Specification of the zebrafish nervous system by nonaxial signals

Science

Volumn 277, Issue 5323, 1997, Pages 254-257

  Woo, Katherine ^a,b   Fraser, Scott E ^a  

^a CALIFORNIA INSTITUTE OF TECHNOLOGY   (United States)

^b SAN FRANCISCO GENERAL HOSPITAL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

BASIC FIBROBLAST GROWTH FACTOR;

ANIMAL TISSUE; ARTICLE; CELL SPECIFICITY; CONTROLLED STUDY; EMBRYO; GASTRULA; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; SIGNAL TRANSDUCTION; ZEBRA FISH;

ANIMALS; BODY PATTERNING; CELL TRANSPLANTATION; DNA-BINDING PROTEINS; EARLY GROWTH RESPONSE PROTEIN 2; ECTODERM; ENDODERM; FIBROBLAST GROWTH FACTOR 2; GASTRULA; MESENCEPHALON; MESODERM; MORPHOGENESIS; RECOMBINANT PROTEINS; RHOMBENCEPHALON; STEM CELLS; TRANSCRIPTION FACTORS; ZEBRAFISH;

AMPHIBIA; ANIMALIA; DANIO RERIO;

EID: 0030820083     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.277.5323.254     Document Type: Article

References (55)

1. J. M. W. Slack and D. Tannahill, Development 114, 285 (1992); D. S. Kessler and D. A. Melton, Science 266, 596 (1994); O. G. Kelly and D. A. Melton, Trends Genet. 11, 273 (1995).
2. J. M. W. Slack and D. Tannahill, Development 114, 285 (1992); D. S. Kessler and D. A. Melton, Science 266, 596 (1994); O. G. Kelly and D. A. Melton, Trends Genet. 11, 273 (1995).
3. J. M. W. Slack and D. Tannahill, Development 114, 285 (1992); D. S. Kessler and D. A. Melton, Science 266, 596 (1994); O. G. Kelly and D. A. Melton, Trends Genet. 11, 273 (1995).
4. H. Spemann, Embryonic Development and Induction (Yale Univ. Press, New Haven, CT, 1938); T. Doniach, J. Neurobiol. 24, 1256 (1993); A. Ruiz-i-Altaba, ibid., p. 1276.
5. H. Spemann, Embryonic Development and Induction (Yale Univ. Press, New Haven, CT, 1938); T. Doniach, J. Neurobiol. 24, 1256 (1993); A. Ruiz-i-Altaba, ibid., p. 1276.
6. H. Spemann, Embryonic Development and Induction (Yale Univ. Press, New Haven, CT, 1938); T. Doniach, J. Neurobiol. 24, 1256 (1993); A. Ruiz-i-Altaba, ibid., p. 1276.
7. P. D. Nieuwkoop et al., J. Exp. Zool. 120, 1 (1952); H. Eyal-Giladi, Arch. Biol. 65, 179 (1954); M. Sala, Proc. K. Ned. Akad. Wet. Ser. C 58, 635 (1955); L. Saxen and S. Toivonen, Primary Embryonic Induction (Logos, London, 1962).
8. P. D. Nieuwkoop et al., J. Exp. Zool. 120, 1 (1952); H. Eyal-Giladi, Arch. Biol. 65, 179 (1954); M. Sala, Proc. K. Ned. Akad. Wet. Ser. C 58, 635 (1955); L. Saxen and S. Toivonen, Primary Embryonic Induction (Logos, London, 1962).
9. P. D. Nieuwkoop et al., J. Exp. Zool. 120, 1 (1952); H. Eyal-Giladi, Arch. Biol. 65, 179 (1954); M. Sala, Proc. K. Ned. Akad. Wet. Ser. C 58, 635 (1955); L. Saxen and S. Toivonen, Primary Embryonic Induction (Logos, London, 1962).
10. P. D. Nieuwkoop et al., J. Exp. Zool. 120, 1 (1952); H. Eyal-Giladi, Arch. Biol. 65, 179 (1954); M. Sala, Proc. K. Ned. Akad. Wet. Ser. C 58, 635 (1955); L. Saxen and S. Toivonen, Primary Embryonic Induction (Logos, London, 1962).
11. T. Doniach, Cell 83, 1067 (1995); I. Mason, Curr. Biol. 6, 672 (1996).
12. T. Doniach, Cell 83, 1067 (1995); I. Mason, Curr. Biol. 6, 672 (1996).
13. S.-L. Ang and J. Rossant, Cell 78, 561 (1994); D. C. Weinstein et al., ibid., p. 575; D. Psychoyos and C. Stern, Development 122, 3263 (1996).
