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Journal of Hematology & Oncology
Published in: Journal of Hematology & Oncology 1/2022

01-12-2022 | Bladder Carcinoma | Research

Integrated proteogenomic characterization of urothelial carcinoma of the bladder

Authors: Ning Xu, Zhenmei Yao, Guoguo Shang, Dingwei Ye, Haixing Wang, Hailiang Zhang, Yuanyuan Qu, Fujiang Xu, Yunzhi Wang, Zhaoyu Qin, Jiajun Zhu, Fan Zhang, Jinwen Feng, Sha Tian, Yang Liu, Jianyuan Zhao, Jun Hou, Jianming Guo, Yingyong Hou, Chen Ding

Published in: Journal of Hematology & Oncology | Issue 1/2022

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Abstract

Background

Urothelial carcinoma (UC) is the most common pathological type of bladder cancer, a malignant tumor. However, an integrated multi-omics analysis of the Chinese UC patient cohort is lacking.

Methods

We performed an integrated multi-omics analysis, including whole-exome sequencing, RNA-seq, proteomic, and phosphoproteomic analysis of 116 Chinese UC patients, comprising 45 non-muscle-invasive bladder cancer patients (NMIBCs) and 71 muscle-invasive bladder cancer patients (MIBCs).

Result

Proteogenomic integration analysis indicated that SND1 and CDK5 amplifications on chromosome 7q were associated with the activation of STAT3, which was relevant to tumor proliferation. Chromosome 5p gain in NMIBC patients was a high-risk factor, through modulating actin cytoskeleton implicating in tumor cells invasion. Phosphoproteomic analysis of tumors and morphologically normal human urothelium produced UC-associated activated kinases, including CDK1 and PRKDC. Proteomic analysis identified three groups, U-I, U-II, and U-III, reflecting distinct clinical prognosis and molecular signatures. Immune subtypes of UC tumors revealed a complex immune landscape and suggested the amplification of TRAF2 related to the increased expression of PD-L1. Additionally, increased GARS, related to subtype U-II, was validated to promote pentose phosphate pathway by inhibiting activities of PGK1 and PKM2.

