Skip to content
Licensed Unlicensed Requires Authentication Published by De Gruyter October 20, 2020

Thermodynamic Characterization of Red Blood Cell Suspension and Band 3 Protein Oxy-Deoxygenating Functionality: Comparative Study

  • Francesco Farsaci , Ester Tellone EMAIL logo , Annamaria Russo , Antonio Galtieri and Silvana Ficarra

Abstract

The importance of studying storage alterations in erythrocytes is highlighted by the need to understand changes that could potentially serve to optimize the storage system. With this aim, the non-equilibrium thermodynamic theory with internal variables was introduced, and perturbing the erythrocyte samples with a harmonic electric field some functions of the theory have been determined varying in the perturbation frequency. A frequency has been noted that acts as a separator element between two states showing a different entropy production above and below this frequency. In stored red blood cells compared to fresh ones, the increase in entropy production measured shows a greater state of disorder in the latter. Further alterations have been highlighted on the surface charge density of the stored erythrocyte membrane and on the speed of anionic kinetics. All these observations highlight the image of membrane structural and functional alterations of the stored erythrocytes and lead to the elaboration of a technique able to correlate a specific perturbation frequency with the aging time of red blood cells.

References

[1] S. J. Singer and G. L. Nicolson, The fluid mosaic model of the structure of cell membranes, Science175 (1972), no. 4023, 720–731.10.1126/science.175.4023.720Search in Google Scholar

[2] D. N. Wang, Band 3 protein: Structure, flexibility and function, FEBS Lett.346 (1995), 26.10.1016/0014-5793(94)00468-4Search in Google Scholar

[3] M. Stefanovic, E. Puchulu-Campanella, G. Kodippili and P. S. Low, Oxygen regulates the band 3-ankyrin bridge in the human erythrocyte membrane, Biochem. J.449 (2013), no. 1, 143–150.10.1042/BJ20120869Search in Google Scholar

[4] B. M. Willardson, B. J. Thevenin, M. L. Harrison, W. M. Kuster, M. D. Benson and P. S. Low, Localization of the ankyrin-binding site on erythrocyte membrane protein, band 3, J. Biol. Chem.264 (1989), no. 27, 15893–15899.10.1016/S0021-9258(18)71562-7Search in Google Scholar

[5] L. H. Davis and V. Bennett, Mapping the binding sites of human erythrocyte ankyrin for the anion exchanger and spectrin, J. Biol. Chem.265 (1990), no. 18, 10589–10596.10.1016/S0021-9258(18)86987-3Search in Google Scholar

[6] J. Mohanty, E. Nagababu and J. Rifkind, Red blood cell oxidative stress impairs oxygen delivery and induces red blood cell aging, Front. Physiol.5 (2014), 84.10.3389/fphys.2014.00084Search in Google Scholar

[7] G. B. Nash and S. J. Wyard, Changes in surface area and volume measured by micropipette aspiration for erythrocytes ageing in vivo, Biorheology17 (1980), 479–484.Search in Google Scholar

[8] O. Linderkamp and H. J. Meiselman, Geometric, osmotic, and membrane mechanical properties of density-separated human red cells, Blood59 (1982), 1121–1127.10.1182/blood.V59.6.1121.1121Search in Google Scholar

[9] R. E. Waugh, M. Narla, C. W. Jackson, T. J. Mueller, T. Suzuki and G. L. Dale, Rheologic properties of senescent erythrocytes: loss of surface area and volume with red blood cell age, Blood79 (1992), 1351–1358.10.1182/blood.V79.5.1351.1351Search in Google Scholar

[10] J. Connor, C. C. Pak and A. J. Schroit, Exposure of phosphatidylserine in the outer leaflet of human red blood cells. Relationship to cell density, cell age, and clearance by mononuclear cells, J. Biol. Chem.269 (1994), 2399–2404.10.1016/S0021-9258(17)41959-4Search in Google Scholar

[11] J. A. Singer, L. K. Jennings, C. W. Jackson, M. E. Docker, M. Morrison and W. S. Walker, Erythrocyte homeostasis: antibody-mediated recognition of the senescent state by macrophages, Proc. Natl. Acad. Sci. USA83 (1986), 5498–5501.10.1073/pnas.83.15.5498Search in Google Scholar PubMed PubMed Central

[12] H. U. Lutz, F. Bussolino, R. Flepp, S. Fasler, P. Stammler, M. D. Kazatchkine, et al., Naturally occurring anti-band-3 antibodies and complement together mediate phagocytosis of oxidatively stressed human erythrocytes, Proc. Natl. Acad. Sci. USA84 (1987), 7368–7372.10.1073/pnas.84.21.7368Search in Google Scholar

[13] F. Turrini, P. Arese, J. Yuan and P. S. Low, Clustering of integral membrane proteins of the human erythrocyte membrane stimulates autologous IgG binding, complement deposition, and phagocytosis, J. Biol. Chem.266 (1991), 23611–23617.10.1016/S0021-9258(18)54327-1Search in Google Scholar

