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Differential dielectroscopic data on the relation of erythrocyte membrane skeleton to erythrocyte deformability and flicker

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Abstract

Two dielectric relaxations, βsp (1.5 MHz) and γ1sp (7 MHz), have been detected on spectrin-based membrane skeleton (MS) of red blood cells (RBCs) using the plot of admittance changes at the spectrin denaturation temperature (Ivanov and Paarvanova in Bioelectrochemistry 110: 59–68, 2016, Electrochim Acta 317: 289–300, 2019a). In this study, we treated RBCs and RBC ghost membranes with agents that make membranes rigid and suppress membrane flicker, and studied the effect on βsp and γ1sp relaxations. Diamide (diazene dicarboxylic acid bis-(N,N-dimethylamide)) (up to 0.85 mM), taurine mustard (tris(2-chloroethyl)amine) (up to 2 mM), known to specifically cross-link and stiffen spectrin, and glutaraldehyde (up to 0.044%) all inhibited the relaxations in RBC ghost membranes. Similar inhibition was obtained resealing RBC ghost membranes with 2,3-diphosphoglicerate (up to 15 mM), binding WGA (wheat germ agglutinin) (up to 0.025 mg/ml) to exofacial aspect of RBCs, incubating RBCs in hypotonic (200 mOsm) and hypertonic (600–900 mOsm) media and depleting RBCs of ATP. By contrast, concanavalin A (1 mg/ml) and DIDS (4,4′-diiso-thiocyanato stilbene-2,2′-disulfonic acid) (75 μM, pH 8.2), both known to bind specifically band 3 integral protein of RBCs without effect on RBC membrane rigidity, did not affect the relaxations. We conclude there might be a relation between the strength of dielectric relaxations on MS spectrin and the deformability and flicker of RBC membrane.

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Abbreviations

RBC:

Red blood cell

MS:

Spectrin-based membrane skeleton

f :

Frequency of alternating electric field

f c :

Characteristic frequency of dielectric relaxation

f βsp :

Characteristic frequency of βsp-relaxation on MS spectrin

f γ1sp :

Characteristic frequency of γ1sp relaxation on MS spectrin

T A :

Denaturation temperature of RBC spectrin; diamide (diazene dicarboxylic acid bis-(N,N-dimethylamide)); taurine mustard (taumustine), 2-[bis(2-chloroethyl)amino]ethanesulfonic acid

WGA:

Wheat germ agglutinin

2,3-DPG:

2,3-Diphosphoglycerate

DIDS:

4,4′-Diiso-thiocyanato stilbene-2,2′-disulfonic acid

ATP:

Adenosine 5′-triphosphate

References

  • Almizraq R, Tchir JDR, Acker J, Holovati JL (2012) The effects of biochemical rejuvenation on red blood cell microvesiculation, phosphatidylserine and CD47 expression during hypothermic storage. Cryobiology 65(3):349–350

    Article  Google Scholar 

  • Anderson RA, Lovrein R (1981) Lectins utilize glycophorin in cytoskeletal control of human erythrocyte discocyte-echinocyte equilibria. Prog Clin Biol Res 56:207–229

    CAS  PubMed  Google Scholar 

  • Anong WA, Franco T, Chu H, Weis TL, Devlin EE, Bodine DM, An X, Mohandas N, Low PS (2009) Adducin forms a bridge between the erythrocyte membrane and its cytoskeleton and regulates membrane cohesion. Blood 114:1904–1912

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ballas SK, Mohandas N, Marton LJ, Shohet SB (1983) Cell Biology Stabilization of erythrocyte membranes by polyamines. Proc Nati Acad Sci USA 80:1942–1946

    Article  CAS  Google Scholar 

  • Bao JZ, Davis CC, Swicord ML (1994) Microwave dielectric measurements of erythrocyte suspensions. Biophys J 66:2173–2180

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bennett V, Baines AJ (2001) Spectrin and ankyrin-based pathways: metazoan inventions for integrating cells into tissues. Physiol Rev 81:1353–1392

    Article  CAS  PubMed  Google Scholar 

  • Bennett V, Stenbuck PJ (1979) The membrane attachment protein for spectrin is associated with band 3 in human erythrocyte membranes. Nature (London) 280:468–473

