A novel patient-derived intra-femoral xenograft model of bone metastatic prostate cancer that recapitulates mixed osteolytic and osteoblastic lesions

Journal of Translational Medicine

Volumn 9, Issue 1, 2011, Pages

  Raheem, Omer ^a,b   Kulidjian, Anna A ^a,b   Wu, Christina ^a,b   Jeong, Young B ^a,b,d   Yamaguchi, Tomonori ^b   Smith, Kristen M ^a,b   Goff, Daniel ^a,b   Leu, Heather ^a,b   Morris, Sheldon R ^b   Cacalano, Nicholas A ^c   Masuda, Koichi ^b   Jamieson, Catriona H M ^a,b   Kane, Christopher J ^a,b   Jamieson, Christina A M ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

^d Chonbuk National University   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ANDROGEN RECEPTOR; BIOLOGICAL MARKER; CYTOKERATIN 18; CYTOKERATIN 8; PROSTATE SPECIFIC ANTIGEN; PROTEIN AMACR; PROTEIN NKX3.1; TRANSCRIPTION FACTOR; UNCLASSIFIED DRUG; TUMOR MARKER;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTHROPLASTY; ARTICLE; BONE METASTASIS; CANCER CELL CULTURE; CANCER TISSUE; CANCER TRANSPLANTATION; CONTROLLED STUDY; FEMUR; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOHISTOCHEMISTRY; MALE; MICRO-COMPUTED TOMOGRAPHY; MOUSE; NONHUMAN; PROSTATE CANCER; REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; TUMOR XENOGRAFT; ANIMAL; DRUG SCREENING; FEMUR TUMOR; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; METASTASIS; MOUSE MUTANT; OSTEOBLAST; OSTEOLYSIS; PATHOLOGY; PROSTATE TUMOR; RADIOGRAPHY; TUMOR CELL LINE;

ANIMALS; CELL LINE, TUMOR; FEMORAL NEOPLASMS; FEMUR; GENE EXPRESSION REGULATION, NEOPLASTIC; HUMANS; MALE; MICE; MICE, SCID; OSTEOBLASTS; OSTEOLYSIS; PROSTATE-SPECIFIC ANTIGEN; PROSTATIC NEOPLASMS; RECEPTORS, ANDROGEN; TUMOR MARKERS, BIOLOGICAL; X-RAY MICROTOMOGRAPHY; XENOGRAFT MODEL ANTITUMOR ASSAYS;

EID: 80055015466     PISSN: None     EISSN: 14795876     Source Type: Journal    
DOI: 10.1186/1479-5876-9-185     Document Type: Article

References (72)

1. Sturge J, Caley MP, Waxman J. Bone metastasis in prostate cancer: emerging therapeutic strategies. Nat Rev Clin Oncol 2011, 8:357-68.
2. Mehra R, Kumar-Sinha C, Shankar S, Lonigro RJ, Jing X, Philips NE, Siddiqui J, Han B, Cao X, Smith DC, Shah RB, Chinnaiyan AM, Pienta KJ. Characterization of bone metastases from rapid autopsies of prostate cancer patients. Clin Cancer Res 2011, 17:3924-32. 10.1158/1078-0432.CCR-10-3120, 21555375.
3. Koeneman KS, Yeung F, Chung LW. Osteomimetic properties of prostate cancer cells: a hypothesis supporting the predilection of prostate cancer metastasis and growth in the bone environment. Prostate 1999, 39:246-261. 10.1002/(SICI)1097-0045(19990601)39:4<246::AID-PROS5>3.0.CO;2-U, 10344214.
4. Virk MS, Lieberman JR. Tumor metastasis to bone. Arthritis Res Ther 2007, 9(Suppl 1):S5. 10.1186/ar2169, 2072883, 17767743.
5. Kim HS, Freedland SJ. Androgen deprivation therapy in prostate cancer: anticipated side-effects and their management. Curr Opin Support Palliat Care 2010, 4:147-52. 10.1097/SPC.0b013e32833bd913, 20592607.
