Effects of moderate and substantial hypoxia on erythropoietin levels in rainbow trout kidney and spleen

SUMMARYAppetite suppression is a common response to hypoxia in fish that confers significant energy savings. Yet little is known about the endocrine signals involved in the regulation of food intake during chronic hypoxia. Thus, we assessed the impact of chronic hypoxia on food intake, the expression of the potent anorexigenic signal leptin and its receptor (lepr), the mRNA levels of key hypothalamic appetite-regulating genes, and the activity of the hypothalamic-pituitary-interrenal (HPI) axis in common carp, Cyprinus carpio. Fish exposed to 10% O 2 saturation for 8days were chronically anorexic and consumed on average 79% less food than normoxic controls. Hypoxia also elicited gradual and parallel increases in the expression of liver leptin-a-I, leptin-a-II, lepr and erythropoietin, a known hypoxia-responsive gene. In contrast, the liver mRNA levels of all four genes remained unchanged in normoxic fish pair-fed to the hypoxia treatment. In the hypothalamus, expression of the appetite-regulating genes were consistent with an inhibition and stimulation of hunger in the hypoxic and pair-fed fish, respectively, and reduced feed intake led to a decrease in lepr. Although both treatments elicited similar delayed increases in plasma cortisol, they were characterized by distinct HPI axis effector transcript levels and a marked differential increase in pituitary lepr expression. Together, these results show that a reduction in O 2 availability, and not feed intake, stimulates liver leptin-a expression in common carp and suggest that this pleiotropic cytokine is involved in the regulation of appetite and the endocrine stress response during chronic hypoxia.

Section: Discussionmentioning

confidence: 53%

Differential effects of chronic hypoxia and feed restriction on the expression of leptin and its receptor, food intake regulation and the endocrine stress response in common carp

Bernier

Gorissen

Flik

2012

“…Increasing the number of circulating RBCs in response to hypoxia to enhance O 2 transport, via erythropoiesis or splenic release, is a strategy used by many fishes (e.g. Tetens and Lykkeboe, 1981;Murad et al, 1990;Soldatov, 1996;Lai et al, 2006), but there are exceptions (e.g. McLeod et al, 1978;Routley et al, 2002).…”

Section: Research Articlementioning

confidence: 99%

The amphibious fishKryptolebias marmoratususes alternate strategies to maintain oxygen delivery during aquatic hypoxia and air exposure

Turko

Robertson

Bianchini

et al. 2014

Despite the abundance of oxygen in atmospheric air relative to water, the initial loss of respiratory surface area and accumulation of carbon dioxide in the blood of amphibious fishes during emersion may result in hypoxemia. Given that the ability to respond to low oxygen conditions predates the vertebrate invasion of land, we hypothesized that amphibious fishes maintain O 2 uptake and transport while emersed by mounting a co-opted hypoxia response. We acclimated the amphibious fish Kryptolebias marmoratus, which are able to remain active for weeks in both air and water, for 7 days to normoxic brackish water (15‰, ~21 kPa O 2 ; control), aquatic hypoxia (~3.6 kPa), normoxic air (~21 kPa) or aerial hypoxia (~13.6 kPa). Angiogenesis in the skin and bucco-opercular chamber was pronounced in air-versus water-acclimated fish, but not in response to hypoxia. Aquatic hypoxia increased the O 2 -carrying capacity of blood via a large (40%) increase in red blood cell density and a small increase in the affinity of hemoglobin for O 2 (P 50 decreased 11%). In contrast, air exposure increased the hemoglobin O 2 affinity (decreased P 50 ) by 25% without affecting the number of red blood cells. Acclimation to aerial hypoxia both increased the O 2 -carrying capacity and decreased the hemoglobin O 2 affinity . These results suggest that O 2 transport is regulated both by O 2 availability and also, independently, by air exposure. The ability of the hematological system to respond to air exposure independent of O 2 availability may allow extant amphibious fishes, and may also have allowed primitive tetrapods to cope with the complex challenges of aerial respiration during the invasion of land.KEY WORDS: Hemoglobin, Oxygen-carrying capacity, Hemoglobin-oxygen affinity, Air-breathing organ, Air-breathing fish, Mangrove rivulus INTRODUCTIONThe transition from aquatic to terrestrial life represents a major step in vertebrate evolution because the physical conditions between these environments are dramatically different. Oxygen solubility is relatively low in water and even well-oxygenated aquatic environments contain only about 3% of the O 2 available in atmospheric air (Dejours, 1988). Low concentrations of aquatic O 2 , particularly in hypoxic habitats, have often been hypothesized to be one of the driving forces behind the evolution of amphibious or terrestrial life histories because invasion of land would allow animals to exploit the O 2 -rich aerial environment (Graham, 1997). RESEARCH ARTICLEDepartment of Integrative Biology, University of Guelph, Guelph, ON N1G 2W1, Canada.*Author for correspondence (aturko@uoguelph.ca) Received 4 July 2014; Accepted 15 September 2014Taking advantage of aerial O 2 presents several challenges for fishes. Water-breathing fishes exchange respiratory gases across the gills but during emersion the gill lamellae typically collapse and coalesce, reducing the surface area available for respiration. Accumulation of CO 2 in the blood of emersed fishes, resulting from the low solubility of CO 2 in...

“…For example, elevated [Hb] enhances the blood O 2 carrying capacity (Lai et al, 2006;Petersen and Gamperl, 2011;Wells et al, 1989). Similarly, increased Hb-O 2 affinities are commonly reported to improve the O 2 -uptake capacity of Hb during environmental hypoxia (Weber et al, 1976;Wood and Johansen, 1972).…”

Section: Is There Evidence Of Aerobic Adjustments Improving Hypoxia Tmentioning

confidence: 99%

Low O2 acclimation shifts the hypoxia avoidance behaviour of snapper (Pagrus auratus) with only subtle changes in aerobic and anaerobic function

Cook

Iftikar

Baker

et al. 2012

SUMMARYIt was hypothesised that chronic hypoxia acclimation (preconditioning) would alter the behavioural low-O 2 avoidance strategy of fish as a result of both aerobic and anaerobic physiological adaptations. Avoidance and physiological responses of juvenile snapper (Pagrus auratus) were therefore investigated following a 6week period of moderate hypoxia exposure (10.2-12.1kPa P O2 , 21±1°C) and compared with those of normoxic controls (P O2 =20-21kPa, 21±1°C). The critical oxygen pressure (P crit ) limit of both groups was unchanged at ~7kPa, as were standard, routine and maximum metabolic rates. However, hypoxia-acclimated fish showed increased tolerances to hypoxia in behavioural choice chambers by avoiding lower P O2 levels (3.3±0.7 vs 5.3±1.1kPa) without displaying greater perturbations of lactate or glucose. This behavioural change was associated with unexpected physiological adjustments. For example, a decrease in blood O 2 carrying capacity was observed after hypoxia acclimation. Also unexpected was an increase in whole-blood P 50 following acclimation to low O 2 , perhaps facilitating Hb-O 2 off-loading to tissues. In addition, cardiac mitochondria measured in situ using permeabilised fibres showed improved O 2 uptake efficiencies. The proportion of the anaerobic enzyme lactate dehydrogenase, at least relative to the aerobic marker enzyme citrate synthase, also increased in heart and skeletal red muscle, indicating enhanced anaerobic potential, or in situ lactate metabolism, in these tissues. Overall, these data suggest that a prioritization of O 2 delivery and O 2 utilisation over O 2 uptake during long-term hypoxia may convey a significant survival benefit to snapper in terms of behavioural low-O 2 tolerance.