The emerging roles of E3 ubiquitin ligases in ovarian cancer chemoresistance

Yang Meng , Lei Qiu , Su Zhang , Junhong Han

Cancer Drug Resistance ›› 2021, Vol. 4 ›› Issue (2) : 365 -81.

PDF
Cancer Drug Resistance ›› 2021, Vol. 4 ›› Issue (2) :365 -81. DOI: 10.20517/cdr.2020.115
Review
review-article

The emerging roles of E3 ubiquitin ligases in ovarian cancer chemoresistance

Author information +
History +
PDF

Abstract

Epithelial cancer of the ovary exhibits the highest mortality rate of all gynecological malignancies in women today, since the disease is often diagnosed in advanced stages. While the treatment of cancer with specific chemical agents or drugs is the favored treatment regimen, chemotherapy resistance greatly impedes successful ovarian cancer chemotherapy. Thus, chemoresistance becomes one of the most critical clinical issues confronted when treating patients with ovarian cancer. Convincing evidence hints that dysregulation of E3 ubiquitin ligases is a key factor in the development and maintenance of ovarian cancer chemoresistance. This review outlines recent advancement in our understanding of the emerging roles of E3 ubiquitin ligases in ovarian cancer chemoresistance. We also highlight currently available inhibitors targeting E3 ligase activities and discuss their potential for clinical applications in treating chemoresistant ovarian cancer patients.

Keywords

Ovarian cancer / chemoresistance / E3 ubiquitin ligases / inhibitor

Cite this article

Download citation ▾
Yang Meng, Lei Qiu, Su Zhang, Junhong Han. The emerging roles of E3 ubiquitin ligases in ovarian cancer chemoresistance. Cancer Drug Resistance, 2021, 4(2): 365-81 DOI:10.20517/cdr.2020.115

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Popovic D,Dikic I.Ubiquitination in disease pathogenesis and treatment..Nat Med2014;20:1242-53

[2]

Mansour MA.Ubiquitination: Friend and foe in cancer..Int J Biochem Cell Biol2018;101:80-93

[3]

Wang D,Wang B,Wei W.E3 ubiquitin ligases in cancer and implications for therapies..Cancer Metastasis Rev2017;36:683-702

[4]

Pickart CM.Ubiquitin: structures, functions, mechanisms..Biochim Biophys Acta2004;1695:55-72

[5]

Reyes-Turcu FE,Wilkinson KD.Regulation and cellular roles of ubiquitin-specific deubiquitinating enzymes..Annu Rev Biochem2009;78:363-97 PMCID:PMC2734102

[6]

Ramakrishna S,Baek KH.The role of deubiquitinating enzymes in apoptosis..Cell Mol Life Sci2011;68:15-26

[7]

Ramakrishna S,Baek KH.Biological functions of hyaluronan and cytokine-inducible deubiquitinating enzymes..Biochim Biophys Acta2015;1855:83-91

[8]

Richardson PG,Berenson J.A phase 2 study of bortezomib in relapsed, refractory myeloma..N Engl J Med2003;348:2609-17

[9]

Hideshima T,Chauhan D.The proteasome inhibitor PS-341 inhibits growth, induces apoptosis, and overcomes drug resistance in human multiple myeloma cells..Cancer Res2001;61:3071-6

[10]

Schmidt MHH.The Cbl interactome and its functions..Nat Rev Mol Cell Biol2005;6:907-18

[11]

Bray F,Soerjomataram I,Torre LA.Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries..CA Cancer J Clin2018;68:394-424

[12]

Webb PM.Epidemiology of epithelial ovarian cancer..Best Pract Res Clin Obstet Gynaecol2017;41:3-14

[13]

Jazaeri AA,Park J.Overcoming platinum resistance in preclinical models of ovarian cancer using the neddylation inhibitor MLN4924..Mol Cancer Ther2013;12:1958-67 PMCID:PMC3795967

[14]

Matulonis UA,Fallowfield L,Sehouli J.Ovarian cancer..Nat Rev Dis Primers2016;2:16061 PMCID:PMC7290868

