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Andy QiMass SpectrometryShotgun proteomicsLung Cancer3rd generation egfr tkiLung adenocarcinomaResistance mechanismhttps://www.ebi.ac.uk/pride/archive/projects/PXD020108LungCell culture and treatment H1975 parental cell line was obtained from ATCC. The resistant cell lines AZR3/AZR4 (resistant to osimertinib) and COR1/COR10 (resistant to rociletinib) and were obtained from AstraZeneca and Colvis Oncology, respectively. The cells were cultured at 37 °C, 5% CO2 in RPMI medium 1640 with 10% dialyzed fetal bovine serum and 1% penicillin/streptomycin for at least five passages to completely label the proteome with stable isotope labeled heavy Arg and Lys for three-state SILAC experiments. The three state SILAC-labeled cells were TKI-sensitive cell line H1975 (light), the TKI-resistant cell lines AZR3 and COR1 (medium), and the TKI-resistant cell lines AZR4 and COR10 (heavy). The medium state cells were labeled with 13C6-Arg/D4-Lys and the heavy state cells were labeled with 13C615N4-Arg/13C615N2-Lys. Upon complete labeling, the cells were expanded to 15 cm dishes. The resistant cell lines were grown in the presence of TKIs until 3 days before the experiment. Each set of the SILAC labeled cells were treated either with DMSO or the corresponded drugs (50 nM osimertinib or 100 nM rociletinib) for one hour, respectively before harvesting. Protein extraction and sample processing Cells were lysed with urea lysis buffer (20 mM HEPES pH 8.0, 8 M urea, 1 mM sodium orthovanadate, 2.5 mM sodium pyrophosphate and 1 mM-glycerophosphate). Protein concentrations were determined by the Modified Lowry method. Equal amounts of protein from lysates of each SILAC state were mixed together. The combined lysate was reduced with 45 mM dithriothreitol, alkylated with 100 mM iodoacetamide, and subsequently digested with trypsin at 37 °C overnight. The digest was then acidified with 1% TFA and peptides were desalted using C18 solid phase extraction columns, lyophilized and stored at -80° C. Basic reversed phase liquid chromatography fractionation Basic-RPLC separation was performed with an XBridge C18, 100 x 2.1 mm analytical column containing 5 mm particles and equipped with a 10 x 2.1 mm guard column (Waters, Milford, MA) with a flow rate of 0.25 ml/min. The solvent consisted of 10 mM triethylammonium bicarbonate (TEABC) as mobile phase A, and 10 mM TEABC in ACN as mobile phase B. Sample separation was accomplished using the following linear gradient: from 0 to 1% B in 5 min, from 1 to 10% B in 5 min, from 10 to 35% B in 30 min, and from 35 to 100% B in 5 min, and held at 100% B for an additional 3 min. A total of 96 fractions were collected during the LC separation in a 96-well plate containing 12.5 ml of 1% formic acid for immediate acidification. The collected fractions were concatenated into 12 fractions and dried in a vacuum centrifuge. 1/10th of the peptides was injected directly for LC-MS/MS analysis from protein identification. Enrichment of Phosphopeptides Remaining 9/10th of the dried peptides were dissolved in solution A containing 80% ACN, 1% TFA, and 3% 2, 5-DHB and incubated with TiO2 pretreated (2 h at room temperature) with solution A. After 12 h, TiO2 beads were washed thrice using solution A and twice with 80% ACN containing 1% TFA. TiO2 bound peptides were eluted using 3% NH4OH in 40% ACN and immediately acidified using formic acid. The peptides were vacuum dried, C18 stage-tip cleaned before LC-MS/MS analysis. Phosphotyrosine peptides were enriched using a PhosphoScan Kit (p-Tyr-100 and p-Tyr-1000, Cell Signaling, Danvers, MA). The lyophilized peptide was dissolved in IAP buffer (50 mM MOPS, pH 7.2, 10 mM sodium phosphate, 50 mM NaCl) and incubated with 40 ml of immobilized anti-phosphotyrosine antibody for 1 h at 4°C. The antibody beads were centrifuged for 1 min at 1500 x g, and the supernatant was separated and saved. The antibody-bound beads were washed 3 times with 1ml of IAP buffer and twice with water by inverting tube 5 times at 4 °C. The phosphotyrosine-containing peptides were eluted from antibody with 55 ml of 0.15% TFA by gently tapping the bottom of the tube and incubating at room temperature for 10 min. LC-MS/MS Analysis Peptides were analyzed on a Q Exactive HF interfaced with an UltimateTM 3000 RSLCnano System. The dried peptides and the enriched phosphopeptides were loaded onto a nano-trap column (Acclaim PepMap100 Nano Trap Column) and separated on an Easy-sprayTM C18 LC column (Acclaim PepMap100). Mobile phases A and B consisted of 0.1% formic acid in water and 0.1% formic acid in 90% ACN, respectively. Peptides were eluted from the column at 300 nL/min using the following linear gradient: from 4 to 35% B in 60 min, from 35 to 45% B in 5 min, from 45 to 90% B in 5 min, and held at 90% B for an additional 5 min. The heated capillary temperature and spray voltage were 275 °C and 1.7 kV, respectively. Full spectra were collected from 350 to 1800 m/z in the Orbitrap analyzer at a resolution of 120,000, followed by data dependent HCD MS/MS scans of the fifteen most abundant ions at a resolution of 30,000, using 40% collision energy and dynamic exclusion time of 30s.PrideData Analysis Peptides and proteins were identified and quantified using the MaxQuant software package (version 1.5.7.4) with the Andromeda search engine. MS/MS spectra were searched against the Uniprot human protein database (Feb 2017) and quantification was performed using default parameters for 3 state SILAC in MaxQuant. The parameters used for database search include trypsin as a protease with two missed cleavage sites allowed. Carbamidomethyl cysteine was specified as a fixed modification. Phosphorylation at serine, threonine and tyrosine, deamidation of asparagine and glutamine, oxidation of methionine and protein N-terminal acetylation were specified as variable modifications. The precursor mass tolerance was set to 7 ppm and fragment mass tolerance to 20 ppm. False discovery rate was calculated using a decoy database and a 1% cut-off was applied to both peptide table and phosphosite table. Combined normalized SILAC ratio of the proteins and the phosphopeptides and individual ratios of each experiment were obtained from the MaxQuant search. Perseus (version 1.5.5.3) was used to view and further analyze the data. Hierarchical clustering of proteins and phosphorylation were obtained in Perseus using log2 SILAC ratios. One sample t-test was performed in Perseus and the proteins or phosphopeptides with the p-value less than 0.05 and the SILAC ratio above 1.5-fold changes were considered as significantly