puca L, Cyrta J, Marotz C, Giannopoulou E, Chakravarthi BV, Varambally S, et al. Divergent clonal evolution of castration-resistant neuroendocrine prostate cancer. Nat Med 2016; 22:298-305; PMID:26855148; http://dx.doi.org/10.1038/nm.4045
  • Berndsen CE, Wolberger C. New insights into ubiquitin E3 ligase mechanism. Nat Struct Mol Biol 2014; 21:301-7; PMID:24699078; http://dx.doi.org/10.1038/nsmb.2780
  • Deshaies RJ, Joazeiro CA. RING domain E3 ubiquitin ligases. Annu Rev Biochem 2009; 78:399-434; PMID:19489725; http://dx.doi.org/10.1146/annurev.biochem.78.101807.093809
  • Jang KW, Lee KH, Kim SH, Jin T, Choi EY, Jeon HJ, Kim E, Han YS, Chung JH. Ubiquitin ligase CHIP induces TRAF2 proteasomal degradation and NF-kappaB inactivation to regulate breast cancer cell invasion. J Cell Biochem 2011; 112:3612-20; PMID:21793045; http://dx.doi.org/10.1002/jcb.23292
  • Kajiro M, Hirota R, Nakajima Y, Kawanowa K, So-ma K, Ito I, Yamaguchi Y, Ohie SH, Kobayashi Y, Seino Y, et al. The ubiquitin ligase CHIP acts as an upstream regulator of oncogenic pathways. Nat Cell Biol 2009; 11:312-9; PMID:19198599; http://dx.doi.org/10.1038/ncb1839
  • Wang Y, Ren F, Wang Y, Feng Y, Wang D, Jia B, Qiu Y, Wang S, Yu J, Sung JJ, et al. CHIP/Stub1 functions as a tumor suppressor and represses NF-kappaB-mediated signaling in colorectal cancer. Carcinogenesis 2014; 35:983-91; PMID:24302614; http://dx.doi.org/10.1093/carcin/bgt393
  • Wang T, Yang J, Xu J, Li J, Cao Z, Zhou L, You L, Shu H, Lu Z, Li H, et al. CHIP is a novel tumor suppressor in pancreatic cancer through targeting EGFR. Oncotarget 2014; 5:1969-86; PMID:24722501; http://dx.doi.org/10.18632/oncotarget.1890
  • Eirew P, Steif A, Khattra J, Ha G, Yap D, Farahani H, Gelmon K, Chia S, Mar C, Wan A, et al. Dynamics of genomic clones in breast cancer patient xenografts at single-cell resolution. Nature 2015; 518:422-6; PMID:25470049; http://dx.doi.org/10.1038/nature13952
  • Welcker M, Clurman BE. FBW7 ubiquitin ligase: a tumour suppressor at the crossroads of cell division, growth and differentiation. Nat Rev Cancer 2008; 8:83-93; PMID:18094723; http://dx.doi.org/10.1038/nrc2290
  • Ibusuki M, Yamamoto Y, Shinriki S, Ando Y, Iwase H. Reduced expression of ubiquitin ligase FBXW7 mRNA is associated with poor prognosis in breast cancer patients. Cancer Sci 2011; 102:439-45; PMID:21134077; http://dx.doi.org/10.1111/j.1349-7006.2010.01801.x
  • Iwatsuki M, Mimori K, Ishii H, Yokobori T, Takatsuno Y, Sato T, Toh H, Onoyama I, Nakayama KI, Baba H, et al. Loss of FBXW7, a cell cycle regulating gene, in colorectal cancer: clinical significance. Int J Cancer 2010; 126:1828-37; PMID:19739118
  • Yang H, Lu X, Liu Z, Chen L, Xu Y, Wang Y, Wei G, Chen Y. FBXW7 suppresses epithelial-mesenchymal transition, stemness and metastatic potential of cholangiocarcinoma cells. Oncotarget 2015; 6:6310-25; PMID:25749036; http://dx.doi.org/10.18632/oncotarget.3355
