Murine Models of Prostate Cancer

  • Eric C. Kauffman
  • Casey K. Ng
  • Carrie Rinker-Schaeffer
Chapter
First Online:

Abstract

Preclinical investigation of prostate cancer (CaP) has been greatly assisted by the availability of animal models which enable experimentation in physiologic tissue microenvironments that cannot be recapitulated by current in vitro platforms. Such modeling is necessary to study carcinogenesis steps requiring interaction between the cancer cell and microenvironment, such as local invasion, circulatory transit/dissemination, lodging and survival of tumor cells at secondary tissue sites, and tumorigenesis itself. Animal models thus provide invaluable preclinical tools for elucidating molecular mechanisms of CaP carcinogenesis and testing novel CaP therapies. This chapter reviews different approaches to murine modeling of CaP and summarizes various models with respect to their histology, androgen sensitivity, invasiveness, metastatic potential, molecular profiles and preclinical discoveries.

Keywords

Androgen Receptor Bone Metastasis Prostate Tumor Prostatic Intraepithelial Neoplasia Ventral Lobe 
These keywords were added by machine and not by the authors. This process is experimental and the keywords may be updated as the learning algorithm improves.
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References

  1. 1.
    Cunha GR, Donjacour AA, Cooke PS, et al. The endocrinology and developmental biology of the prostate. Endocr Rev. 1987;8:338.PubMedCrossRefGoogle Scholar
  2. 2.
    Sugimura Y, Cunha GR, Donjacour AA. Morphogenesis of ductal networks in the mouse prostate. Biol Reprod. 1986;34:961.PubMedCrossRefGoogle Scholar
  3. 3.
    Shirai T, Takahashi S, Cui L, et al. Experimental prostate carcinogenesis - rodent models. Mutat Res. 2000;462:219.PubMedCrossRefGoogle Scholar
  4. 4.
    Pollard M. Spontaneous prostate adenocarcinomas in aged germfree Wistar rats. J Natl Cancer Inst. 1973;51:1235.PubMedGoogle Scholar
  5. 5.
    Pollard M. Lobund-Wistar rat model of prostate cancer in man. Prostate. 1998;37:1.PubMedCrossRefGoogle Scholar
  6. 6.
    Pugh TD, Chang C, Uemura H, et al. Prostatic localization of spontaneous early invasive carcinoma in Lobund-Wistar rats. Cancer Res. 1994;54:5766.PubMedGoogle Scholar
  7. 7.
    Suckow MA, Wheeler J, Yan M. PAIII prostate tumors express prostate specific antigen (PSA) in Lobund-Wistar rats. Can J Vet Res. 2009;73:39.PubMedGoogle Scholar
  8. 8.
    Pollard M. Prevention of prostate-related cancers in Lobund-Wistar rats. Prostate. 1999;39:305.PubMedCrossRefGoogle Scholar
  9. 9.
    Chan SY. Androgen and glucocorticoid receptors in the Pollard prostate adenocarcinoma cell lines. Prostate. 1980;1:53.PubMedCrossRefGoogle Scholar
  10. 10.
    Pollard M. Dihydrotestosterone prevents spontaneous adenocarcinomas in the prostate-seminal vesicle in aging L-W rats. Prostate. 1998;36:168.PubMedCrossRefGoogle Scholar
  11. 11.
    Pollard M, Snyder DL, Luckert PH. Dihydrotestosterone does not induce prostate adenocarcinoma in L-W rats. Prostate. 1987;10:325.PubMedCrossRefGoogle Scholar
  12. 12.
    Pollard M, Suckow MA. Dietary prevention of hormone refractory prostate cancer in Lobund-Wistar rats: a review of studies in a relevant animal model. Comp Med. 2006;56:461.PubMedGoogle Scholar
  13. 13.
    Isaacs JT. The aging ACI/Seg versus Copenhagen male rat as a model system for the study of prostatic carcinogenesis. Cancer Res. 1984;44:5785.PubMedGoogle Scholar
  14. 14.
    Shain SA, McCullough B, Segaloff A. Spontaneous adenocarcinomas of the ventral prostate of aged A X C rats. J Natl Cancer Inst. 1975;55:177.PubMedGoogle Scholar
  15. 15.
    Homma Y, Kaneko M, Kondo Y, et al. Inhibition of rat prostate carcinogenesis by a 5alpha-reductase inhibitor, FK143. J Natl Cancer Inst. 1997;89:803.PubMedCrossRefGoogle Scholar
  16. 16.
    Ward JM, Reznik G, Stinson SF, et al. Histogenesis and morphology of naturally occurring prostatic carcinoma in the ACI/segHapBR rat. Lab Invest. 1980;43:517.PubMedGoogle Scholar
  17. 17.
    Varma VA, Austin GE. Morphologic characterization of early prostatic carcinomas in the ACI rat: a light and electron microscopic study. Exp Mol Pathol. 1990;52:202.PubMedCrossRefGoogle Scholar
  18. 18.
    Shain SA, Boesel RW, Kalter SS, et al. AXC rat prostatic adenocarcinoma: characterization of cells in culture. Adv Exp Med Biol. 1981;138:337.PubMedCrossRefGoogle Scholar
  19. 19.
    Shain SA, Huot RI, Gorelic LS, et al. Biochemical and morphological characterization of clonal AXC rat prostate cancer cells. Cancer Res. 1984;44:2033.PubMedGoogle Scholar
  20. 20.
    Huot RI, Shain SA. Differential androgen modulation of AXC/SSh rat prostate cancer cell proliferation in vitro and its antagonism by antiandrogen. Cancer Res. 1986;46:3775.PubMedGoogle Scholar
  21. 21.
    Kondo Y, Homma Y, Aso Y, et al. Promotional effect of two-generation exposure to a high-fat diet on prostate carcinogenesis in ACI/Seg rats. Cancer Res. 1994;54:6129.PubMedGoogle Scholar
  22. 22.
    Homma Y, Kondo Y, Kaneko M, et al. Promotion of carcinogenesis and oxidative stress by dietary cholesterol in rat prostate. Carcinogenesis. 2004;25:1011.PubMedCrossRefGoogle Scholar
  23. 23.
    Yamashita S, Suzuki S, Nomoto T, et al. Linkage and microarray analyses of susceptibility genes in ACI/Seg rats: a model for prostate cancers in the aged. Cancer Res. 2005;65:2610.PubMedCrossRefGoogle Scholar
  24. 24.
    Dunning WF. Prostate cancer in the rat. Natl Cancer Inst Monogr. 1963;12:351.PubMedGoogle Scholar
  25. 25.
    Noble RL. The development of prostatic adenocarcinoma in Nb rats following prolonged sex hormone administration. Cancer Res. 1977;37:1929.PubMedGoogle Scholar
  26. 26.
    Reznik G, Hamlin 2nd MH, Ward JM, et al. Prostatic hyperplasia and neoplasia in aging F344 rats. Prostate. 1981;2:261.PubMedCrossRefGoogle Scholar
  27. 27.
    Pollard M, Luckert PH. Prostate cancer in a Sprague-Dawley rat. Prostate. 1985;6:389.PubMedCrossRefGoogle Scholar
  28. 28.
    Pollard M, Luckert PH. Autochthonous prostate adenocarcinomas in Lobund-Wistar rats: a model system. Prostate. 1987;11:219.PubMedCrossRefGoogle Scholar
  29. 29.
    McCormick DL, Rao KV, Dooley L, et al. Influence of N-methyl-N-nitrosourea, testosterone, and N-(4-hydroxyphenyl)-all-trans-retinamide on prostate cancer induction in Wistar-Unilever rats. Cancer Res. 1998;58:3282.PubMedGoogle Scholar
  30. 30.
    Noble RL. Prostate carcinoma of the Nb rat in relation to hormones. Int Rev Exp Pathol. 1982;23:113.PubMedGoogle Scholar
  31. 31.
    Drago JR. The induction of NB rat prostatic carcinomas. Anticancer Res. 1984;4:255.PubMedGoogle Scholar
  32. 32.
    Leav I, Ho SM, Ofner P, et al. Biochemical alterations in sex hormone-induced hyperplasia and dysplasia of the dorsolateral prostates of noble rats. J Natl Cancer Inst. 1988;80:1045.PubMedCrossRefGoogle Scholar
  33. 33.
    Wientjes G, Smith J, Miller R, et al. Noble PRST-1 Ca prostate adenocarcinoma study on noble rats: preliminary study on new androgen sensitive tumor. In Vivo. 1989;3:335.PubMedGoogle Scholar
  34. 34.
    Drago JR. Chemotherapeutic treatment of the Nb rat adenocarcinoma androgen-insensitive tumor III. J Surg Oncol. 1982;21:264.PubMedCrossRefGoogle Scholar
  35. 35.
    Drago JR, Murray C. Control of metastases in the Nb rat prostatic adenocarcinoma model. J Androl. 1984;5:265.PubMedGoogle Scholar
  36. 36.
