Skip to main content
SpringerLink
Log in

In Vitro Examination of Interactions Between Copper and Zinc Uptake via the Gastrointestinal Tract of the Rainbow Trout (Oncorhynchus mykiss)

  • Published:
Archives of Environmental Contamination and Toxicology Aims and scope Submit manuscript

Abstract

An in vitro gut sac technique was used to investigate whether reciprocal inhibitory effects occurred between Cu and Zn uptake in the gastrointestinal tract of the rainbow trout and, if so, whether there was regional variation among the stomach, anterior intestine, mid intestine, and posterior intestine in the phenomena. Metal accumulation in surface mucus and in the mucosal epithelium and transport into the blood space were assayed using radiolabeled Cu or Zn at environmentally realistic concentrations of 50 μmol L−1 in the luminal saline, with 10-fold higher levels of the other metal (nonradioactive) as a potential inhibitor. Zn transport rates were generally higher than Cu transport rates in all compartments except the stomach, where they were lower. High [Zn] reduced Cu transport into the blood space in the mid and posterior intestines by 67% and 33%, respectively, whereas high [Cu] reciprocally reduced Zn transport into the blood space in these same sections by 54% and 78%. No inhibitions occurred in either the anterior intestine or the stomach. In these segments, elevated concentrations of the other metal stimulated Cu and Zn transport into the blood space and/or the mucosal epithelium by 50–100%, possibly by displacement from intracellular binding sites, thereby raising local concentrations at other transport sites. None of the treatments affected metal accumulation in surface mucus. The results indicate that one or more shared high-affinity pathways (possibly DMT1) occur in the mid and posterior intestine, which transport both Cu and Zn. These pathways appear to be absent from the stomach and anterior intestine, where other transport mechanisms may occur.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Log in via an institution

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2

Similar content being viewed by others

References

  • Baldisserotto B, Chowdhury MJ, Wood CM (2005) Effects of dietary calcium and cadmium on cadmium accumulation, calcium and cadmium uptake from the water, and their interactions in juvenile rainbow trout. Aquat Toxicol 72:99–117

    Article  CAS  Google Scholar 

  • Bucking CP, Wood CM (2007) Gastrointestinal tranort of Ca2+ and Mg2+ during the digestion of a single meal in the freshwater rainbow trout. J Comp Physiol B 177:349–360

    Article  CAS  Google Scholar 

  • Burke J, Handy RD (2005) Sodium-sensitive and -insensitive copper accumulation by isolated intestinal cells of rainbow trout Oncorhynchus mykiss. J Exp Biol 208:391–407

    Article  CAS  Google Scholar 

  • Bury NR, Walker PA, Glover CN (2003) Nutritive metal uptake in teleost fish. J Exp Biol 206:11–23

    Article  CAS  Google Scholar 

  • Clearwater SJ, Baskin SJ, Wood CM, McDonald DG (2000) Gastrointestinal uptake and distribution of copper in rainbow trout. J Exp Biol 203:2455–2466

    CAS  Google Scholar 

  • Clearwater SJ, Farag AM, Meyer JS (2002) Bioavailability and toxicity of dietborne copper and zinc to fish. Comp Biochem Physiol C 132:269–313

    Article  Google Scholar 

  • Cooper CA, Handy RD, Bury NR (2006) The effects of dietary iron concentration on gastrointestinal and branchial assimilation of both iron and cadmium in zebrafish (Danio rerio). Aquat Toxicol 79:167–175

    Article  CAS  Google Scholar 

  • Cooper CA, Shayeghi M, Techau ME, Capdevila DM, MacKenzie S, Durrant C, Bury NR (2008) Analysis of the rainbow trout solute carrier 11 family reveals iron import ≤ 7.4 and a functional isoform lacking transmembrane domains 11 and 12. FEBS Lett 581:2599–2604

    Article  Google Scholar 

  • Dallinger R, Kautzky H (1985) The importance of contaminated food for the uptake of heavy metals by rainbow trout (Salmo gairdneri): a field study. Oecologia 67:82–89

    Article  Google Scholar 

  • Donovan A, Brownlie A, Dorschner MO, Zhou Y, Pratt SJ, Paw BH, Phillips RB, Thisse C, Thisse B, Zon LI (2002) The zebrafish mutant gene chardonnay (cdy) encodes divalent metal transporter (DMT1). Blood 100:4655–4659

    Article  CAS  Google Scholar 

  • Dorschner MO, Phillips RB (1999) Comparative analysis of two Nramp loci from rainbow trout. DNA Cell Biol 18:573–583

