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Acute hypoxia up-regulates HIF-1α and VEGF mRNA levels in Amazon hypoxia-tolerant Oscar (Astronotus ocellatus)

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Abstract

Amazon fish maintain oxygen uptake through a variety of strategies considered evolutionary and adaptive responses to the low water oxygen saturation, commonly found in Amazon waters. Oscar (Astronotus ocellatus) is among the most hypoxia-tolerant fish in Amazon, considering its intriguing anaerobic capacity and ability to depress oxidative metabolism. Previous studies in hypoxia-tolerant and non-tolerant fish have shown that hypoxia-inducible factor-1α (HIF-1α) gene expression is positively regulated during low oxygen exposure, affecting vascular endothelial growth factor (VEGF) transcription and fish development or tolerance in different manners. However, whether similar isoforms exists in tolerant Amazon fish and whether they are affected similarly to others physiological responses to improve hypoxia tolerance remain unknown. Here we evaluate the hepatic HIF-1α and VEGF mRNA levels after 3 h of acute hypoxia exposure (0.5 mgO2/l) and 3 h of post-hypoxia recovery. Additionally, hematological parameters and oxidative enzyme activities of citrate synthase (CS) and malate dehydrogenase (MDH) were analyzed in muscle and liver tissues. Overall, three sets of responses were detected: (1) as expected, hematocrit, hemoglobin concentration, red blood cells, and blood glucose increased, improving oxygen carrying capacity and glycolysis potential; (2) oxidative enzymes from liver decreased, corroborating the tendency to a widespread metabolic suppression; and (3) HIF-1α and VEGF increased mRNA levels in liver, revealing their role in the oxygen homeostasis through, respectively, activation of target genes and vascularization. This is the first study to investigate a hypoxia-related transcription factor in a representative Amazon hypoxia-tolerant fish and suggests that HIF-1α and VEGF mRNA regulation have an important role in enhancing hypoxia tolerance in extreme tolerant species.

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Acknowledgments

The authors are grateful to Nazare Paula da Silva, for all logistical support, to the fishermen “China” and Luís, by catching the specimens of Oscar in the field, and to Chris Wood and Gillian Renshaw, for their comments on early versions of this manuscript.

Grants

This work was supported by the Brazilian National Research Council (CNPq), the Amazon State Research Foundation (FAPEAM) and INCT ADAPTA joint grant (CNPq/FAPEAM) to ALV. ALV and VMFAV are the recipients of CNPq research fellowships. RBB was the recipient of a MSc. Fellowship from CAPES.

Author contributions

R.B.B and V.M.F.A.V. were involved in conception and design of research; R.B.B. performed experiments; R.B.B. and N.S.C. interpreted result of experiments; R.B.B and N.S.C. prepared figures; R.B.B drafted the manuscript; A.L.V and V.M.F.A.V. edited and revised manuscript; A.L.V and V.M.F.A.V. approved final version of manuscript.

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  1. Laboratory of Ecophysiology and Molecular Evolution, National Institute for Amazon Research, 1756 Aleixo, Manaus, AM, Brazil

    R. B. Baptista, N. Souza-Castro & V. M. F. Almeida-Val

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  1. R. B. Baptista
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  2. N. Souza-Castro
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  3. V. M. F. Almeida-Val
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Correspondence to R. B. Baptista.

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Baptista, R.B., Souza-Castro, N. & Almeida-Val, V.M.F. Acute hypoxia up-regulates HIF-1α and VEGF mRNA levels in Amazon hypoxia-tolerant Oscar (Astronotus ocellatus). Fish Physiol Biochem 42, 1307–1318 (2016). https://doi.org/10.1007/s10695-016-0219-1

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