    Article  CAS  Google Scholar 

  • Berezina TL, Zaets SB, Morgan C, Spillert CR, Kamiyama M, Spolarics Z, Deitch EA, Machiedo GW (2002) Influence of storage on red blood cell rheological properties. J Surg Res 102:6–12

    Article  CAS  PubMed  Google Scholar 

  • Betz T, Lenz M, Joanny J-F, Sykes C (2009) ATP-dependent mechanics of red blood cells. PNAS 106(36):15320–15325

    Article  CAS  PubMed  Google Scholar 

  • Bitler A, Barbul A, Korenstein R (1999) Detection of movement at the erythrocyte’s edge by scanning phase contrast microscopy. J Microscopy 193:171–178

    Article  CAS  Google Scholar 

  • Blanc L, Salomao M, Guo X, An X, Gratzer W, Mohandas N (2010) Control of erythrocyte membrane-skeletal cohesion by the spectrin-membrane linkage. Biochemistry 49:4516–4523

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Blowers R, Clarkson EM, Maizels M (1951) Flicker phenomenon in human erythrocytes. J Physiol (London) 113:228–239

    Article  CAS  Google Scholar 

  • Boivin P (1988) Role of the phosphorylation of red blood cell membrane proteins. Biochem J 256:689–695

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Bowmann RJ, Levitt DG (1977) Polyol permeability of the human red cell: Interpretation of glucose transport in terms of a pore. Biochim Biophys Acta 466:68–83

    Article  Google Scholar 

  • Brandts JF, Erickson L, Lysko K, Schwartz AT, Taverna RD (1977) Calorimetric studies of the structural transitions of the human erythrocyte membrane. The involvement of spectrin in the A transition. Biochemistry 16:3450–3454

    Article  CAS  PubMed  Google Scholar 

  • Brochard F, Lennon JF (1975) Frequency spectrum of the flicker phenomenon in erythrocytes. J Phys Fr 36:1035–1047

    Article  Google Scholar 

  • Browicz V (1890) Weitere beobachtunger uber bewegungsphanomene an roten blutkorperchen in pathologischen zustanden. Zbl Med Wiss 28:625–627

    Google Scholar 

  • Cabantchik ZI, Greger R (1992) Chemical probes for anion transporters of mammalian cell membranes. Am J Physiol 262:803–827

    Article  Google Scholar 

  • Chasis JA, Mohandas N (1986) Erythrocyte membrane deformability and stability: two distinct membrane properties that are independently regulated by skeletal protein associations. J Cell Biol 103:343–350

    Article  CAS  PubMed  Google Scholar 

  • Chasis JA, Mohandas N, Shohet SB (1985) Erythrocyte membrane rigidity induced by glycophorin A-ligand Interaction. evidence for a ligand-induced association between glycophorin A and skeletal proteins. J Clin Invest 75:1919–1926

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Chasis JA, Reid ME, Jensen RH, Mohandas N (1988) Signal transduction by glycophorin A: role of extracellular and cytoplasmic domains in a modulatable process. J Cell Biol 107:1351–1357

    Article  CAS  PubMed  Google Scholar 

  • Cluitmans J, Gevi F, Siciliano A, Matte A, Leal JKF, De Franceschi L, Zolla L, Brock R, Adjobo-Hermans MJW, Bosman G (2016) Red blood cell homeostasis: pharmacological interventions to explore biochemical, morphological and mechanical properties. Front Mol Biosci 280:811–814

    Google Scholar 

  • De Oliveira S, Saldanha C (2010) An overview about erythrocyte membrane. Clin Hemorheol Microcirc 44:63–74

    Article  PubMed  Google Scholar 

  • Eskelinen S, Coakley WT, Tilley D (1985) Thermal denaturation of the erythrocyte cytoskeleton alters the morphological changes associated with osmotic swelling. J Therm Biol 10:187–190

    Article  Google Scholar 

  • Evans J, Gratzer W, Mohandas N, Parker K, Sleep J (2008) Fluctuations of the red blood cell membrane: relation to mechanical properties and lack of ATP dependence. Biophys J 94:4134–4144

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Fischer TM, Haest CWM, Stöhr M, Kamp D, Deuticke B (1978) Selective alteration of erythrocyte deformability by SH-reagents. Evidence for an involvement of spectrin in membrane shear elasticity. Biochim et Biophys Acta (BBA) 510(2):270–282

