Molecular evidence that invasive adenocarcinoma can mimic prostatic intraepithelial neoplasia (PIN) and intraductal carcinoma through retrograde glandular colonization

Journal of Pathology

Volumn 238, Issue 1, 2016, Pages 31-41

  Haffner, Michael C ^a   Weier, Christopher ^a   Xu, Meng Meng ^b   Vaghasia, Ajay ^a   Gürel, Bora ^c,e   Gümüşkaya, Berrak ^c,f   Esopi, David M ^a   Fedor, Helen ^c   Tan, Hsueh Li ^c   Kulac, Ibrahim ^c   Hicks, Jessica ^c   Isaacs, William B ^a,d   Lotan, Tamara L ^a,c   Nelson, William G ^a,c,d   Yegnasubramanian, Srinivasan ^a   De Marzo, Angelo M ^a,c,d  

^a JOHNS HOPKINS UNIVERSITY   (United States)

^b DUKE UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^d JOHNS HOPKINS UNIVERSITY   (United States)

^e KOCAELI UNIVERSITY   (Turkey)

^f Department of Pathology   (Turkey)

Author keywords

clonality; ductal spreading; ERG; prostate cancer; prostatic intraepithelial neoplasia; PTEN

Indexed keywords

PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; TRANSCRIPTION FACTOR ERG; ERG PROTEIN, HUMAN; ONCOPROTEIN; PTEN PROTEIN, HUMAN; TMPRSS2-ERG FUSION PROTEIN, HUMAN; TRANSACTIVATOR PROTEIN;

ARTICLE; CANCER CELL; CANCER GRADING; CANCER MORPHOLOGY; CELL INVASION; CHROMOSOME ANALYSIS; CLINICAL ARTICLE; CLINICAL FEATURE; CLONAL EVOLUTION; CLONAL VARIATION; CONTROLLED STUDY; GENE DELETION; GENE OVEREXPRESSION; GENE REARRANGEMENT; GENETIC ANALYSIS; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; INTRADUCTAL CARCINOMA; INVASIVE CARCINOMA; MALE; MOLECULAR GENETICS; MOLECULAR MIMICRY; MOLECULAR PHYLOGENY; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; PROSTATE CARCINOMA; PROSTATIC INTRAEPITHELIAL NEOPLASIA; TMPRSS2 GENE; TUMOR GENE; TUMOR INVASION; ADENOCARCINOMA; DIFFERENTIAL DIAGNOSIS; FLUORESCENCE IN SITU HYBRIDIZATION; GENETICS; IMMUNOHISTOCHEMISTRY; PATHOLOGY; PROSTATE TUMOR; TUMOR CELL LINE;

ADENOCARCINOMA; CARCINOMA, INTRADUCTAL, NONINFILTRATING; CELL LINE, TUMOR; DIAGNOSIS, DIFFERENTIAL; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION, FLUORESCENCE; MALE; NEOPLASM INVASIVENESS; ONCOGENE PROTEINS, FUSION; PROSTATIC INTRAEPITHELIAL NEOPLASIA; PROSTATIC NEOPLASMS; PTEN PHOSPHOHYDROLASE; TRANS-ACTIVATORS; TRANSCRIPTIONAL REGULATOR ERG;

EID: 84955190474     PISSN: 00223417     EISSN: 10969896     Source Type: Journal    
DOI: 10.1002/path.4628     Document Type: Article

References (60)

