Abstract

The aggregation of red blood cells (RBC) is of importance for hemorheology, while its mechanism remains debatable. The key question is the role of the adsorption of macromolecules on RBC membranes, which may act as “bridges” between cells. It is especially important that dextran is considered to induce “bridge”-less aggregation due to the depletion forces. We revisit the dextran-RBC interaction on the single cell level using the laser tweezers combined with microfluidic technology and fluorescence microscopy. An immediate sorption of ~104 molecules of 70 kDa dextran per cell was observed. During the incubation of RBC with dextran, a gradual tenfold increase of adsorption was found, accompanied by a moderate change in the RBC deformability. The obtained data demonstrate that dextran sorption and incubation-induced changes of the membrane properties must be considered when studying RBC aggregation in vitro.

© 2018 Optical Society of America under the terms of the OSA Open Access Publishing Agreement

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References

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    [Crossref] [PubMed]
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  8. S. Chien and K. Jan, “Ultrastructural basis of the mechanism of rouleaux formation,” Microvasc. Res. 5(2), 155–166 (1973).
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    [Crossref] [PubMed]
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  21. H. Bäumler, B. Neu, R. Mitlöhner, R. Georgieva, H. J. Meiselman, and H. Kiesewetter, “Electrophoretic and aggregation behavior of bovine, horse and human red blood cells in plasma and in polymer solutions,” Biorheology 38(1), 39–51 (2001).
    [PubMed]
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  25. M. W. Rampling, H. J. Meiselman, B. Neu, and O. K. Baskurt, “Influence of cell-specific factors on red blood cell aggregation,” Biorheology 41(2), 91–112 (2004).
    [PubMed]
  26. R. I. Weed, P. L. LaCelle, and E. W. Merrill, “Metabolic dependence of red cell deformability,” J. Clin. Invest. 48(5), 795–809 (1969).
    [Crossref] [PubMed]
  27. M. Uyuklu, M. Cengiz, P. Ulker, T. Hever, J. Tripette, P. Connes, N. Nemeth, H. J. Meiselman, and O. K. Baskurt, “Effects of storage duration and temperature of human blood on red cell deformability and aggregation,” Clin. Hemorheol. Microcirc. 41(4), 269–278 (2009).
    [PubMed]
  28. T. Betz, M. Lenz, J. F. Joanny, and C. Sykes, “ATP-dependent mechanics of red blood cells,” Proc. Natl. Acad. Sci. U.S.A. 106(36), 15320–15325 (2009).
    [Crossref] [PubMed]
  29. N. Mohandas and S. B. Shohet, “The role of membrane-associated enzymes in regulation of erythrocyte shape and deformability,” Clin. Haematol. 10(1), 223–237 (1981).
    [PubMed]
  30. A. Makhro, R. Huisjes, L. P. Verhagen, M. M. Mañú-Pereira, E. Llaudet-Planas, P. Petkova-Kirova, J. Wang, H. Eichler, A. Bogdanova, R. van Wijk, J.-L. Vives-Corrons, and L. Kaestner, “Red Cell Properties after Different Modes of Blood Transportation,” Front. Physiol. 7, 288 (2016).
    [Crossref] [PubMed]
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    [PubMed]

2017 (1)

K. Lee, C. Wagner, and A. V. Priezzhev, “Assessment of the “cross-bridge”-induced interaction of red blood cells by optical trapping combined with microfluidics,” J. Biomed. Opt. 22(9), 091516 (2017).
[Crossref] [PubMed]

2016 (1)

A. Makhro, R. Huisjes, L. P. Verhagen, M. M. Mañú-Pereira, E. Llaudet-Planas, P. Petkova-Kirova, J. Wang, H. Eichler, A. Bogdanova, R. van Wijk, J.-L. Vives-Corrons, and L. Kaestner, “Red Cell Properties after Different Modes of Blood Transportation,” Front. Physiol. 7, 288 (2016).
[Crossref] [PubMed]

2014 (1)

S. Rad, H. J. Meiselman, and B. Neu, “Impact of glycocalyx structure on red cell-red cell affinity in polymer suspensions,” Colloids Surf. B Biointerfaces 123, 106–113 (2014).
[Crossref] [PubMed]

2013 (1)

P. Steffen, C. Verdier, and C. Wagner, “Quantification of depletion-induced adhesion of red blood cells,” Phys. Rev. Lett. 110(1), 018102 (2013).
[Crossref] [PubMed]

2012 (1)

J. C. A. Cluitmans, M. R. Hardeman, S. Dinkla, R. Brock, and G. J. C. G. M. Bosman, “Red blood cell deformability during storage: towards functional proteomics and metabolomics in the Blood Bank,” Blood Transfus. 10(2), s12–s18 (2012).
[PubMed]

2010 (1)

M. Girasole, G. Pompeo, A. Cricenti, G. Longo, G. Boumis, A. Bellelli, and S. Amiconi, “The how, when, and why of the aging signals appearing on the human erythrocyte membrane: an atomic force microscopy study of surface roughness,” Nanomedicine (Lond.) 6(6), 760–768 (2010).
[Crossref] [PubMed]

2009 (2)

M. Uyuklu, M. Cengiz, P. Ulker, T. Hever, J. Tripette, P. Connes, N. Nemeth, H. J. Meiselman, and O. K. Baskurt, “Effects of storage duration and temperature of human blood on red cell deformability and aggregation,” Clin. Hemorheol. Microcirc. 41(4), 269–278 (2009).
[PubMed]

T. Betz, M. Lenz, J. F. Joanny, and C. Sykes, “ATP-dependent mechanics of red blood cells,” Proc. Natl. Acad. Sci. U.S.A. 106(36), 15320–15325 (2009).
[Crossref] [PubMed]

2008 (1)

B. Neu, R. Wenby, and H. J. Meiselman, “Effects of dextran molecular weight on red blood cell aggregation,” Biophys. J. 95(6), 3059–3065 (2008).
[Crossref] [PubMed]

2007 (2)

A. Pribush, D. Zilberman-Kravits, and N. Meyerstein, “The mechanism of the dextran-induced red blood cell aggregation,” Eur. Biophys. J. 36(2), 85–94 (2007).
[Crossref] [PubMed]

S. Shin, J.X. Hou, and M. Singh, “Validation and application of a microfluidic ektacytometer (RheoScan-D) in measuring erythrocyte deformability,” Clin. Hemorheol. Microcirc.  37, 319–328 (2007)

2004 (1)

M. W. Rampling, H. J. Meiselman, B. Neu, and O. K. Baskurt, “Influence of cell-specific factors on red blood cell aggregation,” Biorheology 41(2), 91–112 (2004).
[PubMed]

2003 (2)

O. K. Baskurt and H. J. Meiselman, “Blood rheology and hemodynamics,” Semin. Thromb. Hemost. 29(5), 435–450 (2003).
[Crossref] [PubMed]

