Home LiteratureArticle Details
PMID: 10725375 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Reelin secretion from glutamatergic neurons in culture is independent from neurotransmitter regulation.

Lacor PN, Grayson DR, Auta J, Sugaya I, Costa E, Guidotti A

Abstract

Reelin (Reln) is a glycoprotein that in postnatal and adult mammalian brain is believed to be secreted from telencephalic GABAergic interneurons and cerebellar glutamatergic granule neurons into the extracellular matrix. To address the question of whether Reln neurosecretion occurs via a regulated or a constitutive process, we exposed postnatal rat cerebellar granule neurons (CGNs) maintained in culture for 7-9 days to: (i) 100 microM N-methyl-D-aspartate (NMDA) in a Mg(+2)-free medium to stimulate NMDA-selective glutamate receptors and Ca(2+)-dependent neurotransmitter release, (ii) 50 mM KCl to depolarize the cells and elicit Ca(2+)-dependent exocytosis, (iii) 10-100 microM nicotine to activate excocytosis by nicotinic receptors present in these cells, (iv) 10 microM 1,2,3,4-tetrahydro-6-nitro-2, 3-dioxo-benzo[f]quinoxaline-7-sulfonamide in combination with 10 microM dizocilpine to block alpha-amino-3-hydroxy-5-methyl-4-isoxazolepropionic acid- and NMDA-preferring glutamate receptors activated by endogenously released glutamate, or (v) EGTA (5 mM) to virtually eliminate extracellular Ca(2+) and block Ca(2+)-dependent exocytosis. Although, CGNs express and secrete Reln (measured by quantitative immunoblotting), none of the above-mentioned conditions that control regulated exocytosis alters the stores or the rate of Reln release. In contrast, application of either: (i) a Reln antisense oligonucleotide (5'-GCAATGTGCAGGGAAATG-3') (10 microM) that reduces Reln biosynthesis or (ii) brefeldin A (5 x 10(-5) M), an inhibitor of the traffic of proteins between the endoplasmic reticulum and the Golgi network, sharply curtail the rate of Reln secretion. Because, in subcellular fractionation studies, we have shown that Reln is not contained in synaptic vesicles, these data suggest that Reln secretion from CGNs does not require Ca(2+)-dependent exocytosis, but probably is related to a Reln pool stored in Golgi secretory vesicles mediating a constitutive secretory pathway.

