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Effects of β-glucan on ROS production and energy metabolism in yellow croaker (Pseudosciaena crocea) under acute hypoxic stress

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Abstract

The aim of the present study was to evaluate the effect of β-glucan on acute hypoxia-induced oxidative stress and the changes in energy metabolism by determining ROS production, activities and mRNA levels of energy metabolism enzyme (PK, F-ATPase, SDH and MDH), and in gene expression of HIF-1α in the liver of large yellow croaker. Fish were injected with β-glucan at a dose of 0 or 5 mg kg−1 body weight on 6, 4 and 2 days before exposed to 1.5 and 7.0 mg DO L−1 for 48 h. The results showed that β-glucan enhanced survival rate and reduced ROS during the lethal hypoxic stress, indicating that β-glucan could ameliorate hypoxia-induced oxidative stress. Obtained results also showed that β-glucan could up-regulate activities and mRNA levels of PK, demonstrating that β-glucan increased anaerobic glycolysis capacity. Furthermore, a coordinated transcriptional regulation of energy metabolism enzyme genes was observed, suggesting that HIF-1α is required for regulating these genes. In conclusion, β-glucan could alleviate cute hypoxia-induced oxidative stress in large yellow croker by enhancing anaerobic glycolysis capacity, emphasizing a central role of transcription factor HIF-1α in the process.

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Abbreviations

ROS:

Reactive oxygen species

HIF-1α:

Hypoxia-inducible factor-1α

PK:

Pyruvate kinase

F-ATPase:

Mitochondrial ATP synthase

SDH:

Succinate dehydrogenase

MDH:

Malate dehydrogenase

PBS:

Phosphate-buffered saline

DO:

Dissolved oxygen

References

  • Ao J, Mu Y, Xiang LX, Fan D, Feng M, Zhang S, Shi Q, Zhu LY, Li T, Ding Y, Nie L, Li QH, Dong WR, Jiang L, Sun B, Zhang XH, Li MY, Zhang HQ, Xie SB, Zhu YB, Jiang XT, Wang XH, Mu PF, Chen W, Yue Z, Wang Z, Wang J, Shao JZ (2015) Genome sequencing of the perciform fish Larimichthys crocea provides insights into molecular and genetic mechanisms of stress adaptation. PLoS Genet 11:e1005118

    Article  PubMed  PubMed Central  Google Scholar 

  • Bárdos JI, Ashcroft M (2005) Negative and positive regulation of HIF-1: a complex network. BBA-Rev Cancer 1755:107–120

    Google Scholar 

  • Barros MM, Falcon DR, de Oliveira Orsi R, Pezzato LE, Fernandes AC, Guimarães IG, Fernandes A Jr, Padovania CR, Sartori MMP (2014) Non-specific immune parameters and physiological response of Nile tilapia fed β-glucan and vitamin C for different periods and submitted to stress and bacterial challenge. Fish Shellfish Immunol 39:188–195

    Article  CAS  PubMed  Google Scholar 

  • Bower CE, Holm-Hansen T (1980) A salicylate-hypochlorite method for determining ammonia in seawater. Can J Fish Aquat Sci 37:794–798

    Article  CAS  Google Scholar 

  • Bradford MM (1976) A rapid and sensitive method for the quantitation of microgram quantities of protein utilizing the principle of protein-dye binding. Anal Biochem 72:248–254

    Article  CAS  PubMed  Google Scholar 

  • Burt K, Hamoutene D, Mabrouk G, Lang C, Puestow T, Drover D, Losier R, Page F (2012) Environmental conditions and occurrence of hypoxia within production cages of Atlantic salmon on the south coast of Newfoundland. Aquac Res 43:607–620

    Article  CAS  Google Scholar 

  • Carvan MJ III, Di Giulio RT (2015) Oxidative stress responses in aquatic and marine fishes. In: Stephen MR, James PK, Lars-Oliver K (eds) Studies on experimental toxicology and pharmacology. Springer, New York, pp 481–493