    Drago JR, Worgul T, Gershwin ME. Combination chemotherapy in a prostate tumor model: Nb rat prostatic adenocarcinoma model. J Surg Oncol. 1981;16:353.PubMedCrossRefGoogle Scholar
  37. 37.
    Pollard M, Luckert PH, Snyder D. Prevention and treatment of experimental prostate cancer in Lobund-Wistar rats. I. Effects of estradiol, dihydrotestosterone, and castration. Prostate. 1989; 15:95.PubMedCrossRefGoogle Scholar
  38. 38.
    Bentel JM, Pickering MA, Pollard M, et al. Androgen receptor expression in primary prostate cancers of Lobund-Wistar rats and in tumor-derived cell lines. In Vitro Cell Dev Biol Anim. 1999;35:655.PubMedCrossRefGoogle Scholar
  39. 39.
    Bosland MC, Prinsen MK. Induction of dorsolateral prostate adenocarcinomas and other accessory sex gland lesions in male Wistar rats by a single administration of N-methyl-N-nitrosourea, 7,12-dimethylbenz(a)anthracene, and 3,2′-dimethyl-4-aminobiphenyl after sequential treatment with cyproterone acetate and testosterone propionate. Cancer Res. 1990;50:691.PubMedGoogle Scholar
  40. 40.
    Bosland MC, Prinsen MK, Dirksen TJ, et al. Characterization of adenocarcinomas of the dorsolateral prostate induced in Wistar rats by N-methyl-N-nitrosourea, 7,12-dimethylbenz(a)anthracene, and 3,2′-dimethyl-4-aminobiphenyl, following sequential treatment with cyproterone acetate and testosterone propionate. Cancer Res. 1990;50:700.PubMedGoogle Scholar
  41. 41.
    McCormick DL, Rao KV, Johnson WD, et al. Null activity of selenium and vitamin e as cancer chemopreventive agents in the rat prostate. Cancer Prev Res (Phila). 2010;3:381.CrossRefGoogle Scholar
  42. 42.
    Liao Z, Wang S, Boileau TW, et al. Increased phospho-AKT is associated with loss of the androgen receptor during the progression of N-methyl-N-nitrosourea-induced prostate carcinogenesis in rats. Prostate. 2005;64:186.PubMedCrossRefGoogle Scholar
  43. 43.
    Banudevi S, Elumalai P, Arunkumar R, et al. Chemopreventive effects of zinc on prostate carcinogenesis induced by N-methyl-N-nitrosourea and testosterone in adult male Sprague-Dawley rats. J Cancer Res Clin Oncol. 2010;137:677.PubMedCrossRefGoogle Scholar
  44. 44.
    Sarkar DK, Boyadjieva NI, Chen CP, et al. Cyclic adenosine monophosphate differentiated beta-endorphin neurons promote immune function and prevent prostate cancer growth. Proc Natl Acad Sci U S A. 2008;105:9105.PubMedCrossRefGoogle Scholar
  45. 45.
    Maekawa A, Matsuoka C, Onodera H, et al. Organ-specific carcinogenicity of N-methyl-N-nitrosourea in F344 and ACI/N rats. J Cancer Res Clin Oncol. 1985;109:178.PubMedCrossRefGoogle Scholar
  46. 46.
    Pollard M, Wolter W, Sun L. Prevention of induced prostate-related cancer by soy protein isolate/isoflavone-supplemented diet in Lobund-Wistar rats. In Vivo. 2000;14:389.PubMedGoogle Scholar
  47. 47.
    Sukumar S, Armstrong B, Bruyntjes JP, et al. Frequent activation of the Ki-ras oncogene at codon 12 in N-methyl-N-nitrosourea-induced rat prostate adenocarcinomas and neurogenic sarcomas. Mol Carcinog. 1991;4:362.PubMedCrossRefGoogle Scholar
  48. 48.
    McCormick DL, Johnson WD, Bosland MC, et al. Chemoprevention of rat prostate carcinogenesis by soy isoflavones and by Bowman-Birk inhibitor. Nutr Cancer. 2007;57:184.PubMedCrossRefGoogle Scholar
  49. 49.
    Arunkumar A, Vijayababu MR, Venkataraman P, et al. Chemoprevention of rat prostate carcinogenesis by diallyl disulfide, an organosulfur compound of garlic. Biol Pharm Bull. 2006;29:375.PubMedCrossRefGoogle Scholar
  50. 50.
    Wilson MJ, Lindgren BR, Sinha AA. The effect of dietary supplementation with limonene or myo-inositol on the induction of neoplasia and matrix metalloproteinase and plasminogen activator activities in accessory sex organs of male Lobund-Wistar rats. Exp Mol Pathol. 2008;85:83.PubMedCrossRefGoogle Scholar
  51. 51.
    Bisson JF, Nejdi A, Rozan P, et al. Effects of long-term administration of a cocoa polyphenolic extract (Acticoa powder) on cognitive performances in aged rats. Br J Nutr. 2008;100:94.PubMedCrossRefGoogle Scholar
  52. 52.
    Narayanan NK, Nargi D, Horton L, et al. Inflammatory processes of prostate tissue microenvironment drive rat prostate carcinogenesis: preventive effects of celecoxib. Prostate. 2009;69:133.PubMedCrossRefGoogle Scholar
  53. 53.
    Ito N, Shirai T, Tagawa Y, et al. Variation in tumor yield in the prostate and other target organs of the rat in response to varied dosage and duration of administration of 3,2′-dimethyl-4-aminobiphenyl. Cancer Res. 1988;48:4629.PubMedGoogle Scholar
  54. 54.
    Shirai T, Nakamura A, Fukushima S, et al. Different carcinogenic responses in a variety of organs, including the prostate, of five different rat strains given 3,2′-dimethyl-4-aminobiphenyl. Carcinogenesis. 1990;11:793.PubMedCrossRefGoogle Scholar
  55. 55.
    Shirai T, Takahashi S, Mori T, et al. Immunohistochemically demonstrated androgen receptor expression in the rat prostate during carcinogenesis induced by 3,2′-dimethyl-4-aminobiphenyl with or without testosterone. Urol Oncol. 1995;1:263.PubMedCrossRefGoogle Scholar
  56. 56.
    Yamauchi A, Kawai K, Tsukamoto S, et al. Persistence of prostatic intraepithelial neoplasia after effective chemoprevention of microscopic prostate cancer with antiandrogen in a rat model. J Urol. 2006;175:348.PubMedCrossRefGoogle Scholar
  57. 57.
    Takai K, Kakizoe T, Tanaka Y, et al. Trial to induce prostatic cancer in ACI/Seg rats treated with a combination of 3,2′-dimethyl-4-aminobiphenyl and ethinyl estradiol. Jpn J Cancer Res. 1991;82:286.PubMedCrossRefGoogle Scholar
  58. 58.
    Shirai T, Tamano S, Kato T, et al. Induction of invasive carcinomas in the accessory sex organs other than the ventral prostate of rats given 3,2′-dimethyl-4-aminobiphenyl and testosterone propionate. Cancer Res. 1991;51:1264.PubMedGoogle Scholar
  59. 59.
    Yaono M, Tamano S, Mori T, et al. Lobe specific effects of testosterone and estrogen on 3,2′-dimethyl-4-aminobiphenyl-induced rat prostate carcinogenesis. Cancer Lett. 2000;150:33.PubMedCrossRefGoogle Scholar
  60. 60.
    Shirai T, Imaida K, Masui T, et al. Effects of testosterone, dihydrotestosterone and estrogen on 3,2′-dimethyl-4-aminobiphenyl-induced rat prostate carcinogenesis. Int J Cancer. 1994;57:224.PubMedCrossRefGoogle Scholar
  61. 61.
    Shirai T, Sakata T, Fukushima S, et al. Rat prostate as one of the target organs for 3,2′-dimethyl-4-aminobiphenyl-induced carcinogenesis: effects of dietary ethinyl estradiol and methyltestosterone. Jpn J Cancer Res. 1985;76:803.PubMedGoogle Scholar
  62. 62.
    Akaza H, Tsukamoto S, Morita T, et al. Promoting effects of antiandrogenic agents on rat ventral prostate carcinogenesis induced by 3,2′-dimethyl-4-aminobiphenyl (DMAB). Prostate Cancer Prostatic Dis. 2000;3:115.PubMedCrossRefGoogle Scholar
  63. 63.
    Iwasaki S, Kato K, Mori T, et al. Development of androgen-independent carcinomas from androgen-dependent preneoplastic lesions in the male accessory sex organs of rats treated with 3,2′-dimethyl-4-aminobiphenyl and testosterone propionate. Jpn J Cancer Res. 1999;90:23.PubMedCrossRefGoogle Scholar
  64. 64.
