CoChat
Sign Up
Cited by 317Glioma Diagnosis and TreatmentCancer Genomics and DiagnosticsChromatin Remodeling and Cancer

Integrated Proteogenomic Characterization across Major Histological Types of Pediatric Brain Cancer

Open access
Petralia, Francesca, Tignor, Nicole, Reva, Boris, Koptyra, Mateusz, Chowdhury, Shrabanti, Rykunov, Dmitry, Krek, Azra, Ma, Weiping +136 more·2020·Cell
DOI 10.1016/j.cell.2020.10.044PMC PMC8143193
Open this paper in CoChat — free accountOpen PDF

Abstract

We report a comprehensive proteogenomics analysis, including whole-genome sequencing, RNA sequencing, and proteomics and phosphoproteomics profiling, of 218 tumors across 7 histological types of childhood brain cancer: low-grade glioma (n = 93), ependymoma (32), high-grade glioma (25), medulloblastoma (22), ganglioglioma (18), craniopharyngioma (16), and atypical teratoid rhabdoid tumor (12). Proteomics data identify common biological themes that span histological boundaries, suggesting that treatments used for one histological type may be applied effectively to other tumors sharing similar proteomics features. Immune landscape characterization reveals diverse tumor microenvironments across and within diagnoses. Proteomics data further reveal functional effects of somatic mutations and copy number variations (CNVs) not evident in transcriptomics data. Kinase-substrate association and co-expression network analysis identify important biological mechanisms of tumorigenesis. This is the first large-scale proteogenomics analysis across traditional histological boundaries to uncover foundational pediatric brain tumor biology and inform rational treatment selection.

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Integrity signals

Registry

Crossref · 10.1016/j.cell.2020.10.044

Cites

23 of 23 references verified0 citation errors · 0 not checkable

Statistics

Claims the paper makes

The claims and statistics of this paper haven’t been checked yet.

Run the check — free, no account needed. It reads the open-access text and checks the sources it cites.

A few free checks a day · papers already verified open instantly · results are public

Claims other papers make about this one

Each is checked against this paper’s own text: does it say what the citing paper says it does?

  • Acute social defeat stress increased systemic inflammation, marked by up-regulation of pro-inflammatory cytokines Cxcl10 and Il-6.

    “RNA-seq analysis revealed increased systemic inflammation, marked by up-regulation of pro-inflammatory cytokines like Cxcl10 and Il-6”

    From Comparative Analysis of HPA-Axis Dysregulation and Dynamic Molecular Mechanisms in Acute Versus Chronic Social Defeat Stress (2025) · cites this paper as [43]

    The Results section on immune infiltration concerns pediatric brain tumors and BRAF-associated immune signatures, not acute social defeat stress or systemic inflammation. The STAR METHOD section describes RNA-seq-based microglia signatures but does not report up-regulation of Cxcl10 or Il-6. Searches for social defeat stress and those cytokines found no passage addressing the claim; page numbers were not provided. (LLM, conf=0.76)

    Experimental — accuracy not yet measured

Self-check

Percentages, sums and reported differences re-computed from the paper’s own numbers.

The self-check needs the paper’s full text.

