Home LiteratureArticle Details
PMID: 7957094 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't

Activity-dependent mobilization of the adhesion molecule polysialic NCAM to the cell surface of neurons and endocrine cells.

The EMBO journal ·Vol. 13 ·No. 22 ·1994-11-15 ·Pages 5284-92

Kiss JZ, Wang C, Olive S, Rougon G, Lang J, Baetens D, Harry D, Pralong WF

Abstract

The alpha-2,8-linked sialic acid polymer (PSA) on the neural cell adhesion molecule (NCAM) is an important regulator of cell surface interactions. We have examined the translocation of PSA-NCAM to the surface of cultured cortical neurons and insulin secreting beta cells under different conditions of cell activity. Endoneuraminidase N, an enzyme that specifically cleaves PSA chains, was used to remove pre-existing PSA from the plasma membrane and the re-expression of the molecule was monitored by immunocytochemistry. Punctate PSA immunostaining was restored on the surface of 68% of neurons within 1 h. This recovery was almost completely prevented by tetrodotoxin, suggesting that spontaneous electrical activity is required. K+ depolarization (50 mM) allowed recovery of PSA surface staining in the presence of tetrodotoxin and this effect required the presence of extracellular Ca2+. Rapid redistribution of PSA-NCAM to the surface of beta cells was observed under conditions that stimulate insulin secretion. Ca2+ channel inhibition decreased both PSA-NCAM expression and insulin secretion to control, non-stimulated levels. Finally, subcellular fractionation of an insulin-secreting cell line showed that the secretory vesicle fraction is highly enriched in PSA-NCAM. These results suggest that PSA-NCAM can be translocated to the cell surface via regulated exocytosis. Taken together, our results provide unprecedented evidence linking cell activity and PSA-NCAM expression, and suggest a mechanism for rapid modulation of cell surface interactions.

