Advertisement

Peripheral Chemoreceptors in Air- Versus Water- Breathers

  • Michael G. JonzEmail author
  • Colin A. Nurse
Conference paper
Part of the Advances in Experimental Medicine and Biology book series (AEMB, volume 758)

Abstract

Among the vertebrates, peripheral chemoreceptors have evolved to play a key role in matching oxygen delivery to the metabolic needs of the body cells and tissues. Specialized neuroepithelial cells (NECs) distributed within the gill filaments and/or lamellae of water-breathers appear to subserve this function by initiating an increase in ventilation in response to lowering of blood or water PO2 (hypoxia). It is only recently, however, that these cells have become amenable for detailed investigations using electrophysiological tools. By contrast, the well-studied specialized neuroendocrine cells (i.e. glomus or type I cells) located principally in the carotid body of air-breathers initiate a similar reflex ventilatory response to hypoxia so as to maintain blood PO2 homeostasis. In some species, however, the carotid body is immature and relatively insensitive to hypoxia at birth; it is during this period that their sympathoadrenal counterparts in the adrenal medulla act as key PO2 receptors, critical for the proper transition to air-breathing life. It is becoming increasingly clear that in general these chemoreceptors act as polymodal receptors, i.e. capable of detecting several sensory modalities including high CO2/H+ or acid hypercapnia. Given the phylogenetic and ontogenetic evidence pointing to homology between the mammalian carotid artery and the first gill arch of teleosts, the question arises whether the mechanisms of chemosensing are conserved among these cell types. This review examines some of the anatomical and functional similarities among these peripheral chemoreceptors, while raising the possibility that the fundamental mechanisms of O2 and CO2/H+ sensing arose first in water-breathers and are conserved among the vertebrates.

Keywords

Fish gill O2 and CO2/H+ receptors Carotid body Adrenal medulla K+ current 

Notes

Acknowledgements

MGJ is supported by the Natural Sciences and Engineering Research Council of Canada (NSERC). CAN received support from the Canadian Institutes of Health Research, NSERC, and Heart and Stroke Foundation of Ontario.

