Lamina-specific connectivity in the brain: Regulation by N-cadherin, neurotrophins, and glycoconjugates

Science

Volumn 276, Issue 5317, 1997, Pages 1428-1431

  Inoue, Akihiro ^a   Sanes, Joshua R ^a  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIBODY; BRAIN DERIVED NEUROTROPHIC FACTOR; CADHERIN; GLYCOCONJUGATE; MONOCLONAL ANTIBODY; NERVE GROWTH FACTOR; NEUROTROPHIN; NEUROTROPHIN 3; PLANT LECTIN;

ANIMAL TISSUE; ARTICLE; BRAIN; CHICKEN; COCULTURE; CONTROLLED STUDY; ELECTRON MICROSCOPY; NERVE FIBER GROWTH; NEURITE; NONHUMAN; OPTIC TECTUM; PRIORITY JOURNAL; RETINA; SYNAPSE;

ANIMALS; AXONS; BASEMENT MEMBRANE; BRAIN; CADHERINS; CELL DIVISION; CHICK EMBRYO; COCULTURE TECHNIQUES; GLYCOCONJUGATES; NERVE GROWTH FACTORS; NEURITES; QUAIL; RETINA; SUPERIOR COLLICULUS; VISUAL PATHWAYS;

EID: 0031007904     PISSN: 00368075     EISSN: None     Source Type: Journal    
DOI: 10.1126/science.276.5317.1428     Document Type: Article

References (43)

