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J. Biol. Chem., Vol. 278, Issue 5, 3220-3226, January 31, 2003
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From the Synaptotagmin IV (Syt IV) is a fourth
member of the Syt family and has been shown to regulate
some forms of memory and learning by analysis of Syt IV null mutant
mice (Ferguson, G. D., Anagnostaras, S. G., Silva, A. J., and Herschman, H. R. (2000) Proc. Natl. Acad. Sci.
U. S. A. 97, 5598-5603). However, the involvement of Syt IV
protein in vesicular trafficking and even its localization in secretory
vesicles are still matters of controversy. Here we present several
lines of evidence showing that the Syt IV protein in PC12 cells is
normally localized in the Golgi or immature vesicles at the cell
periphery and is sorted to fusion-competent mature dense-core vesicles
in response to short nerve growth factor (NGF) stimulation. (i) In
undifferentiated PC12 cells, Syt IV protein is mainly localized in the
Golgi and small amounts are also present at the cell periphery, but
according to the results of an immunocytochemical analysis, they do not
colocalize with conventional secretory vesicle markers (Syt I, Syt IX,
Rab3A, Rab27A, vesicle-associated membrane protein 2, and
synaptophysin) at all. By contrast, limited colocalization of Syt IV
protein with dense-core vesicle markers is found in the distal parts of
the neurites of NGF-differentiated PC12 cells. (ii) Immunoelectron
microscopy with highly specific anti-Syt IV antibody revealed that the
Syt IV protein in undifferentiated PC12 cells is mainly present on the
Golgi membranes and immature secretory vesicles, whereas after NGF
stimulation Syt IV protein is also present on the mature dense-core
vesicles. (iii) An N-terminal antibody-uptake experiment indicated that
Syt IV-containing vesicles in the neurites of NGF-differentiated PC12
cells undergo Ca2+-dependent exocytosis,
whereas no uptake of the anti-Syt IV-N antibody was observed in
undifferentiated PC12 cells. Our results suggest that Syt IV is a
stimulus (e.g. NGF)-dependent regulator for
exocytosis of dense-core vesicles.
Nerve Growth Factor-dependent Sorting of
Synaptotagmin IV Protein to Mature Dense-core Vesicles That Undergo
Calcium-dependent Exocytosis in PC12 Cells*
§,,,,
Fukuda Initiative Research Unit,
RIKEN (The Institute of Physical and Chemical Research), 2-1 Hirosawa,
Wako, Saitama 351-0198, Japan, the ¶ Section on Cellular
Neurobiology, Laboratory of Developmental Neurobiology, NICHD, National
Institutes of Health, Bethesda, Maryland 20892, and the
Department of Physiology, Kansai Medical University,
Moriguchi, Osaka 570-8506, Japan
*
This work was supported in part by grants from the
Science and Technology Agency to Japan (to M. F.) and Grant 13780624 from the Ministry of Education, Science, and Culture of Japan (to
M. F.).The costs of publication of this
article were defrayed in part by the
payment of page charges. The article
must therefore be hereby marked
"advertisement" in
accordance with 18 U.S.C. Section
1734 solely to indicate this fact.
Copyright © 2003 by The American Society for Biochemistry and Molecular Biology, Inc.
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