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Molecular Cancer Research
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Cancer “-omics”

Distinct Genomic Alterations in Prostate Tumors Derived from African American Men

Wennuan Liu, S. Lilly Zheng, Rong Na, Lin Wei, Jishan Sun, Johnie Gallagher, Jun Wei, W. Kyle Resurreccion, Sarah Ernst, Karen S. Sfanos, William B. Isaacs and Jianfeng Xu
Wennuan Liu
1Program for Personalized Cancer Care, NorthShore University HealthSystem, Evanston, Illinois.
2Departments of Surgery, NorthShore University HealthSystem, Evanston, Illinois.
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S. Lilly Zheng
1Program for Personalized Cancer Care, NorthShore University HealthSystem, Evanston, Illinois.
2Departments of Surgery, NorthShore University HealthSystem, Evanston, Illinois.
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Rong Na
1Program for Personalized Cancer Care, NorthShore University HealthSystem, Evanston, Illinois.
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Lin Wei
1Program for Personalized Cancer Care, NorthShore University HealthSystem, Evanston, Illinois.
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Jishan Sun
1Program for Personalized Cancer Care, NorthShore University HealthSystem, Evanston, Illinois.
2Departments of Surgery, NorthShore University HealthSystem, Evanston, Illinois.
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Johnie Gallagher
1Program for Personalized Cancer Care, NorthShore University HealthSystem, Evanston, Illinois.
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Jun Wei
1Program for Personalized Cancer Care, NorthShore University HealthSystem, Evanston, Illinois.
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W. Kyle Resurreccion
1Program for Personalized Cancer Care, NorthShore University HealthSystem, Evanston, Illinois.
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Sarah Ernst
3Department of Pathology, Johns Hopkins School of Medicine, Baltimore, Maryland.
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Karen S. Sfanos
3Department of Pathology, Johns Hopkins School of Medicine, Baltimore, Maryland.
4Department of Urology and Oncology, Johns Hopkins School of Medicine, Baltimore, Maryland.
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William B. Isaacs
4Department of Urology and Oncology, Johns Hopkins School of Medicine, Baltimore, Maryland.
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Jianfeng Xu
1Program for Personalized Cancer Care, NorthShore University HealthSystem, Evanston, Illinois.
2Departments of Surgery, NorthShore University HealthSystem, Evanston, Illinois.
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  • For correspondence: u@northshore.org
DOI: 10.1158/1541-7786.MCR-20-0648 Published December 2020
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  • Figure 1.
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    Figure 1.

    The number and criteria for inclusion/exclusion of AA/black patients in the study. AA, African American; JHH, Johns Hopkins Hospital; MSKCC, Memorial Sloan Kettering Cancer Center; PCBN, Prostate Cancer Biorepository Network; QA, quality assurance.

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    Figure 2.

    The frequency of somatically acquired exon mutations (synonymous, missense, nonsense, and frameshift) identified by targeted deeper NGS in prostate cancer of 77 AA men (A) compared with those in prostate cancer of 410 EA/white men reported in the GDC (B).

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    Figure 3.

    Somatically acquired mutations with >10% mutated copies identified by targeted deeper NGS in 22 genes in prostate cancer from 77 AA men (A) compared with those in prostate cancer from 410 EA/white men reported in the GDC (B); and the landscape of CNAs identified by OncoScan in prostate cancer from 80 AA men (C: bottom) compared with those identified in prostate cancer from 393 EA/white men by Affymetrix SNP 6.0 array and reported in TCGA (C: top). Red in C: deletion/loss; darker blue in C: amplification/gain. Green oval circle marks new and less common CNAs identified in prostate cancer of AA men. Vertical black lines depict the physical position for genes of interests.

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    Figure 4.

    Somatically acquired exon mutations in ZMYM3 (A) and CDK12 (B) identified by our targeted deeper NGS and reported by Huang and colleagues (8) as well as by the GDC in prostate cancer of AA/black men compared with those in prostate cancer of EA/white men reported in the GDC (top); and CNAs along with B-allele frequency identified by OncoScan (bottom) in example tumors harboring frameshift mutations in ZMYM3 or CDK12. In top panels of A and B, red, frameshift; brown, nonsense; blue, missense; green, synonymous; purple arrows mark mutations previously reported in prostate cancer of AA by others; Ch, chromosome.

  • Figure 5.
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    Figure 5.

