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Modeling of Solid-Tumor Microenvironment in Zebrafish (Danio Rerio) Larvae

  • Yuxiao Yao
  • Lei Wang
  • Xu WangEmail author
Chapter
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 1219)

Abstract

The zebrafish larvae have emerged as a powerful model for studying tumorigenesis in vivo, with remarkable conservation with mammals in genetics, molecular and cell biology. Zebrafish tumor models bear the significant advantages of optical clarity in comparison to that in the mammalian models, allowing noninvasive investigation of the tumor cell and its microenvironment at single-cell resolution. Here we review recent progressions in the field of zebrafish models of solid tumor diseases in two main categories: the genetically engineered tumor models in which all cells in the tumor microenvironment are zebrafish cells, and xenograft tumor models in which the tumor microenvironment is composed of zebrafish cells and cells from other species. Notably, the zebrafish patient-derived xenograft (zPDX) models can be used for personalized drug assessment on primary tumor biopsies, including the pancreatic cancer. For the future studies, a series of high throughput drug screenings on the library of transgenic zebrafish models of solid tumor are expected to provide systematic database of oncogenic mutation, cell-of-origin, and leading compounds; and the humanization of zebrafish in genetics and cellular composition will make it more practical hosts for zPDX modeling. Together, zebrafish tumor model systems are unique and convenient in vivo platforms, with great potential to serve as valuable tools for cancer researches.

Keywords

Tumor microenvironment Animal model Zebrafish Transgenesis Xenograft Chimeric antigen receptor (CAR) T-cells 

Notes

Financial Support

  • National Natural Science Foundation of China 81402582 and 81802333.

  • Natural Science Foundation of Shanghai 14YF1400600 and 18ZR1404500.

  • Natural Science Foundation of Guangdong Province 2018A030310053.

