Expression of polysialylated N-CAM in the central nervous system of adult canaries and its possible relation to function
Corresponding Author
P. Rousselot
The Rockefeller University, Field Research Center, Millbrook, New York 12545
Field Research Center, Rockefeller University, Tyrrel Road, Mfllbrook, NY 12545Search for more papers by this authorF. Nottebohm
The Rockefeller University, Field Research Center, Millbrook, New York 12545
Search for more papers by this authorCorresponding Author
P. Rousselot
The Rockefeller University, Field Research Center, Millbrook, New York 12545
Field Research Center, Rockefeller University, Tyrrel Road, Mfllbrook, NY 12545Search for more papers by this authorF. Nottebohm
The Rockefeller University, Field Research Center, Millbrook, New York 12545
Search for more papers by this authorAbstract
Polysialylated neuronal cell adhesion molecule (PSAqN-CAM) is a cell surface molecule associated with neurons that undergo changes in configuration or spatial translocation. In both cases, this molecule is thought to reduce the adhesivity of these cells or of their processes, which can thereby insinuate themselves into the existing parenchyma. We used a monoclonal antibody specific to PSA to offer what we believe is the first account of the distribution of PSA-N-CAM in the adult songbird brain. This antibody stained a diversity of cell classes and processes, as follows: (1) a subset of ventricular zone cells; (2) migrating cells thought to be neuroblasts; (3) a subset of differentiated neurons; (4) some brain surface astrocytes; (5) some tanycytes; (6) the neuropil of some regions; (7) some axonal fibers; and (8) possibly some synapses. Our results demonstrate also, for the first time, the wide distribution of a very numerous population of migrating cells in the telencephalon and the seasonal regulation of PSA-Nq-CAM expression in a part of the adult brain known to undergo seasonal changes in cell recruitment and function. However, we did not find PSA-N-CAM associated with young migrating cells in the high vocal center (HVC), nor was there PSA-N-CAM in the robust nucleus of the archistriatum (RA), which is known to receive new axonal endings from HVC. In these instances spatial translocation may occur with the assistance of other surface molecules. © 1995 Wiley-Liss, Inc.
Literature Cited
- Acheson, A., J. L., Sunshine, and U. Rutishauser (1991) NCAM polysialic acid can regulate both cell-cell and cell-substrate interactions. J. Cell Biol. 114: 143–153.
- Altman, J. (1970) Postnatal neurogenesis and the problem of neural plasticity. In W. A. Himwich (ed): Developmental Neurobiology. Springfield: C. C. Thomas, pp. 197–237.
- Altman, J., and G. D. Das (1965) Autoradiographic and histological evidence of postnatal hippocampal neurogenesis in rats. J. Comp. Neurol. 124: 319–336.
- Alvarez-Buylla, A. (1991) Neurogenesis and plasticity in the CNS of adult birds. Exp. Neurol. 115: 110–114.
- Alvarez-Buylla, A., and F. Nottebohm (1988) Migration of young neurons in adult avian brain. Nature 335: 353–354.
- Alvarez-Buylla, A., D. R., Buskirk, and F. Nottebohm (1987) Monoclonal antibody reveals radial glia in adult avian brain. J. Comp. Neurol. 264: 159–170.
- Alvarez-Buylla, A., M., Theelen, and F. Nottebohm (1988) Mapping of radial glia and of a new cell type in adult canary brain. J. Neurosci. 8: 2707–2712.
- Alvarez-Buylla, A., J. R., Kirn, and F. Nottebohm (1990a) Birth of projection neurons in adult avian brain may be related to perceptual or motor learning. Science 249: 1444–1446.
- Alvarez-Buylla, A., M., Theelen, and F. Nottebohm (1990b) Proliferation “hot spots” in adult avian ventricular zone reveal radial cell division. Neuron 5: 101–109.
- Alvarez-Buylla, A., C. Y., Ling, and W. S. Yu (1994) Contribution of neurons born during embryonic, juvenile and adult life to the brain of adult canaries: regional specificity and delayed birth of neurons in the song nuclei. J. Comp. Neurol. 347: 233–248.
- Barnea, A., and F. Nottebohm (1994) Seasonal recruitment of hippocampal neurons in adult free-ranging black-capped chickadees. Proc. Natl. Acad. Sci. U.S.A. 91: 11217–11221.
