Vital erythrocyte phenomena: what can theory, modeling, and simulation offer?

Acheson DJ (1990) Elemenrary fluid dynamics. Oxford University Press, Oxford Agrawal R, Smart T, Nobre-Caroso J, Richards C, Bhatnagar R, Tufail A, Shima D, Jones PH, Pavesio C (2016) Assessment of red blood cell deformability in type 2 diabetes mewllitus and diabetic retinopathy by dual optical tweezers strectching technique. Sci Rep 6:15873 Agre P, Caselle JF, Zinkham WH, McMillan C, Bennett V (1985) Partial deficiency of erythrocyte spectrin in hereditary sphrocytosis. Nature 314:380–383 Alaarg A, Schiffelers RM, van Solinge WW, van Wijk R (2013) Red blood cell vesiculation in hereditary hemolytic anemia. Front Phys 4:365 Alberts B, Johnson A, Lewis J, Raff M, Roberts K, Walter P (2002) The Cell. Garland Science, New York Allan D, Mitchell RH (1977) Calcium ion-dependent diacylglycerol accumulation in erythrocytes is associated with microvesiculation but not with efflux of potassium ions. Biochem J 166:495–499 An X, Mohandas N (2008) Disorders of red cell membrane. Br J Haematol 141:367–375 An X, Guo X, Sum H, Morrow J, Glatzer W, Mohandas N (2004) Phosphatidylserine binding sites in erythrocyte spectrin: location and implications for membrane stability. Biochemistry 43:310–315 An X, Debnath G, Guo X, Liu S, Baines A, Glatzer W, Mohandas N (2005) Identification and functional characterization of protein 4.1R and actin-binding sites in erythrocyte beta spectrin: regulation of the interactions by phosphatidylinositil-4,5-bisphosphate. Biochemistry 44(31):10681–10688 Anong WA, Franco T, Chu H et al (2009) Adducin forms a bridge between the erythrocyte membrane and its cytoskeleton and regulates membrane cohesion. Blood 114(9):1904–1912 Asaro RJ, Zhu Q, Cabrales P (2018) Erythrocyte aging, protection via vesiculation: an analysis methodology via oscillatory flow. Front Physiol 9:1607 Asaro RJ, Zhu Q, Cabrales P, Carruthers A (2018) Do sleletal dynamics mediate sugar uptake and transport in human erythrocytes. Biophys J 114:1440–1454 Bæk R, Jørgensen MM (2017) Multiplexed phenotyping of small extracellular vesicles using protein microarray (EV Array). In: Exosimes and microvesicles: methods in molecular biology, vol 1543, pp 117–127 Barcroft J (1914) The respiratory function of blood. Cambridge University Press, Cambridge, p 73 Bardell D (1982) The roles of Taste and clean teeth in the discovery of bacteria by Antoni van Leeuwenhoek. Microbiol Rev 47:121–126 Bartosz G (1981) Aging of erythrocytes. VII. On the possible causes of inactivation of red cell enzymes. Mech Ageing Dev 13:379–385 Bennett V (1989) The spectrin–actin junction of erythrocyte membranes. Biochim Biophys Acta 988:107–121 Bennett V (1990) Spectrin: a structural mediator between diverse plasma membrane proteins and the cytoplasm. Curr Opin Cell Biol 2:51–56 Bennett V, Stenbuck PJ (1979) The membrane attachment protein for spectrin is associated with band 3 in human RBC membranes. Nature 280:468–473 Bennet V, Gilligan DM (1993) The spectrin-based membrane skeleton and micron-scale organization of the plasma membrane. Rev Cell Biol 9:27–66 Bessis M, Delpech G (1981) Discovery of the red blood cell with notes on priorities and credits of discoveries, past, present, and future. Blood Cells 7:447–480 Bessis M, Mohandas N, Feo C (1980) Automated ektacytometry: a new method of measuring red cell deformability and red cell indices. Blood Cells 6(3):15–27 Bevers EM, Williamson