Biomarkers of NAFLD progression an omics approach to an epidemic
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1 Biomarkers of NAFLD progression an omics approach to an epidemic D. Lee Gorden 1,2, David S. Myers 3, Pavlina T. Ivanova 3, Eoin Fahy 4, Mano R. Maurya 4, Shakti Gupta 4, Jun Min 4, Nathanael J. Spann 5, Jeffrey G. McDonald 6, Samuel L. Kelly 7, Jingjing Duan 7, M. Cameron Sullards 7, Thomas J. Leiker 8, Robert M. Barkley 8, Oswald Quehenberger 9,10, Aaron M. Armando 10, Stephen B. Milne 3, Thomas P. Mathews 3, Michelle D. Armstrong 3, Chijun Li 11, Willie V. Melvin 1, Ronald H. Clements 1, M. Kay Washington 12, Alisha M. Mendonsa 2, Joseph L. Witztum 9, Ziqiang Guan 11, Christopher K. Glass 5, Robert C. Murphy 8, Edward A. Dennis 10,13, Alfred H. Merrill Jr. 7, David W. Russell 6, Shankar Subramaniam 4,13*, H. Alex Brown 3,14* 1 Department of Surgery, Vanderbilt University Medical Center, Nashville, TN, USA. 2 Department of Cancer Biology, Vanderbilt University Medical Center, Nashville, TN, USA. 3 Department of Pharmacology, Vanderbilt University Medical Center, Nashville, TN, USA. 4 Department of Bioengineering, School of Engineering, University of California, San Diego, La Jolla, CA, USA. 5 Department of Cellular and Molecular Medicine and Department of Medicine, University of California, San Diego, La Jolla, CA, USA. 6 Department of Molecular Genetics, University of Texas Southwestern Medical Center, Dallas, TX, USA. 7 Schools of Biology, Chemistry, and Biochemistry, and the Parker H. Petit Institute for Bioengineering and Bioscience, Georgia Institute of Technology, Atlanta, GA, USA. 8 Department of Pharmacology, University of Colorado at Denver, Aurora, CO, USA. 9 Department of Medicine, School of Medicine, University of California, San Diego, La Jolla, CA, USA. 10 Department of Pharmacology, School of Medicine, University of California, San Diego, La Jolla, CA, USA. 11 Department of Biochemistry, Duke University Medical Center, Durham, NC, USA. 12 Departments of Pathology, Microbiology and Immunology, Vanderbilt University Medical Center, Nashville, TN, USA. 13 Department of Chemistry & Biochemistry, School of Medicine, University of California, San Diego, La Jolla, CA, USA. 14 Department of Biochemistry and the Vanderbilt Institute of Chemical Biology, Vanderbilt University Medical Center, Nashville, TN, USA. *To whom correspondence should be addressed: alex.brown@vanderbilt.edu; shankar@ucsd.edu Running Title: In search for NASH biomarkers
2 List of Supplementary Data Files Supplementary Data file 1. Fold-changes and ANOVA p-values for the lipids in liver and plasma samples. The columns S/N, H/N, C/N and H/S list the fold-change. The column "Pvalue(N,S,H,C)" lists the ANOVA p-value across the four classes. Supplementary Data file 2. Fold-changes for genes related to different lipid categories. Supplementary Data file 3. Cross-correlation between lipids and matrix metalloproteinase (MMP) and related (TIMP) genes. Supplementary Data file 4. Result of pair-wise SNP analysis among the four classes, N, S, H and C, using plink, for PNPLA3 SNPs. For example, the sheet plink_ns_snp_pnpla3 shows the results for comparison between the N and S samples. Supplementary Data file 5. (A) Result of procedure LDA2 on plasma lipids to classify NASH vs. steatosis samples. First, LDA was applied on 30 top ANOVA lipids, then on 20 selected lipids (see also Supplementary Fig. S7). LDA coefficients and mean values for the two classes, steatosis (S) and NASH (H), for the 20 lipids are listed. (B) Prediction of the class, steatosis (S) or NASH (H), during k-fold cross-validation. The columns H and S list the predicted probability for the respective class.
