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Cancer Epidemiology, Biomarkers & Prevention
Cancer Epidemiology, Biomarkers & Prevention

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Research Articles

Genetic Variation in the TGF-β Signaling Pathway and Colon and Rectal Cancer Risk

Martha L. Slattery, Jennifer S. Herrick, Abbie Lundgreen and Roger K. Wolff
Martha L. Slattery
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Jennifer S. Herrick
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Abbie Lundgreen
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Roger K. Wolff
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DOI: 10.1158/1055-9965.EPI-10-0843 Published January 2011
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  • Figure 1.
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    Figure 1.

    Associations between SNPs in the TGF-β signaling pathway and colon and rectal cancer.

Tables

  • Figures
  • Table 1.

    Summary of SNPs

    ColonRectal
    GeneAliasLocationSNPMajor/Minor alleleMAFaHeterozygote OR (95% CI)Homozygote rare OR (95% CI)Heterozygote OR (95% CI)Homozygote rare OR (95% CI)
    Smad2MAD218q21.1rs1787199A/T0.461.08 (0.92–1.26)1.24 (1.03–1.51)0.85 (0.69–1.05)b
    MADH2rs1792689C/T0.130.96 (0.82–1.12)1.30 (0.79–2.13)0.78 (0.62–0.98)b
    JV18rs4940086T/C0.331.08 (0.94–1.25)1.33 (1.06–1.66)1.00 (0.81–1.23)1.05 (0.77–1.42)
    Smad3MAD315q22.33rs750766G/A0.480.98 (0.84–1.15)0.93 (0.77–1.13)1.09 (0.89–1.34)b
    MADH3rs893473C/T0.170.97 (0.84–1.13)0.99 (0.69–1.40)1.09 (0.73–1.62)c
    JV15-2rs991157G/A0.30.93 (0.73–1.18)c1.11 (0.79–1.55)c
    rs1498506A/C0.480.87 (0.75–1.02)0.69 (0.57–0.84)1.10 (0.88–1.38)0.96 (0.72–1.26)
    rs1866317C/G0.110.98 (0.83–1.16)0.92 (0.48–1.76)1.12 (0.88–1.42)1.65 (0.77–3.54)
    rs2118610G/A0.451.11 (0.95–1.29)0.94 (0.78–1.14)1.02 (0.82–1.27)1.02 (0.77–1.36)
    rs2118611A/G0.21.03 (0.90–1.19)b0.89 (0.73–1.09)b
    rs2414937G/C0.20.68 (0.47–0.97)c1.01 (0.82–1.24)1.02 (0.63–1.67)
    rs3743343T/C0.241.10 (0.95–1.26)1.15 (0.87–1.52)0.97 (0.79–1.19)1.10 (0.77–1.58)
    rs3825977C/T0.190.95 (0.82–1.11)1.01 (0.72–1.42)0.96 (0.78–1.18)0.76 (0.47–1.24)
    rs4147358C/A0.221.08 (0.93–1.24)0.99 (0.73–1.33)1.03 (0.84–1.27)0.89 (0.60–1.33)
    rs4776892A/T0.181.02 (0.89–1.18)b0.94 (0.76–1.16)1.14 (0.69–1.88)
    rs7163381G/A0.260.76 (0.59–0.98)c1.11 (0.79–1.56)c
    rs7176870A/G0.431.08 (0.93–1.24)b1.16 (0.94–1.42)b
    rs11071933C/G0.331.04 (0.90–1.20)0.94 (0.75–1.16)0.84 (0.69–1.03)b
    rs12901071A/G0.340.68 (0.55–0.85)c0.80 (0.57–1.10)c
    rs17293443T/C0.220.84 (0.60–1.18)c1.81 (1.12–2.91)c
    Smad4DPC418q21.1rs10502913G/A0.241.03 (0.89–1.19)0.81 (0.61–1.08)1.02 (0.83–1.25)1.09 (0.72–1.67)
    MADH4
    TGFβ1TGFB19q13.1rs1800469G/A0.310.89 (0.78–1.03)0.65 (0.51–0.84)1.02 (0.84–1.23)b
    rs4803455C/A0.481.25 (1.06–1.47)1.43 (1.18–1.73)1.06 (0.84–1.32)1.04 (0.79–1.35)
    TGFβR1ALK-59q22rs1571590A/G0.20.95 (0.82–1.10)1.39 (0.98–1.96)0.91 (0.74–1.12)1.42 (0.85–2.39)
    SKR4rs6478974T/A0.490.85 (0.74–0.99)b0.85 (0.69–1.05)b
    LDS1Ars10733710G/A0.21.07 (0.93–1.23)b1.17 (0.96–1.43)b
    AAT5
    • ↵aMAF based on White control population.