MeSH Terms
Animals Animals, Newborn Calcium Channel Blockers/pharmacology Cell Adhesion Cell Adhesion Molecules, Neuronal/metabolism Cerebral Cortex/cytology Exocytosis/drug effects Flow Cytometry Fluorescent Antibody Technique Glycoside Hydrolases/metabolism Glycosylation Insulin/metabolism Insulin Secretion Islets of Langerhans/cytology,metabolism N-Acetylneuraminic Acid Neurons/cytology,metabolism Polymers Protein Processing, Post-Translational Rats Sialic Acids/metabolism Tetrodotoxin/pharmacology
Chemicals
Calcium Channel Blockers Cell Adhesion Molecules, Neuronal Insulin Polymers Sialic Acids Tetrodotoxin Glycoside Hydrolases endo-alpha-sialidase N-Acetylneuraminic Acid
Authors & Affiliations
8 authors, click to expand affiliations / ORCID
Kiss J Z
Department of Morphology, University of Geneva Medical School, Switzerland.
Wang C
Olive S
Rougon G
Lang J
Baetens D
Harry D
Pralong W F
References (58)
58 references, click to expand
  1. Generation of multiple N-CAM polypeptides from a single gene.
    Bioessays. 1989 Oct;11(4):83-8 PMID: 2695078
  2. Developmental control of N-CAM sialylation state by Golgi sialyltransferase isoforms.
    Development. 1988 Sep;104(1):147-54 PMID: 3253055
  3. Neurite outgrowth in response to transfected N-CAM changes during development and is modulated by polysialic acid.
    Neuron. 1990 Aug;5(2):209-19 PMID: 2200449
  4. Insulin cells of pancreas extend neurites but do not arise from the neuroectoderm.
    Dev Biol. 1990 Dec;142(2):368-79 PMID: 1701737
  5. Neurite outgrowth in response to transfected N-CAM and N-cadherin reveals fundamental differences in neuronal responsiveness to CAMs.
    Neuron. 1991 Feb;6(2):247-58 PMID: 1993122
  6. Extracellular ATP causes Ca2(+)-dependent and -independent insulin secretion in RINm5F cells. Phospholipase C mediates Ca2+ mobilization but not Ca2+ influx and membrane depolarization.
    J Biol Chem. 1991 Feb 25;266(6):3449-57 PMID: 1995609
  7. Regulated plasmalemmal expansion in nerve growth cones.
    J Cell Biol. 1991 Mar;112(6):1215-27 PMID: 1999470
  8. NCAM polysialic acid can regulate both cell-cell and cell-substrate interactions.
    J Cell Biol. 1991 Jul;114(1):143-53 PMID: 2050739
  9. 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. 1991 Jul 1;88(13):5494-8 PMID: 2062831
  10. Leukocyte interactions mediated by selectins.
    Thromb Haemost. 1991 Jul 12;66(1):80-7 PMID: 1718051
  11. Uvomorulin mediates calcium-dependent aggregation of islet cells, whereas calcium-independent cell adhesion molecules distinguish between islet cell types.
    Dev Biol. 1991 Nov;148(1):233-42 PMID: 1936561
  12. Establishment of 2-mercaptoethanol-dependent differentiated insulin-secreting cell lines.
    Endocrinology. 1992 Jan;130(1):167-78 PMID: 1370150
  13. Exo-endocytotic recycling of synaptic vesicles in developing processes of cultured hippocampal neurons.
    J Cell Biol. 1992 May;117(4):849-61 PMID: 1577861
  14. Heterogeneity in pancreatic beta-cell population.
    Diabetes. 1992 Jul;41(7):777-81 PMID: 1612191
  15. NCAM: structural diversity, function and regulation of expression.
    Semin Cell Biol. 1992 Jun;3(3):189-97 PMID: 1623208
  16. Cytoplasmic domain of P-selectin (CD62) contains the signal for sorting into the regulated secretory pathway.
    Mol Biol Cell. 1992 Mar;3(3):309-21 PMID: 1378326
  17. Polysialic acid is required for optimal growth of axons on a neuronal substrate.
    J Neurosci. 1992 Aug;12(8):3107-14 PMID: 1494949
  18. Inhibitors of protein and RNA synthesis block structural changes that accompany long-term heterosynaptic plasticity in Aplysia.
    Neuron. 1992 Oct;9(4):749-58 PMID: 1356372
  19. Differential expression of neural cell adhesion molecule and cadherins in pancreatic islets, glucagonomas, and insulinomas.
    Mol Endocrinol. 1992 Aug;6(8):1332-42 PMID: 1406710
  20. Mapping of the distribution of polysialylated neural cell adhesion molecule throughout the central nervous system of the adult rat: an immunohistochemical study.
    Neuroscience. 1992 Jul;49(2):419-36 PMID: 1436474
  21. The relationship of intramuscular nerve branching and synaptogenesis to motoneuron survival.
    J Neurobiol. 1992 Nov;23(9):1131-9 PMID: 1469380
  22. Developmental mechanisms that generate precise patterns of neuronal connectivity.
    Cell. 1993 Jan;72 Suppl:77-98 PMID: 8428376
  23. Structural changes accompanying memory storage.
    Annu Rev Physiol. 1993;55:397-426 PMID: 8466181
  24. Nerve-dependent expression of high polysialic acid neural cell adhesion molecule in neurohypophysial astrocytes of adult rats.
    Neuroscience. 1993 Mar;53(1):213-21 PMID: 8469308
  25. Depolarization maintains neurites and priming of PC12 cells after nerve growth factor withdrawal.
    J Neurosci. 1993 Jul;13(7):3124-35 PMID: 8331389
  26. Integrin-mediated neurite outgrowth in neuroblastoma cells depends on the activation of potassium channels.
    J Cell Biol. 1993 Sep;122(5):1131-43 PMID: 8354696
  27. Structure, metabolism and cell biology of polysialic acids.
    Eur J Cell Biol. 1993 Aug;61(2):197-207 PMID: 7693470
  28. Single islet beta-cell stimulation by nutrients: relationship between pyridine nucleotides, cytosolic Ca2+ and secretion.
    EMBO J. 1990 Jan;9(1):53-60 PMID: 2403930
