Identification of β‑catenin target genes in colorectal cancer by interrogating gene fitness screening data
- Authors:
- Haomin Zhao
- Liang He
- Dexin Yin
- Bin Song
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Affiliations: Department of Vascular Surgery, China‑Japan Union Hospital of Jilin University, Changchun, Jilin 130033, P.R. China, Department of Gastrointestinal Surgery, First Hospital of Jilin University, Changchun, Jilin 130033, P.R. China, Department of Gastrointestinal Surgery, China‑Japan Union Hospital of Jilin University, Changchun, Jilin 130033, P.R. China - Published online on: August 6, 2019 https://doi.org/10.3892/ol.2019.10724
- Pages: 3769-3777
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Copyright: © Zhao et al. This is an open access article distributed under the terms of Creative Commons Attribution License.
This article is mentioned in:
Abstract
Novellasdemunt L, Antas P and Li VS: Targeting Wnt signaling in colorectal cancer. A review in the theme: Cell signaling: Proteins, pathways and mechanisms. Am J Physiol Cell Physiol. 309:C511–C521. 2015. View Article : Google Scholar : PubMed/NCBI | |
Barker N and Clevers H: Mining the Wnt pathway for cancer therapeutics. Nat Rev Drug Discov. 5:997–1014. 2006. View Article : Google Scholar : PubMed/NCBI | |
Tetsu O and McCormick F: Beta-Catenin regulates expression of cyclin D1 in colon carcinoma cells. Nature. 398:422–426. 1999. View Article : Google Scholar : PubMed/NCBI | |
Shtutman M, Zhurinsky J, Simcha I, Albanese C, D'Amico M, Pestell R and Ben-Ze'ev A: The cyclin D1 gene is a target of the beta-catenin/LEF-1 pathway. Proc Natl Acad Sci USA. 96:5522–5527. 1999. View Article : Google Scholar : PubMed/NCBI | |
He TC, Chan TA, Vogelstein B and Kinzler KW: PPARδ is an APC-regulated target of nonsteroidal anti-inflammatory drugs. Cell. 99:335–345. 1999. View Article : Google Scholar : PubMed/NCBI | |
Crawford HC, Fingleton BM, Rudolph-Owen LA, Goss KJ, Rubinfeld B, Polakis P and Matrisian LM: The metalloproteinase matrilysin is a target of beta-catenin transactivation in intestinal tumors. Oncogene. 18:2883–2891. 1999. View Article : Google Scholar : PubMed/NCBI | |
Brabletz T, Jung A, Dag S, Hlubek F and Kirchner T: Beta-Catenin regulates the expression of the Matrix Metalloproteinase-7 in human colorectal cancer. Am J Pathol. 155:1033–1038. 1999. View Article : Google Scholar : PubMed/NCBI | |
Hlubek F, Spaderna S, Jung A, Kirchner T and Brabletz T: Beta-Catenin activates a coordinated expression of the proinvasive factors laminin-5 gamma2 chain and MT1-MMP in colorectal carcinomas. Int J Cancer. 108:321–326. 2004. View Article : Google Scholar : PubMed/NCBI | |
Clevers H and Nusse R: Wnt/β-catenin signaling and disease. Cell. 149:1192–1205. 2012. View Article : Google Scholar : PubMed/NCBI | |
Herbst A, Jurinovic V, Krebs S, Thieme SE, Blum H, Göke B and Kolligs FT: Comprehensive analysis of β-catenin target genes in colorectal carcinoma cell lines with deregulated Wnt/β-catenin signaling. BMC Genomics. 15:742014. View Article : Google Scholar : PubMed/NCBI | |
