Physiological consequences of gill remodeling in goldfish (<i>Carassius auratus</i>) during exposure to long-term hypoxia

Mitrovic, Dejana; Dymowska, Agnieszka K.; Nilsson, Göran; Perry, Steve F.

doi:10.1152/ajpregu.00189.2009

Cited by 62 publications

(52 citation statements)

References 37 publications

(50 reference statements)

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“…In addition to these explanations, it should also be considered whether an enhanced urinary excretion or efflux via the gills might contribute to lower extracellular nitrite and nitrate in hypoxia. A recent study on goldfish, however, showed that hypoxia actually inhibits passive branchial ion efflux in spite of an increased respiratory surface area of the gills (Mitrovic et al, 2009), and in another hypoxia-tolerant fish (Amazonian oscar), both urinary and branchial ion excretion rates were decreased rather than increased by hypoxia (Wood et al, 2009).…”

Section: Influence Of Hypoxia On No Metabolitesmentioning

confidence: 93%

Nitric oxide metabolites in goldfish under normoxic and hypoxic conditions

Hansen

Frank

2010

Journal of Experimental Biology

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SUMMARYNitric oxide (NO), produced by nitric oxide synthases (NOS enzymes), regulates multiple physiological functions in animals. NO exerts its effects by binding to iron (Fe) of heme groups (exemplified by the activation of soluble guanylyl cyclase) and by Snitrosylation of proteins -and it is metabolized to nitrite and nitrate. Nitrite is used as a marker for NOS activity but it is also a NO donor that can be activated by various cellular proteins under hypoxic conditions. Here, we report the first systematic study of NO metabolites (nitrite, nitrate, S-nitroso, N-nitroso and Fe-nitrosyl compounds) in multiple tissues of a non-mammalian vertebrate (goldfish) under normoxic and hypoxic conditions. NO metabolites were measured in blood (plasma and red cells) and heart, brain, gill, liver, kidney and skeletal muscle, using highly sensitive reductive chemiluminescence. The severity of the chosen hypoxia levels was assessed from metabolic and respiratory variables. In normoxic goldfish, the concentrations of NO metabolites in plasma and tissues were comparable with values reported in mammals, indicative of similar NOS activity. Exposure to hypoxia [at P O2 (partial pressure of O 2 ) values close to and below the critical P O2 ] for two days caused large decreases in plasma nitrite and nitrate, which suggests reduced NOS activity and increased nitrite/nitrate utilization or loss. Tissue NO metabolites were largely maintained at their tissue-specific values under hypoxia, pointing at nitrite transfer from extracellular to intracellular compartments and cellular NO generation from nitrite. The data highlights the preference of goldfish to defend intracellular NO homeostasis during hypoxia.

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Section: Influence Of Hypoxia On No Metabolitesmentioning

confidence: 93%

Nitric oxide metabolites in goldfish under normoxic and hypoxic conditions

Hansen

Frank

2010

Journal of Experimental Biology

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“…Second, they alter the shape and structure of the gill to enhance oxygen exchange [41][42][43][44][45][46]. Some fishes alter the cardiac K(ATP) channel, metabolic rate, and increase the number of red blood cells [47,48].…”

Section: The Acute Hypoxia Stress Response In Fishesmentioning

confidence: 99%

The hypoxia signaling pathway and hypoxic adaptation in fishes

Xiao

2015

Sci. China Life Sci.

