Genetically engineered murine models of prostate cancer: Insights into mechanisms of tumorigenesis and potential utility

Future Oncology

Volumn 1, Issue 3, 2005, Pages 351-360

  Abdulkadir, Sarki A ^a   Kim, Jongchan ^a  

^a University of Alabama at Birmingham   (United States)

Author keywords

androgen; chemoprevention; haploinsufficiency; prostate cancer; rostatic intraepithelial neoplasia; therapy; transgenic mice; tumor suppressor

Indexed keywords

ANIMAL; DISEASE MODEL; GENETICS; HUMAN; MALE; MOUSE; MOUSE MUTANT; PATHOLOGY; PROSTATE TUMOR; REVIEW; TRANSGENIC ANIMAL;

ANIMALS; ANIMALS, GENETICALLY MODIFIED; DISEASE MODELS, ANIMAL; HUMANS; MALE; MICE; MICE, KNOCKOUT; PROSTATIC NEOPLASMS;

EID: 33646438584     PISSN: 14796694     EISSN: 17448301     Source Type: Journal    
DOI: 10.1517/14796694.1.3.351     Document Type: Review

References (91)

1. Bieberich CJ, Fujita K, He WW, Jay G: Prostate-specific and androgen-dependent expression of a novel homeobox gene. J. Biol. Chem. 271, 31779-31782 (1996).
2. Bowen C, Bubendorf L, Voeller HJ et al.: Loss of NKX3.1 expression in human prostate cancers correlates with tumor progression. Cancer Res. 60, 6111-6115 (2000).
3. Bhatia-Gaur R, Donjacour AA, Sciavolino PJ et al.: Roles for Nkx3.1 in prostate development and cancer. Genes Dev. 13, 966-977 (1999).
4. Abdulkadir SA, Magee JA, Peters TJ et al.: Conditional loss of Nkx3.1 in adult mice induces prostatic intraepithelial neoplasia. Mol. Cell Biol. 22, 1495-1503 (2002).
5. Magee JA, Abdulkadir SA, Milbrandt J: Haploinsufficiency at the Nkx3.1 locus. A paradigm for stochastic, dosage-sensitive gene regulation during tumor initiation. Cancer Cell 3, 273-283 (2003).
6. Stanbrough M, Leav I, Kwan PW, Bubley GJ, Balk SP: Prostatic intraepithelial neoplasia in mice expressing an androgen receptor transgene in prostate epithelium. Proc. Natl Acad. Sci. USA 98, 10823-10828 (2001).
7. Han G, Buchanan G, Ittmann M et al.: Mutation of the androgen receptor causes oncogenic transformation of the prostate. Proc. Natl Acad. Sci. USA 102, 1151-1156 (2005).
8. Sun M, Wang G, Paciga JE et al.: AKT1/PKBá kinase is frequently elevated in human cancers and its constitutive activation is required for oncogenic transformation in NIH3T3 cells. Am. J. Pathol. 159, 431-437 (2001).
9. Majumder PK, Yeh JJ, George DJ et al.: Prostate intraepithelial neoplasia induced by prostate restricted Akt activation: the MPAKT model. Proc. Natl Acad. Sci. USA 100, 7841-7846 (2003).
10. Fleming WH, Hamel A, MacDonald R et al.: Expression of the c-myc protooncogene in human prostatic carcinoma and benign prostatic hyperplasia. Cancer Res. 46, 1535-1538 (1986).
11. 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. 57, 524-531 (1997).
12. Qian J, Jenkins RB, Bostwick DG: Detection of chromosomal anomalies and cmyc gene amplification in the cribriform pattern of prostatic intraepithelial neoplasia and carcinoma by fluorescence in situ hybridization. Mod. Pathol. 10, 1113-1119 (1997).
13. Nesbit CE, Tersak JM, Prochownik EV: MYC oncogenes and human neoplastic disease. Oncogene 18, 3004-3016 (1999).
14. Sato K, Qian J, Slezak JM et al.: Clinical significance of alterations of chromosome 8 in high-grade, advanced, nonmetastatic prostate carcinoma. J. Natl Cancer Inst. 91, 1574-1580 (1999).
