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Effects of acute hypoxia and reoxygenation on oxygen sensors, respiratory metabolism, oxidative stress, and apoptosis in hybrid yellow catfish “Huangyou-1”

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Abstract

The regulation mechanism of the hybrid yellow catfish “Huangyou-1” was assessed under conditions of hypoxia and reoxygenation by examination of oxygen sensors and by monitoring respiratory metabolism, oxidative stress, and apoptosis. The expressions of genes related to oxygen sensors (HIF-1α, HIF-2α, VHL, HIF-1β, PHD2, and FIH-1) were upregulated in the brain and liver during hypoxia, and recovered compared with control upon reoxygenation. The expressions of genes related to glycolysis (HK1, PGK1, PGAM2, PFK, and LDH) were increased during hypoxia and then recovered compared with control upon reoxygenation. The mRNA levels of CS did not change during hypoxia in the brain and liver, but increased during reoxygenation. The mRNA levels of SDH decreased significantly only in the liver during hypoxia, but later increased compared with control upon reoxygenation in both tissues. Under hypoxic conditions, the expressions of genes related to oxidative stress (SOD1, SOD2, GSH-Px, and CAT) and the activity of antioxidant enzymes (SOD, CAT, and GSH-Px) and MDA were upregulated compared with control. The expressions of genes related to apoptosis (Apaf-1, Bax, Caspase 3, Caspase 9, and p53) were higher than those in control during hypoxic exposure, while the expressions of Bcl-2 and Cyt C were decreased. The findings of the transcriptional analyses will provide insights into the molecular mechanisms of hybrid yellow catfish “Huangyou-1” under conditions of hypoxia and reoxygenation. Overall, these findings showed that oxygen sensors of “Huangyou-1” are potentially useful biomarkers of environmental hypoxic exposure. Together with genes related to respiratory metabolism, oxidative stress and apoptosis occupy a quite high position in enhancing hypoxia tolerance. Our findings provided new insights into the molecular regulatory mechanism of hypoxia in “Huangyou-1.”

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Data availability

All datasets for this study are included in the manuscript/supplementary files.

Abbreviations

HIF-1α:

Hypoxia-inducible factor-1α

EPO:

Erythropoietin gene

HIF-2α:

Hypoxia-inducible factor-2α

HIF-1β:

Hypoxia-inducible factor-1β

Vhl:

Von Hippel-Lindau tumor suppressor

FIH-1:

HIF-1 asparaginyl hydroxylase 1

PHD2:

Proline hydroxylase 2

HK1:

Hexokinase 1

PFK:

Phosphofructokinase

PGK1:

Phosphoglycerate kinase 1

PGAM2:

Phosphoglycerate mutase 2

LDH:

Actate dehydrogenase

CS:

Citrate synthase

SDH:

Succinate dehydrogenase

SOD1:

Cu/Zn SOD

SOD2:

Mn-SOD

CAT:

Catalase

GSH-Px:

Glutathione peroxidase

Cyt C:

Cytochrome c

Bcl-2:

B-cell lymphoma-2

Bax:

Bcl-2-associated x

Apaf-1:

Apoptotic protease activating factor 1

C-TAD:

C-terminal transactivation domain

GLUT1:

Glucose transporter 1

ROS:

Reactive oxygen species

bp:

Base pair

mRNA:

Messenger ribonucleic acid

cDNA:

Complementary DNA

kDa:

Kilo-Dalton

ANOVA:

Analysis of variance

SDS-PAGE:

SDS–polyacrylamide gel electrophoresis

SD:

Standard deviation

RACE:

Amplification of cDNA end

References

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Funding

This study was supported by the Jiangsu Agriculture Science and Technology Innovation Fund [CX(19)2034], the Creation Project of Major New Species of Agriculture in Jiangsu Province (PZCZ201742), the Key Research and Development Program of Jiangsu Province (BE2017377).

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Authors and Affiliations

Authors

Contributions

YS, WT, MJ, and PX co-conceived this study, and supervised the experiments. PX and ZH performed the experiments. ZXY, ZX, and LJ conducted the data analysis and created the figures and tables. PX and CM wrote the manuscript. PX, CM, and TP contributed to the manuscript revision and read and approved the submitted version.

Corresponding authors

Correspondence to Jie Mei, Tao Wang or Shaowu Yin.

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Ethical approval

All experiments were performed in accordance with the Guidelines for the Care and Use of Laboratory Animals in China. This study was also approved by the Ethics Committee of Experimental Animals at Nanjing Normal University (grant No. SYXK 2015–0028, Jiangsu).

Conflict of interest

The authors declare competing interests.

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Pei, X., Chu, M., Tang, P. et al. Effects of acute hypoxia and reoxygenation on oxygen sensors, respiratory metabolism, oxidative stress, and apoptosis in hybrid yellow catfish “Huangyou-1”. Fish Physiol Biochem 47, 1429–1448 (2021). https://doi.org/10.1007/s10695-021-00989-8

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  • DOI: https://doi.org/10.1007/s10695-021-00989-8

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