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1 Supplementary Materials for Disease Risk Factors Identified Through Shared Genetic Architecture and Electronic Medical Records Li Li, David J. Ruau, Chirag J. Patel, Susan C. Weber, Rong Chen, Nicholas P. Tatonetti, Joel T. Dudley, Atul J. Butte* The PDF file includes: *Corresponding author. Published 30 April 2014, Sci. Transl. Med. 6, 234ra57 (2014) DOI: /scitranslmed Table S1A. Number of genes with variants associated with the 85 traits. Table S1B. Number of genes with variants associated with the 69 diseases. Table S2. One hundred twenty disease-trait pairs with shared common genes, q values derived from random sampling methods, and original GWAS studies from VARIMED. Fig. S1A. Gene density for traits and diseases. Fig. S1B. Published human genetic study density for the shared genes in new discovered and known disease-trait pairs. Fig. S2. Violin plots for one positive control and two negative controls. References (51 127)
2 Supplemental Tables Table S1A. Number of genes with variants associated with the 85 traits. Trait Count Height 120 Cholesterol 50 Protein c 49 HDL cholesterol 46 LDL cholesterol 44 Blood pressure 33 Triglyceride 33 Uric acid 26 Gamma-Glutamyl transferase 24 Acenocoumarol maintenance dosage 21 Antibody titer 21 Monocyte count 21 Hair color 19 Intercellular adhesion molecule 1 (icam-1) 18 Age at menarche 17 Bilirubin 17 C reactive protein 17 Serum magnesium 17 Glomerular filtration rate 16 Dehydroepiandrosterone sulphate 15 Freckles 14 Matrix metalloproteinases 14 Metabolic trait 14 Skin pigmentation 14 Heart rate 13 Mean corpuscular hemoglobin 13 Phenprocoumon maintenance dosage 13 Apolipoprotein b 12 Docosapentaenoic acid 12 Homocysteine 12 Lipoprotein-Associated phospholipase a2 activity 12 Mean corpuscular volume 12 Glycated hemoglobin 11 Longevity 11 Monocyte chemoattractant protein 1 11 QRS interval duration 11 Transferrin receptor 11 Bone mineral density 10 Eye color 10 2
3 Trait Count Fibrinogen 10 Hematological trait 10 Pulmonary function 10 Metabolite traits 10 Smoking 10 Alkaline phosphatase 9 Butyrylcholinesterase activity 9 Eicosapentaenoic acid 9 Hemoglobin 8 Lipoprotein 8 Lipoprotein-Associated phospholipase a(2) 8 Platelet count 8 QT interval 8 Serum calcium 8 Von willebrand factor activity 8 Acute-Phase serum amyloid a 7 Alpha linolenic acid 7 Liver enzyme 7 Fetal hemoglobin 6 Forced expiratory volume 6 Hematocrit 6 PR interval 6 Proinsulin 6 Apolipoprotein 5 Carbohydrate deficient transferrin concentration 5 Erythrocyte sedimentation rate 5 Factor viii coagulant activity 5 Lipoprotein-Associated phospholipase a2 mass 5 Menopause 5 Pro-brain natriuretic peptide 5 Prostate-Specific antigen 5 Adiponectin 4 ADP-Stimulated platelet aggregation after clopidogrel therapy 4 Alanine aminotransferase 4 Apolipoprotein a1 4 Creatinine 4 Dose requirement of warfarin 4 E-Selectin 4 Factor vii coagulant activity 4 Ferritin 4 Mean cell hemoglobin concentration 4 Neutrophil count 4 Serum transferrin 4 3
