Advertisement

Cytology and Genetics

, Volume 52, Issue 6, pp 406–415 | Cite as

The Zebrafish as a New Model System for Experimental Biology

  • V. KorzhEmail author
  • I. KondrychynEmail author
  • C. WinataEmail author
Article
  • 24 Downloads

Abstract

The emergence of genomics and its use in combination with high-resolution bioimaging for the study of animal development mechanisms provide scientists with information on gene sets and regulation thereof during development. This enabled the identification of the core set of transcription factors involved in the development of invertebrates and vertebrates. This approach was particularly efficient due to the widespread use of transparent embryos of zebrafish and other bony fishes in these studies. These embryos can be used as model systems for the analysis of vertebrate development, even at the level of individual cells, as the various processes of development unfold in vivo.

Keywords:

genomics of development transgenesis Tol2 transposon bioimaging lateral line Zic3 

Notes

ACKNOWLEDGMENTS

We are grateful to the International Institute of Molecular and Cell Biology and the National Center for Science (Poland) for their financial support and to S.N. Korzh for excellent editing of this text.

COMPLIANCE WITH ETHICAL STANDARDS

Conflict of interests. The authors declare that they have no conflict of interest.

Statement on the welfare of animals. This article does not contain any studies involving animals performed by any of the authors.

REFERENCES

  1. 1.
    Korzh, V. and Bregestovski, P., Elie Metchnikoff: Father of phagocytosis theory and pioneer of experiments in vivo, Cytol. Genet., 2016, vol. 50, no. 2, pp. 143–150.CrossRefGoogle Scholar
  2. 2.
    Korzh, V., Genetic control of early neuronal development in vertebrates, Curr. Opin. Neurobiol., 1994, vol. 4, no. 1, pp. 21–28. org/ doi 10.1016/0959-4388(94)90027-2Google Scholar
  3. 3.
    Kimmel, C.B., Ballard, W.W., Kimmel, S.R., Ullmann, B., and Schilling, T.F., Stages of embryonic development of the zebrafish, Dev. Dynam., 1995, vol. 203, no. 3, pp. 253–310. doi 10.1002/aja.1002030302CrossRefGoogle Scholar
  4. 4.
    Westerfield, M., A Guide for the Laboratory Use of Zebrafish (Brachydanio rerio), Eugene OR: Univ. of Oregon Press, 1995.Google Scholar
  5. 5.
    Barriuso, J., Nagaraju, R., and Hurlstone, A., Zebrafish: a new companion for translational research in oncology, Clin. Cancer Res., 2015, vol. 21, no. 5, pp. 969–975. doi 10.1158/1078-0432.CCR-14-2921CrossRefPubMedPubMedCentralGoogle Scholar
  6. 6.
    Patten, S.A., Armstrong, G.A., Lissouba, A., Kabashi, E., Parker, J.A., and Drapeau, P., Fishing for causes and cures of motor neuron disorders, Dis. Model. Mech., 2014, vol. 7, no. 7, pp. 799–809. doi 10.1242/ dmm.015719CrossRefPubMedPubMedCentralGoogle Scholar
  7. 7.
    Li, M., Zhao, L., Page-McCaw, P.S., and Chen, W., Zebrafish Genome Engineering Using the CRISPRCas9 System, Trends Genet., 2016, vol. 32, no. 12. doi 10.1016/j.tig.2016.10.005Google Scholar
  8. 8.