3 Supplementary Data File 1 liver S/N H/N C/N H/S p-value(n,s,h,c) plasma S/N H/N C/N H/S p-value(n,s,h,c) 6k PGF1a E-03 tetranor 12-HETE E-10 6,15 dk-,dh- PGF1a E-04 LTE Inf 2.01E-04 dhk PGD E-03 5-HETE E-05 LTE E-03 9-HOTrE E HETrE E-03 5-HETrE E HETE E HETE E HDoHE E HODE E-09 CL (72:8) E HETrE E-03 CL (74:8) E-03 8-HETE E-05 CL (74:7) E HETE E-03 Dolichol E-07 9-HODE E-06 Dolichol E HETE E-03 Dolichol E-07 19,20 DiHDPA E-02 Dolichol E-07 9,10 EpOME E-04 22R -hydroxycholesterol E-03 12,13 EpOME E hydroxycholesterol E-04 8,9-diHETrE E-05 7α-hydroxycholesterol E-03 11,12-diHETrE E-05 Desmosterol E-03 14,15-diHETrE E desmethyl-14-dehydrolanosterol E-09 12,13 dihome E-05 Lanosterol E-06 20cooh AA E-12 Cholestanol E-06 FA(14:0) E-06 3-oxo,7α-hydroxycholesterol E-07 FA(15:0) E-03 CE(16:1) E-03 FA(16:1) E-06 CE(16:0) E-04 FA(17:1) E-03 CE(18:3) E-06 FA(18:0) E-03 CE(18:2) E-09 FA(20:2) E-04 CE(18:1) E-03 FA(20:3 N9) E-04 CE(20:4) E-05 Dolichol E-03 CE(20:3) E-04 7α,27-dihydroxycholesterol E-03 CE(22:6) E-06 24S-hydroxycholesterol E-02 CE(22:5) E hydroxycholesterol E-03 TAG(44:3) E-02 24,25-epoxycholesterol E-04 TAG(44:2) E-03 7α-hydroxycholesterol E-03 TAG(44:1) E-04 5α-hydroxycholesterol E-03 TAG(44:0) E-04 5,6β-epoxycholesterol E-04 TAG(46:4) E-02 5,6α-epoxycholesterol E-03 TAG(46:3) E desmethyl-14-dehydrolanosterol E-05 TAG(46:2) E Desmethyllanosterol E-04 TAG(46:1) E-05 Lanosterol E-04 TAG(46:0) E-04 Sitosterol E-06 TAG(47:3) E-03 Stigmastanol E-03 TAG(47:2) E-03 Cholesterol-total E-08 TAG(47:1) E-04 3-oxo,7α-hydroxycholesterol E-05 TAG(47:0) E-03 CE(18:2) E-04 TAG(48:4) E-04 CE(20:4) E-07 TAG(48:3) E-06 CE(20:3) E-04 TAG(48:2) E-05 CE(22:6) E-03 TAG(48:1) E-05 TAG(50:2) E-03 TAG(48:0) E-05 TAG(52:5) E-03 TAG(49:5) E-03 TAG(52:4) E-04 TAG(49:3) E-04 TAG(52:3) E-04 TAG(49:2) E-05 TAG(52:2) E-03 TAG(49:1) E-06 TAG(52:1) E-03 TAG(49:0) E-05 TAG(54:5) E-03 TAG(50:5) E-04 TAG(54:4) E-03 TAG(50:4) E-07 TAG(54:3) E-02 TAG(50:3) E-08 TAG(56:6) E-02 TAG(50:2) E-03 1,2-DAG(34:3) E-03 TAG(50:1) E-04 1,2-DAG(34:2) E-03 TAG(50:0) E-04 1,2-DAG(36:3) E-03 TAG(51:5) E-04 1,2-DAG(36:2) E-04 TAG(51:4) E-06 C18:1 Cer E-03 TAG(51:3) E-07 C18 Cer E-10 TAG(51:2) E-05 C20 