The SUMOylation and ubiquitination crosstalk in cancer.
Cancer therapy
Crosstalk
SUMOylation
Tumorigenesis
Ubiquitination
Journal
Journal of cancer research and clinical oncology
ISSN: 1432-1335
Titre abrégé: J Cancer Res Clin Oncol
Pays: Germany
ID NLM: 7902060
Informations de publication
Date de publication:
Nov 2023
Nov 2023
Historique:
received:
17
07
2023
accepted:
16
08
2023
medline:
2
11
2023
pubmed:
29
8
2023
entrez:
28
8
2023
Statut:
ppublish
Résumé
The cancer occurrence and progression are largely affected by the post-translational modifications (PTMs) of proteins. Currently, it has been shown that the relationship between ubiquitination and SUMOylation is highly complex and interactive. SUMOylation affects the process of ubiquitination and degradation of substrates. Contrarily, SUMOylation-related proteins are also regulated by the ubiquitination process thus altering their protein levels or activity. Emerging evidence suggests that the abnormal regulation between this crosstalk may lead to tumorigenesis. In this review, we have discussed the study of the relationship between ubiquitination and SUMOylation, as well as the possibility of a corresponding application in tumor therapy. The relevant literatures from PubMed have been reviewed for this article. The interaction between ubiquitination and SUMOylation is crucial for the occurrence and development of cancer. A greater understanding of the crosstalk of SUMOylation and ubiquitination may be more conducive to the development of more selective and effective SUMOylation inhibitors, as well as a promotion of synergy with other tumor treatment strategies.
Sections du résumé
BACKGROUND
BACKGROUND
The cancer occurrence and progression are largely affected by the post-translational modifications (PTMs) of proteins. Currently, it has been shown that the relationship between ubiquitination and SUMOylation is highly complex and interactive. SUMOylation affects the process of ubiquitination and degradation of substrates. Contrarily, SUMOylation-related proteins are also regulated by the ubiquitination process thus altering their protein levels or activity. Emerging evidence suggests that the abnormal regulation between this crosstalk may lead to tumorigenesis.
PURPOSE
OBJECTIVE
In this review, we have discussed the study of the relationship between ubiquitination and SUMOylation, as well as the possibility of a corresponding application in tumor therapy.
METHODS
METHODS
The relevant literatures from PubMed have been reviewed for this article.
CONCLUSION
CONCLUSIONS
The interaction between ubiquitination and SUMOylation is crucial for the occurrence and development of cancer. A greater understanding of the crosstalk of SUMOylation and ubiquitination may be more conducive to the development of more selective and effective SUMOylation inhibitors, as well as a promotion of synergy with other tumor treatment strategies.
Identifiants
pubmed: 37640846
doi: 10.1007/s00432-023-05310-z
pii: 10.1007/s00432-023-05310-z
doi:
Substances chimiques
Proteins
0
Types de publication
Journal Article
Review
Langues
eng
Sous-ensembles de citation
IM
Pagination
16123-16146Subventions
Organisme : Natural Science Foundation of Ningbo
ID : No.2022J040
Organisme : Natural Science Foundation of Ningbo
ID : No.2022J230
Organisme : Natural Science Foundation of Ningbo
ID : No.2021J065
Organisme : National Natural Science Foundation of China
ID : 32270821
Organisme : Fundamental Research Funds for the Provincial Universities of Zhejiang,
ID : No. SJLZ2022004
Informations de copyright
© 2023. The Author(s), under exclusive licence to Springer-Verlag GmbH Germany, part of Springer Nature.
Références
Abdel-Hafiz H, Takimoto GS, Tung L, Horwitz KB (2002) The inhibitory function in human progesterone receptor N termini binds SUMO-1 protein to regulate autoinhibition and transrepression. J Biol Chem 277:33950–33956. https://doi.org/10.1074/jbc.M204573200
doi: 10.1074/jbc.M204573200
pubmed: 12114521
Albadari N, Deng S, Li W (2019) The transcriptional factors HIF-1 and HIF-2 and their novel inhibitors in cancer therapy. Expert Opin Drug Discov 14:667–682. https://doi.org/10.1080/17460441.2019.1613370
doi: 10.1080/17460441.2019.1613370
pubmed: 31070059
pmcid: 6559821
Alsamman K, El-Masry OS (2018) Interferon regulatory factor 1 inactivation in human cancer. Biosci Rep. https://doi.org/10.1042/bsr20171672
An J, Wang C, Deng Y, Yu L, Huang H (2014) Destruction of full-length androgen receptor by wild-type SPOP, but not prostate-cancer-associated mutants. Cell Rep 6:657–669. https://doi.org/10.1016/j.celrep.2014.01.013
doi: 10.1016/j.celrep.2014.01.013
pubmed: 24508459
pmcid: 4361392
Anderson DD, Eom JY, Stover PJ (2012) Competition between sumoylation and ubiquitination of serine hydroxymethyltransferase 1 determines its nuclear localization and its accumulation in the nucleus. J Biol Chem 287:4790–4799. https://doi.org/10.1074/jbc.M111.302174
doi: 10.1074/jbc.M111.302174
pubmed: 22194612
Annunziata CM, Davis RE, Demchenko Y, Bellamy W, Gabrea A, Zhan F, Lenz G, Hanamura I, Wright G, Xiao W et al (2007) Frequent engagement of the classical and alternative NF-kappaB pathways by diverse genetic abnormalities in multiple myeloma. Cancer Cell 12:115–130. https://doi.org/10.1016/j.ccr.2007.07.004
doi: 10.1016/j.ccr.2007.07.004
pubmed: 17692804
pmcid: 2730509
Armstrong MJ, Stang MT, Liu Y, Yan J, Pizzoferrato E, Yim JH (2015) IRF-1 inhibits NF-κB activity, suppresses TRAF2 and cIAP1 and induces breast cancer cell specific growth inhibition. Cancer Biol Ther 16:1029–1041. https://doi.org/10.1080/15384047.2015.1046646
doi: 10.1080/15384047.2015.1046646
pubmed: 26011589
pmcid: 4622679
Ashikari D, Takayama K, Tanaka T, Suzuki Y, Obinata D, Fujimura T, Urano T, Takahashi S, Inoue S (2017) Androgen induces G3BP2 and SUMO-mediated p53 nuclear export in prostate cancer. Oncogene 36:6272–6281. https://doi.org/10.1038/onc.2017.225
doi: 10.1038/onc.2017.225
pubmed: 28692047
Aziz D, Lee C, Chin V, Fernandez KJ, Phan Z, Waring P, Caldon CE (2022) High cyclin E1 protein, but not gene amplification, is prognostic for basal-like breast cancer. J Pathol Clin Res 8:355–370. https://doi.org/10.1002/cjp2.269
doi: 10.1002/cjp2.269
pubmed: 35384378
pmcid: 9161326
Baik H, Boulanger M, Hosseini M, Kowalczyk J, Zaghdoudi S, Salem T, Sarry JE, Hicheri Y, Cartron G, Piechaczyk M et al (2018) Targeting the SUMO pathway primes all-trans retinoic acid-induced differentiation of nonpromyelocytic acute myeloid leukemias. Cancer Res 78:2601–2613. https://doi.org/10.1158/0008-5472.Can-17-3361
doi: 10.1158/0008-5472.Can-17-3361
pubmed: 29487199
Bawa-Khalfe T, Yang FM, Ritho J, Lin HK, Cheng J, Yeh ET (2017) SENP1 regulates PTEN stability to dictate prostate cancer development. Oncotarget 8:17651–17664. https://doi.org/10.18632/oncotarget.13283
doi: 10.18632/oncotarget.13283
pubmed: 27852060
Beishline K, Azizkhan-Clifford J (2015) Sp1 and the ‘hallmarks of cancer.’ FEBS J 282:224–258. https://doi.org/10.1111/febs.13148
doi: 10.1111/febs.13148
pubmed: 25393971
