Biology of urothelial tumorigenesis: Insights from genetically engineered mice

Cancer and Metastasis Reviews

Volumn 28, Issue 3-4, 2009, Pages 281-290

  Wu, Xue Ru ^a,b  

^a NEW YORK UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b VETERANS AFFAIRS MEDICAL CENTER   (United States)

Author keywords

Bladder cancer; Cellular context; Knockout; Transgenic; Tumorigenesis; Urothelium

Indexed keywords

ANTINEOPLASTIC AGENT; FIBROBLAST GROWTH FACTOR RECEPTOR 3; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN P107; PROTEIN P53; PROTEIN TYROSINE KINASE; RETINOBLASTOMA PROTEIN;

CANCER GROWTH; CANCER INVASION; CARCINOGENESIS; ENZYME ACTIVATION; GENE EXPRESSION; HUMAN; NONHUMAN; ONCOGENE H RAS; PRIORITY JOURNAL; PROTEIN DEFICIENCY; REVIEW; UROGENITAL TRACT TUMOR; UROTHELIUM;

ANIMALS; CARCINOMA, TRANSITIONAL CELL; CELL TRANSFORMATION, NEOPLASTIC; GENES, P53; GENES, RAS; GENES, RETINOBLASTOMA; GENETIC ENGINEERING; HUMANS; HYPERPLASIA; MICE; MICE, KNOCKOUT; MICE, TRANSGENIC; NEOPLASM INVASIVENESS; PRECANCEROUS CONDITIONS; PTEN PHOSPHOHYDROLASE; RECEPTOR PROTEIN-TYROSINE KINASES; RETINOBLASTOMA-LIKE PROTEIN P107; UROLOGIC NEOPLASMS; UROTHELIUM;

EID: 76649100093     PISSN: 01677659     EISSN: None     Source Type: Journal    
DOI: 10.1007/s10555-009-9189-4     Document Type: Review

References (109)

1. D Hanahan RA Weinberg 2000 The hallmarks of cancer Cell 100 57 70 1:CAS:528:DC%2BD3cXks1CktA%3D%3D 10647931
2. PA Jones SB Baylin 2007 The epigenomics of cancer Cell 128 683 692 1:CAS:528:DC%2BD2sXis12ju7k%3D 17320506
3. MR Stratton PJ Campbell PA Futreal 2009 The cancer genome Nature 458 719 724 1:CAS:528:DC%2BD1MXksVehtb8%3D 19360079
4. KW Hunter 2006 Context-dependent cancer risk Nature Genetics 38 864 865 1:CAS:528:DC%2BD28XnsVChurk%3D 16874325
5. KW Kinzler B Vogelstein 1996 Lessons from hereditary colorectal cancer Cell 87 159 170 1:CAS:528:DyaK28XmsVGhs7g%3D 8861899
6. I Nathke 2006 Cytoskeleton out of the cupboard: Colon cancer and cytoskeletal changes induced by loss of APC Nature Reviews Cancer 6 967 974 17093505
7. A de la Chapelle 2004 Genetic predisposition to colorectal cancer Nature Reviews Cancer 4 769 780 15510158
8. WM Linehan B Zbar 2004 Focus on kidney cancer Cancer Cell 6 223 228 1:CAS:528:DC%2BD2cXot1Kis7o%3D 15380513
9. WY Kim WG Kaelin 2004 Role of VHL gene mutation in human cancer Journal of Clinical Oncology 22 4991 5004 1:CAS:528:DC%2BD2MXptVWrsw%3D%3D 15611513
10. D Malkin 1994 Germline p53 mutations and heritable cancer Annual Review of Genetics 28 443 465 1:CAS:528:DyaK2MXislWlsr8%3D 7893135
11. FP Li JF Fraumeni Jr JJ Mulvihill WA Blattner MG Dreyfus MA Tucker, et al. 1988 A cancer family syndrome in twenty-four kindreds Cancer Research 48 5358 5362 1:STN:280:DyaL1czhtV2htg%3D%3D 3409256
12. Y Aoki T Niihori H Kawame K Kurosawa H Ohashi Y Tanaka, et al. 2005 Germline mutations in HRAS proto-oncogene cause Costello syndrome Nature Genetics 37 1038 1040 1:CAS:528:DC%2BD2MXhtVCntL%2FP 16170316
13. KW Gripp 2005 Tumor predisposition in Costello syndrome American Journal of Medical Genetics. Part C, Seminars in Medical Genetics 137 72 77