Cites

Flagged first, then by citations

Research works printed but not linked: 169

  1. Abate M, Laezza C, Pisanti S, Torelli G, Seneca V, Catapano G, Montella F, Ranieri R, Notarnicola M, Gazzerro P, (2017). Deregulated expression and activity of Farnesyl Diphosphate Synthase (FDPS) in Glioblastoma. Scientific reports 7, 14123. 29075041 PMC5658376
  2. Apps JR, Carreno G, Gonzalez-Meljem JM, Haston S, Guiho R, Cooper JE, Manshaei S, Jani N, Holsken A, Pettorini B, (2018). Tumour compartment transcriptomics demonstrates the activation of inflammatory and odontogenic programmes in human adamantinomatous craniopharyngioma and identifies the MAPK/ERK pathway as a novel therapeutic target. Acta neuropathologica 135, 757– 777. 29541918 PMC5904225
  3. Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, (2000). Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nature genetics 25, 25– 29. 10802651 PMC3037419
  4. Baroti T, Zimmermann Y, Schillinger A, Liu L, Lommes P, Wegner M, and Stolt CC (2016). Transcription factors Sox5 and Sox6 exert direct and indirect influences on oligodendroglial migration in spinal cord and forebrain. Glia 64, 122– 138. 26345464
  5. Beausoleil SA, Villén J, Gerber SA, Rush J, and Gygi SP (2006). A probability-based approach for high-throughput protein phosphorylation analysis and site localization. Nature biotechnology 24, 1285– 1292. 16964243
  6. Bednarek E, and Caroni P (2011). beta-Adducin is required for stable assembly of new synapses and improved memory upon environmental enrichment. Neuron 69, 1132– 1146. 21435558
  7. Behrens J, Kameritsch P, Wallner S, Pohl U, and Pogoda K (2010). The carboxyl tail of Cx43 augments p38 mediated cell migration in a gap junction-independent manner. European journal of cell biology 89, 828– 838. 20727616
  8. Belletti B, and Baldassarre G (2011). Stathmin: a protein with many tasks. New biomarker and potential target in cancer. Expert opinion on therapeutic targets 15, 1249– 1266. 21978024
  9. Benjamini Y, and Hochberg Y (1995). Controlling the False Discovery Rate: A Practical and Powerful Approach to Multiple Testing. Journal of the Royal Statistical Society Series B (Methodological) 57, 289– 300.
  10. Bergaggio E, and Piva R (2019). Wild-Type IDH Enzymes as Actionable Targets for Cancer Therapy. Cancers 11. PMC6520797 31010244
  11. Box JK, Paquet N, Adams MN, Boucher D, Bolderson E, O’Byrne KJ, and Richard DJ (2016). Nucleophosmin: from structure and function to disease development. BMC molecular biology 17, 19. 27553022 PMC4995807
  12. Brastianos PK, Taylor-Weiner A, Manley PE, Jones RT, Dias-Santagata D, Thorner AR, Lawrence MS, Rodriguez FJ, Bernardo LA, Schubert L, (2014). Exome sequencing identifies BRAF mutations in papillary craniopharyngiomas. Nature genetics 46, 161– 165. 24413733 PMC3982316
  13. Briancon-Marjollet A, Balenci L, Fernandez M, Esteve F, Honnorat J, Farion R, Beaumont M, Barbier E, Remy C, and Baudier J (2010). NG2-expressing glial precursor cells are a new potential oligodendroglioma cell initiating population in N-ethyl-N-nitrosourea-induced gliomagenesis. Carcinogenesis 31, 1718– 1725. 20651032 PMC3308186
  14. Buckingham SC, Campbell SL, Haas BR, Montana V, Robel S, Ogunrinu T, and Sontheimer H (2011). Glutamate release by primary brain tumors induces epileptic activity. Nature medicine 17, 1269– 1274. PMC3192231 21909104
  15. Cai Y, Guo T, Wang Y, and Du J (2018). Glutamate Metabolism Regulates Immune Escape of Glioma. Madridge Journal of Immunology 2, 53– 57.
  16. Cai Z, Wang Y, Yu W, Xiao J, Li Y, Liu L, Zhu C, Tan K, Deng Y, Yuan W, (2006). hnulp1, a basic helix-loop-helix protein with a novel transcriptional repressive domain, inhibits transcriptional activity of serum response factor. Biochemical and biophysical research communications 343, 973– 981. 16574069
  17. Calvert AE, Chalastanis A, Wu Y, Hurley LA, Kouri FM, Bi Y, Kachman M, May JL, Bartom E, Hua Y, (2017). Cancer-Associated IDH1 Promotes Growth and Resistance to Targeted Therapies in the Absence of Mutation. Cell reports 19, 1858– 1873. 28564604 PMC5564207
  18. Campanini ML, Colli LM, Paixao BM, Cabral TP, Amaral FC, Machado HR, Neder LS, Saggioro F, Moreira AC, Antonini SR, (2010). CTNNB1 gene mutations, pituitary transcription factors, and MicroRNA expression involvement in the pathogenesis of adamantinomatous craniopharyngiomas. Hormones & cancer 1, 187– 196. 21761366 PMC10358030
  19. Campbell SL, Buckingham SC, and Sontheimer H (2012). Human glioma cells induce hyperexcitability in cortical networks. Epilepsia 53, 1360– 1370. 22709330 PMC3418468
  20. Cancer Genome Atlas Research, N. (2008). Comprehensive genomic characterization defines human glioblastoma genes and core pathways. Nature 455, 1061– 1068. 18772890 PMC2671642
  21. Capper D, Jones DTW, Sill M, Hovestadt V, Schrimpf D, Sturm D, Koelsche C, Sahm F, Chavez L, Reuss DE, (2018). DNA methylation-based classification of central nervous system tumours. Nature 555, 469– 474. 29539639 PMC6093218
  22. Cesca F, Baldelli P, Valtorta F, and Benfenati F (2010). The synapsins: key actors of synapse function and plasticity. Progress in neurobiology 91, 313– 348. 20438797
  23. Chalmers ZR, Connelly CF, Fabrizio D, Gay L, Ali SM, Ennis R, Schrock A, Campbell B, Shlien A, Chmielecki J, (2017). Analysis of 100,000 human cancer genomes reveals the landscape of tumor mutational burden. Genome medicine 9, 34. 28420421 PMC5395719
  24. Chang CV, Araujo RV, Cirqueira CS, Cani CM, Matushita H, Cescato VA, Fragoso MC, Bronstein MD, Zerbini MC, Mendonca BB, (2017). Differential Expression of Stem Cell Markers in Human Adamantinomatous Craniopharyngioma and Pituitary Adenoma. Neuroendocrinology 104, 183– 193. 27161333
  25. Chen JH, Huang SM, Chen CC, Tsai CF, Yeh WL, Chou SJ, Hsieh WT, and Lu DY (2011). Ghrelin induces cell migration through GHS-R, CaMKII, AMPK, and NF-κB signaling pathway in glioma cells. Journal of cellular biochemistry 112, 2931– 2941. 21630326
  26. Chisci E, De Giorgi M, Zanfrini E, Testasecca A, Brambilla E, Cinti A, Farina L, Kutryb-Zajac B, Bugarin C, Villa C, (2017). Simultaneous overexpression of human E5NT and ENTPD1 protects porcine endothelial cells against H2O2-induced oxidative stress and cytotoxicity in vitro. Free radical biology & medicine 108, 320– 333. 28389406
  27. Clark DJ, Dhanasekaran SM, Petralia F, Pan J, Song X, Hu Y, da Veiga Leprevost F, Reva B, Lih TM, Chang HY, (2019). Integrated Proteogenomic Characterization of Clear Cell Renal Cell Carcinoma. Cell 179, 964– 983.e931. 31675502 PMC7331093
  28. Colaprico A, Olsen C, Bailey MH, Odom GJ, Terkelsen T, Silva TC, Olsen AV, Cantini L, Zinovyev A, Barillot E, (2020). Interpreting pathways to discover cancer driver genes with Moonlight. Nature communications 11, 69. PMC6941958 31900418
