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Generation of a biliary tract cancer cell line atlas identifies molecular subtypes and therapeutic targets

ABSTRACT: Biliary tract cancers (BTCs) are lethal malignancies, including intrahepatic and extrahepatic cholangiocarcinoma, gallbladder carcinoma, and ampullary carcinoma. Through multi-omics profiling and CRISPR screens of 63 BTC cell lines, we identify widespread EGFR dependency and subtype-specific vulnerabilities with predictive markers. Strategies to overcome targeted therapy resistance include EGFR inhibition potentiating mutant-KRAS and FGFR inhibition, while SHP2 inhibition counters FGFR inhibitor resistance. Clustering by gene/protein expression and dependencies reveals functional subtypes ductal, squamous, and bi-lineage each with distinct survival dependencies. Transcriptional analysis of patient samples highlights the prognostic value of this classification. This BTC cell line atlas uncovers therapeutic targets, defines disease subtypes, and serves as a critical resource for BTC research. Multiplexed proteomics was performed using TMT tags (TMT1 to TMT12) and TMTpro tags (TMT13 to TMT17) and the SPS3 method on an Orbitrap Fusion Lumos instrument. Sample key is as follows: CCLP (ICCL_TMT2:129c, ICCL_TMT6:127n), CCSW1(ICCL_TMT2:128c, ICCL_TMT7:130c), AOVC1 (ICCL_TMT9:129n, ICCL_TMT10:129c), EGI1(ICCL_TMT16:126, ICCL_TMT16:127n), ETK1 (ICCL_TMT16:127c, ICCL_TMT16:128n), G415 (ICCL_TMT11:129c, ICCLTMT12:130n), GB2 (ICCL_TMT1:127n, ICCL_TMT5:128n), HKGZCC (ICCL_TMT4:129n, ICCL_TMT8:128c), HUCCT1 (ICCL_TMT1:127c, ICCL_TMT6:129n), HUH28 (ICCL_TMT4:130n, ICCL_TMT8:128n), GB3 (ICCL_TMT3:131n, ICCL_TMT7:131n), ICC10 (ICCL_TMT1:128c, ICCL_TMT7:126), ICC10-6 (ICCL_TMT4:128n, ICCL_TMT7:127n), ICC10-8 (ICCL_TMT2:131n, ICCL_TMT7:127c), ICC11 (ICCL_TMT4:128c, ICCL_TMT5:129n), ICC12 (ICCL_TMT4:130c, ICCL_TMT6:129c), ICC13-7 (ICCL_TMT2:126, ICCL_TMT8:127c, ICCL_TMT11:129n, ICCL_TMT12:131n), ECC3 (ICCL_TMT1:128n, ICCL_TMT5:127c), ICC16 (ICCL_TMT11:128n, ICCL_TMT12:128c), ICC17 (ICCL_TMT3:129c, ICCL_TMT7:129n), ICC18 (ICCL_TMT13:127c, ICCL_TMT13:128n), ICC19 (ICCL_TMT11:128c, ICCL_TMT12:127c), ICC2 (ICCL_TMT4:127c, ICCL_TMT5:126), ICC20 (ICCL_TMT13:128c, ICCL_TMT13:129n), ICC21 (ICCL_TMT14:131n, ICCL_TMT14:131c), ICC24 (ICCL_TMT13:129c, ICCL_TMT13:130n), ICC25 (ICCL_TMT13:130c, ICCL_TMT13:131n), ICC26 (ICCL_TMT15:128c, ICCL_TMT15:129n), ECC4 (ICCL_TMT4:127n, ICCL_TMT6:131n, ICCL_TMT13:126, ICCL_TMT13:127n), ICC4 (ICCL_TMT9:128n, ICCL_TMT10:130n), ICC5 (ICCL_TMT3:127c, ICCL_TMT6:130n), ICC8 (ICCL_TMT2:127n, ICCL_TMT7:129c), ICC9 (ICCL_TMT2:127c, ICCL_TMT7:128c), KKU100 (ICCL_TMT9:127n, ICCL_TMT10:131n), KKU312 (ICCL_TMT9:129c, ICCL_TMT10:127n), GB4 (ICCL_TMT15:127n, ICCL_TMT15:128n), NOZ (ICCL_TMT16:132c, ICCL_TMT16:133n), OCUG1 (ICCL_TMT16:129n), RBE (ICCL_TMT1:126, ICCL_TMT7:128n), SG231 (ICCL_TMT9:126, ICCL_TMT10:127c), SNU1079 (ICCL_TMT9:130c, ICCL_TMT10:128n), SNU1196 (ICCL_TMT1:130n, ICCL_TMT8:130n), SNU245 (ICCL_TMT17:128n, ICCL_TMT17:129c), SNU308 (ICCL_TMT4:131n, ICCL_TMT8:131n), SNU478 (ICCL_TMT2:128n, ICCL_TMT6:130c), SNU869 (ICCL_TMT4:129c, ICCL_TMT5:130n), SSP25 (ICCL_TMT2:130c, ICCL_TMT5, 131n), TFK1 (ICCL_TMT17:126, ICCL_TMT17:130c) TGC1TKB (ICCL_TMT17:127c, ICCL_TMT17:129n), TGBC52TKB (ICCL_TMT11:130c, ICCL_TMT12:128n), TKKK (ICCL_TMT9:128c, ICCL_TTM10:129n), YSCCC (ICCL_TMT9:127c, ICCL_TMT10:126), ICC7 (ICCL_TMT3:128c, ICCL_TMT5:129c), OZ (ICCL_TMT11:127n, ICCL_TMT12:129n), KMCH1 (ICCL_TMT1:129n, ICCL_TMT8:129c), KKU055 (ICCL_TMT16:131c), ICC28 (ICCL_TMT2:132n, ICCL_TMT3:126), TGBC14TKB (ICCL_TMT11:131n, ICCL_TMT12:130c), PLCPRF5 (ICCL_TMT14:129n, ICCL_TMT14:129c) TONG (ICCL_TMT14:127n, ICCL_TMT14:127c), HUH7 (ICCL_TMT15:129c, ICCL_TMT14:130n, ICCL_TMT14:130c), SNU449 (ICCL_TMT15:131n), SNU387 (ICCL_TMT17:126, ICCL_TMT17:128c), JHH7 (ICCL_TMT15:130n, ICCL_TMT1:130c), SNU475 (ICCL_TMT17:130n, ICCL_TMT17:132n), HEPG2 (ICCL_TMT13:131c, ICCL_TMT13:132n), SNU423 (ICCL_TMT17:131n, ICC_TMT17:131c)

