The sensing of respiratory gases in fish: Mechanisms and signalling pathways

Perry, Steve F.; Tzaneva, Velislava

doi:10.1016/j.resp.2015.06.007

Cited by 33 publications

(14 citation statements)

References 126 publications

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“…A NO-dependent O 2 -sensing mechanism has been proposed based on the identification of nNOS in neuroepithelial cells of adult and larvae of the zebrafish (Porteus et al, 2015 ). According to Perry and Tzaneva ( 2016 ), like in mammalian glomus cells (Summers et al, 1999 ), NO may inhibit ion channels involved in neurosecretion. This is supported by the NO-dependent regulation of intracellular Ca 2+ observed in the melanophore of the Indian snakehead Channa punctatus (Biswas et al, 2011 ) and in the growth hormone release of goldfish (Chang et al, 2014 ).…”

Section: Three Hypotheses For Oxygen-sensing and Downstream Responsesmentioning

confidence: 99%

Hypoxia Tolerance in Teleosts: Implications of Cardiac Nitrosative Signals

Gattuso¹,

Garofalo²,

Cerra³

et al. 2018

Front. Physiol.

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Changes in environmental oxygen (O2) are naturally occurring phenomena which ectotherms have to face on. Many species exhibit a striking capacity to survive and remain active for long periods under hypoxia, even tolerating anoxia. Some fundamental adaptations contribute to this capacity: metabolic suppression, tolerance of pH and ionic unbalance, avoidance and/or repair of free-radical-induced cell injury during reoxygenation. A remarkable feature of these species is their ability to preserve a normal cardiovascular performance during hypoxia/anoxia to match peripheral (tissue pO2) requirements. In this review, we will refer to paradigms of hypoxia- and anoxia-tolerant teleost fish to illustrate cardiac physiological strategies that, by involving nitric oxide and its metabolites, play a critical role in the adaptive responses to O2 limitation. The information here reported may contribute to clarify the molecular and cellular mechanisms underlying heart vulnerability vs. resistance in relation to O2 availability.

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Section: Three Hypotheses For Oxygen-sensing and Downstream Responsesmentioning

confidence: 99%

Hypoxia Tolerance in Teleosts: Implications of Cardiac Nitrosative Signals

Gattuso¹,

Garofalo²,

Cerra³

et al. 2018

Front. Physiol.

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“…Hif-1α is thought to be one of the most critical transcription factors underlying the hypoxic phenotype in vertebrates because it is involved in numerous biological processes, including angiogenesis, erythropoiesis, apoptosis, metabolism, cell survival and cell proliferation (reviewed in Semenza, 2003). More recently, Hif-1α was implicated in the control of breathing (reviewed in Prabhakar and Semenza, 2012;Perry and Tzaneva, 2016). A knockout of Hif-1A or Hif-1B in larval zebrafish led to a significant blunting or abolishment of the hypoxic ventilatory response during the early stages of development.…”

Section: Loss Of Hif-1α Function Blunts the Hypoxic Ventilatory Responsementioning

confidence: 99%

Hif-1α paralogs play a role in the hypoxic ventilatory response of larval and adult zebrafish (Danio rerio)

Mandic

Tzaneva

Careau

et al. 2018

Journal of Experimental Biology

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Hypoxia-inducible factor (Hif) 1α, an extensively studied transcription factor, is involved in the regulation of many biological processes in hypoxia including the hypoxic ventilatory response. In zebrafish, there are two paralogs of Hif-1α (Hif-1A and Hif-1B), but little is known about the specific roles or potential sub-functionalization of the paralogs in response to hypoxia. Using knockout lines of Hif-1α paralogs, we examined their involvement in the hypoxic ventilatory response, measured as ventilation frequency (f V) in larval and adult zebrafish (Danio rerio). In wild-type zebrafish, f V increased across developmental time (4, 7, 10 and 15 days post-fertilization, dpf) in response to hypoxia (55 mmHg). In contrast, the Hif-1B knockout fish did not exhibit an increase in hypoxic f V at 4 dpf. Similar to wild-type, as larvae of all knockout lines developed, the magnitude of f V increased but to a lesser degree than in the wild-type larvae, until 15 dpf at which point there was no difference among the genotypes. In adult zebrafish, only in Hif-1B knockout fish was there an attenuation in f V during sustained exposure to 30 mmHg for 1 h but there was no effect when fish were exposed for a shorter duration to progressive hypoxia. The mechanism of action of Hif-1α, in part, may be through its downstream target, nitric oxide synthase, and its product, nitric oxide. Overall, the effect of each Hif-1α paralog on the hypoxic ventilatory response of zebrafish varies over development and is dependent on the type of hypoxic stress.

