Pattern discovery and cancer gene identification in integrated cancer genomic data
Open accessAbstract
Large-scale integrated cancer genome characterization efforts including the cancer genome atlas and the cancer cell line encyclopedia have created unprecedented opportunities to study cancer biology in the context of knowing the entire catalog of genetic alterations. A clinically important challenge is to discover cancer subtypes and their molecular drivers in a comprehensive genetic context. Curtis et al. [ Nature (2012) 486(7403):346–352] has recently shown that integrative clustering of copy number and gene expression in 2,000 breast tumors reveals novel subgroups beyond the classic expression subtypes that show distinct clinical outcomes. To extend the scope of integrative analysis for the inclusion of somatic mutation data by massively parallel sequencing, we propose a framework for joint modeling of discrete and continuous variables that arise from integrated genomic, epigenomic, and transcriptomic profiling. The core idea is motivated by the hypothesis that diverse molecular phenotypes can be predicted by a set of orthogonal latent variables that represent distinct molecular drivers, and thus can reveal tumor subgroups of biological and clinical importance. Using the cancer cell line encyclopedia dataset, we demonstrate our method can accurately group cell lines by their cell-of-origin for several cancer types, and precisely pinpoint their known and potential cancer driver genes. Our integrative analysis also demonstrates the power for revealing subgroups that are not lineage-dependent, but consist of different cancer types driven by a common genetic alteration. Application of the cancer genome atlas colorectal cancer data reveals distinct integrated tumor subtypes, suggesting different genetic pathways in colon cancer progression.
Integrity signals
Registry
Cites
Statistics
Claims the paper makes
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?
A large set of multi-omics data integrative tools and methods have been reported for the discovery of biomarkers.
“Along with the introduction of high-throughput technologies and the availability of multi-omics data derived from a number of samples, a large set of multi-omics data integrative tools and methods have been reported for the discovery of biomarkers.”
From Bioinformatics Analysis and Validation of Potential Markers Associated with Prediction and Prognosis of Gastric Cancer (2024) · cites this paper as [98]
These methods can be divided into categories, such as Bayesian integration, network and pathway integration, fusion-based integration, similarity-based integration, and other multivariate approaches.
“These methods can be divided into categories, such as Bayesian integration (e.g., Pathway Recognition Algorithm using Data Integration on Genomic Models (PARADIGM) [97], iClusterPlus [98], Patient-specific data fusion (PSDF) [99]), network and pathway integration (e.g., Similarity network fusion (SNF) [100], PaintOmics [101], MultiGSEA [102], multi-omics gene-set analysis (MOGSA) [103], Cytoscape”
From Bioinformatics Analysis and Validation of Potential Markers Associated with Prediction and Prognosis of Gastric Cancer (2024) · cites this paper as [98]
Cites
Regression shrinkage and selection via the lasso
Tibshirani, R. (1996) · Journal of the Royal Statistical Society Series B: Statistical Methodology · doi:10.1111/j.2517-6161.1996.tb02080.x · Cited by 51,482 · see citing works
Regularization Paths for Generalized Linear Models via Coordinate Descent
Friedman, J., Hastie, T., & Tibshirani, R. (2010) · Journal of Statistical Software · doi:10.18637/jss.v033.i01 · Cited by 19,927 · see citing works
Huang, D. W., Sherman, B. T., & Lempicki, R. A. (2009) · Nucleic Acids Research · doi:10.1093/nar/gkn923 · Cited by 14,108 · see citing works
Comprehensive molecular portraits of human breast tumours
The Cancer Genome Atlas Network (2012) · Nature · doi:10.1038/nature11412 · Cited by 12,129 · see citing works
Comprehensive molecular characterization of human colon and rectal cancer
The Cancer Genome Atlas Network (2012) · Nature · doi:10.1038/nature11252 · Cited by 8,499 · see citing works
The Cancer Cell Line Encyclopedia enables predictive modelling of anticancer drug sensitivity
Barretina, J., Caponigro, G., Stransky, N., Venkatesan, K., Margolin, A. A., Kim, S., Wilson, C. J., Lehár, J., Kryukov, G. V., Sonkin, D., et al. (2012) · Nature · doi:10.1038/nature11003 · Cited by 7,950 · see citing works
Integrated genomic analyses of ovarian carcinoma
Perou, C. M. (2019) · Carolina Digital Repository (University of North Carolina at Chapel Hill) · doi:10.17615/hvp3-wg08 · Cited by 7,927 · see citing works
Comprehensive genomic characterization defines human glioblastoma genes and core pathways