1. Lindberg J, Klevebring D, Liu W, et al,. Exome sequencing of prostate cancer supports the hypothesis of independent tumour origins. Eur Urol 2013; 63: 347-353.
2. Baca SC, Prandi D, Lawrence MS, et al,. Punctuated evolution of prostate cancer genomes. Cell 2013; 153: 666-677.
3. Haffner MC, Mosbruger T, Esopi DM, et al,. Tracking the clonal origin of lethal prostate cancer. J Clin Invest 2013; 123: 4918-4922.
4. Bostwick DG, Shan A, Qian J,. Matched foci of prostate carcinoma. Cancer 1998; 83: 1995-2002.
5. Clark J, Attard G, Jhavar S,. Prostate. Oncogene 2007; 27: 1993-2003.
6. Brocks D, Assenov Y, Minner S, et al,. Intratumor DNA methylation heterogeneity reflects clonal evolution in aggressive prostate cancer. Cell Rep 2014; 8: 798-806.
7. Gumuskaya B, Gurel B, Fedor H, et al,. Assessing the order of critical alterations in prostate cancer development and progression by IHC: further evidence that PTEN loss occurs subsequent to ERG gene fusion. Prostate Cancer Prostatic Dis 2013; 16: 209-215.
8. Qian J, Bostwick DG, Takahashi S, et al,. Chromosomal anomalies in prostatic intraepithelial neoplasia and carcinoma detected by fluorescence in situ hybridization. Cancer Res 1995; 55: 5408-5414.
9. Ruijter ET, Miller GJ, van de Kaa CA, et al,. Molecular analysis of multifocal prostate cancer lesions. J Pathol 1999; 188: 271-277.
10. Cooper CS, Eeles R, Wedge DC, et al,. Analysis of the genetic phylogeny of multifocal prostate cancer identifies multiple independent clonal expansions in neoplastic and morphologically normal prostate tissue. Nature Genet 2015; 47: 367-372.
11. Bostwick DG, Cheng L,. Precursors of prostate cancer. Histopathology 2011; 60: 4-27.
12. Epstein JI,. Precursor lesions to prostatic adenocarcinoma. Virchows Arch 2008; 454: 1-16.
13. Lee MC, Moussa AS, Yu C, et al,. Multifocal high grade prostatic intraepithelial neoplasia is a risk factor for subsequent prostate cancer. J Urol 2010; 184: 1958-1962.
14. Netto GJ, Epstein JI,. Widespread high-grade prostatic intraepithelial neoplasia on prostatic needle biopsy: a significant likelihood of subsequently diagnosed adenocarcinoma. Am J Surg Pathol 2006; 30: 1184-1188.
15. Park K, Dalton JT, Narayanan R, et al,. TMPRSS2:ERG gene fusion predicts subsequent detection of prostate cancer in patients with high-grade prostatic intraepithelial neoplasia. J Clin Oncol 2014; 32: 206-211.
16. Roscigno M, Scattoni V, Freschi M, et al,. Diagnosis of isolated high-grade prostatic intra-epithelial neoplasia: proposal of a nomogram for the prediction of cancer detection at saturation re-biopsy. BJU Int 2012; 109: 1329-1334.
17. McNeal JE, Villers A, Redwine EA, et al,. Microcarcinoma in the prostate: its association with duct-acinar dysplasia. Hum Pathol 1991; 22: 644-652.
18. Bostwick DG, Qian J,. High-grade prostatic intraepithelial neoplasia. Mod Pathol 2004; 17: 360-379.
19. Magi-Galluzzi C, Xu X, Hlatky L, et al,. Heterogeneity of androgen receptor content in advanced prostate cancer. Mod Pathol 1997; 10: 839-845.
20. Sakr WA, Partin AW,. Histological markers of risk and the role of high-grade prostatic intraepithelial neoplasia. Urology 2001; 57 (Suppl 1): 115-20.
21. Bostwick DG,. Prospective origins of prostate carcinoma. Prostatic intraepithelial neoplasia and atypical adenomatous hyperplasia. Cancer 1996; 78: 330-336.
22. Meeker AK, Hicks JL, Platz EA, et al,. Telomere shortening is an early somatic DNA alteration in human prostate tumorigenesis. Cancer Res 2002; 62: 6405-6409.
