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Roles of USP9X in cellular functions and tumorigenesis (Review)
- Authors:
- Yimei Meng
- Chaojin Hong
- Sifu Yang
- Zhiquan Qin
- Liu Yang
- Yumei Huang
-
Affiliations: Cancer Center, Department of Medical Oncology, Zhejiang Provincial People's Hospital (Affiliated People's Hospital), Hangzhou Medical College, Hangzhou, Zhejiang 310014, P.R. China - Published online on: October 10, 2023 https://doi.org/10.3892/ol.2023.14093
- Article Number: 506
-
Copyright: © Meng et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
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Ermolaeva M, Neri F, Ori A and Rudolph KL: Cellular and epigenetic drivers of stem cell ageing. Nat Rev Mol Cell Biol. 19:594–610. 2018. View Article : Google Scholar : PubMed/NCBI | |
Holguin-Cruz JA, Foster LJ and Gsponer J: Where protein structure and cell diversity meet. Trends Cell Biol. 32:996–1007. 2022. View Article : Google Scholar : PubMed/NCBI | |
Toyama BH and Hetzer MW: Protein homeostasis: Live long, won't prosper. Nat Rev Mol Cell Biol. 14:55–61. 2013. View Article : Google Scholar : PubMed/NCBI | |
Beynon RJ and Bond JS: Catabolism of intracellular protein: Molecular aspects. Am J Physiol. 251:141–152. 1986. View Article : Google Scholar : PubMed/NCBI | |
Komander D and Rape M: The ubiquitin code. Annu Rev Biochem. 81:203–229. 2012. View Article : Google Scholar : PubMed/NCBI | |
Li X, Elmira E, Rohondia S, Wang J, Liu J and Dou QP: A patent review of the ubiquitin ligase system: 2015–2018. Expert Opin Ther Pat. 28:919–937. 2018. View Article : Google Scholar : PubMed/NCBI | |
Jang HH: Regulation of protein degradation by proteasomes in cancer. J Cancer Prev. 23:153–161. 2018. View Article : Google Scholar : PubMed/NCBI | |
Becker JR, Clifford G, Bonnet C, Groth A, Wilson MD and Chapman JR: BARD1 reads H2A lysine 15 ubiquitination to direct homologous recombination. Nature. 596:433–437. 2021. View Article : Google Scholar : PubMed/NCBI | |
Roberts JZ, Crawford N and Longley DB: The role of ubiquitination in apoptosis and necroptosis. Cell Death Differ. 29:272–284. 2022. View Article : Google Scholar : PubMed/NCBI | |
Sun T, Liu Z and Yang Q: The role of ubiquitination and deubiquitination in cancer metabolism. Mol Cancer. 19:1462020. View Article : Google Scholar : PubMed/NCBI | |
Schmidt MF, Gan ZY, Komander D and Dewson G: Ubiquitin signalling in neurodegeneration: Mechanisms and therapeutic opportunities. Cell Death Differ. 28:570–590. 2021. View Article : Google Scholar : PubMed/NCBI | |
Fhu CW and Ali A: Dysregulation of the ubiquitin proteasome system in human malignancies: A window for therapeutic intervention. Cancers (Basel). 13:15132021. View Article : Google Scholar : PubMed/NCBI | |
Grabbe C, Husnjak K and Dikic I: The spatial and temporal organization of ubiquitin networks. Nat Rev Mol Cell Biol. 12:295–307. 2011. View Article : Google Scholar : PubMed/NCBI | |
Shimizu K, Gi M, Suzuki S, North BJ, Watahiki A, Fukumoto S, Asara JM, Tokunaga F, Wei W and Inuzuka H: Interplay between protein acetylation and ubiquitination controls MCL1 protein stability. Cell Rep. 37:1099882021. View Article : Google Scholar : PubMed/NCBI | |
Murtaza M, Jolly LA, Gecz J and Wood SA: La FAM fatale: USP9X in development and disease. Cell Mol Life Sci. 72:2075–2089. 2015. View Article : Google Scholar : PubMed/NCBI | |
Johnson BV, Kumar R, Oishi S, Alexander S, Kasherman M, Vega MS, Ivancevic A, Gardner A, Domingo D, Corbett M, et al: Partial loss of USP9X function leads to a male neurodevelopmental and behavioral disorder converging on transforming growth factor beta signaling. Biol Psychiatry. 87:100–112. 2020. View Article : Google Scholar : PubMed/NCBI | |
Delbridge ARD, Kueh AJ, Ke F, Zamudio NM, El-Saafin F, Jansz N, Wang GY, Iminitoff M, Beck T, Haupt S, et al: Loss of p53 causes stochastic aberrant x-chromosome inactivation and female-specific neural tube defects. Cell Rep. 27:442–454. 2019. View Article : Google Scholar : PubMed/NCBI | |
