Slow disease progression in a C57BL/6 Pten-deficient mouse model of prostate cancer

American Journal of Pathology

Volumn 179, Issue 1, 2011, Pages 502-512

  Svensson, Robert U ^a   Haverkamp, Jessica M ^a,b   Thedens, Daniel R ^a   Cohen, Michael B ^a   Ratliff, Timothy L ^b   Henry, Michael D ^a  

^a UNIVERSITY OF IOWA   (United States)

^b PURDUE UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN; LUCIFERASE; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ANTERIOR PROSTATE; ARTICLE; BIOLUMINESCENCE; C57BL 6 MOUSE; CANCER GROWTH; CANCER INVASION; CANCER MODEL; CANCER RELAPSE; CANCER RISK; CONTROLLED STUDY; DISEASE DURATION; ENVIRONMENTAL FACTOR; FLUID RETENTION; GENETIC RISK; INFLAMMATION; MOUSE; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; PHENOTYPE; PRIORITY JOURNAL; PROSTATE; PROSTATE CANCER; STROMA; SUPPRESSOR CELL; TUMOR VOLUME;

ANIMALS; CELL PROLIFERATION; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; FLUORESCENT ANTIBODY TECHNIQUE; HUMANS; INFLAMMATION; INTEGRASES; LUCIFERASES; LYMPHATIC METASTASIS; MAGNETIC RESONANCE IMAGING; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; PHENOTYPE; PROSTATE; PROSTATIC NEOPLASMS; PTEN PHOSPHOHYDROLASE; STROMAL CELLS; TIME FACTORS;

EID: 80052469556     PISSN: 00029440     EISSN: 15252191     Source Type: Journal    
DOI: 10.1016/j.ajpath.2011.03.014     Document Type: Article

References (46)

