The Promise of Zebrafish as a Chemical Screening Tool in Cancer Therapy

References

• Siegel R , MaJ, ZouZet al. Cancer statistics, 2014. CA Cancer J. Clin.64, 9–29 (2014).
   PubMed Web of Science ®Google Scholar
• Teng Y , XieX, WalkerSet al. Knockdown of zebrafish Lgi1a results in abnormal development, brain defects and a seizure-like behavioral phenotype. Hum. Mol. Genet.19, 4409–4420 (2010).
   PubMed Web of Science ®Google Scholar
• Teng Y , XieX, WalkerSet al. Loss of zebrafish lgi1b leads to hydrocephalus and sensitization to pentylenetetrazol induced seizure-like behavior. PLoS ONE6, e24596 (2011).
   PubMed Web of Science ®Google Scholar
• Xie X , MathiasJR, SmithMAet al. Silencer-delimited transgenesis: NRSE/RE1 sequences promote neural-specific transgene expression in a NRSF/REST-dependent manner. BMC Biol.10, 93 (2012).
   PubMed Web of Science ®Google Scholar
• Veinotte C , DellaireG, BermanJ. Hooking the big one: the potential of zebrafish xenotransplantation to reform cancer drug screening in the genomic era. Dis. Model Mech.7, 745–754 (2014).
   PubMed Web of Science ®Google Scholar
• Langenau DM , KeefeMD, StorerNYet al. Effects of RAS on the genesis of embryonal rhabdomyosarcoma. Genes Dev.21, 1382–1395 (2007).
   PubMed Web of Science ®Google Scholar
• Shimada Y , NishimuraY, TanakaT. Zebrafish-based systems pharmacology of cancer metastasis. Methods Mol. Biol.1165, 223–238 (2014).
   PubMedGoogle Scholar
• Berghmans S , JetteC, LangenauDet al. Making waves in cancer research: new models in the zebrafish. Biotechniques39, 227–237 (2005).
   PubMed Web of Science ®Google Scholar
• Goessling W , NorthTE, ZonLI. New waves of discovery: modeling cancer in zebrafish. J. Clin. Oncol.25, 2473–2479 (2007).
   PubMed Web of Science ®Google Scholar
• Kari G , RodeckU, DickerAP. Zebrafish: an emerging model system for human disease and drug discovery. Clin. Pharmacol. Ther.82, 70–80 (2007).
   PubMed Web of Science ®Google Scholar
• Mizgireuv IV , MajorovaIG, GorodinskayaVMet al. Carcinogenic effect of N-nitrosodimethylamine on diploid and triploid zebrafish (Danio rerio). Toxicol. Pathol.32, 514–518 (2004).
   PubMed Web of Science ®Google Scholar
• Mizgireuv IV , RevskoySY. Transplantable tumor lines generated in clonal zebrafish. Cancer Res.66, 3120–3125 (2006).
   PubMed Web of Science ®Google Scholar
• Spitsbergen JM , TsaiHW, ReddyAet al. Neoplasia in zebrafish (Danio rerio) treated with 7,12-dimethylbenz[a]anthracene by two exposure routes at different developmental stages. Toxicol. Pathol.28, 705–715 (2000).
   PubMed Web of Science ®Google Scholar
• Spitsbergen JM , TsaiHW, ReddyAet al. Neoplasia in zebrafish (Danio rerio) treated with N-methyl-N’-nitro-N-nitrosoguanidine by three exposure routes at different developmental stages. Toxicol. Pathol.28, 716–725 (2000).
   PubMed Web of Science ®Google Scholar
• Haramis AP , HurlstoneA, van der VeldenYet al. Adenomatous polyposis coli-deficient zebrafish are susceptible to digestive tract neoplasia. EMBO Rep.7, 444–449 (2006).
   PubMed Web of Science ®Google Scholar
• Shepard JL , AmatrudaJF, FinkelsteinDet al. A mutation in separase causes genome instability and increased susceptibility to epithelial cancer. Genes Dev.21, 55–59 (2007).
   PubMed Web of Science ®Google Scholar
• Teng Y , XieX, WalkerSet al. Evaluating human cancer cell metastasis in zebrafish. BMC Cancer13, 453 (2013).
