Login Register Cart 0
Generic placeholder image

Current Pharmaceutical Design

Editor-in-Chief

ISSN (Print): 1381-6128
ISSN (Online): 1873-4286

Back
Journal Home About Journal Editorial Board Journal Insight Current Issue Volumes/Issues
Subscribe
Review Article

Sumoylation as an Emerging Target in Therapeutics against Cancer

Author(s): Sitong Liu, Lichun Wang, Dongjun Jiang, Wei Wei, Mushyeda Fatima Nasir, Muhammad Saad Khan, Qudsia Yousafi, Xintong Liu, Xueqi Fu*, Xiaomeng Li* and Jiang Li*

Volume 26, Issue 37, 2020

Page: [4764 - 4776] Pages: 13

DOI: 10.2174/1381612826666200622124134

Price: $65

Abstract

Sumoylation is the Post-translational modification gaining most of the research interest recently. Sumoylation is involved in various crucial functions of the cell such as regulation of cell cycle, DNA damage repair, apoptosis, etc. Oncology is advancing in radiotherapy, targeted chemotherapy, various forms of immunotherapy and targeted gene therapy. Researches are being conducted to prove its connotation with a variety of cancers and inhibitors are being developed to obstruct the fatal effect caused by misbalance of the SUMO-catalytic cycle. It has been shown that up-regulation of certain enzymes of Sumoylation correlates with cancer incidence in most of the cases. However, in some cases, down-regulation also associates with cancer invasion such as underexpression of UBC9 in initial stage breast cancer. This can aid in future study, treatment, and diagnosis of a variety of cancers including breast cancer, prostate cancer, lung adenocarcinoma, melanoma, multiple myeloma, etc. Various mechanistic assays are being developed and used to identify potential inhibitors against the dysregulated proteins of Sumoylation. This review summarizes the normal roles of the enzymes involved in the SUMOcatalytic cycle, their misbalanced regulation leading to tumorigenesis and nearly all the potent inhibitors identified to date, while after detailed studied it was observed that ML-792 could be a promising inhibitor in treating cancers by inhibiting Sumoylation enzymes.

Keywords: Post-translational modifications, ubiquitination, sumoylation, sentrin-specific proteases, sumo activating enzyme, RWD-domaincontaining sumoylation enhancer.

