Free amino acids in fish brain: Normal levels and changes upon exposure to high ammonia concentrations in vivo, and upon incubation of brain slices

Levi, Giulio; Morisi, G; Colettp, Alberto; Catanzaro, R

doi:10.1016/0300-9629(74)90890-1

Cited by 69 publications

(23 citation statements)

References 14 publications

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“…The control brain ammonia concentration of ~2mmolkg -1 WM was in the same range or slightly higher than values previously reported in goldfish (Levi et al, 1974), trout (Arillo et al, 1981), mudskippers (Ip et al, 2005), and the toadfishes O. beta and O. tau (Wang and Walsh, 2000). After 2-5days of ammonia exposure, however, the concentration of ammonia measured in the whole brain of goldfish was 6-7mmolkg -1 WM, which is in the same range measured in ammonia-tolerant fishes following sub-lethal IP injections of NH 4 + , air exposure or elevated external ammonia.…”

Section: Discussion the Anoxia-tolerant Goldfish Is Ammonia Tolerantsupporting

confidence: 74%

“…As expected, exposure to ammonia resulted in pronounced increases in brain glutamine concentration in the goldfish. Baseline (pre-exposure) glutamine levels were comparable to concentrations reported by Levi et al (Levi et al, 1974) in goldfish, but about 2-3-fold greater than concentrations reported by Schenone et al (Schenone et al, 1982) on the same species. This variation could be due to differences in the genetic strain of goldfish used, season, feeding status and/or diet.…”

Section: Discussion the Anoxia-tolerant Goldfish Is Ammonia Tolerantsupporting

confidence: 65%

“…Such studies suggest that fish may have a 'reserve capacity' to detoxify ammonia (Sanderson et al, 2010). Indeed, 'partial amino acid catabolism' of NH 4 + to alanine has been proposed for mudskippers (Ip et al, 2004b), the Indian air-breathing catfishes (Saha and Ratha, 2007) and for goldfish (Levi et al, 1974). This reserve capacity may also partially explain why the effects of MSO on trout and goldfish survival at HEA varied.…”

Section: P Wilkie and Othersmentioning

confidence: 99%

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The relationship between NMDA receptor function and the high ammonia tolerance of anoxia-tolerant goldfish

Wilkie

Pamenter

Duquette

et al. 2011

Journal of Experimental Biology

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SUMMARY Acute ammonia toxicity in vertebrates is thought to be characterized by a cascade of deleterious events resembling those associated with anoxic/ischemic injury in the central nervous system. A key event is the over-stimulation of neuronal N-methyl-D-aspartate (NMDA) receptors, which leads to excitotoxic cell death. The similarity between the responses to acute ammonia toxicity and anoxia suggests that anoxia-tolerant animals such as the goldfish (Carassius auratus Linnaeus) may also be ammonia tolerant. To test this hypothesis, the responses of goldfish were compared with those of the anoxia-sensitive rainbow trout (Oncorhynchus mykiss Walbaum) during exposure to high external ammonia (HEA). Acute toxicity tests revealed that goldfish are ammonia tolerant, with 96 h median lethal concentration (LC50) values of 199 μmol l–1 and 4132 μmol l–1 for NH3 and total ammonia ([TAmm]=[NH3]+[NH4+]), respectively. These values were ∼5–6 times greater than corresponding NH3 and TAmm LC50 values measured in rainbow trout. Further, the goldfish readily coped with chronic exposure to NH4Cl (3–5 mmol l–1) for 5 days, despite 6-fold increases in plasma [T] to ∼1300 μmol l–1 and 3-fold increases in brain [TAmm] to 6700 μmol l–1. Muscle [TAmm] increased by almost 8-fold from ∼900 μmol kg–1 wet mass (WM) to greater than 7000 μmol kg–1 WM by 48 h, and stabilized. Although urea excretion rates (JUrea) increased by 2–3-fold during HEA, the increases were insufficient to offset the inhibition of ammonia excretion that occurred, and increases in urea were not observed in the brain or muscle. There was a marked increase in brain glutamine concentration at HEA, from ∼3000 μmol kg–1 WM to 15,000 μmol kg–1 WM after 48 h, which is consistent with the hypothesis that glutamine production is associated with ammonia detoxification. Injection of the NMDA receptor antagonists MK801 (0.5–8 mg kg–1) or ethanol (1–8 mg kg–1) increased trout survival time by 1.5–2.0-fold during exposure to 2 mmol l–1 ammonia, suggesting that excitotoxic cell death contributes to ammonia toxicity in this species. In contrast, similar doses of MK801 or ethanol had no effect on ammonia-challenged (8–9.5 mmol l–1TAmm) goldfish survival times, suggesting that greater resistance to excitotoxic cell death contributes to the high ammonia-tolerance of the goldfish. Whole-cell recordings measured in isolated brain slices of goldfish telencephalon during in vitro exposure to 5 mmol l–1 or 10 mmol l–1TAmm reversibly potentiated NMDA receptor currents. This observation suggested that goldfish neurons may not be completely resistant to ammonia-induced excitotoxicity. Subsequent western blot and densitometric analyses revealed that NMDA receptor NR1 subunit abundance was 40–60% lower in goldfish exposed to 3–5 mmol l–1TAmm for 5 days, which was followed by a restoration of NR1 subunit abundance after 3 days recovery in ammonia-free water. We conclude that the goldfish brain may be protected from excitotoxicity by downregulating the abundance of functional NMDA receptors during periods when it experiences increased internal ammonia.