V. Schechner, I. Shapira, S. Berliner, D. Comaneshter, T. Hershcovici, J. Orlin, D. Zeltser, M. Rozenblat, K. Lachmi, M. Hirsch, and Y. Beigel, “Significant dominance of fibrinogen over immunoglobulins, C-reactive protein, cholesterol and triglycerides in maintaining increased red blood cell adhesiveness/aggregation in the peripheral venous blood: a model in hypercholesterolaemic patients,” Eur. J. Clin. Invest. 33(11), 955–961 (2003).
[Crossref] [PubMed]

2002 (2)

D. Lominadze and W. L. Dean, “Involvement of fibrinogen specific binding in erythrocyte aggregation,” FEBS Lett. 517(1-3), 41–44 (2002).
[Crossref] [PubMed]

B. Neu and H. J. Meiselman, “Depletion-Mediated Red Blood Cell Aggregation in Polymer Solutions,” Biophys. J. 83(5), 2482–2490 (2002).
[Crossref] [PubMed]

2001 (1)

H. Bäumler, B. Neu, R. Mitlöhner, R. Georgieva, H. J. Meiselman, and H. Kiesewetter, “Electrophoretic and aggregation behavior of bovine, horse and human red blood cells in plasma and in polymer solutions,” Biorheology 38(1), 39–51 (2001).
[PubMed]

1999 (1)

H. Bäumler, B. Neu, S. Iovtchev, A. Budde, H. Kiesewetter, R. Latza, and E. Donath, “Electroosmosis and polymer depletion layers near surface conducting particles are detectable by low frequency electrorotation,” Colloids Surf. A Physicochem. Eng. Asp. 149(1), 389–396 (1999).
[Crossref]

1997 (1)

P. J. Bronkhorst, J. Grimbergen, G. J. Brakenhoff, R. M. Heethaar, and J. J. Sixma, “The mechanism of red cell (dis)aggregation investigated by means of direct cell manipulation using multiple optical trapping,” Br. J. Haematol. 96(2), 256–258 (1997).
[Crossref] [PubMed]

1996 (1)

F. J. Alvarez, A. Herráez, M. C. Tejedor, and J. C. Díez, “Behaviour of isolated rat and human red blood cells upon hypotonic-dialysis encapsulation of carbonic anhydrase and dextran,” Biotechnol. Appl. Biochem. 23(Pt 2), 173–179 (1996).
[PubMed]

1989 (1)

A. Cudd, T. Arvinte, B. Schulz, and C. Nicolau, “Dextran protection of erythrocytes from low-pH-induced hemolysis,” FEBS Lett. 250(2), 293–296 (1989).
[Crossref] [PubMed]

1987 (1)

K. J. A. Davies and A. L. Goldberg, “Proteins damaged by oxygen radicals are rapidly degraded in extracts of red blood cells,” J. Biol. Chem. 262(17), 8227–8234 (1987).
[PubMed]

1986 (1)

K. Fricke, K. Wirthensohn, R. Laxhuber, and E. Sackmann, “Flicker spectroscopy of erythrocytes. A sensitive method to study subtle changes of membrane bending stiffness,” Eur. Biophys. J. 14(2), 67–81 (1986).
[PubMed]

1981 (1)

N. Mohandas and S. B. Shohet, “The role of membrane-associated enzymes in regulation of erythrocyte shape and deformability,” Clin. Haematol. 10(1), 223–237 (1981).
[PubMed]

1977 (2)

S. Chien, L. A. Sung, S. Kim, A. M. Burke, and S. Usami, “Determination of aggregation force in rouleaux by fluid mechanical technique,” Microvasc. Res. 13(3), 327–333 (1977).
[Crossref] [PubMed]

S. Chien and K. M. Jan, “Surface adsorption of dextrans on human red cell membrane,” J. Colloid Interface Sci. 62(3), 461–470 (1977).
[Crossref]

1973 (2)

S. Chien and K. Jan, “Ultrastructural basis of the mechanism of rouleaux formation,” Microvasc. Res. 5(2), 155–166 (1973).
[Crossref] [PubMed]

D. E. Brooks, “The effect of neutral polymers on the electrokinetic potential of cells and other charged particles: III. Experimental studies on the dextran/erythrocyte system,” J. Colloid Interface Sci. 43(3), 700–713 (1973).
[Crossref]

1969 (1)

R. I. Weed, P. L. LaCelle, and E. W. Merrill, “Metabolic dependence of red cell deformability,” J. Clin. Invest. 48(5), 795–809 (1969).
[Crossref] [PubMed]

Alvarez, F. J.

F. J. Alvarez, A. Herráez, M. C. Tejedor, and J. C. Díez, “Behaviour of isolated rat and human red blood cells upon hypotonic-dialysis encapsulation of carbonic anhydrase and dextran,” Biotechnol. Appl. Biochem. 23(Pt 2), 173–179 (1996).
[PubMed]

Amiconi, S.

M. Girasole, G. Pompeo, A. Cricenti, G. Longo, G. Boumis, A. Bellelli, and S. Amiconi, “The how, when, and why of the aging signals appearing on the human erythrocyte membrane: an atomic force microscopy study of surface roughness,” Nanomedicine (Lond.) 6(6), 760–768 (2010).
[Crossref] [PubMed]

Arvinte, T.

A. Cudd, T. Arvinte, B. Schulz, and C. Nicolau, “Dextran protection of erythrocytes from low-pH-induced hemolysis,” FEBS Lett. 250(2), 293–296 (1989).
[Crossref] [PubMed]

Baskurt, O. K.

M. Uyuklu, M. Cengiz, P. Ulker, T. Hever, J. Tripette, P. Connes, N. Nemeth, H. J. Meiselman, and O. K. Baskurt, “Effects of storage duration and temperature of human blood on red cell deformability and aggregation,” Clin. Hemorheol. Microcirc. 41(4), 269–278 (2009).
[PubMed]

M. W. Rampling, H. J. Meiselman, B. Neu, and O. K. Baskurt, “Influence of cell-specific factors on red blood cell aggregation,” Biorheology 41(2), 91–112 (2004).
[PubMed]

O. K. Baskurt and H. J. Meiselman, “Blood rheology and hemodynamics,” Semin. Thromb. Hemost. 29(5), 435–450 (2003).
[Crossref] [PubMed]

Bäumler, H.

H. Bäumler, B. Neu, R. Mitlöhner, R. Georgieva, H. J. Meiselman, and H. Kiesewetter, “Electrophoretic and aggregation behavior of bovine, horse and human red blood cells in plasma and in polymer solutions,” Biorheology 38(1), 39–51 (2001).
[PubMed]

H. Bäumler, B. Neu, S. Iovtchev, A. Budde, H. Kiesewetter, R. Latza, and E. Donath, “Electroosmosis and polymer depletion layers near surface conducting particles are detectable by low frequency electrorotation,” Colloids Surf. A Physicochem. Eng. Asp. 149(1), 389–396 (1999).
[Crossref]

Beigel, Y.

V. Schechner, I. Shapira, S. Berliner, D. Comaneshter, T. Hershcovici, J. Orlin, D. Zeltser, M. Rozenblat, K. Lachmi, M. Hirsch, and Y. Beigel, “Significant dominance of fibrinogen over immunoglobulins, C-reactive protein, cholesterol and triglycerides in maintaining increased red blood cell adhesiveness/aggregation in the peripheral venous blood: a model in hypercholesterolaemic patients,” Eur. J. Clin. Invest. 33(11), 955–961 (2003).
[Crossref] [PubMed]

Bellelli, A.

