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Zebrafish: Speeding up the Cancer Drug Discovery
Process
Patricia Letrado1,2, Irene de Miguel2, Iranzu Lamberto1, Roberto Díez-Martínez1,*
and Julen Oyarzabal2,*
1 Ikan Biotech SL, The Zebrafish Lab Department, Centro Europeo de Empresas e
Innovación de Navarra (CEIN), Plaza CEIN 5 D9-A4, 31110 Noain, Spain.
2 Small Molecule Discovery Platform, Molecular Therapeutics Program, Center for
Applied Medical Research (CIMA), University of Navarra, Avenida Pio XII 55, E-
31008 Pamplona, Spain.
Table of Contents
S5.1. Supplementary Table S5....................................................................................................S2
S5.2. References S5......................................................................................................................... S3
S6.1. Supplementary Table S6....................................................................................................S7
S6.2. References S6......................................................................................................................... S8
S7.1. Supplementary Table S7....................................................................................................S9
S7.2. References S7.......................................................................................................................S10
S8.1. Supplementary Table S8.................................................................................................S14
S8.2. References S8.......................................................................................................................S15
S1
Supplementary Table S5. Cancer models carried out in zebrafish using genetics approaches.
Cancer Gene Methodology (ref)
Ewing´s sarcomaHRASV12 Transgenesis (1)
hsp70 or β-actin-EWSR1-FLI1
Transgenesis (2)
GliomaRAS(G12D) Transgenesis (3)
Nf1, nf2 Mutagenesis (4)
Hepatocarcinoma
Mycsrc
Transgenesis (5)
UHRF1 Transgenesis (6)fabp10:beta-catenin Transgenesis (7)
apc Mutagenesis (8)
Hemangiosarcoma pten Mutagenesis (9)
Leukemia (T-ALL)
Myc Transgenesis (10-13)
akt Transgenesis (14)
Noch1 Transgenesis (12,15)
Leukemia (B-ALL) TEL-AML1 Transgenesis (16)
Leukemia (AML)Mycn Transgenesis (5)
MOZ/TIF2, -MYST3/NCOA2 Transgenesis (17)Malignant peripheral neural sheath tumor
(MPNST)
tp53 Mutagenesis (18)Nf1 Mutagenesis (4)
KRAS(G12D) Transgenesis (19)
MelanomaBRAF(V600E) Transgenesis (20,21)
HRAS(G12V) Transgenesis (22,23)NRAS(Q61K) Transgenesis (21,24)
Myeloproliferative neoplams
NUP98-HOXA9 (NHA9) Transgenesis (25)
KIT-D816V Transgenesis (26)sp1-NUP98-HOXA9 Transgenesis (27)
Ocular tumors pten Mutagenesis (28)
PancreaticKRAS(G12D) Transgenesis (29)
apc Mutagenesis (8)
Rabdomyosarcoma KRAS(G12D) Transgenesis (30,31)
S2
References S5
1. Burger A, Vasilyev A, Tomar R, Selig MK, Nielsen GP, Peterson RT, et al. A
zebrafish model of chordoma initiated by notochord-driven expression of
HRASV12. Dis Model Mech 2014;7:907–13.
2. Leacock SW, Basse AN, Chandler GL, Kirk AM, Rakheja D, Amatruda JF. A
zebrafish transgenic model of Ewing’s sarcoma reveals conserved mediators of
EWS-FLI1 tumorigenesis. Dis Model Mech;5:95–106.
3. Ju B, Chen W, Orr BA, Spitsbergen JM, Jia S, Eden CJ, et al. Oncogenic KRAS
promotes malignant brain tumors in zebrafish. Mol Cancer 2015;14:18.
4. Shin J, Padmanabhan A, de Groh ED, Lee J-S, Haidar S, Dahlberg S, et al.
Zebrafish neurofibromatosis type 1 genes have redundant functions in
tumorigenesis and embryonic development. Dis Model Mech 2012;5:881–94.
