Advertisement

Fish Physiology and Biochemistry

, Volume 45, Issue 6, pp 1933–1940 | Cite as

Hemoglobin deoxygenation and methemoglobinemia prevent regulatory volume decrease in crucian carp (Carassius carassius) red blood cells

  • A. Y. AndreyevaEmail author
  • A. A. Soldatov
  • A. I. Krivchenko
  • I. V. Mindukshev
  • S. Gambaryan
Article
  • 31 Downloads

Abstract

Fish red blood cells (RBCs) exhibit an oxygen-dependent regulatory volume decrease (RVD) in hypoosmotic environment. In higher vertebrates, membrane-associated hemoglobin is involved in the regulation of osmotic ion movements across the cellular membrane. However, whether the hemoglobin conformational state plays a role in the regulation of osmotic responses in fish red blood cells is still not fully understood. We found that changes in hemoglobin conformation influence the pattern of the regulatory volume decrease in Carassius carassius red blood cells. In oxygenated cells (96.4 ± 3.7% oxygenated hemoglobin), the volume recovery was completed within 125 min. Deoxygenation of hemoglobin (96.5 ± 2.7% of deoxygenated hemoglobin) inhibited the volume decrease in hyposmotically swollen red blood cells. Reoxygenation restored regulatory volume decrease in cells within 5 min. Induced methemoglobinemia (48.4 ± 1.8% of methemoglobin and 41.3 ± 2.3% of deoxygenated hemoglobin) blocked the process of volume recovery and significantly decreased osmotic stability of red blood cells.

Keywords

Hemoglobin conformational state Osmolarity Volume regulation Red blood cells Teleosts 

Notes

Acknowledgments

These studies were supported by the Ministry of Science and Higher Education of the Russian Federation (No. АААА-А18-118012290371-3; No. AAAA-A18-118021490093-4).

Compliance with ethical standards

All procedures using fish were accomplished in accordance with the European Communities Council Directive (2010/63/EU) and approved by the local Institutional Animal Care and Use Committee (protocol #28 from 15.02. 2018).