The Cancer Genome Atlas Research Network (2008) · Nature · doi:10.1038/nature07385 · Cited by 7,735 · see citing works
Atomic Decomposition by Basis Pursuit
Chen, S. S., Donoho, D. L., & Saunders, M. A. (1998) · SIAM Journal on Scientific Computing · doi:10.1137/s1064827596304010 · Cited by 6,734 · see citing works
The genomic and transcriptomic architecture of 2,000 breast tumours reveals novel subgroups
METABRIC Group, Curtis, C., Shah, S. P., Chin, S.-F., Turashvili, G., Rueda, O. M., Dunning, M. J., Speed, D., Lynch, A. G., Samarajiwa, S., et al. (2012) · Nature · doi:10.1038/nature10983 · Cited by 6,097 · see citing works
Comprehensive genomic characterization of squamous cell lung cancers
The Cancer Genome Atlas Research Network (2012) · Nature · doi:10.1038/nature11404 · Cited by 3,994 · see citing works
Self-citationA census of human cancer genes
Futreal, P. A., Coin, L., Marshall, M., Down, T., Hubbard, T., Wooster, R., Rahman, N., & Stratton, M. R. (2004) · Nature Reviews Cancer · doi:10.1038/nrc1299 · Cited by 3,184 · see citing works
Systematic identification of genomic markers of drug sensitivity in cancer cells
Garnett, M. J., Edelman, E. J., Heidorn, S. J., Greenman, C. D., Dastur, A., Lau, K. W., Greninger, P., Thompson, I. R., Luo, X., Soares, J., et al. (2012) · Nature · doi:10.1038/nature11005 · Cited by 2,456 · see citing works
Absolute quantification of somatic DNA alterations in human cancer
Carter, S. L., Cibulskis, K., Helman, E., McKenna, A., Shen, H., Zack, T. I., Laird, P. W., Onofrio, R. C., Winckler, W., Weir, B. A., et al. (2012) · Nature Biotechnology · doi:10.1038/nbt.2203 · Cited by 2,003 · see citing works
Garraway, L. A., Widlund, H. R., Rubin, M. A., Getz, G., Berger, A. J., Ramaswamy, S., Beroukhim, R., Milner, D. A., Granter, S. R., Du, J., et al. (2005) · Nature · doi:10.1038/nature03664 · Cited by 1,548 · see citing works
High-throughput oncogene mutation profiling in human cancer
Thomas, R. K., Baker, A. C., Debiasi, R. M., Winckler, W., LaFramboise, T., Lin, W. M., Wang, M., Feng, W., Zander, T., MacConaill, L. E., et al. (2007) · Nature Genetics · doi:10.1038/ng1975 · Cited by 978 · see citing works
Shen, R., Olshen, A. B., & Ladanyi, M. (2009) · Bioinformatics · doi:10.1093/bioinformatics/btp543 · Cited by 849 · see citing works
Self-citationMaximum Likelihood Algorithms for Generalized Linear Mixed Models
McCulloch, C. E. (1997) · Journal of the American Statistical Association · doi:10.1080/01621459.1997.10473613 · Cited by 762 · see citing works
Bott, M., Brevet, M., Taylor, B. S., Shimizu, S., Ito, T., Wang, L., Creaney, J., Lake, R. A., Zakowski, M. F., Reva, B., et al. (2011) · Nature Genetics · doi:10.1038/ng.855 · Cited by 717 · see citing works
Mutual exclusivity analysis identifies oncogenic network modulesPreprint
Ciriello, G., Cerami, E. G., Sander, C., & Schultz, N. D. (2011) · Genome Research · doi:10.1101/gr.125567.111 · Cited by 676 · see citing works
Self-citationNumber-theoretic Methods in Statistics
Fang, K.-T., & Wang, Y.-X. (1994) · Springer eBooks · doi:10.1007/978-1-4899-3095-8 · Cited by 641 · see citing works
Number-Theoretic Methods in Statistics.
Ripley, B. D., Fang, K.-T., & Wang, Y. (1995) · Journal of the Royal Statistical Society Series A (Statistics in Society) · doi:10.2307/2983421 · Cited by 621 · see citing works
Valid post-selection inference
Berk, R. A., Brown, L., Buja, A., Zhang, K., & Zhao, L. H. (2013) · The Annals of Statistics · doi:10.1214/12-aos1077 · Cited by 617 · see citing works
Genomic analysis of a key innovation in an experimental Escherichia coli population
Blount, Z. D., Barrick, J. E., Davidson, C. J., & Lenski, R. E. (2012) · Nature · doi:10.1038/nature11514 · Cited by 612 · see citing works
Shen, R., Olshen, A. B., & Ladanyi, M. (2010) · Bioinformatics · doi:10.1093/bioinformatics/btp659 · Cited by 566 · see citing works
Self-citationJoint and individual variation explained (JIVE) for integrated analysis of multiple data types
Lock, E. F., Hoadley, K. A., Marron, J. S., & Nobel, A. B. (2013) · The Annals of Applied Statistics · doi:10.1214/12-aoas597 · Cited by 554 · see citing works
De Novo Discovery of Mutated Driver Pathways in Cancer
Vandin, F., Upfal, E., & Raphael, B. J. (2011) · Lecture notes in computer science · doi:10.1007/978-3-642-20036-6_44 · Cited by 434 · see citing works
The t(8;9)(p22;p24) Is a Recurrent Abnormality in Chronic and Acute Leukemia that Fuses PCM1 to JAK2
Reiter, A., Walz, C., Watmore, A. E., Schoch, C., Blau, I., Schlegelberger, B., Berger, U., Telford, N., Aruliah, S., Yin, J. A. L., et al. (2005) · Cancer Research · doi:10.1158/0008-5472.can-04-4263 · Cited by 269 · see citing works
Can one estimate the conditional distribution of post-model-selection estimators?