PI (2016) Getting to the outer leaflet: physiology of phosphatidylserine exposure at the plasma membrane. Physiol Rev 96:605–645 Boey SK, Boal DH, Discher DE (1998) Simulations of the erythrocyte skeleton at large deformation. I. Microscopic models. Biophys J 75:1573–1583 Bosman GJ, Kay MM (1990) Alterations of band 3 transport protein by cellular aging and disease: erythrocyte band 3 and glucose transporter share a functional relationship. Biochem Cell Biol 68:1419–1427 Bosman GJCGM, Lasonder E, Luten M, Roerdinkholder-Stoelwinder B, Novotný VMJ, Bos H, De Grip WJ (2008) The proteome of red cell membranes and vesicles during storage in blood bank conditions. Transfusion 48:827–835 Bosman GJCGM, Lasonder E, Groenen-Döpp YAM, Willekens FLA, Weere JM, Novotný VMJ (2010) Comparitive proteomics of erythrocyte aging in vivo and in vitro. J Proteom 73:396–402 Bosman G, Willekens FLA, Weere JM (2012) Erythocyte senesecence. In: Land F, Föller M (eds) Erythrocytes, physiology and pathophysiology. Imperial College Press, London Boulanger CM, Loyer X, Rautou PE, Amaabile N (2017) Extracellular vesicles in coronary artery disease. Nat Rev Cardiol 14:259–272 Braunstein GM, Roman RM, Clancy JP, Kudlow BA, Taylor AL et al (2001) Cystic fibrosis transmembrane conductance regulator facilitates ATP release by stimulating a separate ATP channel for autocrine control of cell volume regulation. J Biol Chem 9:6621–6630 Brochard F, Lennon JF (1975) Frequency spectrum of the flicker phenomena erythrocytes. J Phys 36:1035–1047 Browicz T (1890) Further observation of motion phenomena on red blood cells in pathological states. Zbl med Wissen 28:625–627 Brown FLH (2003) Regulation of protein mobility via thermal membrane undulations. Biophys J 84:842–853 Brown FLH, Leitner DM, McCammon JA, Wilson KR (2000) Lateral diffusion of membrane proteins in the presence of static and dynamic corrals: suggestions for appropriate observables. Biophys J 78:2257–2269 Bruce LJ, Beckmann R, Ribeiro ML, Peters LL, Chasis JA, Delaunay J, Mohandas N, Anstee DJ, Tanner MJ (2003) A band 3-based macrocomplex of integral and peripheral proteins in the RBC membrane. Blood 101:4180–4188 Buffet PA, Milon G, Brousse V, Correas JM, Dousset B, Couvelard A et al (2012) Ex vivo perfusion of human spleens maintains clearing and processing functions. Blood 107:3745–3752 Butler J, Mohandas N, Waugh RE (2008) Integral protein linkage and the bilayer-skeletal separation energy in red blood cells. Biophys J 95:1826–1836 Buys AV, Rooy MJ, Sorna P, Van Papendorp D, Lipinski B (2013) Changes in red blood cell membrane structure in type 2 diabetes: a scanning electron and atomic force microscopy study. Cardiovasc Diabetol 12:25–31 Cantiello HF (1996) Role of the actin cytoskeleton in the regulation of the cystic fibrosis transmembrane conductance regulator. Exp Physiol 81:505–514 Chang SH, Low PS (2001) Regulation of the glycophorin C-protein 4.1 membrane-to-skeleton bridge and evaluation of its contribution to erythrocyte membrane stability. J Biol Chem 276:22223–22230 Chang CH, Takeuchi H, Ito T, Machida K, Ohnishi S (1981) Lateral mobility of erythrocyte membrane proteins studied by the fluorescence photobleaching recovery technique. J Biochem 90:997–1004 Chang HY, Li X, Li H, Em Karniadakis G (2016) MD/DPD multiscale framework for predicting morphology and stresses of red blood cells in health and disease. PLOS 10:1371–1393 Chasan B, Geisse NA, Pedatella K, Wooster