The zebrafish xenograft platform: Evolution of a novel cancer model and preclinical screening tool

Advances in Experimental Medicine and Biology

Volumn 916, Issue , 2016, Pages 289-314

  Wertman, Jaime ^a   Veinotte, Chansey J ^b   Dellaire, Graham ^a   Berman, Jason N ^a,b  

^a DALHOUSIE UNIVERSITY   (Canada)

^b IWK HEALTH CENTRE   (Canada)

Author keywords

Cancer; Model organism; Xenograft; Xenotransplant; Zebrafish

Indexed keywords

DOXORUBICIN; VISNAGIN; ENHANCED GREEN FLUORESCENT PROTEIN; GREEN FLUORESCENT PROTEIN;

ANGIOGENESIS; CANCER CELL; CANCER INHIBITION; CANCER RESEARCH; CANCER SCREENING; CELL MIGRATION; CELL POPULATION; CELL PROLIFERATION; DONOR; FLUORESCENCE ACTIVATED CELL SORTING; HEMATOPOIETIC STEM CELL; HOST SELECTION; HUMAN; NONHUMAN; PRIORITY JOURNAL; TUMOR XENOGRAFT; XENOTRANSPLANTATION; ZEBRA FISH; ANIMAL; DISEASE MODEL; GENETICS; NEOPLASMS; PATHOLOGY; XENOGRAFT;

ANIMALS; DISEASE MODELS, ANIMAL; GREEN FLUORESCENT PROTEINS; HETEROGRAFTS; HUMANS; NEOPLASMS; ZEBRAFISH;

EID: 84979022118     PISSN: 00652598     EISSN: 22148019     Source Type: Book Series    
DOI: 10.1007/978-3-319-30654-4_13     Document Type: Chapter

References (80)

