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Dose‐dependent proteomic analysis of glioblastoma cancer stem cells upon treatment with γ‐secretase inhibitor

dc.contributor.authorDai, Lanen_US
dc.contributor.authorHe, Jintangen_US
dc.contributor.authorLiu, Yashuen_US
dc.contributor.authorByun, Jaemanen_US
dc.contributor.authorVivekanandan, Anuradhaen_US
dc.contributor.authorPennathur, Subramaniamen_US
dc.contributor.authorFan, Xingen_US
dc.contributor.authorLubman, David M.en_US
dc.date.accessioned2011-12-05T18:33:24Z
dc.date.available2013-02-01T20:26:17Zen_US
dc.date.issued2011-12en_US
dc.identifier.citationDai, Lan; He, Jintang; Liu, Yashu; Byun, Jaeman; Vivekanandan, Anuradha; Pennathur, Subramaniam; Fan, Xing; Lubman, David M. (2011). "Dose‐dependent proteomic analysis of glioblastoma cancer stem cells upon treatment with γ‐secretase inhibitor." PROTEOMICS 11(23): 4529-4540. <http://hdl.handle.net/2027.42/88055>en_US
dc.identifier.issn1615-9853en_US
dc.identifier.issn1615-9861en_US
dc.identifier.urihttps://hdl.handle.net/2027.42/88055
dc.description.abstractNotch signaling has been demonstrated to have a central role in glioblastoma (GBM) cancer stem cells (CSCs) and we have demonstrated recently that Notch pathway blockade by γ‐secretase inhibitor (GSI) depletes GBM CSCs and prevents tumor propagation both in vitro and in vivo. In order to understand the proteome alterations involved in this transformation, a dose‐dependent quantitative mass spectrometry (MS)‐based proteomic study has been performed based on the global proteome profiling and a target verification phase where both Immunoassay and a multiple reaction monitoring (MRM) assay are employed. The selection of putative protein candidates for confirmation poses a challenge due to the large number of identifications from the discovery phase. A multilevel filtering strategy together with literature mining is adopted to transmit the most confident candidates along the pipeline. Our results indicate that treating GBM CSCs with GSI induces a phenotype transformation towards non‐tumorigenic cells with decreased proliferation and increased differentiation, as well as elevated apoptosis. Suppressed glucose metabolism and attenuated NFR2‐mediated oxidative stress response are also suggested from our data, possibly due to their crosstalk with Notch Signaling. Overall, this quantitative proteomic‐based dose‐dependent work complements our current understanding of the altered signaling events occurring upon the treatment of GSI in GBM CSCs.en_US
dc.publisherWILEY‐VCH Verlagen_US
dc.subject.otherCancer Stem Cellsen_US
dc.subject.otherCell Biologyen_US
dc.subject.otherGlioblastomaen_US
dc.subject.otherLabel‐Freeen_US
dc.subject.otherMultiple Reaction Monitoringen_US
dc.subject.otherPathway Analysisen_US
dc.titleDose‐dependent proteomic analysis of glioblastoma cancer stem cells upon treatment with γ‐secretase inhibitoren_US
dc.typeArticleen_US
dc.rights.robotsIndexNoFollowen_US
dc.subject.hlbsecondlevelBiological Chemistryen_US
dc.subject.hlbsecondlevelChemical Engineeringen_US
dc.subject.hlbsecondlevelChemistryen_US
dc.subject.hlbsecondlevelMaterials Science and Engineeringen_US
dc.subject.hlbsecondlevelMolecular, Cellular and Developmental Biologyen_US
dc.subject.hlbtoplevelHealth Sciencesen_US
dc.subject.hlbtoplevelScienceen_US
dc.subject.hlbtoplevelEngineeringen_US
dc.description.peerreviewedPeer Revieweden_US
dc.contributor.affiliationumProgram of Bioinformatics, University of Michigan Medical Center, Ann Arbor, MI, USAen_US