14. LA Donehower M Harvey BL Slagle MJ McArthur CA Montgomery Jr JS Butel, et al. 1992 Mice deficient for p53 are developmentally normal but susceptible to spontaneous tumours Nature 356 215 221 1:CAS:528:DyaK38XitFajsLc%3D 1552940
15. FM Watt M Frye SA Benitah 2008 MYC in mammalian epidermis: how can an oncogene stimulate differentiation? Nature Review Cancer 8 234 242 1:CAS:528:DC%2BD1cXitlOjurg%3D
16. D Ahuja MT Saenz-Robles JM Pipas 2005 SV40 large T antigen targets multiple cellular pathways to elicit cellular transformation Oncogene 24 7729 7745 1:CAS:528:DC%2BD2MXht1aqsrvN 16299533
17. M Rassoulzadegan F Cuzin 1987 "Sub-threshold neoplastic states" created in transgenic mice Oncogene Research 1 1 6 1:CAS:528:DyaL1MXltFaqs78%3D 2835726
18. N Ghebranious LA Donehower 1998 Mouse models in tumor suppression Oncogene 17 3385 3400 9917000
19. Wu, X.-R., Sun, T.-T., McConkey, D. J., Shrader, M., & Papageorgiou, A. (2006). Animal models of bladder cancer. In S. P. Lerner, M. P. Schoenberg & C. N. Sternberg (Eds.), Textbook of bladder cancer (pp. 157-169). Boca Raton: Taylor & Francis.
20. CP Dinney DJ McConkey RE Millikan X Wu M Bar-Eli L Adam, et al. 2004 Focus on bladder cancer Cancer Cell 6 111 116 1:CAS:528:DC%2BD2cXns1arsr4%3D 15324694
21. SM Cohen 2002 Comparative pathology of proliferative lesions of the urinary bladder Toxicologic Pathology 30 663 671 1:CAS:528:DC%2BD38XovVCqt7g%3D 12512866
22. XR Wu XP Kong A Pellicer G Kreibich TT Sun 2009 Uroplakins in urothelial biology, function, and disease Kidney International 75 1153 1165 1:CAS:528:DC%2BD1MXlvV2htL8%3D 19340092
23. TT Sun 2006 Altered phenotype of cultured urothelial and other stratified epithelial cells: implications for wound healing American Journal of Physiology and Renal Physiology 291 F9 F21 1:CAS:528:DC%2BD28XntFGgsr0%3D
24. Khandelwal, P., Abraham, S. N., & Apodaca, G. (2009). Cell biology and physiology of the uroepithelium. American Journal of Physiology and Renal Physiology (in press)
25. SA Lewis 2000 Everything you wanted to know about the bladder epithelium but were afraid to ask American Journal of Physiology and Renal Physiology 278 F867 F874 1:CAS:528:DC%2BD3cXks1ymtL0%3D
26. HO Negrete JP Lavelle J Berg SA Lewis ML Zeidel 1996 Permeability properties of the intact mammalian bladder epithelium American Journal of Physiology 271 F886 F894 1:CAS:528:DyaK28Xms1OnsbY%3D 8898019
27. RM Hicks 1975 The mammalian urinary bladder: An accommodating organ Biological Reviews of the Cambridge Philosophical Society 50 215 246 1:STN:280:DyaE28%2FhvFeisA%3D%3D 1100129
28. RE Walker 1960 Renewal of cell populations in the female mouse American Journal of Anatomy 102 95 100
29. EA Kurzrock DK Lieu LA Degraffenried CW Chan RR Isseroff 2008 Label-retaining cells of the bladder: candidate urothelial stem cells American Journal of Physiology and Renal Physiology 294 F1415 F1421 1:CAS:528: DC%2BD1cXnsVartro%3D
