Potential role of cytoplasmic protein binding to erythrocyte membrane in counteracting oxidative and metabolic stress

  • O. I. Dotsenko Vasyl’ Stus Donetsk National University
  • I. V. Mykutska Vasyl’ Stus Donetsk National University
  • G. V. Taradina Vasyl’ Stus Donetsk National University
  • Z. O. Boiarska Vasyl’ Stus Donetsk National University
Keywords: oxidative stress; catalase; superoxide dismutase; ascorbate; copper ions; ligand forms of hemoglobin; membrane-bound hemoglobin.

Abstract

The ability of protein to reversibly bind with membrane components is considered to be one of the oldest mechanisms of cell response to external stimuli. Erythrocytes have a well-developed mechanism of an adaptive response involving sorption-desorption processes, e.g. interactions of key glycolytic enzymes and hemoglobin with band 3 protein. A few publications have shown that under oxidative stress, cytoplasmic enzymes such as catalase, glutathione peroxidase and рeroxiredoxin bind to the erythrocyte membrane. The present work is a continuation of research in this direction to determine the causes and consequences of the interaction of cytoplasmic proteins with the membrane under conditions of oxidative stress and different glucose content. Human erythrocytes were incubated for five hours at 20 °C in an oxidizing medium of AscH – 1 · 10–4 M, Cu2+– 5 · 10–6 M with different glucose content (0–8 mM). Dynamic changes in the accumulation of membrane-bound hemoglobin, the distribution of ligand forms of hemoglobin in the cytoplasmic and membrane-bound fractions, the activity of membrane-associated and cytoplasmic forms of Cu/Zn superoxide dismutase (SOD1) and catalase, H2O2 content in extracellular and intracellular media were recorded. It was shown that binding of catalase and SOD1 to the erythrocyte membrane is initiated by oxidative stress and is a physiological function aimed at complete inactivation of extracellular and H2O2 and protection against their entry into the cell. It was shown that under conditions of glucose depletion and oxidative loading, catalase and SOD1 bind to the erythrocyte membrane, leading to inactivation of these enzymes. Membrane-bound hemoglobin was higher in cells incubated under these conditions than in glucose experiments. Glucose introduced into the incubation medium in an amount 4–8 mM causes complete binding of SOD1 to the membrane of erythrocytes, by involving it in the processes of casein kinase stabilization and glycolytic fluxes regulation. With mild oxidation, the amount of hemoglobin bound to the membrane does not change, indicating the presence of certain binding sites for hemoglobin with membrane proteins. We show that the activity of membrane-bound SOD1 along with the content of ligand forms in the composition of membrane-bound hemoglobin are informative indicators of the metabolic and redox state of erythrocytes.

References

Allen, D. W., Cadman, S., McCann, S. R., & Finkel, B. (1977). Increased membrane binding of erythrocyte catalase in hereditary spherocytosis and in metabolically stressed normal cells. Blood, 49(1), 113–123.

Andreyeva, A. Y., Soldatov, A. A., Krivchenko, A. I., Mindukshev, I. V., & Gambaryan, S. (2019). Hemoglobin deoxygenation and methemoglobinemia prevent regulatory volume decrease in crucian carp (Carassius carassius) red blood cells. Fish Physiology and Biochemistry, 45, 1933–1940.

Attia, A. M. M., Aboulthana, W. M., Hassan, G. M., & Aboelezz, E. (2020). Assessment of absorbed dose of gamma rays using the simultaneous determination of inactive hemoglobin derivatives as a biological dosimeter. Radiation and Environmental Biophysics, 59(1), 131–144.

Attia, A. M. M., Ibrahim, F. A. A., Abd El-Latif, N. A., Aziz, S. W., Moussa, S. A. A. (2015). Biophysical study on conformational stability against autoxidation of oxyhemoglobin and erythrocytes oxidative status in humans and rats. Wulfenia Journal, 22(12), 264–281.