    • ↵bDominant model.

    • ↵cRecessive model.

  • Table 2.

    Interaction between variants in the TGF-β signaling pathway and NFκB1 and IKBκB and risk of colon cancera

    Controls, nCases, nOR95% CIControls, nCases, nOR95% CIControls, nCases, nOR95% CI
     TGFβ1 rs1800469
    GGGAAA
    Smad3 rs3825977
     CC6105211.005424190.920.77 1.09116800.800.58 1.08
     CT2772300.990.80 1.232592010.900.72 1.1268350.570.37 0.88
     TT30431.671.03 2.7035190.640.36 1.141320.170.04 0.75
     Pinteraction<0.01
     TGFβ1 rs4803455
    CCCAAA
    Smad2 rs4940086
     TT2321521.004653601.210.94–1.552071701.270.95–1.70
     TC2281621.100.83–1.474253351.240.96–1.591961801.461.09–1.95
     CC58260.710.43–1.181051131.711.22–2.3929502.721.64–4.49
     Pinteraction0.02
    Smad3 rs17293443
     TT/TC4853301.009477791.231.04–1.454203801.351.11–1.64
     CC33100.460.22–0.9448290.930.57–1.5111202.921.38–6.19
     Pinteraction<0.01
    Smad7 rs4939827
     TT1151061.002552250.990.72–1.371231100.990.69–1.44
     TC/CC4032330.630.46–0.867385820.870.65–1.163092901.040.76–1.42
     Pinteraction0.02
     TGFβR1 rs6478974
    CCCAAA
    IKBκB rs3747811
     TT1481551.002552080.780.58–1.05124840.660.46–0.95
     TA2702190.780.58–1.044723520.720.55–0.952501710.670.49–0.90
     AA1151040.870.61–1.242391710.690.51–0.9483901.040.71–1.52
     Pinteraction0.04
    NFκB1 rs4648110
     TT3462891.006154740.930.76–1.142822331.010.80–1.28
     TA1631751.290.99–1.683112340.910.72–1.151561050.820.61–1.10
     AA24140.710.36–1.4040230.690.40–1.181970.470.20–1.15
     Pinteraction0.04
     TGFβR1 rs1571590
    AAAGGG
    IKBκB rs3747811b
    TT3472681.001661561.240.94–1.6214232.241.13–4.44
    TA6405001.030.85–1.263172090.860.68–1.0935331.250.75–2.06
    AA2732391.140.90–1.441471111.010.75–1.3617161.240.61–2.51
    Pinteraction0.04
    • ↵aAssociations adjusted for age, sex, center and race.

    • ↵bSimilar associations were observed for NFκB1 rs13117745 (C > T), Pinteraction = 0.02.

  • Table 3.

    Associations between variants in the TGF-β signaling pathway and NFκB1 and Smad2 and Smad3 and rectal cancer riska