5. Shen LJ, Chen FY, Zhang Y, Cao LF, Kuang Y, Zhong M, et al. MYCN Transgenic
Zebrafish Model with the Characterization of Acute Myeloid Leukemia and
Altered Hematopoiesis. PLoS One 2013;8:1–12.
6. Mudbhary R, Hoshida Y, Chernyavskaya Y, Jacob V, Villanueva A, Fiel MI, et al.
UHRF1 overexpression drives DNA hypomethylation and hepatocellular
carcinoma. Cancer Cell 2014;25:196–209.
7. Evason KJ, Francisco MT, Juric V, Balakrishnan S, Lopez Pazmino M del P, Gordan
JD, et al. Identification of Chemical Inhibitors of β-Catenin-Driven Liver
Tumorigenesis in Zebrafish. PLoS Genet 2015;11:e1005305.
8. Haramis APG, Hurlstone A, van der Velden Y, Begthel H, van den Born M,
Offerhaus GJA, et al. Adenomatous polyposis coli-deficient zebrafish are
susceptible to digestive tract neoplasia. EMBO Rep 2006;7:444–9.
S3
9. Choorapoikayil S, Kuiper R V, de Bruin A, den Hertog J. Haploinsufficiency of the
genes encoding the tumor suppressor Pten predisposes zebrafish to
hemangiosarcoma. Dis Model Mech 2012;5:241–7.
10. Langenau DM, Feng H, Berghmans S, Kanki JP, Kutok JL, Look AT. Cre/lox-
regulated transgenic zebrafish model with conditional myc-induced T cell acute
lymphoblastic leukemia. Proc Natl Acad Sci U S A. 2005;102(17):6068-6073.
11. Gutierrez A, Pan L, Groen RWJ, et al. Phenothiazines induce PP2A-mediated
apoptosis in T cell acute lymphoblastic leukemia. J Clin Investig.
2014;124(2):644-655.
12. Blackburn JS, Liu S, Wilder JL, et al. Clonal evolution enhances leukemia
propagating cell frequency in T-cell acute lymphoblastic leukemia through
akt/mtorc1 pathway activation. Cancer Cell. 2014;25(3):366-378.
13. Ridges S, Heaton WL, Joshi D, et al. Zebrafish screen identifies novel compound
with selective toxicity against leukemia. Blood. 2012;119(24):5621-5631.
14. Gutierrez A, Grebliunaite R, Feng H, et al. Pten mediates Myc oncogene
dependence in a conditional zebrafish model of T cell acute lymphoblastic
leukemia. J Exp Med. 2011;208(8):1595-1603.
15. Chen J, Jette C, Kanki JP, Aster JC, Look AT, Griffin JD. NOTCH1-induced T-cell
leukemia in transgenic zebrafish. Leukemia. 2007;21(3):462-471.
16. Sabaawy HE, Azuma M, Embree LJ, Tsai H-J, Starost MF, Hickstein DD. TEL-AML1
transgenic zebrafish model of precursor B cell acute lymphoblastic leukemia.
Proc Natl Acad Sci U S A. 2006;103(41):15166-15171.
17. Zhuravleva J, Paggetti J, Martin L, Hammann A, Solary E, Bastie J-N, et al.
MOZ/TIF2-induced acute myeloid leukaemia in transgenic fish. Br J Haematol
S4
2008;143:378–82.
18. Berghmans S, Murphey RD, Wienholds E, Neuberg D. tp53 mutant zebrafish
develop malignant peripheral nerve sheath tumors. Proc Natl Acad Sci
2005;102:407–12.
19. Patton, E. Elizabeth, Windlund, Hans R, Kutok Jeffery L, Kopani KR. BRAF
Mutations Are Sufficient to Promote Nevi Formation and Cooperate with p53 in
the Genesis of Melanoma. Curr Biol 2005;15:249–54.