  29. Colaprico A, Silva TC, Olsen C, Garofano L, Cava C, Garolini D, Sabedot TS, Malta TM, Pagnotta SM, Castiglioni I, (2016). TCGAbiolinks: an R/Bioconductor package for integrative analysis of TCGA data. Nucleic acids research 44, e71. 26704973 PMC4856967
  30. Cole AR (2012). GSK3 as a Sensor Determining Cell Fate in the Brain. Frontiers in molecular neuroscience 5, 4. 22363258 PMC3275790
  31. Cooper CD, and Lampe PD (2002). Casein kinase 1 regulates connexin-43 gap junction assembly. The Journal of biological chemistry 277, 44962– 44968. 12270943
  32. Coy S, Rashid R, Lin JR, Du Z, Donson AM, Hankinson TC, Foreman NK, Manley PE, Kieran MW, Reardon DA, (2018). Multiplexed immunofluorescence reveals potential PD-1/PD-L1 pathway vulnerabilities in craniopharyngioma. Neuro-oncology 20, 1101– 1112. 29509940 PMC6280314
  33. Cuddapah VA, and Sontheimer H (2010). Molecular interaction and functional regulation of ClC-3 by Ca2+/calmodulin-dependent protein kinase II (CaMKII) in human malignant glioma. The Journal of biological chemistry 285, 11188– 11196. 20139089 PMC2856996
  34. da Veiga Leprevost F, Haynes SE, Avtonomov DM, Chang H, Shanmugam AK, Mellacheruvu D, Kong AT, and Nesvizhskii AI (2020). Philosopher: a versatile toolkit for shotgun proteomics data analysis. Nature methods in press. PMC7509848 32669682
  35. Daily K, Ho Sui SJ, Schriml LM, Dexheimer PJ, Salomonis N, Schroll R, Bush S, Keddache M, Mayhew C, Lotia S, (2017). Molecular, phenotypic, and sample-associated data to describe pluripotent stem cell lines and derivatives. Scientific data 4, 170030. 28350385 PMC5369318
  36. Darmanis S, Sloan SA, Croote D, Mignardi M, Chernikova S, Samghababi P, Zhang Y, Neff N, Kowarsky M, Caneda C, (2017). Single-Cell RNA-Seq Analysis of Infiltrating Neoplastic Cells at the Migrating Front of Human Glioblastoma. Cell reports 21, 1399– 1410. 29091775 PMC5810554
  37. Dello Russo C, Lisi L, Tentori L, Navarra P, Graziani G, and Combs CK (2017). Exploiting Microglial Functions for the Treatment of Glioblastoma. Current cancer drug targets 17, 267– 281. 27528361
  38. Djomehri SI, Gonzalez ME, da Veiga Leprevost F, Tekula SR, Chang HY, White MJ, Cimino-Mathews A, Burman B, Basrur V, Argani P, (2020). Quantitative proteomic landscape of metaplastic breast carcinoma pathological subtypes and their relationship to triple-negative tumors. Nature communications 11, 1723. PMC7138853 32265444
  39. Easley-Neal C, Fierro J Jr., Buchanan J, and Washbourne P (2013). Late recruitment of synapsin to nascent synapses is regulated by Cdk5. Cell reports 3, 1199– 1212. 23602570 PMC3742072
  40. Fabregat A, Jupe S, Matthews L, Sidiropoulos K, Gillespie M, Garapati P, Haw R, Jassal B, Korninger F, May B, (2018). The Reactome Pathway Knowledgebase. Nucleic acids research 46, D649– d655. 29145629 PMC5753187
  41. Fangusaro J, Onar-Thomas A, Young Poussaint T, Wu S, Ligon AH, Lindeman N, Banerjee A, Packer RJ, Kilburn LB, Goldman S, (2019). Selumetinib in paediatric patients with BRAF-aberrant or neurofibromatosis type 1-associated recurrent, refractory, or progressive low-grade glioma: a multicentre, phase 2 trial. The Lancet Oncology 20, 1011– 1022. 31151904 PMC6628202
  42. Farghaian H, Turnley AM, Sutherland C, and Cole AR (2011). Bioinformatic prediction and confirmation of beta-adducin as a novel substrate of glycogen synthase kinase 3. The Journal of biological chemistry 286, 25274– 25283. 21606488 PMC3137098
  43. Fasolini M, Wu X, Flocco M, Trosset JY, Oppermann U, and Knapp S (2003). Hot spots in Tcf4 for the interaction with beta-catenin. The Journal of biological chemistry 278, 21092– 21098. 12657632
  44. Fei L, and Xu H (2018). Role of MCM2–7 protein phosphorylation in human cancer cells. Cell & bioscience 8, 43. 30062004 PMC6056998
  45. Finzsch M, Stolt CC, Lommes P, and Wegner M (2008). Sox9 and Sox10 influence survival and migration of oligodendrocyte precursors in the spinal cord by regulating PDGF receptor alpha expression. Development (Cambridge, England) 135, 637– 646. 18184726
  46. Fumagalli M, Lombardi M, Gressens P, and Verderio C (2018). How to reprogram microglia toward beneficial functions. Glia 66, 2531– 2549. 30195261 PMC6585737
  47. Gao C, Wang Y, Broaddus R, Sun L, Xue F, and Zhang W (2018). Exon 3 mutations of CTNNB1 drive tumorigenesis: a review. Oncotarget 9, 5492– 5508. 29435196 PMC5797067
  48. Gibbons BC, Chambers MC, Monroe ME, Tabb DL, and Payne SH (2015). Correcting systematic bias and instrument measurement drift with mzRefinery. Bioinformatics (Oxford, England) 31, 3838– 3840. PMC4653383 26243018
  49. Grobner SN, Worst BC, Weischenfeldt J, Buchhalter I, Kleinheinz K, Rudneva VA, Johann PD, Balasubramanian GP, Segura-Wang M, Brabetz S, (2018). The landscape of genomic alterations across childhood cancers. Nature 555, 321– 327. 29489754
  50. Grosely R, Kopanic JL, Nabors S, Kieken F, Spagnol G, Al-Mugotir M, Zach S, and Sorgen PL (2013). Effects of phosphorylation on the structure and backbone dynamics of the intrinsically disordered connexin43 C-terminal domain. The Journal of biological chemistry 288, 24857– 24870. 23828237 PMC3750180
  51. Haage V, Semtner M, Vidal RO, Hernandez DP, Pong WW, Chen Z, Hambardzumyan D, Magrini V, Ly A, Walker J, (2019). Comprehensive gene expression meta-analysis identifies signature genes that distinguish microglia from peripheral monocytes/macrophages in health and glioma. Acta neuropathologica communications 7, 20. 30764877 PMC6376799
  52. Hayashi H, Matsuzaki O, Muramatsu S, Tsuchiya Y, Harada T, Suzuki Y, Sugano S, Matsuda A, and Nishida E (2006). Centaurin-alpha1 is a phosphatidylinositol 3-kinase-dependent activator of ERK1/2 mitogen-activated protein kinases. The Journal of biological chemistry 281, 1332– 1337. 16287813
  53. Holcik M (2015). Could the eIF2alpha-Independent Translation Be the Achilles Heel of Cancer? Frontiers in oncology 5, 264. 26636041 PMC4659918
  54. Hong X, Sin WC, Harris AL, and Naus CC (2015). Gap junctions modulate glioma invasion by direct transfer of microRNA. Oncotarget 6, 15566– 15577. 25978028 PMC4558171
  55. Hornbeck PV, Zhang B, Murray B, Kornhauser JM, Latham V, and Skrzypek E (2015). PhosphoSitePlus, 2014: mutations, PTMs and recalibrations. Nucleic acids research 43, D512– 520. 25514926 PMC4383998
  56. Ito T, Chiba T, Ozawa R, Yoshida M, Hattori M, and Sakaki Y (2001). A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proceedings of the National Academy of Sciences of the United States of America 98, 4569– 4574. 11283351 PMC31875
  57. Itoh T, Satoh M, Kanno E, and Fukuda M (2006). Screening for target Rabs of TBC (Tre-2/Bub2/Cdc16) domain-containing proteins based on their Rab-binding activity. Genes to cells: devoted to molecular & cellular mechanisms 11, 1023– 1037. 16923123
  58. Jain P, Silva A, Han HJ, Lang SS, Zhu Y, Boucher K, Smith TE, Vakil A, Diviney P, Choudhari N, (2017). Overcoming resistance to single-agent therapy for oncogenic BRAF gene fusions via combinatorial targeting of MAPK and PI3K/mTOR signaling pathways. Oncotarget 8, 84697– 84713. 29156677 PMC5689567