M. Girasole, G. Pompeo, A. Cricenti, G. Longo, G. Boumis, A. Bellelli, and S. Amiconi, “The how, when, and why of the aging signals appearing on the human erythrocyte membrane: an atomic force microscopy study of surface roughness,” Nanomedicine (Lond.) 6(6), 760–768 (2010).
[Crossref] [PubMed]

Berliner, S.

V. Schechner, I. Shapira, S. Berliner, D. Comaneshter, T. Hershcovici, J. Orlin, D. Zeltser, M. Rozenblat, K. Lachmi, M. Hirsch, and Y. Beigel, “Significant dominance of fibrinogen over immunoglobulins, C-reactive protein, cholesterol and triglycerides in maintaining increased red blood cell adhesiveness/aggregation in the peripheral venous blood: a model in hypercholesterolaemic patients,” Eur. J. Clin. Invest. 33(11), 955–961 (2003).
[Crossref] [PubMed]

Betz, T.

T. Betz, M. Lenz, J. F. Joanny, and C. Sykes, “ATP-dependent mechanics of red blood cells,” Proc. Natl. Acad. Sci. U.S.A. 106(36), 15320–15325 (2009).
[Crossref] [PubMed]

Bogdanova, A.

A. Makhro, R. Huisjes, L. P. Verhagen, M. M. Mañú-Pereira, E. Llaudet-Planas, P. Petkova-Kirova, J. Wang, H. Eichler, A. Bogdanova, R. van Wijk, J.-L. Vives-Corrons, and L. Kaestner, “Red Cell Properties after Different Modes of Blood Transportation,” Front. Physiol. 7, 288 (2016).
[Crossref] [PubMed]

Bosman, G. J. C. G. M.

J. C. A. Cluitmans, M. R. Hardeman, S. Dinkla, R. Brock, and G. J. C. G. M. Bosman, “Red blood cell deformability during storage: towards functional proteomics and metabolomics in the Blood Bank,” Blood Transfus. 10(2), s12–s18 (2012).
[PubMed]

Boumis, G.

M. Girasole, G. Pompeo, A. Cricenti, G. Longo, G. Boumis, A. Bellelli, and S. Amiconi, “The how, when, and why of the aging signals appearing on the human erythrocyte membrane: an atomic force microscopy study of surface roughness,” Nanomedicine (Lond.) 6(6), 760–768 (2010).
[Crossref] [PubMed]

Brakenhoff, G. J.

P. J. Bronkhorst, J. Grimbergen, G. J. Brakenhoff, R. M. Heethaar, and J. J. Sixma, “The mechanism of red cell (dis)aggregation investigated by means of direct cell manipulation using multiple optical trapping,” Br. J. Haematol. 96(2), 256–258 (1997).
[Crossref] [PubMed]

Brock, R.

J. C. A. Cluitmans, M. R. Hardeman, S. Dinkla, R. Brock, and G. J. C. G. M. Bosman, “Red blood cell deformability during storage: towards functional proteomics and metabolomics in the Blood Bank,” Blood Transfus. 10(2), s12–s18 (2012).
[PubMed]

Bronkhorst, P. J.

P. J. Bronkhorst, J. Grimbergen, G. J. Brakenhoff, R. M. Heethaar, and J. J. Sixma, “The mechanism of red cell (dis)aggregation investigated by means of direct cell manipulation using multiple optical trapping,” Br. J. Haematol. 96(2), 256–258 (1997).
[Crossref] [PubMed]

Brooks, D. E.

D. E. Brooks, “The effect of neutral polymers on the electrokinetic potential of cells and other charged particles: III. Experimental studies on the dextran/erythrocyte system,” J. Colloid Interface Sci. 43(3), 700–713 (1973).
[Crossref]

Budde, A.

H. Bäumler, B. Neu, S. Iovtchev, A. Budde, H. Kiesewetter, R. Latza, and E. Donath, “Electroosmosis and polymer depletion layers near surface conducting particles are detectable by low frequency electrorotation,” Colloids Surf. A Physicochem. Eng. Asp. 149(1), 389–396 (1999).
[Crossref]

Burke, A. M.

S. Chien, L. A. Sung, S. Kim, A. M. Burke, and S. Usami, “Determination of aggregation force in rouleaux by fluid mechanical technique,” Microvasc. Res. 13(3), 327–333 (1977).
[Crossref] [PubMed]

Cengiz, M.

M. Uyuklu, M. Cengiz, P. Ulker, T. Hever, J. Tripette, P. Connes, N. Nemeth, H. J. Meiselman, and O. K. Baskurt, “Effects of storage duration and temperature of human blood on red cell deformability and aggregation,” Clin. Hemorheol. Microcirc. 41(4), 269–278 (2009).
[PubMed]

Chien, S.

S. Chien, L. A. Sung, S. Kim, A. M. Burke, and S. Usami, “Determination of aggregation force in rouleaux by fluid mechanical technique,” Microvasc. Res. 13(3), 327–333 (1977).
[Crossref] [PubMed]

S. Chien and K. M. Jan, “Surface adsorption of dextrans on human red cell membrane,” J. Colloid Interface Sci. 62(3), 461–470 (1977).
[Crossref]

S. Chien and K. Jan, “Ultrastructural basis of the mechanism of rouleaux formation,” Microvasc. Res. 5(2), 155–166 (1973).
[Crossref] [PubMed]

Cluitmans, J. C. A.

J. C. A. Cluitmans, M. R. Hardeman, S. Dinkla, R. Brock, and G. J. C. G. M. Bosman, “Red blood cell deformability during storage: towards functional proteomics and metabolomics in the Blood Bank,” Blood Transfus. 10(2), s12–s18 (2012).
[PubMed]

Comaneshter, D.

V. Schechner, I. Shapira, S. Berliner, D. Comaneshter, T. Hershcovici, J. Orlin, D. Zeltser, M. Rozenblat, K. Lachmi, M. Hirsch, and Y. Beigel, “Significant dominance of fibrinogen over immunoglobulins, C-reactive protein, cholesterol and triglycerides in maintaining increased red blood cell adhesiveness/aggregation in the peripheral venous blood: a model in hypercholesterolaemic patients,” Eur. J. Clin. Invest. 33(11), 955–961 (2003).
[Crossref] [PubMed]

Connes, P.

M. Uyuklu, M. Cengiz, P. Ulker, T. Hever, J. Tripette, P. Connes, N. Nemeth, H. J. Meiselman, and O. K. Baskurt, “Effects of storage duration and temperature of human blood on red cell deformability and aggregation,” Clin. Hemorheol. Microcirc. 41(4), 269–278 (2009).
[PubMed]

Cricenti, A.

M. Girasole, G. Pompeo, A. Cricenti, G. Longo, G. Boumis, A. Bellelli, and S. Amiconi, “The how, when, and why of the aging signals appearing on the human erythrocyte membrane: an atomic force microscopy study of surface roughness,” Nanomedicine (Lond.) 6(6), 760–768 (2010).
[Crossref] [PubMed]

Cudd, A.

