Antimalarial Drug Combination Predictions Using the Machine Learning Synergy Predictor (MLSyPred©) tool

Acta Parasitologica - Trang 1-11 - 2024
Abiel Roche-Lima1, Angélica M. Rosado-Quiñones2, Roberto A. Feliu-Maldonado1, María Del Mar Figueroa-Gispert2, Jennifer Díaz-Rivera2, Roberto G. Díaz-González2, Kelvin Carrasquillo-Carrion1, Brenda G. Nieves1, Emilee E. Colón-Lorenzo2, Adelfa E. Serrano2
1Center for Collaborative Research in Health Disparities, University of Puerto Rico, San Juan, USA
2Department of Microbiology and Medical Zoology, School of Medicine, University of Puerto Rico, Medical Sciences Campus, San Juan, USA

Tóm tắt

Antimalarial drug resistance is a global public health problem that leads to treatment failure. Synergistic drug combinations can improve treatment outcomes and delay the development of drug resistance. Here, we describe the implementation of a freely available computational tool, Machine Learning Synergy Predictor (MLSyPred©), to predict potential synergy in antimalarial drug combinations. The MLSyPred© synergy prediction method extracts molecular fingerprints from the drugs’ biochemical structures to use as features and also cleans and prepares the raw data. Five machine learning algorithms (Logistic Regression, Random Forest, Support vector machine, Ada Boost, and Gradient Boost) were implemented to build prediction models. Implementation and application of the MLSyPred© tool were tested using datasets from 1540 combinations of 79 drugs and compounds biologically evaluated in pairs for three strains of Plasmodium falciparum (3D7, HB3, and Dd2). The best prediction models were obtained using Logistic Regression for antimalarials with the strains Dd2 and HB3 (0.81 and 0.70 AUC, respectively) and Random Forest for antimalarials with 3D7 (0.69 AUC). The MLSyPred© tool yielded 45% precision for synergistically predicted antimalarial drug combinations that were annotated and biologically validated, thus confirming the functionality and applicability of the tool.  The MLSyPred© tool is freely available and represents a promising strategy for discovering potential synergistic drug combinations for further development as novel antimalarial therapies.

