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Pflügers Archiv

, Volume 425, Issue 1–2, pp 22–27 | Cite as

Effects of acidic stimuli on intracellular calcium in isolated type I cells of the neonatal rat carotid body

  • K. J. Buckler
  • R. D. Vaughan-Jones
Molecular and Cellular Physiology

Abstract

We have investigated the effects of acidic stimuli upon [Ca2+]i in isolated carotid body type I cells from the neonatal rat using indo-1 (AM-loaded). Under normocapnic, non-hypoxic conditions (23 mM HCO3, 5% CO2 in air, pHo=7.4), the mean [Ca2+]i for single cells was 102±5.0 nM (SEM, n=55) with 58% of cells showing sporadic [Ca2+]i fluctuations. A hypercapnic acidosis (increase in CO2 to 10%–20% at constant HCO3, pHo 7.15–6.85), an isohydric hypercapnia (increase in CO2 to 10% at constant pHo=7.4) and an isocapnic acidosis (pHo=7.0, constant CO2) all increased [Ca2+]i in single cells and cell clusters. The averaged [Ca2+]i response to both hypercapnic acidosis and isohydric hypercapnia displayed a rapid rise followed by a secondary decline. The averaged [Ca2+]i response to isocapnic acidosis displayed a slower rise and little secondary decline. The rise of [Ca2+]i in response to all the above stimuli can be attributed to no single factor other than to a fall of pHi. The hypercapnia-induced rise of [Ca2+]i was almost completely abolished in Ca2+-free solution, suggesting a role for Ca2+ influx in triggering and/or sustaining the [Ca2+]i response. These results are consistent with a role for type I cell [Ca2+]i in mediating pH/PCO2 chemoreception.

Key words

Carotid body Chemoreceptor Intracellular calcium Intracellular pH Extracellular pH Acidosis Hypercapnia 