Leeb, H., & Pötscher, B. M. (2006) · The Annals of Statistics · doi:10.1214/009053606000000821 · Cited by 163 · see citing works
Hollander, M. C., Philburn, R. T., Patterson, A. D., Velasco-Miguel, S., Friedberg, E. C., Linnoila, R. I., & Fornace, A. J. (2005) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0503133102 · Cited by 135 · see citing works
Studies of the Human c- myb Gene and Its Product in Human Acute Leukemias
Slamon, D. J., Boone, T. C., Murdock, D. C., Keith, D. E., Press, M. F., Larson, R. A., & Souza, L. M. (1986) · Science · doi:10.1126/science.3014652 · Cited by 125 · see citing works
Patient-specific data fusion defines prognostic cancer subtypes
Yuan, Y., Savage, R. S., & Markowetz, F. (2011) · PLoS Computational Biology · doi:10.1371/journal.pcbi.1002227 · Cited by 97 · see citing works
Relationship Between the c- myb Locus and the 6q- Chromosomal Aberration in Leukemias and Lymphomas
Barletta, C., Pelicci, P. G., Kenyon, L. C., Smith, S. D., & Dalla‐Favera, R. (1987) · Science · doi:10.1126/science.3469751 · Cited by 97 · see citing works
Alter, O., & Golub, G. H. (2004) · Proceedings of the National Academy of Sciences · doi:10.1073/pnas.0406767101 · Cited by 78 · see citing works
p73-alpha is capable of inducing scotin and ER stress
Terrinoni, A., Ranalli, M., Cadot, B., Leta, A., Bagetta, G., Vousden, K. H., & Melino, G. (2004) · Oncogene · doi:10.1038/sj.onc.1207342 · Cited by 58 · see citing works
Fang, K., & Wang, Y. (2014) · Wiley StatsRef: Statistics Reference Online · doi:10.1002/9781118445112.stat02239 · Cited by 17 · see citing works
Flagged first, then by citations
Cited by
Sorted by citations
Comprehensive molecular profiling of lung adenocarcinoma
The Cancer Genome Atlas Research Network (2014) · Nature · doi:10.1038/nature13385 · Cited by 5,732 · see citing works
Hoadley, K. A., Yau, C., Hinoue, T., Wolf, D. M., Lazar, A. J., Drill, E., Shen, R., Taylor, A. M., Cherniack, A. D., Thorsson, V., et al. (2018) · Cell · doi:10.1016/j.cell.2018.03.022 · Cited by 2,546 · see citing works
“Integrative clustering with iCluster—The iCluster clustering algorithm formulates the problem of subgroup discovery as a joint multivariate regression of multiple data types with reference to a set of common latent variables, which represent the underlying 28 tumor subtypes (Mo et al., 2013; Shen et al., 2009, 2012).”
MethodSelf-citationComprehensive and Integrative Genomic Characterization of Hepatocellular Carcinoma
Ally, A., Balasundaram, M., Carlsen, R., Chuah, E., Clarke, A., Dhalla, N., Holt, R. A., Jones, S. J. M., Lee, D., Ma, Y., et al. (2017) · Cell · doi:10.1016/j.cell.2017.05.046 · Cited by 2,490 · see citing works
Integrated genomic characterization of oesophageal carcinoma
Sun, Q., Kelsen, D. P., Wiznerowicz, M., Lu, Y., Marra, M. A., Wan, Y., Weinhold, N., Wong, A. M., Carvalho, A. L., Luketich, J. D., et al. (2017) · Nature · doi:10.1038/nature20805 · Cited by 1,833 · see citing works
Multi-omics Data Integration, Interpretation, and Its Application
Subramanian, I., Verma, S., Kumar, S., Jere, A., & Anamika, K. (2020) · Bioinformatics and Biology Insights · doi:10.1177/1177932219899051 · Cited by 1,609 · see citing works
Multi-Omics Factor Analysis—a framework for unsupervised integration of multi-omics data sets
Argelaguet, R., Velten, B., Arnol, D., Dietrich, S., Zenz, T., Marioni, J. C., Buettner, F., Huber, W., & Stegle, O. (2018) · Molecular Systems Biology · doi:10.15252/msb.20178124 · Cited by 1,510 · see citing works
Genomic spectra of biliary tract cancer
Nakamura, H. K., Arai, Y., Totoki, Y., Shirota, T., Elzawahry, A., Kato, M., Hama, N., Hosoda, F., Urushidate, T., Ohashi, S., et al. (2015) · Nature Genetics · doi:10.1038/ng.3375 · Cited by 1,287 · see citing works
Intertumoral Heterogeneity within Medulloblastoma Subgroups
Cavalli, F. M. G., Remke, M., Rampasek, L., Peacock, J., Shih, D. J. H., Luu, B., Garzia, L., Torchia, J., Nor, C., Morrissy, A. S., et al. (2017) · Cancer Cell · doi:10.1016/j.ccell.2017.05.005 · Cited by 1,219 · see citing works
Comprehensive and Integrated Genomic Characterization of Adult Soft Tissue Sarcomas
Abeshouse, A., Adebamowo, C., Adebamowo, S. N., Akbani, R., Akeredolu, T., Ally, A., Anderson, M. L., Anur, P., Appelbaum, E. L., Armenia, J., et al. (2017) · Cell · doi:10.1016/j.cell.2017.10.014 · Cited by 1,069 · see citing works
Jiang, Y., Ma, D., Suo, C., Shi, J., Xue, M., Hu, X., Xiao, Y., Yu, K., Liu, Y., Yu, Y., et al. (2019) · Cancer Cell · doi:10.1016/j.ccell.2019.02.001 · Cited by 1,069 · see citing works