changed. Kinase Enrichment Analysis The goal of the enrichment analysis was to identify kinases whose targets were significantly over-represented among the phosphorylation sites that were significantly hyper- or hypo-phosphorylated in drug-resistant vs. sensitive cells when matched with the kinase-target site data in iPTMnet v.4.1. The enrichment analysis was performed at the level of kinase families rather than individual kinases. Human kinases in iPTMnet were classified into families using a mapping table provided by KinBase (http://kinase.com/web/current/human/). Phosphorylation sites that were significantly hyper- or hypo-phosphorylated in drug resistant vs. sensitive cells were selected using volcano plots (p-value greater than 0.05 and more than 1.5-fold change). Kinases for these sites were retrieved from iPTMnet using the iptmnetr R package (https://cran.r-project.org/web/packages/iptmnetr/index.html) and mapped to kinase families as above. An enrichment p-value for each family was obtained by performing Fisher’s Exact Test on the two-by-two contingency table. Only families whose kinases phosphorylated three or more significantly changed sites were included in the analysis. Calculations for significantly hyper- or hypophosphorylated sites were done separately. Multiple testing correction was performed with the Benjamin-Hochberg method. All statistical calculations were carried out using R. Drug Signature Comparison Drug signature comparisons were performed using two methods. First, we used querying Touchstone-P, a library of phosphoproteomic signatures from several cell lines treated with a panel of small molecule drugs (46). The Proteomic Query tool, available through the ConnectivityMap web interface (http://clue.io/proteomics-query), compares an input P100 phosphorylation signature to each signature in the library and reports a connectivity score ranging from -1 (strong negative connection/most “opposite” profile) to 1 (strong positive connection/most similar profile). The tool can calculate scores for data with and without replicates. To analyze our data with replicates, for each replicate of each cell line/drug combination in our dataset, we constructed a list of the log2 abundance ratios (TKI-resistant vs. sensitive) for all sites in the P100 set for which we had data. Replicates in which fewer than 40 of the P100 sites were observed were discarded. Depending on the cell line/drug combination, between two and four replicates had enough P100 data to be included in the analysis. The data was formatted as a gct file using the parse.gctx function in the cmap/cmapR R package (https://rdrr.io/github/cmap/cmapR) and submitted to the Proteomics Query tool to obtain connectivity scores. We also calculated the mean log2 abundance ratio across all replicates for the P100 sites observed in each cell line/drug combination in our data and submitted these profiles to the Proteomics Query tool using the “no replicates” option. Second, we calculated the Pearson correlation coefficient between each cell line/drug combination in our dataset and each experiment in the P100 dataset. We obtained the P100 data for this analysis from the P100 Level 3 data file P100Level3.08_16_2016.gct.txt.ProteomicsUdayan GuhaThoracic and GI Malignancies Branch, CCR, NCI, NIH, Bethesda, MDPARTIALHomo Sapiens (human)andy.qi@nih.govNot availableCenter for Alzheimer’s Disease and Related Dementias (CARD)/NIHUnited Statessodium salt, Water, ammonium formate, 13C-labeled, ion, AI326280, Longterm., H(2)O, SCP3, Visible Light, l(3)72Dc, magnesium formate, Capillary, zinc salt, heavy chain disease, Solvent, P270, WATER, HOH, dmTAF[[II]]230, diap1/thread, Glycerolphosphate, Beds, B1, SCO5, SCO1, Sodium Ion, nup154, SET, C79325, N'-bis(aminoiminomethyl)-, K, cel, 2-amino-3-(4-hydroxyphenyl)propanoic acid, 3-(p-Hydroxyphenyl)alanine, R, dimethyl sulphoxide, W, Y, Sinusoidal Bed, DmelCG4299, c, salt, LYS, dibasic, h, disodium acid phosphate, D1, Solid Phase Extractions, Acn, n, osimertinib mesilate, Bs, osimertinib mesylate, nickel salt, Diha, LC-MS2, hOSA1, sulfinylbis-, eye-lt-m03Jus-gt-, dTAF[[II]]230, dILP, cobalt (+2) salt, UNQ391/PRO726, Longterm Effect, arginine, Light, Intestinal alkaline phosphatase, Sinusoids, tip, Expanded, OA3, dibasic (anhydrous), (CH3)2SO, common salt, sodium (4:1:1) salt, LIGHT, magnesium salt, 1270, trisodium phosphate, DIAPI, Sulfinylbis(methane), Estreptomicina Normon, AI848868, pbt, DI-2, Rimso50, I-2Dm, OSA1, formate, expanded, Ex, Iap1, Solid Phase, DIAP1, DIAP2, I-2PP1, Lysm, light quantum, B cell receptor accessory molecule complex, Taf250, label, liquid chromatography-tandem mass spectroscopy, duct, B lymphocyte receptor complex, bacteriolytic toxin activity, ammonium (4:1) salt, Cell Cultures, Diap2, Diap1, tlp, AW108519, Dimethyl, developmental stage, number, l(3)72CDe, 17alpha)-isomer, CG7826, agua, mass-to-charge ratio, Ion Level, Sulphoxide, Gene Products, CG7835, dIAP-1, Capillary Bed, AZD-9291 mesylate, Technique, sulfinylbis(methane), DmelCG18104, anatomical systems, dTAF[[II]]250, sodium (2:3) salt, Acinus, thallium (+1) salt, Longterm, cell, Lichtquant, rubidium salt, BAF250, Argos, 2pp2a, albino, CG4531, ions, CG10574, acinusL, Study, dTAF250, drugs, acinusS, BRG1-associated factor 250, dSet, peptidos, S048915, rlt, 4-(2-hydroxyethyl)-, dibasic sodium phosphate, PTHB1, Pharmaceuticals, N-(2-((2-(dimethylamino)ethyl)methylamino)-4-methoxy-5-((4-(1-methyl-1H-indol-3-yl)-2-pyrimidinyl)amino)phenyl)-2-propenamide methanesulfonate (1:1), Lyzs, proto-oncogene c-Kit, BM029, CG4114, copper (+2) salt, CD258, buffer, mKIAA0670, Abll, dTAF230, Experiment, native protein, Temperatures, carbonyldiamide, C18, cupric formate, chemical analysis, Long Term Effects, Sodium, NaCl, l(3)05959, aluminum formate, Sinusoidal, dJ142L7.2, XKrk1, AU020952, MRD14, Taf[[II]]250, Calcium, Diap-1, holin, ensemble, HVEM-L, Separations, (2S)-2-amino-5-guanidinopentanoic acid, CG4579, dimethyl sulfoxide, Na, Natrium, CDA08, l(2)01270, plan specification, disodium hydrogen phosphate, Aos, Photoradiations, Capillary Beds, signalling process, C-Kit, dodecahydrate, EG:65F1.3, Sodium 23, reversed, Integrin-associated protein, zinc formate, HEPES Monosodium Salt, lead salt, protein, B-cell receptor complex, diap 1, peptide, BAF250a, Techniques, ammonium tetraformate, peptido, skc35, Pharmaceutical Product, Arg, protein aggregate, IAP, l(3)j5C8, HEPES Monosodium, mKIAA0458, LCMSMS, peptides, TAF-I, membrane bound, ATN1L, E927b, 2610036I19Rik, hypoplasia, mAPC, arg, IGAAD, Tagrisso, TNFSF14, lithium salt, DmelCG10574, 1-Piperazineethanesulfonic acid, Fetal, Pharmaceutical, Tyr, disease