INSTRUMENT(S): Orbitrap Fusion Lumos

ORGANISM(S): Homo Sapiens (ncbitaxon:9606)

SUBMITTER: Vindhya Vijay Wilhelm Haas Nabeel Bardeesy

PROVIDER: MSV000097266 | MassIVE | Fri Mar 07 05:51:00 GMT 2025

REPOSITORIES: MassIVE

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Project description:Mass spectrometry-based proteomics was applied to unravel Erk signaling in mouse embryonic stem cells (ESCs). A previously described engineered ESCs system for Erk induction via a drug-inducible cRAF-ErT2 fusion (Hamilton, W. B. & Brickman, J. M., Cell Rep 2014) was used in two different setups measuring the phosphoproteome in an 11-plex tandem mass tag (TMT)-based approach as described below. Fgf4 stimulation and MEK inhibition: ESCs were stimulated with Fgf4 (40 nM, recombinant, mouse, 5 minutes) following pretreatment (30 minutes) with either DMSO (1:10000) or MEK inhibition (MEKi: 1 microM PD0325901): The experimental treatment conditions and TMT11-plex labeling are specified below: 126: DMSO, unstimulated control replicate 1 127N: DMSO, unstimulated control replicate 2 127C: DMSO, unstimulated control replicate 3 128N: DMSO + Fgf4 replicate 1 128C: DMSO + Fgf4 replicate 2 129N: DMSO + Fgf4 replicate 3 129C: MEKi + Fgf4 replicate 1 130N: MEKi + Fgf4 replicate 2 130C: MEKi + Fgf4 replicate 3 131N: MEKi replicate 1 131C: MEKi replicate 2 Analog sensitive Erk2 setup: In the ESC system the ERK2-/- ESCs (Hamilton et al., PloS ONE, 2013) were engineered to stably express an inducible cRAF-ErT2 fusion protein expressed from the same transgene as a FLAG-tagged analogue sensitive Erk2Q103A. Erk1 was subsequently removed by CRISPR-Cas9 mutagenesis using sgRNAs flanking exon 2. Cells were pre-treated for 30 minutes with either the ATP-mimetic compound 1-NM-PP1 (2 microM) (Endo et al., Biochem Biophys Res Commun 2006), the Mek1 inhibitor PD0325901 (1 microM), or DMSO (0.01%), followed by induction or not of the cRAF-ErT2 fusion by (Z)-4-Hydroxytamoxifen (4OHT) (250 nM) for 2 hours as indicated. The experimental treatment conditions and TMT11-plex labeling are specified below: 126: DMSO pretreatment, non-induced control, replicate 1 127N: DMSO pretreatment, non-induced control, replicate 2 127C: DMSO pretreatment, non-induced control, replicate 3 128N: DMSO pretreatment, 4OHT-induction, replicate 1 128C: DMSO pretreatment, 4OHT-induction, replicate 2 129N: DMSO pretreatment, 4OHT-induction, replicate 3 129C: PP1 pretreatment, 4OHT-induction, replicate 1 130N: PP1 pretreatment, 4OHT-induction, replicate 2 130C: PP1 pretreatment, 4OHT-induction, replicate 3 131N: MEKi pretreatment, 4OHT-induction, replicate 1 131C: MEKi pretreatment, 4OHT-induction, replicate 2

