Developmental and Comparative Immunology 46 (2014) 1–2
Contents lists available at ScienceDirect
Developmental and Comparative Immunology journal homepage: www.elsevier.com/locate/dci
Preface
Preface to the Special Issue: Zebrafish immunity and infection models The zebrafish (Danio rerio) has arisen over the past three decades as a valuable genetic model system with a number of unique experimental advantages over other existing vertebrate models. The most significant of these advantages was the development of mutagenesis and genetic analyses methods by George Streisinger and colleagues (Chakrabarti et al., 1983; Streisinger et al., 1981; Streisinger, 1983; Walker and Streisinger, 1983). The subsequent dedication of an entire issue of Development to describe the thousands of mutant zebrafish phenotypes identified by large scale mutagenesis screens in the laboratories of Christiane Nüsslein-Volhard and Wolfgang Driever established the zebrafish as a highly feasible genetic model for developmental deformity and congenital diseases (Driever et al., 1996; Haffter et al., 1996). The need to identify and map candidate genes then led to the development of a solid repertoire of genomic resources for zebrafish including genomic libraries, radiation hybrid panels and, most recently, the sequencing of a reference genome by the Wellcome Trust Sanger Institute (Amemiya and Zon, 1999; Geisler et al., 1999; Howe et al., 2013; Hukriede et al., 1999), which now provides researchers with a rich resource for identifying orthologous genes in other species, as well as for identifying genes that are unique to bony fish. The utility of zebrafish as a genetic model increased further with the report that anti-sense morpholino oligonucleotides can effectively and specifically (albeit transiently) inhibit protein production from target genes in the developing zebrafish embryo (Nasevicius and Ekker, 2000). These powerful tools have been successfully used for more than a decade to confirm that the dysregulation of specific candidate genes indeed accounts for phenotypes discovered in earlier mutagenesis screens, as well as for studies on genes with unknown function and for developing models for human genetic diseases. Although morpholino oligonucleotides have thus become the ‘‘gold standard’’ for targeted gene disruption in the zebrafish embryo, recent advances in genome editing in zebrafish via ZFNS, TALENs, and CRISPR/Cas9 now permit the efficient generation of targeted gene disruptions (e.g. gene knock-outs) (Cade et al., 2012; Hwang et al., 2013), and the application of templated DNA repair to these genome editing systems promises to soon make precise gene modifications, including ‘‘designer’’ alleles and conditional knock-outs, a reality in the zebrafish model (Bedell et al., 2012; Zu et al., 2013). It also may be feasible to employ these technologies to delete an entire gene or cluster of genes from the zebrafish genome, a potentially powerful approach to address issues of functional redundancy within clusters of diversified gene families. While all of these genetic and genomic resources were being developed, many labs were beginning to employ the zebrafish as a model for cellular immunity and infectious disease. The transparent nature of zebrafish embryos makes them an ideal system for http://dx.doi.org/10.1016/j.dci.2014.04.007 0145-305X/Ó 2014 Elsevier Ltd. All rights reserved.
