Abstract
E10 chick sympathetic ganglion cells display a cell contact-dependent rise in choline acetyltransferase (ChAT) specific activity over the first several days in culture. This effect can be mimicked by addition of crude membrane fractions prepared from E10 retina and adult chicken brain, but not by those from E10 brain. The effects of both cell-cell and membrane-cell contact are inhibited by the addition of anti-NCAM Fab fragments. The membranes capable of increasing ChAT and those which are ineffective all contain NCAM, however their relative levels of NCAM polysialic acid differ. Whereas membranes with high polysialic acid NCAM are ineffective, selective enzymatic removal of polysialic acid renders them capable of producing an increase in ChAT. The inhibition of NCAM-mediated adhesion produced by Fab fragments can be compensated for by addition of wheat germ agglutinin, but only with membranes whose NCAM has low levels of polysialic acid. Taken together, these data suggest that NCAM can regulate cell contact-mediated increases in ChAT activity. We propose that NCAM-mediated adhesion promotes contact between cell membranes to allow the transmission of an otherwise NCAM- independent signal. In addition, NCAM's polysialic acid moiety appears to influence the ability of cells to transmit this signal, even in the presence of an alternative adhesion mechanism.
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- Acheson A. L., Thoenen H. Cell contact-mediated regulation of tyrosine hydroxylase synthesis in cultured bovine adrenal chromaffin cells. J Cell Biol. 1983 Sep;97(3):925–928. doi: 10.1083/jcb.97.3.925. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Adler J. E., Black I. B. Membrane contact regulates transmitter phenotypic expression. Brain Res. 1986 Dec;395(2):237–241. doi: 10.1016/s0006-8993(86)80202-5. [DOI] [PubMed] [Google Scholar]
- Adler J. E., Black I. B. Sympathetic neuron density differentially regulates transmitter phenotypic expression in culture. Proc Natl Acad Sci U S A. 1985 Jun;82(12):4296–4300. doi: 10.1073/pnas.82.12.4296. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Bock E., Richter-Landsberg C., Faissner A., Schachner M. Demonstration of immunochemical identity between the nerve growth factor-inducible large external (NILE) glycoprotein and the cell adhesion molecule L1. EMBO J. 1985 Nov;4(11):2765–2768. doi: 10.1002/j.1460-2075.1985.tb04001.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chang S., Rathjen F. G., Raper J. A. Extension of neurites on axons is impaired by antibodies against specific neural cell surface glycoproteins. J Cell Biol. 1987 Feb;104(2):355–362. doi: 10.1083/jcb.104.2.355. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Chuong C. M., Edelman G. M. Alterations in neural cell adhesion molecules during development of different regions of the nervous system. J Neurosci. 1984 Sep;4(9):2354–2368. doi: 10.1523/JNEUROSCI.04-09-02354.1984. [DOI] [PMC free article] [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]
- Edgar D., Barde Y. A., Thoenen H. Subpopulations of cultured chick sympathetic neurones differ in their requirements for survival factors. Nature. 1981 Jan 22;289(5795):294–295. doi: 10.1038/289294a0. [DOI] [PubMed] [Google Scholar]
- Edgar D., Timpl R., Thoenen H. The heparin-binding domain of laminin is responsible for its effects on neurite outgrowth and neuronal survival. EMBO J. 1984 Jul;3(7):1463–1468. doi: 10.1002/j.1460-2075.1984.tb01997.x. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Fonnum F. A rapid radiochemical method for the determination of choline acetyltransferase. J Neurochem. 1975 Feb;24(2):407–409. doi: 10.1111/j.1471-4159.1975.tb11895.x. [DOI] [PubMed] [Google Scholar]
- Frazier W., Glaser L. Surface components and cell recognition. Annu Rev Biochem. 1979;48:491–523. doi: 10.1146/annurev.bi.48.070179.002423. [DOI] [PubMed] [Google Scholar]
- Fukada K. Purification and partial characterization of a cholinergic neuronal differentiation factor. Proc Natl Acad Sci U S A. 1985 Dec;82(24):8795–8799. doi: 10.1073/pnas.82.24.8795. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Gray D. B., Tuttle J. B. [3H]acetylcholine synthesis in cultured ciliary ganglion neurons: effects of myotube membranes. Dev Biol. 1987 Jan;119(1):290–298. doi: 10.1016/0012-1606(87)90230-2. [DOI] [PubMed] [Google Scholar]
- Grumet M., Edelman G. M. Heterotypic binding between neuronal membrane vesicles and glial cells is mediated by a specific cell adhesion molecule. J Cell Biol. 1984 May;98(5):1746–1756. doi: 10.1083/jcb.98.5.1746. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Grumet M., Rutishauser U., Edelman G. M. Neural cell adhesion molecule is on embryonic muscle cells and mediates adhesion to nerve cells in vitro. Nature. 1982 Feb 25;295(5851):693–695. doi: 10.1038/295693a0. [DOI] [PubMed] [Google Scholar]
