In vitro modeling of the prostate cancer microenvironment

Advanced Drug Delivery Reviews

Volumn 79, Issue , 2014, Pages 214-221

  Ellem, Stuart J ^a   De Juan Pardo, Elena M ^b   Risbridger, Gail P ^a  

^a MONASH UNIVERSITY   (Australia)

^b QUEENSLAND UNIVERSITY OF TECHNOLOGY   (Australia)

Author keywords

2D; 3D; Matrix; Microenvironment; Prostate; Prostate cancer; Scaffolds; Stroma

Indexed keywords

CELL CULTURE; MATRIX ALGEBRA; SCAFFOLDS; UROLOGY;

DEVELOPMENT AND TESTING; MICROENVIRONMENTS; NEW THERAPEUTIC AGENT; PROSTATE; PROSTATE CANCERS; STROMA; THREEDIMENSIONAL (3-D); TWO DIMENSIONAL (2 D);

DISEASES;

ADVANCED CANCER; CANCER CELL LINE; CANCER INCIDENCE; CANCER MODEL; CELL GROWTH; HUMAN; IN VITRO STUDY; MONOCULTURE; MULTICELLULAR SPHEROID; NONHUMAN; PROSTATE CANCER; PROSTATE DISEASE; REVIEW; TUMOR MICROENVIRONMENT; ANIMAL; BIOLOGICAL MODEL; CULTURE TECHNIQUE; MALE; PATHOLOGY; PHYSIOLOGY; PROSTATE TUMOR; TUMOR CELL LINE;

ANIMALS; CELL CULTURE TECHNIQUES; CELL LINE, TUMOR; HUMANS; IN VITRO TECHNIQUES; MALE; MODELS, BIOLOGICAL; PROSTATIC NEOPLASMS; TUMOR MICROENVIRONMENT;

EID: 84919598885     PISSN: 0169409X     EISSN: 18728294     Source Type: Journal    
DOI: 10.1016/j.addr.2014.04.008     Document Type: Review

References (103)

