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PMID: 14742706 Published · ppublish English Journal Article Research Support, U.S. Gov't, P.H.S.

SNAP-23 functions in docking/fusion of granules at low Ca2+.

Molecular biology of the cell ·Vol. 15 ·No. 4 ·2004-04-00 ·Pages 1918-30

Chieregatti E, Chicka MC, Chapman ER, Baldini G

Abstract

Ca(2+)-triggered exocytosis of secretory granules mediates the release of hormones from endocrine cells and neurons. The plasma membrane protein synaptosome-associated protein of 25 kDa (SNAP-25) is thought to be a key component of the membrane fusion apparatus that mediates exocytosis in neurons. Recently, homologues of SNAP-25 have been identified, including SNAP-23, which is expressed in many tissues, albeit at different levels. At present, little is known concerning functional differences among members of this family of proteins. Using an in vitro assay, we show here that SNAP-25 and SNAP-23 mediate the docking of secretory granules with the plasma membrane at high (1 microM) and low (100 nM) Ca(2+) levels, respectively, by interacting with different members of the synaptotagmin family. In intact endocrine cells, expression of exogenous SNAP-23 leads to high levels of hormone secretion under basal conditions. Thus, the relative expression levels of SNAP-25 and SNAP-23 might control the mode (regulated vs. basal) of granule release by forming docking complexes at different Ca(2+) thresholds.

MeSH Terms
Animals Antigens, Surface/metabolism Calcium/metabolism Calcium-Binding Proteins/metabolism Carrier Proteins Cell Division Cell Line Cell Line, Tumor Cell Membrane/metabolism Cells, Cultured DNA, Complementary/metabolism Dose-Response Relationship, Drug Exocytosis Green Fluorescent Proteins Luminescent Proteins/metabolism Membrane Glycoproteins/metabolism Membrane Proteins/metabolism Mice Models, Biological Nerve Tissue Proteins/metabolism Precipitin Tests Protein Binding Protein Structure, Tertiary Qb-SNARE Proteins Qc-SNARE Proteins R-SNARE Proteins Subcellular Fractions/metabolism Synaptotagmins Syntaxin 1 Time Factors Transfection
Chemicals
Antigens, Surface Calcium-Binding Proteins Carrier Proteins DNA, Complementary Luminescent Proteins Membrane Glycoproteins Membrane Proteins Nerve Tissue Proteins Qb-SNARE Proteins Qc-SNARE Proteins R-SNARE Proteins SNAP23 protein, human Snap23 protein, mouse Syntaxin 1 Synaptotagmins Green Fluorescent Proteins Calcium
Authors & Affiliations
4 authors, click to expand affiliations / ORCID
Chieregatti Evelina
Department of Anatomy and Cell Biology, Columbia University, College of Physicians and Surgeons, New York, New York 10032, USA.
Chicka Michael C
Chapman Edwin R
Baldini Giulia
References (67)
67 references, click to expand
  1. SNAP-25 is expressed in islets of Langerhans and is involved in insulin release.
    J Cell Biol. 1995 Mar;128(6):1019-28 PMID: 7896868
  2. Botulinum neurotoxin type C cleaves a single Lys-Ala bond within the carboxyl-terminal region of syntaxins.
    J Biol Chem. 1995 May 5;270(18):10566-70 PMID: 7737992
  3. Ca(2+)-dependent and -independent activities of neural and non-neural synaptotagmins.
    Nature. 1995 Jun 15;375(6532):594-9 PMID: 7791877
  4. SNARE complex formation is triggered by Ca2+ and drives membrane fusion.
    Cell. 1999 Apr 16;97(2):165-74 PMID: 10219238
  5. SNAP23 promotes insulin-dependent glucose uptake in 3T3-L1 adipocytes: possible interaction with cytoskeleton.
    Am J Physiol. 1999 May;276(5 Pt 1):C1108-14 PMID: 10329959
  6. Synaptic function modulated by changes in the ratio of synaptotagmin I and IV.
    Nature. 1999 Aug 19;400(6746):757-60 PMID: 10466723
  7. The role of Ca2+ in insulin-stimulated glucose transport in 3T3-L1 cells.
    J Biol Chem. 2001 Jul 27;276(30):27816-24 PMID: 11375387
  8. Plasma membrane repair is mediated by Ca(2+)-regulated exocytosis of lysosomes.
    Cell. 2001 Jul 27;106(2):157-69 PMID: 11511344
  9. Munc18-1 promotes large dense-core vesicle docking.
    Neuron. 2001 Aug 30;31(4):581-91 PMID: 11545717
  10. The tandem C2 domains of synaptotagmin contain redundant Ca2+ binding sites that cooperate to engage t-SNAREs and trigger exocytosis.