  • Cheng SC, Quintin J, Cramer RA, Shepardson KM, Saeed S, Kumar V, Giamarellos-Bourboulis EJ, Martens JHA, Rao NA, Aghajanirefah A, Manjeri GR, Li Y, Ifrim DC, Arts RJW, van der Veer BMJW, Deen PMT, Logie C, O’Neill LA, Willems P, van de Veerdonk FL, van der Meer JWM, Ng A, Joosten LAB, Wijmenga C, Stunnenberg HG, Xavier RJ, Netea MG (2014) mTOR-and HIF-1α–mediated aerobic glycolysis as metabolic basis for trained immunity. Science 345:1250684

    Article  PubMed  PubMed Central  Google Scholar 

  • Chippari-Gomes AR, Gomes LC, Lopes NP, Val AL, Almeida-Val VMF (2005) Metabolic adjustments in two Amazonian cichlids exposed to hypoxia and anoxia. Comp Biochem Phys B 141:347–355

    Article  CAS  Google Scholar 

  • Dawood MAO, Koshio S, Ishikawa M, Yokoyama S, El Basuini MF, Hossain MS, Nhu TH, Moss AS, Dossou S, Wei H (2015) Dietary supplementation of β-glucan improves growth performance, the innate immune response and stress resistance of red sea bream, Pagrus major. Aquac Nutr. doi:10.1111/anu.12376

  • Drotar A, Phelps P, Fall R (1985) Evidence for glutathione peroxidase activities in cultured plant cells. Plant Sci 42:35–40

    Article  CAS  Google Scholar 

  • Farombi EO, Adelowo OA, Ajimoko YR (2007) Biomarkers of oxidative stress and heavy metal levels as indicators of environmental pollution in African cat fish (Clarias gariepinus) from Nigeria Ogun River. Inter J Env Res Public Health 4:158–165

    Article  CAS  Google Scholar 

  • Foster GD, Moon TW (1986) Enzyme activities in the Atlantic hagfish, Myxine glutinosa: changes with captivity and food deprivation. Can J Zool 64:1080–1085

    Article  CAS  Google Scholar 

  • Froehlich HE, Roberts SB, Essington TE (2015) Evaluating hypoxia-inducible factor-1α mRNA expression in a pelagic fish, Pacific herring Clupea pallasii, as a biomarker for hypoxia exposure. Comp Biochem Phys A 189:58–66

    Article  CAS  Google Scholar 

  • Gracey AY, Troll JV, Somero GN (2001) Hypoxia-induced gene expression profiling in the euryoxic fish Gillichthys mirabilis. Proc Natl Acad Sci USA 98:1993–1998

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gu X, Xu Z (2011) Effect of hypoxia on the blood of large yellow croaker (Pseudosciaena crocea). Chin J Oceanol Limnol 29:524–530

    Article  CAS  Google Scholar 

  • Guzmán-Villanueva LT, Ascencio-Valle F, Macías-Rodríguez ME, Tovar-Ramírez D (2014) Effects of dietary β-1, 3/1, 6-glucan on the antioxidant and digestive enzyme activities of Pacific red snapper (Lutjanus peru) after exposure to lipopolysaccharides. Fish Physiol Biochem 40:827–837

    Article  PubMed  Google Scholar 

  • Hamanaka RB, Chandel NS (2009) Mitochondrial reactive oxygen species regulate hypoxic signaling. Curr Opin Cell Biol 21:894–899

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Howarth R, Chan F, Conley DJ, Garnier J, Doney S, Marino R, Billen G (2011) Coupled biogeochemical cycles: eutrophication and hypoxia in temperate estuaries and coastal marine ecosystems. Front Ecol Environ 9:18–26

    Article  Google Scholar 

  • Huang LE, Gu J, Schau M, Bunn HF (1998) Regulation of hypoxia-inducible factor 1α is mediated by an O2-dependent degradation domain via the ubiquitin-proteasome pathway. Proc Natl Acad Sci USA 95:7987–7992

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Huang Y, Hickey RP, Yeh JL, Liu DG, Dadak A, Young LH, Johnson RS, Giordano FJ (2004) Cardiac myocyte-specific HIF-1 alpha deletion alters vascularization, energy availability, calcium flux, and contractility in the normoxic heart. FASEB J 18:1138–1140

    Article  CAS  PubMed  Google Scholar 

  • Kim J, Tchernyshyov I, Semenza GL, Dang CV (2006) HIF-1-mediated expression of pyruvate dehydrogenase kinase: a metabolic switch required for cellular adaptation to hypoxia. Cell Metab 3:177–185