Conclusions

This study provides a valuable resource for researchers and clinicians to further identify molecular pathogenesis and therapeutic opportunities in urothelial carcinoma of the bladder.
Appendix
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Literature
1.
Sung H, Ferlay J, Siegel RL, Laversanne M, Soerjomataram I, Jemal A, Bray F. Global Cancer Statistics 2020: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin. 2021;71(3):209–49.CrossRefPubMed
2.
Flaig TW, Spiess PE, Agarwal N, Bangs R, Boorjian SA, Buyyounouski MK, Chang S, Downs TM, Efstathiou JA, Friedlander T, et al. Bladder cancer, Version 3.2020, NCCN Clinical Practice Guidelines in Oncology. J Natl Compr Canc Netw. 2020;18(3):329–54.PubMedCrossRef
3.
Kamat AM, Hahn NM, Efstathiou JA, Lerner SP, Malmström PU, Choi W, Guo CC, Lotan Y, Kassouf W. Bladder cancer. Lancet. 2016;388(10061):2796–810.PubMedCrossRef
4.
5.
Ghandour R, Singla N, Lotan Y. Treatment options and outcomes in nonmetastatic muscle invasive bladder cancer. Trends Cancer. 2019;5(7):426–39.PubMedCrossRef
6.
7.
Hedegaard J, Lamy P, Nordentoft I, Algaba F, Høyer S, Ulhøi BP, Vang S, Reinert T, Hermann GG, Mogensen K, et al. Comprehensive transcriptional analysis of early-stage urothelial carcinoma. Cancer Cell. 2016;30(1):27–42.PubMedCrossRef
8.
Robertson AG, Kim J, Al-Ahmadie H, Bellmunt J, Guo G, Cherniack AD, Hinoue T, Laird PW, Hoadley KA, Akbani R, et al. Comprehensive molecular characterization of muscle-invasive bladder cancer. Cell. 2017;171(3):540–56e525.
9.
Sjödahl G, Lauss M, Lövgren K, Chebil G, Gudjonsson S, Veerla S, Patschan O, Aine M, Fernö M, Ringnér M, et al. A molecular taxonomy for urothelial carcinoma. Clin Cancer Res. 2012;18(12):3377–86.PubMedCrossRef
10.
Choi W, Porten S, Kim S, Willis D, Plimack ER, Hoffman-Censits J, Roth B, Cheng T, Tran M, Lee IL, et al. Identification of distinct basal and luminal subtypes of muscle-invasive bladder cancer with different sensitivities to frontline chemotherapy. Cancer Cell. 2014;25(2):152–65.PubMedPubMedCentralCrossRef
11.
Damrauer JS, Hoadley KA, Chism DD, Fan C, Tiganelli CJ, Wobker SE, Yeh JJ, Milowsky MI, Iyer G, Parker JS, et al. Intrinsic subtypes of high-grade bladder cancer reflect the hallmarks of breast cancer biology. Proc Natl Acad Sci USA. 2014;111(8):3110–5.PubMedPubMedCentralCrossRef
12.
Robertson AG, Kim J, Al-Ahmadie H, Bellmunt J, Guo G, Cherniack AD, Hinoue T, Laird PW, Hoadley KA, Akbani R, et al. Comprehensive molecular characterization of muscle-invasive bladder cancer. Cell. 2018;174(4):1033.PubMedCrossRef
13.
14.
Fessas P, Lee H, Ikemizu S, Janowitz T. A molecular and preclinical comparison of the PD-1-targeted T-cell checkpoint inhibitors nivolumab and pembrolizumab. Semin Oncol. 2017;44(2):136–40.PubMedPubMedCentralCrossRef
15.
Audenet F, Attalla K, Sfakianos JP. The evolution of bladder cancer genomics: What have we learned and how can we use it? Urol Oncol. 2018;36(7):313–20.PubMedCrossRef
16.
17.
Bhullar KS, Lagaron NO, McGowan EM, Parmar I, Jha A, Hubbard BP, Rupasinghe HPV. Kinase-targeted cancer therapies: progress, challenges and future directions. Mol Cancer. 2018;17(1):48.PubMedPubMedCentralCrossRef
18.
Wu X, Xing X, Dowlut D, Zeng Y, Liu J, Liu X. Integrating phosphoproteomics into kinase-targeted cancer therapies in precision medicine. J Proteomics. 2019;191:68–79.PubMedCrossRef
19.
Li R, Du Y, Chen Z, Xu D, Lin T, Jin S, Wang G, Liu Z, Lu M, Chen X, et al. Macroscopic somatic clonal expansion in morphologically normal human urothelium. Science. 2020;370(6512):82–9.PubMedCrossRef
