Change in chemoattractant responsiveness of developing axons at an intermediate target

Science

Volumn 279, Issue 5347, 1998, Pages 105-107

  Shirasaki, Ryuichi ^a   Katsumata, Ryuta ^a   Murakami, Fujio ^a  

^a OSAKA UNIVERSITY   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CHEMOATTRACTANT;

ANIMAL CELL; ARTICLE; CEREBELLUM; EMBRYO; EMBRYO DEVELOPMENT; NERVE CELL CULTURE; NERVE FIBER GROWTH; NERVOUS SYSTEM DEVELOPMENT; NONHUMAN; PRIORITY JOURNAL; RAT;

ANIMALS; AXONS; CARBOCYANINES; CELL ADHESION MOLECULES, NEURONAL; CHEMOTAXIS; CULTURE TECHNIQUES; FLUORESCENT DYES; MEMBRANE GLYCOPROTEINS; NERVE GROWTH FACTORS; PONS; RATS; RATS, WISTAR; RHOMBENCEPHALON; TUMOR SUPPRESSOR PROTEINS;

ANIMALIA;

EID: 0032472231     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.279.5347.105     Document Type: Article

References (41)

1. C. S. Goodman, Annu. Rev. Neurosci. 19, 341 (1996); M. Tessier-Lavigne and C. S. Goodman, Science 274, 1123 (1996).
2. C. S. Goodman, Annu. Rev. Neurosci. 19, 341 (1996); M. Tessier-Lavigne and C. S. Goodman, Science 274, 1123 (1996).
3. A. G. S. Lumsden and A. M. Davies, Nature 306, 786 (1983); ibid. 323, 538 (1986); J. Bolz, N. Novak, M. Götz, T. Bonhoeffer, ibid. 346, 359 (1990); C. D. Heffner, A. G. S. Lumsden, D. D. M. O'Leary, Science 247, 217 (1990); M. Sato, L. Lopez-Mascaraque, C. D. Heffner, D. D. M. O'Leary, Neuron 13, 791 (1994).
4. A. G. S. Lumsden and A. M. Davies, Nature 306, 786 (1983); ibid. 323, 538 (1986); J. Bolz, N. Novak, M. Götz, T. Bonhoeffer, ibid. 346, 359 (1990); C. D. Heffner, A. G. S. Lumsden, D. D. M. O'Leary, Science 247, 217 (1990); M. Sato, L. Lopez-Mascaraque, C. D. Heffner, D. D. M. O'Leary, Neuron 13, 791 (1994).
5. A. G. S. Lumsden and A. M. Davies, Nature 306, 786 (1983); ibid. 323, 538 (1986); J. Bolz, N. Novak, M. Götz, T. Bonhoeffer, ibid. 346, 359 (1990); C. D. Heffner, A. G. S. Lumsden, D. D. M. O'Leary, Science 247, 217 (1990); M. Sato, L. Lopez-Mascaraque, C. D. Heffner, D. D. M. O'Leary, Neuron 13, 791 (1994).
6. A. G. S. Lumsden and A. M. Davies, Nature 306, 786 (1983); ibid. 323, 538 (1986); J. Bolz, N. Novak, M. Götz, T. Bonhoeffer, ibid. 346, 359 (1990); C. D. Heffner, A. G. S. Lumsden, D. D. M. O'Leary, Science 247, 217 (1990); M. Sato, L. Lopez-Mascaraque, C. D. Heffner, D. D. M. O'Leary, Neuron 13, 791 (1994).
7. A. G. S. Lumsden and A. M. Davies, Nature 306, 786 (1983); ibid. 323, 538 (1986); J. Bolz, N. Novak, M. Götz, T. Bonhoeffer, ibid. 346, 359 (1990); C. D. Heffner, A. G. S. Lumsden, D. D. M. O'Leary, Science 247, 217 (1990); M. Sato, L. Lopez-Mascaraque, C. D. Heffner, D. D. M. O'Leary, Neuron 13, 791 (1994).
8. M. Tessier-Lavigne, M. Placzek, A. G. S. Lumsden, J. Dodd, T. M. Jessell, Nature 336, 775 (1988); M. Placzek, M. Tessier-Lavigne, T. M. Jessell, J. Dodd, Development 110, 19 (1990).
9. M. Tessier-Lavigne, M. Placzek, A. G. S. Lumsden, J. Dodd, T. M. Jessell, Nature 336, 775 (1988); M. Placzek, M. Tessier-Lavigne, T. M. Jessell, J. Dodd, Development 110, 19 (1990).
10. H. Yaginuma and R. W. Oppenheim, J. Neurosci. 11, 2598 (1991).
11. T. Serafini et al., Cell 78, 409 (1994); T. E. Kennedy, T. Serafini, J. R. dela Torre, M. Tessier-Lavigne, ibid., p. 425.
12. T. Serafini et al., Cell 78, 409 (1994); T. E. Kennedy, T. Serafini, J. R. dela Torre, M. Tessier-Lavigne, ibid., p. 425.