  59. John Lin CC, Yu K, Hatcher A, Huang TW, Lee HK, Carlson J, Weston MC, Chen F, Zhang Y, Zhu W, (2017). Identification of diverse astrocyte populations and their malignant analogs. Nature neuroscience 20, 396– 405. 28166219 PMC5824716
  60. Johnson WE, Li C, and Rabinovic A (2007). Adjusting batch effects in microarray expression data using empirical Bayes methods. Biostatistics (Oxford, England) 8, 118– 127. 16632515
  61. Kalayci S, and Gumus ZH (2018). Exploring Biological Networks in 3D, Stereoscopic 3D, and Immersive 3D with iCAVE. Current protocols in bioinformatics 61, 8.27.21– 28.27.26. 30040198
  62. Kanehisa M, Furumichi M, Tanabe M, Sato Y, and Morishima K (2017). KEGG: new perspectives on genomes, pathways, diseases and drugs. Nucleic acids research 45, D353– d361. 27899662 PMC5210567
  63. Karczewski KJ, Francioli LC, Tiao G, Cummings BB, Alföldi J, Wang Q, Collins RL, Laricchia KM, Ganna A, Birnbaum DP, (2019). Variation across 141,456 human exomes and genomes reveals the spectrum of loss-of-function intolerance across human protein-coding genes. bioRxiv, 531210.
  64. Karmakar S, Dey P, Vaz AP, Bhaumik SR, Ponnusamy MP, and Batra SK (2018). PD2/PAF1 at the Crossroads of the Cancer Network. Cancer research 78, 313– 319. 29311159 PMC5771812
  65. Karremann M, Gielen GH, Hoffmann M, Wiese M, Colditz N, Warmuth-Metz M, Bison B, Claviez A, van Vuurden DG, von Bueren AO, (2018). Diffuse high-grade gliomas with H3 K27M mutations carry a dismal prognosis independent of tumor location. Neuro-oncology 20, 123– 131. 29016894 PMC5761525
  66. Keller A, Nesvizhskii AI, Kolker E, and Aebersold R (2002). Empirical statistical model to estimate the accuracy of peptide identifications made by MS/MS and database search. Analytical chemistry 74, 5383– 5392. 12403597
  67. Khuong-Quang DA, Buczkowicz P, Rakopoulos P, Liu XY, Fontebasso AM, Bouffet E, Bartels U, Albrecht S, Schwartzentruber J, Letourneau L, (2012). K27M mutation in histone H3.3 defines clinically and biologically distinct subgroups of pediatric diffuse intrinsic pontine gliomas. Acta neuropathologica 124, 439– 447. 22661320 PMC3422615
  68. Kilday JP, Mitra B, Domerg C, Ward J, Andreiuolo F, Osteso-Ibanez T, Mauguen A, Varlet P, Le Deley MC, Lowe J, (2012). Copy number gain of 1q25 predicts poor progression-free survival for pediatric intracranial ependymomas and enables patient risk stratification: a prospective European clinical trial cohort analysis on behalf of the Children’s Cancer Leukaemia Group (CCLG), Societe Francaise d’Oncologie Pediatrique (SFOP), and International Society for Pediatric Oncology (SIOP). Clinical cancer research: an official journal of the American Association for Cancer Research 18, 2001– 2011. 22338015
  69. Kim HY, Kim DK, Bae SH, Gwak H, Jeon JH, Kim JK, Lee BI, You HJ, Shin DH, Kim YH, (2018a). Farnesyl diphosphate synthase is important for the maintenance of glioblastoma stemness. Experimental & molecular medicine 50, 137. PMC6193020 30333528
  70. Kim S, Gupta N, and Pevzner PA (2008). Spectral probabilities and generating functions of tandem mass spectra: a strike against decoy databases. Journal of proteome research 7, 3354– 3363. 18597511 PMC2689316
  71. Kim S, Scheffler K, Halpern AL, Bekritsky MA, Noh E, Kallberg M, Chen X, Kim Y, Beyter D, Krusche P, (2018b). Strelka2: fast and accurate calling of germline and somatic variants. Nature methods 15, 591– 594. 30013048
  72. Kim W, and Liau LM (2012). IDH mutations in human glioma. Neurosurgery clinics of North America 23, 471– 480. 22748659 PMC3618997
  73. Kong AT, Leprevost FV, Avtonomov DM, Mellacheruvu D, and Nesvizhskii AI (2017). MSFragger: ultrafast and comprehensive peptide identification in mass spectrometry-based proteomics. Nature methods 14, 513– 520. 28394336 PMC5409104
  74. Kordass T, Osen W, and Eichmuller SB (2018). Controlling the Immune Suppressor: Transcription Factors and MicroRNAs Regulating CD73/NT5 E. Frontiers in immunology 9, 813. PMC5915482 29720980
  75. Koschmann C, Zamler D, MacKay A, Robinson D, Wu YM, Doherty R, Marini B, Tran D, Garton H, Muraszko K, (2016). Characterizing and targeting PDGFRA alterations in pediatric high-grade glioma. Oncotarget 7, 65696– 65706. 27582545 PMC5323185
  76. Koscielny G, An P, Carvalho-Silva D, Cham JA, Fumis L, Gasparyan R, Hasan S, Karamanis N, Maguire M, Papa E, (2017). Open Targets: a platform for therapeutic target identification and validation. Nucleic acids research 45, D985– d994. 27899665 PMC5210543
  77. Koseki J, Colvin H, Fukusumi T, Nishida N, Konno M, Kawamoto K, Tsunekuni K, Matsui H, Doki Y, Mori M, (2015). Mathematical analysis predicts imbalanced IDH1/2 expression associates with 2-HG-inactivating β-oxygenation pathway in colorectal cancer. International journal of oncology 46, 1181– 1191. 25586680
  78. Kouidhi S, Ben Ayed F, and Benammar Elgaaied A (2018). Targeting Tumor Metabolism: A New Challenge to Improve Immunotherapy. Frontiers in immunology 9, 353. 29527212 PMC5829092
  79. Kunze A, Congreso MR, Hartmann C, Wallraff-Beck A, Hüttmann K, Bedner P, Requardt R, Seifert G, Redecker C, Willecke K, (2009). Connexin expression by radial glia-like cells is required for neurogenesis in the adult dentate gyrus. Proceedings of the National Academy of Sciences of the United States of America 106, 11336– 11341. 19549869 PMC2700144
  80. Lakka SS, and Rao JS (2008). Antiangiogenic therapy in brain tumors. Expert review of neurotherapeutics 8, 1457– 1473. 18928341 PMC2656359
  81. Lee S, Lee S, Ouellette S, Park WY, Lee EA, and Park PJ (2017). NGSCheckMate: software for validating sample identity in next-generation sequencing studies within and across data types. Nucleic acids research 45, e103. 28369524 PMC5499645
  82. Leone RD, and Emens LA (2018). Targeting adenosine for cancer immunotherapy. Journal for immunotherapy of cancer 6, 57. 29914571 PMC6006764
  83. Li B, and Dewey CN (2011). RSEM: accurate transcript quantification from RNA-Seq data with or without a reference genome. BMC bioinformatics 12, 323. 21816040 PMC3163565
  84. Li J, Davidson D, Martins Souza C, Zhong MC, Wu N, Park M, Muller WJ, and Veillette A (2015). Loss of PTPN12 Stimulates Progression of ErbB2-Dependent Breast Cancer by Enhancing Cell Survival, Migration, and Epithelial-to-Mesenchymal Transition. Molecular and cellular biology 35, 4069– 4082. 26391955 PMC4628068
  85. Li J, He Y, Tan Z, Lu J, Li L, Song X, Shi F, Xie L, You S, Luo X, (2018a). Wild-type IDH2 promotes the Warburg effect and tumor growth through HIF1α in lung cancer. Theranostics 8, 4050– 4061. 30128035 PMC6096397
  86. Li L, Xing R, Cui J, Li W, and Lu Y (2018b). Investigation of frequent somatic mutations of MTND5 gene in gastric cancer cell lines and tissues. Mitochondrial DNA Part B 3, 1002– 1008. 33474396 PMC7800514