DG, Teintze M, Carattino MD, Goldmann WH, Cantiello HF (2002) Evidence for direct interaction between actin and the cystic fibrosis transmembrane conductance regulator. Eur Biophys J 30:617–624 Chien S (1987) Red cell deformability and its relevance to blood flow. Ann Rev Physiol 49:177–192 Chin JJ, Jung EKY, Jung CY (1986) Structural basis of human erythrocyte glucose transporter function in reconstituted system. J Biol Chem 261:7101–7104 Chou AC, Fitch CD (1980) Hemolysis of mouse erythrocytes by ferriproporphin IV and cholorquibe. Chemotherapeutic implications. J Clin Investig 66:856–858 Chou AC, Fitch CD (1981) Mechanism of hemolysis induced by ferriprotoporhin IX. J Clin Investig 68:672–677 Ciana A, Achilli C, Gaur A, Minetti G (2017) Membrane remodeling and vesicle formation during ageing of human red blood cells. Cell Physiol Biochem 42:1127–1138 Ciana A, Achilli C, Minetti G (2017) Spectrin and other membrane-skeletal components in human red blood cells of different age. Cell Physiol Biochem 42:1139–1152 Cloherty EK, Sultzman LA, Zottola RJ, Carruthers A (1995) Net sugar transport is a multistep process: evidence for cytosolic sugar binding sites in erythrocytes. Biochemistry 34:15395–15406 Cloherty EK, Heard KS, Carruthers A (1996) Human erythrocyte sugar transport is incompatible with available carrier models. Biochemistry 35:10411–10421 Cloherty EK, Levin KB, Carruthers A (2001) The red blood cell glucose transporter presents multiple, nucleotide-sensitive sugar exit sites. Biochemistry 40:15549–15561 Coetzer TL, Palek J (1986) Partial spectrin deficiency in hereditary pyropoikilocytosis. Blood 67:919–924 Cohen CM, Tyler JM, Branton D (1980) Spectrin-actin associations studied by electron microscopy of shadowed preparations. Cell 21:875–883 Cunningham P, Afzal-Ahmed I, Naftalin RJ (2006) Docking studies show that D-glucose and quercetin slide through the transporter GLUT1. J Biol Chem 281(9):5797–5803 De La Cruz EM, Pollard TD (1994) Transient kinetic analysis of rhodamine phalloidin binding to actin filaments. Biochemistry 33:14387–14392 De La Cruz EM, Pollard TD (1996) Kinetics and thermodynamics of phalloidin binding to actin filaments from three divergent species. Biochemistry 35:14054–14061 Dearnley M, Chu T, Zhang Y, Looker O, Huang C, Klonis N, Yeoman J, Kenny S, Arora M, Osborne JM, Chandramohanadas R, Zhang S, Dixon MWA, Tilley L (2016) Reversible host cell modeling underpins deformability changes in malaria parasit sexual blood stages. PNAS 113(17):4800–4805 Del Giudice EM, Iolascon A, Pinto L, Nobili B, Perrotta S (1994) Erythrocyte membrane protein alterations underlying clinical heterogenity in heredirary spherocytosis. Br J Haematol 88:52–55 Delaynay J (1995) Genetic disorders of the red cell membrane. FEBS Lett 369:34–37 Deplaine G, Safeukui I, Jeddi F, Lacoste F, Brousse V et al (2011) The sensing of pooly deformable red blood cells by the human spleen can be mimicked in vitro. Blood 117(8):e88–e99 Dietrich HH, Ellsworth ML, Sprague RS, Darcey RG Jr (2000) Red blood cell regulation of microvascular tone through adenosine triphosphate. Am J Physiol 278:H1294–H1298 Discher DE (2000) New insights into erythrocyte membrane organization and microelasticity. Curr Opin Hematol 7:117–122 Discher DE, Boal DH, Boey SK (1998) Simulations of the erythrocyte cytoskeleton at large deformation. II. Micropipette aspiration. Biophys J 75:1584–1597 Dubus C, Fournier JB (2006) A Gaussian model for the