Abstract
A novel neural surface protein, Bravo, shows a pattern of topological restriction in the embryonic chick retinotectal system. Bravo is present on the developing optic fibers in the retina; however, retinal axons in the tectum do not display Bravo. The appearance of Bravo in vitro is modulated by environmental cues. Axons growing out from retinal explants on retinal basal lamina, their natural substrate, express Bravo, whereas such axons growing on collagen do not. Retinal explants provide a valuable system to characterize the mechanism of Bravo restriction, as well as the cellular signals controlling it. Bravo was identified with monoclonal antibodies from a collection generated against exposed molecules isolated by using a selective cell surface biotinylation procedure. The NH2-terminal sequence of Bravo shows similarity with L1, a neural surface molecule which is a member of the immunoglobulin superfamily. This possible relationship to L1, together with its restricted appearance, suggests an involvement of Bravo in axonal growth and guidance.
Full Text
The Full Text of this article is available as a PDF (3.3 MB).
Selected References
These references are in PubMed. This may not be the complete list of references from this article.
- Bastiani M. J., Harrelson A. L., Snow P. M., Goodman C. S. Expression of fasciclin I and II glycoproteins on subsets of axon pathways during neuronal development in the grasshopper. Cell. 1987 Mar 13;48(5):745–755. doi: 10.1016/0092-8674(87)90072-9. [DOI] [PubMed] [Google Scholar]
- Bastiani M. J., Raper J. A., Goodman C. S. Pathfinding by neuronal growth cones in grasshopper embryos. III. Selective affinity of the G growth cone for the P cells within the A/P fascicle. J Neurosci. 1984 Sep;4(9):2311–2328. doi: 10.1523/JNEUROSCI.04-09-02311.1984. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bieber A. J., Snow P. M., Hortsch M., Patel N. H., Jacobs J. R., Traquina Z. R., Schilling J., Goodman C. S. Drosophila neuroglian: a member of the immunoglobulin superfamily with extensive homology to the vertebrate neural adhesion molecule L1. Cell. 1989 Nov 3;59(3):447–460. doi: 10.1016/0092-8674(89)90029-9. [DOI] [PubMed] [Google Scholar]
- Bixby J. L., Zhang R. Purified N-cadherin is a potent substrate for the rapid induction of neurite outgrowth. J Cell Biol. 1990 Apr;110(4):1253–1260. doi: 10.1083/jcb.110.4.1253. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bonhoeffer F., Huf J. In vitro experiments on axon guidance demonstrating an anterior-posterior gradient on the tectum. EMBO J. 1982;1(4):427–431. doi: 10.1002/j.1460-2075.1982.tb01186.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Brümmendorf T., Wolff J. M., Frank R., Rathjen F. G. Neural cell recognition molecule F11: homology with fibronectin type III and immunoglobulin type C domains. Neuron. 1989 Apr;2(4):1351–1361. doi: 10.1016/0896-6273(89)90073-1. [DOI] [PubMed] [Google Scholar]
- Chang S., Rathjen F. G., Raper J. A. Neurite outgrowth promoting activity of G4 and its inhibition by monoclonal antibodies. J Neurosci Res. 1990 Feb;25(2):180–186. doi: 10.1002/jnr.490250205. [DOI] [PubMed] [Google Scholar]
- Clark B. R., Todd C. W. Avidin as a precipitant for biotin-labeled antibody in a radioimmunoassay for carcinoembryonic antigen. Anal Biochem. 1982 Apr;121(2):257–262. doi: 10.1016/0003-2697(82)90477-8. [DOI] [PubMed] [Google Scholar]
- Crossland W. J., Cowan W. M., Rogers L. A. Studies on the development of the chick optic tectum. IV. An autoradiographic study of the development of retino-tectal connections. Brain Res. 1975 Jun 20;91(1):1–23. doi: 10.1016/0006-8993(75)90463-1. [DOI] [PubMed] [Google Scholar]
