Animal models of human prostate cancer: The consensus report of the new york meeting of the mouse models of human cancers consortium prostate pathology committee

Cancer Research

Volumn 73, Issue 9, 2013, Pages 2718-2736

  Ittmann, Michael ^a,b   Huang, Jiaoti ^c   Radaelli, Enrico ^q   Martin, Philip ^f   Signoretti, Sabina ⁱ   Sullivan, Ruth ^l,m,n   Simons, Brian W ^g   Ward, Jerrold M ^h   Robinson, Brian D ^o   Chu, Gerald C ^k   Loda, Massimo ^i,j,k   Thomas, George ^p   Borowsky, Alexander ^d,e   Cardiff, Robert D ^d,e  

^a BAYLOR COLLEGE OF MEDICINE   (United States)

^b MICHAEL E DEBAKEY VETERANS AFFAIRS MEDICAL CENTER   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Department of Pathology and Laboratory Medicine ^*  (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

^f FREDERICK NATIONAL LABORATORY FOR CANCER RESEARCH   (United States)

^g JOHNS HOPKINS UNIVERSITY SCHOOL OF MEDICINE   (United States)

^h NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

ⁱ BRIGHAM AND WOMEN S HOSPITAL   (United States)

^j Center for Molecular Oncologic Pathology   (United States)

^k HARVARD MEDICAL SCHOOL   (United States)

^l UNIVERSITY OF WISCONSIN MADISON   (United States)

^m Research Animal Resources Center   (United States)

ⁿ Laboratory for Optical and Computational Instrumentation   (United States)

^o WEILL CORNELL MEDICAL COLLEGE   (United States)

^p OREGON HEALTH AND SCIENCE UNIVERSITY   (United States)

^q UNIVERSITY OF MILAN   (Italy)

more..

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; APC PROTEIN; BETA CATENIN; FIBROBLAST GROWTH FACTOR; MITOGEN ACTIVATED PROTEIN KINASE; MYC PROTEIN; PHOSPHATIDYLINOSITOL 3,4,5 TRISPHOSPHATE 3 PHOSPHATASE; PROTEIN KINASE B; RAF PROTEIN; RAS PROTEIN; RETINOBLASTOMA PROTEIN; TRANSCRIPTION FACTOR ERG; TRANSFORMING GROWTH FACTOR BETA; WNT PROTEIN;

CANCER MODEL; CARCINOGENESIS; DOG; EPITHELIAL MESENCHYMAL TRANSITION; EPITHELIUM HYPERPLASIA; HUMAN; IMMUNOHISTOCHEMISTRY; METASTASIS; NICK END LABELING; NONHUMAN; ONCOGENE MYC; PRIORITY JOURNAL; PROSTATE ADENOCARCINOMA; PROSTATE CANCER; PROSTATIC INTRAEPITHELIAL NEOPLASIA; REVIEW; SARCOMATOID CARCINOMA; SIGNAL TRANSDUCTION; TRANSGENIC ANIMAL; TUMOR INVASION; TUMOR XENOGRAFT;

ADENOCARCINOMA; ANIMALS; CONSENSUS; DISEASE MODELS, ANIMAL; DISEASE PROGRESSION; GENE EXPRESSION REGULATION, NEOPLASTIC; GENETIC ENGINEERING; HUMANS; MALE; MICE; NEOPLASM METASTASIS; NEOPLASM TRANSPLANTATION; NEW YORK; ONCOGENES; PROSTATIC NEOPLASMS; RATS; SOCIETIES, MEDICAL;

EID: 84877785851     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-12-4213     Document Type: Review

References (74)

1. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, et al. Integrative genomic profiling of human prostate cancer. Cancer Cell 2010;18:11-22.
2. Bavik C, Coleman I, Dean JP, Knudsen B, Plymate S, Nelson PS. The gene expression program of prostate fibroblast senescence modulates neoplastic epithelial cell proliferation through paracrine mechanisms. Cancer Res 2006;66:794-802.
3. Bianchi-Frias D, Vakar-Lopez F, Coleman IM, Plymate SR, Reed MJ, Nelson PS. The effects of aging on the molecular and cellular composition of the prostate microenvironment. PLoS ONE 2010;5:e12501
4. Zong Y, Xin L, Goldstein AS, Lawson DA, Teitell MA, Witte ON. ETS family transcription factors collaborate with alternative signaling pathways to induce carcinoma from adult murine prostate cells. Proc Natl Acad Sci U S A 2009;106:12465-70.
5. Memarzadeh S, Xin L, Mulholland DJ, Mansukhani A,WuH, TeitellMA, et al. Enhanced paracrine FGF10 expression promotes formation of multifocal prostate adenocarcinoma and an increase in epithelial androgen receptor. Cancer Cell 2007;12:572-85.
6. Xin L, Teitell MA, Lawson DA, Kwon A, Mellinghoff IK, Witte ON. Progression of prostate cancer by synergy of AKT with genotropic and nongenotropic actions of the androgen receptor. Proc Natl Acad Sci U S A 2006;103:7789-94.
7. Goldstein AS, Huang J, Guo C, Garraway IP, Witte ON. Identification of a cell of origin for human prostate cancer. Science 2010;329:568-71.
8. Ammirante M, Luo JL, Grivennikov S, Nedospasov S, Karin M. B-cellderived lymphotoxin promotes castration-resistant prostate cancer. Nature 2010;464:302-5.
9. Shirai T, Takahashi S, Cui L, Futakuchi M, Kato K, Tamano S, et al. Experimental prostate carcinogenesis - rodent models. Mutat Res 2000;462:219-26.
10. Shappell SB, Thomas GV, Roberts RL, Herbert R, Ittmann MM, Rubin MA, et al. 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 2004;64:2270-305.
11. Wang F. Modeling human prostate cancer in genetically engineered mice. Prog Mol Biol Transl Sci 2011;100:1-49.
12. Jeet V, Russell PJ, Khatri A. Modeling prostate cancer: a perspective on transgenic mouse models. Cancer Metastasis Rev 2010;29: 123-42.
13. van Weerden WM, Bangma C, de Wit R. Human xenograft models as useful tools to assess the potential of novel therapeutics in prostate cancer. Br J Cancer 2009;100:13-8.
14. Irshad S, Abate-Shen C. Modeling prostate cancer in mice: something old, something new, something premalignant, something metastatic. Cancer Metastasis Rev. 2012 Nov 1. [Epub ahead of print].
15. Mahler JF, Stokes W, Mann PC, Takaoka M, Maronpot RR. Spontaneous lesions in aging FVB/N mice. Toxicol Pathol 1996;24:710-6.
16. Park JH, Walls JE, Galvez JJ, Kim M, Abate-Shen C, Shen MM, et al. Prostatic intraepithelial neoplasia in genetically engineered mice. Am J Pathol 2002;161:727-35.
17. Choi N, Zhang B, Zhang L, Ittmann M, Xin L. Adult murine prostate basal and luminal cells are self-sustained lineages that can both serve as targets for prostate cancer initiation. Cancer Cell 2012;21:253-65.
18. Robinson B, Magi-Galluzzi C, Zhou M. Intraductal carcinoma of the prostate. Arch Pathol Lab Med 2012;136:418-25.
19. Acevedo VD, Gangula RD, Freeman KW, Li R, Zhang Y, Wang F, et al. Inducible FGFR-1 activation leads to irreversible prostate adenocarcinoma and an epithelial-to-mesenchymal transition. Cancer Cell 2007;12:559-71.
20. Nauseef JT, Henry MD. Epithelial-to-mesenchymal transition in prostate cancer: paradigm or puzzle? Nat Rev Urol 2011;8:428-39.