dc.contributor.affiliationumDepartment of Surgery, University of Michigan Medical Center, Ann Arbor, MI, USAen_US
dc.contributor.affiliationumDepartment of Internal Medicine, University of Michigan Medical Center, Ann Arbor, MI, USAen_US
dc.contributor.affiliationumDepartment of Neurosurgery and Cell and Developmental Biology, University of Michigan Medical Center, Ann Arbor, MI, USAen_US
dc.contributor.affiliationumMaude T. Lane Professor of Surgery University of Michigan Medical Center, Department of Surgery, 1150 W. Medical Center Drive, MSRB I, A510B, Ann Arbor, MI 48109‐0650, USA Fax: +1‐734‐615‐2088en_US
dc.identifier.pmid21932445en_US
dc.description.bitstreamurlhttp://deepblue.lib.umich.edu/bitstream/2027.42/88055/1/4529_ftp.pdf
dc.identifier.doi10.1002/pmic.201000730en_US
dc.identifier.sourcePROTEOMICSen_US
dc.identifier.citedreferenceStupp, R., Mason, W. P., van den Bent, M. J., Weller, M. et al., Radiotherapy plus concomitant and adjuvant temozolomide for glioblastoma. N. Engl. J. Med. 2005, 352, 987 – 996.en_US
dc.identifier.citedreferenceVescovi, A. L., Galli, R., Reynolds, B. A., Brain tumour stem cells. Nat. Rev. Cancer 2006, 6, 425 – 436.en_US
dc.identifier.citedreferenceRead, T. A., Fogarty, M. P., Markant, S. L., McLendon, R. E. et al., Identification of CD15 as a marker for tumor‐propagating cells in a mouse model of medulloblastoma. Cancer Cell 2009, 15, 135 – 147.en_US
dc.identifier.citedreferenceWard, R. J., Lee, L., Graham, K., Satkunendran, T. et al., Multipotent CD15+ cancer stem cells in patched‐1‐deficient mouse medulloblastoma. Cancer Res. 2009, 69, 4682 – 4690.en_US
dc.identifier.citedreferenceSon, M. J., Woolard, K., Nam, D. H., Lee, J., Fine, H. A., SSEA‐1 is an enrichment marker for tumor‐initiating cells in human glioblastoma. Cell Stem Cell 2009, 4, 440 – 452.en_US
dc.identifier.citedreferenceGilbert, C. A., Ross, A. H., Cancer stem cells: cell culture, markers, and targets for new therapies. J. Cell Biochem. 2009, 108, 1031 – 1038.en_US
dc.identifier.citedreferenceFan, X., Khaki, L., Zhu, T. S., Soules, M. E. et al., NOTCH pathway blockade depletes CD133‐positive glioblastoma cells and inhibits growth of tumor neurospheres and xenografts. Stem Cells 2010, 28, 5 – 16.en_US
dc.identifier.citedreferenceStockhausen, M. T., Kristoffersen, K., Poulsen, H. S., The functional role of Notch signaling in human gliomas. Neuro. Oncol. 2010, 12, 199 – 211.en_US
dc.identifier.citedreferenceFan, X., Matsui, W., Khaki, L., Stearns, D. et al., Notch pathway inhibition depletes stem‐like cells and blocks engraftment in embryonal brain tumors. Cancer Res. 2006, 66, 7445 – 7452.en_US
dc.identifier.citedreferenceWang, J., Wakeman, T. P., Lathia, J. D., Hjelmeland, A. B. et al., Notch promotes radioresistance of glioma stem cells. Stem Cells 2010, 28, 17 – 28.en_US
dc.identifier.citedreferenceChiba, S., Notch signaling in stem cell systems. Stem Cells 2006, 24, 2437 – 2447.en_US
dc.identifier.citedreferenceFan, X., Eberhart, C. G., Medulloblastoma stem cells. J. Clin. Oncol. 2008, 26, 2821 – 2827.en_US
dc.identifier.citedreferenceSteiniger, S. C., Coppinger, J. A., Kruger, J. A., Yates 3rd, J., Janda, K. D., Quantitative mass spectrometry identifies drug targets in cancer stem cell‐containing side population. Stem Cells 2008, 26, 3037 – 3046.en_US
dc.identifier.citedreferenceBendall, S. C., Hughes, C., Campbell, J. L., Stewart, M. H. et al., An enhanced mass spectrometry approach reveals human embryonic stem cell growth factors in culture. Mol. Cell. Proteomics 2009, 8, 421 – 432.en_US