References

  1. Allen-Rhoades W, Whittle SB, Rainusso N (2018) Pediatric solid tumors of infancy: an overview. Pediatr Rev 39(2):57–67.  https://doi.org/10.1542/pir.2017-0057CrossRefPubMedGoogle Scholar
  2. Avci ME, Keskus AG, Targen S, Isilak ME, Ozturk M, Atalay RC, Adams MM, Konu O (2018) Development of a novel zebrafish xenograft model in ache mutants using liver cancer cell lines. Sci Rep 8(1):1570.  https://doi.org/10.1038/s41598-018-19817-wCrossRefPubMedPubMedCentralGoogle Scholar
  3. Balar AV, Weber JS (2017) PD-1 and PD-L1 antibodies in cancer: current status and future directions. Cancer Immunol Immunother 66(5):551–564.  https://doi.org/10.1007/s00262-017-1954-6CrossRefPubMedGoogle Scholar
  4. Ban J, Aryee DN, Fourtouna A, van der Ent W, Kauer M, Niedan S, Machado I, Rodriguez-Galindo C, Tirado OM, Schwentner R, Picci P, Flanagan AM, Berg V, Strauss SJ, Scotlandi K, Lawlor ER, Snaar-Jagalska E, Llombart-Bosch A, Kovar H (2014) Suppression of deacetylase SIRT1 mediates tumor-suppressive NOTCH response and offers a novel treatment option in metastatic Ewing sarcoma. Cancer Res 74(22):6578–6588.  https://doi.org/10.1158/0008-5472.CAN-14-1736CrossRefPubMedGoogle Scholar
  5. Barriuso J, Nagaraju R, Hurlstone A (2015) Zebrafish: a new companion for translational research in oncology. Clin Cancer Res 21(5):969–975.  https://doi.org/10.1158/1078-0432.CCR-14-2921CrossRefPubMedPubMedCentralGoogle Scholar
  6. Belikov AV (2017) The number of key carcinogenic events can be predicted from cancer incidence. Sci Rep 7(1):12170.  https://doi.org/10.1038/s41598-017-12448-7CrossRefPubMedPubMedCentralGoogle Scholar
  7. Berghmans S, Murphey RD, Wienholds E, Neuberg D, Kutok JL, Fletcher CD, Morris JP, Liu TX, Schulte-Merker S, Kanki JP, Plasterk R, Zon LI, Look AT (2005) tp53 mutant zebrafish develop malignant peripheral nerve sheath tumors. Proc Natl Acad Sci U S A 102(2):407–412.  https://doi.org/10.1073/pnas.0406252102CrossRefPubMedPubMedCentralGoogle Scholar
  8. Bray F, Ferlay J, Soerjomataram I, Siegel RL, Torre LA, Jemal A (2018) Global cancer statistics 2018: GLOBOCAN estimates of incidence and mortality worldwide for 36 cancers in 185 countries. CA Cancer J Clin 68(6):394–424.  https://doi.org/10.3322/caac.21492CrossRefGoogle Scholar
  9. Cekanova M, Rathore K (2014) Animal models and therapeutic molecular targets of cancer: utility and limitations. Drug Des Devel Ther 8:1911–1921.  https://doi.org/10.2147/DDDT.S49584CrossRefPubMedPubMedCentralGoogle Scholar
  10. Chiavacci E, Rizzo M, Pitto L, Patella F, Evangelista M, Mariani L, Rainaldi G (2015) The zebrafish/tumor xenograft angiogenesis assay as a tool for screening anti-angiogenic miRNAs. Cytotechnology 67(6):969–975.  https://doi.org/10.1007/s10616-014-9735-yCrossRefPubMedGoogle Scholar
  11. DE Fatima FBDC, DE Castro SAC, Muniz J, RC DA, Lamarao LM, DE Fatima AMNC, DE Assumpcao PP, Burbano RR (2018) Deregulation of the SRC family tyrosine kinases in gastric carcinogenesis in non-human primates. Anticancer Res 38(11):6317–6320.  https://doi.org/10.21873/anticanres.12988CrossRefGoogle Scholar
  12. den Hertog J (2016) Tumor suppressors in zebrafish: from TP53 to PTEN and beyond. Adv Exp Med Biol 916:87–101.  https://doi.org/10.1007/978-3-319-30654-4_4CrossRefPubMedGoogle Scholar
  13. Drabsch Y, He S, Zhang L, Snaar-Jagalska BE, Ten DP (2013) Transforming growth factor-beta signalling controls human breast cancer metastasis in a zebrafish xenograft model. Breast Cancer Res 15(6):R106.  https://doi.org/10.1186/bcr3573CrossRefPubMedPubMedCentralGoogle Scholar
  14. Evason KJ, Francisco MT, Juric V, Balakrishnan S, Lopez PMP, Gordan JD, Kakar S, Spitsbergen J, Goga A, Stainier DY (2015) Identification of chemical inhibitors of beta-catenin-driven liver tumorigenesis in zebrafish. PLoS Genet 11(7):e1005305.  https://doi.org/10.1371/journal.pgen.1005305CrossRefPubMedPubMedCentralGoogle Scholar
