Serotonergic and cholinergic elements of the hypoxic ventilatory response in developing zebrafish

Journal of Experimental Biology

Volumn 216, Issue 5, 2013, Pages 869-880

  Shakarchi, Kamila ^a   Zachar, Peter C ^a   Jonz, Michael G ^a  

^a UNIVERSITY OF OTTAWA   (Canada)

Author keywords

5 HT; ACh; Chemoreceptor; Hypoxia; NEC; Zebrafish

Indexed keywords

HEXAMETHONIUM; KETANSERIN; NICOTINIC RECEPTOR BLOCKING AGENT; OXYGEN; SEROTONIN ANTAGONIST;

ANIMAL; ARTICLE; CHEMORECEPTOR; CHOLINERGIC NERVE CELL; CYTOLOGY; GILL; GROWTH, DEVELOPMENT AND AGING; HISTOLOGY; IMMUNOHISTOCHEMISTRY; METABOLISM; NEUROEPITHELIUM; PHYSIOLOGY; PRENATAL DEVELOPMENT; SEROTONINERGIC NERVE CELL; ZEBRA FISH;

ANIMALS; CHEMORECEPTOR CELLS; CHOLINERGIC NEURONS; GILLS; HEXAMETHONIUM; IMMUNOHISTOCHEMISTRY; KETANSERIN; NEUROEPITHELIAL CELLS; NICOTINIC ANTAGONISTS; OXYGEN; SEROTONERGIC NEURONS; SEROTONIN ANTAGONISTS; ZEBRAFISH;

EID: 84874140779     PISSN: 00220949     EISSN: None     Source Type: Journal    
DOI: 10.1242/jeb.079657     Document Type: Article

References (56)

