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MicroRNA MIR21 and T Cells in Colorectal Cancer

Kosuke Mima, Reiko Nishihara, Jonathan A. Nowak, Sun A. Kim, Mingyang Song, Kentaro Inamura, Yasutaka Sukawa, Atsuhiro Masuda, Juhong Yang, Ruoxu Dou, Katsuhiko Nosho, Hideo Baba, Edward L. Giovannucci, Michaela Bowden, Massimo Loda, Marios Giannakis, Adam J. Bass, Glenn Dranoff, Gordon J. Freeman, Andrew T. Chan, Charles S. Fuchs, Zhi Rong Qian and Shuji Ogino
Kosuke Mima
1Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
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Reiko Nishihara
1Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
2Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
3Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
4Department of Biostatistics, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
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Jonathan A. Nowak
5Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.
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Sun A. Kim
1Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
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Mingyang Song
2Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
3Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
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Kentaro Inamura
1Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
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Yasutaka Sukawa
1Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
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Atsuhiro Masuda
1Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
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Juhong Yang
1Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
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Ruoxu Dou
1Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
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Katsuhiko Nosho
6Department of Gastroenterology, Rheumatology, and Clinical Immunology, Sapporo Medical University School of Medicine, Sapporo, Japan.
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Hideo Baba
7Department of Gastroenterological Surgery, Graduate School of Medical Science, Kumamoto University, Kumamoto, Japan.
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Edward L. Giovannucci
2Department of Nutrition, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
3Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
8Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.
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Michaela Bowden
1Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
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Massimo Loda
1Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
5Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.
9Broad Institute of Massachusetts Institute of Technology and Harvard, Cambridge, Massachusetts.
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Marios Giannakis
1Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
9Broad Institute of Massachusetts Institute of Technology and Harvard, Cambridge, Massachusetts.
10Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.
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Adam J. Bass
1Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
9Broad Institute of Massachusetts Institute of Technology and Harvard, Cambridge, Massachusetts.
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Glenn Dranoff
1Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
10Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.
11Cancer Vaccine Center, Dana-Farber Cancer Institute, Boston, Massachusetts.
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Gordon J. Freeman
1Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
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Andrew T. Chan
8Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.
12Division of Gastroenterology, Massachusetts General Hospital, Boston, Massachusetts.
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Charles S. Fuchs
1Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
8Channing Division of Network Medicine, Department of Medicine, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.
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Zhi Rong Qian
1Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
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  • For correspondence: shuji_ogino@dfci.harvard.edu zhirong_qian@dfci.harvard.edu
Shuji Ogino
1Department of Medical Oncology, Dana-Farber Cancer Institute and Harvard Medical School, Boston, Massachusetts.
3Department of Epidemiology, Harvard T.H. Chan School of Public Health, Boston, Massachusetts.
5Department of Pathology, Brigham and Women's Hospital and Harvard Medical School, Boston, Massachusetts.
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  • For correspondence: shuji_ogino@dfci.harvard.edu zhirong_qian@dfci.harvard.edu
DOI: 10.1158/2326-6066.CIR-15-0084 Published January 2016
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    Figure 1.

    MIR21 expression in colorectal cancer. A, quantitative RT-PCR assays for MIR21 and RNU6-2 using 10-fold dilution series (1:1,000, 1:100, 1:10, and 1:1) from the same specimen. Mean cycle threshold values (± SD) of triplicate runs and the coefficient of determination (r2) in the assays for MIR21 and RNU6-2 are shown. cDNA, complementary DNA. B, MIR21 expression in 54 pairs of colorectal cancer and adjacent nontumor colonic mucosa. A statistical analysis was performed using the two-sided Wilcoxon signed rank test.

Tables

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  • Table 1.

    Interassay coefficients of variation in quantitative RT-PCR assays for MIR21 and RNU6-2

    Targets in quantitative RT-PCR assays
    MIR21RNU6-2
    Mean cycle threshold ± SDInterassay coefficient of variation (%)Mean cycle threshold ± SDInterassay coefficient of variation (%)
    Specimen 119.5 ± 0.060.2819.9 ± 0.130.65
    Specimen 219.5 ± 0.070.3621.2 ± 0.150.73
    Specimen 319.3 ± 0.090.4421.0 ± 0.180.86
    Specimen 420.0 ± 0.090.4622.1 ± 0.090.39
    Specimen 518.0 ± 0.100.5521.0 ± 0.120.59
    Mean coefficient of variation (%)0.420.64

    NOTE: Interassay coefficient of variation of cycle threshold values from the same specimen were assessed by repeating assays in five different batches with the use of five colorectal cancers.