  • Quail DF, Joyce JA. Microenvironmental regulation of tumor progression and metastasis. Nat Med 2013; 19:1423-37; PMID:24202395; http://dx.doi.org/10.1038/nm.3394
  • Paolino M, Choidas A, Wallner S, Pranjic B, Uribesalgo I, Loeser S, Jamieson AM, Langdon WY, Ikeda F, Fededa JP, et al. The E3 ligase Cbl-b and TAM receptors regulate cancer metastasis via natural killer cells. Nature 2014; 507:508-12; PMID:24553136; http://dx.doi.org/10.1038/nature12998
  • Vaughan L, Tan CT, Chapman A, Nonaka D, Mack NA, Smith D, Booton R, Hurlstone AF, Malliri A. HUWE1 ubiquitylates and degrades the RAC activator TIAM1 promoting cell-cell adhesion disassembly, migration, and invasion. Cell reports 2015; 10:88-102; PMID:25543140; http://dx.doi.org/10.1016/j.celrep.2014.12.012
  • Tsai YC, Mendoza A, Mariano JM, Zhou M, Kostova Z, Chen B, Veenstra T, Hewitt SM, Helman LJ, Khanna C, et al. The ubiquitin ligase gp78 promotes sarcoma metastasis by targeting KAI1 for degradation. Nat Med 2007; 13:1504-9; PMID:18037895; http://dx.doi.org/10.1038/nm1686
  • Zhang L, Zhou F, Garcia de Vinuesa A, de Kruijf EM, Mesker WE, Hui L, Drabsch Y, Li Y, Bauer A, Rousseau A, et al. TRAF4 promotes TGF-beta receptor signaling and drives breast cancer metastasis. Mol Cell 2013; 51:559-72; PMID:23973329; http://dx.doi.org/10.1016/j.molcel.2013.07.014
  • Martelotto LG, De Filippo MR, Ng CK, Natrajan R, Fuhrmann L, Cyrta J, Piscuoglio S, Wen HC, Lim RS, Shen R, et al. Genomic landscape of adenoid cystic carcinoma of the breast. J Pathol 2015; 237:179-89; PMID:26095796; http://dx.doi.org/10.1002/path.4573
  • Lin JH, Hsieh SC, Chen JN, Tsai MH, Chang CC. WWP1 gene is a potential molecular target of human oral cancer. Oral Surg Oral Med Oral Pathol Oral Radiol 2013; 116:221-31; PMID:23849376; http://dx.doi.org/10.1016/j.oooo.2013.05.006
  • Cheng Q, Cao X, Yuan F, Li G, Tong T. Knockdown of WWP1 inhibits growth and induces apoptosis in hepatoma carcinoma cells through the activation of caspase3 and p53. Biochem Biophys Res Commun 2014; 448:248-54; PMID:24792179; http://dx.doi.org/10.1016/j.bbrc.2014.04.117
  • Zhang L, Wu Z, Ma Z, Liu H, Wu Y, Zhang Q. WWP1 as a potential tumor oncogene regulates PTEN-Akt signaling pathway in human gastric carcinoma. Tumour Biol 2015; 36:787-98; PMID:25293520; http://dx.doi.org/10.1007/s13277-014-2696-0
  • Chen C, Zhou Z, Ross JS, Zhou W, Dong JT. The amplified WWP1 gene is a potential molecular target in breast cancer. Int J Cancer 2007; 121:80-7; PMID:17330240; http://dx.doi.org/10.1002/ijc.22653
  • Chen C, Zhou Z, Sheehan CE, Slodkowska E, Sheehan CB, Boguniewicz A, Ross JS. Overexpression of WWP1 is associated with the estrogen receptor and insulin-like growth factor receptor 1 in breast carcinoma. Int J Cancer 2009; 124:2829-36; PMID:19267401; http://dx.doi.org/10.1002/ijc.24266
  • Zhou Z, Liu R, Chen C. The WWP1 ubiquitin E3 ligase increases TRAIL resistance in breast cancer. Int J Cancer 2012; 130:1504-10; PMID:21480222; http://dx.doi.org/10.1002/ijc.26122