Whole-Genome and Epigenomic Landscapes of Etiologically Distinct Subtypes of Cholangiocarcinoma
Jusakul, A., Cutcutache, I., Yong, C. H., Lim, J. Q., Huang, M. N., Padmanabhan, N., Nellore, V., Kongpetch, S., Ng, A. W. T., Ng, L. M., et al. (2017) · Cancer Discovery · doi:10.1158/2159-8290.cd-17-0368 · Cited by 972 · see citing works
Using machine learning approaches for multi-omics data analysis: A review
Reel, P. S., Reel, S., Pearson, E., Trucco, E., & Jefferson, E. (2021) · Biotechnology Advances · doi:10.1016/j.biotechadv.2021.107739 · Cited by 903 · see citing works
More Is Better: Recent Progress in Multi-Omics Data Integration Methods
Huang, S., Chaudhary, K., & Garmire, L. (2017) · Frontiers in Genetics · doi:10.3389/fgene.2017.00084 · Cited by 637 · see citing works
Integration strategies of multi-omics data for machine learning analysis
Picard, M., Scott-Boyer, M.-P., Bodein, A., Périn, O., & Droit, A. (2021) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2021.06.030 · Cited by 696 · see citing works
Targeting the STAT3 signaling pathway in cancer: Role of synthetic and natural inhibitors
Siveen, K. S., Sikka, S., Surana, R., Dai, X., Zhang, J., Kumar, A. P., Tan, B. K. H., Sethi, G., & Bishayee, A. (2014) · Biochimica et Biophysica Acta (BBA) - Reviews on Cancer · doi:10.1016/j.bbcan.2013.12.005 · Cited by 637 · see citing works
Multi-omic and multi-view clustering algorithms: review and cancer benchmark
Rappoport, N., & Ron Shamir, A. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky889 · Cited by 549 · see citing works
The IBD interactome: an integrated view of aetiology, pathogenesis and therapy
de Souza, H. S. P., Fiocchi, C., & Iliopoulos, D. (2017) · Nature Reviews Gastroenterology & Hepatology · doi:10.1038/nrgastro.2017.110 · Cited by 447 · see citing works
MOLI: multi-omics late integration with deep neural networks for drug response prediction
Sharifi-Noghabi, H., Zolotareva, O., Collins, C. C., & Ester, M. (2019) · Bioinformatics · doi:10.1093/bioinformatics/btz318 · Cited by 421 · see citing works
Menyhárt, O., & Győrffy, B. (2021) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2021.01.009 · Cited by 388 · see citing works
Machine learning and integrative analysis of biomedical big data
Mirza, B., Wang, W., Wang, J., Choi, H., Chung, N. C., & Ping, P. (2019) · Genes · doi:10.3390/genes10020087 · Cited by 380 · see citing works
A genomic and epigenomic atlas of prostate cancer in Asian populations
Li, J., Xu, C., Lee, H. J., Ren, S., Zi, X., Zhang, Z., Wang, H., Yu, Y., Yang, C., Gao, X., et al. (2020) · Nature · doi:10.1038/s41586-020-2135-x · Cited by 343 · see citing works
Self-citationMachine learning for multi-omics data integration in cancer
Cai, Z., Poulos, R. C., Liu, J., & Zhong, Q. (2022) · iScience · doi:10.1016/j.isci.2022.103798 · Cited by 341 · see citing works
Yang, Z., & Michailidis, G. (2016) · Bioinformatics · doi:10.1093/bioinformatics/btv544 · Cited by 295 · see citing works
Ross‐Adams, H., Lamb, A. D. G., Dunning, M., Halim, S., Lindberg, J., Massie, C. E., Egevad, L., Russell, R. B., Ramos‐Montoya, A., Vowler, S. L., et al. (2015) · EBioMedicine · doi:10.1016/j.ebiom.2015.07.017 · Cited by 312 · see citing works
Lock, E. F., & Dunson, D. B. (2013) · Bioinformatics · doi:10.1093/bioinformatics/btt425 · Cited by 308 · see citing works
Proteogenomic Characterization of Human Early-Onset Gastric Cancer
Mun, D.-G., Bhin, J., Kim, S., Kim, H., Jung, J. H., Jung, Y., Jang, Y. E., Park, J. M., Kim, H., Jung, Y., et al. (2019) · Cancer Cell · doi:10.1016/j.ccell.2018.12.003 · Cited by 294 · see citing works
Statistical and integrative system-level analysis of DNA methylation data
Teschendorff, A. E., & Relton, C. L. (2017) · Nature Reviews Genetics · doi:10.1038/nrg.2017.86 · Cited by 292 · see citing works
Integrative multi-omics approaches in cancer research: from biological networks to clinical subtypes
Heo, Y. J., Hwa, C., Lee, G.-H., Park, J.-M., & An, J.-Y. (2021) · Molecules and Cells · doi:10.14348/molcells.2021.0042 · Cited by 294 · see citing works
NEMO: cancer subtyping by integration of partial multi-omic data
Rappoport, N., & Shamir, R. (2019) · Bioinformatics · doi:10.1093/bioinformatics/btz058 · Cited by 286 · see citing works
A fully Bayesian latent variable model for integrative clustering analysis of multi-type omics data
Mo, Q., Shen, R., Guo, C., Vannucci, M., Chan, K. S., & Hilsenbeck, S. G. (2017) · Biostatistics · doi:10.1093/biostatistics/kxx017 · Cited by 281 · see citing works