Homan CC, Kumar R, Nguyen LS, Haan E, Raymond FL, Abidi F, Raynaud M, Schwartz CE, Wood SA, Gecz J, et al: Mutations in USP9X are associated with X-linked intellectual disability and disrupt neuronal cell migration and growth. Am J Hum Genet. 94:470–478. 2014. View Article : Google Scholar : PubMed/NCBI | |
Wang B, Tang X, Yao L, Wang Y, Chen Z, Li M, Wu N, Wu D, Dai X, Jiang H and Ai D: Disruption of USP9X in macrophages promotes foam cell formation and atherosclerosis. J Clin Invest. 132:e1542172022. View Article : Google Scholar : PubMed/NCBI | |
Greenhill C: Pancreatic cancer: USP9X can be used to predict pancreatic cancer outcomes. Nat Rev Gastroenterol Hepatol. 9:3022012. View Article : Google Scholar : PubMed/NCBI | |
Jones MH, Furlong RA, Burkin H, Chalmers IJ, Brown GM, Khwaja O and Affara NA: The Drosophila developmental gene fat facets has a human homologue in Xp11.4 which escapes X-inactivation and has related sequences on Yq11.2. Hum Mol Gene. 5:1695–1701. 1996. View Article : Google Scholar : PubMed/NCBI | |
Wood SA, Pascoe WS, Ru K, Yamada T, Hirchenhain J, Kemler R and Mattick JS: Cloning and expression analysis of a novel mouse gene with sequence similarity to the Drosophila fat facets gene. Mech Dev. 63:29–38. 1997. View Article : Google Scholar : PubMed/NCBI | |
Chen X, Overstreet E, Wood SA and Fischer JA: On the conservation of function of the Drosophila fat facets deubiquitinating enzyme and Fam, its mouse homolog. Dev Genes Evol. 210:603–610. 2000. View Article : Google Scholar : PubMed/NCBI | |
Fischer-Vize JA, Rubin GM and Lehmann R: The fat facets gene is required for Drosophila eye and embryo development. Development. 116:985–1000. 1992. View Article : Google Scholar : PubMed/NCBI | |
Khut PY, Tucker B, Lardelli M and Wood SA: Evolutionary and expression analysis of the zebrafish deubiquitylating enzyme, usp9. Zebrafish. 4:95–101. 2007. View Article : Google Scholar : PubMed/NCBI | |
Nijman SM, Luna-Vargas MP, Velds A, Brummelkamp TR, Dirac AM, Sixma TK and Bernards R: A genomic and functional inventory of deubiquitinating enzymes. Cell. 123:773–786. 2005. View Article : Google Scholar : PubMed/NCBI | |
Amerik AY and Hochstrasser M: Mechanism and function of deubiquitinating enzymes. Biochim Biophys Acta. 1695:189–207. 2004. View Article : Google Scholar : PubMed/NCBI | |
Paudel P, Zhang Q, Leung C, Greenberg HC, Guo Y, Chern YH, Dong A, Li Y, Vedadi M, Zhuang Z and Tong Y: Crystal structure and activity-based labeling reveal the mechanisms for linkage-specific substrate recognition by deubiquitinase USP9X. Proc Natl Acad Sci USA. 116:7288–7297. 2019. View Article : Google Scholar : PubMed/NCBI | |
Marx C, Held JM, Gibson BW and Benz CC: ErbB2 trafficking and degradation associated with K48 and K63 polyubiquitination. Cancer Res. 70:3709–3717. 2010. View Article : Google Scholar : PubMed/NCBI | |
Al-Hakim AK, Zagorska A, Chapman L, Deak M, Peggie M and Alessi DR: Control of AMPK-related kinases by USP9X and atypical Lys(29)/Lys(33)-linked polyubiquitin chains. Biochem J. 411:249–260. 2008. View Article : Google Scholar : PubMed/NCBI | |
Dupont S, Mamidi A, Cordenonsi M, Montagner M, Zacchigna L, Adorno M, Martello G, Stinchfield MJ, Soligo S, Morsut L, et al: FAM/USP9×, a deubiquitinating enzyme essential for TGFbeta signaling, controls Smad4 monoubiquitination. Cell. 136:123–135. 2009. View Article : Google Scholar : PubMed/NCBI | |
Mouchantaf R, Azakir BA, McPherson PS, Millard SM, Wood SA and Angers A: The ubiquitin ligase itch is auto-ubiquitylated in vivo and in vitro but is protected from degradation by interacting with the deubiquitylating enzyme FAM/USP9X. J Biol Chem. 281:38738–38747. 2006. View Article : Google Scholar : PubMed/NCBI | |
Taya S, Yamamoto T, Kano K, Kawano Y, Iwamatsu A, Tsuchiya T, Tanaka K, Kanai-Azuma M, Wood SA, Mattick JS and Kaibuchi K: The Ras target AF-6 is a substrate of the fam deubiquitinating enzyme. J Cell Biol. 142:1053–1062. 1998. View Article : Google Scholar : PubMed/NCBI | |