23. Qian J, Jenkins RB, Bostwick DG,. Detection of chromosomal anomalies and c-myc gene amplification in the cribriform pattern of prostatic intraepithelial neoplasia and carcinoma by fluorescence in situ hybridization. Mod Pathol 1997; 10: 1113-1119.
24. Brooks JD, Weinstein M, Lin X, et al,. CG island methylation changes near the GSTP1 gene in prostatic intraepithelial neoplasia. Cancer Epidemiol Biomarkers Prev 1998; 7: 531-536.
25. Nakayama M, Bennett CJ, Hicks JL, et al,. Hypermethylation of the human glutathione S-transferase-π gene (GSTP1) CpG island is present in a subset of proliferative inflammatory atrophy lesions but not in normal or hyperplastic epithelium of the prostate: a detailed study using laser-capture microdissection. Am J Pathol 2003; 163: 923-933.
26. Bismar TA, Yoshimoto M, Vollmer RT, et al,. PTEN genomic deletion is an early event associated with ERG gene rearrangements in prostate cancer. BJU Int 2011; 107: 477-485.
27. Vukovic B, Park PC, Al-Maghrabi J, et al,. Evidence of multifocality of telomere erosion in high-grade prostatic intraepithelial neoplasia (HPIN) and concurrent carcinoma. Oncogene 2003; 22: 1978-1987.
28. Rubin MA, Maher CA, Chinnaiyan AM,. Common gene rearrangements in prostate cancer. J Clin Oncol 2011; 29: 3659-3668.
29. Tomlins SA, Bjartell A, Chinnaiyan AM, et al,. ETS gene fusions in prostate cancer: from discovery to daily clinical practice. Eur Urol 2009; 56: 275-286.
30. Mosquera J-M, Perner S, Genega EM, et al,. Characterization of TMPRSS2-ERG fusion high-grade prostatic intraepithelial neoplasia and potential clinical implications. Clin Cancer Res 2008; 14: 3380-3385.
31. Cerveira N, Ribeiro FR, Peixoto A, et al,. TMPRSS2-ERG gene fusion causing ERG overexpression precedes chromosome copy number changes in prostate carcinomas and paired HGPIN lesions. Neoplasia 2006; 8: 826-832.
32. Han B, Mehra R, Lonigro RJ, et al,. Fluorescence in situ hybridization study shows association of PTEN deletion with ERG rearrangement during prostate cancer progression. Mod Pathol 2009; 22: 1083-1093.
33. Furusato B, Tan S-H, Young D, et al,. ERG oncoprotein expression in prostate cancer: clonal progression of ERG-positive tumor cells and potential for ERG-based stratification. Prostate Cancer Prostatic Dis 2010; 13: 228-237.
34. Weier C, Haffner MC, Mosbruger T, et al,. Nucleotide resolution analysis of TMPRSS2 and ERG rearrangements in prostate cancer. J Pathol 2013; 230: 174-183.
35. Haffner MC, Aryee MJ, Toubaji A, et al,. Androgen-induced TOP2B-mediated double-strand breaks and prostate cancer gene rearrangements. Nature Genet 2010; 42: 668-675.
36. Sowalsky AG, Ye H, Bubley GJ, et al,. Clonal progression of prostate cancers from Gleason grade 3 to grade 4. Cancer Res 2013; 73: 1050-1055.
37. Krohn A, Freudenthaler F, Harasimowicz S, et al,. Heterogeneity and chronology of PTEN deletion and ERG fusion in prostate cancer. Mod Pathol 2014; 27: 1612-1620.
38. Chaux A, Peskoe SB, Gonzalez-Roibon N, et al,. Loss of PTEN expression is associated with increased risk of recurrence after prostatectomy for clinically localized prostate cancer. Mod Pathol 2012; 25: 1543-1549.
39. Antonarakis ES, Keizman D, Zhang Z, et al,. An immunohistochemical signature comprising PTEN, MYC, and Ki67 predicts progression in prostate cancer patients receiving adjuvant docetaxel after prostatectomy. Cancer 2012; 118: 6063-6071.
40. Lotan TL, Gurel B, Sutcliffe S, et al,. PTEN protein loss by immunostaining: analytic validation and prognostic indicator for a high risk surgical cohort of prostate cancer patients. Clin Cancer Res 2011; 17: 6563-6573.