30. NH Chow HS Liu HB Yang SH Chan IJ Su 1997 Expression patterns of erbB receptor family in normal urothelium and transitional cell carcinoma. An immunohistochemical study Virchows Archiv 430 461 466 1:STN:280: DyaK2sznsVClsA%3D%3D 9230911
31. EM Messing 1990 Clinical implications of the expression of epidermal growth factor receptors in human transitional cell carcinoma Cancer Research 50 2530 2537 1:CAS:528:DyaK3cXitleitb8%3D 1690599
32. EM Messing 1992 Growth factors and bladder cancer: clinical implications of the interactions between growth factors and their urothelial receptors Seminars in Surgical Oncology 8 285 292 1:STN:280:DyaK3s%2FpslSltg%3D%3D 1462099
33. RM Hicks 1965 The fine structure of the transitional epithelium of rat ureter Journal of Cell Biology 26 25 48 1:STN:280:DyaF28%2FotVKrsg%3D%3D 5859020
34. LG Koss 1969 The asymmetric unit membranes of the epithelium of the urinary bladder of the rat. An electron microscopic study of a mechanism of epithelial maturation and function Laboratory Investigation 21 154 168 1:STN:280:DyaF1M3mslKmtg%3D%3D 5804627
35. Porter, K. R., & Bonneville, M. A. (1963). An introduction to the fine structure of cells and tissues. Philadelphia: Lea & Febiger.
36. XR Wu TT Sun 1993 Molecular cloning of a 47 kDa tissue-specific and differentiation-dependent urothelial cell surface glycoprotein Journal of Cell Science 106 31 43 1:CAS:528:DyaK2cXhsFOjtrg%3D 8270634
37. JH Lin XR Wu G Kreibich TT Sun 1994 Precursor sequence, processing, and urothelium-specific expression of a major 15-kDa protein subunit of asymmetric unit membrane Journal of Biological Chemistry 269 1775 1784 1:CAS:528: DyaK2cXhvVGmu7s%3D 7507484
38. J Yu JH Lin XR Wu TT Sun 1994 Uroplakins Ia and Ib, two major differentiation products of bladder epithelium, belong to a family of four transmembrane domain (4TM) proteins Journal of Cell Biology 125 171 182 1:CAS:528:DyaK2cXis1CisLw%3D 8138569
39. J Yu M Manabe XR Wu C Xu B Surya TT Sun 1990 Uroplakin I: a 27-kD protein associated with the asymmetric unit membrane of mammalian urothelium Journal Cell Biology 111 1207 1216 1:CAS:528:DyaK3cXlsV2gsL8%3D
40. XR Wu JH Lin T Walz M Haner J Yu U Aebi, et al. 1994 Mammalian uroplakins. A group of highly conserved urothelial differentiation-related membrane proteins Journal of Biological Chemistry 269 13716 13724 1:CAS:528:DyaK2cXkt12msrw%3D 8175808
41. FM Deng FX Liang L Tu KA Resing P Hu M Supino, et al. 2002 Uroplakin IIIb, a urothelial differentiation marker, dimerizes with uroplakin Ib as an early step of urothelial plaque assembly Journal of Cell Biology 159 685 694 1:CAS:528:DC%2BD38XptVyqtbg%3D 12446744
42. R Moll XR Wu JH Lin TT Sun 1995 Uroplakins, specific membrane proteins of urothelial umbrella cells, as histological markers of metastatic transitional cell carcinomas American Journal of Pathology 147 1383 1397 1:STN:280: DyaK28%2FmsFSruw%3D%3D 7485401
43. RL Wu I Osman XR Wu ML Lu ZF Zhang FX Liang, et al. 1998 Uroplakin II gene is expressed in transitional cell carcinoma but not in bilharzial bladder squamous cell carcinoma: alternative pathways of bladder epithelial differentiation and tumor formation [published erratum appears in Cancer Res 1998 Jul 1;58(13):2904] Cancer Research 58 1291 1297 1:CAS:528: DyaK1cXhvV2rsL0%3D 9515818