    Controls, nCases, nOR95% CIControls, nCases, nOR95% CIControls, nCases, nOR95% CI
     TGFβ1 rs1800469
    GGGAAA
    Smad3 rs2118610b
     GG1581191.001401040.990.70–1.4023351.951.09–3.48
     GA2241661.030.75–1.401781561.180.86–1.6352350.910.56–1.49
     AA83721.220.82–1.8176611.110.73–1.681940.290.10–0.88
     Pinteraction0.01
    Smad3 rs4147358c
     CC2542041.0022018110.76–1.3163310.580.36–0.93
     CA1841370.890.89–1.191381150.990.72–1.3526341.590.92–2.74
     AA27160.670.35–1.2836250.830.48–1.43591.960.64–6.03
     Pinteraction<0.01
     TGFβ1 rs4803455
    CCCAAA
    NFκB1 rs13117745d
     CC2011301.003392741.250.95–1.651551321.350.98–1.86
     CT/TT52662.001.30–3.061421051.180.84–1.6569441.000.64–1.55
     Pinteraction<0.01
     TGFβR1 rs10733710
    GGGA/AA
    NFκB1 rs4648110e
     TT4052701.002072011.451.13–1.86
     TA/AA2101841.331.04–1.72136981.080.80–1.47
     Pinteraction<0.01
     TGFβR1 rs1571590
    AAAGGG
    Smad2 rs1792689
     CC4553791.002411830.910.72–1.1615282.421.27–4.61
     CT/TT1561120.840.63–1.1178480.750.51–1.111440.320.10–0.99
     Pinteraction0.003
    • ↵aAssociation adjusted for age, sex, race and center.

    • ↵bSimilar associations were observed for SMAD3 rs991157 (G > A), Pinteraction < 0.01.

    • ↵cSimilar associations were observed for SMAD3 rs745103 (T > A), Pinteraction < 0.01.

    • ↵dSimilar associations were observed for NFκB1 rs4648110 (T > A), Pinteraction = 0.02.

    • ↵dSimilar associations were observed for NFκB1 rs13117745 (C > T), Pinteraction = 0.01.

  • Table 4.

    Interaction between genetic variants in the TGF-β signaling pathway and lifestyle factors and risk of colon and rectal cancer

    Controls, nCases, nORa95% CIControls, nCases, nORa95% CI
    Colon cancerNever smoker/Former smokerRecent smoker
    TGFβ1 rs4803455
     CC4222741.0096661.040.74–1.48
     CA8156501.251.04–1.501801551.311.01–1.71
     AA3633061.331.07–1.6568942.091.47–2.96
     Pinteraction0.05
    TGFβR1 rs10733710
     GG1,0047751.002231780.990.79–1.24
     GA/AA5864520.990.85–1.161201381.461.12–1.90
     Pinteraction0.03
    TGFβR1 rs1571590
     AA1,0537971.002062071.291.04–1.60
     AG5053760.990.84–1.171251011.04(0.78–1.37)
     GG51621.631.10–2.3715100.880.39–1.98
     Pinteraction0.05
    Rectal cancer
    TGFβ1 rs1800469
     GG3852951.0080610.970.67–1.40
     GA/AA4193050.930.75–1.1569871.581.11–2.24
     Pinteraction0.03
    Colon cancerNo recent aspirin/NSAID useRecent aspirin NSAID use
    TGFβR1 rs6478974
     TT3293131.002021600.830.64–1.07
     TA5545020.950.78–1.164012230.590.47–0.74
     AA2532381.010.79–1.282011010.540.40–0.71
     Pinteraction0.03
    Smad3 rs3743343
     TT6635671.004622910.730.61–0.88
     TC4024011.150.96–1.382951770.700.56–0.87
     CC70851.431.02–2.0047180.450.26–0.78
     Pinteraction0.02
    Smad3 rs7173811
     CC3232631.002281470.790.61–1.03
     CT5495201.150.94–1.413782350.770.61–0.96
     TT2642701.240.98–1.571981040.630.47–0.85
     Pinteraction0.03
    Rectal cancer
    Smad3 rs3743343
     TT2722681.002451370.570.44–0.75
     TC2051730.840.65–1.101561050.69(0.51–0.93)
     CC44360.810.50–1.3027291.030.59–1.80
     Pinteraction0.01
    Smad3 rs7163381c
     GG2682291.002061510.870.66–1.14
     GA2191981.040.80–1.35176960.630.46–0.86
     AA34501.651.02–2.6746240.580.34–0.99
     Pinteraction0.01
    Colon cancerNo recent estrogen exposureRecent estrogen exposure
    TGFβ1 rs1800469
     GG2532091.006535790.780.59–1.03
     GA2132001.160.89–1.516124330.620.47–0.82
     AA53390.850.54–1.34141770.470.32–0.68
     Pinteraction0.03
    Rectal cancer
    TGFβ1 rs4803455
     CC40401.002131550.530.32–0.90
     CA84760.890.52–1.533973030.570.34–0.94
     AA45250.540.28–1.051791510.640.38–1.08
     Pinteraction0.04
    Smad4 rs10502913cMenWomen
     GG3182451.002481971.040.81–1.33
     GA1961741.170.90–1.53144940.860.63–1.17
     AA26321.570.91–2.7225120.640.31–1.30
     Pinteraction0.02
    • ↵aAdjusted for age, center, race, and sex.