References

  1. Andreyeva AY, Skverchinskaya EA, Gambaryan S, Soldatov AA, Mindukshev IV (2018) Hypoxia inhibits the regulatory volume decrease in red blood cells of common frog (Rana temporaria). Comp Biochem Physiol A 219-220:44–47CrossRefGoogle Scholar
  2. Arashiki N, Kimata N, Manno S, Mohandas N, Takakuwa Y (2013) Membrane peroxidation and methemoglobin formation are both necessary for band 3 clustering: mechanistic insights into human erythrocyte senescence. Biochemistry 52(34):5760–5769CrossRefGoogle Scholar
  3. Barbul A, Zipser Y, Nachles A, Korenstein R (1999) Deoxygenation and elevation of intracellular magnesium induce tyrosine phosphorylation of band 3 in human erythrocytes. FEBS Lett 455:87–91CrossRefGoogle Scholar
  4. Barvitenko N, Adragna N, Weber R (2005) Erythrocyte signal transduction pathways, their oxygenation dependence and functional significance. Cell Physiol Biochem 15(1–4):001–018CrossRefGoogle Scholar
  5. Benesch RE, Benesch R, Yung S (1973) Equations for the spectrophotometric analysis of hemoglobin mixtures. Anal Biochem 55:245–248CrossRefGoogle Scholar
  6. Berenbrink M, Völkel S, Heisler N, Nikinmaa M (2000) O2-dependent K+ fluxes in trout red blood cells: the nature of O2 sensing revealed by the O2 affinity, cooperativity and pH dependence of transport. J Physiol 526(1):69–80CrossRefGoogle Scholar
  7. Borgese F, Motais R, Garcia-Romeu F (1991) Regulation of Cl-dependent K transport by oxy-deoxyhemoglobin transitions in trout red cells. Biochim Biophys Acta Biomembr 1066(2):252–256CrossRefGoogle Scholar
  8. Cala PM (1977) Volume regulation by flounder red blood cells in anisotonic media. J Gen Physiol 69(5):537–552CrossRefGoogle Scholar
  9. Chu H, Breite A, Ciraolo P, Franco RS, Low PS (2008) Characterization of the deoxyhemoglobin binding site on human erythrocyte band 3: implications for O2 regulation of erythrocyte properties. Blood 111(2):932–938CrossRefGoogle Scholar
  10. Cooper A, Taylor EW, Wang T (2001) Volume regulation by red blood cells from brown trout. J Fish Biol 59(4):1098–1103CrossRefGoogle Scholar
  11. Cossins AR, Gibson JS (1997) Volume-sensitive transport systems and volume homeostasis in vertebrate red blood cells. J Exp Biol 200(2):343–352PubMedGoogle Scholar
  12. Datta P, Chakrabarty SB, Chakrabarty A, Chakrabarti A (2003) Interaction of erythroid spectrin with hemoglobin variants: implications in beta-thalassemia. Blood Cells Mol Dis 30:248–253CrossRefGoogle Scholar
  13. De Rosa MC, Alinovi CC, Galtieri A, Russo A, Giardina B (2008) Allosteric properties of hemoglobin and the plasma membrane of the erythrocyte: new insights in gas transport and metabolic modulation. IUBMB Life 60(2):87–93CrossRefGoogle Scholar
  14. Galtieri A et al (2002) Band-3 protein function in human erythrocytes: effect of oxygenation–deoxygenation. Biochim Biophys Acta Biomembr 1564(1):214–218CrossRefGoogle Scholar
  15. Garcia-Romeu F, Cossins AR, Motais R (1991) Cell volume regulation by trout erythrocytes: characteristics of the transport systems activated by hypotonic swelling. J Physiol 440(1):547–567CrossRefGoogle Scholar
  16. Gibson JS, Cossins AR, Ellory JC (2000) Oxygen-sensitive membrane transporters in vertebrate red cells. J Exp Biol 203(9):1395–1407PubMedGoogle Scholar
  17. Grosell M, Jensen FB (2000) Uptake and effects of nitrite in the marine teleost fish Platichthys flesus. Aquat Toxicol 50(1–2):97–107CrossRefGoogle Scholar
  18. Haynes JK, Goldstein L (1993) Volume-regulatory amino acid transport in erythrocytes of the little skate, Raja erinacea. Am J Phys Regul Integr Comp Phys 265(1):R173–R179Google Scholar
  19. Hoffmann EK, Lambert IH, Pedersen SF (2009) Physiology of cell volume regulation in vertebrates. Physiol Rev 89(1):193–277CrossRefGoogle Scholar
  20. Jensen F (1995) Regulatory volume decrease in carp red blood cells: mechanisms and oxygenation-dependency of volume-activated potassium and amino acid transport. J Exp Biol 198(1):155–165PubMedGoogle Scholar