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“…The experiments also did not localize the internal chemoreception sites for ammonia. In teleosts, there is strong evidence that NECs in the gills are involved, serving as trimodal receptors for O 2 , CO 2 and ammonia (Zhang et al, 2011(Zhang et al, , 2015Perry and Tzaneva, 2016), as well as correlative evidence that central chemoreception of elevated ammonia concentrations in the brain may also contribute to ammonia detection (Zhang et al, 2013). In mammals, the situation is unclear, but central chemoreception of elevated brain ammonia appears to be important in the hyperventilatory response (see Introduction).…”

Section: Ventilation Changes In Hagfish Loaded Internally With Ammoniamentioning

confidence: 99%

“…Ammonia is produced and excreted at a rate of about 10-20% of carbon dioxide excretion (ṀC O2 ) in ammoniotelic teleost fish (Wood, 2001). Building on pioneering studies by Hillaby and Randall (1979) and McKenzie et al (1993), Zhang and co-workers have shown that ammonia plays an important role in stimulating ventilation in the freshwater rainbow trout (Oncorhynchus mykiss; Zhang and Wood, 2009;Zhang et al, 2015), and the same appears to be true in the zebrafish (Danio rerio; Perry and Tzaneva, 2016). Somewhat surprisingly, breathing is also stimulated by ammonia in a ureotelic elasmobranch, the Pacific spiny dogfish (Squalus acanthias suckleyi; De .…”

Section: Introductionmentioning

confidence: 99%

“…HEA acts by causing ammonia to diffuse across the body surface, predominantly the gills, into the bloodstream where it acts on internal receptors. At least in part, these internal ammonia receptors are the neuroepithelial cells (NECs) in the gills (Zhang et al, 2011), which are now believed to be trimodal oxygen, carbon dioxide and ammonia detectors for respiratory sensing (Zhang et al, 2015;Perry and Tzaneva, 2016), although there is also some evidence that ammonia may also act centrally on the brain (Wilkie et al, 2011;Zhang et al, 2013;Lisser et al, 2017). Ammonia can also act as a ventilatory stimulant in mammals, which are ureotelic like elasmobranchs, and this stimulation is thought to be important in exercise-induced hyperventilation (Mutch and Banister, 1983), as well as in supporting breathing during severe respiratory acidosis and hepatic coma (Roberts et al, 1956;Warren, 1958;Felipo and Butterworth, 2002).…”

Section: Introductionmentioning

confidence: 99%

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Ventilatory sensitivity to ammonia in the Pacific hagfish (Eptatretus stoutii), a representative of the oldest extant connection to the ancestral vertebrates

Eom

Giacomin

Clifford

et al. 2019

Journal of Experimental Biology

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Ventilatory sensitivity to ammonia occurs in teleosts, elasmobranchs and mammals. Here, we investigated whether the response is also present in hagfish. Ventilatory parameters (nostril flow, pressure amplitude, velar frequency and ventilatory index, the last representing the product of pressure amplitude and frequency), together with blood and water chemistry, were measured in hagfish exposed to either high environmental ammonia (HEA) in the external sea water or internal ammonia loading by intra-vascular injection. HEA exposure (10 mmol l −1 NH 4 HCO 3 or 10 mmol l −1 NH 4 Cl) caused a persistent hyperventilation by 3 h, but further detailed analysis of the NH 4 HCO 3 response showed that initially (within 5 min) there was a marked decrease in ventilation (80% reduction in ventilatory index and nostril flow), followed by a later 3-fold increase, by which time plasma total ammonia concentration had increased 11-fold. Thus, hyperventilation in HEA appeared to be an indirect response to internal ammonia elevation, rather than a direct response to external ammonia. HEA-mediated increases in oxygen consumption also occurred. Responses to NH 4 HCO 3 were greater than those to NH 4 Cl, reflecting greater increases over time in water pH and P NH3 in the former. Hagfish also exhibited hyperventilation in response to direct injection of isotonic NH 4 HCO 3 or NH 4 Cl solutions into the caudal sinus. In all cases where hyperventilation occurred, plasma total ammonia and P NH3 levels increased significantly, while blood acid-base status remained unchanged, indicating specific responses to internal ammonia elevation. The sensitivity of breathing to ammonia arose very early in vertebrate evolution.

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The sensing of respiratory gases in fish: Mechanisms and signalling pathways

Cited by 33 publications

References 126 publications

Hypoxia Tolerance in Teleosts: Implications of Cardiac Nitrosative Signals

Hypoxia Tolerance in Teleosts: Implications of Cardiac Nitrosative Signals

Hif-1α paralogs play a role in the hypoxic ventilatory response of larval and adult zebrafish (Danio rerio)

Ventilatory sensitivity to ammonia in the Pacific hagfish (Eptatretus stoutii), a representative of the oldest extant connection to the ancestral vertebrates

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