  • Chen C, Sun X, Guo P, Dong XY, Sethi P, Zhou W, Zhou Z, Petros J, Frierson HF, Jr., Vessella RL, et al. Ubiquitin E3 ligase WWP1 as an oncogenic factor in human prostate cancer. Oncogene 2007; 26:2386-94; PMID:17016436; http://dx.doi.org/10.1038/sj.onc.1210021
  • Maher ER, Neumann HP, Richard S. von Hippel-Lindau disease: a clinical and scientific review. Eur J Hum Genet 2011; 19:617-23; PMID:21386872; http://dx.doi.org/10.1038/ejhg.2010.175
  • Feng C, Sun Y, Ding G, Wu Z, Jiang H, Wang L, Ding Q, Wen H. PI3Kbeta inhibitor TGX221 selectively inhibits renal cell carcinoma cells with both VHL and SETD2 mutations and links multiple pathways. Scientific reports 2015; 5:9465; PMID:25853938; http://dx.doi.org/10.1038/srep09465
  • Rechsteiner MP, von Teichman A, Nowicka A, Sulser T, Schraml P, Moch H. VHL gene mutations and their effects on hypoxia inducible factor HIFalpha: identification of potential driver and passenger mutations. Cancer Res 2011; 71:5500-11; PMID:21715564; http://dx.doi.org/10.1158/0008-5472.CAN-11-0757
  • Makishima H, Cazzolli H, Szpurka H, Dunbar A, Tiu R, Huh J, Muramatsu H, O'Keefe C, Hsi E, Paquette RL, et al. Mutations of e3 ubiquitin ligase cbl family members constitute a novel common pathogenic lesion in myeloid malignancies. J Clin Oncol 2009; 27:6109-16; PMID:19901108; http://dx.doi.org/10.1200/JCO.2009.23.7503
  • Muramatsu H, Makishima H, Jankowska AM, Cazzolli H, O'Keefe C, Yoshida N, Xu Y, Nishio N, Hama A, Yagasaki H, et al. Mutations of an E3 ubiquitin ligase c-Cbl but not TET2 mutations are pathogenic in juvenile myelomonocytic leukemia. Blood 2010; 115:1969-75; PMID:20008299; http://dx.doi.org/10.1182/blood-2009-06-226340
  • Grand FH, Hidalgo-Curtis CE, Ernst T, Zoi K, Zoi C, McGuire C, Kreil S, Jones A, Score J, Metzgeroth G, et al. Frequent CBL mutations associated with 11q acquired uniparental disomy in myeloproliferative neoplasms. Blood 2009; 113:6182-92; PMID:19387008; http://dx.doi.org/10.1182/blood-2008-12-194548
  • Loh ML, Sakai DS, Flotho C, Kang M, Fliegauf M, Archambeault S, Mullighan CG, Chen L, Bergstraesser E, Bueso-Ramos CE, et al. Mutations in CBL occur frequently in juvenile myelomonocytic leukemia. Blood 2009; 114:1859-63; PMID:19571318; http://dx.doi.org/10.1182/blood-2009-01-198416
  • Sargin B, Choudhary C, Crosetto N, Schmidt MH, Grundler R, Rensinghoff M, Thiessen C, Tickenbrock L, Schwable J, Brandts C, et al. Flt3-dependent transformation by inactivating c-Cbl mutations in AML. Blood 2007; 110:1004-12; PMID:17446348; http://dx.doi.org/10.1182/blood-2007-01-066076
  • Kassenbrock CK, Anderson SM. Regulation of ubiquitin protein ligase activity in c-Cbl by phosphorylation-induced conformational change and constitutive activation by tyrosine to glutamate point mutations. J Biol Chem 2004; 279:28017-27; PMID:15117950; http://dx.doi.org/10.1074/jbc.M404114200