management, TEAB, blood capillary, dihydrogen oxide, B-lymphocyte receptor complex, Sl, ammonium (2:1) salt, Long-Term Effects, Sinusoid, Tube, ZC2HC5, 32P-labeled, 2-Amino-3-(p-hydroxyphenyl)propionic acid, Dmel_CG7826, StF-IT-1, Tr-kit, Th, HTATIP1, TAFII-250, TAF250/230, Sodium-23, TAFII250, DIAP I, bacteriocin activity, KIT, nickel (+2) salt, CD47, Dmel_CG7835, Lines, Rimso 50, MNB, SHEP3, tyrosine-protein kinase Kit, ammonium salt, resistant, cobaltous formate, CG4299, AW124434, CG17603, Methodological Study, TAF[[II]], Treatments, acqua, lysin activity, enlarged, copper salt, l(2)ey, Wasser, HEPES, i2pp2a, 1728, dIap1, MOPS, Procedures, SPGF4, cesium salt, SCF receptor activity, Rimso 100, dTAFII250, disodium hydrogen phosphate anhydrous, neutral sodium hydrogen phosphate, PHAPII, hELD, morpholine propanesulphonic acid, l(3)rQ526, BCR complex, dmTAF1, 14C-labeled, Studies, sodium dihydrogen phosphate, Strepto Hefa, tiny, Cell Culture, immunoglobulin complex, TAF250, l(2)10432, Fdc, D-Streptamine, Glycerophosphate, ipp2a2, DIAP, AW742570, calcium formate, 3.1.3.1, diap, Bovine, Estreptomicina CEPA, great, Long-Term Effect, l(2)01501, Preparation, TAF, 2-iodo-, small, DYRK1, TAF[[II]]250, heptahydrate, sodium phosphate, protein complex, igaad, Cell Lines, l(3)84Ab, strontium salt, group, count in organism, LC/MS/MS, OCA1A, Cor1, p230, water, I2PP2A, CG8293, Dyrk1, Sulfoxide, Bovine Serum Albumin, (3alpha, tetrasodium pyrophosphate, sodium phosphate monobasic anhydrous, Radiations, E(rpr)3-1, C1orf4, c-KIT, nup32D, 10^[-9], glyceric acid phosphates, PRSS, TAF[[II]]230, CC1, Tripcellim, sample population, chromic formate, Drug, Protein Gene Products, AA407862, dSET/TAF-Ibeta, Preparations, 2610030F17Rik, DmelCG17603, Therapeutic, calcium salt, Treatment, 3-OHECN, TAF1, Methane, Glycerolphosphates, PLIP, cadmium salt, Product, Calf Serum, Scp3, BOUND WATER, Basodexan, oxidane, Type 2A-interacting protein, DIHA, Long Term, 5730420M11Rik, actin-dependent regulator of chromatin subfamily F member 1, Polypeptides, KL receptor activity, Fetal Bovine Serum, cobalt(II) formate dihydrate, Method, tribasic, hnu, Line, DIAP-1, DIAP-2, Gsfsow3, HTATIP, O-2-deoxy-2-(methylamino)-alpha-L-glucopyranosyl-(1-2)-O-5-deoxy-3-C-formyl-alpha-L-lyxofuranosyl-(1-4)-N, treatment, (S)-2-amino-5-guanidinopentanoic acid, Divorced, TFIID TAF250, 32P2-labeled cpd, Salt, l(3)S030605, Divorces, AI047805, Bed, allergic reaction, set, Strepto-Hefa, Lys, column, cPLA2, medicine, 0736/01, anatomical tube, Lysin, ACN, sample, stage, autolysin activity, TIP, Dimethylsulfoxid, ELD, Lzm, single organism signaling, trisodium phosphate dodecahydrate, diap-1, Lzp, DMSO, Radiation, dmso, Liquid Chromatography, TAF200, Bovine Albumin, Penicillin, Procedure, antibodies, ANAC091, Calcium Glycerophosphate, Putative MAPK-activating protein PM10, PBT, H2O, Dm1, Tyrosine O phosphate, Fetal Calf Serum, sodium, Streptomycine Panpharma, TIP60, natrium, CG18104, Hydrogen Oxide, Culture Technique, HVEML, HLA-DR-associated protein II, disodium salt, cromium (+3), alpha, Methodological, LNKN-1, IAP2, beta Trypsin, IAP1, TAF-IBETA, dihydrogen phosphate (ester), Tyrosine-O-phosphate, TAF-Ibeta, lead (+2) salt, L-tyrosine, TIP41, TAF230, krk1, big, CO-1686, nickel formate dihydrate, lead formate, Effects, aluminum salt, dimethylsulfoxyde, high weight, Strepto Fatol, Carbamide, glycerophosphate, protein-containing complex, thomson, ESA1, Ly113, large, DmelCG4114, sensitive, LC-MSMS, heavy, CG42273, Carmol, l(3)S106503, 2310061K05Rik, Sinusoidal Beds, Monosodium Salt, beta-Trypsin, Extractions, Long-Term, methanoic acid, Cell Culture Technique, Solution, Rimso-50, dimetil sulfoxido, DmelCG4579, ms(2)zk, N-(2-((2-(dimethylamino)ethyl)methylamino)-4-methoxy-5-((4-(1-methyl-1H-indol-3-yl)-2-pyrimidinyl)amino)phenyl)-2-propenamide, Rimso, 2PP2A, Kochsalz, photon, dSET, L-Arg, Antibiotics, TR2, D8Wsu49e, Tyrosin, Streptomycin Grünenthal, ABLL, Products, decahydrate, SMARCF1, Phosphotyrosine, Atr2, BcDNA:LD21772, Proteins, potassium formate, BG:DS00004.13, MER6, anhydrous sodium pyrophosphate, backward, Cell, 1065/03, polypeptide, tetrasodium salt, Natriumchlorid, I-2PP2A, tirosina, KIT ligand receptor activity, Dimethylsulphoxide, Dm I-2, TAF[[II]]250/230, 5alpha, Diap-1/Th, Sodium Ion Level, BAF250A, lithium formate, Pharmaceutic Preparations, underdeveloped, Sclerosol, Dimethyl Sulphoxide, mereletinib, eyes3, CD117, SWI|SNF complex protein p270, l(3)05845, monobasic anhydrous, Longterm Effects, ME-IV, DmelCG4531, Gene Proteins, matrix-associated, AZD9291 mesylate, ARID domain-containing protein 1A, Fetal Bovine, Ssm, l(3)rJ472, xkl-1, liquid chromatography tandem mass spectrometry, [OH2], Pharmaceutical Products, liquid chromatography tandem mass spectroscopy, Nup32D, IPP2A2, 1110033A15Rik, insensitive, determination, Xkl-1, Serum, DNB1, B430305P08Rik, brl, sodium diphosphate, sodio, Gsfsco1, halite, Streptomycin Sulfate, mereletinib mesilate, BANF, dJ69E11.3, SWI|SNF-related, Min, ARG, sty, Gsfsco5, Effect, foton, Rheumabene, DmelCG42273, SOW3, Penicillin Antibiotics, ARP, 3-hydroxy-5-estrane-17-carbonitrile, D-IAP2, D-IAP1, (S)-2-Amino-5-guanidinovaleric acid, 2610510L13Rik, epsilon-diaminocaproic acid, min, analyzer, copper, cloruro sodico, fSAP152, Dimethylsulfoxide, Methodological Studies, Therapies, sodium hydrophosphate, dihydridooxygen, necrosis, D-iap1, D-iap2, sodium biphosphate, AZD9291, gamma, L-Arginin, Therapy, phapii, monobasic, rock salt, dimethyli sulfoxidum, diap2, diap1, methylsulfinylmethane, EG:171D11.4, Osa homolog 1, LC-MS/MS, aqua, glyceric acid phosphate, ur, TUBE, carbamide, HCD, anhydrous, Ionen, Streptomycin Sulphate, kl1-A, B120, Pharmaceutic, Lzm-s1, phosphoric acid, OCAIA, Fetal Calf, Visible Radiations, Mnb, Visible Radiation, l(3)S030605b, acidification, hydrogen hydroxide, kit, natrii chloridum, Bovine Serum, monosodium salt, H2NC(O)NH2, immunoglobulin, AZD-9291, Acetamide, SR3-5, Polypeptide, Proteomes, DmelCG8293, dIAP2, dIAP1, sodium dihydrogen orthophosphate, d230, Gene, ACINUS, mereletinib mesylate, EfW1, presence, LC-MS-MS, L-(+)-arginine, Buffer, formic acid, Karbamid, antibody, method, potassium salt, (2S)-2-amino-5-(carbamimidamido)pentanoic acid, reduced, scfr, Strepto-Fatol, Taf230, SWI-like protein, method used in an experiment, Arabidopsis NAC domain containing protein 91, MOD_RES Phosphotyrosine, Harnstoff, zk, l(3)j5E11, Level, SCFR, CG12284, Separated, sensitivity, S(O)Me2, Drugs, Taf200, Gm17754, iones, diphosphoric acid, chlorure de sodium, Taf1p, labeling, Itgp, Visible, eau, Dimethylsulphinyl, lysate, taf-ibeta, CMM8, DmAos, Albumin