Bellail AC, Olson JJ, Yang X, Chen ZJ, Hao C (2012) A20 ubiquitin ligase-mediated polyubiquitination of RIP1 inhibits caspase-8 cleavage and TRAIL-induced apoptosis in glioblastoma. Cancer Discov 2:140–155. https://doi.org/10.1158/2159-8290.Cd-11-0172
doi: 10.1158/2159-8290.Cd-11-0172
pubmed: 22585859
pmcid: 3354650
Bellail AC, Olson JJ, Hao C (2014) SUMO1 modification stabilizes CDK6 protein and drives the cell cycle and glioblastoma progression. Nat Commun 5:4234. https://doi.org/10.1038/ncomms5234
doi: 10.1038/ncomms5234
pubmed: 24953629
Bellail AC, Jin HR, Lo HY, Jung SH, Hamdouchi C, Kim D, Higgins RK, Blanck M, le Sage C, Cross BCS et al (2021) Ubiquitination and degradation of SUMO1 by small-molecule degraders extends survival of mice with patient-derived tumors. Sci Transl Med 13:eabh1486. https://doi.org/10.1126/scitranslmed.abh1486
doi: 10.1126/scitranslmed.abh1486
pubmed: 34644148
pmcid: 9450956
Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J, Barretina J, Boehm JS, Dobson J, Urashima M et al (2010) The landscape of somatic copy-number alteration across human cancers. Nature 463:899–905. https://doi.org/10.1038/nature08822
doi: 10.1038/nature08822
pubmed: 20164920
pmcid: 2826709
Berta MA, Mazure N, Hattab M, Pouysségur J, Brahimi-Horn MC (2007) SUMOylation of hypoxia-inducible factor-1alpha reduces its transcriptional activity. Biochem Biophys Res Commun 360:646–652. https://doi.org/10.1016/j.bbrc.2007.06.103
doi: 10.1016/j.bbrc.2007.06.103
pubmed: 17610843
Bian Z, Zhou M, Cui K, Yang F, Cao Y, Sun S, Liu B, Gong L, Li J, Wang X et al (2021) SNHG17 promotes colorectal tumorigenesis and metastasis via regulating Trim23-PES1 axis and miR-339-5p-FOSL2-SNHG17 positive feedback loop. J Exp Clin Cancer Res CR 40:360. https://doi.org/10.1186/s13046-021-02162-8
doi: 10.1186/s13046-021-02162-8
pubmed: 34782005
Biederstädt A, Hassan Z, Schneeweis C, Schick M, Schneider L, Muckenhuber A, Hong Y, Siegers G, Nilsson L, Wirth M et al (2020) SUMO pathway inhibition targets an aggressive pancreatic cancer subtype. Gut 69:1472–1482. https://doi.org/10.1136/gutjnl-2018-317856
doi: 10.1136/gutjnl-2018-317856
pubmed: 32001555
Blanco-Aparicio C, Carnero A (2013) Pim kinases in cancer: diagnostic, prognostic and treatment opportunities. Biochem Pharmacol 85:629–643. https://doi.org/10.1016/j.bcp.2012.09.018
doi: 10.1016/j.bcp.2012.09.018
pubmed: 23041228
Brandt M, Szewczuk LM, Zhang H, Hong X, McCormick PM, Lewis TS, Graham TI, Hung ST, Harper-Jones AD, Kerrigan JJ et al (2013) Development of a high-throughput screen to detect inhibitors of TRPS1 sumoylation. Assay Drug Dev Technol 11:308–325. https://doi.org/10.1089/adt.2012.501
doi: 10.1089/adt.2012.501
pubmed: 23772552
Bueno MT, Richard S (2013) SUMOylation negatively modulates target gene occupancy of the KDM5B, a histone lysine demethylase. Epigenetics 8:1162–1175. https://doi.org/10.4161/epi.26112
doi: 10.4161/epi.26112
pubmed: 23970103
Buschmann T, Lerner D, Lee CG, Ronai Z (2001) The Mdm-2 amino terminus is required for Mdm2 binding and SUMO-1 conjugation by the E2 SUMO-1 conjugating enzyme Ubc9. J Biol Chem 276:40389–40395. https://doi.org/10.1074/jbc.M103786200
doi: 10.1074/jbc.M103786200
pubmed: 11384992
Capili AD, Lima CD (2007) Taking it step by step: mechanistic insights from structural studies of ubiquitin/ubiquitin-like protein modification pathways. Curr Opin Struct Biol 17:726–735. https://doi.org/10.1016/j.sbi.2007.08.018
doi: 10.1016/j.sbi.2007.08.018
pubmed: 17919899
pmcid: 2174906
Chandhoke AS, Karve K, Dadakhujaev S, Netherton S, Deng L, Bonni S (2016) The ubiquitin ligase Smurf2 suppresses TGFβ-induced epithelial–mesenchymal transition in a sumoylation-regulated manner. Cell Death Differ 23:876–888. https://doi.org/10.1038/cdd.2015.152
doi: 10.1038/cdd.2015.152
pubmed: 26679521
Chandhoke AS, Chanda A, Karve K, Deng L, Bonni S (2017) The PIAS3-Smurf2 sumoylation pathway suppresses breast cancer organoid invasiveness. Oncotarget 8:21001–21014. https://doi.org/10.18632/oncotarget.15471
doi: 10.18632/oncotarget.15471
pubmed: 28423498
pmcid: 5400561
Chang HM, Yeh ETH (2020) SUMO: from bench to bedside. Physiol Rev 100:1599–1619. https://doi.org/10.1152/physrev.00025.2019
doi: 10.1152/physrev.00025.2019
pubmed: 32666886
pmcid: 7717128
Chen L, Chen J (2003) MDM2-ARF complex regulates p53 sumoylation. Oncogene 22:5348–5357. https://doi.org/10.1038/sj.onc.1206851
doi: 10.1038/sj.onc.1206851
pubmed: 12917636
Chen L, Chen DT, Kurtyka C, Rawal B, Fulp WJ, Haura EB, Cress WD (2012) Tripartite motif containing 28 (Trim28) can regulate cell proliferation by bridging HDAC1/E2F interactions. J Biol Chem 287:40106–40118. https://doi.org/10.1074/jbc.M112.380865
doi: 10.1074/jbc.M112.380865
pubmed: 23060449
pmcid: 3504725
Chen XL, Lei L, Hong LL, Ling ZQ (2018) Potential role of NDRG2 in reprogramming cancer metabolism and epithelial-to-mesenchymal transition. Histol Histopathol 33:655–663. https://doi.org/10.14670/hh-11-957
doi: 10.14670/hh-11-957
pubmed: 29285747
Cheng J, Kang X, Zhang S, Yeh ET (2007) SUMO-specific protease 1 is essential for stabilization of HIF1alpha during hypoxia. Cell 131:584–595. https://doi.org/10.1016/j.cell.2007.08.045
doi: 10.1016/j.cell.2007.08.045
pubmed: 17981124
pmcid: 2128732
Cheng L, Li J, Han Y, Lin J, Niu C, Zhou Z, Yuan B, Huang K, Li J, Jiang K et al (2012) PES1 promotes breast cancer by differentially regulating ERα and ERβ. J Clin Invest 122:2857–2870. https://doi.org/10.1172/jci62676
doi: 10.1172/jci62676
pubmed: 22820289
pmcid: 3408741
Citro S, Chiocca S (2017) Assessing the role of paralog-specific sumoylation of HDAC1. Methods Mol Biol (Clifton, NJ) 1510:329–337. https://doi.org/10.1007/978-1-4939-6527-4_24
doi: 10.1007/978-1-4939-6527-4_24
Czerwińska P, Mazurek S, Wiznerowicz M (2017) The complexity of TRIM28 contribution to cancer. J Biomed Sci 24:63. https://doi.org/10.1186/s12929-017-0374-4
doi: 10.1186/s12929-017-0374-4
pubmed: 28851455
pmcid: 5574234
Dai C, Heemers H, Sharifi N (2017) Androgen signaling in prostate cancer. Cold Spring Harbor Perspect Med. https://doi.org/10.1101/cshperspect.a030452
doi: 10.1101/cshperspect.a030452
Deng S, Zhou H, Xiong R, Lu Y, Yan D, Xing T, Dong L, Tang E, Yang H (2007) Over-expression of genes and proteins of ubiquitin specific peptidases (USPs) and proteasome subunits (PSs) in breast cancer tissue observed by the methods of RFDD-PCR and proteomics. Breast Cancer Res Treat 104:21–30. https://doi.org/10.1007/s10549-006-9393-7
doi: 10.1007/s10549-006-9393-7
pubmed: 17004105
Denuc A, Bosch-Comas A, Gonzàlez-Duarte R, Marfany G (2009) The UBA-UIM domains of the USP25 regulate the enzyme ubiquitination state and modulate substrate recognition. PloS One 4:e5571. https://doi.org/10.1371/journal.pone.0005571
doi: 10.1371/journal.pone.0005571
pubmed: 19440361
pmcid: 2679190
Devine T, Dai MS (2013) Targeting the ubiquitin-mediated proteasome degradation of p53 for cancer therapy. Curr Pharm Des 19:3248–3262. https://doi.org/10.2174/1381612811319180009
doi: 10.2174/1381612811319180009
pubmed: 23151129
pmcid: 3637405