  15. Fior R, Povoa V, Mendes RV, Carvalho T, Gomes A, Figueiredo N, Ferreira MG (2017) Single-cell functional and chemosensitive profiling of combinatorial colorectal therapy in zebrafish xenografts. Proc Natl Acad Sci U S A 114(39):E8234–E8243.  https://doi.org/10.1073/pnas.1618389114CrossRefPubMedPubMedCentralGoogle Scholar
  16. Franzetti GA, Laud-Duval K, van der Ent W, Brisac A, Irondelle M, Aubert S, Dirksen U, Bouvier C, de Pinieux G, Snaar-Jagalska E, Chavrier P, Delattre O (2017) Cell-to-cell heterogeneity of EWSR1-FLI1 activity determines proliferation/migration choices in Ewing sarcoma cells. Oncogene 36(25):3505–3514.  https://doi.org/10.1038/onc.2016.498CrossRefPubMedPubMedCentralGoogle Scholar
  17. Gardner HL, Fenger JM, London CA (2016) Dogs as a model for cancer. Annu Rev Anim Biosci 4:199–222.  https://doi.org/10.1146/annurev-animal-022114-110911CrossRefPubMedGoogle Scholar
  18. Gaudenzi G, Albertelli M, Dicitore A, Wurth R, Gatto F, Barbieri F, Cotelli F, Florio T, Ferone D, Persani L, Vitale G (2017) Patient-derived xenograft in zebrafish embryos: a new platform for translational research in neuroendocrine tumors. Endocrine 57(2):214–219.  https://doi.org/10.1007/s12020-016-1048-9CrossRefPubMedGoogle Scholar
  19. Guo M, Wei H, Hu J, Sun S, Long J, Wang X (2015) U0126 inhibits pancreatic cancer progression via the KRAS signaling pathway in a zebrafish xenotransplantation model. Oncol Rep 34(2):699–706.  https://doi.org/10.3892/or.2015.4019CrossRefPubMedGoogle Scholar
  20. Hanahan D, Weinberg RA (2011) Hallmarks of cancer: the next generation. Cell 144(5):646–674.  https://doi.org/10.1016/j.cell.2011.02.013CrossRefGoogle Scholar
  21. He S, Mansour MR, Zimmerman MW, Ki DH, Layden HM, Akahane K, Gjini E, de Groh ED, Perez-Atayde AR, Zhu S, Epstein JA, Look AT (2016) Synergy between loss of NF1 and overexpression of MYCN in neuroblastoma is mediated by the GAP-related domain. Elife 5:5.  https://doi.org/10.7554/eLife.14713CrossRefGoogle Scholar
  22. He S, Jing CB, Look AT (2017) Zebrafish models of leukemia. Methods Cell Biol 138:563–592.  https://doi.org/10.1016/bs.mcb.2016.11.013CrossRefPubMedGoogle Scholar
  23. Hou Y, Chu M, Du FF, Lei JY, Chen Y, Zhu RY, Gong XH, Ma X, Jin J (2013) Recombinant disintegrin domain of ADAM15 inhibits the proliferation and migration of Bel-7402 cells. Biochem Biophys Res Commun 435(4):640–645.  https://doi.org/10.1016/j.bbrc.2013.05.037CrossRefPubMedGoogle Scholar
  24. Ikonomopoulou MP, Fernandez-Rojo MA, Pineda SS, Cabezas-Sainz P, Winnen B, Morales R, Brust A, Sanchez L, Alewood PF, Ramm GA, Miles JJ, King GF (2018) Gomesin inhibits melanoma growth by manipulating key signaling cascades that control cell death and proliferation. Sci Rep 8(1):11519.  https://doi.org/10.1038/s41598-018-29826-4CrossRefPubMedPubMedCentralGoogle Scholar
  25. Jo DH, Son D, Na Y, Jang M, Choi JH, Kim JH, Yu YS, Seok SH, Kim JH (2013) Orthotopic transplantation of retinoblastoma cells into vitreous cavity of zebrafish for screening of anticancer drugs. Mol Cancer 12:71.  https://doi.org/10.1186/1476-4598-12-71CrossRefPubMedPubMedCentralGoogle Scholar
  26. Kim IS, Heilmann S, Kansler ER, Zhang Y, Zimmer M, Ratnakumar K, Bowman RL, Simon-Vermot T, Fennell M, Garippa R, Lu L, Lee W, Hollmann T, Xavier JB, White RM (2017) Microenvironment-derived factors driving metastatic plasticity in melanoma. Nat Commun 8:14343.  https://doi.org/10.1038/ncomms14343CrossRefPubMedPubMedCentralGoogle Scholar
  27. Kirchberger S, Sturtzel C, Pascoal S, Distel M (2017) Quo natas, Danio?-Recent progress in modeling cancer in zebrafish. Front Oncol 7:186.  https://doi.org/10.3389/fonc.2017.00186CrossRefPubMedPubMedCentralGoogle Scholar
  28. Klimstra DS, Modlin IR, Coppola D, Lloyd RV, Suster S (2010) The pathologic classification of neuroendocrine tumors: a review of nomenclature, grading, and staging systems. Pancreas 39(6):707–712.  https://doi.org/10.1097/MPA.0b013e3181ec124eCrossRefGoogle Scholar