- Hanson G. R., Partlow L. M. A comparison of two factors affecting the proliferation of non-neuronal (glial) cells in vitro. Brain Res. 1980 Jun 23;192(2):371–381. doi: 10.1016/0006-8993(80)90890-2. [DOI] [PubMed] [Google Scholar]
- Hatten M. E. Neuronal inhibition of astroglial cell proliferation is membrane mediated. J Cell Biol. 1987 May;104(5):1353–1360. doi: 10.1083/jcb.104.5.1353. [DOI] [PMC free article] [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]
- Hawrot E. Cultured sympathetic neurons: effects of cell-derived and synthetic substrata on survival and development. Dev Biol. 1980 Jan;74(1):136–151. doi: 10.1016/0012-1606(80)90057-3. [DOI] [PubMed] [Google Scholar]
- Hoffman S., Sorkin B. C., White P. C., Brackenbury R., Mailhammer R., Rutishauser U., Cunningham B. A., Edelman G. M. Chemical characterization of a neural cell adhesion molecule purified from embryonic brain membranes. J Biol Chem. 1982 Jul 10;257(13):7720–7729. [PubMed] [Google Scholar]
- Keilhauer G., Faissner A., Schachner M. Differential inhibition of neurone-neurone, neurone-astrocyte and astrocyte-astrocyte adhesion by L1, L2 and N-CAM antibodies. Nature. 1985 Aug 22;316(6030):728–730. doi: 10.1038/316728a0. [DOI] [PubMed] [Google Scholar]
- Kessler J. A., Conn G., Hatcher V. B. Isolated plasma membranes regulate neurotransmitter expression and facilitate effects of a soluble brain cholinergic factor. Proc Natl Acad Sci U S A. 1986 May;83(10):3528–3532. doi: 10.1073/pnas.83.10.3528. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Laemmli U. K. Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature. 1970 Aug 15;227(5259):680–685. doi: 10.1038/227680a0. [DOI] [PubMed] [Google Scholar]
- Linser P. J., Perkins M. Gliogenesis in the embryonic avian optic tectum: neuronal-glial interactions influence astroglial phenotype maturation. Brain Res. 1987 Feb;428(2):277–290. doi: 10.1016/0165-3806(87)90125-8. [DOI] [PubMed] [Google Scholar]
- Linser P., Moscona A. A. Hormonal induction of glutamine synthetase in cultures of embryonic retina cells: requirement for neuron-glia contact interactions. Dev Biol. 1983 Apr;96(2):529–534. doi: 10.1016/0012-1606(83)90190-2. [DOI] [PubMed] [Google Scholar]
- Lucas C. A., Edgar D., Thoenen H. Regulation of tyrosine hydroxylase and choline acetyltransferase activities by cell density in the PC12 rat pheochromocytoma clonal cell line. Exp Cell Res. 1979 Jun;121(1):79–86. doi: 10.1016/0014-4827(79)90446-4. [DOI] [PubMed] [Google Scholar]
- Nishi R., Berg D. K. Two components from eye tissue that differentially stimulate the growth and development of ciliary ganglion neurons in cell culture. J Neurosci. 1981 May;1(5):505–513. doi: 10.1523/JNEUROSCI.01-05-00505.1981. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Peterson G. L. A simplification of the protein assay method of Lowry et al. which is more generally applicable. Anal Biochem. 1977 Dec;83(2):346–356. doi: 10.1016/0003-2697(77)90043-4. [DOI] [PubMed] [Google Scholar]
- Rathjen F. G., Rutishauser U. Comparison of two cell surface molecules involved in neural cell adhesion. EMBO J. 1984 Feb;3(2):461–465. doi: 10.1002/j.1460-2075.1984.tb01828.x. [DOI] [PMC free article] [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]
- Ratner N., Bunge R. P., Glaser L. A neuronal cell surface heparan sulfate proteoglycan is required for dorsal root ganglion neuron stimulation of Schwann cell proliferation. J Cell Biol. 1985 Sep;101(3):744–754. doi: 10.1083/jcb.101.3.744. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Ratner N., Glaser L., Bunge R. P. PC12 cells as a source of neurite-derived cell surface mitogen, which stimulates Schwann cell division. J Cell Biol. 1984 Mar;98(3):1150–1155. doi: 10.1083/jcb.98.3.1150. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rohrer H., Thoenen H., Edgar D. Presence of nerve growth factor receptors and catecholamine uptake in subpopulations of chick sympathetic neurons: correlation with survival factor requirements in culture. Dev Biol. 1983 Sep;99(1):34–40. doi: 10.1016/0012-1606(83)90251-8. [DOI] [PubMed] [Google Scholar]
- Rutishauser U. Developmental biology of a neural cell adhesion molecule. Nature. 1984 Aug 16;310(5978):549–554. doi: 10.1038/310549a0. [DOI] [PubMed] [Google Scholar]