    Nakanishi H, Takeuchi S, Kato K, et al. Establishment and characterization of three androgen-independent, metastatic carcinoma cell lines from 3,2′-dimethyl-4-aminobiphenyl-induced prostatic tumors in F344 rats. Jpn J Cancer Res. 1996;87:1218.PubMedCrossRefGoogle Scholar
  65. 65.
    Yamashita S, Takahashi S, McDonell N, et al. Methylation silencing of transforming growth factor-beta receptor type II in rat prostate cancers. Cancer Res. 2008;68:2112.PubMedCrossRefGoogle Scholar
  66. 66.
    Masui T, Shirai T, Imaida K, et al. Ki-ras mutations with frequent normal allele loss versus absence of p53 mutations in rat prostate and seminal vesicle carcinomas induced with 3,2′-dimethyl-4-aminobiphenyl. Mol Carcinog. 1995;13:21.PubMedCrossRefGoogle Scholar
  67. 67.
    Kohno H, Suzuki R, Sugie S, et al. Dietary supplementation with silymarin inhibits 3,2′-dimethyl-4-aminobiphenyl-induced prostate carcinogenesis in male F344 rats. Clin Cancer Res. 2005;11:4962.PubMedCrossRefGoogle Scholar
  68. 68.
    Mori T, Imaida K, Tamano S, et al. Beef tallow, but not perilla or corn oil, promotion of rat prostate and intestinal carcinogenesis by 3,2′-dimethyl-4-aminobiphenyl. Jpn J Cancer Res. 2001;92:1026.PubMedCrossRefGoogle Scholar
  69. 69.
    Onozawa M, Kawamori T, Baba M, et al. Effects of a soybean isoflavone mixture on carcinogenesis in prostate and seminal vesicles of F344 rats. Jpn J Cancer Res. 1999;90:393.PubMedCrossRefGoogle Scholar
  70. 70.
    Tsukamoto S, Akaza H, Onozawa M, et al. A five-alpha reductase inhibitor or an antiandrogen prevents the progression of microscopic prostate carcinoma to macroscopic carcinoma in rats. Cancer. 1998;82:531.PubMedCrossRefGoogle Scholar
  71. 71.
    Pour PM, Stepan K. Induction of prostatic carcinomas and lower urinary tract neoplasms by combined treatment of intact and castrated rats with testosterone propionate and N-nitrosobis(2-oxopropyl)amine. Cancer Res. 1987;47:5699.PubMedGoogle Scholar
  72. 72.
    Newhall KR, Isaacs JT, Wright Jr GL. Dunning rat prostate tumors and cultured cell lines fail to express human prostate carcinoma-associated antigens. Prostate. 1990;17:317.PubMedCrossRefGoogle Scholar
  73. 73.
    Markland Jr FS, Lee L. Characterization and comparison of the estrogen and androgen receptors from the R-3327 rat prostatic adenocarcinoma. J Steroid Biochem. 1979;10:13.PubMedCrossRefGoogle Scholar
  74. 74.
    Smolev JK, Heston WD, Scott WW, et al. Characterization of the Dunning R3327H prostatic adenocarcinoma: an appropriate animal model for prostatic cancer. Cancer Treat Rep. 1977;61:273.PubMedGoogle Scholar
  75. 75.
    Isaacs JT, Isaacs WB, Feitz WF, et al. Establishment and characterization of seven Dunning rat prostatic cancer cell lines and their use in developing methods for predicting metastatic abilities of prostatic cancers. Prostate. 1986;9:261.PubMedCrossRefGoogle Scholar
  76. 76.
    Isaacs JT, Heston WD, Weissman RM, et al. Animal models of the hormone-sensitive and -insensitive prostatic adenocarcinomas, Dunning R-3327-H, R-3327-HI, and R-3327-AT. Cancer Res. 1978;38:4353.PubMedGoogle Scholar
  77. 77.
    Sestili MA, Norris JS, Smith RG. Isolation and characterization of a cloned cell line R3327H-G8-A1 derived from the dunning R3327H rat adenocarcinoma. Cancer Res. 1983;43:2167.PubMedGoogle Scholar
  78. 78.
    Lee C, Murphy GP, Chu TM. Purification and characterization of acid phosphatase from Dunning R3327H prostatic adenocarcinoma. Cancer Res. 1980;40:1245.PubMedGoogle Scholar
  79. 79.
    Garde SV, Sheth AR, Porter AT, et al. A comparative study on expression of prostatic inhibin peptide, prostate acid phosphatase and prostate specific antigen in androgen independent human and rat prostate carcinoma cell lines. Cancer Lett. 1993;70:159.PubMedCrossRefGoogle Scholar
  80. 80.
    Tennant TR, Kim H, Sokoloff M, et al. The Dunning model. Prostate. 2000;43:295.PubMedCrossRefGoogle Scholar
  81. 81.
    Oltean S, Febbo PG, Garcia-Blanco MA. Dunning rat prostate adenocarcinomas and alternative splicing reporters: powerful tools to study epithelial plasticity in prostate tumors in vivo. Clin Exp Metastasis. 2008;25:611.PubMedCrossRefGoogle Scholar
  82. 82.
    Pfundt R, Smit F, Jansen C, et al. Identification of androgen-responsive genes that are alternatively regulated in androgen-dependent and androgen-independent rat prostate tumors. Genes Chromosomes Cancer. 2005;43:273.PubMedCrossRefGoogle Scholar
  83. 83.
    Kauffman EC, Robinson VL, Stadler WM, et al. Metastasis suppression: the evolving role of metastasis suppressor genes for regulating cancer cell growth at the secondary site. J Urol. 2003;169:1122.PubMedCrossRefGoogle Scholar
  84. 84.
    Oltean S, Sorg BS, Albrecht T, et al. Alternative inclusion of fibroblast growth factor receptor 2 exon IIIc in Dunning prostate tumors reveals unexpected epithelial mesenchymal plasticity. Proc Natl Acad Sci U S A. 2006;103:14116.PubMedCrossRefGoogle Scholar
  85. 85.
    Zhang M, Coen JJ, Suzuki Y, et al. Survivin is a potential mediator of prostate cancer metastasis. Int J Radiat Oncol Biol Phys. 2010;78:1095.PubMedCrossRefGoogle Scholar
  86. 86.
    Blount LV, Cooke 3rd DB. Point mutations in the Ki-ras2 gene of codon 12 in the Dunning R-3327 Prostatic Adenocarcinoma system. Prostate. 1996;28:44.PubMedCrossRefGoogle Scholar
  87. 87.
    Isaacs JT, Coffey DS. Adaptation versus selection as the mechanism responsible for the relapse of prostatic cancer to androgen ablation therapy as studied in the Dunning R-3327-H adenocarcinoma. Cancer Res. 1981;41:5070.PubMedGoogle Scholar
  88. 88.
    Redding TW, Schally AV. Inhibition of prostate tumor growth in two rat models by chronic administration of D-Trp6 analogue of luteinizing hormone-releasing hormone. Proc Natl Acad Sci U S A. 1981;78:6509.PubMedCrossRefGoogle Scholar
  89. 89.
    English HF, Heitjan DF, Lancaster S, et al. Beneficial effects of androgen-primed chemotherapy in the Dunning R3327 G model of prostatic cancer. Cancer Res. 1991;51:1760.PubMedGoogle Scholar
  90. 90.
    George DJ, Dionne CA, Jani J, et al. Sustained in vivo regression of Dunning H rat prostate cancers treated with combinations of androgen ablation and Trk tyrosine kinase inhibitors, CEP-751 (KT-6587) or CEP-701 (KT-5555). Cancer Res. 1999;59:2395.PubMedGoogle Scholar
  91. 91.
    Isaacs JT. Relationship between tumor size and curability of prostatic cancer by combined chemo-hormonal therapy in rats. Cancer Res. 1989;49:6290.PubMedGoogle Scholar
  92. 92.
    Kaminski JM, Hanlon AL, Joon DL, et al. Effect of sequencing of androgen deprivation and radiotherapy on prostate cancer growth. Int J Radiat Oncol Biol Phys. 2003;57:24.PubMedCrossRefGoogle Scholar
  93. 93.
    Xu Y, Dalrymple SL, Becker RE, et al. Pharmacologic basis for the enhanced efficacy of dutasteride against prostatic cancers. Clin Cancer Res. 2006;12:4072.PubMedCrossRefGoogle Scholar
  94. 94.
    Zechmann CM, Woenne EC, Brix G, et al. Impact of stroma on the growth, microcirculation, and metabolism of experimental prostate tumors. Neoplasia. 2007;9:57.PubMedCrossRefGoogle Scholar
  95. 95.
    Morton RA, Isaacs JT, Isaacs WB. Differential effects of growth factor antagonists on neoplastic and normal prostatic cells. Prostate. 1990;17:327.PubMedCrossRefGoogle Scholar
  96. 96.
    Saffrin R, Chou P, Ray V, et al. Suramin as adjuvant therapy with radical prostatectomy. Prostate. 1996;28:325.PubMedCrossRefGoogle Scholar
  97. 97.