Cer E-08 TAG(51:1) E-06 C22 Cer E-08 TAG(51:0) E-05 C24:1 Cer E-06 TAG(52:5) E-07 C24 Cer E-07 TAG(52:4) E-05 C24:1 HexCer E-06 TAG(52:3) E-03 C24 HexCer E-03 TAG(52:1) E-04 C26:1 HexCer E-06 TAG(52:0) E-04 C26 HexCer E-03 TAG(53:5) E-06 C18:1 Sphingomyelin E-10 TAG(53:4) E-06 C18 Sphingomyelin E-08 TAG(53:3) E-06 C20 Sphingomyelin E-09 TAG(53:2) E-04 C22 Sphingomyelin E-06
4 TAG(53:1) E-05 C24 Sphingomyelin E-04 TAG(53:0) E-03 C18DH Cer E-07 TAG(54:6) E-06 C24:1DH Cer E-06 TAG(54:5) E-06 C24:1DH HexCer E-03 TAG(54:4) E-05 C18DH Sphingomyelin E-06 TAG(54:3) E-04 C22DH Sphingomyelin E-05 TAG(54:2) E-03 C24DH Sphingomyelin E-03 TAG(54:1) E-05 Sphingosine E-03 TAG(54:0) E-03 Sphingosine-P E-03 TAG(55:6) E-03 Sphinganine-P E-03 TAG(55:5) E-05 C16 1-deoxyCer E-04 TAG(55:4) E-05 C26:1 1-deoxyCer E-05 TAG(55:3) E-04 C18DH 1-deoxyCer E-04 TAG(55:2) E-03 C20DH 1-deoxyCer E-04 TAG(55:1) E-05 C22DH 1-deoxyCer E-04 TAG(55:0) E-03 C24DH 1-deoxyCer E-04 TAG(56:6) E-05 C24:1 GlcCer E-06 TAG(56:5) E-05 C24 GlcCer E-03 TAG(56:4) E-05 C26:1 GlcCer E-07 TAG(56:3) E-05 C26 GlcCer E-04 TAG(56:2) E-04 PC(32:0) E-06 TAG(56:1) E-04 PC(34:3) E-06 TAG(57:6) E-04 PC(34:2) E-03 TAG(57:5) E-04 PC(36:1e) E-03 TAG(57:4) E-04 PC(36:4) E-15 TAG(57:3) E-04 PC(38:6) E-07 TAG(57:2) E-03 PC(38:5) E-10 TAG(57:1) E-03 PC(38:4) E-12 TAG(57:0) E-03 PC(38:3) E-05 TAG(58:6) E-04 PC(40:6) E-05 TAG(58:5) E-05 PC(40:5) E-03 TAG(58:4) E-06 LPC(16:0) E-04 TAG(58:3) E-05 LPC(18:0) E-02 TAG(58:2) E-02 PE(36:4) E-04 TAG(60:12) E-05 PE(36:3) E-02 TAG(59:2) E-03 PE(38:5p) E-03 TAG(59:0) E-03 PE(38:4p) E-03 TAG(60:4) E-05 PE(38:6) E-04 TAG(60:3) E-03 PE(38:5) E-04 1,2-DAG(32:0) E-02 PE(38:4) E-06 1,2-DAG(34:4) E-03 PE(40:5p) E-03 1,2-DAG(34:2) E-02 PE(40:4p) E-03 1,2-DAG(34:1) E-03 PE(40:6) E-04 1,2-DAG(34:0) E-03 PE(40:5) E-05 1,2-DAG(35:4) E-03 PI(32:1) E-02 1,2-DAG(35:1) E-02 PI(36:3) E-03 1,2-DAG(35:0) E-03 PI(36:1) E-04 1,2-DAG(36:5) E-03 PI(38:4) E-06 1,2-DAG(36:4) E-02 PI(38:3) E-04 1,2-DAG(36:3) E-03 PI(40:5) E-02 1,2-DAG(36:2) E-03 glutamate E-03 1,2-DAG(36:1) E-03 citrate E-07 1,2-DAG(36:0) E-03 F16BP E-03 1,2-DAG(37:2) E-02 PGA E-04 1,2-DAG(37:0) E-03 ATP E-05 1,2-DAG(38:6) E-03 ADP E-03 