Mokry M, Hatzis P, Schuijers J, Lansu N, Ruzius FP, Clevers H and Cuppen E: Integrated genome-wide analysis of transcription factor occupancy, RNA polymerase II binding and steady-state RNA levels identify differentially regulated functional gene classes. Nucleic Acids Res. 40:148–158. 2012. View Article : Google Scholar : PubMed/NCBI | |
Ewing RM, Song J, Gokulrangan G, Bai S, Bowler EH, Bolton R, Skipp P, Wang Y and Wang Z: Multiproteomic and transcriptomic analysis of oncogenic β-Catenin molecular networks. J Proteome Res. 17:2216–2225. 2018. View Article : Google Scholar : PubMed/NCBI | |
Liu Y, Beyer A and Aebersold R: On the dependency of cellular protein levels on mRNA abundance. Cell. 165:535–550. 2016. View Article : Google Scholar : PubMed/NCBI | |
Baryshnikova A, Costanzo M, Myers CL, Andrews B and Boone C: Genetic interaction networks: Toward an understanding of heritability. Annu Rev Genomics Hum Genet. 14:111–133. 2013. View Article : Google Scholar : PubMed/NCBI | |
Costanzo M, VanderSluis B, Koch EN, Baryshnikova A, Pons C, Tan G, Wang W, Usaj M, Hanchard J, Lee SD, et al: A global genetic interaction network maps a wiring diagram of cellular function. Science. 353:aaf14202016. View Article : Google Scholar : PubMed/NCBI | |
Boettcher M, Tian R, Blau JA, Markegard E, Wagner RT, Wu D, Mo X, Biton A, Zaitlen N, Fu H, et al: Dual gene activation and knockout screen reveals directional dependencies in genetic networks. Nat Biotechnol. 36:170–178. 2018. View Article : Google Scholar : PubMed/NCBI | |
Shen JP, Zhao D, Sasik R, Luebeck J, Birmingham A, Bojorquez-Gomez A, Licon K, Klepper K, Pekin D, Beckett AN, et al: Combinatorial CRISPR-Cas9 screens for de novo mapping of genetic interactions. Nat Methods. 14:573–576. 2017. View Article : Google Scholar : PubMed/NCBI | |
Tsherniak A, Vazquez F, Montgomery PG, Weir BA, Kryukov G, Cowley GS, Gill S, Harrington WF, Pantel S, Krill-Burger JM, et al: Defining a cancer dependency map. Cell. 170:564–576.e16. 2017. View Article : Google Scholar : PubMed/NCBI | |
Meyers RM, Bryan JG, McFarland JM, Weir BA, Sizemore AE, Xu H, Dharia NV, Montgomery PG, Cowley GS, Pantel S, et al: Computational correction of copy number effect improves specificity of CRISPRCas9 essentiality screens in cancer cells. Nat Genet. 49:1779–1784. 2017. View Article : Google Scholar : PubMed/NCBI | |
Barretina J, Caponigro G, Stransky N, Venkatesan K, Margolin AA, Kim S, Wilson CJ, Lehár J, Kryukov GV, Sonkin D, et al: The cancer cell line encyclopedia enables predictive modelling of anticancer drug sensitivity. Nature. 483:603–607. 2012. View Article : Google Scholar : PubMed/NCBI | |
Barrett T, Wilhite SE, Ledoux P, Evangelista C, Kim IF, Tomashevsky M, Marshall KA, Phillippy KH, Sherman PM, Holko M, et al: NCBI GEO: Archive for functional genomics data sets-update. Nucleic Acids Res. 41(Database Issue): D991–D995. 2012. View Article : Google Scholar : PubMed/NCBI | |
Tsafrir D, Bacolod M, Selvanayagam Z, Tsafrir I, Shia J, Zeng Z, Liu H, Krier C, Stengel RF, Barany F, et al: Relationship of gene expression and chromosomal abnormalities in colorectal cancer. Cancer Res. 66:2129–2137. 2006. View Article : Google Scholar : PubMed/NCBI | |
