Deficiency in metabolic regulators PPARγ and PTEN cooperates to drive keratinizing squamous metaplasia in novel models of human tissue regeneration

American Journal of Pathology

Volumn 182, Issue 2, 2013, Pages 449-459

  Strand, Douglas W ^a   Degraff, David J ^a   Jiang, Ming ^a   Sameni, Mansoureh ^c   Franco, Omar E ^a   Love, Harold D ^a   Hayward, William J ^a   Lin Tsai, Opal ^a   Wang, Anne Y ^a   Cates, Justin M M ^a   Sloane, Bonnie F ^c   Matusik, Robert J ^a,b   Hayward, Simon W ^a,b  

^a VANDERBILT INGRAM CANCER CENTER   (United States)

^b VANDERBILT UNIVERSITY SCHOOL OF MEDICINE   (United States)

^c WAYNE STATE UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 1; PEROXISOME PROLIFERATOR ACTIVATED RECEPTOR GAMMA 2; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BLADDER CARCINOGENESIS; CANCER MODEL; CELL TRANSDIFFERENTIATION; CONTROLLED STUDY; EMBRYO; ENZYME INACTIVATION; GENE EXPRESSION; GENE SILENCING; GENETIC ENGINEERING; GENETIC RECOMBINATION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; IN VITRO STUDY; IN VIVO STUDY; KERATINIZING SQUAMOUS METAPLASIA; KNOCKOUT GENE; MALE; MESENCHYME CELL; METABOLIC REGULATION; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSTATE EPITHELIUM; SQUAMOUS CELL METAPLASIA; TISSUE REGENERATION; UROTHELIUM;

ADULT; ANIMALS; BASE SEQUENCE; CELL LINE; CELL TRANSDIFFERENTIATION; COCULTURE TECHNIQUES; EPITHELIAL CELLS; HUMANS; HYPERPLASIA; MESODERM; METAPLASIA; MICE; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; PPAR GAMMA; PTEN PHOSPHOHYDROLASE; REGENERATION; UROTHELIUM;

EID: 84872703824     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2012.10.007     Document Type: Article

References (45)

