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Evolution of microRNA expression during human bronchial squamous carcinogenesis

C. Mascaux, J. F. Laes, G. Anthoine, A. Haller, V. Ninane, A. Burny, J. P. Sculier
European Respiratory Journal 2009 33: 352-359; DOI: 10.1183/09031936.00084108
C. Mascaux
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J. F. Laes
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G. Anthoine
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A. Haller
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V. Ninane
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A. Burny
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J. P. Sculier
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  • Fig. 1—
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    Fig. 1—

    Classification of samples from groups 2 and 3, based on microRNAs differentially expressed between these groups. Dendrogram for clustering experiments, using centred correlation and average linkage. The dendrogram, based on the differentially expressed microRNAs between groups 2 (metaplasia, mild and moderate dysplasia) and 3 (severe dysplasia, carcinoma in situ (CIS) and invasive carcinoma), segregated samples of groups 2 and 3 into two groups. Only three samples of group 3 (two severe dysplasias and one CIS) were misclassified into group 2.

  • Fig. 2—
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    Fig. 2—

    Classification of samples from groups 2 and 3A (A), based on microRNAs differentially expressed between these groups. Dendrogram for clustering experiments, using centred correlation and average linkage. The dendrogram, based on the differentially expressed microRNAs between groups 2 (metaplasia, mild and moderate dysplasia) and 3A (severe dysplasia and carcinoma in situ (CIS)), segregated samples of groups 2 and 3A into two groups. Only three samples of group 3A (two severe dysplasias and one CIS) were misclassified into group 2.

  • Fig. 3—
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    Fig. 3—

    Classification of samples between carcinoma in situ (CIS; stage 8) and invasive squamous cell carcinoma (SQCC; stage 9), based on microRNAs differentially expressed between these groups. a) Dendrogram for clustering experiments, using centred correlation and average linkage. MicroRNAs differentially expressed between CIS and SQCC segregated the samples of these stages into two groups according to their histological classification: the six samples of stage 8 and of stage 9 were well separated into two different branches. b) The log intensities are directly proportional to the cycle threshold (CT), and the green (smaller CT) and the red (higher CT) represent up- and downregulated microRNAs, respectively. The first five microRNAs were upregulated in SQCC (the first six samples) compared with CIS (the last six samples). The last five microRNAs were downregulated from CIS to SQCC.

Tables

  • Figures
  • Table 1—

    Composition of groups

    NonsmokersSmokers
    Nl nsNl NflNl HfHMMiDMoDSDCISSQCC
    Stage0123456789
    Group01112223A#3A#3B#
    • Nl ns: normal of nonsmokers; Nl Nfl: normal in normofluorescent area; Nl Hf: normal in hypofluorescent area; H: hyperplasia; M: metaplasia; MiD: mild dysplasia; MoD: moderate dysplasia; SD: severe dysplasia; CIS: carcinoma in situ; SQCC: squamous cell carcinoma. Stages 0 to 9 were assembled in larger groups of samples according to transcriptomic analyses performed on the same samples, thereby increasing the power of statistical tests. #: subdivision of group 3.