Bovine, N-2-Hydroxyethylpiperazine-N'-2'-ethanesulfonic Acid, cromium (+3) salt, dIAP, sodium formate, disodium pyrophosphate, Culture Techniques, nickel formate, Ilp, total expressed protein, strontium formate, COR1, QCR1, 9130415E20Rik, Medications, Extraction, Peptide, Isotope, l(3)rJ812, capillary vessel, Phosphopeptide, Dimexide, Protein, AI551343, TFIID, table salt, Diap, Vacuums, DIAPII, AI414665, trisodium salt, opsonin activity, Separation, Streptomycin Sulfate (2:3) Salt, gil, uree, DmelCG12284, Photoradiation, N 2 Hydroxyethylpiperazine N' 2' ethanesulfonic Acid, TAF[II]250, LTg, Trypure, trisodium pyrophosphate, 11Na, c-kit, Albumin, BRG1-associated factor 250a, Ion, monosodium dihydrogen phosphate, Estreptomicina Clariana, TCV-interacting protein, B cell receptor activity, AA536808, Peptid, assay, dimethyl sulfur oxide, AA407739, SCH, Pharmaceutical PreparationDER/faint little ball, Elp-B1RB1, Products, Elp, D-Egf, Product, Wa5, l(2)09261, TGF-alpha receptor activity, ERBB, C-erb, dEGFR1, DEgfr, drug, Elp-B1, der, Elp-1, mor1, total expressed protein, Errb1, mENA, EK2-6, CG10079, PIG61, torpedo/egfr, epidermal growth factor receptor activity, wa2, DmelCG10079, epidermal growth factor-activated receptor activity, AI552599, c-erbB, EGFr, Egfr, resistance, Pharmaceutical Product, torpedo/Egfr, EGF receptor activity, TOP, Pharmaceutic, Egf-r, DER/top, d-egf-r, Drugs, egfr, EGF-R, resistance., HD-33, El, top/DER, Pharmaceutic Preparations, DER/EGFR, EGFR, EGfr, EgfR, dEgfr, DER flb, top, Torpedo/DER, ERBB1, wa-2, Torpedo/Egfr, flb, top/flb, Degfr, Drug, Preparations, Egf, drugs, EFG-R, Errp, l(2)57EFa, medicine, Pharmaceutical, Erbb, DEGFR, l(2)57DEFa, l(2)05351, Der, DER, 9030024J15Rik, D-EGFR, dEGFR, l(2)57Ea, transforming growth factor-alpha receptor activity, DmHD-33, Preparation, Pharmaceutical Products, Proteomes, DER/torpedo, HER1, NISBD2, Pharmaceutical Preparation, DER1, Pharmaceuticalspara Tyrosine, PEP/X4, Kinship, Product, Ass-1, Nbla10317, CDP, Clox, Information Extraction, electronic data file, phosphorylation, DmelCG6143, Data Storage, 2-Amino-3-hydroxypropionic acid, 5730420M11Rik, Polypeptides, tudor staphylococcus/micrococcal nuclease, Method, SND1, Line, fold, 2, L-2-aminoglutaramic acid, Life Cycle, Software Engineering, 2-amino-3-mercaptopropanoic acid, Kinase, TIP110, Analysis, Drug Combination, WMS, Threonin, DL-Asparagine, strong, C, SET, asparagina, F, Kinship Network, Analyses, M, N, 2-amino-3-(4-hydroxyphenyl)propanoic acid, 3-(p-Hydroxyphenyl)alanine, L-Asparagine, Q, procedures, Y, Data Storage and Retrieval, CDP|Cut, CVID10, TUDOR-SN, DmelCG4299, allergic reaction, set, medicine, sample, NF-kappaB2, CT, s, Restricted expression proliferation-associated protein 100, Half Cystine, ATP Phosphotransferases, COY1, Glutamin, SGS, NK/GPI, Gpi, lyt, Data Set, Zinc Cysteinate, DIL2, acetylation, Ct, para-Tyrosine, Procedure, LYT10, Software Tools, ACMICD, Computer Applications, Computer Applications Software, computer data file, Methionin, Storage, NK|GPI, Hmet, Hepatocellular carcinoma-associated antigen 90, (2R)-2-amino-3-sulfanylpropanoic acid, Machine-Readable, neoplasm of granular cell, granular cell tumor NOS (morphologic abnormality), Software Applications, HLA-DR-associated protein II, DI-2, Source Software, I-2Dm, Information Storage, Methodological, Information Extractions, 2-amino-3-carbamoylpropanoic acid, (S)-2, beta Trypsin, human, L isomer, CUTL1, I-2PP1, Applications, TAF-IBETA, CDP/Cut, L-Tyrosine, TAF-Ibeta, Liquimeth, PEP, Bglap-rs1, Computer Software Applications, GLUTAMINE, 2-amino-4-(methylsulfanyl)butanoic acid, l(1)VE614, GOLIM6, False, Peptidomics, 2610005B21Rik, L-Zystein, Levoglutamide, Hasp, DSAP1, precursor, protein-containing complex, pep, Human, Glutaminsaeure-5-amid, Combinations, sensitive, Hepatocellular carcinoma-associated antigen 519, tough, Gene Products, Pgi, Half-Cystine, 2-Aminoglutaramic acid, p110(nrb), Man, Technique, Application, Open Source Softwares, Gpi-1r, NF-kB2, Software Application, L Cysteine, (2S)-2, Gpi-1s, E-920, Phi, beta-Trypsin, Gpi-1t, Open Source Software, 2pp2a, Hcys, kf, CG10574, Computer Software Application, Study, drugs, 2-amino-4-(methylthio)butanoic acid, 2PP2A, Tools, CYSTEINE, FLS353, dSET, dSet, FREE CYSTEINE, peptidos, Tyrosin, (2R)-2-amino-3-mercaptopropanoic acid, metionina, TDRD11, Pharmaceuticals, Retrieval, Products, Family Research, Proteins, Phosphorylations, function, MF, L-Isomer, Amf, Cell, Machine-Readable Data Files, Engine, Tool, Family Members, polypeptide, Serin, Experiment, native protein, tirosina, I-2PP2A, Dm I-2, chemical analysis, TSN, Glutamic acid 5-amide, MFS1, p49|p100, Met, NK, sQC, Glutamic acid amide, ensemble, Pharmaceutic Preparations, Information, (R)-2-amino-3-mercaptopropanoic acid, 4-diamino-4-oxobutanoic acid, 2-Amino-3-mercaptopropionic acid, plan specification, Computer Programs, Gene Proteins, Applications Softwares, Families, E920, Pharmaceutical Products, Relatives, Data Analyses, Networks, IPP2A2, E 920, insensitive, determination, Data File, cleavage, QC, L-Threonine, Combination, protein, granular cell tumour NOS (morphologic abnormality), HCA519, CDP1, L-(+)-glutamine, peptide, Cut, L-Isomer Methionine, Techniques, Machine Readable Data Files, L-Glutaminsaeure-5-amid, Methionine, CUX, peptido, l(1)7Ba, l(1)7Bb, AA408052, Pharmaceutical Product, Cystein, protein aggregate, Gpi-1, Computer Program, Family Life Cycle, Cux/CDP, Man (Taxonomy), peptides, TAF-I, HCTP4, cisteina, Nlk, Open, D-Glutamine, human protein, Computer Programs and Programming, tudor-SN, granular cell tumor NOS (morphologic abnormality)., X4/PEP, ASN, Files, Asn, CG11387, ASS, IGAAD, 2-amino-3-hydroxypropanoic acid, Methodological Studies, DmelCG10574, Pharmaceutical, Tyr, ppm, REPP86, Family Life Cycles, GPHYSD2, Racemethionine, Information Retrieval, ATP, phapii, C20orf1, CG6143, T5E21.12, Modern, 2-Amino-3-(p-hydroxyphenyl)propionic acid, 2-Amino-4-(methylthio)butyric acid, StF-IT-1, Search, Cys, C20orf2, Source Softwares, Programs, Tyrosine, Program, p50B, mOC-X, 3-Hydroxyalanine, GD:C20orf1, Computer Applications Softwares, p100OAS, Pharmaceutic, GD - C20orf1, Softwares, Data Linkage, BcDNA:GH10590, Filiation, region, L Glutamine, T5E21_12, Lines, parent ion, Hgln, Transphosphorylases, Org, ORG, Machine-Readable Data File, resistant, L-isomer, Gpi1-r, Gpi1-s, L-Cysteine, MASS, CG4299, Gpi1-t, Methodological Study, H2TF1, L-Cystein, L-glutamic acid gamma-amide, Life Cycles, data analysis, precursor ion, L Serine, Machine-Readable Data, p49, Polypeptide, L-Serine, GCT, i2pp2a, Gpi1s, Cysteine Hydrochloride, human being, Family