- Rutishauser U., Grumet M., Edelman G. M. Neural cell adhesion molecule mediates initial interactions between spinal cord neurons and muscle cells in culture. J Cell Biol. 1983 Jul;97(1):145–152. doi: 10.1083/jcb.97.1.145. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rutishauser U., Hoffman S., Edelman G. M. Binding properties of a cell adhesion molecule from neural tissue. Proc Natl Acad Sci U S A. 1982 Jan;79(2):685–689. doi: 10.1073/pnas.79.2.685. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rutishauser U., Thiery J. P., Brackenbury R., Edelman G. M. Adhesion among neural cells of the chick embryo. III. Relationship of the surface molecule CAM to cell adhesion and the development of histotypic patterns. J Cell Biol. 1978 Nov;79(2 Pt 1):371–381. doi: 10.1083/jcb.79.2.371. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Rutishauser U., Watanabe M., Silver J., Troy F. A., Vimr E. R. Specific alteration of NCAM-mediated cell adhesion by an endoneuraminidase. J Cell Biol. 1985 Nov;101(5 Pt 1):1842–1849. doi: 10.1083/jcb.101.5.1842. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Saadat S., Thoenen H. Selective induction of tyrosine hydroxylase by cell-cell contact in bovine adrenal chromaffin cells is mimicked by plasma membranes. J Cell Biol. 1986 Nov;103(5):1991–1997. doi: 10.1083/jcb.103.5.1991. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Salzer J. L., Bunge R. P., Glaser L. Studies of Schwann cell proliferation. III. Evidence for the surface localization of the neurite mitogen. J Cell Biol. 1980 Mar;84(3):767–778. doi: 10.1083/jcb.84.3.767. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Salzer J. L., Bunge R. P. Studies of Schwann cell proliferation. I. An analysis in tissue culture of proliferation during development, Wallerian degeneration, and direct injury. J Cell Biol. 1980 Mar;84(3):739–752. doi: 10.1083/jcb.84.3.739. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Salzer J. L., Williams A. K., Glaser L., Bunge R. P. Studies of Schwann cell proliferation. II. Characterization of the stimulation and specificity of the response to a neurite membrane fraction. J Cell Biol. 1980 Mar;84(3):753–766. doi: 10.1083/jcb.84.3.753. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Silver J., Rutishauser U. Guidance of optic axons in vivo by a preformed adhesive pathway on neuroepithelial endfeet. Dev Biol. 1984 Dec;106(2):485–499. doi: 10.1016/0012-1606(84)90248-3. [DOI] [PubMed] [Google Scholar]
- Stallcup W. B., Beasley L. Involvement of the nerve growth factor-inducible large external glycoprotein (NILE) in neurite fasciculation in primary cultures of rat brain. Proc Natl Acad Sci U S A. 1985 Feb;82(4):1276–1280. doi: 10.1073/pnas.82.4.1276. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thanos S., Bonhoeffer F., Rutishauser U. Fiber-fiber interaction and tectal cues influence the development of the chicken retinotectal projection. Proc Natl Acad Sci U S A. 1984 Mar;81(6):1906–1910. doi: 10.1073/pnas.81.6.1906. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Thiery J. P., Duband J. L., Rutishauser U., Edelman G. M. Cell adhesion molecules in early chicken embryogenesis. Proc Natl Acad Sci U S A. 1982 Nov;79(21):6737–6741. doi: 10.1073/pnas.79.21.6737. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Tosney K. W., Watanabe M., Landmesser L., Rutishauser U. The distribution of NCAM in the chick hindlimb during axon outgrowth and synaptogenesis. Dev Biol. 1986 Apr;114(2):437–452. doi: 10.1016/0012-1606(86)90208-3. [DOI] [PubMed] [Google Scholar]
- Towbin H., Staehelin T., Gordon J. Electrophoretic transfer of proteins from polyacrylamide gels to nitrocellulose sheets: procedure and some applications. Proc Natl Acad Sci U S A. 1979 Sep;76(9):4350–4354. doi: 10.1073/pnas.76.9.4350. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Vogel Z., Sytkowski A. J., Nirenberg M. W. Acetylcholine receptors of muscle grown in vitro. Proc Natl Acad Sci U S A. 1972 Nov;69(11):3180–3184. doi: 10.1073/pnas.69.11.3180. [DOI] [PMC free article] [PubMed] [Google Scholar]
- Wakade A. R., Edgar D., Thoenen H. Substrate requirement and media supplements necessary for the long-term survival of chick sympathetic and sensory neurons cultured without serum. Exp Cell Res. 1982 Jul;140(1):71–78. doi: 10.1016/0014-4827(82)90157-4. [DOI] [PubMed] [Google Scholar]
- White H. L., Cavallito C. J. Inhibition of bacterial and mammalian choline acetyltransferases by styrylpyridine analogues. J Neurochem. 1970 Nov;17(11):1579–1589. doi: 10.1111/j.1471-4159.1970.tb03728.x. [DOI] [PubMed] [Google Scholar]
- Zurn A. D., Mudry F. Conditions increasing the adrenergic properties of dissociated chick superior cervical ganglion neurons grown in long-term culture. Dev Biol. 1986 Oct;117(2):365–379. doi: 10.1016/0012-1606(86)90306-4. [DOI] [PubMed] [Google Scholar]