Aviram, I., & Shaklai, N. (1981). The association of human erythrocyte catalase with the cell membrane. Archives of Biochemistry and Biophysics, 212(2), 329–337.

Bayer, S. B., Low, F. M., Hampton, M. B., & Winterbourn, C. C. (2016). Interactions between peroxiredoxin 2, hemichrome and the erythrocyte membrane. Free Radical Research, 50(12), 1329–1339.

Benesch, R. E., Benesch, R., & Yung, S. (1973). Equations for the spectrophotometric analysis of hemoglobin mixtures. Analytical Biochemistry, 55(1), 245–248.

Bonaventura, J., Schroeder, W. A., & Fang, S. (1972). Human erythrocyte catalase: An improved method of isolation and a reevaluation of reported properties. Archives of Biochemistry and Biophysics, 150, 606–617.

Bou, R., Codony, R., Tres, A., Decker, E. A., & Guardiola, F. (2008). Determination of hydroperoxides in foods and biological samples by the ferrous oxidation–xylenol orange method: A review of the factors that influence the method’s performance. Analytical Biochemistry, 377(1), 1–15.

Boulet, C., Doerig, C. D., & Carvalho, T. G. (2018). Manipulating eryptosis of human red blood cells: A novel antimalarial strategy? Frontiers in Cellular and Infection Microbiology, 8, 419.

Bychkova, V. E., Basova, L. V., & Balobanov, V. A. (2014). How membrane surface affects protein structure. Biochemistry (Moscow), 79(13), 1483–1514.

Carelli-Alinovi, C., & Misiti, F. (2017). Erythrocytes as potential link between diabetes and Alzheimer’s disease. Frontiers in Aging Neuroscience, 9, 276.

Cheng, S. Y., Chou, G., Buie, C., Vaughn, M. W., Compton, C., & Cheng, K. H. (2016). Maximally asymmetric transbilayer distribution of anionic lipids alters the structure and interaction with lipids of an amyloidogenic protein dimer bound to the membrane surface. Chemistry and Physics of Lipids, 196, 33–51.

Chu, H., McKenna, M. M., Krump, N. A., Zheng, S., Mendelsohn, L., Thein, S. L., Garrett, L. J., Bodine, D. M., & Low, P. S. (2016). Reversible binding of hemoglobin to band 3 constitutes the molecular switch that mediates O2 regulation of erythrocyte properties. Blood, 128(23), 2708–2716.

Cortese-Krott, M. M., & Shiva, S. (2019). The redox physiology of red blood cells and platelets: Implications for their interactions and potential use as systemic biomarkers. Current Opinion in Physiology, 9, 56–66.

D’Alessandro, A., Kriebardis, A. G., Rinalducci, S., Antonelou, M. H., Hansen, K. C., Papassideri, I. S., & Zolla, L. (2015). An update on red blood cell storage lesions, as gleaned through biochemistry and omics technologies. Transfusion, 55(1), 205–219.

Dotsenko, O. I., Dragushenko, O. O., & Dotsenko, V. A. (2010). Doslidzhennia prooksydantnoi ta tsytotoksychnoi dii system Cu2+–AscH, Cu2+–AscH–o-phenanthroline [The investigation of the action of prooxidant and cytotoxic systems Cu2+–AscH, Cu2+–AscH–o-phenanthroline]. Dosiahnennia Biolohii ta Medytsyny, 15, 1–7 (in Ukrainian).

Dotsenko, O. I., Troshchynskaуа, Y. A., & Konyukhova, N. R. (2012). Izuchenie processov obrazovanija membranosvjazannogo gemoglobina v eritrocitah pod dejstviem nizkochastotnoj vibracii [Studying of processes of formation of membrane-bound hemoglobin in erythrocytes under the influence of low-frequency vibration]. Problems of Ecology and Nature Protection of Techogen Region, 12, 274–280 (in Russian).

