Genomic rearrangements of PTEN in prostate cancer

Frontiers in Oncology

Volumn 3 SEP, Issue , 2013, Pages

  Phin, Sopheap ^a   Moore, Mathew W ^a   Cotter, Philip D ^a,b  

^a Genetics   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Fluorescence in situ hybridization; Genomic rearrangements; Prostate cancer; PTEN

Indexed keywords

ANDROGEN RECEPTOR; ENZALUTAMIDE; EPIDERMAL GROWTH FACTOR RECEPTOR; FAS ANTIGEN; MAMMALIAN TARGET OF RAPAMYCIN; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3, 4, 5 TRISPHOSPHATE 3 PHOSPHATASE; PLATELET DERIVED GROWTH FACTOR RECEPTOR; PROTEIN KINASE B; SOMATOMEDIN RECEPTOR; STEROID RECEPTOR; TRANSCRIPTION FACTOR ERG; UNCLASSIFIED DRUG;

ARTICLE; CARCINOGENESIS; CHROMOSOME10; CIRCULATING TUMOR CELL; COMPARATIVE GENOMIC HYBRIDIZATION; COPY NUMBER VARIATION; DNA REPAIR; DNA REPLICATION; FLUORESCENCE IN SITU HYBRIDIZATION; GENE DELETION; GENE DOSAGE; GENE REARRANGEMENT; GENE SILENCING; HUMAN; METHYLATION; NONHUMAN; POINT MUTATION; PROSTATE CANCER; TUMOR GROWTH;

EID: 84891052481     PISSN: None     EISSN: 2234943X     Source Type: Journal    
DOI: 10.3389/fonc.2013.00240     Document Type: Article

References (82)

1. Siegel R, Naishadham D, Jemal A. Cancer statistics, 2012. Cancer J Clin (2012) 62:10-29. doi:10.3322/caac.21149 OPMID
2. Beltran H, Yelensky R, Frampton GM, Park K, Downing SR, Macdonald TY, et al. Targeted next-generation sequencing of advanced prostate cancer identifies potential therapeutic targets and disease heterogeneity. Eur Urol (2012) 63(5):920-6. doi:10.1016/j.eururo.2012.08.053
3. Lu-Yao GL, Albertsen PC, Moore DF, Shih W, Lin Y, DiPaola RS, et al. Survival following primary androgen deprivation therapy among men with localized prostate cancer. JAMA (2008) 300:173-81. doi:10.1001/jama.300.2.173
4. Lu-Yao GL, Albertsen PC, Stanford JL, Stukel TA, Walker-Corkery E, Barry MJ. Screening, treatment, and prostate cancer mortality in the Seattle area and Connecticut: fifteen-year follow-up. J Gen Intern Med (2008) 23:1809-14. doi:10.1007/s11606-008-0785-8
5. Pomerantz M, Kantoff P. Advances in the treatment of prostate cancer. Annu Rev Med (2007) 58:205-20. doi:10.1146/annurev.med.58.101505.115650
6. De Velasco MA, Uemura H. Preclinical remodeling of human prostate cancer through the PTEN/AKT pathway. Adv Urol (2012) 2012:419348. doi:10.1155/2012/419348
7. Suzuki H, Freije D, Nusskern DR, Okami K, Cairns P, Sidransky D, et al. Interfocal heterogeneity of PTEN/MMAC1 gene alterations in multiple metastatic prostate cancer tissues. Cancer Res (1998) 58:204-9.