21. Sun Y, Niu J, Huang J. Neuroendocrine differentiation in prostate cancer. Am J Transl Res 2009;1:148-62.
22. Di Cristofano A, Pesce B, Cordon-Cardo C, Pandolfi PP. Pten is essential for embryonic development and tumour suppression. Nat Genet 1998;19:348-55.
23. Wang S, Gao J, Lei Q, Rozengurt N, Pritchard C, Jiao J, et al. Prostatespecific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer. Cancer Cell 2003;4:209-21.
24. 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.
25. Thomsen MK, Ambroisine L, Wynn S, Cheah KS, Foster CS, Fisher G, et al. SOX9 elevation in the prostate promotes proliferation and cooperates with PTEN loss to drive tumor formation. Cancer Res 2010;70:979-87.
26. Clegg NJ, Couto SS, Wongvipat J, Hieronymus H, Carver BS, Taylor BS, et al. MYC cooperates with AKT in prostate tumorigenesis and alters sensitivity to mTOR inhibitors. PLoS ONE 2011; 6:e17449.
27. Mulholland DJ, Kobayashi N, Ruscetti M, Zhi A, Tran LM, Huang J, et al. Pten loss and RAS/MAPK activation cooperate to promote EMT and metastasis initiated from prostate cancer stem/progenitor cells. Cancer Res 2012;72:1878-89.
28. Wang J, Kobayashi T, Floc'h N, Kinkade CW, Aytes A, Dankort D, et al. B-Raf activation cooperates with PTEN loss to drive c-Myc expression in advanced prostate cancer. Cancer Res 2012;72:4765-76.
29. Chen Z, Trotman LC, Shaffer D, Lin HK, Dotan ZA, Niki M, et al. Crucial role of p53-dependent cellular senescence in suppression of Ptendeficient tumorigenesis. Nature 2005;436:725-30.
30. Martin P, Liu YN, Pierce R, Abou-Kheir W, Casey O, Seng V, et al. Prostate epithelial Pten/TP53 loss leads to transformation of multipotential progenitors and epithelial to mesenchymal transition. Am J Pathol 2011;179:422-35.
31. Ding Z, Wu CJ, Chu GC, Xiao Y, Ho D, Zhang J, et al. SMAD4- dependent barrier constrains prostate cancer growth and metastatic progression. Nature 2011;470:269-73.
32. Ding Z, Wu CJ, Jaskelioff M, Ivanova E, Kost-Alimova M, Protopopov A, et al. Telomerase reactivation following telomere dysfunction yields murine prostate tumors with bone metastases. Cell 2012;148: 896-907.
33. Mulholland DJ, Tran LM, Li Y, Cai H, Morim A, Wang S, et al. Cell autonomous role of PTEN in regulating castration-resistant prostate cancer growth. Cancer Cell 2011;19:792-804.
34. Lai KP, Yamashita S, Huang CK, Yeh S, Chang C. Loss of stromal androgen receptor leads to suppressed prostate tumourigenesis via modulation of pro-inflammatory cytokines/chemokines. EMBO Mol Med 2012;4:791-807.
35. Majumder PK, Yeh JJ, George DJ, Febbo PG, Kum J, Xue Q, et al. Prostate intraepithelial neoplasia induced by prostate restricted Akt activation: the MPAKT model. Proc Natl Acad Sci U S A 2003;100: 7841-6.
36. Ellwood-Yen K, Graeber TG, Wongvipat J, Iruela-Arispe ML, Zhang J, Matusik R, et al. Myc-driven murine prostate cancer shares molecular features with human prostate tumors. Cancer Cell 2003; 4:223-38.
37. Iwata T, Schultz D, Hicks J, Hubbard GK, Mutton LN, Lotan TL, et al. MYC overexpression induces prostatic intraepithelial neoplasia and loss of Nkx3.1 in mouse luminal epithelial cells. PLoS One 2010;5: e9427.
38. Kim J, Roh M, Doubinskaia I, Algarroba GN, Eltoum IE, Abdulkadir SA. A mouse model of heterogeneous, c-MYC-initiated prostate cancer with loss of Pten and p53. Oncogene 2012;31:322-32.
39. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 2005;310:644-8.
40. WangJ, Cai Y, Ren C, Ittmann M. Expression of variant TMPRSS2/ERG fusion messenger RNAs is associated with aggressive prostate cancer. Cancer Res 2006;66:8347-51.