  87. Liberzon A, Subramanian A, Pinchback R, Thorvaldsdottir H, Tamayo P, and Mesirov JP (2011). Molecular signatures database (MSigDB) 3.0. Bioinformatics (Oxford, England) 27, 1739– 1740. PMC3106198 21546393
  88. Liluashvili V, Kalayci S, Fluder E, Wilson M, Gabow A, and Gumus ZH (2017). iCAVE: an open source tool for visualizing biomolecular networks in 3D, stereoscopic 3D and immersive 3D. GigaScience 6, 1– 13. PMC5554349 28814063
  89. Lin AP, Demeler B, Minard KI, Anderson SL, Schirf V, Galaleldeen A, and McAlister-Henn L (2011). Construction and analyses of tetrameric forms of yeast NAD+-specific isocitrate dehydrogenase. Biochemistry 50, 230– 239. 21133413 PMC3137751
  90. Lin AP, and McAlister-Henn L (2011). Basis for half-site ligand binding in yeast NAD(+)-specific isocitrate dehydrogenase. Biochemistry 50, 8241– 8250. 21861471 PMC3177981
  91. Litichevskiy L, Peckner R, Abelin JG, Asiedu JK, Creech AL, Davis JF, Davison D, Dunning CM, Egertson JD, Egri S, (2018). A Library of Phosphoproteomic and Chromatin Signatures for Characterizing Cellular Responses to Drug Perturbations. Cell systems 6, 424– 443.e427. 29655704 PMC5951639
  92. Liu H, Sun Y, O’Brien JA, Franco-Barraza J, Qi X, Yuan H, Jin W, Zhang J, Gu C, Zhao Z, (2019). Necroptotic astrocytes contribute to maintaining stemness of disseminated medulloblastoma through CCL2 secretion. Neuro-oncology. PMC7229261 31729527
  93. Liu PK, Kraus E, Wu TA, Strong LC, and Tainsky MA (1996). Analysis of genomic instability in Li-Fraumeni fibroblasts with germline p53 mutations. Oncogene 12, 2267– 2278. 8649766 PMC2719722
  94. Liu WR, Tian MX, Jin L, Yang LX, Ding ZB, Shen YH, Peng YF, Zhou J, Qiu SJ, Dai Z, (2014). High expression of 5-hydroxymethylcytosine and isocitrate dehydrogenase 2 is associated with favorable prognosis after curative resection of hepatocellular carcinoma. Journal of experimental & clinical cancer research: CR 33, 32. 24716838 PMC4081660
  95. Lou Y, Diao L, Cuentas ER, Denning WL, Chen L, Fan YH, Byers LA, Wang J, Papadimitrakopoulou VA, Behrens C, (2016). Epithelial-Mesenchymal Transition Is Associated with a Distinct Tumor Microenvironment Including Elevation of Inflammatory Signals and Multiple Immune Checkpoints in Lung Adenocarcinoma. Clinical cancer research: an official journal of the American Association for Cancer Research 22, 3630– 3642. 26851185 PMC4947453
  96. Louis DN, Perry A, Reifenberger G, von Deimling A, Figarella-Branger D, Cavenee WK, Ohgaki H, Wiestler OD, Kleihues P, and Ellison DW (2016). The 2016 World Health Organization Classification of Tumors of the Central Nervous System: a summary. Acta neuropathologica 131, 803– 820. 27157931
  97. Lun AT, McCarthy DJ, and Marioni JC (2016). A step-by-step workflow for low-level analysis of single-cell RNA-seq data with Bioconductor. F1000Research 5, 2122. 27909575 PMC5112579
  98. Ma QL, Wang JH, Wang YG, Hu C, Mu QT, Yu MX, Wang L, Wang DM, Yang M, Yin XF, (2015). High IDH1 expression is associated with a poor prognosis in cytogenetically normal acute myeloid leukemia. International journal of cancer 137, 1058– 1065. 25523507
  99. Ma W, Kim S, Chowdhury S, Li Z, Yang M, Yoo S, Petralia F, Jacobsen J, Li JJ, Ge X, (2020). DreamAI: algorithm for the imputation of proteomics data. bioRxiv, 2020.2007.2021.214205.
  100. MacDonald TJ, Aguilera D, and Kramm CM (2011). Treatment of high-grade glioma in children and adolescents. Neuro-oncology 13, 1049– 1058. 21784756 PMC3177659
  101. Magupalli VG, Mochida S, Yan J, Jiang X, Westenbroek RE, Nairn AC, Scheuer T, and Catterall WA (2013). Ca2+-independent activation of Ca2+/calmodulin-dependent protein kinase II bound to the C-terminal domain of CaV2.1 calcium channels. The Journal of biological chemistry 288, 4637– 4648. 23255606 PMC3576069
  102. Marie SK, Oba-Shinjo SM, da Silva R, Gimenez M, Nunes Reis G, Tassan JP, Rosa JC, and Uno M (2016). Stathmin involvement in the maternal embryonic leucine zipper kinase pathway in glioblastoma. Proteome science 14, 6. 26973435 PMC4788929
  103. Meel MH, Schaper SA, Kaspers GJL, and Hulleman E (2018). Signaling pathways and mesenchymal transition in pediatric high-grade glioma. Cellular and molecular life sciences: CMLS 75, 871– 887. 29164272 PMC5809527
  104. Merlo LM, Pepper JW, Reid BJ, and Maley CC (2006). Cancer as an evolutionary and ecological process. Nature reviews Cancer 6, 924– 935. 17109012
  105. Mertins P, Mani DR, Ruggles KV, Gillette MA, Clauser KR, Wang P, Wang X, Qiao JW, Cao S, Petralia F, (2016). Proteogenomics connects somatic mutations to signalling in breast cancer. Nature 534, 55– 62. 27251275 PMC5102256
  106. Mertins P, Yang F, Liu T, Mani DR, Petyuk VA, Gillette MA, Clauser KR, Qiao JW, Gritsenko MA, Moore RJ, (2014). Ischemia in tumors induces early and sustained phosphorylation changes in stress kinase pathways but does not affect global protein levels. Molecular & cellular proteomics: MCP 13, 1690– 1704. 24719451 PMC4083109
  107. Moniaux N, Nemos C, Schmied BM, Chauhan SC, Deb S, Morikane K, Choudhury A, Vanlith M, Sutherlin M, Sikela JM, (2006). The human homologue of the RNA polymerase II-associated factor 1 (hPaf1), localized on the 19q13 amplicon, is associated with tumorigenesis. Oncogene 25, 3247– 3257. 16491129
  108. Monroe ME, Shaw JL, Daly DS, Adkins JN, and Smith RD (2008). MASIC: a software program for fast quantitation and flexible visualization of chromatographic profiles from detected LC-MS(/MS) features. Computational biology and chemistry 32, 215– 217. 18440872 PMC2487672
  109. Morrissy AS, Garzia L, Shih DJ, Zuyderduyn S, Huang X, Skowron P, Remke M, Cavalli FM, Ramaswamy V, Lindsay PE, (2016). Divergent clonal selection dominates medulloblastoma at recurrence. Nature 529, 351– 357. 26760213 PMC4936195
  110. Mounir M, Lucchetta M, Silva TC, Olsen C, Bontempi G, Chen X, Noushmehr H, Colaprico A, and Papaleo E (2019). New functionalities in the TCGAbiolinks package for the study and integration of cancer data from GDC and GTEx. PLoS computational biology 15, e1006701. 30835723 PMC6420023
  111. Naus CC, Aftab Q, and Sin WC (2016). Common mechanisms linking connexin43 to neural progenitor cell migration and glioma invasion. Seminars in cell & developmental biology 50, 59– 66. 26706148
  112. Navarrete-Perea J, Yu Q, Gygi SP, and Paulo JA (2018). Streamlined Tandem Mass Tag (SL-TMT) Protocol: An Efficient Strategy for Quantitative (Phospho)proteome Profiling Using Tandem Mass Tag-Synchronous Precursor Selection-MS3. Journal of proteome research 17, 2226– 2236. 29734811 PMC5994137
  113. Nesvizhskii AI, Keller A, Kolker E, and Aebersold R (2003). A statistical model for identifying proteins by tandem mass spectrometry. Analytical chemistry 75, 4646– 4658. 14632076
  114. Ng EL, and Tang BL (2008). Rab GTPases and their roles in brain neurons and glia. Brain research reviews 58, 236– 246. 18485483
