Advertisement

Models of Tumor Progression in Prostate Cancer

  • Waqas Azeem
  • Yaping Hua
  • Karl-Henning Kalland
  • Xisong Ke
  • Jan Roger Olsen
  • Anne Margrete Øyan
  • Yi Qu
Chapter

Abstract

Human prostate cancer is initiated in a benign prostate epithelial cell which gains the potential to progress to metastatic disease. The exact cell of origin of prostate cancer has been debated in recent years based upon different models. Primary prostate epithelial cells have restricted life-spans in culture, but can be immortalized. Prostate cancer cell lines have been difficult to establish and new ones are desirable. Attempts to transform benign prostate epithelial cells in vitro have proved difficult without the use of strong carcinogens or oncogenes in processes not likely to mimic closely carcinogenesis in the aging human prostate. Models of epithelial-to-mesenchymal transition (EMT) and cancer stem cells in prostate carcinogenesis have become available, and advances in three-dimensional organoid culture technology represent a breakthrough in prostate cancer research. Organoids may recapitulate multiple features of prostate cancer and have the potential to replace costly and laborious animal experiments. Still, animal models are needed to investigate and validate molecular mechanisms and to develop therapeutic principles in the pipeline between in vitro experiments and clinical applications. Although mice represent the most common experimental animal in prostate cancer research, species like rat, dog, and zebrafish may have advantages depending upon the hypothesis or question. Animal models can generally be categorized into spontaneous or induced development of cancer, immunodeficient animals with xenografts, and genetically engineered animals. In prostate cancer, neuroendocrine differentiation and bone metastases are prevalent in the final stages of cancer progression and animal models that recapitulate these processes are available.

