Overcome cancer drug resistance by targeting epigenetic modifications of centrosome

Zan-Hui Jia , Xing-Gang Wang , Hong Zhang

Cancer Drug Resistance ›› 2019, Vol. 2 ›› Issue (2) : 210 -224.

PDF
Cancer Drug Resistance ›› 2019, Vol. 2 ›› Issue (2) :210 -224. DOI: 10.20517/cdr.2018.010
Review
Review

Overcome cancer drug resistance by targeting epigenetic modifications of centrosome

Author information +
History +
PDF

Abstract

The centrosome is an organelle that serves as the microtubule- and actin-organizing center of human cells. Although the centrosome is small of size, it is great important on cellular function that regulates cytoskeletal organization and governs precise spindle orientation/positioning ensuring equal distribution of cellular components in cell division. Epigenetic modifications to centrosome proteins can lead to centrosome aberrations, such as disorganized spindles and centrosome amplification causing aneuploidy and genomic instability. Epigenetic disturbances are associated not only with carcinogenesis and cancer progression, but also with drug resistance to chemotherapy. In this review, we discuss mechanisms of epigenetic alteration during the centrosome biogenesis in cancer. We provide an update on the current status of clinical trials that aim to target epigenetic modifications in centrosome aberrations and to thwart drug resistance.

Keywords

Centrosome / genomic instability / epigenetic disturbance / carcinogenesis / cancer / clinical trials

Cite this article

Download citation ▾
Zan-Hui Jia, Xing-Gang Wang, Hong Zhang. Overcome cancer drug resistance by targeting epigenetic modifications of centrosome. Cancer Drug Resistance, 2019, 2(2): 210-224 DOI:10.20517/cdr.2018.010

登录浏览全文

4963

注册一个新账户 忘记密码

References

[1]

Hanahan D.Hallmarks of cancer: the next generation..Cell2011;144:646-74

[2]

Baylin SB.A decade of exploring the cancer epigenome-biological and translational implications..Nat Rev Cancer2011;11:726-34 PMCID:PMC3307543

[3]

Sandoval J.Cancer epigenomics: beyond genomics..Curr Opin Genet Dev2012;22:50-5

[4]

Salisbury JL.The contribution of epigenetic changes to abnormal centrosomes and genomic instability in breast cancer..J Mammary Gland Biol Neoplasia2001;6:203-12

[5]

Pihan GA,Wallace J,Woda B.Centrosome defects and genetic instability in malignant tumors..Cancer Res1998;58:3974-85

[6]

Denu RA,Kanugh C,Weaver BA.Centrosome amplification induces high grade features and is prognostic of worse outcomes in breast cancer..BMC Cancer2016;16:47 PMCID:PMC4734858

[7]

Lingle WL.Altered centrosome structure is associated with abnormal mitoses in human breast tumors..Am J Pathol1999;155:1941-51 PMCID:PMC1866918

[8]

Lingle WL,Ingle JN,Salisbury JL.Centrosome hypertrophy in human breast tumors: implications for genomic stability and cell polarity..Proc Natl Acad Sci U S A1998;95:2950-5 PMCID:PMC19675

[9]

Krämer A,Ho AD.Centrosome aberrations in hematological malignancies..Cell Biol Int2005;29:375-83

[10]

Giehl M,Frank O,Hafner M.Centrosome aberrations in chronic myeloid leukemia correlate with stage of disease and chromosomal instability..Leukemia2005;19:1192-7

[11]

Starita LM,Sankaran S,Griffin K.BRCA1-dependent ubiquitination of gamma-tubulin regulates centrosome number..Mol Cell Biol2004;24:8457-66 PMCID:PMC516733

[12]

Conduit PT,Raff JW.Centrosome function and assembly in animal cells..Nat Rev Mol Cell Biol2015;16:611-24

[13]

Jakobsen L,Skogs M,Lundberg E.Novel asymmetrically localizing components of human centrosomes identified by complementary proteomics methods..EMBO J2011;30:1520-35 PMCID:PMC3102290