    Article  PubMed  Google Scholar 

  • Kim Y, Ke F, Zhang QY (2009) Effect of β-glucan on activity of antioxidant enzymes and Mx gene expression in virus infected grass carp. Fish Shellfish Immunol 27:336–340

    Article  CAS  PubMed  Google Scholar 

  • Kodama K, Rahman MS, Horiguchi T, Thomas P (2012) Upregulation of hypoxia-inducible factor (HIF)-1α and HIF-2α mRNA levels in dragonet Callionymus valenciennei exposed to environmental hypoxia in Tokyo Bay. Mar Pollut Bull 64:1339–1347

    Article  CAS  PubMed  Google Scholar 

  • Korshunov SS, Skulachev VP, Starkov AA (1997) High protonic potential actuates a mechanism of production of reactive oxygen species in mitochondria. FEBS Lett 416:15–18

    Article  CAS  PubMed  Google Scholar 

  • LeBel CP, Ischiropoulos H, Bondy SC (1992) Evaluation of the probe 2′, 7′-dichlorofluorescin as an indicator of reactive oxygen species formation and oxidative stress. Chem Res Toxicol 5:227–231

    Article  CAS  PubMed  Google Scholar 

  • Lendahl U, Lee KL, Yang H, Poellinger L (2009) Generating specificity and diversity in the transcriptional response to hypoxia. Nat Rev Genet 10:821–832

    Article  CAS  PubMed  Google Scholar 

  • Liu P, Yu Y, Liu C (1991) Studies on the situation of pollution and countermeasures of control of the oceanic environment in Zhoushan fishing ground—the largest fishing ground in China. Mar Pollut Bull 23:281–288

    Article  Google Scholar 

  • Liu XD, Zhao GT, Cai MY, Wang ZY (2013) Estimated genetic parameters for growth-related traits in large yellow croaker Larimichthys crocea using microsatellites to assign parentage. J Fish Biol 82:34–41

    Article  CAS  PubMed  Google Scholar 

  • Lushchak VI (2011) Environmentally induced oxidative stress in aquatic animals. Aquat Toxicol 101:13–30

    Article  CAS  PubMed  Google Scholar 

  • Martínez-Reyes I, Cuezva JM (2014) The H + -ATP synthase: a gate to ROS-mediated cell death or cell survival. Biochim Biophys Acta 1837:1099–1112

    Article  PubMed  Google Scholar 

  • Mason SD, Howlett RA, Kim MJ, Olfert IM, Hogan MC, McNulty W, Hickey RP, Wagner PD, Kahn CR, Giordano FJ, Johnson RS (2004) Loss of skeletal muscle HIF-1alpha results in altered exercise endurance. PLoS Biol 2:1540–1548

    Article  CAS  Google Scholar 

  • Meena DK, Das P, Kumar S, Mandal SC, Prusty AK, Singh SK, Akhtar MS, Behera BK, Kumar K, Pal AK, Mukherjee SC (2013) Beta-glucan: an ideal immunostimulant in aquaculture (a review). Fish Physiol Biochem 39:431–457

    Article  CAS  PubMed  Google Scholar 

  • Miest JJ, Arndt C, Adam M, Steinhagen D, Reusch TB (2016) Dietary β-glucan (MacroGard®) enhances survival of first feeding turbot (Scophthalmus maximus) larvae by altering immunity, metabolism and microbiota. Fish Shellfish Immunol 48:94–104

    Article  CAS  PubMed  Google Scholar 

  • Morin C, Zini R, Simon N, Tillement J (2002) Dehydroepiandrosterone and α-estradiol limit the functional alterations of rat brain mitochondria submitted to different experimental stresses. Neuroscience 115:415–424

    Article  CAS  PubMed  Google Scholar 

  • Moyson S, Liew HJ, Diricx M, Sinha AK, Blust R, De Boeck G (2015) The combined effect of hypoxia and nutritional status on metabolic and ionoregulatory responses of common carp (Cyprinus carpio). Comp Biochem Phys A 179:133–143

    Article  CAS  Google Scholar 

  • Mustafa SA, Karieb SS, Davies SJ, Jha AN (2015) Assessment of oxidative damage to DNA, transcriptional expression of key genes, lipid peroxidation and histopathological changes in carp Cyprinus carpio L. following exposure to chronic hypoxic and subsequent recovery in normoxic conditions. Mutagenesis 30:107–116