[15]

Eltabbakh GH.Current treatment for ovarian cancer..Expert Opin Pharmacother2001;2:109-24

[16]

Amawi H,Tiwari AK,Shukla S.ABC transporter-mediated multidrug-resistant cancer..Adv Exp Med Biol2019;1141:549-80

[17]

Li W,Assaraf YG.Overcoming ABC transporter-mediated multidrug resistance: molecular mechanisms and novel therapeutic drug strategies..Drug Resist Updat2016;27:14-29

[18]

Perego P,Righetti SC.Association between cisplatin resistance and mutation of p53 gene and reduced bax expression in ovarian carcinoma cell systems..Cancer Res1996;56:556-62

[19]

Reed JC,Takayama S.BCL-2 family proteins: regulators of cell death involved in the pathogenesis of cancer and resistance to therapy..J Cell Biochem1996;60:23-32

[20]

Zheng N.Ubiquitin Ligases: Structure, function, and regulation..Annu Rev Biochem2017;86:129-57

[21]

Fajner V,Polo S.Targeting HECT-type E3 ligases - insights from catalysis, regulation and inhibitors..FEBS Lett2017;591:2636-47

[22]

Berndsen CE.New insights into ubiquitin E3 ligase mechanism..Nat Struct Mol Biol2014;21:301-7

[23]

Dove KK.RING-Between-RING E3 Ligases: Emerging themes amid the variations..J Mol Biol2017;429:3363-75 PMCID:PMC5675740

[24]

Yang L,Huang X,He J.Novel insights into E3 ubiquitin ligase in cancer chemoresistance..Am J Med Sci2018;355:368-76

[25]

Rotin D.Physiological functions of the HECT family of ubiquitin ligases..Nat Rev Mol Cell Biol2009;10:398-409

[26]

Ozkan E,Deisenhofer J.Mechanistic insight into the allosteric activation of a ubiquitin-conjugating enzyme by RING-type ubiquitin ligases..Proc Natl Acad Sci U S A2005;102:18890-5 PMCID:PMC1316884

[27]

van der Reijden BA,Lowenberg B.TRIADs: a new class of proteins with a novel cysteine-rich signature..Protein Sci1999;8:1557-61 PMCID:PMC2144383

[28]

Morett E.A novel transactivation domain in parkin..Trends Biochem Sci1999;24:229-31

[29]

Wenzel DM,Brzovic PS.UBCH7 reactivity profile reveals parkin and HHARI to be RING/HECT hybrids..Nature2011;474:105-8 PMCID:PMC3444301

[30]

Ho SR,Lee YJ.RNF144A, an E3 ubiquitin ligase for DNA-PKcs, promotes apoptosis during DNA damage..Proc Natl Acad Sci U S A2014;111:E2646-55 PMCID:PMC4084471

[31]

Kelsall IR,Olszewski JL.TRIAD1 and HHARI bind to and are activated by distinct neddylated Cullin-RING ligase complexes..EMBO J2013;32:2848-60 PMCID:PMC3817463

[32]

Stieglitz B,Koliopoulos MG,Rittinger K.LUBAC synthesizes linear ubiquitin chains via a thioester intermediate..EMBO Rep2012;13:840-6 PMCID:PMC3432797

[33]

Smit JJ,Noordermeer SM,van der Reijden BA.The E3 ligase HOIP specifies linear ubiquitin chain assembly through its RING-IBR-RING domain and the unique LDD extension..EMBO J2012;31:3833-44 PMCID:PMC3463842

[34]

Li W,Ulbrich A.Genome-wide and functional annotation of human E3 ubiquitin ligases identifies MULAN, a mitochondrial E3 that regulates the organelle’s dynamics and signaling..PLoS One2008;3:e1487 PMCID:PMC2198940

[35]

Scheffner M.HECT E3s and human disease..BMC Biochem.2007;8 Suppl 1:S6 PMCID:PMC2106370

[36]