44. J Cheng H Huang ZT Zhang E Shapiro A Pellicer TT Sun, et al. 2002 Overexpression of epidermal growth factor receptor in urothelium elicits urothelial hyperplasia and promotes bladder tumor growth Cancer Research 62 4157 4163 1:CAS:528:DC%2BD38XlsV2ltrg%3D 12124355
45. S Signoretti MM Pires M Lindauer JW Horner C Grisanzio S Dhar, et al. 2005 p63 regulates commitment to the prostate cell lineage Proceedings of the National Academy of Sciences of the United States of America 102 11355 11360 1:CAS:528:DC%2BD2MXoslKitL0%3D 16051706
46. L Mo X Zheng HY Huang E Shapiro H Lepor C Cordon-Cardo, et al. 2007 Hyperactivation of Ha-ras oncogene, but not Ink4a/Arf deficiency, triggers bladder tumorigenesis Journal of Clinical Investigation 117 314 325 1:CAS:528:DC%2BD2sXhs1Oqsbo%3D 17256055
47. J Gao HY Huang J Pak J Cheng ZT Zhang E Shapiro, et al. 2004 p53 deficiency provokes urothelial proliferation and synergizes with activated Ha-ras in promoting urothelial tumorigenesis Oncogene 23 687 696 1:CAS:528:DC%2BD2cXlt1alsQ%3D%3D 14737103
48. He, F., Mo, L., Zheng, X. -Y., Hu, C., Lepor, H., Lee, E. Y.-H. P., et al. (2009). Deficiency of pRb family proteins and p53 in invasive urothelial tumorigenesis. Cancer Research (in press)
49. XR Wu 2005 Urothelial tumorigenesis: A tale of divergent pathways Nature Reviews Cancer 5 713 725 1:CAS:528:DC%2BD2MXpsleksLs%3D 16110317
50. ZT Zhang J Pak HY Huang E Shapiro TT Sun A Pellicer, et al. 2001 Role of Ha-ras activation in superficial papillary pathway of urothelial tumor formation Oncogene 20 1973 1980 1:CAS:528:DC%2BD3MXjt1Wltb8%3D 11360181
51. A Garcia-Espana E Salazar TT Sun XR Wu A Pellicer 2005 Differential expression of cell cycle regulators in phenotypic variants of transgenically induced bladder tumors: implications for tumor behavior Cancer Research 65 1150 1157 1:CAS:528:DC%2BD2MXhsFKqsLs%3D 15734997
52. P Franceschini D Licata G Di Cara A Guala M Bianchi G Ingrosso, et al. 1999 Bladder carcinoma in Costello syndrome: report on a patient born to consanguineous parents and review American Journal of Medical Genetics 86 174 179 1:STN:280:DyaK1Mzot1ajsA%3D%3D 10449656
53. KW Gripp CI Scott Jr L Nicholson TE Figueroa 2000 Second case of bladder carcinoma in a patient with Costello syndrome American Journal of Medical Genetics 90 256 259 1:STN:280:DC%2BD3c7kt1WgtA%3D%3D 10678668
54. S Urakami M Igawa H Shiina K Shigeno N Kikuno T Yoshino 2002 Recurrent transitional cell carcinoma in a child with the Costello syndrome Journal of Urology 168 1133 1134 12187253
55. YM Agazie N Movilla I Ischenko MJ Hayman 2003 The phosphotyrosine phosphatase SHP2 is a critical mediator of transformation induced by the oncogenic fibroblast growth factor receptor 3 Oncogene 22 6909 6918 1:CAS:528:DC%2BD3sXnvFSgsbo%3D 14534538
56. M Kanai M Goke S Tsunekawa DK Podolsky 1997 Signal transduction pathway of human fibroblast growth factor receptor 3. Identification of a novel 66-kDa phosphoprotein Journal of Biological Chemistry 272 6621 6628 1:CAS:528:DyaK2sXhvVOgtbg%3D 9045692