Project description:The small molecule YC-1 was identified as identified as a selectively active agent against subsets of the two major live cancer subtypes, intrahepatic cholangiocarcinoma and hepatocellular carcinoma. Response to YC-1 is dependent on the expression of the sulfotransferase SULT1A1, which activates YC-1 through sulfonation. The contributions of mass spectrometry to the study were: (i) identifying SULT1A1 as the key player in YC-1 response through observing the protein in a cell line with acquired resistance to the small molecule treatment, (ii) corroborating the role of SULT1A1 in the YC-1 activity by correlating protein expression profiles and drug responses across 37 biliary cancer cell lines, (iii) showing that SULT1A1 expression was associated with IDH mutations, FGFR2 fusion, and BAP1 loss in vivo studying patient-derived xenograft (PDX) models, and (iv) identifying protein targets in a protein enrichment experiment with an immobilized drug. (i) and (ii): Cell line samples from datasets (i) and (ii) were analyzed together in a set of 12 TMT sets (ShiBardeesy_CellLines_TMT1 to TMT12) using TMT11-barcoding. The samples were analyzed on an Orbitrap Lumos mass spectrometer using the SPS-MS3 method. Prior to analysis, samples were fractionated offline using high pH reversed chromatography (12 fractions per TMT set). Across all TMT sets, channel 131c was used as the bridge channel (pooled digests of all samples). Samples were labeled as follows (rep = replicate: (i) Cell lines samples with acquired resistance to YC-1 treatment: ShiBardeesy_CellLines_TMT1: RBE_rep_1 (126), RBE YC1 Resistant 6_rep_1 (129c). ShiBardeesy_CellLines_TMT2: RBE YC1 Resistant 3_rep_1 (129n), RBE YC1 Resistant 1_rep_1 (130n). ShiBardeesy_CellLines_TMT3: RBE YC1 Resistant 2_rep_1 (126), RBE YC1 Resistant 5_rep_1 (130c). ShiBardeesy_CellLines_TMT4: RBE YC1 Resistant 4_rep_1 (126). ShiBardeesy_CellLines_TMT5: RBE YC1 Resistant 1_rep_2 (127n), RBE YC1 Resistant 4_rep_2 (128c), RBE YC1 Resistant 3_rep_2 (130c). ShiBardeesy_CellLines_TMT6: RBE YC1 Resistant 2_rep_2 (126), RBE YC1 Resistant 6_rep_2 (127c). ShiBardeesy_CellLines_TMT7: RBE_rep_2 (128n), RBE YC1 Resistant 5_rep_2 (130n). (ii) Proteomes of untreated biliary cell lines (baseline): ShiBardeesy_CellLines_TMT1: RBE_rep_1 (126), GB2_rep_1 (127n), HuCCT1_rep_1 (127c), ECC3_rep_1 (128n), ICC10_rep_1 (128c), KMCH-1_rep_1 (129n), SNU-1196_rep_1 (130n). ShiBardeesy_CellLines_TMT2: ICC13-7_rep_1 (126), ICC8_rep_1 (127n), ICC9_rep_1 (127c), SNU-478_rep_1 (128n), CC-SW-1_rep_1 (128c), CC-LP-1_rep_1 (129c), SSP-25_rep_1 (130c), ICC10-8_rep_1 (131n) ShiBardeesy_CellLines_TMT3: SNU-1079_rep_1 (127n), ICC5_rep_1 (127c), ICC7_rep_1 (128c), COR-L105_rep_1 (129n), ICC17_rep_1 (129c), GBC1_rep_1 (131n). ShiBardeesy_CellLines_TMT4: ICC3_rep_1 (127n), ICC2_rep_1 (127c), ICC106_rep_1 (128n), ICC11_rep_1 (128c), HKGZ-CC_rep_1 (129n), SNU-869_rep_1 (129c), HuH28_rep_1 (130n), ICC12_rep_1 (130c), SNU-308_rep_1 (131n). ShiBardeesy_CellLines_TMT5: ICC2_rep_2 (126), ECC3_rep_2 (127c), GB2_rep_2 (128n), ICC11_rep_2 (129n), ICC7_rep_2 (129c), SNU-869_rep_2 (130n), SSP-25_rep_2 (131n). ShiBardeesy_CellLines_TMT6: CC-LP-1_rep_2 (127n), COR-L105_rep_2 (128n), HuCCT1_rep_2 (129n), ICC12_rep_2 (129c), ICC3_rep_2 (131n), ICC5_rep_2 (130n), SNU-478_rep_2 (130c). ShiBardeesy_CellLines_TMT7: ICC10_rep_2 (126), ICC10-6_rep_2 (127n), ICC10-8_rep_2 (127c), RBE_rep_2 (128n), ICC9_rep_2 (128c), ICC17_rep_2 (129n), ICC8_rep_2 (129c), CC-SW-1_rep_2 (130c), GBC1_rep_2 (131n). ShiBardeesy_CellLines_TMT8: ICC13-7_rep_2 (127c), HuH28_rep_2 (128n), HKGZ-CC_rep_2 (128c), SNU-1079_rep_2 (129n), KMCH-1_rep_2 (129c), SNU-1196_rep_2 (130n), SNU-308_rep_2 (131n). ShiBardeesy_CellLines_TMT9: SG231_rep_1 (126), KKU-100_rep_1 (127n), YSCCC_rep_1 (127c), ICC4_rep_1 (128n), TKKK_rep_1 (128c), ECC2_rep_1 (129n), KKU-M213/M214 (129c). ShiBardeesy_CellLines_TMT10: YSCCC_rep_2 (126), KKU-M213/M214_rep_2 (127n), SG231_rep_2 (127c), TKKK_rep_2 (129n), ECC2_rep_2 (129c), ICC4_rep_2 (130n), KKU-100_rep_2 (131n). ShiBardeesy_CellLines_TMT11: ICC13-7_rep_1 (129n). ShiBardeesy_CellLines_TMT12: ICC13-7_rep2 (131n)