    • Table 2.

      Clinical, pathologic, and molecular features according to tumor MIR21 expression in 538 colorectal cancer cases

      Tumor MIR21 expression (quartile)
      CharacteristicaTotal (N = 538)Q1 (lowest; n = 135)Q2 (second; n = 134)Q3 (third; n = 134)Q4 (highest; n = 135)Pb
      Mean age ± SD, y67.6 ± 8.366.7 ± 8.267.2 ± 8.568.8 ± 8.167.5 ± 8.30.19
      Sex0.044
       Men185 (34%)50 (37%)44 (33%)56 (42%)35 (26%)
       Women353 (66%)85 (63%)90 (67%)78 (58%)100 (74%)
      Year of diagnosis0.006
       Prior to 1995201 (38%)63 (47%)55 (41%)42 (32%)41 (30%)
       1996–2000202 (38%)43 (32%)54 (40%)44 (34%)61 (45%)
       2001–2008131 (24%)28 (21%)25 (19%)45 (34%)33 (25%)
      Family history of colorectal cancer in a first-degree relative0.21
       Absent422 (79%)105 (78%)111 (83%)96 (74%)110 (82%)
       Present109 (21%)29 (22%)22 (17%)34 (26%)24 (18%)
      Tumor location0.30
       Cecum96 (18%)20 (15%)22 (17%)27 (20%)27 (20%)
       Ascending to transverse colon173 (32%)39 (29%)40 (30%)43 (32%)51 (38%)
       Splenic flexure to sigmoid149 (28%)39 (29%)44 (33%)31 (23%)35 (26%)
       Rectosigmoid and rectum117 (22%)36 (27%)27 (20%)33 (25%)21 (16%)
      Disease stage0.009
       I110 (21%)37 (28%)29 (22%)23 (18%)21 (16%)
       II173 (34%)44 (34%)45 (35%)44 (35%)40 (31%)
       III164 (32%)31 (24%)44 (34%)48 (39%)41 (32%)
       IV67 (13%)18 (14%)11 (8.5%)10 (8.0%)28 (21%)
      Tumor differentiation0.24
       Well to moderate486 (91%)121 (90%)127 (95%)119 (89%)119 (88%)
       Poor51 (9.5%)13 (9.7%)7 (5.2%)15 (11%)16 (12%)
      MSI status0.26
       MSI-low/MSS440 (84%)114 (87%)115 (86%)107 (82%)104 (79%)
       MSI-high86 (16%)17 (13%)18 (14%)24 (18%)27 (21%)
      MLH1 hypermethylation0.15
       Absent461 (87%)118 (89%)121 (91%)109 (83%)113 (85%)
       Present69 (13%)14 (11%)12 (9.0%)23 (17%)20 (15%)
      CIMP status0.015
       Low/negative440 (83%)113 (86%)119 (89%)108 (82%)100 (75%)
       High90 (17%)19 (14%)14 (11%)24 (18%)33 (25%)
      BRAF mutation0.003
       Wild-type444 (84%)120 (90%)116 (88%)110 (82%)98 (75%)
       Mutant86 (16%)13 (9.8%)16 (12%)24 (18%)33 (25%)
      KRAS mutation0.11
       Wild-type311 (59%)76 (58%)67 (51%)88 (66%)80 (61%)
       Mutant216 (41%)55 (42%)64 (49%)46 (34%)51 (39%)
      PIK3CA mutation0.86
       Wild-type408 (83%)99 (84%)104 (82%)105 (82%)100 (85%)
       Mutant82 (17%)19 (16%)23 (18%)23 (18%)17 (15%)
      Mean LINE-1 methylation level (%) ± SD61.6 ± 9.661.6 ± 8.459.6 ± 10.462.1 ± 10.263.0 ± 9.10.032

      Abbreviations: Q1 to Q4, quartile 1 to quartile 4.