[14]

Andersen JS,Mayor T,Nigg EA.Proteomic characterization of the human centrosome by protein correlation profiling..Nature2003;426:570-4

[15]

Loncarek J.Building the right centriole for each cell type..J Cell Biol2018;217:823-35 PMCID:PMC5839779

[16]

O’Connell KF,Kopish KR,Kemphues KJ.The C. elegans zyg-1 gene encodes a regulator of centrosome duplication with distinct maternal and paternal roles in the embryo..Cell2001;105:547-58

[17]

Habedanck R,Wilkinson CJ.The Polo kinase Plk4 functions in centriole duplication..Nat Cell Biol2005;7:1140-6

[18]

Arquint C.The PLK4-STIL-SAS-6 module at the core of centriole duplication..Biochem Soc Trans2016;44:1253-63 PMCID:PMC5095913

[19]

Pihan GA.Centrosome dysfunction contributes to chromosome instability, chromoanagenesis, and genome reprograming in cancer..Front Oncol2013;3:277 PMCID:PMC3824400

[20]

Yang J,Li T.Rootletin interacts with C-Nap1 and may function as a physical linker between the pair of centrioles/basal bodies in cells..Mol Biol Cell2006;17:1033-40 PMCID:PMC1356609

[21]

Mardin BR,Baxter JE,Scholz SR.Components of the Hippo pathway cooperate with Nek2 kinase to regulate centrosome disjunction..Nat Cell Biol2010;12:1166-76 PMCID:PMC3939356

[22]

Fry AM,Nigg EA.A centrosomal function for the human Nek2 protein kinase, a member of the NIMA family of cell cycle regulators..EMBO J1998;17:470-81 PMCID:PMC1170398

[23]

Centrosome. Available from: https://www.proteinatlas.org/humanproteome/cell/centrosome. [Last accessed on 22 Apr 2019]

[24]

Boveri T. 1900. Ueber die Natur der Centrosomen. Zellen-Studien 4. Jena, Germany G. Fischer

[25]

Farina F,Guérin C,Sillibourne J.The centrosome is an actin-organizing centre..Nat Cell Biol2016;18:65-75 PMCID:PMC4880044

[26]

Nam HJ,van Deursen JM.Centrosome dynamics as a source of chromosomal instability..Trends Cell Biol2015;25:65-73 PMCID:PMC4312731

[27]

Pihan GA,Zhou Y.Centrosome abnormalities and chromosome instability occur together in pre-invasive carcinomas..Cancer Res2003;63:1398-1404

[28]

Chan JY.A clinical overview of centrosome amplification in human cancers..Int J Biol Sci2011;7:1122-44 PMCID:PMC3204404

[29]

Kwon M,Chandhok NS,Azioune A.Mechanisms to suppress multipolar divisions in cancer cells with extra centrosomes..Genes Dev2008;22:2189-203 PMCID:PMC2518815

[30]

Neben K,Schweizer S,Krämer A.Centrosome aberrations in acute myeloid leukemia are correlated with cytogenetic risk profile..Blood2003;101:289-91

[31]

Mahathre MM,Aneja R.The more the messier: centrosome amplification as a novel biomarker for personalized treatment of colorectal cancers..J Biomed Res2015;30:441-51 PMCID:PMC5138576

[32]

Kais Z.Regulation of centrosomes by the BRCA1-dependent ubiquitin ligase..Cancer Biol Ther2008;7:1540-3 PMCID:PMC2628548

[33]

Fukasawa K,Kuriyama R,Vande Woude GF.Abnormal centrosome amplification in the absence of p53..Science1996;271:1744-7

[34]

Li X,Liu L,Ding X.USP9X regulates centrosome duplication and promotes breast carcinogenesis..Nat Commun2017;8:14866 PMCID:PMC5380967

[35]

Xie S,Liu S,Wang J.Cep70 overexpression stimulates pancreatic cancer by inducing centrosome abnormality and microtubule disorganization..Sci Rep2016;6:21263 PMCID:PMC4759539