  • Table 2—

    Statistically significantly evolving microRNAs during lung carcinogenesis

    MicroRNA nameGroups compared
    0 and 10 and 20 and 31 and 22 and 32 and 3A3A and 3BCIS and 3B
    hsa-miR-1Down 5.88Down 10.00
    hsa-miR-7Up 4.11Up 3.96
    hsa-miR-9Down 11.11Up 17.89#Up 15.97#Up 3.05
    hsa-miR-9*Up 2.49Up 5.66
    hsa-miR-10bDown 3.03Up 2.95
    hsa-miR-15aDown 5.00Down 6.67Down 3.45
    hsa-miR-17-5pUp 2.15
    hsa-miR-32Down 6.67Down 5.88Down 4.17
    hsa-miR-34aDown 5.00
    hsa-miR-34cDown 6.67Down 14.29#Down 25.00#Down 2.50
    hsa-miR-99aDown 1.96Down 1.89
    hsa-miR-101Down 5.56Down 3.57#
    hsa-miR-106bUp 2.06Up 2.36
    hsa-miR-132Up 2.18
    hsa-miR-133aDown 5.88
    hsa-miR-134Down 2.70
    hsa-miR-135aDown 4.17Down 4.00#Down 4.00
    hsa-miR-139Down 2.27Down 5.26Down 5.88#
    hsa-miR-142-3pDown 2.94Down 5.56Up 2.60Up 2.50Up 2.51Up 2.24
    hsa-miR-142-5pDown 2.38Up 2.86Up 3.36
    hsa-miR-143Down 3.85
    hsa-miR-145Down 2.70
    has-miR-183Up 2.66
    hsa-miR-190Down 4.76
    hsa-miR-193aDown 8.33#
    hsa-miR-193bDown 4.17Up 5.66
    hsa-miR-196aUp 16.95#Up 25.69#Up 28.29#
    hsa-miR-196bUp 10.48Up 10.80#Up 10.78#
    hsa-miR-199aUp 8.77#Up 20.87
    hsa-miR-203Up 5.26#Up 4.89Up 5.79#
    hsa-miR-204Down 11.11Down 16.67
    hsa-miR-206Up 3.86Down 2.33
    hsa-miR-213Down 3.57
    hsa-miR-214Down 2.00#Up 2.35Up 2.67
    hsa-miR-216Down 3.33Down 2.63Down 2.44
    hsa-miR-218Down 5.56Down 3.57
    hsa-miR-224Up 2.58Up 1.63#Up 3.79#Up 1.63
    hsa-miR-301Down 3.57Up 2.47
    hsa-miR-324-5pDown 10.00
    hsa-miR-338Up 5.07
    hsa-miR-361Down 6.25Down 4.76
    hsa-miR-362Up 2.75Up 3.36
    hsa-miR-374Down 1.49
    hsa-miR-375Down 6.25Down 7.14#Down 11.11
    hsa-miR-382Down 2.44
    hsa-miR-410Down 2.63
    hsa-miR-411Down 4.76
    hsa-miR-422bDown 4.76Down 4.76Down 4.17
    hsa-miR-432Up 3.46
    hsa-miR-449Down 3.33Down 5.56Down 5.56
    hsa-miR-449bDown 11.11
    hsa-miR-451Down 8.33
    hsa-miR-452Up 14.81#Up 6.47#Up 6.10#
    hsa-miR-486Down 10.00
    hsa-miR-487bUp 8.19Up 19.03#
    hsa-miR-492Down 2.5
    hsa-miR-518dDown 2.63
    hsa-miR-521Down 1.56
    hsa-miR-545Down 2.78
    hsa-miR-565Down 1.67Down 2.08
    hsa-miR-572Down 3.45Down 3.85
    hsa-miR-597Up 5.43
    hsa-miR-615Up 9.74
    hsa-miR-622Down 6.25
    hsa-miR-639Down 2.86
    has-miR-642Down 5.00#Down 12.50Down 2.17Down 3.33Down 6.67
    hsa-miR-646Down 5.00
    hsa-miR-650Up 4.97
    hsa-miR-659Up 4.83Down 3.70Up 6.81
    • Data are presented as fold changes. CIS: carcinoma in situ; down: downregulated; up: upregulated. All the microRNAs found differentially expressed in at least one of the eight comparisons are shown (t-test p<0.05). #: microRNAs remaining statistically differentially expressed in a specific comparison after correction for multiple testing (CMT) at Bonferroni corrected p-value <0.05. In the first comparison (group 0 versus group 1), no microRNA expression difference remained statistically significant after CMT, whereas, in the seven other comparisons, the numbers of microRNAs with differential expression remaining statistically significant after CMT were three, six, four, five, four, one and two (from left to right).

  • Table 3—

    Two-step evolution of microRNAs in lung squamous carcinogenesis

    Differentially expressed microRNAsGroups compared
    0 and 10 and 20 and 31 and 22 and 32 and 3A3A and 3BCIS and 3B
    Total number619191630152010
    Downregulated5 (83)16 (84)14 (74)14 (87.5)17 (57)3 (20)8 (40)5 (50)
    Upregulated1 (17)3 (16)5 (26)4 (12.5)13 (43)12 (80)12 (60)5 (50)
    • Data are presented as n or n (%). CIS: carcinoma in situ. Two successive waves were observed in microRNA expression profiles during lung squamous carcinogenesis: first, a downregulation and, secondly, an upregulation of microRNAs. In the first four comparisons of microRNA profiles, between groups 0 and 1, 0 and 2, 0 and 3, and 1 and 2, the large majority of microRNAs were downregulated. In the later four comparisons, the proportion of downregulated microRNAs decreased and that of upregulated microRNAs increased, with ≥50% being upregulated for comparisons between groups 2 and 3A, 3A and 3B, and CIS and 3B.

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Evolution of microRNA expression during human bronchial squamous carcinogenesis
C. Mascaux, J. F. Laes, G. Anthoine, A. Haller, V. Ninane, A. Burny, J. P. Sculier
European Respiratory Journal Feb 2009, 33 (2) 352-359; DOI: 10.1183/09031936.00084108

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Evolution of microRNA expression during human bronchial squamous carcinogenesis
C. Mascaux, J. F. Laes, G. Anthoine, A. Haller, V. Ninane, A. Burny, J. P. Sculier
European Respiratory Journal Feb 2009, 33 (2) 352-359; DOI: 10.1183/09031936.00084108
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