15. Zhang X, Lee C, Ng PY, Rubin M, Shabsigh A, Buttyan R: Prostatic neoplasia in transgenic mice with prostate-directed overexpression of the c-myc oncoprotein. Prostate 43, 278-285 (2000).
16. Ellwood-Yen K, Graeber TG, Wongvipat J et al.: Myc-driven murine prostate cancer shares molecular features with human prostate tumors. Cancer Cell 4, 223-238 (2003).
17. Castrillon DH, DePinho RA: Modeling prostate cancer in the mouse. Adv. Cancer Res. 82, 187-204 (2001).
18. Scherl A, Li JF, Cardiff RD, Schreiber-Agus N: Prostatic intraepithelial neoplasia and intestinal metaplasia in prostates of probasin-RAS transgenic mice. Prostate 59, 448-459 (2004).
19. Chambon P: A decade of molecular biology of retinoic acid receptors. FASEB J. 10, 940-954 (1996).
20. Pandey KK, Batra SK: RXRá: a novel target for prostate cancer. Cancer Biol. Ther. 2, 185-186 (2003).
21. Zhong C, Yang S, Huang J, Cohen MB, Roy-Burman P: Aberration in the expression of the retinoid receptor, RXRá, in prostate cancer. Cancer Biol. Ther. 2, 179-184 (2003).
22. Huang J, Powell WC, Khodavirdi AC et al.: Prostatic intraepithelial neoplasia in mice with conditional disruption of the retinoid X receptor á allele in the prostate epithelium. Cancer Res. 62, 4812-4819 (2002).
23. Weinberg RA: The retinoblastoma protein and cell cycle control. Cell 81, 323-330 (1995).
24. Kranenburg O, van der Eb AJ, Zantema A: Cyclin-dependent kinases and pRb: regulators of the proliferation-differentiation switch. FEBS Lett. 367, 103-106 (1995).
25. Brooks JD, Bova GS, Isaacs WB: Allelic loss of the retinoblastoma gene in primary human prostatic adenocarcinomas. Prostate 26, 35-39 (1995).
26. Bookstein R, Shew JY, Chen PL, Scully P, Lee WH: Suppression of tumorigenicity of human prostate carcinoma cells by replacing a mutated RB gene. Science 247, 712-715 (1990).
27. Kubota Y, Fujinami K, Uemura H et al.: Retinoblastoma gene mutations in primary human prostate cancer. Prostate 27, 314-320 (1995).
28. Maddison LA, Sutherland BW, Barrios RJ, Greenberg NM: Conditional deletion of Rb causes early stage prostate cancer. Cancer Res. 64, 6018-6025 (2004).
29. Basilico C, Moscatelli D: The FGF family of growth factors and oncogenes. Adv. Cancer Res. 59, 115-165 (1992).
30. McKeehan WL, Wang F, Kan M: The heparan sulfate-fibroblast growth factor family: diversity of structure and function. Prog. Nucleic Acid Res. Mol. Biol. 59, 135-176 (1998).
31. Cunha GR, Alarid ET, Turner T, Donjacour AA, Boutin EL, Foster BA: Normal and abnormal development of the male urogenital tract. Role of androgens, mesenchymal-epithelial interactions, and growth factors. J. Androl. 13, 465-475 (1992).
32. Heer R, Douglas D, Mathers ME, Robson CN, Leung HY: Fibroblast growth factor 17 is overexpressed in human prostate cancer. J. Pathol. 204, 578-586 (2004).
33. Polnaszek N, Kwabi-Addo B, Peterson LE et al.: Fibroblast growth factor 2 promotes tumor progression in an autochthonous mouse model of prostate cancer. Cancer Res. 63, 5754-5760 (2003).
34. Ozen M, Giri D, Ropiquet F, Mansukhani A, Ittmann M: Role of fibroblast growth factor receptor signalling in prostate cancer cell survival. J. Natl Cancer Inst. 93, 1783-1790 (2001).
35. Ropiquet F, Giri D, Kwabi-Addo B, Mansukhani A, Ittmann M: Increased expression of fibroblast growth factor 6 in human prostatic intraepithelial neoplasia and prostate cancer. Cancer Res. 60, 4245-4250 (2000).