    • bSimilar association observed for Smad3 rs11071933; Pinteraction = 0.03.

    • ↵cSimilar associations observed for Smad4 rs8096092; Pinteraction = 0.02.

  • Table 5.

    Associations between tumor molecular phenotype and TGFβ and Smad genes

    Controls, nCases, nORa95% CI
    Colon tumorsCIMP+
     Smad2 rs1787199AA601641.00
     Note: Similar results for rs4940086AT/TT1,3552081.461.09–1.97
     Smad3 rs2118611bAA1,2261521.00
    AG/GG7291201.871.26–2.79
     Smad3 rs4776892AA1,2881751.00
    AT/TT667970.630.42–0.95
    KRAS2 mutation
     TGFβ1 rs4803455CC526741.00
    CA/AA1,4572801.401.06–1.85
     TGFβ1 rs1800469GG9321871.00
    GA/AA1,0461660.780.62–0.98
    TP53 mutation
     Smad2 rs4940086TT/TC1,7624491.00
    CC194671.381.02–1.86
     Smad3 rs7176870AA6441461.00
    AG/GG1,3113711.281.03–1.59
     TGFβ1 rs4803455CC5261111.00
    CA1,0142671.270.99–1.63
    AA4431441.561.18–2.07
     TGFβ1 rs1800469GG9322751.00
    GA/AA1,0462430.780.64–0.95
    MSI unstable
     Smad2 rs1792689CC1,4771321.00
     Note: Similar results for rs1787199CT448451.120.79–1.60
    TT3182.851.28–6.36
     Smad3 rs12901071bAA/AG1,7161741.00
     Note: Similar results for rs731874GG240110.430.23–0.83
     TGFβ1 rs1800469GG9321101.00
    GA/AA1,046800.640.47–0.86
    Rectal tumorsCIMP+
     Smad3 rs893473CC/CT899491.00
    TT60103.601.62–7.98
     TGFβR1 rs10733710GG615271.00
    GA/AA343322.101.24–3.57
    KRAS2 mutation
     Smad3 (rs991157)GG/GA8761501.00
    AA83231.691.03–2.79
    TP53 mutation
     Smad3 rs11071933bCC3851271.00
    CG/GG5721500.720.54–0.95
     Smad3 rs750766GG304701.00
     Note: Similar results for rs12102171 and rs7176870GA/AA6532071.491.09–2.04
     TGFβR1 rs10733710GG6151551.00
    GA/AA3431051.401.06–1.84
    • ↵aAdjusted for age, center, sex, and race.

    • ↵btagSNPs presented for this gene are adjusted for one another.