  115. Nie W, Xu MD, Gan L, Huang H, Xiu Q, and Li B (2015). Overexpression of stathmin 1 is a poor prognostic biomarker in non-small cell lung cancer. Laboratory investigation; a journal of technical methods and pathology 95, 56– 64. 25384122
  116. Ostrom QT, Gittleman H, Truitt G, Boscia A, Kruchko C, and Barnholtz-Sloan JS (2018). CBTRUS Statistical Report: Primary Brain and Other Central Nervous System Tumors Diagnosed in the United States in 2011–2015. Neuro-oncology 20, iv1– iv86. 30445539 PMC6129949
  117. Panisko EA, and McAlister-Henn L (2001). Subunit interactions of yeast NAD+-specific isocitrate dehydrogenase. The Journal of biological chemistry 276, 1204– 1210. 11042198
  118. Parsons DW, Li M, Zhang X, Jones S, Leary RJ, Lin JC, Boca SM, Carter H, Samayoa J, Bettegowda C, (2011). The genetic landscape of the childhood cancer medulloblastoma. Science (New York, NY) 331, 435– 439. PMC3110744 21163964
  119. Pereira MSL, Klamt F, Thome CC, Worm PV, and de Oliveira DL (2017). Metabotropic glutamate receptors as a new therapeutic target for malignant gliomas. Oncotarget 8, 22279– 22298. 28212543 PMC5400663
  120. Perrot I, Michaud HA, Giraudon-Paoli M, Augier S, Docquier A, Gros L, Courtois R, Dejou C, Jecko D, Becquart O, (2019). Blocking Antibodies Targeting the CD39/CD73 Immunosuppressive Pathway Unleash Immune Responses in Combination Cancer Therapies. Cell reports 27, 2411– 2425.e2419. 31116985
  121. Petralia F, Song WM, Tu Z, and Wang P (2016). New Method for Joint Network Analysis Reveals Common and Different Coexpression Patterns among Genes and Proteins in Breast Cancer. Journal of proteome research 15, 743– 754. 26733076 PMC4782177
  122. Petralia F, Wang L, Peng J, Yan A, Zhu J, and Wang P (2018). A new method for constructing tumor specific gene co-expression networks based on samples with tumor purity heterogeneity. Bioinformatics (Oxford, England) 34, i528– i536. PMC6022554 29949994
  123. Petralia F, Wang P, Yang J, and Tu Z (2015). Integrative random forest for gene regulatory network inference. Bioinformatics (Oxford, England) 31, i197– 205. PMC4542785 26072483
  124. Pilarczyk M, Najafabadi MF, Kouril M, Vasiliauskas J, Niu W, Shamsaei B, Mahi N, Zhang L, Clark N, Ren Y, (2019). Connecting omics signatures of diseases, drugs, and mechanisms of actions with iLINCS. bioRxiv, 826271.
  125. Porro F, Rosato-Siri M, Leone E, Costessi L, Iaconcig A, Tongiorgi E, and Muro AF (2010). beta-adducin (Add2) KO mice show synaptic plasticity, motor coordination and behavioral deficits accompanied by changes in the expression and phosphorylation levels of the alpha- and gamma-adducin subunits. Genes, brain, and behavior 9, 84– 96. 19900187
  126. Pratilas CA, Taylor BS, Ye Q, Viale A, Sander C, Solit DB, and Rosen N (2009). (V600E)BRAF is associated with disabled feedback inhibition of RAF-MEK signaling and elevated transcriptional output of the pathway. Proceedings of the National Academy of Sciences of the United States of America 106, 4519– 4524. 19251651 PMC2649208
  127. Pugh TJ, Weeraratne SD, Archer TC, Pomeranz Krummel DA, Auclair D, Bochicchio J, Carneiro MO, Carter SL, Cibulskis K, Erlich RL, (2012). Medulloblastoma exome sequencing uncovers subtype-specific somatic mutations. Nature 488, 106– 110. 22820256 PMC3413789
  128. Qiao S, Peng R, Yan H, Gao Y, Wang C, Wang S, Zou Y, Xu X, Zhao L, Dong J, (2014). Reduction of phosphorylated synapsin I (ser-553) leads to spatial memory impairment by attenuating GABA release after microwave exposure in Wistar rats. PloS one 9, e95503. 24743689 PMC3990695
  129. Rivero-Hinojosa S, Lau LS, Stampar M, Staal J, Zhang H, Gordish-Dressman H, Northcott PA, Pfister SM, Taylor MD, Brown KJ, (2018). Proteomic analysis of Medulloblastoma reveals functional biology with translational potential. Acta neuropathologica communications 6, 48. 29880060 PMC5992829
  130. Robbins D, Wittwer JA, Codarin S, Circu ML, Aw TY, Huang TT, Van Remmen H, Richardson A, Wang DB, Witt SN, (2012). Isocitrate dehydrogenase 1 is downregulated during early skin tumorigenesis which can be inhibited by overexpression of manganese superoxide dismutase. Cancer science 103, 1429– 1433. 22533343 PMC3407305
  131. Robinson G, Parker M, Kranenburg TA, Lu C, Chen X, Ding L, Phoenix TN, Hedlund E, Wei L, Zhu X, (2012). Novel mutations target distinct subgroups of medulloblastoma. Nature 488, 43– 48. 22722829 PMC3412905
  132. Salomonis N, Dexheimer PJ, Omberg L, Schroll R, Bush S, Huo J, Schriml L, Ho Sui S, Keddache M, Mayhew C, (2016). Integrated Genomic Analysis of Diverse Induced Pluripotent Stem Cells from the Progenitor Cell Biology Consortium. Stem cell reports 7, 110– 125. 27293150 PMC4944587
  133. Santamaria D, Barriere C, Cerqueira A, Hunt S, Tardy C, Newton K, Caceres JF, Dubus P, Malumbres M, and Barbacid M (2007). Cdk1 is sufficient to drive the mammalian cell cycle. Nature 448, 811– 815. 17700700
  134. Savage SR, Shi Z, Liao Y, and Zhang B (2019). Graph Algorithms for Condensing and Consolidating Gene Set Analysis Results. Molecular & cellular proteomics: MCP 18, S141– s152. 31142576 PMC6692773
  135. Schmitt JM, and Stork PJ (2001). Cyclic AMP-mediated inhibition of cell growth requires the small G protein Rap1. Molecular and cellular biology 21, 3671– 3683. 11340161 PMC86997
  136. Schreck KC, Grossman SA, and Pratilas CA (2019). BRAF Mutations and the Utility of RAF and MEK Inhibitors in Primary Brain Tumors. Cancers 11. PMC6769482 31466300
  137. Shah K, and Lahiri DK (2017). A Tale of the Good and Bad: Remodeling of the Microtubule Network in the Brain by Cdk5. Molecular neurobiology 54, 2255– 2268. 26944284 PMC5011452
  138. Shin HJ, Lee S, and Jung HJ (2019). A curcumin derivative hydrazinobenzoylcurcumin suppresses stem-like features of glioblastoma cells by targeting Ca(2+) /calmodulin-dependent protein kinase II. Journal of cellular biochemistry 120, 6741– 6752. 30390339
  139. Shteynberg DD, Deutsch EW, Campbell DS, Hoopmann MR, Kusebauch U, Lee D, Mendoza L, Midha MK, Sun Z, Whetton AD, (2019). PTMProphet: Fast and Accurate Mass Modification Localization for the Trans-Proteomic Pipeline. Journal of proteome research 18, 4262– 4272. 31290668 PMC6898736
  140. Sokolov A, Paull EO, and Stuart JM (2016). ONE-CLASS DETECTION OF CELL STATES IN TUMOR SUBTYPES. Pacific Symposium on Biocomputing Pacific Symposium on Biocomputing 21, 405– 416. 26776204 PMC4856035
  141. Solga AC, Pong WW, Walker J, Wylie T, Magrini V, Apicelli AJ, Griffith M, Griffith OL, Kohsaka S, Wu GF, (2015). RNA-sequencing reveals oligodendrocyte and neuronal transcripts in microglia relevant to central nervous system disease. Glia 63, 531– 548. 25258010 PMC4331255
  142. Song X, Ji J, Gleason KJ, Yang F, Martignetti JA, Chen LS, and Wang P (2019). Insights into Impact of DNA Copy Number Alteration and Methylation on the Proteogenomic Landscape of Human Ovarian Cancer via a Multi-omics Integrative Analysis. Molecular & cellular proteomics: MCP 18, S52– s65. 31227599 PMC6692782