A. Cudd, T. Arvinte, B. Schulz, and C. Nicolau, “Dextran protection of erythrocytes from low-pH-induced hemolysis,” FEBS Lett. 250(2), 293–296 (1989).
[Crossref] [PubMed]

Davies, K. J. A.

K. J. A. Davies and A. L. Goldberg, “Proteins damaged by oxygen radicals are rapidly degraded in extracts of red blood cells,” J. Biol. Chem. 262(17), 8227–8234 (1987).
[PubMed]

Dean, W. L.

D. Lominadze and W. L. Dean, “Involvement of fibrinogen specific binding in erythrocyte aggregation,” FEBS Lett. 517(1-3), 41–44 (2002).
[Crossref] [PubMed]

Díez, J. C.

F. J. Alvarez, A. Herráez, M. C. Tejedor, and J. C. Díez, “Behaviour of isolated rat and human red blood cells upon hypotonic-dialysis encapsulation of carbonic anhydrase and dextran,” Biotechnol. Appl. Biochem. 23(Pt 2), 173–179 (1996).
[PubMed]

Dinkla, S.

J. C. A. Cluitmans, M. R. Hardeman, S. Dinkla, R. Brock, and G. J. C. G. M. Bosman, “Red blood cell deformability during storage: towards functional proteomics and metabolomics in the Blood Bank,” Blood Transfus. 10(2), s12–s18 (2012).
[PubMed]

Donath, E.

H. Bäumler, B. Neu, S. Iovtchev, A. Budde, H. Kiesewetter, R. Latza, and E. Donath, “Electroosmosis and polymer depletion layers near surface conducting particles are detectable by low frequency electrorotation,” Colloids Surf. A Physicochem. Eng. Asp. 149(1), 389–396 (1999).
[Crossref]

Eichler, H.

A. Makhro, R. Huisjes, L. P. Verhagen, M. M. Mañú-Pereira, E. Llaudet-Planas, P. Petkova-Kirova, J. Wang, H. Eichler, A. Bogdanova, R. van Wijk, J.-L. Vives-Corrons, and L. Kaestner, “Red Cell Properties after Different Modes of Blood Transportation,” Front. Physiol. 7, 288 (2016).
[Crossref] [PubMed]

Fricke, K.

K. Fricke, K. Wirthensohn, R. Laxhuber, and E. Sackmann, “Flicker spectroscopy of erythrocytes. A sensitive method to study subtle changes of membrane bending stiffness,” Eur. Biophys. J. 14(2), 67–81 (1986).
[PubMed]

Georgieva, R.

H. Bäumler, B. Neu, R. Mitlöhner, R. Georgieva, H. J. Meiselman, and H. Kiesewetter, “Electrophoretic and aggregation behavior of bovine, horse and human red blood cells in plasma and in polymer solutions,” Biorheology 38(1), 39–51 (2001).
[PubMed]

Girasole, M.

M. Girasole, G. Pompeo, A. Cricenti, G. Longo, G. Boumis, A. Bellelli, and S. Amiconi, “The how, when, and why of the aging signals appearing on the human erythrocyte membrane: an atomic force microscopy study of surface roughness,” Nanomedicine (Lond.) 6(6), 760–768 (2010).
[Crossref] [PubMed]

Goldberg, A. L.

K. J. A. Davies and A. L. Goldberg, “Proteins damaged by oxygen radicals are rapidly degraded in extracts of red blood cells,” J. Biol. Chem. 262(17), 8227–8234 (1987).
[PubMed]

Grimbergen, J.

P. J. Bronkhorst, J. Grimbergen, G. J. Brakenhoff, R. M. Heethaar, and J. J. Sixma, “The mechanism of red cell (dis)aggregation investigated by means of direct cell manipulation using multiple optical trapping,” Br. J. Haematol. 96(2), 256–258 (1997).
[Crossref] [PubMed]

Hardeman, M. R.

J. C. A. Cluitmans, M. R. Hardeman, S. Dinkla, R. Brock, and G. J. C. G. M. Bosman, “Red blood cell deformability during storage: towards functional proteomics and metabolomics in the Blood Bank,” Blood Transfus. 10(2), s12–s18 (2012).
[PubMed]

Heethaar, R. M.

P. J. Bronkhorst, J. Grimbergen, G. J. Brakenhoff, R. M. Heethaar, and J. J. Sixma, “The mechanism of red cell (dis)aggregation investigated by means of direct cell manipulation using multiple optical trapping,” Br. J. Haematol. 96(2), 256–258 (1997).
[Crossref] [PubMed]

Herráez, A.

F. J. Alvarez, A. Herráez, M. C. Tejedor, and J. C. Díez, “Behaviour of isolated rat and human red blood cells upon hypotonic-dialysis encapsulation of carbonic anhydrase and dextran,” Biotechnol. Appl. Biochem. 23(Pt 2), 173–179 (1996).
[PubMed]

Hershcovici, T.

V. Schechner, I. Shapira, S. Berliner, D. Comaneshter, T. Hershcovici, J. Orlin, D. Zeltser, M. Rozenblat, K. Lachmi, M. Hirsch, and Y. Beigel, “Significant dominance of fibrinogen over immunoglobulins, C-reactive protein, cholesterol and triglycerides in maintaining increased red blood cell adhesiveness/aggregation in the peripheral venous blood: a model in hypercholesterolaemic patients,” Eur. J. Clin. Invest. 33(11), 955–961 (2003).
[Crossref] [PubMed]

Hever, T.

M. Uyuklu, M. Cengiz, P. Ulker, T. Hever, J. Tripette, P. Connes, N. Nemeth, H. J. Meiselman, and O. K. Baskurt, “Effects of storage duration and temperature of human blood on red cell deformability and aggregation,” Clin. Hemorheol. Microcirc. 41(4), 269–278 (2009).
[PubMed]

Hirsch, M.

V. Schechner, I. Shapira, S. Berliner, D. Comaneshter, T. Hershcovici, J. Orlin, D. Zeltser, M. Rozenblat, K. Lachmi, M. Hirsch, and Y. Beigel, “Significant dominance of fibrinogen over immunoglobulins, C-reactive protein, cholesterol and triglycerides in maintaining increased red blood cell adhesiveness/aggregation in the peripheral venous blood: a model in hypercholesterolaemic patients,” Eur. J. Clin. Invest. 33(11), 955–961 (2003).
[Crossref] [PubMed]

Hou, J.X.

S. Shin, J.X. Hou, and M. Singh, “Validation and application of a microfluidic ektacytometer (RheoScan-D) in measuring erythrocyte deformability,” Clin. Hemorheol. Microcirc.  37, 319–328 (2007)

Huisjes, R.

A. Makhro, R. Huisjes, L. P. Verhagen, M. M. Mañú-Pereira, E. Llaudet-Planas, P. Petkova-Kirova, J. Wang, H. Eichler, A. Bogdanova, R. van Wijk, J.-L. Vives-Corrons, and L. Kaestner, “Red Cell Properties after Different Modes of Blood Transportation,” Front. Physiol. 7, 288 (2016).
[Crossref] [PubMed]

Iovtchev, S.