tracking the migration and differentiation of different hemaopoietic lineages, as well as observing host-pathogen interactions, in vivo. In 1999, Philippe Herbomel, Bernard Thisse and Christine Thisse published one of the first reports demonstrating the utility of employing DIC video microscopy to visualize the migration and differentiation of macrophage precursors, macrophage chemotaxis and phagocytosis, as well as the real time response to infection, within the context of live transparent zebrafish embryos (Herbomel et al., 1999). More recently, the identification of numerous immune cell lineage-specific promoter regions facilitated the generation of transgenic zebrafish lines in which different hematopoietic lineages express a fluorescent protein; partnering these transgenic lines with fluorescent microscopy and/or cell sorting provides a powerful means to visually differentiate and isolate different immune cell lineages (reviewed by Renshaw and Trede, 2012). Finally, combining these fluorescent reporter lines with pathogens expressing a complementary fluorescent protein has enabled experiments designed to elucidate in vivo host-pathogen interactions in real time. In this Special Issue of Developmental and Comparative Immunology, review articles are presented on three themes: immune genes, immune cells and infection models. Five reviews present the current knowledge on a large number of immune-related genes, including those encoding proteins of the complement system (Zhang and Cui), mediators of the Toll-like receptor signaling pathways (Kanwal and colleagues), mediators of the IL-1 processing and signaling network (Ogryzko and colleagues), three distinct MHC class I lineages (Dirscherl and colleagues) and multi-gene families of additional innate immune receptors (Rodriguez-Nunez and colleagues). Two reviews bring us up to date on the use of zebrafish to model mast cell biology (Prykhozhij and Berman) and on antigen-presenting cells in zebrafish (Lewis and colleagues). Three reviews discuss the application of zebrafish to study zoonotic pathogens (Rowe and colleagues), viral infections (Goody and colleagues), and eukaryotic pathogens (Gratacap and Wheeler). It has been a pleasure working with the authors in this Special Issue whose reviews provide great insight into the current knowledge-base of zebrafish immunity and infection models as well as the similarities and differences between zebrafish, human and other bony fish. It is likely that the work described here will serve as the primary roadmap over the next decade for investigations of the immunity of infections in this powerful model system. References Amemiya, C.T., Zon, L.I., 1999. Generation of a zebrafish P1 artificial chromosome library. Genomics 58, 211–213. Bedell, V.M., Wang, Y., Campbell, J.M., Poshusta, T.L., Starker, C.G., Krug, R.G., Tan, W., Penheiter, S.G., Ma, A.C., Leung, A.Y., Fahrenkrug, S.C., Carlson, D.F., Voytas,
2
Preface / Developmental and Comparative Immunology 46 (2014) 1–2
D.F., Clark, K.J., Essner, J.J., Ekker, S.C., . In vivo genome editing using a highefficiency TALEN system. Nature 491, 114–118. Cade, L., Reyon, D., Hwang, W.Y., Tsai, S.Q., Patel, S., Khayter, C., Joung, J.K., Sander, J.D., Peterson, R.T., Yeh, J.R., 2012. Highly efficient generation of heritable zebrafish gene mutations using homo- and heterodimeric TALENs. Nucleic Acids Res. 40, 8001–8010. Chakrabarti, S., Streisinger, G., Singer, F., Walker, C., 1983. Frequency of gamma-ray induced specific locus and recessive lethal mutations in mature germ cells of the zebrafish, Brachydanio rerio. Genetics 103, 109–123. Driever, W., Solnica-Krezel, L., Schier, A.F., Neuhauss, S.C., Malicki, J., Stemple, D.L., Stainier, D.Y., Zwartkruis, F., Abdelilah, S., Rangini, Z., Belak, J., Boggs, C., 1996. A genetic screen for mutations affecting embryogenesis in zebrafish. Development 123, 37–46. Geisler, R., Rauch, G.