[36]

Denu RA,Kanugh C,Weaver BA.Centrosome amplification induces high grade features and is prognostic of worse outcomes in breast cancer..BMC Cancer2016;16:47 PMCID:PMC4734858

[37]

Miyachika Y,Matsumoto H,Kawai Y.Centrosome amplification in bladder washing cytology specimens is a useful prognostic biomarker for non-muscle invasive bladder cancer..Cancer Genet2013;206:12-8

[38]

Zeng YR,Wang C,Huang YQ.Overexpression of NIMA-related kinase 2 is associated with progression and poor prognosis of prostate cancer..BMC Urol2015;15:90 PMCID:PMC4553013

[39]

Ogden A,Aneja R.Prognostic value of CA20, a score based on centrosome amplification-associated genes, in breast tumors..Sci Rep2017;7:262 PMCID:PMC5428291

[40]

Huang J,Hou S.Aberrant NEK2 expression might be an independent predictor for poor recurrence-free survival and overall survival of skin cutaneous melanoma..Eur Rev Med Pharmacol Sci2018;22:3694-3702

[41]

Yun M,Lin ZR,Zhang JX.High expression of transforming acidic coiled coil-containing protein 3 strongly correlates with aggressive characteristics and poor prognosis of gastric cancer..Oncol Rep2015;34:1397-1405

[42]

Karkera JD,Bell K,Portale JC.Oncogenic characterization and pharmacologic sensitivity of activating fibroblast growth factor receptor (FGFR) genetic alterations to the selective FGFR inhibitor erdafitinib..Mol Cancer Ther2017;16:1717-26

[43]

Lauffart B,Eddy R,DiCioccio RA.Aberrations of TACC1 and TACC3 are associated with ovarian cancer..BMC Women’s Health2005;5:8 PMCID:PMC1175095

[44]

Fan G,Shan P,Huan J.Loss of KLF14 triggers centrosome amplification and tumorigenesis..Nat Commun2015;6:8450 PMCID:PMC4600754

[45]

Hodis E,Kryukov GV,Imielinski M.A landscape of driver mutations in melanoma..Cell2012;150:251-63 PMCID:PMC3600117

[46]

Tamotsu K,Uchikado Y,Sasaki K.Correlation of Aurora-A expression with the effect of chemoradiation therapy on esophageal squamous cell carcinoma..BMC Cancer2015;15:323 PMCID:PMC4423148

[47]

Rakha EA,Paish CE.Expression of the transcription factor CTCF in invasive breast cancer: a candidate gene located at 16q22.1..Br J Cancer2004;91:1591-6 PMCID:PMC2409935

[48]

Lee J.Nek2-targeted ASO or siRNA pretreatment enhances anticancer drug sensitivity in triplenegative breast cancer cells..Int J Oncol2013;42:839-47 PMCID:PMC3597451

[49]

Zhou W,Xia J,Salama ME.NEK2 induces drug resistance mainly through activation of efflux drug pumps and is associated with poor prognosis in myeloma and other cancers..Cancer Cell2013;23:48-62 PMCID:PMC3954609

[50]

Liu X,Lu Y,Li L.Upregulation of NEK2 is associated with drug resistance in ovarian cancer..Oncol Rep2014;31:745-54

[51]

Wu SM,Lee KY,Feng PH.Hepatoma cell functions modulated by NEK2 are associated with liver cancer progression..Int J Cancer2017;140:1581-96

[52]

Zhao W,Xu B.Overexpression of centrosomal protein Nlp confers breast carcinoma resistance to paclitaxel..Cancer Biol Ther.2012;13:156-63

[53]

Kleylein-Sohn J,Ohmer M,Nigg EA.Acentrosomal spindle organization renders cancer cells dependent on the kinesin HSET..J Cell Sci2012;125:5391-402

[54]

Kwon M,Danuser G.Direct microtubule-binding by myosin-10 orients centrosomes toward retraction fibers and subcortical actin clouds..Dev Cell2015;34:323-37 PMCID:PMC4672950