20. Lister JA, Capper A, Zeng Z, Mathers ME, Richardson J, Paranthaman K, et al. A
conditional zebrafish MITF mutation reveals MITF levels are critical for
melanoma promotion vs. regression in vivo. J Invest Dermatol 2014;134:133–40.
21. Yen J, White RM, Wedge DC, Van Loo P, de Ridder J, Capper A, et al. The genetic
heterogeneity and mutational burden of engineered melanomas in zebrafish
models. Genome Biol 2013;14:R113.
22. Michailidou C, Jones M, Walker P, Kamarashev J, Kelly A, Hurlstone AFL.
Dissecting the roles of Raf- and PI3K-signalling pathways in melanoma formation
and progression in a zebrafish model. Dis Model Mech 2009;2:399–411.
23. Anelli V, Santoriello C, Distel M, Köster RW, Ciccarelli FD, Mione M. Global
Repression of Cancer Gene Expression in a Zebrafish Model of Melanoma Is
Linked to Epigenetic Regulation. Zebrafish 2009;6:417–24.
24. Dovey M, White RM, Zon LI. Oncogenic NRAS Cooperates with p53 Loss to
Generate Melanoma in Zebrafish. Zebrafish 2009;6:397–404.
25. Deveau AP, Forrester AM, Coombs AJ, Wagner GS, Grabher C, Chute IC, et al.
Epigenetic therapy restores normal hematopoiesis in a zebrafish model of
NUP98–HOXA9-induced myeloid disease. Leukemia 2015;29:2086–97.
S5
26. Balci TB, Prykhozhij S V., Teh EM, Da’as SI, McBride E, Liwski R, et al. A
transgenic zebrafish model expressing KIT -D816V recapitulates features of
aggressive systemic mastocytosis. Br J Haematol 2014;167:48–61.
27. Forrester AM, Grabher C, McBride ER, Boyd ER, Vigerstad MH, Edgar A, et al.
NUP98-HOXA9-transgenic zebrafish develop a myeloproliferative neoplasm and
provide new insight into mechanisms of myeloid leukaemogenesis. Br J
Haematol 2011;155:167–81.
28. Faucherre A, Taylor GS, Overvoorde J, Dixon JE, Den Hertog J. Zebrafish pten
genes have overlapping and non-redundant functions in tumorigenesis and
embryonic development. Oncogene 2008;27:1079–86.
29. Provost E, Bailey JM, Aldrugh S, Liu S, Iacobuzio-Donahue C, Leach SD. The
tumor suppressor rpl36 restrains KRAS(G12V)-induced pancreatic cancer.
Zebrafish 2014;11:551–9.
30. Storer NY, White RM, Uong A, Price E, Nielsen GP, Langenau DM, et al. Zebrafish
rhabdomyosarcoma reflects the developmental stage of oncogene expression
during myogenesis. Development 2013;140:3040–50.
31. Ignatius MS, Chen EY, Elpek NM, Fuller A, Tenente IM, Clagg R, et al. NIH Public
Access. Cancer Cell 2012;21:680–93.
S6
Supplementary Table S6. Allograft assays carried out in zebrafish.