Jorissen RN, Gibbs P, Christie M, Prakash S, Lipton L, Desai J, Kerr D, Aaltonen LA, Arango D, Kruhøffer M, et al: Metastasis-Associated gene expression changes predict poor outcomes in patients with dukes Stage B and C colorectal cancer. Clin Cancer Res. 15:7642–7651. 2009. View Article : Google Scholar : PubMed/NCBI | |
Smith JJ, Deane NG, Wu F, Merchant NB, Zhang B, Jiang A, Lu P, Johnson JC, Schmidt C, Bailey CE, et al: Experimentally derived metastasis gene expression profile predicts recurrence and death in patients with colon cancer. Gastroenterology. 138:958–968. 2010. View Article : Google Scholar : PubMed/NCBI | |
Freeman TJ, Smith JJ, Chen X, Washington MK, Roland JT, Means AL, Eschrich SA, Yeatman TJ, Deane NG and Beauchamp RD: Smad4-mediated signaling inhibits intestinal neoplasia by inhibiting expression of β-catenin. Gastroenterology. 142:562–571.e2. 2012. View Article : Google Scholar : PubMed/NCBI | |
Sveen A, Agesen TH, Nesbakken A, Rognum TO, Lothe RA and Skotheim RI: Transcriptome instability in colorectal cancer identified by exon microarray analyses: Associations with splicing factor expression levels and patient survival. Genome Med. 3:322011. View Article : Google Scholar : PubMed/NCBI | |
Agesen TH, Sveen A, Merok MA, Lind GE, Nesbakken A, Skotheim RI and Lothe RA: ColoGuideEx: A robust gene classifier specific for stage II colorectal cancer prognosis. Gut. 61:1560–1567. 2012. View Article : Google Scholar : PubMed/NCBI | |
Thorsteinsson M, Kirkeby LT, Hansen R, Lund LR, Sørensen LT, Gerds TA, Jess P and Olsen J: Gene expression profiles in stages II and III colon cancers: Application of a 128-gene signature. Int J Colorectal Dis. 27:1579–1586. 2012. View Article : Google Scholar : PubMed/NCBI | |
Laibe S, Lagarde A, Ferrari A, Monges G, Birnbaum D and Olschwang S; COL2 Project, : A seven-gene signature aggregates a subgroup of stage II colon cancers with stage III. OMICS. 16:560–565. 2012. View Article : Google Scholar : PubMed/NCBI | |
Marisa L, de Reyniès A, Duval A, Selves J, Gaub MP, Vescovo L, Etienne-Grimaldi MC, Schiappa R, Guenot D, Ayadi M, et al: Gene expression classification of colon cancer into molecular subtypes: Characterization, validation, and prognostic value. PLoS Med. 10:e10014532013. View Article : Google Scholar : PubMed/NCBI | |
Gentles AJ, Newman AM, Liu CL, Bratman SV, Feng W, Kim D, Nair VS, Xu Y, Khuong A, Hoang CD, et al: The prognostic landscape of genes and infiltrating immune cells across human cancers. Nat Med. 21:938–945. 2015. View Article : Google Scholar : PubMed/NCBI | |
RCoreTeam: R, . A language and environment for statistical computing. 2018. | |
Carvalho BS and Irizarry RA: A framework for oligonucleotide microarray preprocessing. Bioinformatics. 26:2363–2367. 2010. View Article : Google Scholar : PubMed/NCBI | |
Dai M, Wang P, Boyd AD, Kostov G, Athey B, Jones EG, Bunney WE, Myers RM, Speed TP, Akil H, et al: Evolving gene/transcript definitions significantly alter the interpretation of GeneChip data. Nucleic Acids Res. 33:e1752005. View Article : Google Scholar : PubMed/NCBI | |