    Peterson, R.T., Zebrafish as tools for drug discovery, Nat. Rev. Drug. Discov., 2015, vol. 14, no. 10, pp. 721–731. doi 10.1038/nrd4627CrossRefPubMedGoogle Scholar
  9. 9.
    Yan, H., The C., Sreejith S., Zhu L.L., Kwok A., Ma X., Nguyen K.T., Korzh V., Zhao Y. Functional mechanized mesoporous silica nano-particles for controlled drug release in vivo, Angew. Chem. Int., vol. 51, no. 33, pp. 8373–8377. doi 10.1002/anie.201203993Google Scholar
  10. 10.
    Aanes, H., Winata, C.L., Lin, C.H., Chen, J.P., Srinivasan, K.G., Lee, S.G., Lim, A.Y., Hajan, H.S., Collas, P., Bourque, G., Gong, Z., Korzh, V., Alestrom, P., and Mathavan, S., Zebrafish mRNA sequencing deciphers novelties in transcriptome dynamics during maternal to zygotic transition, Genome Res., 2011, vol. 21, no. 8, pp. 1328–1338. doi 10.1101/gr.116012.110CrossRefPubMedPubMedCentralGoogle Scholar
  11. 11.
    Winata, C.L., Kondrychyn, I., Kumar, V., Srinivasan, K.G., Orlov, Yu., Ravishankar, A., Prabhakar, S., Stanton, L., Korzh, V., and Mathavan, S., Genome wide analysis reveals Zic3 interaction with distal regulatory elements of stage specific developmental genes in zebrafish, PLoS Genet., 2013, vol. 9, no. 10. e1003852. doi 10.1371/journal.pgen.1003852CrossRefPubMedPubMedCentralGoogle Scholar
  12. 12.
    Winata, C.L., Kondrychyn, I., and Korzh, V., Changing faces of transcriptional regulation by Zic3, Curr. Genom., 2015, vol. 16, no. 2, pp. 117–27. 10.2174/ 1389202916666150205124519Google Scholar
  13. 13.
    Mikut, R., Dickmeis, T., Driever, W., Geurts, P., Hamprecht, F.A., Kausler, B.X., Ledesma-Carbayo, M.J., Maree, R., Mikula, K., Pantazis, P., Ronneberger, O., Santos, A., Stotzka, R., Strahle, U., and Peyrieras, N., Automated processing of zebrafish imaging data: a survey, Zebra Fish, 2013, vol. 10, no. 3, pp. 401–421. doi 10.1089/zeb.2013.0886CrossRefPubMedGoogle Scholar
  14. 14.
    Fraser, P., Transcriptional control thrown for a loop, Curr. Opin. Genet. Dev., 2006, vol. 1, no. 5, pp. 490–495.CrossRefGoogle Scholar
  15. 15.
    Weipoltshammer, K. and Schofer, C., Morphology of nuclear transcription, Histochem., Cell Biol., 2016, vol. 145, no. 4, pp. 343–358. doi 10.1007/s00418-016-1412-0CrossRefGoogle Scholar
  16. 16.
    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., Elliot, D., Threadgold, G., Harden, G., Ware, D., Begum, S., Mortimore, 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., Lloyd, C., 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., Lanz, C., Raddatz, G., Osoegawa, K., Zhu, B., Rapp, A., Widaa, S., Langford, C., Yang, F., Schuster, S.C., 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 Crollius, H., Rogers, J., and Stemple, D.L., The zebrafish reference genome sequence and its relationship to the human genome, Nature, 2013, vol. 496, no. 7446, pp. 498–503. doi 10.1038/nature12111CrossRefPubMedPubMedCentralGoogle Scholar
  17. 17.
