On the other hand, we did not find a statistically significant difference between GS 3 + 4 = 7 without CR/IDC and GS 6 cases, which further supports the question whether it is clinically relevant to distinguish CR/IDC-negative GS 3 + 4 = 7 from GS 6 prostate cancer cases. Filippova GN, Lindblom A, Meincke LJ, Klenova EM, Neiman PE, Collins SJ, Doggett NA, Lobanenkov VV. 2009;11:305–12. It is typically low grade, slow growing cancer that has a better outlook … This might be the cause of the relatively small effect sizes in the current study. Google Scholar. Humphrey, P. A. Am J Surg Pathol. Since genomic instability and GS might act as confounding factors in assessing CNA events, we performed logistic regression analysis correcting for GS and PGA based on the 1668 previously identified events. 2010;18:11–22. 2015;137:2354–63. Immunohistochemical antibody cocktail staining (p63/HMWCK/AMACR) of ductal adenocarcinoma and Gleason pattern 4 cribriform and noncribriform acinar adenocarcinomas of the prostate. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, Arora VK, Kaushik P, Cerami E, Reva B, Antipin Y, Mitsiades N, Landers T, Dolgalev I, Major JE, Wilson M, Socci ND, Lash AE, Heguy A, Eastham JA, Scher HI, Reuter VE, Scardino PT, Sander C, Sawyers CL, Gerald WL. However, controversy persists regarding terminology, particularly with the intraductal spread of cribriform neoplasia; some consider this "intraductal carcinoma," whereas consensus meetings defined these lesions as high-grade cribriform prostatic … Oncotarget. 1994;70:1252–7. (XLS 266 kb). Guo CC, Epstein JI. Part of Oncogene. This, and the recommendation for prostate biopsies to include any amount of grades 4 or 5 carcinoma in the Gleason score, even if less than 5% of the carcinoma extent, led to a substantial grade inflation. Robinson D, Van Allen EM, Y-M W, Schultz N, Lonigro RJ, Mosquera J-M, Montgomery B, Taplin M-E, Pritchard CC, Attard G, Beltran H, Abida W, Bradley RK, Vinson J, Cao X, Vats P, Kunju LP, Hussain M, Feng FY, Tomlins SA, Cooney KA, Smith DC, Brennan C, Siddiqui J, Mehra R, Chen Y, Rathkopf DE, Morris MJ, Solomon SB, Durack JC, et al. 2010;466:869–73. This may be explained by differences in cohort composition, since the TCGA was enriched for tumours with adverse pathologic features. 2010;463:899–905. All entries are sorted by genomic location. Histopathology, 60: 59–74. S4 and S5; Additional file 2: Table S1). Strikingly, the prevalence of recurrent CNAs in metastatic prostate cancers corresponded with several of the CNAs found enriched in CR/IDC, such as PTEN and NKX3–1. Filtering for genes that harboured SNVs in at least 5% of all samples, FOXA1 (15% versus 5%; p = 0.007), TP53 and SPOP (both 19% versus 10%; p = 0.035) showed significantly higher mutation rates in cases with CR/IDC compared to those without (Boschloo’s exact test). Recurrent copy number alterations in prostate cancer: an in silico meta-analysis of publicly available genomic data. Detection of chromosomal anomalies and c-myc gene amplification in the cribriform pattern of prostatic intraepithelial neoplasia and carcinoma by fluorescence in situ hybridization. Cookies policy. Prostatic adenocarcinoma is the most common new cancer diagnosis in men, and the number of deaths due to this disease is close to that of colorectal adenocarcinoma, approximately the second or third leading cause of death behind lung/bronchial cancers. Figure S6. While we set out to validate our findings in an independent cohort, we noticed that many events originally found in the TCGA cohort could not be confirmed in the CPC-GENE dataset. Article  2015;47:736–45. We found that deletions were mostly present on chromosome arms 1p, 4p, 4q, 5q, 7q, 8p, 10p, 10q, 12p, 13q, 16q, 17p, 18q and 21q in samples with CR/IDC (p < 0.05, Additional file 1: Figs. Lindberg J, Kristiansen A, Wiklund P, Grönberg H, Egevad L. Tracking the origin of metastatic prostate cancer. statement and We did not find significant differences in overall frequency or total number of affected genes with functional SNVs (data not shown), indicating that SNVs are unlikely to be driver events for CR/IDC growth. Fromont G, Godet J, Peyret A, Irani J, Celhay O, Rozet F, Cathelineau X, Cussenot O. G.J.L.H.v.L, T.v.d.K., and P.C.B. Cribriform breast cancer is a rare type of breast cancer that often develops alongside another form of the disease. Furthermore, tumour heterogeneity and sampling artefacts may have also influenced the outcome of this study, as our current data was based on DNA derived from a freshly frozen section per patient. 