Grzelak, A., Kruszewski, M., Macierzyńska, E., Piotrowski, Ł., Pułaski, Ł., Rychlik, B., & Bartosz, G. (2009). The effects of superoxide dismutase knockout on the oxidative stress parameters and survival of mouse erythrocytes. Cellular and Molecular Biology Letters, 14(1), 23–34.

Iakovenko, I. N., Zhirnov, V. V., Kozachenko, A. P., Shablykin, O. V., & Brovarets, V. S. (2012). Uchast’ proteinkinazy SK2 v reguljaciji aktyvnosti redoks-systemy plazmatychnyh membran erytrocytiv ljudyny: Vidnosnyj vnesok Ca2+-zalezhnyh ta Ca2+-nezalezhnyh mehanizmiv jiji aktyvaciji [Participation of proteinkinase CK2 in regulation of human erythrocytes plasma membrane redox system activity: Relative contribution of Са2+-dependent and Са2+-independent mechanisms of its activation]. The Ukrainian Biochemical Journal, 84(5), 55–60 (in Ukrainian).

Kosmachevskaya, O. V., Nasybullina, E. I., Topunov, A. F., & Blindar, V. N. (2019). Binding of erythrocyte hemoglobin to the membrane to realize signal-regulatory function (review). Applied Biochemistry and Microbiology, 55 (2), 83–98.

Kuhn, V., Diederich, L., Keller, T. C. S. IV, Kramer, C. M., Lückstädt, W., Panknin, C., Suvorava, T., Isakson, B. E., Kelm, M., & Cortese-Krott, M. M. (2017). Red blood cell function and dysfunction: Redox regulation, nitric oxide metabolism, anemia. Antioxidants and Redox Signaling, 26(13), 718–742.

Lin, Y.-S., Wu, C.-W., Lin, T.-S., Chen, N.-Y., Wu, D.-C., & Chen, H.-J. C. (2020). Analysis of oxidative and advanced oxidative modifications in hemoglobin of oral cancer patients by mass spectrometry. Analytical Chemistry, 92(1), 724–731.

Melo, D., Rocha, S., Coimbra, S., & Santos Silva, A. (2019). Interplay between erythrocyte peroxidases and membrane. In: Tombak, A. (Ed.). Erythrocyte. IntechOpen, London. Pp. 486.

Puchulu-Campanella, E., Chu, H., Anstee, D. J., Galan, J. A., Tao, W. A., & Low, P. S. (2013). Identification of the components of a glycolytic enzyme metabolon on the human red blood cell membrane. The Journal of Biological Chemistry, 288(2), 848–858.

Ratanasopa, K., Strader, M. B., Alayash, A. I., & Bulow, L. (2015). Dissection of the radical reactions linked to fetal hemoglobin reveals enhanced pseudoperoxidase activity. Frontiers in Physiology, 6, 39.

Reddi, A. R., & Culotta, V. C. (2013). SOD1 integrates signals from oxygen and glucose to repress respiration. Cell, 152(1–2), 224–235.

Rifkind, J. M., & Nagababu, E. (2013). Hemoglobin redox reactions and red blood cell aging. Antioxidants and Redox Signaling, 18(17), 2274–2283.

Rocha, S., Gomes, D., Lima, M., Bronze-da-Rocha, E., & Santos-Silva, A. (2015). Peroxiredoxin 2, glutathione peroxidase, and catalase in the cytosol and membrane of erythrocytes under H2O2-induced oxidative stress. Free Radical Research, 49(8), 990–1003.

Rocha, S., Rocha-Pereira, P., Cleto, E., Ferreira, F., Belo, L., & Santos-Silva, A. (2019). Linkage of typically cytosolic peroxidases to erythrocyte membrane – A possible mechanism of protection in hereditary spherocytosis. Biochimica et Biophysica Acta (BBA) – Biomembranes, 1862(3), 183172.

Sega, M. F., Chu, H., Christian, J. A., & Low, P. S. (2015). Fluorescence assay of the interaction between hemoglobin and the cytoplasmic domain of erythrocyte membrane band 3. Blood Cells, Molecules, and Diseases, 55(3), 266–271.

