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First published online March 31, 2005
Journal of Experimental Biology 208, 1537-1549 (2005)
Published by The Company of Biologists 2005
doi: 10.1242/jeb.01564

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Development of oxygen sensing in the gills of zebrafish

Michael G. Jonz^* and Colin A. Nurse

Department of Biology, McMaster University, 1280 Main Street West, Hamilton, ON, Canada L8S 4K1

^* Author for correspondence at present address: Department of Physiology and Biophysics, Dalhousie University, 5859 University Avenue, Halifax, NS, Canada, B3H 4H7 (e-mail: mjonz{at}dal.ca)

Accepted 1 March 2005

Previous studies have described the morphology, innervation and O₂-chemoreceptive properties of neuroepithelial cells (NECs) of the zebrafish gill filaments. The present work describes the ontogenesis of these cells, and the formation of functional O₂-sensing pathways in developing zebrafish. Confocal immunofluorescence was performed on whole-mount gill preparations using antibodies against serotonin (5-HT) and a zebrafish-derived neuronal marker (zn-12) to identify the appearance and innervation of gill NECs during larval stages. NECs were first expressed in gill filament primordia of larvae at 5 days postfertilization (d.p.f.) and were fully innervated by 7 d.p.f. In vivo ventilation frequency analysis revealed that a behavioural response to hypoxia (11.2±2.8 min^–1) developed in embryos as early as 2 d.p.f., and a significant increase (P<0.05) in the ventilatory response to hypoxia (200.8±23.0 min^–1) coincided with innervation of NECs of the filaments. In addition, exogenous application of quinidine, a blocker of O₂-sensitive background K⁺ channels in NECs, induced hyperventilation in adults in a dose-dependent manner and revealed the development of a quinidine-sensitive ventilatory response in 7 d.p.f. larvae. This study shows that NEC innervation in the gill filaments may account for the development of a functional O₂-sensing pathway and the hyperventilatory response to hypoxia in zebrafish larvae. At earlier stages, however, O₂-sensing must occur through another pathway. The possibility that a new type of 5-HT-positive NEC of the gill arches may account for this earlier hypoxic response is discussed.

Key words: O₂ chemoreceptor, development, gill, hypoxia, neuroepithelial cells, zebrafish, Danio rerio

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