dc.identifier.citedreferenceWilliamson, A. J., Smith, D. L., Blinco, D., Unwin, R. D. et al., Quantitative proteomics analysis demonstrates post‐transcriptional regulation of embryonic stem cell differentiation to hematopoiesis. Mol. Cell. Proteomics 2008, 7, 459 – 472.en_US
dc.identifier.citedreferenceDai, L., Li, C., Shedden, K. A., Lee, C. J. et al., Quantitative proteomic profiling studies of pancreatic cancer stem cells. J. Proteome Res. 2010, 9, 3394 – 3402.en_US
dc.identifier.citedreferenceKitteringham, N. R., Jenkins, R. E., Lane, C. S., Elliott, V. L., Park, B. K., Multiple reaction monitoring for quantitative biomarker analysis in proteomics and metabolomics. J. Chromatogr. B Analyt. Technol. Biomed. Life Sci. 2009, 877, 1229 – 1239.en_US
dc.identifier.citedreferencePrakash, A., Tomazela, D. M., Frewen, B., Maclean, B. et al., Expediting the development of targeted SRM assays: using data from shotgun proteomics to automate method development. J. Proteome Res. 2009, 8, 2733 – 2739.en_US
dc.identifier.citedreferenceLopez, M. F., Kuppusamy, R., Sarracino, D. A., Prakash, A. et al., Mass spectrometric discovery and selective reaction monitoring (SRM) of putative protein biomarker candidates in first trimester Trisomy 21 maternal serum. J. Proteome Res. 2011, 10, 133 – 142.en_US
dc.identifier.citedreferenceGalli, R., Binda, E., Orfanelli, U., Cipelletti, B. et al., Isolation and characterization of tumorigenic, stem‐like neural precursors from human glioblastoma. Cancer Res. 2004, 64, 7011 – 7021.en_US
dc.identifier.citedreferenceKeller, A., Nesvizhskii, A. I., Kolker, E., Aebersold, R., Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Anal. Chem. 2002, 74, 5383 – 5392.en_US
dc.identifier.citedreferenceDai, L., Li, C., Shedden, K. A., Misek, D. E., Lubman, D. M., Comparative proteomic study of two closely related ovarian endometrioid adenocarcinoma cell lines using cIEF fractionation and pathway analysis. Electrophoresis 2009, 30, 1119 – 1131.en_US
dc.identifier.citedreferenceLiu, J. W., Jiao, N. Z., Hong, H. S., Luo, T. W., Cai, H. Y., Proliferating cell nuclear antigen (PCNA) as a marker of cell proliferation in the marine dinoflagellate Prorocentrum donghaiense Lu and the green alga Dunaliella salina Teodoresco. J. Appl. Phycol. 2005, 17, 323 – 330.en_US
dc.identifier.citedreferenceMa, X. B., Jia, X. S., Liu, Y. L., Wang, L. L. et al., Expression and role of Notch signalling in the regeneration of rat tracheal epithelium. Cell Prolif. 2009, 42, 15 – 28.en_US
dc.identifier.citedreferenceMitchell, K. E., Weiss, M. L., Mitchell, B. M., Martin, P. et al., Matrix cells from Wharton's jelly form neurons and glia. Stem Cells 2003, 21, 50 – 60.en_US
dc.identifier.citedreferencePrestegarden, L., Svendsen, A., Wang, J., Sleire, L. et al., Glioma cell populations grouped by different cell type markers drive brain tumor growth. Cancer Res. 2010, 70, 4274 – 4279.en_US
dc.identifier.citedreferenceRebetz, J., Tian, D., Persson, A., Widegren, B. et al., Glial progenitor‐like phenotype in low‐grade glioma and enhanced CD133‐expression and neuronal lineage differentiation potential in high‐grade glioma. PLoS One 2008, 3, e1936.en_US
dc.identifier.citedreferenceSingh, S. K., Clarke, I. D., Terasaki, M., Bonn, V. E. et al., Identification of a cancer stem cell in human brain tumors. Cancer Res. 2003, 63, 5821 – 5828.en_US
dc.identifier.citedreferencePark, K. H., Choi, S. E., Eom, M., Kang, Y., Downregulation of the anaphase‐promoting complex (APC)7 in invasive ductal carcinomas of the breast and its clinicopathologic relationships. Breast Cancer Res. 2005, 7, R238 – R247.en_US