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References

  1. 1.
    Biscoe TJ, Duchen MR (1990) Responses of type I cells dissociated from the rabbit carotid body to hypoxia. J Physiol 428: 39–59Google Scholar
  2. 2.
    Biscoe TJ, Duchen MR (1990) The cellular basis of transduction in carotid chemoreceptors. Am J Physiol 258: L271-L278Google Scholar
  3. 3.
    Biscoe TJ, Duchen MR, Eisner DA, O'Neill SC, Valdeolmillos M (1989) Measurements of intracellular Ca2+ in dissociated type-I cells of the rabbit carotid body. J Physiol (Lond) 416: 421–434Google Scholar
  4. 4.
    Black AMS, McCloskey DI, Torrance RW (1971) The responses of carotid body chemoreceptors in the cat to sudden changes of hypercapnic and hypoxic stimuli. Respir Physiol 13: 36–49Google Scholar
  5. 5.
    Buckler KJ, Vaughan-Jones RD (1990) Application of a new pH-sensitive fluoroprobe (carboxy-SNARF-1) for intracellular pH measurement in small, isolated cells. Pflügers Arch 417: 234–239Google Scholar
  6. 6.
    Buckler KJ, Vaughan-Jones RD (1992) Raising P CO2 elevates [Ca2+]i in isolated carotid body glomus cells of the neonatal rat. J Physiol (Lond) 452: 228PGoogle Scholar
  7. 7.
    Buckler KJ, Vaughan-Jones RD (1993) Increasing P CO2 raises [Ca2+]i through voltage gated Ca2+ entry in isolated carotid body glomus cells of the neontal rat. J Physiol (Lond) 459: 272PGoogle Scholar
  8. 8.
    Buckler KJ, Vaughan-Jones RD, Peers C, Lagadic-Gossmann D, Nye PCG (1991) Effects of extracellular pH, P CO2 and HCO3 on intracellular pH in isolated type-I cells of the neonatal rat carotid body. J Physiol (Lond) 444: 703–721Google Scholar
  9. 9.
    Buckler KJ, Vaughan-Jones RD, Peers C, Nye PCG (1991) Intracellular pH and its regulation in isolated type-I carotid body cells of the neonatal rat. J Physiol (Lond) 436: 107–129Google Scholar
  10. 10.
    Cheek TR, O'Sullivan AJ, Moreton RB, Berridge MJ, Burgoyne RD (1989) Spatial localization of the stimulus-induced rise in cytosolic Ca2+ in bovine adrenal chromaffin cells. FEBS Lett 247: 429–434Google Scholar
  11. 11.
    Donnelly DP, Kholwadwala D (1992) Hypoxia decreases intracellular calcium in adult rat carotid body glomus cells. J Neurophysiol 67: 1543–1551Google Scholar
  12. 12.
    Duchen MR, Valdeolmillos M, O'Neill SC, Eisner DA (1990) Effects of metabolic blockade on the regulation of intracellular calcium in dissociated mouse sensory neurones. J Physiol (Lond) 424: 411–426Google Scholar
  13. 13.
    Duchen MR, Caddy KWT, Kirby GC, Patterson DL, Ponte J, Biscoe TJ (1988) Biophysical studies of the cellular elements of the rabbit carotid body. Neuroscience 26: 291–313Google Scholar
  14. 14.
    Gray BA (1968) Responses of the perfused carotid body to changes in pH and pCO2. Respir Physiol 4: 580–584Google Scholar
  15. 15.
    Grynkiewicz G, Poenie M, Tsien RY (1985) A new generation of Ca2+ indicators with greatly improved fluorescence properties. J Biol Chem 260: 3440–3450Google Scholar
  16. 16.
    Guerineau N, Corcuff J-B, Tabarin A, Mollard P (1991) Spontaneous and corticotrophin-releasing factor-induced calcium transients in corticotrophs. Endocrinology 129: 409–420Google Scholar
  17. 17.
    Hanson MA, Nye PCG, Torrance RW (1971) The exodus of an intracellular bicarbonate theory of chemoreception and the genesis of an intracellular one. In: Belmonte C, Pallot DJ, Acker H, Fidone S (eds) Arterial chemoreceptors. Leicester University Press, LeicesterGoogle Scholar
  18. 18.
    Hornbein TF, Roos A (1963) Specificity of H ion concentration as a carotid chemoreceptor stimulus. J Appl Physiol 18: 580–584Google Scholar
  19. 19.
    Iturriaga R, Lahiri S (1991) Carotid body chemoreception in the absence and presence of CO2-HCO3 . Brain Res 568: 253–260Google Scholar
  20. 20.
    Iturriaga R, Lahiri S, Mokashi A (1991) Carbonic anhydrase and chemoreception in the cat carotid body. Am J Physiol 261: C565-C573Google Scholar
  21. 21.
    Lattanzio FAJ (1990) The effects of pH and temperature on fluorescent calcium indicators as determined with Chelex-100 and EDTA buffer systems. Biochem Biophys Res Commun 171: 102–108Google Scholar
  22. 22.
    Milani D, Malgaroli A, Guidolin D, Fasolato C, Skaper SD, Meldolesi J, Pozzan T (1990) Ca2+ channels and intracellular Ca2+ stores in neuronal and neuroendocrine cells. Cell Calcium 11: 191–199Google Scholar
  23. 23.
    Peers C (1990) Selective effects of extracellular pH on Ca2+-dependent K-currents in type-I cells isolated from the neontal rat carotid body. J Physiol (Lond) 422: 381–395Google Scholar
  24. 24.
    Peers C, Green FK (1991) Inhibition of Ca2+-activated K+ currents by intracellular acidosis in isolated type-I cells of the neonatal rat carotid body. J Physiol (Lond) 437: 589–602Google Scholar
  25. 25.
    Rigual R, Lopez-Lopez JR, Gonzales C (1991) Release of dopamine and chemoreceptor discharge induced by low pH and high pCO2 stimulation of the cat carotid body. J Physiol (Lond) 433: 519–531Google Scholar
  26. 26.
    Rocher A, Obeso A, Gonzalez C, Herreros B (1991) Ionic mechanisms for the transduction of acidic stimuli in rabbit carotid body glomus cells. J Physiol (Lond) 433: 533–548Google Scholar
  27. 27.
    Stea A, Alexander SA, Nurse CA (1991) Effects of pHi and pHo on membrane currents recorded with the perforated-patch method from cultured chemoreceptors of the rat carotid body. Brain Res 567: 83–90Google Scholar

Copyright information

© Springer-Verlag 1993

Authors and Affiliations

  • K. J. Buckler
    • 1
  • R. D. Vaughan-Jones
    • 1
  1. 1.University Laboratory of PhysiologyUniversity of OxfordOxfordUK

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