membrane of red cells with cytoskeleton defects. Europhys Lett 75(1):181–187 Dumaswala UJ, Greenwalt TJ (1984) Human reuthrocytes shed exocytic vesicles in vivo. Transfusion 24:490–492 Elgsaeter A, Branton D (1974) Intramembrane particle aggregation in erythrocyte ghosts. J Cell Biol 63:1018–1030 Ellsworth ML, Ellis CG, Sprague RS (2016) Role of erythrocyte-released ATP in the regulation of microvascular oxygen supply in skeletal muscle. Acta Physiol 216(3):265–276 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 Fadeel B, Xue D (2009) The ins and outs of phospholipid asymmetry in the plasma membrane: roles in health and disease. Crit Rev Biochem Mol Biol 44(5):264–277 Fedosov DA, Peltomäki M, Gomper G (2014) Deformation and dynamics of red blood cells in flow through cylindrical microchannels. Soft Matter 10:4258–4267 Fischer H (1930) On haemin and the relationships between haemin and chorophyll. Nobel Prize Lecture, December 11, 1930 Forsyth AM, Wan J, Owrutsky PD, Abkarian M, Stone HA (2011) Multiscale approach to link red blood cell dynamics, shear viscosity, and ATP release. PNAS 108:10986–10991 Forsyth AM, Braunmüler S, Wan J, Franke T, Stone HA (2012) The effects of membrane cholesterol and simvastatin on red blood cell deformability. Microvasc Res 83:347–351 Fowler VM (1996) Regulation of actin filament length in erythroctes and striated muscle. Curr Opin Cell Biol 8:86–96 Fowler VM (2013) The human erythrocyte plasma membrane: a Rosetta Stone for decoding membrane–cytoskeleton structure. Curr Topics Membr 72:39–88 Freund J (2013) The flow of red blood cells through a narrow spleenlike slit. Phys Fluids 25:110807 Friedman MH (2008) Principles and models of biological transport. Springer, New York Gallagher PG (2004) Hereditary elliptocytosis: spectrin and protein 4.1R. Semin Hematol 41:142–164 Gallagher PG (2005) Red cell membrane disorders. Hemotology 2005:13–18 Gallagher PG, Ferriera JD (1997) Molecular basis of erythrocyte membrane disorders. Curr Opin Hemotol 4:128–135 Gambhire P, Atwell S, Iss C, Bedeu F, Ozerov I, Badens C, Helfer E, Villat A, Charrier A (2017) High aspect ratio sub-micrometer channels using wet etching: application to the dynamics of red blood cell transiting through biomimetic splenic slits. Small 13:1700967 Gautier EF, Leduc M, Cochet S, Bailly K, Lacombe C, Mohandas N, Guillonneau F, El Nemer W, Mayeux P (2018) Absolute preteome quantification of highly purified populations of circulating reticulocytes and mature erythrocytes. Blood Adv 2:2646–2657 Giorgi M, Cianci CD, Gallagher PG, Morrow JS (2001) Spectrin oligomerization is cooperatively coupled to membrane assembly: a linkage targeted by many hereditary hemolytic amemias. Exp Mol Pathol 70(3):215–230 Gokhin DS, Nowak RB, Khoory JA, de la Piedra A, Ghiran IC, Fowler VM (2015) Dynamic actin filaments control the mechanical behavior of the human red blood cell membrane. Mol Biol Cell 26:1699–1710 Golan DE, Veatch W (1980) Lateral mobility of band 3 in the human erythrocyte membrane studied by fluorescence photobleaching recovery: evidence for control by cytoskeletal interactions. PNAS 77(5):2537–2541 Golan DE, Corbett JD, Korsgren C, Thatte HS, Hayette S, Yawata Y, Cohen CM (1996) Control of band 3 lateral and rotational mobility by band 4.2 in intact erythrocytes: release of band 3 oligomers from low affinity binding sites. Biophys J 70:1534–1542 Gorter E, Grendel F (1927) On bimolecular layers of lipids on the chromocytes