36. Mydlo JH, Michaeli J, Heston WD, Fair WR: Expression of basic fibroblast growth factor mRNA in benign prostatic hyperplasia and prostatic carcinoma. Prostate 13, 241-247 (1988).
37. Konno-Takahashi N, Takeuchi T, Nishimatsu H et al.: Engineered FGF-2 Expression Induces Glandular Epithelial Hyperplasia in theMurine Prostatic Dorsal Lobe. Eur. Urol. 46, 126-132 (2004).
38. Foster BA, Evangelou A, Gingrich JR, Kaplan PJ, DeMayo F, Greenberg NM: Enforced expression of FGF-7 promotes epithelial hyperplasia whereas a dominant negative FGFR23b promotes the emergence of neuroendocrine phenotype in prostate glands of transgenic mice. Differentiation 70, 624-632 (2002).
39. Chua SS, Ma Z-Q, Gong L, Lin SH, DeMayo FJ, Tsai SY: Ectopic expression of FGF-3 results in abnormal prostate and Wolffian duct development. Oncogene 21, 1899-1908 (2002).
40. Freeman KW, Welm BE, Gangula RD et al.: Inducible prostate intraepithelial neoplasia with reversible hyperplasia in conditional FGFR1-expressing mice. Cancer Res. 63, 8256-8263 (2003).
41. Jin C, McKeehan K, Guo W et al.: Cooperation between ectopic FGFR1 and depression of FGFR2 in induction of prostatic intraepithelial neoplasia in the mouse prostate. Cancer Res. 63, 8784-8790 (2003).
42. Roy-Burman P, Wu H, Powell WC, Hagenkord J, Cohen MB: Genetically defined mouse models that mimic natural aspects of human prostate cancer development. Endocr. Relat. Cancer 11, 225-254 (2004).
43. Shim EH, Johnson L, Noh HL et al.: Expression of the F-box protein SKP2 induces hyperplasia, dysplasia, and lowgrade carcinoma in the mouse prostate. Cancer Res. 63, 1583-1588 (2003).
44. Gary B, Azuero R, Mohanty GS, Bell WC, Eltoum IE, Abdulkadir SA: Interaction of Nkx3.1 and p27kip1 in prostate tumor initiation. Am. J. Pathol. 164, 1607-1614 (2004).
45. Costello LC, Franklin RB: Effect of prolactin on the prostate. Prostate 24, 162-166 (1994).
46. Reiter E, Hennuy B, Bruyninx M et al.: Effects of pituitary hormones on the prostate. Prostate 38, 159-165 (1999).
47. Kindblom J, Dillner K, Sahlin L et al.: Prostate hyperplasia in a transgenic mouse with prostate-specific expression of prolactin. Endocrinology 144, 2269-2278 (2003).
48. Couse JF, Lindzey J, Grandien K, Gustafsson JA, Korach, KS: Tissue distribution and quantitative analysis of oestrogen receptor-á (ERá) and oestrogen receptor- (ER) messenger ribonucleic acid in the wild type and ERá-knockout mouse. Endocrinology 138, 4613-4621 (1997).
49. Prins GS, Birch L, Couse JF, Choi I, Katzenellenbogen B, Korach KS: Estrogen imprinting of the developing prostate gland is mediated through stromal oestrogen receptor á: studies with áERKO and betaERKO mice. Cancer Res. 61, 6089-6097 (2001).
50. Krege JH, Hodgin JB, Couse JF et al.: Generation and reproductive phenotypes of mice lacking oestrogen receptor . Proc. Natl Acad. Sci. USA 95, 15677-15682 (1998).
51. Weihua Z, Mäkelä S, Andersson LC et al.: A role for oestrogen receptor beta in the regulation of growth of the ventral prostate. Proc. Natl Acad. Sci. USA 98, 6330-6335 (2001).
52. Guo QM, Malek RL, Kim S et al.: Identification of c-myc responsive genes using rat cDNA microarray. Cancer Res. 60, 5922-5928 (2000).
53. Kim MJ, Cardiff RD, Desai N et al.: Cooperativity of Nkx3.1 and Pten loss of function in a mouse model of prostate carcinogenesis. Proc. Natl Acad. Sci. USA 99, 2884-2889 (2002).
