Supplemental Information. Genetic Regulation of Plasma Lipid Species. and Their Association with Metabolic Phenotypes
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1 Cell Systems, Volume 6 Supplemental Information Genetic Regulation of Plasma Lipid Species and Their Association with Metabolic Phenotypes Pooja Jha, Molly T. McDevitt, Emina Halilbasic, Evan G. Williams, Pedro M. Quiros, Karim Gariani, Maroun B. Sleiman, Rahul Gupta, Arne Ulbrich, Adam Jochem, Joshua J. Coon, Michael Trauner, David J. Pagliarini, and Johan Auwerx
2 Supplementary Figures and Figure Legends Figure S1. Quality assessment of MS measurements and reproducibility. Related to Figure 1. (A) Heatmap of correlations between technical replicates (from separate runs) of six plasma samples showing high Spearman correlation between the replicates vs. between the strains. (B) Heatmap of extraction replicates of the same liver sample extracted and run in 12 batches, equivalent to the 12 batches of the BXD samples. A B TAG(5:3) QTL in at chr. 5 GWAS traits in humans Gckr: 3. Hypertriglyceridemia Cholesterol Coronary artery disease Metabolic Syndrome Fasting glucose, Insulin NAFLD Type 2 diabetes Gckr Lrpap Map position (Mb) 14 Mouse chr. 19 lqtls in HFD GWAS traits in humans FADS 1, 2, 3: Omega-6 PUFA Phospholipid levels Triglyceride Fasting glucose Type 2 diabetes Fads1,2,3 1 Lrpap1: Triglyceride Cholesterol LCL-cholesterol PC(32:2) PC(33:1) PC(36:1) PC(16:_18:1) TAG(52:3) TAG(53:4) 4 LOD score LOD score Map position (Mb) 5 6 Human chr. 11 5' 3' FADS2 61 3' 62 FADS1 FADS Mb 5' Figure S2. lqtls harboring genes associated with abnormal lipid metabolism in human GWAS. Related to Figure 3. (A) QTL locus for TAG(5:3) enclosing the human GWAS gene: Gckr and Lrpap1. (B) QTL hotspot locus for the 6 lipid species on mouse Chr19 enclosing the GWAS genes: Fads 1, 2, 3. The syntenic region on human Chr11 is shown below. The genomic location of the genes is shown in green in the positive stand for FADS2 and in the negative strand for FADS1 and FADS3. The GWAS phenotypes associated with the genes is indicated on the right. Blue dotted line represents the suggestive QTL threshold.
3 A TAG_58.1_1 LinoleicAcid PE_16._18.2 PE_18.1_18.2 PG_LP PI_17._2.4 TAG_48.3 TAG_5.4 TAG_54.6_2 TAG_56.8 PC_18.e_22.6 PE_18.e_18.1 PC_17.1_18.2 PC_32.2 PG_OP TAG_51.3 DG_18.1_18.2 TAG_44.1 PC_18.2_18.2 TAG_48. TAG_5. PE_16._18.1 PE_2.e_18.2 TAG_51.1 PE_2.e_22.6 NervonicAcid TAG_6.13 PE_18.e_22.6 DAG_AoP CoQ8 PE_16.e_22.6 TAG_56.1 TAG_55.2 TAG_55.3 TAG_54.1 TAG_56.2 TAG_58.2 TAG_58.3 TAG_58.4 PE_AoP PE_DhaP PE_AoS PC_19._22.6 PC_16.e_2.4 PI_DhaS PC_34.2 PI_AoP PI_18.1_2.4 PC_16._18.1 PC_33.1 PI_AoS PalmitoleicAcid StearicAcid DG_18.1_2.4 