Vong QP, Cao K, Li HY, Iglesias PA and Zheng Y: Chromosome alignment and segregation regulated by ubiquitination of survivin. Science. 310:1499–1504. 2005. View Article : Google Scholar : PubMed/NCBI | |
Narayanan N, Wang Z, Li L and Yang Y: Arginine methylation of USP9X promotes its interaction with TDRD3 and its anti-apoptotic activities in breast cancer cells. Cell Discov. 3:160482017. View Article : Google Scholar : PubMed/NCBI | |
Murray RZ, Jolly LA and Wood SA: The FAM deubiquitylating enzyme localizes to multiple points of protein trafficking in epithelia, where it associates with E-cadherin and beta-catenin. Mol Biol Cell. 15:1591–1599. 2004. View Article : Google Scholar : PubMed/NCBI | |
Theard D, Labarrade F, Partisani M, Milanini J, Sakagami H, Fon EA, Wood SA, Franco M and Luton F: USP9×-mediated deubiquitination of EFA6 regulates de novo tight junction assembly. EMBO J. 29:1499–1509. 2010. View Article : Google Scholar : PubMed/NCBI | |
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. 463:103–107. 2010. View Article : Google Scholar : PubMed/NCBI | |
Trinkle-Mulcahy L, Boulon S, Lam YW, Urcia R, Boisvert FM, Vandermoere F, Morrice NA, Swift S, Rothbauer U, Leonhardt H and Lamond A: Identifying specific protein interaction partners using quantitative mass spectrometry and bead proteomes. J Cell Biol. 183:223–239. 2008. View Article : Google Scholar : PubMed/NCBI | |
Li X, Song N, Liu L, Liu X, Ding X, Song X, Yang S, Shan L, Zhou X, Su D, et al: USP9X regulates centrosome duplication and promotes breast carcinogenesis. Nat Commun. 8:148662017. View Article : Google Scholar : PubMed/NCBI | |
Engel K, Rudelius M, Slawska J, Jacobs L, Abhari BA, Altmann B, Kurutz J, Rathakrishnan A, Fernandez-Saiz V, Brunner A, et al: USP9X stabilizes XIAP to regulate mitotic cell death and chemoresistance in aggressive B-cell lymphoma. EMBO Mol Med. 8:851–862. 2016. View Article : Google Scholar : PubMed/NCBI | |
Grou CP, Francisco T, Rodrigues TA, Freitas MO, Pinto MP, Carvalho AF, Domingues P, Wood SA, Rodriguez-Borges JE, Sa-Miranda C, et al: Identification of ubiquitin-specific protease 9X (USP9X) as a deubiquitinase acting on ubiquitin-peroxin 5 (PEX5) thioester conjugate. J Biol Chem. 287:12815–12827. 2012. View Article : Google Scholar : PubMed/NCBI | |
Akiyama H, Umezawa Y, Ishida S, Okada K, Nogami A and Miura O: Inhibition of USP9X induces apoptosis in FLT3-ITD-positive AML cells cooperatively by inhibiting the mutant kinase through aggresomal translocation and inducing oxidative stress. Cancer Lett. 453:84–94. 2019. View Article : Google Scholar : PubMed/NCBI | |
Wang P, Wang J, Yao S, Cui M, Cheng Y, Liu W, Gao Z, Hu J, Zhang J and Zhang H: Deubiquitinase USP9X stabilizes RNA m(6)A demethylase ALKBH5 and promotes acute myeloid leukemia cell survival. J Biol Chem. 299:1050552023. View Article : Google Scholar : PubMed/NCBI | |
Akiyama H, Umezawa Y, Watanabe D, Okada K, Ishida S, Nogami A and Miura O: Inhibition of USP9X downregulates JAK2-V617F and induces apoptosis synergistically with BH3 mimetics preferentially in ruxolitinib-persistent JAK2-V617F-positive leukemic cells. Cancers (Basel). 12:4062020. View Article : Google Scholar : PubMed/NCBI | |
Wu Y, Yu X, Yi X, Wu K, Dwabe S, Atefi M, Elshimali Y, Kemp KT II, Bhat K, Haro J, et al: Aberrant phosphorylation of SMAD4 Thr277-mediated USP9×-SMAD4 interaction by free fatty acids promotes breast cancer metastasis. Cancer Res. 77:1383–1394. 2017. View Article : Google Scholar : PubMed/NCBI | |
Li L, Liu T, Li Y, Wu C, Luo K, Yin Y, Chen Y, Nowsheen S, Wu J, Lou Z and Yuan J: The deubiquitinase USP9X promotes tumor cell survival and confers chemoresistance through YAP1 stabilization. Oncogene. 37:2422–2431. 2018. View Article : Google Scholar : PubMed/NCBI | |