1. Sharpless NE, Depinho RA (2006) The mighty mouse: genetically engineered mouse models in cancer drug development. Nat Rev Drug Discov 5:741–754
2. Cariati M, Marlow R, Dontu G (2011) Cancer cell culture. Methods Mol Biol 731:471–482
3. Voskoglou-Nomikos T, Pater JL, Seymour L (2003) Clinical predictive value of the in vitro cell line, human xenograft, and mouse allograft preclinical cancer models. Clin Cancer Res 9:4227–4239
4. Howe K, Clark MD, Torroja CF, Torrance J, Berthelot C, Muffato M, Collins JE, Humphray S, McLaren K, Matthews L, McLaren S, Sealy I, Caccamo M, Churcher C, Scott C, Barrett JC, Koch R, Rauch G-J, White S, Chow W, Kilian B, Quintais LT, Guerra-Assunção JA, Zhou Y, Gu Y, Yen J, Vogel J-H, Eyre T, Redmond S, Banerjee R et al (2013) The zebrafish reference genome sequence and its relationship to the human genome. Nature 496:498–503
5. Agliano A, Martin-Padura I, Mancuso P, Marighetti P, Rabascio C, Pruneri G, Shultz LD, Bertolini F (2008) Human acute leukemia cells injected in NOD/LtSz-scid/IL-2R?? null mice generate a faster and more efficient disease compared to other NOD/scid-related strains. Int J Cancer 123(August):2222–2227
6. Shultz LD, Lyons BL, Burzenski LM, Gott B, Chen X, Chaleff S, Kotb M, Gillies SD, King M, Mangada J, Greiner DL, Handgretinger R (2005) Human lymphoid and myeloid cell development in NOD/LtSz-scid IL2R gamma null mice engrafted with mobilized human hemopoietic stem cells. J Immunol 174:6477–6489
7. Konantz M, Balci TB, Hartwig UF, Dellaire G, André MC, Berman JN, Lengerke C (2012) Zebrafish xenografts as a tool for in vivo studies on human cancer. Ann N Y Acad Sci 1266:124–137
8. Berman JN, Chiu PPL, Dellaire G (2014) Preclinical animal models for cancer genomics. In Dellaire G, Berman J, Arceci R (eds) Cancer genomics from bench to bedside, 1st edn. Elsevier, pp 109–131
9. Rathinam C, Poueymirou WT, Rojas J, Murphy AJ, Valenzuela DM, Yancopoulos GD, Rongvaux A, Eynon EE, Manz MG, Flavell RA (2011) Efficient differentiation and function of human macrophages in humanized CSF-1 mice. Blood 118:3119–3128
10. Wunderlich M, Chou F-S, Link KA, Mizukawa B, Perry RL, Carroll M, Mulloy JC (2010) AML xenograft efficiency is significantly improved in NOD/SCID-IL2RG mice constitutively expressing human SCF, GM-CSF and IL-3. Leukemia 24:1785–1788
11. Kuperwasser C, Chavarria T, Wu M, Magrane G, Gray JW, Carey L, Richardson A, Weinberg RA (2004) Reconstruction of functionally normal and malignant human breast tissues in mice. Proc Natl Acad Sci U S A 101:4966–4971
12. Johnson JI, Decker S, Zaharevitz D, Rubinstein LV, Venditti JM, Schepartz S, Kalyandrug S, Christian M (2001) Relationships between drug activity in NCI preclinical in vitro and in vivo models and early clinical trials. Br J Cancer 84:1424–1431
13. White R, Rose K, Zon L (2013) Zebrafish cancer: the state of the art and the path forward. Nat Rev Cancer 13:624–636
14. Lieschke GJ, Currie PD (2007) Animal models of human disease: zebrafish swim into view. Nat Rev Genet 8:353–367
15. Stern HM, Zon LI (2003) Cancer genetics and drug discovery in the zebrafish. Nat Rev Cancer 3:533–539
16. Streisinger G, Walker C, Dower N, Knauber D, Singer F (1981) Production of clones of homozygous diploid zebra fish (Brachydanio rerio). Nature 291:293–296
17. Pliss GB, Zabezhinski MA, Petrov AS, Khudoley VV (1982) Peculiarities of N-nitramines carcinogenic action. Arch Geschwulstforsch 52:629–634
18. Long HK, Sims D, Heger A, Blackledge NP, Kutter C, Wright ML, Grützner F, Odom DT, Patient R, Ponting CP, Klose RJ (2013) Epigenetic conservation at gene regulatory elements revealed by non-methylated DNA profiling in seven vertebrates. Elife 2013:1–19
19. Spitsbergen J, Kent M (2003) The state of the art of the zebrafish model for toxicology and toxicologic pathology research – advantages and current limitations. Toxicol Pathol 31:62–87