- Cunningham B. A., Hemperly J. J., Murray B. A., Prediger E. A., Brackenbury R., Edelman G. M. Neural cell adhesion molecule: structure, immunoglobulin-like domains, cell surface modulation, and alternative RNA splicing. Science. 1987 May 15;236(4803):799–806. doi: 10.1126/science.3576199. [DOI] [PubMed] [Google Scholar]
- Deschamps J. R., Hildreth J. E., Derr D., August J. T. A high-performance liquid chromatographic procedure for the purification of mouse monoclonal antibodies. Anal Biochem. 1985 Jun;147(2):451–454. doi: 10.1016/0003-2697(85)90296-9. [DOI] [PubMed] [Google Scholar]
- Dodd J., Jessell T. M. Axon guidance and the patterning of neuronal projections in vertebrates. Science. 1988 Nov 4;242(4879):692–699. doi: 10.1126/science.3055291. [DOI] [PubMed] [Google Scholar]
- Dodd J., Morton S. B., Karagogeos D., Yamamoto M., Jessell T. M. Spatial regulation of axonal glycoprotein expression on subsets of embryonic spinal neurons. Neuron. 1988 Apr;1(2):105–116. doi: 10.1016/0896-6273(88)90194-8. [DOI] [PubMed] [Google Scholar]
- Edelman G. M. CAMs and Igs: cell adhesion and the evolutionary origins of immunity. Immunol Rev. 1987 Dec;100:11–45. doi: 10.1111/j.1600-065x.1987.tb00526.x. [DOI] [PubMed] [Google Scholar]
- Edelman G. M. Cell adhesion and the molecular processes of morphogenesis. Annu Rev Biochem. 1985;54:135–169. doi: 10.1146/annurev.bi.54.070185.001031. [DOI] [PubMed] [Google Scholar]
- Edelman G. M. Modulation of cell adhesion during induction, histogenesis, and perinatal development of the nervous system. Annu Rev Neurosci. 1984;7:339–377. doi: 10.1146/annurev.ne.07.030184.002011. [DOI] [PubMed] [Google Scholar]
- Furley A. J., Morton S. B., Manalo D., Karagogeos D., Dodd J., Jessell T. M. The axonal glycoprotein TAG-1 is an immunoglobulin superfamily member with neurite outgrowth-promoting activity. Cell. 1990 Apr 6;61(1):157–170. doi: 10.1016/0092-8674(90)90223-2. [DOI] [PubMed] [Google Scholar]
- Gennarini G., Cibelli G., Rougon G., Mattei M. G., Goridis C. The mouse neuronal cell surface protein F3: a phosphatidylinositol-anchored member of the immunoglobulin superfamily related to chicken contactin. J Cell Biol. 1989 Aug;109(2):775–788. doi: 10.1083/jcb.109.2.775. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gennarini G., Rougon G., Vitiello F., Corsi P., Di Benedetta C., Goridis C. Identification and cDNA cloning of a new member of the L2/HNK-1 family of neural surface glycoproteins. J Neurosci Res. 1989 Jan;22(1):1–12. doi: 10.1002/jnr.490220102. [DOI] [PubMed] [Google Scholar]
- Halfter W., Claviez M., Schwarz U. Preferential adhesion of tectal membranes to anterior embryonic chick retina neurites. Nature. 1981 Jul 2;292(5818):67–70. doi: 10.1038/292067a0. [DOI] [PubMed] [Google Scholar]
- Halfter W., Newgreen D. F., Sauter J., Schwarz U. Oriented axon outgrowth from avian embryonic retinae in culture. Dev Biol. 1983 Jan;95(1):56–64. doi: 10.1016/0012-1606(83)90006-4. [DOI] [PubMed] [Google Scholar]
- Halfter W., Reckhaus W., Kröger S. Nondirected axonal growth on basal lamina from avian embryonic neural retina. J Neurosci. 1987 Nov;7(11):3712–3722. doi: 10.1523/JNEUROSCI.07-11-03712.1987. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Harrelson A. L., Goodman C. S. Growth cone guidance in insects: fasciclin II is a member of the immunoglobulin superfamily. Science. 1988 Nov 4;242(4879):700–708. doi: 10.1126/science.3187519. [DOI] [PubMed] [Google Scholar]
