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The Journal of Neuroscience, November 15, 1998, 18(22):9471-9479
Activation of Vagal Afferents after Intravenous Injection of
Interleukin-1 : Role of Endogenous Prostaglandins
Monica
Ek1,
Mieko
Kurosawa2,
Thomas
Lundeberg2, and
Anders
Ericsson1
Departments of 1 Medicine, Unit of Rheumatology, and
2 Physiology, The Karolinska Institute, Stockholm, Sweden
Intravenous administration of interleukin-1 (IL-1) activates
central autonomic neuronal circuitries originating in the nucleus of
the solitary tract (NTS). The mechanism(s) by which blood-borne IL-1
regulates brain functions, whether by operating across the blood-brain
barrier and/or by activating peripheral sensory afferents, remains to
be characterized. It has been proposed that vagal afferents originating
in the periphery may monitor circulating IL-1 levels, because neurons
within the NTS are primary recipients of sensory information from the
vagus nerve and also exhibit exquisite sensitivity to blood-borne IL-1.
In this study, we present evidence that viscerosensory afferents of the
vagus nerve respond to intravenously administered IL-1 . Specific
labeling for mRNAs encoding the type 1 IL-1 receptor and the EP3
subtype of the prostaglandin E2 receptor was detected in
situ over neuronal cell bodies in the rat nodose ganglion. Moreover, intravenously applied IL-1 increased the number of sensory neurons in the nodose ganglion that express the cellular activation marker c-Fos, which was matched by an increase in
discharge activity of vagal afferents arising from gastric
compartments. This response to IL-1 administration was attenuated in
animals pretreated with the cyclooxygenase inhibitor indomethacin,
suggesting partial mediation by prostaglandins. In conclusion, these
results demonstrate that somata and/or fibers of sensory neurons of the
vagus nerve express receptors to IL-1 and prostaglandin E2 and that
circulating IL-1 stimulates vagal sensory activity via both
prostaglandin-dependent and -independent mechanisms.
Key words:
nodose ganglion; viscerosensory; nucleus of the solitary
tract; autonomic; cytokine; c-Fos; blood-brain barrier; neuroimmunomodulation; inflammation; acute-phase response
Copyright © 1998 Society for Neuroscience 0270-6474/98/18229471-09$05.00/0
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