14. S.-L. Ang and J. Rossant, Cell 78, 561 (1994); D. C. Weinstein et al., ibid., p. 575; D. Psychoyos and C. Stern, Development 122, 3263 (1996).
15. S.-L. Ang and J. Rossant, Cell 78, 561 (1994); D. C. Weinstein et al., ibid., p. 575; D. Psychoyos and C. Stern, Development 122, 3263 (1996).
16. J. Shih and S. E. Fraser, Development 122, 1313 (1996).
17. K. Woo and S. E. Fraser, ibid. 121, 2595 (1995).
18. Donor embryos were injected, at the two-to four-cell stage, with a 1:1 mixture of rhodamine and biotin dextrans (50 mg/ml, Molecular Probes), which allowed for subsequent detection of grafted cells both fluorescently and histochemically. All surrical manipulations were performed by established methods with the use of an eyelash-hair knife and hairloop in full-strength Danieau solution (6). Embryos were then raised individually in 24-well plates. Microscopic documentation was performed as described (7). Full-color documentation was performed with a ProgRes 3012 digital color camera and ImageManager software (Roche Image Analysis Systems).
19. K. Woo and S. E. Fraser, Dev. Biol. 170, 764 (1995); in preparation.
20. J. Shih and S. E. Fraser, Development 121, 2755 (1995).
21. At shield stage, nonaxial germring cells share molecular characteristics distinct from the shield region: They express snail1 [M. Hammerschmidt and C. Nüsslein-Volhard, ibid. 119, 1107 (1993); C. Thisse, B. Thisse, T. F. Schilling, J. H. Postlethwait, ibid., p. 1203] and eve1 (S. Joly, C. Joly, S. Schulte-Merker, H. Boulekbache, H. Condamine, ibid., p. 1261), and they down-regulate zf-T as gastrulation proceeds [ S. Schulte-Merker, R. K. Ho, B. G. Herrmann, C. Nüsslein-Volhard, ibid. 116, 1021 (1992)].
22. At shield stage, nonaxial germring cells share molecular characteristics distinct from the shield region: They express snail1 [M. Hammerschmidt and C. Nüsslein-Volhard, ibid. 119, 1107 (1993); C. Thisse, B. Thisse, T. F. Schilling, J. H. Postlethwait, ibid., p. 1203] and eve1 (S. Joly, C. Joly, S. Schulte-Merker, H. Boulekbache, H. Condamine, ibid., p. 1261), and they down-regulate zf-T as gastrulation proceeds [ S. Schulte-Merker, R. K. Ho, B. G. Herrmann, C. Nüsslein-Volhard, ibid. 116, 1021 (1992)].
23. At shield stage, nonaxial germring cells share molecular characteristics distinct from the shield region: They express snail1 [M. Hammerschmidt and C. Nüsslein-Volhard, ibid. 119, 1107 (1993); C. Thisse, B. Thisse, T. F. Schilling, J. H. Postlethwait, ibid., p. 1203] and eve1 (S. Joly, C. Joly, S. Schulte-Merker, H. Boulekbache, H. Condamine, ibid., p. 1261), and they down-regulate zf-T as gastrulation proceeds [ S. Schulte-Merker, R. K. Ho, B. G. Herrmann, C. Nüsslein-Volhard, ibid. 116, 1021 (1992)].
24. At shield stage, nonaxial germring cells share molecular characteristics distinct from the shield region: They express snail1 [M. Hammerschmidt and C. Nüsslein-Volhard, ibid. 119, 1107 (1993); C. Thisse, B. Thisse, T. F. Schilling, J. H. Postlethwait, ibid., p. 1203] and eve1 (S. Joly, C. Joly, S. Schulte-Merker, H. Boulekbache, H. Condamine, ibid., p. 1261), and they down-regulate zf-T as gastrulation proceeds [ S. Schulte-Merker, R. K. Ho, B. G. Herrmann, C. Nüsslein-Volhard, ibid. 116, 1021 (1992)].
25. K. Woo and S. E. Fraser, data not shown.