    J Cell Biol. 2001 Sep 17;154(6):1117-23 PMID: 11551981
  11. Synaptotagmin modulation of fusion pore kinetics in regulated exocytosis of dense-core vesicles.
    Science. 2001 Nov 2;294(5544):1111-5 PMID: 11691996
  12. The Tlg SNARE complex is required for TGN homotypic fusion.
    J Cell Biol. 2001 Dec 10;155(6):969-78 PMID: 11739408
  13. Genetic ablation of the t-SNARE SNAP-25 distinguishes mechanisms of neuroexocytosis.
    Nat Neurosci. 2002 Jan;5(1):19-26 PMID: 11753414
  14. Synaptotagmins form a hierarchy of exocytotic Ca(2+) sensors with distinct Ca(2+) affinities.
    EMBO J. 2002 Feb 1;21(3):270-80 PMID: 11823420
  15. Synaptotagmins: why so many?
    J Biol Chem. 2002 Mar 8;277(10):7629-32 PMID: 11739399
  16. Fast insulin secretion reflects exocytosis of docked granules in mouse pancreatic B-cells.
    Pflugers Arch. 2002 May;444(1-2):43-51 PMID: 11976915
  17. SNAP-25 and synaptotagmin 1 function in Ca2+-dependent reversible docking of granules to the plasma membrane.
    Traffic. 2002 Jul;3(7):496-511 PMID: 12047557
  18. Ca2+-dependent synaptotagmin binding to SNAP-25 is essential for Ca2+-triggered exocytosis.
    Neuron. 2002 May 16;34(4):599-611 PMID: 12062043
  19. Alternative splicing isoforms of synaptotagmin VII in the mouse, rat and human.
    Biochem J. 2002 Jul 1;365(Pt 1):173-80 PMID: 12071850
  20. Synaptotagmin function in dense core vesicle exocytosis studied in cracked PC12 cells.
    Nat Neurosci. 2002 Jul;5(7):649-56 PMID: 12055633
  21. Inhibition of SNARE complex assembly differentially affects kinetic components of exocytosis.
    Cell. 1999 Dec 23;99(7):713-22 PMID: 10619425
  22. The C terminus of SNAP25 is essential for Ca(2+)-dependent binding of synaptotagmin to SNARE complexes.
    J Biol Chem. 2000 Mar 3;275(9):6328-36 PMID: 10692432
  23. Role of SNAP23 in insulin-induced translocation of GLUT4 in 3T3-L1 adipocytes. Mediation of complex formation between syntaxin4 and VAMP2.
    J Biol Chem. 2000 Mar 17;275(11):8240-7 PMID: 10713150
  24. Synaptotagmin III isoform is compartmentalized in pancreatic beta-cells and has a functional role in exocytosis.
    Diabetes. 2000 Mar;49(3):383-91 PMID: 10868959
  25. Priming in exocytosis: attaining fusion-competence after vesicle docking.
    Biochimie. 2000 May;82(5):399-407 PMID: 10865127
  26. Membrane fusion and exocytosis.
    Annu Rev Biochem. 1999;68:863-911 PMID: 10872468
  27. The C2B domain of synaptotagmin is a Ca(2+)-sensing module essential for exocytosis.
    J Cell Biol. 2000 Sep 4;150(5):1125-36 PMID: 10974000
  28. Vimentin filaments in fibroblasts are a reservoir for SNAP23, a component of the membrane fusion machinery.
    Mol Biol Cell. 2000 Oct;11(10):3485-94 PMID: 11029050
  29. Synaptotagmin III/VII isoforms mediate Ca2+-induced insulin secretion in pancreatic islet beta -cells.
    J Biol Chem. 2000 Nov 17;275(46):36079-85 PMID: 10938083
  30. Rab3A and Rab3D control the total granule number and the fraction of granules docked at the plasma membrane in PC12 cells.