   PubMed Web of Science ®Google Scholar
• Konantz M , BalciTB, HartwigUFet al. Zebrafish xenografts as a tool for in vivo studies on human cancer. Ann. NY Acad. Sci.1266, 124–137 (2012).
   PubMed Web of Science ®Google Scholar
• Bentley VL , VeinotteCJ, CorkeryDPet al. Focused chemical genomics using zebrafish xenotransplantation as a pre-clinical therapeutic platform for T-cell acute lymphoblastic leukemia. Haematologica100, 70–76 (2015).
   PubMed Web of Science ®Google Scholar
• Haldi M , TonC, SengWLet al. Human melanoma cells transplanted into zebrafish proliferate, migrate, produce melanin, form masses and stimulate angiogenesis in zebrafish. Angiogenesis9, 139–151 (2005).
   Google Scholar
• Lee LM , SeftorEA, BondeGet al. 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 (2005).
   PubMed Web of Science ®Google Scholar
• Topczewska JM , PostovitLM, MargaryanNVet al. Embryonic and tumorigenic pathways converge via Nodal signaling: role in melanoma aggressiveness. Nat. Med.12, 925–932 (2006).
   PubMed Web of Science ®Google Scholar
• Nicoli S , RibattiD, CotelliFet al. Mammalian tumor xeno-grafts induce neovascularization in zebrafish embryos. Cancer Res.67, 2927–2931 (2007).
   PubMed Web of Science ®Google Scholar
• Stoletov K , MontelV, LesterRDet al. High-resolution imaging of the dynamic tumor cell vascular interface in transparent zebrafish. Proc. Natl Acad. Sci. USA104, 17406–17411 (2007).
   PubMed Web of Science ®Google Scholar
• Mione M , TredeN. The zebrafish as a model for cancer. Dis. Model Mech.3, 517–523 (2010).
   PubMed Web of Science ®Google Scholar
• Shao J , TengY, PadiaRet al. COP1 and GSK3β cooperate to promote c-Jun degradation and inhibit breast cancer cell tumorigenesis. Neoplasia15, 1075–1085 (2013).
   PubMed Web of Science ®Google Scholar
• Hong S , NohH, TengYet al. SHOX2 is a direct miR-375 target and a novel epithelial-to-mesenchymal transition inducer in breast cancer cells. Neoplasia16, 279–290 (2014).
   PubMed Web of Science ®Google Scholar
• Teng Y , RenM, CheneyRet al. Inactivation of the WASF3 gene in prostate cancer cells leads to suppression of tumorigenicity and metastases. Br. J. Cancer103, 1066–1075 (2010).
   PubMed Web of Science ®Google Scholar
• Teng Y , LiuM, CowellJK. Functional interrelationship between the WASF3 and KISS1 metastasis-associated genes in breast cancer cells. Int. J. Cancer129, 2825–2835 (2011).
   PubMed Web of Science ®Google Scholar
• Barriuso J , NagarajuR, HurlstoneA. Zebrafish: a new companion for translational research in oncology. Clin. Cancer Res.21, 969–975 (2015).
   PubMed Web of Science ®Google Scholar
• Langenau DM , TraverD, FerrandoAAet al. Myc-induced T-cell leukemia in transgenic zebrafish. Science299, 887–890 (2003).
   PubMed Web of Science ®Google Scholar
• White R , RoseK, ZonL. Zebrafish cancer: the state of the art and the path forward. Nat. Rev. Cancer13, 624–636 (2013).
   PubMed Web of Science ®Google Scholar
• Tat J , LiuM, WenXY. Zebrafish cancer and metastasis models for in vivo drug discovery. Drug Discov. Today Technol.10, e83–e89 (2012).
   Google Scholar
• Mathias JR , SaxenaMT, MummJS. Advances in zebrafish chemical screening technologies. Future Med. Chem.4, 1811–1822 (2012).
   PubMed Web of Science ®Google Scholar
• Funfak A , BrösingA, BrandMet al. Micro fluid segment technique for screening and development studies on Danio rerio embryos. Lab Chip7, 1132–1138 (2007).