-J., Baier, H., van Beber, F., Bross, L., Dekens, M.P.S., Finger, K., Fricke, C., Gates, M.A., Geiger, H., Geiger-Rudolph, S., Gilmour, D., Glaser, S., Gnugge, L., Habeck, H., Hingst, K., Holley, S., Keenan, J., Kirn, A., Knaut, H., Lashkari, D., Maderspacher, F., Martyn, U., Neuhauss, S., Neumann, C., Nicolson, T., Pelegri, F., Ray, R., Rick, J.M., Roehl, H., Roeser, T., Schauerte, H.E., Schier, A.F., Schonberger, U., Schonthaler, H.-B., Schulte-Merker, S., Seydler, C., Talbot, W.S., Weiler, C., Nusslein-Volard, C., Haffter, P., 1999. A radiation hybrid map of the zebrafish genome. Nat. Genet. 23, 86–89. Haffter, P., Granato, M., Brand, M., Mullins, M.C., Hammerschmidt, M., Kane, D.A., Odenthal, J., van Eeden, F.J., Jiang, Y.J., Heisenberg, C.P., Kelsh, R.N., FurutaniSeiki, M., Vogelsang, E., Beuchele, D., Schach, U., Fabian, C., Nusslein-Volhard, C., 1996. The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development 123, 1–36. Herbomel, P., Thisse, B., Thisse, C., 1999. Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 126, 3735–3745. Howe, K., Clark, M.D., Torroja, C.F., Torrance, J., Berthelot, C., Muffato, M., Collins, J.E., Humphray, S., McLaren, K., Matthews, L., McLaren, S., Sealy, I., Caccamo, M., Churcher, C., Scott, C., Barrett, J.C., Koch, R., Rauch, G.J., White, S., Chow, W., Kilian, B., Quintais, L.T., Guerra-Assuncao, J.A., Zhou, Y., Gu, Y., Yen, J., Vogel, J.H., Eyre, T., Redmond, S., Banerjee, R., Chi, J., Fu, B., Langley, E., Maguire, S.F., Laird, G.K., Lloyd, D., Kenyon, E., Donaldson, S., Sehra, H., Almeida-King, J., Loveland, J., Trevanion, S., Jones, M., Quail, M., Willey, D., Hunt, A., Burton, J., Sims, S., McLay, K., Plumb, B., Davis, J., Clee, C., Oliver, K., Clark, R., Riddle, C., Eliott, D., Threadgold, G., Harden, G., Ware, D., Mortimer, B., Kerry, G., Heath, P., Phillimore, B., Tracey, A., Corby, N., Dunn, M., Johnson, C., Wood, J., Clark, S., Pelan, S., Griffiths, G., Smith, M., Glithero, R., Howden, P., Barker, N., Stevens, C., Harley, J., Holt, K., Panagiotidis, G., Lovell, J., Beasley, H., Henderson, C., Gordon, D., Auger, K., Wright, D., Collins, J., Raisen, C., Dyer, L., Leung, K., Robertson, L., Ambridge, K., Leongamornlert, D., McGuire, S., Gilderthorp, R., Griffiths, C., Manthravadi, D., Nichol, S., Barker, G., Whitehead, S., Kay, M., Brown, J.,
Murnane, C., Gray, E., Humphries, M., Sycamore, N., Barker, D., Saunders, D., Wallis, J., Babbage, A., Hammond, S., Mashreghi-Mohammadi, M., Barr, L., Martin, S., Wray, P., Ellington, A., Matthews, N., Ellwood, M., Woodmansey, R., Clark, G., Cooper, J., Tromans, A., Grafham, D., Skuce, C., Pandian, R., Andrews, R., Harrison, E., Kimberley, A., Garnett, J., Fosker, N., Hall, R., Garner, P., Kelly, D., Bird, C., Palmer, S., Gehring, I., Berger, A., Dooley, C.M., Ersan-Urun, Z., Eser, C., Geiger, H., Geisler, M., Karotki, L., Kirn, A., Konantz, J., Konantz, M., Oberlander, M., Rudolph-Geiger, S., Teucke, M., Osoegawa, K., Zhu, B., Rapp, A., Widaa, S., Langford, C., Yang, F., Carter, N.P., Harrow, J., Ning, Z., Herrero, J., Searle, S.M., Enright, A., Geisler, R., Plasterk, R.H., Lee, C., Westerfield, M., de Jong, P.J., Zon, L.I., Postlethwait, J.H., Nusslein-Volhard, C., Hubbard, T.J., Roest, C.H., Rogers, J., Stemple, D.L., 2013. The zebrafish reference genome sequence and its relationship to the human genome. Nature 496, 498–503. Hukriede, N.A., Joly, L., Tsang, M., Miles, J., Tellis, P., Epstein, J.A., Barbazuk, W.B., Li, F.N., Paw, B., Postlethwait, J.H., Hudson, T.J., Zon, L.I., McPherson, J.D., Chevrette, M., Dawid, I.B., Johnson, S.L., Ekker, M., 1999. Radiation hybrid mapping of the zebrafish genome. Proc. Natl. Acad. Sci. USA 96, 9745–9750. Hwang, W.Y., Fu, Y., Reyon, D., Maeder, M.L., Tsai, S.Q., Sander, J.D., Peterson, R.T., Yeh, J.R., Joung, J.K., 2013. Efficient genome editing in zebrafish using a CRISPRCas system. Nat. Biotechnol. 31, 227–229. Nasevicius, A., Ekker, S.C., 2000. Effective targeted gene ‘knockdown’ in zebrafish. Nat. Genet. 26, 216–220. Renshaw, S.A., Trede, N.S., 2012. A model 450 million years in the making: zebrafish and vertebrate immunity. Dis. Model. Mech. 5, 38–47. Streisinger, G., 1983. Extrapolations from species to species and from various cell types in assessing risks from chemical mutagens. Mutat. Res. 114, 93–105. Streisinger, G., Walker, C., Dower, N., Knauber, D., Singer, F., 1981. Production of clones of homozygous diploid zebra fish (Brachydanio rerio). Nature 291, 293– 296. Walker, C., Streisinger, G., 1983. Induction of mutations by gamma-rays in pregonial germ cells of zebrafish embryos. Genetics 103, 125–136. Zu, Y., Tong, X., Wang, Z., Liu, D., Pan, R., Li, Z., Hu, Y., Luo, Z., Huang, P., Wu, Q., Zhu, Z., Zhang, B., Lin, S., 2013. TALEN-mediated precise genome modification by homologous recombination in zebrafish. Nat. Methods 10, 329–331.