    Small EJ, Meyer M, Marshall ME, et al. Suramin therapy for patients with symptomatic hormone-refractory prostate cancer: results of a randomized phase III trial comparing suramin plus hydrocortisone to placebo plus hydrocortisone. J Clin Oncol. 2000;18:1440.PubMedGoogle Scholar
  98. 98.
    Vogelzang NJ, Karrison T, Stadler WM, et al. A Phase II trial of suramin monthly x 3 for hormone-refractory prostate carcinoma. Cancer. 2004;100:65.PubMedCrossRefGoogle Scholar
  99. 99.
    Getzenberg RH, Light BW, Lapco PE, et al. Vitamin D inhibition of prostate adenocarcinoma growth and metastasis in the Dunning rat prostate model system. Urology. 1997;50:999.PubMedCrossRefGoogle Scholar
  100. 100.
    Lindshield BL, Ford NA, Canene-Adams K, et al. Selenium, but not lycopene or vitamin E, decreases growth of transplantable dunning R3327-H rat prostate tumors. PLoS One. 2010;5:e10423.PubMedCrossRefGoogle Scholar
  101. 101.
    Siler U, Barella L, Spitzer V, et al. Lycopene and vitamin E interfere with autocrine/paracrine loops in the Dunning prostate cancer model. FASEB J. 2004;18:1019.PubMedGoogle Scholar
  102. 102.
    Canene-Adams K, Lindshield BL, Wang S, et al. Combinations of tomato and broccoli enhance antitumor activity in dunning r3327-h prostate adenocarcinomas. Cancer Res. 2007;67:836.PubMedCrossRefGoogle Scholar
  103. 103.
    Claflin AJ, McKinney EC, Fletcher MA. The Dunning R3327 prostate adenocarcinoma in the Fischer-Copenhagen F1 rat: a useful model for immunological studies. Oncology. 1977;34:105.PubMedCrossRefGoogle Scholar
  104. 104.
    Sharma N, Luo J, Kirschmann DA, et al. A novel immunological model for the study of prostate cancer. Cancer Res. 1999;59:2271.PubMedGoogle Scholar
  105. 105.
    Joseph IB, Isaacs JT. Macrophage role in the anti-prostate cancer response to one class of antiangiogenic agents. J Natl Cancer Inst. 1998;90:1648.PubMedCrossRefGoogle Scholar
  106. 106.
    Tjota A, Zhang YQ, Piedmonte MR, et al. Adoptive immunotherapy using lymphokine-activated killer cells and recombinant interleukin-2 in preventing and treating spontaneous pulmonary metastases of syngeneic Dunning rat prostate tumor. J Urol. 1991;146:177.PubMedGoogle Scholar
  107. 107.
    Junco JA, Peschke P, Zuna I, et al. Immunotherapy of prostate cancer in a murine model using a novel GnRH based vaccine candidate. Vaccine. 2007;25:8460.PubMedCrossRefGoogle Scholar
  108. 108.
    Moody DB, Robinson JC, Ewing CM, et al. Interleukin-2 transfected prostate cancer cells generate a local antitumor effect in vivo. Prostate. 1994;24:244.PubMedCrossRefGoogle Scholar
  109. 109.
    Halin S, Rudolfsson SH, Van Rooijen N, et al. Extratumoral macrophages promote tumor and vascular growth in an orthotopic rat prostate tumor model. Neoplasia. 2009;11:177.PubMedGoogle Scholar
  110. 110.
    Vieweg J, Boczkowski D, Roberson KM, et al. Efficient gene transfer with adeno-associated virus-based plasmids complexed to cationic liposomes for gene therapy of human prostate cancer. Cancer Res. 1995;55:2366.PubMedGoogle Scholar
  111. 111.
    Henry JM, Isaacs JT. Relationship between tumor size and the curability of metastatic prostatic cancer by surgery alone or in combination with adjuvant chemotherapy. J Urol. 1988;139:1119.PubMedGoogle Scholar
  112. 112.
    Joon DL, Hasegawa M, Sikes C, et al. Supraadditive apoptotic response of R3327-G rat prostate tumors to androgen ablation and radiation. Int J Radiat Oncol Biol Phys. 1997;38:1071.PubMedCrossRefGoogle Scholar
  113. 113.
    Bischof JC, Smith D, Pazhayannur PV, et al. Cryosurgery of ­dunning AT-1 rat prostate tumor: thermal, biophysical, and ­viability response at the cellular and tissue level. Cryobiology. 1997;34:42.PubMedCrossRefGoogle Scholar
  114. 114.
    Chapelon JY, Margonari J, Vernier F, et al. In vivo effects of high-intensity ultrasound on prostatic adenocarcinoma Dunning R3327. Cancer Res. 1992;52:6353.PubMedGoogle Scholar
  115. 115.
    Debus J, Spoo J, Jenne J, et al. Sonochemically induced radicals generated by pulsed high-energy ultrasound in vitro and in vivo. Ultrasound Med Biol. 1999;25:301.PubMedCrossRefGoogle Scholar
  116. 116.
    Oosterhof GO, Cornel EB, Smits GA, et al. Influence of high-intensity focused ultrasound on the development of metastases. Eur Urol. 1997;32:91.PubMedGoogle Scholar
  117. 117.
    Paparel P, Curiel L, Chesnais S, et al. Synergistic inhibitory effect of high-intensity focused ultrasound combined with chemotherapy on Dunning adenocarcinoma. BJU Int. 2005;95:881.PubMedCrossRefGoogle Scholar
  118. 118.
    Standish BA, Lee KK, Jin X, et al. Interstitial Doppler optical coherence tomography as a local tumor necrosis predictor in photodynamic therapy of prostatic carcinoma: an in vivo study. Cancer Res. 2008;68:9987.PubMedCrossRefGoogle Scholar
  119. 119.
    Xiao Z, Halls S, Dickey D, et al. Fractionated versus standard continuous light delivery in interstitial photodynamic therapy of dunning prostate carcinomas. Clin Cancer Res. 2007;13:7496.PubMedCrossRefGoogle Scholar
  120. 120.
    Johannsen M, Thiesen B, Gneveckow U, et al. Thermotherapy using magnetic nanoparticles combined with external radiation in an orthotopic rat model of prostate cancer. Prostate. 2006;66:97.PubMedCrossRefGoogle Scholar
  121. 121.
    Johannsen M, Thiesen B, Jordan A, et al. Magnetic fluid hyperthermia (MFH)reduces prostate cancer growth in the orthotopic Dunning R3327 rat model. Prostate. 2005;64:283.PubMedCrossRefGoogle Scholar
  122. 122.
    Chang CF, Pollard M. In vitro propagation of prostate adenocarcinoma cells from rats. Invest Urol. 1977;14:331.PubMedGoogle Scholar
  123. 123.
    Pollard M, Luckert PH. Effects of dichloromethylene diphosphonate on the osteolytic and osteoplastic effects of rat prostate adenocarcinoma cells. J Natl Cancer Inst. 1985;75:949.PubMedGoogle Scholar
  124. 124.
    Koutsilieris M, Polychronakos C. Proteinolytic activity against IGF-binding proteins involved in the paracrine interactions between prostate adenocarcinoma cells and osteoblasts. Anticancer Res. 1992;12:905.PubMedGoogle Scholar
  125. 125.
    Koutsilieris M. Skeletal metastases in advanced prostate cancer: cell biology and therapy. Crit Rev Oncol Hematol. 1995;18:51.PubMedCrossRefGoogle Scholar
  126. 126.
    Shain SA, McCullough B, Nitchuk WM. Primary and transplantable adenocarcinomas of the A times C rat ventral prostate gland: morphologic characterization and examination of C19-steroid metabolism by early-passage tumors. J Natl Cancer Inst. 1979;62:313.PubMedGoogle Scholar
  127. 127.
    Zhao L, Futakuchi M, Suzuki S, et al. Kinetics of marked development of lung metastasis of rat prostatic carcinomas transplanted in syngeneic rats. Clin Exp Metastasis. 2005;22:309.PubMedCrossRefGoogle Scholar
  128. 128.
    Kawai N, Ito A, Nakahara Y, et al. Anticancer effect of hyperthermia on prostate cancer mediated by magnetite cationic liposomes and immune-response induction in transplanted syngeneic rats. Prostate. 2005;64:373.PubMedCrossRefGoogle Scholar
  129. 129.
    Lynch CC, Hikosaka A, Acuff HB, et al. MMP-7 promotes prostate cancer-induced osteolysis via the solubilization of RANKL. Cancer Cell. 2005;7:485.PubMedCrossRefGoogle Scholar
  130. 130.
    Drago JR, Maurer RE, Gershwin ME, et al. The effect of 5-fluorouracil and adriamycin on heterotransplantation of Noble rat prostatic tumors in congenitally athymic (nude) mice. Cancer. 1979;44:424.PubMedCrossRefGoogle Scholar
  131. 131.