    Kettleborough, R.N., Busch-Nentwich, E.M., Harvey, S.A., Dooley, C.M., de Bruijn, E., van Eeden, F., Sealy, I., White, R.J., Herd, C., Nijman, I.J., Fenyes, F., Mehroke, S., Scahill, C., Gibbons, R., Wali, N., Carruthers, S., Hall, A., Yen, J., Cuppen, E., and Stemple, D.L., A systematic genome-wide analysis of zebrafish protein-coding gene function, Nature, 2013, vol. 496, pp. 494–497.CrossRefPubMedPubMedCentralGoogle Scholar
  18. 18.
    Brenner, S., Elgar, G., Sandford, R., Macrae, A., Venkatesh, B., and Aparicio, S., Characterization of the pufferfish (Fugu) genome as a compact model vertebrate genome, Nature, 1993, vol. 366, no. 6452, pp. 265–268. doi 10.1038/366265a0CrossRefPubMedGoogle Scholar
  19. 19.
    Venkatesh, B., Lee, A., Ravi, V., Lian, M., Maurya, A., Swann, J., Ohta, Y., Flajnik, M., Sutoh, Y., Kasahara, M., Hoon, S., Gangu, V., Roy, S., Irimia, M., Korzh, V., Kondrychyn, I., Tay, B.T., Tohari, S., Lim, S., Kong, K., Ho, S., Lorente-Galdos, B., Qui, J., Marques-Bonet, T., Raney, B., Ingham, P., Tay, A., Hillier, L., Minx, P., Boehm, T., Wilson, R., Brenner, S., and Warren, W., Elephant shark genome provides insights into gnathostome evolution, Nature, 2014, vol. 505, pp. 174–179.CrossRefPubMedPubMedCentralGoogle Scholar
  20. 20.
    Mathavan, S., Lee, S.G., Mak, A., Miller, L.D., Murthy, K.R., Govindarajan, K.R., Tong, Y., Wu, Y.L., Lam, S.H., Yang, H., Ruan, Y., Korzh, V., Gong, Z., Liu, E.T., and Lufkin, T., Transcriptome analysis of zebrafish embryogenesis using microarrays, PLoS Genet., 2005, vol. 1, no. 2, pp. 260–276. doi 10.1371/ journal.pgen.0010029CrossRefPubMedGoogle Scholar
  21. 21.
    Harvey, S.A., Sealy, I., Kettleborough, R., Fenyes, F., White, R., Stemple, D., and Smith, J.C., Identification of the zebrafish maternal and paternal transcriptomes, Development, 2013, vol. 140, no. 13, pp. 2703–2710. doi 10.1242/dev.095091CrossRefPubMedPubMedCentralGoogle Scholar
  22. 22.
    Armant, O., Marz, M., Schmidt, R., Ferg, M., Diotel, N., Ertzer, R., Bryne, J.C., Yang, L., Baader, I., Reischl, M., Legradi, J., Mikut, R., Stemple, D., van IJcken, W., van der Sloot, A., Lenhard, B., Strahle, U., and Rastegar, S., Genome-wide, whole mount in situ analysis of transcriptional regulators in zebrafish embryos, Dev Biol., 2013, vol. 380, no. 2, pp. 351–362. doi 10.1016/j.ydbio.2013.05.006CrossRefPubMedPubMedCentralGoogle Scholar
  23. 23.
    Thisse, B. and Thisse, C., Fast release clones: a high throughput expression analysis, ZFIN direct data submission, 2004. http://zfin.orgGoogle Scholar
  24. 24.
    Seth, A., Stemple, D.L., and Barroso, I., The emerging use of zebrafish to model metabolic disease, Dis. Model Mech., 2013, vol. 6, no. 5, pp. 1080–1088. doi 10.1242/dmm.011346CrossRefPubMedPubMedCentralGoogle Scholar
  25. 25.
    Tan, H., Onichtchouk, D., and Winata, C., DANIOCODE: toward an encyclopedia of DNA elements in zebrafish, Zebrafish, vol. 13, no. 1, pp. 54–60. doi 10.1089/zeb.2015.1179Google Scholar
  26. 26.