of the blood. J Exp Med 41:439–443 Guo Q, Duffy SP, Matthews K, Santoso AT, Scott MD, Ma H (2014) Microfluidic analysis of red blood cell deformability. J Biomech 47:1767–1776 Hall D, Hoshino M (2010) Effects of macromolecular crowding on intracellular diffusion from a single particle perspective. Biophys Rev 2:39–53 Hattangadi SM, Lodish HF (2007) Regulation of erythrocyte lifespan: do reactive oxygen species set the clock? J Clin Investig 117(8):2075–2077 Helgerson AL, Carruthers A (1989) Analysis of protein-mediated 3-O-methylglucose transport in rat erythrocytes: rejection of the altrnating carrier model for sugar transport. Biochemistry 28:4580–4594 Helgerson AL, Hebert DN, Naderi S, Carruthers A (1989) Characterization of two independent modes of action of ATP on human erythrocyte sugar transport. Biochemistry 28:6410–6417 Hochmuth RM, Marcus D (2002) Membrane tethers formed from blood cells with available area and determination of the adhesion energy. Biophys J 82:2964–2969 Hoffman JF (2001) Questions for red blood cell physiologists to ponder in this millenium. Blood Cells Mol Dis 27:57–61 Hu X, Peng F, Zhou HQ, Zhang ZH, Cheng WY, Feng HF (2000) The abmormality of glucose transporter in the erythrocyte membrane of Chinese type 2 diabetic patients. Biochim Biophys Acta 1466:306–314 Huisjes R, Bogdanova A, van Solinge WW, Schiffelers RM, Kaestner L, van Wijk R (2018) Squeezing for life—properties of red blood cell deformability. Front Phys 9:656 Iglesias-Fernandez J, Quinn PJ, Naftalin RJ, Domene C (2017) Membrane phase-dependent occlusion of intramolecular GLUT1 cavities demonstrated by simulations. Biophys J 112(6):1176–1184 Ipsaro JJ, Mondragón A (2010) Structural basis for spectrin recognition by ankyrin. Blood 115(20):4093–4101 Jacob HS, Winterhalter KH (1970) The role of hemoglobin heme loss in Heinz Body formation: studeis with a partially heme-deficient hemoglobin and with a gentically unstable hemoglobin. J Clin Investig 49:2008–2016 Jacob HS, MacDonald RA, Jandl JH (1963) Regulation of spleen growth and sequestering function. J Clin Investig 42:1476–1490 Jacquez JA (1983) Modulation of glucose transport in human red blood cells by ATP. Biochim Biophys Acta 727:367–378 Jagger JE, Bateman RM, Ellsworth ML, Ellis CG (2001) Role of erythrocyte in regulating local \(O_2\) delivery mediated by hemoglobin oxygenation. Am J Physiol Heart Physiol 280:H2833–2839 Jandl JH (1955) Sequestration by the spleen of red cells sentitized with incomplete antibody and with metallo-protein complexes (abstract). J Clin Investig 34:912 Jandl JH, Greeberg MS, Yonemoto RH, Castle WB (1956) Clinical determination of the sites of red cell sequestration in hemolytic anemias. J Clin Investig 35:842–867 Jandl JH, Jones AR, Castle WB (1957) The destruction of red cells by antibodies in man. I. Observations on the sequestration and lusis of red cells altered by immune mechanisms. J Clin Investig 36:1428–1459 Jiang W, Yu D, Xiaojian H, Feng P, Hanqing Z, Zhihong Z (2002) Effect on membrane transport in the erythrocytes by band 3 cross-linking. Chin Sci Bull 47:1889–1892 Johnson CP, Tang HY, Carag C, Speicher DW, Discher DE (2007) Forced unfolding of proteins within cells. Science 317:663–666 Jørgensen M, Bæk R, Pedersen S, Søndergaard EKL, Kristensrn SR, Varming K (2013) Extracellular vesicle (EV) array: microarray capturing of exosomes and other extracellular vesicles for multiplexed phenotyping. J Extracell Vesicles 