    Drago JR, Lombard J. Nb rat prostate adenocarcinoma model: evaluation of the subrenal capsular assay system. J Surg Oncol. 1985;28:270.PubMedCrossRefGoogle Scholar
  132. 132.
    Ellis WJ, Vessella RL, Buhler KR, et al. Characterization of a novel androgen-sensitive, prostate-specific antigen-producing prostatic carcinoma xenograft: LuCaP 23. Clin Cancer Res. 1996;2:1039.PubMedGoogle Scholar
  133. 133.
    Lopez-Barcons LA. Human prostate cancer heterotransplants: a review on this experimental model. Asian J Androl. 2010;12:509.PubMedCrossRefGoogle Scholar
  134. 134.
    Thalmann GN, Sikes RA, Wu TT, et al. LNCaP progression model of human prostate cancer: androgen-independence and osseous metastasis. Prostate. 2000;44:91.PubMedCrossRefGoogle Scholar
  135. 135.
    Troyer DA, Tang Y, Bedolla R, et al. Characterization of PacMetUT1, a recently isolated human prostate cancer cell line. Prostate. 2008;68:883.PubMedCrossRefGoogle Scholar
  136. 136.
    Webber MM, Quader ST, Kleinman HK, et al. Human cell lines as an in vitro/in vivo model for prostate carcinogenesis and progression. Prostate. 2001;47:1.PubMedCrossRefGoogle Scholar
  137. 137.
    Weijerman PC, Zhang Y, Shen J, et al. Expression of prostatic factors measured by reverse transcription polymerase chain reaction in human papillomavirus type 18 deoxyribonucleic acid immortalized prostate cell lines. Urology. 1998;51:657.PubMedCrossRefGoogle Scholar
  138. 138.
    Wang Y, Revelo MP, Sudilovsky D, et al. Development and characterization of efficient xenograft models for benign and malignant human prostate tissue. Prostate. 2005;64:149.PubMedCrossRefGoogle Scholar
  139. 139.
    Schroeder FH, Okada K, Jellinghaus W, et al. Human prostatic adenoma and carcinoma. Transplantation of cultured cells and primary tissue fragments in “nude” mice. Invest Urol. 1976;13:395.PubMedGoogle Scholar
  140. 140.
    Jones MA, Williams G, Davies AJ. Value of xenografts in the investigation of prostatic function: preliminary communication. J R Soc Med. 1980;73:708.PubMedGoogle Scholar
  141. 141.
    Reid LM, Minato N, Gresser I, et al. Influence of anti-mouse interferon serum on the growth and metastasis of tumor cells persistently infected with virus and of human prostatic tumors in athymic nude mice. Proc Natl Acad Sci U S A. 1981;78:1171.PubMedCrossRefGoogle Scholar
  142. 142.
    Huss WJ, Gray DR, Werdin ES, et al. Evidence of pluripotent human prostate stem cells in a human prostate primary xenograft model. Prostate. 2004;60:77.PubMedCrossRefGoogle Scholar
  143. 143.
    Presnell SC, Werdin ES, Maygarden S, et al. Establishment of short-term primary human prostate xenografts for the study of prostate biology and cancer. Am J Pathol. 2001;159:855.PubMedCrossRefGoogle Scholar
  144. 144.
    Lubaroff DM, Cohen MB, Schultz LD, et al. Survival of human prostate carcinoma, benign hyperplastic prostate tissues, and IL-2-activated lymphocytes in scid mice. Prostate. 1995;27:32.PubMedCrossRefGoogle Scholar
  145. 145.
    Gray DR, Huss WJ, Yau JM, et al. Short-term human prostate primary xenografts: an in vivo model of human prostate cancer vasculature and angiogenesis. Cancer Res. 2004;64:1712.PubMedCrossRefGoogle Scholar
  146. 146.
    van Weerden WM, de Ridder CM, Verdaasdonk CL, et al. Development of seven new human prostate tumor xenograft models and their histopathological characterization. Am J Pathol. 1996;149:1055.PubMedGoogle Scholar
  147. 147.
    Klein KA, Reiter RE, Redula J, et al. Progression of metastatic human prostate cancer to androgen independence in immunodeficient SCID mice. Nat Med. 1997;3:402.PubMedCrossRefGoogle Scholar
  148. 148.
    Rubin MA, Putzi M, Mucci N, et al. Rapid (“warm”) autopsy study for procurement of metastatic prostate cancer. Clin Cancer Res. 2000;6:1038.PubMedGoogle Scholar
  149. 149.
    Kleinman HK, McGarvey ML, Liotta LA, et al. Isolation and characterization of type IV procollagen, laminin, and heparan sulfate proteoglycan from the EHS sarcoma. Biochemistry. 1982;21:6188.PubMedCrossRefGoogle Scholar
  150. 150.
    Fridman R, Giaccone G, Kanemoto T, et al. Reconstituted basement membrane (matrigel) and laminin can enhance the tumorigenicity and the drug resistance of small cell lung cancer cell lines. Proc Natl Acad Sci U S A. 1990;87:6698.PubMedCrossRefGoogle Scholar
  151. 151.
    Fridman R, Kibbey MC, Royce LS, et al. Enhanced tumor growth of both primary and established human and murine tumor cells in athymic mice after coinjection with Matrigel. J Natl Cancer Inst. 1991;83:769.PubMedCrossRefGoogle Scholar
  152. 152.
    Lim DJ, Liu XL, Sutkowski DM, et al. Growth of an androgen-sensitive human prostate cancer cell line, LNCaP, in nude mice. Prostate. 1993;22:109.PubMedCrossRefGoogle Scholar
  153. 153.
    Pretlow TG, Wolman SR, Micale MA, et al. Xenografts of primary human prostatic carcinoma. J Natl Cancer Inst. 1993;85:394.PubMedCrossRefGoogle Scholar
  154. 154.
    McCulloch DR, Opeskin K, Thompson EW, et al. BM18: a novel androgen-dependent human prostate cancer xenograft model derived from a bone metastasis. Prostate. 2005;65:35.PubMedCrossRefGoogle Scholar
  155. 155.
    Hoehn W, Walther R, Hermanek P. Human prostatic adenocarcinoma: comparative experimental treatment of the tumor line PC 82 in nude mice. Prostate. 1982;3:193.PubMedCrossRefGoogle Scholar
  156. 156.
    Hoehn W, Schroeder FH, Reimann JF, et al. Human prostatic adenocarcinoma: some characteristics of a serially transplantable line in nude mice (PC 82). Prostate. 1980;1:95.PubMedCrossRefGoogle Scholar
  157. 157.
    van Steenbrugge GJ, van Dongen JJ, Reuvers PJ, et al. Transplantable human prostatic carcinoma (PC-82) in athymic nude mice: I. Hormone dependence and the concentration of androgens in plasma and tumor tissue. Prostate. 1987;11:195.PubMedCrossRefGoogle Scholar
  158. 158.
    van Weerden WM, van Kreuningen A, Elissen NM, et al. Castration-induced changes in morphology, androgen levels, and proliferative activity of human prostate cancer tissue grown in athymic nude mice. Prostate. 1993;23:149.PubMedCrossRefGoogle Scholar
  159. 159.
    Ito YZ, Mashimo S, Nakazato Y, et al. Hormone dependency of a serially transplantable human prostatic cancer (HONDA) in nude mice. Cancer Res. 1985;45:5058.PubMedGoogle Scholar
  160. 160.
    Hoehn W, Wagner M, Riemann JF, et al. Prostatic adenocarcinoma PC EW, a new human tumor line transplantable in nude mice. Prostate. 1984;5:445.PubMedCrossRefGoogle Scholar
  161. 161.
    de Pinieux G, Legrier ME, Poirson-Bichat F, et al. Clinical and experimental progression of a new model of human prostate cancer and therapeutic approach. Am J Pathol. 2001;159:753.PubMedCrossRefGoogle Scholar
  162. 162.
    Wainstein MA, He F, Robinson D, et al. CWR22: androgen-dependent xenograft model derived from a primary human prostatic carcinoma. Cancer Res. 1994;54:6049.PubMedGoogle Scholar
  163. 163.
    Ito YZ, Nakazato Y. A new serially transplantable human prostatic cancer (HONDA) in nude mice. J Urol. 1984;132:384.PubMedGoogle Scholar
  164. 164.
    Corey E, Quinn JE, Buhler KR, et al. LuCaP 35: a new model of prostate cancer progression to androgen independence. Prostate. 2003;55:239.PubMedCrossRefGoogle Scholar
  165. 165.
    Yoshida T, Kinoshita H, Segawa T, et al. Antiandrogen bicalutamide promotes tumor growth in a novel androgen-dependent prostate cancer xenograft model derived from a bicalutamide-treated patient. Cancer Res. 2005;65:9611.PubMedCrossRefGoogle Scholar
  166. 166.