1. H.I. Scher Prostate carcinoma: defining therapeutic objectives and improving overall outcomes Cancer 97 2003 758 771
2. A. Jemal, R. Siegel, E. Ward, Y. Hao, J. Xu, and M.J. Thun Cancer statistics, 2009 CA Cancer J Clin 59 2009 225 249
3. K.J. Pienta, C. Abate-Shen, D.B. Agus, R.M. Attar, L.W. Chung, N.M. Greenberg, W.C. Hahn, J.T. Isaacs, N.M. Navone, D.M. Peehl, J.W. Simons, D.B. Solit, H.R. Soule, T.A. VanDyke, M.J. Weber, L. Wu, and R.L. Vessella The current state of preclinical prostate cancer animal models Prostate 68 2008 629 639
4. S. Wang, J. Gao, Q. Lei, N. Rozengurt, C. Pritchard, J. Jiao, G.V. Thomas, G. Li, P. Roy-Burman, P.S. Nelson, X. Liu, and H. Wu Prostate-specific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer Cancer Cell 4 2003 209 221
5. Z. Chen, L.C. Trotman, D. Shaffer, H.K. Lin, Z.A. Dotan, M. Niki, J.A. Koutcher, H.I. Scher, T. Ludwig, W. Gerald, C. Cordon-Cardo, and P.P. Pandolfi Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis Nature 436 2005 725 730
6. S. Wang, A.J. Garcia, M. Wu, D.A. Lawson, O.N. Witte, and H. Wu Pten deletion leads to the expansion of a prostatic stem/progenitor cell subpopulation and tumor initiation Proc Natl Acad Sci USA 103 2006 1480 1485
7. E.J. Akins, M.L. Moore, S. Tang, M.C. Willingham, J.A. Tooze, and P. Dubey In situ vaccination combined with androgen ablation and regulatory T-cell depletion reduces castration-resistant tumor burden in prostate-specific Pten knockout mice Cancer Res 70 2010 3473 3482
8. M. Moussavi, L. Fazli, H. Tearle, Y. Guo, M. Cox, J. Bell, C. Ong, W. Jia, and P.S. Rennie Oncolysis of prostate cancers induced by vesicular stomatitis virus in PTEN knockout mice Cancer Res 70 2010 1367 1376
9. S. Gross, and D. Piwnica-Worms Spying on cancer: molecular imaging in vivo with genetically encoded reporters Cancer Cell 7 2005 5 15
10. C.P. Liao, C. Zhong, G. Saribekyan, J. Bading, R. Park, P.S. Conti, R. Moats, A. Berns, W. Shi, Z. Zhou, A.Y. Nikitin, and P. Roy-Burman Mouse models of prostate adenocarcinoma with the capacity to monitor spontaneous carcinogenesis by bioluminescence or fluorescence Cancer Res 67 2007 7525 7533
11. M. Safran, W.Y. Kim, A.L. Kung, J.W. Horner, R.A. DePinho, and W.G. Kaelin Jr Mouse reporter strain for noninvasive bioluminescent imaging of cells that have undergone Cre-mediated recombination Mol Imaging 2 2003 297 302
12. X. Wu, J. Wu, J. Huang, W.C. Powell, J. Zhang, R.J. Matusik, F.O. Sangiorgi, R.E. Maxson, H.M. Sucov, and P. Roy-Burman Generation of a prostate epithelial cell-specific Cre transgenic mouse model for tissue-specific gene ablation Mech Dev 101 2001 61 69
13. R. Lesche, M. Groszer, J. Gao, Y. Wang, A. Messing, H. Sun, X. Liu, and H. Wu Cre/loxP-mediated inactivation of the murine Pten tumor suppressor gene Genesis 32 2002 148 149
14. A.K. Esser, M.B. Cohen, and M.D. Henry Dystroglycan is not required for maintenance of the luminal epithelial basement membrane or cell polarity in the mouse prostate Prostate 70 2010 777 787
15. J.M. Drake, C.L. Gabriel, and M.D. Henry Assessing tumor growth and distribution in a model of prostate cancer metastasis using bioluminescence imaging Clin Exp Metastasis 22 2005 674 684
16. R.U. Svensson, M.R. Shey, Z.K. Ballas, J.R. Dorkin, M. Goldberg, A. Akinc, R. Langer, D.G. Anderson, D. Bumcrot, and M.D. Henry Assessing siRNA pharmacodynamics in a luciferase-expressing mouse Mol Ther 16 2008 1995 2001
17. R.U. Svensson, J.M. Barnes, O.W. Rokhlin, M.B. Cohen, and M.D. Henry Chemotherapeutic agents up-regulate the cytomegalovirus promoter: implications for bioluminescence imaging of tumor response to therapy Cancer Res 67 2007 10445 10454