« Previous Next »
[1]
Xu Y, Chou K-C. Recent Progress in Predicting Posttranslational Modification Sites in Proteins. Curr Top Med Chem 2016; 16(6): 591-603.
[http://dx.doi.org/10.2174/1568026615666150819110421 ] [PMID: 26286211]
[2]
Zamaraev AV, Kopeina GS, Prokhorova EA, Zhivotovsky B, Lavrik IN. Post-translational Modification of Caspases: The Other Side of Apoptosis Regulation. Trends Cell Biol 2017; 27(5): 322-39.
[http://dx.doi.org/10.1016/j.tcb.2017.01.003 ] [PMID: 28188028]
[3]
Gong L, Qi R, Li DW. Sumoylation Pathway as Potential Therapeutic Targets in Cancer. Curr Mol Med 2017; 16(10): 900-5.
[http://dx.doi.org/10.2174/1566524016666161223105201 ] [PMID: 28017138]
[4]
Duan X, Trent JO, Ye H. Targeting the SUMO E2 conjugating enzyme Ubc9 interaction for anti-cancer drug design. Anticancer Agents Med Chem 2009; 9(1): 51-4.
[http://dx.doi.org/10.2174/187152009787047716 ] [PMID: 19149481]
[5]
Mo YY, Yu Y, Theodosiou E, Ee PLR, Beck WT. A role for Ubc9 in tumorigenesis. Oncogene 2005; 24(16): 2677-83.
[http://dx.doi.org/10.1038/sj.onc.1208210 ] [PMID: 15735760]
[6]
Kobayashi S, Shibata H, Yokota K, et al. FHL2, UBC9, and PIAS1 are novel estrogen receptor α-interacting proteins. Endocr Res 2004; 30(4): 617-21.
[http://dx.doi.org/10.1081/ERC-200043789 ] [PMID: 15666801]
[7]
McDoniels-Silvers AL, Nimri CF, Stoner GD, Lubet RA, You M. Differential gene expression in human lung adenocarcinomas and squamous cell carcinomas. Clin Cancer Res 2002; 8(4): 1127-38.
[PMID: 11948124]
[8]
Kim JH, Lee JM, Nam HJ, et al. SUMOylation of pontin chromatin-remodeling complex reveals a signal integration code in prostate cancer cells. Proc Natl Acad Sci USA 2007; 104(52): 20793-8.
[http://dx.doi.org/10.1073/pnas.0710343105 ] [PMID: 18087039]
[9]
Müller S, Matunis MJ, Dejean A. Conjugation with the ubiquitin-related modifier SUMO-1 regulates the partitioning of PML within the nucleus. EMBO J 1998; 17(1): 61-70.
[http://dx.doi.org/10.1093/emboj/17.1.61 ] [PMID: 9427741]
[10]
Kim KIL, Baek SH, Chung CH. Versatile protein tag, SUMO: its enzymology and biological function. J Cell Physiol 2002; 191(3): 257-68.
[http://dx.doi.org/10.1002/jcp.10100 ] [PMID: 12012321]
[11]
Gao M, Karin M. Regulating the regulators: control of protein ubiquitination and ubiquitin-like modifications by extracellular stimuli. Mol Cell 2005; 19(5): 581-93.
[http://dx.doi.org/10.1016/j.molcel.2005.08.017 ] [PMID: 16137616]
[12]
Tang X, Chen Z, Deng M, et al. The Sumoylation Modulated Tumor Suppressor p53 Regulates Cell Cycle Checking Genes to Mediate Lens Differentiation. Curr Mol Med 2018; 18(8): 556-65.
[http://dx.doi.org/10.2174/1566524019666190111154450 ] [PMID: 30636605]
[13]
Isogai S, Shirakawa M. [Protein modification by SUMO]. Seikagaku 2007; 79(12): 1120-30..
[PMID: 18203451]
[14]
Bohren KM, Nadkarni V, Song JH, Gabbay KH, Owerbach DA. M55V polymorphism in a novel SUMO gene (SUMO-4) differentially activates heat shock transcription factors and is associated with susceptibility to type I diabetes mellitus. J Biol Chem 2004; 279(26): 27233-8.
