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Journal of Neuroscience, Vol 5, 3111-3123, Copyright © 1985 by Society for Neuroscience
The neuronal endomembrane system. I. Direct links between rough endoplasmic reticulum and the cis element of the Golgi apparatus
JD Lindsey and MH Ellisman
This is the first of three papers describing new components and structural
relationships within the neuronal endomembrane system. This system
includes: the nuclear envelope, rough endoplasmic reticulum, the Golgi
apparatus, lysosomes, axoplasmic reticulum, and discrete cytoplasmic
compartments such as vesicles, multivesicular bodies, and so on. Previous
high voltage electron microscope studies of osmium- impregnated Golgi
apparatus have shown that small varicose tubules often arise from the cis
element. In bullfrog spinal ganglia, these tubules have been seen to extend
into cytoplasmic domains occupied by rough endoplasmic reticulum (RER).
This study was undertaken to determine whether varicose tubules form direct
connections with RER and to measure cytoplasmic density of varicose
tubules. Spinal ganglia from Rana catesbeiana were fixed by osmium
impregnation and, in some cases, were then stained en bloc with lead
aspartate. Sixty- to 3000-nm-thick sections of this tissue, as well as of
ganglia prepared by conventional protocol, were studied using standard and
high voltage electron microscopy. Quantitative analysis revealed that 9% of
the varicose tubules connected with the Golgi cis element. To determine
whether continuities existed between RER and any of these tubules, more
than 50 tubules were fully reconstructed from images of serial sections.
The "ends" of these reconstructed tubules were then studied by high
magnification stereoscopy. This was facilitated by the en bloc lead
staining which allowed visualization of unimpregnated RER elements along
with the impregnated tubules. Small varicose tubules as well as larger
smooth tubules were found to have formed confluent bridges between the cis
element and RER. In addition, the varicose tubules were found to bridge
widely separated elements of RER. Finally, numerous examples of varicose
and smooth tubules were seen to extend from RER and from cis elements to
eventually form blind endings. These findings raise the possibility that
the tubules form highly dynamic transitory connections between RER and the
Golgi apparatus as well as between separated elements of RER. Those between
RER and Golgi apparatus are ideally positioned to play a major role in the
transfer of protein or lipid components first assembled in RER to the Golgi
apparatus for terminal synthetic modification.
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