6. Guise T. Examining the metastatic niche: targeting the microenvironment. Semin Oncol 2010, 37(Suppl 2):S2-14.
7. Suva LJ, Washam C, Nicholas RW, Griffin RJ. Bone metastasis: mechanisms and therapeutic opportunities. Nat Rev Endocrinol 2011, 7:208-18. 10.1038/nrendo.2010.227, 3134309, 21200394.
8. Wilson C, Coleman RE. Adjuvant therapy with bone-targeted agents. CurrOpinSupportPalliatCare 2011, 5:241-50.
9. Body JJ. New developments for treatment and prevention of bone metastases. Curr Opin Oncol 2011, 23:338-42. 10.1097/CCO.0b013e328347918b, 21519257.
10. Puhaindran ME, Farooki A, Steensma MR, Hameed M, Healey JH, Boland PJ. Atypical subtrochanteric femoral fractures in patients with skeletal malignant involvement treated with intravenous bisphosphonates. J Bone Joint Surg Am 2011, 93:1235-42. 10.2106/JBJS.J.01199, 21776577.
11. Henry DH, Costa L, Goldwasser F, Hirsh V, Hungria V, Prausova J, Scagliotti GV, Sleeboom H, Spencer A, Vadhan-Raj S, von Moos R, Willenbacher W, Woll PJ, Wang J, Jiang Q, Jun S, Dansey R, Yeh HJ. Randomized, double-blind study of denosumab versus zoledronic acid in the treatment of bone metastases in patients with advanced cancer (excluding breast and prostate cancer) or multiple myeloma. Clin Oncol 2011, 29:1125-32.
12. Lee RJ, Saylor PJ, Smith MR. Treatment and prevention of bone complications from prostate cancer. Bone 2011, 48:88-95. 10.1016/j.bone.2010.05.038, 20621630.
13. Fizazi K, Carducci M, Smith M, Damião R, Brown J, Karsh L, Milecki P, Shore N, Rader M, Wang H, Jiang Q, Tadros S, Dansey R, Goessl C. Denosumab versus zoledronic acid for treatment of bone metastases in men with castration-resistant prostate cancer: a randomised, double-blind study. Lancet 2011, 377:813-22. 10.1016/S0140-6736(10)62344-6, 3090685, 21353695.
14. Sartor O. Denosumab in bone-metastatic prostate cancer: known effects on skeletal-related events but unknown effects on quality of life. Asian J Androl 2011, 13:612-3. 10.1038/aja.2011.33, 21499282.
15. Sonpavde G, Sternberg CN. Contemporary management of metastatic castration-resistant prostate cancer. Curr Opin Urol 2011, 21:241-7. 10.1097/MOU.0b013e3283449e19, 21455038.
16. Smith MR, Brown GA, Saad F. New opportunities in the management of prostate cancer-related bone complications. Urologic Oncology: Seminars and Original Investigations 2009, 27(Suppl 1):S1-S20.
17. Hurwitz AA, Foster BA, Allison JP, Greenberg NM, Kwon ED. The TRAMP mouse as a model for prostate cancer. Current Protocols in Immunology 2001, 20.5.1-20.5.23.
18. Pienta KJ, Abate-Shen C, Agus DB, Attar RM, Chung LW, Greenberg NM, Hahn WC, Isaacs JT, Navone NM, Peehl DM, Simons JW, Solit DB, Soule HR, VanDyke TA, Weber MJ, Wu L, Vessella RL. The current state of preclinical prostate cancer animal models. Prostate 2008, 68:629-39. 10.1002/pros.20726, 18213636.
19. Lopez-Barcons LA. Human prostate cancer heterotransplants: a review on this experimental model. Asian J Androl 2010, 12:509-18. 10.1038/aja.2010.17, 20364154.
20. Corey E, Quinn JE, Bladou F, Brown LG, Roudier MP, Brown JM, Buhler KR, Vessella RL. Establishment and characterization of osseous prostate cancer models: intra-tibial injection of human prostate cancer cells. Prostate 2002, 52:20-33. 10.1002/pros.10091, 11992617.