  29. Knudson AG (2001) Two genetic hits (more or less) to cancer. Nat Rev Cancer 1(2):157–162.  https://doi.org/10.1038/35101031CrossRefPubMedPubMedCentralGoogle Scholar
  30. Korzh S, Pan X, Garcia-Lecea M, Winata CL, Pan X, Wohland T, Korzh V, Gong Z (2008) Requirement of vasculogenesis and blood circulation in late stages of liver growth in zebrafish. BMC Dev Biol 8:84.  https://doi.org/10.1186/1471-213X-8-84CrossRefPubMedPubMedCentralGoogle Scholar
  31. Kwan W, North TE (2017) Netting novel regulators of hematopoiesis and hematologic malignancies in zebrafish. Curr Top Dev Biol 124:125–160.  https://doi.org/10.1016/bs.ctdb.2016.11.005CrossRefPubMedGoogle Scholar
  32. Latifi A, 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(10):2850–2864.  https://doi.org/10.1002/jcb.23199CrossRefPubMedGoogle Scholar
  33. Lee LM, Seftor EA, Bonde G, Cornell RA, Hendrix MJ (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(4):1560–1570.  https://doi.org/10.1002/dvdy.20471CrossRefPubMedGoogle Scholar
  34. Leung A, Veinotte CJ, Melong N, Oh MH, Chen K, Enfield K, Backstrom I, Warburton C, Yapp D, Berman JN, Bally MB, Lockwood WW (2017) In vivo validation of PAPSS1 (3′-phosphoadenosine 5′-phosphosulfate synthase 1) as a cisplatin-sensitizing therapeutic target. Clin Cancer Res 23(21):6555–6566.  https://doi.org/10.1158/1078-0432.CCR-17-0700CrossRefPubMedGoogle Scholar
  35. Li Z, Huang X, Zhan H, Zeng Z, Li C, Spitsbergen JM, Meierjohann S, Schartl M, Gong Z (2012) Inducible and repressable oncogene-addicted hepatocellular carcinoma in Tet-on xmrk transgenic zebrafish. J Hepatol 56(2):419–425.  https://doi.org/10.1016/j.jhep.2011.07.025CrossRefPubMedGoogle Scholar
  36. Li Z, Zheng W, Wang Z, Zeng Z, Zhan H, Li C, Zhou L, Yan C, Spitsbergen JM, Gong Z (2013) A transgenic zebrafish liver tumor model with inducible Myc expression reveals conserved Myc signatures with mammalian liver tumors. Dis Model Mech 6(2):414–423.  https://doi.org/10.1242/dmm.010462CrossRefPubMedGoogle Scholar
  37. Liu S, Leach SD (2011) Screening pancreatic oncogenes in zebrafish using the Gal4/UAS system. Methods Cell Biol 105:367–381.  https://doi.org/10.1016/B978-0-12-381320-6.00015-1CrossRefPubMedPubMedCentralGoogle Scholar
  38. Lord CJ, Ashworth A (2012) The DNA damage response and cancer therapy. Nature 481(7381):287–294.  https://doi.org/10.1038/nature10760CrossRefPubMedGoogle Scholar
  39. Lu JW, Yang WY, Tsai SM, Lin YM, Chang PH, Chen JR, Wang HD, Wu JL, Jin SL, Yuh CH (2013) Liver-specific expressions of HBx and src in the p53 mutant trigger hepatocarcinogenesis in zebrafish. PLoS One 8(10):e76951.  https://doi.org/10.1371/journal.pone.0076951CrossRefPubMedPubMedCentralGoogle Scholar
  40. Lu JW, Liao CY, Yang WY, Lin YM, Jin SL, Wang HD, Yuh CH (2014) Overexpression of endothelin 1 triggers hepatocarcinogenesis in zebrafish and promotes cell proliferation and migration through the AKT pathway. PLoS One 9(1):e85318.  https://doi.org/10.1371/journal.pone.0085318CrossRefPubMedPubMedCentralGoogle Scholar
  41. MacRae CA, Peterson RT (2015) Zebrafish as tools for drug discovery. Nat Rev Drug Discov 14(10):721–731.  https://doi.org/10.1038/nrd4627CrossRefPubMedGoogle Scholar
  42. Maddalo D, Manchado E, Concepcion CP, Bonetti C, Vidigal JA, Han YC, Ogrodowski P, Crippa A, Rekhtman N, de Stanchina E, Lowe SW, Ventura A (2014) In vivo engineering of oncogenic chromosomal rearrangements with the CRISPR/Cas9 system. Nature 516(7531):423–427.  https://doi.org/10.1038/nature13902CrossRefPubMedPubMedCentralGoogle Scholar
  43. Maresch R, Mueller S, Veltkamp C, Ollinger R, Friedrich M, Heid I, Steiger K, Weber J, Engleitner T, Barenboim M, Klein S, Louzada S, Banerjee R, Strong A, Stauber T, Gross N, Geumann U, Lange S, Ringelhan M, Varela I, Unger K, Yang F, Schmid RM, Vassiliou GS, Braren R, Schneider G, Heikenwalder M, Bradley A, Saur D, Rad R (2016) Multiplexed pancreatic genome engineering and cancer induction by transfection-based CRISPR/Cas9 delivery in mice. Nat Commun 7:10770.  https://doi.org/10.1038/ncomms10770CrossRefPubMedPubMedCentralGoogle Scholar