  • Summary of All Genes and SNPs Assessed

    GeneChromosome locationSNPRegionMAFMajor/Minor alleleFDR HWE probabilityColon homozygote are ORRectal homozygote rare OR
    Smad14q31rs714195Intronic0.42G/A0.730.99 (0.80–1.21)1.02 (0.74–1.39)
    rs65373555 upstream0.12A/G0.881.35 (0.72–2.54)0.93 (0.37–2.32)
    rs2118438Intronic0.19G/A0.611.11 (0.75–1.65)1.29 (0.72–2.34)
    rs1016792Intronic0.19T/C1.001.00 (0.69–1.46)0.90 (0.51–1.58)
    rs125050853 downstream0.23A/G0.890.88 (0.65–1.20)0.91 (0.57–1.47)
    Smad218q21.1rs1787199Intronic0.46A/T1.001.24 (1.03–1.51)0.83 (0.63–1.08)
    rs1792658Intronic0.21A/C0.961.18 (0.88–1.58)1.12 (0.72–1.74)
    rs1792689Intronic0.13C/T0.951.30 (0.79–2.13)0.95 (0.41–2.22)
    rs4940086Intronic0.33T/C1.001.33 (1.06–1.66)1.05 (0.77–1.42)
    Smad315q22.33rs731874Intronic0.28G/A1.001.06 (0.82–1.37)0.94 (0.65–1.37)
    rs745103Intronic0.45T/C0.860.96 (0.79–1.16)0.98 (0.75–1.29)
    rs750766Unknown0.48G/A1.000.93 (0.77–1.13)1.06 (0.81–1.39)
    rs893473Intronic0.17C/T1.000.99 (0.69–1.40)1.06 (0.71–1.59)
    rs991157Intronic0.30G/A1.000.96 (0.75–1.23)1.07 (0.75–1.51)
    rs1470003Intronic0.48G/C0.960.95 (0.79–1.15)1.19 (0.90–1.57)
    rs1498506Intronic0.48A/C1.000.69 (0.57–0.84)0.96 (0.72–1.26)
    rs1866317Unknown0.11C/G1.000.92 (0.48–1.76)1.65 (0.77–3.54)
    rs1992215Unknown0.33T/C1.001.00 (0.80–1.25)0.86 (0.62–1.21)
    rs2118610Intronic0.45G/A0.610.94 (0.78–1.14)1.02 (0.77–1.36)
    rs2118611Intronic0.20A/G0.990.94 (0.66–1.34)0.93 (0.62–1.42)
    rs2414937Intronic0.20G/C1.000.67 (0.47–0.97)1.02 (0.63–1.67)
    rs37433433 UTR0.24T/C1.001.15 (0.87–1.52)1.10 (0.77–1.58)
    rs3784681Intronic0.29G/C0.960.91 (0.71–1.17)0.79 (0.56–1.11)
    rs3825977Intronic0.19C/T1.001.01 (0.72–1.42)0.76 (0.47–1.24)
    rs4147358Intronic0.22C/A0.960.99 (0.73–1.33)0.89 (0.60–1.33)
    rs4601989Intronic0.24C/T0.680.81 (0.60–1.08)0.66 (0.44–1.00)
    rs4776881Intronic0.44T/C1.001.07 (0.89–1.30)1.21 (0.92–1.60)
    rs4776890Intronic0.40T/G0.960.97 (0.80–1.19)0.96 (0.72–1.28)
    rs4776892Intronic0.18A/T0.451.00 (0.67–1.48)1.14 (0.69–1.88)
    rs7163381Intronic0.26G/A1.000.79 (0.61–1.03)1.06 (0.74–1.51)
    rs7173811Intronic0.47C/T0.961.06 (0.88–1.28)0.96 (0.73–1.26)
    rs7176870Intronic0.43A/G1.001.06 (0.88–1.29)1.19 (0.90–1.58)
    rs7181556Intronic0.24C/T0.990.91 (0.69–1.22)0.75 (0.50–1.12)
    rs7183244Intronic0.39C/T0.841.00 (0.81–1.23)1.04 (0.77–1.41)
    rs9972423Intronic0.37T/A1.000.97 (0.79–1.20)1.27 (0.94–1.73)
    rs11071933Intronic0.33C/G1.000.94 (0.75–1.16)0.92 (0.68–1.25)
    rs11637581Intronic0.28C/T0.950.98 (0.76–1.28)1.11 (0.77–1.59)
    rs11639295Intronic0.31C/T1.000.88 (0.70–1.12)0.83 (0.59–1.16)
    rs12102171Intronic0.17C/T0.860.90 (0.62–1.30)0.84 (0.49–1.43)