Self-citationChalise, P., & Fridley, B. L. (2017) · PLoS ONE · doi:10.1371/journal.pone.0176278 · Cited by 233 · see citing works
Wu, D., Wang, D., Zhang, M. Q., & Gu, J. (2015) · BMC Genomics · doi:10.1186/s12864-015-2223-8 · Cited by 229 · see citing works
Baião, A. R., Cai, Z., Poulos, R. C., Robinson, P. J., Reddel, R. R., Zhong, Q., Vinga, S., & Gonçalves, E. (2025) · Briefings in Bioinformatics · doi:10.1093/bib/bbaf355 · Cited by 249 · see citing works
Alcala, N., Leblay, N., Gabriel, A., Mangiante, L., Hervás, D., Giffon, T., Sertier, A.-S., Ferrari, A., Derks, J. L., Ghantous, A., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11276-9 · Cited by 222 · see citing works
Integrative methods for analyzing big data in precision medicine
Gligorijević, V., Malod‐Dognin, N., & Pržulj, N. (2015) · PROTEOMICS · doi:10.1002/pmic.201500396 · Cited by 216 · see citing works
A Selective Review of Multi-Level Omics Data Integration Using Variable Selection
Wu, C., Zhou, F., Ren, J., Li, X., Jiang, Y., & Ma, S. (2019) · Microarrays · doi:10.3390/ht8010004 · Cited by 213 · see citing works
Multi-omic tumor data reveal diversity of molecular mechanisms that correlate with survival
Ramazzotti, D., Lal, A., Wang, B., Batzoglou, S., & Sidow, A. (2018) · Nature Communications · doi:10.1038/s41467-018-06921-8 · Cited by 211 · see citing works
NADPH Oxidases: A Perspective on Reactive Oxygen Species Production in Tumor Biology
Meitzler, J. L., Antony, S., Wu, Y., Juhasz, A. N., Liu, H., Jiang, G., Lu, J., Roy, K., & Doroshow, J. H. (2013) · Antioxidants and Redox Signaling · doi:10.1089/ars.2013.5603 · Cited by 205 · see citing works
A guide to multi-omics data collection and integration for translational medicine
Athieniti, E., & Spyrou, G. M. (2022) · Computational and Structural Biotechnology Journal · doi:10.1016/j.csbj.2022.11.050 · Cited by 185 · see citing works
A novel approach for data integration and disease subtypingPreprint
Nguyen, T., Tagett, R., Diaz, D., & Drăghici, S. (2017) · Genome Research · doi:10.1101/gr.215129.116 · Cited by 178 · see citing works
Unsupervised Multi-Omics Data Integration Methods: A Comprehensive Review
Vahabi, N., & Michailidis, G. C. (2022) · Frontiers in Genetics · doi:10.3389/fgene.2022.854752 · Cited by 159 · see citing works
Subtype-GAN: a deep learning approach for integrative cancer subtyping of multi-omics data
Yang, H., Chen, R., Li, D., & Wang, Z. (2021) · Bioinformatics · doi:10.1093/bioinformatics/btab109 · Cited by 157 · see citing works
Methods, Tools and Current Perspectives in Proteogenomics
Ruggles, K. V., Krug, K., Wang, X., Clauser, K. R., Wang, J., Payne, S., Fenyö, D., Zhang, B., & Mani, D. R. (2017) · Molecular & Cellular Proteomics · doi:10.1074/mcp.mr117.000024 · Cited by 148 · see citing works
Multi-omics integration—a comparison of unsupervised clustering methodologies
Tini, G., Marchetti, L., Priami, C., & Scott‐Boyer, M. (2017) · Briefings in Bioinformatics · doi:10.1093/bib/bbx167 · Cited by 147 · see citing works
Jiang, Y., Wang, J., Sun, M., Zuo, D., Wang, H., Shen, J., Jiang, W., Mu, H., Ma, X., Yin, F., et al. (2022) · Nature Communications · doi:10.1038/s41467-022-34689-5 · Cited by 148 · see citing works
Self-citationMultiplatform-based molecular subtypes of non-small-cell lung cancer
Chen, F., Zhang, Y., Parra, E. R., Rodriguez‐Canales, J., Behrens, C., Akbani, R., Lu, Y., Kurie, J. M., Gibbons, D. L., Mills, G. B., et al. (2016) · Oncogene · doi:10.1038/onc.2016.303 · Cited by 142 · see citing works
moCluster: Identifying Joint Patterns Across Multiple Omics Data Sets
Meng, C., Helm, D., Frejno, M., & Küster, B. (2015) · Journal of Proteome Research · doi:10.1021/acs.jproteome.5b00824 · Cited by 141 · see citing works
PINSPlus: a tool for tumor subtype discovery in integrated genomic data
Nguyen, H., Shrestha, S., Drăghici, S., & Nguyen, T. (2018) · Bioinformatics · doi:10.1093/bioinformatics/bty1049 · Cited by 140 · see citing works
Localized Data Fusion for Kernel k-Means Clustering with Application to Cancer Biology
Gönen, M., & Margolin, A. A. (2014) · neural information processing systems · Cited by 138 · see citing works
Evaluation and comparison of multi-omics data integration methods for cancer subtyping
Duan, R., Gao, L., Gao, Y., Hu, Y., Xu, H., Huang, M., Song, K., Wang, H., Dong, Y., Jiang, C., et al. (2021) · PLOS Computational Biology · doi:10.1371/journal.pcbi.1009224 · Cited by 122 · see citing works