1. Leroy B.E., Northrup N. Prostate cancer in dogs: comparative and clinical aspects. Vet. J. 2009, 180:149-162.
2. Mubiru J.N., Hubbard G.B., Dick E.J., Furman J., Troyer D.A., Rogers J. Nonhuman primates as models for studies of prostate specific antigen and prostatic diseases. Prostate 2008, 68:1546-1554.
3. Shirai T., Takahashi S., Cui L., Futakuchi M., Kato K., Tamano S., Imaida K. Experimental prostate carcinogenesis - rodent models. Mutat. Res. 2000, 462:219-226.
4. Gingrich J.R., Barrios R.J., Kattan M.W., Nahm H.S., Finegold M.J., Greenberg N.M. Androgen-independent prostate cancer progression in the TRAMP model. Cancer Res. 1997, 57:4687-4691.
5. Kasper S., Sheppard P., Yan Y., Pettigrew N., Borowsky A., Prins G., Dodd J., Duckworth M., Matusik R. Development, progression and androgen-dependence of prostate tumors in probasin-large T antigen transgenic mice: a model for prostate cancer. Lab. Investig. 1998, 78:1/15.
6. Ellwood-Yen K., Graeber T.G., Wongvipat J., Iruela-Arispe M.L., Zhang J., Matusik R., Thomas G.V., Sawyers C.L. Myc-driven murine prostate cancer shares molecular features with human prostate tumors. Cancer Cell 2003, 4:223-238.
7. Wang X., Kruithof-de Julio M., Economides K.D., Walker D., Yu H., Halili M.V., Hu Y.P., Price S.M., Abate-Shen C., Shen M.M. A luminal epithelial stem cell that is a cell of origin for prostate cancer. Nature 2009, 461:495-500.
8. Dunning W.F. Prostate cancer in the rat. Natl. Cancer Inst. Monogr. 1963, 12:351-369.
9. Noble R.L. Development of androgen-stimulated transplants of Nb rat carcinoma of the dorsal prostate and their response to sex hormones and tamoxifen. Cancer Res. 1980, 40:3551-3554.
10. Pollard M., Luckert P.H. Production of autochthonous prostate cancer in Lobund-Wistar rats by treatments with N-nitroso-N-methylurea and testosterone. J. Natl. Cancer Inst. 1986, 77:583-587.
11. Zhao H., Nolley R., Chen Z., Peehl D.M. Tissue slice grafts: an in vivo model of human prostate androgen signaling. Am. J. Pathol. 2010, 177:229-239.
12. Gleave M.E., Hsieh J.T., Wu H.C., von Eschenbach A.C., Chung L.W. Serum prostate specific antigen levels in mice bearing human prostate LNCaP tumors are determined by tumor volume and endocrine and growth factors. Cancer Res. 1992, 52:1598-1605.
13. Sobel R.E., Sadar M.D. Cell lines used in prostate cancer research: a compendium of old and new lines-part 2. J. Urol. 2005, 173:360-372.
14. Ellis W.J., Vessella R.L., Buhler K.R., Bladou F., True L.D., Bigler S.A., Curtis D., Lange P.H. Characterization of a novel androgen-sensitive, prostate-specific antigen-producing prostatic carcinoma xenograft: LuCaP 23. Clin. Cancer Res. 1996, 2:1039-1048.
15. Hoehn W., Schroeder F.H., Reimann J.F., Joebsis A.C., Hermanek P. Human prostatic adenocarcinoma: some characteristics of a serially transplantable line in nude mice (PC 82). Prostate 1980, 1:95-104.
16. Wang Y., Revelo M.P., Sudilovsky D., Cao M., Chen W.G., Goetz L., Xue H., Sadar M., Shappell S.B., Cunha G.R., Hayward S.W. Development and characterization of efficient xenograft models for benign and malignant human prostate tissue. Prostate 2005, 64:149-159.
17. Lopez-Barcons L.A. Human prostate cancer heterotransplants: a review on this experimental model. Asian J. Androl. 2010, 12:509-518.
18. Priolo C., Agostini M., Vena N., Ligon A.H., Fiorentino M., Shin E., Farsetti A., Pontecorvi A., Sicinska E., Loda M. Establishment and genomic characterization of mouse xenografts of human primary prostate tumors. Am. J. Pathol. 2010, 176:1901-1913.
