Skip to main content
Log in

Modulation of redox regulatory molecules and electron transport chain activity in muscle of air breathing fish Heteropneustes fossilis under air exposure stress

Journal of Comparative Physiology B Aims and scope Submit manuscript

Cite this article

Abstract

Responses of redox regulatory system to long-term survival (>18 h) of the catfish Heteropneustes fossilis in air are not yet understood. Lipid and protein oxidation level, oxidant (H2O2) generation, antioxidative status (levels of superoxide dismutase, catalase, glutathione peroxidase and reductase, ascorbic acid and non-protein sulfhydryl) and activities of respiratory complexes (I, II, III and IV) in mitochondria were investigated in muscle of H. fossilis under air exposure condition (0, 3, 6, 12 and 18 h at 25 °C). The increased levels of both H2O2 and tissue oxidation were observed due to the decreased activities of antioxidant enzymes in muscle under water deprivation condition. However, ascorbic acid and non-protein thiol groups were the highest at 18 h air exposure time. A linear increase in complex II activity with air exposure time and an increase up to 12 h followed by a decrease in activity of complex I at 18 h were observed. Negative correlation was observed for complex III and V activity with exposure time. Critical time to modulate the above parameters was found to be 3 h air exposure. Dehydration induced oxidative stress due to modulation of electron transport chain and redox metabolizing enzymes in muscle of H. fossilis was clearly observed. Possible contribution of redox regulatory system in muscle tissue of the fish for long-term survival in air is elucidated. Results of the present study may be useful to understand the redox metabolism in muscle of fishes those are exposed to air in general and air breathing fishes in particular.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Institutional subscriptions

Fig. 1
Fig. 2
Fig. 3
Fig. 4
Fig. 5

References

  • Abele D, Philipp E, Gonzalez PM, Puntarulo S (2007) Marine invertebrate mitochondria and oxidative stress. Front Biosci 12:933–946

    Article  CAS  PubMed  Google Scholar 

  • Abele D, Vazquez-Medina JP, Zenteno-Savin T (2011) Oxidative stress in aquatic ecosystems, 1st edn. Blackwell and Wiley, USA, p 548

    Book  Google Scholar 

  • Aebi H (1974) Catalase. In: Bergeyer HU (ed) Methods of enzymatic analysis, vol 2. Academic Press, New York, pp 673–678

    Chapter  Google Scholar 

  • Bailly N (2013) Heteropneustes fossilis (Bloch 1794). In: Froese R, Pauly D (eds) FishBase 2013: concepts, design and data sources. ICLARM, Los Baños, p 344

    Google Scholar 

  • Borkovic SS, Pavlovic SZ, Kovacevic TB, Stajn AS, Petrovic VM, Saicic ZS (2008) Antioxidant defence enzyme activities in hepatopancreas, gills and muscle of Spiny cheek crayfish (Orconectes limosus) from the River Danube. Comp Biochem Physiol C 147:122–128

    Google Scholar 

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

    Article  CAS  PubMed  Google Scholar 

  • Brand MD, Couture P, Else PL, Withers KW, Hulbert AJ (1991) Evolution of energy metabolism proton permeability of the inner membrane of liver mitochondria is greater in a mammal than in a reptile. Biochem J 275:81–86

    CAS  PubMed  Google Scholar 

  • Bridges R (2013) Air-breathing in Tropical Fresh Water Fishes. Federation of British Aquatic Society. http://www.fbas.co.uk/index.html retrieved on 20.03.2013

  • Chen PS, Toribara TY, Warner H (1956) Microdetermination of phosphorus. Anal Chem 28:1756–1758

    Article  CAS  Google Scholar 

  • Colleoni F, Padmanabhan N, Yung H, Watson ED, Cetin I, Patot MCT, Burton GJ, Murray AJ (2013) Suppression of mitochondrial electron transport chain function in the hypoxic human placenta: A Role for miRNA-210 and protein synthesis inhibition. PLOS One 8:e55194–e55194

