A CDC20-APC/SOX2 Signaling Axis Regulates Human Glioblastoma Stem-like Cells

Cell Reports

Volumn 11, Issue 11, 2015, Pages 1809-1821

  Mao, Diane D ^a   Gujar, Amit D ^a   Mahlokozera, Tatenda ^a   Chen, Ishita ^a   Pan, Yanchun ^a   Luo, Jingqin ^a   Brost, Taylor ^a   Thompson, Elizabeth A ^a   Turski, Alice ^a   Leuthardt, Eric C ^a   Dunn, Gavin P ^a,b   Chicoine, Michael R ^a,b   Rich, Keith M ^a,b   Dowling, Joshua L ^a,b   Zipfel, Gregory J ^a,b   Dacey, Ralph G ^a,b   Achilefu, Samuel ^c   Tran, David D ^a,b   Yano, Hiroko ^a,b   Kim, Albert H ^a,b  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b Washington University in St Louis School of Medicine   (United States)

^c WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANAPHASE PROMOTING COMPLEX; CELL CYCLE PROTEIN 20; TRANSCRIPTION FACTOR SOX2; CDC20 PROTEIN, HUMAN; TRANSCRIPTION FACTOR SOX; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CANCER PROGNOSIS; CANCER STEM CELL; CARCINOGENESIS; CELL INVASION; CELL RENEWAL; CONTROLLED STUDY; FEMALE; GLIOBLASTOMA; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; MALE; MOUSE; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; SIGNAL TRANSDUCTION; TUMOR XENOGRAFT; ANIMAL; BRAIN TUMOR; CELL CULTURE; GENETICS; METABOLISM; NERVE CELL; PATHOLOGY;

ANAPHASE-PROMOTING COMPLEX-CYCLOSOME; ANIMALS; BIOMARKERS, TUMOR; BRAIN NEOPLASMS; CDC20 PROTEINS; CELLS, CULTURED; GLIOBLASTOMA; HUMANS; MICE; NEOPLASTIC STEM CELLS; NEURONS; SIGNAL TRANSDUCTION; SOXB1 TRANSCRIPTION FACTORS;

EID: 84937633710     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2015.05.027     Document Type: Article

References (44)