20.
Feng J, Ding C, Qiu N, Ni X, Zhan D, Liu W, Xia X, Li P, Lu B, Zhao Q, et al. Firmiana: towards a one-stop proteomic cloud platform for data processing and analysis. Nat Biotechnol. 2017;35(5):409–12.PubMedCrossRef
21.
Ge S, Xia X, Ding C, Zhen B, Zhou Q, Feng J, Yuan J, Chen R, Li Y, Ge Z, et al. A proteomic landscape of diffuse-type gastric cancer. Nat Commun. 2018;9(1):1012.PubMedPubMedCentralCrossRef
22.
Clark DJ, Dhanasekaran SM, Petralia F, Pan J, Song X, Hu Y, da Veiga Leprevost F, Reva B, Lih TM, Chang HY, et al. Integrated proteogenomic characterization of clear cell renal cell carcinoma. Cell. 2019;179(4):964–83e931.
23.
Thomas SN, Friedrich B, Schnaubelt M, Chan DW, Zhang H, Aebersold R. Orthogonal proteomic platforms and their implications for the stable classification of high-grade serous ovarian cancer subtypes. Science. 2020;23(6):10–1079.
24.
Guo G, Sun X, Chen C, Wu S, Huang P, Li Z, Dean M, Huang Y, Jia W, Zhou Q, et al. Whole-genome and whole-exome sequencing of bladder cancer identifies frequent alterations in genes involved in sister chromatid cohesion and segregation. Nat Genet. 2013;45(12):1459–63.PubMedPubMedCentralCrossRef
25.
Mhawech-Fauceglia P, Cheney RT, Schwaller J. Genetic alterations in urothelial bladder carcinoma: an updated review. Cancer. 2006;106(6):1205–16.PubMedCrossRef
26.
27.
Gupta S, Hau AM, Beach JR, Harwalker J, Mantuano E, Gonias SL, Egelhoff TT, Hansel DE. Mammalian target of rapamycin complex 2 (mTORC2) is a critical determinant of bladder cancer invasion. PLoS ONE. 2013;8(11): e81081.PubMedPubMedCentralCrossRef
28.
Ma K, Qiu L, Mrasek K, Zhang J, Liehr T, Quintana LG, Li Z. Common fragile sites: genomic hotspots of DNA damage and carcinogenesis. Int J Mol Sci. 2012;13(9):11974–99.PubMedPubMedCentralCrossRef
29.
Elbarbary RA, Miyoshi K, Myers JR, Du P, Ashton JM, Tian B, Maquat LE. Tudor-SN-mediated endonucleolytic decay of human cell microRNAs promotes G1/S phase transition. Science. 2017;356(6340):859–62.PubMedPubMedCentralCrossRef
30.
Yang J, Aittomäki S, Pesu M, Carter K, Saarinen J, Kalkkinen N, Kieff E, Silvennoinen O. Identification of p100 as a coactivator for STAT6 that bridges STAT6 with RNA polymerase II. Embo j. 2002;21(18):4950–8.PubMedPubMedCentralCrossRef
31.
Su C, Zhang C, Tecle A, Fu X, He J, Song J, Zhang W, Sun X, Ren Y, Silvennoinen O, et al. Tudor staphylococcal nuclease (Tudor-SN), a novel regulator facilitating G1/S phase transition, acting as a co-activator of E2F–1 in cell cycle regulation. J Biol Chem. 2015;290(11):7208–20.PubMedPubMedCentralCrossRef
32.
Arretxe E, Armengol S, Mula S, Chico Y, Ochoa B, Martinez MJ. Profiling of promoter occupancy by the SND1 transcriptional coactivator identifies downstream glycerolipid metabolic genes involved in TNFalpha response in human hepatoma cells. Nucleic Acids Res. 2015;43(22):10673–88.PubMedPubMedCentralCrossRef
33.
Fu AK, Fu WY, Ng AK, Chien WW, Ng YP, Wang JH, Ip NY. Cyclin-dependent kinase 5 phosphorylates signal transducer and activator of transcription 3 and regulates its transcriptional activity. Proc Natl Acad Sci USA. 2004;101(17):6728–33.PubMedPubMedCentralCrossRef
34.
Chen CL, Cen L, Kohout J, Hutzen B, Chan C, Hsieh FC, Loy A, Huang V, Cheng G, Lin J. Signal transducer and activator of transcription 3 activation is associated with bladder cancer cell growth and survival. Mol Cancer. 2008;7:78.PubMedPubMedCentralCrossRef
