In precision oncology, two major strategies are being pursued for predicting clinically relevant tumour behaviours, such as treatment response and emergence of drug resistance: inference based on genomic, transcriptomic, epigenomic and/or proteomic analysis of patient samples, and phenotypic assays in personalized cancer avatars. The latter approach has historically relied on in vivo mouse xenografts and in vitro organoids or 2D cell cultures. Recent progress in rapid combinatorial genetic modelling, the development of a genetically immunocompromised strain for xenotransplantation of human patient samples in adult zebrafish and the first clinical trial using xenotransplantation in zebrafish larvae for phenotypic testing of drug response bring this tiny vertebrate to the forefront of the precision medicine arena. In this Review, we discuss advances in transgenic and transplantation-based zebrafish cancer avatars, and how these models compare with and complement mouse xenografts and human organoids. We also outline the unique opportunities that these different models present for prediction studies and current challenges they face for future clinical deployment.
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L.I.Z. is supported by the Melanoma Research Alliance and US National Institutes of Health (grants P01CA163222 and R01 CA103846). M.F. was supported by Boehringer Ingelheim Fonds. D.M.L. is funded by the US National Institutes of Health (grants R01CA154923, R01CA211734, R01CA215118, R01CA226926 and R24OD016761) and the MGH Research Scholars Program. Y.C. is supported by the Alex Lemonade Stand Foundation.
L.I.Z. is a founder and stockholder of Fate Therapeutics Inc., Scholar Rock and Camp4 Therapeutics Inc., and is a scientific adviser for Stemgent. The other authors declare no competing interests.
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- One-cell stage
The zebrafish embryonic stage where the egg has been fertilized by sperm, but before the first cell division.
Benign skin lesions of melanocytes, also known as moles, which are thought to be senescent.
- Tol2 transposon
Tol2 is an active transposon derived from the medaka fish and is used as a gene delivery method.
- U6 promoter
An RNA polymerase III type 3 promoter commonly used to drive short hairpin RNAs or guide RNAs.
- Casper zebrafish strain
An optically clear strain of zebrafish obtained by crossing the roy (mpv17−/−) and nacre (mitfa−/−) mutants, which results in the lack of iridophores and melanocytes, respectively.
- NSG mice
Genetically engineered immunocompromised strain of mice widely used as recipients for engraftment of human primary cells or tumours (for example, patient-derived xenografts).
- RECIST criteria
A set of published rules that define when patients with cancer improve (‘respond’), stay the same (‘stable’) or worsen (‘progression’) during treatments.
- Hydrodynamic injection
Rapid injection of a relatively large volume of DNA solution, which is used for gene delivery in mouse livers.
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Fazio, M., Ablain, J., Chuan, Y. et al. Zebrafish patient avatars in cancer biology and precision cancer therapy. Nat Rev Cancer 20, 263–273 (2020). https://doi.org/10.1038/s41568-020-0252-3
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