Skip to main content
Top
Published in: Tumor Biology 12/2014

01-12-2014 | Research Article

Zebrafish xenotransplantation model for cancer stem-like cell study and high-throughput screening of inhibitors

Authors: Beibei Zhang, Yasuhito Shimada, Junya Kuroyanagi, Yuhei Nishimura, Noriko Umemoto, Tsuyoshi Nomoto, Taichi Shintou, Takeshi Miyazaki, Toshio Tanaka

Published in: Tumor Biology | Issue 12/2014

Login to get access

Abstract

Xenotransplantation studies are important tools for studying cancer biology, especially for assaying tumor cell malignancy and providing cancer information in vivo. Cancer stem-like cells (CSCs) have been identified in many cancer types to drive tumor growth and recurrence, from "keeping" to "keep" resistant to chemotherapy and radiation therapy. In this study, we developed the xenotransplantation of CSCs derived from the leukemia and solid tumor cell lines using the zebrafish models. In adult zebrafish, we investigated that the xenografted leukemia stem cells (LSCs) from K562 cells could proliferate in vivo and keep the cancer property by re-transplantation. As for the solid tumor, these CSCs from DU145 cells (human prostate cancer) and HepG2 cells (human liver cancer) could form the tumor mass and even metastasis after xenotransplantation. In addition, the zebrafish embryos with CSC xenotransplantation could evaluate docetaxel in vivo efficiently and be available to screen the novel inhibitors by high-throughput manner. In summary, these zebrafish xenotransplantation models devote a good platform for the CSC mechanism investigation and anti-CSC inhibitor screening.
Appendix
Available only for authorised users
Literature
1.
go back to reference Jordan CT. The leukemic stem cell. Best Pract Res Clin Haematol. 2007;20:13–8.CrossRef Jordan CT. The leukemic stem cell. Best Pract Res Clin Haematol. 2007;20:13–8.CrossRef
2.
go back to reference Bachovchin DA, Brown SJ, Rosen H, Cravatt BF. Identification of selective inhibitors of uncharacterized enzymes by high-throughput screening with fluorescent activity-based probes. Nat Biotechnol. 2009;27:387–94.CrossRef Bachovchin DA, Brown SJ, Rosen H, Cravatt BF. Identification of selective inhibitors of uncharacterized enzymes by high-throughput screening with fluorescent activity-based probes. Nat Biotechnol. 2009;27:387–94.CrossRef
3.
go back to reference Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003;100:3983–8.CrossRef Al-Hajj M, Wicha MS, Benito-Hernandez A, Morrison SJ, Clarke MF. Prospective identification of tumorigenic breast cancer cells. Proc Natl Acad Sci U S A. 2003;100:3983–8.CrossRef
4.
go back to reference Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756–60.CrossRef Bao S, Wu Q, McLendon RE, Hao Y, Shi Q, Hjelmeland AB, et al. Glioma stem cells promote radioresistance by preferential activation of the DNA damage response. Nature. 2006;444:756–60.CrossRef
5.
go back to reference Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell. 2007;1:555–67.CrossRef Ginestier C, Hur MH, Charafe-Jauffret E, Monville F, Dutcher J, Brown M, et al. ALDH1 is a marker of normal and malignant human mammary stem cells and a predictor of poor clinical outcome. Cell Stem Cell. 2007;1:555–67.CrossRef
6.
go back to reference Hellsten R, Johansson M, Dahlman A, Sterner O, Bjartell A. Galiellalactone inhibits stem cell-like ALDH-positive prostate cancer cells. PLoS ONE. 2011;6:e22118.CrossRef Hellsten R, Johansson M, Dahlman A, Sterner O, Bjartell A. Galiellalactone inhibits stem cell-like ALDH-positive prostate cancer cells. PLoS ONE. 2011;6:e22118.CrossRef