    Birnbaum, R.Y., Clowney, E.J., Agamy, O., Kim, M.J., Zhao, J., Yamanaka, T., Pappalardo, Z., Clar-ke, S.L., Wenger, A.M., Nguyen, L., Gurrieri, F., Everman, D.B., Schwartz, C.E., Birk, O.S., Beje-rano, G., Lomvardas, S., and Ahituv, N., Coding exons function as tissue-specific enhancers of nearby genes, Genome Res., 2012, vol. 22, no. 6, pp. 1059–1068. doi 10.1101/gr.133546.111CrossRefPubMedPubMedCentralGoogle Scholar
  27. 27.
    Gehrig, J., Reischl, M., Kalmar, E., Ferg, M., Hadzhiev, Y., Zaucker, A., Song, C., Schindler, S., Liebel, U., and Muller, F., Automated high-throughput mapping of promoter-enhancer interactions in zebrafish embryos, Nat. Methods, 2009, vol. 6, no. 12, pp. 911–916. doi 10.1038/nmeth.1396CrossRefPubMedGoogle Scholar
  28. 28.
    Gebbi, M., Ferrero, G.B., Pilia, G., Bassi, M.T., Aylsworth, A., Penman-Splitt, M., Bird, L.M., Bamforth, J.S., Burn, J., Schlessinger, D., Nelson, D.L., and Casey, B., X-linked situs abnormalities result from mutations in ZIC3, Nat. Genet., 1997, vol. 17, no. 3, pp. 305–308. doi 10.1038/ng1197-305CrossRefGoogle Scholar
  29. 29.
    Ishiguro, A., Inoue, T., Mikoshiba, K., and Aruga, J., Molecular properties of Zic4 and Zic5 proteins: functional diversity within Zic family, Biochem. Biophys. Res. Commun., 2004, vol. 324, no. 1, pp. 302–307. doi 10.1016/j.bbrc.2004.09.052CrossRefPubMedGoogle Scholar
  30. 30.
    Ware, S.M., Peng, J., Zhu, L., Fernbach, S., Colicos, S., Casey, B., Towbin, J., and Belmont, J.W., Identification and functional analysis of ZIC3 mutations in heterotaxy and related congenital heart defects, Am. J. Hum. Genet., 2004, vol. 74, no. 1, pp. 93–105. doi 10.1086/380998CrossRefPubMedGoogle Scholar
  31. 31.
    Cowan, J., Tariq, M., and Ware, S.M., Genetic and functional analyses of ZIC3 variants in congenital heart disease, Hum. Mut., 2014, vol. 35, no. 1, pp. 66–75. doi 10.1002/humu.22457CrossRefPubMedGoogle Scholar
  32. 32.
    Aruga, J., Yokota, N., Hashimoto, M., Furuichi, T., Fukuda, M., and Mikoshiba, K., A novel zinc finger protein, zic, is involved in neurogenesis, especially in the cell lineage of cerebellar granule cells, J. Neurochem., 1994, vol. 63, no. 5, pp. 1880–1890.CrossRefPubMedGoogle Scholar
  33. 33.
    Logan, C.Y. and Nusse, R., The Wnt signaling pathway in development and disease, Ann. Rev. Cell Dev. Biol., 2004, vol. 20, pp. 781–810. doi 10.1146/annurev.cellbio.20.010403.113126CrossRefGoogle Scholar
  34. 34.
    Nonaka, S., Tanaka, Y., Okada, Y., Takeda, S., Harada, A., Kanai, Y., Kido, M., and Hirokawa, N., Randomization of left-right asymmetry due to loss of nodal cilia generating leftward flow of extraembryonic fluid in mice lacking KIF3B motor protein, Cell, 1998, vol. 95, no. 6, pp. 829–837.CrossRefPubMedGoogle Scholar
  35. 35.
    Tanaka, Y., Okada, Y., and Hirokawa, N., FGF-induced vesicular release of Sonic hedgehog and retinoic acid in leftward nodal flow is critical for left-right determination, Nature, 2005, vol. 435, no. 7039, pp. 172–177. doi 10.1038/nature03494CrossRefPubMedGoogle Scholar
  36. 36.
    Essner, J.J., Amack, J.D., Nyholm, M.K., Harris, E.B., and Yost, H.J., Kupffer’s vesicle is a ciliated organ of asymmetry in the zebrafish embryo that initiates left-right development of the brain, heart and gut, Development, 2005, vol. 13, no. 6, pp. 1247–1260. doi 10.1242/dev.01663CrossRefGoogle Scholar
