Abstract
The in vivo and in vitro effect of hypoxia (0.57–8.17 mg O2l−1) on functional characteristics of nucleated erythrocytes of the benthic scorpionfish Scorpaena porcus L. was studied. The cellular systems in this species were established to be characterized by a balanced suppression of membrane and metabolic functions in conditions of external oxygen deficit (in vivo experiments). It manifests itself in the capacity of cells to maintain the intracellular ATP concentration and transmembrane Na+ and K+ gradients within the norm at low activity of Na+, K+-ATPase and hexokinase. This phenomenon appears to be underlain by the reduction in the number of active plasma membrane ion channels diminishing energetic costs of cationic gradient maintenance (metabolic arrest phenomenon). The same is also evidenced by the rise in FDA and R123 fluorescence intensity in erythrocyte suspensions under hypoxia (in vitro experiments). The mechanisms underlying this phenomenon are discussed.
This is a preview of subscription content, log in via an institution to check access.
Similar content being viewed by others
References
Hochachka, P., Defence Strategies Against Hypoxia and Hypothermia, Science, 1986, vol. 231, pp. 324–241.
Waarde, A., Biochemistry of Non-Protein Nitrogenous Compounds in Fish Including the Use of Amino Acids for Anaerobic Energy Production, Comp. Biochem. Physiol., 1988, vol. 91B, pp. 207–228.
Savina, M.V., Mekhanizmy adaptatsii tkanevogo dykhaniya v evolutsii pozvonochnykh (Adaptation Mechanisms of Tissue Respiration in Evolution of Vertebrates), Sankt-Petersburg, Nauka, 1992, 200 pp.
Shulman, G.E., Abolmasova, G.I., and Stolbov, A.Ya., Using the Protein in Energetic Exchange of Hydrobionts, Usp. Sovr. Biol., 1993, vol. 113, no. 5, pp. 576–586.
Chew, S.F., Gan, J., and Ip, Y.K., Nitrogen Metabolism and Excretion in the Swamp Eel, Monopterus albus, During 6 or 40 Days of Estivation in Mud, Physiol. Biochem. Zool., 2005, vol. 78, no. 4, pp. 620–629.
Wells, R.M.G., Blood-Gas Transport and Hemoglobin Function: Adaptations for Functional and Environmental Hypoxia, Fish Physiology, 2009, vol. 27, pp. 255–299.
Lowe, T.E., Bril, R.W., and Cousins, K.L., Responses of the Red Blood Cells from Two High Energy-Demand Teleosts, Yellowfin Tuna (Thunnus albacares) and Skipjack Tuna (Katsuwonus pelamis), to Catecholamines, J. Comp. Physiol. B., 1998, vol. 168, no. 6, pp. 405–418.
Soldatov, A.A., Parfenova, I.A., and Novitskaya, V.N., Content of Monovalent Cations and ATP in Erythrocytes of Sea Fishes Under Experimental Hypoxia, Ukr. Biokhim. Zh., 2010, vol. 82, pp. 36–41.
Novitskaya, V.N. and Soldatov, A.A., Hemolymph Erythroid Elements of Anadara inaequivalvis (Mollusca: Arcidae) Under Conditions of Experimental Anoxia: Functional and Morphometric Characteristics, Morsk. Ekol. Zh., 2011, vol. X, no. 1, pp. 56–64.
Soldatov, A.A., Physiological Aspects of Action of Uretane Anesthesia on Organism of Sea Fishes, Hidrobiol. Zh., 2003, vol. 39, no. 1, pp. 51–63.
Kochetov, G.A., Prakticheskoe rukovodstvo po enzimologii (Handbook on Enzymology), Moscow, Vysshaya shkola, 1980, 272 pp.
Tiihonen, K. and Nikinmaa, M., Short Communication: Substrate Utilization by Carp (Cyprinus carpio) Erythrocytes, J. Exp. Biol., 1991, vol. 161, pp. 509–514.
Bickler, P.E. and Buck, L.T.,, Hypoxia Tolerance in Reptiles, Amphibians, and Fishes: Life with Variable Oxygen Availability, Annu. Rev. Physiol., 2007, vol. 69, no. 2, pp. 145–170.