2:20920 Jørgensen M, Bæk R, Varming K (2015) Potentials and capabilities of the extracellular vesicle (EV) array. J Extracell Vesicles 4:26048 Jung EKY, Chin JJ, Jung CY (1986) Structural basis of human erythrocyte glucose transporter function in reconstituted system. Hydrogen exchange. J Biol Chem 261:9155–9160 Khan AA, Hanada T, Mohseni M, Jeong JJ, Zeng L, Gaetani M, Li D, Speicher BC, Chishti AH (2008) Dematin and adducin provide a novel link between the spectrin cytoskeleton and human erythrocyte membrane by directly interacting with glucose transporter-1. J Biol Chem 283(21):14600–14609 Kim J, Lee HY, Shin S (2015) Advances in the measurement of red blood cell deformability: A brief review. J Cell Biotech 1:63–79 Kirschner-Zilber ER, Shakiai N (1982) The interactionb of hemin and bilirubin with the human membrane. Biochim Biophys Acta 690(1):20–30 Knowles DW, Chasis JA, Evans EA, Mohandas N (1994) Cooperative action between Band 3 and glycophorin A in human erythrocytes: immobilization of band 3 induced by antibodies to glycophorin A. Biophys J 66:1726–1732 Knowles DW, Tilley L, Mohandas N, Chasis JA (1997) Erythrocyte membrane vesiculation: model for the molecular mechanism of protein sorting. PNAS 94:12969–12974 Kodippili GC, Spector J, Sullivan C, Kuypers FA, Labotka R, Gallagher PG, Ritchie K, Low PS (2009) Imaging of the diffusion of single band 3 molecules on normal amd mutant erythrocytes. Blood 113:6237–6245 Kodippili GC, Spector J, Kang GE, Liu H, Wickrema A, Ritchie K, Low PS (2010) Analysis of the kinetics of band 3 diffusion in human erythrocytes during the assembly of the skeleton. Br J Haemotol 150(5):592–600 Koppel DE, Sheetz MP, Schindler M (1981) Matrix control of protein diffusion in biological membranes. PNAS 78(6):3576–3580 Koslover EF, Chan CK, Theriot JA (2016) Cytoplasmic flow and mixing due to deformation of motile cells. Biophys J 110(3):700–709 Kuhlman PA, Hughes CA, Bennet CA, Fowler V (1996) A new function for adducin: calcium/calmodulin-regulated capping of the barbed ends of actin filaments. J Biol Chem 271:7986–7991 Kuhn V, Diederich L, Stevenson TC IV, Kramer CM, Lückstädt W, Panknin C, Suvorava T, Isakson BE, Kelm M, Cortese-Krott MM (2017) Antioxid Redox Signal 26:718–742 Küster W (1917) Über die konstitution des hämins und modifikation des bilirubins. Z Physiol Chem 99:86 Küster W (1927) Über des chemismus der porphyrinbildung und die konstitution des hämins. Z Physiol Chem 172:199 Landsteiner K (1900) Zur Kenntnis der antifermentativen, lytis-chen und agglutinierenden Wirkungen des Blutserums und der Lymphe. Centralblatt fur Bacteriologie 27:357–362 Landsteiner K (1901) Ueber Agglutinationserscheinungen norm-alen menschlichen Blutes. Weiner Klinische Wochenschrift 46:1132–1134 Lange Y, Slayton JM (1982) Interaction of cholesterol and lysophosphatidylcholine in determaining red cell shape. J Lipid Res 23:1121–1127 Larson MC, Karafin MS, Hillery CA, Hogg N (2017) Phosphatidylethanolamine is progressively exposed on RBCs during storage. Trans Med 27:136–141 Laurén E, Tigistu-Shale F, Valkonen S, Westberg M, Valkeäjarvi A et al (2018) Phospholipid composition of packed red blood cells and that of extracellular vesciles show a high resemblence and stability during storage. Biochim Biophys Acta 1863:1–8 Law R, Carl P, Harper S, Dalhaimer P, Speicher DW, Discher DE (2003) Cooperativity in unfolding of tandem spectrin repeats. Biophys J 84:533–544 Leal JK, Adjobo-Hermans MJW, Bosman