19. Lawrence M.G., Taylor R.A., Toivanen R., Pedersen J., Norden S., Pook D.W., Frydenberg M., Papargiris M.M., Niranjan B., Richards M.G., Wang H., Collins A.T., Maitland N.J., Risbridger G.P. A preclinical xenograft model of prostate cancer using human tumors. Nat. Protoc. 2013, 8:836-848.
20. van Bokhoven A., Varella-Garcia M., Korch C., Johannes W.U., Smith E.E., Miller H.L., Nordeen S.K., Miller G.J., Lucia M.S. Molecular characterization of human prostate carcinoma cell lines. Prostate 2003, 57:205-225.
21. Diaz M., Patterson S.G. Management of androgen-independent prostate cancer. Cancer Control 2004, 11:364-373.
22. Hirschhaeuser F., Menne H., Dittfeld C., West J., Mueller-Klieser W., Kunz-Schughart L.A. Multicellular tumor spheroids: an underestimated tool is catching up again. J. Biotechnol. 2010, 148:3-15.
23. Sutherland R.M., McCredie J.A., Inch W.R. Growth of multicell spheroids in tissue culture as a model of nodular carcinomas. J. Natl. Cancer Inst. 1971, 46:113-120.
24. Taylor R.A., Risbridger G.P. Prostatic tumor stroma: a key player in cancer progression. Curr. Cancer Drug Targets 2008, 8:490-497.
25. Olumi A.F., Grossfeld G.D., Hayward S.W., Carroll P.R., Tlsty T.D., Cunha G.R. Carcinoma-associated fibroblasts direct tumor progression of initiated human prostatic epithelium. Cancer Res. 1999, 59:5002-5011.
26. Joesting M.S., Perrin S., Elenbaas B., Fawell S.E., Rubin J.S., Franco O.E., Hayward S.W., Cunha G.R., Marker P.C. Identification of SFRP1 as a candidate mediator of stromal-to-epithelial signaling in prostate cancer. Cancer Res. 2005, 65:10423-10430.
27. Ao M., Franco O.E., Park D., Raman D., Williams K., Hayward S.W. Cross-talk between paracrine-acting cytokine and chemokine pathways promotes malignancy in benign human prostatic epithelium. Cancer Res. 2007, 67:4244-4253.
28. Clark A.K., Taubenberger A.V., Taylor R.A., Niranjan B., Chea Z.Y., Zotenko E., Sieh S., Pedersen J.S., Norden S., Frydenberg M., Grummet J.P., Pook D.W., Stirzaker C., Clark S.J., Lawrence M.G., Ellem S.J., Hutmacher D.W., Risbridger G.P. A bioengineered microenvironment to quantitatively measure the tumorigenic properties of cancer-associated fibroblasts in human prostate cancer. Biomaterials 2013, 34:4777-4785.
29. De Marzo A.M., Platz E.A., Sutcliffe S., Xu J., Gronberg H., Drake C.G., Nakai Y., Isaacs W.B., Nelson W.G. Inflammation in prostate carcinogenesis. Nat. Rev. Cancer 2007, 7:256-269.
30. Palapattu G.S., Sutcliffe S., Bastian P.J., Platz E.A., De Marzo A.M., Isaacs W.B., Nelson W.G. Prostate carcinogenesis and inflammation: emerging insights. Carcinogenesis 2005, 26:1170-1181.
31. Pittoni P., Tripodo C., Piconese S., Mauri G., Parenza M., Rigoni A., Sangaletti S., Colombo M.P. Mast cell targeting hampers prostate adenocarcinoma development but promotes the occurrence of highly malignant neuroendocrine cancers. Cancer Res. 2011, 71:5987-5997.
32. Fang L.Y., Izumi K., Lai K.P., Liang L., Li L., Miyamoto H., Lin W.J., Chang C. Infiltrating macrophages promote prostate tumorigenesis via modulating androgen receptor-mediated CCL4-STAT3 signaling. Cancer Res. 2013, 73:5633-5646.
33. Hanahan D., Weinberg R.A. The hallmarks of cancer. Cell 2000, 100:57-70.
34. Hanahan D., Weinberg R.A. Hallmarks of cancer: the next generation. Cell 2011, 144:646-674.
35. Russo G., Mischi M., Scheepens W., De la Rosette J.J., Wijkstra H. Angiogenesis in prostate cancer: onset, progression and imaging. BJU Int. 2012, 110:E794-E808.