41. Casey OM, Fang L, Hynes PG, Abou-Kheir WG, Martin PL, Tillman HS, et al. TMPRSS2-driven ERG expression in vivo increases self-renewal and maintains expression in a castration resistant subpopulation. PLoS ONE 2012;7:e41668.
42. Klezovitch O, Risk M, Coleman I, Lucas JM, Null M, True LD, et al. A causal role forERGin neoplastic transformation of prostate epithelium. Proc Natl Acad Sci U S A 2008;105:2105-10.
43. Hill R, Song Y, Cardiff RD, Van Dyke T. Heterogeneous tumor evolution initiated by loss of pRb function in a preclinical prostate cancer model. Cancer Res 2005;65:10243-54.
44. Yu X, Wang Y, DeGraff DJ, Wills ML, Matusik RJ. Wnt/beta-catenin activation promotes prostate tumor progression in a mouse model. Oncogene 2011;30:1868-79.
45. Klezovitch O, Chevillet J, Mirosevich J, Roberts RL, Matusik RJ, Vasioukhin V. Hepsin promotes prostate cancer progression and metastasis. Cancer Cell 2004;6:185-95.
46. Kwabi-Addo B, Ozen M, Ittmann M. The role of fibroblast growth factors and their receptors in prostate cancer. Endocr Relat Cancer 2004;11:709-24.
47. Wang F, McKeehan K, Yu C, Ittmann M, McKeehan WL. Chronic activity of ectopic type 1 fibroblast growth factor receptor tyrosine kinase in prostate epithelium results in hyperplasia accompanied by intraepithelial neoplasia. Prostate 2004;58:1-12.
48. Jin C, McKeehan K, Guo W, Jauma S, Ittmann MM, Foster B, et al. Cooperation between ectopic FGFR1 and depression of FGFR2 in induction of prostatic intraepithelial neoplasia in the mouse prostate. Cancer Res 2003;63:8784-90.
49. Freeman KW, Welm BE, Gangula RD, Rosen JM, Ittmann M, Greenberg NM, et al. Inducible prostate intraepithelial neoplasia with reversible hyperplasia in conditional FGFR1-expressing mice. Cancer Res 2003;63:8256-63.
50. Freeman KW, Gangula RD, Welm BE, Ozen M, Foster BA, Rosen JM, et al. Conditional activation of fibroblast growth factor receptor (FGFR) 1, but not FGFR2, in prostate cancer cells leads to increased osteopontin induction, extracellular signal-regulated kinase activation, and in vivo proliferation. Cancer Res 2003;63:6237-43.
51. Elo TD, Valve EM, Seppanen JA, Vuorikoski HJ, Makela SI, Poutanen M, et al. Stromal activation associated with development of prostate cancer in prostate-targeted fibroblast growth factor 8b transgenic mice. Neoplasia 2010;12:915-27.
52. Zhu C, Luong R, Zhuo M, Johnson DT, McKenney JK, Cunha GR, et al. Conditional expression of the androgen receptor induces oncogenic transformation of the mouse prostate. J Biol Chem 2011;286: 33478-88.
53. Bruxvoort KJ, Charbonneau HM, Giambernardi TA, Goolsby JC, Qian CN, Zylstra CR, et al. Inactivation of Apc in the mouse prostate causes prostate carcinoma. Cancer Res 2007;67:2490-6.
54. Shahi P, Park D, Pond AC, Seethammagari M, Chiou SH, Cho K, et al. Activation of Wnt signaling by chemically induced dimerization of LRP5 disrupts cellular homeostasis. PLoS ONE 2012;7:e30814.
55. Pearson HB, Perez-Mancera PA,DowLE, Ryan A, Tennstedt P, Bogani D, et al. SCRIB expression is deregulated in human prostate cancer, and its deficiency in mice promotes prostate neoplasia. J Clin Invest 2011;121:4257-67.
56. Qi J, Nakayama K, Cardiff RD, Borowsky AD, Kaul K, Williams R, et al. Siah2-dependent concerted activity of HIF and FoxA2 regulates formation of neuroendocrine phenotype and neuroendocrine prostate tumors. Cancer Cell 2010;18:23-38.
57. Polnaszek N, Kwabi-Addo B, Peterson LE, Ozen M, Greenberg NM, Ortega S, et al. Fibroblast growth factor 2 promotes tumor progression in an autochthonous mouse model of prostate cancer. Cancer Res 2003;63:5754-60.
