Characterization of branchial lead-calcium interaction in the freshwater rainbow trout Oncorhynchus mykiss

Joseph T. Rogers, Chris M. Wood

Research output: Contribution to journalArticle

92 Citations (Scopus)

Abstract

The mechanism of branchial lead uptake and interplay with Ca2+ transport was investigated in the freshwater rainbow trout Oncorhynchus mykiss. Lead significantly reduced Ca2+ influx by approximately 40% and 30% after exposure to 2.3±0.1 and 1.4±0.2 μmol l-1 dissolved lead, respectively, for 0-48 h. Acute inhibition of Ca2+ influx by lead exhibited typical Michaelis-Menten kinetics with an approximate 16-fold increase in Km, whereas Jmax values did not significantly change, yielding an inhibitor constant (Ki,Pb) of 0.48 μmol l-1. Alternative analyses suggest the possibility of a mixed competitive/non-competitive interaction at the highest lead concentration tested (4.8 μmol l-1). Branchial lead accumulation was reduced with increasing waterborne Ca2+ concentrations, suggesting a protective effect of Ca2+ against lead uptake at the gill. The apical entries of Ca2+ and lead were both inhibited (55% and 77%, respectively) by the addition of lanthanum (1 μmol l-1) to the exposure water. The use of cadmium (1 μmol l-1) and zinc (100 μmol l-1) as voltage-independent calcium channel competitors also reduced branchial lead uptake by approximately 56% and 47%, respectively. Nifedipine and verapamil (up to 100 μmol l-1), both voltage-dependent calcium channel blockers, had no effect on gill lead accumulation. CaCl2 injection reduced both Ca2+ and lead uptake by the gills. This suggests transport of lead through apical voltage-independent calcium channels, similar to the entry of Ca2+. High-affinity Ca2+-ATPase activity was not acutely affected by lead, but a significant 80% reduction in activity occurred during exposure for 96 h to 5.5±0.4 μmol l-1 dissolved lead, indicating a possible non-competitive component to lead-induced Ca2+ disruption. The effect of lead on Ca2+ efflux was investigated and found to be insignificant. We conclude that uptake of lead occurs, at least in part, by the same mechanism as Ca2+, which results in disruption of Ca 2+ influx and ultimately Ca2+ homeostasis.

Original languageEnglish
Pages (from-to)813-825
Number of pages13
JournalJournal of Experimental Biology
Volume207
Issue number5
DOIs
StatePublished - Feb 1 2004

Fingerprint

Oncorhynchus mykiss
Fresh Water
rainbow
calcium
Calcium
uptake mechanisms
Calcium Channels
gills
calcium channels
Lead
calcium channel blockers
Lanthanum
lanthanum
enzyme kinetics
verapamil
Ca2-transporting ATPase
Calcium-Transporting ATPases
Calcium Channel Blockers
homeostasis
Nifedipine

Keywords

  • Branchial uptake
  • Calcium
  • Competition
  • Oncorhynchus mykiss
  • Rainbow trout
  • Waterborne lead

ASJC Scopus subject areas

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

Cite this

Characterization of branchial lead-calcium interaction in the freshwater rainbow trout Oncorhynchus mykiss. / Rogers, Joseph T.; Wood, Chris M.

In: Journal of Experimental Biology, Vol. 207, No. 5, 01.02.2004, p. 813-825.

Research output: Contribution to journalArticle

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N2 - The mechanism of branchial lead uptake and interplay with Ca2+ transport was investigated in the freshwater rainbow trout Oncorhynchus mykiss. Lead significantly reduced Ca2+ influx by approximately 40% and 30% after exposure to 2.3±0.1 and 1.4±0.2 μmol l-1 dissolved lead, respectively, for 0-48 h. Acute inhibition of Ca2+ influx by lead exhibited typical Michaelis-Menten kinetics with an approximate 16-fold increase in Km, whereas Jmax values did not significantly change, yielding an inhibitor constant (Ki,Pb) of 0.48 μmol l-1. Alternative analyses suggest the possibility of a mixed competitive/non-competitive interaction at the highest lead concentration tested (4.8 μmol l-1). Branchial lead accumulation was reduced with increasing waterborne Ca2+ concentrations, suggesting a protective effect of Ca2+ against lead uptake at the gill. The apical entries of Ca2+ and lead were both inhibited (55% and 77%, respectively) by the addition of lanthanum (1 μmol l-1) to the exposure water. The use of cadmium (1 μmol l-1) and zinc (100 μmol l-1) as voltage-independent calcium channel competitors also reduced branchial lead uptake by approximately 56% and 47%, respectively. Nifedipine and verapamil (up to 100 μmol l-1), both voltage-dependent calcium channel blockers, had no effect on gill lead accumulation. CaCl2 injection reduced both Ca2+ and lead uptake by the gills. This suggests transport of lead through apical voltage-independent calcium channels, similar to the entry of Ca2+. High-affinity Ca2+-ATPase activity was not acutely affected by lead, but a significant 80% reduction in activity occurred during exposure for 96 h to 5.5±0.4 μmol l-1 dissolved lead, indicating a possible non-competitive component to lead-induced Ca2+ disruption. The effect of lead on Ca2+ efflux was investigated and found to be insignificant. We conclude that uptake of lead occurs, at least in part, by the same mechanism as Ca2+, which results in disruption of Ca 2+ influx and ultimately Ca2+ homeostasis.

AB - The mechanism of branchial lead uptake and interplay with Ca2+ transport was investigated in the freshwater rainbow trout Oncorhynchus mykiss. Lead significantly reduced Ca2+ influx by approximately 40% and 30% after exposure to 2.3±0.1 and 1.4±0.2 μmol l-1 dissolved lead, respectively, for 0-48 h. Acute inhibition of Ca2+ influx by lead exhibited typical Michaelis-Menten kinetics with an approximate 16-fold increase in Km, whereas Jmax values did not significantly change, yielding an inhibitor constant (Ki,Pb) of 0.48 μmol l-1. Alternative analyses suggest the possibility of a mixed competitive/non-competitive interaction at the highest lead concentration tested (4.8 μmol l-1). Branchial lead accumulation was reduced with increasing waterborne Ca2+ concentrations, suggesting a protective effect of Ca2+ against lead uptake at the gill. The apical entries of Ca2+ and lead were both inhibited (55% and 77%, respectively) by the addition of lanthanum (1 μmol l-1) to the exposure water. The use of cadmium (1 μmol l-1) and zinc (100 μmol l-1) as voltage-independent calcium channel competitors also reduced branchial lead uptake by approximately 56% and 47%, respectively. Nifedipine and verapamil (up to 100 μmol l-1), both voltage-dependent calcium channel blockers, had no effect on gill lead accumulation. CaCl2 injection reduced both Ca2+ and lead uptake by the gills. This suggests transport of lead through apical voltage-independent calcium channels, similar to the entry of Ca2+. High-affinity Ca2+-ATPase activity was not acutely affected by lead, but a significant 80% reduction in activity occurred during exposure for 96 h to 5.5±0.4 μmol l-1 dissolved lead, indicating a possible non-competitive component to lead-induced Ca2+ disruption. The effect of lead on Ca2+ efflux was investigated and found to be insignificant. We conclude that uptake of lead occurs, at least in part, by the same mechanism as Ca2+, which results in disruption of Ca 2+ influx and ultimately Ca2+ homeostasis.

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