  • Yang Y, Schmitz R, Mitala J, Whiting A, Xiao W, Ceribelli M, Wright GW, Zhao H, Yang Y, Xu W, et al. Essential role of the linear ubiquitin chain assembly complex in lymphoma revealed by rare germline polymorphisms. Cancer Dis 2014; 4:480-93; PMID:24491438; http://dx.doi.org/10.1158/2159-8290.CD-13-0915
  • Yuan L, Lu L, Yang Y, Sun H, Chen X, Huang Y, Wang X, Zou L, Bao L. Genetic mutational profiling analysis of T cell acute lymphoblastic leukemia reveal mutant FBXW7 as a prognostic indicator for inferior survival. Ann Hematol 2015; 94:1817-28; PMID:26341754; http://dx.doi.org/10.1007/s00277-015-2474-0
  • Cancer Genome Atlas Research N. Comprehensive molecular characterization of urothelial bladder carcinoma. Nature 2014; 507:315-22; PMID:24476821; http://dx.doi.org/10.1038/nature12965
  • Seshagiri S, Stawiski EW, Durinck S, Modrusan Z, Storm EE, Conboy CB, Chaudhuri S, Guan Y, Janakiraman V, Jaiswal BS, et al. Recurrent R-spondin fusions in colon cancer. Nature 2012; 488:660-4; PMID:22895193; http://dx.doi.org/10.1038/nature11282
  • Jones S, Stransky N, McCord CL, Cerami E, Lagowski J, Kelly D, Angiuoli SV, Sausen M, Kann L, Shukla M, et al. Genomic analyses of gynaecologic carcinosarcomas reveal frequent mutations in chromatin remodelling genes. Nat Commun 2014; 5:5006; PMID:25233892; http://dx.doi.org/10.1038/ncomms6006
  • Muller E, Brault B, Holmes A, Legros A, Jeannot E, Campitelli M, Rousselin A, Goardon N, Frebourg T, Krieger S, et al. Genetic profiles of cervical tumors by high-throughput sequencing for personalized medical care. Cancer Med 2015; 4:1484-93; PMID:26155992; http://dx.doi.org/10.1002/cam4.492
  • Aydin IT, Melamed RD, Adams SJ, Castillo-Martin M, Demir A, Bryk D, Brunner G, Cordon-Cardo C, Osman I, Rabadan R, et al. FBXW7 mutations in melanoma and a new therapeutic paradigm. J Natl Cancer Inst 2014; 106:dju107; PMID:24838835; http://dx.doi.org/10.1093/jnci/dju107
  • Sato M, Rodriguez-Barrueco R, Yu J, Do C, Silva JM, Gautier J. MYC is a critical target of FBXW7. Oncotarget 2015; 6:3292-305; PMID:25669969; http://dx.doi.org/10.18632/oncotarget.3203
  • Fujii Y, Yada M, Nishiyama M, Kamura T, Takahashi H, Tsunematsu R, Susaki E, Nakagawa T, Matsumoto A, Nakayama KI. Fbxw7 contributes to tumor suppression by targeting multiple proteins for ubiquitin-dependent degradation. Cancer Sci 2006; 97:729-36; PMID:16863506; http://dx.doi.org/10.1111/j.1349-7006.2006.00239.x
  • Richards MW, Burgess SG, Poon E, Carstensen A, Eilers M, Chesler L, Bayliss R. Structural basis of N-Myc binding by Aurora-A and its destabilization by kinase inhibitors. Proc Natl Acad Sci U S A 2016; 113:13726-31; PMID:27837025; http://dx.doi.org/10.1073/pnas.1610626113
  • Jardim DL, Wheler JJ, Hess K, Tsimberidou AM, Zinner R, Janku F, Subbiah V, Naing A, Piha-Paul SA, Westin SN, et al. FBXW7 mutations in patients with advanced cancers: clinical and molecular characteristics and outcomes with mTOR inhibitors. PLoS One 2014; 9:e89388; PMID:24586741; http://dx.doi.org/10.1371/journal.pone.0089388