GJCM (2018) Red blood cell Homeostatis: mechanics and effects of microvesicle generation in health and disease. Front Phys 9:703 Lee JCM, Discher DE (2001) Deformation-enhanced fluctuations in the red cell skeleton with theoretical relations to elasticity, connectivity, and spectrin unfolding. Biophys J 81:3178–3192 Leitch JM, Carrithers A (2007) ATP-dependent transport complexity in human erythrocytes. Am J Physiol Cell Physiol 292:C974–C986 Leitch JM, Carrithers A (2009) \(\alpha\) and \(\beta\) monosaccharide transport in human erythrocytes. Am J Physiol Cell Physiol 296:C151–161 Leonard C, Conrad L, Guthmann M, Pollet H, Carquin M, Vermylen C, Gailly P, Van Der Smissen P, Minggeot-Leclercq MP, Tyteca D (2017) Contribution of plasma membrane lipid domains to red blood cell (re) shaping. Sci Rep 7(1):4264 Levin SV, Korenstein R (1991) Membrane fluctuations in erythrocytes are linked to Mg-ATP-dependent dynamic assembly of the membrane skeleton. Biophys J 60:733–737 Li X, Bennett V (1996) Identification of the spectrin subunit and domains required for formation of spectrin/adducin/actin complexes. J Biol Chem 271(26):15695–15702 Li H, Lykotrafitis G (2014) Erythrocyte membrane model with explicit description of the lipid bilayer and spectrin network. Biophys J 107:642–653 Li J, Dao M, Lim CT, Suresh S (2005) Spectrin-level modeling of the cytoskeleton and optical tweezers stretching of the erythrocyte. Biophys J 88:3707–3719 Li H, Zhang Y, Ha V, Lykotrafitis G (2016) Modeling of band 3 protein diffusion in the normal and defective red blood cell membrane. Soft Matter 12:3643–3653 Li H, Lu L, Li X, Buffet PA, Dao M, Karniadakis GE, Suresh S (2018) Mechanics of diseased red blood cells in human spleen and consequences for hereditary blood disorders. PNAS 115(38):9574–9579 Lin LC, Brown LH (2004) Dynamics of pinned membranes with application to protein diffusion on the surface of red blood cells. Biophys J 86:764–780 Liu SC, Pakek J (1980) Spectrin tetramer–dimer equilibrium and the stability of erythrocyte membrane skeletons. Nature 285:586–588 Liu SC, Windisch P, Kim S, Palek J (1984) Oligomeric states of spectrin in normal erythrocyte membrane: biochemical and electron microscopic studies. Cell 37(2):587–594 Liu SC, Zhai S, Lawler J, Palek J (1985) Hem-mediated dissociation of erythrocyte membrane skeletal proteins. J Biol Chem 260:12234–12239 Liu SC, Derick LH, Palek J (1987) Visualization of the hexagonal lattice in the erythrocyte membrane skeleton. J Cell Biol 104(3):527–536 Low PS, Waugh SM, Zinke K (1985) The role of hemoglobin denaturation and band 3 clustering in red cell aging. Science 227:531–533 Lowe AG, Walmsley AR (1986) The kinetics of glucose in human red blood cells. Biochim Biophys Acta 857:146–154 Lu H, Peng Z (2019) Boundary interal simulations of a red blood cell squeezing through a submicron slit under prescribed inlet and outlet pressures. Phys Fluids 31(3):031902 Lutz HU, Bogdanova A (2013) Mechanisms tagging senescent red blood cells for clearance in healthy humans. Front Phys 4:387 Lutz HU, Liu SH, Palek J (1977) Release of spectrin-free vesicles from human erythrocytes during ATP depletion. J Cell Biol 73:548–560 Lux SE (2015) Anatomy of the red blood cell membrane skeleton: unanswered questions. Blood 127(2):187–199 MacDonald IC, Ragan DM, Schmidt EE, Groom AC (1987) Kinetics of red blood cell passage through interendothelial slits into vevous sinuses in rat spleen, analyzed