7.
8.
go back to reference Ma S, Chan KW, Lee TK, Tang KH, Wo JY, Zheng BJ, et al. Aldehyde dehydrogenase discriminates the CD133 liver cancer stem cell populations. Mol Cancer Res: MCR. 2008;6:1146–53.CrossRef Ma S, Chan KW, Lee TK, Tang KH, Wo JY, Zheng BJ, et al. Aldehyde dehydrogenase discriminates the CD133 liver cancer stem cell populations. Mol Cancer Res: MCR. 2008;6:1146–53.CrossRef
9.
go back to reference Taylor AM, Zon LI. Zebrafish tumor assays: the state of transplantation. Zebrafish. 2009;6:339–46.CrossRef Taylor AM, Zon LI. Zebrafish tumor assays: the state of transplantation. Zebrafish. 2009;6:339–46.CrossRef
10.
go back to reference Kruczynski A, Hill BT: Classic in vivo cancer models: three examples of mouse models used in experimental therapeutics. Curr Protoc Pharmacol. 2002. Chapter 5: Unit5. 24. Kruczynski A, Hill BT: Classic in vivo cancer models: three examples of mouse models used in experimental therapeutics. Curr Protoc Pharmacol. 2002. Chapter 5: Unit5. 24.
11.
go back to reference Goldsmith P. Zebrafish as a pharmacological tool: the how, why and when. Curr Opin Pharmacol. 2004;4:504–12.CrossRef Goldsmith P. Zebrafish as a pharmacological tool: the how, why and when. Curr Opin Pharmacol. 2004;4:504–12.CrossRef
12.
go back to reference Amatruda JF, Shepard JL, Stern HM, Zon LI. Zebrafish as a cancer model system. Cancer Cell. 2002;1:229–31.CrossRef Amatruda JF, Shepard JL, Stern HM, Zon LI. Zebrafish as a cancer model system. Cancer Cell. 2002;1:229–31.CrossRef
13.
go back to reference Yang XJ, Cui W, Gu A, Xu C, Yu SC, Li TT, et al. A novel zebrafish xenotransplantation model for study of glioma stem cell invasion. PLoS ONE. 2013;8:e61801.CrossRef Yang XJ, Cui W, Gu A, Xu C, Yu SC, Li TT, et al. A novel zebrafish xenotransplantation model for study of glioma stem cell invasion. PLoS ONE. 2013;8:e61801.CrossRef
14.
go back to reference Zhang B, Shimada Y, Kuroyanagi J, Umemoto N, Nishimura Y, Tanaka T. Quantitative phenotyping-based in vivo chemical screening in a zebrafish model of leukemia stem cell xenotransplantation. PLoS ONE. 2014;9:e85439.CrossRef Zhang B, Shimada Y, Kuroyanagi J, Umemoto N, Nishimura Y, Tanaka T. Quantitative phenotyping-based in vivo chemical screening in a zebrafish model of leukemia stem cell xenotransplantation. PLoS ONE. 2014;9:e85439.CrossRef
15.
go back to reference White RM, Sessa A, Burke C, Bowman T, LeBlanc J, Ceol C, et al. Transparent adult zebrafish as a tool for in vivo transplantation analysis. Cell Stem Cell. 2008;2:183–9.CrossRef White RM, Sessa A, Burke C, Bowman T, LeBlanc J, Ceol C, et al. Transparent adult zebrafish as a tool for in vivo transplantation analysis. Cell Stem Cell. 2008;2:183–9.CrossRef
16.
go back to reference Peal DS, Peterson RT, Milan D. Small molecule screening in zebrafish. J Cardiovasc Transl Res. 2010;3:454–60.CrossRef Peal DS, Peterson RT, Milan D. Small molecule screening in zebrafish. J Cardiovasc Transl Res. 2010;3:454–60.CrossRef
17.
go back to reference Nicoli S, Ribatti D, Cotelli F, Presta M. Mammalian tumor xenografts induce neovascularization in zebrafish embryos. Cancer Res. 2007;67:2927–31.CrossRef Nicoli S, Ribatti D, Cotelli F, Presta M. Mammalian tumor xenografts induce neovascularization in zebrafish embryos. Cancer Res. 2007;67:2927–31.CrossRef
18.
go back to reference Marques IJ, Weiss FU, Vlecken DH, Nitsche C, Bakkers J, Lagendijk AK, et al. Metastatic behaviour of primary human tumours in a zebrafish xenotransplantation model. BMC Cancer. 2009;9:128.CrossRef Marques IJ, Weiss FU, Vlecken DH, Nitsche C, Bakkers J, Lagendijk AK, et al. Metastatic behaviour of primary human tumours in a zebrafish xenotransplantation model. BMC Cancer. 2009;9:128.CrossRef