  21. Jensen FB, Brahm J (1995) Kinetics of chloride transport across fish red blood cell membranes. J Exp Biol 198:2237–2244PubMedGoogle Scholar
  22. Jensen FB, Jakobsen MH, Weber RE (1998) Interaction between haemoglobin and synthetic peptides of the N-terminal cytoplasmic fragment of trout band 3 (AE1) protein. J Exp Biol 201(19):2685–2690PubMedGoogle Scholar
  23. Khan AI, Drew C, Ball SE, Ball V, Ellory JC, Gibson JS (2004) Oxygen dependence of K+-Cl-cotransport in human red cell ghosts and sickle cells. Bioelectrochem 62(2):141–146CrossRefGoogle Scholar
  24. Lewis IA, Campanella ME, Markley JL, Low PS (2009) Role of band 3 in regulating metabolic flux of red blood cells. Proc Natl Acad Sci 106(44):18515–18520CrossRefGoogle Scholar
  25. Lopez-Barneo J, Pardal R, Ortega-Saenz P (2001) Cellular mechanisms of oxygen sensing. Annu Rev Physiol 63:259–287CrossRefGoogle Scholar
  26. Marttila ONT, Nikinmaa M (1988) Binding of b-adrenergic antagonists 3H-DHA and 3H-CGP 12177 to intact rainbow trout (Salmo gairdneri) and carp (Cyprinus carpio) red blood cells. Gen Comp Endocrinol 70:429–435CrossRefGoogle Scholar
  27. Mindukshev IV, Krivoshlyk VV, Ermolaeva EE, Dobrylko IA, Senchenkov EV, Goncharov NV, Jenkins RO, Krivchenko AI (2007) Necrotic and apoptotic volume changes of red blood cells investigated by low-angle light scattering technique. J Spectrosc 21:105–120CrossRefGoogle Scholar
  28. Mindukshev I, Kudryavtsev I, Serebriakova M, Trulioff A, Gambaryan S, Sudnitsyna J, Khmelevskoy D, Voitenko N, Avdonin P, Jenkins R, Goncharov N (2016) Flow cytometry and light scattering technique in evaluation of nutraceuticals. In: Neutraceuticals. Efficacy, safety and toxicity. Elsevier, pp 319–332Google Scholar
  29. Motais R, Garcia Romeu F, Borgese F (1987) The control of Na+/H+ exchange by molecular oxygen in trout erythrocytes. A possible role of hemoglobin as a transducer. J Gen Physiol 90:197–207CrossRefGoogle Scholar
  30. Muzyamba MC, Speake PF, Gibson JS (2000) Oxidants and regulation of K+-Cl-cotransport in equine red blood cells. Am J Phys Cell Physiol 279(4):C981–C989CrossRefGoogle Scholar
  31. Nielsen OB, Lykkeboe G, Cossins AR (1992) Oxygenation-activated K fluxes in trout red blood cells. Am J Phys Cell Physiol 263(5):C1057–C1064CrossRefGoogle Scholar
  32. Papakonstanti EA, Vardaki EA, Stournaras C (2000) Actin cytoskeleton: a signaling sensor in cell volume regulation. Cell Physiol Biochem 10:257–264CrossRefGoogle Scholar
  33. Pedersen SF, Hoffmann EK, Mills JW (2001) The cytoskeleton and cell volume regulation. Comp Biochem Physiol A Mol Integr Physiol 130:385–399CrossRefGoogle Scholar
  34. Rodriguez-Moreno PA, Tarazona JV (1994) Nitrite-induced methemoglobin formation and recovery in rainbow trout (Oncorhynchus mykiss) at high chloride concentrations. Bull Environ Contam Toxicol 53(1):113–119CrossRefGoogle Scholar
  35. Romano L, Passow H (1984) Characterization of anion transport system in trout red blood cell. Am J Phys 246:C330–C338CrossRefGoogle Scholar
  36. Strange K, Emma F, Jackson PS (1996) Cellular and molecular physiology of volume-sensitive anion channels. Am J Phys Cell Physiol 270(3):C711–C730.  https://doi.org/10.1152/ajpcell.1996.270.3.c711 CrossRefGoogle Scholar
  37. Stutzin A, Hoffmann EK (2006) Swelling-activated ion channels: functional regulation in cell-swelling, proliferation and apoptosis. Acta Physiol 187(1–2):27–42CrossRefGoogle Scholar
  38. Szabo A (1978) Kinetics of hemoglobin and transition state theory. Proc Natl Acad Sci 75:2108–2111CrossRefGoogle Scholar

Copyright information

© Springer Nature B.V. 2019

Authors and Affiliations

  1. 1.The A.O. Kovalevsky Institute of Marine Biological ResearchRussian Academy of SciencesMoscowRussia
  2. 2.Sechenov Institute of Evolutionary Physiology and BiochemistryRussian Academy of SciencesSt. PetersburgRussia
  3. 3.Department of Cytology and HistologySt. Petersburg State UniversitySt. PetersburgRussia

Personalised recommendations