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Journal of Neuroscience, Vol 14, 39-53, Copyright © 1994 by Society for Neuroscience
Aggregation of vasopressin mRNA in a subset of axonal swellings of the median eminence and posterior pituitary: light and electron microscopic evidence
A Trembleau, M Morales and FE Bloom
Department of Neuropharmacology, Scripps Research Institute, La Jolla, California 92037.
The mRNA encoding vasopressin has recently been documented within the
magnocellular hypothalamo-neurohypophyseal projections of the rat such as
the median eminence (ME) and the posterior pituitary (PP), suggesting the
possibility of its axonal transport. To address the origin of this mRNA and
to investigate the functional significance of this unexpected axonal
transport of mRNA, we have examined its subcellular localization within
both magnocellular perikarya and their axonal projections. For this
purpose, we have used nonradioactive in situ hybridization techniques in
order to localize the vasopressin mRNA with precision at the
ultrastructural level in magnocellular perikarya, dendrites, and axons from
control, salt-loaded, and lactating rats. This approach permitted us to
demonstrate directly the axonal localization of vasopressin mRNA. Moreover,
we were able to obtain novel information concerning vasopressin mRNA
compartmentation within both perikarya and axons. At both light and
electron microscopic levels, we observed vasopressin mRNA-containing cells
in the hypothalamic magnocellular cell body groups, but not in the ME or in
the PP. When vasopressin mRNA was detected in medium-size dendrites, it was
always associated with the rough endoplasmic reticulum (RER). Within the
labeled magnocellular perikarya, the abundant vasopressin mRNA was mainly
associated with discrete areas of the RER. However, vasopressin mRNA was
never detected in the Golgi apparatus or in association with neurosecretory
granules, in perikarya or axons. These data suggest that vasopressin mRNA
translation is restricted to certain segments within the RER, and that
axonal transport of vasopressin mRNA does not involve the classical
neurosecretory pathway, via the Golgi apparatus and the neurosecretory
granules, as has been proposed. Within the magnocellular neuron axons,
vasopressin mRNA could be detected only in a subset of axonal swellings,
all of which were confined to the internal layer of the ME and the PP. The
mRNA-containing swellings were numerous in 7 d salt-loaded animals, less
abundant in lactating animals, and almost undetectable in control animals.
In all groups of animals, no vasopressin mRNA was detectable in any other
region of the magnocellular neuron axons, including undilated axonal
segments or varicose swellings. These results strongly suggest that, under
physiological activation such as chronic salt loading, axonal vasopressin
mRNA is increased and becomes aggregated in a selected subset of swellings
of the ME and the PP. Furthermore, these data indicate that along the
magnocellular neuron axons, the swellings may differ in their biochemical
and functional features. Further analysis focused on the mRNA-accumulating
swellings may illuminate the function of RNA within the axonal compartment.
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