36. Ayala G.E., Wheeler T.M., Shine H.D., Schmelz M., Frolov A., Chakraborty S., Rowley D. In vitro dorsal root ganglia and human prostate cell line interaction: redefining perineural invasion in prostate cancer. Prostate 2001, 49:213-223.
37. Magnon C., Hall S.J., Lin J., Xue X., Gerber L., Freedland S.J., Frenette P.S. Autonomic nerve development contributes to prostate cancer progression. Science 2013, 341:1236361.
38. Comito G., Giannoni E., Segura C.P., Barcellos-de-Souza P., Raspollini M.R., Baroni G., Lanciotti M., Serni S., Chiarugi P. Cancer-associated fibroblasts and M2-polarized macrophages synergize during prostate carcinoma progression. Oncogene 2014, 33(19):2423-2431.
39. Yamada K.M., Cukierman E. Modeling tissue morphogenesis and cancer in 3D. Cell 2007, 130:601-610.
40. Baker B.M., Chen C.S. Deconstructing the third dimension: how 3D culture microenvironments alter cellular cues. J. Cell Sci. 2012, 125:3015-3024.
41. Chignola R., Schenetti A., Andrighetto G., Chiesa E., Foroni R., Sartoris S., Tridente G., Liberati D. Forecasting the growth of multicell tumour spheroids: implications for the dynamic growth of solid tumours. Cell Prolif. 2000, 33:219-229.
42. Mueller-Klieser W. Three-dimensional cell cultures: from molecular mechanisms to clinical applications. Am. J. Physiol. 1997, 273:C1109-C1123.
43. Hotary K.B., Allen E.D., Brooks P.C., Datta N.S., Long M.W., Weiss S.J. Membrane type I matrix metalloproteinase usurps tumor growth control imposed by the three-dimensional extracellular matrix. Cell 2003, 114:33-45.
44. Camps J.L., Chang S.M., Hsu T.C., Freeman M.R., Hong S.J., Zhau H.E., von Eschenbach A.C., Chung L.W. Fibroblast-mediated acceleration of human epithelial tumor growth in vivo. Proc. Natl. Acad. Sci. U. S. A. 1990, 87:75-79.
45. Barrett J.M., Mangold K.A., Jilling T., Kaul K.L. Bi-directional interactions of prostate cancer cells and bone marrow endothelial cells in three-dimensional culture. Prostate 2005, 64:75-82.
46. Chlenski A., Nakashiro K., Ketels K.V., Korovaitseva G.I., Oyasu R. Androgen receptor expression in androgen-independent prostate cancer cell lines. Prostate 2001, 47:66-75.
47. Veldscholte J., Berrevoets C.A., Ris-Stalpers C., Kuiper G.G., Jenster G., Trapman J., Brinkmann A.O., Mulder E. The androgen receptor in LNCaP cells contains a mutation in the ligand binding domain which affects steroid binding characteristics and response to antiandrogens. J. Steroid Biochem. Mol. Biol. 1992, 41:665-669.
48. Esquenet M., Swinnen J.V., Heyns W., Verhoeven G. LNCaP prostatic adenocarcinoma cells derived from low and high passage numbers display divergent responses not only to androgens but also to retinoids. J. Steroid Biochem. Mol. Biol. 1997, 62:391-399.
49. Chang-Liu C.M., Woloschak G.E. Effect of passage number on cellular response to DNA-damaging agents: cell survival and gene expression. Cancer Lett. 1997, 113:77-86.
50. Wenger S.L., Senft J.R., Sargent L.M., Bamezai R., Bairwa N., Grant S.G. Comparison of established cell lines at different passages by karyotype and comparative genomic hybridization. Biosci. Rep. 2004, 24:631-639.
51. Horning J.L., Sahoo S.K., Vijayaraghavalu S., Dimitrijevic S., Vasir J.K., Jain T.K., Panda A.K., Labhasetwar V. 3-D tumor model for in vitro evaluation of anticancer drugs. Mol. Pharm. 2008, 5:849-862.
52. Fang X., Sittadjody S., Gyabaah K., Opara E.C., Balaji K.C. Novel 3D co-culture model for epithelial-stromal cells interaction in prostate cancer. PLoS One 2013, 8:e75187.
53. Serebriiskii I., Castello-Cros R., Lamb A., Golemis E.A., Cukierman E. Fibroblast-derived 3D matrix differentially regulates the growth and drug-responsiveness of human cancer cells. Matrix Biol. 2008, 27:573-585.