- Bayer, S. A., J. W., Yackel, and P. S. Puri (1982) Neurons in the rat dentate gyrus granular layer substantially increase duringjuvenile and adult life. Science 216: 890–892.
- Bernocchi, G., E. Scherini, S. Giacometti, and V. Mares (1990) Premitotic DNA synthesis in the brain of the adult frog (Rana esculenta L.): an autoradiographic 3H-thymidine study. Anat. Rec. 228: 461–470.
- Birse, S. C., R. B., Leonard, and R. E. Coggeshall (1980) Neuronal increase in various areas of the nervous system of the guppy, Lebistes. J. Comp. Neurol. 194: 291–301.
- Boisseau, S., J., Nedelec, V. Poirier, G. Rougon, and M. Simonneau (1991) Analysis of high PSA N-CAM expression during mammalian spinal cord and peripheral nervous system development. Development 112: 69–82.
- Bonfanti, L., and D. T. Theodosis (1994) Expression of polysialylated neural cell adhesion molecule by proliferating cells in the subependymal layer of the adult rat, in its rostral extension and in the olfactory bulb. Neuroscience 62: 291–305.
- Bonfanti, L., S., Olive, D. A. Poulain, and D. T. Theodosis (1992) Mapping of the distribution of polysialylated neural cell adhesion molecule throughout the central nervous system of the adult rat: an immunohistochemical study. Neuroscience 49: 419–436.
- Bonfanti, L., D. A., Poulain, and D. T. Theodosis (1993) Putative factors implicated in the structural plasticity of the hypothalamo-neurohypophy-sial system. Regul. Pept. 45: 165–170.
- Chetverukhin, V. K., and A. L. Polenov (1993) Ultrastructural radioautographic analysis of neurogenesis in the hypothalamus of the adult frog, Rana temporaria, with special reference to physiological regeneration of the preoptic nucleus. I. Ventricular zone cell proliferation. Cell Tissue Res. 271: 341–350.
- Corotto, F. S., J. A., Henegar, and J. A. Maruniak (1993) Neurogenesis persists in the subependymal layer of the adult mouse brain. Neurosci. Lett. 149: 111–114.
- Dahm, I., and L. Landmeser (1988) The regulation of intramuscular nerve branching during normal development and following activity blockade. Dev. Biol. 130: 621–644.
- Edelman, G. M. (1984) Modulation of cell adhesion during induction, histogenesis, and perinatal development of the nervous system. Annu. Rev. Neurosci. 7: 339–377.
- Fredette, B., U., Rutishauser, and L. Landmesser (1993) Regulation and activity-dependence of N-adherin, NCAM isoforms, and polysialic acid on chick myotubes during development. J. Cell Biol. 123: 1867–1888.
- Garcia-Verdugo, J. M., S., Llahi, I. Ferrer, and C. Lopez-Garcia (1989) Postnatal neurogenesis in the olfactory bulbs of a lizard. A tritiated thymidine autoradiographic study. Neurosci. Lett. 98: 247–252.
- Goldman, S. A., and F. Nottebohm (1983) Neuronal production, migration, and differentiation in a vocal control nucleus of the adult female canary brain. Proc. Natl. Acad. Sci. U.S.A. 80: 2390–2394.
- Hayrinen, J., D., Bitter-Suermann, and J. Finne (1989) Interaction of meningococcal group B monoclonal antibody and its Fab fragment with alpha 2-8-linked sialic acid polymers: requirement of a long oligosaccharide segment for binding. Mol. Immunol. 26: 523–529.
- Hoffman, S., and G. M. Edelman (1983) Kinetics of homophilic binding by embryonic and adult forms of the neural cell adhesion molecule. Proc. Natl. Acad. Sci. U.S.A. 80: 5762–5766.
- Hoffman, S., B. C., Sorkin, P. C. White, R. Brackenbury, R. Mailhammer, U. Rutishauser, B. A. Cunningham, and G. M. Edelman (1982) Chemical characterization of a neural cell adhesion molecule purified from embryonic brain membranes. J. Biol. Chem. 257: 7720–7729.
- Hynes, R. O., and A. D. Lander (1992) Contact and adhesive specificities in the associations, migrations, and targeting of cells and axons. Cell 68: 303–322.