[http://dx.doi.org/10.1074/jbc.M402273200 ] [PMID: 15123604]
[15]
Wang CY, Yang P, Li M, Gong F. Characterization of a negative feedback network between SUMO4 expression and NFkappaB transcriptional activity. Biochem Biophys Res Commun 2009; 381(4): 477-81.
[http://dx.doi.org/10.1016/j.bbrc.2009.02.060 ] [PMID: 19222990]
[16]
Eifler K, Vertegaal ACO. SUMOylation-Mediated Regulation of Cell Cycle Progression and Cancer. Trends Biochem Sci 2015; 40(12): 779-93.
[http://dx.doi.org/10.1016/j.tibs.2015.09.006 ] [PMID: 26601932]
[17]
Flotho A, Melchior F. Sumoylation: a regulatory protein modification in health and disease. Annu Rev Biochem 2013; 82(1): 357-85.
[http://dx.doi.org/10.1146/annurev-biochem-061909-093311 ] [PMID: 23746258]
[18]
Hoellein A, Fallahi M, Schoeffmann S, et al. Myc-induced SUMOylation is a therapeutic vulnerability for B-cell lymphoma. Blood 2014; 124(13): 2081-90.
[http://dx.doi.org/10.1182/blood-2014-06-584524 ] [PMID: 25143484]
[19]
Desterro JMP, Rodriguez MS, Kemp GD, Hay RT. Identification of the enzyme required for activation of the small ubiquitin-like protein SUMO-1. J Biol Chem 1999; 274(15): 10618-24.
[http://dx.doi.org/10.1074/jbc.274.15.10618 ] [PMID: 10187858]
[20]
Tatham MH, Kim S, Jaffray E, Song J, Chen Y, Hay RT. Unique binding interactions among Ubc9, SUMO and RanBP2 reveal a mechanism for SUMO paralog selection. Nat Struct Mol Biol 2005; 12(1): 67-74.
[http://dx.doi.org/10.1038/nsmb878 ] [PMID: 15608651]
[21]
Rytinki MM, Kaikkonen S, Pehkonen P, Jääskeläinen T, Palvimo JJ. PIAS proteins: pleiotropic interactors associated with SUMO. Cell Mol Life Sci 2009; 66(18): 3029-41.
[http://dx.doi.org/10.1007/s00018-009-0061-z ] [PMID: 19526197]
[22]
Stephan AK, Kliszczak M, Morrison CG. The Nse2/Mms21 SUMO ligase of the Smc5/6 complex in the maintenance of genome stability. FEBS Lett 2011; 585(18): 2907-13.
[http://dx.doi.org/10.1016/j.febslet.2011.04.067 ] [PMID: 21550342]
[23]
Reverter D, Lima CD. Insights into E3 ligase activity revealed by a SUMO-RanGAP1-Ubc9-Nup358 complex. Nature 2005; 435(7042): 687-92.
[http://dx.doi.org/10.1038/nature03588 ] [PMID: 15931224]
[24]
Hatakeyama S. TRIM Family Proteins: Roles in Autophagy, Immunity, and Carcinogenesis. Trends Biochem Sci 2017; 42(4): 297-311.
[http://dx.doi.org/10.1016/j.tibs.2017.01.002 ] [PMID: 28118948]
[25]
Yang SH, Sharrocks AD. The SUMO E3 ligase activity of Pc2 is coordinated through a SUMO interaction motif. Mol Cell Biol 2010; 30(9): 2193-205.
[http://dx.doi.org/10.1128/MCB.01510-09 ] [PMID: 20176810]
[26]
Koliopoulos MG, Esposito D, Christodoulou E, Taylor IA, Rittinger K. Functional role of TRIM E3 ligase oligomerization and regulation of catalytic activity. EMBO J 2016; 35(11): 1204-18.
[http://dx.doi.org/10.15252/embj.201593741 ] [PMID: 27154206]
[27]
Moschos SJ, Jukic DM, Athanassiou C, et al. Expression analysis of Ubc9, the single small ubiquitin-like modifier (SUMO) E2 conjugating enzyme, in normal and malignant tissues. Hum Pathol 2010; 41(9): 1286-98.
[http://dx.doi.org/10.1016/j.humpath.2010.02.007 ] [PMID: 20561671]
[28]