Moving towards a molecular taxonomy of autoimmune rheumatic diseases
Barturen, G., Beretta, L., Cervera, R., van Vollenhoven, R., & Alarcón-Riquelme, M. E. (2018) · Nature Reviews Rheumatology · doi:10.1038/nrrheum.2017.220 · Cited by 125 · see citing works
Recent human adaptation: genomic approaches, interpretation and insights
Scheinfeldt, L., & Tishkoff, S. A. (2013) · Nature Reviews Genetics · doi:10.1038/nrg3604 · Cited by 113 · see citing works
Yu, Y., Zhang, N., Mai, Y., Ren, L., Chen, Q., Cao, Z., Chen, Q., Liu, Y., Hou, W., Yang, J., et al. (2023) · Genome biology · doi:10.1186/s13059-023-03047-z · Cited by 116 · see citing works
iOmicsPASS: network-based integration of multiomics data for predictive subnetwork discovery
Koh, H. W. L., Fermin, D., Vogel, C., Choi, K. P., Ewing, R. M., & Choi, H. (2019) · npj Systems Biology and Applications · doi:10.1038/s41540-019-0099-y · Cited by 113 · see citing works
Integrating Clinical and Multiple Omics Data for Prognostic Assessment across Human Cancers
Zhu, B., Song, N., Shen, R., Arora, A., Machiela, M. J., Song, L., Landi, M. T., Ghosh, D., Chatterjee, N., Baladandayuthapani, V., et al. (2017) · Scientific Reports · doi:10.1038/s41598-017-17031-8 · Cited by 109 · see citing works
Self-citationMulti-omics strategies for biomarker discovery and application in personalized oncology
Jiang, Z., Zhang, H., Gao, Y., & Sun, Y. (2025) · Molecular Biomedicine · doi:10.1186/s43556-025-00340-0 · Cited by 124 · see citing works
Rahnenführer, J., de Bin, R., Benner, A., Ambrogi, F., Lusa, L., Boulesteix, A., Migliavacca, E., Binder, H., Michiels, S., Sauerbrei, W., et al. (2023) · BMC Medicine · doi:10.1186/s12916-023-02858-y · Cited by 103 · see citing works
Systematic analysis of somatic mutations impacting gene expression in 12 tumour types
Ding, J., McConechy, M. K., Horlings, H. M., Ha, G., Chan, F. C., Funnell, T., Mullaly, S. C., Reimand, J., Bashashati, A., Bader, G. D., et al. (2015) · Nature Communications · doi:10.1038/ncomms9554 · Cited by 104 · see citing works
O’Connor, L. M., O’Connor, B. A., Lim, S. B., Zeng, J., & Lo, C. H. (2023) · Journal of Pharmaceutical Analysis · doi:10.1016/j.jpha.2023.06.011 · Cited by 107 · see citing works
Statistical Methods in Integrative Genomics
Richardson, S. T., Tseng, G. C., & Sun, W. (2016) · Annual Review of Statistics and Its Application · doi:10.1146/annurev-statistics-041715-033506 · Cited by 97 · see citing works
Bae, J. M., Kim, J. H., & Kang, G. H. (2016) · Archives of Pathology & Laboratory Medicine · doi:10.5858/arpa.2015-0310-ra · Cited by 100 · see citing works
Evaluation of colorectal cancer subtypes and cell lines using deep learning
Ronen, J., Hayat, S., & Akalin, A. (2019) · Life Science Alliance · doi:10.26508/lsa.201900517 · Cited by 101 · see citing works
Pierre‐Jean, M., Deleuze, J., Floch, É. L., & Mauger, F. (2019) · Briefings in Bioinformatics · doi:10.1093/bib/bbz138 · Cited by 100 · see citing works
Advances in bulk and single-cell multi-omics approaches for systems biology and precision medicine
Li, Y., Ma, L., Wu, D., & Chen, G. (2021) · Briefings in Bioinformatics · doi:10.1093/bib/bbab024 · Cited by 101 · see citing works
Angle-based joint and individual variation explained
Feng, Q., Jiang, M., Hannig, J., & Marron, J. S. (2018) · Journal of Multivariate Analysis · doi:10.1016/j.jmva.2018.03.008 · Cited by 93 · see citing works
Raufaste-Cazavieille, V., Santiago, R., & Droit, A. (2022) · Frontiers in Molecular Biosciences · doi:10.3389/fmolb.2022.962743 · Cited by 98 · see citing works
Pattern fusion analysis by adaptive alignment of multiple heterogeneous omics data
Shi, Q., Zhang, C., Peng, M., Yu, X., Zeng, T., Liu, J., & Chen, L. (2017) · Bioinformatics · doi:10.1093/bioinformatics/btx176 · Cited by 90 · see citing works
Wang, D. Y. Q., Pham, N., Tong, J., Sakashita, S., Allo, G., Kim, L., Yanagawa, N., Raghavan, V., Wei, Y., To, C., et al. (2016) · International Journal of Cancer · doi:10.1002/ijc.30472 · Cited by 89 · see citing works
Machine learning: its challenges and opportunities in plant system biology
Hesami, M., Alizadeh, M., Jones, A. M. P., & Torkamaneh, D. (2022) · Applied Microbiology and Biotechnology · doi:10.1007/s00253-022-11963-6 · Cited by 87 · see citing works
Comprehensive molecular profiling of lung adenocarcinoma
Lander, E. S. (2014) · DSpace@MIT (Massachusetts Institute of Technology) · Cited by 84 · see citing works