  29. Regulation and activity-dependence of N-cadherin, NCAM isoforms, and polysialic acid on chick myotubes during development.
    J Cell Biol. 1993 Dec;123(6 Pt 2):1867-88 PMID: 8276904
  30. Activity-dependent neuronal-glial and synaptic plasticity in the adult mammalian hypothalamus.
    Neuroscience. 1993 Dec;57(3):501-35 PMID: 8309521
  31. Inactivation of the N-CAM gene in mice results in size reduction of the olfactory bulb and deficits in spatial learning.
    Nature. 1994 Feb 3;367(6462):455-9 PMID: 8107803
  32. A triggered mechanism retrieves membrane in seconds after Ca(2+)-stimulated exocytosis in single pituitary cells.
    J Cell Biol. 1994 Mar;124(5):667-75 PMID: 8120090
  33. Membrane traffic in polarized neurons in culture.
    J Cell Sci Suppl. 1993;17:85-92 PMID: 8144707
  34. Traffic of synaptic vesicle proteins in polarized and nonpolarized cells.
    J Cell Sci Suppl. 1993;17:93-100 PMID: 8144709
  35. Recognition, adhesion, transmembrane signaling and cell motility in guided neuronal migration.
    Curr Opin Neurobiol. 1994 Feb;4(1):63-9 PMID: 8173327
  36. Freeze-fracturing of nerve growth cones and young fibers. A study of developing plasma membrane.
    J Cell Biol. 1974 Oct;63(1):180-96 PMID: 4609396
  37. High concentration of GABA and high glutamate decarboxylase activity in rat pancreatic islets and human insulinoma.
    Science. 1976 Nov 5;194(4265):620-2 PMID: 185693
  38. Na+-channel-associated scorpion toxin receptor sites as probes for neuronal evolution in vivo and in vitro.
    Proc Natl Acad Sci U S A. 1981 Feb;78(2):1245-9 PMID: 6262759
  39. Regulation of insulin release by calcium.
    Physiol Rev. 1981 Oct;61(4):914-73 PMID: 6117094
  40. Macro- and micro-domains in the endocrine pancreas.
    Diabetes. 1982 Jun;31(6 Pt 1):538-65 PMID: 6759269
  41. Occurrence of alpha 2-8 linked polysialosyl units in a neural cell adhesion molecule.
    Biochem Biophys Res Commun. 1983 Apr 29;112(2):482-7 PMID: 6847662
  42. Use of prokaryotic-derived probes to identify poly(sialic acid) in neonatal neuronal membranes.
    Proc Natl Acad Sci U S A. 1984 Apr;81(7):1971-5 PMID: 6371806
  43. Biosynthesis of the D2 cell adhesion molecule: pulse-chase studies in cultured fetal rat neuronal cells.
    J Cell Biol. 1984 Jun;98(6):2077-81 PMID: 6725409
  44. Cleavage of the polysialosyl units of brain glycoproteins by a bacteriophage endosialidase. Involvement of a long oligosaccharide segment in molecular interactions of polysialic acid.
    J Biol Chem. 1985 Jan 25;260(2):1265-70 PMID: 3968060
  45. Interplay of nutrients and hormones in the regulation of insulin release.
    Endocrinology. 1985 Sep;117(3):824-33 PMID: 2862021
  46. A platelet alpha-granule membrane protein (GMP-140) is expressed on the plasma membrane after activation.
    J Cell Biol. 1985 Sep;101(3):880-6 PMID: 2411738
  47. Structural and immunological characterization of the amino-terminal domain of mammalian neural cell adhesion molecules.
    J Biol Chem. 1986 Mar 5;261(7):3396-401 PMID: 3512556
  48. A platelet alpha granule membrane protein that is associated with the plasma membrane after activation. Characterization and subcellular localization of platelet activation-dependent granule-external membrane protein.
    J Clin Invest. 1986 Jul;78(1):130-7 PMID: 2941452
  49. A monoclonal antibody against meningococcus group B polysaccharides distinguishes embryonic from adult N-CAM.
    J Cell Biol. 1986 Dec;103(6 Pt 1):2429-37 PMID: 3536966
  50. Cell adhesion molecules in the regulation of animal form and tissue pattern.
    Annu Rev Cell Biol. 1986;2:81-116 PMID: 3548776
  51. Cell lineage analysis of pancreatic islet development: glucagon and insulin cells arise from catecholaminergic precursors present in the pancreatic duct.
    Dev Biol. 1987 Jun;121(2):454-66 PMID: 2884153
  52. The neural cell adhesion molecule (NCAM) as a regulator of cell-cell interactions.
    Science. 1988 Apr 1;240(4848):53-7 PMID: 3281256
  53. Expression of cell adhesion molecules in the olfactory system of the adult mouse: presence of the embryonic form of N-CAM.
    Dev Biol. 1988 Oct;129(2):516-31 PMID: 3417050
  54. Distinct roles for adhesion molecules during innervation of embryonic chick muscle.
    Dev Biol. 1988 Dec;130(2):645-70 PMID: 3058545
  55. Compensatory growth of pancreatic beta-cells in adult rats after short-term glucose infusion.
    Diabetes. 1989 Jan;38(1):49-53 PMID: 2642434
  56. Heterogeneous distribution of polysialylated neuronal-cell adhesion molecule during post-natal development and in the adult: an immunohistochemical study in the rat brain.
    Neuroscience. 1989;28(3):701-10 PMID: 2710339
  57. Stimulated secretion of endothelial von Willebrand factor is accompanied by rapid redistribution to the cell surface of the intracellular granule membrane protein GMP-140.
    J Biol Chem. 1989 May 15;264(14):7768-71 PMID: 2470733
  58. Polysialic acid as a regulator of intramuscular nerve branching during embryonic development.
    Neuron. 1990 May;4(5):655-67 PMID: 2344405
Article Info
Journal
The EMBO journal
Abbr.
EMBO J
ISSN
0261-4189
Published
1994-11-15
Pages
5284-92
Language
English
Region
England
NLM ID
8208664
PMCID
PMC395484
Subset
IM
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: product@genelibs.com