21. Davies MR, Lee YP, Lee C, Zhang X, Afar DE, Lieberman JR. Use of a SCID mouse model to select for a more aggressive strain of prostate cancer. Anticancer Res 2003, 23:2245-52.
22. Lin DL, Tarnowski CP, Zhang J, Dai J, Rohn E, Patel AH, Morris MD, Keller ET. Bone metastatic LNCaP-derivative C4-2B prostate cancer cell line mineralizes in vitro. Prostate 2001, 47:212-221. 10.1002/pros.1065, 11351351.
23. Morrissey C, Kostenuik PL, Brown LG, Vessella RL, Corey E. Host-derived RANKL is responsible for osteolysis in a C4-2 human prostate cancer xenograft model of experimental bone metastases. BMC Cancer 2007, 7:148. 10.1186/1471-2407-7-148, 2034387, 17683568.
24. Tsingotjidou AS, Zotalis G, et al. Development of an animal model for prostate cancer cell metastasis to adult human bone. Anticancer Res 2001, 21:971-8.
25. Lee Y, Schwarz E, Davies M, Jo M, Gates J, Wu J, Zhang X, Lieberman JR. Differences in the cytokine profiles associated with prostate cancer cell induced osteoblastic and osteolytic lesions in bone. J Orthop Res 2003, 21:62-72. 10.1016/S0736-0266(02)00095-5, 12507581.
26. Craft N, Chor C, et al. Evidence for clonal outgrowth of androgen-independent prostate cancer cells from androgen-dependent tumors through a two-step process. Cancer Research 1999, 59:5030-5036.
27. Gamradt SC, Feeley BT, Liu NQ, Roostaeian J, Lin YQ, Zhu LX, Sharma S, Dubinett SM, Lieberman JR. The effect of cyclooxygenase-2 (COX-2) inhibition on human prostate cancer induced osteoblastic and osteolytic lesions in bone. Anticancer Res 2005, 25:107-15.
28. Feeley B, Gamradt SC, Hsu WK, et al. Influence of BMPs on the formation of osteoblastic lesions in metastatic prostate cancer. J Bone and Mineral Research 2005, 20:2189-2199.
29. Ristevski B, Jenkinson RJ, Stephen DJ, Finkelstein J, Schemitsch EH, McKee MD, Kreder HJ. Mortality and complications following stabilization of femoral metastatic lesions: a population-based study of regional variation and outcome. Can J Surg 2009, 52:302-308. 2724796, 19680515.
30. Piccioli A, Maccauro G, Rossi B, Scaramuzzo L, Frenos F, Capanna R. Surgical treatment of pathologic fractures of humerus. Injury 2010, 41:1112-6. 10.1016/j.injury.2010.08.015, 20828692.
31. Hsu WK, Virk MS, Feeley BT, Stout DB, Chatziioannou AF, Lieberman JR. Characterization of osteolytic, osteoblastic, and mixed lesions in a prostate cancer mouse model using 18F-FDG and 18F-fluoride PET/CT. J Nucl Med 2008, 49:414-21. 10.2967/jnumed.107.045666, 2678960, 18287261.
32. Li X, Loberg R, Liao J, Ying C, Snyder LA, Pienta KJ, McCauley LK. A destructive cascade mediated by CCL2 facilitates prostate cancer growth in bone. CancerRes 2009, 69:1685-92.
33. Klein KA, Reiter RE, Redula J, Moradi H, Zhu XL, Brothman AR, Lamb DJ, Marcelli M, Belldegrun A, Witte ON, Sawyers CL. Progression of metastatic human prostate cancer to androgen independence in immunodeficient SCID mice. Nat Med 1997, 3:402-408. 10.1038/nm0497-402, 9095173.
34. Nickerson T, Chang F, Lorimer D, et al. In vivo progression of LAPC-9 and LNCaP prostate cancer models to androgen independence is associated with increased expression of insulin-like growth factor I (IGF-I) and IGF-I receptor (IGF-IR). Cancer Res 2001, 61:6276-80.