Member, Procedures, AI461847, 5-diamino-5-oxopentanoic acid, p52, p49/p100, L Isomer, Goal, FBN, Gene, Network, Computer, (2S)-2-amino-4-carbamoylbutanoic acid, PHAPII, method, CASP, Homo sapiens, resilient, ECTOL1, method used in an experiment, Studies, L-Methionine, RP11-13G14, Differentially expressed in cancerous and non-cancerous lung cells 2, Phosphotransferase, sensitivity, Pedameth, Drugs, Search Engines, Data Retrieval, Research, p75, ipp2a2, Acetylations, CG7008, TSN-1, L Threonine, Transphosphorylase, OCTD, Asparagin, Table, data processing, 10^[-6], DmelCG11387, L Tyrosine, taf-ibeta, p200, site, L-Glutamine, Preparation, Kinship Networks, Family, Applications Software, Open Source, P100, Cux|CDP, Computer Software, DL-Methionine, protein complex, ASC1p100, drug, igaad, Cell Lines, p110, L-2-Aminoglutaramic acid, Medications, Extraction, Peptide, Phosphotransferases, group, dP100, Software Tool, Phosphopeptide, DIL-2, Protein, I2PP2A, p100, L-Glutamin, techniques, Software, Zystein, Data Base, WMS2, PRSS, 2-amino-3-sulfanylpropanoic acid, Kinases, Engineering, Tripcellim, L-2-Amino-3-mercaptopropionic acid, Data Files, sample population, Protein Gene Products, Drug, Trypure, dSET/TAF-Ibeta, 2-amino-4-carbamoylbutanoic acid, Preparations, 2610030F17Rik, DmelCG7008, D Glutamine, Data, Indexes, glutamic acid gamma-amide, Modern Man, SSKS, alpha-amino-gamma-methylmercaptobutyric acid, Peptid, assay, variable, LYT-10, AA407739, Protein fls353, Pharmaceutical Preparation, methodologyErbb-2, Ras, DmErk, Afatinib Maleate, l(1)G0098, pp44mapk, dP60, Vps34, Nbla10317, AGL5, Clox, A4, Tarceva, Tumor, Ras-1, phosphorylation, Case Fatality Rates, PI-3 kinase, Death Rates, ErbB-1, ras, c-ras2, tudor staphylococcus/micrococcal nuclease, ATP-protein transphosphorylase activity, epidermal growth factor-activated receptor activity, SND1, AA120551, TIP110, 2-amino-3-mercaptopropanoic acid, Analysis, SEM, gamma sarcoglycan, Lung Cancer, C, Analyses, M, Tissue, Dsor2, Lung Cancers, SAP-2, PI3Kgamma, Epidermal Growth Factor Receptor Kinase, LYK, PKB signaling cascade, PKB signalling cascade, 11C-erlotinib, TGF-alpha, NF-kappaB2, CP, osimertinib mesilate, 9030024J15Rik, s, protein kinase B signal transduction, Restricted expression proliferation-associated protein 100, Age-Specific Death Rate, COY1, osimertinib mesylate, ATP - 1-phosphatidyl-1D-myo-inositol 3-phosphotransferase activity, Tumors, ERK-A, dpERK, 5-c)quinolin-1-yl)phenyl)propanenitrile, Elp, Ras2, Data Set, Ras1, DEgfr, rea, betaIIPKC, Crude Death, p50alpha, DmMAPK, dp-ERK, not genetically inherited, Spectrum Analysis, DmelCG5373, TKI Tyrosine Kinase Inhibitors, Wee-kinase activity, torpedo/egfr, Benign, Role Concept, Emt, type-1 PI3K, pMAPK, tyrphostins, Methionin, Hmet, Urogastrone, activation, c-neu, BcDNA:RE36103, Erlotinib HCl, HGF/SF receptor, egfr, CG11621, HD-33, El, death rate, DER/EGFR, EGFR, erbB 1 Proto Oncogene Protein, Hras-1, TGF-alpha Receptor, Benign Neoplasms, DER flb, Dm Ras1, l(2)41Ac, erbB-1 Proto-Oncogene Protein, Torpedo/Egfr, Malignant Neoplasms, APDS, RasI, CT34260, Transforming-Growth Factor alpha, Mortality Rate, erlotinib, dpERk, NVP-BEZ235, 35kD dystrophin-associated glycoprotein, SAPK, lung neoplasm, Cancer of the Lung, Wee 1-like kinase activity, Harvey-ras, AA473386, Tcsk, Lung, D-Egf, GOLIM6, Family Receptors, Neoplasms, 2610005B21Rik, glycogen synthase kinase 3 activity, lung cancer, number, Transforming Growth Factor alpha Receptor, DRAS1, mENA, pep, c-erbB-1 Protein, Age-Specific Death, Dras2, Dras1, PIK3, Rate, D-Ras, Pi3Kp60, EGFr, Gene Products, AZD-9291 mesylate, dPI3K, IMPdH, MAM, ribosomal protein S6 kinase II activity, HER-2/neu, Ha-ras, EMTH, Pulmonary, Erk, Dras, Differential Mortality, protein-serine kinase activity, Excess Mortality, raspberry/impd, STK32, LNCR, C87398, top, Ras[V12], Pi3Kp110, epithelial-mesenchymal transition, EK3-4, CP358, erk, DRas, Neoplasias, Dmras64B, drugs, 2-amino-4-(methylthio)butanoic acid, Lung Neoplasm, protein tyrosine kinase inhibitors, (2E)-N-(4-(3-Chloro-4-fluoroanilino)-7-(((3S)-oxolan-3-yl)oxy)quinoxazolin-6-yl)-4-(dimethylamino)but-2-enamide, Epidermal Growth Factor Urogastrone, FREE CYSTEINE, rll, STK26, MCM, Receptor Tyrosine-protein Kinase erbB-1, (2R)-2-amino-3-mercaptopropanoic acid, p38-2, myelin basic protein kinase activity, Pharmaceuticals, Cpk, Neu, N-(2-((2-(dimethylamino)ethyl)methylamino)-4-methoxy-5-((4-(1-methyl-1H-indol-3-yl)-2-pyrimidinyl)amino)phenyl)-2-propenamide methanesulfonate (1:1), inhibitors, AKT signaling, Papilio tithonus, Malignant Neoplasm, Epidermal Growth Factor Receptor Family Proteins, CP 358774, TGF-alpha receptor activity, ERBB, type III phosphoinositide 3-kinase activity, HER-2|neu, stress-activated kinase activity, MAP-2 kinase activity, BRAF1, PTP-1D, protein phosphokinase activity, cpk, Concept, near to, PI3K-92E/Dp110, DmelCG1167, PIK3C1, MS, MT, native protein, Tsk, stress-activated protein kinase activity, Nonsmall cell lung cancer, DER/top, Death, PTP-2C, p49|p100, 7-bis(2-methoxyethoxy)quinazolin-4-amine, protein kinase p58 activity, Mass Spectrum Analyses, MET, Lung Adenocarcinomas, serine/threonine protein kinase activity, Death Rate, RAS85D, Dmras85D, CG12559, l(1)9Eb, c-erbB2, 2700084A17Rik, dpERK1, wa-2, dsk1, malignant tumor, atypical PKC activity, 2-Amino-3-mercaptopropionic acid, Differential, lung adenocarcinoma, signalling process, DmVps34, Braf2, PI3K_68D, PI3K-92D, vicinity of, BPTP3, HER Family, protection against, E920, Dmp110, BIBW-2992-MA2, 5730455C01Rik, protein serine-threonine kinase activity, Neoplasia, SAP kinase activity, Differential Mortalities, glycogen synthase kinase activity, protein kinase A activity, CG5373, Postprandial Hyperglycemias, Hgfr, ATVPS34, Mpk2, p42mapk, protein, side effects, HCA519, CG11485, SR2-1, High blood glucose, PHOSPHATIDYLINOSITOL 3-KINASE, DmelCG2699, Roles, F8A5.4, Kinase Inhibitors, Tyrosine Kinase Inhibitor, AI552599, Pharmaceutical Product, kinase-related transforming protein, p110alpha, Cystein, d-egf-r, protein aggregate, D-Ras1, CD221, IGFR, HCTP4, alveolar cell carcinoma, l(1)G0436, catalyst activity, DERK-A, E(sina)7, PI[[3]]K, Rl, Raf kinase activity, Tagrisso, MP kinase activity, serine kinase activity, Proto oncogene c ErbB 1 Protein, CP-358, atypical protein kinase C activity, Pharmaceutical, disease management, mitogen-activated S6 kinase activity, protein-aspartyl kinase activity, D-EGFR, dERK, D6Ertd631e, Tyrosine Protein Kinase Inhibitors, AKT signal transduction, Wa5, l(2)09261, Mapk, Ki-ras, P110DELTA, 2-Amino-4-(methylthio)butyric acid, Cancer of Lung, ERK1, ERK2, mapk1a, Cys, dPIK, M