High fidelity patient-derived xenografts for accelerating prostate cancer discovery and drug development

Cancer Research

Volumn 74, Issue 4, 2014, Pages 1272-1283

  Lin, Dong ^a,b   Wyatt, Alexander W ^a   Xue, Hui ^b   Wang, Yuwei ^b   Dong, Xin ^b   Haegert, Anne ^a   Wu, Rebecca ^b   Brahmbhatt, Sonal ^a   Mo, Fan ^a   Jong, Lina ^a   Bell, Robert H ^a   Anderson, Shawn ^a   Hurtado Coll, Antonio ^a   Fazli, Ladan ^a   Sharma, Manju ^a   Beltran, Himisha ^c   Rubin, Mark ^c   Cox, Michael ^a   Gout, Peter W ^b   Morris, James ^b   Goldenberg, Larry ^a   Volik, Stanislav V ^a   Gleave, Martin E ^a   Collins, Colin C ^a   Wang, Yuzhuo ^a,b   more..

^a UNIVERSITY OF BRITISH COLUMBIA   (Canada)

^b BC Cancer Agency   (Canada)

^c WEILL CORNELL MEDICAL COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOCARCINOMA; ANIMALS; ANTINEOPLASTIC AGENTS; CELL LINE, TUMOR; DRUG DISCOVERY; EARLY DETECTION OF CANCER; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, INBRED NOD; MICE, SCID; MICE, TRANSGENIC; NEOPLASM TRANSPLANTATION; PROSTATIC NEOPLASMS; TISSUE AND ORGAN PROCUREMENT; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 84894275509     PISSN: 00085472     EISSN: 15387445     Source Type: Journal    
DOI: 10.1158/0008-5472.CAN-13-2921-T     Document Type: Article

References (57)