35.
Zhou Y, Lih TM, Pan J, Höti N, Dong M, Cao L, Hu Y, Cho KC, Chen SY, Eguez RV, et al. Proteomic signatures of 16 major types of human cancer reveal universal and cancer-type-specific proteins for the identification of potential therapeutic targets. J Hematol Oncol. 2020;13(1):170.PubMedPubMedCentralCrossRef
36.
37.
Gao Q, Zhu H, Dong L, Shi W, Chen R, Song Z, Huang C, Li J, Dong X, Zhou Y, et al. Integrated proteogenomic characterization of HBV-related hepatocellular carcinoma. Cell. 2019;179(2):561–77e522.
38.
Huang C, Chen L, Savage SR, Eguez RV, Dou Y, Li Y, da Veiga Leprevost F, Jaehnig EJ, Lei JT, Wen B, et al. Proteogenomic insights into the biology and treatment of HPV-negative head and neck squamous cell carcinoma. Cancer Cell. 2021;39(3):361–79e316.
39.
Barretina J, Caponigro G, Stransky N, Venkatesan K, Margolin AA, Kim S, Wilson CJ, Lehar J, Kryukov GV, Sonkin D, et al. The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature. 2012;483(7391):603–7.PubMedPubMedCentralCrossRef
40.
McDonald ER, 3rd, de Weck A, Schlabach MR, Billy E, Mavrakis KJ, Hoffman GR, Belur D, Castelletti D, Frias E, Gampa K, et al. Project DRIVE: a compendium of cancer dependencies and synthetic lethal relationships uncovered by large-scale, deep RNAi screening. Cell. 2017;170(3):577–92e510.
41.
Humphrey PA, Moch H, Cubilla AL, Ulbright TM, Reuter VE. The 2016 WHO classification of tumours of the urinary system and male genital organs-part B: prostate and bladder tumours. Eur Urol. 2016;70(1):106–19.PubMedCrossRef
42.
Nassar AH, Umeton R, Kim J, Lundgren K, Harshman L, Van Allen EM, Preston M, Dong F, Bellmunt J, Mouw KW, et al. Mutational analysis of 472 urothelial carcinoma across grades and anatomic sites. Clin Cancer Res. 2019;25(8):2458–70.PubMedCrossRef
43.
Valdivia A, Goicoechea SM, Awadia S, Zinn A, Garcia-Mata R. Regulation of circular dorsal ruffles, macropinocytosis, and cell migration by RhoG and its exchange factor. Trio Mol Biol Cell. 2017;28(13):1768–81.PubMedCrossRef
44.
Bellanger JM, Astier C, Sardet C, Ohta Y, Stossel TP, Debant A. The Rac1- and RhoG-specific GEF domain of Trio targets filamin to remodel cytoskeletal actin. Nat Cell Biol. 2000;2(12):888–92.PubMedCrossRef
45.
Blangy A, Vignal E, Schmidt S, Debant A, Gauthier-Rouvière C, Fort P. TrioGEF1 controls Rac- and Cdc42-dependent cell structures through the direct activation of rhoG. J Cell Sci. 2000;113(Pt 4):729–39.PubMedCrossRef
46.
47.
Green TP, Fennell M, Whittaker R, Curwen J, Jacobs V, Allen J, Logie A, Hargreaves J, Hickinson DM, Wilkinson RW, et al. Preclinical anticancer activity of the potent, oral Src inhibitor AZD0530. Mol Oncol. 2009;3(3):248–61.PubMedPubMedCentralCrossRef
48.
Rose TL, Chism DD, Alva AS, Deal AM, Maygarden SJ, Whang YE, Kardos J, Drier A, Basch E, Godley PA, et al. Phase II trial of palbociclib in patients with metastatic urothelial cancer after failure of first-line chemotherapy. Br J Cancer. 2018;119(7):801–7.PubMedPubMedCentralCrossRef
49.
Sathe A, Koshy N, Schmid SC, Thalgott M, Schwarzenbock SM, Krause BJ, Holm PS, Gschwend JE, Retz M, Nawroth R. CDK4/6 inhibition controls proliferation of bladder cancer and transcription of RB1. J Urol. 2016;195(3):771–9.PubMedCrossRef
50.
King MA, Ganley IG, Flemington V. Inhibition of cholesterol metabolism underlies synergy between mTOR pathway inhibition and chloroquine in bladder cancer cells. Oncogene. 2016;35(34):4518–28.PubMedPubMedCentralCrossRef
51.