⇑
Jeffrey A. Yoder Department of Molecular Biomedical Sciences, North Carolina State University, 1060 William Moore Drive, Raleigh, NC 27607, USA ⇑ Tel.: +1 919 515 7406; fax: +1 919 513 7301. E-mail address: [email protected] Available online 18 April 2014
Contents lists available at ScienceDirect
Developmental and Comparative Immunology journal homepage: www.elsevier.com/locate/dci
Preface
Preface to the Special Issue: Zebrafish immunity and infection models The zebrafish (Danio rerio) has arisen over the past three decades as a valuable genetic model system with a number of unique experimental advantages over other existing vertebrate models. The most significant of these advantages was the development of mutagenesis and genetic analyses methods by George Streisinger and colleagues (Chakrabarti et al., 1983; Streisinger et al., 1981; Streisinger, 1983; Walker and Streisinger, 1983). The subsequent dedication of an entire issue of Development to describe the thousands of mutant zebrafish phenotypes identified by large scale mutagenesis screens in the laboratories of Christiane Nüsslein-Volhard and Wolfgang Driever established the zebrafish as a highly feasible genetic model for developmental deformity and congenital diseases (Driever et al., 1996; Haffter et al., 1996). The need to identify and map candidate genes then led to the development of a solid repertoire of genomic resources for zebrafish including genomic libraries, radiation hybrid panels and, most recently, the sequencing of a reference genome by the Wellcome Trust Sanger Institute (Amemiya and Zon, 1999; Geisler et al., 1999; Howe et al., 2013; Hukriede et al., 1999), which now provides researchers with a rich resource for identifying orthologous genes in other species, as well as for identifying genes that are unique to bony fish. The utility of zebrafish as a genetic model increased further with the report that anti-sense morpholino oligonucleotides can effectively and specifically (albeit transiently) inhibit protein production from target genes in the developing zebrafish embryo (Nasevicius and Ekker, 2000). These powerful tools have been successfully used for more than a decade to confirm that the dysregulation of specific candidate genes indeed accounts for phenotypes discovered in earlier mutagenesis screens, as well as for studies on genes with unknown function and for developing models for human genetic diseases. Although morpholino oligonucleotides have thus become the ‘‘gold standard’’ for targeted gene disruption in the zebrafish embryo, recent advances in genome editing in zebrafish via ZFNS, TALENs, and CRISPR/Cas9 now permit the efficient generation of targeted gene disruptions (e.g. gene knock-outs) (Cade et al., 2012; Hwang et al., 2013), and the application of templated DNA repair to these genome editing systems promises to soon make precise gene modifications, including ‘‘designer’’ alleles and conditional knock-outs, a reality in the zebrafish model (Bedell et al., 2012; Zu et al., 2013). It also may be feasible to employ these technologies to delete an entire gene or cluster of genes from the zebrafish genome, a potentially powerful approach to address issues of functional redundancy within clusters of diversified gene families. While all of these genetic and genomic resources were being developed, many labs were beginning to employ the zebrafish as a model for cellular immunity and infectious disease. The transparent nature of zebrafish embryos makes them an ideal system for http://dx.doi.org/10.1016/j.dci.2014.04.007 0145-305X/Ó 2014 Elsevier Ltd. All rights reserved.