Keywords

Prostate cancer Animal model Cell culture model Prostate cell 

References

  1. 1.
    Rostad K, Mannelqvist M, Halvorsen OJ, Oyan AM, Bo TH, Stordrange L, et al. ERG upregulation and related ETS transcription factors in prostate cancer. Int J Oncol. 2007;30(1):19–32.PubMedGoogle Scholar
  2. 2.
    Antony L, van der Schoor F, Dalrymple SL, Isaacs JT. Androgen receptor (AR) suppresses normal human prostate epithelial cell proliferation via AR/beta-catenin/TCF-4 complex inhibition of c-MYC transcription. Prostate. 2014;74(11):1118–31.CrossRefPubMedPubMedCentralGoogle Scholar
  3. 3.
    Lee SH, Shen MM. Cell types of origin for prostate cancer. Curr Opin Cell Biol. 2015;37:35–41.CrossRefPubMedGoogle Scholar
  4. 4.
    Strand DW, Goldstein AS. The many ways to make a luminal cell and a prostate cancer cell. Endocr Relat Cancer. 2015;22(6):T187–97.CrossRefPubMedPubMedCentralGoogle Scholar
  5. 5.
    Watson PA, Arora VK, Sawyers CL. Emerging mechanisms of resistance to androgen receptor inhibitors in prostate cancer. Nat Rev Cancer. 2015;15:701.CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Berman-Booty LD, Knudsen KE. Models of neuroendocrine prostate cancer. Endocr Relat Cancer. 2015;22(1):R33–49.CrossRefPubMedGoogle Scholar
  7. 7.
    Terry S, Beltran H. The many faces of neuroendocrine differentiation in prostate cancer progression. Front Oncol. 2014;4:60.CrossRefPubMedPubMedCentralGoogle Scholar
  8. 8.
    Rane JK, Pellacani D, Maitland NJ. Advanced prostate cancer--a case for adjuvant differentiation therapy. Nat Rev Urol. 2012;9(10):595–602.CrossRefPubMedGoogle Scholar
  9. 9.
    Rhim JS, Li H, Furusato B. Novel human prostate epithelial cell culture models for the study of carcinogenesis and of normal stem cells and cancer stem cells. Adv Exp Med Biol. 2011;720:71–80.CrossRefPubMedGoogle Scholar
  10. 10.
    Sobel RE, Wang Y, Sadar MD. Molecular analysis and characterization of PrEC, commercially available prostate epithelial cells. In Vitro Cell Dev Biol Anim. 2006;42(1-2):33–9.CrossRefPubMedGoogle Scholar
  11. 11.
    van Bokhoven A, Varella-Garcia M, Korch C, Johannes WU, Smith EE, Miller HL, et al. Molecular characterization of human prostate carcinoma cell lines. Prostate. 2003;57(3):205–25.CrossRefPubMedGoogle Scholar
  12. 12.
    Litvinov IV, Vander Griend DJ, Xu Y, Antony L, Dalrymple SL, Isaacs JT. Low-calcium serum-free defined medium selects for growth of normal prostatic epithelial stem cells. Cancer Res. 2006;66(17):8598–607.CrossRefPubMedPubMedCentralGoogle Scholar
  13. 13.
    Yasunaga Y, Nakamura K, Ewing CM, Isaacs WB, Hukku B, Rhim JS. A novel human cell culture model for the study of familial prostate cancer. Cancer Res. 2001;61(16):5969–73.PubMedGoogle Scholar
  14. 14.
    Kogan I, Goldfinger N, Milyavsky M, Cohen M, Shats I, Dobler G, et al. hTERT-immortalized prostate epithelial and stromal-derived cells: an authentic in vitro model for differentiation and carcinogenesis. Cancer Res. 2006;66(7):3531–40.CrossRefPubMedGoogle Scholar
  15. 15.
    Bello D, Webber MM, Kleinman HK, Wartinger DD, Rhim JS. Androgen responsive adult human prostatic epithelial cell lines immortalized by human papillomavirus 18. Carcinogenesis. 1997;18(6):1215–23.CrossRefPubMedGoogle Scholar
  16. 16.
    Jiang M, Strand DW, Fernandez S, He Y, Yi Y, Birbach A, et al. Functional remodeling of benign human prostatic tissues in vivo by spontaneously immortalized progenitor and intermediate cells. Stem Cells. 2010;28(2):344–56.PubMedPubMedCentralGoogle Scholar
  17. 17.
    Karthaus WR, Iaquinta PJ, Drost J, Gracanin A, van Boxtel R, Wongvipat J, et al. Identification of multipotent luminal progenitor cells in human prostate organoid cultures. Cell. 2014;159(1):163–75.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Palechor-Ceron N, Suprynowicz FA, Upadhyay G, Dakic A, Minas T, Simic V, et al. Radiation induces diffusible feeder cell factor(s) that cooperate with ROCK inhibitor to conditionally reprogram and immortalize epithelial cells. Am J Pathol. 2013;183(6):1862–70.CrossRefPubMedPubMedCentralGoogle Scholar