- Kaplan, M. S. (1983) Proliferation of subependymal cells in the adult primate CNS: differential uptake of DNA labeled precursors. J. Hirnforsch. 24: 23–33.
- Kaplan, M. S., and J. W. Hinds (1977) Neurogenesis in the adult rat: electron microscopic analysis of light radioautographs. Science 197: 1092–1094.
- Kirn, J., B., O'Loughlin, S. Kasparian, and F. Nottebohni (1994) Cell death and neuronal recruitment in the high vocal center of adult male canaries are temporally related to changes in song. Proc. Natl. Acad. Sci. U.S.A. 91: 7844–7848.
- Kishi, K. (1987) Golgi studies on the development of granule cells of the rat olfactory bulb with reference to migration in the subependymal layer. J. Comp. Neurol. 258: 112–124.
- Landmesser, L., L., Dahm, J. C. Tang, and U. Rutishauser (1990) Polysialic acid as a regulator of intramuscular nerve branching during embryonic development. Neuron 4: 655–667.
- Le Gal La Salle, G., G. Rougon, and A. Valin (1992) The embryonic form of neural cell surface molecule (E-NCAM) in the rat hippocampus and its reexpression on glial cells following kainic acid-induced status epilepticus. J. Neurosci. 12: 872–882.
- Lopez-Garcia, C., A., Molowny, J. M. Garcia-Verdugo, and I. Ferrer (1988) Delayed postnatal neurogenesis in the cerebral cortex of lizards. Dev. Brain Res. 43: 167–174.
- Luskin, M. B. (1993) Restricted proliferation and migration of postnatally generated neurons derived from the forebrain subventricular zone. Neuron 11: 173–189.
- Miragall, F., G., Kadmon, M. Husmann, and M. Schachner (1988) Expression of cell adhesion molecules in the olfactory system of the adult mouse: presence of the embryonic form of N-CAM. Dev. Biol. 129: 516–531.
- Nottebohm, F. (1985) Neuronal replacement in adulthood. Ann. N. Y. Acad. Sci. 457: 143–161.
- Nottebohm, F., T. M., Stokes, and C. M. Leonard (1976) Central control of song in the canary, Serinus canaria. J. Comp. Neurol. 165. 457–486.
- Nottebohm, F., D. B., Kelley, and J. A. Paton (1982) Connections of vocal control nuclei in the canary telencephalon. J. Comp. Neurol. 207: 344–357.
- Nottebohm, F., M. E., Nottebohm, L. A. Crane, and J. C. Wingfield (1987) Seasonal changes in gonadal hormone levels of adult male canaries and their relation to song. Behav. Neurol. Biol. 47: 197–211.
- Nybroe, O., and E. Bock (1990) Structure and function of the neural cell adhesion molecules NCAM and L1. Adv. Exp. Med. Biol. 265: 185–196.
- Ono, K., H., Tomasiewicz, T. Magnuson, and U. Rutishauser (1994) N-CAM mutation inhibits tangential neuronal migration and is phenocopied by enzymatic removal of polysialic acid. Neuron 13: 595–609.
- Perez-Sanchez, F., A., Molowny, J. M. Garcia-Verdugo, and C. Lopez-Garcia (1989) Postnatal neurogenesis in the nucleus sphericus of the lizard, Podarcis hispanica. Neurosci. Lett. 106: 71–75.
- Polenov, A. L., and V. K. Chetverukhin (1993) Ultrastructural radioautographic analysis of neurogenesis in the hypothalamus of the adult frog, Rana temporaria, with special reference to physiological regeneration of the preoptic nucleus. II. Types of neuronal cells produced. Cell Tissue Res. 271: 351–362.
- Raymond, P. A. (1991) Retinal regeneration in teleost fish. Ciba Found. Symp. 160: 171–186.
- Raymond, P. A., and S. S. Easter (1983) Post-embryonic growth of the optic tectum in goldfish. I. Location of germinal cells and numbers of neurons produced. J. Neurosci. 3: 1077–1091.
- Rougon, G., C., Dubois, N. Buckley, J. L. Magnani, and W. Zollinger (1986) A monoclonal antibody against meningococcus group B polysaccharides distinguishes embryonic from adult N-CAM. J. Cell Biol. 103: 2429–2437.