    Article  CAS  PubMed Central  PubMed  Google Scholar 

  • Cormier A, Morin C, Zini R, Tillement JP, Lagrue G (2001) In vitro effects of nicotine on mitochondrial respiration and superoxide anion generation. Brain Res 900:72–79

    Article  CAS  PubMed  Google Scholar 

  • Das K, Samanta L, Chainy GBN (2000) A modified spectrophotometric assay of superoxide dismutase using nitrite formation by super oxide radicals. Ind J Biochem Biophys 37:201–204

    CAS  Google Scholar 

  • Dirmeier R, O’Brien KM, Engle M, Dodd A, Spears E, Poyton RO (2002) Exposure of yeast cells to anoxia induces transient oxidative stress. Implications for the induction oh hypoxic genes. J Biol Chem 277:34773–34784

    Article  CAS  PubMed  Google Scholar 

  • Drouin G, Godin J, Pagé B (2011) The genetics of vitamin C loss in vertebrates. Curr Genomics 12:371–378

    Article  CAS  PubMed  Google Scholar 

  • Erfanullah, Jafri AK (1999) Growth, feed conversion, body composition and nutrient retention in fingerling catfish, Heteropneustes fossilis (Bloch), fed different sources of dietary carbohydrates. Aquac Res 30:43–49

  • Garson GD (2008) Statnotes: Topics in multivariate analysis. http://www2.chass.ncsu.edu/garson/pa765/statnote.htm. Retrieved on 24 Feb 2013

  • Gassner B, Wuthrich A, Scholtysik G, Solioz M (1997) The pyrethroids permethrin and cyhalothrin are potent inhibitors of the mitochondrial complex I. J Pharmacol Exp Ther 281:855–860

    CAS  PubMed  Google Scholar 

  • Graham JB (1997) Air-breathing fishes: evolution, diversity, and adaptation. Academic Press, USA 299

    Google Scholar 

  • Halliwell B, Gutteridge JMC (2001) Free radicals in biology and medicine, 3rd edn. Oxford University Press, New York

    Google Scholar 

  • Jennrich RI (1977) Stepwise discriminant analysis. In: Enslein K, Ralston A, Wilf HS (eds) Statistical methods for digital computers. Wiley, New York, pp 76–95

    Google Scholar 

  • Lambowitz AM (1979) Preparation and analysis of mitochondrial ribosomes. Method Enzymol 59:421–433

    CAS  Google Scholar 

  • Levine RL, Williams JA, Stadtman ER, Shacter E (1994) Carbonyl assays for determination of oxidatively modified proteins. In: Packer L (ed) Methods Enzymol, vol 233. Academic press, California, pp 346–357

    Google Scholar 

  • Lushchak VI, Bagnyukova TV (2006) Effects of different environmental oxygen levels on free radical processes in fish. Comp Biochem Physiol B Biochem Mol Biol 144:283–289

    Article  PubMed  Google Scholar 

  • Lushchak VI, Lushchak LP, Mota AA, Hermes-Lima M (2001) Oxidative stress and antioxidant defenses in goldfish Carassius auratus during anoxia and reoxygenation. Am J Physiol Regul Integr Comp Physiol 280:R100–R107

    CAS  PubMed  Google Scholar 

  • Lushchak VI, Bagnyukova TV, Lushchak OV, Storey JM, Storey KB (2005) Hypoxia and recovery perturb free radical processes and antioxidant potential in common carp (Cyprinus carpio) tissues. Int J Biochem Cell Biol 37:1319–1330

    Article  CAS  PubMed  Google Scholar 

  • Maiti AK, Saha NC, Paul G (2010) Effect of lead on oxidative stress, Na+K+ATPase activity and mitochondrial electron transport chain activity of the brain of Clarias batrachus L. Bull Environ Contam Toxicol 84:672–676

    Article  CAS  PubMed  Google Scholar 

  • Massey V, Williams CH (1965) On the reaction mechanism of yeast glutathione reductase. J Biol Chem 240:4470–4481

    CAS  PubMed  Google Scholar 

  • Menon AGK (1999) Check list: fresh water fishes of India. Rec Zool Surv India, Misc. Publ., Occas. Pap. No. 175, 366 p