Guan T, Yang X, Liang H, Chen J, Chen Y, Zhu Y and Liu T: Deubiquitinating enzyme USP9X regulates metastasis and chemoresistance in triple-negative breast cancer by stabilizing Snail1. J Cell Physiol. 237:2992–3000. 2022. View Article : Google Scholar : PubMed/NCBI | |
Lu H, Lyu Y, Tran L, Lan J, Xie Y, Yang Y, Murugan NL, Wang YJ and Semenza GL: HIF-1 recruits NANOG as a coactivator for TERT gene transcription in hypoxic breast cancer stem cells. Cell Rep. 36:1097572021. View Article : Google Scholar : PubMed/NCBI | |
Jie X, Fong WP, Zhou R, Zhao Y, Zhao Y, Meng R, Zhang S, Dong X, Zhang T, Yang K, et al: USP9X-mediated KDM4C deubiquitination promotes lung cancer radioresistance by epigenetically inducing TGF-β2 transcription. Cell Death Differ. 28:2095–2111. 2021. View Article : Google Scholar : PubMed/NCBI | |
Chen X, Yu C, Gao J, Zhu H, Cui B, Zhang T, Zhou Y, Liu Q, He H, Xiao R, et al: A novel USP9X substrate TTK contributes to tumorigenesis in non-small-cell lung cancer. Theranostics. 8:2348–2360. 2018. View Article : Google Scholar : PubMed/NCBI | |
Kushwaha D, O'Leary C, Cron KR, Deraska P, Zhu K, D'Andrea AD and Kozono D: USP9X inhibition promotes radiation-induced apoptosis in non-small cell lung cancer cells expressing mid-to-high MCL1. Cancer Biol Ther. 16:392–401. 2015. View Article : Google Scholar : PubMed/NCBI | |
Sulkshane P, Pawar SN, Waghole R, Pawar SS, Rajput P, Uthale A, Oak S, Kalkar P, Wani H, Patil R, et al: Elevated USP9X drives early-to-late-stage oral tumorigenesis via stabilisation of anti-apoptotic MCL-1 protein and impacts outcome in oral cancers. Br J Cancer. 125:547–560. 2021. View Article : Google Scholar : PubMed/NCBI | |
Cheng P, Wang J, Waghmare I, Sartini S, Coviello V, Zhang Z, Kim SH, Mohyeldin A, Pavlyukov MS, Minata M, et al: FOXD1-ALDH1A3 signaling is a determinant for the self-renewal and tumorigenicity of mesenchymal glioma stem cells. Cancer Res. 76:7219–7230. 2016. View Article : Google Scholar : PubMed/NCBI | |
Khan OM, Carvalho J, Spencer-Dene B, Mitter R, Frith D, Snijders AP, Wood SA and Behrens A: The deubiquitinase USP9X regulates FBW7 stability and suppresses colorectal cancer. J Clin Invest. 128:1326–1337. 2018. View Article : Google Scholar : PubMed/NCBI | |
Potu H, Peterson LF, Kandarpa M, Pal A, Sun H, Durham A, Harms PW, Hollenhorst PC, Eskiocak U, Talpaz M and Donato NJ: Usp9× regulates Ets-1 ubiquitination and stability to control NRAS expression and tumorigenicity in melanoma. Nat Commun. 8:144492017. View Article : Google Scholar : PubMed/NCBI | |
Chen W, Song J, Liu S, Tang B, Shen L, Zhu J, Fang S, Wu F, Zheng L, Qiu R, et al: USP9X promotes apoptosis in cholangiocarcinoma by modulation expression of KIF1Bbeta via deubiquitinating EGLN3. J Biomed Sci. 28:442021. View Article : Google Scholar : PubMed/NCBI | |
Czabotar PE, Lessene G, Strasser A and Adams JM: Control of apoptosis by the BCL-2 protein family: Implications for physiology and therapy. Nat Rev Mol Cell Biol. 15:49–63. 2014. View Article : Google Scholar : PubMed/NCBI | |
Nagai H, Noguchi T, Homma K, Katagiri K, Takeda K, Matsuzawa A and Ichijo H: Ubiquitin-like sequence in ASK1 plays critical roles in the recognition and stabilization by USP9X and oxidative stress-induced cell death. Mol Cell. 36:805–818. 2009. View Article : Google Scholar : PubMed/NCBI | |
Huntwork-Rodriguez S, Wang B, Watkins T, Ghosh AS, Pozniak CD, Bustos D, Newton K, Kirkpatrick DS and Lewcock JW: JNK-mediated phosphorylation of DLK suppresses its ubiquitination to promote neuronal apoptosis. J Cell Biol. 202:747–763. 2013. View Article : Google Scholar : PubMed/NCBI | |
Lai MC, Chen YP, Li DA, Yu JS, Hung HY and Tarn WY: DDX3 interacts with USP9X and participates in deubiquitination of the anti-apoptotic protein MCL1. FEBS J. 289:1043–1061. 2022. View Article : Google Scholar : PubMed/NCBI | |
Hogh-Binder SA, Klein D, Wolfsperger F, Huber SM, Hennenlotter J, Stenzl A and Rudner J: Protein levels of anti-apoptotic Mcl-1 and the deubiquitinase USP9× are cooperatively upregulated during prostate cancer progression and limit response of prostate cancer cells to radiotherapy. Cancers (Basel). 15:24962023. View Article : Google Scholar : PubMed/NCBI | |