- Rousselot, P., C., Lois, and A. Alvarez-Buylla (1995) Embryonic (PSA) N-CAM reveals chains of migrating neuroblasts between the lateralventricle and the olfactory bulb of adult mice. J. Comp. Neurol. 351: 51–61.
- Rutishauser, U. (1989) Membrane apposition as a regulating parameter in cell-cell interactions. In L. T. Landmesser (ed): The Assembly of the Nervous System. New York: Alan R. Liss, pp. 137–149.
- Rutishauser, U. (1993) Adhesion molecules of the nervous system. Curr. Opin. Neurobiol. 3: 709–715.
- Rutishauser, U., and L. Landinesser (1991) Polysialic acid on the surface of axons regulates patterns of normal and activity-dependent innervation. Trends Neurosci. 14: 528–532.
- Rutishauser, U., A., Acheson, A. K. Hall, D. M. Mann, and J. Sunshine (1988) The neural cell adhesion molecule (NCAM) as a regulator of cell-cell interactions. Science 240: 53–57.
- Seki, T., and Y. Arai (1991a) Expression of highly polysialylated NCAM in the neocortex and piriform cortex of the developing and the adult rat. Anat. Embryol. (Berl.) 184: 395–401.
- Seki, T., and Y. Arai (1991b) The persistent expression of a highly polysialylated NCAM in the dentate gyrus of the adult rat. Neurosci. Res. 12: 503–513.
- Shu, S., G., Ju, and L. Fan (1988) The glucose oxidase-DAB-nickel method in peroxidase histochemistry of the nervous system. Neurosci. Lett. 85: 169–171.
- Stokes, T. M., C. M., Leonard, and F. Nottebohm (1974) The telencephalon, diencephalon, and mesencephalon of the canary, Serinus canaria, in stereotaxic coordinates. J. Comp. Neurol. 156. - 337–374.
- Szele, F. G., J. J., Dowling, C. Gonzales, M. Theveniau, G. Rougon, and M. -F. Chesselet (1994) Pattern of expression of highly polysialylated neural cell adhesion molecule in the developing and adult rat striatum. Neuroscience 60: 133–144.
- Tang, J., L., Landmesser, and U. Rutishauser (1992) Polysialic acid influences specific pathfinding by avian motoneurons. Neuron 8: 1031–1044.
- Tang, J., U., Rutishauser, and L. Landmesser (1994) Polysialic acid regulates growth cone behavior during sorting or motor axons in the plexus region. Neuron 13: 405–414.
- Theodosis, D. T., and D. A. Poulain (1993) Activity-dependent neuronal-glial and synaptic plasticity in the adult mammalian hypothalamus. Neuroscience 57: 501–535.
- Theodosis, D. T., G., Rougon, and D. A. Poulain (1991) Retention of embryonic features by an adult neuronal system capable of plasticity: polysialylated neural cell adhesion molecule in the hypothalamo-neurohypophysial system. Proc. Natl. Acad. Sci. U.S.A. 88: 5494–5498.
- Tomasiewicz, H., K., Ono, D. Yee, C. Thompson, C. Goridis, U. Rutishauser, and T. Magnuson (1993) Genetic deletion of a neural cell adhesion molecule variant (N-CAM-180) produces distinct defects in the central nervous system. Neuron 11: 1163–1174.
-
Townes, P., and
J. Holtfreter
(1955)
Directed movements and selective adhesion of embryonic amphibian cells.
J. Exp. Zool.
128:
53–120.
10.1002/jez.1401280105 Google Scholar
- Wang, C., G., Rougon, and J. Z. Kiss (1994) Requirement of polysialic acid for the migration of the 0–2A glial progenitor cell from neurohypophyseal explants. J. Neurosci. 14: 4446–4457.
- Wilson, S. W., and S. S. Easter, Jr. (1991) A pioneering growth cone in the embryonic zebrafish brain. Proc. Natl. Acad. Sci. U.S.A. 88: 2293–2296.
- Zuber, C., P. M., Lackie, W. A. Catterall, and J. Roth (1992) Polysialic acid is associated with sodium channels and the neural c611 adhesion molecule N-CAM in adult rat brain. J. Biol. Chem. 267: 9965–9971.