    Article  CAS  Google Scholar 

  • Forsyth AM, Wan J, Ristenpart WD, Stone HA (2010) The dynamic behavior of chemically “Stiffened” red blood cells in microchannel flows. Microvasc Res 80(1):37–43

    Article  CAS  PubMed  Google Scholar 

  • Fricke K, Sackmann E (1984) Variation of frequency spectrum of the erythrocyte flickering caused by aging, osmolarity, temperature and pathological changes. Biochim Biophys Acta 803(3):145–152

    Article  CAS  PubMed  Google Scholar 

  • Fricke K, Wirthensohn K, Laxhuber R, Sackmann E (1986) Flicker spectroscopy of erythrocytes: a sensitive method to study subtle changes of membrane bending stiffness. Eur Biophys J 14:67–81

    Article  CAS  PubMed  Google Scholar 

  • Fung LWM, Kalaw BO, Hatfield RM, Dias MN (1996) Erythrocyte spectrin maintains its segmental motions on oxidation: a spin-label EPR Study. Biophys J 70:841–851

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gimsa J (2017) Electric and magnetic fields in cells and tissues. In: Hashmi S (ed) Reference module in materials science and materials engineering. Elsevier, Oxford, pp 1–10

    Google Scholar 

  • Glomski CA, Pica A (2011) The avian erythrocyte: Its Phylogenic Odyssey. CRC Press, Science Publishers, Tylor and Francis Group, London, pp 23–31

    Google Scholar 

  • Gokhale SM, Mehta NG (1987) Concanavalin A binding to human erythrocytes leads to alterations in properties of the membrane skeleton. Biochem J 241:521–525

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Gov NS (2007) Active elastic network: cytoskeleton of the red blood cell. Phys Rev E 75(1Pt1):011921

    Article  Google Scholar 

  • Grinfel’dt MG, Krol AI, Levin SV (1989) The suppression of rapid local surface oscillations in human erythrocytes slows and weakens their adhesion to glass. Tsitologiia 31(11):1395–1397

    CAS  PubMed  Google Scholar 

  • Humpert C, Baumann M (2003) Local membrane curvature affects spontaneous membrane fluctuation characteristics. Mol Membr Biol 20:155–162

    Article  CAS  PubMed  Google Scholar 

  • Ivanov IT, Gadjeva V (2000) Influence of some DNA-alkylating drugs on thermal stability, acid and osmotic resistance of the membrane of whole human erythrocytes and their ghosts. Pharmazie 55(9):672–677

    CAS  PubMed  Google Scholar 

  • Ivanov IT, Paarvanova BK (2016) Dielectric relaxations on erythrocyte membrane as revealed by spectrin denaturation. Bioelectrochemistry 110:59–68

    Article  CAS  PubMed  Google Scholar 

  • Ivanov IT, Paarvanova BK (2019a) Thermal dielectroscopy study on the vertical and horizontal interactions in erythrocyte sub-membrane skeleton. Electrochim Acta 317:289–300

    Article  CAS  Google Scholar 

  • Ivanov IT, Paarvanova BK (2019b) Effect of permeant cryoprotectants on membrane skeleton of erythrocytes. Probl Cryobiol Cryomed 29:237–245

    Article  Google Scholar 

  • Ivanov IT, Popov BK (1993) Do changes in cell shape affect suspension conductivity? Gen Physiol Biophys 12(4):311–315

    CAS  PubMed  Google Scholar 

  • Ivanov IT, Paarvanova BK, Ivanov V, Smuda K, Bäumler H, Georgieva R (2017) Effects of heat and freeze on isolated erythrocyte submembrane skeletons. Gen Physiol Biophys 36:155–165

    Article  CAS  PubMed  Google Scholar 

  • Ivanov IT, Paarvanova BK, Tacheva BB, Slavov T (2020) Species-dependent variations in the dielectric activity of membrane skeleton of erythrocytes. Gen Physiol Biophys 39(6):505–518

    Article  PubMed  Google Scholar 

  • Jennings ML, Passow H (1979) Anion transport across the erythrocyte membrane, in situ proteolysis of band 3 protein, and cross-linking of proteolytic fragments by 4,4’-diisothiocyano dihydrostilbene-2,2’-disulfonate. Biochim Biophys Acta 554:498–519

    Article  CAS  PubMed  Google Scholar 

  • Kapus A, Janmey P (2013) Plasma membrane-cortical cytoskeleton interactions: a cell biology approach with biophysical considerations. Compr Physiol 3:1231–1281