54. Fey S.J., Wrzesinski K. Determination of drug toxicity using 3D spheroids constructed from an immortal human hepatocyte cell line. Toxicol. Sci. 2012, 127:403-411.
55. Kunz-Schughart L.A., Freyer J.P., Hofstaedter F., Ebner R. The use of 3-D cultures for high-throughput screening: the multicellular spheroid model. J. Biomol. Screen. 2004, 9:273-285.
56. Friedrich J., Seidel C., Ebner R., Kunz-Schughart L.A. Spheroid-based drug screen: considerations and practical approach. Nat. Protoc. 2009, 4:309-324.
57. Ulrich T.A., Jain A., Tanner K., MacKay J.L., Kumar S. Probing cellular mechanobiology in three-dimensional culture with collagen-agarose matrices. Biomaterials 2010, 31:1875-1884.
58. Blatchford D.R., Quarrie L.H., Tonner E., McCarthy C., Flint D.J., Wilde C.J. Influence of microenvironment on mammary epithelial cell survival in primary culture. J. Cell. Physiol. 1999, 181:304-311.
59. Dontu G., Al-Hajj M., Abdallah W.M., Clarke M.F., Wicha M.S. Stem cells in normal breast development and breast cancer. Cell Prolif. 2003, 36(Suppl. 1):59-72.
60. Grimshaw M.J., Cooper L., Papazisis K., Coleman J.A., Bohnenkamp H.R., Chiapero-Stanke L., Taylor-Papadimitriou J., Burchell J.M. Mammosphere culture of metastatic breast cancer cells enriches for tumorigenic breast cancer cells. Breast Cancer Res. 2008, 10:R52.
61. Hedlund T.E., Duke R.C., Miller G.J. Three-dimensional spheroid cultures of human prostate cancer cell lines. Prostate 1999, 41:154-165.
62. Garraway I.P., Sun W., Tran C.P., Perner S., Zhang B., Goldstein A.S., Hahm S.A., Haider M., Head C.S., Reiter R.E., Rubin M.A., Witte O.N. Human prostate sphere-forming cells represent a subset of basal epithelial cells capable of glandular regeneration in vivo. Prostate 2010, 70:491-501.
63. Hu W.Y., Shi G.B., Lam H.M., Hu D.P., Ho S.M., Madueke I.C., Kajdacsy-Balla A., Prins G.S. Estrogen-initiated transformation of prostate epithelium derived from normal human prostate stem-progenitor cells. Endocrinology 2011, 152:2150-2163.
64. Lukacs R.U., Goldstein A.S., Lawson D.A., Cheng D., Witte O.N. Isolation, cultivation and characterization of adult murine prostate stem cells. Nat. Protoc. 2010, 5:702-713.
65. Xin L., Lukacs R.U., Lawson D.A., Cheng D., Witte O.N. Self-renewal and multilineage differentiation in vitro from murine prostate stem cells. Stem Cells 2007, 25:2760-2769.
66. Takagi A., Watanabe M., Ishii Y., Morita J., Hirokawa Y., Matsuzaki T., Shiraishi T. Three-dimensional cellular spheroid formation provides human prostate tumor cells with tissue-like features. Anticancer Res. 2007, 27:45-53.
67. Streuli C.H., Bailey N., Bissell M.J. Control of mammary epithelial differentiation: basement membrane induces tissue-specific gene expression in the absence of cell-cell interaction and morphological polarity. J. Cell Biol. 1991, 115:1383-1395.
68. Lee G.Y., Kenny P.A., Lee E.H., Bissell M.J. Three-dimensional culture models of normal and malignant breast epithelial cells. Nat. Methods 2007, 4:359-365.
69. Foty R. A simple hanging drop cell culture protocol for generation of 3D spheroids. J. Vis. Exp. 2011, 51:e2720. 10.3791/2720.
70. Kelm J.M., Fussenegger M. Microscale tissue engineering using gravity-enforced cell assembly. Trends Biotechnol. 2004, 22:195-202.
71. Ying L., Wang Q. Microfluidic chip-based technologies: emerging platforms for cancer diagnosis. BMC Biotechnol. 2013, 13:76.