  44. Mercatali L, La Manna F, Groenewoud A, Casadei R, Recine F, Miserocchi G, Pieri F, Liverani C, Bongiovanni A, Spadazzi C, de Vita A, van der Pluijm G, Giorgini A, Biagini R, Amadori D, Ibrahim T, Snaar-Jagalska E (2016) Development of a patient-derived xenograft (PDX) of breast cancer bone metastasis in a zebrafish model. Int J Mol Sci 17(8).  https://doi.org/10.3390/ijms17081375CrossRefGoogle Scholar
  45. Mir R, Pradhan SJ, Patil P, Mulherkar R, Galande S (2016) Wnt/beta-catenin signaling regulated SATB1 promotes colorectal cancer tumorigenesis and progression. Oncogene 35(13):1679–1691.  https://doi.org/10.1038/onc.2015.232CrossRefPubMedGoogle Scholar
  46. Moore JC, Tang Q, Yordan NT, Moore FE, Garcia EG, Lobbardi R, Ramakrishnan A, Marvin DL, Anselmo A, Sadreyev RI, Langenau DM (2016) Single-cell imaging of normal and malignant cell engraftment into optically clear prkdc-null SCID zebrafish. J Exp Med 213(12):2575–2589.  https://doi.org/10.1084/jem.20160378CrossRefPubMedPubMedCentralGoogle Scholar
  47. Moshal KS, Ferri-Lagneau KF, Haider J, Pardhanani P, Leung T (2011) Discriminating different cancer cells using a zebrafish in vivo assay. Cancers (Basel) 3(4):4102–4113.  https://doi.org/10.3390/cancers3044102CrossRefGoogle Scholar
  48. Mueller S, Engleitner T, Maresch R, Zukowska M, Lange S, Kaltenbacher T, Konukiewitz B, Ollinger R, Zwiebel M, Strong A, Yen HY, Banerjee R, Louzada S, Fu B, Seidler B, Gotzfried J, Schuck K, Hassan Z, Arbeiter A, Schonhuber N, Klein S, Veltkamp C, Friedrich M, Rad L, Barenboim M, Ziegenhain C, Hess J, Dovey OM, Eser S, Parekh S, Constantino-Casas F, de la Rosa J, Sierra MI, Fraga M, Mayerle J, Kloppel G, Cadinanos J, Liu P, Vassiliou G, Weichert W, Steiger K, Enard W, Schmid RM, Yang F, Unger K, Schneider G, Varela I, Bradley A, Saur D, Rad R (2018) Evolutionary routes and KRAS dosage define pancreatic cancer phenotypes. Nature 554(7690):62–68.  https://doi.org/10.1038/nature25459CrossRefPubMedPubMedCentralGoogle Scholar
  49. Nguyen AT, Emelyanov A, Koh CH, Spitsbergen JM, Lam SH, Mathavan S, Parinov S, Gong Z (2011) A high level of liver-specific expression of oncogenic Kras(V12) drives robust liver tumorigenesis in transgenic zebrafish. Dis Model Mech 4(6):801–813.  https://doi.org/10.1242/dmm.007831CrossRefPubMedPubMedCentralGoogle Scholar
  50. Nguyen AT, Emelyanov A, Koh CH, Spitsbergen JM, Parinov S, Gong Z (2012) An inducible kras(V12) transgenic zebrafish model for liver tumorigenesis and chemical drug screening. Dis Model Mech 5(1):63–72.  https://doi.org/10.1242/dmm.008367CrossRefPubMedGoogle Scholar
  51. Nicoli S, Presta M (2007) The zebrafish/tumor xenograft angiogenesis assay. Nat Protoc 2(11):2918–2923.  https://doi.org/10.1038/nprot.2007.412CrossRefPubMedGoogle Scholar
  52. Parada-Kusz M, Penaranda C, Hagedorn EJ, Clatworthy A, Nair AV, Henninger JE, Ernst C, Li B, Riquelme R, Jijon H, Villablanca EJ, Zon LI, Hung D, Allende ML (2018) Generation of mouse-zebrafish hematopoietic tissue chimeric embryos for hematopoiesis and host-pathogen interaction studies. Dis Model Mech 11(11):dmm034876.  https://doi.org/10.1242/dmm.034876CrossRefPubMedPubMedCentralGoogle Scholar
  53. Park SW, Davison JM, Rhee J, Hruban RH, Maitra A, Leach SD (2008) Oncogenic KRAS induces progenitor cell expansion and malignant transformation in zebrafish exocrine pancreas. Gastroenterology 134(7):2080–2090.  https://doi.org/10.1053/j.gastro.2008.02.084CrossRefPubMedPubMedCentralGoogle Scholar
  54. Pettitt D, Arshad Z, Smith J, Stanic T, Hollander G, Brindley D (2018) CAR-T cells: a systematic review and mixed methods analysis of the clinical trial landscape. Mol Ther 26(2):342–353.  https://doi.org/10.1016/j.ymthe.2017.10.019CrossRefPubMedGoogle Scholar