H. Bäumler, B. Neu, S. Iovtchev, A. Budde, H. Kiesewetter, R. Latza, and E. Donath, “Electroosmosis and polymer depletion layers near surface conducting particles are detectable by low frequency electrorotation,” Colloids Surf. A Physicochem. Eng. Asp. 149(1), 389–396 (1999).
[Crossref]

Jan, K.

S. Chien and K. Jan, “Ultrastructural basis of the mechanism of rouleaux formation,” Microvasc. Res. 5(2), 155–166 (1973).
[Crossref] [PubMed]

Jan, K. M.

S. Chien and K. M. Jan, “Surface adsorption of dextrans on human red cell membrane,” J. Colloid Interface Sci. 62(3), 461–470 (1977).
[Crossref]

Joanny, J. F.

T. Betz, M. Lenz, J. F. Joanny, and C. Sykes, “ATP-dependent mechanics of red blood cells,” Proc. Natl. Acad. Sci. U.S.A. 106(36), 15320–15325 (2009).
[Crossref] [PubMed]

Kaestner, L.

A. Makhro, R. Huisjes, L. P. Verhagen, M. M. Mañú-Pereira, E. Llaudet-Planas, P. Petkova-Kirova, J. Wang, H. Eichler, A. Bogdanova, R. van Wijk, J.-L. Vives-Corrons, and L. Kaestner, “Red Cell Properties after Different Modes of Blood Transportation,” Front. Physiol. 7, 288 (2016).
[Crossref] [PubMed]

Kiesewetter, H.

H. Bäumler, B. Neu, R. Mitlöhner, R. Georgieva, H. J. Meiselman, and H. Kiesewetter, “Electrophoretic and aggregation behavior of bovine, horse and human red blood cells in plasma and in polymer solutions,” Biorheology 38(1), 39–51 (2001).
[PubMed]

H. Bäumler, B. Neu, S. Iovtchev, A. Budde, H. Kiesewetter, R. Latza, and E. Donath, “Electroosmosis and polymer depletion layers near surface conducting particles are detectable by low frequency electrorotation,” Colloids Surf. A Physicochem. Eng. Asp. 149(1), 389–396 (1999).
[Crossref]

Kim, S.

S. Chien, L. A. Sung, S. Kim, A. M. Burke, and S. Usami, “Determination of aggregation force in rouleaux by fluid mechanical technique,” Microvasc. Res. 13(3), 327–333 (1977).
[Crossref] [PubMed]

LaCelle, P. L.

R. I. Weed, P. L. LaCelle, and E. W. Merrill, “Metabolic dependence of red cell deformability,” J. Clin. Invest. 48(5), 795–809 (1969).
[Crossref] [PubMed]

Lachmi, K.

V. Schechner, I. Shapira, S. Berliner, D. Comaneshter, T. Hershcovici, J. Orlin, D. Zeltser, M. Rozenblat, K. Lachmi, M. Hirsch, and Y. Beigel, “Significant dominance of fibrinogen over immunoglobulins, C-reactive protein, cholesterol and triglycerides in maintaining increased red blood cell adhesiveness/aggregation in the peripheral venous blood: a model in hypercholesterolaemic patients,” Eur. J. Clin. Invest. 33(11), 955–961 (2003).
[Crossref] [PubMed]

Latza, R.

H. Bäumler, B. Neu, S. Iovtchev, A. Budde, H. Kiesewetter, R. Latza, and E. Donath, “Electroosmosis and polymer depletion layers near surface conducting particles are detectable by low frequency electrorotation,” Colloids Surf. A Physicochem. Eng. Asp. 149(1), 389–396 (1999).
[Crossref]

Laxhuber, R.

K. Fricke, K. Wirthensohn, R. Laxhuber, and E. Sackmann, “Flicker spectroscopy of erythrocytes. A sensitive method to study subtle changes of membrane bending stiffness,” Eur. Biophys. J. 14(2), 67–81 (1986).
[PubMed]

Lee, K.

K. Lee, C. Wagner, and A. V. Priezzhev, “Assessment of the “cross-bridge”-induced interaction of red blood cells by optical trapping combined with microfluidics,” J. Biomed. Opt. 22(9), 091516 (2017).
[Crossref] [PubMed]

Lenz, M.

T. Betz, M. Lenz, J. F. Joanny, and C. Sykes, “ATP-dependent mechanics of red blood cells,” Proc. Natl. Acad. Sci. U.S.A. 106(36), 15320–15325 (2009).
[Crossref] [PubMed]

Llaudet-Planas, E.

A. Makhro, R. Huisjes, L. P. Verhagen, M. M. Mañú-Pereira, E. Llaudet-Planas, P. Petkova-Kirova, J. Wang, H. Eichler, A. Bogdanova, R. van Wijk, J.-L. Vives-Corrons, and L. Kaestner, “Red Cell Properties after Different Modes of Blood Transportation,” Front. Physiol. 7, 288 (2016).
[Crossref] [PubMed]

Lominadze, D.

D. Lominadze and W. L. Dean, “Involvement of fibrinogen specific binding in erythrocyte aggregation,” FEBS Lett. 517(1-3), 41–44 (2002).
[Crossref] [PubMed]

Longo, G.

M. Girasole, G. Pompeo, A. Cricenti, G. Longo, G. Boumis, A. Bellelli, and S. Amiconi, “The how, when, and why of the aging signals appearing on the human erythrocyte membrane: an atomic force microscopy study of surface roughness,” Nanomedicine (Lond.) 6(6), 760–768 (2010).
[Crossref] [PubMed]

Makhro, A.

A. Makhro, R. Huisjes, L. P. Verhagen, M. M. Mañú-Pereira, E. Llaudet-Planas, P. Petkova-Kirova, J. Wang, H. Eichler, A. Bogdanova, R. van Wijk, J.-L. Vives-Corrons, and L. Kaestner, “Red Cell Properties after Different Modes of Blood Transportation,” Front. Physiol. 7, 288 (2016).
[Crossref] [PubMed]

Mañú-Pereira, M. M.

A. Makhro, R. Huisjes, L. P. Verhagen, M. M. Mañú-Pereira, E. Llaudet-Planas, P. Petkova-Kirova, J. Wang, H. Eichler, A. Bogdanova, R. van Wijk, J.-L. Vives-Corrons, and L. Kaestner, “Red Cell Properties after Different Modes of Blood Transportation,” Front. Physiol. 7, 288 (2016).
[Crossref] [PubMed]

Meiselman, H. J.

