Extracellular H+ induces Ca2+ signals in respiratory chemoreceptors of zebrafish

Pflugers Archiv European Journal of Physiology

Volumn 467, Issue 2, 2015, Pages 399-413

  Abdallah, Sara J ^a   Jonz, Michael G ^a   Perry, Steve F ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

Calcium; Chemoreceptor; Hypercapnia; Neuroepithelial cells; pH; Zebrafish

Indexed keywords

PROTON;

ANIMAL; BREATHING; CALCIUM SIGNALING; CELL CULTURE; CHEMORECEPTOR CELL; CYTOLOGY; GILL; HYPERCAPNIA; METABOLISM; PHYSIOLOGY; ZEBRA FISH;

ANIMALS; CALCIUM SIGNALING; CELLS, CULTURED; CHEMORECEPTOR CELLS; GILLS; HYPERCAPNIA; PROTONS; RESPIRATION; ZEBRAFISH;

EID: 84939894821     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-014-1514-2     Document Type: Article

References (62)

1. Bailly Y (2009) Serotonergic neuroepithelial cells in fish gills: cytology and innervation. In: Zaccone G, Cutz E, Adriaensen D, Nurse CA, Mauceri A (eds) Airway chemoreceptors in the vertebrates. Science Publishers, Enfield, pp 61–97. doi:10.1201/b10181-5
2. Biscoe TJ, Duchen MR (1990) Responses of type I cells dissociated from the rabbit carotid body to hypoxia. J Physiol 428:39–59, PMID: 2231419
3. +-currents and oxygen sensing in carotid body type 1 cells. Respir Physiol 115:179–187. doi:10.1016/S0034-5687(99)00015-8
4. Buckler KJ (2007) TASK-like potassium channels and oxygen sensing in the carotid body. Respir Physiol Neurobiol 157:55–64. doi:10.1016/j.resp.2007.02.013, PMID: 17416212
5. Buckler KJ, Vaughan-Jones RD (1993) Effects of acidic stimuli on intracellular calcium in isolated type I cells of the neonatal rat carotid body. Pflugers Arch 425:22–27. doi:10.1007/BF00374499, PMID: 8272380
6. i in acid chemoreception in type-I cells of the carotid body. Adv Exp Med Biol 360:41–55. doi:10.1007/978-1-4615-2572-1_5, PMID: 7532906
7. Buckler K, Vaughan-Jones R (1994) Effects of hypercapnia on membrane-potential and intracellular calcium in rat carotid-body type-I cells. J Physiol 478:157–171, PMID: 7965831
8. 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 436:107–129, PMID: 2061827
9. Burleson ML, Smatresk NJ (2000) Branchial chemoreceptors mediate ventilatory responses to hypercapnic acidosis in channel catfish. Comp Biochem Physiol Mol Integ Physiol 125:403–414. doi:10.1016/S1095-6433(00)00167-7
10. 2 chemoreceptor cells from the gills of channel catfish (Ictalurus punctatus). Brain Res 1092:100–107. doi:10.1016/j.brainres.2006.03.085, PMID: 16690040
11. Chipperfield AR, Davis JP, Harper AA (1993) An acetazolamide-sensitive inward chloride pump in vascular smooth muscle. Biochem Biophys Res Commun 194:407–412. doi:10.1006/bbrc.1993.1834, PMID: 7687435
12. Dasso LL, Buckler KJ, Vaughan-Jones RD (2000) Interactions between hypoxia and hypercapnic acidosis on calcium signaling in carotid body type I cells. Am J Physiol Lung Cell Mol Physiol 279:36–42
13. Dunel-Erb S, Bailly Y, Laurent P (1982) Neuroepithelial cells in fish gill primary lamellae. J Appl Physiol 53:1342–1353, PMID: 7153134
14. 2/pH ventilatory drive in fish. Comp Biochem Physiol A Mol Integr Physiol 130:219–240. doi:10.1016/S1095-6433(01)00391-9
15. Gilmour KM & Perry SF (2006). Branchial chemoreceptor regulation of cardiorespiratory function. In Fish physiology; sensory systems neuroscience (ed. Toshiaki J. Hara and Barbara S. Zielinski), pp. 97-151: Academic Press. doi: 10.1016/S1546-5098(06)25003-9
16. Gilmour KM, Milsom WK, Rantin FT, Reid SG, Perry SF (2005) Cardiorespiratory responses to hypercarbia in tambaqui Colossoma macropomum: chemoreceptor orientation and specificity. J Exp Biol 208:1095–1107. doi:10.1242/jeb.01480, PMID: 15767310
17. Gonzalez C, Almaraz L, Obeso A, Rigual R (1992) Oxygen and acid chemoreception in the carotid body chemoreceptors. Trends Neurosci 15:146–153. doi:10.1016/0166-2236(92)90357-E
