Ex vivo culture of human prostate tissue and drug development

Nature Reviews Urology

Volumn 10, Issue 8, 2013, Pages 483-487

  Centenera, Margaret M ^a   Raj, Ganesh V ^b   Knudsen, Karen E ^c   Tilley, Wayne D ^a   Butler, Lisa M ^a  

^a UNIVERSITY OF ADELAIDE   (Australia)

^b UNIVERSITY OF TEXAS SOUTHWESTERN MEDICAL CENTER   (United States)

^c THOMAS JEFFERSON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; BIOLOGICAL MARKER; CISPLATIN; CYCLIN DEPENDENT KINASE 1; CYPROTERONE ACETATE; GENISTEIN; HEAT SHOCK PROTEIN 90 INHIBITOR; HISTONE H2AX; HYDROXYFLUTAMIDE; PROTEIN P53; PROTEIN P63; SHORT HAIRPIN RNA; STEROID;

APOPTOSIS; BONE METASTASIS; CANCER SURVIVAL; CELL PROLIFERATION; CLINICAL RESEARCH; DRUG EFFICACY; DRUG PENETRATION; DRUG RESPONSE; EX VIVO STUDY; HORMONE RESPONSE; HUMAN; LYMPH NODE METASTASIS; NONHUMAN; OVERALL SURVIVAL; PRIORITY JOURNAL; PROSTATE CANCER; RESEARCH; REVIEW; SIGNAL TRANSDUCTION; THERAPY RESISTANCE; TRANSURETHRAL RESECTION; TUMOR MICROENVIRONMENT;

ANTINEOPLASTIC AGENTS; DRUG DISCOVERY; DRUG RESISTANCE, NEOPLASM; HUMANS; MALE; PROSTATE; PROSTATIC NEOPLASMS; TUMOR CELLS, CULTURED; TUMOR MICROENVIRONMENT;

EID: 84881612540     PISSN: 17594812     EISSN: 17594820     Source Type: Journal    
DOI: 10.1038/nrurol.2013.126     Document Type: Review

References (49)