20. Beckwith LG, Moore JL, Tsao-Wu GS, Harshbarger JC, Cheng KC (2000) Ethylnitrosourea induces neoplasia in zebrafish (Danio rerio). Lab Invest 80:379–385
21. Lam S, Chua H, Gong Z, Lam T, Sin Y (2004) Development and maturation of the immune system in zebrafish, Danio rerio: a gene expression profiling, in situ hybridization and immunological study. Dev Comp Immunol 28:9–28
22. Lee LMJ, Seftor EA, Bonde G, Cornell RA, Hendrix MJC (2005) The fate of human malignant melanoma cells transplanted into zebrafish embryos: assessment of migration and cell division in the absence of tumor formation. Dev Dyn 233:1560–1570
23. Hendrix MJC, Seftor EA, Hess AR, Seftor REB (2003) Vasculogenic mimicry and tumour- cell plasticity: lessons from melanoma. Nat Rev Cancer 3:411–421
24. Mintz B, Illmensee K (1975) Normal genetically mosaic mice produced from malignant teratocarcinoma cells. Proc Natl Acad Sci U S A 72:3585–3589
25. Haldi M, Ton C, Seng WL, McGrath P (2006) Human melanoma cells transplanted into zebrafish proliferate, migrate, produce melanin, form masses and stimulate angiogenesis in zebrafish. Angiogenesis 9:139–151
26. Marques IJ, Weiss FU, Vlecken DH, Nitsche C, Bakkers J, Lagendijk AK, Partecke LI, Heidecke C-D, Lerch MM, Bagowski CP (2009) Metastatic behaviour of primary human tumours in a zebrafish xenotransplantation model. BMC Cancer 9:128
27. Herpers R, Van De Kamp E, Duckers HJ, Schulte-Merker S (2008) Redundant roles for sox7 and sox18 in arteriovenous specification in Zebrafish. Circ Res 102:12–15
28. Lawson ND, Weinstein BM (2002) In vivo imaging of embryonic vascular development using transgenic zebrafish. Dev Biol 248:307–318
29. Stoletov K, Montel V, Lester RD, Gonias SL, Klemke R (2007) High-resolution imaging of the dynamic tumor cell vascular interface in transparent zebrafish. Proc Natl Acad Sci U S A 104:17406–17411
30. Corkery DP, Dellaire G, Berman JN (2011) Leukaemia xenotransplantation in zebrafish—chemotherapy response assay in vivo. Br J Haematol 153:786–789
31. Nicoli S, Presta M (2007) The zebrafish/tumor xenograft angiogenesis assay. Nat Protoc 2:2918–2923
32. Nicoli S, Ribatti D, Cotelli F, Presta M (2007) Mammalian tumor xenografts induce neovascularization in zebrafish embryos. Cancer Res 67:2927–2931
33. Zhao H, Tang C, Cui K, Ang B-T, Wong STC (2009) A screening platform for glioma growth and invasion using bioluminescence imaging. Laboratory investigation. J Neurosurg 111:238–246
34. Topczewska JM, Postovit L-M, Margaryan NV, Sam A, Hess AR, Wheaton WW, Nickoloff BJ, Topczewski J, Hendrix MJC (2006) Embryonic and tumorigenic pathways converge via Nodal signaling: role in melanoma aggressiveness. Nat Med 12:925–932
35. Bentley VL, Veinotte CJ, Corkery DP, Pinder JB, LeBlanc MA, Bedard K, Weng AP, Berman JN, Dellaire G (2015) Focused chemical genomics using zebrafish xenotransplantation as a pre-clinical therapeutic platform for T-cell acute lymphoblastic leukemia. Haematologica 100:70–76
36. Rawls JF, Mellgren EM, Johnson SL (2001) How the zebrafish gets its stripes. Dev Biol 240:301–314
37. Lister JA, Robertson CP, Lepage T, Johnson SL, Raible DW (1999) Nacre encodes a zebrafish microphthalmia-related protein that regulates neural-crest-derived pigment cell fate. Development 126:3757–3767
38. White RM, Sessa A, Burke C, Bowman T, LeBlanc J, Ceol C, Bourque C, Dovey M, Goessling W, Burns CE, Zon LI (2008) Transparent adult zebrafish as a tool for in vivo transplantation analysis. Cell Stem Cell 2:183–189
39. Veinotte CJ, Dellaire G, Berman JN (2014) Hooking the big one: the potential of zebrafish xenotransplantation to reform cancer drug screening in the genomic era. Dis Model Mech 7:745–754
40. Taylor AM, Zon LI (2009) Zebrafish tumor assays: the state of transplantation. Zebrafish 6:339–346