    Comparison of CNA frequencies that were significantly different in prostate cancer of AA/black versus EA/white men (A), new distinct somatically acquired CNAs identified by OncoScan in prostate cancer of AA men (B) and the frequencies of deletions affecting genes of interest in prostate cancer of 171 AA/black and 860 EA/white men (C). P value is calculated with two-tailed Fisher exact test. *, P < 0.05; **, P < 0.01; ***, P < 0.001; red horizontal bar: deletion/loss; darker blue horizontal bar: amplification/gain; _d, deletion/loss; _g, amplification/gain. Vertical green line marks MORs of deletion on each of the chromosomes in the tumor genomes from different patients of AA. A representative gene(s) potentially relevant in each of the regions is listed at the bottom in each of panels.

Tables

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  • Table 1.

    Associations between GG or pathologic stage and genes with CNAs at higher frequency in AA/black than EA/white men.

    Gleason gradeLocalized vs. locally advanced
    N≤2 (n = 109)3 (n = 26)≥4 (n = 35)P (Spearman)≤T2 (n = 102)T3 (n = 69)ORP
    LRP1B319 (8.3%)12 (46.2%)10 (28.6%)4.37E-0516 (15.7%)15 (21.7%)1.49 (0.68–3.27)0.32
    MAP3K77237 (33.9%)10 (38.5%)25 (71.4%)4.83E-0433 (32.4%)39 (56.5%)2.72 (1.45–5.11)0.002
    BNIP3L7838 (34.9%)19 (73.1%)21 (60.0%)3.37E-0434 (33.3%)45 (65.2%)3.75 (1.97–7.14)5.77E-05
    MYC4117 (15.6%)9 (34.6%)15 (42.9%)3.28E-0417 (16.7%)25 (36.2%)2.84 (1.39–5.81)0.004
    RB16025 (22.9%)12 (46.2%)23 (65.7%)1.08E-0625 (24.5%)36 (52.2%)3.36 (1.75–6.46)2.76E-04
    THADA146 (5.5%)4 (15.4%)4 (11.4%)0.125 (4.9%)10 (14.5%)3.29 (1.07–10.09)0.037
    NEIL3142 (1.8%)8 (30.8%)4 (11.4%)0.0014 (3.9%)10 (14.5%)4.15 (1.25–13.84)0.02
    BUB1B164 (3.7%)6 (23.1%)6 (17.1%)0.0018 (7.8%)8 (11.6%)1.54 (0.55–4.32)0.41

Additional Files

  • Figures
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  • Supplementary Data

    • Supplementary Figure 1 - Somatically acquired exon mutations of PIK3CA identified by targeted deeper NGS in PCa of AA/black are compared with those reported in PCa of EA/white in the GDC (upper panel); and CNAs together with B-allele frequency identified by OncoScan (lower panels) in 2 example tumors harboring missense mutation p.I391M. In upper panel, blue = missense, green = synonymous, purple arrow marking a mutation previously reported in AA PCa.
    • Supplementary Tables 1-6 - Supplementary Table 1. Gleason grade and TNM stage of the tumors from 83 African American men. Supplementary Table 2. Somatic exon mutations identified by Mutect2 in tumors of 77 AA men. Supplementary Table 3. Performance of the Agilent SureSelect and NimbleGen SeqCap enrichment. Supplementary Table 4. Frequency of exon somatic mutations in targeted 39 genes among 77 AA tumors. Supplementary Table 5. Number of EA/white and AA/black patients in different cohorts used for analysis of DNA copy number alterations. Supplementary Table 6. Comparing the frequency of 13 most common CNAs in EA/white and AA/black PCa.
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Molecular Cancer Research: 18 (12)
December 2020
Volume 18, Issue 12
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Distinct Genomic Alterations in Prostate Tumors Derived from African American Men
Wennuan Liu, S. Lilly Zheng, Rong Na, Lin Wei, Jishan Sun, Johnie Gallagher, Jun Wei, W. Kyle Resurreccion, Sarah Ernst, Karen S. Sfanos, William B. Isaacs and Jianfeng Xu
Mol Cancer Res December 1 2020 (18) (12) 1815-1824; DOI: 10.1158/1541-7786.MCR-20-0648

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Distinct Genomic Alterations in Prostate Tumors Derived from African American Men
Wennuan Liu, S. Lilly Zheng, Rong Na, Lin Wei, Jishan Sun, Johnie Gallagher, Jun Wei, W. Kyle Resurreccion, Sarah Ernst, Karen S. Sfanos, William B. Isaacs and Jianfeng Xu
Mol Cancer Res December 1 2020 (18) (12) 1815-1824; DOI: 10.1158/1541-7786.MCR-20-0648
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