  • Mitsui A, Ohta T (1961) Photooxidative consumption and photoreductive formation of ascorbic acid in green leaves. Plant Cell Physiol 2:31–44

    CAS  Google Scholar 

  • Munshi JSD, Pandey BN, Pandey PK, Ojha J (1978) Oxygen uptake through gills and skin in relation to body weight of an air-breathing siluroid fish, Saccobranchus (=Heteropneustes) fossilis. J Zool Lond 184:171–180

    Article  Google Scholar 

  • Ohkawa H, Ohishi N, Yagi K (1979) Assay for lipid peroxides in animal tissue by thiobarbituric acid reaction. Anal Biochem 95:351–358

    Article  CAS  PubMed  Google Scholar 

  • Paglia DE, Valentine WN (1967) Studies on the quantitative and qualitative characterization of erythrocyte glutathione peroxidase. J Lab Clin Med 70:158–169

    CAS  PubMed  Google Scholar 

  • Paital B (2013) Antioxidant and oxidative stress parameters in brain of Heteropneustes fossilis under air exposure condition; role of mitochondrial electron transport chain. Ecotoxicol Environ Saf 95:69–77

    Article  CAS  PubMed  Google Scholar 

  • Paital B, Chainy GBN (2010) Antioxidant defenses and oxidative stress parameters in tissues of mud crab (Scylla serrata) with reference to changing salinity. Comp Biochem Physiol C 151:142–151

    Google Scholar 

  • Paital B, Chainy GBN (2012) Effects of salinity on O2 consumption, ROS generation and oxidative stress status of gill mitochondria of the mud crab Scylla serrata. Comp Biochem Physiol C 155:228–237

    CAS  Google Scholar 

  • Paital B, Chainy GBN (2013a) Modulation of expression of SOD isoenzymes in mud crab (Scylla serrata): effects of inhibitors, salinity and season. J Enz Inhibition Med Chem 28:195–204

    Article  CAS  Google Scholar 

  • Paital B, Chainy GBN (2013b) Seasonal variability of antioxidant biomarkers in mud crabs (Scylla serrata). Ecotoxic Environ Saf 87:33–41

    Article  CAS  Google Scholar 

  • Paital B, Kumar S, Farmer R, Tripathy NK, Chainy GBN (2011) In silico prediction and characterization of 3D structure and binding properties of catalase from the commercially important crab, Scylla serrata. Interdiscip Sci Comput Life Sci 3:1913–2751

    Article  Google Scholar 

  • Paital B, Kumar S, Farmer R, Tripathy NK, Chainy GBN (2013) In silico prediction of 3D structure of superoxide dismutase of Scylla serrata and its binding properties with inhibitors. Interdiscip Sci Comput Life Sci 5:69–76

    Article  CAS  Google Scholar 

  • Parihar MS, Dubey AK (1995) Lipid peroxidation and ascorbic acid status in respiratory organs of male and female freshwater catfish Heteropneustes fossilis exposed to temperature increase. Comp Biochem Physiol C 112:309–313

    CAS  PubMed  Google Scholar 

  • Powell CS, Jackson RM (2003) Mitochondrial complex I, aconitase, and succinate dehydrogenase during hypoxia-reoxygenation: modulation of enzyme activities by MnSOD. Am J Physiol Lung Cell Mol Physiol 285:L189–L198

    CAS  PubMed  Google Scholar 

  • Romero MC, Ansaldo M, Lovrich GA (2007) Effect of aerial exposure on the antioxidant status in the subantarctic stone crab Paralomis granulosa (Decapoda: Anomura). Comp Biochem Physiol C 146:54–59

    Google Scholar 

  • Saha N, Ratha BK (1989) A comparative study of ureogenesis in freshwater air-breathing teleosts. J Exp Zool 252:1–8

    Article  Google Scholar 

  • Saha N, Das L, Dutta S, Goswami UC (2001) Role of ureogenesis in the mud-dwelled singhi catfish (Heteropneustes fossilis) under condition of water shortage. Comp Biochem Physiol A 128:137–146

