Identification of Lipidomic Biomarkers for Coexposure to Subtoxic Doses of Benzo[a]pyrene and Cadmium: The Toxicological Cascade Biomarker Approach
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1 Supporting Information Identification of Lipidomic Biomarkers for Coexposure to Subtoxic Doses of Benzo[a]pyrene and Cadmium: The Toxicological Cascade Biomarker Approach Harald Jungnickel,*,1 Sarah Potratz, 1 Sven Baumann, 2,3 Patrick Tarnow, 1 Martin von Bergen, 2,4,5 and Andreas Luch 1 1 German Federal Institute for Risk Assessment (BfR), Department of Product Safety, Max- Dohrn-Strasse 8-10, Berlin, Germany 2 UFZ Helmholtz-Centre for Environmental Research, Department of Metabolomics, Permoserstrasse 15, Leipzig, Germany 3 University of Leipzig, Institute of Pharmacy, Faculty of Biosciences, Pharmacology and Psychology, Leipzig, Germany 4 UFZ Helmholtz-Centre for Environmental Research, Department of Proteomics, Permoserstrasse 15, Leipzig, Germany 5 Aalborg University, Department of Biotechnology, Chemistry and Environmental Engineering, 9000 Aalborg, Denmark * Correspondence: harald.jungnickel@bfr.bund.de Summary The number of pages: 10 The number of tables: 2 The number of figures: 3 Page S2: Page S4: Page S6: Page S7: Page S8: Page S9: Page S10: Table S1. List of metabolites (Biocrates Kit p150). Table S2. List of 18 metabolites used for multivariate statistics. Full figure captions. Figure S1. Color code model based on standard deviation changes of mean values for MCF-7 cells treated with benzo[a]pyrene (BP) and BP plus cadmium (Cd). Figure S2. Color code model based on standard deviation changes of mean values for MCF-7 cells treated with different compounds. Figure S3. Metabolic changes in the lipid composition of MCF-7 cells. List of abbreviations used in the text.
2 Supplementary Table S1. List of metabolites (Biocrates Kit p150). Metabolite class Number of analytes quantitative measurement Analyte name or abbreviation for: semi-quantitative measurement* Amino acids arginine, glutamine, glycine, histidine, 14 methionine, ornithine, phenylalanine, proline, serine, threonine, tryptophan, tyrosine, valine, (iso)leucine Sum of hexoses 1 H1 Carnitine 1 C0 Acylcarnitines 26 Hydroxy- and dicarboxyacylcarnitines Sphingomyelins Hydroxysphingomyelins Diacyl-phosphatidylcholines C2, C3, C4, C5, C6 (or C4:1-DC), C8, C10, C12, C14, C16, C18, C3:1, C4:1, C5:1, C6:1, C8:1, C9, C10:1, C10:2, C12:1, C14:1, C14:2, C16:1, C16:2, C18:1, C18:2 C3-OH, C4-OH (or C3-DC), C5-DC (or C6-OH), C5-OH (or C3-DC-M), C5:1-DC, C5-M-DC, C7-DC, C12-DC, C14:1-OH, C14:2-OH, C16:1-OH, C16:2- OH, C16-OH, C18:1-OH SM C16:0, SM C16:1, SM C18:0, SM C18:1, SM C20:2, SM C22:3, SM C24:0, SM C24:1, SM C26:0, SM C26:1 SM (OH) C14:1, SM (OH) C16:1, SM (OH) C22:1, SM (OH) C22:2, SM (OH) C24:1 PC aa C24:0/C26:0/C28:1/C30:0/C30:2/C32:0/C32:1/ C32:2/C32:3/ C34:1/C34:2/C34:3/C34:4/C36:0/C36:1/C36:2/ C36:3/C36:4/C36:5/ C36:6/C38:0/C38:1/C38:3/C38:4/C38:5/C38:6/ C40:1/C40:2/C40:3/ C40:4/C40:5/C40:6/C42:0/C42:1/C42:2/C42:4/ C42:5/C42:6
3 Acyl-alkyl-phosphatidylcholines 39 Lyso-phosphatidylcholines 15 total 163 PC ae C30:0/C30:1/C30:2/C32:1/C32:2/C34:0/C34:1/ C34:2/C34:3/C36:0/ C36:1/C36:2/C36:3/C36:4/C36:5/C38:0/C38:1/ C38:2/C38:3/C38:4/ C38:5/C38:6/C40:0/C40:1/C40:2/C40:3/C40:4/ C40:5/C40:6/C42:0/ C42:1/C42:2/C42:3/C42:4/C42:5/C44:3/C44:4/ C44:5/C44:6 lysopc a C6:0/C14:0/C16:0/C16:1/C17:0/C18:0/C18:1/C 18:2/C20:3/ C20:4/C24:0/C26:0/C26:1/C28:0/C28:1 Abbreviations are as follows: Cx:y (x=number of carbons in the fatty acid side chain, y = number of double bonds in the fatty acid side chain), decarboxyl (DC), hydroxyl (OH), methyl (M), phosphatidylcholine (PC), acyl-acyl (aa), acyl-alkyl (ae), lyso (a), sphingomyelin (SM). *For semi-quantitative analytes no exactly matched isotope labeled internal standard is available, which may affect their accuracy, nevertheless many of these metabolites can be measured with high precision.