72. Torisawa Y.S., Takagi A., Nashimoto Y., Yasukawa T., Shiku H., Matsue T. A multicellular spheroid array to realize spheroid formation, culture, and viability assay on a chip. Biomaterials 2007, 28:559-566.
73. Wu L.Y., Di Carlo D., Lee L.P. Microfluidic self-assembly of tumor spheroids for anticancer drug discovery. Biomed. Microdevices 2008, 10:197-202.
74. Fukuda J., Khademhosseini A., Yeh J., Eng G., Cheng J., Farokhzad O.C., Langer R. Micropatterned cell co-cultures using layer-by-layer deposition of extracellular matrix components. Biomaterials 2006, 27:1479-1486.
75. Kelm J.M., Diaz Sanchez-Bustamante C., Ehler E., Hoerstrup S.P., Djonov V., Ittner L., Fussenegger M. VEGF profiling and angiogenesis in human microtissues. J. Biotechnol. 2005, 118:213-229.
76. Korff T., Kimmina S., Martiny-Baron G., Augustin H.G. Blood vessel maturation in a 3-dimensional spheroidal coculture model: direct contact with smooth muscle cells regulates endothelial cell quiescence and abrogates VEGF responsiveness. FASEB J. 2001, 15:447-457.
77. Hsiao A.Y., Torisawa Y.S., Tung Y.C., Sud S., Taichman R.S., Pienta K.J., Takayama S. Microfluidic system for formation of PC-3 prostate cancer co-culture spheroids. Biomaterials 2009, 30:3020-3027.
78. Hutmacher D.W. Scaffolds in tissue engineering bone and cartilage. Biomaterials 2000, 21:2529-2543.
79. Hutmacher D.W., Horch R.E., Loessner D., Rizzi S., Sieh S., Reichert J.C., Clements J.A., Beier J.P., Arkudas A., Bleiziffer O., Kneser U. Translating tissue engineering technology platforms into cancer research. J. Cell. Mol. Med. 2009, 13:1417-1427.
80. Nyga A., Cheema U., Loizidou M. 3D tumour models: novel in vitro approaches to cancer studies. J. Cell Commun. Signal. 2011, 5:239-248.
81. Fischbach C., Chen R., Matsumoto T., Schmelzle T., Brugge J.S., Polverini P.J., Mooney D.J. Engineering tumors with 3D scaffolds. Nat. Methods 2007, 4:855-860.
82. Reichert J.C., Quent V.M., Burke L.J., Stansfield S.H., Clements J.A., Hutmacher D.W. Mineralized human primary osteoblast matrices as a model system to analyse interactions of prostate cancer cells with the bone microenvironment. Biomaterials 2010, 31:7928-7936.
83. Hartman O., Zhang C., Adams E.L., Farach-Carson M.C., Petrelli N.J., Chase B.D., Rabolt J.F. Biofunctionalization of electrospun PCL-based scaffolds with perlecan domain IV peptide to create a 3-D pharmacokinetic cancer model. Biomaterials 2010, 31:5700-5718.
84. Sieh S., Lubik A.A., Clements J.A., Nelson C.C., Hutmacher D.W. Interactions between human osteoblasts and prostate cancer cells in a novel 3D in vitro model. Organogenesis 2010, 6:181-188.
85. Centenera M.M., Raj G.V., Knudsen K.E., Tilley W.D., Butler L.M. Ex vivo culture of human prostate tissue and drug development. Nat. Rev. Urol. 2013, 10:483-487.
86. Kreisberg J.I., Brattain M.G., Pretlow T.G. Studies on human hyperplastic prostates maintained in organ culture. Investig. Urol. 1977, 15:252-255.
87. Varani J., Dame M.K., Wojno K., Schuger L., Johnson K.J. Characteristics of nonmalignant and malignant human prostate in organ culture. Lab. Investig. 1999, 79:723-731.
88. Sanefuji H., Heatfield B.M., Trump B.F., Young J.D. Studies on carcinogenesis of human prostate. II. Long-term explant culture of normal prostate and benign prostatic hyperplasia: light microscopy. J. Natl. Cancer Inst. 1982, 69:751-756.
89. Parrish A.R., Sallam K., Nyman D.W., Orozco J., Cress A.E., Dalkin B.L., Nagle R.B., Gandolfi A.J. Culturing precision-cut human prostate slices as an in vitro model of prostate pathobiology. Cell Biol. Toxicol. 2002, 18:205-219.