26. In situ hybridization of Krox20 was performed as described [E. Oxtoby and T. Jowett, Nucleic Acids Res. 21, 1087 (1993)]. Grafted cells were visualized by incubating post-in situ embryos overnight with streptavidin-horseradish peroxidase (Molecular Probes), then developing with diaminobenzidine, yielding an orange-brown color.
27. In 30% of the cases, presumably because the graft had occupied most of the retinal domain on its side, a morphologically normal retina on the side of the graft was not formed. In section, however, pigmented epithelium and some retinal tissues were present.
28. Reviewed in H. Sive and L. Bradley, Dev. Dyn. 205, 265 (1996); Y. Sasai and E. M. DeRobertis, Dev. Biol. 182, 5 (1997).
29. Reviewed in H. Sive and L. Bradley, Dev. Dyn. 205, 265 (1996); Y. Sasai and E. M. DeRobertis, Dev. Biol. 182, 5 (1997).
30. W. G. Cox and A. Hemmati-Brivanlou, Development 121, 4349 (1995); M. Kengaku and H. Okamoto, ibid., p. 3121; T. M. Lamb and R. M. Harland, ibid., p. 3627.
31. W. G. Cox and A. Hemmati-Brivanlou, Development 121, 4349 (1995); M. Kengaku and H. Okamoto, ibid., p. 3121; T. M. Lamb and R. M. Harland, ibid., p. 3627.
32. W. G. Cox and A. Hemmati-Brivanlou, Development 121, 4349 (1995); M. Kengaku and H. Okamoto, ibid., p. 3121; T. M. Lamb and R. M. Harland, ibid., p. 3627.
33. A. J. Durston et al., Nature 340, 140 (1989); N. Papalopulu et al., Development 113, 1145 (1991); C. R. Sharpe, Neuron 7, 239 (1991); B. Blumberg et al., Development 124, 373 (1997).
34. A. J. Durston et al., Nature 340, 140 (1989); N. Papalopulu et al., Development 113, 1145 (1991); C. R. Sharpe, Neuron 7, 239 (1991); B. Blumberg et al., Development 124, 373 (1997).
35. A. J. Durston et al., Nature 340, 140 (1989); N. Papalopulu et al., Development 113, 1145 (1991); C. R. Sharpe, Neuron 7, 239 (1991); B. Blumberg et al., Development 124, 373 (1997).
36. A. J. Durston et al., Nature 340, 140 (1989); N. Papalopulu et al., Development 113, 1145 (1991); C. R. Sharpe, Neuron 7, 239 (1991); B. Blumberg et al., Development 124, 373 (1997).
37. L. L. McGrew, C.-J. Lai, R. T. Moon, Dev. Biol. 172, 337 (1995).
38. R. T. Moon, J. D. Brown, M. Torres, Trends Genet. 13, 157 (1997).
39. N. Holder and J. Hill, Development 113, 1159 (1991).
40. G. A. Hyatt et al., ibid. 122, 195 (1996).
41. S. Takada et al., Genes Dev. 8, 174 (1994); Y. Yoshikawa, T. Fujimori, A. P. McMahon, S. Takada, Dev. Biol. 183, 234 (1997); I. Dominguez, K. Itoh, S. Y. Sokol, Proc. Natl. Acad. Sci. U.S.A. 92, 8498 (1995). Interfering with some Wnt members and their signaling cascade causes axis duplication (18, 23) [X. He et al., Science 275, 1652 (1997)].
42. S. Takada et al., Genes Dev. 8, 174 (1994); Y. Yoshikawa, T. Fujimori, A. P. McMahon, S. Takada, Dev. Biol. 183, 234 (1997); I. Dominguez, K. Itoh, S. Y. Sokol, Proc. Natl. Acad. Sci. U.S.A. 92, 8498 (1995). Interfering with some Wnt members and their signaling cascade causes axis duplication (18, 23) [X. He et al., Science 275, 1652 (1997)].
43. S. Takada et al., Genes Dev. 8, 174 (1994); Y. Yoshikawa, T. Fujimori, A. P. McMahon, S. Takada, Dev. Biol. 183, 234 (1997); I. Dominguez, K. Itoh, S. Y. Sokol, Proc. Natl. Acad. Sci. U.S.A. 92, 8498 (1995). Interfering with some Wnt members and their signaling cascade causes axis duplication (18, 23) [X. He et al., Science 275, 1652 (1997)].