Ingham RJ,Pawson T.The Nedd4 family of E3 ubiquitin ligases: functional diversity within a common modular architecture..Oncogene2004;23:1972-84

[37]

Scheffner M.Mammalian HECT ubiquitin-protein ligases: biological and pathophysiological aspects..Biochim Biophys Acta2014;1843:61-74

[38]

Zhu K,Chen X.Allosteric auto-inhibition and activation of the Nedd4 family E3 ligase Itch..EMBO Rep2017;18:1618-30 PMCID:PMC5579370

[39]

Yao W,Gu A,Shi Z.WW domain-mediated regulation and activation of E3 ubiquitin ligase Suppressor of Deltex..J Biol Chem2018;293:16697-708 PMCID:PMC6204921

[40]

Yang Q,Cui M,Wang W.Nedd4L expression is decreased in ovarian epithelial cancer tissues compared to ovarian non-cancer tissue..J Obstet Gynaecol Res2015;41:1959-64

[41]

Sun H,Wang J.Phosphatase and tensin homolog deleted on chromosome 10 degradation induced by NEDD4 promotes acquired erlotinib resistance in non-small-cell lung cancer..Tumour Biol2017;39:1010428317709639

[42]

Huang X,Zhang E.The NEDD4-1 E3 ubiquitin ligase: A potential molecular target for bortezomib sensitivity in multiple myeloma..Int J Cancer2020;146:1963-78 PMCID:PMC7027789

[43]

Akkaya BG,Ritchie TK.The multidrug resistance pump ABCB1 is a substrate for the ubiquitin ligase NEDD4-1..Mol Membr Biol2015;32:39-45 PMCID:PMC4844833

[44]

Yin Q,Han T,Wan L.ITCH as a potential therapeutic target in human cancers..Semin Cancer Biol2020;67:117-30 PMCID:PMC7724637

[45]

Riling C,Kumar S.Itch WW Domains Inhibit Its E3 Ubiquitin Ligase Activity by Blocking E2-E3 Ligase Trans-thiolation..J Biol Chem2015;290:23875-87 PMCID:PMC4583040

[46]

Abedini MR,Brun J,Gray DA.Cisplatin induces p53-dependent FLICE-like inhibitory protein ubiquitination in ovarian cancer cells..Cancer Res2008;68:4511-7

[47]

Abedini MR,Bergeron R,Tsang BK.Akt promotes chemoresistance in human ovarian cancer cells by modulating cisplatin-induced, p53-dependent ubiquitination of FLICE-like inhibitory protein..Oncogene2010;29:11-25

[48]

Abedini MR,Huang YF.Cell fate regulation by gelsolin in human gynecologic cancers..Proc Natl Acad Sci U S A2014;111:14442-7 PMCID:PMC4209992

[49]

Henderson MJ,Hird S.EDD, the human hyperplastic discs protein, has a role in progesterone receptor coactivation and potential involvement in DNA damage response..J Biol Chem2002;277:26468-78

[50]

Munoz MA,Henderson MJ.The E3 ubiquitin ligase EDD regulates S-phase and G(2)/M DNA damage checkpoints..Cell Cycle2007;6:3070-7

[51]

Gudjonsson T,Savic V.TRIP12 and UBR5 suppress spreading of chromatin ubiquitylation at damaged chromosomes..Cell2012;150:697-709

[52]

Wang Y,Kane EI,Spratt DE.HECT E3 ubiquitin ligases - emerging insights into their biological roles and disease relevance..J Cell Sci2020;133:jcs228072 PMCID:PMC7157599

[53]

Clancy JL,Russell AJ.EDD, the human orthologue of the hyperplastic discs tumour suppressor gene, is amplified and overexpressed in cancer..Oncogene2003;22:5070-81

[54]

O’Brien PM,Scurry JP.The E3 ubiquitin ligase EDD is an adverse prognostic factor for serous epithelial ovarian cancer and modulates cisplatin resistance in vitro..Br J Cancer2008;98:1085-93 PMCID:PMC2275489

[55]