Cancer type (ref)
Donor zebrafish
Cancer origin
Receptor zebrafish
Immuno-suppresio
nStage
ERMS (1)
rag2-Myc orrag2-kRASG12D
Transgenesis
rag2E450fs Immuno-suppresed mutant
Not needed Adult
Hepatocarcinoma (2)
MutantDEN mutagenesis
Syngenic Not needed Adult
Hepatocarcinoma (3)
MutantDEN mutagenesis
Syngenic Not neededAdult, embryo
Leukemia (ALL) (4)
TransgenicTEL-AMIL1
Transgenesis
Wild-type Irradiation Adult
Leukemia(TALL y TLBL)
(5)Mutant
ENU mutagenesis
Wild-type Irradiation Adult
Leukemia (TALL) (6)
TransgenicNotch1 induced
Transgenesis
AB Wild-type
Irradiation Adult
Leukemia (TALL) (7)
Transgenic
Transgenesis
Syngenic CG1-strain,Wild-type
Not needed, irradiation
Adult
Leukemia (TALL) (8)
rag2-Myc orrag2-kRASG12D
Transgenesis
rag2E450fs,immuno-suppresed mutant
Not needed Adult
Melanoma (9)Transgenic BRAF
Transgenesis
Wild-type Irradiation Adult
Melanoma (8)
rag2-Myc orrag2-kRASG12D
Transgenesis
rag2E450fs, immuno-suppresed mutant
Not needed Adult
Pancreatic (3) MutantDEN mutagenesis
Syngenic Not neededAdult, embryo
Rhabdo-Myosarcoma
(7)
Transgenic
Transgenesis
Syngenic CG1-strain, Wild-type
Not needed, irradiation
Adult
S7
References S6
1. Tang Q, Abdelfattah NS, Blackburn JS, Moore JC. Optimized cell transplantation
using adult rag2 mutant zebrafish. Nat Methods 2014;11:821–4.
2. Mizgirev I, Revskoy S. Generation of clonal zebrafish lines and transplantable
hepatic tumors. Nat Protoc 2010;5:383–94.
3. Mizgireuv I V., Revskoy SY. Transplantable Tumor Lines Generated in Clonal
Zebrafish. Cancer Res 2006;66:3120–5.
4. Sabaawy HE, Azuma M, Embree LJ, Tsai H-J, Starost MF, Hickstein DD. TEL-AML1
transgenic zebrafish model of precursor B cell acute lymphoblastic leukemia.
Proc Natl Acad Sci 2006;103:15166–71.
5. Frazer JK, Meeker ND, Rudner L, Bradley DF, Smith ACH, Demarest B, et al.
Heritable T-cell malignancy models established in a zebrafish phenotypic screen.
Leukemia 2009;23:1825–35.
6. Chen J, Jette C, Kanki JP, Aster JC, Look AT, Griffin JD. NOTCH1-induced T-cell
leukemia in transgenic zebrafish. Leukemia 2007;21:462–71.
7. Smith ACH, Raimondi AR, Salthouse CD, Ignatius MS, Blackburn JS, Mizgirev I V,
et al. High-throughput cell transplantation establishes that tumor-initiating cells
are abundant in zebrafish T-cell acute lymphoblastic leukemia. Blood
2010;115:3296–303.
8. Tang Q, Abdelfattah NS, Blackburn JS, Moore JC. Optimized cell transplantation
S8
using adult rag2 mutant zebrafish. Nat Methods 2014;11:821–4.
9. Patton, E. Elizabeth, Windlund, Hans R, Kutok Jeffery L, Kopani KR. BRAF
Mutations Are Sufficient to Promote Nevi Formation and Cooperate with p53 in
the Genesis of Melanoma. Curr Biol 2005;15:249–54.
Supplementary Table S7. Xenograft assays performed in embryo zebrafish.