    Article  CAS  Google Scholar 

  • Sedlak J, Lindsay RH (1968) Estimation of total, protein-bound and nonprotein sulfhydryl groups in tissue with Ellman’s reagent. Anal Biochem 25:192–205

    Article  CAS  PubMed  Google Scholar 

  • Staniek K, Nohl H (1999) H2O2 detection from intact mitochondria as a measure for one-electron reduction of oxygen requires a non-invasive assay system. Biochim Biophys Acta 1413:70–80

    Article  CAS  PubMed  Google Scholar 

  • Storey KB, Storey JM (2004) Metabolic rate depression in animals: transcriptional and translational controls. Biol Rev 79:207–233

    Article  PubMed  Google Scholar 

  • Takano H, Zou Y, Hasegawa H, Akazawa H, Nagai T, Komuro I (2003) Oxidative stress-induced signal transduction pathways in cardiac myocytes: involvement of ROS in heart diseases. Antioxid Redox Sign 5:789–794

    Article  CAS  Google Scholar 

  • Talwar PK, Jhingran AG (1991) Inland fishes of India and adjacent countries, vol 2. Oxford and IBH Publishing Company Ltd., New Delhi 1158 pp

    Google Scholar 

  • Thurston RV, Gehrke PC (1993) Respiratory oxygen requirements of fishes: description of OXYREF, a data file based on test results reported in the published literature. In: Russo RC, Thurston RV (eds) Fish physiology, toxicology, and water quality management. proceedings of an international symposium, Sacramento, US Environmental Protection Agency EPA/600/R-93/157, California, USA, p 95–108

  • Tisdale HD (1967) Preparation and properties of succinic-cytochrome c reductase (Complex II-III). Method Enzymol 10:213–215

    CAS  Google Scholar 

  • Turrens JF (2003) Mitochondrial formation of reactive oxygen species. J Physiol 552(2):335–344

    Article  CAS  PubMed  Google Scholar 

  • Van den Thillart G, van Waarde A (1985) Teleosts in hypoxia: aspects of anaerobic metabolism. Mol Physiol 8:393–409

    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 Physiol A Mol Integr Physiol 165:384–404

    Article  CAS  PubMed  Google Scholar 

  • William WW, Chandel NS (2011) Hypoxia. 2. Hypoxia regulates cellular metabolism. Am J Physiol Cell Physiol 300:C385–C393

    Article  Google Scholar 

  • Zaccone G, Casio PL, Fasulo S, Licata A (1985) The effect of an anionic detergent on complex carbohydrates and enzyme activities in the epidermis of the catfish Heteropneustes fossilis (Bloch). Histochem J 17:453–466

    Article  CAS  PubMed  Google Scholar 

Download references

Acknowledgments

The work was supported by the financial grant from Department of Biotechnology, Govt. of India, New Delhi under DBT-RA program at Biochemical Adaptation Laboratory, Banaras Hindu University, Varanasi India. The laboratory facilities offered by Prof. B.K. Ratha to conduct the entire work at Biochemical Adaptation Laboratory are highly acknowledged. I am also extremely grateful to the Heads, Dept. of Botany (for fluorimetric analysis in central facility) and Dept. of Zoology, BHU for providing necessary laboratory facilities. The inputs given by Prof. G.B.N. Chainy during the work are also duly acknowledged. Helps rendered by Mr. Ashok Yadav, Ms. Suman Mishra and Smita Verma during animal handling and tissue collection are highly acknowledged.

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Biswaranjan Paital.

Additional information

Communicated by G. Heldmaier.

Electronic supplementary material

Below is the link to the electronic supplementary material.

Supplementary material 1 (DOC 62 kb)

Rights and permissions

Reprints and Permissions

About this article

Cite this article

Paital, B. Modulation of redox regulatory molecules and electron transport chain activity in muscle of air breathing fish Heteropneustes fossilis under air exposure stress. J Comp Physiol B 184, 65–76 (2014). https://doi.org/10.1007/s00360-013-0778-8

Download citation

  • Received:

  • Revised:

  • Accepted:

  • Published:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00360-013-0778-8

Keywords

Navigation