   PubMed Web of Science ®Google Scholar
• Zhang B , ShimadaY, KuroyanagiJet al. Quantitative phenotyping-based in vivo chemical screening in a zebrafish model of leukemia stem cell xenotransplantation. PLoS ONE9, e85439 (2014).
   PubMed Web of Science ®Google Scholar
• Gallardo VE , VarshneyGK, LeeMet al. Phenotype-driven chemical screening in zebrafish for collective cell migration inhibitors identifies multiple potential pathways for targeting metastasis. Dis. Model. Mech.8 (6), 565–576 (2015).
   PubMedGoogle Scholar
• Spaink HP , CuiC, WiwegerMIet al. Robotic injection of zebrafish embryos for high-throughput screening in disease models. Methods62, 246–254 (2013).
   PubMed Web of Science ®Google Scholar
• Schindelin J , Arganda-CarrerasI, FriseEet al. Fiji: an open-source platform for biological-image analysis. Nat. Methods9, 676–682 (2012).
   PubMed Web of Science ®Google Scholar
• Annila T , LihavainenE, MarquesIJet al. ZebIAT, an image analysis tool for registering zebrafish embryos and quantifying cancer metastasis. BMC Bioinformatics14 (Suppl.), S5 (2013).
   PubMedGoogle Scholar
• Li Y , HuangW, HuangSet al. Screening of anti-cancer agent using zebrafish: comparison with the MTT assay. Biochem. Biophys. Res. Commun.422, 85–90 (2012).
   PubMed Web of Science ®Google Scholar
• Parng C , SengWL, SeminoCet al. Zebrafish: a preclinical model for drug screening. Assay Drug Dev. Technol.1, 41–48 (2002).
   PubMed Web of Science ®Google Scholar
• van der Ent W , BurrelloC, TeunisseAFet al. Modeling of human uveal melanoma in zebrafish xenograft embryos. Invest. Ophthalmol. Vis. Sci.55, 6612–6622 (2014).
   PubMed Web of Science ®Google Scholar
• White RM , CechJ, RatanasirintrawootSet al. DHODH modulates transcriptional elongation in the neural crest and melanoma. Nature471, 518–522 (2011).
   PubMed Web of Science ®Google Scholar
• Taylor K , GrantN, TemperleyNet al. Small molecule screening in zebrafish: an in vivo approach to identifying new chemical tools and drug leads. Cell Commun. Signal8, 11 (2010).
   PubMed Web of Science ®Google Scholar
• Anastasaki C , EstepAL, MaraisRet al. Kinase-activating and kinase-impaired cardio-facio-cutaneous syndrome alleles have activity during zebrafish development and are sensitive to small molecule inhibitors. Hum. Mol. Genet.18, 2543–2554 (2009).
   PubMed Web of Science ®Google Scholar
• Chimote G , SreenivasanJ, PawarNet al. Comparison of effects of anti-angiogenic agents in the zebrafish efficacy-toxicity model for translational anti-angiogenic drug discovery. Drug Des. Devel. Ther.19, 1107–1123 (2014).
   Google Scholar
• Xia Y , SongX, LiDet al. YLT192, a novel, orally active bioavailable inhibitor of VEGFR2 signaling with potent antiangiogenic activity and antitumor efficacy in preclinical models. Sci. Rep.4, 6031 (2014).
   PubMed Web of Science ®Google Scholar
• Zhong L , FuXY, ZouCet al. A preclinical evaluation of a novel multikinase inhibitor, SKLB-329, as a therapeutic agent against hepatocellular carcinoma. Int. J. Cancer135, 2972–2983 (2014).
   PubMed Web of Science ®Google Scholar
• Patton EE , WidlundHR, KutokJLet al. BRAF mutations are sufficient to promote nevi formation and cooperate with p53 in the genesis of melanoma. Curr. Biol.15, 249–254 (2005).
   PubMed Web of Science ®Google Scholar
• Dovey M , WhiteRM, ZonLI. Oncogenic NRAS cooperates with p53 loss to generate melanoma in zebrafish. Zebrafish6, 397–404 (2009).