    Marques RB, Erkens-Schulze S, de Ridder CM, et al. Androgen receptor modifications in prostate cancer cells upon long-termandrogen ablation and antiandrogen treatment. Int J Cancer. 2005;117:221.PubMedCrossRefGoogle Scholar
  167. 167.
    Nagabhushan M, Miller CM, Pretlow TP, et al. CWR22: the first human prostate cancer xenograft with strongly androgen-dependent and relapsed strains both in vivo and in soft agar. Cancer Res. 1996;56:3042.PubMedGoogle Scholar
  168. 168.
    Thin TH, Wang L, Kim E, et al. Isolation and characterization of androgen receptor mutant, AR(M749L), with hypersensitivity to 17-beta estradiol treatment. J Biol Chem. 2003;278:7699.PubMedCrossRefGoogle Scholar
  169. 169.
    Welsh JB, Sapinoso LM, Su AI, et al. Analysis of gene expression identifies candidate markers and pharmacological targets in prostate cancer. Cancer Res. 2001;61:5974.PubMedGoogle Scholar
  170. 170.
    Kaighn ME, Narayan KS, Ohnuki Y, et al. Establishment and characterization of a human prostatic carcinoma cell line (PC-3). Invest Urol. 1979;17:16.PubMedGoogle Scholar
  171. 171.
    Stone KR, Mickey DD, Wunderli H, et al. Isolation of a human prostate carcinoma cell line (DU 145). Int J Cancer. 1978;21:274.PubMedCrossRefGoogle Scholar
  172. 172.
    Horoszewicz JS, Leong SS, Kawinski E, et al. LNCaP model of human prostatic carcinoma. Cancer Res. 1983;43:1809.PubMedGoogle Scholar
  173. 173.
    van Haaften-Day C, Raghavan D, Russell P, et al. Xenografted small cell undifferentiated cancer of prostate: possible common origin with prostatic adenocarcinoma. Prostate. 1987;11:271.PubMedCrossRefGoogle Scholar
  174. 174.
    Jelbart ME, Russell PJ, Russell P, et al. Site-specific growth of the prostate xenograft line UCRU-PR-2. Prostate. 1989;14:163.PubMedCrossRefGoogle Scholar
  175. 175.
    Pinthus JH, Waks T, Schindler DG, et al. WISH-PC2: a unique xenograft model of human prostatic small cell carcinoma. Cancer Res. 2000;60:6563.PubMedGoogle Scholar
  176. 176.
    Corey E, Quinn JE, Emond MJ, et al. Inhibition of androgen-independent growth of prostate cancer xenografts by 17beta-estradiol. Clin Cancer Res. 2002;8:1003.PubMedGoogle Scholar
  177. 177.
    Danielpour D, Kadomatsu K, Anzano MA, et al. Development and characterization of nontumorigenic and tumorigenic epithelial cell lines from rat dorsal-lateral prostate. Cancer Res. 1994;54:3413.PubMedGoogle Scholar
  178. 178.
    Cunha GR. Epithelio-mesenchymal interactions in primordial gland structures which become responsive to androgenic stimulation. Anat Rec. 1972;172:179.PubMedCrossRefGoogle Scholar
  179. 179.
    Thompson TC, Timme TL, Kadmon D, et al. Genetic predisposition and mesenchymal-epithelial interactions in ras  +  myc-induced carcinogenesis in reconstituted mouse prostate. Mol Carcinog. 1993;7:165.PubMedCrossRefGoogle Scholar
  180. 180.
    Thompson TC, Southgate J, Kitchener G, et al. Multistage carcinogenesis induced by ras and myc oncogenes in a reconstituted organ. Cell. 1989;56:917.PubMedCrossRefGoogle Scholar
  181. 181.
    Thompson TC, Timme TL, Park SH, et al. Mouse prostate reconstitution model system: a series of in vivo and in vitro models for benign and malignant prostatic disease. Prostate. 2000;43:248.PubMedCrossRefGoogle Scholar
  182. 182.
    Thompson TC, Park SH, Timme TL, et al. Loss of p53 function leads to metastasis in ras  +  myc-initiated mouse prostate cancer. Oncogene. 1995;10:869.PubMedGoogle Scholar
  183. 183.
    Baley PA, Yoshida K, Qian W, et al. Progression to androgen insensitivity in a novel in vitro mouse model for prostate cancer. J Steroid Biochem Mol Biol. 1995;52:403.PubMedCrossRefGoogle Scholar
  184. 184.
    Hall SJ, Thompson TC. Spontaneous but not experimental metastatic activities differentiate primary tumor-derived vs metastasis-derived mouse prostate cancer cell lines. Clin Exp Metastasis. 1997;15:630.PubMedCrossRefGoogle Scholar
  185. 185.
    Yang G, Truong LD, Timme TL, et al. Elevated expression of caveolin is associated with prostate and breast cancer. Clin Cancer Res. 1998;4:1873.PubMedGoogle Scholar
  186. 186.
    Yang G, Truong LD, Wheeler TM, et al. Caveolin-1 expression in clinically confined human prostate cancer: a novel prognostic marker. Cancer Res. 1999;59:5719.PubMedGoogle Scholar
  187. 187.
    Ellwood-Yen K, Graeber TG, Wongvipat J, et al. Myc-driven murine prostate cancer shares molecular features with human prostate tumors. Cancer Cell. 2003;4:223.PubMedCrossRefGoogle Scholar
  188. 188.
    Zhang X, Lee C, Ng PY, et al. Prostatic neoplasia in transgenic mice with prostate-directed overexpression of the c-myc oncoprotein. Prostate. 2000;43:278.PubMedCrossRefGoogle Scholar
  189. 189.
    Winter SF, Cooper AB, Greenberg NM. Models of metastatic prostate cancer: a transgenic perspective. Prostate Cancer Prostatic Dis. 2003;6:204.PubMedCrossRefGoogle Scholar
  190. 190.
    Maroulakou IG, Anver M, Garrett L, et al. Prostate and mammary adenocarcinoma in transgenic mice carrying a rat C3(1) simian virus 40 large tumor antigen fusion gene. Proc Natl Acad Sci U S A. 1994;91:11236.PubMedCrossRefGoogle Scholar
  191. 191.
    Shibata MA, Ward JM, Devor DE, et al. Progression of prostatic intraepithelial neoplasia to invasive carcinoma in C3(1)/SV40 large T antigen transgenic mice: histopathological and molecular biological alterations. Cancer Res. 1996;56:4894.PubMedGoogle Scholar
  192. 192.
    Calvo A, Xiao N, Kang J, et al. Alterations in gene expression profiles during prostate cancer progression: functional correlations to tumorigenicity and down-regulation of selenoprotein-P in mouse and human tumors. Cancer Res. 2002;62:5325.PubMedGoogle Scholar
  193. 193.
    Greenberg NM, DeMayo F, Finegold MJ, et al. Prostate cancer in a transgenic mouse. Proc Natl Acad Sci U S A. 1995;92:3439.PubMedCrossRefGoogle Scholar
  194. 194.
    Gingrich JR, Barrios RJ, Morton RA, et al. Metastatic prostate cancer in a transgenic mouse. Cancer Res. 1996;56:4096.PubMedGoogle Scholar
  195. 195.
    Kaplan-Lefko PJ, Chen TM, Ittmann MM, et al. Pathobiology of autochthonous prostate cancer in a pre-clinical transgenic mouse model. Prostate. 2003;55:219.PubMedCrossRefGoogle Scholar
  196. 196.
    Gingrich JR, Barrios RJ, Kattan MW, et al. Androgen-independent prostate cancer progression in the TRAMP model. Cancer Res. 1997;57:4687.PubMedGoogle Scholar
  197. 197.
    Gupta S, Hastak K, Ahmad N, et al. Inhibition of prostate carcinogenesis in TRAMP mice by oral infusion of green tea polyphenols. Proc Natl Acad Sci U S A. 2001;98:10350.PubMedCrossRefGoogle Scholar
  198. 198.
    Klein RD. The use of genetically engineered mouse models of prostate cancer for nutrition and cancer chemoprevention research. Mutat Res. 2005;576:111.PubMedCrossRefGoogle Scholar
  199. 199.
    Foster BA, Gingrich JR, Kwon ED, et al. Characterization of prostatic epithelial cell lines derived from transgenic adenocarcinoma of the mouse prostate (TRAMP) model. Cancer Res. 1997;57:3325.PubMedGoogle Scholar
  200. 200.
    Kasper S, Sheppard PC, Yan Y, et al. Development, progression, and androgen-dependence of prostate tumors in probasin-large T antigen transgenic mice: a model for prostate cancer. Lab Invest. 1998;78:i.PubMedGoogle Scholar
  201. 201.
    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. 2001;61:2239.PubMedGoogle Scholar
  202. 202.
    Asamoto M, Hokaiwado N, Cho YM, et al. Prostate carcinomas developing in transgenic rats with SV40 T antigen expression under probasin promoter control are strictly androgen dependent. Cancer Res. 2001;61:4693.PubMedGoogle Scholar
  203. 203.