OleicAcid PE_18.e_2.4 Q9 PC_4.8 PC_18._16. PC_36.2 PC_18.2_2.4 PC_38.6 PE_2.2_22.6 TAG_62.14 TAG_58.9 TAG_64.16 TAG_56.7 TAG_58.1_2 MyristicAcid PalmiticAcid ErucicAcid TAG_5.3 TAG_46.1 TAG_48.2 TAG_53.3 TAG_53.2 TAG_51.2 TAG_54.4 TAG_56.4 TAG_5.1 TAG_52.1 TAG_54.5_2 TAG_48.1 TAG_5.2 DG_18.1_18.1 TAG_56.3 TAG_54.2 TAG_52.3 TAG_6.12 PC_18._2.5 PC_2._22.6 PC_2._2.4 HFD Run distance post training (m) NisinicAcid Liver mass (g) Run distance post training (m) Heart weight (%) Liver mass (g) B TAG_51.3 TAG_5.4 TAG_48.3 TAG_52.3 DG_18.1_18.2 TAG_53.3 TAG_54.6_2 PE_16._18.2 PC_2._22.6 TAG_58.4 TAG_58.3 TAG_58.2 TAG_56.1 TAG_55.2 TAG_56.2 TAG_51.1 TAG_52.1 TAG_54.1 PE_2.e_18.2 PE_18.e_18.1 TAG_56.8 PC_19._22.6 TAG_6.13 TAG_58.1_1 TAG_56.7 PC_18.e_22.6 PE_2.e_22.6 TAG_54.4 TAG_55.3 TAG_54.5_2 PC_2._2.4 TAG_5.3 TAG_48.2 TAG_51.2 TAG_44.1 TAG_46.1 TAG_48.1 TAG_5.1 ErucicAcid TAG_53.2 TAG_54.2 NervonicAcid PE_18.1_18.2 PC_18.2_18.2 TAG_5. TAG_48. LinoleicAcid PE_16.e_22.6 PE_18.e_22.6 TAG_62.14 TAG_58.9 TAG_58.1_2 TAG_64.16 DG_18.1_2.4 TAG_6.12 PE_2.2_22.6 PE_AoS PE_DhaP PE_AoP TAG_56.4 TAG_56.3 NisinicAcid PG_LP PG_OP DG_18.1_18.1 TAG_5.2 PI_17._2.4 PC_16.e_2.4 PalmitoleicAcid MyristicAcid PalmiticAcid StearicAcid DAG_AoP PE_16._18.1 PI_DhaS OleicAcid PC_32.2 PI_AoP PC_17.1_18.2 PC_34.2 PC_36.2 PE_18.e_2.4 PC_18._2.5 PC_16._18.1 CoQ8 Q9 PC_33.1 PC_18.2_2.4 PC_38.6 PC_18._16. PI_18.1_2.4 PC_4.8 PI_AoS TAG_58.1_1 PC_18.2_18.2 PE_16._18.2 PE_18.1_18.2 PG_LP PI_17._2.4 PE_18.e_18.1 PC_17.1_18.2 TAG_48. PC_18._2.5 NisinicAcid TAG_6.12 TAG_52.3 TAG_5.2 PC_2._22.6 PC_2._2.4 DG_18.1_18.1 TAG_56.3 TAG_54.2 lipids HFD lipids Heart weight (%) Run distance (m) Liver mass (g) TAG_51.3 TAG_5.4 TAG_48.3 TAG_51.1 TAG_52.1 TAG_54.1 PE_2.e_18.2 TAG_58.4 TAG_58.3 TAG_58.2 TAG_55.2 TAG_56.2 PC_16._18.1 CoQ8 CoQ9 PC_33.1 PC_18.2_2.4 PC_38.6 PC_18._16. PI_18.1_2.4 PC_4.8 PI_AoS lipids lipids Run distance (m) Heart weight (%) Liver mass (g) spearman s rho
4 Figure S3. Association of lipid species with. Related to Figure 4 and Table S6. (A and B) Heatmap with an unsupervised hierarchical clustering of Spearman s correlation rho of (A) all the lipid species and in (top) and HFD (bottom); (B) select lipid species in each diet which show maximum number of significant correlation with (the lateral lipid species cluster of panel A). For panel B, the vertical green lipid cluster represents healthy lipids (specific and common in each diet), whereas the vertical red cluster represents the unhealthy lipids (specific and common in each diet). For A and B the horizontal green phenotype cluster represents healthy whereas the red cluster represents unhealthy. Red indicates positive correlation and blue negative correlation.