90. Nevalainen M.T., Harkonen P.L., Valve E.M., Ping W., Nurmi M., Martikainen P.M. Hormone regulation of human prostate in organ culture. Cancer Res. 1993, 53:5199-5207.
91. Mistry D., Weaver J.P., Riches A. Organ culture studies of human prostatic adenocarcinomas. Prostate 1983, 4:307-314.
92. Geller J., Sionit L., Partido C., Li L., Tan X., Youngkin T., Nachtsheim D., Hoffman R.M. Genistein inhibits the growth of human-patient BPH and prostate cancer in histoculture. Prostate 1998, 34:75-79.
93. Papini S., Rosellini A., De Matteis A., Campani D., Selli C., Caporali A., Bettuzzi S., Revoltella R.P. Establishment of an organotypic in vitro culture system and its relevance to the characterization of human prostate epithelial cancer cells and their stromal interactions. Pathol. Res. Pract. 2007, 203:209-216.
94. Centenera M.M., Gillis J.L., Hanson A.R., Jindal S., Taylor R.A., Risbridger G.P., Sutherland P.D., Scher H.I., Raj G.V., Knudsen K.E., Yeadon T., Tilley W.D., Butler L.M. Evidence for efficacy of new Hsp90 inhibitors revealed by ex vivo culture of human prostate tumors. Clin. Cancer Res. 2012, 18:3562-3570.
95. Geller J., Sionit L.R., Connors K., Hoffman R.M. Measurement of androgen sensitivity in the human prostate in in vitro three-dimensional histoculture. Prostate 1992, 21:269-278.
96. Kiviharju-af Hallstrom T.M., Jaamaa S., Monkkonen M., Peltonen K., Andersson L.C., Medema R.H., Peehl D.M., Laiho M. Human prostate epithelium lacks Wee1A-mediated DNA damage-induced checkpoint enforcement. Proc. Natl. Acad. Sci. U. S. A. 2007, 104:7211-7216.
97. Jaamaa S., Af Hallstrom T.M., Sankila A., Rantanen V., Koistinen H., Stenman U.H., Zhang Z., Yang Z., De Marzo A.M., Taari K., Ruutu M., Andersson L.C., Laiho M. DNA damage recognition via activated ATM and p53 pathway in nonproliferating human prostate tissue. Cancer Res. 2010, 70:8630-8641.
98. Ni X., Zhang Y., Ribas J., Chowdhury W.H., Castanares M., Zhang Z., Laiho M., DeWeese T.L., Lupold S.E. Prostate-targeted radiosensitization via aptamer-shRNA chimeras in human tumor xenografts. J. Clin. Invest. 2011, 121:2383-2390.
99. Schiewer M.J., Goodwin J.F., Han S., Brenner J.C., Augello M.A., Dean J.L., Liu F., Planck J.L., Ravindranathan P., Chinnaiyan A.M., McCue P., Gomella L.G., Raj G.V., Dicker A.P., Brody J.R., Pascal J.M., Centenera M.M., Butler L.M., Tilley W.D., Feng F.Y., Knudsen K.E. Dual roles of PARP-1 promote cancer growth and progression. Cancer Disc. 2012, 2:1134-1149.
100. Bhowmick N.A., Chytil A., Plieth D., Gorska A.E., Dumont N., Shappell S., Washington M.K., Neilson E.G., Moses H.L. TGF-beta signaling in fibroblasts modulates the oncogenic potential of adjacent epithelia. Science 2004, 303:848-851.
101. Zong Y., Huang J., Sankarasharma D., Morikawa T., Fukayama M., Epstein J.I., Chada K.K., Witte O.N. Stromal epigenetic dysregulation is sufficient to initiate mouse prostate cancer via paracrine Wnt signaling. Proc. Natl. Acad. Sci. U. S. A. 2012, 109:E3395-E3404.
102. Henshall S.M., Quinn D.I., Lee C.S., Head D.R., Golovsky D., Brenner P.C., Delprado W., Stricker P.D., Grygiel J.J., Sutherland R.L. Altered expression of androgen receptor in the malignant epithelium and adjacent stroma is associated with early relapse in prostate cancer. Cancer Res. 2001, 61:423-427.
103. Memarzadeh S., Xin L., Mulholland D.J., Mansukhani A., Wu H., Teitell M.A., Witte O.N. Enhanced paracrine FGF10 expression promotes formation of multifocal prostate adenocarcinoma and an increase in epithelial androgen receptor. Cancer Cell 2007, 12:572-585.