Sidorenko, S. V., Ziganshin, R. H., Luneva, O. G., Deev, L. I., Alekseeva, N. V., Maksimov, G. V., & Orlov, S. N. (2018). Proteomics-based identification of hypoxia-sensitive membrane-bound proteins in rat erythrocytes. Journal of Proteomics, 184, 25–33.

Sirota, T. V. (1999). Novyj podhod v issledovanii processa autookislenija adrenalina i ispol’zovanie ego dlja izmerenija aktivnosti superoksiddismutazy [A new approach to the investigation of adrenaline autooxidation and its application for determination of superoxide dismutase activity]. Voprosy Medicinskoj Himii, 45(3), 263–272 (in Russian).

Taradina, G. V., & Dotsenko, O. I. (2011). Oligomernye intermediaty katalazy v rastvore pri dejstvii nizkochastotnoj vibracii [Оligomeric intermediates of catalases in a solution at influence of low-frequency vibration]. Problems of Ecology and Nature Protection of Techogen Region, 11, 323–329 (in Russian).

Tharaux, P.-L. (2019). Posttranslational modifications of sickle hemoglobin in microparticles may promote injury. Kidney International, 95(6), 1289–1291.

Tiwari, M. K., Hägglund, P. M., Møller, I. M., Davies, M. J., & Bjerrum, M. J. (2019). Copper ion/H2O2 oxidation of Cu/Zn-superoxide dismutase: Implications for enzymatic activity and antioxidant action. Redox Biology, 26, 101262.

Tu, H., Wang, Y., Li, H., Brinster, L. R., & Levine, M. (2017). Chemical transport knockout for oxidized vitamin C, dehydroascorbic acid, reveals its functions in vivo. EBioMedicine, 23, 125–135.

Ugurel, E., Piskin, S., Aksu, A. C., Eser, A., & Yalcin, O. (2020). From experiments to simulation: Shear-induced responses of red blood cells to different oxygen saturation levels. Frontiers in Physiology, 10, 1559.

Wang, C. C., Tao, M., Wei, T., & Low, P. S. (1997). Identification of the major casein kinase I phosphorylation sites on erythrocyte band 3. Blood, 89(8), 3019–3024.

Wang, Y., Branicky, R., Noë, A., & Hekimi, S. (2018). Superoxide dismutases: Dual roles in controlling ROS damage and regulating ROS signaling. The Journal of Cell Biology, 217(6), 1915–1928.

Welbourn, E. M., Wilson, M. T., Yusof, A., Metodiev, M. V., & Cooper, C. E. (2017). The mechanism of formation, structure and physiological relevance of covalent hemoglobin attachment to the erythrocyte membrane. Free Radical Biology and Medicine, 103, 95–106.

Wolff, S. P. (1994). Ferrous ion oxidation in presence of ferric ion indicator xylenol orange for measurement of hydroperoxides. Methods in Enzymology, 233, 182–189.

Wolff, S. P., & Dean, R. T. (1987). Monosaccharide autoxidation: A potential source of oxidative stress in diabetes? Bioelectrochemistry and Bioenergetics, 18, 283–293.

Zhou, S., Giannetto, M., DeCourcey, J., Kang, H., Kang, N., Li, Y., Zheng, S., Zhao, H., Simmons, W. R., Wei, H. S., Bodine, D. M., Low, P. S., Nedergaard, M., & Wan, J. (2019). Oxygen tension-mediated erythrocyte membrane interactions regulate cerebral capillary hyperemia. Science Advances, 5(5), eaaw4466.

Published
2020-08-15
How to Cite
Dotsenko, O. I., Mykutska, I. V., Taradina, G. V., & Boiarska, Z. O. (2020). Potential role of cytoplasmic protein binding to erythrocyte membrane in counteracting oxidative and metabolic stress . Regulatory Mechanisms in Biosystems, 11(3), 455–462. https://doi.org/10.15421/022070