1. Kamb, A., Wee, S. & Lengauer, C. Why is cancer drug discovery so difficult? Nat. Rev. Drug Discov. 6, 115-120 (2007).
2. Huggins, C., Stephens, R. C. & Hodges, C. V. Studies on prostatic cancer: the effects of castration on advanced carcinoma of the prostate gland. Arch. Surg. 43, 209 (1941).
3. Tannock, I. F. et al. Docetaxel plus prednisone or mitoxantrone plus prednisone for advanced prostate cancer. N. Engl. J. Med. 351, 1502-1512 (2004).
4. de Bono, J. S. et al. Prednisone plus cabazitaxel or mitoxantrone for metastatic castration-resistant prostate cancer progressing after docetaxel treatment: a randomised open-label trial. Lancet 376, 1147-1154 (2010).
5. de Bono, J. S. et al. Abiraterone and increased survival in metastatic prostate cancer. N. Engl. J. Med. 364, 1995-2005 (2011).
6. Scher, H. I. et al. Increased survival with enzalutamide in prostate cancer after chemotherapy. N. Engl. J. Med. 367, 1187-1197 (2012).
7. Adams, D. J. The Valley of Death in anticancer drug development: a reassessment. Trends Pharmacol. Sci. 33, 173-180 (2012).
8. Swartz, M. A. et al. Tumour microenvironment complexity: emerging roles in cancer therapy. Cancer Res. 72, 2473-2480 (2012).
9. Ricke, E. A. et al. Androgen hormone action in prostatic carcinogenesis: stromal androgen receptors mediate prostate cancer progression, malignant transformation and metastasis. Carcinogenesis 33, 1391-1398 (2012).
10. Matrisian, L. M., Cunha, G. R. & Mohla, S. Epithelial-stromal interactions and tumour progression: meeting summary and future directions. Cancer Res. 61, 844-846 (2001).
11. Johnson, J. I. et al. Relationships between drug activity in NCI preclinical in vitro and in vivo models and early clinical trials. Br. J. Cancer 84, 1424-1431 (2001).
12. Voskoglou-Nomikos, T., Pater, J. L. & Seymour, L. Clinical predictive value of the in vitro cell line, human xenograft, and mouse allograft preclinical cancer models. Clin. Cancer Res. 9, 227-239 (2003).
13. Toivanen, R., Taylor, R. A., Pook, D. W., Ellem, S. J. & Risbridger, G. P. Breaking through a roadblock in prostate cancer research: an update on human model systems. J. Steroid Biochem. Mol. Biol. 131, 122-131 (2012).
14. DeRose, Y. S. et al. Tumour grafts derived from women with breast cancer authentically reflect tumour pathology, growth, metastasis and disease outcomes. Nat. Med. 17, 1514-1520 (2011).
15. Lopez-Barcons, L. A. Human prostate cancer heterotransplants: a review on this experimental model. Asian J. Androl. 12, 509-518 (2010).
16. Breslin, S. & O'Driscoll, L. Three-dimensional cell culture: the missing link in drug discovery. Drug Discov. Today 18, 240-249 (2012).
17. Gerlinger, M. et al. Intratumour heterogeneity and branched evolution revealed by multiregion sequencing. N. Engl. J. Med. 366, 883-892 (2012).
18. Pretlow, T. G., Yang, B. & Pretlow, T. P. Organ culture of benign, aging, and hyperplastic human prostate. Microsc. Res. Tech. 30, 271-281 (1995).
19. Varani, J., Dame, M. K., Wojno, K., Schuger, L. & Johnson, K. J. Characteristics of nonmalignant and malignant human prostate in organ culture. Lab. Invest. 79, 723-731 (1999).
20. Ni, X. et al. Prostate-targeted radiosensitization via aptamer-shRNA chimeras in human tumour xenografts. J. Clin. Invest. 121, 2383-2390 (2011).
21. McRae, C. U., Ghanadian, R., Fotherby, K. & Chisholm, G. D. The effect of testosterone on the human prostate in organ culture. Br. J. Urol. 45, 156-162 (1973).
22. Parrish, A. R. et al. Culturing precision-cut human prostate slices as an in vitro model of prostate pathobiology. Cell Biol. Toxicol. 18, 205-219 (2002).
23. Kiviharju-af Hallstrom, T. M. et al. Human prostate epithelium lacks Wee1A-mediated DNA damage-induced checkpoint enforcement. Proc. Natl Acad. Sci. USA 104, 7211-7216 (2007).
24. Centenera, M. M. et al. Evidence for efficacy of new Hsp90 inhibitors revealed by ex vivo culture of human prostate tumours. Clin. Cancer Res. 18, 3562-3570 (2012).
25. Schiewer, M. J. et al. Dual roles of PARP-1 promote cancer growth and progression. Cancer Discov. 2, 1134-1149 (2012).
26. Bray, K. et al. Bcl-2 modulation to activate apoptosis in prostate cancer. Mol. Cancer Res. 7, 1487-1496 (2009).
27. Geller, J. et al. Genistein inhibits the growth of human-patient BPH and prostate cancer in histoculture. Prostate 34, 75-79 (1998).
28. Papini, S. et al. 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. 203, 209-216 (2007).
29. Nevalainen, M. T. et al. Hormone regulation of human prostate in organ culture. Cancer Res. 53, 199-207 (1993).
30. 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 21, 269-278 (1992).
31. Jaamaa, S. et al. DNA damage recognition via activated ATM and p53 pathway in nonproliferating human prostate tissue. Cancer Res. 70, 630-641 (2010).
32. Castells, M., Thibault, B., Delord, J. P. & Couderc, B. Implication of tumour microenvironment in chemoresistance: tumour-associated stromal cells protect tumour cells from cell death. Int. J. Mol. Sci. 13, 545-571 (2012).
33. Hallden, G. Adenoviral gene expression and replication in human tumour explant models. Methods Mol. Biol. 797, 65-78 (2012).
34. Scher, H. I. et al. Design and end points of clinical trials for patients with progressive prostate cancer and castrate levels of testosterone: recommendations of the Prostate Cancer Clinical Trials Working Group. J. Clin. Oncol. 26, 1148-1159 (2008).
35. Collette, L. et al. Is prostate-specific antigen a valid surrogate end point for survival in hormonally treated patients with metastatic prostate cancer? Joint research of the European Organization for Research and Treatment of Cancer, the Limburgs Universitair Centrum, and AstraZeneca Pharmaceuticals. J. Clin. Oncol. 23, 139-148 (2005).
36. Tan, D. S. et al. Biomarker-driven early clinical trials in oncology: a paradigm shift in drug development. Cancer J. 15, 406-420 (2009).
37. Khleif, S. N., Doroshow, J. H. & Hait, W. N. AACR-FDA-NCI Cancer Biomarkers Collaborative consensus report: advancing the use of biomarkers in cancer drug development. Clin. Cancer Res. 16, 299-318 (2010).
38. Stonington, O. G. & Haemmingsen, H. Culture of cells as a monolayer derived from the epithelium of the human prostate: a new cell growth technique. J. Urol. 106, 393-400 (1971).
39. Kreisberg, J. I., Brattain, M. G. & Pretlow, T. G. Studies on human hyperplastic prostates maintained in organ culture. Invest. Urol. 15, 252-255 (1977).
40. Sanefuji, H., Heatfield, B. M., Trump, B. F. & Young, J. D. Jr. Studies on carcinogenesis of human prostate. II. Long-term explant culture of normal prostate and benign prostatic hyperplasia: light microscopy. J. Natl Cancer Inst. 69, 751-756 (1982).
41. Jones, E. G. & Harper, M. E. Studies on the proliferation, secretory activities, and epidermal growth factor receptor expression in benign prostatic hyperplasia explant cultures. Prostate 20, 133-149 (1992).
42. Nakhla, A. M., Khan, M. S., Romas, N. P. & Rosner, W. Oestradiol causes the rapid accumulation of cAMP in human prostate. Proc. Natl Acad. Sci. USA 91, 402-405 (1994).
43. Olbina, G., Miljkovic, D., Hoffman, R. M. & Geller, J. New sensitive discovery histoculture model for growth-inhibition studies in prostate cancer and BPH. Prostate 37, 126-129 (1998).
44. Geller, J. et al. Comparison of androgen-independent growth and androgen-dependent growth in BPH and cancer tissue from the same radical prostatectomies in sponge-gel matrix histoculture. Prostate 31, 250-254 (1997).
45. Schrodt, G. R. & Foreman, C. D. In vitro maintenance of human hyperplastic prostate tissue. Invest. Urol. 9, 85-94 (1971).
46. McMahon, M. J., Butler, A. V. & Thomas, G. H. Morphological responses of prostatic carcinoma to testosterone in organ culture. Br. J. Cancer 26, 388-394 (1972).
47. McMahon, M. J. & Thomas, G. H. Morphological changes of benign prostatic hyperplasia in culture. Br. J. Cancer 27, 323-335 (1973).
48. Mistry, D., Weaver, J. P. & Riches, A. Organ culture studies of human prostatic adenocarcinomas. Prostate 4, 307-314 (1983).
49. Eigeliene, N., Harkonen, P. & Erkkola, R. Effects of oestradiol and medroxyprogesterone acetate in morphology, proliferation and apoptosis of human breast tissue in organ cultures. BMC Cancer 6, 246-259 (2006).