A network-assisted co-clustering algorithm to discover cancer subtypes based on gene expression
Liu, Y., Gu, Q., Hou, J. P., Han, J., & Ma, J. (2014) · BMC Bioinformatics · doi:10.1186/1471-2105-15-37 · Cited by 84 · see citing works
Integrative clustering methods of multi‐omics data for molecule‐based cancer classifications
Wang, D., & Gu, J. (2016) · Quantitative Biology · doi:10.1007/s40484-016-0063-4 · Cited by 81 · see citing works
Matsuoka, T., & Yashiro, M. (2024) · International Journal of Molecular Sciences · doi:10.3390/ijms25115880 · Cited by 83 · see citing works
“…such as Bayesian integration (e.g., Pathway Recognition Algorithm using Data Integration on Genomic Models (PARADIGM) [97], iClusterPlus [98], Patient-specific data fusion (PSDF) [99]), network and pathway integration (e.g., Similarity network fusion (SNF) [100], PaintOmics [101],…”
African-specific molecular taxonomy of prostate cancer
Jaratlerdsiri, W., Jiang, J., Gong, T., Patrick, S. M., Willet, C. E., Chew, T., Lyons, R. J., Haynes, A., Pasqualim, G., Louw, M., et al. (2022) · Nature · doi:10.1038/s41586-022-05154-6 · Cited by 76 · see citing works
Integration of Online Omics-Data Resources for Cancer Research
Das, T., Andrieux, G., Ahmed, M., & Chakraborty, S. (2020) · Frontiers in Genetics · doi:10.3389/fgene.2020.578345 · Cited by 63 · see citing works
EL‐Manzalawy, Y., Hsieh, T.-Y., Shivakumar, M., Kim, D., & Honavar, V. (2018) · BMC Medical Genomics · doi:10.1186/s12920-018-0388-0 · Cited by 70 · see citing works
Sathyanarayanan, A., Gupta, R., Thompson, E. W., Nyholt, D. R., Bauer, D. C., & Nagaraj, S. H. (2019) · Briefings in Bioinformatics · doi:10.1093/bib/bbz121 · Cited by 68 · see citing works
Comprehensive analysis of oncogenic determinants across tumor types via multi-omics integration
Ubaid, S., Kushwaha, R., Kashif, M., & Singh, V. K. (2025) · Cancer Genetics · doi:10.1016/j.cancergen.2025.08.010 · Cited by 72 · see citing works
Yang, Z., Xu, J., Li, L., Li, R., Wang, Y., Tian, Y., Guo, W., Wang, Z., Tan, F., Ying, J., et al. (2020) · Nature Communications · doi:10.1038/s41467-020-18702-3 · Cited by 68 · see citing works
Lu, X., Meng, J., Su, L., Jiang, L., Wang, H., Zhu, J., Huang, M., Cheng, W., Xu, L., Ruan, X., et al. (2021) · Clinical and Translational Medicine · doi:10.1002/ctm2.601 · Cited by 66 · see citing works
A phenotypic and genomics approach in a multi-ethnic cohort to subtype systemic lupus erythematosus
Lanata, C. M., Paranjpe, I., Nititham, J., Taylor, K. E., Gianfrancesco, M. A., Paranjpe, M. D., Andrews, S. V., Chung, S. A., Rhead, B. L., Barcellos, L. F., et al. (2019) · Nature Communications · doi:10.1038/s41467-019-11845-y · Cited by 65 · see citing works
Kong, R., Song, Z., Meng, H., Zhang, X., Shen, G., & Yu, R. (2013) · Biosensors and Bioelectronics · doi:10.1016/j.bios.2013.11.041 · Cited by 64 · see citing works
Deep latent space fusion for adaptive representation of heterogeneous multi-omics data
Zhang, C., Chen, Y., Zeng, T., Zhang, C., & Chen, L. (2021) · Briefings in Bioinformatics · doi:10.1093/bib/bbab600 · Cited by 63 · see citing works
Systematic exploration of cell morphological phenotypes associated with a transcriptomic query
Nassiri, I., & McCall, M. N. (2018) · Nucleic Acids Research · doi:10.1093/nar/gky626 · Cited by 62 · see citing works
The Discovery of Mutated Driver Pathways in Cancer: Models and Algorithms
Zhang, J., & Zhang, S. (2016) · IEEE Transactions on Computational Biology and Bioinformatics · doi:10.1109/tcbb.2016.2640963 · Cited by 60 · see citing works
From systems biology to P4 medicine: applications in respiratory medicine
Noell, G. G., Faner, R., & Agustí, A. G. N. (2018) · European Respiratory Review · doi:10.1183/16000617.0110-2017 · Cited by 60 · see citing works
Xu, A., Chen, J., Peng, H., Han, G., & Cai, H. (2019) · Frontiers in Genetics · doi:10.3389/fgene.2019.00236 · Cited by 59 · see citing works
Integrative Analysis of Omics Big Data
Yu, X., & Zeng, T. (2018) · Methods in molecular biology · doi:10.1007/978-1-4939-7717-8_7 · Cited by 59 · see citing works
Machine learning analysis of TCGA cancer data
Liñares-Blanco, J., Pazos, A., & Fernandez-Lozano, C. (2021) · PeerJ Computer Science · doi:10.7717/peerj-cs.584 · Cited by 60 · see citing works
Machine learning-based analysis of multi-omics data on the cloud for investigating gene regulations
Oh, M., Park, S., Kim, S., & Chae, H. (2020) · Briefings in Bioinformatics · doi:10.1093/bib/bbaa032 · Cited by 55 · see citing works