[14] A. Tinmouth, D. Fergusson, I. C. Yee, P. C. Hébert, ABLE Investigators, Canadian Critical Care Trials Group, Clinical consequences of red cell storage in the critically ill, Transfusion46 (Nov. 2006), no. 11, 2014–2027, doi:10.1111/j.1537-2995.2006.01026.x. PMID: 17076859.Search in Google Scholar

[15] L. R. Sparrow, Red blood cell storage and transfusion-related immunomodulation, Blood Transfus.8 (2010), no. 3, s26–s30.Search in Google Scholar

[16] G. A. Kluitenberg, On dielectric and magnetic relaxation phenomena and non-equilibrium thermodynamics, Physica68 (1973), no. 1, 75–82.10.1016/0031-8914(73)90131-6Search in Google Scholar

[17] G. A. Kluitenberg, On vectorial internal variables and dielectric and magnetic relaxation phenomena, Physica A109 (1981), 91–122.10.1016/0378-4371(81)90039-XSearch in Google Scholar

[18] S. R. De Groot and P. Mazur, Non-Equilibrium Thermodynamics, Dover Publication, New York, 1984.Search in Google Scholar

[19] G. A. Kluitenberg, On dielectric and magnetic relaxation phenomena and vectorial internal degrees, Physica A87 (1977), no. 2, 302–330.10.1016/0378-4371(77)90019-XSearch in Google Scholar

[20] F. Farsaci, S. Ficarra, A. Russo, A. Galtieri and E. Tellone, Dielectric properties of human diabetic blood: thermodynamic characterization and new prospective for alternative diagnostic techniques, J. Adv. Dielectr.5 (2015), 3.10.1142/S2010135X15500216Search in Google Scholar

[21] F. Farsaci and P. Rogolino, An alternative dielectric model for low and high frequencies: A non-equilibrium thermodynamic approach, J. Non-Equilib. Thermodyn.37 (2012), 27–41.10.1515/jnetdy.2011.024Search in Google Scholar

[22] F. Farsaci, E. Tellone, M. Cavallaro, A. Russo and S. Ficarra, Low frequency dielectric characteristics of human blood: a non-equilibrium thermodynamic approach, J. Mol. Liq.188 (2013), 113–119.10.1016/j.molliq.2013.09.033Search in Google Scholar

[23] F. Farsaci, A. Russo, S. Ficarra and E. Tellone, Dielectric properties of human normal and malignant liver tissue: a non-equilibrium thermodynamics approach, Open Access Libr. J.2 (2015), 1395.10.4236/oalib.1101395Search in Google Scholar

[24] F. Farsaci, S. Ficarra, A. Russo, A. Galtieri and E. Tellone, On evaluation of electric conductivity by mean of non-equilibrium thermodynamic approach with internal variables. An application to human erythrocyte suspension for metabolic characterizations, J. Mol. Liq.224 (2016), 1181–1188.10.1016/j.molliq.2016.10.096Search in Google Scholar

[25] F. Farsaci, E. Tellone, A. Galtieri, A. Russo and S. Ficarra, Evaluation of the human blood entropy production: a new thermodynamic approach, J. Ultrasound19 (2016), 265–273.10.1007/s40477-016-0210-9Search in Google Scholar PubMed PubMed Central

[26] F. Farsaci, E. Tellone, A. Russo, A. Galtieri and S. Ficarra, Rheological properties of human blood in the network of non-equilibrium thermodynamic with internal variables by means of ultrasound wave perturbation, J. Mol. Liq.231 (2017), 206–212.10.1016/j.molliq.2017.02.001Search in Google Scholar

[27] F. Farsaci, S. Ficarra, A. Galtieri and E. Tellone, New non-equilibrium thermodynamic fractional visco-inelastic model to predict experimentally inaccessible processes and investigate pathophysiological cellular structures, Fluids2 (2017), 59.10.3390/fluids2040059Search in Google Scholar

[28] F. Farsaci, E. Tellone, A. Galtieri and S. Ficarra, Molecular characterization of a peculiar blood clot fluidification by theoretical thermodynamic models and entropy production study, J. Mol. Liq.265 (2018), 457–462.10.1016/j.molliq.2018.06.032Search in Google Scholar

[29] F. Farsaci, E. Tellone, A. Galtieri and S. Ficarra, Expanding the repertoire of dielectric fractional models: a comprehensive development and functional applications to predict metabolic alterations in experimentally-inaccessible cells or tissues, Fluids3 (2018), 9.10.3390/fluids3010009Search in Google Scholar

[30] F. Farsaci, E. Tellone, A. Galtieri and S. Ficarra, Is a dangerous blood clot formation a reversible process? Introduction of new characteristic parameter for thermodynamic clot blood characterization: possible molecular mechanisms and pathophysiologic applications, J. Mol. Liq.262 (2018), 345–353.10.1016/j.molliq.2018.04.071Search in Google Scholar

