Cytoplasmic PTEN protein loss distinguishes intraductal carcinoma of the prostate from high-grade prostatic intraepithelial neoplasia

Modern Pathology

Volumn 26, Issue 4, 2013, Pages 587-603

  Lotan, Tamara L ^a   Gumuskaya, Berrak ^a   Rahimi, Hameed ^a   Hicks, Jessica L ^a   Iwata, Tsuyoshi ^b   Robinson, Brian D ^a   Epstein, Jonathan I ^a   De Marzo, Angelo M ^a  

^a DEPARTMENT OF PATHOLOGY   (United States)

^b KYOTO PREFECTURAL UNIVERSITY   (Japan)

Author keywords

ERG; immunohistochemistry; intraductal carcinoma; prostatic adenocarcinoma; PTEN

Indexed keywords

CYTOKERATIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P63; TRANSCRIPTION FACTOR ERG;

ARTICLE; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; DIAGNOSTIC ACCURACY; DIAGNOSTIC TEST ACCURACY STUDY; HISTOPATHOLOGY; HUMAN; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; INTRADUCTAL CARCINOMA OF THE PROSTATE; INTRADUCTAL CRIBRIFORM PROLIFERATION; MALE; PRIORITY JOURNAL; PROSTATE CARCINOMA; PROSTATIC INTRAEPITHELIAL NEOPLASIA; PROTEIN EXPRESSION; RETROSPECTIVE STUDY; SENSITIVITY AND SPECIFICITY;

CARCINOMA, DUCTAL; CYTOPLASM; HUMANS; IMMUNOHISTOCHEMISTRY; MALE; NEOPLASM GRADING; NEOPLASM STAGING; PROSTATIC INTRAEPITHELIAL NEOPLASIA; PROSTATIC NEOPLASMS; PTEN PHOSPHOHYDROLASE; TUMOR MARKERS, BIOLOGICAL;

EID: 84876483693     PISSN: 08933952     EISSN: 15300285     Source Type: Journal    
DOI: 10.1038/modpathol.2012.201     Document Type: Article

References (55)