  55. Platt RJ, Chen S, Zhou Y, Yim MJ, Swiech L, Kempton HR, Dahlman JE, Parnas O, Eisenhaure TM, Jovanovic M, Graham DB, Jhunjhunwala S, Heidenreich M, Xavier RJ, Langer R, Anderson DG, Hacohen N, Regev A, Feng G, Sharp PA, Zhang F (2014) CRISPR-Cas9 knockin mice for genome editing and cancer modeling. Cell 159(2):440–455.  https://doi.org/10.1016/j.cell.2014.09.014CrossRefPubMedPubMedCentralGoogle Scholar
  56. Rai K, Sarkar S, Broadbent TJ, Voas M, Grossmann KF, Nadauld LD, Dehghanizadeh S, Hagos FT, Li Y, Toth RK, Chidester S, Bahr TM, Johnson WE, Sklow B, Burt R, Cairns BR, Jones DA (2010) DNA demethylase activity maintains intestinal cells in an undifferentiated state following loss of APC. Cell 142(6):930–942.  https://doi.org/10.1016/j.cell.2010.08.030CrossRefPubMedPubMedCentralGoogle Scholar
  57. Romero R, Sayin VI, Davidson SM, Bauer MR, Singh SX, LeBoeuf SE, Karakousi TR, Ellis DC, Bhutkar A, Sanchez-Rivera FJ, Subbaraj L, Martinez B, Bronson RT, Prigge JR, Schmidt EE, Thomas CJ, Goparaju C, Davies A, Dolgalev I, Heguy A, Allaj V, Poirier JT, Moreira AL, Rudin CM, Pass HI, Vander HM, Jacks T, Papagiannakopoulos T (2017) Keap1 loss promotes Kras-driven lung cancer and results in dependence on glutaminolysis. Nat Med 23(11):1362–1368.  https://doi.org/10.1038/nm.4407CrossRefPubMedPubMedCentralGoogle Scholar
  58. Rycaj K, Tang DG (2015) Cell-of-origin of cancer versus cancer stem cells: assays and interpretations. Cancer Res 75(19):4003–4011.  https://doi.org/10.1158/0008-5472.CAN-15-0798CrossRefPubMedPubMedCentralGoogle Scholar
  59. Sanchez-Rivera FJ, Papagiannakopoulos T, Romero R, Tammela T, Bauer MR, Bhutkar A, Joshi NS, Subbaraj L, Bronson RT, Xue W, Jacks T (2014) Rapid modelling of cooperating genetic events in cancer through somatic genome editing. Nature 516(7531):428–431.  https://doi.org/10.1038/nature13906CrossRefPubMedPubMedCentralGoogle Scholar
  60. Shive HR, West RR, Embree LJ, Azuma M, Sood R, Liu P, Hickstein DD (2010) brca2 in zebrafish ovarian development, spermatogenesis, and tumorigenesis. Proc Natl Acad Sci U S A 107(45):19350–19355.  https://doi.org/10.1073/pnas.1011630107CrossRefPubMedPubMedCentralGoogle Scholar
  61. Shive HR, West RR, Embree LJ, Golden CD, Hickstein DD (2014) BRCA2 and TP53 collaborate in tumorigenesis in zebrafish. PLoS One 9(1):e87177.  https://doi.org/10.1371/journal.pone.0087177CrossRefPubMedPubMedCentralGoogle Scholar
  62. Smith MP, Ferguson J, Arozarena I, Hayward R, Marais R, Chapman A, Hurlstone A, Wellbrock C (2013) Effect of SMURF2 targeting on susceptibility to MEK inhibitors in melanoma. J Natl Cancer Inst 105(1):33–46.  https://doi.org/10.1093/jnci/djs471CrossRefPubMedGoogle Scholar
  63. Solin SL, Shive HR, Woolard KD, Essner JJ, McGrail M (2015) Rapid tumor induction in zebrafish by TALEN-mediated somatic inactivation of the retinoblastoma1 tumor suppressor rb1. Sci Rep 5:13745.  https://doi.org/10.1038/srep13745CrossRefPubMedPubMedCentralGoogle Scholar
  64. Sonoshita M, Cagan RL (2017) Modeling human cancers in drosophila. Curr Top Dev Biol 121:287–309.  https://doi.org/10.1016/bs.ctdb.2016.07.008CrossRefPubMedGoogle Scholar
  65. Tan DS, Haaland B, Gan JM, Tham SC, Sinha I, Tan EH, Lim KH, Takano A, Krisna SS, Thu MM, Liew HP, Ullrich A, Lim WT, Chua BT (2014) Bosutinib inhibits migration and invasion via ACK1 in KRAS mutant non-small cell lung cancer. Mol Cancer 13:13.  https://doi.org/10.1186/1476-4598-13-13CrossRefPubMedPubMedCentralGoogle Scholar
  66. 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(8):821–824.  https://doi.org/10.1038/nmeth.3031CrossRefPubMedPubMedCentralGoogle Scholar
  67. Tang Q, Moore JC, Ignatius MS, Tenente IM, Hayes MN, Garcia EG, Torres YN, Bourque C, He S, Blackburn JS, Look AT, Houvras Y, Langenau DM (2016) Imaging tumour cell heterogeneity following cell transplantation into optically clear immune-deficient zebrafish. Nat Commun 7:10358.  https://doi.org/10.1038/ncomms10358CrossRefPubMedPubMedCentralGoogle Scholar