Bradley A,Ziebarth A.EDD enhances cell survival and cisplatin resistance and is a therapeutic target for epithelial ovarian cancer..Carcinogenesis2014;35:1100-9 PMCID:PMC4004201

[56]

Eblen ST.MOAP-1, UBR5 and cisplatin resistance in ovarian cancer..Transl Cancer Res2017;6:S18-21 PMCID:PMC5878060

[57]

Matsuura K,Cocce K,Kornbluth S.Downregulation of the proapoptotic protein MOAP-1 by the UBR5 ubiquitin ligase and its role in ovarian cancer resistance to cisplatin..Oncogene2017;36:1698-706 PMCID:PMC5447866

[58]

Burger AM.The ubiquitin-mediated protein degradation pathway in cancer: therapeutic implications..Eur J Cancer2004;40:2217-29

[59]

Morreale FE.Types of Ubiquitin Ligases..Cell2016;165:248.e1

[60]

Cui D,Zhao Y.Cullin-RING ligases in regulation of autophagy..Cell Div2016;11:8 PMCID:PMC4902950

[61]

Bulatov E.Targeting Cullin-RING E3 ubiquitin ligases for drug discovery: structure, assembly and small-molecule modulation..Biochem J2015;467:365-86 PMCID:PMC4403949

[62]

Pan WW,Yu C.Ubiquitin E3 ligase CRL4(CDT2/DCAF2) as a potential chemotherapeutic target for ovarian surface epithelial cancer..J Biol Chem2013;288:29680-91 PMCID:PMC3795265

[63]

Lydeard JR,Harper JW.Building and remodelling Cullin-RING E3 ubiquitin ligases..EMBO Rep2013;14:1050-61 PMCID:PMC3849489

[64]

Chen Z,Zhang F.Cullin family proteins and tumorigenesis: genetic association and molecular mechanisms..J Cancer2015;6:233-42 PMCID:PMC4317758

[65]

Zhao Y.Cullin-RING Ligases as attractive anti-cancer targets..Curr Pharm Des2013;19:3215-25 PMCID:PMC4034125

[66]

Skaar JR,Pagano M.SCF ubiquitin ligase-targeted therapies..Nat Rev Drug Discov2014;13:889-903 PMCID:PMC4410837

[67]

Lee EK.SCFs in the new millennium..Oncogene2014;33:2011-8

[68]

Zhang Q,Gao Q.beta-TRCP-mediated AEBP2 ubiquitination and destruction controls cisplatin resistance in ovarian cancer..Biochem Biophys Res Commun2020;523:274-9

[69]

Gutgemann I,Jackson PK.Emi1 protein accumulation implicates misregulation of the anaphase promoting complex/cyclosome pathway in ovarian clear cell carcinoma..Mod Pathol2008;21:445-54

[70]

Chou JL,Chen LY.Promoter hypermethylation of FBXO32, a novel TGF-beta/SMAD4 target gene and tumor suppressor, is associated with poor prognosis in human ovarian cancer..Lab Invest2010;90:414-25 PMCID:PMC2829100

[71]

Kim S,DeLisi C.Pathway-based classification of cancer subtypes..Biol Direct2012;7:21 PMCID:PMC3485163

[72]

Chiu HW,Lin HY.FBXL7 Upregulation Predicts a Poor Prognosis and Associates with a Possible Mechanism for Paclitaxel Resistance in Ovarian Cancer..J Clin Med2018;7:330 PMCID:PMC6209951

[73]

Kamran M,Xu D.Aurora kinase A regulates Survivin stability through targeting FBXL7 in gastric cancer drug resistance and prognosis..Oncogenesis2017;6:e298 PMCID:PMC5337621

[74]

He J,Tsukada Y.The H3K36 demethylase Jhdm1b/Kdm2b regulates cell proliferation and senescence through p15(Ink4b)..Nat Struct Mol Biol2008;15:1169-75 PMCID:PMC2612995

[75]

