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PMID: 12538853 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Secretory granules are recaptured largely intact after stimulated exocytosis in cultured endocrine cells.

Taraska JW, Perrais D, Ohara-Imaizumi M, Nagamatsu S, Almers W

Abstract

Classical cell biology teaches that exocytosis causes the membrane of exocytic vesicles to disperse into the cell surface and that a cell must later retrieve by molecular sorting whatever membrane components it wishes to keep inside. We have tested whether this view applies to secretory granules in intact PC-12 cells. Three granule proteins were labeled with fluorescent proteins in different colors, and two-color evanescent-field microscopy was used to view single granules during and after exocytosis. Whereas neuro-peptide Y was lost from granules in seconds, tissue plasminogen activator (tPA) and the membrane protein phogrin remained at the granule site for over 1 min, thus providing markers for postexocytic granules. When tPA was imaged simultaneously with cyan fluorescent protein (CFP) as a cytosolic marker, the volume occupied by the granule appeared as a dark spot where it excluded CFP. The spot remained even after tPA reported exocytosis, indicating that granules failed to flatten into the cell surface. Phogrin was labeled with GFP at its luminal end and used to sense the pH in granules. When exocytosis caused the acidic granule interior to neutralize, GFP-phogrin at first brightened and later dimmed again as the interior separated from the extracellular space and reacidified. Reacidification and dimming could be reversed by application of NH(4)Cl. We conclude that most granules reseal in <10 s after releasing cargo, and that these empty or partially empty granules are recaptured otherwise intact.