57. D Cappellen C De Oliveira D Ricol S de Medina J Bourdin X Sastre-Garau, et al. 1999 Frequent activating mutations of FGFR3 in human bladder and cervix carcinomas Nature Genetics 23 18 20 1:CAS:528:DyaK1MXlvFWhs7s%3D 10471491
58. KM Rieger-Christ A Mourtzinos PJ Lee RM Zagha J Cain M Silverman, et al. 2003 Identification of fibroblast growth factor receptor 3 mutations in urine sediment DNA samples complements cytology in bladder tumor detection Cancer 98 737 744 1:CAS:528:DC%2BD3sXntVWgurw%3D 12910517
59. BW van Rhijn TH van der Kwast AN Vis WJ Kirkels ER Boeve AC Jobsis, et al. 2004 FGFR3 and P53 characterize alternative genetic pathways in the pathogenesis of urothelial cell carcinoma Cancer Research 64 1911 1914 15026322
60. MC Naski Q Wang J Xu DM Ornitz 1996 Graded activation of fibroblast growth factor receptor 3 by mutations causing achondroplasia and thanatophoric dysplasia Nature Genetics 13 233 237 1:CAS:528:DyaK28XktlOhurc%3D 8640234
61. E Monsonego-Ornan R Adar T Feferman O Segev A Yayon 2000 The transmembrane mutation G380R in fibroblast growth factor receptor 3 uncouples ligand-mediated receptor activation from down-regulation Molecular and Cellular Biology 20 516 522 1:CAS:528:DC%2BD3cXjtVKnuw%3D%3D 10611230
62. AH Jebar CD Hurst DC Tomlinson C Johnston CF Taylor MA Knowles 2005 FGFR3 and Ras gene mutations are mutually exclusive genetic events in urothelial cell carcinoma Oncogene 24 5218 5225 1:CAS:528:DC%2BD2MXmvFemsbo%3D 15897885
63. M Tartaglia LA Pennacchio C Zhao KK Yadav V Fodale A Sarkozy, et al. 2007 Gain-of-function SOS1 mutations cause a distinctive form of Noonan syndrome Nature Genetics 39 75 79 1:CAS:528:DC%2BD28XhtlGktLjI 17143282
64. SV Madhunapantula GP Robertson 2008 Is B-Raf a good therapeutic target for melanoma and other malignancies? Cancer Research 68 5 8 1:CAS:528: DC%2BD1cXoslag 18172288
65. K Sibley P Stern MA Knowles 2001 Frequency of fibroblast growth factor receptor 3 mutations in sporadic tumours Oncogene 20 4416 4418 1:CAS:528:DC%2BD3MXlvFOisLc%3D 11466624
66. R Wu D Connolly C Ngelangel FX Bosch N Munoz KR Cho 2000 Somatic mutations of fibroblast growth factor receptor 3 (FGFR3) are uncommon in carcinomas of the uterine cervix Oncogene 19 5543 5546 1:CAS:528: DC%2BD3cXosl2msrg%3D 11114733
67. NS Fracchiolla S Luminari L Baldini L Lombardi AT Maiolo A Neri 1998 FGFR3 gene mutations associated with human skeletal disorders occur rarely in multiple myeloma Blood 92 2987 2989 1:CAS:528:DyaK1cXms1elu7g%3D 9763594
68. CA Reznikoff CD Belair TR Yeager E Savelieva RH Blelloch JA Puthenveettil, et al. 1996 A molecular genetic model of human bladder cancer pathogenesis Seminars in Oncology 23 571 584 1:CAS:528:DyaK28XmvFWrtbo%3D 8893868
69. RJ Cote MD Dunn SJ Chatterjee JP Stein SR Shi QC Tran, et al. 1998 Elevated and absent pRb expression is associated with bladder cancer progression and has cooperative effects with p53 Cancer Research 58 1090 1094 1:CAS:528:DyaK1cXhvV2ku78%3D 9515785