phase-specific cdc2 kinase activity, Spectroscopy, wa2, mapk1b, MapK, protein kinase B signaling, dRas1, erk2, ras-2, Lines, ERKa, phosphorylase B kinase kinase activity, BcDNA:RE08694, resistant, N-(4-((3-chloro-4-fluorophenyl)amino)-7-(((3S)-tetrahydro-3-furanyl)oxy)-6-quinazolinyl)-4-(dimethylamino)-, DmelCG1799, l(2R)EMS45-39, l(1)G0238, Encephalon, SHP2, DmelCG12559, AA387315, 7-bis-(2-methoxy-ethoxy)-quinazolin-4-yl]-(3-ethynyl-phenyl)-amine, C-ras1, p38, PI3K 68_D, Treatments, C-ras2, Tyrosine Kinase, L-Cystein, DpErk, l(1)G0002, MLN 19, Lung Adenocarcinoma, ERKA, l(1)G0482, hydroxyalkyl-protein kinase activity, Receptor Tyrosine protein Kinase erbB 1, WEE1Hu, p110D, DMDA, c-H-ras, TKR1, dEGFR, p49, c-ErbB-1 Protein, droPIK57, the brain, bronchogenic lung adenocarcinoma, SHPTP2, calcium/phospholipid-dependent protein kinase activity, SGCG_HUMAN, RasV12, p52, Mortality Declines, PI3K92E, p49/p100, Transforming Growth Factor alpha, Kras2, TKI inhibitor, mor1, Spectrum Analyses, PKB signaling, Malignant, mortality measurement, Mortality Determinants, CASP, RRG6, p60, c-erbB, Mass, RP11-13G14, PHOSPATIDYLINOSITOL 3-KINASE, Differentially expressed in cancerous and non-cancerous lung cells 2, [6, T-antigen kinase activity, p21B, galactosyltransferase-associated kinase activity, study, EGF-R, LUAD, p75, Age-Specific, CG18732, AUTS9, Pyronia tithonus, top/flb, Family Receptor, protein kinase (phosphorylating) activity, PI3K-68D, GEP6, inhibidor, l(2)57EFa, Clients, Mortality Rates, mortality rate, mesenchymal cell differentiation from epithelial cell, p200, Preparation, AI838057, ras-l, casein kinase (phosphorylating) activity, Age Specific Death Rate, SH-PTP3, SH-PTP2, l(1)G0056, P100, ert1, CG9375, DL-Methionine, protein complex, Cell Lines, K-ras, Vps34p, Protein-tyrosine phosphatase 1D, count in organism, 3-dihydroimidazo(4, fs(3)05703, ATP:1-phosphatidyl-1D-myo-inositol 3-phosphotransferase activity, survival, epidermal growth factor receptor activity, vps34, DIL-2, AP50 kinase activity, MBP kinase I activity, dp110, Erlotinib, AI929937, PI3CG, Protein-tyrosine phosphatase 2C, Xp42, PI-3-K, antagonists, Rates, Mass Spectrum, CP358774, mitogen activated kinase activity, Su(Raf)2B, class III, L-2-Amino-3-mercaptopropionic acid, Drug, Protein Gene Products, Preparations, EGF, EFG-R, D-ERK, DmelCG7008, Therapeutic, Braf-2, approaches, SCARMD2, Der, alpha-amino-gamma-methylmercaptobutyric acid, Treatment, transforming growth factor-alpha receptor activity, DER/torpedo, MAP kinase 1 activity, A-kinase activity, Urogastrone Receptor, RAS, extracellular signal-regulated kinase activity, PEP/X4, Product, Organic cation transporter 3, CDP, Elp-B1, der, Elp-1, Receptors, Errb1, BcDNA:LD15217, growth and development, VPS34, 11621, AKT signalling cascade, DmelCG6143, Epidermal Growth Factor Receptor Family Protein, Prp4 protein kinase activity, PIG61, Mutations, p110-alpha, LeMPK3, Kiaa3023, p44mpk, ATP:protein phosphotransferase (non-specific) activity, Line, Dp38, Excess Mortalities, Protein-tyrosine phosphatase SYP, SAPK2, Sem, treatment, CFC, MAP-k, Dp60, pp42, PI3K_59F, chemical analysis., PI3-kinase activity, AKT signaling cascade, suprasegmental levels of nervous system, Epidermal Growth Factor Receptor, BIBW 2992 MA2, sem, flb, CDP|Cut, CVID10, TUDOR-SN, allergic reaction, MCAP, medicine, Role Concepts, PI3K 68D, RG7MT1, single organism signaling, CG1799, p82 kinase activity, close to, dVps34, suprasegmental structures, lyt, dpErk, RAS2, EGF Receptors, RAS1, DIL2, N-(3-ethynylphenyl)-6, (2E)-, MLN19, PMK-2, PMK-1, CG2699, LYT10, PMK-3, C530050K14, Postprandial Hyperglycemia, EMT, dRas85D, Role, pMapK, sarcoglycan, erlotinibum, Hepatocellular carcinoma-associated antigen 90, ras1, (2R)-2-amino-3-sulfanylpropanoic acid, ras2, NVPBEZ235, DmERKA, rl/MAPK, NVP BEZ235, BIBW-2992, BIBW-2992MA2, EGfr, EgfR, PSCTK2, Spectrometry, non-specific serine/threonine protein kinase activity, non-small cell lung adenocarcinoma, hCMT1c, c-Met, DmelCG4141, F8A5_4, ErbB-1 Receptor, Degfr, CUTL1, nonsmall cell adenocarcinoma, BIBW 2992, antagonists and inhibitors, CDP/Cut, serine-specific protein kinase activity, BIBW 2992MA2, DEGFR, cancer of the lung, PI3KBETA, l(2)05351, HIPK2, cytidine 3', Extraneuronal monoamine transporter, Mortality Determinant, other neoplasm, PEP, Hras1, Adenocarcinoma, CO-1686, 2-amino-4-(methylsulfanyl)butanoic acid, glycogen synthase A kinase activity, dRas, CG1167, 3-dihydro-1h-imidazo(4, Excess, 12559, Hyperglycemia, L-Zystein, H-ras, DRas2, PKB signal transduction, DSAP1, Crude Mortality Rate, IMPDH, hyperglycaemia, EK2-6, protein-containing complex, LD06825, phosphorylase b kinase kinase activity, EK2-1, c erbB 1 Protein, Postprandial, Determinant, dVps34/PI3K59F, CP 358, sensitive, Hepatocellular carcinoma-associated antigen 519, PI3K-dp110, Egfr, Kras-2, Case Fatality, torpedo/Egfr, 7-bis(2-methoxy-ethoxy)quinazoline-4-yl]-(3-ethynylphenyl)amine, TOP, anon-92Ed, RCCP2, Pulmonary Cancer, p110(nrb), gamma-SG, erbB-1, ERK, PRKM1, class I, ras 1, PRKM2, F15E12_6, TKI inhibitors, NF-kB2, scatter factor receptor, E-920, LPFS1, 774, Hcys, OSI 774, P110BETA, DRas85D/Ras, N-(2-((2-(dimethylamino)ethyl)methylamino)-4-methoxy-5-((4-(1-methyl-1H-indol-3-yl)-2-pyrimidinyl)amino)phenyl)-2-propenamide, PI3K21B, protein-cysteine kinase activity, CYSTEINE, FLS353, Hpr kinase activity, Crude Death Rates, PTP1D, 358774, TDRD11, metionina, Cancer, NEU, Elp-B1RB1, Products, EGF Receptor, AW536184, Mortality Decline, AA414921, 35 kDa dystrophin-associated glycoprotein, class II, ErbB, dEGFR1, Proteins, Phosphorylations, Proto-Oncogene Protein, D-ras-1, protein serine kinase activity, encephalon, Cell, PI(3)K, SGCG, E(faf), Case Fatality Rate, PKA, PKC, CWS5, mapk2, TSN, mapk1, Neoplasm, S35097, NGL, protein kinase B signaling cascade, Met, ATCMPG1, ATCMPG2, primary cancer, DMDA1, Pharmaceutic Preparations, Afatinib Dimaleate, Pulmonary Neoplasm, tyrosine-protein kinase Met, postnatal growth, mereletinib, (R)-2-amino-3-mercaptopropanoic acid, Cancers, DmelCG11621, 5'-cyclic monophosphate-responsive protein kinase activity, Gene Proteins, AZD9291 mesylate, caPI3K, CLOVE, dpMAPK, IMD14, Erbb, Epidermal Growth Factor, Decline, Pulmonary Cancers, Receptor, Pharmaceutical Products, General activity, DER/faint little ball, Ras1/RAs85D, MGC130048, F7D19.17, E 920, insensitive, Activity, determination, postnatal development, 5730555F13Rik, c-rasHa, PI3K, E(sev)3C, Dp110, CP-358774, 358, JTK13, CDP1, CD340, CUX, mereletinib mesilate, F7D19_17, HGFR, Concepts, TGF alpha, Inhibitors, synganglion, mitogen-activated protein kinase activity, phosphatidylinositol 