Phosphoproteome of human Glioblastoma initiating cells reveals novel signaling regulators encoded by the transcriptome

PLoS ONE

Volumn 7, Issue 8, 2012, Pages

  Kozuka Hata, Hiroko ^a   Nasu Nishimura, Yukiko ^a   Koyama Nasu, Ryo ^a   Ao Kondo, Hiroko ^a   Tsumoto, Kouhei ^a   Akiyama, Tetsu ^a   Oyama, Masaaki ^a  

^a UNIVERSITY OF TOKYO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II DELTA; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II GAMMA; DISHEVELLED 3; DISHEVELLED PROTEIN; E1A ASSOCIATED P300 PROTEIN; EPIDERMAL GROWTH FACTOR RECEPTOR; GLYCOGEN SYNTHASE KINASE 3BETA; HISTONE DEACETYLASE 1; HISTONE DEACETYLASE 2; MITOGEN ACTIVATED PROTEIN KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE KINASE 7; NCK ADAPTOR PROTEIN 1; NCK ADAPTOR PROTEIN 2; NCK PROTEIN; NESTIN; P21 ACTIVATED KINASE 2; P21 ACTIVATED KINASE 4; PHOSPHOPROTEOME; PRESENILIN 1; PRESENILIN 2; PROTEIN C JUN; PROTEIN KINASE C ALPHA; PROTEIN KINASE C BETA; PROTEIN TYROSINE PHOSPHATASE SHP 1; PROTEOME; SILENCING MEDIATOR OF RETINOID AND THYROID HORMONE RECEPTOR; TRANSCRIPTOME; TUMOR NECROSIS FACTOR ALPHA CONVERTING ENZYME; UNCLASSIFIED DRUG;

ARTICLE; CANCER CELL; CELL DIFFERENTIATION; CELL PROLIFERATION; CONTROLLED STUDY; DOWN REGULATION; GLIOBLASTOMA; HUMAN; HUMAN CELL; LIQUID CHROMATOGRAPHY; MOLECULAR DYNAMICS; NUCLEOTIDE SEQUENCE; OPEN READING FRAME; PROTEIN ANALYSIS; PROTEIN METABOLISM; PROTEIN PHOSPHORYLATION; SEQUENCE ALIGNMENT; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; UPREGULATION;

AMINO ACID SEQUENCE; AMINO ACIDS; BLOTTING, WESTERN; BRAIN NEOPLASMS; CELL LINE, TUMOR; CHROMATOGRAPHY, LIQUID; EPIDERMAL GROWTH FACTOR; FIBROBLAST GROWTH FACTORS; GLIOBLASTOMA; HUMANS; ISOTOPE LABELING; MASS SPECTROMETRY; MOLECULAR SEQUENCE DATA; NEOPLASTIC STEM CELLS; PHOSPHOPEPTIDES; PHOSPHOPROTEINS; PROTEOME; PROTEOMICS; SEQUENCE HOMOLOGY, AMINO ACID; SIGNAL TRANSDUCTION; TRANSCRIPTOME;

EID: 84865077341     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0043398     Document Type: Article

References (41)