Yoshihara K, Shahmoradgoli M, Martinez E, Vegesna R, Kim H, Torres-Garcia W, Trevino V, Shen H, Laird PW, Levine DA, et al. Inferring tumour purity and stromal and immune cell admixture from expression data. Nat Commun. 2013;4:2612.PubMedCrossRef
52.
Owen KL, Brockwell NK, Parker BS. JAK-STAT signaling: a double-edged sword of immune regulation and cancer progression. Cancers. 2019;11(12):66.CrossRef
53.
54.
55.
Villanueva JE, Malle EK, Gardam S, Silveira PA, Zammit NW, Walters SN, Brink R, Grey ST. TRAF2 regulates peripheral CD8(+) T-cell and NKT-cell homeostasis by modulating sensitivity to IL-15. Eur J Immunol. 2015;45(6):1820–31.PubMedCrossRef
56.
Amin MB. Histological variants of urothelial carcinoma: diagnostic, therapeutic and prognostic implications. Mod Pathol. 2009;22(Suppl 2):S96–118.PubMedCrossRef
57.
Comperat E, Roupret M, Yaxley J, Reynolds J, Varinot J, Ouzaid I, Cussenot O, Samaratunga H. Micropapillary urothelial carcinoma of the urinary bladder: a clinicopathological analysis of 72 cases. Pathology. 2010;42(7):650–4.PubMedCrossRef
58.
Kamat AM, Dinney CP, Gee JR, Grossman HB, Siefker-Radtke AO, Tamboli P, Detry MA, Robinson TL, Pisters LL. Micropapillary bladder cancer: a review of the University of Texas M. D. Anderson Cancer Center experience with 100 consecutive patients. Cancer. 2007; 110(1):62–7.
59.
Malumbres M, Barbacid M. Cell cycle, CDKs and cancer: a changing paradigm. Nat Rev Cancer. 2009;9(3):153–66.PubMedCrossRef
60.
He XD, Gong W, Zhang JN, Nie J, Yao CF, Guo FS, Lin Y, Wu XH, Li F, Li J, et al. Sensing and transmitting intracellular amino acid signals through reversible lysine aminoacylations. Cell Metab. 2018;27(1):151–66e156.
61.
62.
Malats N, Real FX. Epidemiology of bladder cancer. Hematol Oncol Clin N Am. 2015;29(2):177–89.CrossRef
63.
Stroggilos R, Mokou M, Latosinska A, Makridakis M, Lygirou V, Mavrogeorgis E, Drekolias D, Frantzi M, Mullen W, Fragkoulis C, et al. Proteome-based classification of nonmuscle invasive bladder cancer. Int J Cancer. 2020;146(1):281–94.PubMedCrossRef
64.
Chan KS, Espinosa I, Chao M, Wong D, Ailles L, Diehn M, Gill H, Presti J Jr, Chang HY, van de Rijn M, et al. Identification, molecular characterization, clinical prognosis, and therapeutic targeting of human bladder tumor-initiating cells. Proc Natl Acad Sci USA. 2009;106(33):14016–21.PubMedPubMedCentralCrossRef
65.
Chen Y, Wang Y, Luo H, Meng X, Zhu W, Wang D, Zeng H, Zhang H. The frequency and inter-relationship of PD-L1 expression and tumour mutational burden across multiple types of advanced solid tumours in China. Exp Hematol Oncol. 2020;9:17.PubMedPubMedCentralCrossRef
66.
67.
Etherington GJ, Ramirez-Gonzalez RH, MacLean D. bio-samtools 2: a package for analysis and visualization of sequence and alignment data with SAMtools in Ruby. Bioinformatics. 2015;31(15):2565–7.PubMedCrossRef
68.
Cibulskis K, Lawrence MS, Carter SL, Sivachenko A, Jaffe D, Sougnez C, Gabriel S, Meyerson M, Lander ES, Getz G. Sensitive detection of somatic point mutations in impure and heterogeneous cancer samples. Nat Biotechnol. 2013;31(3):213–9.PubMedPubMedCentralCrossRef
69.
Saunders CT, Wong WS, Swamy S, Becq J, Murray LJ, Cheetham RK. Strelka: accurate somatic small-variant calling from sequenced tumor-normal sample pairs. Bioinformatics. 2012;28(14):1811–7.PubMedCrossRef
70.
Mermel CH, Schumacher SE, Hill B, Meyerson ML, Beroukhim R, Getz G. GISTIC2.0 facilitates sensitive and confident localization of the targets of focal somatic copy-number alteration in human cancers. Genome Biol. 2011;12(4):R41.PubMedPubMedCentralCrossRef