1,2-DAG(38:0) E-02 AMP E-03 1,2-DAG(40:0) E-03 C18 Cer E-03 C20 Cer E-03 C22 Cer E-04 C24 Cer E-04 C22 HexCer E-03 C24 HexCer E-03 C22 Sphingomyelin E-02 C24:1DH Cer E-03 C16DH Sphingomyelin E-07 Sphinganine E-03 Sphingosine E-03 Sphingosine-P E-03 C18 1-deoxyCer E-04 C22 1-deoxyCer E-03 C24 1-deoxyCer E-03 C16DH 1-deoxyCer E-02 C18DH 1-deoxyCer E-04 C20DH 1-deoxyCer E-03 C22DH 1-deoxyCer E-04
5 C24DH 1-deoxyCer E-02 C22 GlcCer E-03 C24 GlcCer E-02 C24 GalCer E-03 PA(36:1) E-03 PA(40:6) E-04 PA(40:4) E-03 PC(36:4) E-04 PC(38:5e) E-05 PC(38:4) E-03 LPC(18:0) E-03 PE(32:1) E-02 PE(36:4p) E-04 PE(36:3) E-03 PE(38:4p) E-04 PE(38:6) E-02 PE(40:6) E-04 LPE(18:2) E-03 LPE(18:1) E-02 LPE(20:4) E-03 LPE(22:6) E-03 LPE(22:5) E-03 LPE(22:4) E-03 BMP(40:8) E-04 BMP(40:7) E-03 PI(36:3) E-04 PI(38:5) E-03 PS(34:2) E-03 PS(34:1) E-03 PS(36:3) E-04 PS(36:2) E-05 PS(40:6) E-03 malate E-03 F16BP E-02
6 Supplementary Data File 2 TranscriptID EntrezID GeneSym S/N H/N H/S ENST PTGES ENST CYP2E ENST CYP2E ENST EPHX ENST GGT ENST CYP2C ENST CYP2C ENST GGT ENST PTGS ENST GGT ENST EPHX ENST CYP2C ENST PTGDS Color-scale ENST PLA2G4C ENST AKR1C ENST CYP2C ENST PLA2G2A ENST TBXAS ENST CYP2C ENST EPHX ENST PLA2G Fold changes of the medians, S/N, H/N and S/H, for the genes related to eicosanoids. Genes with H/S>1.25 or <0.80 are listed.
7 TranscriptID EntrezID GeneSym S/N H/N H/S ENST KDSR ENST SMPD ENST GBA ENST CERS ENST ARSA ENST UGCG Fold changes of the medians, S/N, H/N and S/H, for the genes related to sphingolipids.
8 TranscriptID EntrezID GeneSym S/N H/N H/S ENST ABCG ENST FDFT ENST CYP51A ENST HMGCS ENST MVK ENST TM7SF ENST DHCR ENST HMGCR ENST EBP ENST MSMO ENST HMGCR ENST SREBF ENST LSS ENST SQLE ENST LSS ENST FDPS ENST SQLE ENST MVD ENST FDPS ENST FDFT ENST NSDHL ENST HMGCS ENST FDPS Fold changes of the medians, S/N, H/N and S/H, for the genes related to sterols.
9 TranscriptID EntrezID GeneSym S/N H/N H/S ENST CHPT ENST CHPT ENST AGPAT ENST PLD ENST DGKZ ENST PCYT ENST PLA2G4C ENST DGKZ ENST PNPLA ENST PLA2G2A ENST CEPT ENST AGPAT ENST LCLAT ENST CRLS ENST AGPAT ENST AGPAT ENST PLA2G Fold changes of the medians, S/N, H/N and S/H, for the genes related to glycerophospholipids.