70. HB Grossman M Liebert M Antelo CP Dinney SX Hu JL Palmer, et al. 1998 p53 and Rb expression predict progression in T1 bladder cancer Clinical Cancer Research 4 829 834 1:CAS:528:DyaK1cXisFels7o%3D 9563875
71. C Cordon-Cardo ZF Zhang G Dalbagni M Drobnjak E Charytonowicz SX Hu, et al. 1997 Cooperative effects of p53 and pRB alterations in primary superficial bladder tumors Cancer Research 57 1217 1221 1:CAS:528:DyaK2sXit1Kqu74%3D 9102201
72. AR Clarke ER Maandag M van Roon NM van der Lugt M van der Valk ML Hooper, et al. 1992 Requirement for a functional Rb-1 gene in murine development Nature 359 328 330 1:CAS:528:DyaK38XmtV2mtbs%3D 1406937
73. T Jacks A Fazeli EM Schmitt RT Bronson MA Goodell RA Weinberg 1992 Effects of an Rb mutation in the mouse Nature 359 295 300 1:CAS:528: DyaK38XlvV2hu7s%3D 1406933
74. EY Lee CY Chang N Hu YC Wang CC Lai K Herrup, et al. 1992 Mice deficient for Rb are nonviable and show defects in neurogenesis and haematopoiesis Nature 359 288 294 1:CAS:528:DyaK38XmtV2mtbo%3D 1406932
75. L Mo J Cheng EY Lee TT Sun XR Wu 2005 Gene deletion in urothelium by specific expression of Cre recombinase American Journal of Physiology and Renal Physiology 289 F562 F568 1:CAS:528:DC%2BD2MXhtVWktrfO
76. A Flesken-Nikitin KC Choi JP Eng EN Shmidt AY Nikitin 2003 Induction of carcinogenesis by concurrent inactivation of p53 and Rb1 in the mouse ovarian surface epithelium Cancer Research 63 3459 3463 1:CAS:528:DC%2BD3sXltVGrtL8%3D 12839925
77. S Marino M Vooijs H van Der Gulden J Jonkers A Berns 2000 Induction of medulloblastomas in p53-null mutant mice by somatic inactivation of Rb in the external granular layer cells of the cerebellum Genes and Development 14 994 1004 1:CAS:528:DC%2BD3cXivFyltrk%3D 10783170
78. J Cheng H Huang J Pak E Shapiro TT Sun C Cordon-Cardo, et al. 2003 Allelic loss of p53 gene is associated with genesis and maintenance, but not invasion, of mouse carcinoma in situ of the bladder Cancer Research 63 179 185 1:CAS:528:DC%2BD3sXjvFKgtw%3D%3D 12517796
79. ZT Zhang J Pak E Shapiro TT Sun XR Wu 1999 Urothelium-specific expression of an oncogene in transgenic mice induced the formation of carcinoma in situ and invasive transitional cell carcinoma Cancer Research 59 3512 3517 1:CAS:528:DyaK1MXks1Omsbg%3D 10416618
80. PJ Grippo EP Sandgren 2000 Highly invasive transitional cell carcinoma of the bladder in a simian virus 40 T-antigen transgenic mouse model American Journal of Pathology 157 805 813 1:CAS:528:DC%2BD3cXmvFWqt7s%3D 10980120
81. SH Ali JA DeCaprio 2001 Cellular transformation by SV40 large T antigen: interaction with host proteins Seminars in Cancer Biology 11 15 23 1:CAS:528:DC%2BD3MXhslSntLc%3D 11243895
82. A Sun L Bagella S Tutton G Romano A Giordano 2007 From G0 to S phase: a view of the roles played by the retinoblastoma (Rb) family members in the Rb-E2F pathway Journal of Cellular Biochemistry 102 1400 1404 1:CAS:528: DC%2BD2sXhsVeitL7O 17979151
83. A Vidal C Carneiro JB Zalvide 2007 Of mice without pockets: mouse models to study the function of Rb family proteins Front and Bioscience 12 4483 4496 1:CAS:528:DC%2BD2sXms1Kltr0%3D