8. Yoshimoto M, Cunha IW, Coudry RA, Fonseca FP, Torres CH, Soares FA, et al. FISH analysis of 107 prostate cancers shows that PTEN genomic deletion is associated with poor clinical outcome. Br J Cancer (2007) 97:678-85. doi:10.1038/sj.bjc.6603924
9. Feldman BJ, Feldman D. The development of androgen-independent prostate cancer. Nat Rev Cancer (2001) 1:34-45. doi:10.1038/35094009
10. Chia JY, Gajewski JE, Xiao Y, Zhu HJ, Cheng HC. Unique biochemical properties of the protein tyrosine phosphatase activity of PTEN-demonstration of different active site structural requirements for phosphopeptide and phospholipid phosphatase activities of PTEN. Biochim Biophys Acta (2010) 1804:1785-95. doi:10.1016/j.bbapap.2010.05.009
11. Paramio JM, Navarro M, Segrelles C, Gomez-Casero E, Jorcano JL. PTEN tumour suppressor is linked to the cell cycle control through the retinoblastoma protein. Oncogene (1999) 18:7462-8. doi:10.1038/sj.onc.1203151
12. Radu A, Neubauer V, Akagi T, Hanafusa H, Georgescu MM. PTEN induces cell cycle arrest by decreasing the level and nuclear localization of cyclin D1. Mol Cell Biol (2003) 23:6139-49. doi:10.1128/MCB.23.17.6139-6149.2003
13. Carnero A, Blanco-Aparicio C, Renner O, Link W, Leal JF. The PTEN/PI3K/AKT signalling pathway in cancer, therapeutic implications. Curr Cancer Drug Targets (2008) 8:187-98. doi:10.2174/156800908784293659
14. Kwabi-Addo B, Giri D, Schmidt K, Podsypanina K, Parsons R, Greenberg N, et al. Haploinsufficiency of the Pten tumor suppressor gene promotes prostate cancer progression. Proc Natl Acad Sci U S A (2001) 98:11563-8. doi:10.1073/pnas.201167798
15. Dong JT. Prevalent mutations in prostate cancer. J Cell Biochem (2006) 97:433-47. doi:10.1002/jcb.20696
16. Konishi N, Nakamura M, Kishi M, Nishimine M, Ishida E, Shimada K. Heterogeneous methylation and deletion patterns of the INK4a/ARF locus within prostate carcinomas. Am J Pathol (2002) 160:1207-14. doi:10.1016/S0002-9440(10)62547-3
17. Whang YE, Wu X, Suzuki H, Reiter RE, Tran C, Vessella RL, et al. Inactivation of the tumor suppressor PTEN/MMAC1 in advanced human prostate cancer through loss of expression. Proc Natl Acad Sci U S A (1998) 95:5246-50. doi:10.1073/pnas.95.9.5246
18. Yoshimoto M, Joshua AM, Cunha IW, Coudry RA, Fonseca FP, Ludkovski O, 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. doi:10.1038/modpathol.2008.96
19. Poliseno L, Salmena L, Riccardi L, Fornari A, Song MS, Hobbs RM, et al. Identification of the miR-106b ~25 microRNA cluster as a proto-oncogenic PTEN-targeting intron that cooperates with its host gene MCM7 in transformation. Sci Signal (2010) 3:ra29. doi:10.1126/scisignal.2000594
20. Tay Y, Kats L, Salmena L, Weiss D, Tan SM, Ala U, et al. Coding-independent regulation of the tumor suppressor PTEN by competing endogenous mRNAs. Cell (2011) 147:344-57. doi:10.1016/j.cell.2011.09.029
21. Singh G, Chan AM. Post-translational modifications of PTEN and their potential therapeutic implications. Curr Cancer Drug Targets (2011) 11:536-47. doi:10.2174/156800911795655930
22. Wang X, Jiang X. Post-translational regulation of PTEN. Oncogene (2008) 27:5454-63. doi:10.1038/onc.2008.242
23. Yoshimoto M, Cutz JC, Nuin PA, Joshua AM, Bayani J, Evans AJ, 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) 169:128-37. doi:10.1016/j.cancergencyto.2006.04.003
24. Bismar TA, Yoshimoto M, Vollmer RT, Duan Q, Firszt M, Corcos J, et al. PTEN genomic deletion is an early event associated with ERG gene rearrangements in prostate cancer. BJU Int (2011) 107:477-85. doi:10.1111/j.1464-410X.2010.09470.x
25. Han B, Mehra R, Lonigro RJ, Wang L, Suleman K, Menon A, et al. Fluorescence in situ hybridization study shows association of PTEN deletion with ERG rearrangement during prostate cancer progression. Mod Pathol (2009) 22:1083-93. doi:10.1038/modpathol.2009.69