1. Kovi J, Jackson MA, Heshmat MY. Ductal spread in prostatic carcinoma. Cancer 1985;56:1566-1573. (Pubitemid 15228503)
2. McNeal JE, Yemoto CE. Spread of adenocarcinoma within prostatic ducts and acini: morphologic and clinical correlations. Am J Surg Pathol 1996;20: 802-814. (Pubitemid 26230743)
3. Wilcox G, Soh S, Chakraborty S, et al. Patterns of high-grade prostatic intraepithelial neoplasia associated with clinically aggressive prostate cancer. Hum Pathol 1998;29:1119-1123. (Pubitemid 28467533)
4. Rubin MA, de La Taille A, Bagiella E, et al. Cribriform carcinoma of the prostate and cribriform prostatic intraepithelial neoplasia: incidence and clinical implications. Am J Surg Pathol 1998;22:840-848. (Pubitemid 28328230)
5. Cohen RJ, McNeal JE, Baillie T. Patterns of differentiation and proliferation in intraductal carcinoma of the prostate: significance for cancer progression. Prostate 2000;43:11-19. (Pubitemid 30164239)
6. 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. (Pubitemid 47057901)
7. 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.
8. Guo CC, Epstein JI. Intraductal carcinoma of the prostate on needle biopsy: histologic features and clinical significance. Mod Pathol 2006;19:1528-1535. (Pubitemid 44789920)
9. Robinson BD, Epstein JI. Intraductal carcinoma of the prostate without invasive carcinoma on needle biopsy: emphasis on radical prostatectomy findings. J Urol 2010;184:1328-1333.
10. Van der Kwast T, Al Daoud N, Collette L, et al. Biopsy diagnosis of intraductal carcinoma is prognostic in intermediate and high risk prostate cancer patients treated by radiotherapy. Eur J Cancer 2012;48: 1318-1325.
11. Watts K, Li J, Magi-Galluzzi C, et al. Incidence and clinicopathological characteristics of intraductal carcinoma of the prostate detected in prostate biopsies: a prospective cohort study. Mod Pathol 2012;25:250A.
12. Herawi M, Epstein JI. Immunohistochemical antibody cocktail staining (p63/HMWCK/AMACR) of ductal adenocarcinoma and gleason pattern 4 cribriform and noncribriform acinar adenocarcinomas of the prostate. Am J Surg Pathol 2007;31:889-894. (Pubitemid 47165142)
13. Dawkins HJ, Sellner LN, Turbett GR, et al. Distinction between intraductal carcinoma of the prostate (IDC-P), high-grade dysplasia (PIN), and invasive prostatic adenocarcinoma, using molecular markers of cancer progression. Prostate 2000;44:265-270.
14. Bettendorf O, Schmidt H, Staebler A, et al. Chromosomal imbalances, loss of heterozygosity, and immunohistochemical expression of TP53, RB1, and PTEN in intraductal cancer, intraepithelial neoplasia, and invasive adenocarcinoma of the prostate. Genes Chromosomes Cancer 2008;47:565-572. (Pubitemid 351748343)
15. 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.
16. Tomlins SA, Rhodes DR, Perner S, et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 2005;310:644-648. (Pubitemid 41528150)
17. Tu JJ, Rohan S, Kao J, et al. Gene fusions between TMPRSS2 and ETS family genes in prostate cancer: frequency and transcript variant analysis by RT-PCR and FISH on paraffin-embedded tissues. Mod Pathol 2007;20:921-928. (Pubitemid 47267823)
18. Perner S, Demichelis F, Beroukhim R, et al. TMPRSS2:ERG fusion-associated deletions provide insight into the heterogeneity of prostate cancer. Cancer Res 2006;66:8337-8341. (Pubitemid 44449140)
19. Attard G, Clark J, Ambroisine L, et al. Transatlantic Prostate Group. Duplication of the fusion of TMPRSS2 to ERG sequences identifies fatal human prostate cancer. Oncogene 2008;27:253-263.
20. Demichelis F, Fall K, Perner S, et al. TMPRSS2:ERG gene fusion associated with lethal prostate cancer in a watchful waiting cohort. Oncogene 2007;26:4596-4599. (Pubitemid 47037039)
21. Fine SW, Gopalan A, Al-Ahmadie HA, et al. Does TMPRSS2-ERG gene fusion status in prostate cancer correlate with gleason score? Mod Pathol 2008;21:156A.
22. Fine SW, Gopalan A, Leversha MA, et al. TMPRSS2-ERG gene fusion is associated with low gleason scores and not with high-grade morphological features. Mod Pathol 2010;23:1325-1333.
23. Gopalan A, Leversha MA, Satagopan JM, et al. TMPRSS2-ERG gene fusion is not associated with outcome in patients treated by prostatectomy. Cancer Res 2009;69:1400-1406.
24. Toubaji A, Albadine R, Meeker AK, et al. Increased gene copy number of ERG on chromosome 21 but not TMPRSS2-ERG fusion predicts outcome in prostatic adenocarcinomas. Mod Pathol 2011;24:1511-1520.
25. Cairns P, Okami K, Halachmi S, et al. Frequent inactivation of PTEN/MMAC1 in primary prostate cancer. Cancer Res 1997;57:4997-5000. (Pubitemid 27498107)
26. Li J, Yen C, Liaw D, et al. PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 1997;275: 1943-1947. (Pubitemid 27148818)