    Traffic. 2000 Dec;1(12):976-86 PMID: 11208087
  31. Accessory factors in clathrin-dependent synaptic vesicle endocytosis.
    Nat Rev Neurosci. 2000 Dec;1(3):161-72 PMID: 11257904
  32. Active-site mutagenesis of tetanus neurotoxin implicates TYR-375 and GLU-271 in metalloproteolytic activity.
    Toxicon. 2001 Aug;39(8):1151-9 PMID: 11306125
  33. Synaptotagmin VII as a plasma membrane Ca(2+) sensor in exocytosis.
    Neuron. 2001 May;30(2):459-73 PMID: 11395007
  34. Synaptotagmin: a Ca(2+) sensor that triggers exocytosis?
    Nat Rev Mol Cell Biol. 2002 Jul;3(7):498-508 PMID: 12094216
  35. Plasma membrane targeting of SNAP-25 increases its local concentration and is necessary for SNARE complex formation and regulated exocytosis.
    J Cell Sci. 2002 Aug 15;115(Pt 16):3341-51 PMID: 12140265
  36. Emerging roles of presynaptic proteins in Ca++-triggered exocytosis.
    Science. 2002 Oct 25;298(5594):781-5 PMID: 12399579
  37. Regulated exocytosis: a novel, widely expressed system.
    Nat Cell Biol. 2002 Dec;4(12):955-62 PMID: 12447386
  38. Cyclic AMP is sufficient for triggering the exocytic recruitment of aquaporin-2 in renal epithelial cells.
    EMBO Rep. 2003 Jan;4(1):88-93 PMID: 12524527
  39. Differential control of the releasable vesicle pools by SNAP-25 splice variants and SNAP-23.
    Cell. 2003 Jul 11;114(1):75-86 PMID: 12859899
  40. Identification of synaptotagmin effectors via acute inhibition of secretion from cracked PC12 cells.
    J Cell Biol. 2003 Jul 21;162(2):199-209 PMID: 12860971
  41. The identification of a novel synaptosomal-associated protein, SNAP-25, differentially expressed by neuronal subpopulations.
    J Cell Biol. 1989 Dec;109(6 Pt 1):3039-52 PMID: 2592413
  42. Phospholipid binding by a synaptic vesicle protein homologous to the regulatory region of protein kinase C.
    Nature. 1990 May 17;345(6272):260-3 PMID: 2333096
  43. Cloning and sequence analysis of cDNA for a neuronal cell membrane antigen, HPC-1.
    J Biol Chem. 1992 May 25;267(15):10613-9 PMID: 1587842
  44. Synaptotagmin: a calcium sensor on the synaptic vesicle surface.
    Science. 1992 May 15;256(5059):1021-5 PMID: 1589771
  45. Kinetic analysis of secretion from permeabilized adrenal chromaffin cells reveals distinct components.
    J Biol Chem. 1992 Aug 15;267(23):16219-25 PMID: 1644807
  46. Quantal transmitter secretion from myocytes loaded with acetylcholine.
    Nature. 1992 Oct 22;359(6397):733-6 PMID: 1436036
  47. Tetanus and botulinum-B neurotoxins block neurotransmitter release by proteolytic cleavage of synaptobrevin.
    Nature. 1992 Oct 29;359(6398):832-5 PMID: 1331807
  48. SNAP receptors implicated in vesicle targeting and fusion.
    Nature. 1993 Mar 25;362(6418):318-24 PMID: 8455717
  49. Botulinum neurotoxin C1 blocks neurotransmitter release by means of cleaving HPC-1/syntaxin.
    EMBO J. 1993 Dec;12(12):4821-8 PMID: 7901002
  50. Membrane fusion and the cell cycle: Cdc48p participates in the fusion of ER membranes.
    Cell. 1995 Sep 22;82(6):885-93 PMID: 7553849
  51. Botulinum neurotoxin C1 cleaves both syntaxin and SNAP-25 in intact and permeabilized chromaffin cells: correlation with its blockade of catecholamine release.