136

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The hypoxia signaling pathway is an evolutionarily conserved cellular signaling pathway present in animals ranging from Caenorhabditis elegans to mammals. The pathway is crucial for oxygen homeostasis maintenance. Hypoxia-inducible factors (HIF-1α and HIF-2α) are master regulators in the hypoxia signaling pathway. Oxygen concentrations vary a lot in the aquatic environment. To deal with this, fishes have adapted and developed varying strategies for living in hypoxic conditions. Investigations into the strategies and mechanisms of hypoxia adaptation in fishes will allow us to understand fish speciation and breed hypoxia-tolerant fish species/strains. This review summarizes the process of the hypoxia signaling pathway and its regulation, as well as the mechanism of hypoxia adaptation in fishes. Approximately 2.5 billion years ago, photosynthesis led to the accumulation of oxygen to levels that were likely toxic to many obligate anaerobes. However, increased availability of atmospheric O 2 led to the evolution of an extraordinarily efficient system of oxidative phosphorylation. In this system, chemical energy stored in the carbon bonds of organic molecules is transferred to the high-energy phosphate bond in ATP, which is then used to power physicochemical reactions in living cells [1]. Additionally, O 2 serves as the final electron acceptor in oxidative phosphorylation, which is not only required for energy production, but is also the direct substrate of many enzymes. Thus, it is critical for the growth, development, and reproduction of organisms. Consequently, metazoans have evolved complicated systems of cellular metabolism and physiology to maintain oxygen homeostasis and have developed a biochemical response to low oxygen levels [2]. There are a number of oxygen-sensing pathways that promote hypoxia tolerance by activating transcription and inhibiting translation: the energy and nutrient sensor mTOR, the unfolded protein response that activates the endoplasmic stress response, and the nuclear factor (NF)-B transcriptional response [3]. However, hypoxia-inducible factors (HIFs) are recognized as master regulators of the cellular response to hypoxic stress [4,5]. The hypoxia signaling pathway is evolutionarily conserved from Caenorhabditis elegans to human beings and it activates similar or homogenous gene expression, resulting in similar physical and biochemical responses. Compared with the terrestrial environment, oxygen concentrations vary greatly in the aquatic environment [6]. Thus, compared with most birds and mammals, fishes are tolerant of this varying oxygen availability. Natural selection by oxygen concentration has facilitated the evolution of fishes with a range of adaptations to variable oxygen concentration. Even in waters at the same latitude, closely related species or different strains within a species exhibit varied adaptations to oxygen concentration. Additionally, closely related fishes distributed in waters at different latitudes exhibit extensive variation in their tolerance of hypoxia. De...

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“…oxyregulation) (see Richards, 2011). Possible adjustments include increased heart rate, enhanced gill surface area via remodeling (Mitrovic et al, 2009), increased blood pigment levels, adjustment of enzyme systems, and elevated rates of ventilation. Some of these adjustments are triggered by hypoxia-mediated upregulation of gene expression patterns (Flück et al, 2007) while others are regulated physiologically.…”

Section: Defining Critical O 2 Levelsmentioning

confidence: 99%

Critical oxygen levels and metabolic suppression in oceanic oxygen minimum zones

Seibel

2011

Journal of Experimental Biology

299

243

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SummaryThe survival of oceanic organisms in oxygen minimum zones (OMZs) depends on their total oxygen demand and the capacities for oxygen extraction and transport, anaerobic ATP production and metabolic suppression. Anaerobic metabolism and metabolic suppression are required for daytime forays into the most extreme OMZs. Critical oxygen partial pressures are, within a range, evolved to match the minimum oxygen level to which a species is exposed. This fact demands that low oxygen habitats be defined by the biological response to low oxygen rather than by some arbitrary oxygen concentration. A broad comparative analysis of oxygen tolerance facilitates the identification of two oxygen thresholds that may prove useful for policy makers as OMZs expand due to climate change. Between these thresholds, specific physiological adaptations to low oxygen are required of virtually all species. The lower threshold represents a limit to evolved oxygen extraction capacity. Climate change that pushes oxygen concentrations below the lower threshold (~0.8kPa) will certainly result in a transition from an ecosystem dominated by a diverse midwater fauna to one dominated by diel migrant biota that must return to surface waters at night. Animal physiology and, in particular, the response of animals to expanding hypoxia, is a critical, but understudied, component of biogeochemical cycles and oceanic ecology. Here, I discuss the definition of hypoxia and critical oxygen levels, review adaptations of animals to OMZs and discuss the capacity for, and prevalence of, metabolic suppression as a response to temporary residence in OMZs and the possible consequences of climate change on OMZ ecology.

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Physiological consequences of gill remodeling in goldfish (Carassius auratus) during exposure to long-term hypoxia

Cited by 62 publications

References 37 publications

Nitric oxide metabolites in goldfish under normoxic and hypoxic conditions

Nitric oxide metabolites in goldfish under normoxic and hypoxic conditions

The hypoxia signaling pathway and hypoxic adaptation in fishes

Critical oxygen levels and metabolic suppression in oceanic oxygen minimum zones

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