84. ME Crosby A Almasan 2004 Opposing roles of E2Fs in cell proliferation and death Cancer Biology Therapeutic 3 1208 1211 1:CAS:528:DC%2BD2MXjvVyntrs%3D
85. D MacPherson J Sage T Kim D Ho ME McLaughlin T Jacks 2004 Cell type-specific effects of Rb deletion in the murine retina Genes and Development 18 1681 1694 1:CAS:528:DC%2BD2cXlvFKltrc%3D 15231717
86. MF Lara M Santos S Ruiz C Segrelles M Moral AB Martinez-Cruz, et al. 2008 p107 acts as a tumor suppressor in pRb-deficient epidermis Molecular Carcinogenesis 47 105 113 1:CAS:528:DC%2BD1cXit1Sgtrg%3D 17932945
87. LM Chow SJ Baker 2006 PTEN function in normal and neoplastic growth Cancer Letters 241 184 196 1:CAS:528:DC%2BD28XotV2msL4%3D 16412571
88. F Vazquez S Matsuoka WR Sellers T Yanagida M Ueda PN Devreotes 2006 Tumor suppressor PTEN acts through dynamic interaction with the plasma membrane Proceedings of the National Academy of Sciences of the United States of America 103 3633 3638 1:CAS:528:DC%2BD28XivFWju70%3D 16537447
89. M Tanaka D Koul MA Davies M Liebert PA Steck HB Grossman 2000 MMAC1/PTEN inhibits cell growth and induces chemosensitivity to doxorubicin in human bladder cancer cells Oncogene 19 5406 5412 1:CAS:528:DC%2BD3cXosFKktLk%3D 11103942
90. JJ Gildea M Herlevsen MA Harding KM Gulding CA Moskaluk HF Frierson, et al. 2004 PTEN can inhibit in vitro organotypic and in vivo orthotopic invasion of human bladder cancer cells even in the absence of its lipid phosphatase activity Oncogene 23 6788 6797 1:CAS:528:DC%2BD2cXntFGnurs%3D 15273733
91. J Li L Simpson M Takahashi C Miliaresis MP Myers N Tonks, et al. 1998 The PTEN/MMAC1 tumor suppressor induces cell death that is rescued by the AKT/protein kinase B oncogene Cancer Research 58 5667 5672 1:CAS:528: DyaK1MXivV2l 9865719
92. A Di Cristofano B Pesce C Cordon-Cardo PP Pandolfi 1998 Pten is essential for embryonic development and tumour suppression Nature Genetics 19 348 355 9697695
93. K Podsypanina LH Ellenson A Nemes J Gu M Tamura KM Yamada, et al. 1999 Mutation of Pten/Mmac1 in mice causes neoplasia in multiple organ systems Proceedings of the National Academy of Sciences of the United States of America 96 1563 1568 1:CAS:528:DyaK1MXhsFSqsrc%3D 9990064
94. A Suzuki JL de la Pompa V Stambolic AJ Elia T Sasaki I del Barco Barrantes, et al. 1998 High cancer susceptibility and embryonic lethality associated with mutation of the PTEN tumor suppressor gene in mice Current Biology 8 1169 1178 1:CAS:528:DyaK1cXntFWgsb8%3D 9799734
95. LI Yoo DW Liu S Le Vu RT Bronson H Wu J Yuan 2006 Pten deficiency activates distinct downstream signaling pathways in a tissue-specific manner Cancer Research 66 1929 1939 1:CAS:528:DC%2BD28XhsFamur4%3D 16488991
96. X Ma AC Ziel-van der Made B Autar HA van der Korput M Vermeij P van Duijn, et al. 2005 Targeted biallelic inactivation of Pten in the mouse prostate leads to prostate cancer accompanied by increased epithelial cell proliferation but not by reduced apoptosis Cancer Research 65 5730 5739 1:CAS:528: DC%2BD2MXlslOqsb4%3D 15994948