Sanchez C,Demmers JA,Strouboulis J.Proteomics analysis of Ring1B/Rnf2 interactors identifies a novel complex with the Fbxl10/Jhdm1B histone demethylase and the Bcl6 interacting corepressor..Mol Cell Proteomics2007;6:820-34

[76]

Yan M,Shen R.miR-146b promotes cell proliferation and increases chemosensitivity, but attenuates cell migration and invasion via FBXL10 in ovarian cancer..Cell Death Dis2018;9:1123 PMCID:PMC6224598

[77]

Wang X,Bird K.VprBP/DCAF1 regulates the degradation and nonproteolytic activation of the cell cycle transcription factor FoxM1..Mol Cell Biol2017;37:e00609-16 PMCID:PMC5472828

[78]

Hu X,Xu L.Cul4 E3 ubiquitin ligase regulates ovarian cancer drug resistance by targeting the antiapoptotic protein BIRC3..Cell Death Dis2019;10:104 PMCID:PMC6362125

[79]

Jang SM,Fu H.The RepID-CRL4 ubiquitin ligase complex regulates metaphase to anaphase transition via BUB3 degradation..Nat Commun2020;11:24 PMCID:PMC6946706

[80]

Acquaviva C.The anaphase-promoting complex/cyclosome: APC/C..J Cell Sci2006;119:2401-4

[81]

Peters JM.The anaphase promoting complex/cyclosome: a machine designed to destroy..Nat Rev Mol Cell Biol2006;7:644-56

[82]

Raab M,Becker S.Boosting the apoptotic response of high-grade serous ovarian cancers with CCNE1 amplification to paclitaxel in vitro by targeting APC/C and the pro-survival protein MCL-1..Int J Cancer2020;146:1086-98

[83]

Belur Nagaraj A,Avelar R.Mitotic exit dysfunction through the deregulation of APC/C characterizes cisplatin-resistant state in epithelial ovarian cancer..Clin Cancer Res2018;24:4588-601 PMCID:PMC6139058

[84]

Deveraux QL,Salvesen GS.X-linked IAP is a direct inhibitor of cell-death proteases..Nature1997;388:300-4

[85]

Yang YL.The IAP family: endogenous caspase inhibitors with multiple biological activities..Cell Res2000;10:169-77

[86]

Li J,Kim JM.Human ovarian cancer and cisplatin resistance: possible role of inhibitor of apoptosis proteins..Endocrinology2001;142:370-80

[87]

Sasaki H,Kotsuji F.Down-regulation of X-linked inhibitor of apoptosis protein induces apoptosis in chemoresistant human ovarian cancer cells..Cancer Res2000;60:5659-66

[88]

Fraser M,Jahani-Asl A,Thompson WE.Chemoresistance in human ovarian cancer: the role of apoptotic regulators..Reprod Biol Endocrinol2003;1:66 PMCID:PMC270001

[89]

He X,Maguire JL,Shridhar V.HtrA1 sensitizes ovarian cancer cells to cisplatin-induced cytotoxicity by targeting XIAP for degradation..Int J Cancer2012;130:1029-35 PMCID:PMC3206182

[90]

Yang X,Gao Q.Regulation of HtrA2/Omi by X-linked inhibitor of apoptosis protein in chemoresistance in human ovarian cancer cells..Gynecol Oncol2005;97:413-21

[91]

Shangary S.Targeting the MDM2-p53 interaction for cancer therapy..Clin Cancer Res2008;14:5318-24 PMCID:PMC2676446

[92]

Iwakuma T.MDM2, an introduction..Mol Cancer Res2003;1:993-1000

[93]

Kubbutat MH,Vousden KH.Regulation of p53 stability by Mdm2..Nature1997;387:299-303

[94]

Honda R,Yasuda H.Oncoprotein MDM2 is a ubiquitin ligase E3 for tumor suppressor p53..FEBS Lett1997;420:25-7

[95]

Haupt Y,Kazaz A.Mdm2 promotes the rapid degradation of p53..Nature1997;387:296-9

[96]

Oliner JD,Meltzer PS,Vogelstein B.Amplification of a gene encoding a p53-associated protein in human sarcomas..Nature1992;358:80-3

