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Dietary exposure to ochratoxin A reduces growth performance and impairs hepatic purinergic signaling in tambaqui (Colossoma macropomum)

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Abstract

The practice of replacing costly animal-derived proteins with more economical plant proteins has augmented the risk of mycotoxin contamination in fish feeds, including contamination with ochratoxin A (OTA). OTA is a secondary metabolite produced by molds commonly found in fish feeds that causes impairment of performance in several fish species and some hepatic biochemical alterations. However, the pathways involved in hepatic damage remain unknown and are limited to histopathological alterations. Purinergic signaling is a homeostatic system that continuously monitors the internal environment to detect injury primarily by two intercellular messengers: adenosine triphosphate (ATP) and adenosine (Ado). The objective of this study was to determine whether OTA-contaminated feed induces the release of nucleotides in the extracellular milieu, as well as whether ectoenzymes modulate ATP pro-inflammatory effects in liver of tambaqui (Colossoma macropomum). Final mean weight, weight gain (WG), and liver weight were significantly lower in tambaqui fed feeds containing 1.6 and 2.4 mg OTA/kg feed than in the control group. Liver ATP and Ado levels were significantly higher in tambaqui fed feeds containing 1.6 and 2.4 mg OTA/kg feed compared with control, while no significant difference was observed regarding adenosine diphosphate and adenosine monophosphate levels. Hepatic triphosphate diphosphohydrolase (NTPDase) activity (for ATP) was significantly greater in tambaqui fed feeds containing 1.6 and 2.4 mg OTA/kg feed compared with control, while adenosine deaminase (ADA) activity was lower. No significant difference was observed with respect to hepatic NTPDase activity (for ADP) or for 5′-nucleotidase activity. Finally, levels of liver metabolites of nitric oxide were significantly higher in tambaqui fed feeds containing 1.6 and 2.4 mg OTA/kg feed than in the control group. Based on these data, exposure to 1.6 and 2.4 mg OTA/kg feed impaired tambaqui growth performance associated with final mean weight and WG. Levels of two important intercellular messengers, ATP and Ado, increased in the extracellular space as a consequence of hepatic damage, exerting opposite immune responses. Finally, liver NTPDase and ADA activities were altered to modulate ATP and Ado levels, respectively, exerting anti-inflammatory effects to counteract OTA-induced hepatic injury.

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Authors and Affiliations

  1. Department of Physiology and Pharmacology, Universidade Federal de Santa Maria, Santa Maria, Rio Grande do Sul, Brazil

    Matheus D. Baldissera, Carine F. Souza & Bernardo Baldisserotto

  2. LEEM—Laboratory of Ecophysiology and Molecular Evolution, Brazilian National Institute for Research of the Amazon, Manaus, Amazonas, Brazil

    Jefferson A. da Silva, Danilo C. Barroso & Adalberto L. Val

  3. Laboratório de Micologia, Universidade de São Paulo, São Paulo, SP, Brazil

    Eduardo M. Glória

Authors
  1. Matheus D. Baldissera
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  2. Carine F. Souza
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  3. Jefferson A. da Silva
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  4. Danilo C. Barroso
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  5. Eduardo M. Glória
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  6. Bernardo Baldisserotto
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  7. Adalberto L. Val
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Correspondence to Matheus D. Baldissera.

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This experiment was approved by the Ethics Committee of Brazilian National Institute for Research of the Amazon under protocol number 004/2018.

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Baldissera, M.D., Souza, C.F., da Silva, J.A. et al. Dietary exposure to ochratoxin A reduces growth performance and impairs hepatic purinergic signaling in tambaqui (Colossoma macropomum). Fish Physiol Biochem 46, 2055–2064 (2020). https://doi.org/10.1007/s10695-020-00854-0

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