Abstract
During postnatal development rats demonstrate an age-dependent increase in NaCl chorda tympani (CT) responses and the number of functional apical amiloride-sensitive epithelial Na+ channels (ENaCs) in salt sensing fungiform (FF) taste receptor cells (TRCs). Currently, the intracellular signals that regulate the postnatal development of salt taste have not been identified. We investigated the effect of cAMP, a downstream signal for arginine vasopressin (AVP) action, on the postnatal development of NaCl responses in 19–23 day old rats. ENaC-dependent NaCl CT responses were monitored after lingual application of 8-chlorophenylthio-cAMP (8-CPT-cAMP) under open-circuit conditions and under ±60 mV lingual voltage clamp. Behavioral responses were tested using 2 bottle/24h NaCl preference tests. The effect of [deamino-Cys1, D-Arg8]-vasopressin (dDAVP, a specific V2R agonist) was investigated on ENaC subunit trafficking in rat FF TRCs and on cAMP generation in cultured adult human FF taste cells (HBO cells). Our results show that in 19–23 day old rats, the ENaC-dependent maximum NaCl CT response was a saturating sigmoidal function of 8-CPT-cAMP concentration. 8-CPT-cAMP increased the voltage-sensitivity of the NaCl CT response and the apical Na+ response conductance. Intravenous injections of dDAVP increased ENaC expression and γ-ENaC trafficking from cytosolic compartment to the apical compartment in rat FF TRCs. In HBO cells dDAVP increased intracellular cAMP and cAMP increased trafficking of γ- and δ-ENaC from cytosolic compartment to the apical compartment 10 min post-cAMP treatment. Control 19–23 day old rats were indifferent to NaCl, but showed clear preference for appetitive NaCl concentrations after 8-CPT-cAMP treatment. Relative to adult rats, 14 day old rats demonstrated significantly less V2R antibody binding in circumvallate TRCs. We conclude that an age-dependent increase in V2R expression produces an AVP-induced incremental increase in cAMP that modulates the postnatal increase in TRC ENaC and the neural and behavioral responses to NaCl.
Highlights
Changes in gustatory sensitivity to salty taste occur during postnatal development in mammals [1]
The Bz-sensitive response represents the component of the NaCl chorda tympani (CT) response that arises due to Na+ influx through apical epithelial Na+ channels (ENaCs) in salt sensing FF taste receptor cells (TRCs)
It represents the ENaC-independent component of NaCl CT response. This component most likely arises due to apical Na+ influx through non-selective cation channel(s) in TRCs that are sensitive to cetylpyridinium chloride (CPC) [50]
Summary
Changes in gustatory sensitivity to salty taste occur during postnatal development in mammals [1]. In the rat neonate chorda tympani (CT) taste nerve the Na+-selective fibers accounted for the increase in response with age [6]. Action potentials in these fibers were blocked by amiloride [9, 10]. In fungiform (FF) taste receptor cells (TRCs), the Na+ specific salt taste receptor is the amiloride- and benzamil (Bz)-sensitive epithelial Na+ channel (ENaC) [12,13,14,15,16,17,18,19,20,21,22]. The δβγ-ENaC demonstrates 26–30 fold higher IC50 values for amiloride and Bz relative to αβγ-ENaC [18, 24, 25]. δ-ENaC gene is absent in rats and mice [18, 26]
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