[55]

De S,Jackson MW.Overexpression of kinesins mediates docetaxel resistance in breast cancer cells..Cancer Res2009;69:8035-42

[56]

Li JJ,Lingle WL,Salisbury JL.Estrogen mediates Aurora-A overexpression, centrosome amplification, chromosomal instability, and breast cancer in female ACI rats..Proc Natl Acad Sci USA2004;101:18123-8 PMCID:PMC539804

[57]

Marina M.Nek2 and Plk4: prognostic markers, drivers of breast tumorigenesis and drug resistance..Front Biosci (Landmark Ed)2014;19:352-65 PMCID:PMC3999971

[58]

Jusino S,Saavedra HI.Centrosome aberrations and chromosome instability contribute to tumorigenesis and intra-tumor heterogeneity..J Cancer Metastasis Treat2018;4:pii:43 PMCID:PMC6205736

[59]

Lomonosova E.BH3-only proteins in apoptosis and beyond: an overview..Oncogene2008;27:S2-19 PMCID:PMC2928556

[60]

Zhou W,Xia J,Salama ME.NEK2 induces drug resistance mainly through activation of efflux drug pumps and is associated with poor prognosis in myeloma and other cancers..Cancer Cell2013;23:48-62 PMCID:PMC3954609

[61]

Moustafa-Kamal M,Lu Y,Teodoro JG.BimEL is phosphorylated at mitosis by Aurora A and targeted for degradation by βTrCP1..Cell Death Differ2013;20:1393-1403 PMCID:PMC3770328

[62]

Kalimutho M,Jeffery J,Srihari S.CEP55 is a determinant of cell fate during perturbed mitosis in breast cancer..EMBO Mol Med2018;10:e8566 PMCID:PMC6127888

[63]

Hayward DG,Faragher AJ,Hagan IM.The centrosomal kinase Nek2 displays elevated levels of protein expression in human breast cancer..Cancer Res2004;64:7370-6

[64]

Yoo BH,Park CH,Bae CD.CKAP2 phosphorylation by CDK1/cyclin B1 is crucial for maintaining centrosome integrity..Exp Mol Med2017;49:e354 PMCID:PMC5565958

[65]

Boutros R.Asymmetric localization of the CDC25B phosphatase to the mother centrosome during interphase..Cell Cycle2008;7:401-6

[66]

Cazales M,Montembault E,Prigent C.CDC25B phosphorylation by Aurora-A occurs at the G2/M transition and is inhibited by DNA damage..Cell Cycle2005;4:1233-8

[67]

Bouché JP,Dozier C,Lemaire M.NanoLC-MS/MS analysis provides new insights into the phosphorylation pattern of Cdc25B in vivo: full overlap with sites of phosphorylation by Chk1 and Cdk1/cycB kinases in vitro..J Proteome Res2008;7:1264-73

[68]

Dutertre S,Quaranta M,Trabut V.Phosphorylation of cdc25b by aurora-a at the centrosome contributes to the g2-m transition..J Cell Sci2004;117:2523-31

[69]

Boutros R,Ducommun B.CDC25B involvement in the centrosome duplication cycle and in microtubule nucleation..Cancer Res2007;67:11557-64

[70]

Wang J,Viccaro K,Jacobsen M.The Aurora-A-Twist1 axis promotes highly aggressive phenotypes in pancreatic carcinoma..J Cell Sci2017;130:1078-93 PMCID:PMC5358340

[71]

Joukov V,Rodriguez A,Livingston DM.Centrosomal protein of 192 kDa (Cep192) promotes centrosome-driven spindle assembly by engaging in organelle-specific Aurora A activation..Proc Natl Acad Sci USA2010;107:21022-7 PMCID:PMC3000277

[72]

Scutt PJ,Sloane DA,Bignell CR.Discovery and exploitation of inhibitor-resistant aurora and polo kinase mutants for the analysis of mitotic networks..J Biol Chem2009;284:15880-93 PMCID:PMC2708884

[73]