Diets IJ, Hoyer J, Ekici AB, Popp B, Hoogerbrugge N, van Reijmersdal SV, Bhaskaran R, Hadjihannas M, Vasileiou G, Thiel CT et al (2019) TRIM28 haploinsufficiency predisposes to Wilms tumor. Int J Cancer 145:941–951. https://doi.org/10.1002/ijc.32167
doi: 10.1002/ijc.32167
pubmed: 30694527
Ding B, Sun Y, Huang J (2012) Overexpression of SKI oncoprotein leads to p53 degradation through regulation of MDM2 protein sumoylation. J Biol Chem 287:14621–14630. https://doi.org/10.1074/jbc.M111.301523
doi: 10.1074/jbc.M111.301523
pubmed: 22411991
pmcid: 3340287
Dong XY, Fu X, Fan S, Guo P, Su D, Dong JT (2012) Oestrogen causes ATBF1 protein degradation through the oestrogen-responsive E3 ubiquitin ligase EFP. Biochem J 444:581–590. https://doi.org/10.1042/bj20111890
doi: 10.1042/bj20111890
pubmed: 22452784
Dong G, Ma G, Wu R, Liu J, Liu M, Gao A, Li X, Jun A, Liu X, Zhang Z et al (2020) ZFHX3 promotes the proliferation and tumor growth of ER-positive breast cancer cells likely by enhancing stem-like features and MYC and TBX3 transcription. Cancers. https://doi.org/10.3390/cancers12113415
doi: 10.3390/cancers12113415
pubmed: 33396603
pmcid: 7794746
Dong X, Liu Z, Zhang E, Zhang P, Wang Y, Hang J, Li Q (2021) USP39 promotes tumorigenesis by stabilizing and deubiquitinating SP1 protein in hepatocellular carcinoma. Cell Signal 85:110068. https://doi.org/10.1016/j.cellsig.2021.110068
doi: 10.1016/j.cellsig.2021.110068
pubmed: 34197957
Fang S, Qiu J, Wu Z, Bai T, Guo W (2017) Down-regulation of UBC9 increases the sensitivity of hepatocellular carcinoma to doxorubicin. Oncotarget 8:49783–49795. https://doi.org/10.18632/oncotarget.17939
doi: 10.18632/oncotarget.17939
pubmed: 28572537
pmcid: 5564807
Fu L, Cui CP, Zhang X, Zhang L (2020a) The functions and regulation of Smurfs in cancers. Semin Cancer Biol 67:102–116. https://doi.org/10.1016/j.semcancer.2019.12.023
doi: 10.1016/j.semcancer.2019.12.023
pubmed: 31899247
Fu YD, Huang MJ, Guo JW, You YZ, Liu HM, Huang LH, Yu B (2020b) Targeting histone demethylase KDM5B for cancer treatment. Eur J Med Chem 208:112760. https://doi.org/10.1016/j.ejmech.2020.112760
doi: 10.1016/j.ejmech.2020.112760
pubmed: 32883639
Fukuda I, Ito A, Hirai G, Nishimura S, Kawasaki H, Saitoh H, Kimura K, Sodeoka M, Yoshida M (2009a) Ginkgolic acid inhibits protein SUMOylation by blocking formation of the E1-SUMO intermediate. Chem Biol 16:133–140. https://doi.org/10.1016/j.chembiol.2009.01.009
doi: 10.1016/j.chembiol.2009.01.009
pubmed: 19246003
Fukuda I, Ito A, Uramoto M, Saitoh H, Kawasaki H, Osada H, Yoshida M (2009b) Kerriamycin B inhibits protein SUMOylation. J Antibiot 62:221–224. https://doi.org/10.1038/ja.2009.10
doi: 10.1038/ja.2009.10
Gallardo M, Hornbaker MJ, Zhang X, Hu P, Bueso-Ramos C, Post SM (2016) Aberrant hnRNP K expression: all roads lead to cancer. Cell Cycle (Georgetown, TX) 15:1552–1557. https://doi.org/10.1080/15384101.2016.1164372
doi: 10.1080/15384101.2016.1164372
Gallardo-Chamizo F, Lara-Ureña N, Correa-Vázquez JF, Reyes JC, Gauthier BR, García-Domínguez M (2022) SENP7 overexpression protects cancer cells from oxygen and glucose deprivation and associates with poor prognosis in colon cancer. Genes Dis 9:1419–1422. https://doi.org/10.1016/j.gendis.2022.02.019
doi: 10.1016/j.gendis.2022.02.019
pubmed: 36157488
pmcid: 9485274
Ge MK, Zhang N, Xia L, Zhang C, Dong SS, Li ZM, Ji Y, Zheng MH, Sun J, Chen GQ et al (2020) FBXO22 degrades nuclear PTEN to promote tumorigenesis. Nat Commun 11:1720. https://doi.org/10.1038/s41467-020-15578-1
doi: 10.1038/s41467-020-15578-1
pubmed: 32249768
pmcid: 7136256
Gill G (2004) SUMO and ubiquitin in the nucleus: different functions, similar mechanisms? Genes Dev 18:2046–2059. https://doi.org/10.1101/gad.1214604
doi: 10.1101/gad.1214604
pubmed: 15342487
Gong L, Kamitani T, Fujise K, Caskey LS, Yeh ET (1997) Preferential interaction of sentrin with a ubiquitin-conjugating enzyme, Ubc9. J Biol Chem 272:28198–28201. https://doi.org/10.1074/jbc.272.45.28198
doi: 10.1074/jbc.272.45.28198
pubmed: 9353268
Gong X, Kong P, Yu T, Xiao X, Wang L, Sang Y, Li X, Zhang B, Tao Z, Liu W (2022) Adefovir dipivoxil inhibits APL progression through degradation of the oncoprotein PML-RARA. Exp Hematol Oncol 11:103. https://doi.org/10.1186/s40164-022-00355-1
doi: 10.1186/s40164-022-00355-1
pubmed: 36404334
pmcid: 9676767
González-Prieto R, Cuijpers SA, Kumar R, Hendriks IA, Vertegaal AC (2015) c-Myc is targeted to the proteasome for degradation in a SUMOylation-dependent manner, regulated by PIAS1, SENP7 and RNF4. Cell Cycle (Georgetown, TX) 14:1859–1872. https://doi.org/10.1080/15384101.2015.1040965
doi: 10.1080/15384101.2015.1040965
Guo WH, Yuan LH, Xiao ZH, Liu D, Zhang JX (2011) Overexpression of SUMO-1 in hepatocellular carcinoma: a latent target for diagnosis and therapy of hepatoma. J Cancer Res Clin Oncol 137:533–541. https://doi.org/10.1007/s00432-010-0920-x
doi: 10.1007/s00432-010-0920-x
pubmed: 20502916
Han ZJ, Feng YH, Gu BH, Li YM, Chen H (2018) The post-translational modification, SUMOylation, and cancer (review). Int J Oncol 52:1081–1094. https://doi.org/10.3892/ijo.2018.4280
doi: 10.3892/ijo.2018.4280
pubmed: 29484374
pmcid: 5843405
He X, Riceberg J, Soucy T, Koenig E, Minissale J, Gallery M, Bernard H, Yang X, Liao H, Rabino C et al (2017) Probing the roles of SUMOylation in cancer cell biology by using a selective SAE inhibitor. Nat Chem Biol 13:1164–1171. https://doi.org/10.1038/nchembio.2463
doi: 10.1038/nchembio.2463
pubmed: 28892090
Hellerbrand C, Bumes E, Bataille F, Dietmaier W, Massoumi R, Bosserhoff AK (2007) Reduced expression of CYLD in human colon and hepatocellular carcinomas. Carcinogenesis 28:21–27. https://doi.org/10.1093/carcin/bgl081
doi: 10.1093/carcin/bgl081
pubmed: 16774947
Hendriks IA, Schimmel J, Eifler K, Olsen JV, Vertegaal ACO (2015) Ubiquitin-specific protease 11 (USP11) deubiquitinates hybrid small ubiquitin-like modifier (SUMO)-ubiquitin chains to counteract RING finger protein 4 (RNF4). J Biol Chem 290:15526–15537. https://doi.org/10.1074/jbc.M114.618132
doi: 10.1074/jbc.M114.618132
pubmed: 25969536
pmcid: 4477612
Hilton HN, Clarke CL, Graham JD (2018) Estrogen and progesterone signalling in the normal breast and its implications for cancer development. Mol Cell Endocrinol 466:2–14. https://doi.org/10.1016/j.mce.2017.08.011
doi: 10.1016/j.mce.2017.08.011
pubmed: 28851667
Hirohama M, Kumar A, Fukuda I, Matsuoka S, Igarashi Y, Saitoh H, Takagi M, Shin-ya K, Honda K, Kondoh Y et al (2013) Spectomycin B1 as a novel SUMOylation inhibitor that directly binds to SUMO E2. ACS Chem Biol 8:2635–2642. https://doi.org/10.1021/cb400630z
doi: 10.1021/cb400630z
pubmed: 24143955
Hsu KS, Kao HY (2018) PML: Regulation and multifaceted function beyond tumor suppression. Cell Biosci 8:5. https://doi.org/10.1186/s13578-018-0204-8
doi: 10.1186/s13578-018-0204-8
pubmed: 29416846
pmcid: 5785837
Huang W, He T, Chai C, Yang Y, Zheng Y, Zhou P, Qiao X, Zhang B, Liu Z, Wang J et al (2012) Triptolide inhibits the proliferation of prostate cancer cells and down-regulates SUMO-specific protease 1 expression. PloS ONE 7:e37693. https://doi.org/10.1371/journal.pone.0037693
doi: 10.1371/journal.pone.0037693
pubmed: 22666381
pmcid: 3364364