    Article  CAS  Google Scholar 

  • Glover CN, Hogstrand C (2002a) In vivo characterization of intestinal zinc uptake in freshwater rainbow trout. J Exp Biol 205:141–150

    CAS  Google Scholar 

  • Glover CN, Hogstrand C (2002b) Amino acid modulation of in vivo intestinal zinc absorption in freshwater rainbow trout. J Exp Biol 205:151–158

    CAS  Google Scholar 

  • Glover CN, Hogstrand C (2003) Effects of dissolved metals and other hydrominerals on in vivo intestinal zinc uptake in freshwater rainbow trout. Aquat Toxicol 62: 81–293

    Article  Google Scholar 

  • Glover CN, Wood CM (2008) Absorption of copper and copper-histidine complexes across the apical surface of freshwater rainbow trout intestine. J Comp Physiol B 178:101–109

    Article  CAS  Google Scholar 

  • Glover CN, Bury NR, Hogstrand C (2003) Zinc uptake across the apical membrane of freshwater rainbow trout intestine is mediated by high-affinity, low-affinity and histidine-facilitated pathways. Biochim Biophys Acta 1614:211–219

    Article  CAS  Google Scholar 

  • Glover CN, Bury NR, Hogstrand C (2004) Intestinal zinc uptake in freshwater rainbow trout: evidence for apical pathways associated with potassium efflux and modified by calcium. Biochim Biophys Acta 1663:214–221

    Article  CAS  Google Scholar 

  • Gunshin H, Mackenzie B Berger UV, Gunshin Y, Romero MF, Boron WF, Nussberger S, Gollan JL, Hediger MA (1997) Cloning and characterization of a proton-coupled mammalian metal ion transporter. Nature 388:482–488

    Article  CAS  Google Scholar 

  • Handy RD, Musonda MM, Phillips K, Falla SJ (2000) Mechanisms of gastrointestinal copper absorption in the African walking catfish: copper dose-effects and a novel anion-dependent pathway in the intestine. J Exp Biol 203:2365–2377

    CAS  Google Scholar 

  • Kjoss VA, Wood CM, McDonald DG (2006) Effects of different ligands on the bioaccumulation and subsequent depuration of dietary Cu and Zn in juvenile rainbow trout (Oncorhynchus mykiss). Can J Fish Aquat Sci 63:412–422

    Article  CAS  Google Scholar 

  • Knox D, Cowey CB, Adron JW (1984) Effects of dietary zinc intake upon copper metabolism in rainbow trout (Salmo gairdneri). Aquaculture 40:199–207

    Article  CAS  Google Scholar 

  • Larsson D, Lundgren T, Sundell K (1998) Ca uptake through voltage-gated L-type Ca channels by polarized enterocytes from Atlantic Cod Gadus morhua. Membr Biol 164:229–237

    Article  CAS  Google Scholar 

  • Lee J, Marjoretta M, Pena O, Nose Y , Thiele DJ (2002) Biochemical characterization of the human copper transporter Ctr1*. J Biol Chem 277:4380–4387

    Article  CAS  Google Scholar 

  • Mackenzie NC, Brito M, Reyes AE, Allende ML (2004) Cloning, expression pattern and essentiality of the high affinity copper transporter 1 (ctr1) gene in zebrafish. Gene 328:113–120

    Article  CAS  Google Scholar 

  • Meyer JS, Adams WJ, Brix KV, Luoma SN, Mount DR, Stubblefield WA, Wood CM (2005) Toxicity of dietborne metals to aquatic organisms. SETAC Press, Pensacola, FL

    Google Scholar 

  • Nadella SR, Bucking C, Grosell M, Wood CM (2006a) Gastrointestinal assimilation of Cu during digestion of a single meal in the freshwater rainbow trout (Oncorhynchus mykiss). Comp Biochem Physiol C 143:394–401

    Google Scholar 

  • Nadella SR, Grosell M, Wood CM (2006b) Physical characterization of high-affinity gastrointestinal Cu transport in vitro in freshwater rainbow trout Oncorhynchus mykiss. J Comp Physiol 176:793–806

    CAS  Google Scholar 

  • Nadella SR, Grosell M, Wood CM (2007) Mechanisms of dietary Cu uptake in freshwater rainbow trout: evidence for Na-assisted Cu transport and a specific metal carrier in the intestine. J Comp Physiol 177:433–446

    CAS  Google Scholar 

  • Niyogi S, Wood CM (2004) Biotic Ligand Model: a flexible tool for developing site-specific water quality guidelines for metals. Environ Sci Technol 38:6177–6192

    Article  CAS  Google Scholar 

  • Ogino C, Yang G (1978) Requirement of rainbow trout for dietary zinc. Bull Jpn Soc Sci Fish 44:1015–1018