Zorba A,Kutter S,Pontiggia F.Molecular mechanism of Aurora A kinase autophosphorylation and its allosteric activation by TPX2..ELife2014;3:e02667 PMCID:PMC4032492

[74]

Nakamura T,Takekawa M.SAPK pathways and p53 cooperatively regulate PLK4 activity and centrosome integrity under stress..Nat Commun2013;4:1775

[75]

Rauch N,Kolch W.MAPK kinase signaling dynamics regulate cell fate decisions and drug resistance..Current Opin Struct Biol2016;41:151-8

[76]

Cunha-Ferreira I,Pimenta-Marques A,Lince-Faria M.Regulation of autophosphorylation controls PLK4 self-destruction and centriole number..Current Biology2013;23:2245-54

[77]

Guderian G,Uldschmid A.Plk4 trans-autophosphorylation regulates centriole number by controlling betaTrCP-mediated degradation..J Cell Sci2010;123:2163-9

[78]

Slevin LK,Pinkerton DC,Rogers GC.The structure of the plk4 cryptic polo box reveals two tandem polo boxes required for centriole duplication..Structure2012;20:1905-17 PMCID:PMC3496063

[79]

Fournier M,Grauffel C,Garnier JM.KAT2A/KAT2B-targeted acetylome reveals a role for PLK4 acetylation in preventing centrosome amplification..Nat Commun2016;7:13227 PMCID:PMC5095585

[80]

Ling H,Seto E.Suppression of centrosome duplication and amplification by deacetylases..Cell Cycle2012;11:3779-91 PMCID:PMC3495821

[81]

Tachibana M,Fukushima T.Set domain-containing protein, G9a, is a novel lysine-preferring mammalian histone methyltransferase with hyperactivity and specific selectivity to lysines 9 and 27 of histone H3..J Biol Chem2001;276:25309-17

[82]

Kondo Y,Ahmed S,Sekido Y.Downregulation of histone H3 lysine 9 methyltransferase G9a induces centrosome disruption and chromosome instability in cancer cells..PLoS ONE2008;3:e2037 PMCID:PMC2323574

[83]

Romanov SR,Holst CR,Haupt LM.Normal human mammary epithelial cells spontaneously escape senescence and acquire genomic changes..Nature2001;409:633

[84]

McConnell BB,Stott FJ,Peters G.Induced expression of p16INK4a inhibits both CDK4- and CDK2-associated kinase activity by reassortment of cyclin-CDK-inhibitor complexes..Mol Cell Biol1999;19:1981-9 PMCID:PMC83991

[85]

Lacey KR,Stearns T.Cyclin-dependent kinase control of centrosome duplication..Proc Natl Acad Sci U S A1999;96:2817-22 PMCID:PMC15852

[86]

Matsumoto Y,Nishida E.Cyclin-dependent kinase 2 (Cdk2) is required for centrosome duplication in mammalian cells..Curr Biol1999;9:429-32

[87]

Foster SA,Barrett MT.Inactivation of p16 in human mammary epithelial cells by CpG island methylation..Mol Cell Biol1998;18:1793-1801 PMCID:PMC121409

[88]

Holst CR,Esteller M,Baylin SB.Methylation of p16(INK4a) promoters occurs in vivo in histologically normal human mammary epithelia..Cancer Res2003;63:1596-601

[89]

McDermott KM,Holst CR,Singla V.p16(INK4a) prevents centrosome dysfunction and genomic instability in primary cells..PLoS Biol2006;4:e51 PMCID:PMC1361797

[90]

Berman H,Crawford YG,Fordyce CA.Genetic and epigenetic changes in mammary epithelial cells identify a subpopulation of cells involved in early carcinogenesis..Cold Spring Harb Symp Quant Biol2005;70:317-27

[91]

Pietromonaco SF,Aitken A.Association of 14-3-3 proteins with centrosomes..Blood Cells Mol Dis1996;22:225-37

[92]

Mukhopadhyay A,Bose A,Senapati P.14-3-3γ prevents centrosome amplification and neoplastic progression..Sci Rep2016;6:26580 PMCID:PMC4890593

