Genome-wide association study of esophageal squamous cell carcinoma in Chinese subjects identifies susceptibility loci at PLCE1 and C20orf54

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1 CORRECTION NOTICE Nat. Genet. 42, (2010); published online 22 August 2010; corrected online 27 August 2014 Genome-wide association study of esophageal squamous cell carcinoma in Chinese subjects identifies susceptibility loci at PLCE1 and C20orf54 Li-Dong Wang, Fu-You Zhou, Xue-Min Li, Liang-Dan Sun, Xin Song, Yan Jin, Jiang-Man Li, Guo-Qiang Kong, Hong Qi, Juan Cui, Lian- Qun Zhang, Jie-Zhi Yang, Ji-Lin Li, Xing-Chuan Li, Jing-Li Ren, Zhi-Cai Liu, Wen-Jun Gao, Ling Yuan, Wu Wei, Yan-Rui Zhang, Wei-Peng Wang, Ilyar Sheyhidin, Feng Li, Bao-Ping Chen, Shu-Wei Ren, Bin Liu, Dan Li, Jian-Wei Ku, Zong-Min Fan, Sheng-Li Zhou, Zhi-Gang Guo, Xue-Ke Zhao, Na Liu, Yong-Hong Ai, Fang-Fang Shen, Wen-Yan Cui, Shuang Song, Tao Guo, Jing Huang, Chao Yuan, Jia Huang, Yue Wu, Wen-Bin Yue, Chang-Wei Feng, Hong-Lei Li, Yan Wang, Jin-Ya Tian, Yue Lu, Yi Yuan, Wen-Liang Zhu, Min Liu, Wen-Jing Fu, Xia Yang, Han-Jing Wang, Suo-Li Han, Jie Chen, Min Han, Hai-Yan Wang, Peng Zhang, Xiu-Min Li, Jin-Cheng Dong, Guo-Lan Xing, Ran Wang, Ming Guo, Zhi-Wei Chang, Hai-Lin Liu, Li Guo, Zhi-Qing Yuan, Hai Liu, Qin Lu, Liu-Qin Yang, Fu-Guo Zhu, Xiu-Feng Yang, Xiao-Shan Feng, Zhou Wang, Yin Li, She-Gan Gao, Qirenwang Qige, Long-Tang Bai, Wen-Jun Yang, Guang-Yan Lei, Zhong-Ying Shen, Long-Qi Chen, En-Min Li, Li-Yan Xu, Zhi-Yong Wu, Wei-Ke Cao, Jian-Po Wang, Zhi-Qin Bao, Ji-Li Chen, Guang-Cheng Ding, Xiang Zhuang, Ying-Fa Zhou, Hou-Feng Zheng, Zheng Zhang, Xian-Bo Zuo, Zi-Ming Dong, Dong-Mei Fan, Xin He, Jin Wang, Qi Zhou, Qin- Xian Zhang, Xin-Ying Jiao, Shi-Yong Lian, Ai-Fang Ji, Xiao-Mei Lu, Jin-Sheng Wang, Fu-Bao Chang, Chang-Dong Lu, Zhi-Guo Chen, Jian-Jun Miao, Zeng-Lin Fan, Ruo-Bai Lin, Tai-Jiang Liu, Jin-Chang Wei, Qing-Peng Kong, Yu Lan, Yu-Jing Fan, Fu-Sheng Gao, Tian-Yun Wang, Dong Xie, Shu-Qing Chen, Wan-Cai Yang, Jun-Yan Hong, Liang Wang, Song-Liang Qiu, Zhi-Ming Cai & Xue-Jun Zhang In the version of this supplementary file originally posted online, the authors provided evidence to support the association with esophageal squamous cell carcinoma susceptibility of rs [t] at 20p13. They now find no evidence for this association in their original data, in two independent sets of cases and controls collected in other Chinese populations or in the joint analysis of these three studies (see the accompanying corrigendum for full details). Corrected versions of Supplementary Figures 1 4 and Supplementary Table 1 will be made available in a revised version of this file to be provided by the authors. NATURE GENETICS

2 Genome wide association study of esophageal squamous cell carcinoma in Chinese identifies susceptibility loci at PLCE1 and C20orf54 Supplementary Materials Index Supplementary Figure 1. The principal components analysis (PCA) of 2,810 samples and 206 reference samples from the HapMap. Supplementary Figure 2. The principal components analysis (PCA) of 1,629 samples and 206 reference samples from the HapMap. Supplementary Figure 3. Summary results of esophageal squamous cell carcinoma genome-wide association study. Supplementary Figure 4. Stratified analyses of rs and rs by gender, age, smoking, alcohol consumption and BMI. Supplementary Figure 5. Immunohistochemical staining of PLCE1 protein in ESCC and GCA. Supplementary Figure 6. Stratified analyses of rs671 by gender, age, smoking, alcohol consumption and BMI. Supplementary Table 1. Summary of association results for 18 SNPs. Supplementary Table 2. A comparison of the genotype distribution of rs671 between Chinese and Japanese. Supplementary Note: The criteria of subject enrollment for the cases and controls. 1