Huang Y, Pan XW, Li L, Chen L, Liu X, Lu JL, Zhu XM, Huang H, Yang QW, Ye JQ et al (2016) Overexpression of USP39 predicts poor prognosis and promotes tumorigenesis of prostate cancer via promoting EGFR mRNA maturation and transcription elongation. Oncotarget 7:22016–22030. https://doi.org/10.18632/oncotarget.7882
doi: 10.18632/oncotarget.7882
pubmed: 26959883
pmcid: 5008341
Ikeda F, Dikic I (2008) Atypical ubiquitin chains: new molecular signals. ‘Protein modifications: beyond the usual suspects’ review series. EMBO Rep 9:536–542. https://doi.org/10.1038/embor.2008.93
doi: 10.1038/embor.2008.93
pubmed: 18516089
pmcid: 2427391
Ito F, Yoshimoto C, Yamada Y, Sudo T, Kobayashi H (2018) The HNF-1β-USP28-Claspin pathway upregulates DNA damage-induced Chk1 activation in ovarian clear cell carcinoma. Oncotarget 9:17512–17522. https://doi.org/10.18632/oncotarget.24776
doi: 10.18632/oncotarget.24776
pubmed: 29707125
pmcid: 5915133
Ivan M, Kondo K, Yang H, Kim W, Valiando J, Ohh M, Salic A, Asara JM, Lane WS, Kaelin WG Jr (2001) HIFalpha targeted for VHL-mediated destruction by proline hydroxylation: implications for O
doi: 10.1126/science.1059817
pubmed: 11292862
Iyer RS, Chatham L, Sleigh R, Meek DW (2017) A functional SUMO-motif in the active site of PIM1 promotes its degradation via RNF4, and stimulates protein kinase activity. Sci Rep 7:3598. https://doi.org/10.1038/s41598-017-03775-w
doi: 10.1038/s41598-017-03775-w
pubmed: 28620180
pmcid: 5472562
Ji P, Liang S, Li P, Xie C, Li J, Zhang K, Zheng X, Feng M, Li Q, Jiao H et al (2018) Speckle-type POZ protein suppresses hepatocellular carcinoma cell migration and invasion via ubiquitin-dependent proteolysis of SUMO1/sentrin specific peptidase 7. Biochem Biophys Res Commun 502:30–42. https://doi.org/10.1016/j.bbrc.2018.05.115
doi: 10.1016/j.bbrc.2018.05.115
pubmed: 29777712
Jiao J, Zhang R, Li Z, Yin Y, Fang X, Ding X, Cai Y, Yang S, Mu H, Zong D et al (2018) Nuclear Smad6 promotes gliomagenesis by negatively regulating PIAS3-mediated STAT3 inhibition. Nat Commun 9:2504. https://doi.org/10.1038/s41467-018-04936-9
doi: 10.1038/s41467-018-04936-9
pubmed: 29950561
pmcid: 6021382
Jin X, Fang R, Fan P, Zeng L, Zhang B, Lu X, Liu T (2019) PES1 promotes BET inhibitors resistance and cells proliferation through increasing c-Myc expression in pancreatic cancer. J Exp Clin Cancer Res CR 38:463. https://doi.org/10.1186/s13046-019-1466-7
doi: 10.1186/s13046-019-1466-7
pubmed: 31718704
Jin JO, Lee GD, Nam SH, Lee TH, Kang DH, Yun JK, Lee PC (2021) Sequential ubiquitination of p53 by TRIM28, RLIM, and MDM2 in lung tumorigenesis. Cell Death Differ 28:1790–1803. https://doi.org/10.1038/s41418-020-00701-y
doi: 10.1038/s41418-020-00701-y
pubmed: 33328571
Jung JG, Stoeck A, Guan B, Wu RC, Zhu H, Blackshaw S, Shih Ie M, Wang TL (2014) Notch3 interactome analysis identified WWP2 as a negative regulator of Notch3 signaling in ovarian cancer. PLoS Genet 10:e1004751. https://doi.org/10.1371/journal.pgen.1004751
doi: 10.1371/journal.pgen.1004751
pubmed: 25356737
pmcid: 4214668
Kim YS, Nagy K, Keyser S, Schneekloth JS Jr (2013) An electrophoretic mobility shift assay identifies a mechanistically unique inhibitor of protein sumoylation. Chem Biol 20:604–613. https://doi.org/10.1016/j.chembiol.2013.04.001
doi: 10.1016/j.chembiol.2013.04.001
pubmed: 23601649
pmcid: 3711074
Kim JH, Ham S, Lee Y, Suh GY, Lee YS (2019) TTC3 contributes to TGF-β(1)-induced epithelial-mesenchymal transition and myofibroblast differentiation, potentially through SMURF2 ubiquitylation and degradation. Cell Death Dis 10:92. https://doi.org/10.1038/s41419-019-1308-8
doi: 10.1038/s41419-019-1308-8
pubmed: 30696809
pmcid: 6351531
Kovalenko A, Chable-Bessia C, Cantarella G, Israël A, Wallach D, Courtois G (2003) The tumour suppressor CYLD negatively regulates NF-kappaB signalling by deubiquitination. Nature 424:801–805. https://doi.org/10.1038/nature01802
doi: 10.1038/nature01802
pubmed: 12917691
Kruiswijk F, Labuschagne CF, Vousden KH (2015) p53 in survival, death and metabolic health: a lifeguard with a licence to kill. Nat Rev Mol Cell Biol 16:393–405. https://doi.org/10.1038/nrm4007
doi: 10.1038/nrm4007
pubmed: 26122615
Kumar R, Sabapathy K (2019) RNF4—a paradigm for SUMOylation-mediated ubiquitination. Proteomics 19:e1900185. https://doi.org/10.1002/pmic.201900185
doi: 10.1002/pmic.201900185
pubmed: 31566917
Kumar A, Ito A, Takemoto M, Yoshida M, Zhang KY (2014) Identification of 1,2,5-oxadiazoles as a new class of SENP2 inhibitors using structure based virtual screening. J Chem Inf Model 54:870–880. https://doi.org/10.1021/ci4007134
doi: 10.1021/ci4007134
pubmed: 24512059
Lallemand-Breitenbach V, Jeanne M, Benhenda S, Nasr R, Lei M, Peres L, Zhou J, Zhu J, Raught B, de Thé H (2008) Arsenic degrades PML or PML-RARalpha through a SUMO-triggered RNF4/ubiquitin-mediated pathway. Nat Cell Biol 10:547–555. https://doi.org/10.1038/ncb1717
doi: 10.1038/ncb1717
pubmed: 18408733
Lange CA, Shen T, Horwitz KB (2000) Phosphorylation of human progesterone receptors at serine-294 by mitogen-activated protein kinase signals their degradation by the 26S proteasome. Proc Natl Acad Sci U S A 97:1032–1037. https://doi.org/10.1073/pnas.97.3.1032
doi: 10.1073/pnas.97.3.1032
pubmed: 10655479
pmcid: 15511
Langston SP, Grossman S, England D, Afroze R, Bence N, Bowman D, Bump N, Chau R, Chuang BC, Claiborne C et al (2021) Discovery of TAK-981, a first-in-class inhibitor of SUMO-activating enzyme for the treatment of cancer. J Med Chem 64:2501–2520. https://doi.org/10.1021/acs.jmedchem.0c01491
doi: 10.1021/acs.jmedchem.0c01491
pubmed: 33631934
Lecona E, Rodriguez-Acebes S, Specks J, Lopez-Contreras AJ, Ruppen I, Murga M, Muñoz J, Mendez J, Fernandez-Capetillo O (2016) USP7 is a SUMO deubiquitinase essential for DNA replication. Nat Struct Mol Biol 23:270–277. https://doi.org/10.1038/nsmb.3185
doi: 10.1038/nsmb.3185
pubmed: 26950370
pmcid: 4869841
Lee MH, Lee SW, Lee EJ, Choi SJ, Chung SS, Lee JI, Cho JM, Seol JH, Baek SH, Kim KI et al (2006) SUMO-specific protease SUSP4 positively regulates p53 by promoting Mdm2 self-ubiquitination. Nat Cell Biol 8:1424–1431. https://doi.org/10.1038/ncb1512
doi: 10.1038/ncb1512
pubmed: 17086174
Lee SW, Lee MH, Park JH, Kang SH, Yoo HM, Ka SH, Oh YM, Jeon YJ, Chung CH (2012) SUMOylation of hnRNP-K is required for p53-mediated cell-cycle arrest in response to DNA damage. Embo J 31:4441–4452. https://doi.org/10.1038/emboj.2012.293
doi: 10.1038/emboj.2012.293
pubmed: 23092970
pmcid: 3512394
Li M, Brooks CL, Wu-Baer F, Chen D, Baer R, Gu W (2003) Mono- versus polyubiquitination: differential control of p53 fate by Mdm2. Science 302:1972–1975. https://doi.org/10.1126/science.1091362
doi: 10.1126/science.1091362
pubmed: 14671306
Li J, Tan Q, Yan M, Liu L, Lin H, Zhao F, Bao G, Kong H, Ge C, Zhang F et al (2014) miRNA-200c inhibits invasion and metastasis of human non-small cell lung cancer by directly targeting ubiquitin specific peptidase 25. Mol Cancer 13:166. https://doi.org/10.1186/1476-4598-13-166
doi: 10.1186/1476-4598-13-166
pubmed: 24997798
pmcid: 4105889
