Increasing consensus of context-specific metabolic models by integrating data-inferred cell functions

Genome-scale metabolic models provide a valuable context for analyzing data from diverse high-throughput experimental techniques. Models can quantify the activities of diverse pathways and cellular functions. Since some metabolic reactions are only catalyzed in specific environments, several algorithms exist that build context-specific models. However, these methods make differing assumptions that influence the content and associated predictive capacity of resulting models, such that model content varies more due to methods used than cell types. Here we overcome this problem with a novel framework for inferring the metabolic functions of a cell before model construction. For this, we curated a list of metabolic tasks and developed a framework to infer the activity of these functionalities from transcriptomic data. We protected the data-inferred tasks during the implementation of diverse context-specific model extraction algorithms for 44 cancer cell lines. We show that the protection of data-inferred metabolic tasks decreases the variability of models across extraction methods. Furthermore, resulting models better capture the actual biological variability across cell lines. This study highlights the potential of using biological knowledge, inferred from omics data, to obtain a better consensus between existing extraction algorithms. It further provides guidelines for the development of the next-generation of data contextualization methods.

[1]  Steffen Klamt,et al.  An algorithm for the reduction of genome-scale metabolic network models to meaningful core models , 2015, BMC Systems Biology.

[2]  Steffen Klamt,et al.  Memote: A community driven effort towards a standardized genome-scale metabolic model test suite , 2018, bioRxiv.

[3]  Bernhard O. Palsson,et al.  Context-Specific Metabolic Networks Are Consistent with Experiments , 2008, PLoS Comput. Biol..

[4]  Jens Nielsen,et al.  Flux balance analysis predicts essential genes in clear cell renal cell carcinoma metabolism , 2015, Scientific Reports.

[5]  V. Mootha,et al.  Metabolite Profiling Identifies a Key Role for Glycine in Rapid Cancer Cell Proliferation , 2012, Science.

[6]  Aarash Bordbar,et al.  Systems biology analysis of drivers underlying hallmarks of cancer cell metabolism , 2017, Scientific Reports.

[7]  Nathan E. Lewis,et al.  Multi-Tissue Computational Modeling Analyzes Pathophysiology of Type 2 Diabetes in MKR Mice , 2014, PloS one.

[8]  Miguel Rocha,et al.  A Critical Evaluation of Methods for the Reconstruction of Tissue-Specific Models , 2015, EPIA.

[9]  Daniel C. Zielinski,et al.  A Consensus Genome-scale Reconstruction of Chinese Hamster Ovary Cell Metabolism. , 2016, Cell systems.

[10]  Nathan D. Price,et al.  Reconstruction of genome-scale metabolic models for 126 human tissues using mCADRE , 2012, BMC Systems Biology.

[11]  J. Nodwell,et al.  Towards a new science of secondary metabolism , 2013, The Journal of Antibiotics.

[12]  Jason A. Papin,et al.  TIGER: Toolbox for integrating genome-scale metabolic models, expression data, and transcriptional regulatory networks , 2011, BMC Systems Biology.

[13]  J. Cornelis,et al.  Impact of rice cultivar and organ on elemental composition of phytoliths and the release of bio-available silicon , 2014, Front. Plant Sci..

[14]  Monica L. Mo,et al.  Global reconstruction of the human metabolic network based on genomic and bibliomic data , 2007, Proceedings of the National Academy of Sciences.

[15]  T. Golub,et al.  Genomic Copy Number Dictates a Gene-Independent Cell Response to CRISPR/Cas9 Targeting. , 2016, Cancer discovery.

[16]  J. Nielsen,et al.  Identification of anticancer drugs for hepatocellular carcinoma through personalized genome‐scale metabolic modeling , 2014, Molecular systems biology.

[17]  U. Sauer,et al.  Coordination of microbial metabolism , 2014, Nature Reviews Microbiology.

[18]  Nikos Vlassis,et al.  Fast Reconstruction of Compact Context-Specific Metabolic Network Models , 2013, PLoS Comput. Biol..

[19]  Thomas Sauter,et al.  Benchmarking Procedures for High-Throughput Context Specific Reconstruction Algorithms , 2016, Front. Physiol..

[20]  Lake-Ee Quek,et al.  Reducing Recon 2 for steady-state flux analysis of HEK cell culture. , 2014, Journal of biotechnology.

[21]  Markus J. Herrgård,et al.  Network-based prediction of human tissue-specific metabolism , 2008, Nature Biotechnology.

[22]  J. Mesirov,et al.  The Molecular Signatures Database Hallmark Gene Set Collection , 2015 .