  37. 37.
    Sampath, K., Rubinstein, A.L., Cheng, A.M., Liang, J.O., Fekany, K., Solnica-Krezel, L., Korzh, V., Halpern, M.E., and Wright, C.V., Induction of the zebrafish ventral brain and floor plate requires cyclops/nodal signaling, Nature, 1998, vol. 395, no. 6698, pp. 185–189. doi 10.1038/26020CrossRefPubMedGoogle Scholar
  38. 38.
    Yu, X., Ng, C.P., Habacher, H., and Roy, S., Foxj1 transcription factors are master regulators of the motile ciliogenic program, Nat. Genet., 2008, vol. 40, no. 12, pp. 1445–1453. doi 10.1038/ng.263CrossRefPubMedGoogle Scholar
  39. 39.
    Aruga, J., The role of Zic genes in neural development, Mol. Cell. Neurosci., 2004, vol. 26, no. 2, pp. 205–221.CrossRefPubMedGoogle Scholar
  40. 40.
    Grinblat, Y. and Sive, H., Zic gene expression marks anteroposterior pattern in the presumptive neurectoderm of the zebrafish gastrula, Dev. Dyn., 2001, vol. 222, no. 1, pp. 688–693. doi 10.1002/dvdy.1221CrossRefPubMedGoogle Scholar
  41. 41.
    Kondrychyn, I., Teh, C., Sin, M., and Korzh, V., Stretching morphogenesis of the roof plate during coordinated formation of the central canal, PLoS One, 2013, vol. 8, no. 2. e56219. doi 10.1371/journal.pone.0056219CrossRefPubMedPubMedCentralGoogle Scholar
  42. 42.
    Wan, H., He, J., Ju, B., Yan, T., Lam, T.J., and Gong, Z., Generation of two-color transgenic zebrafish using the green and red fluorescent protein reporter genes gfp and rfp, Mar. Biotechnol., 2002, vol. 4, no. 2, pp. 146–154. doi 10.1007/s10126-001-0085-3CrossRefPubMedGoogle Scholar
  43. 43.
    Korzh, V. and Wohland, T., Analysis of single molecules in vivo or… why a small fish is better than an empty dish. Ontogenesis, Russ. J. Dev. Biol., 2012, vol. 43, no. 2, pp. 83–93.CrossRefGoogle Scholar
  44. 44.
    Teh, C., Sun, G., Shen, H.Y., Korzh, V., and Wohland, T., Modulating the expression level of secreted Wnt3 influences cerebellum development in zebrafish transgenics, Development, 2015, vol. 142, no. 21, pp. 3721–3733. doi 10.1242/dev.127589CrossRefPubMedGoogle Scholar
  45. 45.
    Keller, P.J., Schmidt, A.D., Wittbrodt, J., and Stelzer, E.H., Reconstruction of zebrafish early embryonic development by scanned light sheet microscopy, Science, 2008, vol. 322, no. 5904, pp. 1065–1069. doi 10.1126/science.1162493CrossRefPubMedGoogle Scholar
  46. 46.
    Long, Q., Meng, A., Wang, H., Jessen, J.R., Farrell, M.J., and Lin, S., GATA-1 expression pattern can be recapitulated in living transgenic zebrafish using GFP reporter gene, Development. 1997, vol. 124, no. 20, pp. 4105–4111.PubMedGoogle Scholar
  47. 47.
    Parinov, S., Kondrichin, I., Korzh, V., and Emelya-nov, A., Tol2 transposon-mediated enhancer trap to identify developmentally regulated zebrafish genes in vivo, Dev. Dynam., 2004, vol. 231, no. 2, pp. 449–459. doi 10.1002/dvdy.20157CrossRefGoogle Scholar
  48. 48.