1. Bailly, Y., Dunel-Erb, S. and Laurent, P. (1992). The neuroepithelial cells of the fish gill filament: indolamine-immunocytochemistry and innervation. Anat. Rec. 233, 143-161.
2. Bairam, A. and Carroll, J. L. (2005). Neurotransmitters in carotid body development. Respir. Physiol. Neurobiol. 149, 217-232.
3. Bairam, A., Joseph, V., Lajeunesse, Y. and Kinkead, R. (2007). Developmental profile of cholinergic and purinergic traits and receptors in peripheral chemoreflex pathway in cats. Neuroscience 146, 1841-1853.
4. Barrionuevo, W. R., Fernandes, M. N. and Rocha, O. (2010). Aerobic and anaerobic metabolism for the zebrafish, Danio rerio, reared under normoxic and hypoxic conditions and exposed to acute hypoxia during development. Braz. J. Biol. 70, 425-434.
5. Bradford, C. S., Sun, L., Collodi, P. and Barnes, D. W. (1994). Cell cultures from zebrafish embryos and adult tissues. J. Tissue Cult. Meth. 16, 99-107.
6. Buckley, K. and Kelly, R. B. (1985). Identification of a transmembrane glycoprotein specific for secretory vesicles of neural and endocrine cells. J. Cell Biol. 100, 1284-1294.
7. Burleson, M. L. and Milsom, W. K. (1993). Sensory receptors in the first gill arch of rainbow trout. Respir. Physiol. 93, 97-110.
8. Burleson, M. L. and Milsom, W. K. (1995a). Cardio-ventilatory control in rainbow trout: I. Pharmacology of branchial, oxygen-sensitive chemoreceptors. Respir. Physiol. 100, 231-238.
9. Burleson, M. L. and Milsom, W. K. (1995b). Cardio-ventilatory control in rainbow trout: II. Reflex effects of exogenous neurochemicals. Respir. Physiol. 101, 289-299.
10. Burleson, M. L., Mercer, S. E. and Wilk-Blaszczak, M. A. (2006). Isolation and characterization of putative O2 chemoreceptor cells from the gills of channel catfish (Ictalurus punctatus). Brain Res. 1092, 100-107.
11. Coccimiglio, M. L. and Jonz, M. G. (2012). Serotonergic neuroepithelial cells of the skin in developing zebrafish: morphology, innervation and oxygen-sensitive properties. J. Exp. Biol. 215, 3881-3894.
12. Coolidge, E. H., Ciuhandu, C. S. and Milsom, W. K. (2008). A comparative analysis of putative oxygen-sensing cells in the fish gill. J. Exp. Biol. 211, 1231-1242.
13. Dunel-Erb, S., Bailly, Y. and Laurent, P. (1982). Neuroepithelial cells in fish gill primary lamellae. J. Appl. Physiol. 53, 1342-1353.
14. Fu, X. W., Nurse, C. A., Wong, V. and Cutz, E. (2002). Hypoxia-induced secretion of serotonin from intact pulmonary neuroepithelial bodies in neonatal rabbit. J. Physiol. 539, 503-510.
15. Fujita, T. (1989). Present status of paraneuron concept. Arch. Histol. Cytol. 52 SUPPL., 1-8.
16. Gauda, E. B., Cooper, R., Johnson, S. M., McLemore, G. L. and Marshall, C. (2004). Autonomic microganglion cells: a source of acetylcholine in the rat carotid body. J. Appl. Physiol. 96, 384-391.
17. Houser, A., McNair, C., Piccinini, R., Luxhoj, A., Bell, W. E. and Turner, J. E. (2011). Effects of estrogen on the neuromuscular system in the embryonic zebrafish (Danio rerio). Brain Res. 1381, 106-116.
18. Jonz, M. G. and Nurse, C. A. (2003). Neuroepithelial cells and associated innervation of the zebrafish gill: a confocal immunofluorescence study. J. Comp. Neurol. 461, 1-17.
19. Jonz, M. G. and Nurse, C. A. (2005). Development of oxygen sensing in the gills of zebrafish. J. Exp. Biol. 208, 1537-1549.
20. Jonz, M. G. and Nurse, C. A. (2006). Ontogenesis of oxygen chemoreception in aquatic vertebrates. Respir. Physiol. Neurobiol. 154, 139-152.
21. Jonz, M. G. and Nurse, C. A. (2009). Oxygen-sensitive neuroepithelial cells in the gills of aquatic vertebrates. In Airway Chemoreceptors in the Vertebrates: Structure, Evolution and Function (ed. G. Zaccone, E. Cutz, D. Adriaensen, C. A. Nurse and A. Mauceri), pp 1-30. Enfield, NH: Science Publishers.
22. Jonz, M. G. and Zaccone, G. (2009). Nervous control of the gills. Acta Histochem. 111, 207-216.
23. Jonz, M. G., Fearon, I. M. and Nurse, C. A. (2004). Neuroepithelial oxygen chemoreceptors of the zebrafish gill. J. Physiol. 560, 737-752.
24. Kameda, Y. (2005). Mash1 is required for glomus cell formation in the mouse carotid body. Dev. Biol. 283, 128-139.
25. Kimmel, C. B., Ballard, W. W., Kimmel, S. R., Ullmann, B. and Schilling, T. F. (1995). Stages of embryonic development of the zebrafish. Dev. Dyn. 203, 253-310.
26. López-Barneo, J., Ortega-Sáenz, P., Pardal, R., Pascual, A. and Piruat, J. I. (2008). Carotid body oxygen sensing. Eur. Respir. J. 32, 1386-1398.
27. Mendelsohn, B. A., Kassebaum, B. L. and Gitlin, J. D. (2008). The zebrafish embryo as a dynamic model of anoxia tolerance. Dev. Dyn. 237, 1780-1788.
28. Metcalfe, W. K., Myers, P. Z., Trevarrow, B., Bass, M. B. and Kimmel, C. B. (1990). Primary neurons that express the L2/HNK-1 carbohydrate during early development in the zebrafish. Development 110, 491-504.