3-kinase activity, IGFIR, mpk1, Cux/CDP, Mass Spectrum Analysis, Erk/Map kinase, RTK, Crude Mortality Rates, Pi3K92D, CG4141, MUB3_18, ErbB 1, cisteina, tyrosine kinase inhibitors, Pi3k, tudor-SN, ras85B, X4/PEP, ras85D, MUB3.18, 9930012E13Rik, DERK, D-ras-2, p55alpha, C230098H17, malignant neoplasm, CFR Case Fatality Rate, REPP86, Therapies, MBP kinase II activity, ErbB Receptor, gamma-sarcoglycan, AGAMOUS-like 5, Malignancies, Pi3K, PI3k, tyrphostin, MCMTC, Racemethionine, NISBD2, AZD9291, DER1, Therapy, C20orf1, l(3)s1747, PI3K68D, MAP kinase 2 activity, proto-oncogene c-Met, B-RAF1, Lung cancer, CG6143, PRO, PtdIns-3-kinase activity, HER Family Receptors, SG-gamma, Erk1, PTP2C, 9130215G10Rik, Adenocarcinomas, C20orf2, CYS, CG10079, vacuolar protein sorting 34, Crude Mortality, 1-phosphatidylinositol 3-kinase activity, Programs, Tyrosine, adenocarcinoma of the lung, p50B, OSI-774, Mortality, BEZ235, cancer of lung, Syp, MAPK, GD:C20orf1, 3.1.3.48, High Blood Sugar, p100OAS, NOS, p21[Ras1], Pharmaceutic, GD - C20orf1, dRAS1, serine protein kinase activity, and GLY protein 2, Dras85D, mapk, region, HGF receptor, Epistemology, RAFB1, and GLY protein 1, l(1)G0351, LD02673, protein glutamyl kinase activity, p85alpha, c-Ha-ras, adenocarcinoma of lung, D-ras1, D-ras2, dEgfr, Shp2, HCl, Mortalities, common, Dras64B, gamma (35kDa dystrophin-associated glycoprotein), H2TF1, l(3)06677, DpERK, ErkA, Crude Death Rate, AZD-9291, Patient, epsilon PKC, l(1)G0127, l(2)57DEFa, HER, DmHD-33, p120-PI3K, Proteomes, pERK, ribosomal S6 protein kinase activity, GroupII, C-erb, NS1, Benign Neoplasm, NS7, Gene, Pi3K_59F, OCT3, DmelCG9375, mereletinib mesylate, type I phosphatidylinositol kinase activity, presence, TYPE, phosphatidylinositol 3-kinase, DAGA4, Crude, l(1)G0388, HGF, resistance, 35DAG, EGF receptor activity, serine(threonine) protein kinase activity, SHP-2, F15E12.6, Egf-r, l(1)G0380, SCG3, sensitivity, Dp110/PI3K, 2-methyl-2-(4-(3-methyl-2-oxo-8-(quinolin-3-yl)-2, Mass Spectroscopy, PI3K-68D/E, Drugs, dras1, Dm-ras-64B, 11C erlotinib, BIBW2992, Malignancy, HER-2, xp42, CG7008, inhibiteur, Torpedo/DER, TSN-1, PI3'K, l(1)G0391, p42 mitogen-activated protein kinase activity, ATP:protein phosphotransferase (MAPKK-activated) activity, Ras 85D, Epidermal Growth Factor-Urogastrone, Raf-1, 2-methyl-2-(4-(3-methyl-2-oxo-8-quinolin-3-yl-2, site, DmERK-A, l(2)57Ea, Proto-oncogene, dP110, Pulmonary Neoplasms, protein kinase B signalling cascade, Cux|CDP, 6330412C24Rik, Epidermal Growth Factor Receptor Protein Tyrosine Kinase, p120, ASC1p100, drug, mKIAA3023, prkm2, prkm1, CT39192, total expressed protein, p110, inhibitor, Medications, Hyperglycemias, Client, LGMD2C, p38delta, development, dP100, twitchin kinase activity, DmelCG10079, EP(X)1093, SHATTERPROOF 2, Protein, High blood sugar, Epidermal Growth Factor Receptor Protein-Tyrosine Kinase, protein tyrosine kinase inhibitor, Hydrochloride, p100, Proto-oncogene c-ErbB-1 Protein, B-raf, rare (European definition), HER Family Receptor, Determinants, Zystein, threonine-specific protein kinase activity, PI3K-59F, top/DER, PI3K-Dp110, 2-amino-3-sulfanylpropanoic acid, OSI774, gatekeeper, ERBB1, EY2-2, 2-Butenamide, Age-Specific Death Rates, p110gamma, Su(tor)3-2, Gilotrif, Egf, Errp, DER, assay, Par4, LYT-10, Protein fls353, growth, HER2, BIBW2992 MA2, HER1, Pharmaceutical Preparation, SF receptorfalseGlobal proteome and phosphoproteome alterations in 3rd generation EGFR TKI resistance reveal drug targets to circumvent resistanceLung cancer continues to be the leading cause of cancer mortality worldwide. The treatment of lung cancer patients harboring mutant EGFR with orally administered EGFR TKIs has been a paradigm shift. Osimertinib and rociletinib are two 3rd generation irreversible EGFR TKIs targeting the EGFR T790M mutation. Osimertinib is the current standard care for patients with EGFR mutations due to increased efficacy, lower side effects, and enhanced brain penetrance. Unfortunately, all patients develop resistance to it. Genomic approaches have primarily been used to interrogate resistance mechanisms. Here, we have characterized the proteome and phosphoproteome of a series of isogenic EGFR mutant lung adenocarcinoma cell lines that are either sensitive or resistant to these drugs. To our knowledge, this is the most comprehensive proteomic dataset resource to date to investigate 3rd generation EGFR TKI resistance in lung adenocarcinoma. We have interrogated this unbiased global quantitative proteomic and phosphoproteomic dataset to uncover alterations in signaling pathways, and to reveal a proteomic signature of EMT and kinases / phosphatases with altered protein expression and phosphorylation in the TKI resistant cells. We validated the significant role of SHP2 in the activation of RAS/MAPK and PI3K/AKT signaling pathways. Furthermore, we performed anticorrelation analyses of this phosphoproteomic dataset with the published drug-induced P100 phosphoproteomic datasets from the Library of Integrated Network-Based Cellular Signatures (LINCS) program to predict drugs with the potential to overcome EGFR TKI resistance. We identified that dactolisib, a PI3K/mTOR inhibitor, in combination with osimertinib, may overcome osimertinib resistance both in vitro and in vivo. Introduction Lung cancer continues to be the leading cause of cancer mortality in the world (1). Many lung adenocarcinoma patients with activating epidermal growth factor receptor (EGFR) mutations initially respond dramaticlly to the first- or second-generation EGFR tyrosine kinase inhibitors (TKIs). However, they eventually develop resistance. The most common mechanism of acquired resistance is the EGFR T790M gatekeeper site residue mutation (2). Osimertinib, a third generation irreversible EGFR TKI has been approved by the FDA to treat patients harboring the EGFR T790M mutation who have developed resistance to first- and second- generation EGFR TKIs (3). Recently, osimertinib was also approved for the front-line treatment of patients harboring EGFR mutations (4). Rociletinib is another irreversible inhibitor targeting the EGFR T790M mutation, which has minimal activity against wild-type EGFR. Both drugs have therapeutic benefits and have demonstrated activity in tumors with T790M-mediated resistance to other EGFR tyrosine kinase inhibitors (5, 6). Further development of rociletinib was ceased in 2016 due to less than expected efficacy, poor brain penetration leading to tumor progression in brain tissues and off-target effects on IGFR activation leading to hyperglycemia (7, 8). Although 3rd-generation TKIs provide clinical benefit to most