  143. Stathias V, Turner J, Koleti A, Vidovic D, Cooper D, Fazel-Najafabadi M, Pilarczyk M, Terryn R, Chung C, Umeano A, (2019). LINCS Data Portal 2.0: next generation access point for perturbation-response signatures. Nucleic acids research 48, D431– D439. PMC7145650 31701147
  144. Stenson PD, Mort M, Ball EV, Evans K, Hayden M, Heywood S, Hussain M, Phillips AD, and Cooper DN (2017). The Human Gene Mutation Database: towards a comprehensive repository of inherited mutation data for medical research, genetic diagnosis and next-generation sequencing studies. Human genetics 136, 665– 677. 28349240 PMC5429360
  145. Stepulak A, Rola R, Polberg K, and Ikonomidou C (2014). Glutamate and its receptors in cancer. Journal of neural transmission (Vienna, Austria: 1996) 121, 933– 944. PMC4133641 24610491
  146. Sun Q, Guo S, Wang CC, Sun X, Wang D, Xu N, Jin SF, and Li KZ (2015). Cross-talk between TGF-beta/Smad pathway and Wnt/beta-catenin pathway in pathological scar formation. International journal of clinical and experimental pathology 8, 7631– 7639. 26261683 PMC4526017
  147. Talevich E, Shain AH, Botton T, and Bastian BC (2016). CNVkit: Genome-Wide Copy Number Detection and Visualization from Targeted DNA Sequencing. PLoS computational biology 12, e1004873. 27100738 PMC4839673
  148. Tanaka H, Sasayama T, Tanaka K, Nakamizo S, Nishihara M, Mizukawa K, Kohta M, Koyama J, Miyake S, Taniguchi M, (2013). MicroRNA-183 upregulates HIF-1α by targeting isocitrate dehydrogenase 2 (IDH2) in glioma cells. Journal of neuro-oncology 111, 273– 283. 23263745
  149. Tian GY, Zang SF, Wang L, Luo Y, Shi JP, and Lou GQ (2015). Isocitrate Dehydrogenase 2 Suppresses the Invasion of Hepatocellular Carcinoma Cells via Matrix Metalloproteinase 9. Cellular physiology and biochemistry: international journal of experimental cellular physiology, biochemistry, and pharmacology 37, 2405– 2414. 26646705
  150. Tomson BN, and Arndt KM (2013). The many roles of the conserved eukaryotic Paf1 complex in regulating transcription, histone modifications, and disease states. Biochimica et biophysica acta 1829, 116– 126. 22982193 PMC3541448
  151. Turnescu T, Arter J, Reiprich S, Tamm ER, Waisman A, and Wegner M (2018). Sox8 and Sox10 jointly maintain myelin gene expression in oligodendrocytes. Glia 66, 279– 294. 29023979
  152. Tusher VG, Tibshirani R, and Chu G (2001). Significance analysis of microarrays applied to the ionizing radiation response. Proceedings of the National Academy of Sciences of the United States of America 98, 5116– 5121. 11309499 PMC33173
  153. Uchida S, Martel G, Pavlowsky A, Takizawa S, Hevi C, Watanabe Y, Kandel ER, Alarcon JM, and Shumyatsky GP (2014). Learning-induced and stathmin-dependent changes in microtubule stability are critical for memory and disrupted in ageing. Nature communications 5, 4389. PMC4137320 25007915
  154. Venkataramani V, Tanev DI, Strahle C, Studier-Fischer A, Fankhauser L, Kessler T, Korber C, Kardorff M, Ratliff M, Xie R, (2019). Glutamatergic synaptic input to glioma cells drives brain tumour progression. Nature 573, 532– 538. 31534219
  155. Venkatesh HS, Morishita W, Geraghty AC, Silverbush D, Gillespie SM, Arzt M, Tam LT, Espenel C, Ponnuswami A, Ni L, (2019). Electrical and synaptic integration of glioma into neural circuits. Nature 573, 539– 545. 31534222 PMC7038898
  156. Vu NT, Park MA, Shultz JC, Goehe RW, Hoeferlin LA, Shultz MD, Smith SA, Lynch KW, and Chalfant CE (2013). hnRNP U enhances caspase-9 splicing and is modulated by AKT-dependent phosphorylation of hnRNP L. The Journal of biological chemistry 288, 8575– 8584. 23396972 PMC3605676
  157. Wang X, Park J, Susztak K, Zhang NR, and Li M (2019). Bulk tissue cell type deconvolution with multi-subject single-cell expression reference. Nature communications 10, 380. PMC6342984 30670690
  158. Whiteaker JR, Zhao L, Saul R, Kaczmarczyk JA, Schoenherr RM, Moore HD, Jones-Weinert C, Ivey RG, Lin C, Hiltke T, (2018). A Multiplexed Mass Spectrometry-Based Assay for Robust Quantification of Phosphosignaling in Response to DNA Damage. Radiation research 189, 505– 518. 29474155 PMC5939939
  159. Wilkerson MD, and Hayes DN (2010). ConsensusClusterPlus: a class discovery tool with confidence assessments and item tracking. Bioinformatics (Oxford, England) 26, 1572– 1573. PMC2881355 20427518
  160. Wittstatt J, Reiprich S, and Kuspert M (2019). Crazy Little Thing Called Sox-New Insights in Oligodendroglial Sox Protein Function. International journal of molecular sciences 20. PMC6600536 31159496
  161. Yoo S, Huang T, Campbell JD, Lee E, Tu Z, Geraci MW, Powell CA, Schadt EE, Spira A, and Zhu J (2014). MODMatcher: multi-omics data matcher for integrative genomic analysis. PLoS computational biology 10, e1003790. 25122495 PMC4133046
  162. Yoshihara K, Shahmoradgoli M, Martinez E, Vegesna R, Kim H, Torres-Garcia W, Trevino V, Shen H, Laird PW, Levine DA, (2013). Inferring tumour purity and stromal and immune cell admixture from expression data. Nature communications 4, 2612. PMC3826632 24113773
  163. Yu K, Lin CJ, Hatcher A, Lozzi B, Kong K, Huang-Hobbs E, Cheng YT, Beechar VB, Zhu W, Zhang Y, (2020). PIK3CA variants selectively initiate brain hyperactivity during gliomagenesis. Nature 578, 166– 171. 31996845 PMC7577741
  164. Yuan J, Levitin HM, Frattini V, Bush EC, Boyett DM, Samanamud J, Ceccarelli M, Dovas A, Zanazzi G, Canoll P, (2018). Single-cell transcriptome analysis of lineage diversity in high-grade glioma. Genome medicine 10, 57. 30041684 PMC6058390
  165. Zecha J, Satpathy S, Kanashova T, Avanessian SC, Kane MH, Clauser KR, Mertins P, Carr SA, and Kuster B (2019). TMT Labeling for the Masses: A Robust and Cost-efficient, In-solution Labeling Approach. Molecular & cellular proteomics: MCP 18, 1468– 1478. 30967486 PMC6601210
  166. Zhang B, Wang J, Wang X, Zhu J, Liu Q, Shi Z, Chambers MC, Zimmerman LJ, Shaddox KF, Kim S, (2014). Proteogenomic characterization of human colon and rectal cancer. Nature 513, 382– 387. 25043054 PMC4249766
  167. Zhang H, Liu T, Zhang Z, Payne SH, Zhang B, McDermott JE, Zhou JY, Petyuk VA, Chen L, Ray D, (2016). Integrated Proteogenomic Characterization of Human High-Grade Serous Ovarian Cancer. Cell 166, 755– 765. 27372738 PMC4967013
  168. Zhang Y, Lv W, Li Q, Wang Q, Ru Y, Xiong X, Yan F, Pan T, Lin W, and Li X (2019). IDH2 compensates for IDH1 mutation to maintain cell survival under hypoxic conditions in IDH1‑mutant tumor cells. Molecular medicine reports 20, 1893– 1900. 31257503
  169. Zhao L, Whiteaker JR, Pope ME, Kuhn E, Jackson A, Anderson NL, Pearson TW, Carr SA, and Paulovich AG (2011). Quantification of proteins using peptide immunoaffinity enrichment coupled with mass spectrometry. Journal of visualized experiments: JoVE. PMC3197439 21841765