10 TranscriptID EntrezID GeneSym S/N H/N H/S ENST AGPAT ENST ALDH7A ENST GK ENST ALDH3A ENST ALDH ENST DGKZ ENST DGAT ENST ALDH7A ENST DGKZ ENST AKR1A ENST AKR1A ENST AGPAT ENST LCLAT ENST LIPC ENST AGPAT ENST AGPAT Fold changes of the medians, S/N, H/N and S/H, for the genes related to glycerolipids.
11 Supplementary Data File 3 crosscorrelation: MMP1 MMP2 MMP7 MMP8 MMP9 MMP11 MMP12 MMP14 MMP15 MMP16 MMP17 MMP19 MMP21 MMP23B TIMP1 TIMP2 TIMP3 FA(16:1) FA(18:0) FA(20:0) FA(20:2) hydroxycholesterol Desmethyllanosterol CE(16:0) CE(20:1) CE(22:2) CE(22:0) TAG(48:3) TAG(48:2) TAG(48:1) TAG(48:0) TAG(50:3) TAG(50:2) TAG(50:1) TAG(50:0) TAG(52:4) TAG(52:3) TAG(52:2) TAG(52:1) TAG(52:0) TAG(54:5) TAG(54:4) TAG(54:3) TAG(54:2) TAG(54:1) TAG(54:0) TAG(56:5) TAG(56:4) TAG(56:3) TAG(56:2) TAG(56:1) TAG(58:6) TAG(58:4) TAG(58:3) TAG(58:2) TAG(60:4) ,2-DAG(30:0) ,2-DAG(32:0) ,2-DAG(34:3) ,2-DAG(34:1) ,2-DAG(34:0) ,2-DAG(36:5) ,2-DAG(36:4) ,2-DAG(36:3) ,2-DAG(36:2) ,2-DAG(36:1) ,2-DAG(36:0) ,2-DAG(38:6) ,2-DAG(38:2) ,2-DAG(38:1) ,2-DAG(38:0) ,2-DAG(40:7) ,2-DAG(40:6) ,2-DAG(40:2) ,2-DAG(40:1) ,2-DAG(40:0) C14 Cer C16 Cer C18:1 Cer C26:1 Cer C14 HexCer C18:1 HexCer C26DH Cer C14DH HexCer C24DH Sphingomyelin Sphinganine Sphingosine C26:1 1-deoxyCer C26 1-deoxyCer
12 C26:1DH 1-deoxyCer C26DH 1-deoxyCer C14 GlcCer C18:1 GalCer C18 GalCer PA(34:0) PA(36:2) PA(36:1) PC(32:0) PC(36:4) PC(38:5) PC(38:4) LPC(16:0) PI(32:1) PI(34:1) PI(36:4) PI(36:3) PI(36:1) PI(38:5) PI(40:4) glutamate G6P
13 Supplementary Data File 4 SNP GeneSym P OR Alleles Mutation CHR SNP.1 BP A1 F_A F_U A2 CHISQ exm PNPLA [T/G] Missense_S453I 22 exm rs PNPLA [A/C] Silent 22 rs rs PNPLA [C/G] Missense_I148M 22 rs exm PNPLA [T/G] Missense_C99G 22 exm rs PNPLA [A/G] Silent 22 rs rs PNPLA [T/G] Silent 22 rs plink NS snp PNPLA3
14 SNP GeneSym P OR Alleles Mutation CHR SNP.1 BP A1 F_A F_U A2 CHISQ rs PNPLA [C/G] Missense_I148M 22 rs exm PNPLA [T/G] Missense_S453I 22 exm rs PNPLA [A/G] Silent 22 rs rs PNPLA [A/C] Silent 22 rs rs PNPLA [T/G] Silent 22 rs exm PNPLA [A/G] Missense_K434E 22 exm exm PNPLA [T/G] Missense_C99G 22 exm exm PNPLA [T/G] Missense_G115C 22 exm plink NH snp PNPLA3
15 SNP GeneSym P OR Alleles Mutation CHR SNP.1 BP A1 F_A F_U A2 CHISQ rs PNPLA [C/G] Missense_I148M 22 rs rs PNPLA [A/G] Silent 22 rs rs PNPLA [T/G] Silent 22 rs exm PNPLA [T/G] Missense_G115C 22 exm exm PNPLA [A/G] Missense_K434E 22 exm exm PNPLA [T/G] Missense_C99G 22 exm rs PNPLA [A/C] Silent 22 rs plink SH snp PNPLA3