41. Tobia C, De Sena G, Presta M (2011) Zebrafish embryo, a tool to study tumor angiogenesis. Int J Dev Biol 55:505–509
42. Cheng J, Yan-Juan G, Wang Y, Cheng SH, Wong W-T (2011) Nanotherapeutics in angiogenesis: synthesis and in vivo assessment of drug efficacy and biocompatibility in zebrafish embryos. Int J Nanomedicine 6:2007–2021
43. Vlecken DH, Bagowski CP (2009) LIMK1 and LIMK2 are important for metastatic behavior and tumor cell-induced angiogenesis of pancreatic cancer cells. Zebrafish 6:433–439
44. Camus S, Quevedo C, Menéndez S, Paramonov I, Stouten PFW, Janssen RA, Rueb S, He S, Snaar-Jagalska BE, Laricchia-Robbio L, Izpisua Belmonte JC (2012) Identification of phosphorylase kinase as a novel therapeutic target through high-throughput screening for antiangiogenesis compounds in zebrafish. Oncogene 31:4333–4342
45. De Visser KE, Eichten A, Coussens LM (2006) Paradoxical roles of the immune system during cancer development. Nat Rev Cancer 6:24–37
46. Renshaw SA, Loynes CA, Trushell DMI, Elworthy S, Ingham PW, Whyte MKB (2006) A transgenic zebrafish model of neutrophilic inflammation. Blood 108:3976–3978
47. Ellett F, Pase L, Hayman JW, Andrianopoulos A, Lieschke GJ (2011) Mpeg1 promoter transgenes direct macrophage-lineage expression in zebrafish. Blood 117:49–56
48. Lin H-F, Traver D, Zhu H, Dooley K, Paw BH, Zon LI, Handin RI (2005) Analysis of thrombocyte development in CD41-GFP transgenic zebrafish. Blood 106:3803–3810
49. He S, Lamers GE, Beenakker J-WM, Cui C, Ghotra VP, Danen EH, Meijer AH, Spaink HP, Snaar-Jagalska BE (2012) Neutrophil-mediated experimental metastasis is enhanced by VEGFR inhibition in a zebrafish xenograft model. J Pathol 227:431–445
50. Auer TO, Del Bene F (2014) CRISPR/Cas9 and TALEN-mediated knock-in approaches in zebrafish. Methods 69:142–150
51. Prykhozhij S, Rajan V, Gaston D, Berman JN (2015) CRISPR MultiTargeter: a web tool to find common and unique CRISPR single guide RNA targets in a set of similar sequences. PLoS One 10, e0119372
52. Willinger T, Rongvaux A, Strowig T, Manz MG, Flavell RA (2011) Improving human hematolymphoid- system mice by cytokine knock-in gene replacement. Trends Immunol 32:321–327
53. Jung D-W, Oh E-S, Park S-H, Chang Y-T, Kim C-H, Choi S-Y, Williams DR (2012) A novel zebrafish human tumor xenograft model validated for anti-cancer drug screening. Mol Biosyst 8:1930–1939
54. Pruvot B, Jacquel A, Droin N, Auberger P, Bouscary D, Tamburini J, Muller M, Fontenay M, Chluba J, Solary E (2011) Leukemic cell xenograft in zebrafish embryo for investigating drug efficacy. Haematologica 96:612–616
55. El-Naggar A, Veinotte C, Tognon C, Corkery D, Cheng H, Tirode F, Grunewald T, Kyle A, Baker J, Mathers J, Somasekharad S, LePard N, McKinney S, Bennewith K, Minchinton A, Delattre O, Wang Y, Dellaire G, Berman J, Sorensen P (2015) Translational activation of HIF1a by YB-1 promotes sarcoma metastasis. Cancer Cell 27:682–697
56. Lara R, Mauri FA, Taylor H, Derua R, Shia A, Gray C, Nicols A, Shiner RJ, Schofield E, Bates PA, Waelkens E, Dallman M, Lamb J, Zicha D, Downward J, Seckl MJ, Pardo OE (2011) An siRNA screen identifies RSK1 as a key modulator of lung cancer metastasis. Oncogene 30:3513–3521
57. Vlecken DH, Bagowski CP (2009) LIMK1 and LIMK2 are important for metastatic behavior of pancreatic. Cancer Cells 6
58. Veinotte CJ, Corkery D, Dellaire G, El-Naggar A, Sinclair K, Bernstein ML, Sorensen PB, Berman JN (2012) Using zebrafish xenotransplantation to study the role of Y-Box binding protein (YB-1) in the metastasis of Ewing family tumors. In Proceedings of the 103rd Annual Meeting of the American Association for Cancer Research, 2012, Abstract no 1398
59. Greaves M, Maley CC (2012) Clonal evolution in cancer. Nature 481:306–313
60. Geiger GA, Fu W, Kao GD (2008) Temozolomide-mediated radiosensitization of human glioma cells in a zebrafish embryonic system. Cancer Res 68:3396–3404