Cited by

Sorted by citations

Authors
Petralia, F., Tignor, N., Reva, B., Koptyra, M., Chowdhury, S., Rykunov, D., Krek, A., Ma, W., Zhu, Y., Ji, J., Calinawan, A., Whiteaker, J. R., Colaprico, A., Stathias, V., Omelchenko, T., Song, X., Raman, P., Guo, Y., Brown, M. A., Ivey, R. G., Szpyt, J., Guha Thakurta, S., Gritsenko, M. A., Weitz, K. K., Lopez, G., Kalayci, S., Gümüş, Z. H., Yoo, S., da Veiga Leprevost, F., Chang, H.-Y., Krug, K., Katsnelson, L., Wang, Y., Kennedy, J. J., Voytovich, U. J., Zhao, L., Gaonkar, K. S., Ennis, B. M., Zhang, B., Baubet, V., Tauhid, L., Lilly, J. V., Mason, J. L., Farrow, B., Young, N., Leary, S., Moon, J., Petyuk, V. A., Nazarian, J., Adappa, N. D., Palmer, J. N., Lober, R. M., Rivero-Hinojosa, S., Wang, L.-B., Wang, J. M., Broberg, M., Chu, R. K., Moore, R. J., Monroe, M. E., Zhao, R., Smith, R. D., Zhu, J., Robles, A. I., Mesri, M., Boja, E., Hiltke, T., Rodriguez, H., Zhang, B., Schadt, E. E., Mani, D. R., Ding, L., Iavarone, A., Wiznerowicz, M., Schürer, S., Chen, X. S., Heath, A. P., Rokita, J. L., Nesvizhskii, A. I., Fenyö, D., Rodland, K. D., Liu, T., Gygi, S. P., Paulovich, A. G., Resnick, A. C., Storm, P. B., Rood, B. R., Wang, P., Francis, A., Morgan, A. M., Waanders, A. J., Viaene, A. N., Buccoliero, A. M., Chinnaiyan, A. M., Leonard, C. A., Kline, C. N., Caporalini, C., Kinsinger, C. R., Li, C., Kram, D. E., Hanson, D., Appert, E., Kawaler, E. A., Raabe, E. H., Jackson, E. M., Greenfield, J. P., Stone, G. S., Getz, G., Grant, G., Teo, G. C., Pollack, I. F., Cain, J. E., Foster, J. B., Phillips, J. J., Palma, J. E., Ketchum, K. A., Ruggles, K. V., Blumenberg, L., Cornwell, M., Sarmady, M., Domagalski, M. J., Cieślik, M. P., Santi, M., Li, M. M., Ellis, M. J., Wyczalkowski, M. A., Connors, M., Scagnet, M., Gupta, N., Edwards, N. J., Vitanza, N. A., Vaske, O. M., Becher, O., McGarvey, P. B., Firestein, R., Mueller, S., Winebrake, S. G., Dhanasekaran, S. M., Cai, S., Partap, S., Patton, T., Le, T., Lorentzen, T. D., Liu, W., & Bocik, W. E.
Affiliations
  • Icahn School of Medicine at Mount Sinai (US)
  • Children's Hospital of Philadelphia (US)
  • Tisch Cancer Institute (US)
  • Fred Hutch Cancer Center (US)
  • University of Miami (US)
  • Memorial Sloan Kettering Cancer Center (US)
  • Harvard University (US)
  • Pacific Northwest National Laboratory (US)
  • University of Michigan (US)
  • Broad Institute (US)
  • New York University (US)
  • Seattle Children's Hospital (US)
  • Children's National (US)
  • University of Pennsylvania (US)
  • Dayton Children's Hospital (US)
  • Washington University in St. Louis (US)
  • National Institutes of Health (US)
  • Columbia University Irving Medical Center (US)
  • Poznan University of Medical Sciences (PL)
Corresponding author
  • Resnick, Adam C.
  • Storm, Phillip B.
  • Rood, Brian R.
  • Wang, Pei
ORCID
Venue
Cell
Publisher
Elsevier BV
Published
2020-12
Volume
183
Issue
7
Pages
1962-1985.e31
ISSN
0092-8674 (ISSN-L)
DOI
10.1016/j.cell.2020.10.044
PMC
PMC8143193
OpenAlex
W3108158555
Cited by
317
References
23
Citations by year
2026: 34 · 2025: 56 · 2024: 56 · 2023: 69 · 2022: 60 · 2021: 41
FWCI
22.13
Type
journal article
Language
en
Open access
Licence
Locations
  • Cell (publishedVersion, cc-by-nc-nd)
  • PubMed (publishedVersion)
  • Zurich Open Repository and Archive (University of Zurich) (acceptedVersion, cc-by-nc-nd)
  • PubMed Central (acceptedVersion)
  • Digital Commons@Becker (Washington University School of Medicine) (submittedVersion)
  • eScholarship (California Digital Library) (submittedVersion, cc-by-nc-nd)
  • OSTI OAI (U.S. Department of Energy Office of Scientific and Technical Information) (submittedVersion)
  • Zurich Open Repository and Archive (University of Zurich) (submittedVersion, cc-by-nc-nd)
  • Zurich Open Repository and Archive (University of Zurich)
Funders
  • National Institutes of Health
  • U.S. Department of Energy
Topics
  • Health Sciences › Medicine › Genetics › Glioma Diagnosis and Treatment
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
  • Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Chromatin Remodeling and Cancer
Keywords
pediatric brain tumors, proteogenomics, low-grade glioma, ependymoma, high-grade glioma, medulloblastoma, ganglioglioma, craniopharyngioma, atypical teratoid/rhabdoid tumor, tumor microenvironment, immune landscape, somatic mutations, copy number variation, kinase-substrate interactions, co-expression network, tumor biology, treatment selection
MeSH terms
Proteogenomics, Brain Neoplasms, Child, Glioma, Humans, Mutation, Neoplasm Recurrence, Local, Phosphoproteins, Phosphorylation, RNA, Messenger, Genome, Human, Gene Expression Regulation, Neoplastic, Lymphocytes, Tumor-Infiltrating, Gene Regulatory Networks, DNA Copy Number Variations, Transcriptome, Neoplasm Grading

About these checks

Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.

Statistics and arithmetic are recomputed, not judged.

Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.

What counts as a claim ›How we measure confidence ›How we check this ›

Are you an author, or do you see a problem with this page? Request a review