Kim SK, Kim SY, Kim JH, Roh SA, Cho DH, Kim YS and Kim JC: A nineteen gene-based risk score classifier predicts prognosis of colorectal cancer patients. Mol Oncol. 8:1653–66. 2014. View Article : Google Scholar : PubMed/NCBI | |
Liu D, Skomorovska Y, Song J, Bowler E, Harris R, Ravasz M, Bai S, Ayati M, Tamai K, Koyuturk M, et al: ELF3 is an antagonist of oncogenic-signalling-induced expression of EMT-TF ZEB1. Cancer Biol Ther. 20:90–100. 2019. View Article : Google Scholar : PubMed/NCBI | |
Patro R, Duggal G, Love MI, Irizarry RA and Kingsford C: Salmon provides fast and bias-aware quantification of transcript expression. Nat Methods. 14:417–419. 2017. View Article : Google Scholar : PubMed/NCBI | |
Colaprico A, Silva TC, Olsen C, Garofano L, Cava C, Garolini D, Sabedot TS, Malta TM, Pagnotta SM, Castiglioni I, et al: TCGAbiolinks: An R/Bioconductor package for integrative analysis of TCGA data. Nucleic Acids Res. 44:e712016. View Article : Google Scholar : PubMed/NCBI | |
Ritchie ME, Phipson B, Wu D, Hu Y, Law CW, Shi W and Smyth GK: Limma powers differential expression analyses for RNA-sequencing and microarray studies. Nucleic Acids Res. 43:e472015. View Article : Google Scholar : PubMed/NCBI | |
Benjamini Y and Hochberg Y: Controlling the false discovery rate: A practical and powerful approach to multiple testing. J R Stat Soc Series B (Methodological). 57:289–300. 1995. View Article : Google Scholar | |
Sergushichev A: An algorithm for fast preranked gene set enrichment analysis using cumulative statistic calculation. Jun 20–2016.doi: https://doi.org/10.1101/060012. View Article : Google Scholar | |
Subramanian A, Tamayo P, Mootha VK, Mukherjee S, Ebert BL, Gillette MA, Paulovich A, Pomeroy SL, Golub TR, Lander ES and Mesirov JP: Gene set enrichment analysis: A knowledge-based approach for interpreting genome-wide expression profiles. Proc Natl Acad Sci USA. 102:15545–15550. 2005. View Article : Google Scholar : PubMed/NCBI | |
Pan J, Meyers RM, Michel BC, Mashtalir N, Sizemore AE, Wells JN, Cassel SH, Vazquez F, Weir BA, Hahn WC, et al: Interrogation of mammalian protein complex structure, function, and membership using genome-scale fitness screens. Cell Syst. 6:555–568.e7. 2018. View Article : Google Scholar : PubMed/NCBI | |
Dihlmann S, Kloor M, Fallsehr C and von Knebel Doeberitz M: Regulation of AKT1 expression by beta-catenin/Tcf/Lef signaling in colorectal cancer cells. Carcinogenesis. 26:1503–1512. 2005. View Article : Google Scholar : PubMed/NCBI | |
Lopez CD, Martinovsky G and Naumovski L: Inhibition of cell death by ribosomal protein L35a. Cancer Lett. 180:195–202. 2002. View Article : Google Scholar : PubMed/NCBI | |
Henry JL, Coggin DL and King CR: High-level expression of the ribosomal protein L19 in human breast tumors that overexpress erbB-2. Cancer Res. 53:1403–1408. 1993.PubMed/NCBI | |
Wang Q, Yang C, Zhou J, Wang X, Wu M and Liu Z: Cloning and characterization of full-length human ribosomal protein L15 cDNA which was overexpressed in esophageal cancer. Gene. 263:205–209. 2001. View Article : Google Scholar : PubMed/NCBI | |