S. Rad, H. J. Meiselman, and B. Neu, “Impact of glycocalyx structure on red cell-red cell affinity in polymer suspensions,” Colloids Surf. B Biointerfaces 123, 106–113 (2014).
[Crossref] [PubMed]

M. Uyuklu, M. Cengiz, P. Ulker, T. Hever, J. Tripette, P. Connes, N. Nemeth, H. J. Meiselman, and O. K. Baskurt, “Effects of storage duration and temperature of human blood on red cell deformability and aggregation,” Clin. Hemorheol. Microcirc. 41(4), 269–278 (2009).
[PubMed]

B. Neu, R. Wenby, and H. J. Meiselman, “Effects of dextran molecular weight on red blood cell aggregation,” Biophys. J. 95(6), 3059–3065 (2008).
[Crossref] [PubMed]

M. W. Rampling, H. J. Meiselman, B. Neu, and O. K. Baskurt, “Influence of cell-specific factors on red blood cell aggregation,” Biorheology 41(2), 91–112 (2004).
[PubMed]

O. K. Baskurt and H. J. Meiselman, “Blood rheology and hemodynamics,” Semin. Thromb. Hemost. 29(5), 435–450 (2003).
[Crossref] [PubMed]

B. Neu and H. J. Meiselman, “Depletion-Mediated Red Blood Cell Aggregation in Polymer Solutions,” Biophys. J. 83(5), 2482–2490 (2002).
[Crossref] [PubMed]

H. Bäumler, B. Neu, R. Mitlöhner, R. Georgieva, H. J. Meiselman, and H. Kiesewetter, “Electrophoretic and aggregation behavior of bovine, horse and human red blood cells in plasma and in polymer solutions,” Biorheology 38(1), 39–51 (2001).
[PubMed]

Merrill, E. W.

R. I. Weed, P. L. LaCelle, and E. W. Merrill, “Metabolic dependence of red cell deformability,” J. Clin. Invest. 48(5), 795–809 (1969).
[Crossref] [PubMed]

Meyerstein, N.

A. Pribush, D. Zilberman-Kravits, and N. Meyerstein, “The mechanism of the dextran-induced red blood cell aggregation,” Eur. Biophys. J. 36(2), 85–94 (2007).
[Crossref] [PubMed]

Mitlöhner, R.

H. Bäumler, B. Neu, R. Mitlöhner, R. Georgieva, H. J. Meiselman, and H. Kiesewetter, “Electrophoretic and aggregation behavior of bovine, horse and human red blood cells in plasma and in polymer solutions,” Biorheology 38(1), 39–51 (2001).
[PubMed]

Mohandas, N.

N. Mohandas and S. B. Shohet, “The role of membrane-associated enzymes in regulation of erythrocyte shape and deformability,” Clin. Haematol. 10(1), 223–237 (1981).
[PubMed]

Nemeth, N.

M. Uyuklu, M. Cengiz, P. Ulker, T. Hever, J. Tripette, P. Connes, N. Nemeth, H. J. Meiselman, and O. K. Baskurt, “Effects of storage duration and temperature of human blood on red cell deformability and aggregation,” Clin. Hemorheol. Microcirc. 41(4), 269–278 (2009).
[PubMed]

Neu, B.

S. Rad, H. J. Meiselman, and B. Neu, “Impact of glycocalyx structure on red cell-red cell affinity in polymer suspensions,” Colloids Surf. B Biointerfaces 123, 106–113 (2014).
[Crossref] [PubMed]

B. Neu, R. Wenby, and H. J. Meiselman, “Effects of dextran molecular weight on red blood cell aggregation,” Biophys. J. 95(6), 3059–3065 (2008).
[Crossref] [PubMed]

M. W. Rampling, H. J. Meiselman, B. Neu, and O. K. Baskurt, “Influence of cell-specific factors on red blood cell aggregation,” Biorheology 41(2), 91–112 (2004).
[PubMed]

B. Neu and H. J. Meiselman, “Depletion-Mediated Red Blood Cell Aggregation in Polymer Solutions,” Biophys. J. 83(5), 2482–2490 (2002).
[Crossref] [PubMed]

H. Bäumler, B. Neu, R. Mitlöhner, R. Georgieva, H. J. Meiselman, and H. Kiesewetter, “Electrophoretic and aggregation behavior of bovine, horse and human red blood cells in plasma and in polymer solutions,” Biorheology 38(1), 39–51 (2001).
[PubMed]

H. Bäumler, B. Neu, S. Iovtchev, A. Budde, H. Kiesewetter, R. Latza, and E. Donath, “Electroosmosis and polymer depletion layers near surface conducting particles are detectable by low frequency electrorotation,” Colloids Surf. A Physicochem. Eng. Asp. 149(1), 389–396 (1999).
[Crossref]

Nicolau, C.

A. Cudd, T. Arvinte, B. Schulz, and C. Nicolau, “Dextran protection of erythrocytes from low-pH-induced hemolysis,” FEBS Lett. 250(2), 293–296 (1989).
[Crossref] [PubMed]

Orlin, J.

V. Schechner, I. Shapira, S. Berliner, D. Comaneshter, T. Hershcovici, J. Orlin, D. Zeltser, M. Rozenblat, K. Lachmi, M. Hirsch, and Y. Beigel, “Significant dominance of fibrinogen over immunoglobulins, C-reactive protein, cholesterol and triglycerides in maintaining increased red blood cell adhesiveness/aggregation in the peripheral venous blood: a model in hypercholesterolaemic patients,” Eur. J. Clin. Invest. 33(11), 955–961 (2003).
[Crossref] [PubMed]

Petkova-Kirova, P.

A. Makhro, R. Huisjes, L. P. Verhagen, M. M. Mañú-Pereira, E. Llaudet-Planas, P. Petkova-Kirova, J. Wang, H. Eichler, A. Bogdanova, R. van Wijk, J.-L. Vives-Corrons, and L. Kaestner, “Red Cell Properties after Different Modes of Blood Transportation,” Front. Physiol. 7, 288 (2016).
[Crossref] [PubMed]

Pompeo, G.

M. Girasole, G. Pompeo, A. Cricenti, G. Longo, G. Boumis, A. Bellelli, and S. Amiconi, “The how, when, and why of the aging signals appearing on the human erythrocyte membrane: an atomic force microscopy study of surface roughness,” Nanomedicine (Lond.) 6(6), 760–768 (2010).
[Crossref] [PubMed]

Pribush, A.

A. Pribush, D. Zilberman-Kravits, and N. Meyerstein, “The mechanism of the dextran-induced red blood cell aggregation,” Eur. Biophys. J. 36(2), 85–94 (2007).
[Crossref] [PubMed]

Priezzhev, A. V.

K. Lee, C. Wagner, and A. V. Priezzhev, “Assessment of the “cross-bridge”-induced interaction of red blood cells by optical trapping combined with microfluidics,” J. Biomed. Opt. 22(9), 091516 (2017).
[Crossref] [PubMed]

Rad, S.

S. Rad, H. J. Meiselman, and B. Neu, “Impact of glycocalyx structure on red cell-red cell affinity in polymer suspensions,” Colloids Surf. B Biointerfaces 123, 106–113 (2014).
[Crossref] [PubMed]

Rampling, M. W.

M. W. Rampling, H. J. Meiselman, B. Neu, and O. K. Baskurt, “Influence of cell-specific factors on red blood cell aggregation,” Biorheology 41(2), 91–112 (2004).
[PubMed]

Rozenblat, M.