    Article  PubMed  Google Scholar 

  • Klösgen B, Rümenapp C, Gleich B (2011) Bioimpedance spectroscopy. In: Choi S (ed) BetaSys: systems biology of regulated exocytosis in pancreatic β-cells. Springer Publishing Company, New York, pp 241–271

    Chapter  Google Scholar 

  • Kononenko VL (2009) Flicker in erythrocytes II. Results of experimental studies. Biochemistry (Moscow) 4:372–387

    Google Scholar 

  • Krol AY, Grinfeldt MG, Smilgavichus AD, Levin SV (1989) Fast local oscillations of human erythrocyte surface. Tsitologiya Rus 31:563–567

    Google Scholar 

  • Krol AY, Grinfeldt MG, Levin SV, Smilgavichus AD (1990a) Local mechanical oscillations of the cell surface within the range 0.2–30 Hz. Eur Biophys J 19(2):93–99

    Article  PubMed  Google Scholar 

  • Krol AI, Grinfel’dt MG, Smil’giavichius AD, Levin SV (1990b) Rapid local oscillations of the surface of the human erythrocyte. Tsitologiia 31(5):563–568

    Google Scholar 

  • Levin S, Korenstein R (1991) Membrane fluctuations in erythrocytes are linked to MgATP-dependent dynamic assembly of the membrane skeleton. Biophys J 60:733–737

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Li J, Lykotrafitis G, Dao M, Suresh S (2007) Cytoskeletal dynamics of human erythrocyte. Proc Natl Acad Sci USA 104(12):4937–4942

    Article  CAS  PubMed  Google Scholar 

  • Liu SC, Derick LH, Agre P, Palek J (1990) Alteration of the erythrocyte membrane skeletal ultrastructure in hereditary spherocytosis, hereditary elliptocytosis, and pyropoikilocytosis. Blood 76:198–205

    Article  CAS  PubMed  Google Scholar 

  • Manno S, Takakuwa Y, Mohandas N (2005) Modulation of erythrocyte membrane mechanical function by protein 4.1 phosphorylation. J Biol Chem 280:7581–7587

    Article  CAS  PubMed  Google Scholar 

  • Marchesi VT (2008) The relevance of research on red cell membranes to the understanding of complex human disease: a personal perspective. Annu Rev Pathol 3:1–9

    Article  CAS  PubMed  Google Scholar 

  • Martinsen OG, Grimnes S, Schwan HP (2002) Interface phenomena and dielectric properties of biological tissue. In: Somasundaran P (ed) Encyclopedia of surface and colloid science anonymous. Marcel Dekker Inc, New York, pp 2643–2652

    Google Scholar 

  • Minetti G, Seppi C, Ciana A, Balduini C, Low PS, Brovelli A (1998) Characterization of the hypertonically induced tyrosine phosphorylation of erythrocyte band 3. Biochem J 335:305–311

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Mokken EC, Kedaria M, Henny CP, Hardeman MR, Gelb AW (1992) The clinical importance of erythrocyte deformability, a hemorrheological parameter. Ann Hematol 64:113–122

    Article  CAS  PubMed  Google Scholar 

  • Mueller TJ, Morrison M (1981) Glyconnectin (PAS2), a membrane attachment site for human erythrocyte cytoskeleton. In: Kruckeberg WC, Eaton JW, Brewer GJ (eds) Erythrocyte membranes 2: recent clinical and experimental advances. Alan R Liss Inc, New York, pp 95–112

    Google Scholar 

  • Nakashima K, Beutler E (1978) Effect of anti-spectrin antibody and ATP on deformability of resealed erythrocyte membranes. Proc Natl Acad Sci USA 75(8):3823–3825

    Article  CAS  PubMed  Google Scholar 

  • Nash GB, Gratzer WB (1993) Structural determinants of the rigidity of the red cell membrane. Biorheology 30:397–407

    Article  CAS  PubMed  Google Scholar 

  • Nishio I, Tanaka T, Imanishi Y, Ohnishi S (1983) Hemoglobin aggregation in single red blood cells of sickle cell anemia. Science (Washington DC) 220:1173–1175

    Article  CAS  Google Scholar 

  • Nishio I, Peetermans J, Tanaka T (1985) Microscope laser light scattering spectroscopy of single biological cells. Cell Biophys 7:91–105