4 Trait Count Transferrin 4 Weight 4 White blood cell count 4 Table S1B. Number of genes with variants associated with the 69 diseases. Disease Count Rheumatoid arthritis 122 Membranous nephropathy 88 Myocardial infarction 73 Systemic lupus erythematosus 62 Type 1 diabetes 60 Multiple sclerosis 48 Crohn's disease 44 HIV infection 40 Obesity 33 Coronary artery disease 31 Esophageal cancer 29 Type 2 diabetes 29 Alzheimer's disease 28 Vitiligo 24 Asthma 23 Primary biliary cirrhosis 22 Parkinson's disease 21 Celiac disease 20 Psoriasis 20 Alopecia areata 19 Glucose intolerance 19 Prostate cancer 19 Ulcerative colitis 19 Schizophrenia 18 Lung cancer 16 Insulin resistance 15 Ankylosing spondylitis 14 Breast cancer 14 Gastric cancer 13 Venous thromboembolism 12 Hypertension 11 Systemic sclerosis 11 Age related macular degeneration 10 Alcohol dependence 10 Biliary liver cirrhosis 10 Inflammatory bowel disease 10 Melanoma 10 4
5 Disease Count Creutzfeldt-Jakob disease 8 Kawasaki disease 8 Beta thalassemia 7 Colorectal cancer 7 Graves' disease 7 Sudden cardiac arrest 7 Bipolar disorder 6 Chronic lymphocytic leukemia 6 Chronic obstructive pulmonary disease 6 Meningococcal disease 6 Paget's disease 6 Tauopathy progressive supranuclear palsy 6 Testicular cancer 6 Acquired immunodeficiency syndrome 5 Basal cell carcinoma 5 Drug-Induced liver injury 5 End stage renal disease 5 Leprosy 5 Metabolic syndrome 5 Neonatal lupus 5 Wegener's granulomatosis 5 Acute lymphoblastic leukemia 4 Amyotrophic lateral sclerosis 4 Chronic hepatitis b 4 Cleft palate 4 Dilated cardiomyopathy 4 Glioma 4 Kidney disease 4 Nasopharyngeal carcinoma 4 Open-Angle glaucoma 4 Restless legs syndrome 4 Vitamin d deficiency 4 5
6 Table S2: One hundred twenty disease-trait pairs with shared common genes, q values derived from random sampling methods, and original GWAS studies from VARIMED. Reference refers to the known clinical association. Category is based on timing of the disease progression. Trait Disease Common Genes Gene Symbol Shared Q- value Reference Category(#) Mean corpuscular Acute lymphoblastic volume leukemia 1 IKZF New New 1 Alanine aminotransferase Alcohol dependence 1 C12orf (30) 3 1 Cholesterol Alcohol dependence 3 ALDH2; BRAP; C12orf (29) 3 1 HDL cholesterol Alcohol dependence 2 C12orf51; OAS3 <0.001 (28) 3 1 Mean cell hemoglobin concentration Alcohol dependence 1 ALDH New New 1 Platelet count Alcohol dependence 1 C12orf New New 1 Antibody titer Alopecia areata 4 BTNL2; C6orf10; RDBP; TNXB <0.001 (51) 2 1 Pulmonary function Alopecia areata 1 AGER 0.01 New New 1 Apolipoprotein b Alzheimer's disease 4 APOC1; APOE; PVRL2; TOMM40 <0.001 (52) 3 1 C reactive protein APOC1; APOE; Alzheimer's disease 3 TOMM (53) 1 1 Cholesterol Alzheimer's disease 4 APOC1; APOE; PVRL2; TOMM (54) 3 1 Erythrocyte sedimentation rate GWAS Study (ⱡ) Alzheimer's disease 1 CR (8) 1 1 LDL cholesterol Alzheimer's disease 4 Lipoprotein-Associated phospholipase a2 activity Alzheimer's disease 3 APOC1; APOE; PVRL2; TOMM40 APOC1;PVRL2; TOMM (55) 3 1 <0.001 (56) 1 1 Antibody titer Ankylosing spondylitis 2 BTNL2; LOC (57) 2 1 6