19.
go back to reference Dovey MC, Zon LI. Defining cancer stem cells by xenotransplantation in zebrafish. Methods Mol Biol. 2009;568:1–5.CrossRef Dovey MC, Zon LI. Defining cancer stem cells by xenotransplantation in zebrafish. Methods Mol Biol. 2009;568:1–5.CrossRef
20.
go back to reference Ignatius MS, Langenau DM. Zebrafish as a model for cancer self-renewal. Zebrafish. 2009;6:377–87.CrossRef Ignatius MS, Langenau DM. Zebrafish as a model for cancer self-renewal. Zebrafish. 2009;6:377–87.CrossRef
21.
go back to reference Yang IH, Lee D, Lee SH, Kang JY. Characterization of proteolytically digested zebrafish chorion as extracellular matrix. Conf Proc: IEEE Eng Med Biol Soc. 2008;2008:1837–40. Yang IH, Lee D, Lee SH, Kang JY. Characterization of proteolytically digested zebrafish chorion as extracellular matrix. Conf Proc: IEEE Eng Med Biol Soc. 2008;2008:1837–40.
22.
go back to reference Zang L, Shimada Y, Nishimura Y, Tanaka T, Nishimura N. A novel, reliable method for repeated blood collection from aquarium fish. Zebrafish. 2013;10:425–32.CrossRef Zang L, Shimada Y, Nishimura Y, Tanaka T, Nishimura N. A novel, reliable method for repeated blood collection from aquarium fish. Zebrafish. 2013;10:425–32.CrossRef
23.
go back to reference Eguiara A, Holgado O, Beloqui I, Abalde L, Sanchez Y, Callol C, et al. Xenografts in zebrafish embryos as a rapid functional assay for breast cancer stem-like cell identification. Cell Cycle. 2011;10:3751–7.CrossRef Eguiara A, Holgado O, Beloqui I, Abalde L, Sanchez Y, Callol C, et al. Xenografts in zebrafish embryos as a rapid functional assay for breast cancer stem-like cell identification. Cell Cycle. 2011;10:3751–7.CrossRef
24.
go back to reference Rohena CC, Mooberry SL. Recent progress with microtubule stabilizers: new compounds, binding modes and cellular activities. Nat Prod Rep. 2014;31:335–55.CrossRef Rohena CC, Mooberry SL. Recent progress with microtubule stabilizers: new compounds, binding modes and cellular activities. Nat Prod Rep. 2014;31:335–55.CrossRef
25.
go back to reference Lee C, Wu SS, Chen LB. Photosensitization by 3,3ʹ-dihexyloxacarbocyanine iodide: specific disruption of microtubules and inactivation of organelle motility. Cancer Res. 1995;55:2063–9.PubMed Lee C, Wu SS, Chen LB. Photosensitization by 3,3ʹ-dihexyloxacarbocyanine iodide: specific disruption of microtubules and inactivation of organelle motility. Cancer Res. 1995;55:2063–9.PubMed
26.
go back to reference Rowinsky EK, Onetto N, Canetta RM, Arbuck SG. Taxol: the first of the taxanes, an important new class of antitumor agents. Semin Oncol. 1992;19:646–62.PubMed Rowinsky EK, Onetto N, Canetta RM, Arbuck SG. Taxol: the first of the taxanes, an important new class of antitumor agents. Semin Oncol. 1992;19:646–62.PubMed
27.
go back to reference Arbuck SG, Christian MC, Fisherman JS, Cazenave LA, Sarosy G, Suffness M, et al. Clinical development of taxol. J Natl Cancer Inst Monogr. 1993;15:11–24. Arbuck SG, Christian MC, Fisherman JS, Cazenave LA, Sarosy G, Suffness M, et al. Clinical development of taxol. J Natl Cancer Inst Monogr. 1993;15:11–24.
28.
go back to reference Foa R, Norton L, Seidman AD. Taxol (paclitaxel): a novel anti-microtubule agent with remarkable anti-neoplastic activity. Int J Clin Lab Res. 1994;24:6–14.CrossRef Foa R, Norton L, Seidman AD. Taxol (paclitaxel): a novel anti-microtubule agent with remarkable anti-neoplastic activity. Int J Clin Lab Res. 1994;24:6–14.CrossRef