3 Supplementary Figures Supplementary Figure 1. The principal components analysis (PCA) of 2,810 samples and 206 reference samples from the HapMap. PCA of our 2,810 GWAS samples (1,077 cases, 1,733 controls) alone or in combination with 206 reference HapMap samples was performed. (a-d): PCA of 2,810 samples (from our GWAS and HapMap); (e-h): PCA of 2,810 samples from our GWAS. 2

4 3

5 Supplementary Figure 2. The principal components analysis (PCA) of 1,629 samples and 206 reference samples from the HapMap. PCA of our 1,629 GWAS samples (937 cases, 692 controls) alone or in combination with 206 reference HapMap samples was performed. (a-d): PCA of 1,629 samples (from our GWAS and HapMap); (e-h): PCA of 1,629 samples from our GWAS. 4

6 5

7 Supplementary Figure 3. Summary results of esophageal squamous cell carcinoma genome-wide association study. (a): Summary of genome-wide association results for 1,077 cases and 1,733 controls. The genome-wide P values (-log 10 P) of the association analysis for 506,666 SNPs are plotted against positions on each chromosome. Each chromosome is depicted in different colors. (b): Summary of genome-wide association results for 937 cases and 692 controls. The genome-wide P values (-log 10 P) of the association analysis for 506,666 SNPs are plotted against positions on each chromosome. Each chromosome is depicted in different colors. (c): Quantile-quantile plots of the observed P values versus the expected P value of association. The plot in purple is based on 1,629 samples. 6

8 (a) 7

9 (b) 8

10 (c) 9

11 Supplementary Figure 4. Stratified analyses of rs and rs by gender, age, smoking, alcohol consumption and BMI. (a): Stratified analyses of rs The heterogeneity analysis of each subgroup indicated that these confounding environmental factors did not significantly alter the effect of these 2 SNPs on the risk to ESCC (P het >0.05). (b): Stratified analyses of rs The heterogeneity analysis of each subgroup indicated that these confounding environmental factors did not significantly alter the effect of these 2 SNPs on the risk to ESCC (P het >0.05). 10

12 (a) n/n represents the allele counts in cases and controls. 11

13 (b) n/n represents the allele counts in cases and controls. 12

14 Supplementary Figure 5. Immunohistochemical staining of phospholipase C espsilon-1 (PLCE1) protein in ESCC (A, negative, 20X; B, weak positive, 10X; C, strong positive 10X), and GCA (F, negative, 20X; G, weak positive, 10X; H, strong positive, 10X); D (10X) and I (10X) were the negative control of B and H (omission of the first antibody application); E and J were the positive staining for PLCE1 in normal esophageal squamous epithelium (10X) and normal gastric cardia columnar epithelium (10X), respectively. 13

15 Supplementary Figure 6. Stratified analyses of rs671 by gender, age, smoking, alcohol consumption and BMI. The heterogeneity analysis of each subgroup indicated that rs671 increased the risk to ESCC prominently in the smoker (P het =0.01) and alcohol drinker populations (P het =0.008). n/n represents the allele counts in cases and controls. 14

16 Supplementary Tables Supplementary Table 1. Summary of association results for 18 SNPs. (a) Summary of association results for 18 SNPs in the ESCC GWAS, ESCC Replication 1 and ESCC Replication 2. (b) Summary of association results for 18 SNPs in the ESCC GWAS and GCA cases. Supplementary Table 1a ESCC GWAS ESCC Replication 1 ESCC Replication 2 MAF b MAF MAF CHR Gene SNP BP Allele a F_A c F_U d P value OR(95%CI) F_A F_U P value OR(95%CI) P e F_A F_U P value OR(95%CI) 1p36.13 AHDC1 rs G E ( ) E ( ) 2.42E E ( ) 5p15.3 IRX1 rs C E ( ) E ( ) 2.42E E ( ) 5p15.3 IRX1 rs C E ( ) E ( ) 5.46E E ( ) 8q21.13 FABP5 rs A E ( ) E ( ) 1.45E E ( ) 10q23 PLCE1 rs A E ( ) E ( ) 3.92E E ( ) 10q23 PLCE1 rs G E ( ) E ( ) 7.46E E ( ) 12q24.33 FZD10 rs C E ( ) E ( ) 1.16E E ( ) 18q22.3 TSHZ1 rs A E ( ) E ( ) 2.19E E ( ) 18q22.3 TSHZ1 rs C E ( ) E ( ) 8.06E E ( ) 19q13.1 PPP1R14A rs C E ( ) E ( ) 4.60E E ( ) 19q13.4 CACNG6 rs A E ( ) E ( ) 2.16E E ( ) 20p13 C20orf54 rs A E ( ) E ( ) 3.46E E ( ) 20p13 C20orf54 rs T E ( ) E ( ) 1.21E E ( ) 20q13.2 DOK5 rs C E ( ) E ( ) 3.32E E ( ) 20q13.2 DOK5 rs T E ( ) E ( ) 7.64E E ( ) 21q21.3 ADAMTS5 rs C E ( ) E ( ) 4.41E E ( ) 22q11.2 IGLV9-49 rs G E ( ) E ( ) 2.72E E ( ) 22q12.1 PES1 rs T E ( ) E ( ) 9.21E E ( ) a Minor allele; b Minor allele frequency; c Frequency of minor allele in cases; d Frequency of minor allele in controls; e Han-combined. 15