1. Bianco P, Robey PG, ((2001)) Stem cells in tissue engineering. Nature 414:: 118--121.
2. Reya T, Morrison SJ, Clarke MF, Weissman IL, ((2001)) Stem cells, cancer, and cancer stem cells. Nature 414:: 105--111.
3. Cho RW, Clarke MF, ((2008)) Recent advances in cancer stem cells. Curr Opin Genet Dev 18:: 48--53.
4. Singh SK, Clarke ID, Terasaki M, Bonn VE, Hawkins C, et al. ((2003)) Identification of a cancer stem cell in human brain tumors. Cancer Res 63:: 5821--5828.
5. Singh SK, Hawkins C, Clarke ID, Squire JA, Bayani J, et al. ((2004)) Identification of human brain tumour initiating cells. Nature 432:: 396--401.
6. Lee J, Kotliarova S, Kotliarov Y, Li A, Su Q, et al. ((2006)) 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 9:: 391--403.
7. Maher EA, Furnari FB, Bachoo RM, Rowitch DH, Louis DN, et al. ((2001)) Malignant glioma: Genetics and biology of a grave matter. Genes Dev 15:: 1311--1333.
8. Legler JM, Ries LA, Smith MA, Warren JL, Heineman EF, et al. ((1999)) Brain and other central nervous system cancers: Recent trends in incidence and mortality. J Natl Cancer Inst 91:: 1382--1390.
9. Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, et al. ((2009)) Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature 458:: 780--783.
10. Liu G, Yuan X, Zeng Z, Tunici P, Ng H, et al. ((2006)) Analysis of gene expression and chemoresistance of CD133+ cancer stem cells in glioblastoma. Mol Cancer 5:: 67.
11. Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, et al. ((2006)) Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature 444:: 756--760.
12. Hunter T, ((1995)) Protein kinases and phosphatases: The Yin and Yang of protein phosphorylation and signaling. Cell 80:: 225--236.
13. Hunter T, ((2000)) Signaling-2000 and beyond. Cell 100:: 113--127.
14. Schlessinger J, ((2000)) Cell signaling by receptor tyrosine kinases. Cell 103:: 211--225.
15. Pawson T, Nash P, ((2003)) Assembly of cell regulatory systems through protein interaction domains. Science 300:: 445--452.
16. Blume-Jensen P, Hunter T, ((2001)) Oncogenic kinase signalling. Nature 411:: 355--365.
17. Aebersold R, Mann M, ((2003)) Mass spectrometry-based proteomics. Nature 422:: 198--207.
18. Mann M, ((2006)) Functional and quantitative proteomics using SILAC. Nat Rev Mol Cell Biol 7:: 952--958.
19. Ong SE, Blagoev B, Kratchmarova I, Kristensen DB, Steen H, et al. ((2002)) Stable isotope labeling by amino acids in cell culture, SILAC, as a simple and accurate approach to expression proteomics. Mol Cell Proteomics 1:: 376--386.
20. Olsen JV, Blagoev B, Gnad F, Macek B, Kumar C, et al. ((2006)) Global, in vivo, and site-specific phosphorylation dynamics in signaling networks. Cell 127:: 635--648.
21. Pollard SM, Yoshikawa K, Clarke ID, Danovi D, Stricker S, et al. ((2009)) Glioma stem cell lines expanded in adherent culture have tumor-specific phenotypes and are suitable for chemical and genetic screens. Cell Stem Cell 4:: 568--580.
22. Van Hoof D, Muñoz J, Braam SR, Pinkse MW, Linding R, et al. ((2009)) Phosphorylation dynamics during early differentiation of human embryonic stem cells. Cell Stem Cell 5:: 214--226.
23. Mani SA, Guo W, Liao MJ, Eaton EN, Ayyanan A, et al. ((2008)) The epithelial-mesenchymal transition generates cells with properties of stem cells. Cell 133:: 704--715.
24. Aguirre A, Rubio ME, Gallo V, ((2010)) Notch and EGFR pathway interaction regulates neural stem cell number and self-renewal. Nature 467:: 323--327.
25. Peri S, Navarro JD, Amanchy R, Kristiansen TZ, Jonnalagadda CK, et al. ((2003)) Development of human protein reference database as an initial platform for approaching systems biology in humans. Genome Res 13:: 2363--2371.
26. Dennis G Jr, Sherman BT, Hosack DA, Yang J, Gao W, et al. ((2003)) DAVID: Database for Annotation, Visualization, and Integrated Discovery. Genome Biol 4:: P3.
27. Huang Z, Cheng L, Guryanova OA, Wu Q, Bao S, ((2010)) Cancer stem cells in glioblastoma-molecular signaling and therapeutic targeting. Protein Cell 1:: 638--655.
28. Brill LM, Xiong W, Lee KB, Ficarro SB, Crain A, et al. ((2009)) Phosphoproteomic analysis of human embryonic stem cells. Cell Stem Cell 5:: 204--213.
29. Rigbolt KT, Prokhorova TA, Akimov V, Henningsen J, Johansen PT, et al. ((2011)) System-wide temporal characterization of the proteome and phosphoproteome of human embryonic stem cell differentiation. Sci Signal 4:: rs3.
30. Dai L, Li C, Shedden KA, Lee CJ, Li C, et al. ((2010)) Quantitative proteomic profiling studies of pancreatic cancer stem cells. J Proteome Res 9:: 3394--3402.
31. Zou J, Yu XF, Bao ZJ, Dong J, ((2011)) Proteome of human colon cancer stem cells: A comparative analysis. World J Gastroenterol 17:: 1276--1285.
32. Huang PH, Mukasa A, Bonavia R, Flynn RA, Brewer ZE, et al. ((2007)) Quantitative analysis of EGFRvIII cellular signaling networks reveals a combinatorial therapeutic strategy for glioblastoma. Proc Natl Acad Sci 104:: 12867--12872.
33. Nilsson CL, Dillon R, Devakumar A, Shi SD, Greig M, et al. ((2010)) Quantitative phosphoproteomic analysis of the STAT3/IL-6/HIF1alpha signaling network: An initial study in GSC11 glioblastoma stem cells. J Proteome Res 9:: 430--443.
34. Murakami M, Ichisaka T, Maeda M, Oshiro N, Hara K, et al. ((2004)) mTOR is essential for growth and proliferation in early mouse embryos and embryonic stem cells. Mol Cell Biol 24:: 6710--6718.
35. Gangloff YG, Mueller M, Dann SG, Svoboda P, Sticker M, et al. ((2004)) Disruption of the mouse mTOR gene leads to early postimplantation lethality and prohibits embryonic stem cell development. Mol Cell Biol 24:: 9508--9516.
36. International Human Genome Sequencing Consortium, ((2004)) Finishing the euchromatic sequence of the human genome. Nature 431:: 931--945.
37. Xu N, Papagiannakopoulos T, Pan G, Thomson JA, Kosik KS, ((2009)) MicroRNA-145 regulates OCT4, SOX2, and KLF4 and represses pluripotency in human embryonic stem cells. Cell 137:: 647--658.
38. Wang X, Yu J, Sreekumar A, Varambally S, Shen R, et al. ((2005)) Autoantibody signatures in prostate cancer. N Engl J Med 353:: 1224--1235.
39. Son MJ, Woolard K, Nam DH, Lee J, Fine HA, ((2009)) SSEA-1 is an enrichment marker for tumor-initiating cells in human glioblastoma. Cell Stem Cell 4:: 440--452.
40. Olsen JV, Macek B, Lange O, Makarov A, Horning S, et al. ((2007)) Higher-energy C-trap dissociation for peptide modification analysis. Nat Methods 4:: 709--712.
41. Olsen JV, de Godoy LM, Li G, Macek B, Mortensen P, et al. ((2005)) Parts per million mass accuracy on an Orbitrap mass spectrometer via lock mass injection into a C-trap. Mol Cell Proteomics 4:: 2010--2021.