tracking the migration and differentiation of different hemaopoietic lineages, as well as observing host-pathogen interactions, in vivo. In 1999, Philippe Herbomel, Bernard Thisse and Christine Thisse published one of the first reports demonstrating the utility of employing DIC video microscopy to visualize the migration and differentiation of macrophage precursors, macrophage chemotaxis and phagocytosis, as well as the real time response to infection, within the context of live transparent zebrafish embryos (Herbomel et al., 1999). More recently, the identification of numerous immune cell lineage-specific promoter regions facilitated the generation of transgenic zebrafish lines in which different hematopoietic lineages express a fluorescent protein; partnering these transgenic lines with fluorescent microscopy and/or cell sorting provides a powerful means to visually differentiate and isolate different immune cell lineages (reviewed by Renshaw and Trede, 2012). Finally, combining these fluorescent reporter lines with pathogens expressing a complementary fluorescent protein has enabled experiments designed to elucidate in vivo host-pathogen interactions in real time. In this Special Issue of Developmental and Comparative Immunology, review articles are presented on three themes: immune genes, immune cells and infection models. Five reviews present the current knowledge on a large number of immune-related genes, including those encoding proteins of the complement system (Zhang and Cui), mediators of the Toll-like receptor signaling pathways (Kanwal and colleagues), mediators of the IL-1 processing and signaling network (Ogryzko and colleagues), three distinct MHC class I lineages (Dirscherl and colleagues) and multi-gene families of additional innate immune receptors (Rodriguez-Nunez and colleagues). Two reviews bring us up to date on the use of zebrafish to model mast cell biology (Prykhozhij and Berman) and on antigen-presenting cells in zebrafish (Lewis and colleagues). Three reviews discuss the application of zebrafish to study zoonotic pathogens (Rowe and colleagues), viral infections (Goody and colleagues), and eukaryotic pathogens (Gratacap and Wheeler). It has been a pleasure working with the authors in this Special Issue whose reviews provide great insight into the current knowledge-base of zebrafish immunity and infection models as well as the similarities and differences between zebrafish, human and other bony fish. It is likely that the work described here will serve as the primary roadmap over the next decade for investigations of the immunity of infections in this powerful model system. References Amemiya, C.T., Zon, L.I., 1999. Generation of a zebrafish P1 artificial chromosome library. Genomics 58, 211–213. Bedell, V.M., Wang, Y., Campbell, J.M., Poshusta, T.L., Starker, C.G., Krug, R.G., Tan, W., Penheiter, S.G., Ma, A.C., Leung, A.Y., Fahrenkrug, S.C., Carlson, D.F., Voytas,
2
Preface / Developmental and Comparative Immunology 46 (2014) 1–2