1. S. A. Bayer and J. Altman, Prog. Neurobiol. 29, 57 (1987); L. C. Katz and E. M. Callaway, Annu. Rev. Neurosci. 15, 31 (1992).
2. S. A. Bayer and J. Altman, Prog. Neurobiol. 29, 57 (1987); L. C. Katz and E. M. Callaway, Annu. Rev. Neurosci. 15, 31 (1992).
3. J. Bolz, M. Götz, M. Hübener, N. Novak, Trends Neurosci. 16, 310 (1993); M. Frotscher and B. Heimrich, J. Neurobiol. 26, 350 (1995).
4. J. Bolz, M. Götz, M. Hübener, N. Novak, Trends Neurosci. 16, 310 (1993); M. Frotscher and B. Heimrich, J. Neurobiol. 26, 350 (1995).
5. C. J. Shatz, Proc. Natl. Acad. Sci. U.S.A. 93, 602 (1996).
6. S. P. Hunt and N. Brecha, in Comparative Neurology of the Optic Tectum, H. Vanegas, Ed. (Plenum, New York, 1984), pp. 619-648; H. J. Karten, A. Reiner, N. Brecha, in Cytochemical Methods in Neuroanatomy, V. Chan-Palay and S. L. Palay, Eds. (Liss, New York, 1982), pp. 189-204.
7. S. P. Hunt and N. Brecha, in Comparative Neurology of the Optic Tectum, H. Vanegas, Ed. (Plenum, New York, 1984), pp. 619-648; H. J. Karten, A. Reiner, N. Brecha, in Cytochemical Methods in Neuroanatomy, V. Chan-Palay and S. L. Palay, Eds. (Liss, New York, 1982), pp. 189-204.
8. M. Yamagata and J. R. Sanes, Development 121, 189 (1995).
9. _, ibid., p. 3763.
10. M. Yamagata, J. P. Hermann, J. R. Sanes, J. Neurosci. 15, 4556 (1995).
11. L. Schnell, R. Schneider, R. Kolbeck, Y.-A. Barde, M. E. Schwab, Nature 367, 170 (1994); R. J. Cabelli, A. Hohn, C. J. Shatz, Science 267, 1662 (1995); N. Prakash, S. Cohen-Corey, R. D. Frostig, Nature 381, 702 (1996).
12. L. Schnell, R. Schneider, R. Kolbeck, Y.-A. Barde, M. E. Schwab, Nature 367, 170 (1994); R. J. Cabelli, A. Hohn, C. J. Shatz, Science 267, 1662 (1995); N. Prakash, S. Cohen-Corey, R. D. Frostig, Nature 381, 702 (1996).
13. L. Schnell, R. Schneider, R. Kolbeck, Y.-A. Barde, M. E. Schwab, Nature 367, 170 (1994); R. J. Cabelli, A. Hohn, C. J. Shatz, Science 267, 1662 (1995); N. Prakash, S. Cohen-Corey, R. D. Frostig, Nature 381, 702 (1996).
14. S. Cohen-Corey and S. E. Fraser, Nature 378, 192 (1995).
15. M. Matsunaga, K. Hatta, M. Takeichi, Neuron 1, 289 (1988); M. Takeichi, Curr. Opin. Cell Biol. 7, 619 (1995).
16. M. Matsunaga, K. Hatta, M. Takeichi, Neuron 1, 289 (1988); M. Takeichi, Curr. Opin. Cell Biol. 7, 619 (1995).
17. A. M. Fannon and D. R. Colman, Neuron 17, 423 (1996); N. Uchida, Y. Honjo, K. R. Johnson, M. J. Wheelock, M. Takeichi, J. Cell Biol. 135, 767 (1996).
18. A. M. Fannon and D. R. Colman, Neuron 17, 423 (1996); N. Uchida, Y. Honjo, K. R. Johnson, M. J. Wheelock, M. Takeichi, J. Cell Biol. 135, 767 (1996).
19. Culture methods were modified from (5). Tecta from E17-E18 embryos were fixed in 3% paraformaldehyde and sectioned horizontally at 150 μm with a vibratome. Sections were mounted on Nuclepore filters (Costar). E6.5 retinas were flattened onto nitro-cellulose membranes and cut perpendicular to the optic fissure at 300 μm. Retinal strips from the dorso-central retina were then laid atop tectal sections. Cocultures were incubated in a 1:1 mixture of hybridoma-conditioned and fresh media containing 30% Ham's F12, 30% Dulbecco's modified Eagle's medium, 10% fetal calf serum, 10% (v/v) E12 embryo extract, 2.5 mM glutamine, 17.5 mM glucose, and 25 mM Hepes. The final concentration of antibody was ∼50 μg/ml. The medium was changed every other day for 6 days.
20. NCD-2; K. Hatta and M. Takeichi, Nature 320, 447 (1986).
21. Cocultures were incubated in 10 μM calcein AM (Molecular Probes, Eugene, OR), a vital stain, to label retinal neurites, plus Hoechst 33342 (5 ng/ml, Molecular Probes), a nuclear stain, to identify tectal laminae. Calcein-stained neurites and laminar boundaries were drawn with a camera lucida.
22. M. Matsunaga, K. Hatta, A. Nagafuchi, M. Takeichi, Nature 334, 62 (1988); J. Bixby and R. Zhang, J. Cell Biol. 110, 1253 (1990).
23. M. Matsunaga, K. Hatta, A. Nagafuchi, M. Takeichi, Nature 334, 62 (1988); J. Bixby and R. Zhang, J. Cell Biol. 110, 1253 (1990).
24. P. Doherty and F. S. Walsh, Curr. Opin. Neurobiol. 4, 49 (1994). Antibodies used were mAb H23 for L1 (7) and mAB 224-1A6 for N-CAM [V. Lemmon, E. B. Staros, H. E. Perry, D. I. Gottlieb, Dev. Brain Res. 3, 349 (1982)].