26. Sircar K, Yoshimoto M, Monzon FA, Koumakpayi IH, Katz RL, Khanna A, et al. PTEN genomic deletion is associated with p-Akt and AR signalling in poorer outcome, hormone refractory prostate cancer. J Pathol (2009) 218:505-13. doi:10.1002/path.2559
27. Squire JA. TMPRSS2-ERG and PTEN loss in prostate cancer. Nat Genet (2009) 41:509-10. doi:10.1038/ng0509-509
28. Zordan A. Fluorescence in situ hybridization on formalin-fixed, paraffin-embedded tissue sections. Methods Mol Biol (2011) 730:189-202. doi:10.1007/978-1-61779-074-4_14
29. Yoshimoto M, Ludkovski O, DeGrace D, Williams JL, Evans A, Sircar K, et al. PTEN genomic deletions that characterize aggressive prostate cancer originate close to segmental duplications. Genes Chromosomes Cancer (2012) 51:149-60. doi:10.1002/gcc.20939
30. Zhe X, Cher ML, Bonfil RD. Circulating tumor cells: finding the needle in the haystack. Am J Cancer Res (2011) 1:740-51.
31. Grasso YZ, Gupta MK, Levin HS, Zippe CD, Klein EA. Combined nested RT-PCR assay for prostate-specific antigen and prostate-specific membrane antigen in prostate cancer patients: correlation with pathological stage. Cancer Res (1998) 58:1456-9.
32. Kantoff PW, Halabi S, Farmer DA, Hayes DF, Vogelzang NA, Small EJ. Prognostic significance of reverse transcriptase polymerase chain reaction for prostate-specific antigen in men with hormone-refractory prostate cancer. J Clin Oncol (2001) 19:3025-8.
33. Schmidt H, DeAngelis G, Eltze E, Gockel I, Semjonow A, Brandt B. Asynchronous growth of prostate cancer is reflected by circulating tumor cells delivered from distinct, even small foci, harboring loss of heterozygosity of the PTEN gene. Cancer Res (2006) 66:8959-65. doi:10.1158/0008-5472.CAN-06-1722
34. Attard G, Swennenhuis JF, Olmos D, Reid AH, Vickers E, A'Hern R, et al. Characterization of ERG, AR and PTEN gene status in circulating tumor cells from patients with castration-resistant prostate cancer. Cancer Res (2009) 69:2912-8. doi:10.1158/0008-5472.CAN-08-3667
35. Thalgott M, Rack B, Maurer T, Souvatzoglou M, Eiber M, Kress V, et al. Detection of circulating tumor cells in different stages of prostate cancer. J Cancer Res Clin Oncol (2013) 139(5):755-63. doi:10.1007/s00432-013-1377-5
36. Yoshimoto M, Ding K, Sweet JM, Ludkovski O, Trottier G, Song KS, et al. PTEN losses exhibit heterogeneity in multifocal prostatic adenocarcinoma and are associated with higher Gleason grade. Mod Pathol (2012) 26(3):435-47. doi:10.1038/modpathol.2012.162
37. Bismar TA, Yoshimoto M, Duan Q, Liu S, Sircar K, Squire JA. Interactions and relationships of PTEN, ERG, SPINK1 and AR in castration-resistant prostate cancer. Histopathology (2012) 60:645-52. doi:10.1111/j.1365-2559.2011.04116.x
38. King JC, Xu J, Wongvipat J, Hieronymus H, Carver BS, Leung DH, et al. Cooperativity of TMPRSS2-ERG with PI3-kinase pathway activation in prostate oncogenesis. Nat Genet (2009) 41:524-6. doi:10.1038/ng.371
39. Carver BS, Tran J, Gopalan A, Chen Z, Shaikh S, Carracedo A, et al. Aberrant ERG expression cooperates with loss of PTEN to promote cancer progression in the prostate. Nat Genet (2009) 41:619-24. doi:10.1038/ng.370
40. Krohn A, Diedler T, Burkhardt L, Mayer PS, De Silva C, Meyer-Kornblum M, et al. Genomic deletion of PTEN is associated with tumor progression and early PSA recurrence in ERG fusion-positive and fusion-negative prostate cancer. Am J Pathol (2012) 181:401-12. doi:10.1016/j.ajpath.2012.04.026
41. Choucair K, Ejdelman J, Brimo F, Aprikian A, Chevalier S, Lapointe J. PTEN genomic deletion predicts prostate cancer recurrence and is associated with low AR expression and transcriptional activity. BMC Cancer (2012) 12:543. doi:10.1186/1471-2407-12-543
42. El Sheikh SS, Romanska HM, Abel P, Domin J, Lalani el-N. Predictive value of PTEN and AR coexpression of sustained responsiveness to hormonal therapy in prostate cancer-a pilot study. Neoplasia (2008) 10:949-53.