97. NR Leslie CP Downes 2004 PTEN function: How normal cells control it and tumour cells lose it Biochemical Journal 382 1 11 1:CAS:528:DC%2BD2cXmsVChsLo%3D 15193142
98. S Gustafson KM Zbuk C Scacheri C Eng 2007 Cowden syndrome Seminars in Oncology 34 428 434 1:CAS:528:DC%2BD2sXhtleltrzP 17920899
99. H Tsuruta H Kishimoto T Sasaki Y Horie M Natsui Y Shibata, et al. 2006 Hyperplasia and carcinomas in Pten-deficient mice and reduced PTEN protein in human bladder cancer patients Cancer Research 66 8389 8396 1:CAS:528: DC%2BD28XovF2isr0%3D 16951148
100. AM Puzio-Kuter M Castillo-Martin CW Kinkade X Wang TH Shen T Matos, et al. 2009 Inactivation of p53 and Pten promotes invasive bladder cancer Genes and Development 23 675 680 1:CAS:528:DC%2BD1MXktVWltrk%3D 19261747
101. JS Aveyard A Skilleter T Habuchi MA Knowles 1999 Somatic mutation of PTEN in bladder carcinoma British Journal of Cancer 80 904 908 1:CAS:528: DyaK1MXjsV2ru7c%3D 10360673
102. J Kagan J Liu JD Stein SS Wagner R Babkowski BH Grossman, et al. 1998 Cluster of allele losses within a 2.5 cM region of chromosome 10 in high-grade invasive bladder cancer Oncogene 16 909 913 1:CAS:528:DyaK1cXhs1yjtbo%3D 9484782
103. D Cappellen G Diez S de Medina D Chopin JP Thiery F Radvanyi 1997 Frequent loss of heterozygosity on chromosome 10q in muscle-invasive transitional cell carcinomas of the bladder Oncogene 14 3059 3066 1:CAS:528:DyaK2sXksF2itr0%3D 9223669
104. CD Hurst H Fiegler P Carr S Williams NP Carter MA Knowles 2004 High-resolution analysis of genomic copy number alterations in bladder cancer by microarray-based comparative genomic hybridization Oncogene 23 2250 2263 1:CAS:528:DC%2BD2cXitFCmsLo%3D 14968109 (Pubitemid 38482541)
105. DS Wang K Rieger-Christ JM Latini A Moinzadeh J Stoffel JA Pezza, et al. 2000 Molecular analysis of PTEN and MXI1 in primary bladder carcinoma International Journal of Cancer 88 620 625 1:CAS:528:DC%2BD3cXotVKit7k%3D
106. J Liu DC Babaian M Liebert PA Steck J Kagan 2000 Inactivation of MMAC1 in bladder transitional-cell carcinoma cell lines and specimens Molecular Carcinogenesis 29 143 150 1:CAS:528:DC%2BD3cXoslWrurc%3D 11108659
107. P Cairns E Evron K Okami N Halachmi M Esteller JG Herman, et al. 1998 Point mutation and homozygous deletion of PTEN/MMAC1 in primary bladder cancers Oncogene 16 3215 3218 1:CAS:528:DyaK1cXkt1Omu7o%3D 9671402
108. LC Pagliaro A Keyhani D Williams D Woods B Liu P Perrotte, et al. 2003 Repeated intravesical instillations of an adenoviral vector in patients with locally advanced bladder cancer: a phase I study of p53 gene therapy Journal of Clinical Oncology 21 2247 2253 1:CAS:528:DC%2BD2cXpsVGqu7s%3D 12805322
109. X Zhang AS Multani JH Zhou JW Shay D McConkey L Dong, et al. 2003 Adenoviral-mediated retinoblastoma 94 produces rapid telomere erosion, chromosomal crisis, and caspase-dependent apoptosis in bladder cancer and immortalized human urothelial cells but not in normal urothelial cells Cancer Research 63 760 765 1:CAS:528:DC%2BD3sXht1GqsrY%3D 12591722