   PubMed Web of Science ®Google Scholar
• Santoriello C , GennaroE, AnelliVet al. Kita driven expression of oncogenic HRAS leads to early onset and highly penetrant melanoma in zebrafish. PLoS ONE5, e15170 (2010).
   PubMed Web of Science ®Google Scholar
• Nguyen AT , EmelyanovA, KohCHet al. An inducible krasV12 transgenic zebrafish model for liver tumorigenesis and chemical drug screening. Dis. Model Mech.5, 63–72 (2012).
   PubMed Web of Science ®Google Scholar
• Li Z , HuangX, ZhanHet al. Inducible and repressable oncogene addicted hepatocellular carcinoma in Tet-on xmrk transgenic zebrafish. J. Hepatol.56, 419–425 (2012).
   PubMed Web of Science ®Google Scholar
• Liu S , LeachSD. Screening pancreatic oncogenes in zebrafish using the Gal4/UAS system. Methods Cell Biol.105, 367–381 (2011).
   PubMed Web of Science ®Google Scholar
• Park SW , DavisonJM, RheeJet al. Oncogenic KRAS induces progenitor cell expansion and malignant transformation in zebrafish exocrine pancreas. Gastroenterology134, 2080–2090 (2008).
   PubMed Web of Science ®Google Scholar
• Yang HW , KutokJL, LeeNHet al. Targeted expression of human MYCN selectively causes pancreatic neuroendocrine tumors in transgenic zebrafish. Cancer Res.64, 7256–7262 (2004).
   PubMed Web of Science ®Google Scholar
• Feng H , LangenauDM, MadgeJAet al. Heat-shock induction of T-cell lymphoma/leukaemia in conditional Cre/lox-regulated transgenic zebrafish. Br. J. Haematol.138, 169–175 (2007).
   PubMed Web of Science ®Google Scholar
• Feng H , StachuraDL, WhiteRMet al. T-lymphoblastic lymphoma cells express high levels of BCL2, S1P1, and ICAM1, leading to a blockade of tumor cell intravasation. Cancer Cell18, 353–366 (2010).
   PubMed Web of Science ®Google Scholar
• Langenau DM , FengH, BerghmansSet al. Cre/lox-regulated transgenic zebrafish model with conditional myc-induced T cell acute lymphoblastic leukemia. Proc. Natl Acad. Sci. USA102, 6068–6073 (2005).
   PubMed Web of Science ®Google Scholar
• Chen J , JetteC, KankiJPet al. NOTCH1-induced T-cell leukemia in transgenic zebrafish. Leukemia21, 462–471 (2007).
   PubMed Web of Science ®Google Scholar
• Kalev-Zylinska ML , HorsfieldJA, FloresMVet al. Runx1 is required for zebrafish blood and vessel development and expression of a human RUNX1–2T1 transgene advances a model for studies of leukemogenesis. Development129, 2015–2030 (2002).
   PubMed Web of Science ®Google Scholar
• Sabaawy HE , AzumaM, EmbreeLJet al. TEL-AML1 transgenic zebrafish model of precursor B cell acute lymphoblastic leukemia. Proc. Natl Acad. Sci. USA103, 15166–15171 (2006).
   PubMed Web of Science ®Google Scholar
• Zhuravleva J , PaggettiJ, MartinLet al. MOZ/TIF2-induced acute myeloid leukaemia in transgenic fish. Br. J. Haematol.143, 378–382 (2008).
   PubMed Web of Science ®Google Scholar
• Forrester AM , GrabherC, McBrideERet al. NUP98-HOXA9-transgenic zebrafish develop a myeloproliferative neoplasm and provide new insight into mechanisms of myeloid leukaemogenesis. Br. J. Haematol.155, 167–181 (2011).
   PubMed Web of Science ®Google Scholar
• Zhu S , LeeJS, GuoFet al. Activated ALK collaborates with MYCN in neuroblastoma pathogenesis. Cancer Cell21, 362–373 (2012).
   PubMed Web of Science ®Google Scholar
• Berghmans S , MurpheyRD, WienholdsEet al. tp53 mutant zebrafish develop malignant peripheral nerve sheath tumors. Proc. Natl Acad. Sci. USA102, 407–412 (2005).