Wang S, Jiao B, Geng S, Ma S, Liang Z, Lu S. Combined aberrant expression of microRNA-214 and UBC9 is an independent unfavorable prognostic factor for patients with gliomas. Med Oncol 2014; 31(1): 767.
[http://dx.doi.org/10.1007/s12032-013-0767-5 ] [PMID: 24277415]
[29]
Hickey CM, Wilson NR, Hochstrasser M. Function and regulation of SUMO proteases. Nat Rev Mol Cell Biol 2012; 13(12): 755-66.
[http://dx.doi.org/10.1038/nrm3478 ] [PMID: 23175280]
[30]
Mukhopadhyay D, Dasso M. Modification in reverse: the SUMO proteases. Trends Biochem Sci 2007; 32(6): 286-95.
[http://dx.doi.org/10.1016/j.tibs.2007.05.002 ] [PMID: 17499995]
[31]
Liu Y, Zhang L, Tang X, et al. Determination of Expression Patterns of Seven De-sumoylation Enzymes in Major Ocular Cell Lines. Curr Mol Med 2018; 18(9): 584-93.
[http://dx.doi.org/10.2174/1566524019666190107153440 ] [PMID: 30621560]
[32]
Liu Y, Kieslich CA, Morikis D, Liao J. Engineering pre-SUMO4 as efficient substrate of SENP2. Protein Eng Des Sel 2014; 27(4): 117-26.
[http://dx.doi.org/10.1093/protein/gzu004 ] [PMID: 24671712]
[33]
Owerbach D, McKay EM, Yeh ETH, Gabbay KH, Bohren KMA. A proline-90 residue unique to SUMO-4 prevents maturation and sumoylation. Biochem Biophys Res Commun 2005; 337(2): 517-20.
[http://dx.doi.org/10.1016/j.bbrc.2005.09.090 ] [PMID: 16198310]
[34]
Xu Z, Chau SF, Lam KH, Chan HY, Ng TB, Au SWN. Crystal structure of the SENP1 mutant C603S-SUMO complex reveals the hydrolytic mechanism of SUMO-specific protease. Biochem J 2006; 398(3): 345-52.
[http://dx.doi.org/10.1042/BJ20060526 ] [PMID: 16712526]
[35]
Hu C, Jiang X. The SUMO-specific protease family regulates cancer cell radiosensitivity. Biomed Pharmacother 2019; 109: 66-70.
[http://dx.doi.org/10.1016/j.biopha.2018.10.071 ] [PMID: 30396093]
[36]
Schimmel J, Eifler K, Sigurðsson JO, et al. Uncovering SUMOylation dynamics during cell-cycle progression reveals FoxM1 as a key mitotic SUMO target protein. Mol Cell 2014; 53(6): 1053-66.
[http://dx.doi.org/10.1016/j.molcel.2014.02.001 ] [PMID: 24582501]
[37]
Ouyang KJ, Woo LL, Zhu J, Huo D, Matunis MJ, Ellis NA. SUMO modification regulates BLM and RAD51 interaction at damaged replication forks. PLoS Biol 2009; 7(12) e1000252
[http://dx.doi.org/10.1371/journal.pbio.1000252 ] [PMID: 19956565]
[38]
Keusekotten K, Bade VN, Meyer-Teschendorf K, et al. Multivalent interactions of the SUMO-interaction motifs in RING finger protein 4 determine the specificity for chains of the SUMO. Biochem J 2014; 457(1): 207-14.
[http://dx.doi.org/10.1042/BJ20130753 ] [PMID: 24151981]
[39]
Song J, Durrin LK, Wilkinson TA, Krontiris TG, Chen Y. Identification of a SUMO-binding motif that recognizes SUMO-modified proteins. Proc Natl Acad Sci USA 2004; 101(40): 14373-8.
[http://dx.doi.org/10.1073/pnas.0403498101 ] [PMID: 15388847]
[40]
Merrill JC, Melhuish TA, Kagey MH, Yang SH, Sharrocks AD, Wotton D. A role for non-covalent SUMO interaction motifs in Pc2/CBX4 E3 activity. PLoS One 2010; 5(1) e8794
[http://dx.doi.org/10.1371/journal.pone.0008794 ] [PMID: 20098713]
[41]
