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Research Article

Examination of Whole Blood DNA Methylation as a Potential Risk Marker for Gastric Cancer

Tomomitsu Tahara, Shinji Maegawa, Woonbok Chung, Judith Garriga, Jaroslav Jelinek, Marcos R.H. Estécio, Tomoyuki Shibata, Ichiro Hirata, Tomiyasu Arisawa and Jean-Pierre J. Issa
Tomomitsu Tahara
1Fels Institute for Cancer Research & Molecular Biology, Temple University School of Medicine, Philadelphia, Pennsylvania; 2Department of Molecular Carcinogenesis, The University of Texas MD Anderson Cancer Center, Smithville; 3Center for Cancer Epigenetics, The University of Texas MD Anderson Cancer Center, Houston, Texas; 4Department of Gastroenterology, Fujita Health University School of Medicine, Toyoake; and 5Department of Gastroenterology, Kanazawa Medical University, Ishikawa, Japan
1Fels Institute for Cancer Research & Molecular Biology, Temple University School of Medicine, Philadelphia, Pennsylvania; 2Department of Molecular Carcinogenesis, The University of Texas MD Anderson Cancer Center, Smithville; 3Center for Cancer Epigenetics, The University of Texas MD Anderson Cancer Center, Houston, Texas; 4Department of Gastroenterology, Fujita Health University School of Medicine, Toyoake; and 5Department of Gastroenterology, Kanazawa Medical University, Ishikawa, Japan
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Shinji Maegawa
1Fels Institute for Cancer Research & Molecular Biology, Temple University School of Medicine, Philadelphia, Pennsylvania; 2Department of Molecular Carcinogenesis, The University of Texas MD Anderson Cancer Center, Smithville; 3Center for Cancer Epigenetics, The University of Texas MD Anderson Cancer Center, Houston, Texas; 4Department of Gastroenterology, Fujita Health University School of Medicine, Toyoake; and 5Department of Gastroenterology, Kanazawa Medical University, Ishikawa, Japan
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Woonbok Chung
1Fels Institute for Cancer Research & Molecular Biology, Temple University School of Medicine, Philadelphia, Pennsylvania; 2Department of Molecular Carcinogenesis, The University of Texas MD Anderson Cancer Center, Smithville; 3Center for Cancer Epigenetics, The University of Texas MD Anderson Cancer Center, Houston, Texas; 4Department of Gastroenterology, Fujita Health University School of Medicine, Toyoake; and 5Department of Gastroenterology, Kanazawa Medical University, Ishikawa, Japan
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Judith Garriga
1Fels Institute for Cancer Research & Molecular Biology, Temple University School of Medicine, Philadelphia, Pennsylvania; 2Department of Molecular Carcinogenesis, The University of Texas MD Anderson Cancer Center, Smithville; 3Center for Cancer Epigenetics, The University of Texas MD Anderson Cancer Center, Houston, Texas; 4Department of Gastroenterology, Fujita Health University School of Medicine, Toyoake; and 5Department of Gastroenterology, Kanazawa Medical University, Ishikawa, Japan
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Jaroslav Jelinek
1Fels Institute for Cancer Research & Molecular Biology, Temple University School of Medicine, Philadelphia, Pennsylvania; 2Department of Molecular Carcinogenesis, The University of Texas MD Anderson Cancer Center, Smithville; 3Center for Cancer Epigenetics, The University of Texas MD Anderson Cancer Center, Houston, Texas; 4Department of Gastroenterology, Fujita Health University School of Medicine, Toyoake; and 5Department of Gastroenterology, Kanazawa Medical University, Ishikawa, Japan
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Marcos R.H. Estécio
1Fels Institute for Cancer Research & Molecular Biology, Temple University School of Medicine, Philadelphia, Pennsylvania; 2Department of Molecular Carcinogenesis, The University of Texas MD Anderson Cancer Center, Smithville; 3Center for Cancer Epigenetics, The University of Texas MD Anderson Cancer Center, Houston, Texas; 4Department of Gastroenterology, Fujita Health University School of Medicine, Toyoake; and 5Department of Gastroenterology, Kanazawa Medical University, Ishikawa, Japan
1Fels Institute for Cancer Research & Molecular Biology, Temple University School of Medicine, Philadelphia, Pennsylvania; 2Department of Molecular Carcinogenesis, The University of Texas MD Anderson Cancer Center, Smithville; 3Center for Cancer Epigenetics, The University of Texas MD Anderson Cancer Center, Houston, Texas; 4Department of Gastroenterology, Fujita Health University School of Medicine, Toyoake; and 5Department of Gastroenterology, Kanazawa Medical University, Ishikawa, Japan
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Tomoyuki Shibata
1Fels Institute for Cancer Research & Molecular Biology, Temple University School of Medicine, Philadelphia, Pennsylvania; 2Department of Molecular Carcinogenesis, The University of Texas MD Anderson Cancer Center, Smithville; 3Center for Cancer Epigenetics, The University of Texas MD Anderson Cancer Center, Houston, Texas; 4Department of Gastroenterology, Fujita Health University School of Medicine, Toyoake; and 5Department of Gastroenterology, Kanazawa Medical University, Ishikawa, Japan
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Ichiro Hirata
1Fels Institute for Cancer Research & Molecular Biology, Temple University School of Medicine, Philadelphia, Pennsylvania; 2Department of Molecular Carcinogenesis, The University of Texas MD Anderson Cancer Center, Smithville; 3Center for Cancer Epigenetics, The University of Texas MD Anderson Cancer Center, Houston, Texas; 4Department of Gastroenterology, Fujita Health University School of Medicine, Toyoake; and 5Department of Gastroenterology, Kanazawa Medical University, Ishikawa, Japan
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Tomiyasu Arisawa
1Fels Institute for Cancer Research & Molecular Biology, Temple University School of Medicine, Philadelphia, Pennsylvania; 2Department of Molecular Carcinogenesis, The University of Texas MD Anderson Cancer Center, Smithville; 3Center for Cancer Epigenetics, The University of Texas MD Anderson Cancer Center, Houston, Texas; 4Department of Gastroenterology, Fujita Health University School of Medicine, Toyoake; and 5Department of Gastroenterology, Kanazawa Medical University, Ishikawa, Japan
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Jean-Pierre J. Issa
1Fels Institute for Cancer Research & Molecular Biology, Temple University School of Medicine, Philadelphia, Pennsylvania; 2Department of Molecular Carcinogenesis, The University of Texas MD Anderson Cancer Center, Smithville; 3Center for Cancer Epigenetics, The University of Texas MD Anderson Cancer Center, Houston, Texas; 4Department of Gastroenterology, Fujita Health University School of Medicine, Toyoake; and 5Department of Gastroenterology, Kanazawa Medical University, Ishikawa, Japan
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DOI: 10.1158/1940-6207.CAPR-13-0034 Published October 2013
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  • Figure 1.
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    Figure 1.