  19. 19.
    Ke XS, Qu Y, Goldfinger N, Rostad K, Hovland R, Akslen LA, et al. Epithelial to mesenchymal transition of a primary prostate cell line with switches of cell adhesion modules but without malignant transformation. PLoS One. 2008;3(10):e3368.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Ke XS, Li WC, Hovland R, Qu Y, Liu RH, McCormack E, et al. Reprogramming of cell junction modules during stepwise epithelial to mesenchymal transition and accumulation of malignant features in vitro in a prostate cell model. Exp Cell Res. 2011;317(2):234–47.CrossRefPubMedGoogle Scholar
  21. 21.
    Qu Y, Oyan AM, Liu R, Hua Y, Zhang J, Hovland R, et al. Generation of prostate tumor-initiating cells is associated with elevation of reactive oxygen species and IL-6/STAT3 signaling. Cancer Res. 2013;73(23):7090–100.CrossRefPubMedGoogle Scholar
  22. 22.
    Ke XS, Qu Y, Cheng Y, Li WC, Rotter V, Oyan AM, et al. Global profiling of histone and DNA methylation reveals epigenetic-based regulation of gene expression during epithelial to mesenchymal transition in prostate cells. BMC Genomics. 2010;11:669.CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Gravdal K, Halvorsen OJ, Haukaas SA, Akslen LA. A switch from E-cadherin to N-cadherin expression indicates epithelial to mesenchymal transition and is of strong and independent importance for the progress of prostate cancer. Clin Cancer Res. 2007;13(23):7003–11.CrossRefPubMedGoogle Scholar
  24. 24.
    Xie D, Gore C, Liu J, Pong RC, Mason R, Hao G, et al. Role of DAB2IP in modulating epithelial-to-mesenchymal transition and prostate cancer metastasis. Proc Natl Acad Sci U S A. 2010;107(6):2485–90.CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Jadaan DY, Jadaan MM, McCabe JP. Cellular plasticity in prostate cancer bone metastasis. Prostate Cancer. 2015;2015:651580.CrossRefPubMedPubMedCentralGoogle Scholar
  26. 26.
    Nouri M, Ratther E, Stylianou N, Nelson CC, Hollier BG, Williams ED. Androgen-targeted therapy-induced epithelial mesenchymal plasticity and neuroendocrine transdifferentiation in prostate cancer: an opportunity for intervention. Front Oncol. 2014;4:370.CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Olsen JR, Azeem W, Hellem MR, Marvyin K, Hua Y, Qu Y, et al. Context dependent regulatory patterns of the androgen receptor and androgen receptor target genes. BMC Cancer. 2016;16:377.CrossRefPubMedPubMedCentralGoogle Scholar
  28. 28.
    Sun Y, Wang BE, Leong KG, Yue P, Li L, Jhunjhunwala S, et al. Androgen deprivation causes epithelial-mesenchymal transition in the prostate: implications for androgen-deprivation therapy. Cancer Res. 2012;72(2):527–36.CrossRefPubMedGoogle Scholar
  29. 29.
    Wellner U, Schubert J, Burk UC, Schmalhofer O, Zhu F, Sonntag A, et al. The EMT-activator ZEB1 promotes tumorigenicity by repressing stemness-inhibiting microRNAs. Nat Cell Biol. 2009;11(12):1487–95.CrossRefPubMedGoogle Scholar
  30. 30.
    Sampson N, Neuwirt H, Puhr M, Klocker H, Eder IE. In vitro model systems to study androgen receptor signaling in prostate cancer. Endocr Relat Cancer. 2013;20(2):R49–64.CrossRefPubMedGoogle Scholar
  31. 31.
    Sobel RE, Sadar MD. Cell lines used in prostate cancer research: a compendium of old and new lines--part 2. J Urol. 2005;173(2):360–72.CrossRefPubMedGoogle Scholar
  32. 32.
    Sobel RE, Sadar MD. Cell lines used in prostate cancer research: a compendium of old and new lines--part 1. J Urol. 2005;173(2):342–59.CrossRefPubMedGoogle Scholar
  33. 33.
    Wu X, Gong S, Roy-Burman P, Lee P, Culig Z. Current mouse and cell models in prostate cancer research. Endocr Relat Cancer. 2013;20(4):R155–70.CrossRefPubMedGoogle Scholar
  34. 34.
    Lu J, Van der Steen T, Tindall DJ. Are androgen receptor variants a substitute for the full-length receptor? Nat Rev Urol. 2015;12(3):137–44.CrossRefPubMedGoogle Scholar
  35. 35.