Sun H, Kapuria V, Peterson LF, Fang D, Bornmann WG, Bartholomeusz G, Talpaz M and Donato NJ: Bcr-Abl ubiquitination and Usp9× inhibition block kinase signaling and promote CML cell apoptosis. Blood. 117:3151–3162. 2011. View Article : Google Scholar : PubMed/NCBI | |
Kapuria V, Peterson LF, Fang D, Bornmann WG, Talpaz M and Donato NJ: Deubiquitinase inhibition by small-molecule WP1130 triggers aggresome formation and tumor cell apoptosis. Cancer Res. 70:9265–9276. 2010. View Article : Google Scholar : PubMed/NCBI | |
Karpel-Massler G, Ishida CT, Bianchetti E, Shu C, Perez-Lorenzo R, Horst B, Banu M, Roth KA, Bruce JN, Canoll P, et al: Inhibition of mitochondrial matrix chaperones and antiapoptotic Bcl-2 family proteins empower antitumor therapeutic responses. Cancer Res. 77:3513–3526. 2017. View Article : Google Scholar : PubMed/NCBI | |
Kim S, Woo SM, Min KJ, Seo SU, Lee TJ, Kubatka P, Kim DE and Kwon TK: WP1130 enhances TRAIL-induced apoptosis through USP9X-dependent miR-708-mediated downregulation of c-FLIP. Cancers (Basel). 11:3442019. View Article : Google Scholar : PubMed/NCBI | |
Liu Y, Xu X, Lin P, He Y, Zhang Y, Cao B, Zhang Z, Sethi G, Liu J, Zhou X and Mao X: Inhibition of the deubiquitinase USP9× induces pre-B cell homeobox 1 (PBX1) degradation and thereby stimulates prostate cancer cell apoptosis. J Biol Chem. 294:4572–4582. 2019. View Article : Google Scholar : PubMed/NCBI | |
Dominguez-Brauer C, Thu KL, Mason JM, Blaser H, Bray MR and Mak TW: Targeting mitosis in cancer: Emerging strategies. Mol Cell. 60:524–536. 2015. View Article : Google Scholar : PubMed/NCBI | |
Motofei IG: Biology of cancer: Understanding the supracellular control of mitosis in physiological processes and malignancy. Semin Cancer Biol. 92:42–44. 2023. View Article : Google Scholar : PubMed/NCBI | |
Schoonen PM, Talens F, Stok C, Gogola E, Heijink AM, Bouwman P, Foijer F, Tarsounas M, Blatter S, Jonkers J, et al: Progression through mitosis promotes PARP inhibitor-induced cytotoxicity in homologous recombination-deficient cancer cells. Nat Commun. 8:159812017. View Article : Google Scholar : PubMed/NCBI | |
Skowyra A, Allan LA, Saurin AT and Clarke PR: USP9X limits mitotic checkpoint complex turnover to strengthen the spindle assembly checkpoint and guard against chromosomal instability. Cell Rep. 23:852–865. 2018. View Article : Google Scholar : PubMed/NCBI | |
Dietachmayr M, Rathakrishnan A, Karpiuk O, von Zweydorf F, Engleitner T, Fernandez-Saiz V, Schenk P, Ueffing M, Rad R, Eilers M, et al: Antagonistic activities of CDC14B and CDK1 on USP9X regulate WT1-dependent mitotic transcription and survival. Nat Commun. 11:12682020. View Article : Google Scholar : PubMed/NCBI | |
Wang Q, Tang Y, Xu Y, Xu S, Jiang Y, Dong Q, Zhou Y and Ge W: The X-linked deubiquitinase USP9X is an integral component of centrosome. J Biol Chem. 292:12874–12884. 2017. View Article : Google Scholar : PubMed/NCBI | |
Clancy A, Heride C, Pinto-Fernandez A, Elcocks H, Kallinos A, Kayser-Bricker KJ, Wang W, Smith V, Davis S, Fessler S, et al: The deubiquitylase USP9X controls ribosomal stalling. J Cell Biol. 220:2020042112021. View Article : Google Scholar | |
Weimer JM and Anton ES: Doubling up on microtubule stabilizers: Synergistic functions of doublecortin-like kinase and doublecortin in the developing cerebral cortex. Neuron. 49:3–4. 2006. View Article : Google Scholar : PubMed/NCBI | |
Gleeson JG, Lin PT, Flanagan LA and Walsh CA: Doublecortin is a microtubule-associated protein and is expressed widely by migrating neurons. Neuron. 23:257–271. 1999. View Article : Google Scholar : PubMed/NCBI | |
Kharitidi D, Apaja PM, Manteghi S, Suzuki K, Malitskaya E, Roldan A, Gingras MC, Takagi J, Lukacs GL and Pause A: Interplay of endosomal pH and ligand occupancy in integrin alpha5beta1 ubiquitination, endocytic sorting, and cell migration. Cell Rep. 13:599–609. 2015. View Article : Google Scholar : PubMed/NCBI | |