54. Kasper S, Sheppard PC, Yan Y et al.: Development, progression, and androgendependence of prostate tumors in probasinlarge T antigen transgenic mice: a model for prostate cancer. Lab. Invest. 78, 1-15 (1998).
55. Masumori N, Thomas TZ, Chaurand P et al.: A probasin-large T antigen transgenic mouse line develops prostate adenocarcinoma and neuroendocrine carcinoma with metastatic potential. Cancer Res. 61, 2239-2249 (2001).
56. Klezovitch O, Chevillet J, Mirosevich J, Roberts RL, Matusik RJ, Vasioukhin V: Hepsin promotes prostate cancer progression and metastasis. Cancer Cell 6, 185-195 (2004).
57. Trotman LC, Niki M, Dotan ZA et al.: Pten dose dictates cancer progression in the prostate. PLoS Biol. 1, E59 (2003).
58. Greenberg NM, DeMayo F, Finegold MJ et al.: Prostate cancer in a transgenic mouse. Proc. Natl Acad. Sci. USA 92, 3439-3443 (1995).
59. Gingrich JR, Barrios RJ, Foster BA, Greenberg NM: Pathologic progression of autochthonous prostate cancer in the TRAMP model. Prostate Cancer Prostatic Dis. 2, 70-75 (1999).
60. Kaplan-Lefko PJ, Chen TM, Ittmann MM et al.: Pathobiology of autochthonous prostate cancer in a preclinical transgenic mouse model. Prostate 55, 219-237 (2003).
61. Abdulkadir SA, Qu Z, Garabedian E et al.: Impaired prostate tumorigenesis in Egr1- deficient mice. Naure Med. 7, 101-117 (2001).
62. Eid MA, Kumar MV, Iczkowski KA, Bostwick DG, Tindall DJ: Expression of early growth response genes in human prostate cancer. Cancer Res. 58, 2461-2468 (1998).
63. Shibata MA, Ward JM, Devor DE, Liu ML, Green JE: Progression of prostatic intraepithelial neoplasia to invasive carcinoma in C3(1)/SV40 large T antigen transgenic mice: histopathological and molecular biological alterations. Cancer Res. 56, 4894-4903 (1996).
64. Gabril MY, Onita T, Ji PG et al.: Prostate targeting: PSP94 gene promoter/enhancer region directed prostate tissue-specific expression in a transgenic mouse prostate cancer model. Gene Ther. 9, 1589-1599 (2002).
65. Skalnik DG, Dorfman DM, Williams DA, Orkin SH: Restriction of neuroblastoma to the prostate gland in transgenic mice. Mol. Cell Biol. 11, 4518-4527 (1991).
66. Garabedian EM, Humphrey PA, Gordon JI: A transgenic mouse model of metastatic prostate cancer originating from neuroendocrine cells. Proc. Natl Acad. Sci. USA 95, 15382-15387 (1998).
67. Steck PA, Pershouse MA, Jasser SA et al.: Identification of a candidate tumor suppressor gene, MMAC 1, at chromosome 10q23.3 that is mutated in multiple advanced cancers. Nature Genet. 15(4), 356-362 (1997).
68. Li J, Yen C, Liaw D et al.: PTEN, a putative protein tyrosine phosphatase gene mutated in human brain, breast, and prostate cancer. Science 275, 1943-1947 (1997).
69. Di Cristofano A, Pesce B, Cordon-Cardo C, Pandolfi PP: Pten is essential for embryonic development and tumor suppression. Nature Genet. 19, 348-355 (1998).
70. Wang S, Gao J, Lei Q et al.: Prostate-specific deletion of the murine Pten tumor suppressor gene leads to metastatic prostate cancer. Cancer Cell 4(3), 209-221 (2003).
71. Backman SA, Ghazarian D, So K et al.: Early onset of neoplasia in the prostate and skin of mice with tissue-specific deletion of Pten. Proc. Natl Acad. Sci. USA 101, 1725-1730 (2004).
72. Majumder PK, Febbo PG, Bikoff R et al.: mTOR inhibition reverses Akt-dependent prostate intraepithelial neoplasia through regulation of apoptotic and HIF-1- dependent pathways. Nature Med. 10, 594-601 (2004).
