Predictive Models for Fast and Effective Profiling of Kinase Inhibitors
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1 Predictive Models for Fast and Effective Profiling of Kinase Inhibitors Alina Bora, 1,2,# Sorin Avram, 2,#, * Ionel Ciucanu, 1 Marius Raica 3, Stefana Avram 4 1 Department of Chemistry, West University of Timisoara, Faculty of Chemistry -Biology-Geography, 16 Pestalozzi Str., , Timisoara, Romania 2 Department of Computational Chemistry, Institute of Chemistry Timisoara of Romanian Academy, 24 Mihai Viteazu Avenue, Timisoara, , Romania 3 Department of Microscopic Morphology/Histology, Angiogenesis Research Center, University of Medicine and Pharmacy Victor Babes Timisoara, 2 Eftimie Murgu, Timisoara, , Romania 4 Department Pharmacy II, Discipline of Pharmacognosy, University of Medicine and Pharmacy Victor Babes Timisoara, Faculty of # These authors contributed equally to the article. Pharmacy, 2 Eftimie Murgu, Timisoara, , Romania *Corresponding author. sorin_avram@acad-icht.tm.edu.ro or 5orin.4vram@gmail.com, Phone: Table S1. Description of kinase sets of actives... 2 Table S2. Standardization steps and parameters applied to process molecular structures using module Chemaxon Standardizer Table S3. Control parameters for random forest model generation using cforest, 6-9 in package party available in R statistical software system Table S4. Number of active and inactive compounds (according to the corresponding data source) in the training and test sets... 5 Table S5. Median, average and standard deviation of the number of compounds and the actives (computed per kinase set) ranked before the top 0.5% FP in the external VS test sets... 7 Table S6. Wilcoxon right shift p-values (α = 0.05): row elements contain significantly greater values compared to column elements; median values are reported in parentheses... 7 Table S7. Classification results of the kinase model prediction for kinase sets with actives and inactives defined as pk i 7 and pk i < 5, respectively, in Metz et al 11 profiling results... 8 Table S8. Classification results of the kinase model prediction for kinase sets with actives and inactives defined as scaled Activity % 0.1 and > 0.9, respectively, in Anastassiadis et al 12 profiling kinase sets Figure S1. Density distribution plots of the activity values (IC 50 in µm) and hot spot cutoff (red line) for the first three kinases (according to the ID number assigned in the paper) in cluster k1 (a), k2 (b), k3 (c) and k4 (d). The plot title contains the UniProt ID of the kinase and the ID number (in parenthesis) used in the paper Figure S2. Dendrograms resulted from Ward hierarchical clustering of 107 kinase sets in a first run (left), resulting in k4 (magenta) and a larger cluster of 103 kinase sets. These were clustered separately into 3 more groups (right) k2 (blue), k3 (red) and k1 (green) Figure S3. Accuracy (Acc), sensitivity (Se) and specificity (Sp) values of the internal (training sets) evaluation of the 107 kinase models Figure S4. Phylogenetic tree of the human kinases (generated using Kinome Render 13, 14 ) Target IDs and abbreviations of the kinases modeled in the current study are colored in red; two Atypical:PI3/PI4-kinase kinases, i.e., PIK3CA and PIK3CG could not be mapped and