Zhu H, Kavsak P, Abdollah S, Wrana JL and Thomsen GH: A SMAD ubiquitin ligase targets the BMP pathway and affects embryonic pattern formation. Nature. 400:687–693. 1999. View Article : Google Scholar : PubMed/NCBI | |
Ebisawa T, Fukuchi M, Murakami G, Chiba T, Tanaka K, Imamura T and Miyazono K: Smurf1 interacts with transforming growth factor-beta type I receptor through Smad7 and induces receptor degradation. J Biol Chem. 276:12477–12480. 2001. View Article : Google Scholar : PubMed/NCBI | |
Xie Y, Avello M, Schirle M, McWhinnie E, Feng Y, Bric-Furlong E, Wilson C, Nathans R, Zhang J, Kirschner MW, et al: Deubiquitinase FAM/USP9X interacts with the E3 ubiquitin ligase SMURF1 protein and protects it from ligase activity-dependent self-degradation. J Biol Chem. 288:2976–2985. 2013. View Article : Google Scholar : PubMed/NCBI | |
Wang T, Jing B, Sun B, Liao Y, Song H, Xu D, Guo W, Li K, Hu M, Liu S, et al: Stabilization of PTGES by deubiquitinase USP9X promotes metastatic features of lung cancer via PGE(2) signaling. Am J Cancer Res. 9:1145–1160. 2019.PubMed/NCBI | |
Harrigan JA, Jacq X, Martin NM and Jackson SP: Deubiquitylating enzymes and drug discovery: Emerging opportunities. Nat Rev Drug Discov. 17:57–78. 2018. View Article : Google Scholar : PubMed/NCBI | |
Negrini S, Gorgoulis VG and Halazonetis TD: Genomic instability-an evolving hallmark of cancer. Nat Rev Mol Cell Biol. 11:220–228. 2010. View Article : Google Scholar : PubMed/NCBI | |
Kang JW, Zhan Z, Ji G, Sang Y, Zhou D, Li Y, Feng H and Cheng T: PUMA facilitates EMI1-promoted cytoplasmic Rad51 ubiquitination and inhibits DNA repair in stem and progenitor cells. Signal Transduct Target Ther. 6:1292021. View Article : Google Scholar : PubMed/NCBI | |
McGarry E, Gaboriau D, Rainey MD, Restuccia U, Bachi A and Santocanale C: The deubiquitinase USP9X maintains DNA replication fork stability and DNA damage checkpoint responses by regulating CLASPIN during S-Phase. Cancer Res. 76:2384–2393. 2016. View Article : Google Scholar : PubMed/NCBI | |
Wolfsperger F, Hogh-Binder SA, Schittenhelm J, Psaras T, Ritter V, Bornes L, Huber SM, Jendrossek V and Rudner J: Deubiquitylating enzyme USP9× regulates radiosensitivity in glioblastoma cells by Mcl-1-dependent and -independent mechanisms. Cell Death Dis. 7:20392016. View Article : Google Scholar : PubMed/NCBI | |
Lautenbacher L, Samaras P, Muller J, Grafberger A, Shraideh M, Rank J, Fuchs ST, Schmidt TK, The M, Dallago C, et al: ProteomicsDB: Toward a FAIR open-source resource for life-science research. Nucleic Acids Res. 50:D1541–D1552. 2022. View Article : Google Scholar : PubMed/NCBI | |
Zhang C, Cai TY, Zhu H, Yang LQ, Jiang H, Dong XW, Hu YZ, Lin NM, He QJ and Yang B: Synergistic antitumor activity of gemcitabine and ABT-737 in vitro and in vivo through disrupting the interaction of USP9X and Mcl-1. Mol Cancer Ther. 10:1264–1275. 2011. View Article : Google Scholar : PubMed/NCBI | |
Oosterkamp HM, Hijmans EM, Brummelkamp TR, Canisius S, Wessels LF, Zwart W and Bernards R: USP9X downregulation renders breast cancer cells resistant to tamoxifen. Cancer Res. 74:3810–3820. 2014. View Article : Google Scholar : PubMed/NCBI | |
Tang Z, Li C, Kang B, Gao G, Li C and Zhang Z: GEPIA: A web server for cancer and normal gene expression profiling and interactive analyses. Nucleic Acids Res. 45:W98–W102. 2017. View Article : Google Scholar : PubMed/NCBI | |
Zhang C, Qian H, Liu K, Zhao W and Wang L: A feedback loop regulation of LINC01433 and YAP promotes malignant behavior in gastric cancer cells. Onco Targets Ther. 12:7949–7962. 2019. View Article : Google Scholar : PubMed/NCBI | |
Chen H, Yang F, Li X, Gong ZJ and Wang LW: Long noncoding RNA LNC473 inhibits the ubiquitination of survivin via association with USP9X and enhances cell proliferation and invasion in hepatocellular carcinoma cells. Biochem Biophys Res Commun. 499:702–710. 2018. View Article : Google Scholar : PubMed/NCBI | |