1. Alonso M.M., Diez-Valle R., Manterola L., Rubio A., Liu D., Cortes-Santiago N., Urquiza L., Jauregi P., Lopez de Munain A., Sampron N., et al. Genetic and epigenetic modifications of Sox2 contribute to the invasive phenotype of malignant gliomas. PLoS ONE 2011, 6:e26740.
2. Baltus G.A., Kowalski M.P., Zhai H., Tutter A.V., Quinn D., Wall D., Kadam S. Acetylation of sox2 induces its nuclear export in embryonic stem cells. Stem Cells 2009, 27:2175-2184.
3. Bao S., Wu Q., McLendon R.E., Hao Y., Shi Q., Hjelmeland A.B., Dewhirst M.W., Bigner D.D., Rich J.N. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 2006, 444:756-760.
4. Berezovsky A.D., Poisson L.M., Cherba D., Webb C.P., Transou A.D., Lemke N.W., Hong X., Hasselbach L.A., Irtenkauf S.M., Mikkelsen T., deCarvalho A.C. Sox2 promotes malignancy in glioblastoma by regulating plasticity and astrocytic differentiation. Neoplasia 2014, 16:193-206.e19-e25.
5. Bhat K.P., Balasubramaniyan V., Vaillant B., Ezhilarasan R., Hummelink K., Hollingsworth F., Wani K., Heathcock L., James J.D., Goodman L.D., et al. Mesenchymal differentiation mediated by NF-κB promotes radiation resistance in glioblastoma. Cancer Cell 2013, 24:331-346.
6. Bie L., Zhao G., Cheng P., Rondeau G., Porwollik S., Ju Y., Xia X.Q., McClelland M. The accuracy of survival time prediction for patients with glioma is improved by measuring mitotic spindle checkpoint gene expression. PLoS ONE 2011, 6:e25631.
7. Chen J., Li Y., Yu T.S., McKay R.M., Burns D.K., Kernie S.G., Parada L.F. A restricted cell population propagates glioblastoma growth after chemotherapy. Nature 2012, 488:522-526.
8. Cheng L., Wu Q., Guryanova O.A., Huang Z., Huang Q., Rich J.N., Bao S. Elevated invasive potential of glioblastoma stem cells. Biochem. Biophys. Res. Commun. 2011, 406:643-648.
9. Fang L., Zhang L., Wei W., Jin X., Wang P., Tong Y., Li J., Du J.X., Wong J. A methylation-phosphorylation switch determines Sox2 stability and function in ESC maintenance or differentiation. Mol. Cell 2014, 55:537-551.
10. Forghanifard M.M., Ardalan Khales S., Javdani-Mallak A., Rad A., Farshchian M., Abbaszadegan M.R. Stemness state regulators SALL4 and SOX2 are involved in progression and invasiveness of esophageal squamous cell carcinoma. Med. Oncol. 2014, 31:922.
11. Fukushima H., Ogura K., Wan L., Lu Y., Li V., Gao D., Liu P., Lau A.W., Wu T., Kirschner M.W., et al. SCF-mediated Cdh1 degradation defines a negative feedback system that coordinates cell-cycle progression. Cell Rep. 2013, 4:803-816.
12. Gangemi R.M., Griffero F., Marubbi D., Perera M., Capra M.C., Malatesta P., Ravetti G.L., Zona G.L., Daga A., Corte G. SOX2 silencing in glioblastoma tumor-initiating cells causes stop of proliferation and loss of tumorigenicity. Stem Cells 2009, 27:40-48.
13. Girouard S.D., Laga A.C., Mihm M.C., Scolyer R.A., Thompson J.F., Zhan Q., Widlund H.R., Lee C.W., Murphy G.F. SOX2 contributes to melanoma cell invasion. Lab. Invest. 2012, 92:362-370.
14. Han X., Fang X., Lou X., Hua D., Ding W., Foltz G., Hood L., Yuan Y., Lin B. Silencing SOX2 induced mesenchymal-epithelial transition and its expression predicts liver and lymph node metastasis of CRC patients. PLoS ONE 2012, 7:e41335.
15. Hartmann C., Hentschel B., Wick W., Capper D., Felsberg J., Simon M., Westphal M., Schackert G., Meyermann R., Pietsch T., et al. Patients with IDH1 wild type anaplastic astrocytomas exhibit worse prognosis than IDH1-mutated glioblastomas, and IDH1 mutation status accounts for the unfavorable prognostic effect of higher age: implications for classification of gliomas. Acta Neuropathol. 2010, 120:707-718.
16. He S., Nakada D., Morrison S.J. Mechanisms of stem cell self-renewal. Annu. Rev. Cell Dev. Biol. 2009, 25:377-406.
17. Hu Y., Smyth G.K. ELDA: extreme limiting dilution analysis for comparing depleted and enriched populations in stem cell and other assays. J. Immunol. Methods 2009, 347:70-78.
18. Jeong C.H., Cho Y.Y., Kim M.O., Kim S.H., Cho E.J., Lee S.Y., Jeon Y.J., Lee K.Y., Yao K., Keum Y.S., et al. Phosphorylation of Sox2 cooperates in reprogramming to pluripotent stem cells. Stem Cells 2010, 28:2141-2150.
19. Kallio M., Weinstein J., Daum J.R., Burke D.J., Gorbsky G.J. Mammalian p55CDC mediates association of the spindle checkpoint protein Mad2 with the cyclosome/anaphase-promoting complex, and is involved in regulating anaphase onset and late mitotic events. J. Cell Biol. 1998, 141:1393-1406.
20. Kim A.H., Puram S.V., Bilimoria P.M., Ikeuchi Y., Keough S., Wong M., Rowitch D., Bonni A. A centrosomal Cdc20-APC pathway controls dendrite morphogenesis in postmitotic neurons. Cell 2009, 136:322-336.
21. Lee J., Kotliarova S., Kotliarov Y., Li A., Su Q., Donin N.M., Pastorino S., Purow B.W., Christopher N., Zhang W., et al. Tumor stem cells derived from glioblastomas cultured in bFGF and EGF more closely mirror the phenotype and genotype of primary tumors than do serum-cultured cell lines. Cancer Cell 2006, 9:391-403.