16 SNP GeneSym P OR Alleles Mutation CHR SNP.1 BP A1 F_A F_U A2 CHISQ rs PNPLA3 1.77E [C/G] Missense_I148M 22 rs rs PNPLA3 1.45E [A/G] Silent 22 rs rs PNPLA3 4.19E [T/G] Silent 22 rs exm PNPLA [T/G] Missense_S453I 22 exm exm PNPLA [T/G] Missense_C99G 22 exm exm PNPLA [A/G] Missense_K434E 22 exm exm PNPLA [T/G] Missense_G115C 22 exm rs PNPLA [A/C] Silent 22 rs plink NC snp PNPLA3
17 SNP GeneSym P OR Alleles Mutation CHR SNP.1 BP A1 F_A F_U A2 CHISQ rs PNPLA [C/G] Missense_I148M 22 rs rs PNPLA [A/G] Silent 22 rs exm-rs228113pnpla [A/G] Silent 22 exm-rs rs PNPLA [T/G] Silent 22 rs exm PNPLA [T/G] Missense_C99G 22 exm exm PNPLA [T/G] Missense_G115C 22 exm rs PNPLA [A/C] Silent 22 rs exm PNPLA [A/G] Missense_K434E 22 exm plink SC snp PNPLA3
18 SNP GeneSym P OR Alleles Mutation CHR SNP.1 BP A1 F_A F_U A2 CHISQ rs PNPLA [C/G] Missense_I148M 22 rs rs PNPLA [A/G] Silent 22 rs exm-rs PNPLA [A/G] Silent 22 exm-rs rs PNPLA [T/G] Silent 22 rs exm PNPLA [T/G] Missense_S453I 22 exm exm PNPLA [T/G] Missense_C99G 22 exm exm PNPLA [A/C] Missense_P186H 22 exm rs PNPLA [A/C] Silent 22 rs exm PNPLA [T/G] Missense_G115C 22 exm exm PNPLA3 1 1 [A/G] Missense_K434E 22 exm plink HC snp PNPLA3
19 Supplementary Data File 5 Sample/Person H S Comments S E E+00 S E E+00 S E E-01 S E E+00 S E E+00 S E E+00 S E E+00 S E E+00 S E E+00 S E E+00 S E E+00 S E E+00 S E E+00 S E E+00 S E E-01 S E E+00 H E E-15 H E E-43 H E E-17 H E E+00 misclassified H E E-13 H E E-26 H E E-12 H E E-24 H E E-02 H E E-21 H E E-29 H E E-11 H E E-29 H E E-08 H E E-01 misclassified Posterior
20 Lipid name LDA 1 coefficiemean_of_s Mean_of_H PC(36:2e) -4.19E PC(36:0e) 4.19E Dolichol E LPI(18:0) 1.79E PE(38:5p) 1.13E LPI(20:4) -4.34E C26DH 1-deoxyCer 3.30E CE(22:5) 2.29E C16 Cer 2.48E C18 GalCer -2.80E hydroxycholesterol -2.39E PI(32:1) -5.31E C18DH Cer 2.84E C20 Cer -5.70E C18 Cer -3.54E CE(22:6) -3.03E ,25-epoxycholesterol -7.22E Sphingosine 1.23E PC(32:0) 7.79E FA(20:2) 1.27E Result of procedure LDA2 on plasma lipids to classify NASH vs. steatosis samples. First LDA was applied on 30 top ANOVA lipids, then on 20 selected lipids (see also Supplementary Figure S7).
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