Li S, Wang M, Qu X, Xu Z, Yang Y, Su Q, Wu H (2016) SUMOylation of PES1 upregulates its stability and function via inhibiting its ubiquitination. Oncotarget 7:50522–50534. https://doi.org/10.18632/oncotarget.10494
doi: 10.18632/oncotarget.10494
pubmed: 27409667
pmcid: 5226600
Li M, Xu X, Chang CW, Zheng L, Shen B, Liu Y (2018) SUMO2 conjugation of PCNA facilitates chromatin remodeling to resolve transcription-replication conflicts. Nat Commun 9:2706. https://doi.org/10.1038/s41467-018-05236-y
doi: 10.1038/s41467-018-05236-y
pubmed: 30006506
pmcid: 6045570
Li M, Xu X, Chang CW, Liu Y (2020) TRIM28 functions as the SUMO E3 ligase for PCNA in prevention of transcription induced DNA breaks. Proc Natl Acad Sci U S A 117:23588–23596. https://doi.org/10.1073/pnas.2004122117
doi: 10.1073/pnas.2004122117
pubmed: 32900933
pmcid: 7519263
Li Z, Lu X, Liu Y, Zhao J, Ma S, Yin H, Huang S, Zhao Y, He X (2021) Gain of LINC00624 enhances liver cancer progression by disrupting the histone deacetylase 6/tripartite motif containing 28/zinc finger protein 354C corepressor complex. Hepatology (Baltimore, MD) 73:1764–1782. https://doi.org/10.1002/hep.31530
doi: 10.1002/hep.31530
pubmed: 32869873
Li K, Li J, Ye M, Jin X (2022) The role of Siah2 in tumorigenesis and cancer therapy. Gene 809:146028. https://doi.org/10.1016/j.gene.2021.146028
doi: 10.1016/j.gene.2021.146028
pubmed: 34687788
Lin HK, Wang L, Hu YC, Altuwaijri S, Chang C (2002) Phosphorylation-dependent ubiquitylation and degradation of androgen receptor by Akt require Mdm2 E3 ligase. EMBO J 21:4037–4048. https://doi.org/10.1093/emboj/cdf406
doi: 10.1093/emboj/cdf406
pubmed: 12145204
pmcid: 126152
Lindenmann U, Brand M, Gall F, Frasson D, Hunziker L, Kroslakova I, Sievers M, Riedl R (2020) Discovery of a class of potent and selective non-competitive sentrin-specific protease 1 inhibitors. ChemMedChem 15:675–679. https://doi.org/10.1002/cmdc.202000067
doi: 10.1002/cmdc.202000067
pubmed: 32083799
Liu X, Xu Y, Pang Z, Guo F, Qin Q, Yin T, Sang Y, Feng C, Li X, Jiang L et al (2015) Knockdown of SUMO-activating enzyme subunit 2 (SAE2) suppresses cancer malignancy and enhances chemotherapy sensitivity in small cell lung cancer. J Hematol Oncol 8:67. https://doi.org/10.1186/s13045-015-0164-y
doi: 10.1186/s13045-015-0164-y
pubmed: 26063074
pmcid: 4483218
Liu Y, Zhao D, Qiu F, Zhang LL, Liu SK, Li YY, Liu MT, Wu D, Wang JX, Ding XQ et al (2017) Manipulating PML SUMOylation via silencing UBC9 and RNF4 regulates cardiac fibrosis. Mol Ther J Am Soc Gene Ther 25:666–678. https://doi.org/10.1016/j.ymthe.2016.12.021
doi: 10.1016/j.ymthe.2016.12.021
Liu Y, Cao B, Hu L, Ye J, Tian W, He X (2022) The dual roles of MAGE-C2 in p53 ubiquitination and cell proliferation through E3 ligases MDM2 and TRIM28. Front Cell Dev Biol 10:922675. https://doi.org/10.3389/fcell.2022.922675
doi: 10.3389/fcell.2022.922675
pubmed: 35927984
pmcid: 9344466
Liu J, Zhang N, Zeng J, Wang T, Shen Y, Ma C, Yang M (2022) N(6)-methyladenosine-modified lncRNA ARHGAP5-AS1 stabilises CSDE1 and coordinates oncogenic RNA regulons in hepatocellular carcinoma. Clin Transl Med 12:e1107. https://doi.org/10.1002/ctm2.1107
doi: 10.1002/ctm2.1107
pubmed: 36354136
pmcid: 9647857
Lv Z, Yuan L, Atkison JH, Williams KM, Vega R, Sessions EH, Divlianska DB, Davies C, Chen Y, Olsen SK (2018) Molecular mechanism of a covalent allosteric inhibitor of SUMO E1 activating enzyme. Nat Commun 9:5145. https://doi.org/10.1038/s41467-018-07015-1
doi: 10.1038/s41467-018-07015-1
pubmed: 30514846
pmcid: 6279746
Mabb AM, Miyamoto S (2007) SUMO and NF-kappaB ties. Cell Mol Life Sci CMLS 64:1979–1996. https://doi.org/10.1007/s00018-007-7005-2
doi: 10.1007/s00018-007-7005-2
pubmed: 17530464
Maddika S, Kavela S, Rani N, Palicharla VR, Pokorny JL, Sarkaria JN, Chen J (2011) WWP2 is an E3 ubiquitin ligase for PTEN. Nat Cell Biol 13:728–733. https://doi.org/10.1038/ncb2240
doi: 10.1038/ncb2240
pubmed: 21532586
pmcid: 3926303
Maison C, Romeo K, Bailly D, Dubarry M, Quivy JP, Almouzni G (2012) The SUMO protease SENP7 is a critical component to ensure HP1 enrichment at pericentric heterochromatin. Nat Struct Mol Biol 19:458–460. https://doi.org/10.1038/nsmb.2244
doi: 10.1038/nsmb.2244
pubmed: 22388734
Man JH, Li HY, Zhang PJ, Zhou T, He K, Pan X, Liang B, Li AL, Zhao J, Gong WL et al (2006) PIAS3 induction of PRB sumoylation represses PRB transactivation by destabilizing its retention in the nucleus. Nucleic Acids Res 34:5552–5566. https://doi.org/10.1093/nar/gkl691
doi: 10.1093/nar/gkl691
pubmed: 17020914
pmcid: 1635300
Mansour MA (2018) Ubiquitination: friend and foe in cancer. Int J Biochem Cell Biol 101:80–93. https://doi.org/10.1016/j.biocel.2018.06.001
doi: 10.1016/j.biocel.2018.06.001
pubmed: 29864543
Masoumi KC, Massoumi R (2016) CYLD and SUMO in neuroblastoma therapy. Oncoscience 3:3–4. https://doi.org/10.18632/oncoscience.287
doi: 10.18632/oncoscience.287
pubmed: 26973854
pmcid: 4751910
Massoumi R, Kuphal S, Hellerbrand C, Haas B, Wild P, Spruss T, Pfeifer A, Fässler R, Bosserhoff AK (2009) Down-regulation of CYLD expression by Snail promotes tumor progression in malignant melanoma. J Exp Med 206:221–232. https://doi.org/10.1084/jem.20082044
doi: 10.1084/jem.20082044
pubmed: 19124656
pmcid: 2626666
Matunis MJ, Guzzo CM (2012) SUMO PTEN and tumor suppression. Pigment Cell Melanoma Res. https://doi.org/10.1111/pcmr.12001
doi: 10.1111/pcmr.12001
pubmed: 22846175
pmcid: 5288311
Meng C, Zhan J, Chen D, Shao G, Zhang H, Gu W, Luo J (2021) The deubiquitinase USP11 regulates cell proliferation and ferroptotic cell death via stabilization of NRF2 USP11 deubiquitinates and stabilizes NRF2. Oncogene 40:1706–1720. https://doi.org/10.1038/s41388-021-01660-5
doi: 10.1038/s41388-021-01660-5
pubmed: 33531626
Minervini G, Pennuto M, Tosatto SCE (2020) The pVHL neglected functions, a tale of hypoxia-dependent and -independent regulations in cancer. Open Biol 10:200109. https://doi.org/10.1098/rsob.200109
doi: 10.1098/rsob.200109
pubmed: 32603638
pmcid: 7574549
Miyamoto M, Fujita T, Kimura Y, Maruyama M, Harada H, Sudo Y, Miyata T, Taniguchi T (1988) Regulated expression of a gene encoding a nuclear factor, IRF-1, that specifically binds to IFN-beta gene regulatory elements. Cell 54:903–913. https://doi.org/10.1016/s0092-8674(88)91307-4
doi: 10.1016/s0092-8674(88)91307-4
pubmed: 3409321
Morris JR, Boutell C, Keppler M, Densham R, Weekes D, Alamshah A, Butler L, Galanty Y, Pangon L, Kiuchi T et al (2009) The SUMO modification pathway is involved in the BRCA1 response to genotoxic stress. Nature 462:886–890. https://doi.org/10.1038/nature08593
doi: 10.1038/nature08593
pubmed: 20016594
Moschos SJ, Smith AP, Mandic M, Athanassiou C, Watson-Hurst K, Jukic DM, Edington HD, Kirkwood JM, Becker D (2007) SAGE and antibody array analysis of melanoma-infiltrated lymph nodes: identification of Ubc9 as an important molecule in advanced-stage melanomas. Oncogene 26:4216–4225. https://doi.org/10.1038/sj.onc.1210216
doi: 10.1038/sj.onc.1210216
pubmed: 17297476