44. S. Takada et al., Genes Dev. 8, 174 (1994); Y. Yoshikawa, T. Fujimori, A. P. McMahon, S. Takada, Dev. Biol. 183, 234 (1997); I. Dominguez, K. Itoh, S. Y. Sokol, Proc. Natl. Acad. Sci. U.S.A. 92, 8498 (1995). Interfering with some Wnt members and their signaling cascade causes axis duplication (18, 23) [X. He et al., Science 275, 1652 (1997)].
45. G. M. Kelly, P. Greenstein, D. F. Erezyilmaz, R. T. Moon, Development 121, 1787 (1995).
46. S. Krauss, V. Korzh, A. Fjose, T. Johansen, ibid. 116, 249 (1992); G. M. Kelly, C.-J. Lai, R. T. Moon, Dev. Biol. 158, 113 (1993); G. M. Kelly and R. T. Moon, Dev. Genet. 17, 129 (1995); P. Blader, U. Strähle, P. W. Ingham, Dev. Genes Evol. 206, 3 (1996).
47. S. Krauss, V. Korzh, A. Fjose, T. Johansen, ibid. 116, 249 (1992); G. M. Kelly, C.-J. Lai, R. T. Moon, Dev. Biol. 158, 113 (1993); G. M. Kelly and R. T. Moon, Dev. Genet. 17, 129 (1995); P. Blader, U. Strähle, P. W. Ingham, Dev. Genes Evol. 206, 3 (1996).
48. S. Krauss, V. Korzh, A. Fjose, T. Johansen, ibid. 116, 249 (1992); G. M. Kelly, C.-J. Lai, R. T. Moon, Dev. Biol. 158, 113 (1993); G. M. Kelly and R. T. Moon, Dev. Genet. 17, 129 (1995); P. Blader, U. Strähle, P. W. Ingham, Dev. Genes Evol. 206, 3 (1996).
49. S. Krauss, V. Korzh, A. Fjose, T. Johansen, ibid. 116, 249 (1992); G. M. Kelly, C.-J. Lai, R. T. Moon, Dev. Biol. 158, 113 (1993); G. M. Kelly and R. T. Moon, Dev. Genet. 17, 129 (1995); P. Blader, U. Strähle, P. W. Ingham, Dev. Genes Evol. 206, 3 (1996).
50. K. Griffin, R. Patient, N. Holder, Development 121, 2983 (1995).
51. The bFGF bead-coating procedure was adopted from Z. Dai and H. B. Peng [J. Neurosci. 15, 5466 (1995)]. Polystyrene beads (Polysciences, 45 μm) were coated with a solution of bFGF (50 μg/ml; human recombinant, Gibco) for 2 hours at room temperature, then washed twice (10 min each) with large volumes of Danieau solution (6). One or two beads were implanted into the animal pole region of shield-stage embryos. In most animals, the beads remained in the forebrain; in a few cases, the beads drifted posteriorly or into the yolk, and these were excluded from further analysis. The functional activity of the beads was tested with a modified animal cap assay, in which five to eight beads were sandwiched between two pieces of stage 8.5 animal caps and cultured in modified Barth solution until stage 10.5. Sandwiches with bFGF beads underwent morphogenetic movements similar to those treated with soluble bFGF. Sandwiches made with beads not coated with bFGF developed in the same way as control caps without beads.
52. Y. Li, M. L. Allende, R. Finkelstein, E. Weinberg, Mech. Dev. 48, 229 (1994).
53. C. G. Sagerström, Y. Grinblat, H. Sive, Development 122, 1873 (1996).
54. K. L. Kroll and E. Amaya, ibid., p. 3173.
55. We thank T. Jowett and E. Weinberg for probes, J. Shih for advice on transplantation, M. Selleck and C. LaBonne for advice on bead experiments, and A. Collazo, C. Krull, C. LaBonne, A. Louie, E. Krider, J. Shih, P. Sternberg, B. Wold, K. Zinn, and two anonymous reviewers for comments. Supported by grants from the Beckman Institute and by a National Institute of Mental Health Silvio Conte Center award.