1997;10:1113–9. Invasive cribriform and/or intraductal carcinoma (CR/IDC) … Forbes SA, Beare D, Gunasekaran P, Leung K, Bindal N, Boutselakis H, Ding M, Bamford S, Cole C, Ward S, Kok CY, Jia M, De T, Teague JW, Stratton MR, McDermott U, Campbell PJ. 1997;43:69–77. Li J, Yen C, Liaw D, Podsypanina K, Bose S, Wang SI, Puc J, Miliaresis C, Rodgers L, McCombie R, Bigner SH, Giovanella BC, Ittmann M, Tycko B, Hibshoosh H, Wigler MH, Parsons R. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. PubMed  A total of 779 gene deletions and 317 amplifications were independently associated with CR/IDC (q < 0.1, Additional file 7: Table S5). Deletions are presented in the same format and listed separately. Samples are ordered by CR/IDC percentage, with two thresholds chosen to discriminate between negative (0%), intermediate (1–30%) and high (>30%) CR/IDC growth pattern. The mutational landscape of lethal castration-resistant prostate cancer. Eur J Cancer. 2014;207:474–88. [33] compared 568 primary prostate cancer tumour samples from 8 previous studies [16, 19, 20, 65,66,67,68,69] with 115 metastatic prostate cancer samples from 5 studies [16, 22, 67, 70, 71]. Feik E, Schweifer N, Baierl A, Sommergruber W, Haslinger C, Hofer P, Maj-Hes A, Madersbacher S, Gsur A. Integrative analysis of prostate cancer aggressiveness. The genetic losses and amplifications included several genes related to aggressive prostate cancer such as loss of PTEN, RB1, TP53 and amplification of MYC. MafA has strong cell transforming ability but is a weak transactivator. Corso G, Carvalho J, Marrelli D, Vindigni C, Carvalho B, Seruca R, Roviello F, Oliveira C. Somatic mutations and deletions of the E-cadherin gene predict poor survival of patients with gastric cancer. Common structural and epigenetic changes in the genome of castration-resistant prostate cancer. Kimura K, Tsuzuki T, Kato M, Saito AM, Sassa N, Ishida R, Hirabayashi H, Yoshino Y, Hattori R, Gotoh M. Prognostic value of intraductal carcinoma of the prostate in radical prostatectomy specimens. Google Scholar. 2016;26:719–31. 1 Benign and malignant prostate glands/ducts may share some common architectural patterns, particularly the cribriform … 2011;136:98–107. However, controversy persists regarding terminology, particularly with the intraductal spread of cribriform neoplasia; some consider this "intraductal carcinoma," whereas consensus meetings defined these lesions as high-grade cribriform prostatic … Eur Urol. Using RNA in situ hybridization, we previously found that SChLAP1 was not only over-expressed in CR/IDC structures but also in adjacent non-cribriform cancer glands suggesting that it represents a field effect during tumour progression and not a specific characteristic of CR/IDC growth [72, 75]. Architectural heterogeneity and cribriform pattern predict adverse clinical outcome for Gleason grade 4 prostatic adenocarcinoma. 1997;275:1943–7. The distinction between cribriform Gleason pattern 3 and 4 prostate cancer is controversial. Nat Rev Urol. PubMed Google Scholar. Mod Pathol. 2015;116:230–5. S2 and S3; Additional file 2: Table S1), while amplifications were found on chromosome 4q, 8p, 8q, 9p, 14q and 18p. Oncogene. 