  • Villaruz LC, Socinski MA. Temsirolimus therapy in a patient with lung adenocarcinoma harboring an FBXW7 mutation. Lung cancer (Amsterdam, Netherlands) 2014; 83:300-1; PMID:24360397; http://dx.doi.org/10.1016/j.lungcan.2013.11.018
  • Morrison BJ, Morris JC, Steel JC. Lung cancer-initiating cells: a novel target for cancer therapy. Target Oncol 2013; 8:159-72; PMID:23314952; http://dx.doi.org/10.1007/s11523-012-0247-4
  • Khammanivong A, Gopalakrishnan R, Dickerson EB. SMURF1 silencing diminishes a CD44-high cancer stem cell-like population in head and neck squamous cell carcinoma. Mol Cancer 2014; 13:260; PMID:25471937; http://dx.doi.org/10.1186/1476-4598-13-260
  • Wang J, Huang Y, Guan Z, Zhang JL, Su HK, Zhang W, Yue CF, Yan M, Guan S, Liu QQ. E3-ligase Skp2 predicts poor prognosis and maintains cancer stem cell pool in nasopharyngeal carcinoma. Oncotarget 2014; 5:5591-601; PMID:25015320; http://dx.doi.org/10.18632/oncotarget.2149
  • Chan CH, Morrow JK, Li CF, Gao Y, Jin G, Moten A, Stagg LJ, Ladbury JE, Cai Z, Xu D, et al. Pharmacological inactivation of Skp2 SCF ubiquitin ligase restricts cancer stem cell traits and cancer progression. Cell 2013; 154:556-68; PMID:23911321; http://dx.doi.org/10.1016/j.cell.2013.06.048
  • Aki D, Zhang W, Liu YC. The E3 ligase Itch in immune regulation and beyond. Immunol Rev 2015; 266:6-26; PMID:26085204; http://dx.doi.org/10.1111/imr.12301
  • Rossi M, Rotblat B, Ansell K, Amelio I, Caraglia M, Misso G, Bernassola F, Cavasotto CN, Knight RA, Ciechanover A, et al. High throughput screening for inhibitors of the HECT ubiquitin E3 ligase ITCH identifies antidepressant drugs as regulators of autophagy. Cell Death Dis 2014; 5:e1203; http://dx.doi.org/10.1038/cddis.2014.113
  • Bongiorno-Borbone L, Giacobbe A, Compagnone M, Eramo A, De Maria R, Peschiaroli A, Melino G. Anti-tumoral effect of desmethylclomipramine in lung cancer stem cells. Oncotarget 2015; 6:16926-38; PMID:26219257; http://dx.doi.org/10.18632/oncotarget.4700
  • Takeishi S, Nakayama KI. Role of Fbxw7 in the maintenance of normal stem cells and cancer-initiating cells. Br J Cancer 2014; 111:1054-9; PMID:24853181; http://dx.doi.org/10.1038/bjc.2014.259
  • Wang Y, Liu Y, Lu J, Zhang P, Wang Y, Xu Y, Wang Z, Mao JH, Wei G. Rapamycin inhibits FBXW7 loss-induced epithelial-mesenchymal transition and cancer stem cell-like characteristics in colorectal cancer cells. Biochem Biophys Res Commun 2013; 434:352-6; PMID:23558291; http://dx.doi.org/10.1016/j.bbrc.2013.03.077
  • Takeishi S, Matsumoto A, Onoyama I, Naka K, Hirao A, Nakayama KI. Ablation of Fbxw7 eliminates leukemia-initiating cells by preventing quiescence. Cancer Cell 2013; 23:347-61; PMID:23518349; http://dx.doi.org/10.1016/j.ccr.2013.01.026
  • D'Arcy P, Wang X, Linder S. Deubiquitinase inhibition as a cancer therapeutic strategy. Pharmacol Ther 2015; 147:32-54; PMID:25444757; http://dx.doi.org/10.1016/j.pharmthera.2014.11.002