Xu X, Wang S, Wang H, Pan C, Yang W and Yu J: Hsa_circ_0008434 regulates USP9X expression by sponging miR-6838-5p to promote gastric cancer growth, migration and invasion. BMC Cancer. 21:12892021. View Article : Google Scholar : PubMed/NCBI | |
Shen G, Lin Y, Yang X, Zhang J, Xu Z and Jia H: MicroRNA-26b inhibits epithelial-mesenchymal transition in hepatocellular carcinoma by targeting USP9X. BMC Cancer. 14:3932014. View Article : Google Scholar : PubMed/NCBI | |
Chen W, Huang Y, Zhang S, Zheng X, Xie S, Mao J, Cai Y, Lu X, Hu L, Shen J, et al: MicroRNA-212 suppresses nonsmall lung cancer invasion and migration by regulating ubiquitin-specific protease-9. J Cell Biochem. 120:6482–6489. 2019. View Article : Google Scholar : PubMed/NCBI | |
Chen W, Zhou Y, Zhi X, Ma T, Liu H, Chen BW, Zheng X, Xie S, Zhao B, Feng X, et al: Delivery of miR-212 by chimeric peptide-condensed supramolecular nanoparticles enhances the sensitivity of pancreatic ductal adenocarcinoma to doxorubicin. Biomaterials. 192:590–600. 2019. View Article : Google Scholar : PubMed/NCBI | |
Guo H, Zhang X, Chen Q, Bao Y, Dong C and Wang X: miR-132 suppresses the migration and invasion of lung cancer cells by blocking USP9X-induced epithelial-mesenchymal transition. Am J Transl Res. 10:224–234. 2018.PubMed/NCBI | |
Chen E, Li E, Liu H, Zhou Y, Wen L, Wang J, Wang Y, Ye L and Liang T: miR-26b enhances the sensitivity of hepatocellular carcinoma to Doxorubicin via USP9X-dependent degradation of p53 and regulation of autophagy. Int J Biol Sci. 17:781–795. 2021. View Article : Google Scholar : PubMed/NCBI | |
Madan V, Li J, Zhou S, Teoh WW, Han L, Meggendorfer M, Malcovati L, Cazzola M, Ogawa S, Haferlach T, et al: Distinct and convergent consequences of splice factor mutations in myelodysplastic syndromes. Am J Hematol. 95:133–143. 2020. View Article : Google Scholar : PubMed/NCBI | |
Aqaqe N, Yassin M, Yassin AA, Ershaid N, Katz-Even C, Zipin-Roitman A, Kugler E, Lechman ER, Gan OI, Mitchell A, et al: An ERG enhancer-based reporter identifies leukemia cells with elevated leukemogenic potential driven by ERG-USP9X feed-forward regulation. Cancer Res. 79:3862–3876. 2019. View Article : Google Scholar : PubMed/NCBI | |
Shen SM, Zhang C, Ge MK, Dong SS, Xia L, He P, Zhang N, Ji Y, Yang S, Yu Y, et al: PTENalpha and PTENbeta promote carcinogenesis through WDR5 and H3K4 trimethylation. Nat Cell Biol. 21:1436–1448. 2019. View Article : Google Scholar : PubMed/NCBI | |
Kapoor S, Natarajan K, Baldwin PR, Doshi KA, Lapidus RG, Mathias TJ, Scarpa M, Trotta R, Davila E, Kraus M, et al: Concurrent inhibition of pim and FLT3 kinases enhances apoptosis of FLT3-ITD acute myeloid leukemia cells through increased Mcl-1 proteasomal degradation. Clin Cancer Res. 24:234–247. 2018. View Article : Google Scholar : PubMed/NCBI | |
Sisoudiya SD, Mishra P, Li H, Schraw JM, Scheurer ME, Salvi S, Doddapaneni H, Muzny D, Mitchell D, Taylor O, et al: Identification of USP9X as a leukemia susceptibility gene. Blood Adv. 7:4563–4575. 2023. View Article : Google Scholar : PubMed/NCBI | |
Schwartzman O, Savino AM, Gombert M, Palmi C, Cario G, Schrappe M, Eckert C, von Stackelberg A, Huang JY, Hameiri-Grossman M, et al: Suppressors and activators of JAK-STAT signaling at diagnosis and relapse of acute lymphoblastic leukemia in Down syndrome. Proc Natl Acad Sci USA. 114:4030–4039. 2017. View Article : Google Scholar | |
Moroishi T, Hansen CG and Guan KL: The emerging roles of YAP and TAZ in cancer. Nat Rev Cancer. 15:73–79. 2015. View Article : Google Scholar : PubMed/NCBI | |
Demark-Wahnefried W, Platz EA, Ligibel JA, Blair CK, Courneya KS, Meyerhardt JA, Ganz PA, Rock CL, Schmitz KH, Wadden T, et al: The role of obesity in cancer survival and recurrence. Cancer Epidemiol Biomarkers Prev. 21:1244–1259. 2012. View Article : Google Scholar : PubMed/NCBI | |
