Protein synthesis costs could account for the tissue specific effects of sub-lethal copper on protein synthesis in rainbow trout (Oncorhynchus mykiss)

R. W. Smith, Susan Corral Blaney, K. Dowling, A. Sturm, M. Jonsson, Dominic Francis Joseph Houlihan

Research output: Contribution to journalArticle

28 Citations (Scopus)

Abstract

This study investigates protein synthesis, following exposure to sub-lethal Cu, in rainbow trout in vivo and in vitro. The investigation has two aims: to determine if perturbations in protein synthesis, compared with other physiological changes, are a biomarker of Cu pollution and to evaluate the most productive role of cellular models in ecotoxicology. Protein synthesis rates were measured by labelling with H-3-phenylalanine. In vivo this was applied by a single (i.p.) injection and in vitro by bathing the cells in H-3-phenylalanine labelled culture media. The effects in vivo were tissue specific. After 3 weeks' exposure to 0.7 muM Cu only skin protein synthesis was reduced. Gills and liver from the same fish were unaffected. This reduction in skin protein synthesis appears to be more sensitive than some other biomarkers reported in the literature. However, Cu concentrations greater by orders of magnitude were required to reproduce this reduction in protein synthesis in skin cell explants (200 and 400 muM). Hepatocyte protein synthesis was unaffected by 10, 20 and 40 muM Cu and a separate investigation has also shown that 25 and 75 muM Cu does not effect protein synthesis in cultured gill cells. Oxygen consumption rates were also measured in vitro by monitoring the decline in O-2 partial pressure. The Cu concentrations given above resulted in a decline in O-2 consumption rates in the respective cell types. By measuring protein synthesis and O-2 consumption after treatment with a protein synthesis inhibitor (cycloheximide), the costs of protein synthesis were also determined. Synthesis costs in hepatocytes are close to the theoretical minimum and are only marginally affected by Cu. Gill cell synthesis costs are also minimal and are unaffected. In skin explants, the reduction in protein synthesis was accompanied by greatly increased synthesis costs. This in vitro result offers a hypothesis as to the tissue-specific effects in vivo; i.e. the energetic demand of protein synthesis may determine tissue sensitivity or susceptibility. Cell or tissue types with high protein synthesis rates are able to avoid detrimental increases in the synthesis cost when exposed to Cu. In tissues with a low protein synthesis rate any further reduction is more likely to incur a potentially damaging increase in protein synthesis costs. Thus, whilst in vitro models may have little practical use in environmental monitoring, they may be best used as a mechanistic tool in understanding susceptibility or tolerance to sub-lethal Cu. (C) 2001 Elsevier Science B.V. All rights reserved.

Original languageEnglish
Pages (from-to)265-277
Number of pages12
JournalAquatic Toxicology
Volume53
Issue number3-4
DOIs
Publication statusPublished - 2001

Keywords

  • sub-lethal Cu
  • protein synthesis rate
  • tissue specificity
  • oxygen consumption
  • protein synthesis costs
  • NUCLEIC-ACID CONTENT
  • CULTURED FISH CELLS
  • GROWTH-RATES
  • INVITRO CYTOTOXICITY
  • OXYGEN-CONSUMPTION
  • ENERGY-METABOLISM
  • CYPRINUS-CARPIO
  • SALMO-GAIRDNERI
  • COMMON CARP
  • WHOLE-BODY

Cite this

Protein synthesis costs could account for the tissue specific effects of sub-lethal copper on protein synthesis in rainbow trout (Oncorhynchus mykiss). / Smith, R. W.; Blaney, Susan Corral; Dowling, K.; Sturm, A.; Jonsson, M.; Houlihan, Dominic Francis Joseph.

In: Aquatic Toxicology, Vol. 53, No. 3-4, 2001, p. 265-277.

Research output: Contribution to journalArticle

Smith, R. W. ; Blaney, Susan Corral ; Dowling, K. ; Sturm, A. ; Jonsson, M. ; Houlihan, Dominic Francis Joseph. / Protein synthesis costs could account for the tissue specific effects of sub-lethal copper on protein synthesis in rainbow trout (Oncorhynchus mykiss). In: Aquatic Toxicology. 2001 ; Vol. 53, No. 3-4. pp. 265-277.
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AU - Houlihan, Dominic Francis Joseph