    Article  CAS  PubMed  Google Scholar 

  • Paarvanova B, Tacheva B, Karabaliev M, Ivanov IT (2017) Thermal dielectroscopy. A new method for studying the membrane skeleton of human erythrocytes. AIP Conf Proc 1906:150004

    Article  Google Scholar 

  • Parpart AK, Hoffman JF (1956) Flicker in erythrocytes; vibratory movements in the cytoplasm. J Cell Physiol 47:295–303

    Article  CAS  Google Scholar 

  • Peetermans J, Nishio I, Ohnishi ST, Tanaka T (1986) Lightscattering study of depolymerization kinetics of sickle hemoglobin polymers inside single erythrocytes. Proc Natl Acad Sci USA 83:352–356

    Article  CAS  PubMed  Google Scholar 

  • Popescu G, Badizadegan K, Dasari RR, Feld MS (2006) Observation of dynamic subdomains in red blood cells. J Biomed Opt 11(4):040503

    Article  PubMed  Google Scholar 

  • Puckeridge M, Chapman BE, Conigrave AD, Kuchel PW (2014) Membrane flickering of the human erythrocyte: physical and chemical effectors. Eur Biophys J 43:169–177

    Article  CAS  PubMed  Google Scholar 

  • Rodrίguez-Garcίa R, Lόpez-Montero I, Mell M, Egea G, Gov N, Monroy F (2015) Direct cytoskeleton forces cause membrane softening in red blood cells. Biophys J 108:2794–2806

    Article  Google Scholar 

  • Samuel E, Lux IV (2016) Anatomy of the red cell membrane skeleton: unanswered questions. Blood 127(2):187–199

    Article  Google Scholar 

  • Schwan HP (1981) Dielectric properties of biological tissue and physical mechanisms of electromagnetic field interaction. In: Illinger KH (ed), Biological effects of nonionizing radiation, ACS Symposium Series 157, American Chemical Society, Washington, DC.

  • Schwan HP, Takashima S (1993) Electrical conduction and dielectric behaviour in biological systems. Encycl Appl Phys 5:177–200

    Google Scholar 

  • Sheetz MP, Casaly J (1980) 2,3-Dipbosphoglycerate and ATP dissociate erythrocyte membrane skeletons. J Biol Chem 225:9955–9960

    Article  Google Scholar 

  • Simeonova M, Wachner D, Gimsa J (2002) Cellular absorption of electric field energy: influence of molecular properties of the cytoplasm. Bioelectrochemistry 56:215–218

    Article  CAS  PubMed  Google Scholar 

  • Sinha A, Chu TTT, Dao M, Chandramohanadas R (2015) Single-cell evaluation of red blood cell bio-mechanical and nano-structural alterations upon chemically induced oxidative stress. Sci Rep 5:9768

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sosa JM, Nielsen ND, Vignes SM, Chen TG, Shevkoplyas SS (2014) The relationship between red blood cell deformability metrics and perfusion of an artificial microvascular network. Clin Hemorheol Microcirc 57(3):275–289

    Article  CAS  PubMed  Google Scholar 

  • Strey H, Peterson M, Sackmann E (1995) Measurement of erythrocyte membrane elasticity by flicker eigenmode decomposition. Biophys J 69:478–488

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Sukhorukov VL, Mussauer H, Zimmermann U (1998) The effect of electrical deformation forces on the electropermeabilization of erythrocyte membranes in low- and high-conductivity media. J Membr Biol 163:235–245

    Article  CAS  PubMed  Google Scholar 

  • Szekely D, Yau TW, Kuchel PW (2009) Human erythrocyte flickering: temperature, ATP concentration, water transport, and cell aging, plus a computer simulation. Eur Biophys J 38(7):923–939

    Article  CAS  PubMed  Google Scholar 

  • Tishler RB, Carlson FD (1987) Quasi-elastic light scattering studies of membrane motion in single red blood cells. Biophys J 51:993–997

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Turlier H, Fedosov DA, Audoly B, Auth T, Gov NS, Sykes C, Joanny JF, Gompper G, Betz T (2016) Equilibrium physics breakdown reveals the active nature of red blood cell flickering. Nat Phys 12:513–515