  68. Tubbs A, Nussenzweig A (2017) Endogenous DNA damage as a source of genomic instability in Cancer. Cell 168(4):644–656.  https://doi.org/10.1016/j.cell.2017.01.002CrossRefPubMedPubMedCentralGoogle Scholar
  69. van der Ent W, Jochemsen AG, Teunisse AF, Krens SF, Szuhai K, Spaink HP, Hogendoorn PC, Snaar-Jagalska BE (2014) Ewing sarcoma inhibition by disruption of EWSR1-FLI1 transcriptional activity and reactivation of p53. J Pathol 233(4):415–424.  https://doi.org/10.1002/path.4378CrossRefPubMedGoogle Scholar
  70. van der Ent W, Burrello C, de Lange MJ, van der Velden PA, Jochemsen AG, Jager MJ, Snaar-Jagalska BE (2015) Embryonic zebrafish: different phenotypes after injection of human uveal melanoma cells. Ocul Oncol Pathol 1(3):170–181.  https://doi.org/10.1159/000370159CrossRefPubMedPubMedCentralGoogle Scholar
  71. Van Slyke CE, Bradford YM, Howe DG, Fashena DS, Ramachandran S, Ruzicka L (2018) Using ZFIN: data types, organization, and retrieval. Methods Mol Biol 1757:307–347.  https://doi.org/10.1007/978-1-4939-7737-6_11CrossRefPubMedPubMedCentralGoogle Scholar
  72. 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(7):745–754.  https://doi.org/10.1242/dmm.015784CrossRefPubMedPubMedCentralGoogle Scholar
  73. Visvader JE (2011) Cells of origin in cancer. Nature 469(7330):314–322.  https://doi.org/10.1038/nature09781CrossRefGoogle Scholar
  74. Wagner DS, Delk NA, Lukianova-Hleb EY, Hafner JH, Farach-Carson MC, Lapotko DO (2010) The in vivo performance of plasmonic nanobubbles as cell theranostic agents in zebrafish hosting prostate cancer xenografts. Biomaterials 31(29):7567–7574.  https://doi.org/10.1016/j.biomaterials.2010.06.031CrossRefPubMedPubMedCentralGoogle Scholar
  75. Wang X, Kopinke D, Lin J, McPherson AD, Duncan RN, Otsuna H, Moro E, Hoshijima K, Grunwald DJ, Argenton F, Chien CB, Murtaugh LC, Dorsky RI (2012) Wnt signaling regulates postembryonic hypothalamic progenitor differentiation. Dev Cell 23(3):624–636.  https://doi.org/10.1016/j.devcel.2012.07.012CrossRefPubMedPubMedCentralGoogle Scholar
  76. Wang J, Leng X, Wang G, Wan X, Cao H (2017) The construction of intrahepatic cholangiocarcinoma model in zebrafish. Sci Rep 7(1):13419.  https://doi.org/10.1038/s41598-017-13815-0CrossRefPubMedPubMedCentralGoogle Scholar
  77. Wang J, Fei F, Berberoglu MA, Sun S, Wang L, Dong Z, Wang X (2018) Csy4-based vector system enables conditional chimeric gene editing in zebrafish without interrupting embryogenesis. J Mol Cell Biol 10(6):586–588.  https://doi.org/10.1093/jmcb/mjy017CrossRefPubMedGoogle Scholar
  78. Wang L, Chen H, Fei F, He X, Sun S, Lv K, Yu B, Long J, Wang X (2019) Patient-derived heterogeneous xenograft model of pancreatic cancer using zebrafish larvae as hosts for comparative drug assessment. J Vis Exp 146.  https://doi.org/10.3791/59507
  79. Waster P, Orfanidis K, Eriksson I, Rosdahl I, Seifert O, Ollinger K (2017) UV radiation promotes melanoma dissemination mediated by the sequential reaction axis of cathepsins-TGF-beta1-FAP-alpha. Br J Cancer 117(4):535–544.  https://doi.org/10.1038/bjc.2017.182CrossRefPubMedPubMedCentralGoogle Scholar
  80. White R, Rose K, Zon L (2013) Zebrafish cancer: the state of the art and the path forward. Nat Rev Cancer 13(9):624–636.  https://doi.org/10.1038/nrc3589CrossRefPubMedPubMedCentralGoogle Scholar
  81. Wu JQ, Zhai J, Li CY, Tan AM, Wei P, Shen LZ, He MF (2017) Patient-derived xenograft in zebrafish embryos: a new platform for translational research in gastric cancer. J Exp Clin Cancer Res 36(1):160.  https://doi.org/10.1186/s13046-017-0631-0CrossRefPubMedPubMedCentralGoogle Scholar
  82. Wu Q, Zheng K, Huang X, Li L, Mei W (2018) Tanshinone-IIA-based analogues of imidazole alkaloid act as potent inhibitors to block breast cancer invasion and metastasis in vivo. J Med Chem 61:10488–10501.  https://doi.org/10.1021/acs.jmedchem.8b01018CrossRefPubMedGoogle Scholar