patients with EGFR mutations, some patients, demonstrating primary resistance, still do not respond to these inhibitors. Complete responses are rare, and all patients eventually develop resistance, suggesting primary and acquired resistance mechanisms decrease the efficacy of the drugs (9, 10). Genomic approaches have been used primarily to interrogate osimertinib resistance mechanisms (9, 11-15). Several mechanisms of osimertinib resistance have been identified (16), including novel second site EGFR mutations, activated bypass pathways such as MET amplification, HER2 amplification, RAS mutations, BRAF mutations, PIK3CA mutations, and novel fusion events (17). However, the resistance mechanism is complex and still not fully understood. Previously, we have used SILAC-based quantitative phosphoproteomics to identify the global dynamic modification which occur upon treatment of TKI-sensitive and -resistant lung adenocarcinoma cells with the 1st and 2nd generation EGFR TKIs, erlotinib and afatinib. Utilizing this strategy, we identified the targets of mutant EGFR signaling pathways responsible for TKI resistance, and possible off-target effects of the drugs (18, 19). In this study, we employed SILAC-based quantitative mass spectrometry to characterize alterations in the proteome and phosphoproteome which occur upon acquired resistance and sought to identify novel mechanisms of resistance to the third generation EGFR TKIs, osimertinib and rociletinib. To our knowledge, this is the most comprehensive 3rd generation EGFR TKI resistant proteome and phosphoproteome analysis resource available to date.2021-03-112020-06-30PXD020108NEWT:68239NEWT:108018NEWT:377960NEWT:1131NEWT:190486NEWT:2737160NEWT:2042546NEWT:2042545NEWT:148942NEWT:193528NEWT:295546NEWT:258594NEWT:1126NEWT:1129NEWT:89187NEWT:309807NEWT:89184NEWT:309800NEWT:57577NEWT:1150591NEWT:156563NEWT:1323429NEWT:876138NEWT:44271NEWT:193516NEWT:2315688NEWT:44270NEWT:592321NEWT:1073882NEWT:6819NEWT:93217NEWT:428386NEWT:1117NEWT:498257NEWT:10036NEWT:32264NEWT:10034NEWT:10031NEWT:82569NEWT:661410NEWT:488003NEWT:224326NEWT:109376NEWT:376619NEWT:3765NEWT:2433NEWT:1190602NEWT:3767NEWT:433727NEWT:135622NEWT:672127NEWT:656061NEWT:37965NEWT:656064NEWT:3760NEWT:36630NEWT:381198NEWT:1176302NEWT:418106NEWT:10029NEWT:913645NEWT:2492962NEWT:641809NEWT:44250NEWT:77151NEWT:317447NEWT:698761NEWT:5530NEWT:868565NEWT:135674NEWT:1562698NEWT:1177NEWT:11308NEWT:12637NEWT:2164133NEWT:1180NEWT:2767846NEWT:1343074NEWT:314344NEWT:108061NEWT:143292NEWT:2767842NEWT:314345NEWT:224308NEWT:3134131NEWT:49928NEWT:160621NEWT:110368NCBITaxon:5204NEWT:1916073NEWT:1303873NEWT:305400NEWT:1310161NEWT:1230383NEWT:77133NCBITaxon:5207NEWT:160620NCBITaxon:77643NEWT:1310165NEWT:114727NEWT:5516NEWT:498211NEWT:347256NEWT:5518NEWT:398007NEWT:1527468NEWT:498217NEWT:498216NEWT:32224NEWT:11320NEWT:1410384NEWT:1310173NEWT:37919NEWT:1072569NEWT:1072568NEWT:161934NEWT:156587NEWT:1148NEWT:5508NEWT:135666NEWT:419481NEWT:5507NEWT:1140NCBITaxon:2157NEWT:2066563NEWT:1143NEWT:1336794NEWT:1462472NEWT:1336795NEWT:644042NEWT:709964NEWT:3710NEWT:393133NEWT:65125NEWT:3712NEWT:3711NEWT:3714NEWT:65121NEWT:3716NEWT:3715NEWT:2065263NEWT:1549675NEWT:177437NEWT:9014NEWT:10891NEWT:118221NEWT:32201NEWT:34869NEWT:226126NEWT:1616117NEWT:34865NEWT:28174NEWT:550537NEWT:284812NEWT:284811NEWT:2902907NEWT:3701NEWT:3702NEWT:1245466NEWT:3704NEWT:1246791NEWT:34875NEWT:10882NEWT:1431297NEWT:9005NEWT:34871NEWT:9006NEWT:33548NEWT:1883426NEWT:657321NEWT:1423687NEWT:657322NEWT:10886NEWT:3707NEWT:3708NEWT:536231NEWT:219813NEWT:1301262NEWT:319224NEWT:2305479NEWT:215451NEWT:460519NEWT:292415NEWT:272843NEWT:272844NEWT:1348799NEWT:55784NEWT:485NEWT:223074NEWT:2709072NEWT:2499525NEWT:467144NEWT:142786NEWT:28196NEWT:2853422NEWT:487NEWT:1679718NEWT:387344NEWT:657318NEWT:480NEWT:67767NEWT:46835NEWT:216778NEWT:376686NEWT:237610EFO:0001352NEWT:219809NEWT:219808NEWT:119562NEWT:367737NEWT:1883446NEWT:1233435NEWT:118223NEWT:141469NEWT:272831NEWT:987059NEWT:491NEWT:422203NEWT:460523NEWT:2422NEWT:2423NEWT:3755NEWT:85694NEWT:85692NEWT:911045NEWT:3750NEWT:123606NEWT:1195466NEWT:2483192NEWT:85698NEWT:291146NEWT:29466NEWT:233271NEWT:3745NEWT:1715989NCBITaxon:4751NEWT:3747NEWT:278161NEWT:415978NEWT:410289NEWT:191701NEWT:9054NEWT:472NEWT:29459NEWT:34839NEWT:476NEWT:1380096NEWT:28128NEWT:470NEWT:41122NEWT:1328300NEWT:748693NEWT:106299NCBITaxon:50557NEWT:63363NEWT:3735NEWT:1002697NEWT:29491NEWT:911022NEWT:446NEWT:153481NEWT:714485NEWT:445NEWT:427924NEWT:2003758NEWT:29486NEWT:63366NEWT:64697NEWT:63367NEWT:29488NEWT:215402NEWT:3726NEWT:1120755NEWT:1862567NEWT:591090NEWT:30455NEWT:28141NEWT:9030NEWT:9031NEWT:3728NEWT:29471NEWT:108931NEWT:219799NEWT:1325292NEWT:219798NEWT:548NEWT:150475NEWT:546NEWT:1431340NEWT:256737NEWT:51350NEWT:8694NEWT:8692NEWT:542NEWT:394503NEWT:13076NEWT:219785NEWT:451515NEWT:8673NEWT:550NEWT:10804NEWT:52694NEWT:554NEWT:451516NEWT:552NEWT:1325291NEWT:42410NEWT:40686NEWT:1225786NEWT:366497NEWT:771870NEWT:8665NEWT:51338NEWT:771875NEWT:377142NEWT:9995NEWT:28112NEWT:49012NEWT:28110NEWT:10835NEWT:10832NEWT:311339NEWT:507601NEWT:520NEWT:64657NEWT:186441NEWT:2585209NEWT:643680NEWT:214092NEWT:40697NEWT:13095NEWT:162425NEWT:242124NEWT:9986NEWT:8654NEWT:536NEWT:8658NEWT:1268063NEWT:8657NEWT:9983NEWT:8655NEWT:595495NEWT:80833NEWT:479096NEWT:28108NEWT:28104NEWT:1114957NEWT:568703NEWT:568708NEWT:480020NEWT:51315NEWT:52641NEWT:353152NEWT:116597NEWT:353154NEWT:353153NEWT:116598NEWT:227377NEWT:1774284NEWT:27689NEWT:207769NEWT:40674NEWT:51329NCBITaxon:1763NEWT:443906NEWT:6055NEWT:13037NEWT:518NEWT:519NEWT:941638NEWT:511NEWT:7394NEWT:6063NEWT:404330NEWT:1328388NEWT:13064NEWT:529120NEWT:7375NEWT:300641NEWT:39655NEWT:38323NEWT:206411NEWT:80869NEWT:214053NEWT:80863NEWT:665890NEWT:1295626NEWT:52639NEWT:52638NEWT:8697NEWT:861109NEWT:8695NEWT:1196866NEWT:6039NEWT:37003NEWT:510516NEWT:1045775NEWT:1123869NCBITaxon:1335626NEWT:565663NEWT:7370NEWT:2058152NEWT:280406NEWT:83906NEWT:2172651NEWT:99488NEWT:99487NEWT:1134506NEWT:255470NEWT:762903NEWT:27697NEWT:552364NEWT:41980NEWT:86185NEWT:1869227NEWT:185978NEWT:9935NEWT:266940NEWT:287889NEWT:9938NEWT:1028307NEWT:52603NEWT:92867NEWT:92866NEWT:1344414NEWT:202950NEWT:741158NEWT:1293091NEWT:202956NEWT:483179NEWT:315750NEWT:99490NEWT:632957NEWT:265619NEWT:11294NEWT:754466NEWT:9925NCBITaxon:9606NEWT:1436183NEWT:1479235NEWT:4232NEWT:9922NEWT:416348NEWT:105812NEWT:9923NEWT:11298NEWT:4233NEWT:4236NEWT:398031NEWT:196627NEWT:336685NEWT:523840NEWT:487521NEWT:1076878NEWT:523845NEWT:200308NEWT:200302NEWT:9913NEWT:9915NEWT:105841NEWT:1170227NEWT:2010885NEWT:2666255NEWT:999810NEWT:28995NEWT:1392998NEWT:1150621NEWT:1085791NEWT:745531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