      • ↵aPercentage indicates the proportion of cases with a specific clinical, pathologic, or molecular feature in colorectal cancer cases with each tumor MIR21 expression. There were cases that had missing values for any of the characteristics except for age and sex.

      • ↵bTo assess associations between the ordinal categories (first to fourth quartile) of tumor MIR21 expression and categorical data, the χ2 test was performed. To compare mean age and mean LINE-1 methylation levels, an ANOVA was performed. We adjusted the two-sided α level to 0.003 (= 0.05/14) by simple Bonferroni correction for multiple hypothesis testing.

    • Table 3.

      Distribution of colorectal cancer cases according to tumor MIR21 expression and the density of T cells

      Tumor MIR21 expression (quartile)
      TotalQ1 (lowest)Q2 (second)Q3 (third)Q4 (highest)Ptrenda
      CD3+ cell density (quartile)0.0004
       Q1 (0–115 cells/mm2)130 (25%)26 (20%)29 (22%)31 (25%)44 (33%)
       Q2 (116–252 cells/mm2)129 (25%)26 (20%)30 (23%)35 (28%)38 (29%)
       Q3 (253–533 cells/mm2)130 (25%)42 (32%)33 (25%)30 (24%)25 (19%)
       Q4 (≥534 cells/mm2)129 (25%)38 (28%)38 (30%)28 (23%)25 (19%)
      CD8+ cell density (quartile)0.27
       Q1 (0–66 cells/mm2)128 (25%)23 (18%)31 (24%)40 (32%)34 (26%)
       Q2 (67–185 cells/mm2)127 (25%)42 (33%)26 (20%)28 (23%)31 (24%)
       Q3 (186–410 cells/mm2)128 (25%)30 (24%)34 (26%)28 (23%)36 (27%)
       Q4 (≥411 cells/mm2)127 (25%)31 (25%)39 (30%)27 (22%)30 (23%)
      CD45RO+ cell density (quartile)0.0002
       Q1 (0–183 cells/mm2)131 (25%)24 (18%)30 (23%)31 (24%)46 (35%)
       Q2 (184–430 cells/mm2)130 (25%)32 (25%)33 (25%)39 (31%)26 (20%)
       Q3 (431–805 cells/mm2)131 (25%)26 (20%)37 (27%)30 (24%)38 (29%)
       Q4 (≥806 cells/mm2)130 (25%)48 (37%)33 (25%)27 (21%)22 (16%)
      FOXP3+ cell density (quartile)0.032
       Q1 (0–14 cells/mm2)124 (25%)25 (20%)31 (26%)32 (27%)36 (28%)
       Q2 (15–25 cells/mm2)124 (25%)29 (23%)24 (20%)34 (28%)37 (28%)
       Q3 (26–48 cells/mm2)124 (25%)38 (31%)27 (22%)27 (22%)32 (25%)
       Q4 (≥49 cells/mm2)123 (25%)32 (26%)38 (32%)28 (23%)25 (19%)

      Abbreviations: Q1 to Q4, quartile 1 to quartile 4.

      • ↵aPtrend value was calculated by the linear trend test across the ordinal (first to fourth quartile) categories of tumor MIR21 expression as a continuous variable in a univariable ordinal logistic regression model for the density of CD3+, CD8+, CD45RO+, or FOXP3+ T cells (an ordinal quartile outcome variable). Because we assessed four primary outcome variables, we adjusted the two-sided α level to 0.012 (= 0.05/4) by simple Bonferroni correction.

    • Table 4.