    Methylation status of 14 promoter CpG islands and LINE1 in healthy young individuals (Young), cancer-free subjects (Control), and gastric cancer training set (gastric cancer) groups examined by bisulfite pyrosequencing. Horizontal bars represent mean methylation values. Methylation levels in whole blood DNA between gastric cancer and CONTROL were compared using the Student t test and the logistic regression model was used to adjust for age when the P values were less than 0.05.

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    Figure 2.

    Methylation status of 3 promoter CpG islands in healthy young individuals (Young), cancer-free subjects (Control), and gastric cancer training set (gastric cancer) groups examined by qMSP. Horizontal bars represent mean methylation values. The relative level of methylated DNA is depicted as 40-dCt [Ct of specific gene—Ct of mC-LESS (internal control)]. A higher 40-dCt represents more methylation of the target biomarker. Methylation levels in whole blood DNA between gastric cancer and CONTROL were compared using the Student t test.

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    Figure 3.

    Age-related methylation. A, methylation status of 8 promoter CpG islands and LINE1 in relation to aging. The healthy young individuals, control, and gastric cancer training set groups were all included in this analysis. Statistical analyses were conducted using the Spearman correlation analysis. B, mean Z score of the methylation levels of 9 age-related loci in relation and aging. The healthy young individuals (young subjects), control, and gastric cancer training set groups (control patients and patients with gastric cancer) were all included in this analysis. Statistical analyses were conducted using the Spearman correlation analysis. Left is a scatter plot of all the data by age, whereas right is a bar graph of all the patients divided by study group.

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    Figure 4.

