Peripheral chemoreceptors in fish: A brief history and a look ahead

Jonz, Michael G.; Zachar, Peter C.; Fonte, Dillon F. Da; Mierzwa, Anna S.

doi:10.1016/j.cbpa.2014.09.002

Cited by 44 publications

(38 citation statements)

References 107 publications

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“…Both 5-HT and ACh have been implicated in chemoreceptor control of ventilatory reflexes in developing and adult fish (Burleson and Milsom, 1995a,b;Shakarchi et al, 2013;Jonz et al, 2015), as they have in mammals (Shirahata et al, 2007;Nurse, 2010). In addition, O 2 -chemoreceptive gill NECs in zebrafish retain 5-HT (Jonz and Nurse, 2003), and cells expressing an ACh transporter were reported in the gills of zebrafish (Shakarchi et al, 2013) and the amphibious fish, Kryptolebias marmoratus (Regan et al, 2011).…”

Section: Asr As a Chemoreflexmentioning

confidence: 99%

“…In addition, O 2 -chemoreceptive gill NECs in zebrafish retain 5-HT (Jonz and Nurse, 2003), and cells expressing an ACh transporter were reported in the gills of zebrafish (Shakarchi et al, 2013) and the amphibious fish, Kryptolebias marmoratus (Regan et al, 2011). In zebrafish larvae, 5-HT 2 , 5-HT 3 , and nicotinic receptors of the gills appear to play a role in initiation of the hyperventilatory response to hypoxia (Shakarchi et al, 2013;Jonz et al, 2015) and may be involved in initiating the ASR response. Sensory Merkel-like cells containing 5-HT were described in the oropharyngeal epithelium of zebrafish (Zachar and Jonz, 2012), but these cells did not display any morphological changes following long-term exposure to hypoxia (M.G.J., unpublished observations), as did gill NECs (Jonz et al, 2004), suggesting that the former are not O 2 sensitive.…”

Section: Asr As a Chemoreflexmentioning

confidence: 99%

“…In addition, cells expressing an acetylcholine (ACh) transporter were reported in the gills of zebrafish (Shakarchi et al, 2013) and the amphibious fish Kryptolebias marmoratus (Regan et al, 2011). Both 5-HT and ACh have been implicated in the chemoreceptor control of ventilatory reflexes in developing and adult fish (Burleson and Milsom, 1995a,b;Shakarchi et al, 2013;Jonz et al, 2015).…”

Section: Introductionmentioning

confidence: 99%

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Aquatic surface respiration and swimming behaviour in adult and developing zebrafish exposed to hypoxia

Abdallah

Thomas

Jonz

2015

Journal of Experimental Biology

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Severe hypoxia elicits aquatic surface respiration (ASR) behaviour in many species of fish, where ventilation of the gills at the air-water interface improves O 2 uptake and survival. ASR is an important adaptation that may have given rise to air breathing in vertebrates. The neural substrate of this behaviour, however, is not defined. We characterized ASR in developing and adult zebrafish (Danio rerio) to ascertain a potential role for peripheral chemoreceptors in initiation or modulation of this response. Adult zebrafish exposed to acute, progressive hypoxia (P O2 from 158 to 15 mmHg) performed ASR with a threshold of 30 mmHg, and spent more time at the surface as P O2 decreased. Acclimation to hypoxia attenuated ASR responses. In larvae, ASR behaviour was observed between 5 and 21 days postfertilization with a threshold of 16 mmHg. Zebrafish decreased swimming behaviour (i.e. distance, velocity and acceleration) as P O2 was decreased, with a secondary increase in behaviour near or below threshold P O2 . In adults that underwent a 10-day intraperitoneal injection regime of 10 μg g −1 serotonin (5-HT) or 20 μg g −1 acetylcholine (ACh), an acute bout of hypoxia (15 mmHg) increased the time engaged in ASR by 5.5 and 4.9 times, respectively, compared with controls. Larvae previously immersed in 10 μmol l −1 5-HT or ACh also displayed an increased ASR response. Our results support the notion that ASR is a behavioural response that is reliant upon input from peripheral O 2 chemoreceptors. We discuss implications for the role of chemoreceptors in the evolution of air breathing.