References

  1. Buckler KJ (2007) TASK-like potassium channels and oxygen sensing in the carotid body. Respir Physiol Neurobiol 157:55–64PubMedCrossRefGoogle Scholar
  2. Burleson ML, Mercer SE, Wilk-Blaszczak MA (2006) Isolation and characterization of putative O2 chemoreceptor cells from the gills of channel catfish (Ictalurus punctatus). Brain Res 1092:100–107PubMedCrossRefGoogle Scholar
  3. Buttigieg J, Brown ST, Zhang M, Lowe M, Holloway AC, Nurse CA (2008) Chronic nicotine in utero selectively suppresses hypoxic sensitivity in neonatal rat adrenal chromaffin cells. FASEB J 22:1317–1326PubMedCrossRefGoogle Scholar
  4. Buttigieg J, Brown S, Holloway AC, Nurse CA (2009) Chronic nicotine blunts hypoxic sensitivity in perinatal rat adrenal chromaffin cells via upregulation of KATP channels: Role of α7 nicotinic acetylcholine receptor and hypoxia-inducible factor 2α. J Neurosci 29:7137–7147PubMedCrossRefGoogle Scholar
  5. Comroe JJ (1939) The location and function of the chemoreceptors of the aorta. Am J Physiol 127:176–191Google Scholar
  6. Coolidge EH, Ciuhandu CS, Milsom WK (2008) A comparative analysis of putative oxygen-sensing cells in the fish gill. J Exp Biol 211:1231–1242PubMedCrossRefGoogle Scholar
  7. Cutz E, Pan J, Yeger H (2009) The role of NOX2 and “novel oxidases” in airway chemoreceptor O2 sensing. Adv Exp Med Biol 648:427–438PubMedCrossRefGoogle Scholar
  8. Dahlqvist A, Neuhuber WL, Forsgren S (1994) Innervation of laryngeal nerve paraganglia: an anterograde tracing and immunohistochemical study in the rat. J Comp Neurol 345:440–446PubMedCrossRefGoogle Scholar
  9. Evans DH, Piermarini PM, Choe KP (2005) The multifunctional fish gill: dominant site of gas exchange, osmoregulation, acid–base regulation, and excretion of nitrogenous waste. Physiol Rev 85:97–177PubMedCrossRefGoogle Scholar
  10. Gilmour KM (2001) The CO2/pH ventilatory drive in fish. Comp Biochem Physiol A Mol Integr Physiol 130:219–240PubMedCrossRefGoogle Scholar
  11. Gonzalez C, Almaraz L, Obeso A, Rigual R (1994) Carotid body chemoreceptors: from natural stimuli to sensory discharge. Physiol Rev 74:829–898PubMedGoogle Scholar
  12. Jonz MG, Nurse CA (2006) Ontogenesis of oxygen chemoreception in aquatic vertebrates. Respir Physiol Neurobiol 154:139–152PubMedCrossRefGoogle Scholar
  13. Jonz MG, Fearon IM, Nurse CA (2004) Neuroepithelial oxygen chemoreceptors of the zebrafish gill. J Physiol 560:737–752PubMedCrossRefGoogle Scholar
  14. Kim D, Papreck JR, Kim I, Donnelly DF, Carroll JL (2011) Changes in oxygen sensitivity of TASK in carotid body glomus cells during early development. Respir Physiol Neurobiol 177:228–235PubMedCrossRefGoogle Scholar
  15. Kumar P, Bin-Jaliah I (2007) Adequate stimuli of the carotid body: more than an oxygen sensor? Respir Physiol Neurobiol 157:12–21PubMedCrossRefGoogle Scholar
  16. Levinsky KL, López-Barneo J (2009) Developmental change in T-type Ca2+ channel expression and its role in rat chromaffin cell responsiveness to acute hypoxia. J Physiol 58:1917–1929CrossRefGoogle Scholar
  17. López-Barneo J (2003) Oxygen and glucose sensing by carotid body glomus cells. Curr Opin Neurobiol 13:493–499PubMedCrossRefGoogle Scholar
  18. McDonald DM, Blewett RW (1981) Location and size of carotid body-like organs (paraganglia) revealed in rats by the permeability of blood vessels to Evans blue dye. J Neurocytol 10:607–643PubMedCrossRefGoogle Scholar
  19. Milsom WK, Burleson ML (2007) Peripheral arterial chemoreceptors and the evolution of the carotid body. Respir Physiol Neurobiol 157:4–11PubMedCrossRefGoogle Scholar
  20. Nurse CA (2010) Neurotransmitter and neuromodulatory mechanisms at peripheral arterial chemoreceptors. Exp Physiol 95:657–667PubMedCrossRefGoogle Scholar
  21. Nurse CA, Buttigieg J, Brown S, Holloway AC (2009) Regulation of oxygen sensitivity in adrenal chromaffin cells. Ann N Y Acad Sci 1177:132–139PubMedCrossRefGoogle Scholar
  22. Piskuric NA, Vollmer C, Nurse CA (2011) Confocal immunofluorescence study of rat aortic body chemoreceptors and associated neurons in situ and in vitro. J Comp Neurol 519:856–873PubMedCrossRefGoogle Scholar
  23. Qin Z, Lewis JE, Perry SF (2010) Zebrafish (Danio rerio) gill neuroepithelial cells are sensitive chemoreceptors for environmental CO2. J Physiol 588:861–872PubMedCrossRefGoogle Scholar
  24. Saltys HA, Jonz MG, Nurse CA (2006) Comparative study of gill neuroepithelial cells and their innervation in teleosts and Xenopus tadpoles. Cell Tissue Res 323:1–10PubMedCrossRefGoogle Scholar
  25. Slotkin TA, Seidler FJ (1988) Adrenomedullary catecholamine release in the fetus and newborn: secretory mechanisms and their role in stress and survival. J Devel Physiol 10:1–16Google Scholar
  26. Straus C, Wilson RJ, Remmers JE (2001) Oxygen sensitive chemoreceptors in the first gill arch of the tadpole, Rana catesbeiana. Can J Physiol Pharmacol 79:959–962PubMedGoogle Scholar
  27. Thompson RJ, Jackson A, Nurse CA (1997) Developmental loss of hypoxic chemosensitivity in rat adrenomedullary chromaffin cells. J Physiol 498:503–510PubMedGoogle Scholar
  28. Vulesevic B, McNeill B, Perry SF (2006) Chemoreceptor plasticity and respiratory acclimation in the zebrafish Danio rerio. J Exp Biol 209:1261–1273PubMedCrossRefGoogle Scholar
  29. Weichert CK (1967) Elements of chordate anatomy. McGraw-Hill, New YorkGoogle Scholar
  30. Zhang L, Nurse CA, Jonz MG, Wood CM (2011) Ammonia sensing by neuroepithelial cells and ventilatory responses to ammonia in rainbow trout. J Exp Biol 214:2678–2689PubMedCrossRefGoogle Scholar

Copyright information

© Springer Science+Business Media Dordrecht 2012

Authors and Affiliations

  1. 1.Department of BiologyUniversity of OttawaOttawaCanada
  2. 2.Department of BiologyMcMaster UniversityHamiltonCanada

Personalised recommendations