    Haram KM, Peltier HJ, Lu B, et al. Gene expression profile of mouse prostate tumors reveals dysregulations in major biological processes and identifies potential murine targets for preclinical development of human prostate cancer therapy. Prostate. 2008;68:1517.PubMedCrossRefGoogle Scholar
  204. 204.
    Kaplan PJ, Mohan S, Cohen P, et al. The insulin-like growth factor axis and prostate cancer: lessons from the transgenic adenocarcinoma of mouse prostate (TRAMP) model. Cancer Res. 1999;59:2203.PubMedGoogle Scholar
  205. 205.
    Goc A, Al-Husein B, Kochuparambil ST, et al. PI3 kinase integrates Akt and MAP kinase signaling pathways in the regulation of prostate cancer. Int J Oncol. 2011;38:267.PubMedGoogle Scholar
  206. 206.
    Foster BA, Kaplan PJ, Greenberg NM. Characterization of the FGF axis and identification of a novel FGFR1iiic isoform during prostate cancer progression in the TRAMP model. Prostate Cancer Prostatic Dis. 1999;2:76.PubMedCrossRefGoogle Scholar
  207. 207.
    Nguewa PA, Calvo A. Use of transgenic mice as models for prostate cancer chemoprevention. Curr Mol Med. 2010;10:705.PubMedCrossRefGoogle Scholar
  208. 208.
    Caporali A, Davalli P, Astancolle S, et al. The chemopreventive action of catechins in the TRAMP mouse model of prostate carcinogenesis is accompanied by clusterin over-expression. Carcinogenesis. 2004;25:2217.PubMedCrossRefGoogle Scholar
  209. 209.
    Wang L, Zhang J, Zhang Y, et al. Lobe-specific lineages of carcinogenesis in the transgenic adenocarcinoma of mouse prostate and their responses to chemopreventive selenium. Prostate. 2011;71:1429–40.PubMedCrossRefGoogle Scholar
  210. 210.
    Konijeti R, Henning S, Moro A, et al. Chemoprevention of prostate cancer with lycopene in the TRAMP model. Prostate. 2010;70:1547.PubMedCrossRefGoogle Scholar
  211. 211.
    Raina K, Singh RP, Agarwal R, et al. Oral grape seed extract inhibits prostate tumor growth and progression in TRAMP mice. Cancer Res. 2007;67:5976.PubMedCrossRefGoogle Scholar
  212. 212.
    Venkateswaran V, Klotz LH, Ramani M, et al. A combination of micronutrients is beneficial in reducing the incidence of prostate cancer and increasing survival in the Lady transgenic model. Cancer Prev Res (Phila). 2009;2:473.CrossRefGoogle Scholar
  213. 213.
    Venkateswaran V, Fleshner NE, Sugar LM, et al. Antioxidants block prostate cancer in lady transgenic mice. Cancer Res. 2004;64:5891.PubMedCrossRefGoogle Scholar
  214. 214.
    Bruxvoort KJ, Charbonneau HM, Giambernardi TA, et al. Inactivation of Apc in the mouse prostate causes prostate carcinoma. Cancer Res. 2007;67:2490.PubMedCrossRefGoogle Scholar
  215. 215.
    Yu X, Wang Y, Jiang M, et al. Activation of beta-Catenin in mouse prostate causes HGPIN and continuous prostate growth after castration. Prostate. 2009;69:249.PubMedCrossRefGoogle Scholar
  216. 216.
    Di Cristofano A, Pesce B, Cordon-Cardo C, et al. Pten is essential for embryonic development and tumour suppression. Nat Genet. 1998;19:348.PubMedCrossRefGoogle Scholar
  217. 217.
    Podsypanina K, Ellenson LH, Nemes A, et al. Mutation of Pten/Mmac1 in mice causes neoplasia in multiple organ systems. Proc Natl Acad Sci U S A. 1999;96:1563.PubMedCrossRefGoogle Scholar
  218. 218.
    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. 2003;4:209.PubMedCrossRefGoogle Scholar
  219. 219.
    Majumder PK, Yeh JJ, George DJ, et al. Prostate intraepithelial neoplasia induced by prostate restricted Akt activation: the MPAKT model. Proc Natl Acad Sci U S A. 2003;100:7841.PubMedCrossRefGoogle Scholar
  220. 220.
    Scherl A, Li JF, Cardiff RD, et al. Prostatic intraepithelial neoplasia and intestinal metaplasia in prostates of probasin-RAS transgenic mice. Prostate. 2004;59:448.PubMedCrossRefGoogle Scholar
  221. 221.
    Downing SR, Russell PJ, Jackson P. Alterations of p53 are common in early stage prostate cancer. Can J Urol. 2003;10:1924.PubMedGoogle Scholar
  222. 222.
    Elgavish A, Wood PA, Pinkert CA, et al. Transgenic mouse with human mutant p53 expression in the prostate epithelium. Prostate. 2004;61:26.PubMedCrossRefGoogle Scholar
  223. 223.
    Hill R, Song Y, Cardiff RD, et al. Heterogeneous tumor evolution initiated by loss of pRb function in a preclinical prostate cancer model. Cancer Res. 2005;65:10243.PubMedCrossRefGoogle Scholar
  224. 224.
    Zhang X, Chen MW, Ng A, et al. Abnormal prostate development in C3(1)-bcl-2 transgenic mice. Prostate. 1997;32:16.PubMedCrossRefGoogle Scholar
  225. 225.
    Cordon-Cardo C, Koff A, Drobnjak M, et al. Distinct altered patterns of p27KIP1 gene expression in benign prostatic hyperplasia and prostatic carcinoma. J Natl Cancer Inst. 1998;90:1284.PubMedCrossRefGoogle Scholar
  226. 226.
    Voelkel-Johnson C, Voeks DJ, Greenberg NM, et al. Genomic instability-based transgenic models of prostate cancer. Carcinogenesis. 2000;21:1623.PubMedCrossRefGoogle Scholar
  227. 227.
    Shim EH, Johnson L, Noh HL, et al. Expression of the F-box protein SKP2 induces hyperplasia, dysplasia, and low-grade carcinoma in the mouse prostate. Cancer Res. 2003;63:1583.PubMedGoogle Scholar
  228. 228.
    DiGiovanni J, Kiguchi K, Frijhoff A, et al. Deregulated expression of insulin-like growth factor 1 in prostate epithelium leads to neoplasia in transgenic mice. Proc Natl Acad Sci U S A. 2000;97:3455.PubMedCrossRefGoogle Scholar
  229. 229.
    Li Z, Szabolcs M, Terwilliger JD, et al. Prostatic intraepithelial neoplasia and adenocarcinoma in mice expressing a probasin-Neu oncogenic transgene. Carcinogenesis. 2006;27:1054.PubMedCrossRefGoogle Scholar
  230. 230.
    Song Z, Wu X, Powell WC, et al. Fibroblast growth factor 8 isoform B overexpression in prostate epithelium: a new mouse model for prostatic intraepithelial neoplasia. Cancer Res. 2002;62:5096.PubMedGoogle Scholar
  231. 231.
    Foster BA, Evangelou A, Gingrich JR, et al. Enforced expression of FGF-7 promotes epithelial hyperplasia whereas a dominant negative FGFR2iiib promotes the emergence of neuroendocrine phenotype in prostate glands of transgenic mice. Differentiation. 2002;70:624.PubMedCrossRefGoogle Scholar
  232. 232.
    Freeman KW, Gangula RD, Welm BE, 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.PubMedGoogle Scholar
  233. 233.
    Stanbrough M, Leav I, Kwan PW, et al. Prostatic intraepithelial neoplasia in mice expressing an androgen receptor transgene in prostate epithelium. Proc Natl Acad Sci U S A. 2001;98:10823.PubMedCrossRefGoogle Scholar
  234. 234.
    Eddy EM, Washburn TF, Bunch DO, et al. Targeted disruption of the estrogen receptor gene in male mice causes alteration of spermatogenesis and infertility. Endocrinology. 1996;137:4796.PubMedCrossRefGoogle Scholar
  235. 235.
    Krege JH, Hodgin JB, Couse JF, et al. Generation and reproductive phenotypes of mice lacking estrogen receptor beta. Proc Natl Acad Sci U S A. 1998;95:15677.PubMedCrossRefGoogle Scholar
  236. 236.
    Huang J, Powell WC, Khodavirdi AC, et al. Prostatic intraepithelial neoplasia in mice with conditional disruption of the retinoid X receptor alpha allele in the prostate epithelium. Cancer Res. 2002;62:4812.PubMedGoogle Scholar
  237. 237.
    Lohnes D, Kastner P, Dierich A, et al. Function of retinoic acid receptor gamma in the mouse. Cell. 1993;73:643.PubMedCrossRefGoogle Scholar
  238. 238.