35. Sandberg R, Ernberg I. The molecular portrait of in vitro growth by meta-analysis of gene-expression profiles. Genome Biol 2005, 6:R65. 10.1186/gb-2005-6-8-r65, 1273632, 16086847.
36. Taylor BS, Schultz N, Hieronymus H, Gopalan A, Xiao Y, Carver BS, Arora VK, Kaushik P, Cerami E, Reva B, Antipin Y, Mitsiades N, Landers T, Dolgalev I, Major JE, Wilson M, Socci ND, Lash AE, Heguy A, Eastham JA, Scher HI, Reuter VE, Scardino PT, Sander C, Sawyers CL, Gerald WL. Integrative genomic profiling of human prostate cancer. Cancer Cell 2010, 18:11-22. 10.1016/j.ccr.2010.05.026, 3198787, 20579941.
37. Berger MF, Lawrence MS, Demichelis F, Drier Y, Cibulskis K, Sivachenko AY, Sboner A, Esgueva R, Pflueger D, Sougnez C, Onofrio R, Carter SL, Park K, Habegger L, Ambrogio L, Fennell T, Parkin M, Saksena G, Voet D, Ramos AH, Pugh TJ, Wilkinson J, Fisher S, Winckler W, Mahan S, Ardlie K, Baldwin J, Simons JW, Kitabayashi N, MacDonald TY, Kantoff PW, Chin L, Gabriel SB, Gerstein MB, Golub TR, Meyerson M, Tewari A, Lander ES, Getz G, Rubin MA, Garraway LA. The genomic complexity of primary human prostate cancer. Nature 2011, 470:214-20. 10.1038/nature09744, 3075885, 21307934.
38. Kim JH, Dhanasekaran SM, Prensner JR, Cao X, Robinson D, Kalyana-Sundaram S, Huang C, Shankar S, Jing X, Iyer M, Hu M, Sam L, Grasso C, Maher CA, Palanisamy N, Mehra R, Kominsky HD, Siddiqui J, Yu J, Qin ZS, Chinnaiyan AM. Deep sequencing reveals distinct patterns of DNA methylation in prostate cancer. Genome Res 2011, 21:1028-41. 10.1101/gr.119347.110, 21724842.
39. Virk MS, Petrigliano FA, Liu NQ, Chatziioannou AF, Stout D, Kang CO, Dougall WC, Lieberman JR. Influence of simultaneous targeting of the bone morphogenetic protein pathway and RANK/RANKL axis in osteolytic prostate cancer lesion in bone. Bone 2009, 44:160-7. 10.1016/j.bone.2008.09.009, 2657045, 18929692.
40. Hung TT, Chan J, Russell PJ, Power CA. Zoledronic acid preserves bone structure and increases survival but does not limit tumour incidence in a prostate cancer bone metastasis model. PLoS One 2011, 6:e19389. 10.1371/journal.pone.0019389, 3095598, 21603655.
41. Bruni-Cardoso A, Johnson LC, Vessella RL, Peterson TE, Lynch CC. Osteoclast-Derived Matrix Metalloproteinase-9 Directly Affects Angiogenesis in the Prostate Tumor-Bone Microenvironment. Mol Cancer Res 2010, 8:459-70. 10.1158/1541-7786.MCR-09-0445, 2946627, 20332212.
42. Chen CD, Welsbie DS, Tran C, et al. Molecular determinants of resistance to antiandrogen therapy. Nat Med 2004, 10:33-39. 10.1038/nm972, 14702632.
43. Collins AT, Berry PA, Hyde C, et al. Prospective identification of tumorigenic prostate cancer stem cells. Cancer Res 2005, 65:10946-10951. 10.1158/0008-5472.CAN-05-2018, 16322242.
44. Duhagon MA, Hurte EM, Sotelo-Silveira JR, Zhang X, Farrar WL. Genomic profiling of tumor initiating prostatospheres. BMC Genomics 2010, 11:324. 10.1186/1471-2164-11-324, 2900264, 20500816.
45. Garraway IP, Sun W, Tran CP, et al. Human prostate sphere-forming cells represent a subset of basal epithelial cells capable of glandular regeneration in vivo. Prostate 2010, 70:491-501. 2885946, 19938015.