Moschos SJ, Jukic DM, Athanassiou C, Bhargava R, Dacic S, Wang X, Kuan SF, Fayewicz SL, Galambos C, Acquafondata M et al (2010) Expression analysis of Ubc9, the single small ubiquitin-like modifier (SUMO) E2 conjugating enzyme, in normal and malignant tissues. Hum Pathol 41:1286–1298. https://doi.org/10.1016/j.humpath.2010.02.007
doi: 10.1016/j.humpath.2010.02.007
pubmed: 20561671
Nakagawa K, Yokosawa H (2002) PIAS3 induces SUMO-1 modification and transcriptional repression of IRF-1. FEBS Lett 530:204–208. https://doi.org/10.1016/s0014-5793(02)03486-5
doi: 10.1016/s0014-5793(02)03486-5
pubmed: 12387893
Nawijn MC, Alendar A, Berns A (2011) For better or for worse: the role of Pim oncogenes in tumorigenesis. Nat Rev Cancer 11:23–34. https://doi.org/10.1038/nrc2986
doi: 10.1038/nrc2986
pubmed: 21150935
Nishida T, Yasuda H (2002) PIAS1 and PIASxalpha function as SUMO-E3 ligases toward androgen receptor and repress androgen receptor-dependent transcription. J Biol Chem 277:41311–41317. https://doi.org/10.1074/jbc.M206741200
doi: 10.1074/jbc.M206741200
pubmed: 12177000
Núñez-O’Mara A, Berra E (2013) Deciphering the emerging role of SUMO conjugation in the hypoxia-signaling cascade. Biol Chem 394:459–469. https://doi.org/10.1515/hsz-2012-0319
doi: 10.1515/hsz-2012-0319
pubmed: 23362194
Palayoor ST, Tofilon PJ, Coleman CN (2003) Ibuprofen-mediated reduction of hypoxia-inducible factors HIF-1alpha and HIF-2alpha in prostate cancer cells. Clin Cancer Res Off J Am Assoc Cancer Res 9:3150–3157
Pan X, Feng J, Zhu Z, Yao L, Ma S, Hao B, Zhang G (2018) A positive feedback loop between miR-181b and STAT3 that affects Warburg effect in colon cancer via regulating PIAS3 expression. J Cell Mol Med 22:5040–5049. https://doi.org/10.1111/jcmm.13786
doi: 10.1111/jcmm.13786
pubmed: 30054984
pmcid: 6156246
Park J, Kim K, Lee EJ, Seo YJ, Lim SN, Park K, Rho SB, Lee SH, Lee JH (2007) Elevated level of SUMOylated IRF-1 in tumor cells interferes with IRF-1-mediated apoptosis. Proc Natl Acad Sci U S A 104:17028–17033. https://doi.org/10.1073/pnas.0609852104
doi: 10.1073/pnas.0609852104
pubmed: 17942705
pmcid: 2040422
Park SM, Chae M, Kim BK, Seo T, Jang IS, Choi JS, Kim IC, Lee JH, Park J (2010) SUMOylated IRF-1 shows oncogenic potential by mimicking IRF-2. Biochem Biophys Res Commun 391:926–930. https://doi.org/10.1016/j.bbrc.2009.11.166
doi: 10.1016/j.bbrc.2009.11.166
pubmed: 19962964
Pelisch F, Pozzi B, Risso G, Muñoz MJ, Srebrow A (2012) DNA damage-induced heterogeneous nuclear ribonucleoprotein K sumoylation regulates p53 transcriptional activation. J Biol Chem 287:30789–30799. https://doi.org/10.1074/jbc.M112.390120
doi: 10.1074/jbc.M112.390120
pubmed: 22825850
pmcid: 3436322
Peng C, Tan Y, Yang P, Jin K, Zhang C, Peng W, Wang L, Zhou J, Chen R, Wang T et al (2021) Circ-GALNT16 restrains colorectal cancer progression by enhancing the SUMOylation of hnRNPK. J Exp Clin Cancer Res CR 40:272. https://doi.org/10.1186/s13046-021-02074-7
doi: 10.1186/s13046-021-02074-7
pubmed: 34452628
Pineda CT, Potts PR (2015) Oncogenic MAGEA-TRIM28 ubiquitin ligase downregulates autophagy by ubiquitinating and degrading AMPK in cancer. Autophagy 11:844–846. https://doi.org/10.1080/15548627.2015.1034420
doi: 10.1080/15548627.2015.1034420
pubmed: 25945414
pmcid: 4509443
Popov N, Wanzel M, Madiredjo M, Zhang D, Beijersbergen R, Bernards R, Moll R, Elledge SJ, Eilers M (2007) The ubiquitin-specific protease USP28 is required for MYC stability. Nat Cell Biol 9:765–774. https://doi.org/10.1038/ncb1601
doi: 10.1038/ncb1601
pubmed: 17558397
Qiao Z, Wang W, Wang L, Wen D, Zhao Y, Wang Q, Meng Q, Chen G, Wu Y, Zhou H (2011) Design, synthesis, and biological evaluation of benzodiazepine-based SUMO-specific protease 1 inhibitors. Bioorg Med Chem Lett 21:6389–6392. https://doi.org/10.1016/j.bmcl.2011.08.101
doi: 10.1016/j.bmcl.2011.08.101
pubmed: 21930380
Qin Y, Xu SQ, Pan DB, Ye GX, Wu CJ, Wang S, Wang CJ, Jiang JY, Fu J (2016) Silencing of WWP2 inhibits adhesion, invasion, and migration in liver cancer cells. Tumour Biol J Int Soc Oncodev Biol Med 37:6787–6799. https://doi.org/10.1007/s13277-015-4547-z
doi: 10.1007/s13277-015-4547-z
Qiu YB, Liao LY, Jiang R, Xu M, Xu LW, Chen GG, Liu ZM (2019) PES1 promotes the occurrence and development of papillary thyroid cancer by upregulating the ERα/ERβ protein ratio. Sci Rep 9:1032. https://doi.org/10.1038/s41598-018-37648-7
doi: 10.1038/s41598-018-37648-7
pubmed: 30705367
pmcid: 6355968
Rabellino A, Carter B, Konstantinidou G, Wu SY, Rimessi A, Byers LA, Heymach JV, Girard L, Chiang CM, Teruya-Feldstein J et al (2012) The SUMO E3-ligase PIAS1 regulates the tumor suppressor PML and its oncogenic counterpart PML-RARA. Cancer Res 72:2275–2284. https://doi.org/10.1158/0008-5472.Can-11-3159
doi: 10.1158/0008-5472.Can-11-3159
pubmed: 22406621
pmcid: 3342450
Ren YH, Liu KJ, Wang M, Yu YN, Yang K, Chen Q, Yu B, Wang W, Li QW, Wang J et al (2014) De-SUMOylation of FOXC2 by SENP3 promotes the epithelial–mesenchymal transition in gastric cancer cells. Oncotarget 5:7093–7104. https://doi.org/10.18632/oncotarget.2197
doi: 10.18632/oncotarget.2197
pubmed: 25216525
pmcid: 4196186
Romagnolo AP, Romagnolo DF, Selmin OI (2015) BRCA1 as target for breast cancer prevention and therapy. Anticancer Agents Med Chem 15:4–14. https://doi.org/10.2174/1871520614666141020153543
doi: 10.2174/1871520614666141020153543
pubmed: 25329591
Sarkar S, Brautigan DL, Larner JM (2017) Aurora kinase A promotes AR degradation via the E3 ligase CHIP. Mol Cancer Res MCR 15:1063–1072. https://doi.org/10.1158/1541-7786.Mcr-17-0062
doi: 10.1158/1541-7786.Mcr-17-0062
pubmed: 28536143
Schimmel J, Larsen KM, Matic I, van Hagen M, Cox J, Mann M, Andersen JS, Vertegaal AC (2008) The ubiquitin-proteasome system is a key component of the SUMO-2/3 cycle. Mol Cell Proteom MCP 7:2107–2122. https://doi.org/10.1074/mcp.M800025-MCP200
doi: 10.1074/mcp.M800025-MCP200
pubmed: 18565875
Seeler J-S, Dejean A (2017) SUMO and the robustness of cancer. Nat Rev Cancer 17:184–197. https://doi.org/10.1038/nrc.2016.143
doi: 10.1038/nrc.2016.143
pubmed: 28134258
Shi Q, Jin X, Zhang P, Li Q, Lv Z, Ding Y, He H, Wang Y, He Y, Zhao X et al (2022) SPOP mutations promote p62/SQSTM1-dependent autophagy and Nrf2 activation in prostate cancer. Cell Death Differ 29:1228–1239. https://doi.org/10.1038/s41418-021-00913-w
doi: 10.1038/s41418-021-00913-w
pubmed: 34987184
pmcid: 9177840
Smits VA, Freire R (2016) USP7/HAUSP: A SUMO deubiquitinase at the heart of DNA replication. BioEssays News Rev Mol Cell Dev Biol 38:863–868. https://doi.org/10.1002/bies.201600096
doi: 10.1002/bies.201600096
Song MS, Salmena L, Carracedo A, Egia A, Lo-Coco F, Teruya-Feldstein J, Pandolfi PP (2008) The deubiquitinylation and localization of PTEN are regulated by a HAUSP-PML network. Nature 455:813–817. https://doi.org/10.1038/nature07290
doi: 10.1038/nature07290
pubmed: 18716620
pmcid: 3398484
Song D, Li S, Ning L, Zhang S, Cai Y (2022) Smurf2 suppresses the metastasis of hepatocellular carcinoma via ubiquitin degradation of Smad2. Open Med (Warsaw, Poland) 17:384–396. https://doi.org/10.1515/med-2022-0437
doi: 10.1515/med-2022-0437