    Article  CAS  Google Scholar 

  • Tuvia S, Levin S, Korenstein R (1992) Correlation between local cell membrane displacements and filterability of human red blood cells. FEBS Lett 304(1):32–36

    Article  CAS  PubMed  Google Scholar 

  • Tuvia S, Levin S, Korenstein R (1996) The role of linker proteins (protein 4.1 and ankyrin) in cell membrane fluctuations of human erythrocytes. Biophys J 108:2794–2806

    Google Scholar 

  • Tuvia S, Levin S, Bitler A, Korenstein R (1998) Mechanical fluctuations of the membrane-skeleton are dependent on F-actin ATPase in human erythrocytes. J Cell Biol 141:1551–1561

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Tuvia S, Moses A, Gulayev N, Levin S, Korenstein R (1999) β-Adrenergic agonists regulate cell membrane fluctuations of human erythrocytes. J Physiol 516(3):781–792

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Ungewickell E, Gratzer W (1978) Self-association of human spectrin. A thermodynamic and kinetic study. Eur J Biochem 88(2):379–385

    Article  CAS  PubMed  Google Scholar 

  • Ungewickell E, Bennett PM, Calvert R, Ohanian V, Gratzer WB (1979) In vitro formation of a complex between cytoskeletal proteins of the human erythrocyte. Nature 280:811–814

    Article  CAS  PubMed  Google Scholar 

  • Van Dort HM, Moriyama R, Low PS (1998) Effect of band 3 subunit equilibrium on the kinetics and affinity of ankyrin binding to erythrocyte membrane vesicles. J Biol Chem 273:14819–14826

    Article  PubMed  Google Scholar 

  • Van Dort HM, Knowles DW, Chasis JA, Lee G, Mohandas N, Low PS (2001) Analysis of integral membrane protein contributions to the deformability and stability of the human erythrocyte membrane. J Biol Chem 276:46968–46974

    Article  PubMed  Google Scholar 

  • Wildenauer DB, Reuther H, Remien J (1980) Reactions of the alkylating agent tris(2-chloroethyl)-amine with the erythrocyte membrane. Effects on shape changes of human erythrocytes and ghosts. Biochim Biophys Acta 603:101–116

    Article  CAS  PubMed  Google Scholar 

  • Wolf M, Gulich R, Lunkenheimer P, Loidl A (2011) Broadband dielectric spectroscopy on human blood. BBA-G Subj 1810:727–740

    Article  CAS  Google Scholar 

  • Wolfe LC, Ohanian V, Lux SE (1980) Regulation of spectrin-actin binding by protein 41 and polyphosphates. J Cell Biol 87:203a

    Google Scholar 

  • Xu H, Xu Y, Zhang ZH (1994) The effect of wheat germ agglutinin on anion transport in the erythrocyte membranes. Shi Yan Sheng Wu Xue Bao 27(4):477–481

    CAS  PubMed  Google Scholar 

  • Xu Z, Dou WK, Wang C, Sun Y (2019) Stiffness and ATP recovery of stored red blood cells in serum. Microsyst Nanoeng 5:51

    Article  CAS  PubMed  PubMed Central  Google Scholar 

  • Yokoyama KK, Terao T, Osawa T (1978) Carbohydrate-binding specificity of pokeweed mitogens. Biochem Biophys Acta 538(2):384–396

    Article  CAS  PubMed  Google Scholar 

  • Yoshino H, Minari O (1987) Heat-induced dissociation of human erythrocyte spectrin dimer into monomers. BBA Biomembr 905:100–108

    Article  CAS  Google Scholar 

  • Zeman K, Engelhard H, Sackmann E (1990) Bending undulations and elasticity of the erythrocyte membrane: effects of cell shape and membrane organization. Europ Biophys J 18:203–219

    Article  CAS  Google Scholar 

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This research was funded by the Ministry of Education and Science of Bulgaria–grant number КП-06-Austria-10/29.08.2019.

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  1. Department of Physics and Biophysics, Roentgenology and Radiology, Medical Faculty of Thracian University, 6000, Stara Zagora, Bulgaria

    Ivan T. Ivanov & Boyana K. Paarvanova

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Ivanov, I.T., Paarvanova, B.K. Differential dielectroscopic data on the relation of erythrocyte membrane skeleton to erythrocyte deformability and flicker. Eur Biophys J 50, 69–86 (2021). https://doi.org/10.1007/s00249-020-01491-4

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