D.F., Clark, K.J., Essner, J.J., Ekker, S.C., . In vivo genome editing using a highefficiency TALEN system. Nature 491, 114–118. Cade, L., Reyon, D., Hwang, W.Y., Tsai, S.Q., Patel, S., Khayter, C., Joung, J.K., Sander, J.D., Peterson, R.T., Yeh, J.R., 2012. Highly efficient generation of heritable zebrafish gene mutations using homo- and heterodimeric TALENs. Nucleic Acids Res. 40, 8001–8010. Chakrabarti, S., Streisinger, G., Singer, F., Walker, C., 1983. Frequency of gamma-ray induced specific locus and recessive lethal mutations in mature germ cells of the zebrafish, Brachydanio rerio. Genetics 103, 109–123. Driever, W., Solnica-Krezel, L., Schier, A.F., Neuhauss, S.C., Malicki, J., Stemple, D.L., Stainier, D.Y., Zwartkruis, F., Abdelilah, S., Rangini, Z., Belak, J., Boggs, C., 1996. A genetic screen for mutations affecting embryogenesis in zebrafish. Development 123, 37–46. Geisler, R., Rauch, G.-J., Baier, H., van Beber, F., Bross, L., Dekens, M.P.S., Finger, K., Fricke, C., Gates, M.A., Geiger, H., Geiger-Rudolph, S., Gilmour, D., Glaser, S., Gnugge, L., Habeck, H., Hingst, K., Holley, S., Keenan, J., Kirn, A., Knaut, H., Lashkari, D., Maderspacher, F., Martyn, U., Neuhauss, S., Neumann, C., Nicolson, T., Pelegri, F., Ray, R., Rick, J.M., Roehl, H., Roeser, T., Schauerte, H.E., Schier, A.F., Schonberger, U., Schonthaler, H.-B., Schulte-Merker, S., Seydler, C., Talbot, W.S., Weiler, C., Nusslein-Volard, C., Haffter, P., 1999. A radiation hybrid map of the zebrafish genome. Nat. Genet. 23, 86–89. Haffter, P., Granato, M., Brand, M., Mullins, M.C., Hammerschmidt, M., Kane, D.A., Odenthal, J., van Eeden, F.J., Jiang, Y.J., Heisenberg, C.P., Kelsh, R.N., FurutaniSeiki, M., Vogelsang, E., Beuchele, D., Schach, U., Fabian, C., Nusslein-Volhard, C., 1996. The identification of genes with unique and essential functions in the development of the zebrafish, Danio rerio. Development 123, 1–36. Herbomel, P., Thisse, B., Thisse, C., 1999. Ontogeny and behaviour of early macrophages in the zebrafish embryo. Development 126, 3735–3745. Howe, K., Clark, M.D., Torroja, C.F., Torrance, J., Berthelot, C., Muffato, M., Collins, J.E., Humphray, S., McLaren, K., Matthews, L., McLaren, S., Sealy, I., Caccamo, M., Churcher, C., Scott, C., Barrett, J.C., Koch, R., Rauch, G.J., White, S., Chow, W., Kilian, B., Quintais, L.T., Guerra-Assuncao, J.A., Zhou, Y., Gu, Y., Yen, J., Vogel, J.H., Eyre, T., Redmond, S., Banerjee, R., Chi, J., Fu, B., Langley, E., Maguire, S.F., Laird, G.K., Lloyd, D., Kenyon, E., Donaldson, S., Sehra, H., Almeida-King, J., Loveland, J., Trevanion, S., Jones, M., Quail, M., Willey, D., Hunt, A., Burton, J., Sims, S., McLay, K., Plumb, B., Davis, J., Clee, C., Oliver, K., Clark, R., Riddle, C., Eliott, D., Threadgold, G., Harden, G., Ware, D., Mortimer, B., Kerry, G., Heath, P., Phillimore, B., Tracey, A., Corby, N., Dunn, M., Johnson, C., Wood, J., Clark, S., Pelan, S., Griffiths, G., Smith, M., Glithero, R., Howden, P., Barker, N., Stevens, C., Harley, J., Holt, K., Panagiotidis, G., Lovell, J., Beasley, H., Henderson, C., Gordon, D., Auger, K., Wright, D., Collins, J., Raisen, C., Dyer, L., Leung, K., Robertson, L., Ambridge, K., Leongamornlert, D., McGuire, S., Gilderthorp, R., Griffiths, C., Manthravadi, D., Nichol, S., Barker, G., Whitehead, S., Kay, M., Brown, J.,
