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Volume 17, Number 20,
Issue of October 15, 1997
pp. 7683-7693
Copyright ©1997 Society for Neuroscience
Allergic Inflammation in Isolated Vagal Sensory Ganglia Unmasks
Silent NK-2 Tachykinin Receptors
Received June 9, 1997; revised Aug. 1, 1997; accepted Aug. 5, 1997.
Daniel Weinreich,
Kimberly A. Moore, and
Glen E. Taylor
Department of Pharmacology and Experimental Therapeutics, School of
Medicine, University of Maryland, Baltimore, Maryland 21201-1559
Neuroplastic changes in vagal afferents inflicted by allergic
inflammation were examined in nodose ganglia (NG) removed from guinea
pigs immunized to chick ovalbumin. In control NG neurons, substance P
(SP; 0.1-10 µM) produces no discernable changes in membrane electrophysiological properties or
[Ca2+]i. After exposing NG from
immunized animals to the sensitizing antigen in vitro,
83% of the neurons were depolarized by 100 nM SP. SP also
produces an inward current, an increase in membrane conductance, and an
elevation of [Ca2+]i. Buffering
[Ca2+]i with BAPTA blocked the
[Ca2+]i rise and the SP
depolarization, indicating that internal stores of
Ca2+ are required. When protein synthesis was
inhibited >96% (as determined by [3H] leucine
incorporation), antigen challenge still unmasked SP responses. The SP
response was maximal 30 min after antigen challenge, and it was evident
for at least 8 hr in intact ganglia and for 3.5 d in isolated
neurons. [ -Ala8]Neurokinin A
([-Ala8]NKA; 10 nM), an NK-2
selective agonist, mimicked SP; selective NK-1 and NK-3 agonists were
ineffective. The EC50 values for SP and
[-Ala8]NKA membrane currents were 78 and 33 nM, respectively. Additionally, SR48968, an NK-2 receptor
antagonist, blocked these responses. Thus, antigen challenge appears to
unmask an NK-2 tachykinin receptor. These data further support the
hypothesis that inflammatory mediators released during immediate
hypersensitivity (allergic) reactions can produce profound effects on
the excitability of sensory nerves. Unmasked NK-2 receptors may serve
an excitatory autoreceptor function, provide a pathway for paracrine
signaling between NG neurons, and contribute to ectopic sensory nerve
activity.
Key words:
sensory neuron;
substance P;
nerve injury;
tachykinin receptors;
inflammation;
mast cells;
immediate
hypersensitivity
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