MeSH Terms
Animals Base Sequence Cells, Cultured DNA Primers Exocytosis Microscopy, Fluorescence PC12 Cells Rats Secretory Vesicles/metabolism
Chemicals
DNA Primers
Authors & Affiliations
5 authors, click to expand affiliations / ORCID
Taraska Justin W
Vollum Institute, Oregon Health and Sciences University, 3181 SW Sam Jackson Park Road, Portland, OR 97201, USA.
Perrais David
Ohara-Imaizumi Mica
Nagamatsu Shinya
Almers Wolfhard
References (39)
39 references, click to expand
  1. Limited numbers of recycling vesicles in small CNS nerve terminals: implications for neural signaling and vesicular cycling.
    Trends Neurosci. 2001 Nov;24(11):637-43 PMID: 11672807
  2. Ca2+-induced deprotonation of peptide hormones inside secretory vesicles in preparation for release.
    J Neurosci. 1999 Feb 1;19(3):900-5 PMID: 9920653
  3. Monitoring of exocytosis and endocytosis of insulin secretory granules in the pancreatic beta-cell line MIN6 using pH-sensitive green fluorescent protein (pHluorin) and confocal laser microscopy.
    Biochem J. 2002 Apr 1;363(Pt 1):73-80 PMID: 11903049
  4. Dynamin-dependent and dynamin-independent processes contribute to the regulation of single vesicle release kinetics and quantal size.
    Proc Natl Acad Sci U S A. 2002 May 14;99(10):7124-9 PMID: 11997474
  5. Imaging actin and dynamin recruitment during invagination of single clathrin-coated pits.
    Nat Cell Biol. 2002 Sep;4(9):691-8 PMID: 12198492
  6. Imaging direct, dynamin-dependent recapture of fusing secretory granules on plasma membrane lawns from PC12 cells.
    Proc Natl Acad Sci U S A. 2002 Dec 24;99(26):16806-11 PMID: 12486251
  7. Exocytosis and membrane recycling.
    Philos Trans R Soc Lond B Biol Sci. 1981 Dec 18;296(1080):55-65 PMID: 6121347
  8. Alkalinizing the intralysosomal pH inhibits degranulation of human neutrophils.
    J Clin Invest. 1983 Nov;72(5):1793-800 PMID: 6415117
  9. Capacitance measurements reveal stepwise fusion events in degranulating mast cells.
    Nature. 1984 Nov 29-Dec 5;312(5993):453-5 PMID: 6504157
  10. Properties of the fusion pore that forms during exocytosis of a mast cell secretory vesicle.
    Neuron. 1990 May;4(5):643-54 PMID: 2344404
  11. Membrane recapture and early triggered secretion from the newly formed endocytotic compartment in bovine chromaffin cells.
    J Physiol. 1992;453:15-31 PMID: 1464827
  12. Rapid endocytosis coupled to exocytosis in adrenal chromaffin cells involves Ca2+, GTP, and dynamin but not clathrin.
    Proc Natl Acad Sci U S A. 1995 Aug 29;92(18):8328-32 PMID: 7667289
  13. Direct membrane retrieval into large vesicles after exocytosis in sea urchin eggs.
    J Cell Biol. 1995 Dec;131(5):1183-92 PMID: 8522582
  14. Molecular cloning of phogrin, a protein-tyrosine phosphatase homologue localized to insulin secretory granule membranes.
    J Biol Chem. 1996 Jul 26;271(30):18161-70 PMID: 8663434
  15. Fast steps in exocytosis and endocytosis studied by capacitance measurements in endocrine cells.
    Curr Opin Neurobiol. 1996 Jun;6(3):350-7 PMID: 8794084
  16. Tissue plasminogen activator (t-PA) is targeted to the regulated secretory pathway. Catecholamine storage vesicles as a reservoir for the rapid release of t-PA.
    J Biol Chem. 1997 Jan 17;272(3):1976-82 PMID: 8999889
  17. Photobleaching recovery and anisotropy decay of green fluorescent protein GFP-S65T in solution and cells: cytoplasmic viscosity probed by green fluorescent protein translational and rotational diffusion.
    Biophys J. 1997 Apr;72(4):1900-7 PMID: 9083693
  18. Regulation of dense core release from neuroendocrine cells revealed by imaging single exocytic events.
    Nat Neurosci. 1999 May;2(5):440-6 PMID: 10321248
  19. A variant of yellow fluorescent protein with fast and efficient maturation for cell-biological applications.
    Nat Biotechnol. 2002 Jan;20(1):87-90 PMID: 11753368
  20. Ca2+-triggered peptide secretion in single cells imaged with green fluorescent protein and evanescent-wave microscopy.
    Neuron. 1997 Jun;18(6):857-63 PMID: 9208853
  21. Punctate appearance of dopamine-beta-hydroxylase on the chromaffin cell surface reflects the fusion of individual chromaffin granules upon exocytosis.
    Neuroscience. 1997 Oct;80(3):847-60 PMID: 9276499
  22. The exocytotic event in chromaffin cells revealed by patch amperometry.
    Nature. 1997 Oct 2;389(6650):509-12 PMID: 9333242
  23. Use of the green fluorescent protein and its mutants in quantitative fluorescence microscopy.
    Biophys J. 1997 Nov;73(5):2782-90 PMID: 9370472
  24. Vesicle recycling revisited: rapid endocytosis may be the first step.
    Neuroscience. 1998 Apr;83(4):969-89 PMID: 9502240
  25. Measurement of cytosolic, mitochondrial, and Golgi pH in single living cells with green fluorescent proteins.
    Proc Natl Acad Sci U S A. 1998 Jun 9;95(12):6803-8 PMID: 9618493
  26. Secretory-granule dynamics visualized in vivo with a phogrin-green fluorescent protein chimaera.
    Biochem J. 1998 Jul 1;333 ( Pt 1):193-9 PMID: 9639579
  27. High calcium concentrations shift the mode of exocytosis to the kiss-and-run mechanism.
    Nat Cell Biol. 1999 May;1(1):40-4 PMID: 10559862
  28. Exocytotic insertion of calcium channels constrains compensatory endocytosis to sites of exocytosis.
    J Cell Biol. 2000 Feb 21;148(4):755-67 PMID: 10684256
  29. Real-time measurements of vesicle-SNARE recycling in synapses of the central nervous system.
    Nat Cell Biol. 2000 Apr;2(4):197-204 PMID: 10783237
  30. Single granule pH cycling in antigen-induced mast cell secretion.
    J Cell Sci. 2000 Nov;113 Pt 21:3839-50 PMID: 11034911
  31. Simultaneous evanescent wave imaging of insulin vesicle membrane and cargo during a single exocytotic event.
    Curr Biol. 2000 Oct 19;10(20):1307-10 PMID: 11069115
  32. "Kiss and run" exocytosis at hippocampal synapses.
    Proc Natl Acad Sci U S A. 2000 Nov 7;97(23):12828-33 PMID: 11050187
  33. Selective imaging of surface fluorescence with very high aperture microscope objectives.
    J Biomed Opt. 2001 Jan;6(1):6-13 PMID: 11178575
  34. Control of fusion pore dynamics during exocytosis by Munc18.
    Science. 2001 Feb 2;291(5505):875-8 PMID: 11157167
  35. A real-time view of life within 100 nm of the plasma membrane.
    Nat Rev Mol Cell Biol. 2001 Apr;2(4):268-75 PMID: 11283724
  36. Synaptic vesicles: is kissing a matter of competence?
    Trends Cell Biol. 2001 Aug;11(8):324-8 PMID: 11489637
  37. Quantal size is dependent on stimulation frequency and calcium entry in calf chromaffin cells.
    Neuron. 2001 Sep 13;31(5):819-30 PMID: 11567619
  38. Direct observation of membrane retrieval in chromaffin cells by capacitance measurements.
    FEBS Lett. 2001 Sep 21;505(3):414-8 PMID: 11576539
  39. Real-time imaging of the axonal transport of granules containing a tissue plasminogen activator/green fluorescent protein hybrid.
    Mol Biol Cell. 1998 Sep;9(9):2463-76 PMID: 9725906
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
2003-02-18
Epub
2003-00-21
Pages
2070-5
Language
English
Region
United States
NLM ID
7505876
PMCID
PMC149960
Subset
IM
Grants
NIMH NIH HHS · R01 MH060600 · United States
NIMH NIH HHS · MH60600 · United States
Corrections
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