- Harris W. A., Holt C. E. Early events in the embryogenesis of the vertebrate visual system: cellular determination and pathfinding. Annu Rev Neurosci. 1990;13:155–169. doi: 10.1146/annurev.ne.13.030190.001103. [DOI] [PubMed] [Google Scholar]
- Hawkes R., Niday E., Gordon J. A dot-immunobinding assay for monoclonal and other antibodies. Anal Biochem. 1982 Jan 1;119(1):142–147. doi: 10.1016/0003-2697(82)90677-7. [DOI] [PubMed] [Google Scholar]
- Jessell T. M. Adhesion molecules and the hierarchy of neural development. Neuron. 1988 Mar;1(1):3–13. doi: 10.1016/0896-6273(88)90204-8. [DOI] [PubMed] [Google Scholar]
- Kyhse-Andersen J. Electroblotting of multiple gels: a simple apparatus without buffer tank for rapid transfer of proteins from polyacrylamide to nitrocellulose. J Biochem Biophys Methods. 1984 Dec;10(3-4):203–209. doi: 10.1016/0165-022x(84)90040-x. [DOI] [PubMed] [Google Scholar]
- LaVail J. H., Cowan W. M. The development of the chick optic tectum. I. Normal morphology and cytoarchitectonic development. Brain Res. 1971 May 21;28(3):391–419. doi: 10.1016/0006-8993(71)90053-9. [DOI] [PubMed] [Google Scholar]
- Lagenaur C., Lemmon V. An L1-like molecule, the 8D9 antigen, is a potent substrate for neurite extension. Proc Natl Acad Sci U S A. 1987 Nov;84(21):7753–7757. doi: 10.1073/pnas.84.21.7753. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Layer P. G., Alber R., Rathjen F. G. Sequential activation of butyrylcholinesterase in rostral half somites and acetylcholinesterase in motoneurones and myotomes preceding growth of motor axons. Development. 1988 Feb;102(2):387–396. doi: 10.1242/dev.102.2.387. [DOI] [PubMed] [Google Scholar]
- Matsudaira P. Sequence from picomole quantities of proteins electroblotted onto polyvinylidene difluoride membranes. J Biol Chem. 1987 Jul 25;262(21):10035–10038. [PubMed] [Google Scholar]
- Matsunaga M., Hatta K., Nagafuchi A., Takeichi M. Guidance of optic nerve fibres by N-cadherin adhesion molecules. Nature. 1988 Jul 7;334(6177):62–64. doi: 10.1038/334062a0. [DOI] [PubMed] [Google Scholar]
- McClay D. R., Ettensohn C. A. Cell adhesion in morphogenesis. Annu Rev Cell Biol. 1987;3:319–345. doi: 10.1146/annurev.cb.03.110187.001535. [DOI] [PubMed] [Google Scholar]
- Moos M., Tacke R., Scherer H., Teplow D., Früh K., Schachner M. Neural adhesion molecule L1 as a member of the immunoglobulin superfamily with binding domains similar to fibronectin. Nature. 1988 Aug 25;334(6184):701–703. doi: 10.1038/334701a0. [DOI] [PubMed] [Google Scholar]
- Pesheva P., Horwitz A. F., Schachner M. Integrin, the cell surface receptor for fibronectin and laminin, expresses the L2/HNK-1 and L3 carbohydrate structures shared by adhesion molecules. Neurosci Lett. 1987 Dec 29;83(3):303–306. doi: 10.1016/0304-3940(87)90104-2. [DOI] [PubMed] [Google Scholar]
- Puelles L., Bendala M. C. Differentiation of neuroblasts in the chick optic tectum up to eight days of incubation: a Golgi study. Neuroscience. 1978;3(3):307–325. doi: 10.1016/0306-4522(78)90079-9. [DOI] [PubMed] [Google Scholar]