1. Jemal A, Bray F, Center MM, Ferlay J, Ward E, Forman D.Globalcancer statistics. CA Cancer J Clin 2011;61:69-90.
2. Attard G, Cooper CS, de Bono JS. Steroid hormone receptors in prostate cancer: a hard habit to break? Cancer Cell 2009;16:458-62.
3. Rubin MA, Maher CA, Chinnaiyan AM. Common gene rearrangements in prostate cancer. J Clin Oncol 2011;29:3659-68.
4. Barbieri CE, Baca SC, Lawrence MS, Demichelis F, Blattner M, Theur-illat JP, et al. Exome sequencing identifies recurrent SPOP, FOXA1 and MED12 mutations in prostate cancer. Nat Genet 2012;44:685-9.
5. Grasso CS, Wu YM, Robinson DR, Cao X, Dhanasekaran SM, Khan AP, et al. The mutational landscape of lethal castration-resistant prostate cancer. Nature 2012;487:239-43.
6. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, et al. Integrative genomic profiling of human prostate cancer. Cancer Cell 2010;18:11-22.
7. Lapuk AV, Wu C, Wyatt AW, McPherson A, McConeghy BJ, Brahmb-hatt S, et al. From sequence to molecular pathology, and a mechanism driving the neuroendocrine phenotype in prostate cancer. J Pathol 2012;227:286-97.
8. Johnson JI, Decker S, Zaharevitz D, Rubinstein LV, Venditti JM, Schepartz S, et al. Relationships between drug activity in NCI preclin-ical in vitro and in vivo models and early clinical trials. Br J Cancer 2001;84:1424-31.
9. Sharpless NE, Depinho RA. The mighty mouse: genetically engineered mouse models in cancer drug development. Nat Rev Drug Discov 2006;5:741-54.
10. DiMasi JA, Grabowski HG. Economics of new oncology drug development. J Clin Oncol 2007;25:209-16.
11. Garber K. From human to mouse and back: 'tumorgraft' models surge in popularity. J Natl Cancer Inst 2009;101:6-8.
12. van Weerden WM, de Ridder CM, Verdaasdonk CL, Romijn JC, van der Kwast TH, Schroder FH, et al. Development of seven new human prostate tumor xenograft models and their histopathological characterization. Am J Pathol 1996;149:1055-62.
13. Klein KA, Reiter RE, Redula J, Moradi H, Zhu XL, Brothman AR, et al. Progression of metastatic human prostate cancer to androgen independence in immunodeficient SCID mice. Nat Med 1997;3:402-8.
14. Eva Corey RLV. Xenograft Models of Human Prostate Cancer. In: Leland W.K., Chung WBI, Jonathan W. Simons, editors. Contemporary Cancer Research: Prostate Cancer: Biology, Genetics, and the New Therapeutics. 2nd ed. Totawa: Humana Press Inc.; 2007.
15. Wang Y, Sudilovsky D, Zhang B, Haughney PC, Rosen MA, Wu DS, et al. A human prostatic epithelial model of hormonal carcinogenesis. Cancer Res 2001;61:6064-72.
16. Rubio-Viqueira B, Hidalgo M. Direct in vivo xenograft tumor model for predicting chemotherapeutic drug response in cancer patients. Clin Pharmacol Ther 2009;85:217-21.
17. Staack A, Kassis AP, Olshen A, Wang Y, Wu D, Carroll PR, et al. Quantitation of apoptotic activity following castration in human pros-tatic tissue in vivo. Prostate 2003;54:212-9.
18. Wang Y, Revelo MP, Sudilovsky D, Cao M, Chen WG, Goetz L, et al. Development and characterization of efficient xenograft models for benign and malignant human prostate tissue. Prostate 2005;64: 149-59.
19. Lawrence MG, Taylor RA, Toivanen R, Pedersen J, Norden S, Pook DW, et al. A preclinical xenograft model of prostate cancer using human tumors. Nat Protoc 2013;8:836-48.
20. Toivanen R, Frydenberg M, Murphy D, Pedersen J, Ryan A, Pook D, et al. A preclinical xenograft model identifies castration-tolerant can-cer-repopulating cells in localized prostate tumors. Sci Transl Med 2013;5:187ra71.
21. Lin D, Watahiki A, Bayani J, Zhang F, Liu L, Ling V, et al. ASAP1, a gene at 8q24, is associated with prostate cancer metastasis. Cancer Res 2008;68:4352-9.
22. Wu C, Wyatt AW, Lapuk AV, McPherson A, McConeghy BJ, Bell RH, et al. Integrated genome and transcriptome sequencing identifies a novel form of hybrid and aggressive prostate cancer. J Pathol 2012; 227:53-61.
23. Huang da W, Sherman BT, Lempicki RA. Systematic and integrative analysis of large gene lists using DAVID bioinformatics resources. Nat Protoc 2009;4:44-57.
24. Beltran H, Rickman DS, Park K, Chae SS, Sboner A, MacDonald TY, et al. Molecular characterization of neuroendocrine prostate cancer and identification of new drug targets. Cancer Discov 2011;1: 487-95.
25. McPherson A, Wu C, Wyatt AW, Shah S, Collins C, Sahinalp SC.nFuse: discovery of complex genomic rearrangements in cancer using high-throughput sequencing. Genome Res 2012;22:2250-61.
26. Rowe M, Young LS, Crocker J, Stokes H, Henderson S, Rickinson AB. Epstein-Barr virus (EBV)-associated lymphoproliferative disease in the SCID mouse model: implications for the pathogenesis of EBV-positive lymphomas in man. J Exp Med 1991;173:147-58.
27. Palmgren JS, Karavadia SS, Wakefield MR. Unusual and underappreciated: small cell carcinoma of the prostate. Semin Oncol 2007;34: 22-9.
28. Berger MF, Lawrence MS, Demichelis F, Drier Y, Cibulskis K, Siva-chenko AY, et al. The genomic complexity of primary human prostate cancer. Nature 2011;470:214-20.
29. Volik S, Raphael BJ, Huang G, Stratton MR, Bignel G, Murnane J, et al. Decoding the fine-scale structure of a breast cancer genome and transcriptome. Genome Res 2006;16:394-404.
30. Raphael BJ, Volik S, Yu P, Wu C, Huang G, Linardopoulou EV, et al. A sequence-based survey of the complex structural organization of tumor genomes. Genome Biol 2008;9:R59.