[93]

Suzuki H,Toyota M,Kakiuchi H.Inactivation of the 14-3-3 sigma gene is associated with 5’ CpG island hypermethylation in human cancers..Cancer Res2000;60:4353-7

[94]

Iwata N,Sasaki S,Suzuki H.Frequent hypermethylation of CpG islands and loss of expression of the 14-3-3 sigma gene in human hepatocellular..Oncogene2000;19:5298-302

[95]

Chanda S,Guhamazumder D,Chaudhuri U.DNA hypermethylation of promoter of gene p53 and p16 in arsenic-exposed people with and without malignancy..Toxicol Sci2006;89:431-7

[96]

Jha AK,Jain V,Capalash N.Promoter hypermethylation of p73 and p53 genes in cervical cancer patients among north Indian population..Mol Biol Rep2012;39:9145-57

[97]

Adrian Jarzynski,Malgorzata Polz-Dacewicz.Analysis of mutation and promoter methylation of TP53 gene in tumors of the head and neck..Current Issues in Pharmacy and Medical Sciences2016;29:53-6

[98]

Liu JL,Lu XL,Guo X.NF-κB induces abnormal centrosome amplification by upregulation of CDK2 in laryngeal squamous cell cancer..Int J Oncol2011;39:915-24

[99]

Yu F,Strätling WH.Histone deacetylase-independent transcriptional repression by methyl-CpG-binding protein 2..Nucleic Acids Res2000;28:2201-6 PMCID:PMC105362

[100]

Lee MY,Saavedra HI.E2F activators signal and maintain centrosome amplification in breast cancer cells..Mol Cell Biol2014;34:2581-99 PMCID:PMC4097658

[101]

Liao WT,Lee CH,Chang JG.An interaction between arsenic-induced epigenetic modification and inflammatory promotion in a skin equivalent during arsenic carcinogenesis..J Invest Dermatol2017;137:187-96

[102]

Chen WJ,Tsai TY,Lee YW.DDX3 localizes to the centrosome and prevents multipolar mitosis by epigenetically and translationally modulating p53 expression..Sci Rep2017;7:9411 PMCID:PMC5573351

[103]

Pouysségur J,Mazure NM.Hypoxia signalling in cancer and approaches to enforce tumour regression..Nature2006;441:437-43

[104]

Mittal K,Ogden A,Melton BD.Amplified centrosomes and mitotic index display poor concordance between patient tumors and cultured cancer cells..Sci Rep2017;7:43984 PMCID:PMC5341055

[105]

Bijnsdorp IV,Lagerweij T,Krijgsman O.miR-129-3p controls centrosome number in metastatic prostate cancer cells by repressing CP110..Oncotarget2016;7:16676-87 PMCID:PMC4941343

[106]

Wang ZD,Chang C,Chen ZM.Long noncoding RNA lnc-RI is a new regulator of mitosis via targeting miRNA-210-3p to release PLK1 mRNA activity..Sci Rep2016;6:25385 PMCID:PMC4861912

[107]

Takahashi Y,Sawada G,Matsumura T.Up-regulation of NEK2 by microRNA-128 methylation is associated with poor prognosis in colorectal cancer..Ann Surg Oncol2014;21:205-12

[108]

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

[109]

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

[110]

Leach FS,Meltzer P,Oliner JD.p53 Mutation and MDM2 amplification in human soft tissue sarcomas..Cancer Res1993;53:2231-4

[111]

Akio Suzuki,Yutaka Yamamoto,Mariko Muta.Role of MDM2 overexpression in doxorubicin resistance of breast carcinoma,.Jpn J Cancer Res1998;89:221-7 PMCID:PMC5921757

[112]

Keshelava N,Chen P,Luna MC.Loss of p53 function confers high-level multidrug resistance in neuroblastoma cell lines..Cancer Res2001;61:6185-93

[113]