[97]

Mir R,Martinez-Soler F.Mdm2 antagonists induce apoptosis and synergize with cisplatin overcoming chemoresistance in TP53 wild-type ovarian cancer cells..Int J Cancer2013;132:1525-36

[98]

Wu AY,Cang W.Fn14 overcomes cisplatin resistance of high-grade serous ovarian cancer by promoting Mdm2-mediated p53-R248Q ubiquitination and degradation..J Exp Clin Cancer Res2019;38:176 PMCID:PMC6485139

[99]

Cui L,Chen C.Overexpression of CCDC69 activates p14(ARF)/MDM2/p53 pathway and confers cisplatin sensitivity..J Ovarian Res2019;12:4 PMCID:PMC6334460

[100]

Braschi E,McBride HM.MAPL is a new mitochondrial SUMO E3 ligase that regulates mitochondrial fission..EMBO Rep2009;10:748-54 PMCID:PMC2727426

[101]

Prudent J,Sugiura A,Shore GC.MAPL SUMOylation of Drp1 Stabilizes an ER/Mitochondrial Platform Required for Cell Death..Mol Cell2015;59:941-55

[102]

Zhang B,Li HL.GIDE is a mitochondrial E3 ubiquitin ligase that induces apoptosis and slows growth..Cell Res2008;18:900-10 PMCID:PMC3156110

[103]

Jung JH,Lee JY.E3 ubiquitin ligase Hades negatively regulates the exonuclear function of p53..Cell Death Differ2011;18:1865-75 PMCID:PMC3214910

[104]

Min B,Chi SW.Ubiquitination-dependent degradation of p73 by the mitochondrial E3 ubiquitin ligase Hades..Biochem Biophys Res Commun2015;467:316-21

[105]

Yun J,Yang H.MUL1 acts in parallel to the PINK1/parkin pathway in regulating mitofusin and compensates for loss of PINK1/parkin..Elife2014;3:e01958 PMCID:PMC4044952

[106]

Kim SY,Byeon HK,Kim CH.FOXO3 induces ubiquitylation of AKT through MUL1 regulation..Oncotarget2017;8:110474-89 PMCID:PMC5746397

[107]

Li J,Chen G.Mitochondrial outer-membrane E3 ligase MUL1 ubiquitinates ULK1 and regulates selenite-induced mitophagy..Autophagy2015;11:1216-29 PMCID:PMC4590677

[108]

Peng J,Yang J.Mitochondrial E3 ubiquitin ligase 1: A key enzyme in regulation of mitochondrial dynamics and functions..Mitochondrion2016;28:49-53

[109]

Jenkins K,Sadler A.Mitochondrially localised MUL1 is a novel modulator of antiviral signaling..Immunol Cell Biol2013;91:321-30

[110]

Doiron K,Coyaud E,Raught B.The dynamic interacting landscape of MAPL reveals essential functions for SUMOylation in innate immunity..Sci Rep2017;7:107 PMCID:PMC5427825

[111]

Lee J,Jung JH.MUL1 E3 ligase regulates the antitumor effects of metformin in chemoresistant ovarian cancer cells via AKT degradation..Int J Oncol2019;54:1833-42

[112]

Beitel LK,Lumbroso R.Cloning and characterization of an androgen receptor N-terminal-interacting protein with ubiquitin-protein ligase activity..J Mol Endocrinol2002;29:41-60

[113]

Daks AA,Barlev NA.[The role of different E3 ubiquitin ligases in regulation of the P53 tumor suppressor protein]..Tsitologiia2013;55:673-87

[114]

Wang Z,Dong L,He X.A novel oncoprotein Pirh2: rising from the shadow of MDM2..Cancer Sci2011;102:909-17

[115]

Yang-Hartwich Y,Roberts CM.p53-Pirh2 Complex Promotes Twist1 Degradation and Inhibits EMT..Mol Cancer Res2019;17:153-64 PMCID:PMC6800184

[116]