Kim JH, You KR, Kim IH, Cho BH, Kim CY and Kim DG: Over-expression of the ribosomal protein L36a gene is associated with cellular proliferation in hepatocellular carcinoma. Hepatology. 39:129–138. 2004. View Article : Google Scholar : PubMed/NCBI | |
Cheng Q, Lau WM, Chew SH, Ho TH, Tay SK and Hui KM: Identification of molecular markers for the early detection of human squamous cell carcinoma of the uterine cervix. Br J Cancer. 86:274–281. 2002. View Article : Google Scholar : PubMed/NCBI | |
Kitahara O, Furukawa Y, Tanaka T, Kihara C, Ono K, Yanagawa R, Nita ME, Takagi T, Nakamura Y and Tsunoda T: Alterations of gene expression during colorectal carcinogenesis revealed by cDNA microarrays after laser-capture microdissection of tumor tissues and normal epithelia. Cancer Res. 61:3544–3549. 2001.PubMed/NCBI | |
Bertucci F, Salas S, Eysteries S, Nasser V, Finetti P, Ginestier C, Charafe-Jauffret E, Loriod B, Bachelart L, Montfort J, et al: Gene expression profiling of colon cancer by DNA microarrays and correlation with histoclinical parameters. Oncogene. 23:1377–1391. 2004. View Article : Google Scholar : PubMed/NCBI | |
van de Wetering M, Sancho E, Verweij C, de Lau W, Oving I, Hurlstone A, van der Horn K, Batlle E, Coudreuse D, Haramis AP, et al: The beta-catenin/TCF-4 complex imposes a crypt progenitor phenotype on colorectal cancer cells. Cell. 111:241–250. 2002. View Article : Google Scholar : PubMed/NCBI | |
Ciznadija D, Tothill R, Waterman ML, Zhao L, Huynh D, Yu RM, Ernst M, Ishii S, Mantamadiotis T, Gonda TJ, et al: Intestinal adenoma formation and MYC activation are regulated by cooperation between MYB and Wnt signaling. Cell Death Differ. 16:1530–1538. 2009. View Article : Google Scholar : PubMed/NCBI | |
Gao R, Cao C, Zhang M, Lopez MC, Yan Y, Chen Z, Mitani Y, Zhang L, Zajac-Kaye M, Liu B, et al: A unifying gene signature for adenoid cystic cancer identifies parallel MYB-dependent and MYB-independent therapeutic targets. Oncotarget. 5:12528–12542. 2014. View Article : Google Scholar : PubMed/NCBI | |
Rettig EM, Tan M, Ling S, Yonescu R, Bishop JA, Fakhry C and Ha PK: MYB rearrangement and clinicopathologic characteristics in head and neck adenoid cystic carcinoma. Laryngoscope. 125:E292–E299. 2015. View Article : Google Scholar : PubMed/NCBI | |
North JP, McCalmont TH, Fehr A, van Zante A, Stenman G and LeBoit PE: Detection of MYB alterations and other immunohistochemical markers in primary cutaneous adenoid cystic carcinoma. Am J Surg Pathol. 39:1347–1356. 2015. View Article : Google Scholar : PubMed/NCBI | |
Bishop JA, Yonescu R, Epstein JI and Westra WH: A subset of prostatic basal cell carcinomas harbor the MYB rearrangement of adenoid cystic carcinoma. Hum Pathol. 46:1204–1208. 2015. View Article : Google Scholar : PubMed/NCBI | |
Argyris PP, Wetzel SL, Greipp P, Wehrs RN, Knutson DL, Kloft-Nelson SM, García JJ and Koutlas IG: Clinical utility of myb rearrangement detection and p63/p40 immunophenotyping in the diagnosis of adenoid cystic carcinoma of minor salivary glands: A pilot study. Oral Surg Oral Med Oral Pathol Oral Radiol. 121:282–289. 2016. View Article : Google Scholar : PubMed/NCBI | |