Soond SM, Smith PG, Wahl L, Swingler TE, Clark IM, Hemmings AM, Chantry A (2013) Novel WWP2 ubiquitin ligase isoforms as potential prognostic markers and molecular targets in cancer. Biochim Biophys Acta 1832:2127–2135. https://doi.org/10.1016/j.bbadis.2013.08.001
doi: 10.1016/j.bbadis.2013.08.001
pubmed: 23938591
Stindt MH, Carter S, Vigneron AM, Ryan KM, Vousden KH (2011) MDM2 promotes SUMO-2/3 modification of p53 to modulate transcriptional activity. Cell Cycle (Georgetown, TX) 10:3176–3188. https://doi.org/10.4161/cc.10.18.17436
doi: 10.4161/cc.10.18.17436
Suzawa M, Miranda DA, Ramos KA, Ang KK, Faivre EJ, Wilson CG, Caboni L, Arkin MR, Kim YS, Fletterick RJ et al (2015) A gene-expression screen identifies a non-toxic sumoylation inhibitor that mimics SUMO-less human LRH-1 in liver. elife. https://doi.org/10.7554/eLife.09003
doi: 10.7554/eLife.09003
pubmed: 26653140
pmcid: 4749390
Takemoto M, Kawamura Y, Hirohama M, Yamaguchi Y, Handa H, Saitoh H, Nakao Y, Kawada M, Khalid K, Koshino H et al (2014) Inhibition of protein SUMOylation by davidiin, an ellagitannin from Davidia involucrata. J Antibiot 67:335–338. https://doi.org/10.1038/ja.2013.142
doi: 10.1038/ja.2013.142
Tantai J, Pan X, Hu D (2016) RNF4-mediated SUMOylation is essential for NDRG2 suppression of lung adenocarcinoma. Oncotarget 7:26837–26843. https://doi.org/10.18632/oncotarget.8663
doi: 10.18632/oncotarget.8663
pubmed: 27072586
pmcid: 5042018
Trompouki E, Hatzivassiliou E, Tsichritzis T, Farmer H, Ashworth A, Mosialos G (2003) CYLD is a deubiquitinating enzyme that negatively regulates NF-kappaB activation by TNFR family members. Nature 424:793–796. https://doi.org/10.1038/nature01803
doi: 10.1038/nature01803
pubmed: 12917689
Trotman LC, Wang X, Alimonti A, Chen Z, Teruya-Feldstein J, Yang H, Pavletich NP, Carver BS, Cordon-Cardo C, Erdjument-Bromage H et al (2007) Ubiquitination regulates PTEN nuclear import and tumor suppression. Cell 128:141–156. https://doi.org/10.1016/j.cell.2006.11.040
doi: 10.1016/j.cell.2006.11.040
pubmed: 17218261
pmcid: 1855245
Tsang SV, Rainusso N, Liu M, Nomura M, Patel TD, Nakahata K, Kim HR, Huang S, Rajapakshe K, Coarfa C et al (2022) LncRNA PVT-1 promotes osteosarcoma cancer stem-like properties through direct interaction with TRIM28 and TSC2 ubiquitination. Oncogene 41:5373–5384. https://doi.org/10.1038/s41388-022-02538-w
doi: 10.1038/s41388-022-02538-w
pubmed: 36348010
Uno M, Koma Y, Ban HS, Nakamura H (2012) Discovery of 1-[4-(N-benzylamino)phenyl]-3-phenylurea derivatives as non-peptidic selective SUMO-sentrin specific protease (SENP)1 inhibitors. Bioorg Med Chem Lett 22:5169–5173. https://doi.org/10.1016/j.bmcl.2012.06.084
doi: 10.1016/j.bmcl.2012.06.084
pubmed: 22801642
van Hagen M, Overmeer RM, Abolvardi SS, Vertegaal AC (2010) RNF4 and VHL regulate the proteasomal degradation of SUMO-conjugated hypoxia-inducible factor-2alpha. Nucleic Acids Res 38:1922–1931. https://doi.org/10.1093/nar/gkp1157
doi: 10.1093/nar/gkp1157
pubmed: 20026589
Venne AS, Kollipara L, Zahedi RP (2014) The next level of complexity: crosstalk of posttranslational modifications. Proteomics 14:513–524. https://doi.org/10.1002/pmic.201300344
doi: 10.1002/pmic.201300344
pubmed: 24339426
Vertegaal ACO (2022) Signalling mechanisms and cellular functions of SUMO. Nat Rev Mol Cell Biol 23:715–731. https://doi.org/10.1038/s41580-022-00500-y
doi: 10.1038/s41580-022-00500-y
pubmed: 35750927
Wang YT, Yang WB, Chang WC, Hung JJ (2011) Interplay of posttranslational modifications in Sp1 mediates Sp1 stability during cell cycle progression. J Mol Biol 414:1–14. https://doi.org/10.1016/j.jmb.2011.09.027
doi: 10.1016/j.jmb.2011.09.027
pubmed: 21983342
Wang H, Ji X, Liu X, Yao R, Chi J, Liu S, Wang Y, Cao W, Zhou Q (2013) Lentivirus-mediated inhibition of USP39 suppresses the growth of breast cancer cells in vitro. Oncol Rep 30:2871–2877. https://doi.org/10.3892/or.2013.2798
doi: 10.3892/or.2013.2798
pubmed: 24126978
Wang W, Chen Y, Wang S, Hu N, Cao Z, Wang W, Tong T, Zhang X (2014) PIASxα ligase enhances SUMO1 modification of PTEN protein as a SUMO E3 ligase. J Biol Chem 289:3217–3230. https://doi.org/10.1074/jbc.M113.508515
doi: 10.1074/jbc.M113.508515
pubmed: 24344134
Wang Y, Jiang J, Li Q, Ma H, Xu Z, Gao Y (2016) KAP1 is overexpressed in hepatocellular carcinoma and its clinical significance. Int J Clin Oncol 21:927–933. https://doi.org/10.1007/s10147-016-0979-8
doi: 10.1007/s10147-016-0979-8
pubmed: 27095111
Wang S, Zhao Y, Aguilar A, Bernard D, Yang CY (2017) Targeting the MDM2-p53 protein–protein interaction for new cancer therapy: progress and challenges. Cold Spring Harbor Perspect Med. https://doi.org/10.1101/cshperspect.a026245
doi: 10.1101/cshperspect.a026245
Wang X, Liu Z, Zhang L, Yang Z, Chen X, Luo J, Zhou Z, Mei X, Yu X, Shao Z et al (2018) Targeting deubiquitinase USP28 for cancer therapy. Cell Death Dis 9:186. https://doi.org/10.1038/s41419-017-0208-z
doi: 10.1038/s41419-017-0208-z
pubmed: 29415985
pmcid: 5833459
Wang XM, Yang C, Zhao Y, Xu ZG, Yang W, Wang P, Lin D, Xiong B, Fang JY, Dong C et al (2020) The deubiquitinase USP25 supports colonic inflammation and bacterial infection and promotes colorectal cancer. Nat Cancer 1:811–825. https://doi.org/10.1038/s43018-020-0089-4
doi: 10.1038/s43018-020-0089-4
pubmed: 35122046
Wang S, Wang Z, Li J, Qin J, Song J, Li Y, Zhao L, Zhang X, Guo H, Shao C et al (2021) Splicing factor USP39 promotes ovarian cancer malignancy through maintaining efficient splicing of oncogenic HMGA2. Cell Death Dis 12:294. https://doi.org/10.1038/s41419-021-03581-3
doi: 10.1038/s41419-021-03581-3
pubmed: 33731694
pmcid: 7969951
Warfel NA, Kraft AS (2015) PIM kinase (and Akt) biology and signaling in tumors. Pharmacol Ther 151:41–49. https://doi.org/10.1016/j.pharmthera.2015.03.001
doi: 10.1016/j.pharmthera.2015.03.001
pubmed: 25749412
pmcid: 4957637
Wei C, Cheng J, Zhou B, Zhu L, Khan MA, He T, Zhou S, He J, Lu X, Chen H et al (2016) Tripartite motif containing 28 (TRIM28) promotes breast cancer metastasis by stabilizing TWIST1 protein. Sci Rep 6:29822. https://doi.org/10.1038/srep29822
doi: 10.1038/srep29822
pubmed: 27412325
pmcid: 4944148
Weigel NL (1996) Steroid hormone receptors and their regulation by phosphorylation. Biochem J 319(Pt 3):657–667. https://doi.org/10.1042/bj3190657
doi: 10.1042/bj3190657
pubmed: 8920964
pmcid: 1217840
Wen D, Xu Z, Xia L, Liu X, Tu Y, Lei H, Wang W, Wang T, Song L, Ma C et al (2014) Important role of SUMOylation of Spliceosome factors in prostate cancer cells. J Proteome Res 13:3571–3582. https://doi.org/10.1021/pr4012848
doi: 10.1021/pr4012848
pubmed: 25027693
Wiesener MS, Turley H, Allen WE, Willam C, Eckardt KU, Talks KL, Wood SM, Gatter KC, Harris AL, Pugh CW et al (1998) Induction of endothelial PAS domain protein-1 by hypoxia: characterization and comparison with hypoxia-inducible factor-1alpha. Blood 92:2260–2268
doi: 10.1182/blood.V92.7.2260
pubmed: 9746763
Wu HC, Lin YC, Liu CH, Chung HC, Wang YT, Lin YW, Ma HI, Tu PH, Lawler SE, Chen RH (2014) USP11 regulates PML stability to control Notch-induced malignancy in brain tumours. Nat Commun 5:3214. https://doi.org/10.1038/ncomms4214
doi: 10.1038/ncomms4214
pubmed: 24487962