1. G.R. Cunha, A.A. Donjacour, P.S. Cooke, S. Mee, R.M. Bigsby, S.J. Higgins, and Y. Sugimura The endocrinology and developmental biology of the prostate Endocr Rev 8 1987 338 362
2. A. Staack, A.A. Donjacour, J. Brody, G.R. Cunha, and P. Carroll Mouse urogenital development: a practical approach Differentiation 71 2003 402 413
3. G.R. Cunha, B. Lung, and B. Reese Glandular epithelial induction by embryonic mesenchyme in adult bladder epithelium of Balb/c mice Invest Urol 17 1980 302 304
4. B.L. Neubauer, L.W.K. Chung, K.A. McCormick, O. Taguchi, T.C. Thompson, and G.R. Cunha Epithelial-mesenchymal interactions in prostatic development. II: Biochemical observations of prostatic induction by urogenital sinus mesenchyme in epithelium of the adult rodent urinary bladder J Cell Biol 96 1983 1671 1676
5. G.R. Cunha, H. Fujii, B.L. Neubauer, J.M. Shannon, L.M. Sawyer, and B.A. Reese Epithelial-mesenchymal interactions in prostatic development. I: morphological observations of prostatic induction by urogenital sinus mesenchyme in epithelium of the adult rodent urinary bladder J Cell Biol 96 1983 1662 1670
6. S. Aboseif, A. El-Sakka, P. Young, and G. Cunha Mesenchymal reprogramming of adult human epithelial differentiation Differentiation 65 1999 113 118
7. Y. Li, W. Liu, S.W. Hayward, G.R. Cunha, and L.S. Baskin Plasticity of the urothelial phenotype: effects of gastro-intestinal mesenchyme/stroma and implications for urinary tract reconstruction Differentiation 66 2000 126 135
8. G. Cunha, and B. Lung The possible influences of temporal factors in androgenic responsiveness of urogenital tissue recombinants from wild-type and androgen-insensitive (Tfm) mice J Exp Zool 205 1978 181 194
9. D.J. Degraff, J.M. Cates, J.R. Mauney, P.E. Clark, R.J. Matusik, and R.M. Adam When urothelial differentiation pathways go wrong: implications for bladder cancer development and progression Urol Oncol 2011 doi: 10.1016/j.urolonc.2011.07.017 [Epub ahead of press]
10. W. de Groat, V. Ratner, J.O. DeLancey, A.J. Schaeffer, M. Liebert, W.D. Steers, J.D. McConnell, D. Weaver-Osterholtz Bladder Research Progress Review Group Overcoming Bladder Disease: A Strategic Plan for Bladder Research 2002 National Institutes of Health; National Institute of Diabetes and Digestive and Kidney Diseases Bethesda, MD
11. L. Fajas, D. Auboeuf, E. Raspe, K. Schoonjans, A.M. Lefebvre, R. Saladin, J. Najib, M. Laville, J.C. Fruchart, S. Deeb, A. Vidal-Puig, J. Flier, M.R. Briggs, B. Staels, H. Vidal, and J. Auwerx The organization, promoter analysis, and expression of the human PPARgamma gene J Biol Chem 272 1997 18779 18789
12. A.M. DeMarzo, W.G. Nelson, W.B. Isaacs, and J.I. Epstein Pathological and molecular aspects of prostate cancer Lancet 361 2003 955 964
13. F.M. Platt, C.D. Hurst, C.F. Taylor, W.M. Gregory, P. Harnden, and M.A. Knowles Spectrum of phosphatidylinositol 3-kinase pathway gene alterations in bladder cancer Clin Cancer Res 15 2009 6008 6017
14. C.L. Varley, E.J. Bacon, J.C. Holder, and J. Southgate FOXA1 and IRF-1 intermediary transcriptional regulators of PPARgamma-induced urothelial cytodifferentiation Cell Death Differ 16 2009 103 114
15. J.A. Dormandy, B. Charbonnel, D.J. Eckland, E. Erdmann, M. Massi-Benedetti, I.K. Moules, A.M. Skene, M.H. Tan, P.J. Lefebvre, G.D. Murray, E. Standl, R.G. Wilcox, L. Wilhelmsen, J. Betteridge, K. Birkeland, A. Golay, R.J. Heine, L. Koranyi, M. Laakso, M. Mokan, A. Norkus, V. Pirags, T. Podar, A. Scheen, W. Scherbaum, G. Schernthaner, O. Schmitz, J. Skrha, U. Smith, and J. Taton PROactive investigators: Secondary prevention of macrovascular events in patients with type 2 diabetes in the PROactive Study (PROspective pioglitAzone Clinical Trial In macroVascular Events): a randomised controlled trial Lancet 366 2005 1279 1289