5 R.U. (AUC) e HFD Plasma Liver Plasma Liver p=4e-22 FC=2.11 p=2e-15 FC=1.78 p=3.7e-6 FC=1.55 p=.21 FC=1.16 p=7.4e-9 FC=3.43 TAG(52:2) TAG(54:3) TAG(56:3) TAG(5:2) TAG(54:1) e p=2.3e-6 FC=1.11 p=2.7e-4 FC=1.17 p=8.4e-6 FC=1.47 p=.54 FC=1.5 p=3.1e-3 FC=1.36 e p=2.2e-13 FC=2.25 p=1.3e-16 FC=1.66 p=4.8e-18 FC=3.7 p=3.2e-8 FC=1.77 TAG(52:5) TAG(52:4) TAG(54:6)_1 DAG(L_P) e p=1.2e-12 FC=1.4 p=6e-1 FC=1.15 p=4.2e-12 FC=1.85 p=9.1e-3 FC=1.21 Figure S4. Plasma and liver levels of 9 TAG species having the most significant correlation between plasma and liver in both diets. Related to Figure 5 and Table S2. Dot plot showing the levels of 9 shortlisted lipids as potential lipid signatures of NAFLD in plasma and liver. Lipids in red font indicate pro-nafld signatures and those in blue font indicate anti-nafldsignatures. P-value <.5 by Welch s t-test was considered significant between diets.
6 D A NR (9 weeks) B C 1 *** ** HFHS ** Age (wks): E Triglycerides (mg/dl) G Birth GO-BP lipid biosynthetic processes GO-BP lipid catabolic processes HFHS Diet *** *** ** HFHS NR Steatosis NASH, early stage NASH, adv. stage F Sacrifice TG (mg/g) Pro NAFLD signatures Anti NAFLD signatures ATGL mrna expression Sub WAT Liver Heart Quadriceps lipid biosynthetic process monocarboxylic acid biosynthetic process carboxylic acid biosynthetic process small molecule biosynthetic process coenzyme biosynthetic process acetyl CoA biosynthetic process acyl CoA biosynthetic process thioester biosynthetic process organic acid biosynthetic process cofactor biosynthetic process sulfur compound biosynthetic process FA biosynthetic process regulation of FA biosynthetic process positive regulation of FA biosynthetic process glycerolipid biosynthetic process long chain FA biosynthetic process membrane lipid biosynthetic process sphingolipid biosynthetic process small molecule catabolic process carboxylic acid catabolic process organic acid catabolic process lipid catabolic process cellular lipid catabolic process lipid oxidation FA oxidation monocarboxylic acid catabolic process FA catabolic process PC2 ( %) HFHS+NR PC1 ( 78.6 %) PC2 ( 19.5 %) Steatosis NASH, early stage NASH, adv. stage PC1 ( %) Plasma Plasma HFD Liver Liver HFD Association of NAFLD signatures with biological processes Liver Plasma Liver Plasma pro-nafld signatures anti-nafld signatures Figure S5. Assessment of TAG NAFLD signatures in mice and humans and their association with biosynthetic pathways. Related to Figure 6. (A-C) C57BL/6J mice: (A) Schematic illustration of the three experimental groups used for validation of the NAFLD signatures; mice on (green), mice on HFHS diet from 7-25 weeks (grey), mice starting HFHS diet at 7 weeks and treated with nicotinamide riboside (NR) 9 weeks after the start of HFHS diet until the end of the study (for 9 weeks - therapeutic intervention, magenta). (B) Liver total TAG concentration (normalized to liver weight). (C) Principal component analysis (PCA) of 55 TAG species shows clear separation of only the group on PC1. (D and E) Human subjects: (D) PCA of 55 TAG species measured in human plasma from healthy, steatosis and NASH patients. (E) Plasma total TAG levels in human samples. (F and G) BXDs: (F) Correlation matrix showing the Pearson correlation of Atgl mrna expression in four different metabolic tissues with the pro- and anti-nafld TAG signatures in plasma (left) and liver (right) for both diets. (G) Gene ontology biological processes (GO BP) associated with
7 NAFLD TAG signatures. Pathway enrichment analysis was performed with the liver transcripts that significantly correlated (both positively and negatively) with the PC1 of pro- and anti- NAFLD signatures in liver and plasma. Red and blue cells represent the enriched pathways with the positively (scale bar: log 1 p-value) and negatively (scale bar: -log 1 p-value) correlated liver transcripts respectively. For B and E differences in mean TAG levels were compared using two-sample t tests. *p<.5, **p<.1, ***p<.1.
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