Cancer type Cell line Process studied (ref) Monitoring
Breast cancer
MDA-MB-231
Angiogenesis, drug testing (1)
Fluorescence imagingMetastasis, vascularization (2)
Dissemination (3)
MCF7Angiogenesis (4) Fluorescence imaging
Dissemination (5) Confocal imagingMDA-MB-23, M1, M2, M4
Metastasis (6)Confocal imaging, immunohistology
MDA-MB-23, MCF-7 Metastasis (7) Fluorescence imaging
Colon cancer
HCT116DLD-1
Drug screening (8) Fluorescence imaging
SW620HT29
Metastasis (9) Confocal imaging
Fibrosarcoma HT1080 Drug testing (10) Confocal imagingGastric cancer AGS, MGC80-3 Tumor growth (11) Fluorescencen imaging
GlioblastomaU87
Invasion (12)Confocal imaging, flow
citometryGrowth and invasion (13) Bioluminiscence
X12, GBM9 Proliferation (14) Confocal imagingHepatocarcinoma
JHH6Drug testing (15) Fluorescence imaging
Leukemia K562, NB4, Jukart Drug screening (16-18)ImmunofluorescenceFluorescence imaging
Confocal imaging
Lung cancerA549 Metastasis (19) Fluorescence imaging
H1299, H1437 Drug testing (20) Immunofluorescence
Melanoma
C8161 Dissemination (21) Confocal imagingA375 Tumor growth (22) Immunofluorescence
UACC62, 888mel, WM266-4, 501mel
Invasion (23) Confocal imaging
Mieloma MM.1S, BCWM.1, Dissemination (24) Fluorescence imaging
Ovarian cancer
A2780 Angiogenesis (25) Epifluorescence
OVOCAR 8Dissemination, metastasis
(3)Fluoresecence imaging
SKOV3 Drug testing (10) Confocal imagingPancreatic
cancerPANC-1,
PaTu8988TMetastasis, angiogénesis
(26)Confocal imaging
FA6, PaTu 8988s, Dissemination (27) Epifluorescence imaging
S9
CFPAC1, BxPC3AsPC-1, BxPC3 Metastasis (28) Confocal imaging
Prostate cancer
PC3Metastasis, vascularization
(2)Confocal imaging
DU145, PC3, LNCap, CWR22 PCa
Angiogenesis, tumor growth (29)
Fluorescence imaging
LnCAP, PC3 Dissemination (5) Confocal imaging
PC3, DU145 Adhesion (30) Fluorescence imaging
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3. Lee SLC, Rouhi P, Dahl Jensen L, Zhang D, Ji H, Hauptmann G, et al. Hypoxia-
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9. Haldi M, Ton C, Seng WL, McGrath P. Human melanoma cells transplanted into
zebrafish proliferate, migrate, produce melanin, form masses and stimulate
angiogenesis in zebrafish. Angiogenesis 2006;9:139–51.
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angiogenesis: synthesis and in vivo assessment of drug efficacy and
biocompatibility in zebrafish embryos. Int J Nanomedicine 2011;6:2007–21.
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for in vivo cancer study. Fam Cancer. 2015;14:487–93.
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Model for Study of Glioma Stem Cell Invasion. Ribatti D, editor. PLoS One
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14. Welker AM, Jaros BD, Puduvalli VK, Imitola J, Kaur B, Beattie CE. Standardized
orthotopic xenografts in zebrafish reveal glioma cell-line-specific characteristics
and tumor cell heterogeneity. Dis Model Mech 2016;9:199–210.
S11
15. Tonon F, Zennaro C, Dapas B, Carraro M, Mariotti M, Grassi G. Rapid and cost-
effective xenograft hepatocellular carcinoma model in Zebrafish for drug testing.
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therapeutic platform for T-cell acute lymphoblastic leukemia. Haematologica
2015;100:70–6.
17. Corkery DP, Dellaire G, Berman JN. Leukaemia xenotransplantation in zebrafish -
chemotherapy response assay in vivo. Br J Haematol 2011;153:786–9.
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Leukemic cell xenograft in zebrafish embryo for investigating drug efficacy.
Haematologica 2011;96:612–6.
19. Lara R, Mauri FA, Taylor H, Derua R, Shia A, Gray C, et al. An siRNA screen
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20. Chiu C, Chou H, Chen B, Chang K, Tseng C, Fong Y. BPIQ , a novel synthetic
quinoline derivative , inhibits growth and induces mitochondrial apoptosis of
lung cancer cells in vitro and in zebrafish xenograft model. BMC Cancer
2015;15:962.
21. Lee LMJ, Seftor EA, Bonde G, Cornell RA, Hendrix MJC. 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.
2005;233:1560–1570.
22. Zhao C, Zhang W, Zhao Y, Yang Y, Luo H, Ji G, et al. Endothelial Cords Promote
S12
Tumor Initial Growth prior to Vascular Function through a Paracrine Mechanism.
Sci Rep 2016;6:1–13.