    rs12708492Intronic0.48C/T1.001.02 (0.85–1.24)1.10 (0.84–1.44)
    rs12901071Intronic0.34A/G0.680.67 (0.53–0.84)0.85 (0.60–1.20)
    rs12904944Intronic0.34G/A1.000.81 (0.64–1.01)1.07 (0.79–1.47)
    rs12907997Intronic0.50C/T1.000.95 (0.78–1.14)0.91 (0.70–1.20)
    rs12915039Intronic0.24A/C1.001.01 (0.76–1.35)1.08 (0.72–1.61)
    rs16950687Intronic0.28A/G1.000.93 (0.72–1.21)1.22 (0.85–1.76)
    rs17293443Intronic0.22T/C0.920.85 (0.61–1.19)1.74 (1.08–2.82)
    Smad418q21.1rs8096092Intronic0.38C/A0.681.00 (0.81–1.23)1.17 (0.87–1.59)
    rs10502913Intronic0.24G/A0.740.81 (0.61–1.08)1.09 (0.72–1.67)
    Smad718q21.1rs1316447Intronic0.19C/T1.000.86 (0.60–1.23)0.88 (0.53–1.45)
    rs2337106Intronic0.47C/G1.000.88 (0.72–1.06)1.11 (0.85–1.45)
    rs2337107Intronic0.41G/A0.991.12 (0.92–1.36)0.97 (0.74–1.28)
    rs3736242Intronic0.22G/A1.000.94 (0.69–1.28)1.33 (0.84–2.09)
    rs3764482Intronic0.19C/T1.001.25 (0.86–1.81)0.60 (0.34–1.07)
    rs4464148Intronic0.31T/C1.001.06 (0.83–1.35)0.76 (0.54–1.09)
    rs4939827Intronic0.49T/C1.000.79 (0.66–0.95)0.95 (0.73–1.23)
    rs4939832Intronic0.24A/G1.001.00 (0.76–1.32)1.29 (0.87–1.92)
    rs7238442Intronic0.46T/C0.821.12 (0.93–1.35)0.92 (0.71–1.20)
    rs12456328Intronic0.13C/T1.000.81 (0.49–1.33)1.16 (0.51–2.66)
    rs12953717Intronic0.42C/T1.001.36 (1.12–1.65)0.90 (0.68–1.19)
    TGFβ119q13.1rs18004695 upstream0.31G/A1.000.65 (0.51–0.84)0.98 (0.71–1.38)
    rs4803455Intronic0.48C/A0.921.43 (1.18–1.73)1.04 (0.79–1.35)
    TGFβR19q22rs1571590Intronic0.20A/G0.671.39 (0.98–1.96)1.42 (0.85–2.39)
    rs6478974Intronic0.49T/A1.000.86 (0.71–1.04)0.84 (0.63–1.10)
    rs10733710Intronic0.20G/A0.961.06 (0.77–1.46)1.22 (0.78–1.91)

    NOTE: MAF and FDR-adjusted Hardy-Weinberg Equilibrium (FDR HWE) based on White control population. ORs are adjusted for age, center, race, and sex.

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    Cancer Epidemiology Biomarkers & Prevention: 20 (1)
    January 2011
    Volume 20, Issue 1
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    Genetic Variation in the TGF-β Signaling Pathway and Colon and Rectal Cancer Risk
    Martha L. Slattery, Jennifer S. Herrick, Abbie Lundgreen and Roger K. Wolff
    Cancer Epidemiol Biomarkers Prev January 1 2011 (20) (1) 57-69; DOI: 10.1158/1055-9965.EPI-10-0843

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    Genetic Variation in the TGF-β Signaling Pathway and Colon and Rectal Cancer Risk
    Martha L. Slattery, Jennifer S. Herrick, Abbie Lundgreen and Roger K. Wolff
    Cancer Epidemiol Biomarkers Prev January 1 2011 (20) (1) 57-69; DOI: 10.1158/1055-9965.EPI-10-0843
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