73. Granziero L, Krajewski S, Farness P et al.: Adoptive immunotherapy prevents prostate cancer in a transgenic animal model. Eur. J. Immunol. 29, 1127-1138 (1999).
74. Linsley PS, BradyW, Urnes M, Grosmaire LS, Damle NK, Ledbetter JA: CTLA-4 is a second receptor for the B cell activation antigen B7. J. Exp. Med. 174, 561-569 (1991).
75. Lenschow DJ, Walunas TL, Bluestone JA: CD28/B7 system of T cell costimulation. Ann. Rev. Immunol. 14, 233-258 (1996).
76. Thompson CB, Allison JP: The emerging role of CTLA-4 as an immune attenuator. Immunity 7, 445-450 (1997).
77. Hurwitz AA, Foster BA, Kwon ED et al.: Combination immunotherapy of primary prostate cancer in a transgenic mouse model using CTLA-4 blockade. Cancer Res. 60, 2444-2448 (2000).
78. Wechter WJ, Leipold DD, Murray ED Jr et al.: E-7869 (R-flurbiprofen) inhibits progression of prostate cancer in the TRAMP mouse. Cancer Res. 60, 2203-2208 (2000).
79. Gupta S, Adhami VM, Subbarayan M, et al.: Suppression of prostate carcinogenesis by dietary supplementation of celecoxib in transgenic adenocarcinoma of the mouse prostate model. Cancer Res. 64, 3334-3343 (2004).
80. Gupta S, Ahmad N, Marengo SR, MacLennan GT, Greenberg NM, Mukhtar H: Chemoprevention of prostate carcinogenesis by á- difluoromethylornithine in TRAMP mice. Cancer Res. 60, 5125-5133 (2000).
81. Gupta S, Hastak K, Ahmad N, Lewin JS, Mukhtar H: Inhibition of prostate carcinogenesis in TRAMP mice by oral infusion of green tea polyphenols. Proc. Natl Acad. Sci. USA 98, 10350-10355 (2001).
82. Mentor-Marcel R, Lamartiniere CA, Eltoum IE, Greenberg NM, Elgavish A: Genistein in the diet reduces the incidence of poorly differentiated prostatic adenocarcinoma in transgenic mice (TRAMP). Cancer Res. 61, 6777-6782 (2001).
83. Raghow S, Hooshdaran MZ, Katiyar S, Steiner MS: Toremifene prevents prostate cancer in the transgenic adenocarcinoma of mouse prostate model. Cancer Res. 62, 1370-1376 (2002).
84. Huss WJ, Lai L, Barrios RJ, Hirschi KK, Greenberg NM: Retinoic acid slows progression and promotes apoptosis of spontaneous prostate cancer. Prostate 61, 142-152 (2004).
85. Venkateswaran V, Fleshner NE, Sugar LM, Klotz LH: Antioxidants block prostate cancer in lady transgenic mice. Cancer Res. 64, 5891-5896 (2004).
86. Martiniello-Wilks R, Tsatralis T, Russell P et al.: Transcription- targeted gene therapy for androgen-independent prostate cancer. Cancer Gene Ther. 9, 443-452 (2002).
87. Voeks D, Martiniello-Wilks R, Madden V et al.: Gene therapy for prostate cancer delivered by ovine adenovirus and mediated by purine nucleoside phosphorylase and fludarabine in mouse models. Gene Ther. 9, 759-768 (2002).
88. Secrist JA 3rd, Parker WB, Allan PW et al.: Gene therapy of cancer: activation of nucleoside prodrugs with E. coli purine nucleoside phosphorylase. Nucleosides Nucleotides 19, 745-757 (1999).
89. Martiniello-Wilks R, Dane A, Voeks DJ et al.: Gene-directed enzyme prodrug therapy for prostate cancer in a mouse model that imitates the development of human disease. J. Gene Med. 6, 43-54 (2004).
90. Bhowmick NA, Chytil A, Plieth D et al.: TGF- signalling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 303, 848-851 (2004).
91. Shappell SB, Thomas GV, Roberts RL 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. 64, 2270-2305 (2004).