Li S, Wang M, Qu X, et al. SUMOylation of PES1 upregulates its stability and function via inhibiting its ubiquitination. Oncotarget 2016; 7(31): 50522-34.
[http://dx.doi.org/10.18632/oncotarget.10494 ] [PMID: 27409667]
[42]
Finkbeiner E, Haindl M, Raman N, Muller S. SUMO routes ribosome maturation. Nucleus 2011; 2(6): 527-32.
[http://dx.doi.org/10.4161/nucl.2.6.17604 ] [PMID: 22064470]
[43]
Ivanschitz L, Takahashi Y, Jollivet F, Ayrault O, Le Bras M, de Thé H. PML IV/ARF interaction enhances p53 SUMO-1 conjugation, activation, and senescence. Proc Natl Acad Sci USA 2015; 112(46): 14278-83.
[http://dx.doi.org/10.1073/pnas.1507540112 ] [PMID: 26578773]
[44]
Qu Y, Chen Q, Lai X, et al. SUMOylation of Grb2 enhances the ERK activity by increasing its binding with Sos1. Mol Cancer 2014; 13(1): 95.
[http://dx.doi.org/10.1186/1476-4598-13-95 ] [PMID: 24775912]
[45]
Carbia-Nagashima A, Gerez J, Perez-Castro C, et al. RSUME, a small RWD-containing protein, enhances SUMO conjugation and stabilizes HIF-1α during hypoxia. Cell 2007; 131(2): 309-23.
[http://dx.doi.org/10.1016/j.cell.2007.07.044 ] [PMID: 17956732]
[46]
Huang CC, Tu SH, Lien HH, et al. Concurrent gene signatures for han chinese breast cancers. PLoS One 2013; 8(10) e76421
[http://dx.doi.org/10.1371/journal.pone.0076421 ] [PMID: 24098497]
[47]
Lee JS, Thorgeirsson SS. Genome-Scale Profiling of Gene Expression in Hepatocellular Carcinoma: Classification, Survival Prediction, and Identification of Therapeutic Targets. Gastroenterology 2004; 127(5): 51-5.
[48]
Kessler JD, Kahle KT, Sun T, et al. 112 Genfome-Wide ShRNA Screening Defines the SUMO-Activating Enzyme (SAE1/2) as a Novel Therapeutic Target for Tumors Driven by c-Myc Oncogenesis. Neurosurgery 2012; 71(2) E547
[http://dx.doi.org/10.1227/01.neu.0000417701.96799.49]
[49]
Fukuda I, Ito A, Hirai G, et al. Ginkgolic acid inhibits protein SUMOylation by blocking formation of the E1-SUMO intermediate. Chem Biol 2009; 16(2): 133-40.
[http://dx.doi.org/10.1016/j.chembiol.2009.01.009 ] [PMID: 19246003]
[50]
Takemoto M, Kawamura Y, Hirohama M, et al. Inhibition of protein SUMOylation by davidiin, an ellagitannin from Davidia involucrata. J Antibiot (Tokyo) 2014; 67(4): 335-8.
[http://dx.doi.org/10.1038/ja.2013.142 ] [PMID: 24424345]
[51]
Fukuda I, Ito A, Uramoto M, et al. Kerriamycin B inhibits protein SUMOylation. J Antibiot (Tokyo) 2009; 62(4): 221-4.
[http://dx.doi.org/10.1038/ja.2009.10 ] [PMID: 19265871]
[52]
Kumar A, Ito A, Hirohama M, Yoshida M, Zhang KYJ. Identification of sumoylation activating enzyme 1 inhibitors by structure-based virtual screening. J Chem Inf Model 2013; 53(4): 809-20.
[http://dx.doi.org/10.1021/ci300618e ] [PMID: 23544417]
[53]
He X, Riceberg J, Soucy T, et al. Probing the roles of SUMOylation in cancer cell biology by using a selective SAE inhibitor. Nat Chem Biol 2017; 13(11): 1164-71.
[http://dx.doi.org/10.1038/nchembio.2463 ] [PMID: 28892090]
[54]
Decque A, Joffre O, Magalhaes JG, et al. Sumoylation coordinates the repression of inflammatory and anti-viral gene-expression programs during innate sensing. Nat Immunol 2016; 17(2): 140-9.