43. Visakorpi T, Hyytinen E, Koivisto P, Tanner M, Keinanen R, Palmberg C, et al. In vivo amplification of the androgen receptor gene and progression of human prostate cancer. Nat Genet (1995) 9:401-6. doi:10.1038/ng0495-401
44. Yuan X, Balk SP. Mechanisms mediating androgen receptor reactivation after castration. Urol Oncol (2009) 27:36-41. doi:10.1016/j.urolonc.2008.03.021
45. Burnstein KL. Regulation of androgen receptor levels: implications for prostate cancer progression and therapy. J Cell Biochem (2005) 95:657-69. doi:10.1002/jcb.20460
46. Knuutila S, Bjorkqvist AM, Autio K, Tarkkanen M, Wolf M, Monni O, et al. DNA copy number amplifications in human neoplasms: review of comparative genomic hybridization studies. Am J Pathol (1998) 152:1107-23.
47. Jenkins RB, Qian J, Lieber MM, Bostwick DG. Detection of c-myc oncogene amplification and chromosomal anomalies in metastatic prostatic carcinoma by fluorescence in situ hybridization. Cancer Res (1997) 57:524-31.
48. Zafarana G, Ishkanian AS, Malloff CA, Locke JA, Sykes J, Thoms J, et al. Copy number alterations of c-MYC and PTEN are prognostic factors for relapse after prostate cancer radiotherapy. Cancer (2012) 118:4053-62. doi:10.1002/cncr.26729
49. Cairns P, Okami K, Halachmi S, Halachmi N, Esteller M, Herman JG, et al. Frequent inactivation of PTEN/MMAC1 in primary prostate cancer. Cancer Res (1997) 57:4997-5000.
50. Dong JT, Sipe TW, Hyytinen ER, Li CL, Heise C, McClintock DE, et al. PTEN/MMAC1 is infrequently mutated in pT2 and pT3 carcinomas of the prostate. Oncogene (1998) 17:1979-82. doi:10.1038/sj.onc.1202119
51. Feilotter HE, Nagai MA, Boag AH, Eng C, Mulligan LM. Analysis of PTEN and the 10q23 region in primary prostate carcinomas. Oncogene (1998) 16:1743-8. doi:10.1038/sj.onc.1200205
52. Orikasa K, Fukushige S, Hoshi S, Orikasa S, Kondo K, Miyoshi Y, et al. Infrequent genetic alterations of the PTEN gene in Japanese patients with sporadic prostate cancer. J Hum Genet (1998) 43:228-30. doi:10.1007/s100380050078
53. Wang SI, Parsons R, Ittmann M. Homozygous deletion of the PTEN tumor suppressor gene in a subset of prostate adenocarcinomas. Clin Cancer Res (1998) 4:811-5.
54. Vlietstra RJ, van Alewijk DC, Hermans KG, van Steenbrugge GJ, Trapman J. Frequent inactivation of PTEN in prostate cancer cell lines and xenografts. Cancer Res (1998) 58:2720-3.