71.
Vasaikar S, Huang C, Wang X, Petyuk VA, Savage SR, Wen B, Dou Y, Zhang Y, Shi Z, Arshad OA, et al. Proteogenomic analysis of human colon cancer reveals new therapeutic opportunities. Cell. 2019;177(4):1035–49e1019.
72.
Lawrence MS, Stojanov P, Polak P, Kryukov GV, Cibulskis K, Sivachenko A, Carter SL, Stewart C, Mermel CH, Roberts SA, et al. Mutational heterogeneity in cancer and the search for new cancer-associated genes. Nature. 2013;499(7457):214–8.PubMedPubMedCentralCrossRef
73.
Robertson AG, Kim J, Al-Ahmadie H, Bellmunt J, Guo G, Cherniack AD, Hinoue T, Laird PW, Hoadley KA, Akbani R. Comprehensive molecular characterization of muscle-invasive bladder cancer. Cell. 2017;171(3):540–56.e525.
74.
Cerami E, Gao J, Dogrusoz U, Gross BE, Sumer SO, Aksoy BA, Jacobsen A, Byrne CJ, Heuer ML, Larsson E, et al. The cBio cancer genomics portal: an open platform for exploring multidimensional cancer genomics data. Cancer Discov. 2012;2(5):401–4.PubMedCrossRef
75.
Wang S, Tao Z, Wu T, Liu XS. Sigflow: an automated and comprehensive pipeline for cancer genome mutational signature analysis. Bioinformatics. 2021;37(11):1590–2.PubMedCrossRef
76.
Rosenthal R, McGranahan N, Herrero J, Taylor BS, Swanton C. DeconstructSigs: delineating mutational processes in single tumors distinguishes DNA repair deficiencies and patterns of carcinoma evolution. Genome Biol. 2016;17(1):1–11.CrossRef
77.
Wang K, Li M, Hakonarson H. ANNOVAR: functional annotation of genetic variants from high-throughput sequencing data. Nucleic Acids Res. 2010;38(16): e164.PubMedPubMedCentralCrossRef
78.
Chalmers ZR, Connelly CF, Fabrizio D, Gay L, Ali SM, Ennis R, Schrock A, Campbell B, Shlien A, Chmielecki J, et al. Analysis of 100,000 human cancer genomes reveals the landscape of tumor mutational burden. Genome Med. 2017;9(1):34.PubMedPubMedCentralCrossRef
79.
Gao Q, Zhu H, Dong L, Shi W, Chen R, Song Z, Huang C, Li J, Dong X, Zhou Y, et al. Integrated proteogenomic characterization of HBV-related hepatocellular carcinoma. Cell. 2019;179(5):1240.PubMedCrossRef
80.
Tyanova S, Temu T, Cox J. The MaxQuant computational platform for mass spectrometry-based shotgun proteomics. Nat Protoc. 2016;11(12):2301–19.PubMedCrossRef
81.
da Huang W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc. 2009;4(1):44–57.CrossRef
82.
83.
Liberzon A, Birger C, Thorvaldsdóttir H, Ghandi M, Mesirov JP, Tamayo P. The Molecular Signatures Database (MSigDB) hallmark gene set collection. Cell Syst. 2015;1(6):417–25.PubMedPubMedCentralCrossRef
84.
Croft D, Mundo AF, Haw R, Milacic M, Weiser J, Wu G, Caudy M, Garapati P, Gillespie M, Kamdar MR, et al. The Reactome pathway knowledgebase. Nucleic Acids Res. 2014;42(Database issue):D472–77.
85.
Ashburner M, Ball CA, Blake JA, Botstein D, Butler H, Cherry JM, Davis AP, Dolinski K, Dwight SS, Eppig JT, et al. Gene ontology: tool for the unification of biology. The Gene Ontology Consortium. Nat Genet. 2000;25(1):25–9.PubMedPubMedCentralCrossRef
86.
Barbie DA, Tamayo P, Boehm JS, Kim SY, Moody SE, Dunn IF, Schinzel AC, Sandy P, Meylan E, Scholl C, et al. Systematic RNA interference reveals that oncogenic KRAS-driven cancers require TBK1. Nature. 2009;462(7269):108–12.PubMedPubMedCentralCrossRef
87.
Hanzelmann S, Castelo R, Guinney J. GSVA: gene set variation analysis for microarray and RNA-seq data. BMC Bioinform. 2013;14:7.CrossRef
88.
A user's guide to the encyclopedia of DNA elements (ENCODE). PLoS Biol. 2011;9(4):e1001046.