    Sharma NL, Massie CE, Ramos-Montoya A, Zecchini V, Scott HE, Lamb AD, et al. The androgen receptor induces a distinct transcriptional program in castration-resistant prostate cancer in man. Cancer Cell. 2013;23(1):35–47.CrossRefPubMedGoogle Scholar
  36. 36.
    Centenera MM, Raj GV, Knudsen KE, Tilley WD, Butler LM. Ex vivo culture of human prostate tissue and drug development. Nat Rev Urol. 2013;10(8):483–7.CrossRefPubMedGoogle Scholar
  37. 37.
    Ellem SJ, De-Juan-Pardo EM, Risbridger GP. In vitro modeling of the prostate cancer microenvironment. Adv Drug Deliv Rev. 2014;79-80:214–21.CrossRefPubMedGoogle Scholar
  38. 38.
    Jung P, Sato T, Merlos-Suarez A, Barriga FM, Iglesias M, Rossell D, et al. Isolation and in vitro expansion of human colonic stem cells. Nat Med. 2011;17(10):1225–7.CrossRefPubMedGoogle Scholar
  39. 39.
    Sato T, Vries RG, Snippert HJ, van de Wetering M, Barker N, Stange DE, et al. Single Lgr5 stem cells build crypt-villus structures in vitro without a mesenchymal niche. Nature. 2009;459(7244):262–5.CrossRefPubMedGoogle Scholar
  40. 40.
    Sachs N, Clevers H. Organoid cultures for the analysis of cancer phenotypes. Curr Opin Genet Dev. 2014;24:68–73.CrossRefPubMedGoogle Scholar
  41. 41.
    Chua CW, Shibata M, Lei M, Toivanen R, Barlow LJ, Bergren SK, et al. Single luminal epithelial progenitors can generate prostate organoids in culture. Nat Cell Biol. 2014;16(10):951–61. 1–4CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Gao D, Vela I, Sboner A, Iaquinta PJ, Karthaus WR, Gopalan A, et al. Organoid cultures derived from patients with advanced prostate cancer. Cell. 2014;159(1):176–87.CrossRefPubMedPubMedCentralGoogle Scholar
  43. 43.
    Cho SW, Kim S, Kim JM, Kim JS. Targeted genome engineering in human cells with the Cas9 RNA-guided endonuclease. Nat Biotechnol. 2013;31(3):230–2.CrossRefPubMedGoogle Scholar
  44. 44.
    Cong L, Ran FA, Cox D, Lin S, Barretto R, Habib N, et al. Multiplex genome engineering using CRISPR/Cas systems. Science. 2013;339(6121):819–23.CrossRefPubMedPubMedCentralGoogle Scholar
  45. 45.
    Mali P, Yang L, Esvelt KM, Aach J, Guell M, DiCarlo JE, et al. RNA-guided human genome engineering via Cas9. Science. 2013;339(6121):823–6.CrossRefPubMedPubMedCentralGoogle Scholar
  46. 46.
    Drost J, van Jaarsveld RH, Ponsioen B, Zimberlin C, van Boxtel R, Buijs A, et al. Sequential cancer mutations in cultured human intestinal stem cells. Nature. 2015;521(7550):43–7.CrossRefPubMedGoogle Scholar
  47. 47.
    Ittmann M, Huang J, Radaelli E, Martin P, Signoretti S, Sullivan R, et al. Animal models of human prostate cancer: the consensus report of the New York meeting of the mouse models of human cancers consortium prostate pathology committee. Cancer Res. 2013;73(9):2718–36.CrossRefPubMedPubMedCentralGoogle Scholar
  48. 48.
    Toivanen R, Taylor RA, Pook DW, Ellem SJ, Risbridger GP. Breaking through a roadblock in prostate cancer research: an update on human model systems. J Steroid Biochem. 2012;131(3–5):122-131.Google Scholar
  49. 49.
    Zong Y, Goldstein AS, Witte ON. Dissociated prostate regeneration under the renal capsule. Cold Spring Harb Protoc. 2015;2015(11):991.PubMedGoogle Scholar
  50. 50.
    Shultz LD, Goodwin N, Ishikawa F, Hosur V, Lyons BL, Greiner DL. Human cancer growth and therapy in immunodeficient mouse models. Cold Spring Harb Protoc. 2014;2014(7):694–708.PubMedPubMedCentralGoogle Scholar
  51. 51.
    Cassidy JW, Caldas C, Bruna A. Maintaining tumor heterogeneity in patient-derived tumor xenografts. Cancer Res. 2015;75(15):2963–8.CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Eirew P, Steif A, Khattra J, Ha G, Yap D, Farahani H, et al. Dynamics of genomic clones in breast cancer patient xenografts at single-cell resolution. Nature. 2015;518(7539):422–6.CrossRefPubMedGoogle Scholar
  53. 53.
    Choi SY, Lin D, Gout PW, Collins CC, Xu Y, Wang Y. Lessons from patient-derived xenografts for better in vitro modeling of human cancer. Adv Drug Deliv Rev. 2014;79-80:222–37.CrossRefPubMedGoogle Scholar
  54. 54.