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N2 - This study investigates protein synthesis, following exposure to sub-lethal Cu, in rainbow trout in vivo and in vitro. The investigation has two aims: to determine if perturbations in protein synthesis, compared with other physiological changes, are a biomarker of Cu pollution and to evaluate the most productive role of cellular models in ecotoxicology. Protein synthesis rates were measured by labelling with H-3-phenylalanine. In vivo this was applied by a single (i.p.) injection and in vitro by bathing the cells in H-3-phenylalanine labelled culture media. The effects in vivo were tissue specific. After 3 weeks' exposure to 0.7 muM Cu only skin protein synthesis was reduced. Gills and liver from the same fish were unaffected. This reduction in skin protein synthesis appears to be more sensitive than some other biomarkers reported in the literature. However, Cu concentrations greater by orders of magnitude were required to reproduce this reduction in protein synthesis in skin cell explants (200 and 400 muM). Hepatocyte protein synthesis was unaffected by 10, 20 and 40 muM Cu and a separate investigation has also shown that 25 and 75 muM Cu does not effect protein synthesis in cultured gill cells. Oxygen consumption rates were also measured in vitro by monitoring the decline in O-2 partial pressure. The Cu concentrations given above resulted in a decline in O-2 consumption rates in the respective cell types. By measuring protein synthesis and O-2 consumption after treatment with a protein synthesis inhibitor (cycloheximide), the costs of protein synthesis were also determined. Synthesis costs in hepatocytes are close to the theoretical minimum and are only marginally affected by Cu. Gill cell synthesis costs are also minimal and are unaffected. In skin explants, the reduction in protein synthesis was accompanied by greatly increased synthesis costs. This in vitro result offers a hypothesis as to the tissue-specific effects in vivo; i.e. the energetic demand of protein synthesis may determine tissue sensitivity or susceptibility. Cell or tissue types with high protein synthesis rates are able to avoid detrimental increases in the synthesis cost when exposed to Cu. In tissues with a low protein synthesis rate any further reduction is more likely to incur a potentially damaging increase in protein synthesis costs. Thus, whilst in vitro models may have little practical use in environmental monitoring, they may be best used as a mechanistic tool in understanding susceptibility or tolerance to sub-lethal Cu. (C) 2001 Elsevier Science B.V. All rights reserved.

AB - This study investigates protein synthesis, following exposure to sub-lethal Cu, in rainbow trout in vivo and in vitro. The investigation has two aims: to determine if perturbations in protein synthesis, compared with other physiological changes, are a biomarker of Cu pollution and to evaluate the most productive role of cellular models in ecotoxicology. Protein synthesis rates were measured by labelling with H-3-phenylalanine. In vivo this was applied by a single (i.p.) injection and in vitro by bathing the cells in H-3-phenylalanine labelled culture media. The effects in vivo were tissue specific. After 3 weeks' exposure to 0.7 muM Cu only skin protein synthesis was reduced. Gills and liver from the same fish were unaffected. This reduction in skin protein synthesis appears to be more sensitive than some other biomarkers reported in the literature. However, Cu concentrations greater by orders of magnitude were required to reproduce this reduction in protein synthesis in skin cell explants (200 and 400 muM). Hepatocyte protein synthesis was unaffected by 10, 20 and 40 muM Cu and a separate investigation has also shown that 25 and 75 muM Cu does not effect protein synthesis in cultured gill cells. Oxygen consumption rates were also measured in vitro by monitoring the decline in O-2 partial pressure. The Cu concentrations given above resulted in a decline in O-2 consumption rates in the respective cell types. By measuring protein synthesis and O-2 consumption after treatment with a protein synthesis inhibitor (cycloheximide), the costs of protein synthesis were also determined. Synthesis costs in hepatocytes are close to the theoretical minimum and are only marginally affected by Cu. Gill cell synthesis costs are also minimal and are unaffected. In skin explants, the reduction in protein synthesis was accompanied by greatly increased synthesis costs. This in vitro result offers a hypothesis as to the tissue-specific effects in vivo; i.e. the energetic demand of protein synthesis may determine tissue sensitivity or susceptibility. Cell or tissue types with high protein synthesis rates are able to avoid detrimental increases in the synthesis cost when exposed to Cu. In tissues with a low protein synthesis rate any further reduction is more likely to incur a potentially damaging increase in protein synthesis costs. Thus, whilst in vitro models may have little practical use in environmental monitoring, they may be best used as a mechanistic tool in understanding susceptibility or tolerance to sub-lethal Cu. (C) 2001 Elsevier Science B.V. All rights reserved.

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KW - tissue specificity

KW - oxygen consumption

KW - protein synthesis costs

KW - NUCLEIC-ACID CONTENT

KW - CULTURED FISH CELLS

KW - GROWTH-RATES

KW - INVITRO CYTOTOXICITY

KW - OXYGEN-CONSUMPTION

KW - ENERGY-METABOLISM

KW - CYPRINUS-CARPIO

KW - SALMO-GAIRDNERI

KW - COMMON CARP

KW - WHOLE-BODY

U2 - 10.1016/S0166-445X(01)00171-0

DO - 10.1016/S0166-445X(01)00171-0

M3 - Article

VL - 53

SP - 265

EP - 277

JO - Aquatic Toxicology

JF - Aquatic Toxicology

SN - 0166-445X

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ER -