29.
go back to reference Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature. 2009;458:780–3.CrossRef Diehn M, Cho RW, Lobo NA, Kalisky T, Dorie MJ, Kulp AN, et al. Association of reactive oxygen species levels and radioresistance in cancer stem cells. Nature. 2009;458:780–3.CrossRef
30.
go back to reference Rudin CM, Salgia R, Wang X, Hodgson LD, Masters GA, Green M, et al. Randomized phase II study of carboplatin and etoposide with or without the bcl-2 antisense oligonucleotide oblimersen for extensive-stage small-cell lung cancer: CALGB 30103. J Clin Oncol: Off J Am Soc Clin Oncol. 2008;26:870–6.CrossRef Rudin CM, Salgia R, Wang X, Hodgson LD, Masters GA, Green M, et al. Randomized phase II study of carboplatin and etoposide with or without the bcl-2 antisense oligonucleotide oblimersen for extensive-stage small-cell lung cancer: CALGB 30103. J Clin Oncol: Off J Am Soc Clin Oncol. 2008;26:870–6.CrossRef
31.
go back to reference Fulda S, Galluzzi L, Kroemer G. Targeting mitochondria for cancer therapy. Nat Rev Drug Discov. 2010;9:447–64.CrossRef Fulda S, Galluzzi L, Kroemer G. Targeting mitochondria for cancer therapy. Nat Rev Drug Discov. 2010;9:447–64.CrossRef
32.
go back to reference 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.CrossRef 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.CrossRef
33.
go back to reference Traver D, Herbomel P, Patton EE, Murphey RD, Yoder JA, Litman GW, et al. The zebrafish as a model organism to study development of the immune system. Adv Immunol. 2003;81:253–330.PubMed Traver D, Herbomel P, Patton EE, Murphey RD, Yoder JA, Litman GW, et al. The zebrafish as a model organism to study development of the immune system. Adv Immunol. 2003;81:253–330.PubMed
34.
go back to reference Traver D, Paw BH, Poss KD, Penberthy WT, Lin S, Zon LI. Transplantation and in vivo imaging of multilineage engraftment in zebrafish bloodless mutants. Nat Immunol. 2003;4:1238–46.CrossRef Traver D, Paw BH, Poss KD, Penberthy WT, Lin S, Zon LI. Transplantation and in vivo imaging of multilineage engraftment in zebrafish bloodless mutants. Nat Immunol. 2003;4:1238–46.CrossRef
35.
go back to reference Pichler FB, Laurenson S, Williams LC, Dodd A, Copp BR, Love DR. Chemical discovery and global gene expression analysis in zebrafish. Nat Biotechnol. 2003;21:879–83.CrossRef Pichler FB, Laurenson S, Williams LC, Dodd A, Copp BR, Love DR. Chemical discovery and global gene expression analysis in zebrafish. Nat Biotechnol. 2003;21:879–83.CrossRef
Metadata
Title
Zebrafish xenotransplantation model for cancer stem-like cell study and high-throughput screening of inhibitors
Authors
Beibei Zhang
Yasuhito Shimada
Junya Kuroyanagi
Yuhei Nishimura
Noriko Umemoto
Tsuyoshi Nomoto
Taichi Shintou
Takeshi Miyazaki
Toshio Tanaka
Publication date
01-12-2014
Publisher
Springer Netherlands
Published in
Tumor Biology / Issue 12/2014
Print ISSN: 1010-4283
Electronic ISSN: 1423-0380
DOI
https://doi.org/10.1007/s13277-014-2417-8

Other articles of this Issue 12/2014

Tumor Biology 12/2014 Go to the issue
Webinar | 19-02-2024 | 17:30 (CET)

Keynote webinar | Spotlight on antibody–drug conjugates in cancer

Antibody–drug conjugates (ADCs) are novel agents that have shown promise across multiple tumor types. Explore the current landscape of ADCs in breast and lung cancer with our experts, and gain insights into the mechanism of action, key clinical trials data, existing challenges, and future directions.

Dr. Véronique Diéras
Prof. Fabrice Barlesi
Developed by: Springer Medicine