    Malaney P, Nicosia SV, Dave V. One mouse, one patient paradigm: new avatars of personalized cancer therapy. Cancer Lett. 2014;344(1):1–12.CrossRefPubMedGoogle Scholar
  55. 55.
    Grabowska MM, DeGraff DJ, Yu X, Jin RJ, Chen Z, Borowsky AD, et al. Mouse models of prostate cancer: picking the best model for the question. Cancer Metastasis Rev. 2014;33(2-3):377–97.CrossRefPubMedPubMedCentralGoogle Scholar
  56. 56.
    Irshad S, Abate-Shen C. Modeling prostate cancer in mice: something old, something new, something premalignant, something metastatic. Cancer Metastasis Rev. 2013;32(1-2):109–22.CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Jeet V, Russell PJ, Khatri A. Modeling prostate cancer: a perspective on transgenic mouse models. Cancer Metastasis Rev. 2010;29(1):123–42.CrossRefPubMedGoogle Scholar
  58. 58.
    Parisotto M, Metzger D. Genetically engineered mouse models of prostate cancer. Mol Oncol. 2013;7(2):190–205.CrossRefPubMedPubMedCentralGoogle Scholar
  59. 59.
    Saxena M, Christofori G. Rebuilding cancer metastasis in the mouse. Mol Oncol. 2013;7(2):283–96.CrossRefPubMedPubMedCentralGoogle Scholar
  60. 60.
    van Marion DM, Domanska UM, Timmer-Bosscha H, Walenkamp AM. Studying cancer metastasis: existing models, challenges and future perspectives. Crit Rev Oncol Hematol. 2015;97:107.CrossRefPubMedGoogle Scholar
  61. 61.
    Greenberg NM, DeMayo F, Finegold MJ, Medina D, Tilley WD, Aspinall JO, et al. Prostate cancer in a transgenic mouse. Proc Natl Acad Sci U S A. 1995;92(8):3439–43.CrossRefPubMedPubMedCentralGoogle Scholar
  62. 62.
    Hawksworth D, Ravindranath L, Chen Y, Furusato B, Sesterhenn IA, McLeod DG, et al. Overexpression of C-MYC oncogene in prostate cancer predicts biochemical recurrence. Prostate Cancer Prostatic Dis. 2010;13(4):311–5.CrossRefPubMedGoogle Scholar
  63. 63.
    Gil J, Kerai P, Lleonart M, Bernard D, Cigudosa JC, Peters G, et al. Immortalization of primary human prostate epithelial cells by c-Myc. Cancer Res. 2005;65(6):2179–85.CrossRefPubMedGoogle Scholar
  64. 64.
    Iwata T, Schultz D, Hicks J, Hubbard GK, Mutton LN, Lotan TL, et al. MYC overexpression induces prostatic intraepithelial neoplasia and loss of Nkx3.1 in mouse luminal epithelial cells. PLoS One. 2010;5(2):e9427.CrossRefPubMedPubMedCentralGoogle Scholar
  65. 65.
    Mimeault M, Batra SK. Animal models relevant to human prostate carcinogenesis underlining the critical implication of prostatic stem/progenitor cells. Biochim Biophys Acta. 2011;1816(1):25–37.PubMedPubMedCentralGoogle Scholar
  66. 66.
    Barbieri CE, Rubin MA. Molecular characterization of prostate cancer following androgen deprivation: the devil in the details. Eur Urol. 2014;66(1):40–1.CrossRefPubMedGoogle Scholar
  67. 67.
    Cancer Genome Atlas Research Network. The molecular taxonomy of primary prostate cancer. Cell. 2015;163(4):1011–25.CrossRefGoogle Scholar
  68. 68.
    Mou HW, Kennedy Z, Anderson DG, Yin H, Xue W. Precision cancer mouse models through genome editing with CRISPR-Cas9. Genome Med. 2015;7:53.CrossRefPubMedPubMedCentralGoogle Scholar
  69. 69.
    Saunders TL. Inducible transgenic mouse models. Methods Mol Biol. 2011;693:103–15.CrossRefPubMedGoogle Scholar
  70. 70.
    Friedel RH, Wurst W, Wefers B, Kuhn R. Generating conditional knockout mice. Methods Mol Biol. 2011;693:205–31.CrossRefPubMedGoogle Scholar
  71. 71.
    Roebroek AJ, Gordts PL, Reekmans S. Knock-in approaches. Methods Mol Biol. 2011;693:257–75.CrossRefPubMedGoogle Scholar
  72. 72.
    Kasper S. Survey of genetically engineered mouse models for prostate cancer: analyzing the molecular basis of prostate cancer development, progression, and metastasis. J Cell Biochem. 2005;94(2):279–97.CrossRefPubMedGoogle Scholar
  73. 73.
    Coleman RE. Clinical features of metastatic bone disease and risk of skeletal morbidity. Clin Cancer Res. 2006;12(20 Pt 2):6243s–9s.CrossRefPubMedGoogle Scholar
  74. 74.
    Mehra R, Kumar-Sinha C, Shankar S, Lonigro RJ, Jing X, Philips NE, et al. Characterization of bone metastases from rapid autopsies of prostate cancer patients. Clin Cancer Res. 2011;17(12):3924–32.CrossRefPubMedPubMedCentralGoogle Scholar