    Article  CAS  PubMed  Google Scholar 

  • Pacheco R, Ascencio F, Zarain M, Gómez G, Campa Á (2011) Enhancement of superoxide dismutase and catalase activity in juvenile brown shrimp, Farfantepenaeus californiensis (Holmes, 1900), fed β-1.3 glucan vitamin E, and β-carotene and infected with white spot syndrome virus. Lat Am J Aquat Res 39:534–543

    Article  Google Scholar 

  • Pfaffl MW (2001) A new mathematical model for relative quantification in real-time RT–PCR. Nucleic Acids Res 29:e45

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Philip G, Reddy P, Sridevi G (1995) Cypermethrin-induced in vivo alterations in the carbohydrate metabolism of freshwater fish, Labeo rohita. Ecotoxicol Environ Saf 31:173–178

    Article  CAS  PubMed  Google Scholar 

  • Pollard PJ, Briere JJ, Alam NA, Barwell J, Barclay E, Wortham NC, Hunt T, Mitchell M, Olpin S, Moat SJ, Hargreaves IP, Heales SJ, Chung YL, Griffiths JR, Dalgleish A, McGrath JA, Gleeson MJ, Hodgson SV, Poulsom R, Rustin P, Tomlinson IPM (2005) Accumulation of Krebs cycle intermediates and over-expression of HIF1α in tumours which result from germline FH and SDH mutations. Hum Mol Genet 14:2231–2239

    Article  CAS  PubMed  Google Scholar 

  • Rimoldi S, Terova G, Ceccuzzi P, Marelli S, Antonini M, Saroglia M (2012) HIF-1α mRNA levels in Eurasian perch (Perca fluviatilis) exposed to acute and chronic hypoxia. Mol Biol Rep 39:4009–4015

    Article  CAS  PubMed  Google Scholar 

  • Rissanen E, Tranberg HK, Sollid J, Nilsson GE, Nikinmaa M (2006) Temperature regulates hypoxia-inducible factor-1 (HIF-1) in a poikilothermic vertebrate, crucian carp (Carassius carassius). J Exp Biol 209:994–1003

    Article  CAS  PubMed  Google Scholar 

  • Sappal R, Fast M, Stevens D, Kibenge F, Siah A, Kamunde C (2015) Effects of copper, hypoxia and acute temperature shifts on mitochondrial oxidation in rainbow trout (Oncorhynchus mykiss) acclimated to warm temperature. Aquat Toxicol 169:46–57

    Article  CAS  PubMed  Google Scholar 

  • Selvaraj V, Sampath K, Sekar V (2005) Administration of yeast glucan enhances survival and some non-specific and specific immune parameters in carp (Cyprinus carpio) infected with Aeromonas hydrophila. Fish Shellfish Immunol 19:293–306

    Article  CAS  PubMed  Google Scholar 

  • Semenza GL (2002) Signal transduction to hypoxia-inducible factor 1. Biochem Pharmacol 64:993–998

    Article  CAS  PubMed  Google Scholar 

  • Sinha AK, Kumar V, Makkar HPS, De Boeck G, Becker K (2011) Non-starch polysaccharides and their role in fish nutrition–A review. Food Chem 127:1409–1426

    Article  CAS  Google Scholar 

  • Sirimanapong W, Thompson KD, Ooi EL, Bekaert M, Collet B, Taggart JB, Bron JE, Green DM, Shinn AP, Adams A, Leaver MJ (2015) The effects of feeding β-glucan to Pangasianodon hypophthalmus on immune gene expression and resistance to Edwardsiella ictaluri. Fish Shellfish Immunol 47:595–605

    Article  CAS  PubMed  Google Scholar 

  • Soltanian S, Adloo MN, Hafeziyeh M, Ghadimi N (2014) Effect of β-Glucan on cold-stress resistance of striped catfish, Pangasianodon hypophthalmus (Sauvage, 1878). Vet Med-Czech 59:440–446

    Google Scholar 

  • Taylor C (2008) Mitochondria and cellular oxygen sensing in the HIF pathway. Biochem J 409:19–26