31. Friedlander TW, Roy R, Tomlins SA, Ngo VT, Kobayashi Y, Azameera A, et al. Common structural and epigenetic changes in the genome of castration-resistant prostate cancer. Cancer Res 2012;72:616-25.
32. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, et al. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 2005;310:644-8.
33. Perner S, Mosquera JM, Demichelis F, Hofer MD, Paris PL, Simko J, et al. TMPRSS2-ERG fusion prostate cancer: an early molecular event associated with invasion. Am J Surg Pathol 2007;31:882-8.
34. Carver BS, Tran J, Gopalan A, Chen Z, Shaikh S, Carracedo A, et al. Aberrant ERG expression cooperates with loss of PTEN to promote cancer progression in the prostate. Nat Genet 2009;41:619-24.
35. Nelson EC, Cambio AJ, Yang JC, Ok JH, Lara PN Jr, Evans CP. Clinical implications of neuroendocrine differentiation in prostate cancer. Prostate Cancer Prostatic Dis 2007;10:6-14.
36. Williamson SR, Zhang S, Yao JL, Huang J, Lopez-Beltran A, Shen S, et al. ERG-TMPRSS2 rearrangement is shared by concurrent prostatic adenocarcinoma and prostatic small cell carcinoma and absent in small cell carcinoma of the urinary bladder: evidence supporting monoclonal origin. Mod Pathol 2011;24:1120-7.
37. Lotan TL, Gupta NS, Wang W, Toubaji A, Haffner MC, Chaux A, et al. ERG gene rearrangements are common in prostatic small cell carcinomas. Mod Pathol 2011;24:820-8.
38. Priolo C, Agostini M, Vena N, Ligon AH, Fiorentino M, Shin E, et al. Establishment and genomic characterization of mouse xenografts of human primary prostate tumors. Am J Pathol 2010;176:1901-13.
39. Zhao H, Nolley R, Chen Z, Peehl DM. Tissue slice grafts: an in vivo model of human prostate androgen signaling. Am J Pathol 2010; 177:229-39.
40. Ott CE, Knox FG. Tissue pressures and fluid dynamics in the kidney. Fed Proc 1976;35:1872-5.
41. Pinter G. Renal lymph: vital for the kidney and valuable for the physiologist. Physiology 1988;3:189-93.
42. Tunstead JR, Thomas M, Hornsby PJ. Early events in the formation of a tissue structure from dispersed bovine adrenocortical cells following transplantation into scid mice. J Mol Med 1999;77:666-76.
43. Cunha GR. Epithelial-stromal interactions in development of the uro-genital tract. Int Rev Cytol 1976;47:137-94.
44. Griffin TW, Bogden AE, Reich SD, Antonelli D, Hunter RE, Ward A, et al. Initial clinical trials of the subrenal capsule assay as a predictor of tumor response to chemotherapy. Cancer 1983;52:2185-92.
45. Nemeth JA, Harb JF, Barroso U Jr, He Z, Grignon DJ, Cher ML. Severe combined immunodeficient-hu model of human prostate cancer metastasis to human bone. Cancer Res 1999;59:1987-93.
46. Yonou H, Yokose T, Kamijo T, Kanomata N, Hasebe T, Nagai K, 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;61:2177-82.
47. Liu W, Laitinen S, Khan S, Vihinen M, Kowalski J, Yu G, et al. Copy number analysis indicates monoclonal origin of lethal metastatic prostate cancer. Nat Med 2009;15:559-65.
48. Watahiki A, Wang Y, Morris J, Dennis K, O'Dwyer HM, Gleave M, et al. MicroRNAs associated with metastatic prostate cancer. PLoS ONE 2011;6:e24950.
49. DeRose YS, Wang G, Lin YC, Bernard PS, Buys SS, Ebbert MT, et al. Tumor grafts derived from women with breast cancer authentically reflect tumor pathology, growth, metastasis and disease outcomes. Nat Med 2011;17:1514-20.
50. Cutz JC, Guan J, Bayani J, Yoshimoto M, Xue H, Sutcliffe M, et al. Establishment in severe combined immunodeficiency mice of sub-renal capsule xenografts and transplantable tumor lines from a variety of primary human lung cancers: potential models for studying tumor progression-related changes. Clin Cancer Res 2006;12: 4043-54.
51. Tzelepi V, Zhang J, Lu JF, Kleb B, Wu G, Wan X, et al. Modeling a lethal prostate cancer variant with small-cell carcinoma features. Clin Cancer Res 2012;18:666-77.
52. Scher HI, Fizazi K, Saad F, Taplin ME, Sternberg CN, Miller K, et al. Increased survival with enzalutamide in prostate cancer after chemotherapy. N Engl J Med 2012;367:1187-97.
53. Fizazi K, Scher HI, Molina A, Logothetis CJ, Chi KN, Jones RJ, et al. Abiraterone acetate for treatment of metastatic castration-resistant prostate cancer: final overall survival analysis of the COU-AA-301 randomised, double-blind, placebo-controlled phase 3 study. Lancet Oncol 2012;13:983-92.
54. Dong X, Guan J, English JC, Flint J, Yee J, Evans K, et al. Patient-derived first generation xenografts of non-small cell lung cancers: promising tools for predicting drug responses for personalized chemotherapy. Clin Cancer Res 2010;16:1442-51.
55. Kortmann U, McAlpine JN, Xue H, Guan J, Ha G, Tully S, et al. Tumor growth inhibition by olaparib in BRCA2 germline-mutated patient-derived ovarian cancer tissue xenografts. Clin Cancer Res 2011;17: 783-91.
56. Collins CC, Volik SV, Lapuk AV, Wang Y, Gout PW, Wu C, et al. Next generation sequencing of prostate cancer from a patient identifies a deficiency of methylthioadenosine phosphorylase, an exploitable tumor target. Mol Cancer Ther 2012;11:775-83.
57. Andersen RJ, Mawji NR, Wang J, Wang G, Haile S, Myung JK, et al. Regression of castrate-recurrent prostate cancer by a small-molecule inhibitor of the amino-terminus domain of the androgen receptor. Cancer Cell 2010;17:535-46.