are not represented. Illustration reproduced courtesy of Cell Signaling Technology, Inc. ( 13 Figure S5. The distributions of (the kinase-set values) eroce (a, performed on the VS test sets) and AUC (b, performed on the classification test sets) according to the nine kinase groups Figure S6. Venn plot (created using the online software from Microarray Center CRP-Sante) 15 of the chemical scaffolds (BMFs) contained in the PubChemKinIna (only inactives), ChEMBL (only kinase inhibitors) and ColBioS-FlavRC 16 datasets
2 Table S1. Description of kinase sets of actives ID 1 Uniprot ID 2 GENE Name Kinase group Kinase Cluster Num of Actives Num of BMFs 3 Actives /BMF 4 avg TanD 5 avg IC 50 6 Hotspot/ IC 50 cutoff 7 1 P35968 KDR TK / P00533 EGFR TK / Q16539 MAPK14 CMGC / P42336 PIK3CA Atypical / P12931 SRC TK / P08581 MET TK /0.4 7 P49841 GSK3B CMGC / O14757 CHEK1 CAMK / O14965 AURKA Other / P04626 ERBB2 TK / P06239 LCK TK / P31749 AKT1 AGC / P48736 PIK3CG Atypical / P42345 MTOR Atypical / P24941 CDK2 CMGC / P08069 IGF1R TK / P45983 MAPK8 CMGC / P06493 CDK1 CMGC / O14920 IKBKB Other / O60674 JAK2 TK / Q96GD4 AURKB Other / P36888 FLT3 TK / P17948 FLT1 TK / P09619 PDGFRB TK / Q02763 TEK TK / P10721 KIT TK / P53779 MAPK10 CMGC / P52333 JAK3 TK /1 29 P11362 FGFR1 TK / O75116 ROCK2 AGC / P00519 ABL1 TK / P11309 PIM1 CAMK / Q08881 ITK TK / P45984 MAPK9 CMGC / Q02750 MAP2K1 STE / P15056 BRAF TKL / P43405 SYK TK /1 38 P04049 RAF1 TKL / Q13464 ROCK1 AGC / Q9P1W9 PIM2 CAMK / O00311 CDC7 Other / P16234 PDGFRA TK / P04629 NTRK1 TK / Q02156 PRKCE AGC /1.3 2
3 45 P49840 GSK3A CMGC / P35916 FLT4 TK / Q5S007 LRRK2 TKL / Q86V86 PIM3 CAMK / P29597 TYK2 TK / P78527 PRKDC Atypical / P49137 MAPKAPK2 CAMK /3 52 P36897 TGFBR1 TKL / P06213 INSR TK / P54760 EPHB4 TK / P17252 PRKCA AGC / P11802 CDK4 CMGC / O15111 CHUK Other / Q05397 PTK2 TK / Q13627 DYRK1A CMGC / P23458 JAK1 TK / P07949 RET TK / P51812 RPS6KA3 AGC / P30530 AXL TK /2 64 P43403 ZAP70 TK / P49759 CLK1 CMGC / P48730 CSNK1D CK / Q15759 MAPK11 CMGC / Q9NWZ3 IRAK4 TKL / Q00535 CDK5 CMGC / P28482 MAPK1 CMGC / Q9HAZ1 CLK4 CMGC / Q13557 CAMK2D CAMK / P51955 NEK2 Other / Q13535 ATR Atypical / P06241 FYN TK / P50613 CDK7 CMGC / Q9UM73 ALK TK / Q05655 PRKCD AGC / P53350 PLK1 Other / Q04759 PRKCQ AGC / P31751 AKT2 AGC / P05771 PRKCB AGC / P08631 HCK TK / O96017 CHEK2 CAMK / O15530 PDPK1 AGC / P07948 LYN TK / Q06418 TYRO3 TK / P24723 PRKCH AGC / P41279 MAP3K8 STE / Q06187 BTK TK / Q9Y243 AKT3 AGC / P05129 PRKCG AGC /2 93 Q12866 MERTK TK /0.23 3
4 94 P33981 TTK Other / Q9Y463 DYRK1B CMGC / Q9UHD2 TBK1 Other / Q13882 PTK6 TK / Q15139 PRKD1 CAMK / Q07912 TNK2 TK / Q9H4B4 PLK3 Other / Q9NYY3 PLK2 Other / Q14289 PTK2B TK / Q14164 IKBKE Other / P30291 WEE1 Other / Q05513 PRKCZ AGC / P34947 GRK5 AGC / O43318 MAP3K7 STE /4.5 1 identifiers used for kinases throughout the paper; 2 UniProt 1, 2 identifiers; 3 number of Bemis-Murko Frameworks (BMFs) 3 ; 4 number of actives per BMF; 5 average of Tanimoto distances per kinase data set; 6 average of IC 50 values per kinase data set; 7 hotspot value and the real maximum IC 50 value (for actives) per kinase set; 8 although NEK2 is classified by UniProt 1, 2 in the NEK group ( Human and mouse protein kinases: classification and index ; version 2015_02; see in text), here, we