23. Chapman A, del Ama LF, Ferguson J, Kamarashev J, Wellbrock C, Hurlstone A.
Heterogeneous tumor subpopulations cooperate to drive invasion. Cell Rep
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24. Sacco A, Roccaro AM, Ma D, Shi J, Mishima Y, Moschetta M, et al. Cancer Cell
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25. Nicoli S, Ribatti D, Cotelli F, Presta M. Mammalian Tumor Xenografts Induce
Neovascularization in Zebrafish Embryos. Cancer Res 2007;67:2927–31.
26. Vlecken DH, Bagowski CP. LIMK1 and LIMK2 Are Important for Metastatic
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Zebrafish 2009;6:433–9.
27. Dumartin L, Whiteman HJ, Weeks ME, Hariharan D, Dmitrovic B, Iacobuzio-
Donahue CA, et al. AGR2 is a novel surface antigen that promotes the
dissemination of pancreatic cancer cells through regulation of cathepsins B and
D. Cancer Res 2011;71:7091–102.
28. Teng Y, Xie X, Walker S, White DT, Mumm JS, Cowell JK. Evaluating human
cancer cell metastasis in zebrafish. BMC Cancer 2013;13:453.
29. Moshal KS, Ferri-Lagneau KF, Haider J, Pardhanani P, Leung T. Discriminating
Different Cancer Cells Using a Zebrafish in Vivo Assay. Cancers 2011;3:4102–13.
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Enrichment of human prostate cancer cells with tumor initiating properties in
mouse and zebrafish xenografts by differential adhesion. Prostate 2014;74:187–
S13
200.
Supplementary Table S8. Orthotopic transplantation in embryo zebrafish.
Tumor type Cell line (ref) Process studied Tumor monitoring
Glioblastoma
X12, GBM9 (1) ProliferationConfocal imaging,
HistologyU87MG, U251MG,
HT1080 (2)Proliferation Confocal imaging
U3013MG (3)Cell
interactionMicroscopy
U87, U373 (4)Invasion,
Cell interactionConfocal imaging
U87MG (5) Cell interaction Confocal imagingHuman tumor
cells isolated (6)Cell differentiation Confocal imaging
Pancreatic cancer
PaTu-S, PaTu-T (PaTu8988-S and PaTu8988-T) (7)
MetastasisConfocal imaging,
Inmunofluorescence
RetinoblastomaRB355, WERI-
Rb1(8)Invasiveness, metastasis Fluorescence imaging
SNUOT-Rb1 (9) Drug screening Confocal imaging
Uveal melanoma
92.1, Mel270, OMM2.3, OMM2.5,
OMM1 (10)
Proliferation,Migration,
Drug testingConfocal imaging
S14
References S8
1. Welker AM, Jaros BD, Puduvalli VK, Imitola J, Kaur B, Beattie CE. Standardized
orthotopic xenografts in zebrafish reveal glioma cell-line-specific characteristics
and tumor cell heterogeneity. Dis Model Mech 2016;9:199–210.
2. Hamilton L, Astell KR, Velikova G, Sieger D. A Zebrafish Live Imaging Model
Reveals Differential Responses of Microglia Toward Glioblastoma Cells In Vivo.
Zebrafish 2016;13:523–34.
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8. Chen X, Wang J, Cao Z, Hosaka K, Jensen L, Yang H, et al. Invasiveness and
metastasis of retinoblastoma in an orthotopic zebrafish tumor model. Sci Rep
2015;5:10351.
9. Jo DH, Son D, Na Y, Jang M, Choi JH, Kim JH, et al. Orthotopic transplantation of
retinoblastoma cells into vitreous cavity of zebrafish for screening of anticancer
drugs. Mol Cancer 2013;12:71.
10. van der Ent W, Burrello C, Teunisse AFAS, Ksander BR, van der Velden PA, Jager
MJ, et al. Modeling of Human Uveal Melanoma in Zebrafish Xenograft Embryos.
Investig Opthalmology Vis Sci 2014;55:6612–22.
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