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Section: Discussion the Anoxia-tolerant Goldfish Is Ammonia Tolerantsupporting

confidence: 74%

Section: Discussion the Anoxia-tolerant Goldfish Is Ammonia Tolerantsupporting

confidence: 65%

Section: P Wilkie and Othersmentioning

confidence: 99%

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The relationship between NMDA receptor function and the high ammonia tolerance of anoxia-tolerant goldfish

Wilkie

Pamenter

Duquette

et al. 2011

Journal of Experimental Biology

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“…The brain glutamine levels increased significantly upon exposure to high ambient ammonia in the common carp Cyprinus carpio (Dabrowska and Wlasow, 1986), the goldfish Carassius auratus (Levi et al, 1974) and rainbow trout Oncorhynchus mykiss (Arillo et al, 1981). Studies on the mudskippers Periophthalmodon schlosseri and Boleophthalmus boddaerti (Peng et al, 1998), as well as the four-eyed sleeper Bostrichthys sinensis (Anderson et al, 2002), also revealed increased levels of glutamine in their muscle, liver and plasma, in addition to the brain, during exposure to high ambient ammonia.…”

Section: Glutamine Formationmentioning

confidence: 99%

Dogmas and controversies in the handling of nitrogenous wastes: Ammonia tolerance in the oriental weatherloachMisgurnus anguillicaudatus

Tsui

Randall

Hanson

et al. 2004

Journal of Experimental Biology

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SUMMARYThe oriental weatherloach Misgurnus anguillicaudatus is an extremely ammonia-tolerant fish. Many ammonia-protection mechanisms have been reported in this fish. Six strategies used by this fish to deal with the problem of excess ammonia are described. The fish can (1) reduce ammonia production through reduction in protein and/or amino acid catabolism; (2)reduce ammonia production and obtain energy through partial amino acid catabolism leading to alanine formation; (3) detoxify ammonia to glutamine;(4) tolerate very high ammonia levels in its tissues; (5) get rid of ammonia as NH3 gas and, probably, (6) possesses background K+channels that are impermeable to NH4+. The effects of extracellular ammonia on the contraction performance of the heart from this fish were found to be the same as in rainbow trout, an ammonia-sensitive fish. It suggests that the hearts of most, if not all, fish species are protected against ammonia. MK-801, an NMDA receptor blocker, was found to have a protective effect against ammonia intoxication in the oriental weatherloach,which suggests that the NMDA receptor, as in mammals, is involved in ammonia toxicity.

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“…Longer exposure of fishes to ammonia, lasting several days or weeks, caused perturbations in hormonal processes (Ball 1967;Donaldson 1981), qualitative changes of free amino acids in the brain and muscles (Levi et al 1974;Knapp and Wieser 1981;Dqbrowska and Wlasow 1986), perturbations in water exchange (Lloyd and Orr 1969;Arillo et al 1981), decrease in erythrocyte count (Redner and Stickney 1979), necrotic and histopathologic changes in the gills, skin, kidney, liver, and alimentary tract (Flis 1968 b;Lloyd 1971;Smart 1976) and it caused elevated susceptibility of fishes to bacterial diseases (Ferguson 1992).…”

Section: Introductionmentioning

confidence: 99%

Influence of ammonia on performance ability of the common bream (Abramis brama L.)

Kłyszejko¹

1998

Acta Ichthyol. Piscat.

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Influence of NH 3 in doses of 0.1-0.5 mg/dm 3 on per formance ability of the common bream was studied at 15 and 20°C using a method of burdening the fish with predeteffilined physical effort. The ergometric readin � s revealed, that within the range of 0.12-0.13 mg of NH 3 /dm there was no effect of ammonia on lowering the performance ability of the fish. Within the concentration range of 0.37-0.39 mg ofNH 3 /dm3, at 15°C the value of work declined to 54% and at 20°c�to 22% of the respective values of control group.

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Free amino acids in fish brain: Normal levels and changes upon exposure to high ammonia concentrations in vivo, and upon incubation of brain slices

Cited by 69 publications

References 14 publications

The relationship between NMDA receptor function and the high ammonia tolerance of anoxia-tolerant goldfish

The relationship between NMDA receptor function and the high ammonia tolerance of anoxia-tolerant goldfish

Dogmas and controversies in the handling of nitrogenous wastes: Ammonia tolerance in the oriental weatherloachMisgurnus anguillicaudatus

Influence of ammonia on performance ability of the common bream (Abramis brama L.)

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