pmcid: 5645609
Wu J, Lei H, Zhang J, Chen X, Tang C, Wang W, Xu H, Xiao W, Gu W, Wu Y (2016) Momordin Ic, a new natural SENP1 inhibitor, inhibits prostate cancer cell proliferation. Oncotarget 7:58995–59005. https://doi.org/10.18632/oncotarget.10636
doi: 10.18632/oncotarget.10636
pubmed: 27449295
pmcid: 5312290
Wu R, Fang J, Liu M, Jun A, Liu J, Chen W, Li J, Ma G, Zhang Z, Zhang B et al (2020) SUMOylation of the transcription factor ZFHX3 at Lys-2806 requires SAE1, UBC9, and PIAS2 and enhances its stability and function in cell proliferation. J Biol Chem 295:6741–6753. https://doi.org/10.1074/jbc.RA119.012338
doi: 10.1074/jbc.RA119.012338
pubmed: 32249212
pmcid: 7212658
Xhabija B, Kidder BL (2019) KDM5B is a master regulator of the H3K4-methylome in stem cells, development and cancer. Semin Cancer Biol 57:79–85. https://doi.org/10.1016/j.semcancer.2018.11.001
doi: 10.1016/j.semcancer.2018.11.001
pubmed: 30448242
Xu J, Footman A, Qin Y, Aysola K, Black S, Reddy V, Singh K, Grizzle W, You S, Moellering D et al (2016) BRCA1 mutation leads to deregulated Ubc9 levels which triggers proliferation and migration of patient-derived high grade serous ovarian cancer and triple negative breast cancer cells. Int J Chronic Dis Ther 2:31–38
pubmed: 28164176
pmcid: 5287352
Xu XW, Pan CW, Yang XM, Zhou L, Zheng ZQ, Li DC (2018) SP1 reduces autophagic flux through activating p62 in gastric cancer cells. Mol Med Rep 17:4633–4638. https://doi.org/10.3892/mmr.2018.8400
doi: 10.3892/mmr.2018.8400
pubmed: 29328444
Yan S, Sun X, Xiang B, Cang H, Kang X, Chen Y, Li H, Shi G, Yeh ET, Wang B et al (2010) Redox regulation of the stability of the SUMO protease SENP3 via interactions with CHIP and Hsp90. EMBO J 29:3773–3786. https://doi.org/10.1038/emboj.2010.245
doi: 10.1038/emboj.2010.245
pubmed: 20924358
pmcid: 2989103
Yan Y, Zheng L, Du Q, Yazdani H, Dong K, Guo Y, Geller DA (2021) Interferon regulatory factor 1(IRF-1) activates anti-tumor immunity via CXCL10/CXCR3 axis in hepatocellular carcinoma (HCC). Cancer Lett 506:95–106. https://doi.org/10.1016/j.canlet.2021.03.002
doi: 10.1016/j.canlet.2021.03.002
pubmed: 33689775
pmcid: 8009854
Yang WL, Jin G, Li CF, Jeong YS, Moten A, Xu D, Feng Z, Chen W, Cai Z, Darnay B et al (2013) Cycles of ubiquitination and deubiquitination critically regulate growth factor-mediated activation of Akt signaling. Sci Signal 6:ra3. https://doi.org/10.1126/scisignal.2003197
doi: 10.1126/scisignal.2003197
pubmed: 23300340
Yang R, He Y, Chen S, Lu X, Huang C, Zhang G (2016) Elevated expression of WWP2 in human lung adenocarcinoma and its effect on migration and invasion. Biochem Biophys Res Commun 479:146–151. https://doi.org/10.1016/j.bbrc.2016.07.084
doi: 10.1016/j.bbrc.2016.07.084
pubmed: 27462019
Yang N, Liu S, Qin T, Liu X, Watanabe N, Mayo KH, Li J, Li X (2019) SUMO3 modification by PIAS1 modulates androgen receptor cellular distribution and stability. Cell Commun Signal 17:153. https://doi.org/10.1186/s12964-019-0457-9
doi: 10.1186/s12964-019-0457-9
pubmed: 31752909
pmcid: 6868827
Yang P, Liu Y, Qi YC, Lian ZH (2020) High SENP3 expression promotes cell migration, invasion, and proliferation by modulating DNA methylation of E-cadherin in osteosarcoma. Technol Cancer Res Treat 19:1533033820956988. https://doi.org/10.1177/1533033820956988
doi: 10.1177/1533033820956988
pubmed: 33030103
pmcid: 7549150
Zeng M, Liu W, Hu Y, Fu N (2020) Sumoylation in liver disease. Clin Chim Acta Int J Clin Chem 510:347–353. https://doi.org/10.1016/j.cca.2020.07.044
doi: 10.1016/j.cca.2020.07.044
Zhai F, Li J, Ye M, Jin X (2022) The functions and effects of CUL3-E3 ligases mediated non-degradative ubiquitination. Gene 832:146562. https://doi.org/10.1016/j.gene.2022.146562
doi: 10.1016/j.gene.2022.146562
pubmed: 35580799
Zhai F, Wang J, Yang W, Ye M, Jin X (2022) The E3 ligases in cervical cancer and endometrial cancer. Cancers. https://doi.org/10.3390/cancers14215354
doi: 10.3390/cancers14215354
pubmed: 36358773
pmcid: 9658772
Zhang PJ, Zhao J, Li HY, Man JH, He K, Zhou T, Pan X, Li AL, Gong WL, Jin BF et al (2007) CUE domain containing 2 regulates degradation of progesterone receptor by ubiquitin-proteasome. Embo J 26:1831–1842. https://doi.org/10.1038/sj.emboj.7601602
doi: 10.1038/sj.emboj.7601602
pubmed: 17347654
pmcid: 1847652
Zhang RY, Liu ZK, Wei D, Yong YL, Lin P, Li H, Liu M, Zheng NS, Liu K, Hu CX et al (2021) UBE2S interacting with TRIM28 in the nucleus accelerates cell cycle by ubiquitination of p27 to promote hepatocellular carcinoma development. Signal Transduct Target Ther 6:64. https://doi.org/10.1038/s41392-020-00432-z
doi: 10.1038/s41392-020-00432-z
pubmed: 33589597
pmcid: 7884418
Zhang H, Yu H, Ren D, Sun Y, Guo F, Cai H, Zhou C, Zhou Y, Jin X, Wu H (2022a) CBX3 regulated by YBX1 promotes smoking-induced pancreatic cancer progression via inhibiting SMURF2 expression. Int J Biol Sci 18:3484–3497. https://doi.org/10.7150/ijbs.68995
doi: 10.7150/ijbs.68995
pubmed: 35637952
pmcid: 9134897
Zhang H, Jin X, Huang H (2022) Deregulation of SPOP in cancer. Cancer Res. https://doi.org/10.1158/0008-5472.Can-22-2801
doi: 10.1158/0008-5472.Can-22-2801
pubmed: 36524347
pmcid: 9978888
Zhao Y, Ma CA, Wu L, Iwai K, Ashwell JD, Oltz EM, Ballard DW, Jain A (2015) CYLD and the NEMO zinc finger regulate tumor necrosis factor signaling and early embryogenesis. J Biol Chem 290:22076–22084. https://doi.org/10.1074/jbc.M115.658096
doi: 10.1074/jbc.M115.658096
pubmed: 26224629
pmcid: 4571959
Zhao Y, Wang Z, Zhang J, Zhou H (2016) Identification of SENP1 inhibitors through in silico screening and rational drug design. Eur J Med Chem 122:178–184. https://doi.org/10.1016/j.ejmech.2016.06.018
doi: 10.1016/j.ejmech.2016.06.018
pubmed: 27344494
Zhao Y, Li J, Chen J, Ye M, Jin X (2022) Functional roles of E3 ubiquitin ligases in prostate cancer. J Mol Med (Berl) 100:1125–1144. https://doi.org/10.1007/s00109-022-02229-9
doi: 10.1007/s00109-022-02229-9
pubmed: 35816219
Zhen Y, Knobel PA, Stracker TH, Reverter D (2014) Regulation of USP28 deubiquitinating activity by SUMO conjugation. J Biol Chem 289:34838–34850. https://doi.org/10.1074/jbc.M114.601849
doi: 10.1074/jbc.M114.601849
pubmed: 25359778
pmcid: 4263883
Zheng YC, Chang J, Wang LC, Ren HM, Pang JR, Liu HM (2019) Lysine demethylase 5B (KDM5B): a potential anti-cancer drug target. Eur J Med Chem 161:131–140. https://doi.org/10.1016/j.ejmech.2018.10.040
doi: 10.1016/j.ejmech.2018.10.040
pubmed: 30343192
Zhu H, Ren S, Bitler BG, Aird KM, Tu Z, Skordalakes E, Zhu Y, Yan J, Sun Y, Zhang R (2015) SPOP E3 ubiquitin ligase adaptor promotes cellular senescence by degrading the SENP7 deSUMOylase. Cell Rep 13:1183–1193. https://doi.org/10.1016/j.celrep.2015.09.083
doi: 10.1016/j.celrep.2015.09.083
pubmed: 26527005
pmcid: 4644472
Zlotkowski K, Hewitt WM, Sinniah RS, Tropea JE, Needle D, Lountos GT, Barchi JJ Jr, Waugh DS, Schneekloth JS Jr (2017) A small-molecule microarray approach for the identification of E2 enzyme inhibitors in ubiquitin-like conjugation pathways. SLAS Discov Adv Life Sci R & D 22:760–766. https://doi.org/10.1177/2472555216683937
doi: 10.1177/2472555216683937