    Article  CAS  PubMed  Google Scholar 

  • Vandesompele J, De Preter K, Pattyn F, Poppe B, Van Roy N, De Paepe A, Speleman F (2002) Accurate normalization of real-time quantitative RT-PCR data by geometric averaging of multiple internal control genes. Genome Biol. doi:10.1186/gb-2002-3-7-research0034

  • Walsh K, Koshland DE (1984) Determination of flux through the branch point of two metabolic cycles. The tricarboxylic acid cycle and the glyoxylate shunt. J Biol Chem 259:9646–9654

    CAS  PubMed  Google Scholar 

  • Weber G, Convery HJH, Lea MA, Stamm NB (1966) Feedback inhibition of key glycolytic enzymes in liver: action of free fatty acids. Science 154:1357–1360

    Article  CAS  PubMed  Google Scholar 

  • Welker AF, Moreira DC, Campos ÉG, Hermes-Lima M (2013) Role of redox metabolism for adaptation of aquatic animals to drastic changes in oxygen availability. Comp Biochem Phys A 165:384–404

    Article  CAS  Google Scholar 

  • Wu C, Zhang D, Kan M, Lv Z, Zhu A, Su Y, Zhou D, Zhang J, Zhang Z, Xu M, Jiang L, Guo B, Wang T, Chi C, Mao Y, Zhou J, Yu X, Wang H, Weng X, Jin JG, Ye J, He L, Liu Y (2014) The draft genome of the large yellow croaker reveals well-developed innate immunity. Nat Commun 5:5227

    Article  PubMed  PubMed Central  Google Scholar 

  • Xu C, Lv J, Lo YM, Cui SW, Hu X, Fan M (2013) Effects of oat β-glucan on endurance exercise and its anti-fatigue properties in trained rats. Carbohydr Polym 92:1159–1165

    Article  CAS  PubMed  Google Scholar 

  • Yang QL, Yao CL, Wang ZY (2012) Acute temperature and cadmium stress response characterization of small heat shock protein 27 in large yellow croaker, Larimichthys crocea. Comp Biochem Phys C 155:190–197

    CAS  Google Scholar 

  • Yasuda R, Noji H, Kinosita K, Yoshida M (1998) F1-ATPase is a highly efficient molecular motor that rotates with discrete 120 steps. Cell 93:1117–1124

    Article  CAS  PubMed  Google Scholar 

  • Zhang PP, Hu XZ, Zhen HM, Xu C, Fan MT (2012) Oat β-glucan increased ATPases activity and energy charge in small intestine of rats. J Agric Food Chem 60:9822–9827

    Article  CAS  PubMed  Google Scholar 

  • Zhu CD, Wang ZH, Yan B (2013) Strategies for hypoxia adaptation in fish species: a review. J Comp Physiol B 183:1005–1013

    Article  CAS  PubMed  Google Scholar 

  • Zorov DB, Juhaszova M, Sollott SJ (2006) Mitochondrial ROS-induced ROS release: an update and review. BBA-Bioenerg 1757:509–517

    Article  CAS  Google Scholar 

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Acknowledgments

This work was supported by National Project of Scientific and Technical Supporting Programs Funded by Ministry of Science and Technology of China (No. 2011BAD13B08), and Scientific Research Foundation of Zhejiang Ocean University (22115010415). The authors thank the Yuyang Fisheries Co., Ltd, for supporting large yellow croaker.

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Authors and Affiliations

  1. National Engineering Research Center for Marine Aquaculture, Zhejiang Ocean University, Zhoushan, 316000, China

    Lin Zeng, Yong-Hong Wang, Jia-Lang Zheng, Chang-Wen Wu & Rong Cai

  2. College of Ocean and Earth Sciences, Xiamen University, Xiamen, 361005, China

    Chun-Xiang Ai

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  1. Lin Zeng
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  2. Yong-Hong Wang
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  3. Chun-Xiang Ai
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Correspondence to Chang-Wen Wu.

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Zeng, L., Wang, YH., Ai, CX. et al. Effects of β-glucan on ROS production and energy metabolism in yellow croaker (Pseudosciaena crocea) under acute hypoxic stress. Fish Physiol Biochem 42, 1395–1405 (2016). https://doi.org/10.1007/s10695-016-0227-1

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