MeSH Terms
Animals Base Sequence Cell Adhesion Molecules, Neuronal/genetics,metabolism Cells, Cultured Culture Media Extracellular Matrix Proteins/genetics,metabolism Glutamates/metabolism Nerve Tissue Proteins Neurons/metabolism Oligonucleotides, Antisense/pharmacology Rats Rats, Sprague-Dawley Reelin Protein Serine Endopeptidases
Chemicals
Cell Adhesion Molecules, Neuronal Culture Media Extracellular Matrix Proteins Glutamates Nerve Tissue Proteins Oligonucleotides, Antisense Reelin Protein Reln protein, rat Serine Endopeptidases
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Lacor P N
The Psychiatric Institute, Department of Psychiatry, University of Illinois, College of Medicine, Chicago, IL 60612, USA.
Grayson D R
Auta J
Sugaya I
Costa E
Guidotti A
References (33)
33 references, click to expand
  1. Expression of reelin in adult mammalian blood, liver, pituitary pars intermedia, and adrenal chromaffin cells.
    Proc Natl Acad Sci U S A. 2000 Feb 1;97(3):1281-6 PMID: 10655522
  2. Proteins of the CNR family are multiple receptors for Reelin.
    Cell. 1999 Dec 10;99(6):635-47 PMID: 10612399
  3. Gender effect on Purkinje cell loss in the cerebellum of the heterozygous reeler mouse.
    J Neurogenet. 1996 Dec;11(1-2):45-58 PMID: 10876649
  4. gamma-aminobutyric acid B receptors are negatively coupled to adenylate cyclase in brain, and in the cerebellum these receptors may be associated with granule cells.
    Mol Pharmacol. 1984 Jan;25(1):24-8 PMID: 6323949
  5. Coexistence of GABA receptors and GABA-modulin in primary cultures of rat cerebellar granule cells.
    J Neurosci. 1987 Jan;7(1):65-76 PMID: 3027277
  6. Subcellular location and neuronal release of diazepam binding inhibitor.
    J Neurochem. 1987 Apr;48(4):1093-102 PMID: 3819722
  7. Phencyclidine is a negative allosteric modulator of signal transduction at two subclasses of excitatory amino acid receptors.
    Proc Natl Acad Sci U S A. 1987 Jul;84(14):5068-72 PMID: 3037532
  8. Reelin is preferentially expressed in neurons synthesizing gamma-aminobutyric acid in cortex and hippocampus of adult rats.
    Proc Natl Acad Sci U S A. 1998 Mar 17;95(6):3221-6 PMID: 9501244
  9. Reeler: new tales on an old mutant mouse.
    Bioessays. 1998 Mar;20(3):235-44 PMID: 9631651
  10. Role of reelin in the control of brain development.
    Brain Res Brain Res Rev. 1998 May;26(2-3):285-94 PMID: 9651544
  11. The reeler mouse as a model of brain development.
    Adv Anat Embryol Cell Biol. 1998;150:1-106 PMID: 9816727
  12. Changes in AMPA receptor-spliced variant expression and shift in AMPA receptor spontaneous desensitization pharmacology during cerebellar granule cell maturation in vitro.
    J Mol Neurosci. 1998 Aug;11(1):23-41 PMID: 9826784
  13. A decrease of reelin expression as a putative vulnerability factor in schizophrenia.
    Proc Natl Acad Sci U S A. 1998 Dec 22;95(26):15718-23 PMID: 9861036
  14. Cortical bitufted, horizontal, and Martinotti cells preferentially express and secrete reelin into perineuronal nets, nonsynaptically modulating gene expression.
    Proc Natl Acad Sci U S A. 1999 Mar 16;96(6):3217-22 PMID: 10077664
  15. Reelin, the extracellular matrix protein deficient in reeler mutant mice, is processed by a metalloproteinase.
    Exp Neurol. 1999 Mar;156(1):214-7 PMID: 10192793
  16. A panel of monoclonal antibodies against reelin, the extracellular matrix protein defective in reeler mutant mice.
    J Neurosci Methods. 1998 Jul 1;82(1):17-24 PMID: 10223511
  17. Release of endogenous and newly synthesized glutamate and of other amino acids induced by non-N-methyl-D-aspartate receptor activation in cerebellar granule cell cultures.
    J Neurochem. 1991 Jan;56(1):199-206 PMID: 1670952
  18. Sodium nitroprusside inhibits N-methyl-D-aspartate-evoked calcium influx via a nitric oxide- and cGMP-independent mechanism.
    Mol Pharmacol. 1992 Apr;41(4):779-84 PMID: 1314946
  19. Post-Golgi membrane traffic: brefeldin A inhibits export from distal Golgi compartments to the cell surface but not recycling.
    J Cell Biol. 1992 Jul;118(2):267-83 PMID: 1629235
  20. A specific antisense oligodeoxynucleotide to mRNAs encoding receptors with seven transmembrane spanning regions decreases muscarinic m2 and gamma-aminobutyric acidB receptors in rat cerebellar granule cells.
    J Pharmacol Exp Ther. 1993 Jan;264(1):423-30 PMID: 8380868
  21. Temporal and depolarization-induced changes in the absolute amounts of mRNAs encoding metabotropic glutamate receptors in cerebellar granule neurons in vitro.
    J Neurochem. 1994 Oct;63(4):1207-17 PMID: 7931274
  22. Changes in gamma-aminobutyrate type A receptor subunit mRNAs, translation product expression, and receptor function during neuronal maturation in vitro.
    Proc Natl Acad Sci U S A. 1994 Nov 8;91(23):10952-6 PMID: 7971990
  23. A protein related to extracellular matrix proteins deleted in the mouse mutant reeler.
    Nature. 1995 Apr 20;374(6524):719-23 PMID: 7715726
  24. Determination of in vivo amino acid neurotransmitters by high-performance liquid chromatography with o-phthalaldehyde-sulphite derivatisation.
    J Neurosci Methods. 1995 Mar;57(1):93-9 PMID: 7791370
  25. Characterization of nicotinic acetylcholine receptors expressed in primary cultures of cerebellar granule cells.
    Brain Res Mol Brain Res. 1995 May;30(1):17-28 PMID: 7609640
  26. Serum-free B27/neurobasal medium supports differentiated growth of neurons from the striatum, substantia nigra, septum, cerebral cortex, cerebellum, and dentate gyrus.
    J Neurosci Res. 1995 Dec;42(5):674-83 PMID: 8600300
  27. Reelin is a secreted glycoprotein recognized by the CR-50 monoclonal antibody.
    J Neurosci. 1997 Jan 1;17(1):23-31 PMID: 8987733
  28. Regulation of Purkinje cell alignment by reelin as revealed with CR-50 antibody.
    J Neurosci. 1997 May 15;17(10):3599-609 PMID: 9133383
  29. Golgi tubule traffic and the effects of brefeldin A visualized in living cells.
    J Cell Biol. 1997 Dec 1;139(5):1137-55 PMID: 9382862
  30. Mutant mice with scrambled brains: understanding the signaling pathways that control cell positioning in the CNS.
    Genes Dev. 1999 Nov 1;13(21):2758-73 PMID: 10557205
  31. Reelin is a ligand for lipoprotein receptors.
    Neuron. 1999 Oct;24(2):471-9 PMID: 10571240
  32. Direct binding of Reelin to VLDL receptor and ApoE receptor 2 induces tyrosine phosphorylation of disabled-1 and modulates tau phosphorylation.
    Neuron. 1999 Oct;24(2):481-9 PMID: 10571241
  33. Colocalization of integrin receptors and reelin in dendritic spine postsynaptic densities of adult nonhuman primate cortex.
    Proc Natl Acad Sci U S A. 2000 Mar 28;97(7):3550-5 PMID: 10725376
Article Info
Journal
Proceedings of the National Academy of Sciences of the United States of America
Abbr.
Proc Natl Acad Sci U S A
ISSN
0027-8424
Published
2000-03-28
Pages
3556-61
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC16278
Subset
IM
Grants
PHS HHS · NIH 49486 · United States
PHS HHS · NIH 56500 · United States
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