89.
Perkins DN, Pappin DJ, Creasy DM, Cottrell JS. Probability-based protein identification by searching sequence databases using mass spectrometry data. Electrophoresis. 1999;20(18):3551–67.PubMedCrossRef
90.
Käll L, Canterbury JD, Weston J, Noble WS, MacCoss MJ. Semi-supervised learning for peptide identification from shotgun proteomics datasets. Nat Methods. 2007;4(11):923–5.PubMedCrossRef
91.
Taus T, Köcher T, Pichler P, Paschke C, Schmidt A, Henrich C, Mechtler K. Universal and confident phosphorylation site localization using phosphoRS. J Proteome Res. 2011;10(12):5354–62.PubMedCrossRef
92.
Casado P, Alcolea MP, Iorio F, Rodríguez-Prados JC, Vanhaesebroeck B, Saez-Rodriguez J, Joel S, Cutillas PR. Phosphoproteomics data classify hematological cancer cell lines according to tumor type and sensitivity to kinase inhibitors. Genome Biol. 2013;14(4):R37.PubMedPubMedCentralCrossRef
93.
Hornbeck PV, Zhang B, Murray B, Kornhauser JM, Latham V, Skrzypek E. PhosphoSitePlus, 2014: mutations, PTMs and recalibrations. Nucleic Acids Res. 2015;43(Database issue):D512–20.
94.
Horn H, Schoof EM, Kim J, Robin X, Miller ML, Diella F, Palma A, Cesareni G, Jensen LJ, Linding R. KinomeXplorer: an integrated platform for kinome biology studies. Nat Methods. 2014;11(6):603–4.PubMedCrossRef
95.
Wilkerson MD, Hayes DN. ConsensusClusterPlus: a class discovery tool with confidence assessments and item tracking. Bioinformatics. 2010;26(12):1572–3.PubMedPubMedCentralCrossRef
96.
Monti S, Tamayo P, Mesirov J, Golub T. Consensus clustering: a resampling-based method for class discovery and visualization of gene expression microarray data. Mach Learn. 2003;52(1):91–118.CrossRef
97.
Langfelder P, Horvath S. WGCNA: an R package for weighted correlation network analysis. BMC Bioinform. 2008;9:559.CrossRef
98.
Horvath S. Weighted network analysis: applications in genomics and systems biology. Berlin: Springer; 2011.CrossRef
99.
Seckinger A, Meissner T, Moreaux J, Depeweg D, Hillengass J, Hose K, Rème T, Rösen-Wolff A, Jauch A, Schnettler R, et al. Clinical and prognostic role of annexin A2 in multiple myeloma. Blood. 2012;120(5):1087–94.PubMedCrossRef
100.
Zhang B, Wang J, Wang X, Zhu J, Liu Q, Shi Z, Chambers MC, Zimmerman LJ, Shaddox KF, Kim S, et al. Proteogenomic characterization of human colon and rectal cancer. Nature. 2014;513(7518):382–7.PubMedPubMedCentralCrossRef
101.
Bailey MH, Tokheim C, Porta-Pardo E, Sengupta S, Bertrand D, Weerasinghe A, Colaprico A, Wendl MC, Kim J, Reardon B, et al. Comprehensive characterization of cancer driver genes and mutations. Cell. 2018;173(2):371-385.e318.PubMedPubMedCentralCrossRef
102.
Mertins P, Mani DR, Ruggles KV, Gillette MA, Clauser KR, Wang P, Wang X, Qiao JW, Cao S, Petralia F, et al. Proteogenomics connects somatic mutations to signalling in breast cancer. Nature. 2016;534(7605):55–62.PubMedPubMedCentralCrossRef
103.
104.
Metadata
Title
Integrated proteogenomic characterization of urothelial carcinoma of the bladder
Authors
Ning Xu
Zhenmei Yao
Guoguo Shang
Dingwei Ye
Haixing Wang
Hailiang Zhang
Yuanyuan Qu
Fujiang Xu
Yunzhi Wang
Zhaoyu Qin
Jiajun Zhu
Fan Zhang
Jinwen Feng
Sha Tian
Yang Liu
Jianyuan Zhao
Jun Hou
Jianming Guo
Yingyong Hou
Chen Ding
Publication date
01-12-2022
Publisher
BioMed Central
Published in
Journal of Hematology & Oncology / Issue 1/2022
Electronic ISSN: 1756-8722
DOI
https://doi.org/10.1186/s13045-022-01291-7

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