18. Graham MS, Turner JD, Wood CM (1990) Control of ventilation in the hypercapnic skate Raja ocellata: I. Blood and extradural fluid. Respir Physiol 80:259–277. doi:10.1016/0034-5687(90)90088-G
19. 2+ responses in rat glia-rich medullary cultures independent of extracellular pH. Cell Calcium 48:124–132. doi:10.1016/j.ceca.2010.07.006, PMID: 20728216
20. Iturriaga R, Lahiri S, Mokashi A (1991) Carbonic-anhydrase and chemoreception in the cat carotid-body. Am J Physiol 261:C565–C573, PMID: 1928321
21. Iturriaga R, Rumsey WL, Lahiri S, Spergel D, Wilson DF (1992) Intracellular pH and oxygen chemoreception in the cat carotid body in vitro. Appl Physiol 72:2259–2266
22. Jonz MG, Nurse CA (2003) Neuroepithelial cells and associated innervation of the zebrafish gill: a confocal immunofluorescence study. J Comp Neurol 461:1–17. doi:10.1002/cne.10680, PMID: 12722101
23. Jonz MG, Nurse CA (2009) Oxygen-sensitive neuroepithelial cells in the gills of aquatic vertebrates. In: Zaccone G, Cutz E, Adriaensen D, Nurse CA, Mauceri A (eds) Airway chemoreceptors in the vertebrates: structure, evolution and function. Science Publishers, Enfield, pp 1–30. doi:10.1201/b10181-3
24. Jonz MG, Fearon IM, Nurse CA (2004) Neuroepithelial oxygen chemoreceptors of the zebrafish gill. J Physiol 560:737–752. doi:10.1113/jphysiol.2004.069294, PMID: 15331683
25. Kumar P, Bin-Jaliah I (2007) Adequate stimuli of the carotid body: more than an oxygen sensor? Respir Physiol Neurobiol 157:12–21. doi:10.1016/j.resp.2007.01.007, PMID: 17291838
26. Kumar P, Prabhakar NR (2012) Peripheral chemoreceptors: function and plasticity of the carotid body. Compr Physiol 2:141–219, PMID: 23728973
27. + sensing: peripheral and central chemoreception. Int J Biochem Cell Biol 35:1413–1435. doi:10.1016/S1357-2725(03)00050-5
28. Lu Y, Whiteis CA, Sluka KA, Chapleau MW, Abboud FM (2013) Responses of glomus cells to hypoxia and acidosis are uncoupled, reciprocal and linked to ASIC3 expression: selectivity of chemosensory transduction. J Physiol 591:919–932. doi:10.1113/jphysiol.2012.247189, PMID: 23165770
29. McKendry JE, Perry SF (2001) Cardiovascular effects of hypercarbia in rainbow trout (Oncorhynchus mykiss): a role for externally oriented chemoreceptors. J Exp Biol 204:115–125, PMID: 11104715
30. 2+ channels by carbonic anhydrase inhibitors. J Pharmacol Sci 95:240–247. doi:10.1254/jphs.FP0040032, PMID: 15215649
31. Milsom WK (2012) New insights into gill chemoreception: receptor distribution and roles in water and air breathing fish. Respir Physiol Neurobiol 184:326–339. doi:10.1016/j.resp.2012.07.013, PMID: 22841952
32. Milsom WK, Burleson ML (2007) Peripheral arterial chemoreceptors and the evolution of the carotid body. Respir Physiol Neurobiol 157:4–11. doi:10.1016/j.resp.2007.02.007, PMID: 17353155
33. 2. Brain Res 803:194–197. doi:10.1016/S0006-8993(98)00607-6
34. Negulescu PA, Machen TE (1990) Lowering extracellular sodium or pH raises intracellular calcium in gastric cells. J Membr Biol 116:239–248. doi:10.1007/BF01868463, PMID: 2388255
35. Nurse CA (2010) Neurotransmitter and neuromodulatory mechanisms at peripheral arterial chemoreceptors. Exp Physiol 95:657–667. doi:10.1113/expphysiol.2009.049312, PMID: 20360424
36. Peers C, Buckler KJ (1995) Transduction of chemostimuli by the type I carotid body cell. J Membr Biol 144:1–9. doi:10.1007/BF00238411, PMID: 7595937
37. 2 and intracellular acidification. Pflugers Arch. doi:10.1007/s00424-013-1365-2
38. Perry SF, Abdallah S (2012) Mechanisms and consequences of carbon dioxide sensing in fish. Respir Physiol Neurobiol 184:309–315. doi:10.1016/j.resp.2012.06.013, PMID: 22705499
39. Perry SF, Gilmour KM (2002) Sensing and transfer of respiratory gases at the fish gill. J Exp Zool 293:249–263. doi:10.1002/jez.10129, PMID: 12115900