dc.identifier.citedreferenceBentley, A. M., Williams, B. C., Goldberg, M. L., Andres, A. J., Phenotypic characterization of Drosophila ida mutants: defining the role of APC5 in cell cycle progression. J. Cell Sci. 2002, 115, 949 – 961.en_US
dc.identifier.citedreferenceWang, Q., Moyret‐Lalle, C., Couzon, F., Surbiguet‐Clippe, C. et al., Alterations of anaphase‐promoting complex genes in human colon cancer cells. Oncogene 2003, 22, 1486 – 1490.en_US
dc.identifier.citedreferenceHaapasalo, H., Kylaniemi, M., Paunul, N., Kinnula, V. L., Soini, Y., Expression of antioxidant enzymes in astrocytic brain tumors. Brain Pathol. 2003, 13, 155 – 164.en_US
dc.identifier.citedreferenceHemmati, H. D., Nakano, I., Lazareff, J. A., Masterman‐Smith, M. et al., Cancerous stem cells can arise from pediatric brain tumors. Proc. Natl. Acad. Sci. USA 2003, 100, 15178 – 15183.en_US
dc.identifier.citedreferenceShih, A. H., Holland, E. C., Notch signaling enhances nestin expression in gliomas. Neoplasia 2006, 8, 1072 – 1082.en_US
dc.identifier.citedreferenceNefedova, Y., Sullivan, D. M., Bolick, S. C., Dalton, W. S., Gabrilovich, D. I., Inhibition of Notch signaling induces apoptosis of myeloma cells and enhances sensitivity to chemotherapy. Blood 2008, 111, 2220 – 2229.en_US
dc.identifier.citedreferenceJia, X. X., Lu, Z. Z., Wang, H., Duan, H. F. et al., Suppressive effect of Notch signal activation on apoptosis of multiple myeloma cells. Zhongguo Shi Yan Xue Ye Xue Za Zhi 2004, 12, 335 – 339.en_US
dc.identifier.citedreferenceLovat, P. E., Corazzari, M., Armstrong, J. L., Martin, S. et al., Increasing melanoma cell death using inhibitors of protein disulfide isomerases to abrogate survival responses to endoplasmic reticulum stress. Cancer Res. 2008, 68, 5363 – 5369.en_US
dc.identifier.citedreferenceCui, Y., Zhu, H., Zhu, Y., Guo, X. et al., Proteomic analysis of testis biopsies in men treated with injectable testosterone undecanoate alone or in combination with oral levonorgestrel as potential male contraceptive. J. Proteome Res. 2008, 7, 3984 – 3993.en_US
dc.identifier.citedreferencePathil, A., Armeanu, S., Venturelli, S., Mascagni, P. et al., HDAC inhibitor treatment of hepatoma cells induces both TRAIL‐independent apoptosis and restoration of sensitivity to TRAIL. Hepatology 2006, 43, 425 – 434.en_US
dc.identifier.citedreferenceSingh, T. R., Shankar, S., Srivastava, R. K., HDAC inhibitors enhance the apoptosis‐inducing potential of TRAIL in breast carcinoma. Oncogene 2005, 24, 4609 – 4623.en_US
dc.identifier.citedreferenceZhao, Z. L., Li, Q. F., Zheng, Y. B., Chen, L. Y. et al., The aberrant expressions of nuclear matrix proteins during the apoptosis of human osteosarcoma cells. Anat. Rec. (Hoboken) 2010, 293, 813 – 820.en_US
dc.identifier.citedreferenceXing, H., Zhang, S., Weinheimer, C., Kovacs, A., Muslin, A. J., 14‐3‐3 proteins block apoptosis and differentially regulate MAPK cascades. Embo J. 2000, 19, 349 – 358.en_US
dc.identifier.citedreferenceRosenquist, M., 14‐3‐3 proteins in apoptosis. Braz. J. Med. Biol. Res. 2003, 36, 403 – 408.en_US
dc.identifier.citedreferenceCao, W., Yang, X., Zhou, J., Teng, Z. et al., Targeting 14‐3‐3 protein, difopein induces apoptosis of human glioma cells and suppresses tumor growth in mice. Apoptosis 2010, 15, 230 – 241.en_US
dc.identifier.citedreferencePerez‐Martinez, M., Gordon‐Alonso, M., Cabrero, J. R., Barrero‐Villar, M. et al., F‐actin‐binding protein drebrin regulates CXCR4 recruitment to the immune synapse. J. Cell Sci. 2010, 123, 1160 – 1170.en_US
