Gastrointestinal uptake and distribution of copper in rainbow trout

S. J. Clearwater, S. J. Baskin, C. M. Wood, D. G. McDonald

Research output: Contribution to journalArticle

75 Citations (Scopus)

Abstract

A single dose of radioactive copper (64Cu or new Cu) was infused into the stomach of rainbow trout (Oncorhynchus mykiss) to model dietary copper (Cu) uptake under conditions of a normal nutritional dose and optimum environmental temperature (16°C, 0.117 μg Cu g-1 body mass). The distribution of new Cu to the gut and internal organs occurred in two phases: rapid uptake by the gut tissues (almost complete by 24h post-infusion) followed by slower uptake by the internal organs. By 72h, 60 % of the dose had been excreted, 19 % was still retained in the gut tissue, 10 % remained in the lumen and 12 % had been absorbed across the gut and partitioned amongst the internal organs. A reduction in water temperature of 10°C (to 6°C) significantly retarded components of new Cu distribution (movement of the bolus along the gut and excretion); nonetheless, by 72h, the fraction absorbed by all the internal organs was similar to that at 16°C. An increase in water temperature of 3°C (to 19°C) caused a pronounced increase in internal organ uptake by 24h to approximately double the uptake occurring at 16°C. The uptake of new Cu by the gut tissue had a low temperature coefficient (Q10<1) consistent with simple diffusion, while the temperature coefficient for transfer of new Cu from gut tissue to the internal organs was high (Q10>2), consistent with facilitated transport. Internally, the liver and gall bladder (including bile) were the target organs for dietary Cu partitioning since they were the only organs that concentrated new Cu from the plasma. Individual tissues differed in terms of the exchange of their background Cu pools with new Cu. The background Cu in the walls of the gastrointestinal tract (excluding stomach) exchanged 45-94 % with new Cu from the gut lumen, while tissues such as the stomach, gills, kidney, carcass and fat had 5-7 % exchangeable background Cu. The liver, heart, spleen, ovary, bile and plasma had only 0.2-0.8 % exchangeable background Cu. The gastrointestinal tissues appear to act as a homeostatic organ, regulating the absorption of nutritional (non-toxic) doses of Cu (0.117 μg g-1 body mass day-1) by the internal organs. Within the dose range we used and at optimal temperature (16°C), the new Cu content of the gut tissues fluctuated, but absorption of new Cu by the internal organs remained relatively constant. For example, predosing the fish with non-radioactive Cu caused new Cu absorption by the gut tissues to double and decreased new Cn excretion from 38 to 1.5 %, but had no effect on new Cu uptake by the internal organs. Feeding fish after application of the normal liquid dose of new Cu also had no effect on new Cu uptake by the internal organs, even though the presence of food in the digestive tract reduced the binding of new Cu to the gut tissues and assisted with the excretion of new Cu. The gut was therefore able to regulate new Cu internalization at this dosage. Higher new Cu doses (10, 100 and 1000 times the normal dose), however, evoked regurgitation and increased new Cu excretion within 4 h of application but did not elevate new Cu levels in gut tissue beyond a threshold of approximately 40 μg of new Cu. Only at the highest dose (1000 times the normal dose, 192 μg g-1 body mass), equivalent to toxic concentrations in the daily diet (7000 μg Cu g-1 dry mass food), was the buffering capacity of the gut overwhelmed, resulting in an increase in internal new Cu uptake.

Original languageEnglish
Pages (from-to)2455-2466
Number of pages12
JournalJournal of Experimental Biology
Volume203
Issue number16
StatePublished - Jan 1 2000

Fingerprint

Oncorhynchus mykiss
rainbow
Copper
digestive system
copper
uptake mechanisms
dosage
excretion
Temperature
Stomach
body mass
Bile
stomach
Gastrointestinal Tract
Fishes
bile
organ
distribution
water temperature
Food

Keywords

  • Cu
  • Copper
  • Copper homeostasis
  • Dietary copper
  • Gastrointestinal uptake
  • Oncorhynchus mykiss
  • Radioactive copper
  • Rainbow trout
  • Teleost

ASJC Scopus subject areas

  • Agricultural and Biological Sciences(all)
  • Agricultural and Biological Sciences (miscellaneous)

Cite this

Clearwater, S. J., Baskin, S. J., Wood, C. M., & McDonald, D. G. (2000). Gastrointestinal uptake and distribution of copper in rainbow trout. Journal of Experimental Biology, 203(16), 2455-2466.