Bachand, L. and Leray, C., Erythrocyte Metabolism in the Yellow Perch. I. Glycolytic Enzymes, Comp. Biochem. Physiol., 1975, vol. 50B, no. 6, pp. 567–570.
Tufts, B.L. and Boutilier, R.G., Interactions Between Ion Exchange and Metabolism in Erythrocytes of the Rainbow Trout Oncorhynchus mykiss, J. Exp. Biol., 1991, vol. 231, no. 1, pp. 139–151.
Toescu, E.C. and Verkhratsky, A., Assessment of Mitochondrial Polarization Status in Living Cells Based on Analysis of the Spatial Heterogeneity of Rhodamine 123 Fluorescence Staining, Eur. J. Physiol., 2000, vol. 440, pp. 941–947.
Wang, T., Zhang, Z.X., and Xu, Y.J., Effect of Mitochondrial KATP Channel on Voltage-Gated K+ Channel in 24 Hour-Hypoxic Human Pulmonary Artery Smooth Muscle Cells, Chinese Med. J-Peking, 2005, vol. 118, no. 1, pp. 12–19.
Weinberg, J.M., Venkatachalam, M.A., Roeser, N.F., and Nissim, I., Mitochondrial Dysfunction During Hypoxia and Reoxygenation and its Correction by Anaerobic Metabolism of Citric Acid Cycle Intermediates, Proc. Natl. Acad. Sci. USA, 2000, vol. 97, no. 6, pp. 2826–2831.
Rus, A., Del Moral, M.L., and Molina, F., Upregulation of Cardiac NO/NOS System During Short-Term Hypoxia and the Subsequent Reoxygenation Period, Eur. J. Histochem., 2011, vol. 55, no. 2, pp. 91–96.
Prosperi, E., Intracellular Turnover of Fluorescein Diacetate. Influence of Membrane Ionic Gradients on Fluorescein Efflux, Histochem. J., 1990, vol. 22, pp. 227–233.
Heslop-Harrison, J. and Heslop-Harrison, Y., Evaluation of Pollen Viability by Enzymatically Induced Fluorescence; Intracellular Hydrolysis of Fluorescein Diacetate, Stain Technol., 1970, vol. 45, no. 3, pp. 115–120.
Baldisserotto, B., Chippari-Gomes, A.R., and Lopes, N.P., Ion Fluxes and Hematological Parameters of Two Teleosts from the Rio Negro, Amazon, Exposed to hypoxia, Braz. J. Biol., 2008, vol. 68, no. 3, pp. 571–575.
Soulier, P., Peyraud-Waitzenegger, M., and Peyraud, C., Respiratory and Cardiovascular Effects of Hypoxia in the European Eel, Arch. Int. Physiol., Biochem. et Biophys., 1991, vol. 99, no. 5, pp. 124–132.
Swift, D.I. and Lloyd, R., Changes in Urine Flow Rate and Hematocrit Value of Rainbow Trout Salmo gairdneri Exposed to Hypoxia, J. Fish Biol., 1974, vol. 6, no. 4, pp. 379–387.
Edelman, I.S. and Fanestil, D.D., Mineralocorticoids, Biochem. Action of Hormones, vol. 1, New York, Acad., 1972, pp, 321–364.
Buck, L.T., Adenosine as a Signal for Ion Channel Arrest in Anoxia-Tolerant Organisms, Comp. Biochem. Physiol. B. Biochem. Mol. Biol., 2004, vol. 139, no. 3, pp. 401–414.
Author information
Authors and Affiliations
Corresponding author
Additional information
Original Russian Text © A.A. Soldatov, A.Yu. Andreeva, V.N. Novitskaya, I.A. Parfenova, 2014, published in Zhurnal Evolyutsionnoi Biokhimii i Fiziologii, 2014, Vol. 50, No. 5, pp. 358–363.
Rights and permissions
About this article
Cite this article
Soldatov, A.A., Andreeva, A.Y., Novitskaya, V.N. et al. Coupling of membrane and metabolic functions in nucleated erythrocytes of Scorpaena porcus L. Under hypoxia in vivo and in vitro . J Evol Biochem Phys 50, 409–415 (2014). https://doi.org/10.1134/S0022093014050056
Received:
Published:
Issue Date:
DOI: https://doi.org/10.1134/S0022093014050056