   PubMed Web of Science ®Google Scholar
• Liu NA , JiangH, Ben-ShlomoAet al. Targeting zebrafish and murine pituitary corticotroph tumors with a cyclin-dependent kinase (CDK) inhibitor. Proc. Natl Acad. Sci. USA108, 8414–8419 (2011).
   PubMed Web of Science ®Google Scholar
• Gill JA , LoweL, NguyenJet al. Enforced expression of Simian virus 40 large T-antigen leads to testicular germ cell tumors in zebrafish. Zebrafish7, 333–341 (2010).
   PubMed Web of Science ®Google Scholar
• Chu CY , ChenCF, RajendranRSet al. Overexpression of Akt1 enhances adipogenesis and leads to lipoma formation in zebrafish. PLoS ONE7, e36474 (2012).
   PubMed Web of Science ®Google Scholar
• Langenau DM , KeefeMD, StorerNYet al. Effects of RAS on the genesis of embryonal rhabdomyosarcoma. Genes Dev.21, 1382–1395 (2007).
   PubMed Web of Science ®Google Scholar
• Leacock SW , BasseAN, ChandlerGLet al. A zebrafish transgenic model of Ewing's sarcoma reveals conserved mediators of EWS-FLI1 tumorigenesis. Dis. Model. Mech.5, 95–106 (2012).
   PubMed Web of Science ®Google Scholar
• Le X , LangenauDM, KeefeMDet al. Heat shock-inducible Cre/Lox approaches to induce diverse types of tumors and hyperplasia in transgenic zebrafish. Proc. Natl Acad. Sci. USA104, 9410–9415 (2007).
   PubMed Web of Science ®Google Scholar
• Ju B , SpitsbergenJ, EdenCJet al. Co-activation of hedgehog and AKT pathways promote tumorigenesis in zebrafish. Mol. Cancer8, 40 (2009).
   PubMed Web of Science ®Google Scholar
• Onnebo SM , CondronMM, McPheeDOet al. Hematopoietic perturbation in zebrafish expressing a tel-jak2a fusion. Exp. Hematol.33, 182–188 (2005).
   PubMed Web of Science ®Google Scholar
• Ostrup O , ReinerA, AlestromPet al. The specific alteration of histone methylation profiles of DZNep during early zebrafish development. Biochim. Biophys. Acta1839, 1307–1315 (2014).
   PubMed Web of Science ®Google Scholar
• Li S , DangY, OiLamet al. VEGFR tyrosine kinase inhibitor II (VRI) induced vascular insufficiency in zebrafish as a model for studying vascular toxicity and vascular preservation. Toxicol. Appl. Pharmacol.280, 408–420 (2014).
   PubMed Web of Science ®Google Scholar
• Astin J , JamiesonS, EngTet al. An in vivo antilymphatic screen in zebrafish identifies novel inhibitors of mammalian lymphangiogenesis and lymphatic-mediated metastasis. Mol. Cancer Ther.13, 2450–2462 (2014).
   PubMed Web of Science ®Google Scholar
• Veinotte C , DellaireG, BermanJ. Hooking the big one: the potential of zebrafish xenotransplantation to reform cancer drug screening in the genomic era. Dis. Model. Mech.7, 745–754 (2014).
   PubMed Web of Science ®Google Scholar
• Liu J , LuoM, XiaMet al. Marine compound catunargein inhibits angiogenesis through the modulation of phosphorylation of akt and eNOS in vivo and in vitro. Mar. Drugs12, 2790–2801 (2014).
   PubMed Web of Science ®Google Scholar
• Liu G , LiuM, WeiJet al. CS5931, a novel polypeptide in Ciona savignyi, represses angiogenesis via inhibiting vascular endothelial growth factor (VEGF) and matrix metalloproteinases (MMPs). Mar. Drugs12, 1530–1544 (2014).
   PubMed Web of Science ®Google Scholar
• Yang J , HuJ, WanLet al. Barbigerone inhibits tumor angiogenesis, growth and metastasis in melanoma. Asian Pac. J. Cancer Prev.15, 167–174 (2014).
   PubMedGoogle Scholar