Gastrointestinal uptake and distribution of copper in rainbow trout. / Clearwater, S. J.; Baskin, S. J.; Wood, C. M.; McDonald, D. G.

In: Journal of Experimental Biology, Vol. 203, No. 16, 01.01.2000, p. 2455-2466.

Research output: Contribution to journalArticle

Clearwater, SJ, Baskin, SJ, Wood, CM & McDonald, DG 2000, 'Gastrointestinal uptake and distribution of copper in rainbow trout', Journal of Experimental Biology, vol. 203, no. 16, pp. 2455-2466.
Clearwater SJ, Baskin SJ, Wood CM, McDonald DG. Gastrointestinal uptake and distribution of copper in rainbow trout. Journal of Experimental Biology. 2000 Jan 1;203(16):2455-2466.
Clearwater, S. J. ; Baskin, S. J. ; Wood, C. M. ; McDonald, D. G. / Gastrointestinal uptake and distribution of copper in rainbow trout. In: Journal of Experimental Biology. 2000 ; Vol. 203, No. 16. pp. 2455-2466.
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N2 - A single dose of radioactive copper (64Cu or new Cu) was infused into the stomach of rainbow trout (Oncorhynchus mykiss) to model dietary copper (Cu) uptake under conditions of a normal nutritional dose and optimum environmental temperature (16°C, 0.117 μg Cu g-1 body mass). The distribution of new Cu to the gut and internal organs occurred in two phases: rapid uptake by the gut tissues (almost complete by 24h post-infusion) followed by slower uptake by the internal organs. By 72h, 60 % of the dose had been excreted, 19 % was still retained in the gut tissue, 10 % remained in the lumen and 12 % had been absorbed across the gut and partitioned amongst the internal organs. A reduction in water temperature of 10°C (to 6°C) significantly retarded components of new Cu distribution (movement of the bolus along the gut and excretion); nonetheless, by 72h, the fraction absorbed by all the internal organs was similar to that at 16°C. An increase in water temperature of 3°C (to 19°C) caused a pronounced increase in internal organ uptake by 24h to approximately double the uptake occurring at 16°C. The uptake of new Cu by the gut tissue had a low temperature coefficient (Q10<1) consistent with simple diffusion, while the temperature coefficient for transfer of new Cu from gut tissue to the internal organs was high (Q10>2), consistent with facilitated transport. Internally, the liver and gall bladder (including bile) were the target organs for dietary Cu partitioning since they were the only organs that concentrated new Cu from the plasma. Individual tissues differed in terms of the exchange of their background Cu pools with new Cu. The background Cu in the walls of the gastrointestinal tract (excluding stomach) exchanged 45-94 % with new Cu from the gut lumen, while tissues such as the stomach, gills, kidney, carcass and fat had 5-7 % exchangeable background Cu. The liver, heart, spleen, ovary, bile and plasma had only 0.2-0.8 % exchangeable background Cu. The gastrointestinal tissues appear to act as a homeostatic organ, regulating the absorption of nutritional (non-toxic) doses of Cu (0.117 μg g-1 body mass day-1) by the internal organs. Within the dose range we used and at optimal temperature (16°C), the new Cu content of the gut tissues fluctuated, but absorption of new Cu by the internal organs remained relatively constant. For example, predosing the fish with non-radioactive Cu caused new Cu absorption by the gut tissues to double and decreased new Cn excretion from 38 to 1.5 %, but had no effect on new Cu uptake by the internal organs. Feeding fish after application of the normal liquid dose of new Cu also had no effect on new Cu uptake by the internal organs, even though the presence of food in the digestive tract reduced the binding of new Cu to the gut tissues and assisted with the excretion of new Cu. The gut was therefore able to regulate new Cu internalization at this dosage. Higher new Cu doses (10, 100 and 1000 times the normal dose), however, evoked regurgitation and increased new Cu excretion within 4 h of application but did not elevate new Cu levels in gut tissue beyond a threshold of approximately 40 μg of new Cu. Only at the highest dose (1000 times the normal dose, 192 μg g-1 body mass), equivalent to toxic concentrations in the daily diet (7000 μg Cu g-1 dry mass food), was the buffering capacity of the gut overwhelmed, resulting in an increase in internal new Cu uptake.

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KW - Copper homeostasis

KW - Dietary copper

KW - Gastrointestinal uptake

KW - Oncorhynchus mykiss

KW - Radioactive copper

KW - Rainbow trout

KW - Teleost

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