13. R. Shirasaki, A. Tamada, R. Katsumata, F. Murakami, Neuron 14, 961 (1995).
14. A. Tamada, R. Shirasaki, F. Murakami, ibid., p. 1083.
15. T. Serafini et al., Cell 87, 1001 (1996).
16. R. Shirasaki, C. Mirzayan, M. Tessier-Lavigne, F. Murakami, Neuron 17, 1079 (1996).
17. A. Ebens et al., ibid., p. 1157; L. J. Richards, S. E. Koester, R. Tuttle, D. D. M. O'Leary, J. Neurosci. 17, 2445 (1997).
18. A. Ebens et al., ibid., p. 1157; L. J. Richards, S. E. Koester, R. Tuttle, D. D. M. O'Leary, J. Neurosci. 17, 2445 (1997).
19. S. A. Colamarino and M. Tessier-Lavigne, Annu. Rev. Neurosci. 18, 497 (1995).
20. Experimental procedures for tissue dissection and explant culture followed those of Shirasaki et al. (6), with some modifications. In all the chemoattraction assays, the brains of embryonic day 13 (E13) Wistar rats were used, because CP axons leave the CP and head straight toward the floor plate at around E13 (6). A 0.5 to 1 mm wide metencephalic strip containing the entire circumferential trajectory of CP axons was dissected from the rostral hindbrain (Fig. 1A). The metencephalic strip and a floor plate expiant, taken from the hindbrain, were placed on a polycarbonate isopore membrane filter (Millipore, Tokyo, Japan; pore size, 5.0 μm), with the ventricular side of the explants down, followed by embedding in collagen gels (6). The explants on the filter were then cultured for 2 days as previously described (9).
21. After fixation with 4% paraformaldehyde, we labeled CP axons by implanting fluorescent tracer DiI or DiO crystals (Molecular Probes, Eugene, OR) into the lateral margin of the preparation, from which these axons are known to emanate (6).
22. Whole-mount immunohistochemistry was performed on cultured expiants in collagen gels, with an antibody to TAG-1 (monoclonal 4D7 supernatant, diluted 1:3), as described (9), except that each antibody incubation was performed for 1 day at 4°C.
23. M. Yamamoto, A. M. Boyer, J. E. Crandall, M. Edwards, H. Tanaka, J. Neurosci. 6, 3576 (1986); J. Dodd, S. B. Morton, D. Karagogeos, M. Yamamoto, T. M. Jessell, Neuron 1, 105 (1988); P. E. Phelps, R. P. Barber, J. E. Vaughn, J. Comp. Neurol. 330, 1 (1993); D. P. Wolfer, A. Henehan-Beatty, E. T. Stoeckli, P. Sonderegger, H.-P. Lipp, ibid. 345, 1 (1994).
24. M. Yamamoto, A. M. Boyer, J. E. Crandall, M. Edwards, H. Tanaka, J. Neurosci. 6, 3576 (1986); J. Dodd, S. B. Morton, D. Karagogeos, M. Yamamoto, T. M. Jessell, Neuron 1, 105 (1988); P. E. Phelps, R. P. Barber, J. E. Vaughn, J. Comp. Neurol. 330, 1 (1993); D. P. Wolfer, A. Henehan-Beatty, E. T. Stoeckli, P. Sonderegger, H.-P. Lipp, ibid. 345, 1 (1994).
25. M. Yamamoto, A. M. Boyer, J. E. Crandall, M. Edwards, H. Tanaka, J. Neurosci. 6, 3576 (1986); J. Dodd, S. B. Morton, D. Karagogeos, M. Yamamoto, T. M. Jessell, Neuron 1, 105 (1988); P. E. Phelps, R. P. Barber, J. E. Vaughn, J. Comp. Neurol. 330, 1 (1993); D. P. Wolfer, A. Henehan-Beatty, E. T. Stoeckli, P. Sonderegger, H.-P. Lipp, ibid. 345, 1 (1994).
26. M. Yamamoto, A. M. Boyer, J. E. Crandall, M. Edwards, H. Tanaka, J. Neurosci. 6, 3576 (1986); J. Dodd, S. B. Morton, D. Karagogeos, M. Yamamoto, T. M. Jessell, Neuron 1, 105 (1988); P. E. Phelps, R. P. Barber, J. E. Vaughn, J. Comp. Neurol. 330, 1 (1993); D. P. Wolfer, A. Henehan-Beatty, E. T. Stoeckli, P. Sonderegger, H.-P. Lipp, ibid. 345, 1 (1994).