considered it as a member of Other according to Manning et al 4 ; 8 Atypical: PI3/PI4- kinase. Table S2. Standardization steps and parameters applied to process molecular structures using module Chemaxon Standardizer 5 Step Description Parameter 1 Remove Fragment Remove Fragment, Measure="atomCount", Method="keepLargest" 2 StripSalts 3 Dearomatize 4 Neutralize 5 Transformation Transform Isocyanate, Transform Nitroso, Transform Phosphonic,Transform Phosphonium Ylide, Transform Selenite, Transform Silicate, Transform Sulfine, Transform Sulfon, Transform Sulfonium Ylide, 6 Aromatize Type="basic" Table S3. Control parameters for random forest model generation using cforest, 6-9 in package party available in R statistical software system 10 Command cforest_control(teststat = "max", testtype = "Teststatistic", mincriterion = qnorm(0.9), ntrees = 500, mtry=15) 4
5 Table S4. Number of active and inactive compounds (according to the corresponding data source) in the training and test sets Training sets Classification test sets Virtual screening ID 1 test sets ChEMBL Actives Total Inactives 2 PubChem KinIna ChEMBL inactives ChEMBL Actives Total Inactives 3 PubChem KinIna ChEMBL Inactives PubChem KinIna
6
7 Kinase identification used throughout the article; 2 Sums of inactives from PubChemKinIna and ChEMBL inactives used for training; 3 inactives from PubChemKinIna and ChEMBL inactives used for classification testing; 4 virtual screening test sets are composed from ChEMBL actives (used in the classification test sets) and PubChemKinIna set (after removing inactives used for modeling). Table S5. Median, average and standard deviation of the number of compounds and the actives (computed per kinase set) ranked before the top 0.5% FP in the external VS test sets Cluster Num. of compounds Num. of actives retrieved Novel Actives 1 k1 278 / 302 / / 107 / / 19 / 17.5 k2 217 / 225 / / 28 / / 5 / 4.8 k3 219 / 224 / / 27 / / 5 / 3.8 k4 206 / 213 / / 17 / / 2 / 1.7 All 232 / 259 / / 64 / / 12 / Novel in the sense that these actives share BMFs which were not used in training Table S6. Wilcoxon right shift p-values (α = 0.05): row elements contain significantly higher values compared to column elements; median values are reported in parentheses Internal Classification Acc k1 k2 k3 k4 k1 (0.8725) k2 (0.8308) k3 (0.9167) k4 (0.8308) External Classification test set Acc k1 k2 k3 k4 k1 (0.8919) k2 (0.8676) k3 (0.9167) k4 (0.8919)
8 Sp k1 k2 k3 k4 k1 (0.9200) k2 (0.9038) k3 (0.9487) k4 ( ) Se k1 k2 k3 k4 k1 (0.8571) k2 (0.8421) k3 (0.9167) k4 (0.9125) AUC k1 k2 k3 k4 k1 (0.960) k2 (0.946) k3 (0.969) k4 (0.950) External Virtual Screening test set eroce k1 k2 k3 k4 k1 (0.9127) k2 (0.8900) k3 (0.9585) k4 (0.9639) TPR at 0.5% FP k1 k2 k3 k4 k1 (0.8435) k2 (0.8000) k3 (0.9375) k4 (0.9250) Table S7. Classification results of the kinase model prediction for kinase sets with actives and inactives defined as pki 7 and pki< 5, respectively, in Metz et al 11 profiling results Uniprot ID 1 Se Sp Acc AUC SD Actives Inactives P P P P O O P P P P
9 O Q96GD P P P P P P P Q P Q Q P P P Q5S Q86V P P Q Q P P Q Q9HAZ P P P Q9UM Q P Q Q Q9Y Q9Y Q9UHD Q Q Q Q9H4B Q