7 Trait Disease Common Genes Gene Symbol Shared Q- value Reference Category(#) GWAS Study (ⱡ) Antibody titer Asthma 4 BTNL2; C6orf10; HLA- DPA1; NOTCH4; <0.001 (58) 2 1 Eye color Basal cell carcinoma 1 SLC45A (59) 1 1 Freckles Basal cell carcinoma 1 MC1R (60) 1 1 Hair color Basal cell carcinoma 2 MC1R; SLC45A (59) 1 MC1R Prostate-Specific antigen Basal cell carcinoma 1 CLPTM1L New New 1 Skin pigmentation Basal cell carcinoma 2 MC1R; SLC45A (61) 1 1 Fetal hemoglobin BCL11A; HBD; HBG1; Beta thalassemia 5 <0.001 (62) 2 HBG2; HECW1 HBG1 Antibody titer Biliary liver cirrhosis 3 BTNL2; C6orf10; HLA- DPB (63) 2 1 Lipoprotein(a) Bipolar disorder 1 SYNE (64) 3 1 Triglyceride Bipolar disorder 1 NCAN (65) 3 1 Antibody titer Chronic hepatitis b 2 HLA-DPA1; HLA-DPB1 <0.001 (66) 2 1 Eye color Chronic lymphocytic leukemia 1 IRF New New 1 Freckles Chronic lymphocytic leukemia 1 IRF New New 1 Smoking Chronic obstructive pulmonary disease Apolipoprotein b Coronary artery disease 4 Blood pressure Coronary artery disease 6 3 AGPHD1; CHRNA3; RAB4B CELSR2; LDLR; PSRC1; ZNF259 ALDH2, ATXN2, C12orf51, CNNM2, NAA25, SH2B3 <0.001 (23) 1 CHRNA3, RAB4B <0.001 (67) 1 1 <0.001 (68) 1 ATXN2, CNNM2, SH2B3 7
8 Trait Disease Common Genes Cholesterol Coronary artery disease 10 HDL cholesterol Coronary artery disease 4 Intercellular adhesion molecule 1 (icam-1) Coronary artery disease 5 LDL cholesterol Coronary artery disease 5 Gene Symbol Shared ABCA1; ALDH2; BRAP; C12orf51; CELSR2; LDLR; LPA; NAA25; PSRC1; ZNF259 ABCA1; C12orf51; CELSR2; ZNF259 ATXN2; C12orf51; PTPN11; SH2B3; SMARCA4 CELSR2; LDLR; LPA; PSRC1; ZNF259 Q- value Reference Category(#) <0.001 (32) 1 GWAS Study (ⱡ) ABCA1, LPA (32) 1 1 <0.001 (69) (32) 1 Lipoprotein-Associated phospholipase a(2) Coronary artery disease 2 CELSR2; PSRC (70) 1 1 Lipoprotein-Associated CELSR2; LDLR; PSRC1; phospholipase a2 Coronary artery disease 4 ZNF259 activity <0.001 (70) 1 1 Platelet count Coronary artery disease 3 C12orf51; PTPN11; SH2B3 <0.001 (71) 1 Blood pressure Esophageal cancer 3 ALDH2, C12orf51, PLCE New New 1 Cholesterol Esophageal cancer 3 ALDH2; BRAP; C12orf (72) 1 1 Factor vii coagulant activity Esophageal cancer 1 ADH New New 1 Serum magnesium Gastric cancer 3 MUC1; THBS3; TRIM46 <0.001 New New 1 Prostate-Specific antigen Glioma 1 TERT New New 1 Alpha linolenic acid Glucose intolerance 1 FADS New New 1 Ferritin Glucose intolerance 1 HFE (73) 1 1 LPA SH2B3 8
9 Trait Gamma-Glutamyl transferase Disease Common Genes Gene Symbol Shared Q- value Reference Category(#) GWAS Study (ⱡ) Glucose intolerance 2 GCKR; SLC2A (74) 1 1 Glycated hemoglobin Glucose intolerance 5 ABCB11; G6PC2; GCK; HFE; MTNR1B <0.001 (75) 2 LDL cholesterol Glucose intolerance 3 ABCB11; GCK; HFE ADA 3 1 Proinsulin Glucose intolerance 3 MADD, SLC30A8, TCF7L2 <0.001 (76) 3 Serum transferrin ABCB11 and MTNR1B Glucose intolerance 1 HFE 0.01 (77) 1 1 Antibody titer HIV infection 7 Alanine aminotransferase Blood pressure Hypertension 9 C6orf10; HLA-C; LOC ; NOTCH4; PRRC2A; RDBP; TNXB TCF7L2 <0.001 (78) 2 1 Hypertension 1 C12orf New New 1 ARHGAP42, ATP2B1, BAG6, C12orf51, CACNB2, CSK, HFE, MTHFR, NT5C2 <0.001 (79) 2 2 Creatinine Hypertension 1 UMOD (80) 3 1 Ferritin Hypertension 1 HFE (81) 1 1 Hematocrit Hypertension 1 HFE (82) 3 1 Hemoglobin Hypertension 1 HFE (83) 1 1 Homocysteine Hypertension 1 MTHFR 0.01 (84) 1 1 Platelet count Hypertension 1 C12orf (85) 3 1 Pro-brain natriuretic peptide Hypertension 1 MTHFR (86) 1 1 9