Čajánek L,Nigg EA.The E3 ubiquitin ligase Mib1 regulates Plk4 and centriole biogenesis..J Cell Sci2015;128:1674-82

[114]

Shen X,D‘Alonzo D,Bruder E.HECTD1 controls the protein level of IQGAP1 to regulate the dynamics of adhesive structures..Cell Commun Signal2017;15:2 PMCID:PMC5225595

[115]

Wang XG,Jia ZH,Zhang H.HECTD1 regulates expression of SNAIL: implications for epithelial-mesenchymal transition (EMT)..Forthcoming2019;

[116]

Drilon A,Kummar S,Lassen UN.Efficacy of larotrectinib in TRK fusion-positive cancers in adults and children..N Engl J Med2018;378:731-9 PMCID:PMC5857389

[117]

Sampson PB,Patel NK,Forrest B.The discovery of polo-like kinase 4 inhibitors: design and optimization of spiro[cyclopropane-1,3ʹ[3H]indol]-2ʹ(1ʹH)-ones as orally bioavailable antitumor agents..J Med Chem2015;58:130-46

[118]

Mason JM,Wei X,Yao Y.Functional characterization of CFI-400945, a Polo-like kinase 4 inhibitor, as a potential anticancer agent..Cancer Cell2014;26:163-76

[119]

Liu X.The MPS1 family of protein kinases..Annu Rev Biochem2012;81:561-85 PMCID:PMC4026297

[120]

Janssen A,Medema RH.Elevating the frequency of chromosome mis-segregation as a strategy to kill tumor cells..Proc Natl Acad Sci U S A2009;106:19108-13 PMCID:PMC2776415

[121]

Jeong SB,Yoon JH,Lim SC.Essential role of polo-like kinase 1 (Plk1) oncogene in tumor growth and metastasis of tamoxifen-resistant breast cancer..Mol Cancer Ther2018;17:825-37

[122]

Dominguez-Brauer C,Mason JM,Bray MR.Targeting mitosis in cancer: emerging strategies..Mol Cell2015;60:524-36

[123]

Yim H.Current clinical trials with polo-like kinase 1 inhibitors in solid tumors..Anticancer Drugs2013;24:999-1006

[124]

Gjertsen BT.Discovery and development of the Polo-like kinase inhibitor volasertib in cancer therapy..Leukemia2015;29:11-9 PMCID:PMC4335352

[125]

Vijayaraghavan S,Keyomarsi K.Inhibiting CDK in cancer therapy: current evidence and future directions..Target Oncol2018;13:21-38

[126]

Malumbres M.Cell cycle, CDKs and cancer: a changing paradigm..Nat Rev Cancer2009;9:153-66

[127]

Cicenas J,Sorokinas A,Valiunas D.Highlights of the latest advances in research on CDK inhibitors..Cancers (Basel)2014;6:2224-42 PMCID:PMC4276963

[128]

Carlson BA,Sausville EA,Worland PJ.Flavopiridol induces G1 arrest with inhibition of cyclin-dependent kinase (CDK) 2 and CDK4 in human breast carcinoma cells..Cancer Res1996;56:2973-8

[129]

Zeidner JF.Clinical activity of alvocidib (flavopiridol) in acute myeloid leukemia..Leuk Res2015;39:1312-8

[130]

Blachly JS,Grever M.Cyclin-dependent kinase inhibitors for the treatment of chronic lymphocytic leukemia..Semin Oncol2016;43:265-73

[131]

Kollareddy M,Dzubak P,Lepsik M.Aurora kinase inhibitors: progress towards the clinic..Invest New Drugs2012;30:2411-32 PMCID:PMC3484309

[132]

Goldberg SL,Craig MD,Lister J.An exploratory phase 2 study of investigational Aurora A kinase inhibitor alisertib (MLN8237) in acute myelogenous leukemia and myelodysplastic syndromes..Leuk Res Rep2014;3:58-61 PMCID:PMC4110881

AI Summary AI Mindmap
PDF

71

Accesses

0

Citation

Detail

Sections
Recommended

AI思维导图

/