Jaiswal A, Murakami K, Elia A, Shibahara Y, Done SJ, Wood SA, Donato NJ, Ohashi PS and Reedijk M: Therapeutic inhibition of USP9×-mediated Notch signaling in triple-negative breast cancer. Proc Natl Acad Sci USA. 118:e21015921182021. View Article : Google Scholar : PubMed/NCBI | |
Yan J, Zhong N, Liu G, Chen K, Liu X, Su L and Singhal S: Usp9×- and Noxa-mediated Mcl-1 downregulation contributes to pemetrexed-induced apoptosis in human non-small-cell lung cancer cells. Cell Death Dis. 5:e13162014. View Article : Google Scholar : PubMed/NCBI | |
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A and Bray F: Global cancer statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 71:209–249. 2021. View Article : Google Scholar : PubMed/NCBI | |
Perez-Mancera PA, Rust AG, van der Weyden L, Kristiansen G, Li A, Sarver AL, Silverstein KA, Grutzmann R, Aust D, Rummele P, et al: The deubiquitinase USP9X suppresses pancreatic ductal adenocarcinoma. Nature. 486:266–270. 2012. View Article : Google Scholar : PubMed/NCBI | |
Pal A, Dziubinski M, Di Magliano MP, Simeone DM, Owens S, Thomas D, Peterson L, Potu H, Talpaz M and Donato NJ: Usp9× promotes survival in human pancreatic cancer and its inhibition suppresses pancreatic ductal adenocarcinoma in vivo tumor growth. Neoplasia. 20:152–164. 2018. View Article : Google Scholar : PubMed/NCBI | |
Guo M, Luo G, Jin K, Long J, Cheng H, Lu Y, Wang Z, Yang C, Xu J, Ni Q, et al: Somatic genetic variation in solid pseudopapillary tumor of the pancreas by whole exome sequencing. Int J Mol Sci. 18:812017. View Article : Google Scholar : PubMed/NCBI | |
Perurena N, Lock R, Davis RA, Raghavan S, Pilla NF, Ng R, Loi P, Guild CJ, Miller AL, Sicinska E, et al: USP9X mediates an acute adaptive response to MAPK suppression in pancreatic cancer but creates multiple actionable therapeutic vulnerabilities. Cell Rep Med. 4:1010072023. View Article : Google Scholar : PubMed/NCBI | |
Chen Z, Wang HW, Wang S, Fan L, Feng S, Cai X, Peng C, Wu X, Lu J, Chen D, et al: USP9X deubiquitinates ALDH1A3 and maintains mesenchymal identity in glioblastoma stem cells. J Clin Invest. 129:2043–2055. 2019. View Article : Google Scholar : PubMed/NCBI | |
Nguyen HT, Andrejeva D, Gupta R, Choudhary C, Hong X, Eichhorn PJ, Loya AC and Cohen SM: Deubiquitylating enzyme USP9× regulates hippo pathway activity by controlling angiomotin protein turnover. Cell Discov. 2:160012016. View Article : Google Scholar : PubMed/NCBI | |
Bartholomeusz G, Talpaz M, Bornmann W, Kong LY and Donato NJ: Degrasyn activates proteasomal-dependent degradation of c-Myc. Cancer Res. 67:3912–3918. 2007. View Article : Google Scholar : PubMed/NCBI | |
Luo H, Jing B, Xia Y, Zhang Y, Hu M, Cai H, Tong Y, Zhou L, Yang L, Yang J, et al: WP1130 reveals USP24 as a novel target in T-cell acute lymphoblastic leukemia. Cancer Cell Int. 19:562019. View Article : Google Scholar : PubMed/NCBI | |
Peterson LF, Sun H, Liu Y, Potu H, Kandarpa M, Ermann M, Courtney SM, Young M, Showalter HD, Sun D, et al: Targeting deubiquitinase activity with a novel small-molecule inhibitor as therapy for B-cell malignancies. Blood. 125:3588–3597. 2015. View Article : Google Scholar : PubMed/NCBI | |
Cui J, Sun W, Hao X, Wei M, Su X, Zhang Y, Su L and Liu X: EHMT2 inhibitor BIX-01294 induces apoptosis through PMAIP1-USP9X-MCL1 axis in human bladder cancer cells. Cancer Cell Int. 15:42015. View Article : Google Scholar : PubMed/NCBI | |
Boise LH: DUB-ling down on B-cell malignancies. Blood. 125:3522–3523. 2015. View Article : Google Scholar : PubMed/NCBI | |
Chou DH, Vetere A, Choudhary A, Scully SS, Schenone M, Tang A, Gomez R, Burns SM, Lundh M, Vital T, et al: Kinase-independent small-molecule inhibition of JAK-STAT signaling. J Am Chem Soc. 137:7929–7934. 2015. View Article : Google Scholar : PubMed/NCBI | |
Lawson AP, Long MJC, Coffey RT, Qian Y, Weerapana E, El Oualid F and Hedstrom L: Naturally occurring isothiocyanates exert anticancer effects by inhibiting deubiquitinating enzymes. Cancer Res. 75:5130–5142. 2015. View Article : Google Scholar : PubMed/NCBI |