18. S.B. Shappell, G.V. Thomas, R.L. Roberts, R. Herbert, M.M. Ittmann, M.A. Rubin, P.A. Humphrey, J.P. Sundberg, N. Rozengurt, R. Barrios, J.M. Ward, and R.D. Cardiff Prostate pathology of genetically engineered mice: definitions and classification The consensus report from the Bar Harbor meeting of the Mouse Models of Human Cancer Consortium Prostate Pathology Committee Cancer Res 64 2004 2270 2305
19. C.L. Hsieh, Z. Xie, J. Yu, W.D. Martin, M.W. Datta, G.J. Wu, and L.W. Chung Non-invasive bioluminescent detection of prostate cancer growth and metastasis in a bigenic transgenic mouse model Prostate 67 2007 685 691
20. M.R. Seethammagari, X. Xie, N.M. Greenberg, and D.M. Spencer EZC-prostate models offer high sensitivity and specificity for noninvasive imaging of prostate cancer progression and androgen receptor action Cancer Res 66 2006 6199 6209
21. S.K. Lyons, E. Lim, A.O. Clermont, J. Dusich, L. Zhu, K.D. Campbell, R.J. Coffee, D.S. Grass, J. Hunter, T. Purchio, and D. Jenkins Noninvasive bioluminescence imaging of normal and spontaneously transformed prostate tissue in mice Cancer Res 66 2006 4701 4707
22. T. Troy, D. Jekic-McMullen, L. Sambucetti, and B. Rice Quantitative comparison of the sensitivity of detection of fluorescent and bioluminescent reporters in animal models Mol Imaging 3 2004 9 23
23. W. Zhang, J. Zhu, C.L. Efferson, C. Ware, J. Tammam, M. Angagaw, J. Laskey, K.A. Bettano, S. Kasibhatla, J.F. Reilly, C. Sur, and P.K. Majumder Inhibition of tumor growth progression by antiandrogens and mTOR inhibitor in a Pten-deficient mouse model of prostate cancer Cancer Res 69 2009 7466 7472
24. H.K. Lin, Z. Chen, G. Wang, C. Nardella, S.W. Lee, C.H. Chan, W.L. Yang, J. Wang, A. Egia, K.I. Nakayama, C. Cordon-Cardo, J. Teruya-Feldstein, and P.P. Pandolfi Skp2 targeting suppresses tumorigenesis by Arf-p53-independent cellular senescence Nature 464 2010 374 379
25. L.C. Trotman, M. Niki, Z.A. Dotan, J.A. Koutcher, A. Di Cristofano, A. Xiao, A.S. Khoo, P. Roy-Burman, N.M. Greenberg, T. Van Dyke, C. Cordon-Cardo, and P.P. Pandolfi Pten dose dictates cancer progression in the prostate PLoS Biol 1 2003 E59
26. C. Nardella, A. Carracedo, A. Alimonti, R.M. Hobbs, J.G. Clohessy, Z. Chen, A. Egia, A. Fornari, M. Fiorentino, M. Loda, S.C. Kozma, G. Thomas, C. Cordon-Cardo, and P.P. Pandolfi Differential requirement of mTOR in postmitotic tissues and tumorigenesis Sci Signal 2 55 2009 ra2
27. D.I. Gabrilovich, and S. Nagaraj Myeloid-derived suppressor cells as regulators of the immune system Nat Rev Immunol 9 2009 162 174
28. S. Ostrand-Rosenberg, and P. Sinha Myeloid-derived suppressor cells: linking inflammation and cancer J Immunol 182 2009 4499 4506
29. S. Kusmartsev, Y. Nefedova, D. Yoder, and D.I. Gabrilovich Antigen-specific inhibition of CD8+ T cell response by immature myeloid cells in cancer is mediated by reactive oxygen species [Erratum appeared in J Immunol 2004, 172:4647] J Immunol 172 2004 989 999
30. X. Ma, A.C. Ziel-van der Made, B. Autar, H.A. van der Korput, M. Vermeij, P. van Duijn, K.B. Cleutjens, R. de Krijger, P. Krimpenfort, A. Berns, T.H. van der Kwast, and J. Trapman 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 Res 65 2005 5730 5739
31. J.B. Burton, M. Johnson, M. Sato, S.B. Koh, D.J. Mulholland, D. Stout, A.F. Chatziioannou, M.E. Phelps, H. Wu, and L. Wu Adenovirus-mediated gene expression imaging to directly detect sentinel lymph node metastasis of prostate cancer Nat Med 14 2008 882 888