    Abdulkadir SA, Magee JA, Peters TJ, et al. Conditional loss of Nkx3.1 in adult mice induces prostatic intraepithelial neoplasia. Mol Cell Biol. 2002;22:1495.PubMedCrossRefGoogle Scholar
  239. 239.
    Bhatia-Gaur R, Donjacour AA, Sciavolino PJ, et al. Roles for Nkx3.1 in prostate development and cancer. Genes Dev. 1999;13:966.PubMedCrossRefGoogle Scholar
  240. 240.
    Tomlins SA, Laxman B, Varambally S, et al. Role of the TMPRSS2-ERG gene fusion in prostate cancer. Neoplasia. 2008;10:177.PubMedCrossRefGoogle Scholar
  241. 241.
    Zhou Z, Flesken-Nikitin A, Corney DC, et al. Synergy of p53 and Rb deficiency in a conditional mouse model for metastatic prostate cancer. Cancer Res. 2006;66:7889.PubMedCrossRefGoogle Scholar
  242. 242.
    Di Cristofano A, De Acetis M, Koff A, et al. Pten and p27KIP1 cooperate in prostate cancer tumor suppression in the mouse. Nat Genet. 2001;27:222.PubMedCrossRefGoogle Scholar
  243. 243.
    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 U S A. 2002;99:2884.PubMedCrossRefGoogle Scholar
  244. 244.
    Zhong C, Saribekyan G, Liao CP, et al. Cooperation between FGF8b overexpression and PTEN deficiency in prostate tumorigenesis. Cancer Res. 2006;66:2188.PubMedCrossRefGoogle Scholar
  245. 245.
    Chen Z, Trotman LC, Shaffer D, et al. Crucial role of p53-dependent cellular senescence in suppression of Pten-deficient tumorigenesis. Nature. 2005;436:725.PubMedCrossRefGoogle Scholar
  246. 246.
    Garabedian EM, Humphrey PA, Gordon JI. A transgenic mouse model of metastatic prostate cancer originating from neuroendocrine cells. Proc Natl Acad Sci U S A. 1998;95:15382.PubMedCrossRefGoogle Scholar
  247. 247.
    Perez-Stable C, Altman NH, Mehta PP, et al. Prostate cancer progression, metastasis, and gene expression in transgenic mice. Cancer Res. 1997;57:900.PubMedGoogle Scholar
  248. 248.
    Klezovitch O, Chevillet J, Mirosevich J, et al. Hepsin promotes prostate cancer progression and metastasis. Cancer Cell. 2004;6:185.PubMedCrossRefGoogle Scholar
  249. 249.
    Shaker MR, Yang G, Timme TL, et al. Dietary 4-HPR suppresses the development of bone metastasis in vivo in a mouse model of prostate cancer progression. Clin Exp Metastasis. 2000;18:429.PubMedCrossRefGoogle Scholar
  250. 250.
    Holleran JL, Miller CJ, Culp LA. Tracking micrometastasis to multiple organs with lacZ-tagged CWR22R prostate carcinoma cells. J Histochem Cytochem. 2000;48:643.PubMedCrossRefGoogle Scholar
  251. 251.
    Tsingotjidou AS, Ahluwalia R, Zhang X, et al. A metastatic human prostate cancer model using intraprostatic implantation of tumor produced by PC-3 neolacZ transfected cells. Int J Oncol. 2003;23:1569.PubMedGoogle Scholar
  252. 252.
    Dolman CS, Mueller BM, Lode HN, et al. Suppression of human prostate carcinoma metastases in severe combined immunodeficient mice by interleukin 2 immunocytokine therapy. Clin Cancer Res. 1998;4:2551.PubMedGoogle Scholar
  253. 253.
    Gomes Jr RR, Buttke P, Paul EM, et al. Osteosclerotic prostate cancer metastasis to murine bone are enhanced with increased bone formation. Clin Exp Metastasis. 2009;26:641.PubMedCrossRefGoogle Scholar
  254. 254.
    Thalmann GN, Anezinis PE, Chang SM, et al. Androgen-independent cancer progression and bone metastasis in the LNCaP model of human prostate cancer. Cancer Res. 1994;54:2577.PubMedGoogle Scholar
  255. 255.
    Wu TT, Sikes RA, Cui Q, et al. Establishing human prostate cancer cell xenografts in bone: induction of osteoblastic reaction by prostate-specific antigen-producing tumors in athymic and SCID/bg mice using LNCaP and lineage-derived metastatic sublines. Int J Cancer. 1998;77:887.PubMedCrossRefGoogle Scholar
  256. 256.
    Pettaway CA, Pathak S, Greene G, et al. Selection of highly metastatic variants of different human prostatic carcinomas using orthotopic implantation in nude mice. Clin Cancer Res. 1996;2:1627.PubMedGoogle Scholar
  257. 257.
    Jenkins DE, Yu SF, Hornig YS, et al. In vivo monitoring of tumor relapse and metastasis using bioluminescent PC-3M-luc-C6 cells in murine models of human prostate cancer. Clin Exp Metastasis. 2003;20:745.PubMedCrossRefGoogle Scholar
  258. 258.
    Haq M, Goltzman D, Tremblay G, et al. Rat prostate adenocarcinoma cells disseminate to bone and adhere preferentially to bone marrow-derived endothelial cells. Cancer Res. 1992;52:4613.PubMedGoogle Scholar
  259. 259.
    Shukeir N, Arakelian A, Chen G, et al. A synthetic 15-mer peptide (PCK3145) derived from prostate secretory protein can reduce tumor growth, experimental skeletal metastases, and malignancy-associated hypercalcemia. Cancer Res. 2004;64:5370.PubMedCrossRefGoogle Scholar
  260. 260.
    Achbarou A, Kaiser S, Tremblay G, et al. Urokinase overproduction results in increased skeletal metastasis by prostate cancer cells in vivo. Cancer Res. 1994;54:2372.PubMedGoogle Scholar
  261. 261.
    Geldof AA, Rao BR. Prostatic tumor (R3327) skeletal metastasis. Prostate. 1990;16:279.PubMedCrossRefGoogle Scholar
  262. 262.
    Shevrin DH, Kukreja SC, Ghosh L, et al. Development of skeletal metastasis by human prostate cancer in athymic nude mice. Clin Exp Metastasis. 1988;6:401.PubMedCrossRefGoogle Scholar
  263. 263.
    Corey E, Quinn JE, Bladou F, et al. Establishment and characterization of osseous prostate cancer models: intra-tibial injection of human prostate cancer cells. Prostate. 2002;52:20.PubMedCrossRefGoogle Scholar
  264. 264.
    Liepe K, Geidel H, Haase M, et al. New model for the induction of osteoblastic bone metastases in rat. Anticancer Res. 2005;25:1067.PubMedGoogle Scholar
  265. 265.
    Kawai N, Futakuchi M, Yoshida T, et al. Effect of heat therapy using magnetic nanoparticles conjugated with cationic liposomes on prostate tumor in bone. Prostate. 2008;68:784.PubMedCrossRefGoogle Scholar
  266. 266.
    Nemeth JA, Harb JF, Barroso Jr U, et al. Severe combined immunodeficient-hu model of human prostate cancer metastasis to human bone. Cancer Res. 1999;59:1987.PubMedGoogle Scholar
  267. 267.
    Tsingotjidou AS, Zotalis G, Jackson KR, et al. Development of an animal model for prostate cancer cell metastasis to adult human bone. Anticancer Res. 2001;21:971.PubMedGoogle Scholar
  268. 268.
    Yonou H, Yokose T, Kamijo T, et al. Establishment of a novel species- and tissue-specific metastasis model of human prostate cancer in humanized non-obese diabetic/severe combined immunodeficient mice engrafted with human adult lung and bone. Cancer Res. 2001;61:2177.PubMedGoogle Scholar
  269. 269.
    Banerjee S, Hussain M, Wang Z, et al. In vitro and in vivo molecular evidence for better therapeutic efficacy of ABT-627 and taxotere combination in prostate cancer. Cancer Res. 2007;67:3818.PubMedCrossRefGoogle Scholar
  270. 270.
    Deng X, He G, Levine A, et al. Adenovirus-mediated expression of TIMP-1 and TIMP-2 in bone inhibits osteolytic degradation by human prostate cancer. Int J Cancer. 2008;122:209.PubMedCrossRefGoogle Scholar

Copyright information

© Springer-Verlag London 2013

Authors and Affiliations

  • Eric C. Kauffman
    • 1
  • Casey K. Ng
    • 2
  • Carrie Rinker-Schaeffer
    • 3
  1. 1.Department of UrologyRoswell Park Cancer InstituteBuffaloUSA
  2. 2.Department of Urology, Keck School of MedicineUniversity of Southern CaliforniaLos AngelesUSA
  3. 3.Departments of Surgery, Medicine and Obstetrics and GynecologyUniversity of ChicagoChicagoUSA

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