V. Schechner, I. Shapira, S. Berliner, D. Comaneshter, T. Hershcovici, J. Orlin, D. Zeltser, M. Rozenblat, K. Lachmi, M. Hirsch, and Y. Beigel, “Significant dominance of fibrinogen over immunoglobulins, C-reactive protein, cholesterol and triglycerides in maintaining increased red blood cell adhesiveness/aggregation in the peripheral venous blood: a model in hypercholesterolaemic patients,” Eur. J. Clin. Invest. 33(11), 955–961 (2003).
[Crossref] [PubMed]

Sackmann, E.

K. Fricke, K. Wirthensohn, R. Laxhuber, and E. Sackmann, “Flicker spectroscopy of erythrocytes. A sensitive method to study subtle changes of membrane bending stiffness,” Eur. Biophys. J. 14(2), 67–81 (1986).
[PubMed]

Schechner, V.

V. Schechner, I. Shapira, S. Berliner, D. Comaneshter, T. Hershcovici, J. Orlin, D. Zeltser, M. Rozenblat, K. Lachmi, M. Hirsch, and Y. Beigel, “Significant dominance of fibrinogen over immunoglobulins, C-reactive protein, cholesterol and triglycerides in maintaining increased red blood cell adhesiveness/aggregation in the peripheral venous blood: a model in hypercholesterolaemic patients,” Eur. J. Clin. Invest. 33(11), 955–961 (2003).
[Crossref] [PubMed]

Schulz, B.

A. Cudd, T. Arvinte, B. Schulz, and C. Nicolau, “Dextran protection of erythrocytes from low-pH-induced hemolysis,” FEBS Lett. 250(2), 293–296 (1989).
[Crossref] [PubMed]

Shapira, I.

V. Schechner, I. Shapira, S. Berliner, D. Comaneshter, T. Hershcovici, J. Orlin, D. Zeltser, M. Rozenblat, K. Lachmi, M. Hirsch, and Y. Beigel, “Significant dominance of fibrinogen over immunoglobulins, C-reactive protein, cholesterol and triglycerides in maintaining increased red blood cell adhesiveness/aggregation in the peripheral venous blood: a model in hypercholesterolaemic patients,” Eur. J. Clin. Invest. 33(11), 955–961 (2003).
[Crossref] [PubMed]

Shin, S.

S. Shin, J.X. Hou, and M. Singh, “Validation and application of a microfluidic ektacytometer (RheoScan-D) in measuring erythrocyte deformability,” Clin. Hemorheol. Microcirc.  37, 319–328 (2007)

Shohet, S. B.

N. Mohandas and S. B. Shohet, “The role of membrane-associated enzymes in regulation of erythrocyte shape and deformability,” Clin. Haematol. 10(1), 223–237 (1981).
[PubMed]

Singh, M.

S. Shin, J.X. Hou, and M. Singh, “Validation and application of a microfluidic ektacytometer (RheoScan-D) in measuring erythrocyte deformability,” Clin. Hemorheol. Microcirc.  37, 319–328 (2007)

Sixma, J. J.

P. J. Bronkhorst, J. Grimbergen, G. J. Brakenhoff, R. M. Heethaar, and J. J. Sixma, “The mechanism of red cell (dis)aggregation investigated by means of direct cell manipulation using multiple optical trapping,” Br. J. Haematol. 96(2), 256–258 (1997).
[Crossref] [PubMed]

Steffen, P.

P. Steffen, C. Verdier, and C. Wagner, “Quantification of depletion-induced adhesion of red blood cells,” Phys. Rev. Lett. 110(1), 018102 (2013).
[Crossref] [PubMed]

Sung, L. A.

S. Chien, L. A. Sung, S. Kim, A. M. Burke, and S. Usami, “Determination of aggregation force in rouleaux by fluid mechanical technique,” Microvasc. Res. 13(3), 327–333 (1977).
[Crossref] [PubMed]

Sykes, C.

T. Betz, M. Lenz, J. F. Joanny, and C. Sykes, “ATP-dependent mechanics of red blood cells,” Proc. Natl. Acad. Sci. U.S.A. 106(36), 15320–15325 (2009).
[Crossref] [PubMed]

Tejedor, M. C.

F. J. Alvarez, A. Herráez, M. C. Tejedor, and J. C. Díez, “Behaviour of isolated rat and human red blood cells upon hypotonic-dialysis encapsulation of carbonic anhydrase and dextran,” Biotechnol. Appl. Biochem. 23(Pt 2), 173–179 (1996).
[PubMed]

Tripette, J.

M. Uyuklu, M. Cengiz, P. Ulker, T. Hever, J. Tripette, P. Connes, N. Nemeth, H. J. Meiselman, and O. K. Baskurt, “Effects of storage duration and temperature of human blood on red cell deformability and aggregation,” Clin. Hemorheol. Microcirc. 41(4), 269–278 (2009).
[PubMed]

Ulker, P.

M. Uyuklu, M. Cengiz, P. Ulker, T. Hever, J. Tripette, P. Connes, N. Nemeth, H. J. Meiselman, and O. K. Baskurt, “Effects of storage duration and temperature of human blood on red cell deformability and aggregation,” Clin. Hemorheol. Microcirc. 41(4), 269–278 (2009).
[PubMed]

Usami, S.

S. Chien, L. A. Sung, S. Kim, A. M. Burke, and S. Usami, “Determination of aggregation force in rouleaux by fluid mechanical technique,” Microvasc. Res. 13(3), 327–333 (1977).
[Crossref] [PubMed]

Uyuklu, M.

M. Uyuklu, M. Cengiz, P. Ulker, T. Hever, J. Tripette, P. Connes, N. Nemeth, H. J. Meiselman, and O. K. Baskurt, “Effects of storage duration and temperature of human blood on red cell deformability and aggregation,” Clin. Hemorheol. Microcirc. 41(4), 269–278 (2009).
[PubMed]

van Wijk, R.

A. Makhro, R. Huisjes, L. P. Verhagen, M. M. Mañú-Pereira, E. Llaudet-Planas, P. Petkova-Kirova, J. Wang, H. Eichler, A. Bogdanova, R. van Wijk, J.-L. Vives-Corrons, and L. Kaestner, “Red Cell Properties after Different Modes of Blood Transportation,” Front. Physiol. 7, 288 (2016).
[Crossref] [PubMed]

Verdier, C.

P. Steffen, C. Verdier, and C. Wagner, “Quantification of depletion-induced adhesion of red blood cells,” Phys. Rev. Lett. 110(1), 018102 (2013).
[Crossref] [PubMed]

Verhagen, L. P.

A. Makhro, R. Huisjes, L. P. Verhagen, M. M. Mañú-Pereira, E. Llaudet-Planas, P. Petkova-Kirova, J. Wang, H. Eichler, A. Bogdanova, R. van Wijk, J.-L. Vives-Corrons, and L. Kaestner, “Red Cell Properties after Different Modes of Blood Transportation,” Front. Physiol. 7, 288 (2016).
[Crossref] [PubMed]

Vives-Corrons, J.-L.