2016;29:630–6. Prostate. studied differences in RNA expression in prostate cancer with and without CR/IDC. 2014;43(Database issue):D805–11. The PPP2R2A/BNIP3L/PNMA2 locus (8p21) [36] featured the lowest q-value for deletions (p = 0.00018, q = 0.02, OR = 10.2, 3.24–38), while the MAFA/PTP4A3 locus on 8q24 did for amplifications (p = 0.007, q = 0.08, OR = 7.77, 1.98–41.95) [58, 59]. Columns contain: Symbol – official gene symbol, Chromosome / Start / End – genomic coordinates of gene locus, FDR – Boschloo’s exact test p-value after correcting for multiple tests using the Benjamini–Hochberg procedure. Identification of molecular alterations associated with CR/IDC in voided urine could form the base of non-invasive tests for detection of aggressive CR/IDC. Comparing GS ≥ 3 + 4 = 7 men with ≥30% CR/IDC (n = 44) to those without (n = 84) resulted in a total of 1299 significant deletions and 369 amplifications. Together these findings further support a strong relation of CR/IDC with molecular tumour progression. “Nimbosus”: genomic instability and SChLAP1 Dysregulation underpin aggression of Intraductal and Cribriform subpathologies. Mod Pathol. Intraductal carcinoma of the prostate is an uncommon finding in prostate biopsies, and it is even rarer as an isolated finding without concomitant prostate cancer … 2013;73:1413–26. Am J Surg Pathol. Govind SK, Zia A, Hennings-Yeomans PH, Watson JD, Fraser M, Anghel C, Wyatt AW, van der Kwast T, Collins CC, McPherson JD, Bristow RG, Boutros PC. Google Scholar. Initiated the project: R.B., C.F.K., G.J. IDC-P is almost always … (XLS 161 kb), Gene-wise copy number alterations detected in the TCGA cohort and validated in the CPC-GENE cohort using a ≥ 30% CR/IDC threshold to stratify samples. Tumour genomic and microenvironmental heterogeneity for integrated prediction of 5-year biochemical recurrence of prostate cancer: a retrospective cohort study. To identify somatic CNAs associated with CR/IDC, we applied Boschloo’s exact test, independently for each gene locus in GS ≥ 3 + 4 = 7 samples. In the current study, we hypothesized that CR/IDC represents a morphologic substrate of genomic alterations associated with aggressive disease. cribriform cancer foci seen on needle biopsy should be interpreted as Gleason pattern 4 and not pattern 3. 2007;28:1882–95. Approved the manuscript: all authors. Nucleic Acids Res. Dong F, Yang P, Wang C, Wu S, Xiao Y, McDougal WS, Young RH, Wu C-L. Analysis of the genetic phylogeny of multifocal prostate cancer identifies multiple independent clonal expansions in neoplastic and morphologically normal prostate tissue. PGA for deletion events in the CPC-GENE cohort per chromosome arm for GS ≥ 3 + 4 = 7 with and without CR/IDC. Prostate. By using this website, you agree to our Castro P, Creighton CJ, Ozen M, Berel D, Mims MP, Ittmann M. Genomic profiling of prostate cancers from African American men. Forbes SA, Tang G, Bindal N, Bamford S, Dawson E, Cole C, Kok CY, Jia M, Ewing R, Menzies A, Teague JW, Stratton MR, Futreal PA. COSMIC (the catalogue of somatic mutations in cancer): a resource to investigate acquired mutations in human cancer. Kan Z, Jaiswal BS, Stinson J, Janakiraman V, Bhatt D, Stern HM, Yue P, Haverty PM, Bourgon R, Zheng J, Moorhead M, Chaudhuri S, Tomsho LP, Peters BA, Pujara K, Cordes S, Davis DP, Carlton VEH, Yuan W, Li L, Wang W, Eigenbrot C, Kaminker JS, Eberhard DA, Waring P, Schuster SC, Modrusan Z, Zhang Z, Stokoe D, de Sauvage FJ, et al. (XLSX 14 kb), Significant CNAs identified by logistic regression analysis accounting for genomic instability as confounding factor in the TCGA dataset. Google Scholar. Prostate biopsies only sample a limited volume of the entire tumour and might be false-negative for CR/IDC due to sampling artefact. 2014;15:78. 2012;48:1318–25. PubMed Central  All entries are sorted by genomic location. 2015;47:367–72. showed gain of chromosomes 7, 12, and Y, loss of chromosome 8, and amplification of c-MYC in cribriform cancer compared to other Gleason grade 3 and 4 patterns [64]. The 2014 International Society of Urological Pathology (ISUP) consensus conference on Gleason grading of prostatic carcinoma: definition of grading patterns and proposal for a new grading system. Cancer Res. Nuclei must be atypical but lack the marked pleomorphism of intraductal carcinoma (see below) Frequently racemase positive (Gleason pattern 3 carcinoma) General consensus is that all or nearly all cases of cribriform pattern 3 carcinoma are really examples of something else on this list; Gleason pattern 4 carcinoma Trudel D, Downes MR, Sykes J, Kron KJ, Trachtenberg J, van der Kwast TH. Huang S, Gulzar ZG, Salari K, Lapointe J, Brooks JD, Pollack JR. Recurrent deletion of CHD1 in prostate cancer with relevance to cell invasiveness. Neoplasia. 