    Biochemistry. 1996 Feb 27;35(8):2630-6 PMID: 8611567
  52. Clostridial neurotoxins and substrate proteolysis in intact neurons: botulinum neurotoxin C acts on synaptosomal-associated protein of 25 kDa.
    J Biol Chem. 1996 Mar 29;271(13):7694-9 PMID: 8631808
  53. Identification of a novel syntaxin- and synaptobrevin/VAMP-binding protein, SNAP-23, expressed in non-neuronal tissues.
    J Biol Chem. 1996 Jun 7;271(23):13300-3 PMID: 8663154
  54. A biosynthetic regulated secretory pathway in constitutive secretory cells.
    J Cell Biol. 1996 Jun;133(6):1177-91 PMID: 8682857
  55. Binding of the synaptic vesicle v-SNARE, synaptotagmin, to the plasma membrane t-SNARE, SNAP-25, can explain docked vesicles at neurotoxin-treated synapses.
    Proc Natl Acad Sci U S A. 1997 Feb 4;94(3):997-1001 PMID: 9023371
  56. Syndet is a novel SNAP-25 related protein expressed in many tissues.
    J Cell Sci. 1997 Feb;110 ( Pt 4):505-13 PMID: 9067602
  57. The evolutionary pressure to inactivate. A subclass of synaptotagmins with an amino acid substitution that abolishes Ca2+ binding.
    J Biol Chem. 1997 May 30;272(22):14314-9 PMID: 9162066
  58. Botulinum neurotoxin types A and E require the SNARE motif in SNAP-25 for proteolysis.
    FEBS Lett. 1997 Nov 24;418(1-2):1-5 PMID: 9414082
  59. Expression of Rab3D N135I inhibits regulated secretion of ACTH in AtT-20 cells.
    J Cell Biol. 1998 Jan 26;140(2):305-13 PMID: 9442106
  60. Vesicle pools and Ca2+ microdomains: new tools for understanding their roles in neurotransmitter release.
    Neuron. 1998 Mar;20(3):389-99 PMID: 9539117
  61. Syndet, an adipocyte target SNARE involved in the insulin-induced translocation of GLUT4 to the cell surface.
    J Biol Chem. 1998 Jul 24;273(30):18784-92 PMID: 9668052
  62. Protein toxins and membrane transport.
    Curr Opin Cell Biol. 1998 Aug;10(4):530-6 PMID: 9719875
  63. Relocation of the t-SNARE SNAP-23 from lamellipodia-like cell surface projections regulates compound exocytosis in mast cells.
    Cell. 1998 Aug 21;94(4):537-48 PMID: 9727496
  64. Morphologically docked synaptic vesicles are reduced in synaptotagmin mutants of Drosophila.
    J Neurosci. 1998 Oct 1;18(19):7662-73 PMID: 9742137
  65. Role of the cysteine-rich domain of the t-SNARE component, SYNDET, in membrane binding and subcellular localization.
    J Biol Chem. 1999 Mar 26;274(13):9053-60 PMID: 10085154
  66. Proteolysis of SNAP-25 by types E and A botulinal neurotoxins.
    J Biol Chem. 1994 Jan 21;269(3):1617-20 PMID: 8294407
  67. Functional properties of multiple synaptotagmins in brain.
    Neuron. 1994 Dec;13(6):1281-91 PMID: 7993622
Article Info
Journal
Molecular biology of the cell
Abbr.
Mol Biol Cell
ISSN
1059-1524
DOI
10.1091/mbc.e03-09-0684
Published
2004-04-00
Epub
2004-00-23
Pages
1918-30
Language
English
Region
United States
NLM ID
9201390
PMCID
PMC379287
Subset
IM
Grants
NIDDK NIH HHS · R01 DK053293 · United States
NIDDK NIH HHS · DK-53293 · United States
External Links
PubMed source DOI: 10.1091/mbc.e03-09-0684 PMC Full Text View journal details
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