    Relative telomere length examined by quantitative real-time PCR. A, telomere length in healthy young individuals (Young), cancer-free subjects (Control), and gastric cancer training set (gastric cancer) groups. Horizontal bars represent mean telomere length. B, telomere length, in relation to age. C, telomere length in relation to the mean Z score of the methylation levels of 9 age-related loci. Statistical analyses were conducted using the Student t test (A) and Spearman correlation analysis (B, C).

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    Figure 5.

    Methylation status of SFRP1 in cancer-free subjects (CONTROL) and the gastric cancer validation set. Horizontal bars represent mean methylation values. Methylation levels in whole blood DNA between gastric cancer and CONTROL were compared using the Student t test and the logistic regression model was used to adjust for age.

Tables

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  • Table 1.

    Study populations

    VariablesHealthy young individualsControl without gastric cancerGastric cancer training setGastric cancer validation set
    N52677291
    Age (mean ± SEM)a23.2 ± 0.357.4 ± 1.562.3 ± 1.171.3 ± 0.93
    Maleb26 (50%)41 (61.2%)46 (63.9%)67 (73.6%)
    • ↵aControl without gastric cancer versus gastric cancer training set, P = 0.01, Control without gastric cancer versus gastric cancer validation set, P < 0.0001.

    • ↵bHealthy young individuals versus gastric cancer validation set, P = 0.006.

  • Table 2.

    SFRP1 methylation status and clinicopathologic subtypes of gastric cancer

    Variables (n)SFRP1 methylation (mean ± SEM%)
    Gender
     Male (110)11.4 ± 0.26
     Female (48)11.6 ± 0.31
    H. pylori status
     Negative (38)11.2 ± 0.46
     Positive (120)11.5 ± 0.23
    Histology
     Intestinal (110)11.5 ± 0.26
     Diffuse (48)11.3 ± 0.31
    Location
     Antrum (49)11.9 ± 0.43
     Body (81)11.2 ± 0.25
     Cardia (28)11.4 ± 0.48
    Staging
     Early (82)11.8 ± 0.33
     Advanced (76)11.2 ± 0.23
    Morphology
     Elevated or protruding (40)11.8 ± 0.44
     Depressed or with ulceration (105)11.3 ± 0.25
     Scirrhous (13)11.1 ± 0.55

    NOTE: Methylation status was not determined for 5 cases.

    Additional Files

    • Figures
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    • Supplementary Data

      Files in this Data Supplement:

      • Supplementary Figures 1 and 2 - PDF - 96K, Supplementary Fig. 1: Methylation status of 16 CpG island promoters and LINE1 in 8 primary gastric cancer tissues and 6 healthy gastric mucosae. Methylation was measured by bisulfite-pyrosequencing. Horizontal bars represent mean methylation values. Supplementary Fig. 2: Association between relative telomere length and methylation status for 4 promoter CpG islands. Statistical analyses were performed using the Spearman correlation analysis.
      • Supplementary Figure Legends; Supplementary Tables 1-3 - PDF - 86K, Supplementary Table 1. Primer sequences used in pyrosequencing. Supplementary Table 2. Primer and probe sequences used in qMSP. Supplementary Table 3. Primer sequences used in telomere length measurement.
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    Cancer Prevention Research: 6 (10)
    October 2013
    Volume 6, Issue 10
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    Examination of Whole Blood DNA Methylation as a Potential Risk Marker for Gastric Cancer
    Tomomitsu Tahara, Shinji Maegawa, Woonbok Chung, Judith Garriga, Jaroslav Jelinek, Marcos R.H. Estécio, Tomoyuki Shibata, Ichiro Hirata, Tomiyasu Arisawa and Jean-Pierre J. Issa
    Cancer Prev Res October 1 2013 (6) (10) 1093-1100; DOI: 10.1158/1940-6207.CAPR-13-0034

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    Examination of Whole Blood DNA Methylation as a Potential Risk Marker for Gastric Cancer
    Tomomitsu Tahara, Shinji Maegawa, Woonbok Chung, Judith Garriga, Jaroslav Jelinek, Marcos R.H. Estécio, Tomoyuki Shibata, Ichiro Hirata, Tomiyasu Arisawa and Jean-Pierre J. Issa
    Cancer Prev Res October 1 2013 (6) (10) 1093-1100; DOI: 10.1158/1940-6207.CAPR-13-0034
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