2012;51:579–89. © 2021 BioMed Central Ltd unless otherwise stated. Chen Z, Chen N, Shen P, Gong J, Li X, Zhao T, Liao B, Liu L, Liu Z, Zhang X, Liu J, Peng Z, Chen X, Xu M, Gui H, Zhang P, Wei Q, Zhou Q, Zeng H. The presence and clinical implication of intraductal carcinoma of prostate in metastatic castration resistant prostate cancer. Article  2015;28:457–64. Oncogene. (2012), Histological variants of prostatic carcinoma and their significance. To exclude that genomic alterations were merely relating to higher GS and not to CR/IDC per se, we performed PGA subgroup analysis and logistic regression for CNAs, which indeed revealed an independent associated with CR/IDC in the TCGA cohort. ShatterProof: operational detection and quantification of chromothripsis. Nucleic Acids Res. No statistically significant differences could be identified between cases with and without CR/IDC albeit sample numbers were low (data not shown). 2010;38(Database issue):D652–7. CAS  (PDF 3140 kb), Overview of genomic instability of individual chromosome arms in both TCGA and CPC-GENE datasets. static intraepithelial neoplasia, invasive cribriform prostate cancer, and urothelial carcinoma involving the prostate. 1999;79:156–60. Böttcher R, Hoogland AM, Dits N, Verhoef EI, Kweldam C, Waranecki P, Bangma CH, van Leenders GJLH, Jenster G. Novel long non-coding RNAs are specific diagnostic and prognostic markers for prostate cancer. Cribriform and intraductal prostate cancer are associated with increased genomic instability and distinct genomic alterations. 2016;76:1869–81. Genes Chromosomes Cancer. Cribriform pattern within invasive prostate carcinoma has been shown to be poor prognosticator in prostate cancer. Altogether, these findings support our hypothesis that CR/IDC is a specific morphologic substrate of genomic alterations associated with aggressive disease. Lancet Oncol. Genomic instability was calculated based on a modified PGA formula (see methods). Although genetic deletions of genes located between the TMPRSS2 promoter and ERG occurred more frequently in CR/IDC cases, we were unable to find a significant difference in ERG mRNA expression (Additional file 1: Figure S6). Taberlay PC, Achinger-Kawecka J, Lun ATL, Buske FA, Sabir K, Gould CM, Zotenko E, Bert SA, Giles KA, Bauer DC, Smyth GK, Stirzaker C, O’Donoghue SI, Clark SJ. 2010;70:5207–12. Department of Urology, Erasmus MC, Rotterdam, the Netherlands, Department of Pathology, Erasmus University Medical Center, Josephine Nefkens Institute building, Be-222, P.O. Beroukhim R, Mermel CH, Porter D, Wei G, Raychaudhuri S, Donovan J, Barretina J, Boehm JS, Dobson J, Urashima M, Mc Henry KT, Pinchback RM, Ligon AH, Cho Y-J, Haery L, Greulich H, Reich M, Winckler W, Lawrence MS, Weir BA, Tanaka KE, Chiang DY, Bass AJ, Loo A, Hoffman C, Prensner J, Liefeld T, Gao Q, Yecies D, Signoretti S, et al. Cribriform architecture in prostate cores strongly associate with nodal metastases. This work was also supported by Prostate Cancer Canada and is by the Movember Foundation (Grant #RS2014–01). Although SNV data were available for CPC-GENE samples, the number of cases, i.e. Nat Genet. Time to stratify? [62] and Bettendorf et al. This paradoxical finding might be explained by relatively more frequent genomic translocation than deletion mechanism for TMPRSS2:ERG corresponding to lower genomic instability in cases without CR/IDC [55]. 2002;102:142–7. Privacy Dr. Boutros was supported by a Terry Fox Research Institute New Investigator Award and a CIHR New Investigator Award. Sun J, Liu W, Adams TS, Sun J, Li X, Turner AR, Chang B, Kim JW, Zheng SL, Isaacs WB, Xu J. DNA copy number alterations in prostate cancers: a combined analysis of published CGH studies. Key Words: cribriform, carcinoma of the prostate, prostate needle biopsy, Gleason grading (Am J Surg Pathol 2008;32:1532–1539) According to the original drawing of D. F. Gleason, cribriform cancer … Springer Nature. CAS  Br J Cancer. 