Zhao, J. Y., Zhao, B., Song, X., Lyu, C., Chen, W., Xiong, Y., & Wei, D. (2023) · Briefings in Bioinformatics · doi:10.1093/bib/bbad025 · Cited by 54 · see citing works
Sin, T. K., Mokhtar, N. M., Hassan, N. Z. A., Sagap, I., Rose, I. M., Harun, R., & Jamal, R. A. (2015) · Oncology Reports · doi:10.3892/or.2015.3993 · Cited by 53 · see citing works
Approximate Graph Laplacians for Multimodal Data Clustering
Khan, A., & Maji, P. (2019) · IEEE Transactions on Pattern Analysis and Machine Intelligence · doi:10.1109/tpami.2019.2945574 · Cited by 52 · see citing works
Sudhakar, P., Verstockt, B., Cremer, J., Verstockt, S., Sabino, J., Ferrante, M., & Vermeire, S. (2021) · Inflammatory Bowel Diseases · doi:10.1093/ibd/izaa281 · Cited by 49 · see citing works
Multi-omics Data Integration Model Based on UMAP Embedding and Convolutional Neural Network
Elkarami, B., Alkhateeb, A., Qattous, H., Alshomali, L., & Shahrrava, B. (2022) · Cancer Informatics · doi:10.1177/11769351221124205 · Cited by 51 · see citing works
Omics for the future in asthma
Abdel‐Aziz, M. I., Neerincx, A. H., Vijverberg, S. J. H., Kraneveld, A. D., & der Zee, A. H. M. (2020) · Seminars in Immunopathology · doi:10.1007/s00281-019-00776-x · Cited by 52 · see citing works
Results of the Seventh Scientific Workshop of ECCO: Precision Medicine in IBD—What, Why, and How
Fiocchi, C., Dragoni, G., Iliopoulos, D., Katsanos, K. H., Hernández, V., Suzuki, K., Verstockt, B., Fiocchi, C., Torres, J., & Scharl, M. M. (2021) · Journal of Crohn s and Colitis · doi:10.1093/ecco-jcc/jjab051 · Cited by 52 · see citing works
NSD1- and NSD2-damaging mutations define a subset of laryngeal tumors with favorable prognosis
Peri, S., Izumchenko, E., Schubert, A. D., Slifker, M. J., Ruth, K. J., Serebriiskii, I. G., Guo, T. W., Burtness, B. A., Mehra, R., Ross, E. A., et al. (2017) · Nature Communications · doi:10.1038/s41467-017-01877-7 · Cited by 50 · see citing works
Preethi, S., Schomay, T. E., Aiello, K. A., & Alter, O. (2015) · PLoS ONE · doi:10.1371/journal.pone.0121396 · Cited by 46 · see citing works
Multi-omics data integration approaches for precision oncology
Aguila, R. C., Alonso-Pupo, N., & Hernández‐Rodríguez, E. W. (2022) · Molecular Omics · doi:10.1039/d1mo00411e · Cited by 48 · see citing works
- Authors
- Mo, Q., Wang, S., Seshan, V. E., Olshen, A. B., Schultz, N., Sander, C., Powers, R. S., Ladanyi, M., & Shen, R.
- Affiliations
- Baylor College of Medicine (US)
- University of Wisconsin–Madison (US)
- Department of Epidemiology and Biostatistics,
- University of California, San Francisco (US)
- Computational Biology Program, and
- Cancer Genome Center, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY 11797
- Memorial Sloan Kettering Cancer Center (US)
- ORCID
- Venue
- Proceedings of the National Academy of Sciences
- Publisher
- National Academy of Sciences
- Published
- 2013-02-21
- Volume
- 110
- Issue
- 11
- Pages
- 4245-4250
- ISSN
- 0027-8424 (ISSN-L)
- 1091-6490
- PMC
- PMC3600490
- OpenAlex
- W2023461603
- Cited by
- 474
- References
- 36
- Citations by year
- 2026: 29 · 2025: 33 · 2024: 34 · 2023: 54 · 2022: 40 · 2021: 74 · 2020: 40 · 2019: 48 · 2018: 27 · 2017: 27 · 2016: 25 · 2015: 23 · 2014: 13 · 2013: 7
- FWCI
- 7.98
- Type
- journal article
- Language
- en
- Open access
- bronze
- doi.org
- Locations
- Proceedings of the National Academy of Sciences (publishedVersion)
- Europe PMC (PubMed Central) (publishedVersion)
- PubMed Central (publishedVersion)
- PubMed (publishedVersion)
- Cold Spring Harbor Laboratory Institutional Repository (Cold Spring Harbor Laboratory) (acceptedVersion)
- eScholarship (California Digital Library) (submittedVersion)
- Funders
- National Cancer Institute (U24CA143840, CA143840, U01CA168409, P30CA008748)
- Topics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Cancer Research › Cancer Genomics and Diagnostics
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Gene expression and cancer classification
- Life Sciences › Biochemistry, Genetics and Molecular Biology › Molecular Biology › Bioinformatics and Genomic Networks
- Keywords
- tumor subtypes, cancer driver genes, integrative clustering, somatic mutations, copy number alterations, gene expression, Cancer Cell Line Encyclopedia, TCGA, colorectal cancer, breast cancer, cancer subtyping, cell of origin
- MeSH terms
- Breast Neoplasms, Female, Gene Expression Regulation, Humans, Male, Colorectal Neoplasms, Genomics, Databases, Genetic, Genes, Neoplasm, Epigenomics
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