22. Lewitzky M., Yamanaka S. Reprogramming somatic cells towards pluripotency by defined factors. Curr. Opin. Biotechnol. 2007, 18:467-473.
23. Lou X., Han X., Jin C., Tian W., Yu W., Ding D., Cheng L., Huang B., Jiang H., Lin B. SOX2 targets fibronectin 1 to promote cell migration and invasion in ovarian cancer: new molecular leads for therapeutic intervention. OMICS 2013, 17:510-518.
24. Manchado E., Guillamot M., de Cárcer G., Eguren M., Trickey M., García-Higuera I., Moreno S., Yamano H., Cañamero M., Malumbres M. Targeting mitotic exit leads to tumor regression in vivo: Modulation by Cdk1, Mastl, and the PP2A/B55α,δ phosphatase. Cancer Cell 2010, 18:641-654.
25. Marucci G., Morandi L., Magrini E., Farnedi A., Franceschi E., Miglio R., Calò D., Pession A., Foschini M.P., Eusebi V. Gene expression profiling in glioblastoma and immunohistochemical evaluation of IGFBP-2 and CDC20. Virchows Arch. 2008, 453:599-609.
26. Parsons D.W., Jones S., Zhang X., Lin J.C., Leary R.J., Angenendt P., Mankoo P., Carter H., Siu I.M., Gallia G.L., et al. An integrated genomic analysis of human glioblastoma multiforme. Science 2008, 321:1807-1812.
27. Peters J.M. The anaphase promoting complex/cyclosome: a machine designed to destroy. Nat. Rev. Mol. Cell Biol. 2006, 7:644-656.
28. Pevny L.H., Nicolis S.K. Sox2 roles in neural stem cells. Int. J. Biochem. Cell Biol. 2010, 42:421-424.
29. Pollard S.M., Yoshikawa K., Clarke I.D., Danovi D., Stricker S., Russell R., Bayani J., Head R., Lee M., Bernstein M., et al. Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 2009, 4:568-580.
30. Puram S.V., Kim A.H., Ikeuchi Y., Wilson-Grady J.T., Merdes A., Gygi S.P., Bonni A. A CaMKIIβ signaling pathway at the centrosome regulates dendrite patterning in the brain. Nat. Neurosci. 2011, 14:973-983.
31. Sikorska M., Sandhu J.K., Deb-Rinker P., Jezierski A., Leblanc J., Charlebois C., Ribecco-Lutkiewicz M., Bani-Yaghoub M., Walker P.R. Epigenetic modifications of SOX2 enhancers, SRR1 and SRR2, correlate with in vitro neural differentiation. J. Neurosci. Res. 2008, 86:1680-1693.
32. Singh S.K., Hawkins C., Clarke I.D., Squire J.A., Bayani J., Hide T., Henkelman R.M., Cusimano M.D., Dirks P.B. Identification of human brain tumour initiating cells. Nature 2004, 432:396-401.
33. Suvà M.L., Rheinbay E., Gillespie S.M., Patel A.P., Wakimoto H., Rabkin S.D., Riggi N., Chi A.S., Cahill D.P., Nahed B.V., et al. Reconstructing and reprogramming the tumor-propagating potential of glioblastoma stem-like cells. Cell 2014, 157:580-594.
34. Turnell A.S., Stewart G.S., Grand R.J., Rookes S.M., Martin A., Yamano H., Elledge S.J., Gallimore P.H. The APC/C and CBP/p300 cooperate to regulate transcription and cell-cycle progression. Nature 2005, 438:690-695.
35. Valster A., Tran N.L., Nakada M., Berens M.E., Chan A.Y., Symons M. Cell migration and invasion assays. Methods 2005, 37:208-215.
36. Verhaak R.G., Hoadley K.A., Purdom E., Wang V., Qi Y., Wilkerson M.D., Miller C.R., Ding L., Golub T., Mesirov J.P., et al. Integrated genomic analysis identifies clinically relevant subtypes of glioblastoma characterized by abnormalities in PDGFRA, IDH1, EGFR, and NF1. Cancer Cell 2010, 17:98-110. Cancer Genome Atlas Research Network.
37. Wan L., Tan M., Yang J., Inuzuka H., Dai X., Wu T., Liu J., Shaik S., Chen G., Deng J., et al. APC(Cdc20) suppresses apoptosis through targeting Bim for ubiquitination and destruction. Dev. Cell 2014, 29:377-391.
38. Wang L., Zhang J., Wan L., Zhou X., Wang Z., Wei W. Targeting Cdc20 as a novel cancer therapeutic strategy. Pharmacol. Ther. 2015.
39. Wen P.Y., Kesari S. Malignant gliomas in adults. N. Engl. J. Med. 2008, 359:492-507.
40. Wolthuis R., Clay-Farrace L., van Zon W., Yekezare M., Koop L., Ogink J., Medema R., Pines J. Cdc20 and Cks direct the spindle checkpoint-independent destruction of cyclin A. Mol. Cell 2008, 30:290-302.
41. Xia Y., Wu Y., Liu B., Wang P., Chen Y. Downregulation of miR-638 promotes invasion and proliferation by regulating SOX2 and induces EMT in NSCLC. FEBS Lett. 2014, 588:2238-2245.
42. Yan H., Parsons D.W., Jin G., McLendon R., Rasheed B.A., Yuan W., Kos I., Batinic-Haberle I., Jones S., Riggins G.J., et al. IDH1 and IDH2 mutations in gliomas. N. Engl. J. Med. 2009, 360:765-773.
43. Yang Y., Kim A.H., Yamada T., Wu B., Bilimoria P.M., Ikeuchi Y., de la Iglesia N., Shen J., Bonni A. A Cdc20-APC ubiquitin signaling pathway regulates presynaptic differentiation. Science 2009, 326:575-578.
44. Zeng X., Sigoillot F., Gaur S., Choi S., Pfaff K.L., Oh D.C., Hathaway N., Dimova N., Cuny G.D., King R.W. Pharmacologic inhibition of the anaphase-promoting complex induces a spindle checkpoint-dependent mitotic arrest in the absence of spindle damage. Cancer Cell 2010, 18:382-395.