16. C.L. Varley, J. Stahlschmidt, W.C. Lee, J. Holder, C. Diggle, P.J. Selby, L.K. Trejdosiewicz, and J. Southgate Role of PPARgamma and EGFR signalling in the urothelial terminal differentiation programme J Cell Sci 117 Pt 10 2004 2029 2036
17. C.L. Varley, J. Stahlschmidt, B. Smith, M. Stower, and J. Southgate Activation of peroxisome proliferator-activated receptor-gamma reverses squamous metaplasia and induces transitional differentiation in normal human urothelial cells Am J Pathol 164 2004 1789 1798
18. C.L. Varley, M.A. Garthwaite, W. Cross, J. Hinley, L.K. Trejdosiewicz, and J. Southgate PPARgamma-regulated tight junction development during human urothelial cytodifferentiation J Cell Physiol 208 2006 407 417
19. C.L. Varley, and J. Southgate Effects of PPAR agonists on proliferation and differentiation in human urothelium Exp Toxicol Pathol 60 2008 435 441
20. K.I. Nakashiro, Y. Hayashi, A. Kita, T. Tamatani, A. Chlenski, N. Usuda, K. Hattori, J.K. Reddy, and R. Oyasu Role of peroxisome proliferator-activated receptor gamma and its ligands in non-neoplastic and neoplastic human urothelial cells Am J Pathol 159 2001 591 597
21. B.Y. Shorning, D. Griffiths, and A.R. Clarke Lkb1 and Pten synergise to suppress mTOR-mediated tumorigenesis and epithelial-mesenchymal transition in the mouse bladder PLoS One 6 2011 e16209
22. I. Ahmad, J.P. Morton, L.B. Singh, S.M. Radulescu, R.A. Ridgway, S. Patel, J. Woodgett, D.J. Winton, M.M. Taketo, X.R. Wu, H.Y. Leung, and O.J. Sansom β-Catenin activation synergizes with PTEN loss to cause bladder cancer formation Oncogene 30 2011 178 189
23. M. Jiang, D.W. Strand, S. Fernandez, Y. He, Y. Yi, A. Birbach, Q. Qiu, J. Schmid, D.G. Tang, and S.W. Hayward Functional remodeling of benign human prostatic tissues in vivo by spontaneously immortalized progenitor and intermediate cells Stem Cells 28 2010 344 356
24. Y. Furumoto, S. Brooks, A. Olivera, Y. Takagi, M. Miyagishi, K. Taira, R. Casellas, M.A. Beaven, A.M. Gilfillan, and J. Rivera Cutting Edge: Lentiviral short hairpin RNA silencing of PTEN in human mast cells reveals constitutive signals that promote cytokine secretion and cell survival J Immunol 176 2006 5167 5171
25. M. Sameni, A. Anbalagan, M.B. Olive, K. Moin, R.R. Mattingly, and B.F. Sloane MAME models for 4D live-cell imaging of tumor: microenvironment interactions that impact malignant progression J Vis Exp 2012 pii: 3661. doi: 10.3791/3661
26. D.J. Degraff, P.E. Clark, J.M. Cates, H. Yamashita, V.L. Robinson, X. Yu, M.E. Smolkin, S.S. Chang, M.S. Cookson, M.K. Herrick, S.F. Shariat, G.D. Steinberg, H.F. Frierson, X.R. Wu, D. Theodorescu, and R.J. Matusik Loss of the urothelial differentiation marker FOXA1 is associated with high grade, late stage bladder cancer and increased tumor proliferation PLoS One 7 2012 e36669
27. D.W. Strand, M. Jiang, T.A. Murphy, Y. Yi, K.C. Konvinse, O.E. Franco, Y. Wang, J.D. Young, and S.W. Hayward PPARγ isoforms differentially regulate metabolic networks to mediate mouse prostatic epithelial differentiation Cell Death Dis 3 2012 e361
28. M. Jiang, S. Fernandez, W.G. Jerome, Y. He, X. Yu, H. Cai, B. Boone, Y. Yi, M.A. Magnuson, P. Roy-Burman, R.J. Matusik, S.B. Shappell, and S.W. Hayward Disruption of PPARgamma signaling results in mouse prostatic intraepithelial neoplasia involving active autophagy Cell Death Differ 17 2010 469 481