32. S.A. Backman, D. Ghazarian, K. So, O. Sanchez, K.U. Wagner, L. Hennighausen, A. Suzuki, M.S. Tsao, W.B. Chapman, V. Stambolic, and T.W. Mak Early onset of neoplasia in the prostate and skin of mice with tissue-specific deletion of Pten Proc Natl Acad Sci USA 101 2004 1725 1730
33. D. Freeman, R. Lesche, N. Kertesz, S. Wang, G. Li, J. Gao, M. Groszer, H. Martinez-Diaz, N. Rozengurt, G. Thomas, X. Liu, and H. Wu Genetic background controls tumor development in PTEN-deficient mice Cancer Res 66 2006 6492 6496
34. D. Bianchi-Frias, C. Pritchard, B.H. Mecham, I.M. Coleman, and P.S. Nelson Genetic background influences murine prostate gene expression: implications for cancer phenotypes Genome Biol 8 2007 R117
35. J. Blando, M. Portis, F. Benavides, A. Alexander, G. Mills, B. Dave, C.J. Conti, J. Kim, and C.L. Walker PTEN deficiency is fully penetrant for prostate adenocarcinoma in C57BL/6 mice via mTOR-dependent growth Am J Pathol 174 2009 1869 1879
36. J.R. Gingrich, R.J. Barrios, B.A. Foster, and N.M. Greenberg Pathologic progression of autochthonous prostate cancer in the TRAMP model Prostate Cancer Prostatic Dis 2 1999 70 75
37. Q. Xu, P.K. Majumder, K. Ross, Y. Shim, T.R. Golub, M. Loda, and W.R. Sellers Identification of prostate cancer modifier pathways using parental strain expression mapping Proc Natl Acad Sci USA 104 2007 17771 17776
38. M.J. Kim, R. Bhatia-Gaur, W.A. Banach-Petrosky, N. Desai, Y. Wang, S.W. Hayward, G.R. Cunha, R.D. Cardiff, M.M. Shen, and C. Abate-Shen Nkx3.1 mutant mice recapitulate early stages of prostate carcinogenesis Cancer Res 62 2002 2999 3004
39. P.K. Majumder, C. Grisanzio, F. O'Connell, M. Barry, J.M. Brito, Q. Xu, I. Guney, R. Berger, P. Herman, R. Bikoff, G. Fedele, W.K. Baek, S. Wang, K. Ellwood-Yen, H. Wu, C.L. Sawyers, S. Signoretti, W.C. Hahn, M. Loda, and W.R. Sellers A prostatic intraepithelial neoplasia-dependent p27 Kip1 checkpoint induces senescence and inhibits cell proliferation and cancer progression Cancer Cell 14 2008 146 155
40. H.A. Luchman, H. Benediktsson, M.L. Villemaire, A.C. Peterson, and F.R. Jirik The pace of prostatic intraepithelial neoplasia development is determined by the timing of Pten tumor suppressor gene excision PLoS One 3 2008 e3940
41. C.K. Ratnacaram, M. Teletin, M. Jiang, X. Meng, P. Chambon, and D. Metzger Temporally controlled ablation of PTEN in adult mouse prostate epithelium generates a model of invasive prostatic adenocarcinoma Proc Natl Acad Sci USA 105 2008 2521 2526
42. H. Gao, X. Ouyang, W.A. Banach-Petrosky, M.M. Shen, and C. Abate-Shen Emergence of androgen independence at early stages of prostate cancer progression in Nkx3.1; pten mice Cancer Res 66 2006 7929 7933
43. J.I. Youn, S. Nagaraj, M. Collazo, and D.I. Gabrilovich Subsets of myeloid-derived suppressor cells in tumor-bearing mice J Immunol 181 2008 5791 5802
44. F. Zhao, S. Obermann, R. von Wasielewski, L. Haile, M.P. Manns, F. Korangy, and T.F. Greten Increase in frequency of myeloid-derived suppressor cells in mice with spontaneous pancreatic carcinoma Immunology 128 2009 141 149
45. J.M. Haverkamp, S.A. Crist, B.D. Elzey, C. Cimen, and T.L. Ratliff In vivo suppressive function of myeloid-derived suppressor cells is limited to the inflammatory site Eur J Immunol 41 2011 749 759
46. S. Tu, G. Bhagat, G. Cui, S. Takaishi, E.A. Kurt-Jones, B. Rickman, K.S. Betz, M. Penz-Oesterreicher, O. Bjorkdahl, J.G. Fox, and T.C. Wang Overexpression of interleukin-1beta induces gastric inflammation and cancer and mobilizes myeloid-derived suppressor cells in mice [Erratum appeared in Cancer Cell 2011;19:154 and in Cancer Cell 2008;14(6):494] Cancer Cell 14 2008 408 419