Cyclic-AMP regulates postnatal development of neural and behavioral responses to NaCl in rats

Jie Qian, Shobha Mummalaneni, Tam Hao T Phan, Gerard L. Heck, John A. Desimone, David West, Sunila Mahavadi, Deanna Hojati, Karnam S. Murthy, Mee Ra Rhyu, Andrew Spielman, Mehmet Hakan Ozdener, Vijay Lyall

Research output: Contribution to journalArticle

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.

Original languageEnglish (US)
Article number0171335
JournalPLoS One
Volume12
Issue number2
DOIs
StatePublished - Feb 1 2017

Fingerprint

Epithelial Sodium Channels
postnatal development
cyclic AMP
Cyclic AMP
Rats
Tympanis
rats
arginine vasopressin
cells
Arginine Vasopressin
tongue
Tongue
Salts
salts
vasopressin
Amiloride
Clamping devices
Bottles
Electric potential
Vasopressins

ASJC Scopus subject areas

  • Medicine(all)
  • Biochemistry, Genetics and Molecular Biology(all)
  • Agricultural and Biological Sciences(all)

Cite this

Qian, J., Mummalaneni, S., Phan, T. H. T., Heck, G. L., Desimone, J. A., West, D., ... Lyall, V. (2017). Cyclic-AMP regulates postnatal development of neural and behavioral responses to NaCl in rats. PLoS One, 12(2), [0171335]. https://doi.org/10.1371/journal.pone.0171335

Cyclic-AMP regulates postnatal development of neural and behavioral responses to NaCl in rats. / Qian, Jie; Mummalaneni, Shobha; Phan, Tam Hao T; Heck, Gerard L.; Desimone, John A.; West, David; Mahavadi, Sunila; Hojati, Deanna; Murthy, Karnam S.; Rhyu, Mee Ra; Spielman, Andrew; Ozdener, Mehmet Hakan; Lyall, Vijay.

In: PLoS One, Vol. 12, No. 2, 0171335, 01.02.2017.

Research output: Contribution to journalArticle

Qian, J, Mummalaneni, S, Phan, THT, Heck, GL, Desimone, JA, West, D, Mahavadi, S, Hojati, D, Murthy, KS, Rhyu, MR, Spielman, A, Ozdener, MH & Lyall, V 2017, 'Cyclic-AMP regulates postnatal development of neural and behavioral responses to NaCl in rats', PLoS One, vol. 12, no. 2, 0171335. https://doi.org/10.1371/journal.pone.0171335
Qian J, Mummalaneni S, Phan THT, Heck GL, Desimone JA, West D et al. Cyclic-AMP regulates postnatal development of neural and behavioral responses to NaCl in rats. PLoS One. 2017 Feb 1;12(2). 0171335. https://doi.org/10.1371/journal.pone.0171335
Qian, Jie ; Mummalaneni, Shobha ; Phan, Tam Hao T ; Heck, Gerard L. ; Desimone, John A. ; West, David ; Mahavadi, Sunila ; Hojati, Deanna ; Murthy, Karnam S. ; Rhyu, Mee Ra ; Spielman, Andrew ; Ozdener, Mehmet Hakan ; Lyall, Vijay. / Cyclic-AMP regulates postnatal development of neural and behavioral responses to NaCl in rats. In: PLoS One. 2017 ; Vol. 12, No. 2.
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