27. + axons could not be followed to the contralateral side. To assess the chemoattraction of CP axons after they cross the floor plate, we labeled CP axons by implanting DiI into the CP contralateral to an ectopic explant.
28. To examine responsiveness to netrin-1, we used aggregates of 293-EBNA cells secreting recombinant netrin-1 in place of the ectopic floor plate explants. These aggregates were prepared by the hanging drop culture method as described (9). Generation of the 293-EBNA cell line stably secreting netrin-1 has been described (9).
29. CP axons growing within a distance of 0.58 ± 0.01 mm (mean ± SEM, n = 12) from the aggregates showed directed growth toward them.
30. To ascertain whether the floor plate also mediates the change in the netrin-1 responsiveness of CP axons, we repeated the experiments of Fig. 2 but with a netrin-1-secreting cell aggregate in place of an ectopic floor plate expiant. Although CP axons showed directed growth toward and penetration into the aggregate in Fig. 2A-type preparations (n = 5), they did not do so in Fig. 2C-type preparations (n = 6). These results support the view that an encounter with the floor plate by CP axons abolishes their responsiveness to netrin-1.
31. It should be noted, however, that there is evidence that floor plate cells also secrete a chemoattractant other than netrin-1 (8).
32. K. Keino-Masu et al., Cell 87, 175 (1996).
33. A. Fazeli et al., Nature 386, 796 (1997).
34. F. J. Livesey and S. P. Hunt, Mol. Cell. Neurosci. 8, 417 (1997); R. Shirasaki and F. Murakami, unpublished data.
35. F. J. Livesey and S. P. Hunt, Mol. Cell. Neurosci. 8, 417 (1997); R. Shirasaki and F. Murakami, unpublished data.
36. A. Varela-Echavarría, A. Tucker, A. W. Püschel, S. Guthrie, Neuron 18, 193 (1997).
37. R. M. Campbell and A. C. Peterson, Development 119, 1217 (1993); E. Martí, R. Takada, D. A. Bumcrot, H. Sasaki, A. P. McMahon, ibid. 121, 2537 (1995); G. Tear et al., Neuron 16, 501 (1996).
38. R. M. Campbell and A. C. Peterson, Development 119, 1217 (1993); E. Martí, R. Takada, D. A. Bumcrot, H. Sasaki, A. P. McMahon, ibid. 121, 2537 (1995); G. Tear et al., Neuron 16, 501 (1996).
39. R. M. Campbell and A. C. Peterson, Development 119, 1217 (1993); E. Martí, R. Takada, D. A. Bumcrot, H. Sasaki, A. P. McMahon, ibid. 121, 2537 (1995); G. Tear et al., Neuron 16, 501 (1996).
40. I. T. Shepherd and J. S. H. Taylor, J. Comp. Neurol. 354, 501 (1995). In our culture preparations, abrupt turning of CP axons after they crossed the floor plate and their growth along the longitudinal axis were not consistently reproduced.
41. We thank E. S. Ruthazer, N. Yamamoto, A. Tamada, Y. Oda, W.-J. Song, and H. Katsumaru for critical reading of the manuscript; M. Yamamoto for the 4D7 supernatant; M. Tessier-Lavigne for the 293 cell line; and E. S. Ruthazer for grammatical and stylistic improvement of the manuscript. Supported by a grant for priority areas (07279101) from the Ministry of Education. Science, Sports and Culture of Japan (to F.M.) and by a Postdoctoral Research Fellowship from the Japan Society for the Promotion of Science (to-R.S.). F.M. is a Core Research for Evolutional Science and Technology Project researcher.