4 Supplementary Table S2: List of 18 metabolites, which were selected for group separation (normalized mean values ± S.D.). Metabolite Control BP BP + Cd Cd BP + Cd + D609 BP + Cd + Ro PC aa C32: ± ± ± ± ± ± 13.2 PC aa C34: ± ± ± ± ± ±20.6 PC aa C36: ± ± ± ± ± ± 25 PC aa C36: ± ± ± ± ± ± 25.7 PC aa C42: ± ± ± ± ± ± 24.5 PC ae C34: ± ± ± ± ± ± 25.5 PC ae C34: ± ± ± ± ± ± 17 PC ae C36: ± ± ± ± ± ± 24 PC ae C38: ± ± ± ± ± ± 22.6 Lyso-PC C16: ± ± ± ± ± ± 28.9 Lyso-PC C16:1 100 ± ± ± ± ± ± 27.0 SM C16: ± ± ± ± ± ± 17.4 SM C16: ± ± ± ± ± ± 26.9 SM C24: ± ± ± ± ± ± 10.9
5 SM C24: ± ± ± ± ± ± 12.9 SM C26: ± ± ± ± ± ± 19.1 SM C26:1 102 ± ± ± ± ± ± 12.3 SM(OH) C22 : ± ± ± ± ± ± 7.8 All values were within the operational range of the assay.
6 Captions Supplementary Figures: Supplementary Figure S1. Color code model based on standard deviation changes of mean values for MCF-7 cells treated with benzo[a]pyrene (BP) and BP plus cadmium (Cd). a) The colour code model indicates an increase in metabolite levels of MCF-7 cells coexposed to BP (1 µm) plus Cd (0.1 nm). b) The colour code model indicates a decrease in metabolite levels of MCF-7 cells co-exposed to BP (1 µm) plus Cd (0.1 nm) in comparison to cells treated with BP (1 µm) only. c) The colour code model indicates only a increase in metabolite levels of MCF-7 cells co exposed to BP (1 µm) plus Cd (0.1 nm). d). The colour code model indicates no difference in metabolite levels of MCF-7 cells co-exposed to BP (1 µm) plus Cd (0.1 nm) compared to cells treated with BP (1 µm) only. The legend shows the colour code for each group. Supplementary Figure S2. Color code model based on standard deviation changes of mean values for MCF-7 cells treated with different compounds. The following compounds were administered: a) BP (1 µm) or BP (1 µm) plus α-naphthoflavone (α-nf, 1 µm). b) BP (1 µm) plus Cd (0.1 nm) or BP (1 µm) plus Cd (0.1 nm) and α-nf (1 µm). c) Similar treatment of AHR-null MCF cells with BP or BP plus Cd. d) BP (1 µm) plus Cd (0.1 nm), BP (1µM) plus Cd (0.1 nm) and D609 (50 µg/ml), or BP (1µM) plus Cd (0.1 nm) and Ro (1 µm). The legend shows the colour code for each group. Supplementary Figure S3. Metabolic changes in the lipid composition of MCF-7 cells. Cells were treated with BP plus Cd, BP plus Cd and D609, or BP plus Cd and Ro Values of the discriminant scores obtained from Fisher s discriminant analysis of 18 MCF-7 samples for 18 principal compounds, which were selected to discriminate between cells treated as mentioned above. All three groups can be separated from each other. The model was evaluated using the leave-one-out formalism (100% correct grouping of ungrouped cases).
7 Supplementary Fig. S1: a) Control Cd BP BP + Cd SM 16:0 SM 24:1 SM 26:1 PC aa C34:1 PC ae C34:0 PC ae C 36:1 PC ae C 38:2 PC aa C32:1 PC aa C36:2 PC aa C 42:2 PC ae C 34:1 b) c) d) SM 26:0 SM 16:1 SM(OH) C22:1 Lyso PC C16:1 SM 24:0 Lyso PC C16:0 PC aa C 36:1 Control Control Control Cd Cd Cd BP BP BP BP + Cd BP + Cd BP + Cd Group 1 Group 2 Group 3 Group 4 Group 5 Group 6 Group 7 Group 8 No change 2StDev+ 3StDev+ 4StDev+ 5StDev+ 6StDev+ 7StDev+ 8StDev+
8 Supplementary Fig. S2: a) b) c) d) Group 1 Group 2 Group 3 Group 4 Group 5 Group 6 Group 7 Group 8 No change 2StDev+ 3StDev+ 4StDev+ 5StDev+ 6StDev+ 7StDev+ 8StDev+
9 Supplementary Fig. S3:
10 List of Abbreviations: BP = benzo[a]pyrene Cd = cadmium PC-PLC = phosphatidylcholine-specific phospholipase C D609 = O-tricyclo[ ,6698 ]dec-9-yl dithiocarbonate potassium salt HER-2 = human epidermal growth factor receptor 2 MKP-1 = mitogen-activated protein kinase phosphatase-1 Ro =2-{1-[3-(Amidinothio)propyl]-1H-indol-3-yl}-3-(1-methylindol-3-yl)maleimide α-nf = α-naphthoflavone AHR = aryl hydrocarbon receptor ERK = extracellular signal-regulated kinases SM = sphingomyelin PC = phosphatidylcholine lysopc = lysophosphatidylcholine PAH = polycyclic aromatic hydrocarbon NFκB = nuclear factor kappa-light-chain-enhancer of activated B cells SM(OH) = hydroxy sphingomyelin TGF-β = transforming growth factor β Nrf-2 = nuclear factor (erythroid-derived 2)- like 2 c-src = thyrosine kinase (cellular and sarcoma) EGFR = epidermal growth factor receptor
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