[31] F. Farsaci, E. Tellone, A. Galtieri and S. Ficarra, Electromagnetic waves propagation in normal and pathological hemoglobins: Thermodynamic comparative study of the influence of the relative macromolecular variability, J. Mol. Liq.291 (2019), 111319.10.1016/j.molliq.2019.111319Search in Google Scholar

[32] F. Farsaci, E. Tellone, A. Galtieri and S. Ficarra, A new model for thermodynamic characterization of hemoglobin, Fluids4 (2019), 135.10.3390/fluids4030135Search in Google Scholar

[33] F. Farsaci, E. Tellone, A. Galtieri and S. Ficarra, Phenomenological approach on electromagnetic waves propagation in normal and diabetic blood, influence of the relative macromolecular structures, J. Mol. Liq.274 (2019), 577–583.10.1016/j.molliq.2018.11.003Search in Google Scholar

[34] F. Farsaci, E. Tellone, A. Galtieri and S. Ficarra, A new model with internal variables for theoretical thermodynamic characterization of hemoglobin: Entropy determination and comparative study, J. Mol. Liq.279 (2019), 632–639.10.1016/j.molliq.2019.01.161Search in Google Scholar

[35] F. Farsaci, E. Tellone, A. Galtieri and S. Ficarra, A new model for thermodynamic characterization of hemoglobin, Fluids4 (2019), 135.10.3390/fluids4030135Search in Google Scholar

[36] E. Tellone, S. Ficarra, B. Giardina, R. Scatena, A. Russo, M. E. Clementi, et al., Oxidative effects of Gemfibrozil on anion influx and metabolism in normal and beta-thalassaemic erythrocytes. Physiological Implications, J. Membr. Biol.224 (2008), no.  1-3, 1–8.10.1007/s00232-008-9122-8Search in Google Scholar

[37] W. G. Zijlstra, A. Buursma and W. P. Meeuwsen-Van Der Roest, Absorption spectra of human fetal and adult oxyhemoglobin, de-oxyhemoglobin, carboxyhemoglobin and methemoglobin, Clin. Chem.37 (1991), no. 9, 1633–1638.10.1093/clinchem/37.9.1633Search in Google Scholar

[38] R. J. Labotka, Measurement of intracellular pH and deoxyhemoglobin concentration in deoxygenated erythrocytes by phosphorus-31 nuclear magnetic resonance, Biochemistry23 (1984), no. 23, 5549–5555.10.1021/bi00318a026Search in Google Scholar

[39] A. Russo, E. Tellone, S. Ficarra, B. Giardina, E. Bellocco, G. Lagana, et al., Band 3 protein function in teleost fish erythrocytes: effect of oxygenation-deoxygenation, Physiol. Res.57 (2008), no. 1, 49–54.10.33549/physiolres.931178Search in Google Scholar

[40] L. Romano, D. Peritore, E. Simone, A. Sidoti, F. Trischitta and P. Romano, Cell. Mol. Biol.44 (1998), 351–355.Search in Google Scholar

[41] M. David, E. Levy, Y. Feldman, P. B. Ishai, O. Zelig, S. Yedgar, et al., The dielectric spectroscopy of human red blood cells: the differentiation of old from fresh cells, Physiol. Meas.38 (2017), 1335.10.1088/1361-6579/aa707aSearch in Google Scholar

[42] S. Abdalla, Low frequency dielectric properties of human blood, IEEE Trans. Nanobiosci.10 (2011), no. 2, 113.10.1109/TNB.2011.2159734Search in Google Scholar

[43] Y. X. Huang, Z. J. Wu, J. Mehrishi, B. T. Huang, X. Y. Chen, X. J. Zheng, et al., Human red blood cell aging: correlative changes in surface charge and cell properties, J. Cell. Mol. Med.15 (2011), no. 12, 2634–2642.10.1111/j.1582-4934.2011.01310.xSearch in Google Scholar

[44] R. Moriyama, C. R. Lombardo, R. F. Workman and P. S. Low, Regulation of linkages between the erythrocyte membrane and its skeleton by 2,3-diphosphoglycerate, J. Biol. Chem.268 (1993), 10990–10996.10.1016/S0021-9258(18)82083-XSearch in Google Scholar

[45] A. Galtieri, E. Tellone, L. Romano, F. Misiti, E. Bellocco, S. Ficarra, et al., Band-3 protein function in human erythrocytes: effect of oxygenation-deoxygenation, Biochim. Biophys. Acta1564 (2002), 214–218.10.1016/S0005-2736(02)00454-6Search in Google Scholar

[46] A. Sommerfeld, Electrodynamics: Lectures on Theoretical Physics, Vol. III, Hardcover, 1956.Search in Google Scholar

Received: 2020-02-05
Revised: 2020-07-18
Accepted: 2020-10-02
Published Online: 2020-10-20
Published in Print: 2021-04-26

© 2021 Walter de Gruyter GmbH, Berlin/Boston

Downloaded on 24.4.2024 from https://www.degruyter.com/document/doi/10.1515/jnet-2020-0009/html
Scroll to top button