  83. Xu W, Foster BA, Richards M, Bondioli KR, Shah G, Green CC (2018) Characterization of prostate cancer cell progression in zebrafish xenograft model. Int J Oncol 52(1):252–260.  https://doi.org/10.3892/ijo.2017.4189CrossRefPubMedGoogle Scholar
  84. Yan C, Yang Q, Shen HM, Spitsbergen JM, Gong Z (2017a) Chronically high level of tgfb1a induction causes both hepatocellular carcinoma and cholangiocarcinoma via a dominant Erk pathway in zebrafish. Oncotarget 8(44):77096–77109.  https://doi.org/10.18632/oncotarget.20357CrossRefPubMedPubMedCentralGoogle Scholar
  85. Yan C, Yang Q, Gong Z (2017b) Tumor-associated neutrophils and macrophages promote gender disparity in hepatocellular carcinoma in zebrafish. Cancer Res 77(6):1395–1407.  https://doi.org/10.1158/0008-5472.CAN-16-2200CrossRefPubMedGoogle Scholar
  86. Yang HW, Kutok JL, Lee NH, Piao HY, Fletcher CD, Kanki JP, Look AT (2004) Targeted expression of human MYCN selectively causes pancreatic neuroendocrine tumors in transgenic zebrafish. Cancer Res 64(20):7256–7262.  https://doi.org/10.1158/0008-5472.CAN-04-0931CrossRefPubMedGoogle Scholar
  87. Yang XJ, Cui W, Gu A, Xu C, Yu SC, Li TT, Cui YH, Zhang X, Bian XW (2013) A novel zebrafish xenotransplantation model for study of glioma stem cell invasion. PLoS One 8(4):e61801.  https://doi.org/10.1371/journal.pone.0061801CrossRefPubMedPubMedCentralGoogle Scholar
  88. Yang J, Pei H, Luo H, Fu A, Yang H, Hu J, Zhao C, Chai L, Chen X, Shao X, Wang C, Wu W, Wan L, Ye H, Qiu Q, Peng A, Wei Y, Yang L, Chen L (2017) Non-toxic dose of liposomal honokiol suppresses metastasis of hepatocellular carcinoma through destabilizing EGFR and inhibiting the downstream pathways. Oncotarget 8(1):915–932.  https://doi.org/10.18632/oncotarget.13687CrossRefPubMedGoogle Scholar
  89. Yang Q, Yan C, Wang X, Gong Z (2019) Leptin induces muscle wasting in a zebrafish kras-driven hepatocellular carcinoma (HCC) model. Dis Model Mech 12(2):dmm038240.  https://doi.org/10.1242/dmm.038240CrossRefPubMedPubMedCentralGoogle Scholar
  90. Yao Y, Sun S, Fei F, Wang J, Wang Y, Zhang R, Wu J, Liu L, Liu X, Cui Z, Li Q, Yu M, Dang Y, Wang X (2017) Screening in larval zebrafish reveals tissue-specific distribution of fifteen fluorescent compounds. Dis Model Mech 10(9):1155–1164.  https://doi.org/10.1242/dmm.028811CrossRefPubMedPubMedCentralGoogle Scholar
  91. Yao Y, Sun S, Wang J, Fei F, Dong Z, Ke AW, He R, Wang L, Zhang L, Ji MB, Li Q, Yu M, Shi GM, Fan J, Gong Z, Wang X (2018) Canonical Wnt signaling remodels lipid metabolism in zebrafish hepatocytes following Ras oncogenic insult. Cancer Res 78(19):5548–5560.  https://doi.org/10.1158/0008-5472.CAN-17-3964CrossRefPubMedGoogle Scholar
  92. Yee NS, Ignatenko N, Finnberg N, Lee N, Stairs D (2015) Animal models of cancer biology. Cancer Growth Metastasis 8(Suppl 1):115–118.  https://doi.org/10.4137/CGM.S37907CrossRefPubMedPubMedCentralGoogle Scholar
  93. Zhan T, Rindtorff N, Boutros M (2017) Wnt signaling in cancer. Oncogene 36(11):1461–1473.  https://doi.org/10.1038/onc.2016.304CrossRefPubMedGoogle Scholar
  94. Zuckermann M, Hovestadt V, Knobbe-Thomsen CB, Zapatka M, Northcott PA, Schramm K, Belic J, Jones DT, Tschida B, Moriarity B, Largaespada D, Roussel MF, Korshunov A, Reifenberger G, Pfister SM, Lichter P, Kawauchi D, Gronych J (2015) Somatic CRISPR/Cas9-mediated tumour suppressor disruption enables versatile brain tumour modelling. Nat Commun 6:7391.  https://doi.org/10.1038/ncomms8391CrossRefPubMedPubMedCentralGoogle Scholar

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© Springer Nature Switzerland AG 2020

Authors and Affiliations

  1. 1.Cancer Metabolism LaboratoryCancer Institute, Fudan University Shanghai Cancer CenterShanghaiChina
  2. 2.Key Laboratory of Metabolism and Molecular Medicine, Ministry of Education, Department of Biochemistry and Molecular Biology, School of Basic Medical SciencesFudan UniversityShanghaiChina

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