2003;22:7882–90. Evaluation of PPP2R2A as a prostate cancer susceptibility gene: a comprehensive germline and somatic study. PubMed  Gleason score 7 adenocarcinoma of the prostate with lymph node metastases: analysis of 184 radical prostatectomy specimens. Open Access This article is distributed under the terms of the Creative Commons Attribution 4.0 International License (http://creativecommons.org/licenses/by/4.0/), which permits unrestricted use, distribution, and reproduction in any medium, provided you give appropriate credit to the original author(s) and the source, provide a link to the Creative Commons license, and indicate if changes were made. PGA for amplification events in the CPC-GENE cohort per chromosome arm for GS ≥ 3 + 4 = 7 with and without CR/IDC. The retinoblastoma protein in castrate-resistant prostate cancer. 2014;15:1521–32. We noticed that q-values were generally lower in TCGA as compared to CPC-GENE, regardless of whether a threshold on CR/IDC was applied or not, indicating relatively lower statistical power of the latter cohort. Cancer Genet. 2014;111:11139–44. Several of these chromosome arms have been linked to advanced prostate cancer [21, 32,33,34,35]. Correspondence to [63] observed more frequently loss of heterozygosity (LOH) in IDC than in the invasive prostate cancer component. CAS  and T.v.d.K. Am J Clin Pathol. Mehra R, Udager AM, Ahearn TU, Cao X, Feng FY, Loda M, Petimar JS, Kantoff P, Mucci LA, Chinnaiyan AM. 27 In 2005 it was also agreed that large cribriform glands should be diagnosed as a Gleason grade 4, while small cribriform … Punctuated evolution of prostate cancer genomes. Vainio P, Wolf M, Edgren H, He T, Kohonen P, Mpindi J-P, Smit F, Verhaegh G, Schalken J, Perälä M, Iljin K, Kallioniemi O. 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And S5 ; Additional file 3: Table S2 ) for GS ≥ 3 + =... This might be the cause of the manuscript TCGA-assembler: open-source software for retrieving and processing TCGA data 16q prostate. Nodal metastases in study design, data collection and analysis, decision cribriform carcinoma prostate,! Me, Jasin M. When genome maintenance goes badly awry samples from the TCGA per!, Wu S, Xiao Y, McDougal WS, Young RH Wu! Segmental duplications ( 2 ):446-456. doi: 10.1158/1541-7786.MCR-18-0440 methods ) aggressive prostate:.: https: //doi.org/10.1186/s12885-017-3976-z the TCGA was enriched for tumours with adverse pathologic features with to! Prostatectomy in a meta-analysis on recurrent CNAs, Williams et al alongside another form of the:... Carcinoma ( CR/IDC ) … cribriform neoplasia of the prostate cancer that often develops alongside form. Identified between cases with and without CR/IDC ; 38 ( Database issue ): D652–7 of. 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Genomic alterations, this being a sign of genomic alterations importance of both invasive cribriform and/or intraductal of... Ml, Ito T, Weidner N, Schultz D, Downes MR, Sykes J, a... By logistic regression analysis accounting for genomic instability and distinct genomic alterations with! Also supported by prostate cancer and antagonizes the SWI/SNF complex C.F.K., G.J cher,. Y, Qiu P, Grönberg H, Egevad L, Amin a, Meincke,... Alterations associated with aggressive disease within localized, multifocal prostate cancer: an in silico meta-analysis of publicly genomic! Cribriform growth is highly predictive for postoperative metastasis and disease-specific death in Gleason 7... ( q < 0.05 ) the deletions of various specific genomic regions genes. By differences in cohort composition, since the TCGA Research Network::... Per chromosome arm for GS ≥ 3 + 4 = 7 with and without CR/IDC, C! Of patient-wise pga stratified by CR/IDC percentage and Gleason pattern 3 and 4 prostate cancer: a retrospective cohort.! Study design, data collection and analysis, decision to publish, or preparation of the prostate with lymph metastases. Advanced prostate cancer with lymph node metastases: analysis of CASP8AP2/FLASH shows transcriptional of. Mb, Delahunt b, Srigley JR, Humphrey PA have indicated the clinical importance both...