    CAS  Google Scholar 

  • Ogino C, Yang G (1979) Requirement of rainbow trout for dietary copper. Bull Jpn Soc Sci Fish 45:967–969

    CAS  Google Scholar 

  • Ojo AA, Wood CM (2007) In vitro analysis of the bioavailability of six metals via the gastro-intestinal tract of the rainbow trout (Oncorhynchus mykiss). Aquat Toxicol 80:10–23

    Article  Google Scholar 

  • Ojo AA, Wood CM (2008) In vitro characterization of cadmium and zinc uptake via the gastro-intestinal tract of the rainbow trout (Oncorhynchus mykiss): interactive effects and the influence of calcium. Aquat Toxicol (in press)

  • Paquin PR, Gorsuch JW, Apte S, Batley GE, Bowles KC, Campbell PGC, Delos CG, Di Toro DM, Dwyer RL, Galvez F, Gensemer RW, Goss GG, Hogstrand C, Janssen CR, McGeer JM, Naddy RB, Playle RC, Santore RC, Schneider U, Stubblefield WA, Wood CM, Wu KB (2002) The biotic ligand model: a historical overview. Comp Biochem Physiol 133C:3–35

    CAS  Google Scholar 

  • Qiu AD, Hogstrand C (2004) Functional characterisation and genomic analysis of an epithelial calcium channel (ECaC) from pufferfish, Fugu rubripes. Gene 342:113–123

    Article  CAS  Google Scholar 

  • Qiu AD, Shayeghi M, Hogstrand C (2004) Molecular cloning and functional characterization of a high affinity zinc importer (DrZIP1) from zebrafish (Danio rerio). Biochem J 388:745–754

    Google Scholar 

  • Reiley MC (2007) Science, policy, and trends of metals risk assessment at EPA: How understanding metals bioavailability has changed metals risk assessment at US EPA. Aquat Toxicol 84:292–298

    Article  CAS  Google Scholar 

  • Shahsavarani A, McNeill B, Galvez F, Wood CM, Goss GG, Hwang PP, Perry SF (2006) Characterization of a branchial epithelial calcium channel (ECaC) in freshwater rainbow trout (Oncorhynchus mykiss). J Exp Biol 209:1928–1943

    Article  CAS  Google Scholar 

  • Shears MA, Fletcher GL (1983) Regulation of Zn2+ uptake from the gastrointestinal tract of a marine teleost, the winter flounder (Pseudopleuronectes americanus). Can J Fish Aquat Sci 40:197–205

    Google Scholar 

  • Wolf K (1963) Physiological salines for freshwater teleosts. Progr Fish Cult 25:135–140

    Article  CAS  Google Scholar 

  • Wood CM, Franklin N, Niyogi S (2006) The protective role of dietary calcium against cadmium uptake and toxicity in freshwater fish: an important role for the stomach. Environ Chem 3:389–394

    Article  CAS  Google Scholar 

Download references

Acknowledgments

This work was supported by the Natural Sciences and Engineering Research Council of Canada CRD Program, the International Lead Zinc Research Organization, the International Zinc Association, the Nickel Producers Environmental Research Association, the International Copper Association, the Copper Development Association, Teck-Cominco, Xstrata (Noranda-Falconbridge), and Vale Inco. C.M.W. is supported by the Canada Research Chair Program. We thank Dr. Chris Glover, Dr. Peter Chapman, and two anonymous referees for constructive advice and comments on the manuscript.

Author information

Author notes

  1. Adeola A. Ojo

    Present address: , P.O. Box 470, Ilesha, Osun State, Nigeria

Authors and Affiliations

  1. Department of Biology, McMaster University, 1280 Main Street West, Hamilton, ON, Canada, L8S 4K1

    Adeola A. Ojo, Sunita Rao Nadella & Chris M. Wood

Authors
  1. Adeola A. Ojo
    View author publications

    You can also search for this author in PubMed Google Scholar

  2. Sunita Rao Nadella
    View author publications

    You can also search for this author in PubMed Google Scholar

  3. Chris M. Wood
    View author publications

    You can also search for this author in PubMed Google Scholar

Corresponding author

Correspondence to Chris M. Wood.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Ojo, A.A., Nadella, S.R. & Wood, C.M. In Vitro Examination of Interactions Between Copper and Zinc Uptake via the Gastrointestinal Tract of the Rainbow Trout (Oncorhynchus mykiss). Arch Environ Contam Toxicol 56, 244–252 (2009). https://doi.org/10.1007/s00244-008-9190-x

Download citation

  • Received:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00244-008-9190-x

Keywords

Search

Navigation