dc.identifier.citedreferenceBetapudi, V., Myosin II motor proteins with different functions determine the fate of lamellipodia extension during cell spreading. PLoS One 2010, 5, e8560.en_US
dc.identifier.citedreferenceMedjkane, S., Perez‐Sanchez, C., Gaggioli, C., Sahai, E., Treisman, R., Myocardin‐related transcription factors and SRF are required for cytoskeletal dynamics and experimental metastasis. Nat. Cell Biol. 2009, 11, 257 – 268.en_US
dc.identifier.citedreferenceCho, H. Y., Reddy, S. P., Debiase, A., Yamamoto, M., Kleeberger, S. R., Gene expression profiling of NRF2‐mediated protection against oxidative injury. Free Radic. Biol. Med. 2005, 38, 325 – 343.en_US
dc.identifier.citedreferenceGomez‐Pastor, R., Perez‐Torrado, R., Cabiscol, E., Ros, J., Matallana, E., Reduction of oxidative cellular damage by overexpression of the thioredoxin TRX2 gene improves yield and quality of wine yeast dry active biomass. Microb. Cell Fact. 2010, 9, 9.en_US
dc.identifier.citedreferenceRonkainen, H., Vaarala, M. H., Kauppila, S., Soini, Y. et al., Increased BTB‐Kelch type substrate adaptor protein immunoreactivity associates with advanced stage and poor differentiation in renal cell carcinoma. Oncol. Rep. 2009, 21, 1519 – 1523.en_US
dc.identifier.citedreferenceGo, Y. M., Craige, S. E., Orr, M., Gernert, K. M., Jones, D. P., Gene and protein responses of human monocytes to extracellular cysteine redox potential. Toxicol. Sci. 2009, 112, 354 – 362.en_US
dc.identifier.citedreferenceKai, K., Arima, Y., Kamiya, T., Saya, H., Breast cancer stem cells. Breast Cancer 2010, 17, 80 – 85.en_US
dc.identifier.citedreferenceDiehn, M., Cho, R. W., Lobo, N. A., Kalisky, T. et al., Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 2009, 458, 780 – 783.en_US
dc.identifier.citedreferenceWakabayashi, N., Shin, S., Slocum, S. L., Agoston, E. S. et al., Regulation of notch1 signaling by nrf2: implications for tissue regeneration. Sci. Signal 2010, 3, ra52.en_US
dc.identifier.citedreferenceWarburg, O., On the origin of cancer cells. Science 1956, 123, 309 – 314.en_US
dc.identifier.citedreferencePalomero, T., Dominguez, M., Ferrando, A. A., The role of the PTEN/AKT Pathway in NOTCH1‐induced leukemia. Cell Cycle 2008, 7, 965 – 970.en_US
dc.identifier.citedreferenceCiofani, M., Zuniga‐Pflucker, J. C., Notch promotes survival of pre‐T cells at the beta‐selection checkpoint by regulating cellular metabolism. Nat. Immunol. 2005, 6, 881 – 888.en_US
dc.identifier.citedreferenceElstrom, R. L., Bauer, D. E., Buzzai, M., Karnauskas, R. et al., Akt stimulates aerobic glycolysis in cancer cells. Cancer Res. 2004, 64, 3892 – 3899.en_US
dc.identifier.citedreferenceVander Heiden, M. G., Cantley, L. C., Thompson, C. B., Understanding the Warburg effect: the metabolic requirements of cell proliferation. Science 2009, 324, 1029 – 1033.en_US
dc.identifier.citedreferenceKanamori, M., Kawaguchi, T., Nigro, J. M., Feuerstein, B. G. et al., Contribution of Notch signaling activation to human glioblastoma multiforme. J. Neurosurg. 2007, 106, 417 – 427.en_US
dc.identifier.citedreferenceLee, S. H., Kim, M. H., Han, H. J., Arachidonic acid potentiates hypoxia‐induced VEGF expression in mouse embryonic stem cells: involvement of Notch, Wnt, and HIF‐1alpha. Am. J. Physiol. Cell Physiol. 2009, 297, C207 – C216.en_US
dc.owningcollnameInterdisciplinary and Peer-Reviewed


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