    Kawakami, K., Takeda, H., Kawakami, N., Kobayashi, M., Matsuda, N., and Mishina, M., A transposon-mediated gene trap approach identifies developmentally regulated genes in zebrafish, Dev. Cell, 2004, vol. 7, no. 1, pp. 133–144. doi 10.1016/j.devcel.2004.06.005CrossRefPubMedGoogle Scholar
  49. 49.
    Emelyanov, A., Gao, Y., Naqvi, N.I., and Parinov, S., Trans-kingdom transposition of the maize dissociation element, Genetics, 2006, vol. 174, no. 3, pp. 1095–1104. org/ doi 10.1534/genetics.106.061184Google Scholar
  50. 50.
    Ivics, Z., Hackett, P.B., Plasterk, R.H., and Izsvak, Z., Molecular reconstruction of Sleeping Beauty, a Tc1-like transposon from fish, and its trans-position in human cells, Cell, 1997, vol. 91, no. 4, pp. 501–510.CrossRefPubMedGoogle Scholar
  51. 51.
    Kondrychyn, I., Garcia-Lecea, M., Emelyanov, A., Parinov, S., and Korzh, V., Genome-wide analysis of Tol2 transposon reintegration in zebrafish, BMC Genomics, 2009, vol. 10, pp. 418. doi 10.1186/1471-2164-10-418CrossRefPubMedPubMedCentralGoogle Scholar
  52. 52.
    Kondrychyn, I., Teh, C., Garcia-Lecea, M., Guan, Y., Kang, A., and Korzh, V., Zebrafish Enhancer TRAP transgenic line database ZETRAP 2.0, Zebrafish, 2011, vol. 8, no. 4, pp. 181–182. doi 10.1089/zeb.2011.0718CrossRefPubMedGoogle Scholar
  53. 53.
    Garcia-Lecea, M., Kondrychyn, I., Fong, S.H., Ye, Z.-R., and Korzh, V., In vivo analysis of choroid plexus morphogenesis in zebrafish, PLoS One, 2008, vol. 3, no. 9. e3090. doi 10.1371/journal.pone.0003090.53CrossRefPubMedPubMedCentralGoogle Scholar
  54. 54.
    Sivasubbu, S., Balciunas, D., Amsterdam, A., and Ekker, S.C., Insertional mutagenesis strategies in zebrafish, Genome Biol., 2007, vol. 8, suppl. 1, p. S9. doi 10.1186/gb-2007-8-s1-s9CrossRefPubMedPubMedCentralGoogle Scholar
  55. 55.
    Go, W., Bessarab, D., and Korzh, V., atp2b1a regulates Ca(2+) export during differentiation and regeneration of mechanosensory hair cells in zebrafish, Cell Calcium, 2010, vol. 48, no. 5, pp. 302–313. doi 10.1016/ j.ceca.2010.09.012CrossRefPubMedGoogle Scholar
  56. 56.
    Ghysen, A., Dambly-Chaudiere, C., and Raible, D., Making sense of zebrafish neural development in the Minervois, Neural. Dev., 2007, vol. 2, no. 1, p. 15. doi 10.1186/1749-8104-2-15CrossRefPubMedPubMedCentralGoogle Scholar
  57. 57.
    Gomez-Skarmeta, J.L., Lenhard, B., and Becker, T.S., New technologies, new findings, and new concepts in the study of vertebrate cis-regulatory sequences, Dev. Dyn., 2006, vol. 235, no. 4, pp. 870–885. doi 10.1002/dvdy.20659CrossRefPubMedGoogle Scholar
  58. 58.
    Korzh, V., Transposons as tools for enhancer-trap screens in vertebrates, Genome Biol., 2007, vol. 8, suppl. 1, p. S8. doi 10.1186/gb-2007-8-s1-s8CrossRefPubMedPubMedCentralGoogle Scholar

Copyright information

© Allerton Press, Inc. 2018

Authors and Affiliations

  1. 1.International Institute of Molecular and Cell BiologyWarsawPoland
  2. 2.RIKEN Center for Biosystems Dynamics ResearchKobeJapan
  3. 3.Max Planck Institute for Heart and Lung ResearchBad NauheimGermany

Personalised recommendations