61. Dellaire G, Bazett-Jones DP (2004) PML nuclear bodies: dynamic sensors of DNA damage and cellular stress. Bioessays 26:963–977
62. Corkery D, Cann K, Dellaire G (2011) Nuclear subdomains. In Nabi I (ed) Cell domains. Wiley, pp 393–414
63. Traver D, Paw BH, Poss KD, Penberthy WT, Lin S, Zon LI (2003) Transplantation and in vivo imaging of multilineage engraftment in zebrafish bloodless mutants. Nat Immunol 4:1238–1246
64. Tang Q, Abdelfattah NS, Blackburn JS, Moore JC, Martinez SA, Moore FE, Lobbardi R, Tenente IM, Ignatius MS, Berman JN, Liwski RS, Houvras Y, Langenau DM (2014) Optimized cell transplantation using adult rag2 mutant zebrafish. Nat Methods 11:6–11
65. Mizgireuv IV, Revskoy SY (2006) Transplantable tumor lines generated in clonal zebrafish. Cancer Res 66:3120–3125
66. Peterson RT, Link BA, Dowling JE, Schreiber SL (2000) Small molecule developmental screens reveal the logic and timing of vertebrate development. Proc Natl Acad Sci U S A 97:12965–12969
67. Murphey RD, Stern HM, Straub CT, Zon LI (2006) A chemical genetic screen for cell cycle inhibitors in zebrafish embryos. Chem Biol Drug Des 68:213–219
68. Zon LI, Peterson RT (2005) In vivo drug discovery in the zebrafish. Nat Rev Drug Discov 4:35–44
69. Liu Y, Asnani A, Zou L, Bentley VL, Yu M, Wang Y, Dellaire G, Sarkar KS, Dai M, Chen HH, Sosnovik DE, Shin JT, Haber DA, Berman JN, Chao E, Peterson RT (2014) Visnagin protects against doxorubicin-induced cardiomyopathy through inhibition of mitochondrial malate dehydrogenase. Sci Transl Med 6:266ra170
70. Jemal A, Bray F, Ferlay J (2011) Global cancer Statistics. CA Cancer J Clin 61:69–90
71. Weiss FU, Marques IJ, Woltering JM, Vlecken DH, Aghdassi A, Partecke LI, Heidecke C-D, Lerch MM, Bagowski CP (2009) Retinoic acid receptor antagonists inhibit miR-10a expression and block metastatic behavior of pancreatic cancer. Gastroenterology 137:2136–2145.e1–7
72. Harfouche R, Basu S, Soni S, Hentschel DM, Mashelkar RA, Sengupta S (2009) Nanoparticlemediated targeting of phosphatidylinositol-3-kinase signaling inhibits angiogenesis. Angiogenesis 12:325–338
73. Lally BE, Geiger GA, Kridel S, Arcury-Quandt AE, Robbins ME, Kock ND, Wheeler K, Peddi P, Georgakilas A, Kao GD, Koumenis C (2007) Identification and biological evaluation of a novel and potent small molecule radiation sensitizer via an unbiased screen of a chemical library. Cancer Res 67:8791–8799
74. LatifiA, Abubaker K, Castrechini N, Ward AC, Liongue C, Dobill F, Kumar J, Thompson EW, Quinn MA, Findlay JK, Ahmed N (2011) Cisplatin treatment of primary and metastatic epithelial ovarian carcinomas generates residual cells with mesenchymal stem cell-like profile. J Cell Biochem 112:2850–2864
75. Zhao C, Wang X, Zhao Y, Li Z, Lin S, Wei Y, Yang H (2011) A novel xenograft model in zebrafish for high-resolution investigating dynamics of neovascularization in tumors. PLoS One 6:1–9
76. Ghotra VPS, He S, de Bont H, van der Ent W, Spaink HP, van de Water B, Snaar-Jagalska BE, Danen EHJ (2012) Automated whole animal bio-imaging assay for human cancer dissemination. PLoS One 7
77. Yang X-J, Cui W, Gu A, Xu C, Yu S-C, Li T-T, Cui Y-H, Zhang X, Bian X-W (2013) A novel zebrafish xenotransplantation model for study of glioma stem cell invasion. PLoS One 8, e61801
78. Drabsch Y, He S, Zhang L, Snaar-Jagalska BE, Ten Dijke P (2013) Transforming growth factor-β signalling controls human breast cancer metastasis in a zebrafish xenograft model. Breast Cancer Res 15:R106
79. Teng Y, Xie X, Walker S, White DT, Mumm JS, Cowell JK (2013) Evaluating human cancer cell metastasis in zebrafish. BMC Cancer 13:453
80. Van der Ent W, Burrello C, Teunisse AF, Ksander BR, van der Velden PA, Jager MJ, Jochemsen AG, Snaar-Jagalska BE (2014) Modeling of human uveal melanoma in zebrafish xenograft embryos. Invest Ophthalmol Vis Sci 55:6612–6622