58. Wang Y, Revelo MP, Sudilovsky D, Cao M, Chen WG, Goetz L, et al. Development and characterization of efficient xenograft models for benign and malignant human prostate tissue. Prostate 2005;64: 149-59.
59. Lin D, Bayani J, Wang Y, Sadar MD, Yoshimoto M, Gout PW, et al. Development of metastatic and non-metastatic tumor lines from a patient's prostate cancer specimen-identification of a small subpopulation with metastatic potential in the primary tumor. Prostate 2010;70:1636-44.
60. Corey E, Quinn JE, Buhler KR, Nelson PS, Macoska JA, True LD, et al. LuCaP 35: a new model of prostate cancer progression to androgen independence. Prostate 2003;55:239-46.
61. Kumar A, White TA, MacKenzie AP, Clegg N, Lee C, Dumpit RF, et al. Exome sequencing identifies a spectrum of mutation frequencies in advanced and lethal prostate cancers. Proc Natl Acad Sci U S A 2011;108:17087-92.
62. Hayward SW, Haughney PC, Rosen MA, Greulich KM, Weier HU, Dahiya R, et al. Interactions between adult human prostatic epithelium and rat urogenital sinus mesenchyme in a tissue recombination model. Differentiation 1998;63:131-40.
63. Hayward SW, Wang Y, Cao M, Hom YK, Zhang B, Grossfeld GD, et al. Malignant transformation in a nontumorigenic human prostatic epithelial cell line. Cancer Res 2001;61:8135-42.
64. Jiang M, Strand DW, Fernandez S, He Y, Yi Y, Birbach A, et al. Functional remodeling of benign human prostatic tissues in vivo by spontaneously immortalized progenitor and intermediate cells. Stem Cells 2010;28:344-56.
65. Tuxhorn JA, McAlhany SJ, Dang TD, Ayala GE, Rowley DR. Stromal cells promote angiogenesis and growth of human prostate tumors in a differential reactive stroma (DRS) xenograft model. Cancer Res 2002; 62:3298-307.
66. Yang F, Tuxhorn JA, Ressler SJ, McAlhany SJ, Dang TD, Rowley DR. Stromal expression of connective tissue growth factor promotes angiogenesis and prostate cancer tumorigenesis. Cancer Res 2005; 65:8887-95.
67. Yang F, Strand DW, Rowley DR. Fibroblast growth factor-2 mediates transforming growth factor-beta action in prostate cancer reactive stroma. Oncogene 2008;27:450-9.
68. Cho YM, Takahashi S, Asamoto M, Suzuki S, Inaguma S, Hokaiwado N, et al. Age-dependent histopathological findings in the prostate of probasin/SV40 T antigen transgenic rats:lack of influence of carcinogen or testosterone treatment. Cancer Sci 2003;94:153-7.
69. Leroy BE, Northrup N. Prostate cancer in dogs: comparative and clinical aspects. Vet J 2009;180:149-62.
70. Lai CL, van den Ham R, van Leenders G, van der Lugt J, Mol JA, Teske E. Histopathological and immunohistochemical characterization of canine prostate cancer. Prostate 2008;68:477-88.
71. Khanna C, London C, Vail D, Mazcko C, Hirschfeld S. Guiding the optimal translation of new cancer treatments from canine to human cancer patients. Clin Cancer Res 2009;15:5671-7.
72. Giri D, Ropiquet F, Ittmann M. Alterations in expression of basic fibroblast growth factor (FGF) 2 and its receptor FGFR-1 in human prostate cancer. Clin Cancer Res 1999;5:1063-71.
73. Ayala G, Tuxhorn JA, Wheeler TM, Frolov A, Scardino PT, Ohori M, et al. Reactive stroma as a predictor of biochemical-free recurrence in prostate cancer. Clin Cancer Res 2003;9:4792-801.
74. Ayala GE, Muezzinoglu B, Hammerich KH, Frolov A, Liu H, Scardino PT, et al. Determining prostate cancer-specific death through quantification of stromogenic carcinoma area in prostatectomy specimens. Am J Pathol 2011;178:79-87.