Skip to main content
Log in

Catecholamine secretion from rat foetal adrenal chromaffin cells and hypoxia sensitivity

  • Cell and Molecular Physiology
  • Published:
Pflügers Archiv - European Journal of Physiology Aims and scope Submit manuscript

Abstract

The adrenal medulla chromaffin cells (AMCs) secrete catecholamines in response to various types of stress. We examined the hypoxia-sensitivity of catecholamine secretion by rat foetal chromaffin cells in which the innervation by the splanchnic nerve is not established. The experiments were performed in primary cultured cells from two different ages of foetuses (F15 and F19). Membrane potential of AMCs was monitored with the patch clamp technique, and the catecholamine secretion was detected by amperometry. We found that: (1) AMCs from F19 foetuses showed hypoxia-induced catecholamine release. (2) This hypoxia-induced secretion is produced by membrane depolarization generated by an inhibition of Ca2+-activated K+ current [I K(Ca)] current. (3) Chromaffin precursor cells from F15 foetuses secrete catecholamine. The quantal release is calcium-dependent, but the size of the quantum is reduced. (4) In the precursor cells, a hypoxia-induced membrane hyperpolarization is originated by an ATP-sensitive K+ current [I K(ATP)] activation. (5) During the prenatal period, at F15, the percentage of the total outward current for I K(ATP) and I K(Ca) was 50 and 29.5%, respectively, whereas at F19, I K(ATP) is reduced to 14%, and I K(Ca) became 64% of the total current. We conclude that before birth, the age-dependent hypoxia response of chromaffin cells is modulated by the functional activity of KATP and KCa channels.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

Similar content being viewed by others

References

  1. Ashcroft FM, Gribble FM (1998) Correlating structure and function in ATP-sensitive K+ channels. Trends Neurosci 21(7):288–294 (Jul)

    Article  PubMed  CAS  Google Scholar 

  2. Ballanyi K (2004) Protective role of neuronal KATP channels in brain hypoxia. J Exp Biol 207(Pt 18):3201–3212 (Aug)

    Article  PubMed  CAS  Google Scholar 

  3. Bournaud R, Hidalgo J, Yu H, Jaimovich E, Shimahara T (2001) Low threshold T-type calcium current in rat embryonic chromaffin cells. J Physiol 537:35–44

    Article  PubMed  CAS  Google Scholar 

  4. Fearon IM, Thompson RJ, Samjoo I, Vollmer C, Doering LC, Nurse CA (2002) Sensitive K+ channels in immortalised rat chromaffin-cell-derived MAH cells. J Physiol 545(Pt 3):807–818 (15)

    Article  PubMed  CAS  Google Scholar 

  5. Inoue M, Fujishiro N, Imanaga I (1999) Na+ pump inhibition and non-selective cation channel activation by cyanide and anoxia in guinea-pig chromaffin cells. J Physiol 519(Pt 2):385–396

    Article  PubMed  CAS  Google Scholar 

  6. Jiang C, Haddad GG (1994) A direct mechanism for sensing low oxygen levels by central neurons. Proc Natl Acad Sci USA 91(15):7198–7201

    Article  PubMed  CAS  Google Scholar 

  7. Keating DJ, Rychkov GY, Roberts ML (2001) Oxygen sensitivity in the sheep adrenal medulla: role of SK channels. Am J Physiol Cell Physiol 281:C1434–C1441

    PubMed  CAS  Google Scholar 

  8. Keating DJ, Rychkov GY, Adams MB, Holgert H, McMillen IC, Roberts ML (2004) Opioid receptor stimulation suppresses the adrenal medulla hypoxic response in sheep by actions on Ca(2+) and K(+) channels. J Physiol 555(Pt 2):489–502

    PubMed  CAS  Google Scholar 

  9. Keating DJ, Rychkov GY, Giacomin P, Roberts ML (2005) Oxygen-sensing pathway for SK channels in the ovine adrenal medulla. Clin Exp Pharmacol Physiol 32(10):882–887

    Article  PubMed  CAS  Google Scholar 

  10. Kolski-Andreaco A, Tomita H, Shakkottai VG, Gutman GA, Cahalan MD, Gargus JJ, Chandy KG (2004) SK3-1C, a dominant-negative suppressor of SKCa and IKCa channels. J Biol Chem 279(8):6893–6904 (20)

    Article  PubMed  CAS  Google Scholar 

  11. Lee J, Lim W, Eun SY, Kim SJ, Kim J (2000) Inhibition of apamin-sensitive K+ current by hypoxia in adult rat adrenal chromaffin cells. Pflügers Arch 439:700–704

    Article  PubMed  CAS  Google Scholar 

  12. Lopez-Barneo J, Lopez-Lopez JR, Urena J, Gonzalez C (1988) Chemotransduction in the carotid body: K+ current modulated by PO2 in type I chemoreceptor cells. Science 241(4865):580–582 (Jul 29)

    Article  PubMed  CAS  Google Scholar 

  13. Lopez-Barneo J, Pardal R, Ortega-Saenz P (2001) Cellular mechanism of oxygen sensing. Annu Rev Physiol 63:259–287

    Article  PubMed  CAS  Google Scholar 

  14. Lopez-Barneo J (2003) Oxygen and glucose sensing by carotid body glomus cells. Curr Opin Neurobiol 13(4):493–499

    Article  PubMed  CAS  Google Scholar 

  15. Olver RE, Walters DV, M Wilson S (2004) Developmental regulation of lung liquid transport. Annu Rev Physiol 66:77–101

