scholarly journals The Metabolomic Response of Crucian Carp (Carassius carassius) to Anoxia and Reoxygenation Differs between Tissues and Hints at Uncharacterized Survival Strategies

Metabolites ◽  
2021 ◽  
Vol 11 (7) ◽  
pp. 435
Author(s):  
Helge-Andre Dahl ◽  
Anette Johansen ◽  
Göran E. Nilsson ◽  
Sjannie Lefevre
Keyword(s):  
Crucian Carp ◽  
Survival Strategies ◽  
Tissue Type ◽  
Control Fish ◽  
Carassius Carassius ◽  
Physiological Mechanisms ◽  
Normoxic Control ◽  
The Brain ◽  
Crucian Carp Carassius Carassius ◽  
Single Organ

The anoxia-tolerant crucian carp (Carassius carassius) has been studied in detail for numerous years, with particular focus on unravelling the underlying physiological mechanisms of anoxia tolerance. However, relatively little work has been focused on what occurs beyond anoxia, and often the focus is a single organ or tissue type. In this study, we quantified more than 100 metabolites by capillary electrophoresis-mass spectrometry (CE-MS) in brain, heart, liver, and blood plasma from four experimental groups, being normoxic (control) fish, anoxia-exposed fish, and two groups that had been exposed to anoxia followed by reoxygenation for either 3 h or 24 h. The heart, which maintains cardiac output during anoxia, unexpectedly, was slower to recover compared to the brain and liver, mainly due to a slower return to control concentrations of the energy-carrying compounds ATP, GTP, and phosphocreatine. Crucian carp accumulated amino acids in most tissues, and also surprisingly high levels of succinate in all tissues investigated during anoxia. Purine catabolism was enhanced, leading to accumulation of uric acid during anoxia and increasing urea formation that continued into 24 h of reoxygenation. These tissue-specific differences in accumulation and distribution of the metabolites may indicate an intricate system of transport between tissues, opening for new avenues of investigation of possible mechanisms aimed at reducing the generation of reactive oxygen species (ROS) and resultant tissue damage during reoxygenation.

Effects of anoxia on catecholamine levels in brain and kidney of the crucian carp

1989 ◽  
Vol 257 (1) ◽  
pp. R10-R14 ◽  
Author(s):  
G. E. Nilsson
Keyword(s):  
Crucian Carp ◽  
Adaptive Strategy ◽  
Carassius Carassius ◽  
Catecholamine Synthesis ◽  
The Brain ◽  
Short Contacts ◽  
Crucian Carp Carassius Carassius ◽  
Limited Possibility ◽  
Catecholamine Levels ◽  
Chromaffin Tissue

Catecholamine synthesis requires O2. Crucian carp (Carassius carassius L.), which are extremely anoxia tolerant, were exposed to anoxia for 76 or 160 h. The brain levels of dopamine and norepinephrine (no epinephrine was found in brain) remained relatively constant even after nearly 1 wk of anoxia, indicating very well-functioning transmitter reuptake mechanisms and/or the absence of O2-independent degradation. In contrast, in the kidney (which contains chromaffin tissue), the catecholamine content (at least norepinephrine) decreased by 22-60% after 160 h of anoxia. Moreover, when anoxic crucian carps were put in normoxic water for approximately 40 min, the kidney catecholamine levels increased by 50-370%, whereas no significant effect was seen in brain. Thus, in the kidney, all that was lost during nearly 1 wk of anoxia seemed to be regained in less than 40 min of normoxia. This might reflect an adaptive strategy. Because of the limited possibility of recovering catecholamines that have been released into the bloodstream, the crucian carp chromaffin tissue might have become very good at taking the opportunities given by short contacts with O2 to rapidly renew its catecholamine store.

Expression of heat shock proteins in anoxic crucian carp (Carassius carassius): support for cold as a preparatory cue for anoxia

2010 ◽  
Vol 298 (6) ◽  
pp. R1499-R1508 ◽  
Author(s):  
Kåre-Olav Stensløkken ◽  
Stian Ellefsen ◽  
Helene Kile Larsen ◽  
Jarle Vaage ◽  
Göran E. Nilsson
Keyword(s):  
Heat Shock ◽  
Heat Shock Proteins ◽  
Protein Function ◽  
Crucian Carp ◽  
Cellular Damage ◽  
Winter Period ◽  
Carassius Carassius ◽  
Shock Proteins ◽  
The Brain ◽  
Crucian Carp Carassius Carassius

The crucian carp ( Carassius carassius ) tolerates anoxia for days to months depending on temperature. During episodes of stress, heat shock proteins (HSPs) are important for limiting cellular damage, mainly by ensuring protein function. Accordingly, we hypothesized that anoxia would change the expression of HSPs and that this response would be temperature dependent. Real-time RT-PCR was used to investigate the effects of 1 and 7 days anoxia (A1 and A7) on the expression of HSP70a, HSP70b, HSC70, HSP90, and HSP30 in the brain and heart of 8°C- and 13°C-acclimated crucian carp. In general, the expression of all HSPs changed in response to anoxia, although varying in size and direction, and with organ and temperature. HSP70a expression increased drastically (∼10-fold) in A7 brains and hearts at 13°C but not at 8°C. HSC70 and HSP90 expression decreased in A7 brains (by 60–70%), but not in A7 hearts. HSC70 expression increased in A1 brains and hearts at both temperatures (by 60–160%), and HSP30 expression decreased in A7 brains and hearts at both temperatures (by 50–80%). Notably, normoxic fish showed 7- and 11-fold higher HSP70a expression in the brain and heart at 8°C compared with 13°C. This difference disappeared during anoxia, suggesting that cold may function as a cue for preconditioning the crucian carp's HSP70a expression to the approaching anoxic winter period.