41. Yoshimoto M, Joshua AM, Cunha IW, et al,. Absence of TMPRSS2:ERG fusions and PTEN losses in prostate cancer is associated with a favorable outcome. Mod Pathol 2008; 21: 1451-60.
42. Han B, Suleman K, Wang L, et al,. ETS gene aberrations in atypical cribriform lesions of the prostate: implications for the distinction between intraductal carcinoma of the prostate and cribriform high-grade prostatic intraepithelial neoplasia. Am J Surg Pathol 2010; 34: 478-485.
43. Clark J, Attard G, Jhavar S, et al,. Complex patterns of ETS gene alteration arise during cancer development in the human prostate. Oncogene 2008; 27: 1993-2003.
44. Lotan TL, Gumuskaya B, Rahimi H, et al,. Cytoplasmic PTEN protein loss distinguishes intraductal carcinoma of the prostate from high-grade prostatic intraepithelial neoplasia. Mod Pathol 2013; 26: 587-603.
45. Tomlins SA, Laxman B, Varambally S, et al,. Role of the TMPRSS2-ERG gene fusion in prostate cancer. Neoplasia 2008; 10: 177-179.
46. McNeal JE, Yemoto CE,. Spread of adenocarcinoma within prostatic ducts and acini. Morphologic and clinical correlations. Am J Surg Pathol 1996; 20: 802-814.
47. Shah RB, Zhou M,. Atypical cribriform lesions of the prostate: clinical significance, differential diagnosis and current concept of intraductal carcinoma of the prostate. Adv Anat Pathol 2012; 19: 270-278.
48. Guo CC, Epstein JI,. Intraductal carcinoma of the prostate on needle biopsy: histologic features and clinical significance. Mod Pathol 2006; 19: 1528-1535.
49. Bonkhoff H, Wheeler TM, van der Kwast TH, et al,. Intraductal carcinoma of the prostate: precursor or aggressive phenotype of prostate cancer? Prostate 2012; 73: 442-448.
50. Cohen RJ, Wheeler TM, Bonkhoff H, et al,. A proposal on the identification, histologic reporting, and implications of intraductal prostatic carcinoma. Arch Pathol Lab Med 2007; 131: 1103-1109.
51. Lindberg J, Kristiansen A, Wiklund P, et al,. Tracking the origin of metastatic prostate cancer. Eur Urol 2015; 67: 819-822.
52. Kovi J, Jackson MA, Heshmat MY,. Ductal spread in prostatic carcinoma. Cancer 1985; 56: 1566-1573.
53. Shah RB, Magi-Galluzzi C, Han B, et al,. Atypical cribriform lesions of the prostate: relationship to prostatic carcinoma and implication for diagnosis in prostate biopsies. Am J Surg Pathol 2010; 34: 470-477.
54. Putzi MJ, De Marzo AM,. Morphologic transitions between proliferative inflammatory atrophy and high-grade prostatic intraepithelial neoplasia. Urology 2000; 56: 828-832.
55. Yoshimoto M, Ding K, Sweet JM, et al,. PTEN losses exhibit heterogeneity in multifocal prostatic adenocarcinoma and are associated with higher Gleason grade. Mod Pathol 2013; 26: 435-447.
56. Furusato B, Gao C-L, Ravindranath L, et al,. Mapping of TMPRSS2-ERG fusions in the context of multi-focal prostate cancer. Mod Pathol 2008; 21: 67-75.
57. Gao X, Li LY, Zhou FJ, et al,. ERG rearrangement for predicting subsequent cancer diagnosis in high-grade prostatic intraepithelial neoplasia and lymph node metastasis. Clin Cancer Res 2012; 18: 4163-4172.
58. Morais CL, Han JS, Gordetsky J, et al,. Utility of PTEN and ERG immunostaining for distinguishing high-grade PIN from intraductal carcinoma of the prostate on needle biopsy. Am J Surg Pathol 2015; 39: 169-178.
59. Schneider TM, Osunkoya AO,. ERG expression in intraductal carcinoma of the prostate: comparison with adjacent invasive prostatic adenocarcinoma. Mod Pathol 2014; 27: 1174-1178.
60. Becker-Santos DD, Guo Y, Ghaffari M, et al,. Integrin-linked kinase as a target for ERG-mediated invasive properties in prostate cancer models. Carcinogenesis 2012; 33: 2558-2567.