40. 2 receptors on the first gill arch. J Exp Biol 205:3357–3365, PMID: 12324545
41. Ca channel opening properties of acetazolamide in the human vasculature. Br J Pharmacol 132:443–450. doi:10.1038/sj.bjp.0703825, PMID: 11159693
42. 2 and acid signaling in chemosensitive neurons. Am J Physiol Cell Physiol 287:C1493–526. doi:10.1152/ajpcell.00282.2004, PMID: 15525685
43. 2 chemosensitivity in branchial neuroepithelial cells of zebrafish (Danio rerio). University of Ottawa, M.Sc. thesis
44. 2. J Physiol 588:861–872. doi:10.1113/jphysiol.2009.184739, PMID: 20051495
45. Roos A, Boron WF (1981) Intracellular pH. Physiol Rev 61:296–434, PMID: 7012859
46. Rozanov C, Roy A, Mokashi A, Wilson DF, Lahiri S, Acker H (1999) Chemosensory response to high pCO is blocked by cadmium, a voltage-sensitive calcium channel blocker. Brain Res 833:101–107. doi:10.1016/S0006-8993(99)01405-5
47. 2+ fluxes in rat brain synaptosomes. Biochem Biophys Res Commun 242:123–128. doi:10.1006/bbrc.1997.7927, PMID: 9439622
48. 2+ and pH in cultured glomus cells of the newborn rabbit carotid body. Neurosci Lett 173:159–162. doi:10.1016/0304-3940(94)90173-2
49. Shimoda LA, Luke T, Sylvester JT, Shih HW, Jain A, Swenson ER (2007) Inhibition of hypoxia-induced calcium responses in pulmonary arterial smooth muscle by acetazolamide is independent of carbonic anhydrase inhibition. Am J Physiol Lung Cell Mol Physiol 292:L1002–12. doi:10.1152/ajplung.00161.2006, PMID: 17209136
50. Smith JB, Dwyer SD, Smith L (1989) Lowering extracellular pH evokes inositol polyphosphate formation and calcium mobilization. J Biol Chem 264:8723–8728, PMID: 2722798
51. Stuart AE, Hudspeth AJ, Hall ZW (1974) Vital staining of specific monoamine-containing cells in the leech nervous system. Cell Tissue Res 153:55–61. doi:10.1007/BF00225445, PMID: 4140759
52. 2+ current in rabbit carotid body glomus cells. J Neurophysiol 88:604–612, PMID: 12163513
53. Tan ZY, Lu Y, Whiteis CA, Benson CJ, Chapleau MW, Abboud FM (2007) Acid-sensing ion channels contribute to transduction of extracellular acidosis in rat carotid body glomus cells. Circ Res 101:1009–1019. doi:10.1161/CIRCRESAHA.107.154377, PMID: 17872465
54. 2+ channel: a novel mechanism of action that may explain the therapeutic effect of the drug in hypokalemic periodic paralysis. Ann Neurol 48:304–312. doi:10.1002/1531-8249(200009)48:3<304::AID-ANA4>3.0.CO;2-A
55. +-deficient rats. FASEB J 18:760–761, PMID: 14766795
56. Tzaneva V, Gilmour KM, Perry SF (2011) Respiratory responses to hypoxia or hypercapnia in goldfish (Crassius auratus) experiencing gill remodeling. Respir Physiol Neurobiol. doi:10.1016/j.resp.2010.09.018, PMID: 20934539
57. Vulesevic B, McNeill B, Perry SF (2006) Chemoreceptor plasticity and respiratory acclimation in the zebrafish Danio rerio. J Exp Biol 209:1261–1273. doi:10.1242/jeb.02058, PMID: 16547298
58. Wood C, Munger R (1994) Carbonic anhydrase injection provides evidence for the role of blood acid-base status in stimulating ventilation after exhaustive exercise in rainbow trout. J Exp Biol 194:225–253, PMID: 9317687
59. Wood CM, Turner JD, Munger RS, Graham MS (1990) Control of ventilation in the hypercapnic skate Raja ocellata: II. Cerebrospinal fluid and intracellular pH in the brain and other tissues. Respir Physiol 80:279–297. doi:10.1016/0034-5687(90)90089-H
60. Youngson C, Nurse C, Yeger H, Cutz E (1993) Oxygen sensing in airway chemoreceptors. Nature 365:153–155. doi:10.1038/365153a0, PMID: 8371757
61. Zaccone G, Fasulo S, Ainis L, Licata A (1997) Paraneurons in the gills and airways of fishes. Microsc Res Tech 37:4–12. doi:10.1002/(SICI)1097-0029(19970401)37:1<4::AID-JEMT2>3.0.CO;2-R
62. 2/pH chemosensory signaling in co-cultures of rat carotid body receptors and petrosal neurons: role of ATP and ACh. J Neurophysiol 92:3433–3445. doi:10.1152/jn.01099.2003, PMID: 150566