29. M. Jiang, W.G. Jerome, and S.W. Hayward Autophagy in nuclear receptor PPARgamma-deficient mouse prostatic carcinogenesis Autophagy 6 2010 175 176
30. S. Signoretti, M.M. Pires, M. Lindauer, J.W. Horner, C. Grisanzio, S. Dhar, P. Majumder, F. McKeon, P.W. Kantoff, W.R. Sellers, and M. Loda p63 regulates commitment to the prostate cell lineage Proc Natl Acad Sci USA 102 2005 11355 11360
31. C. Abate-Shen, W.A. Banach-Petrosky, X. Sun, K.D. Economides, N. Desai, J.P. Gregg, A.D. Borowsky, R.D. Cardiff, and M.M. Shen Nkx3.1; Pten mutant mice develop invasive prostate adenocarcinoma and lymph node metastases Cancer Res 63 2003 3886 3890
32. A. Di Cristofano, M. De Acetis, A. Koff, C. Cordon-Cardo, and P.P. Pandolfi Pten and p27KIP1 cooperate in prostate cancer tumor suppression in the mouse Nat Genet 27 2001 222 224
33. A. Hubner, D.J. Mulholland, C.L. Standen, M. Karasarides, J. Cavanagh-Kyros, T. Barrett, H. Chi, D.L. Greiner, C. Tournier, C.L. Sawyers, R.A. Flavell, H. Wu, and R.J. Davis JNK and PTEN cooperatively control the development of invasive adenocarcinoma of the prostate Proc Natl Acad Sci USA 109 2012 12046 12051
34. C. Zhong, G. Saribekyan, C.P. Liao, M.B. Cohen, and P. Roy-Burman Cooperation between FGF8b overexpression and PTEN deficiency in prostate tumorigenesis Cancer Res 66 2006 2188 2194
35. L.P. Weng, W.M. Smith, J.L. Brown, and C. Eng PTEN inhibits insulin-stimulated MEK/MAPK activation and cell growth by blocking IRS-1 phosphorylation and IRS-1/Grb-2/Sos complex formation in a breast cancer model Hum Mol Genet 10 2001 605 616
36. S.J. Grille, A. Bellacosa, J. Upson, A.J. Klein-Szanto, F. van Roy, W. Lee-Kwon, M. Donowitz, P.N. Tsichlis, and L. Larue The protein kinase Akt induces epithelial mesenchymal transition and promotes enhanced motility and invasiveness of squamous cell carcinoma lines Cancer Res 63 2003 2172 2178
37. A. Radu, V. Neubauer, T. Akagi, H. Hanafusa, and M.M. Georgescu PTEN induces cell cycle arrest by decreasing the level and nuclear localization of cyclin D1 Mol Cell Biol 23 2003 6139 6149
38. V. Stambolic, A. Suzuki, J.L. de la Pompa, G.M. Brothers, C. Mirtsos, T. Sasaki, J. Ruland, J.M. Penninger, D.P. Siderovski, and T.W. Mak Negative regulation of PKB/Akt-dependent cell survival by the tumor suppressor PTEN Cell 95 1998 29 39
39. I. Ahmad, R.J. Barnetson, and N.S. Krishna Keratinizing squamous metaplasia of the bladder: a review Urol Int 81 2008 247 251
40. I. Honma, N. Masumori, E. Sato, A. Takayanagi, A. Takahashi, N. Itoh, M. Tamagawa, M.A. Sato, and T. Tsukamoto Local recurrence after radical cystectomy for invasive bladder cancer: an analysis of predictive factors Urology 64 2004 744 748
41. A.A. Shokeir Squamous cell carcinoma of the bladder: pathology, diagnosis and treatment BJU Int 93 2004 216 220
42. N. Stransky, A.M. Egloff, and A.D. Tward The mutational landscape of head and neck squamous cell carcinoma Science 333 2011 1157 1160
43. J. Ma, J. Zhang, T. Ning, Z. Chen, and C. Xu Association of genetic polymorphisms in MDM2, PTEN and P53 with risk of esophageal squamous cell carcinoma J Hum Genet 57 2012 261 264
44. J.S. Lee, Y.D. Choi, J.H. Lee, J.H. Nam, C. Choi, M.C. Lee, C.S. Park, H.S. Kim, and K.W. Min Expression of PTEN in the progression of cervical neoplasia and its relation to tumor behavior and angiogenesis in invasive squamous cell carcinoma J Surg Oncol 93 2006 233 240
45. E. Lopez-Knowles, S.A. O'Toole, C.M. McNeil, E.K. Millar, M.R. Qiu, P. Crea, R.J. Daly, E.A. Musgrove, and R.L. Sutherland PI3K pathway activation in breast cancer is associated with the basal-like phenotype and cancer-specific mortality Int J Cancer 126 2010 1121 1131