Tài liệu tham khảo

World Health Organization (2021) World malaria report 2021. Geneva: World Health Organization. https://www.who.int/publications/i/item/9789240040496 Menard D, Dondorp A (2017) Antimalarial drug resistance: a threat to malaria elimination. Cold Spring Harb Perspect Med 7:1–24. https://doi.org/10.1101/cshperspect.a025619 World Health Organization (2022) Global tuberculosis report 2022. Geneva: World Health Organization. https://www.who.int/publications-detail-redirect/9789240083851 Boshoff HIM, Warner DF, Gold B (2023) Editorial: drug-resistant Mycobacterium tuberculosis. Front Cell Infect Microbiol. https://doi.org/10.3389/fcimb.2023.1215294 Bulusu KC, Guha R, Mason DJ, Lewis RPI, Muratov E, KalantarMotamedi Y, Cokol M, Bender A (2016) Modelling of compound combination effects and applications to efficacy and toxicity: state-of-the-art, challenges and perspectives. Drug Discov Today 21:225–238. https://doi.org/10.1016/j.drudis.2015.09.003 Lehar J, Krueger A, Avery W, Heilbut A, Johansen L (2009) Synergistic drug combinations improve therapeutic selectivity. Nat Biotechnol 27:659–666. https://doi.org/10.1038/nbt.1549.Synergistic Sun W, Sanderson PE, Zheng W (2016) Drug combination therapy increases successful drug repositioning. Drug Discov Today 21:1189–1195. https://doi.org/10.1016/j.drudis.2016.05.015 Tallarida RJ (2011) Quantitative methods for assessing drug synergism. Genes Cancer 2:1003–1008. https://doi.org/10.1177/1947601912440575 Bansal M, Yang J, Karan C, Menden MP, Costello JC, Tang H, Xiao G, Li Y, Allen J, Zhong R, Chen B, Kim M, Wang T, Heiser LM, Realubit R, Mattioli M, Alvarez MJ, Shen Y, Gallahan D, Singer D, Saez-Rodriguez J, Xie Y, Stolovitzky G, Califano A, Abbuehl JP, Altman RB, Balcome S, Bell A, Bender A, Berger B, Bernard J, Bieberich AA, Borboudakis G, Chan C, Chen TH, Choi J, Coelho LP, Creighton CJ, Dampier W, Davisson VJ, Deshpande R, Diao L, Di Camillo B, Dundar M, Ertel A, Goswami CP, Gottlieb A, Gould MN, Goya J, Grau M, Gray JW, Hejase HA, Hoffmann MF, Homicsko K, Homilius M, Hwang W, Ijzerman AP, Kallioniemi O, Karacali B, Kaski S, Kim J, Krishnan A, Lee J, Lee YS, Lenselink EB, Lenz P, Li L, Li J, Liang H, Mpindi JP, Myers CL, Newton MA, Overington JP, Parkkinen J, Prill RJ, Peng J, Pestell R, Qiu P, Rajwa B, Sadanandam A, Sambo F, Sridhar A, Sun W, Toffolo GM, Tozeren A, Troyanskaya OG, Tsamardinos I, Van Vlijmen HWT, Wang W, Wegner JK, Wennerberg K, Van Westen GJP, Xia T, Yang Y, Yao V, Yuan Y, Zeng H, Zhang S, Zhao J, Zhou J (2014) A community computational challenge to predict the activity of pairs of compounds. Nat Biotechnol 32:1213–1222. https://doi.org/10.1038/nbt.3052 Chen L, Li BQ, Zheng MY, Zhang J, Feng KY, Cai YD (2013) Prediction of effective drug combinations by chemical interaction, protein interaction and target enrichment of KEGG pathways. Biomed Res Int 2013:1–10. https://doi.org/10.1155/2013/723780 Huang L, Li F, Sheng J, Xia X, Ma J, Zhan M, Wong STC (2014) DrugComboRanker: drug combination discovery based on target network analysis. Bioinformatics 30:228–236. https://doi.org/10.1093/bioinformatics/btu278 Jin G, Zhao H, Zhou X, Wong STC (2011) An enhanced Petri-Net model to predict synergistic effects of pairwise drug combinations from gene microarray data. Bioinformatics 27:310–316. https://doi.org/10.1093/bioinformatics/btr202 Li S, Zhang B, Zhang N (2011) Network target for screening synergistic drug combinations with application to traditional Chinese medicine. BMC Syst Biol 5:1–13. https://doi.org/10.1186/1752-0509-5-S1-S10 Yang J, Tang H, Li Y, Zhong R, Wang T, Wong STC, Xiao G, Xie Y (2015) DIGRE: drug-induced genomic residual effect model for successful prediction of multidrug effects. CPT Pharmacometr Syst Pharmacol 4:91–97. https://doi.org/10.1002/psp4.1 Zhao J, Zhang XS, Zhang S (2014) Predicting cooperative drug effects through the quantitative cellular profiling of response to individual drugs. CPT Pharmacometr Syst Pharmacol 3:1–7. https://doi.org/10.1038/psp.2013.79 Zhao XM, Iskar M, Zeller G, Kuhn M, van Noort V, Bork P (2011) Prediction of drug combinations by integrating molecular and pharmacological data. PLoS Comput Biol. https://doi.org/10.1371/journal.pcbi.1002323 Baker RE, Peña JM, Jayamohan J, Jérusalem A (2018) Mechanistic models versus machine learning, a fight worth fighting for the biological community? Biol Lett 14:1–4. https://doi.org/10.1098/rsbl.2017.0660 Rowe M (2019) An introduction to machine learning for clinicians. Acad Med 94:1433–1436. https://doi.org/10.1097/ACM.0000000000002792 Sun Y, Sheng Z, Ma C, Tang K, Zhu R, Wu Z, Shen R, Feng J, Wu D, Huang D, Huang D, Fei J, Liu Q, Cao Z (2015) Combining genomic and network characteristics for extended capability in predicting synergistic drugs for cancer. Nat Commun. https://doi.org/10.1038/ncomms9481 Preuer K, Lewis RPI, Hochreiter