  75. 75.
    Simmons JK, Hildreth BE 3rd, Supsavhad W, Elshafae SM, Hassan BB, Dirksen WP, et al. Animal models of bone metastasis. Vet Pathol. 2015;52(5):827–41.CrossRefPubMedPubMedCentralGoogle Scholar
  76. 76.
    LeRoy BE, Thudi NK, Nadella MV, Toribio RE, Tannehill-Gregg SH, van Bokhoven A, et al. New bone formation and osteolysis by a metastatic, highly invasive canine prostate carcinoma xenograft. Prostate. 2006;66(11):1213–22.CrossRefPubMedGoogle Scholar
  77. 77.
    Winter SF, Cooper AB, Greenberg NM. Models of metastatic prostate cancer: a transgenic perspective. Prostate Cancer Prostatic Dis. 2003;6(3):204–11.CrossRefPubMedGoogle Scholar
  78. 78.
    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(5):2177–82.PubMedGoogle Scholar
  79. 79.
    Bruxvoort KJ, Charbonneau HM, Giambernardi TA, Goolsby JC, Qian CN, Zylstra CR, et al. Inactivation of Apc in the mouse prostate causes prostate carcinoma. Cancer Res. 2007;67(6):2490–6.CrossRefPubMedGoogle Scholar
  80. 80.
    Poutahidis T, Rao VP, Olipitz W, Taylor CL, Jackson EA, Levkovich T, et al. CD4+ lymphocytes modulate prostate cancer progression in mice. Int J Cancer. 2009;125(4):868–78.CrossRefPubMedPubMedCentralGoogle Scholar
  81. 81.
    Valkenburg KC, Hostetter G, Williams BO. Concurrent Hepsin overexpression and adenomatous polyposis coli deletion causes invasive prostate carcinoma in mice. Prostate. 2015;75(14):1579–85.CrossRefPubMedGoogle Scholar
  82. 82.
    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(6):461–7.PubMedGoogle Scholar
  83. 83.
    Davis BW, Ostrander EA. Domestic dogs and cancer research: a breed-based genomics approach. ILAR J. 2014;55(1):59–68.CrossRefPubMedPubMedCentralGoogle Scholar
  84. 84.
    Leroy BE, Northrup N. Prostate cancer in dogs: comparative and clinical aspects. Vet J. 2009;180(2):149–62.CrossRefPubMedGoogle Scholar
  85. 85.
    Waters DJ, Bostwick DG. The canine prostate is a spontaneous model of intraepithelial neoplasia and prostate cancer progression. Anticancer Res. 1997;17(3A):1467–70.PubMedGoogle Scholar
  86. 86.
    Rosol TJ, Tannehill-Gregg SH, LeRoy BE, Mandl S, Contag CH. Animal models of bone metastasis. Cancer. 2003;97(3 Suppl):748–57.CrossRefPubMedGoogle Scholar
  87. 87.
    White RM. Cross-species oncogenomics using zebrafish models of cancer. Curr Opin Genet Dev. 2015;30:73–9.CrossRefPubMedPubMedCentralGoogle Scholar
  88. 88.
    Teng Y, Xie X, Walker S, White DT, Mumm JS, Cowell JK. Evaluating human cancer cell metastasis in zebrafish. BMC Cancer. 2013;13:453.CrossRefPubMedPubMedCentralGoogle Scholar
  89. 89.
    Bansal N, Davis S, Tereshchenko I, Budak-Alpdogan T, Zhong H, Stein MN, et al. Enrichment of human prostate cancer cells with tumor initiating properties in mouse and zebrafish xenografts by differential adhesion. Prostate. 2014;74(2):187–200.CrossRefPubMedGoogle Scholar
  90. 90.
    Shimizu N, Kawakami K, Ishitani T. Visualization and exploration of Tcf/Lef function using a highly responsive Wnt/beta-catenin signaling-reporter transgenic zebrafish. Dev Biol. 2012;370(1):71–85.CrossRefPubMedGoogle Scholar
  91. 91.
    Valkenburg KC, Pienta KJ. Drug discovery in prostate cancer mouse models. Expert Opin Drug Discovery. 2015;10(9):1011–24.CrossRefGoogle Scholar
  92. 92.
    Wang Y, Xing J, Xu Y, Zhou N, Peng J, Xiong Z, et al. In silico ADME/T modelling for rational drug design. Q Rev Biophys. 2015;48(4):488–515.CrossRefPubMedGoogle Scholar

Copyright information

© Springer International Publishing Switzerland 2017

Authors and Affiliations

  • Waqas Azeem
    • 1
    • 2
  • Yaping Hua
    • 1
    • 2
  • Karl-Henning Kalland
    • 1
    • 2
  • Xisong Ke
    • 1
    • 2
  • Jan Roger Olsen
    • 1
    • 2
  • Anne Margrete Øyan
    • 1
    • 2
  • Yi Qu
    • 1
    • 2
  1. 1.Department of Clinical ScienceUniversity of BergenBergenNorway
  2. 2.Department of MicrobiologyHaukeland University HospitalBergenNorway

Personalised recommendations