17 Supplementary Table 1b ESCC GWAS GCA MAF b MAF CHR Gene SNP BP Allele a F_A c F_U d P value OR(95%CI) F_A F_U P value OR(95%CI) 1p36.13 AHDC1 rs G E ( ) E ( ) 5p15.3 IRX1 rs C E ( ) E ( ) 5p15.3 IRX1 rs C E ( ) E ( ) 8q21.13 FABP5 rs A E ( ) E ( ) 10q23 PLCE1 rs A E ( ) E ( ) 10q23 PLCE1 rs G E ( ) E ( ) 12q24.33 FZD10 rs C E ( ) E ( ) 18q22.3 TSHZ1 rs A E ( ) E ( ) 18q22.3 TSHZ1 rs C E ( ) E ( ) 19q13.1 PPP1R14A rs C E ( ) E ( ) 19q13.4 CACNG6 rs A E ( ) E ( ) 20p13 C20orf54 rs A E ( ) E ( ) 20p13 C20orf54 rs T E ( ) E ( ) 20q13.2 DOK5 rs C E ( ) E ( ) 20q13.2 DOK5 rs T E ( ) E ( ) 21q21.3 ADAMTS5 rs C E ( ) E ( ) 22q11.2 IGLV9-49 rs G E ( ) E ( ) 22q12.1 PES1 rs T E ( ) E ( ) a Minor allele; b Minor allele frequency; c Frequency of minor allele in cases; d Frequency of minor allele in controls. 16

18 Supplementary Table 2. A comparison of the genotype distributions of rs671 between Chinese and Japanese. (a) A comparison of the genotype distributions of rs671 in the Chinese and Japanese populations. (b) A comparison of the genotype distributions of rs671 in alcohol drinker and never drinker, also in smokers and never smokers. Supplementary Table 2a ESCC Cases Controls Genotypes Genotypes n GG GA AA MAF d n P value GG GA AA MAF (Frequency) (Frequency) (Armitage) Chinese GWAS (0.75) Replication (0.74) Total (0.74) (0.23) 963 (0.24) 1180 (0.24) (0.01) HapMap CHB b Japanese a Screening (0.30) Replication (0.28) Total (0.29) 480 (0.68) 255 (0.70) 735 (0.69) HapMap JPT c (0.70) (0.74) (0.74) (0.75) (0.57) (0.55) (0.56) (0.58) (0.28) 982 (0.24) 1173 (0.25) 20 (0.24) 529 (0.37) 509 (0.38) 1038 (0.38) 31 (0.36) (0.01) 80 (0.06) 99 (0.07) 179 (0.06) 5 (0.06) a Data derived from published study by Cui, et al. [Cui, R. et al. Gastroenterology 137, (2009), reference 13 in the main text]; b Han Chinese in Beijing, China; c Japanese in Tokyo, Japan; d Minor allele frequency. 17

19 Supplementary Table 2b ESCC Cases Controls Genotypes Genotypes n GG GA AA MAF a n P value GG GA AA MAF (frequency) (frequency) (Armitage) Drinker (0.75) Never drinker (0.74) Smokers (0.71) (0.23) 753 (0.24) 327 (0.26) (0.01) (0.03) (0.80) (0.72) (0.74) (0.19) 815 (0.26) 321 (0.24) (0.01) (0.01) Never smokers (0.75) (0.23) (0.74) (0.24) a Minor allele frequency. 18

20 Supplementary Note The criteria of subject enrollment for the cases and controls: All the cases and controls in the GWAS scan and replications were recruited using the uniform criteria, and the same questionnaire for the clinical and geographic information collection. The enrollment criteria for cases and controls in this study were: 1) no restrictions on age, gender, ethnicity, risk factor exposures or cancer-stages for cases or controls; 2) local residents in the same geographic areas; 3) no prior history of treatment for ESCC and GCA other than surgery for cases; 4) willingness to participate in the study; 5) histopathologically confirmed ESCC and GCA; 6) the recording of tumor sites and categories based on the International Statistical Classification of Diseases and Related Health Problems (10th Revision, WHO, 2006, online); 7) all the controls used in this study were individuals without any family history of ESCC and GCA (including first-, second-, and third-degree relatives); 8) each participant was undergone esophageal endoscopic examination to exclude the early ESCC and GCA; 9) individuals who did not meet these criteria were excluded from the study. Following the enrollments, informed consent was obtained from each participant. Then, the cases and controls had blood samples drawn and were interviewed to obtain demographic and lifestyle histories related to cancer risks (i.e., age, tobacco, alcohol, and family history of upper gastrointestinal tract cancers). Family histories regarding upper gastrointestinal tract cancers in the first-, second-, and third-degree relatives were obtained through questionnaires. Of the confirmed eligible subjects, more than 95% of the cases and controls had been interviewed in this study. The study was approved by each institutional and hospital ethical committee and conducted according to Declaration of Helsinki principles. 19

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