[http://dx.doi.org/10.1038/ni.3342 ] [PMID: 26657003]
[55]
Moschos SJ, Smith AP, Mandic M, et al. SAGE and antibody array analysis of melanoma-infiltrated lymph nodes: identification of Ubc9 as an important molecule in advanced-stage melanomas. Oncogene 2007; 26(29): 4216-25.
[http://dx.doi.org/10.1038/sj.onc.1210216 ] [PMID: 17297476]
[56]
Tomasi ML, Tomasi I, Ramani K, et al. S-adenosyl methionine regulates ubiquitin-conjugating enzyme 9 protein expression and sumoylation in murine liver and human cancers. Hepatology 2012; 56(3): 982-93.
[http://dx.doi.org/10.1002/hep.25701 ] [PMID: 22407595]
[57]
Wu F, Zhu S, Ding Y, Beck WT, Mo YY. MicroRNA-mediated regulation of Ubc9 expression in cancer cells. Clin Cancer Res 2009; 15(5): 1550-7.
[http://dx.doi.org/10.1158/1078-0432.CCR-08-0820 ] [PMID: 19223510]
[58]
Bellail AC, Olson JJ, Hao C. SUMO1 modification stabilizes CDK6 protein and drives the cell cycle and glioblastoma progression. Nat Commun 2014; 5: 4234.
[http://dx.doi.org/10.1038/ncomms5234 ] [PMID: 24953629]
[59]
Driscoll JJ, Pelluru D, Lefkimmiatis K, et al. The sumoylation pathway is dysregulated in multiple myeloma and is associated with adverse patient outcome. Blood 2010; 115(14): 2827-34.
[http://dx.doi.org/10.1182/blood-2009-03-211045 ] [PMID: 19965618]
[60]
Zhao Z, Tan X, Zhao A, et al. microRNA-214-mediated UBC9 expression in glioma. BMB Rep 2012; 45(11): 641-6.
[http://dx.doi.org/10.5483/BMBRep.2012.45.11.097 ] [PMID: 23187003]
[61]
Brandt M, Szewczuk LM, Zhang H, et al. Development of a high-throughput screen to detect inhibitors of TRPS1 sumoylation. Assay Drug Dev Technol 2013; 11(5): 308-25.
[http://dx.doi.org/10.1089/adt.2012.501 ] [PMID: 23772552]
[62]
Hirohama M, Kumar A, Fukuda I, et al. Spectomycin B1 as a novel SUMOylation inhibitor that directly binds to SUMO E2. ACS Chem Biol 2013; 8(12): 2635-42.
[http://dx.doi.org/10.1021/cb400630z ] [PMID: 24143955]
[63]
Rabellino A, Andreani C, Scaglioni PP. The Role of PIAS SUMO E3-Ligases in Cancer. Cancer Res 2017; 77(7): 1542-7.
[http://dx.doi.org/10.1158/0008-5472.CAN-16-2958 ] [PMID: 28330929]
[64]
Wang L, Banerjee S. Differential PIAS3 expression in human malignancy. Oncol Rep 2004; 11(6): 1319-24.
[PMID: 15138572]
[65]
Coppola D, Parikh V, Boulware D, Blanck G. Substantially reduced expression of PIAS1 is associated with colon cancer development. J Cancer Res Clin Oncol 2009; 135(9): 1287-91.
[http://dx.doi.org/10.1007/s00432-009-0570-z ] [PMID: 19288270]
[66]
Wang X, Li L, Wu Y, et al. CBX4 Suppresses Metastasis via Recruitment of HDAC3 to the Runx2 Promoter in Colorectal Carcinoma. Cancer Res 2016; 76(24): 7277-89.
[http://dx.doi.org/10.1158/0008-5472.CAN-16-2100 ] [PMID: 27864346]
[67]
Li J, Xu Y, Long XD, et al. Cbx4 governs HIF-1α to potentiate angiogenesis of hepatocellular carcinoma by its SUMO E3 ligase activity. Cancer Cell 2014; 25(1): 118-31.
[http://dx.doi.org/10.1016/j.ccr.2013.12.008 ] [PMID: 24434214]
[68]
Felix RS, Colleoni GWB, Caballero OL, et al. SAGE analysis highlights the importance of p53csv, ddx5, mapkapk2 and ranbp2 to multiple myeloma tumorigenesis. Cancer Lett 2009; 278(1): 41-8.