27. Steck PA, MA Pershouse, Jasser SA, et al. Identification of a candidate tumour suppressor gene, MMAC1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nat Genet 1997;15:356-362. (Pubitemid 27147102)
28. Teng DH, Hu R, Lin H, et al. MMAC1/PTEN mutations in primary tumor specimens and tumor cell lines. Cancer Res 1997;57:5221-5225. (Pubitemid 27516352)
29. Feilotter HE, Nagai MA, Boag AH, et al. Analysis of PTEN and the 10q23 region in primary prostate carcinomas. Oncogene 1998;16:1743-1748. (Pubitemid 28175055)
30. Pesche S, Latil A, Muzeau F, et al. PTEN/MMAC1/TEP1 involvement in primary prostate cancers Oncogene 1998;16:2879-2883. (Pubitemid 28383272)
31. Wang SI, Parsons R, Ittmann M. Homozygous deletion of the PTEN tumor suppressor gene in a subset of prostate adenocarcinomas. Clin Cancer Res 1998;4:811-815. (Pubitemid 28193582)
32. Verhagen PC, van Duijn PW, Hermans KG, et al. The PTEN gene in locally progressive prostate cancer is preferentially inactivated by bi-allelic gene deletion. J Pathol 2006;208:699-707.
33. Yoshimoto M, Cutz JC, Nuin PA, et al. Interphase FISH analysis of PTEN in histologic sections shows genomic deletions in 68% of primary prostate cancer and 23% of high-grade prostatic intra-epithelial neoplasias. Cancer Genet Cytogenet 2006;169:128-137. (Pubitemid 44287105)
34. Yoshimoto M, Cunha IW, Coudry RA, et al. FISH analysis of 107 prostate cancers shows that PTEN genomic deletion is associated with poor clinical outcome. Br J Cancer 2007;97:678-685. (Pubitemid 47339893)
35. 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.
36. Mosquera JM, 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.
37. Zhang S, Pavlovitz B, Tull J, et al. Detection of TMPRSS2 gene deletions and translocations in carcinoma, intraepithelial neoplasia, and normal epithelium of the prostate by direct fluorescence in situ hybridization. Diagn Mol Pathol 2010;19: 151-156.
38. Yaskiv O, Zhang X, Simmerman K, et al. The utility of ERG/P63 double immunohistochemical staining in the diagnosis of limited cancer in prostate needle biopsies. Am J Surg Pathol 2011;35:1062-1068.
39. Furusato B, Tan SH, 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.
40. Park K, Tomlins SA, Mudaliar KM, et al. Antibody-based detection of ERG rearrangement-positive prostate cancer. Neoplasia 2010;12:590-598.
41. Sangale Z, Prass C, Carlson A, et al. A robust immunohistochemical assay for detecting PTEN expression in human tumors. Appl Immunohistochem Mol Morphol 2011;19:173-183.
42. Chaux A, Albadine R, Toubaji A, et al. Immunohis-tochemistry for ERG expression as a surrogate for TMPRSS2-ERG fusion detection in prostatic adenocar-cinomas. Am J Surg Pathol 2011;35:1014-1020.
43. Kibel AS, Rosenbaum E, Kattan MW, et al. Adjuvant weekly docetaxel for patients with high risk prostate cancer after radical prostatectomy: a multi-institutional pilot study. J Urol 2007;177:1777-1781. (Pubitemid 46560677)
44. McNeal JE, Yemoto CE. Spread of adenocarcinoma within prostatic ducts and acini. morphologic and clinical correlations. Am J Surg Pathol 1996;20:802-814. (Pubitemid 26230743)
45. King JC, Xu J, Wongvipat J, et al. Cooperativity of TMPRSS2-ERG with PI3-kinase pathway activation in prostate oncogenesis. Nat Genet 2009;41:524-526.
46. Carver BS, Tran J, Gopalan A, et al. Aberrant ERG expression cooperates with loss of PTEN to promote cancer progression in the prostate. Nat Genet 2009;41:619-624.
47. 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.
48. 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.
49. Sircar K, Yoshimoto M, Monzon FA, et al. PTEN genomic deletion is associated with p-akt and AR signalling in poorer outcome, hormone refractory prostate cancer. J Pathol 2009;218:505-513.
50. 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;21:1451-1460.
51. 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; advance online publication.
52. Epstein JI, Herawi M. Prostate needle biopsies containing prostatic intraepithelial neoplasia or atypical foci suspicious for carcinoma: implications for patient care. J Urol 2006;175:820-834. (Pubitemid 43199991)
53. Shen WH, Balajee AS, Wang J, et al. Essential role for nuclear PTEN in maintaining chromosomal integrity. Cell 2007;128:157-170. (Pubitemid 46048887)
54. Denning G, Jean-Joseph B, Prince C, et al. A short N-terminal sequence of PTEN controls cytoplasmic localization and is required for suppression of cell growth. Oncogene 2007;26:3930-3940. (Pubitemid 46884301)
55. Lobo GP, Waite KA, Planchon SM, et al. ATP modulates PTEN subcellular localization in multiple cancer cell lines. Hum Mol Genet 2008;17:2877-2885.