Project description:Supporting raw MS data for paper (doi: 10.1016/j.cell.2024.05.018) by Sinha N.K. et al, titled "The ribotoxic stress response drives UV-mediated cell death". Index of MS files and labels Table S1 - HaCaT Timecourse. 1-1 - Proteome (AO3604-3627 | Unimod:35; 2016; 4 | 126 -UT_01; 127n - UT_02; 127c - UT_03; 128n -1min_01; 128c - 1min_02; 129n - 1min_03; 129c - 1min_04; 130n - 5min_01; 130c - 5min_02; 131n - 5min_03; 131c - 15min_01; 132n - 15min_02; 132c - 15min_03; 133n - 30min_01; 133c - 30min_02; 134n - 30min_03) 1-2 - Phospho (AO3628-3651 | Unimod:35; 2016; 4; 21 | 126 -UT_01; 127n - UT_02; 127c - UT_03; 128n -1min_01; 128c - 1min_02; 129n - 1min_03; 129c - 1min_04; 130n - 5min_01; 130c - 5min_02; 131n - 5min_03; 131c - 15min_01; 132n - 15min_02; 132c - 15min_03; 133n - 30min_01; 133c - 30min_02; 134n - 30min_03) Table S2 - MCF10a KO and inhibitor (Set1 - ZAK & Set 2 - GCN2). 2-1-1 - Proteome (Set 1 - AO4019-4042 | Unimod:35; 2016; 4 | 126 - WT_UT_DMSO01; 127c - WT_UT_DMSO02; 128n - WT_UT_ZAKi01; 128c - WT_UT_ZAKi02; 129n - WT_UV_DMSO01; 129c -WT_UV_DMSO02; 130n - WT_UV_ZAKi01; 130c - WT_UV_ZAKi02; 131n - ZAK-KO_UT_DMSO01; 131c - ZAK-KO_UT_DMSO02; 132n - ZAK-KO_UT_ZAKi01; 132c - ZAK-KO_UT_ZAKi02; 133n - ZAK-KO_UV_DMSO01; 133c - ZAK-KO_UV_DMSO02; 134n - ZAK-KO_UV_ZAKi01; 134c -ZAK-KO_UV_ZAKi02) 2-1-2 - Proteome (Set 2 - AO4049-4072 | Unimod:35; 2016; 4 | 126 - WT_UT_DMSO01; 127c - WT_UT_DMSO02; 128n - WT_UT_GCN2i01; 128c - WT_UT_GCN2i02; 129n - WT_UV_DMSO01; 129c -WT_UV_DMSO02; 130n - WT_UV_GCN2i01; 130c - WT_UV_GCN2i02; 131n - GCN2-KO_UT_DMSO01; 131c - GCN2-KO_UT_DMSO02; 132n - GCN2-KO_UT_GCN2i01; 132c - GCN2-KO_UT_GCN2i02; 133n - GCN2-KO_UV_DMSO01; 133c - GCN2-KO_UV_DMSO02; 134n - GCN2-KO_UV_GCN2i01; 135n -GCN2-KO_UV_GCN2i02) 2-2-1 - Phospho (Set 1 - AO4013-4019 | Unimod:35; 2016; 4; 21 | 126 - WT_UT_DMSO01; 127c - WT_UT_DMSO02; 128n - WT_UT_ZAKi01; 128c - WT_UT_ZAKi02; 129n - WT_UV_DMSO01; 129c -WT_UV_DMSO02; 130n - WT_UV_ZAKi01; 130c - WT_UV_ZAKi02; 131n - ZAK-KO_UT_DMSO01; 131c - ZAK-KO_UT_DMSO02; 132n - ZAK-KO_UT_ZAKi01; 132c - ZAK-KO_UT_ZAKi02; 133n - ZAK-KO_UV_DMSO01; 133c - ZAK-KO_UV_DMSO02; 134n - ZAK-KO_UV_ZAKi01; 134c -ZAK-KO_UV_ZAKi02) 2-2-2 - Phospho (Set 2 - AO4043-4048 | Unimod:35; 2016; 4; 21 | 126 - WT_UT_DMSO01; 127c - WT_UT_DMSO02; 128n - WT_UT_GCN2i01; 