Reed JC.Degrading liaisons: Siah structure revealed..Nat Struct Biol2002;9:8-10

[117]

Christian PA,Schwarze SR.Possible role of death receptor-mediated apoptosis by the E3 ubiquitin ligases Siah2 and POSH..Mol Cancer2011;10:57 PMCID:PMC3115909

[118]

Kilroy G,Newman S.The ubiquitin ligase Siah2 regulates obesity-induced adipose tissue inflammation..Obesity (Silver Spring)2015;23:2223-32 PMCID:PMC4633373

[119]

Sun RC.Hypoxic regulation of glutamine metabolism through HIF1 and SIAH2 supports lipid synthesis that is necessary for tumor growth..Cell Metab2014;19:285-92 PMCID:PMC3920584

[120]

Zhang B,Zheng X.A common variant in the SIAH2 locus is associated with estrogen receptor-positive breast cancer in the Chinese Han population..PLoS One2013;8:e79365 PMCID:PMC3823686

[121]

Muller S,Ginter T.SIAH2 antagonizes TYK2-STAT3 signaling in lung carcinoma cells..Oncotarget2014;5:3184-96 PMCID:PMC4102802

[122]

Rizzardi AE,Koopmeiners JS.Evaluation of protein biomarkers of prostate cancer aggressiveness..BMC Cancer2014;14:244 PMCID:PMC4101830

[123]

Hsieh SC,Zheng YH,Lin YS.The E3 ubiquitin ligase SIAH2 is a prosurvival factor overexpressed in oral cancer..Anticancer Res2013;33:4965-73

[124]

Qiu J,Meng F.SIAH 2 expression predicts chemoresistance and poor clinical outcomes in patients with epithelial ovarian cancer..Int J Clin Exp Pathol2016;9:8432-9

[125]

Perez M,Zapico I.Mutual regulation between SIAH2 and DYRK2 controls hypoxic and genotoxic signaling pathways..J Mol Cell Biol2012;4:316-30

[126]

Shah M,Dewing A,Pellecchia M.Inhibition of Siah2 ubiquitin ligase by vitamin K3 (menadione) attenuates hypoxia and MAPK signaling and blocks melanoma tumorigenesis..Pigment Cell Melanoma Res2009;22:799-808 PMCID:PMC2863310

[127]

Jansen MP,Dorssers LC.Downregulation of SIAH2, an ubiquitin E3 ligase, is associated with resistance to endocrine therapy in breast cancer..Breast Cancer Res Treat2009;116:263-71

[128]

Emmerich CH,Strickson S.Activation of the canonical IKK complex by K63/M1-linked hybrid ubiquitin chains..Proc Natl Acad Sci U S A2013;110:15247-52 PMCID:PMC3780889

[129]

Kirisako T,Murata S.A ubiquitin ligase complex assembles linear polyubiquitin chains..EMBO J2006;25:4877-87 PMCID:PMC1618115

[130]

Garnett MJ,Heidorn SJ.Systematic identification of genomic markers of drug sensitivity in cancer cells..Nature2012;483:570-5 PMCID:PMC3349233

[131]

MacKay C,Ibrahim AFM.E3 ubiquitin ligase HOIP attenuates apoptotic cell death induced by cisplatin..Cancer Res2014;74:2246-57 PMCID:PMC3990471

[132]

Li X.Proteolysis-targeting chimera (PROTAC) for targeted protein degradation and cancer therapy..J Hematol Oncol2020;13:50 PMCID:PMC7218526

[133]

Salami J.Waste disposal-An attractive strategy for cancer therapy..Science2017;355:1163-7

[134]

Noblejas-Lopez MDM,Burgos M.Activity of BET-proteolysis targeting chimeric (PROTAC) compounds in triple negative breast cancer..J Exp Clin Cancer Res2019;38:383 PMCID:PMC6717344

[135]

Soucy TA,Milhollen MA.An inhibitor of NEDD8-activating enzyme as a new approach to treat cancer..Nature2009;458:732-6

[136]