25. P. Doherty and F. S. Walsh, Curr. Opin. Neurobiol. 4, 49 (1994). Antibodies used were mAb H23 for L1 (7) and mAB 224-1A6 for N-CAM [V. Lemmon, E. B. Staros, H. E. Perry, D. I. Gottlieb, Dev. Brain Res. 3, 349 (1982)].
26. A. Inoue and J. R. Sanes, data not shown.
27. J. R. Sanes and J. M. Cheney, Nature 300, 646 (1982); P. T. Martin and J. R. Sanes, Neuron 14, 743 (1995).
28. J. R. Sanes and J. M. Cheney, Nature 300, 646 (1982); P. T. Martin and J. R. Sanes, Neuron 14, 743 (1995).
29. To initiate neunte outgrowth, we incubated cocultures for 18 hours in serum-containing medium (12) and then transferred the culture-bearing filters to serum-free Neurobasal medium with B27 supplement (Gibco-BRL) with or without VVA-B4 (Sigma), mouse NGF, human BDNF, NT-3, or NT-4/5 (PeproTech, Rocky Hill, NJ), all at 5 to 20 μg/ml.
30. F. Hallböök, A. Bäckström, K. Kullander, T. Ebendal, N. G. Carri, J. Comp. Neurol. 364, 664 (1996); S. Cohen-Corey and S. E. Fraser, Neuron 12, 747 (1994).
31. F. Hallböök, A. Bäckström, K. Kullander, T. Ebendal, N. G. Carri, J. Comp. Neurol. 364, 664 (1996); S. Cohen-Corey and S. E. Fraser, Neuron 12, 747 (1994).
32. H. Sawai, D. B. Clarke, P. Kittlerova, G. M. Bray, A. J. Aguayo, J. Neurosci. 16, 3887 (1996); E. J. de la Rosa, A. Arribas, J. M. Frade, A. Rodriguez-Téber, Neuroscience 58, 347 (1994).
33. H. Sawai, D. B. Clarke, P. Kittlerova, G. M. Bray, A. J. Aguayo, J. Neurosci. 16, 3887 (1996); E. J. de la Rosa, A. Arribas, J. M. Frade, A. Rodriguez-Téber, Neuroscience 58, 347 (1994).
34. 4 cells per microliter. Left tecta were injected with 5 to 7 μi of cell suspension or VVA-B4 (1 mg/ml) at E6-E10 (hybridomas) or at E10-E11 (QT6 cells or WA-B4). Manipulated embryos were killed at E14. Only embryos that had reached stage 40 [V. Hamburger and H. L. Hamilton, J. Morphol. 88, 49 (1951)) were analyzed.
35. Cryostat sections were incubated with antibody to the 200-kD neurofilament subunit (Sigma), L1 mAb, or N-CAM mAb (16), followed by second antibodies and Hoechst 33342. Application of second antibody alone confirmed that N-cadherin mAb had penetrated the full thickness of the tectum. Likewise, injection of fluorescein-VVA-B4 (Sigma) demonstrated penetration of the lectin.
36. The right eye was exposed, and a hole was made with a tungsten needle at a temporal-dorsal position. Dil (Molecular Probes) was then injected through the hole with a microelectrode. One day later, embryos were killed, staged, and fixed in 4% paraformaldehyde. Vibratome sections (90 μm) were counter-stained with Hoechst 33342.
37. Digital images were analyzed with IP Lab Spectrum, version 2.5.7 (Signal Analysis, Vienna, VA). Laminar boundaries were determined by staining with Hoechst 33342. The increased density in BDNF-treated tecta could reflect either a greater number of retinal axons or a greater degree of arborization. We could not distinguish these alternatives in vivo, but we favor increased arborization on the basis of the in vitro results.
38. H. Thoenen, Science 270, 593 (1995); T. Bonhoeffer, Curr. Opin. Neurobiol. 6, 119 (1996).
39. H. Thoenen, Science 270, 593 (1995); T. Bonhoeffer, Curr. Opin. Neurobiol. 6, 119 (1996).
40. J. R. Naegele and L. C. Katz, J. Neurosci. 10, 540 (1990); F. Nakagawa, B. A. Schulte, S. S. Spicer, J. Comp. Neurol. 243, 280 (1986); M. Ichikawa, S. Takami, T. Osada, P. P. C. Graziadei, Dev. Brain Res. 78, 1 (1994).
41. J. R. Naegele and L. C. Katz, J. Neurosci. 10, 540 (1990); F. Nakagawa, B. A. Schulte, S. S. Spicer, J. Comp. Neurol. 243, 280 (1986); M. Ichikawa, S. Takami, T. Osada, P. P. C. Graziadei, Dev. Brain Res. 78, 1 (1994).
42. J. R. Naegele and L. C. Katz, J. Neurosci. 10, 540 (1990); F. Nakagawa, B. A. Schulte, S. S. Spicer, J. Comp. Neurol. 243, 280 (1986); M. Ichikawa, S. Takami, T. Osada, P. P. C. Graziadei, Dev. Brain Res. 78, 1 (1994).
43. We thank E. Johnson for mouse NGF, Regeneron Pharmaceuticals (Tarrytown, NY) for human BDNF, J. Cunningham and R. Lewis for technical assistance, and M. Yamagata for advice. Supported by a grant to J.R.S. from NIH. A.I. was a fellow of the Human Frontier Science Program.