      The association of tumor MIR21 expression with the density of T cells

      Univariable OR (95% CI)Multivariable OR (95% CI)a
      Model for CD3+ cell density (n = 518, as an outcome variable)
      MIR21 expressionQ1 (lowest)1 (reference)1 (reference)
      Q2 (second)0.88 (0.57–1.36)0.85 (0.55–1.31)
      Q3 (third)0.67 (0.43–1.04)0.59 (0.37–0.92)
      Q4 (highest)0.47 (0.31–0.73)0.44 (0.28–0.68)
      Ptrendb0.0004<0.0001
      Model for CD8+ cell density (n = 510, as an outcome variable)
      MIR21 expressionQ1 (lowest)1 (reference)1 (reference)
      Q2 (second)1.14 (0.74–1.77)1.25 (0.80–1.96)
      Q3 (third)0.72 (0.46–1.12)0.76 (0.48–1.19)
      Q4 (highest)0.89 (0.58–1.38)0.99 (0.63–1.54)
      Ptrendb0.270.50
      Model for CD45RO+ cell density (n = 522, as an outcome variable)
      MIR21 expressionQ1 (lowest)1 (reference)1 (reference)
      Q2 (second)0.70 (0.46–1.09)0.72 (0.46–1.12)
      Q3 (third)0.57 (0.37–0.89)0.54 (0.34–0.84)
      Q4 (highest)0.45 (0.29–0.70)0.41 (0.26–0.64)
      Ptrendb0.0002<0.0001
      Model for FOXP3+ cell density (n = 495, as an outcome variable)
      MIR21 expressionQ1 (lowest)1 (reference)1 (reference)
      Q2 (second)0.98 (0.63–1.54)0.93 (0.59–1.46)
      Q3 (third)0.73 (0.47–1.14)0.61 (0.39–0.96)
      Q4 (highest)0.66 (0.42–1.02)0.55 (0.35–0.86)
      Ptrendb0.0320.003

      Abbreviations: Q1 to Q4, quartile 1 to quartile 4.

      • ↵aThe multivariable ordinal logistic regression analysis model initially included age; sex; year of diagnosis; family history of colorectal cancer in parent or sibling; tumor location; tumor differentiation; MSI; CpG island methylator phenotype; KRAS, BRAF, and PIK3CA mutations; and LINE-1 methylation level. A backward stepwise elimination with a threshold of P = 0.05 was used to select variables in the final models. Variables remaining in the final multivariable ordinal logistic regression models are shown in Supplementary Table S2.

      • ↵bPtrend value was calculated by the linear trend across the ordinal (first to fourth quartile) categories of MIR21 expression as a continuous variable in the ordinal logistic regression model for the density of CD3+, CD8+, CD45RO+, or FOXP3+ T cells (an ordinal quartile outcome variable). Because we assessed four primary outcome variables, we adjusted the two-sided α level to 0.012 (= 0.05/4) by simple Bonferroni correction.

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    Cancer Immunology Research: 4 (1)
    January 2016
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    MicroRNA MIR21 and T Cells in Colorectal Cancer
    Kosuke Mima, Reiko Nishihara, Jonathan A. Nowak, Sun A. Kim, Mingyang Song, Kentaro Inamura, Yasutaka Sukawa, Atsuhiro Masuda, Juhong Yang, Ruoxu Dou, Katsuhiko Nosho, Hideo Baba, Edward L. Giovannucci, Michaela Bowden, Massimo Loda, Marios Giannakis, Adam J. Bass, Glenn Dranoff, Gordon J. Freeman, Andrew T. Chan, Charles S. Fuchs, Zhi Rong Qian and Shuji Ogino
    Cancer Immunol Res January 1 2016 (4) (1) 33-40; DOI: 10.1158/2326-6066.CIR-15-0084

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    MicroRNA MIR21 and T Cells in Colorectal Cancer
    Kosuke Mima, Reiko Nishihara, Jonathan A. Nowak, Sun A. Kim, Mingyang Song, Kentaro Inamura, Yasutaka Sukawa, Atsuhiro Masuda, Juhong Yang, Ruoxu Dou, Katsuhiko Nosho, Hideo Baba, Edward L. Giovannucci, Michaela Bowden, Massimo Loda, Marios Giannakis, Adam J. Bass, Glenn Dranoff, Gordon J. Freeman, Andrew T. Chan, Charles S. Fuchs, Zhi Rong Qian and Shuji Ogino
    Cancer Immunol Res January 1 2016 (4) (1) 33-40; DOI: 10.1158/2326-6066.CIR-15-0084
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