  • Colland F, Formstecher E, Jacq X, Reverdy C, Planquette C, Conrath S, Trouplin V, Bianchi J, Aushev VN, Camonis J, et al. Small-molecule inhibitor of USP7/HAUSP ubiquitin protease stabilizes and activates p53 in cells. Mol Cancer Ther 2009; 8:2286-95; PMID:19671755; http://dx.doi.org/10.1158/1535-7163.MCT-09-0097
  • Zhao GY, Lin ZW, Lu CL, Gu J, Yuan YF, Xu FK, Liu RH, Ge D, Ding JY. USP7 overexpression predicts a poor prognosis in lung squamous cell carcinoma and large cell carcinoma. Tumour Biol 2015; 36:1721-9; PMID:25519684; http://dx.doi.org/10.1007/s13277-014-2773-4
  • Song MS, Salmena L, Carracedo A, Egia A, Lo-Coco F, Teruya-Feldstein J, Pandolfi PP. The deubiquitinylation and localization of PTEN are regulated by a HAUSP-PML network. Nature 2008; 455:813-7; PMID:18716620; http://dx.doi.org/10.1038/nature07290
  • Rivlin N, Katz S, Doody M, Sheffer M, Horesh S, Molchadsky A, Koifman G, Shetzer Y, Goldfinger N, Rotter V, et al. Rescue of embryonic stem cells from cellular transformation by proteomic stabilization of mutant p53 and conversion into WT conformation. Proc Natl Acad Sci U S A 2014; 111:7006-11; PMID:24778235; http://dx.doi.org/10.1073/pnas.1320428111
  • Zhang L, Zhou F, Drabsch Y, Gao R, Snaar-Jagalska BE, Mickanin C, Huang H, Sheppard KA, Porter JA, Lu CX, et al. USP4 is regulated by AKT phosphorylation and directly deubiquitylates TGF-beta type I receptor. Nat Cell Biol 2012; 14:717-26; PMID:22706160; http://dx.doi.org/10.1038/ncb2522
  • Schwickart M, Huang X, Lill JR, Liu J, Ferrando R, French DM, Maecker H, O'Rourke K, Bazan F, Eastham-Anderson J, et al. Deubiquitinase USP9X stabilizes MCL1 and promotes tumour cell survival. Nature 2010; 463:103-7; PMID:20023629; http://dx.doi.org/10.1038/nature08646
  • Kushwaha D, O'Leary C, Cron KR, Deraska P, Zhu K, D'Andrea AD, Kozono D. USP9X inhibition promotes radiation-induced apoptosis in non-small cell lung cancer cells expressing mid-to-high MCL1. Cancer Biol Ther 2015; 16:392-401; PMID:25692226; http://dx.doi.org/10.1080/15384047.2014.1002358
  • Gu YY, Yang M, Zhao M, Luo Q, Yang L, Peng H, Wang J, Huang SK, Zheng ZX, Yuan XH, et al. The de-ubiquitinase UCHL1 promotes gastric cancer metastasis via the Akt and Erk1/2 pathways. Tumour Biol 2015; 36:8379-87; PMID:26018507; http://dx.doi.org/10.1007/s13277-015-3566-0
  • Kim HJ, Kim YM, Lim S, Nam YK, Jeong J, Kim HJ, Lee KJ. Ubiquitin C-terminal hydrolase-L1 is a key regulator of tumor cell invasion and metastasis. Oncogene 2009; 28:117-27; PMID:18820707; http://dx.doi.org/10.1038/onc.2008.364
  • Goto Y, Zeng L, Yeom CJ, Zhu Y, Morinibu A, Shinomiya K, Kobayashi M, Hirota K, Itasaka S, Yoshimura M, et al. UCHL1 provides diagnostic and antimetastatic strategies due to its deubiquitinating effect on HIF-1alpha. Nat Commun 2015; 6:6153; PMID:25615526; http://dx.doi.org/10.1038/ncomms7153