55. Dong JT, Li CL, Sipe TW, Frierson HF Jr. Mutations of PTEN/MMAC1 in primary prostate cancers from Chinese patients. Clin Cancer Res (2001) 7:304-8.
56. Robbins CM, Tembe WA, Baker A, Sinari S, Moses TY, Beckstrom-Sternberg S, et al. Copy number and targeted mutational analysis reveals novel somatic events in metastatic prostate tumors. Genome Res (2011) 21:47-55. doi:10.1101/gr.107961.110
57. Kovtun IV, Cheville JC, Murphy SJ, Johnson SH, Zarei S, Kosari F, et al. Lineage relationship of Gleason patterns in Gleason score 7 prostate cancer. Cancer Res (2013) 73:3275-84. doi:10.1158/0008-5472.CAN-12-2803
58. Ongenaert M, Van Neste L, De Meyer T, Menschaert G, Bekaert S, Van Criekinge W. PubMeth: a cancer methylation database combining text-mining and expert annotation. Nucleic Acids Res (2008) 36:D842-6. doi:10.1093/nar/gkm788
59. Kang GH, Lee S, Lee HJ, Hwang KS. Aberrant CpG island hypermethylation of multiple genes in prostate cancer and prostatic intraepithelial neoplasia. J Pathol (2004) 202:233-40. doi:10.1002/path.1503
60. Roupret M, Hupertan V, Yates DR, Catto JW, Rehman I, Meuth M, et al. Molecular detection of localized prostate cancer using quantitative methylation-specific PCR on urinary cells obtained following prostate massage. Clin Cancer Res (2007) 13:1720-5. doi:10.1158/1078-0432.CCR-06-2467
61. Yamanaka M, Watanabe M, Yamada Y, Takagi A, Murata T, Takahashi H, et al. Altered methylation of multiple genes in carcinogenesis of the prostate. Int J Cancer (2003) 106:382-7. doi:10.1002/ijc.11227
62. Chin SP, Dickinson JL, Holloway AF. Epigenetic regulation of prostate cancer. Clin Epigenetics (2011) 2:151-69. doi:10.1007/s13148-011-0041-7
63. De Muga S, Hernandez S, Agell L, Salido M, Juanpere N, Lorenzo M, et al. Molecular alterations of EGFR and PTEN in prostate cancer: association with high-grade and advanced-stage carcinomas. Mod pathol (2010) 23:703-12. doi:10.1038/modpathol.2010.45
64. Majumder PK, Sellers WR. Akt-regulated pathways in prostate cancer. Oncogene (2005) 24:7465-74. doi:10.1038/sj.onc.1209096
65. Zhang W, Zhu J, Efferson CL, Ware C, Tammam J, Angagaw M, et al. Inhibition of tumor growth progression by antiandrogens and mTOR inhibitor in a Pten-deficient mouse model of prostate cancer. Cancer Res (2009) 69:7466-72. doi:10.1158/0008-5472.CAN-08-4385
66. Fagone P, Donia M, Mangano K, Quattrocchi C, Mammana S, Coco M, et al. Comparative study of rapamycin and temsirolimus demonstrates superimposable anti-tumour potency on prostate cancer cells. Basic Clin Pharmacol Toxicol (2013) 112:63-9. doi:10.1111/j.1742-7843.2012.00923.x
67. Neshat MS, Mellinghoff IK, Tran C, Stiles B, Thomas G, Petersen R, et al. Enhanced sensitivity of PTEN-deficient tumors to inhibition of FRAP/mTOR. Proc Natl Acad Sci U S A (2001) 98:10314-9. doi:10.1073/pnas.171076798
68. Rivera VM, Squillace RM, Miller D, Berk L, Wardwell SD, Ning Y, et al. Ridaforolimus (AP23573; MK-8669), a potent mTOR inhibitor, has broad antitumor activity and can be optimally administered using intermittent dosing regimens. Mol Cancer Ther (2011) 10:1059-71. doi:10.1158/1535-7163.MCT-10-0792
69. Hirai H, Sootome H, Nakatsuru Y, Miyama K, Taguchi S, Tsujioka K, et al. MK-2206, an allosteric Akt inhibitor, enhances antitumor efficacy by standard chemotherapeutic agents or molecular targeted drugs in vitro and in vivo. Mol Cancer Ther (2010) 9:1956-67. doi:10.1158/1535-7163.MCT-09-1012
70. Zhang W, Haines BB, Efferson C, Zhu J, Ware C, Kunii K, et al. Evidence of mTOR activation by an AKT-independent mechanism provides support for the combined treatment of PTEN-deficient prostate tumors with mTOR and AKT inhibitors. Transl Oncol (2012) 5:422-9.