46. Goldstein AS, Huang J, Guo C, Garraway IP, Witte ON. Identification of a cell of origin for human prostate cancer. Science 2010, 329:568-71. 10.1126/science.1189992, 2917982, 20671189.
47. Gregg JL, Brown KE, Mintz EM, et al. Analysis of gene expression in prostate cancer epithelial and interstitial stromal cells using laser capture microdissection. BMC Cancer 2010, 10:165. 10.1186/1471-2407-10-165, 2876079, 20426842.
48. Mitra N, Banda K, Altheide TK, Schaffer L, Johnson-Pais TL, Beuten J, Leach RJ, Angata T, Varki N, Varki A. SIGLEC12, a Human-specific Segregating (Pseudo)gene, Encodes a Signaling Molecule Expressed in Prostate Carcinomas. J Biol Chem 2011, 286:23003-11. 10.1074/jbc.M111.244152, 21555517.
49. Lavoie, et al. Skin-derived precursors differentiate into skeletogenic cell types and contribute to bone repair. Stem Cells and Development 2009, 18:893-906. 10.1089/scd.2008.0260, 18834279.
50. Ritacco LE, et al. Three-dimensional morphometric analysis of the distal femur: a validity method for allograft selection using a virtual bone bank. Stud Health Technol Inform 2010, 160:1287-90.
51. Ochia RS, et al. Three-dimensional in vivo measurement of lumbar spine segmental motion. Spine 2006, 31:2073-8. 10.1097/01.brs.0000231435.55842.9e, 16915091.
52. Abrahamsson AE, Geron I, Gotlib J, Dao KH, Barroga CF, Newton IG, Giles FJ, Durocher J, Creusot RS, Karimi M, Jones C, Zehnder JL, Keating A, Negrin RS, Weissman IL, Jamieson CH. Glycogen synthase kinase 3beta missplicing contributes to leukemia stem cell generation. Proc Natl Acad Sci USA 2009, 106:3925-9. 10.1073/pnas.0900189106, 2646624, 19237556.
53. Sun S, Sprenger CC, Vessella RL, Haugk K, Soriano K, Mostaghel EA, Page ST, Coleman IM, Nguyen HM, Sun H, Nelson PS, Plymate SR. Castration resistance in human prostate cancer is conferred by a frequently occurring androgen receptor splice variant. J Clin Invest 2010, 120:2715-30. 10.1172/JCI41824, 2912187, 20644256.
54. Watson PA, Chen YF, Balbas MD, Wongvipat J, Socci ND, Viale A, Kim K, Sawyers CL. Constitutively active androgen receptor splice variants expressed in castration-resistant prostate cancer require full-length androgen receptor. Proc Natl Acad SciUSA 2010, 107:16759-65.
55. Lawson DA, Zong Y, Memarzadeh S, Xin L, et al. Basal epithelial stem cells are efficient targets for prostate cancer initiation. Proc Natl Acad SciUSA 2010, 107:2610-5.
56. Ouyang B, Leung YK, Wang V, Chung E, Levin L, Bracken B, Cheng L, Ho SM. α-Methylacyl-CoA racemase spliced variants and their expression in normal and malignant prostate tissues. Urology 2011, 77:249.e1-7.
57. Johnson MB, Kawasawa YI, Mason CE, et al. Functional and evolutionary insights into human brain development through global transcriptome analysis. Neuron 2009, 62:494-509. 10.1016/j.neuron.2009.03.027, 2739738, 19477152.
58. Nervina JM, Magyar CE, Pirih FQ, Tetradis S. PGC-1alpha is induced by parathyroid hormone and coactivates Nurr1-mediated promoter activity in osteoblasts. Bone 2006, 39:1018-25. 10.1016/j.bone.2006.04.023, 16765661.
59. Tomlins SA, Rhodes DR, Perner S, Dhanasekaran SM, Mehra R, Sun XW, Varambally S, Cao X, Tchinda J, Kuefer R, Lee C, Montie JE, Shah RB, Pienta KJ, Rubin MA, Chinnaiyan AM. Recurrent fusion of TMPRSS2 and ETS transcription factor genes in prostate cancer. Science 2005, 310:644-8. 10.1126/science.1117679, 16254181.