  • Xiang T, Li L, Yin X, Yuan C, Tan C, Su X, Xiong L, Putti TC, Oberst M, Kelly K, et al. The ubiquitin peptidase UCHL1 induces G0/G1 cell cycle arrest and apoptosis through stabilizing p53 and is frequently silenced in breast cancer. PLoS One 2012; 7:e29783; PMID:22279545; http://dx.doi.org/10.1371/journal.pone.0029783
  • Ummanni R, Jost E, Braig M, Lohmann F, Mundt F, Barett C, Schlomm T, Sauter G, Senff T, Bokemeyer C, et al. Ubiquitin carboxyl-terminal hydrolase 1 (UCHL1) is a potential tumour suppressor in prostate cancer and is frequently silenced by promoter methylation. Mol Cancer 2011; 10:129; PMID:21999842; http://dx.doi.org/10.1186/1476-4598-10-129
  • Iglesias-Gato D, Chuan YC, Jiang N, Svensson C, Bao J, Paul I, Egevad L, Kessler BM, Wikstrom P, Niu Y, et al. OTUB1 de-ubiquitinating enzyme promotes prostate cancer cell invasion in vitro and tumorigenesis in vivo. Mol Cancer 2015; 14:8; PMID:25623341; http://dx.doi.org/10.1186/s12943-014-0280-2
  • Zhou Y, Wu J, Fu X, Du W, Zhou L, Meng X, Yu H, Lin J, Ye W, Liu J, et al. OTUB1 promotes metastasis and serves as a marker of poor prognosis in colorectal cancer. Mol Cancer 2014; 13:258; PMID:25431208; http://dx.doi.org/10.1186/1476-4598-13-258
  • Karunarathna U, Kongsema M, Zona S, Gong C, Cabrera E, Gomes AR, Man EP, Khongkow P, Tsang JW, Khoo US, et al. OTUB1 inhibits the ubiquitination and degradation of FOXM1 in breast cancer and epirubicin resistance. Oncogene 2016; 35:1433-44; PMID:26148240; http://dx.doi.org/10.1038/onc.2015.208
  • Huang X, Dixit VM. Drugging the undruggables: exploring the ubiquitin system for drug development. Cell Res 2016; 26:484-98; PMID:27002218; http://dx.doi.org/10.1038/cr.2016.31
  • Burgess A, Chia KM, Haupt S, Thomas D, Haupt Y, Lim E. Clinical Overview of MDM2/X-Targeted Therapies. Front Oncol 2016; 6:7; PMID:26858935; http://dx.doi.org/10.3389/fonc.2016.00007
  • Cancer Genome Atlas N. Comprehensive molecular characterization of human colon and rectal cancer. Nature 2012; 487:330-7; PMID:22810696; http://dx.doi.org/10.1038/nature11252
  • Cancer Genome Atlas Research N. Comprehensive molecular characterization of gastric adenocarcinoma. Nature 2014; 513:202-9; PMID:25079317; http://dx.doi.org/10.1038/nature13480
  • Cancer Genome Atlas Research N, Kandoth C, Schultz N, Cherniack AD, Akbani R, Liu Y, Shen H, Robertson AG, Pashtan I, Shen R, et al. Integrated genomic characterization of endometrial carcinoma. Nature 2013; 497:67-73; PMID:23636398; http://dx.doi.org/10.1038/nature12113
  • Campbell JD, Alexandrov A, Kim J, Wala J, Berger AH, Pedamallu CS, Shukla SA, Guo G, Brooks AN, Murray BA, et al. Distinct patterns of somatic genome alterations in lung adenocarcinomas and squamous cell carcinomas. Nat Genet 2016; 48:607-16; PMID:27158780; http://dx.doi.org/10.1038/ng.3564
  • Stephens PJ, Tarpey PS, Davies H, Van Loo P, Greenman C, Wedge DC, Nik-Zainal S, Martin S, Varela I, Bignell GR, et al. The landscape of cancer genes and mutational processes in breast cancer. Nature 2012; 486:400-4; PMID:22722201