71. Templeton AJ, Dutoit V, Cathomas R, Rothermundt C, Bartschi D, Droge C, et al. Phase 2 trial of single-agent everolimus in chemotherapy-naive patients with castration-resistant prostate cancer (SAKK 08/08). Eur Urol (2013) 64:150-8. doi:10.1016/j.eururo.2013.03.040
72. Wu L, Birle DC, Tannock IF. Effects of the mammalian target of rapamycin inhibitor CCI-779 used alone or with chemotherapy on human prostate cancer cells and xenografts. Cancer Res (2005) 65:2825-31. doi:10.1158/0008-5472.CAN-04-3137
73. Cao C, Subhawong T, Albert JM, Kim KW, Geng L, Sekhar KR, et al. Inhibition of mammalian target of rapamycin or apoptotic pathway induces autophagy and radiosensitizes PTEN null prostate cancer cells. Cancer Res (2006) 66:10040-7. doi:10.1158/0008-5472.CAN-06-0802
74. Cao F, Jin TY, Zhou YF. Inhibitory effect of isoflavones on prostate cancer cells and PTEN gene. Biomed Environ Sci (2006) 19:35-41.
75. Chen Y, Sawyers CL, Scher HI. Targeting the androgen receptor pathway in prostate cancer. Curr Opin Pharmacol (2008) 8:440-8. doi:10.1016/j.coph.2008.07.005
76. El-Amm J, Aragon-Ching JB. The changing landscape in the treatment of metastatic castration-resistant prostate cancer. Ther Adv Med Oncol (2013) 5:25-40. doi:10.1177/1758834012458137
77. Fradet Y. Bicalutamide (Casodex) in the treatment of prostate cancer. Expert Rev Anticancer Ther (2004) 4:37-48. doi:10.1586/14737140.4.1.37
78. Carver BS, Chapinski C, Wongvipat J, Hieronymus H, Chen Y, Chandarlapaty S, et al. Reciprocal feedback regulation of PI3K and androgen receptor signaling in PTEN-deficient prostate cancer. Cancer Cell (2011) 19:575-86. doi:10.1016/j.ccr.2011.04.008
79. Cinar B, De Benedetti A, Freeman MR. Post-transcriptional regulation of the androgen receptor by mammalian target of rapamycin. Cancer Res (2005) 65:2547-53. doi:10.1158/0008-5472.CAN-04-3411
80. Wang Y, Mikhailova M, Bose S, Pan CX, deVere White RW, Ghosh PM. Regulation of androgen receptor transcriptional activity by rapamycin in prostate cancer cell proliferation and survival. Oncogene (2008) 27:7106-17. doi:10.1038/onc.2008.318
81. Xu Y, Chen SY, Ross KN, Balk SP. Androgens induce prostate cancer cell proliferation through mammalian target of rapamycin activation and post-transcriptional increases in cyclin D proteins. Cancer Res (2006) 66:7783-92. doi:10.1158/0008-5472.CAN-05-4472
82. Squillace RM, Miller D, Wardwell SD, Wang F, Clackson T, Rivera VM. Synergistic activity of the mTOR inhibitor ridaforolimus and the antiandrogen bicalutamide in prostate cancer models. Int J Oncol (2012) 41:425-32. doi:10.3892/ijo.2012.1487