10 Trait Serum transferrin Weight Disease Common Genes Gene Symbol Shared Q- value Reference Category(#) GWAS Study (ⱡ) Hypertension 1 HFE New New 1 Inflammatory bowel disease 1 ATXN2L (87) 3 1 C reactive protein Insulin resistance 2 GCKR; LPL 0.01 (88) 1 2 Factor vii coagulant activity Insulin resistance 1 GCKR (89) 3 1 Glycated hemoglobin Insulin resistance 2 G6PC2; MTNR1B <0.001 (90) 2 2 HDL cholesterol Insulin resistance 3 CELSR2; FADS1; LPL (91) 3 FADS1 Lipoprotein-Associated phospholipase a(2) Insulin resistance 1 CELSR (92) 1 1 Proinsulin Insulin resistance 2 ARAP1; MADD <0.001 (93) 3 2 Triglyceride Insulin resistance 4 CELSR2; FADS1; GCKR; (94) 1 CELSR2 and LPL FADS1 Smoking Kawasaki disease 1 RAB4B New New 1 Creatinine Chronic Kidney disease 1 UMOD (95) 2 2 Prostate-Specific antigen Lung cancer 2 CLPTM1L; TERT New New 1 Smoking Lung cancer 4 AGPHD1; CHRNA3; CHRNA5; IREB2 <0.001 (96) 1 Eye color Melanoma 2 SLC45A2; TYR <0.001 (97) 1 Freckles Melanoma 4 CDK5RAP1; DEF8; MC1R; NCOA6 <0.001 (98) 1 AGPHD1, IREB2 TYR CDK5RAP1, DEF8, NCOA6 10
11 Trait Disease Common Genes Hair color Melanoma 6 Gene Symbol Shared C16orf55; CDK10; CDK5RAP1; DEF8; MC1R; SLC45A2 11 Q- value Reference Category(#) <0.001 (98) 1 GWAS Study (ⱡ) C16orf55, CDK10, CDK5RAP1, DEF8, MC1R Homocysteine Melanoma 1 C16orf New New 1 Protein c Melanoma 2 NCOA6; PIGU <0.001 New New 1 Skin pigmentation Melanoma 3 MC1R; SLC45A2; TYR <0.001 (99) 1 1 Antibody titer Membranous nephropathy 15 Apolipoprotein a1 AGPAT1; BAG6; BTNL2; C6orf10; EHMT2; GPANK1; LY6G5B; LY6G6C; NOTCH4; PRRC2A; RDBP; RNF5; SLC44A4; TNXB; ZBTB12 <0.001 (100) 2 1 Metabolic syndrome 1 ZNF (101) 3 1 Apolipoprotein b Metabolic syndrome 3 APOA5; BUD13; ZNF259 <0.001 (101) 3 1 C reactive protein Metabolic syndrome 1 LPL (102) 3 1 Cholesterol Metabolic syndrome 2 APOA5; ZNF (103) 2 1 HDL cholesterol Metabolic syndrome 3 APOA5; LPL; ZNF (103) 2 1 LDL cholesterol Metabolic syndrome 2 LPL; ZNF (103) 2 1 Lipoprotein-Associated phospholipase a2 activity Transferrin receptor Metabolic syndrome 2 BUD13; ZNF259 <0.001 (104) 3 1 Metabolic syndrome 3 Triglyceride Metabolic syndrome 4 APOA5; BUD13; ZNF259 APOA5; BUD13; LPL; ZNF259 <0.001 New New 1 <0.001 (105) 2 1
12 Trait Disease Common Genes Antibody titer Multiple sclerosis 7 Antibody titer Neonatal lupus 3 Alanine aminotransferase Gene Symbol Shared AGPAT1; BAG6; BTNL2; C6orf10; EHMT2; NOTCH4; TNXB BAG6; C6orf10; ZBTB12 12 Q- value Reference Category(#) GWAS Study (ⱡ) <0.001 (106) 2 1 <0.001 (107) 2 1 Obesity 2 C12orf51; PNPLA3 <0.001 (108) 3 1 Blood pressure Obesity 3 ALDH2, C12orf51, SLC39A (109) 3 Proinsulin Obesity 1 PCSK (110) 1 2 Weight Obesity 3 ATXN2L; FTO; SH2B1 <0.001 WHO 2000 p PR interval Open-Angle glaucoma 1 CAV New New 1 Antibody titer Primary biliary cirrhosis 3 BTNL2; C6orf10; HLA- DPB (111) 2 1 Prostate-Specific antigen Prostate cancer 3 HNF1B; MSMB; TERT <0.001 (112) 2 1 PR interval Restless legs syndrome 1 MEIS New New 1 Antibody titer Rheumatoid arthritis 20 AGPAT1; BAG6; BTNL2; C6orf10; EHMT2; GPANK1; HLA- C; HLA-DPA1; HLA- DPB1; LOC ; LY6G5B; LY6G6C; LY6G6F; NOTCH4; PRRC2A; RDBP; RNF5; SLC44A4; TNXB; ZBTB12 <0.001 (113) 2 1 Pulmonary function Rheumatoid arthritis 2 AGER; PPT (114) 3 1 Bone mineral density Sudden cardiac arrest 1 ESR New New 1 SLC39A8