[23]  Reinhard Guthke,et al.  Regulatory interactions for iron homeostasis in Aspergillus fumigatus inferred by a Systems Biology approach , 2012, BMC Systems Biology.

[24]  Natapol Pornputtapong,et al.  Reconstruction of Genome-Scale Active Metabolic Networks for 69 Human Cell Types and 16 Cancer Types Using INIT , 2012, PLoS Comput. Biol..

[25]  Alexander Bockmayr,et al.  A mixed-integer linear programming approach to the reduction of genome-scale metabolic networks , 2017, BMC Bioinformatics.

[26]  L. Liau,et al.  Cancer-associated IDH1 mutations produce 2-hydroxyglutarate , 2009, Nature.

[27]  Eytan Ruppin,et al.  iMAT: an integrative metabolic analysis tool , 2010, Bioinform..

[28]  Bernhard O. Palsson,et al.  A detailed genome-wide reconstruction of mouse metabolism based on human Recon 1 , 2010, BMC Systems Biology.

[29]  Ronan M. T. Fleming,et al.  A community-driven global reconstruction of human metabolism , 2013, Nature Biotechnology.

[30]  Ernesto S. Nakayasu,et al.  Model-driven multi-omic data analysis elucidates metabolic immunomodulators of macrophage activation , 2012, Molecular systems biology.

[31]  Jason A. Papin,et al.  Reconciled rat and human metabolic networks for comparative toxicogenomics and biomarker predictions , 2017, Nature Communications.

[32]  Thomas D. Wu,et al.  A comprehensive transcriptional portrait of human cancer cell lines , 2014, Nature Biotechnology.

[33]  Ariën S. Rustenburg,et al.  L-2-hydroxyglutarate production arises from non-canonical enzyme function at acidic pH , 2017, Nature chemical biology.

[34]  Intawat Nookaew,et al.  The RAVEN Toolbox and Its Use for Generating a Genome-scale Metabolic Model for Penicillium chrysogenum , 2013, PLoS Comput. Biol..

[35]  Aarash Bordbar,et al.  A Systems Approach to Predict Oncometabolites via Context-Specific Genome-Scale Metabolic Networks , 2014, PLoS Comput. Biol..

[36]  Zoran Nikoloski,et al.  Generalized framework for context-specific metabolic model extraction methods , 2014, Front. Plant Sci..

[37]  E. Ruppin,et al.  Computational reconstruction of tissue-specific metabolic models: application to human liver metabolism , 2010, Molecular systems biology.

[38]  James M. McFarland,et al.  Computational correction of copy-number effect improves specificity of CRISPR-Cas9 essentiality screens in cancer cells , 2017, bioRxiv.

[39]  Jörg Stülke,et al.  SPABBATS: A pathway-discovery method based on Boolean satisfiability that facilitates the characterization of suppressor mutants , 2011, BMC Systems Biology.

[40]  Anne Richelle,et al.  A Systematic Evaluation of Methods for Tailoring Genome-Scale Metabolic Models. , 2017, Cell systems.

[41]  Anne Osbourn,et al.  From hormones to secondary metabolism: the emergence of metabolic gene clusters in plants. , 2011, The Plant journal : for cell and molecular biology.

[42]  Meagan E. Sullender,et al.  Optimized sgRNA design to maximize activity and minimize off-target effects of CRISPR-Cas9 , 2015, Nature Biotechnology.

[43]  Francisco J. Planes,et al.  Creation and analysis of biochemical constraint-based models: the COBRA Toolbox v3.0. , 2017, 1710.04038.

[44]  Francisco J. Planes,et al.  Assessment of FBA Based Gene Essentiality Analysis in Cancer with a Fast Context-Specific Network Reconstruction Method , 2016, PloS one.

[45]  Miguel Rocha,et al.  Analysing Algorithms and Data Sources for the Tissue-Specific Reconstruction of Liver Healthy and Cancer Cells , 2017, Interdisciplinary Sciences: Computational Life Sciences.

[46]  Neil Swainston,et al.  Recon 2.2: from reconstruction to model of human metabolism , 2016, Metabolomics.

[47]  Anne Richelle,et al.  Assessing key decisions for transcriptomic data integration in biochemical networks , 2019, PLoS Comput. Biol..

[48]  G. von Heijne,et al.  Tissue-based map of the human proteome , 2015, Science.

[49]  Tom M. Conrad,et al.  Omic data from evolved E. coli are consistent with computed optimal growth from genome-scale models , 2010, Molecular systems biology.