S, Bender A, Bulusu KC, Klambauer G (2018) DeepSynergy: predicting anti-cancer drug synergy with deep learning. Bioinformatics 34:1538–1546. https://doi.org/10.1093/bioinformatics/btx806 Cuvitoglu A, Zhou JX, Huang S, Isik Z (2019) Predicting drug synergy for precision medicine using network biology and machine learning. J Bioinform Comput Biol 17:1–24. https://doi.org/10.1142/S0219720019500124 Zagidullin B, Aldahdooh J, Zheng S, Wang W, Wang Y, Saad J, Malyutina A, Jafari M, Tanoli Z, Pessia A, Tang J (2019) DrugComb: an integrative cancer drug combination data portal. Nucleic Acids Res 47:W43–W51. https://doi.org/10.1093/nar/gkz337 Li P, Huang C, Fu Y, Wang J, Wu Z, Ru J, Zheng C, Guo Z, Chen X, Zhou W, Zhang W, Li Y, Chen J, Lu A, Wang Y (2015) Large-scale exploration and analysis of drug combinations. Bioinformatics 31:2007–2016. https://doi.org/10.1093/bioinformatics/btv080 Li X, Qin G, Yang Q, Chen L, Xie L (2016) Biomolecular network-based synergistic drug combination discovery. Biomed Res Int 2016:8518945. https://doi.org/10.1155/2016/8518945 Mason DJ, Stott I, Ashenden S, Weinstein ZB, Karakoc I, Meral S, Kuru N, Bender A, Cokol M (2017) Prediction of antibiotic interactions using descriptors derived from molecular structure. J Med Chem 60:3902–3912. https://doi.org/10.1021/acs.jmedchem.7b00204 Mason DJ, Eastman RT, Lewis RPI, Stott IP, Guha R, Bender A (2018) Using machine learning to predict synergistic antimalarial compound combinations with novel structures. Front Pharmacol 9:1096. https://doi.org/10.3389/fphar.2018.01096 Mott BT, Eastman RT, Guha R, Sherlach KS, Siriwardana A, Shinn P, McKnight C, Michael S, Lacerda-Queiroz N, Patel PR, Khine P, Sun H, Kasbekar M, Aghdam N, Fontaine SD, Liu D, Mierzwa T, Mathews-Griner LA, Ferrer M, Renslo AR, Inglese J, Yuan J, Roepe PD, Su XZ, Thomas CJ (2015) High-throughput matrix screening identifies synergistic and antagonistic antimalarial drug combinations. Sci Rep 5:1–14. https://doi.org/10.1038/srep13891 Muthuselvi M, Sindhumathi S, Swetha R (2020) Gui based prediction of heart stroke stages by supervised machine learning algorithm. IJARIIE 6(2):11823 Kadiyala A, Kumar A (2017) Applications of Python to evaluate environmental data science problems. Environ Prog Sustain Energy 36:1580–1586. https://doi.org/10.1002/ep.12786 G. Landrum (2019) “RDKit Documentation.” RDKit. https://buildmedia.readthedocs.org/media/pdf/rdkit/latest/rdkit.pdf Cereto-Massagué A, José M, Valls C, Mulero M, Garcia-vallvé S, Pujadas G (2015) Molecular fingerprint similarity search in virtual screening. Methods 71:58–63. https://doi.org/10.1016/j.ymeth.2014.08.005 Sud M (2016) MayaChemTools: an open source package for computational drug discovery. J Chem Inf Model 56:2292–2297. https://doi.org/10.1021/acs.jcim.6b00505 Glen RC, Bender A, Arnby CH, Carlsson L, Boyer S, Smith J (2006) Circular fingerprints: flexible molecular descriptors with applications from physical chemistry to ADME. IDrugs 9:199–204 Pedregosa F, Weiss R, Brucher M (2011) Scikit-learn: machine learning in Python. J Learn Res 12:2825–2830. https://doi.org/10.5555/1953048.2078195 Breiman LEO (2001) Random forests. Mach Learn 45:5–32. https://doi.org/10.1023/A:1010933404324 Cessie Le, Van Houwelingen JC (2013) Ridge estimators in logistic regression. J R Stat Soc Ser C Appl Stat 41:191–201 Suykens JA, Vandewalle J (1999) Least squares support vector machine classifiers. Neural Process Lett 9:293–300 Friedman JH (2001) Greedy function approximation: a gradient boosting machine. Ann Stat 29:1189–1232. https://doi.org/10.1214/aos/1013203451 Visa S, Ramsay B, Ralescu A, Van Der Knaap E (2011) Confusion matrix-based feature selection Sofia visa. In: Proceedings of the 22nd Midwest artificial intelligence and cognitive science conference 2011, pp 120–127 Bradley AP (1997) The use of the area under the ROC curve in the evaluation of machine learning algorithms. Pattern Recognit 30:1145–1159. https://doi.org/10.1016/S0031-3203(96)00142-2 Kalantarmotamedi Y, Eastman RT, Guha R, Bender A (2018) A systematic and prospectively validated approach for identifying synergistic drug combinations against malaria. Malar J 17:1–15. https://doi.org/10.1186/s12936-018-2294-5 Ling CX, Schultz MG, Eskin E, Zadok E, Stolfo SJ, Mitra S, Pal SK, Mitra P (2008) Data mining for direct marketing: problems and Ling, Charles X. In: Proc 7th USENIX secur symp, vol 98, pp 38–49 Chawla NV, Bowyer KW, Hall LO (2002) SMOTE: synthetic minority over-sampling technique. J Artif Intell Res 16:321–357. https://doi.org/10.1613/jair.953 Batista GE, Prati RC, Monard M (2004) A study of the behavior of several methods for balancing machine learning data. SIGKDD Explor 6:20–29. https://doi.org/10.1145/1007730.1007735 Rizopoulos D (2018) Max Kuhn and Kjell Johnson applied predictive modeling. Biometrics 74:378–384. https://doi.org/10.1111/biom.12855