13 Trait Acenocoumarol maintenance dosage Antibody titer Disease Systemic lupus erythematosus Systemic lupus erythematosus Common Genes Antibody titer Systemic sclerosis 3 Gene Symbol Shared 13 Q- value Reference Category(#) GWAS Study (ⱡ) 2 ITGAM; ITGAX New New 1 9 BAG6; BTNL2; C6orf10; GPANK1; HLA-DPB1; NOTCH4; PRRC2A; TNXB; ZBTB12 HLA-DPA1; HLA-DPB1; NOTCH4 <0.001 (115) 2 1 <0.001 (116) 2 1 Platelet count Testicular cancer 1 BAK New New 1 Prostate-Specific antigen Testicular cancer 2 CLPTM1L; TERT <0.001 New New 1 Antibody titer Type 1 diabetes 5 BAG6; BTNL2; C6orf10; HLA-C; HLA-DPB (117) 2 1 Blood pressure Type 1 diabetes 4 ATXN2, BAG6, NAA25, SH2B (118) 3 1 Cholesterol Type 1 diabetes 4 HLA-DRA; LCT; MCM6; NAA25 <0.001 (119) 3 1 Intercellular adhesion molecule 1 (icam-1) Type 1 diabetes 4 ATXN2; PTPN11; SH2B3; TYK2 <0.001 (120) 1 1 Adiponectin Type 2 diabetes 1 ADIPOQ (121) 1 1 C reactive protein Type 2 diabetes 3 GCKR; HNF4A; LPL (88) 1 1 Proinsulin Type 2 diabetes 3 ARAP1; SLC30A8; <0.001 (122) 3 TCF7L2 ARAP1 E-Selectin Venous thromboembolism 2 ABO; C9orf7 <0.001 (123) 3 1 Factor viii coagulant activity Venous thromboembolism 1 ABO (124) 1 1 Fibrinogen Venous thromboembolism 2 FGA; FGG <0.001 (125) 1 1 Alkaline phosphatase Venous thromboembolism 1 ABO New New 1
14 Trait Disease Common Genes Gene Symbol Shared Q- value Reference Category(#) Antibody titer Vitiligo 6 AGPAT1; BTNL2; NOTCH4; RNF5; <0.001 (126) 2 1 SLC44A4; TNXB Antibody titer Wegener's granulomatosis 2 HLA-DPA1; HLA-DPB1 <0.001 (127) 2 1 GWAS Study (ⱡ) #: 1: risk factors where traits occur prior to disease onset and may accompany disease, 2) diagnostic tests where traits occur at disease onset, and 3) consequences or complications where traits occur after the disease diagnosis ⱡ: 1: Different GWAS in VARIMED; 2: Same GWAS in VARIME 14
15 Supplemental Figures 15
16 Figure S1A: Gene density for traits and diseases. Kernel density plot shows that the distributions of the gene counts for diseases (red line) and traits (black line). Distribution comparison was done by Kolmogorov-Smirnov testing (p = 0.16). 16
17 17
18 Figure S1B: Published human genetic stud y density for the shared genes in new discovered and known disease-trait pairs. Kernel density plot shows that the distributions of the PubMed counts for genes shared in known disease-trait pairs (red line) and new discovered disease-trait pairs (black line). Distribution comparison was done by Kolmogorov-Smirnov testing (p = 0.51). 18
19 Figure S2: Violin plots for one positive control and two negative controls. 19
20 Violin plots (combination of boxplots and kernel density plots) for clinical validations of three controls from Stanford STRIDE. One positive control is PSA associated with PCA at three centers (A). Two negative controls are PSA and ALL (B) and PSA and GCA (C) at SHC. In the black box plots, bold black lines boundaries indicate the 25th, 75th percentiles of PSA, and white center squares indicate the median value of lab values. The horizontal line indicates reference ranges of PSA (< 4 ng/ml). The grey shapes indicate density of the number of samples. P-values are reported by Wilcoxon Sum Rank testing. 20
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