128c - WT_UT_GCN2i02; 129n - WT_UV_DMSO01; 129c -WT_UV_DMSO02; 130n - WT_UV_GCN2i01; 130c - WT_UV_GCN2i02; 131n - GCN2-KO_UT_DMSO01; 131c - GCN2-KO_UT_DMSO02; 132n - GCN2-KO_UT_GCN2i01; 132c - GCN2-KO_UT_GCN2i02; 133n - GCN2-KO_UV_DMSO01; 133c - GCN2-KO_UV_DMSO02; 134n - GCN2-KO_UV_GCN2i01; 135n -GCN2-KO_UV_GCN2i02) Table S3 - HaCaT Kinase inhibitors (Set 1 & Set 2). 3-1-1 - Proteome (Set 1 - AO3766-3777 | Unimod:35; 2016; 4 | 126 - DMSO_UT01; 127n - DMSO_UT02; 127c - DMSO_UV01; 128n - DMSO_UV02; 128c - ZAKi(Nil)_UT01; 129n - ZAKi(Nil)_UT02; 129c - ZAKi(Nil)_UV01; 130n - ZAKi(Nil)_UV02; 130c - p38i_UT01; 131n - p38i_UT02; 131c - p38i_UV01; 132n - p38i_UV02; 132c - JNKi_UT01; 133n - JNKi_UT02; 133c - JNKi_UV01; 134n - JNKi_UV02) 3-1-2 - Proteome (Set 2 - AO3778-3789 | Unimod:35; 2016; 4 | 126 - DMSO_UT01; 127n - DMSO_UT02; 127c - DMSO_UV01; 128n - DMSO_UV02; 128c - ZAKi(Vem)_UT01; 129n - ZAKi(Vem)_UT02; 129c - ZAKi(Vem)_UV01; 130n - ZAKi(Vem)_UV02; 130c - GCN2i_UT01; 131n - GCN2i_UT02; 131c - GCN2i_UV01; 132n - GCN2i_UV02; 132c - ATRi_UT01; 133n - ATRi_UT02; 133c - ATRi_UV01; 134n - ATRi_UV02) 3-2-1 - Phospho (Set 1 - AO3754-3759 | Unimod:35; 2016; 4; 21 | 126 - DMSO_UT01; 127n - DMSO_UT02; 127c - DMSO_UV01; 128n - DMSO_UV02; 128c - ZAKi(Nil)_UT01; 129n - ZAKi(Nil)_UT02; 129c - ZAKi(Nil)_UV01; 130n - ZAKi(Nil)_UV02; 130c - p38i_UT01; 131n - p38i_UT02; 131c - p38i_UV01; 132n - p38i_UV02; 132c - JNKi_UT01; 133n - JNKi_UT02; 133c - JNKi_UV01; 134n - JNKi_UV02) 3-2-2 - Phospho (Set 2 - AO3760-3765 | Unimod:35; 2016; 4; 21 | 126 - DMSO_UT01; 127n - DMSO_UT02; 127c - DMSO_UV01; 128n - DMSO_UV02; 128c - ZAKi(Vem)_UT01; 129n - ZAKi(Vem)_UT02; 129c - ZAKi(Vem)_UV01; 130n - ZAKi(Vem)_UV02; 130c - GCN2i_UT01; 131n - GCN2i_UT02; 131c - GCN2i_UV01; 132n - GCN2i_UV02; 132c - ATRi_UT01; 133n - ATRi_UT02; 133c - ATRi_UV01; 134n - ATRi_UV02). Tabel S4 - ZAK affinity purification. 4-1 - Label-free ZAK pulldown (mNG-ZAK-WT labeled files | Unimod:35; 4| Untreated or ANS treated cells) Additional file: AO4072_GCN2_RSP10_tMS2: Targeted RPS10-Kgg search | Unimod:35; 2016; 4; 492 | TMT label as 2-1-2.

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Generation of a biliary tract cancer cell line atlas identifies molecular subtypes and therapeutic targets

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