    Article  PubMed  CAS  Google Scholar 

  16. Mojet MH, Mills E, Duchen MR (1997) Hypoxia-induced catecholamine secretion in isolated newborn rat adrenal chromaffin cells is mimicked by inhibition of mitochondrial respiration. J Physiol 504(1):175–189

    Article  PubMed  CAS  Google Scholar 

  17. Murphy KP, Greenfield SA (1992) Neuronal selectivity of ATP-sensitive potassium channels in guinea-pig substantia nigra revealed by responses to anoxia. J Physiol 453:167–183

    PubMed  CAS  Google Scholar 

  18. Peers C, Buckler KJ (1995) Transduction of chemostimuli by the type I carotid body cell. J Membr Biol 144(1):1–9

    PubMed  CAS  Google Scholar 

  19. Seidler FJ, Slotkin TA (1985) Adrenomedullary function in the neonatal rat: responses to acute hypoxia. J Physiol 358:1–16

    PubMed  CAS  Google Scholar 

  20. Seino S (1999) ATP-Sensitive potassium channels: a model of heteromeric potassium channel/receptor assemblies. Annu Rev Physiol 61:337–362

    Article  PubMed  CAS  Google Scholar 

  21. Slotkin TA, Seidler FJ (1988) Adrenomedullary catecholamine release in the foetus and newborn: secretory mechanisms and their role in stress and survival. J Dev Physiol 10:1–16

    PubMed  CAS  Google Scholar 

  22. Stocker M (2004) Ca(2+)-activated K+ channels: molecular determinants and function of the SK family. Nat Rev Neurosci 5(10):758–770

    Article  PubMed  CAS  Google Scholar 

  23. Teitelman G, Baker H, Joh TH, Reis DJ (1979) Appearance of catecholamine-synthesizing enzymes during development of rat sympathetic nervous system: possible role of tissue environment. Proc Natl Acad Sci USA 76(1):509–513 (Jan)

    Article  PubMed  CAS  Google Scholar 

  24. Thompson RJ, Jackson A, Nurse CA (1997) Developmental loss of hypoxic chemosensitivity in rat adrenomedullary chromaffin cells. J Physiol 498:503–510

    PubMed  CAS  Google Scholar 

  25. Thompson RJ, Nurse CA (1998) Anoxia differentially modulates multiple K+ currents and depolarizes neonatal rat adrenal chromaffin cells. J Physiol 512:421–434

    Article  PubMed  CAS  Google Scholar 

  26. Thompson RJ, Farragher SM, Cutz E, Nurse CA (2002) Developmental regulation of O(2) sensing in neonatal adrenal chromaffin cells from wild-type and NADPH-oxidase-deficient mice. Pflügers Arch 444(4):539–548

    Article  PubMed  CAS  Google Scholar 

  27. Thompson RJ (2004) Current understanding of the O2-signalling mechanism of adrenal chromaffin cells. In: Borges R, Gandia L (eds) Cell biology of the chromaffin cells, pp 95–106

  28. Verhofstad AA, Hokfelt T, Goldstein M, Steinbusch HW, Joosten HW (1979) Appearance of tyrosine hydroxylase, aromatic amino-acid decarboxylase, dopamine beta-hydroxylase and phenylethanolamine N-methyltransferase during the ontogenesis of the adrenal medulla: an immunohistochemical study in the rat. Cell Tissue Res 200(1):1–13 (3)

    Article  PubMed  CAS  Google Scholar 

  29. Wightman RM, Jankowski JA, Kennedy RT, Kawagoe KT, Schroeder TJ, Leszczyszyn DJ, Near JA, Diliberto EJ Jr, Viveros OH (1991) Temporally resolved catecholamine spikes correspond to single vesicle release from individual chromaffin cells. Proc Natl Acad Sci USA 88(23):10754–10758 (Dec 1)

    Article  PubMed  CAS  Google Scholar 

  30. Williams SE, Wootton P, Mason HS, Bould J, Iles DE, Riccardi D, Peers C, Kemp PJ (2004) Hemoxygenase-2 is an oxygen sensor for a calcium-sensitive potassium channel. Science 306(5704):2093–2097

    Article  PubMed  CAS  Google Scholar 

  31. Wyatt CN, Buckler KJ (2004) The effect of mitochondrial inhibitors on membrane currents in isolated neonatal rat carotid body type I cells. J Physiol 556(1):175–191

    Article  PubMed  CAS  Google Scholar 

Download references

Acknowledgement

The present study was partially supported by CONICYT-ECOS exchange program (CO3SO2) Confocal microscopy studies were performed on the facility on the CNRS Campus (Plate-forme Imagerie et Biologie Cellulaire) supported in part by the ASTRE program of the Conseil Général de l’Essonne.

Author information

Authors and Affiliations

Authors

Corresponding authors

Correspondence to R. Bournaud or T. Shimahara.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Bournaud, R., Hidalgo, J., Yu, H. et al. Catecholamine secretion from rat foetal adrenal chromaffin cells and hypoxia sensitivity. Pflugers Arch - Eur J Physiol 454, 83–92 (2007). https://doi.org/10.1007/s00424-006-0185-z

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00424-006-0185-z

Keywords

Navigation