Ooi MG,Kotoula V.Interactions of the Hdm2/p53 and proteasome pathways may enhance the antitumor activity of bortezomib..Clin Cancer Res2009;15:7153-60 PMCID:PMC3672410

[137]

Vassilev LT,Graves B.In vivo activation of the p53 pathway by small-molecule antagonists of MDM2..Science2004;303:844-8

[138]

Chargari C,Angevin E.Preclinical assessment of JNJ-26854165 (Serdemetan), a novel tryptamine compound with radiosensitizing activity in vitro and in tumor xenografts..Cancer Lett2011;312:209-18

[139]

Wang H,Ren S,Yan C.A small-molecule inhibitor of MDMX activates p53 and induces apoptosis..Mol Cancer Ther2011;10:69-79 PMCID:PMC3058295

[140]

Manzanillo PS,Watson RO.The ubiquitin ligase parkin mediates resistance to intracellular pathogens..Nature2013;501:512-6 PMCID:PMC3886920

[141]

Cesari R,Calin GA.Parkin, a gene implicated in autosomal recessive juvenile parkinsonism, is a candidate tumor suppressor gene on chromosome 6q25-q27..Proc Natl Acad Sci U S A2003;100:5956-61 PMCID:PMC156308

[142]

Sun X,Hao J.Parkin deficiency contributes to pancreatic tumorigenesis by inducing spindle multipolarity and misorientation..Cell Cycle2013;12:1133-41 PMCID:PMC3646869

[143]

Ong JY.E3 ubiquitin ligases in cancer and their pharmacological targeting. In: Summers M, editor. Ubiquitin Proteasome System-Current Insights into Mechanism Cellular Regulation and Disease. IntechOpen2019;

[144]

Zhang L,Qiang Y.Overexpression of deubiquitinating enzyme USP28 promoted non-small cell lung cancer growth..J Cell Mol Med2015;19:799-805 PMCID:PMC4395194

[145]

Cox JL,Wuebben EL,Hollingsworth MA.Context-dependent function of the deubiquitinating enzyme USP9X in pancreatic ductal adenocarcinoma..Cancer Biol Ther2014;15:1042-52 PMCID:PMC4119071

[146]

Tanguturi P,Ramakrishna S.The role of deubiquitinating enzymes in cancer drug resistance..Cancer Chemother Pharmacol2020;85:627-39

[147]

Jin C,Lou X.UCHL1 Is a putative tumor suppressor in ovarian cancer cells and contributes to cisplatin resistance..J Cancer2013;4:662-70 PMCID:PMC3805994

[148]

Sonego M,Costa A.USP1 links platinum resistance to cancer cell dissemination by regulating Snail stability..Sci Adv2019;5:eaav3235 PMCID:PMC6506239

[149]

Liu D.Long non-coding RNA GEHT1 promoted the proliferation of ovarian cancer cells via modulating the protein stability of HIF1alpha..Biosci Rep2019;39:BSR20181650 PMCID:PMC6504664

[150]

Hu J,Mei Z.Interaction of E3 Ubiquitin Ligase MARCH7 with Long Noncoding RNA MALAT1 and Autophagy-Related Protein ATG7 Promotes Autophagy and Invasion in Ovarian Cancer..Cell Physiol Biochem2018;47:654-66

[151]

Kim SA,Yoon SK,Kuh HJ.Indirect modulation of sensitivity to 5-fluorouracil by microRNA-96 in human colorectal cancer cells..Arch Pharm Res2015;38:239-48

[152]

Chen S,Sun KX,Zhao Y.MicroRNA-133b targets glutathione S-transferase pi expression to increase ovarian cancer cell sensitivity to chemotherapy drugs..Drug Des Devel Ther2015;9:5225-35 PMCID:PMC4577257

[153]

Chang L,Solinas G,Maeda S,Liu YC.The E3 ubiquitin ligase itch couples JNK activation to TNFalpha-induced cell death by inducing c-FLIP(L) turnover..Cell2006;124:601-13

AI Summary AI Mindmap
PDF

65

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/