A. Makhro, R. Huisjes, L. P. Verhagen, M. M. Mañú-Pereira, E. Llaudet-Planas, P. Petkova-Kirova, J. Wang, H. Eichler, A. Bogdanova, R. van Wijk, J.-L. Vives-Corrons, and L. Kaestner, “Red Cell Properties after Different Modes of Blood Transportation,” Front. Physiol. 7, 288 (2016).
[Crossref] [PubMed]

Wagner, C.

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P. Steffen, C. Verdier, and C. Wagner, “Quantification of depletion-induced adhesion of red blood cells,” Phys. Rev. Lett. 110(1), 018102 (2013).
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Wang, J.

A. Makhro, R. Huisjes, L. P. Verhagen, M. M. Mañú-Pereira, E. Llaudet-Planas, P. Petkova-Kirova, J. Wang, H. Eichler, A. Bogdanova, R. van Wijk, J.-L. Vives-Corrons, and L. Kaestner, “Red Cell Properties after Different Modes of Blood Transportation,” Front. Physiol. 7, 288 (2016).
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R. I. Weed, P. L. LaCelle, and E. W. Merrill, “Metabolic dependence of red cell deformability,” J. Clin. Invest. 48(5), 795–809 (1969).
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B. Neu, R. Wenby, and H. J. Meiselman, “Effects of dextran molecular weight on red blood cell aggregation,” Biophys. J. 95(6), 3059–3065 (2008).
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K. Fricke, K. Wirthensohn, R. Laxhuber, and E. Sackmann, “Flicker spectroscopy of erythrocytes. A sensitive method to study subtle changes of membrane bending stiffness,” Eur. Biophys. J. 14(2), 67–81 (1986).
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V. Schechner, I. Shapira, S. Berliner, D. Comaneshter, T. Hershcovici, J. Orlin, D. Zeltser, M. Rozenblat, K. Lachmi, M. Hirsch, and Y. Beigel, “Significant dominance of fibrinogen over immunoglobulins, C-reactive protein, cholesterol and triglycerides in maintaining increased red blood cell adhesiveness/aggregation in the peripheral venous blood: a model in hypercholesterolaemic patients,” Eur. J. Clin. Invest. 33(11), 955–961 (2003).
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A. Pribush, D. Zilberman-Kravits, and N. Meyerstein, “The mechanism of the dextran-induced red blood cell aggregation,” Eur. Biophys. J. 36(2), 85–94 (2007).
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M. Uyuklu, M. Cengiz, P. Ulker, T. Hever, J. Tripette, P. Connes, N. Nemeth, H. J. Meiselman, and O. K. Baskurt, “Effects of storage duration and temperature of human blood on red cell deformability and aggregation,” Clin. Hemorheol. Microcirc. 41(4), 269–278 (2009).
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A. Pribush, D. Zilberman-Kravits, and N. Meyerstein, “The mechanism of the dextran-induced red blood cell aggregation,” Eur. Biophys. J. 36(2), 85–94 (2007).
[Crossref] [PubMed]

K. Fricke, K. Wirthensohn, R. Laxhuber, and E. Sackmann, “Flicker spectroscopy of erythrocytes. A sensitive method to study subtle changes of membrane bending stiffness,” Eur. Biophys. J. 14(2), 67–81 (1986).
[PubMed]

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V. Schechner, I. Shapira, S. Berliner, D. Comaneshter, T. Hershcovici, J. Orlin, D. Zeltser, M. Rozenblat, K. Lachmi, M. Hirsch, and Y. Beigel, “Significant dominance of fibrinogen over immunoglobulins, C-reactive protein, cholesterol and triglycerides in maintaining increased red blood cell adhesiveness/aggregation in the peripheral venous blood: a model in hypercholesterolaemic patients,” Eur. J. Clin. Invest. 33(11), 955–961 (2003).
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D. Lominadze and W. L. Dean, “Involvement of fibrinogen specific binding in erythrocyte aggregation,” FEBS Lett. 517(1-3), 41–44 (2002).
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A. Makhro, R. Huisjes, L. P. Verhagen, M. M. Mañú-Pereira, E. Llaudet-Planas, P. Petkova-Kirova, J. Wang, H. Eichler, A. Bogdanova, R. van Wijk, J.-L. Vives-Corrons, and L. Kaestner, “Red Cell Properties after Different Modes of Blood Transportation,” Front. Physiol. 7, 288 (2016).
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K. Lee, C. Wagner, and A. V. Priezzhev, “Assessment of the “cross-bridge”-induced interaction of red blood cells by optical trapping combined with microfluidics,” J. Biomed. Opt. 22(9), 091516 (2017).
[Crossref] [PubMed]

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P. Steffen, C. Verdier, and C. Wagner, “Quantification of depletion-induced adhesion of red blood cells,” Phys. Rev. Lett. 110(1), 018102 (2013).
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Supplementary Material (1)

NameDescription
» Visualization 1       The procedure of moving the RBC from the microchannel chamber filled with fluorescent dextran to the chamber with with PBS.

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Figures (4)

Fig. 1
Fig. 1 (A) Schematic layout of the holographic laser tweezer combined with microfluidic chip and fluorescence microscopy for measuring the dextran adsorption on RBC. See text for details. (B) Sketch of the experimental chamber used for the measurement of dextran adsorption on RBC (not in scale). The larger chamber contained the fluorescent dextran solution (shown in yellow) and the microchannel was filled with PBS (shown in blue). Gentle flushing (indicated with blue arrows) prevented the diffusion of solutions. The inset shows the fluorescence image obtained from the cell trapped in the chamber and moved to the microchannel with PBS (see Visualization 1 for the transition procedure).
Fig. 2
Fig. 2 (A) The dependence of maximum fluorescence intensity on incubation time: black and red dots correspond to 0 and 135 minutes of RBC preincubation in PBS respectively. The microphotographs in the insets illustrate changes in the fluorescence intensity detected in the channel with PBS. Here, fluorescence intensity was normalized to the value obtained in the first point. Intensity of excitation was kept same for all measurements shown in (A) and was roughly estimated as 5 mW at the sample. The error bars correspond to the averaging over three independent microchannels used in the experiment. (B) and (C) show the fluorescence decay kinetics of one cell obtained at two values of excitation intensities: I0 ~5 mW (B), when no filter was used, and I0/24 (C), when the ND filter was installed.
Fig. 3
Fig. 3 (A) Dependence of the integral fluorescence intensity for the solution of dextran with different concentrations. (B) Schematic layout of the procedure used for measuring the fluorescence detection volume in the z-direction. A 2 µm fluorescent bead was moved with an optical trap using spatial light modulator, while the detection volume was fixed. (C) The dependence of bead’s fluorescence intensity on z-shift. The error bars in Fig. 3(A), C are within the marker sizes.
Fig. 4
Fig. 4 The dependence of the DI on shear stress for different incubation conditions. (A) After 30 minutes of incubation either in ◆ dextran solution (dextran 70 kDa, 20 mg/ml) or in ▲ PBS. (B) After 180 minutes of incubation either in ● dextran solution or in ■ PBS. Graphs show that the DI becomes higher for dextran incubated cells (i.e. cells become “softer”). The insets show typical diffraction patterns obtained at different shear stresses.

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