[http://dx.doi.org/10.1016/j.canlet.2008.12.022 ] [PMID: 19171422]
[69]
Horio Y, Osada H, Shimizu J, Ogawa S, Hida T, Sekido Y. Relationship of mRNA expressions of RanBP2 and topoisomerase II isoforms to cytotoxicity of amrubicin in human lung cancer cell lines. Cancer Chemother Pharmacol 2010; 66(2): 237-43.
[http://dx.doi.org/10.1007/s00280-009-1151-1 ] [PMID: 19809814]
[70]
Cheng J, Wang D, Wang Z, Yeh ETH. SENP1 enhances androgen receptor-dependent transcription through desumoylation of histone deacetylase 1. Mol Cell Biol 2004; 24(13): 6021-8.
[http://dx.doi.org/10.1128/MCB.24.13.6021-6028.2004 ] [PMID: 15199155]
[71]
Ma C, Wu B, Huang X, et al. SUMO-specific protease 1 regulates pancreatic cancer cell proliferation and invasion by targeting MMP-9. Tumour Biol 2014; 35(12): 12729-35.
[http://dx.doi.org/10.1007/s13277-014-2598-1 ] [PMID: 25217324]
[72]
Shen HJ, Zhu HY, Yang C, Ji F. SENP2 regulates hepatocellular carcinoma cell growth by modulating the stability of β-catenin. Asian Pac J Cancer Prev 2012; 13(8): 3583-7.
[http://dx.doi.org/10.7314/APJCP.2012.13.8.3583 ] [PMID: 23098437]
[73]
Jiang M, Chiu SY, Hsu W. SUMO-specific protease 2 in Mdm2-mediated regulation of p53. Cell Death Differ 2011; 18(6): 1005-15.
[http://dx.doi.org/10.1038/cdd.2010.168 ] [PMID: 21183956]
[74]
Sun Z, Hu S, Luo Q, Ye D, Hu D, Chen F. Overexpression of SENP3 in oral squamous cell carcinoma and its association with differentiation. Oncol Rep 2013; 29(5): 1701-6.
[http://dx.doi.org/10.3892/or.2013.2318 ] [PMID: 23467634]
[75]
Zhong JB, Liu ZR, Liu S, Zhao JQ. Inhibition of SENP5 by Cucurbitacin B Suppresses Cell Growth and Promotes Apoptosis in Osteosarcoma Cells. Trop J Pharm Res 2015; 14(9): 1573-9.
[http://dx.doi.org/10.4314/tjpr.v14i9.5]
[76]
Chen Y, Wen D, Huang Z, et al. 2-(4-Chlorophenyl)-2-oxoethyl 4-benzamidobenzoate derivatives, a novel class of SENP1 inhibitors: Virtual screening, synthesis and biological evaluation. Bioorg Med Chem Lett 2012; 22(22): 6867-70.
[http://dx.doi.org/10.1016/j.bmcl.2012.09.037 ] [PMID: 23044371]
[77]
Kumar A, Ito A, Takemoto M, Yoshida M, Zhang KYJ. Identification of 1,2,5-oxadiazoles as a new class of SENP2 inhibitors using structure based virtual screening. J Chem Inf Model 2014; 54(3): 870-80.
[http://dx.doi.org/10.1021/ci4007134 ] [PMID: 24512059]
[78]
Kumar A, Zhang KYJ. Computational Investigation of SENP:SUMO Protein-Protein Interaction for Structure Based Drug Design. Mol Inform 2013; 32(3): 267-80.
[http://dx.doi.org/10.1002/minf.201200124 ] [PMID: 27481522]
[79]
Wu J, Lei H, Zhang J, et al. Momordin Ic, a new natural SENP1 inhibitor, inhibits prostate cancer cell proliferation. Oncotarget 2016; 7(37): 58995-9005.
[http://dx.doi.org/10.18632/oncotarget.10636 ] [PMID: 27449295]
[80]
Pantoliano MW, Bone RF, Rhind AW, Salemme FR. Microplate Thermal Shift Assay Apparatus for Ligand Development and Multi-Variable Protein Chemistry Optimization Biomol screen. Google Patents 2000; 429-4.
[81]