29. Milsom, W. K. and Brill, R. W. (1986). Oxygen sensitive afferent information arising from the first gill arch of yellowfin tuna. Respir. Physiol. 66, 193-203.
30. Milsom, W. K. and Burleson, M. L. (2007). Peripheral arterial chemoreceptors and the evolution of the carotid body. Respir. Physiol. Neurobiol. 157, 4-11.
31. Nurse, C. A. (2010). Neurotransmitter and neuromodulatory mechanisms at peripheral arterial chemoreceptors. Exp. Physiol. 95, 657-667.
32. Padilla, P. A. and Roth, M. B. (2001). Oxygen deprivation causes suspended animation in the zebrafish embryo. Proc. Natl. Acad. Sci. USA 98, 7331-7335.
33. Pardal, R., Ortega-Sáenz, P., Durán, R. and López-Barneo, J. (2007). Glia-like stem cells sustain physiologic neurogenesis in the adult mammalian carotid body. Cell 131, 364-377.
34. Perry, S., Jonz, M. G. and Gilmour, K. M. (2009). Oxygen sensing and the hypoxic ventilatory response. In Fish Physiology, Vol. 27 (ed. J. G. Richards, A. P Farrell and C. J. Brauner), pp 193-253. New York: Academic Press.
35. Porteus, C. S., Brink, D. L., Coolidge, E. H., Fong, A. Y. and Milsom, W. K. (2013). Distribution of acetylcholine and catecholamines in fish gills and their potential roles in the hypoxic ventilatory response. Acta Histochem. 115, 158-169.
36. Prado, M. A., Reis, R. A., Prado, V. F., de Mello, M. C., Gomez, M. V. and de Mello, F. G. (2002). Regulation of acetylcholine synthesis and storage. Neurochem. Int. 41, 291-299.
37. Pumplin, D. W. and Getschman, E. (2000). Synaptic proteins in rat taste bud cells: appearance in the Golgi apparatus and relationship to α-gustducin and the Lewis(b) and A antigens. J. Comp. Neurol. 427, 171-184.
38. Qin, Z., Lewis, J. E. and Perry, S. F. (2010). Zebrafish (Danio rerio) gill neuroepithelial cells are sensitive chemoreceptors for environmental CO2. J. Physiol. 588, 861-872.
39. Regan, K. S., Jonz, M. G. and Wright, P. A. (2011). Neuroepithelial cells and the hypoxia emersion response in the amphibious fish Kryptolebias marmoratus. J. Exp. Biol. 214, 2560-2568.
40. Rihel, J. and Schier, A. F. (2012). Behavioral screening for neuroactive drugs in zebrafish. Dev. Neurobiol. 72, 373-385.
41. Roghani, A., Feldman, J., Kohan, S. A., Shirzadi, A., Gundersen, C. B., Brecha, N. and Edwards, R. H. (1994). Molecular cloning of a putative vesicular transporter for acetylcholine. Proc. Natl. Acad. Sci. USA 91, 10620-10624.
42. Rombough, P. (2002). Gills are needed for ionoregulation before they are needed for O2 uptake in developing zebrafish, Danio rerio. J. Exp. Biol. 205, 1787-1794.
43. Rombough, P. (2007). The functional ontogeny of the teleost gill: which comes first, gas or ion exchange? Comp. Biochem. Physiol. 148A, 732-742.
44. Saltys, H. A., Jonz, M. G. and Nurse, C. A. (2006). Comparative study of gill neuroepithelial cells and their innervation in teleosts and Xenopus tadpoles. Cell Tissue Res. 323, 1-10.
45. Schwerte, T. (2009). Cardio-respiratory control during early development in the model animal zebrafish. Acta Histochem. 111, 230-243.
46. Shirahata, M., Balbir, A., Otsubo, T. and Fitzgerald, R. S. (2007). Role of acetylcholine in neurotransmission of the carotid body. Respir. Physiol. Neurobiol. 157, 93-105.
47. Sundin, L. and Nilsson, S. (2002). Branchial innervation. J. Exp. Zool. 293, 232-248.
48. Trevarrow, B., Marks, D. L. and Kimmel, C. B. (1990). Organization of hindbrain segments in the zebrafish embryo. Neuron 4, 669-679.
49. Turesson, J., Schwerte, T. and Sundin, L. (2006). Late onset of NMDA receptormediated ventilatory control during early development in zebrafish (Danio rerio). Comp. Biochem. Physiol. 143A, 332-339.
50. Vulesevic, B., McNeill, B. and Perry, S. F. (2006). Chemoreceptor plasticity and respiratory acclimation in the zebrafish Danio rerio. J. Exp. Biol. 209, 1261-1273.
51. Westerfield, M. (2000). The Zebrafish Book: A Guide for the Laboratory Use of Zebrafish (Danio rerio), 4th edn. Eugene, OR: University of Oregon Press.
52. Wood, C. M. and Shelton, G. (1980). Cardiovascular dynamics and adrenergic responses of the rainbow trout in vivo. J. Exp. Biol. 87, 247-270.
53. Zaccone, G., Fasulo, S., Ainis, L. and Licata, A. (1997). Paraneurons in the gills and airways of fishes. Microsc. Res. Tech. 37, 4-12.
54. Zachar, P. C. and Jonz, M. G. (2012). Confocal imaging of Merkel-like basal cells in the taste buds of zebrafish. Acta Histochem. 114, 101-115.
55. Zhang, M. and Nurse, C. A. (2004). CO2/pH chemosensory signaling in co-cultures of rat carotid body receptors and petrosal neurons: role of ATP and ACh. J. Neurophysiol. 92, 3433-3445.
56. Zhong, H., Zhang, M. and Nurse, C. A. (1999). Electrophysiological characterization of 5-HT receptors on rat petrosal neurons in dissociated cell culture. Brain Res. 816, 544-553.