60. Ibrahim T, Flamini E, Mercatali L, Sacanna E, Serra P, Amadori D. Pathogenesis of osteoblastic bone metastases from prostate cancer. Cancer 2010, 116:1406-18. 10.1002/cncr.24896, 20108337.
61. Grubb RL, Deng J, Pinto PA, et al. Pathway biomarker profiling of localized and metastatic human prostate cancer reveal metastatic and prognostic signatures. J Proteome Res 2009, 8:3044-54. 10.1021/pr8009337, 2790378, 19275204.
62. Ugolkov AV, Eisengart LJ, Luan C, Yang XJ. Expression analysis of putative stem cell markers in human benign and malignant prostate. Prostate 2011, 71:18-25. 10.1002/pros.21217, 20583131.
63. Wang X, Kruithof-de Julio M, Economides KD, et al. A luminal epithelial stem cell that is a cell of origin for prostate cancer. Nature 2009, 461:495-500. 10.1038/nature08361, 2800362, 19741607.
64. Petrigliano FA, Virk MS, Liu N, Sugiyama O, Yu D, Lieberman JR. Targeting of prostate cancer cells by a cytotoxic lentiviral vector containing a prostate stem cell antigen (PSCA) promoter. Prostate 2009, 69:1422-34. 10.1002/pros.20989, 19489029.
65. Schayek H, Seti H, Greenberg NM, Sun S, Werner H, Plymate SR. Differential regulation of insulin-like growth factor-I receptor gene expression by wild type and mutant androgen receptor in prostate cancer cells. Mol Cell Endocrinol 2010, 323:239-45. 10.1016/j.mce.2010.04.017, 2896981, 20417685.
66. Klarmann GJ, Hurt EM, Mathews LA, Zhang X, Duhagon MA, Mistree T, Thomas SB, Farrar WL. Invasive prostate cancer cells are tumor initiating cells that have a stem cell-like genomic signature. Clin Exp Metastasis 2009, 26:433-46. 10.1007/s10585-009-9242-2, 2782741, 19221883.
67. Koreckij T, Nguyen H, Brown LG, Yu EY, Vessella RL, Corey E. Dasatinib inhibits the growth of prostate cancer in bone and provides additional protection from osteolysis. Br J Cancer 2009, 101:263-8. 10.1038/sj.bjc.6605178, 2720213, 19603032.
68. Tang Y, Hamburger AW, Wang L, et al. Androgen deprivation and stem cell markers in prostate cancers. Int J Clin Exp Pathol 2009, 3:128-38. 2809992, 20126580.
69. Tran C, Ouk S, Clegg NJ, Chen Y, Watson PA, Arora V, Wongvipat J, Smith-Jones PM, Yoo D, Kwon A, Wasielewska T, Welsbie D, Chen CD, Higano CS, Beer TM, Hung DT, Scher HI, Jung ME, Sawyers CL. Development of a second-generation antiandrogen for treatment of advanced prostate cancer. Science 2009, 324:787-90. 10.1126/science.1168175, 2981508, 19359544.
70. Scher HI, Beer TM, Higano CS, et al. Antitumour activity of MDV3100 in castration-resistant prostate cancer: a phase 1-2 study. Lancet 2010, 375:1437-46. 10.1016/S0140-6736(10)60172-9, 2948179, 20398925.
71. Ryan CJ, Shah S, Efstathiou E, Smith MR, Taplin ME, Bubley GJ, Logothetis CJ, Kheoh T, Kilian C, Haqq CM, Molina A, Small EJ. Phase II study of abiraterone acetate in chemotherapy-naive metastatic castration-resistant prostate cancer displaying bone flare discordant with serologic response. Clin Cancer Res 2011, 17:4854-61. 10.1158/1078-0432.CCR-11-0815, 21632851.
72. Scholz M. Cabozantinib. PCRI Insights 2011, 14:12-14.