Murnane, C., Gray, E., Humphries, M., Sycamore, N., Barker, D., Saunders, D., Wallis, J., Babbage, A., Hammond, S., Mashreghi-Mohammadi, M., Barr, L., Martin, S., Wray, P., Ellington, A., Matthews, N., Ellwood, M., Woodmansey, R., Clark, G., Cooper, J., Tromans, A., Grafham, D., Skuce, C., Pandian, R., Andrews, R., Harrison, E., Kimberley, A., Garnett, J., Fosker, N., Hall, R., Garner, P., Kelly, D., Bird, C., Palmer, S., Gehring, I., Berger, A., Dooley, C.M., Ersan-Urun, Z., Eser, C., Geiger, H., Geisler, M., Karotki, L., Kirn, A., Konantz, J., Konantz, M., Oberlander, M., Rudolph-Geiger, S., Teucke, M., Osoegawa, K., Zhu, B., Rapp, A., Widaa, S., Langford, C., Yang, F., Carter, N.P., Harrow, J., Ning, Z., Herrero, J., Searle, S.M., Enright, A., Geisler, R., Plasterk, R.H., Lee, C., Westerfield, M., de Jong, P.J., Zon, L.I., Postlethwait, J.H., Nusslein-Volhard, C., Hubbard, T.J., Roest, C.H., Rogers, J., Stemple, D.L., 2013. The zebrafish reference genome sequence and its relationship to the human genome. Nature 496, 498–503. Hukriede, N.A., Joly, L., Tsang, M., Miles, J., Tellis, P., Epstein, J.A., Barbazuk, W.B., Li, F.N., Paw, B., Postlethwait, J.H., Hudson, T.J., Zon, L.I., McPherson, J.D., Chevrette, M., Dawid, I.B., Johnson, S.L., Ekker, M., 1999. Radiation hybrid mapping of the zebrafish genome. Proc. Natl. Acad. Sci. USA 96, 9745–9750. Hwang, W.Y., Fu, Y., Reyon, D., Maeder, M.L., Tsai, S.Q., Sander, J.D., Peterson, R.T., Yeh, J.R., Joung, J.K., 2013. Efficient genome editing in zebrafish using a CRISPRCas system. Nat. Biotechnol. 31, 227–229. Nasevicius, A., Ekker, S.C., 2000. Effective targeted gene ‘knockdown’ in zebrafish. Nat. Genet. 26, 216–220. Renshaw, S.A., Trede, N.S., 2012. A model 450 million years in the making: zebrafish and vertebrate immunity. Dis. Model. Mech. 5, 38–47. Streisinger, G., 1983. Extrapolations from species to species and from various cell types in assessing risks from chemical mutagens. Mutat. Res. 114, 93–105. Streisinger, G., Walker, C., Dower, N., Knauber, D., Singer, F., 1981. Production of clones of homozygous diploid zebra fish (Brachydanio rerio). Nature 291, 293– 296. Walker, C., Streisinger, G., 1983. Induction of mutations by gamma-rays in pregonial germ cells of zebrafish embryos. Genetics 103, 125–136. Zu, Y., Tong, X., Wang, Z., Liu, D., Pan, R., Li, Z., Hu, Y., Luo, Z., Huang, P., Wu, Q., Zhu, Z., Zhang, B., Lin, S., 2013. TALEN-mediated precise genome modification by homologous recombination in zebrafish. Nat. Methods 10, 329–331.
⇑
Jeffrey A. Yoder Department of Molecular Biomedical Sciences, North Carolina State University, 1060 William Moore Drive, Raleigh, NC 27607, USA ⇑ Tel.: +1 919 515 7406; fax: +1 919 513 7301. E-mail address: [email protected] Available online 18 April 2014