- Ranscht B. Sequence of contactin, a 130-kD glycoprotein concentrated in areas of interneuronal contact, defines a new member of the immunoglobulin supergene family in the nervous system. J Cell Biol. 1988 Oct;107(4):1561–1573. doi: 10.1083/jcb.107.4.1561. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Raper J. A., Bastiani M., Goodman C. S. Pathfinding by neuronal growth cones in grasshopper embryos. I. Divergent choices made by the growth cones of sibling neurons. J Neurosci. 1983 Jan;3(1):20–30. doi: 10.1523/JNEUROSCI.03-01-00020.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Raper J. A., Bastiani M., Goodman C. S. Pathfinding by neuronal growth cones in grasshopper embryos. II. Selective fasciculation onto specific axonal pathways. J Neurosci. 1983 Jan;3(1):31–41. doi: 10.1523/JNEUROSCI.03-01-00031.1983. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rathjen F. G. A neurite outgrowth-promoting molecule in developing fiber tracts. Trends Neurosci. 1988 May;11(5):183–184. doi: 10.1016/0166-2236(88)90116-6. [DOI] [PubMed] [Google Scholar]
- Rathjen F. G., Wolff J. M., Chang S., Bonhoeffer F., Raper J. A. Neurofascin: a novel chick cell-surface glycoprotein involved in neurite-neurite interactions. Cell. 1987 Dec 4;51(5):841–849. doi: 10.1016/0092-8674(87)90107-3. [DOI] [PubMed] [Google Scholar]
- Rathjen F. G., Wolff J. M., Frank R., Bonhoeffer F., Rutishauser U. Membrane glycoproteins involved in neurite fasciculation. J Cell Biol. 1987 Feb;104(2):343–353. doi: 10.1083/jcb.104.2.343. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rutishauser U., Acheson A., Hall A. K., Mann D. M., Sunshine J. The neural cell adhesion molecule (NCAM) as a regulator of cell-cell interactions. Science. 1988 Apr 1;240(4848):53–57. doi: 10.1126/science.3281256. [DOI] [PubMed] [Google Scholar]
- Schlosshauer B., Schwarz U., Rutishauser U. Topological distribution of different forms of neural cell adhesion molecule in the developing chick visual system. Nature. 1984 Jul 12;310(5973):141–143. doi: 10.1038/310141a0. [DOI] [PubMed] [Google Scholar]
- Seeger M. A., Haffley L., Kaufman T. C. Characterization of amalgam: a member of the immunoglobulin superfamily from Drosophila. Cell. 1988 Nov 18;55(4):589–600. doi: 10.1016/0092-8674(88)90217-6. [DOI] [PubMed] [Google Scholar]
- Thanos S., Bonhoeffer F. Investigations on the development and topographic order of retinotectal axons: anterograde and retrograde staining of axons and perikarya with rhodamine in vivo. J Comp Neurol. 1983 Oct 1;219(4):420–430. doi: 10.1002/cne.902190404. [DOI] [PubMed] [Google Scholar]
- Thanos S., Dütting D. Plasticity in the developing chick visual system: topography and maintenance of experimentally induced ipsilateral projections. J Comp Neurol. 1988 Dec 8;278(2):303–311. doi: 10.1002/cne.902780212. [DOI] [PubMed] [Google Scholar]
- Updyke T. V., Nicolson G. L. Immunoaffinity isolation of membrane antigens with biotinylated monoclonal antibodies and immobilized streptavidin matrices. J Immunol Methods. 1984 Oct 12;73(1):83–95. doi: 10.1016/0022-1759(84)90034-6. [DOI] [PubMed] [Google Scholar]
- Walter J., Henke-Fahle S., Bonhoeffer F. Avoidance of posterior tectal membranes by temporal retinal axons. Development. 1987 Dec;101(4):909–913. doi: 10.1242/dev.101.4.909. [DOI] [PubMed] [Google Scholar]
- Walter J., Kern-Veits B., Huf J., Stolze B., Bonhoeffer F. Recognition of position-specific properties of tectal cell membranes by retinal axons in vitro. Development. 1987 Dec;101(4):685–696. doi: 10.1242/dev.101.4.685. [DOI] [PubMed] [Google Scholar]
- Williams A. F., Barclay A. N. The immunoglobulin superfamily--domains for cell surface recognition. Annu Rev Immunol. 1988;6:381–405. doi: 10.1146/annurev.iy.06.040188.002121. [DOI] [PubMed] [Google Scholar]
- von Boxberg Y., Wütz R., Schwarz U. Use of the biotin-avidin system for labelling, isolation and characterization of neural cell-surface proteins. Eur J Biochem. 1990 Jun 20;190(2):249–256. doi: 10.1111/j.1432-1033.1990.tb15569.x. [DOI] [PubMed] [Google Scholar]