Wang Z, Xie W, Zhu M, Zhou H. Development of a highly reliable assay for ubiquitin-specific protease 2 inhibitors. Bioorg Med Chem Lett 2017; 27(17): 4015-8.
[http://dx.doi.org/10.1016/j.bmcl.2017.07.059 ] [PMID: 28778469]
[82]
Vijayakumaran S, Wong MB, Antony H, Pountney DL. Direct and/or Indirect Roles for SUMO in Modulating Alpha-Synuclein Toxicity. Biomolecules 2015; 5(3): 1697-716.
[http://dx.doi.org/10.3390/biom5031697 ] [PMID: 26213981]
[83]
Madu IG, Namanja AT, Su Y, Wong S, Li YJ, Chen Y. Identification and characterization of a new chemotype of noncovalent SENP inhibitors. ACS Chem Biol 2013; 8(7): 1435-41.
[http://dx.doi.org/10.1021/cb400177q ] [PMID: 23614497]
[84]
Qiao Z, Wang W, Wang L, et al. Design, synthesis, and biological evaluation of benzodiazepine-based SUMO-specific protease 1 inhibitors. Bioorg Med Chem Lett 2011; 21(21): 6389-92.
[http://dx.doi.org/10.1016/j.bmcl.2011.08.101 ] [PMID: 21930380]
[85]
Zhao Y, Wang Z, Zhang J, Zhou H. Identification of SENP1 inhibitors through in silico screening and rational drug design. Eur J Med Chem 2016; 122: 178-84.
[http://dx.doi.org/10.1016/j.ejmech.2016.06.018 ] [PMID: 27344494]
[86]
Huang W, He T, Chai C, et al. Triptolide inhibits the proliferation of prostate cancer cells and down-regulates SUMO-specific protease 1 expression. PLoS One 2012; 7(5) e37693
[http://dx.doi.org/10.1371/journal.pone.0037693 ] [PMID: 22666381]
[87]
Uno M, Koma Y, Ban HS, Nakamura H. 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 2012; 22(16): 5169-73.
[http://dx.doi.org/10.1016/j.bmcl.2012.06.084 ] [PMID: 22801642]
[88]
Wen D, Xu Z, Xia L, et al. Important role of SUMOylation of Spliceosome factors in prostate cancer cells. J Proteome Res 2014; 13(8): 3571-82.
[http://dx.doi.org/10.1021/pr4012848 ] [PMID: 25027693]
[89]
Bernstock JD, Ye D, Smith JA, et al. Quantitative high-throughput screening identifies cytoprotective molecules that enhance SUMO conjugation via the inhibition of SUMO-specific protease (SENP)2. FASEB J 2018; 32(3): 1677-91.
[http://dx.doi.org/10.1096/fj.201700711R ] [PMID: 29146736]
[90]
Suzawa M, Miranda DA, Ramos KA, et al. A Gene-Expression Screen Identifies a Non-Toxic Sumoylation Inhibitor That Mimics SUMO-Less Human LRH-1 in Liver. eLife 2015.
[91]
Kim YS, Nagy K, Keyser S, Schneekloth JS Jr. An electrophoretic mobility shift assay identifies a mechanistically unique inhibitor of protein sumoylation. Chem Biol 2013; 20(4): 604-13.
[http://dx.doi.org/10.1016/j.chembiol.2013.04.001 ] [PMID: 23601649]
[92]
Zlotkowski K, Hewitt WM, Sinniah RS, et al. A Small-Molecule Microarray Approach for the Identification of E2 Enzyme Inhibitors in Ubiquitin-Like Conjugation Pathways. SLAS Discov 2017; 22(6): 760-6.
[http://dx.doi.org/10.1177/2472555216683937 ] [PMID: 28346086]
[93]
Huang H-J, Zhou L-L, Fu W-J, et al. β-catenin SUMOylation is involved in the dysregulated proliferation of myeloma cells. Am J Cancer Res 2014; 5(1): 309-20.
[PMID: 25628940]

Rights & Permissions Print Cite
Article Metrics
54
5
World Health Day
© 2024 Bentham Science Publishers | Privacy Policy