Effects of Anoxia on Serotonin Metabolism in Crucian Carp Brain

1989 ◽  
Vol 141 (1) ◽  
pp. 419-428 ◽  
Author(s):  
GÖRAN E. NILSSON
Keyword(s):  
Acetic Acid ◽  
Crucian Carp ◽  
Carassius Carassius ◽  
Serotonin Metabolism ◽  
Brain Oxygen ◽  
Constant Rate ◽  
The Common ◽  
The Brain ◽  
Crucian Carp Carassius Carassius ◽  
Monoamine Transmitters

In the brain, oxygen is required for both the synthesis and the degradation of monoamine transmitters, so monoaminergic systems can be expected to be strongly affected by anoxia. However, crucian carp (Carassius carassius L.) may survive anoxia for many days or even weeks. In the present study, crucian carp were exposed to anoxia for 22, 76, and 160 h at 8°C. All survived and were found to excrete ethanol at a constant rate. The brain concentrations of serotonin and its two main metabolites, 5-hydroxyindole-3-acetic acid (5-HIAA) and 5-hydroxytryptophol, were analysed after each experiment. In a preliminary experiment, it was found that the brain of the crucian carp contained about the same amount of serotonin and 5-HIAA as two species less tolerant to anoxia - the common carp and the rainbow trout. The levels of the serotonin metabolites decreased drastically (by 80–90%) during anoxia, whereas serotonin levels were only slightly reduced (by 15% or less). These results suggest a complete or nearly complete stop in serotonin metabolism during anoxia.

Differential regulation of AMP-activated kinase and AKT kinase in response to oxygen availability in crucian carp (Carassius carassius)

2008 ◽  
Vol 295 (6) ◽  
pp. R1803-R1814 ◽  
Author(s):  
Kåre-Olav Stensløkken ◽  
Stian Ellefsen ◽  
Jonathan A. W. Stecyk ◽  
Mai Britt Dahl ◽  
Göran E. Nilsson ◽  
...  
Keyword(s):  
Crucian Carp ◽  
Mammalian Species ◽  
Energy Charge ◽  
Pcr Analysis ◽  
Carassius Carassius ◽  
Energy Deficiency ◽  
Compound C ◽  
The Brain ◽  
Crucian Carp Carassius Carassius

We investigated whether two kinases critical for survival during periods of energy deficiency in anoxia-intolerant mammalian species, AMP-activated kinase (AMPK), and protein kinase B (AKT), are equally important for hypoxic/anoxic survival in the extremely anoxia-tolerant crucian carp ( Carassius carassius). We report that phosphorylation of AMPK and AKT in heart and brain showed small changes after 10 days of severe hypoxia (0.3 mg O2/l at 9°C). In contrast, anoxia exposure (0.01 mg O2/l at 8°C) substantially increased AMPK phosphorylation but decreased AKT phosphorylation in carp heart and brain, indicating activation of AMPK and deactivation of AKT. In agreement, blocking the activity of AMPK in anoxic fish in vivo with 20 mg/kg Compound C resulted in an elevated metabolic rate (as indicated by increased ethanol production) and tended to reduce energy charge. This is the first in vivo experiment with Compound C in a nonmammalian vertebrate, and it appears that AMPK plays a role in mediating anoxic metabolic depression in crucian carp. Real-time RT-PCR analysis of the investigated AMPK subunit revealed that the most likely composition of subunits in the carp heart is α2, β1B, γ2a, whereas a more even expression of subunits was found in the brain. In the heart, expression of the regulatory γ2-subunit increased in the heart during anoxia. In the brain, expression of the α1-, α2-, and γ1-subunits decreased with anoxia exposure, but expression of the γ2-subunit remained constant. Combined, our findings suggest that AMPK and AKT may play important, but opposing roles for hypoxic/anoxic survival in the anoxia-tolerant crucian carp.

Hypoxia Tolerance, Nitric Oxide, and Nitrite: Lessons From Extreme Animals

Physiology ◽  
2015 ◽  
Vol 30 (2) ◽  
pp. 116-126 ◽  
Author(s):  
Angela Fago ◽  
Frank B. Jensen
Keyword(s):  
Nitric Oxide ◽  
Marine Mammals ◽  
Crucian Carp ◽  
Physiological Responses ◽  
Oxygen Deprivation ◽  
Hypoxia Tolerance ◽  
Carassius Carassius ◽  
Slider Turtle ◽  
Total Lack ◽  
Crucian Carp Carassius Carassius

Among vertebrates able to tolerate periods of oxygen deprivation, the painted and red-eared slider turtles ( Chrysemys picta and Trachemys scripta) and the crucian carp ( Carassius carassius) are the most extreme and can survive even months of total lack of oxygen during winter. The key to hypoxia survival resides in concerted physiological responses, including strong metabolic depression, protection against oxidative damage and–in air-breathing animals–redistribution of blood flow. Each of these responses is known to be tightly regulated by nitric oxide (NO) and during hypoxia by its metabolite nitrite. The aim of this review is to highlight recent work illustrating the widespread roles of NO and nitrite in the tolerance to extreme oxygen deprivation, in particular in the red-eared slider turtle and crucian carp, but also in diving marine mammals. The emerging picture underscores the importance of NO and nitrite signaling in the adaptive response to hypoxia in vertebrate animals.

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