10 Table S8. Classification results of the kinase model prediction for kinase sets with actives and inactives defined as scaled Activity % 0.1 and > 0.9, respectively, in Anastassiadis et al 12 profiling kinase sets Uniprot ID 1 Se Sp Acc AUC SD Actives Inactives P P P24941cA Q96GD P P P Q00535p Q00535p Q
11 Figure S1. Density distribution plots of the activity values (IC50 in µm) and hot spot cutoff (red line) for the first three kinases (according to the ID number assigned in the paper) in cluster k1 (a), k2 (b), k3 (c) and k4 (d). The plot title contains the UniProt ID of the kinase and the ID number (in parenthesis) used in the paper. 11
12 Figure S2. Dendrograms resulted from Ward hierarchical clustering of 107 kinase sets in a first run (left), resulting in k4 (magenta) and a larger cluster of 103 kinase sets. These were clustered separately into 3 more groups (right) k2 (blue), k3 (red) and k1 (green). Figure S3. Accuracy (Acc), sensitivity (Se) and specificity (Sp) values of the internal (training sets) evaluation of the 107 kinase models. 12
13 Figure S4. Phylogenetic tree of the human kinases (generated using Kinome Render 13, 14 ) Target IDs and abbreviations of the kinases modeled in the current study are colored in red; two Atypical:PI3/PI4-kinase kinases, i.e., PIK3CA and PIK3CG could not be mapped and are not represented. Illustration reproduced courtesy of Cell Signaling Technology, Inc. ( 13
14 Figure S5. The distributions of (the kinase-set values) eroce (a, performed on the VS test sets) and AUC (b, performed on the classification test sets) according to the nine kinase groups. Figure S6. Venn plot (created using the online software from Microarray Center CRP-Sante) 15 of the chemical scaffolds (BMFs) contained in the PubChemKinIna (only inactives), ChEMBL (only kinase inhibitors) and ColBioS-FlavRC 16 datasets. 14
15 REFERENCES (1) UniProt, C., Reorganizing the Protein Space at the Universal Protein Resource (UniProt). Nucleic Acids Res. 2012, 40, D (2) UniProtKB. (accessed Feb 4, 2015). (3) Bemis, G. W.; Murcko, M. A. The Properties of Known Drugs. 1. Molecular Frameworks. J. Med. Chem. 1996, 39, (4) Manning, G.; Whyte, D. B.; Martinez, R.; Hunter, T.; Sudarsanam, S. The Protein Kinase Complement of the Human Genome. Science 2002, 298, (5) ChemAxon JChem API package, version ; ChemAxon ( (6) Strobl, C.; Hothorn, T.; Zeileis, A. Party on! - A New, Conditional Variable Importance Measure for Random Forests Available in the party Package. The R Journal 2009, 1, (7) Strobl, C.; Malley, J.; Tutz, G. An Introduction to Recursive Partitioning: Rationale, Application, and Characteristics of Classification and Regression Trees, Bagging, and Random Forests. Psychol. Methods 2009, 14, (8) Strobl, C.; Boulesteix, A. L.; Zeileis, A.; Hothorn, T. Bias in Random Forest Variable Importance Measures: Illustrations, Sources and a Solution. BMC Bioinf. 2007, 8, 25. (9) Hothorn, T.; Buhlmann, P.; Dudoit, S.; Molinaro, A.; van der Laan, M. J. Survival Ensembles. Biostatistics 2006, 7, (10) R Development Core Team. R: A Language and Environment for Statistical Computing, version 3.1.1; The R Foundation for Statistical Computing: Vienna, Austria, 2014; (11) Metz, J. T.; Johnson, E. F.; Soni, N. B.; Merta, P. J.; Kifle, L.; Hajduk, P. J. Navigating the Kinome. Nat. Chem. Biol. 2011, 7,
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