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PLANT PHYSIOLOGY , Vol 101, Issue 4 1363-1373, Copyright © 1993 by American Society of Plant Biologists
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CELL BIOLOGY AND SIGNAL TRANSDUCTION |
Effect of Brefeldin A on the Structure of the Golgi Apparatus and on the Synthesis and Secretion of Proteins and Polysaccharides in Sycamore Maple (Acer pseudoplatanus) Suspension-Cultured Cells
A. Driouich, G. F. Zhang and L. A. Staehelin
Department of Molecular, Cellular, and Developmental Biology, University of Colorado, Boulder, Colorado 80309-0347
Brefeldin A (BFA), a specific inhibitor of Golgi-mediated secretion in
animal cells, has been used to study the organization of the secretory
pathway and the function of the Golgi apparatus in plant cells. To this
end, we have employed a combination of electron microscopical,
immunocytochemical, and biochemical techniques to investigate the effects
of this drug on the architecture of the Golgi apparatus as well as on the
secretion of proteins and complex cell wall polysaccharides in sycamore
maple (Acer pseudoplatanus) suspension-cultured cells. We have used 2.5 and
7.5 [mu]g/mL of BFA, which is comparable to the 1 to 10 [mu]g/mL used in
experiments with animal cells. Electron micrographs of high-pressure frozen
and freeze-substituted cells show that although BFA causes swelling of the
endoplasmic reticulum cisternae, unlike in animal cells, it does not induce
the disassembly of sycamore maple Golgi stacks. Instead, BFA induces the
formation of large clusters of Golgi stacks, an increase in the number of
trans-like Golgi cisternae, and the accumulation in the cytoplasm of very
dense vesicles that appear to be derived from trans Golgi cisternae. These
vesicles contain large amounts of xyloglucan (XG), the major hemicellulosic
cell wall polysaccharide, as shown by immunocytochemical labeling with
anti-XG antibodies. All of these structural changes disappear within 120
min after removal of the drug. In vivo labeling experiments using
[3H]leucine demonstrate that protein secretion into the culture medium, but
not protein synthesis, is inhibited by approximately 80% in the presence of
BFA. In contrast, the incorporation of [3H]fucose into N-linked
glycoproteins, which occurs in trans-Golgi cisternae, appears to be
affected to a greater extent than the incorporation of[3H]xylose, which has
been localized to medial Golgi cisternae. BFA also affects secretion of
complex polysaccharides as evidenced by the approximate 50% drop in
incorporation of [3H]xylose and [3H]fucose into cell wall hemicelluloses.
Taken together, these findings suggest that at concentrations of 2.5 to 7.5
[mu]g/mL BFA causes the following major changes in the secretory pathway of
sycamore maple cells: (a) it inhibits the transport of secretory proteins
to the cell surface by about 80% and of hemicelluloses by about 50%; (b) it
changes the patterns of glycosylation of N-linked glycoproteins and
hemicelluloses; (c) it reduces traffic between trans Golgi cisternae and
secretory vesicles; (d) it produces a major block in the transport of
XG-containing, dense secretory vesicles to the cell surface; and (e) it
induces the formation of large aggregates of Golgi stacks in the vicinity
of the nucleus, possibly mediated by the fusion of Golgi matrix zones.
Thus, although the Golgi apparatus of plant and animal cells share many
functional and structural characteristics, the plant Golgi apparatus
possesses properties that make its response to BFA unique.
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|
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