Drier Y, Cotton MJ, Williamson KE, Gillespie SM, Ryan RJ, Kluk MJ, Carey CD, Rodig SJ, Sholl LM, Afrogheh AH, et al: An oncogenic MYB feedback loop drives alternate cell fates in adenoid cystic carcinoma. Nat Genet. 48:265–272. 2016. View Article : Google Scholar : PubMed/NCBI | |
Chen TY, Keeney MG, Chintakuntlawar AV, Knutson DL, Kloft-Nelson S, Greipp PT, Garrity JA, Salomao DR and Garcia JJ: Adenoid cystic carcinoma of the lacrimal gland is frequently characterized by MYB rearrangement. Eye (Lond). 31:720–725. 2017. View Article : Google Scholar : PubMed/NCBI | |
van der Horst MP, Marusic Z, Hornick JL, Luzar B and Brenn T: Morphologically low-grade spiradenocarcinoma: A clinicopathologic study of 19 cases with emphasis on outcome and MYB expression. Mod Pathol. 28:944–953. 2015. View Article : Google Scholar : PubMed/NCBI | |
Rajan N, Andersson MK, Sinclair N, Fehr A, Hodgson K, Lord CJ, Kazakov DV, Vanecek T, Ashworth A and Stenman G: Overexpression of MYB drives proliferation of CYLD-defective cylindroma cells. J Pathol. 239:197–205. 2016. View Article : Google Scholar : PubMed/NCBI | |
Zhang L, Maul RS, Rao J, Apple S, Seligson D, Sartippour M, Rubio R and Brooks MN: Expression pattern of the novel gene EG-1 in cancer. Clin Cancer Res. 10:3504–3508. 2004. View Article : Google Scholar : PubMed/NCBI | |
Lee EK, Cho H and Kim CW: Proteomic analysis of cancer stem cells in human prostate cancer cells. Biochem Biophys Res Commun. 412:279–285. 2011. View Article : Google Scholar : PubMed/NCBI | |
Wei N, Cheng Y, Wang Z, Liu Y, Luo C, Liu L, Chen L, Xie Z, Lu Y and Feng Y: SRSF10 plays a role in myoblast differentiation and glucose production via regulation of alternative splicing. Cell Rep. 13:1647–1657. 2015. View Article : Google Scholar : PubMed/NCBI | |
Zhou X, Li X, Cheng Y, Wu W, Xie Z, Xi Q, Han J, Wu G, Fang J and Feng Y: BCLAF1 and its splicing regulator SRSF10 regulate the tumorigenic potential of colon cancer cells. Nat Commun. 5:45812014. View Article : Google Scholar : PubMed/NCBI | |
Li H, Cheng Y, Wu W, Liu Y, Wei N, Feng X, Xie Z and Feng Y: SRSF10 regulates alternative splicing and is required for adipocyte differentiation. Mol Cell Biol. 34:2198–2207. 2014. View Article : Google Scholar : PubMed/NCBI | |
Soond SM, Smith PG, Wahl L, Swingler TE, Clark IM, Hemmings AM and Chantry A: Novel WWP2 ubiquitin ligase isoforms as potential prognostic markers and molecular targets in cancer. Biochim Biophys Acta 1832. 2127–2135. 2013. | |
Soond SM and Chantry A: Selective targeting of activating and inhibitory Smads by distinct WWP2 ubiquitin ligase isoforms differentially modulates TGFβ signalling and EMT. Oncogene. 30:2451–2462. 2011. View Article : Google Scholar : PubMed/NCBI | |
Haan JC, Labots M, Rausch C, Koopman M, Tol J, Mekenkamp LJ, van de Wiel MA, Israeli D, van Essen HF, van Grieken NC, et al: Genomic landscape of metastatic colorectal cancer. Nat Commun. 5:54572014. View Article : Google Scholar : PubMed/NCBI | |
Srivastava SK, Bhardwaj A, Arora S, Singh S, Azim S, Tyagi N, Carter JE, Wang B and Singh AP: MYB is a novel regulator of pancreatic tumour growth and metastasis. Br J Cancer. 113:1694–1703. 2015. View Article : Google Scholar : PubMed/NCBI |