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Section: Asr As a Chemoreflexmentioning

confidence: 99%

Section: Asr As a Chemoreflexmentioning

confidence: 99%

Section: Introductionmentioning

confidence: 99%

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Aquatic surface respiration and swimming behaviour in adult and developing zebrafish exposed to hypoxia

Abdallah

Thomas

Jonz

2015

Journal of Experimental Biology

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“…Fishes are thought to sense both O 2 and CO 2 /H + in the environment using externally oriented branchial chemoreceptors named neuroepithelial cells (NECs; Jonz et al, 2004;Qin et al, 2010;Abdallah et al, 2015;Jonz et al, 2015). Branchial NECs display extensive plasticity in response to changes in environmental P O2 .…”

Section: Introductionmentioning

confidence: 99%

“…Chronic exposure to hyperoxia can reduce NEC density, while chronic hypoxia can cause both hypertrophy and proliferation in different cell populations. However, there is no evidence of NEC plasticity in response to chronic hypercapnia in the fully aquatic zebrafish Danio rerio (reviewed in Jonz et al, 2015). Chemoreceptor plasticity may play a role in adaptation to hypercapnic environments, facilitating CO 2 sensing in amphibious fishes, which have evolved under stagnant, 'swampy' conditions and may therefore frequently encounter acute changes in water chemistry; however, this hypothesis remains untested.…”

Section: Introductionmentioning

confidence: 99%

Hypercapnia and low pH induce neuroepithelial cell proliferation and emersion behaviour in the amphibious fish Kryptolebias marmoratus

Robertson

Turko

Jonz

et al. 2015

Journal of Experimental Biology

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Aquatic hypercapnia may have helped to drive ancestral vertebrate invasion of land. We tested the hypothesis that amphibious fishes sense and respond to elevated aquatic P CO2 by behavioural avoidance mechanisms, and by morphological changes at the chemoreceptor level. Mangrove rivulus (Kryptolebias marmoratus) were exposed to 1 week of normocapnic control water (pH 8), air, hypercapnia (5% CO 2 , pH 6.8) or isocapnic acidosis (pH 6.8). We found that the density of CO 2 /H + chemoreceptive neuroepithelial cells (NECs) was increased in hypercapnia or isocapnic acidosis-exposed fish. Projection area (a measure of cell size) was unchanged. Acute exposure to progressive hypercapnia induced the fish to emerse (leave water) at water pH values ∼6.1, whereas addition of HCl to water caused a more variable response with a lower pH threshold (∼pH 5.5). These results support our hypothesis and suggest that aquatic hypercapnia provides an adequate stimulus for extant amphibious fishes to temporarily transition from aquatic to terrestrial habitats.

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Intrinsic and extrinsic innervation of the heart in zebrafish (Danio rerio)

Stoyek

Croll

Smith

2015

J of Comparative Neurology

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In the vertebrate heart the intracardiac nervous system is the final common pathway for autonomic control of cardiac output, but the neuroanatomy of this system is not well understood. In this study we investigated the innervation of the heart in a model vertebrate, the zebrafish. We used antibodies against acetylated tubulin, human neuronal protein C/D, choline acetyltransferase, tyrosine hydroxylase, neuronal nitric oxide synthase, and vasoactive intestinal polypeptide to visualize neural elements and their neurotransmitter content. Most neurons were located at the venous pole in a plexus around the sinoatrial valve; mean total number of cells was 197 ± 23, and 92% were choline acetyltransferase positive, implying a cholinergic role. The plexus contained cholinergic, adrenergic, and nitrergic axons and vasoactive intestinal polypeptide-positive terminals, some innervating somata. Putative pacemaker cells near the plexus showed immunoreactivity for hyperpolarization-activated cyclic nucleotide-gated channel 4 (HCN4) and the transcription factor Islet-1 (Isl1). The neurotracer neurobiotin showed that extrinsic axons from the left and right vagosympathetic trunks innervated the sinoatrial plexus proximal to their entry into the heart; some extrinsic axons from each trunk also projected into the medial dorsal plexus region. Extrinsic axons also innervated the atrial and ventricular walls. An extracardiac nerve trunk innervated the bulbus arteriosus and entered the arterial pole of the heart to innervate the proximal ventricle. We have shown that the intracardiac nervous system in the zebrafish is anatomically and neurochemically complex, providing a substrate for autonomic control of cardiac effectors in all chambers.

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Peripheral chemoreceptors in fish: A brief history and a look ahead

Cited by 44 publications

References 107 publications

Aquatic surface respiration and swimming behaviour in adult and developing zebrafish exposed to hypoxia

Aquatic surface respiration and swimming behaviour in adult and developing zebrafish exposed to hypoxia

Hypercapnia and low pH induce neuroepithelial cell proliferation and emersion behaviour in the amphibious fish Kryptolebias marmoratus

Intrinsic and extrinsic innervation of the heart in zebrafish (Danio rerio)

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