by in vivo microscopy. Microvasc Res 33:118–134 Manno S, Takakuwa Y, Mohandas N (2002) Identification of a functional role for lipid asymmetry in biological membranes: phosphatidylserine-skeletal protein interactions modulate membrane stability. PNAS 99:1943–1948 Manno S, Takakuwa Y, Mohandas N (2005) Modulation of erythrocyte membrane mechanical function by protein 4.1 phosphorylation. J Biol Chem 9:7581–7587 Mannu F, Arese P, Cappellini MD, Fiorelli G, Cappadoro M et al (1995) Role of hemichrome binding to erythrocyte membrane in the generation of band-3 alterations in beta-thalassemia intermedia erythrocytes. Blood 86:2014–2020 Marchesi VT, Steers E Jr (1968) Selective solubilization of a protein component of red cell membrane. Science 159:203–206 Marinkovic D, Zhang X, Yalcin S, Luciano JP, Brugnara C, Huber T, Ghaffari S (2007) Foxo3 is required for the regulation of oxidative stress in erythropoiesis. J Clin Investig 117(8):2133–2144 McMillan DE, Brooks SM (1982) Erythrocyte spectrin glucosylation in diabetes. Diabetes 31(3):64–69 Mebius RE, Kraal G (2005) Structure and function of the spleen. Nat Rev 5:606–616 Mohandas N, Chasis JA (1993) Red blood deformability, membrane material properties and shape regulation by transmembrane, skeletal and cytosolic proteins and lipids. Semin Hematol 30:171–192 Mohandas N, Gallagher PG (2008) Red cell membrane: past, present, and future. Blood 112:3939–3948 Mohandas N, Clark MR, Jacobs MS, Shohet SB (1980) Analysis of factors regulating erythrocyte deformability. J Clin Investig 66:563–573 Mohandas N, Chasis JA, Shohet SB (1983) The influence of membrane skeleton on red cell deformability, membrane material properties, and shape. Semin Hematol 20:225–242 Mohanty JG, Nagababu E, Rifkind JM (2014) Red blood cell oxidative stress inpairs oxygen delivery and induces red blood cell againg. Font Phys 5:1–6 Mueckler M, Thorens B (2013) The SLC2 (GLUT) family of membrane transporters. Mol Asp Med 34(2):121–138 Naftalin RJ, Smith PM, Roselaar SE (1985) Evidence for a non-uniform distribution of D-glucose within human red cells during net exist and counterflow. Biochem Biophys Acta 820:235–249 Narla J, Mohandas N (2017) Red cell membrane disorders. Int J Hematol 39:47–52 Nicolson GL (1976) Transmembrane control of the receptors on normal and tumor cells: I. Influence of cell surface components. Biophys Acta 457:57–108 Nielsen MH, Beck-Nielsen H, Andersen MN, Handberg A (2014) A flow cytometry method for characetrization of circulating cel-derived microparticles in plasma. J Extracell Vesciles 3:1–12 Ohno S, Terada N, Fujii Y, Ueda H (1994) Membrane skeleton in fresh unfixed erythrocytes as revealed by a rapid and deep-etching method. J Anat 185:415–420 Omori T, Ishikawa T, Barthes-Biesel D, Salsac A, Imai Y, Yamaguchi T (2012) Tension of red blood cell membrane in simple shear flow. Phys Rev E 86:056321 Palek J, Lux SE (1983) Red cell membrane skeletal defects in hereditary and acquired hemolytic anemia. Semin Hematol 20:189–224 Pan L, Yan R, Li W, Xu K (2018) Super-resolution microscopy reveals the native untrastructure of the erythrocyte cytoskeleton. Cell Rep 22:1151–1158 Pandey KB, Rizvi SI (2010) Markers of oxidative stress in reythrocytes and plasma during aging in humans. Oxidative Med Cell Longev 3(1):2–12 Pandey KB, Rizvi SI (2011) Biomarkers of oxidative stress in red blood cells. Biomed Papers Med Fac Univ Palacky Czeh Repub 155(2):131–136 Park Y, Best CA, Badizadegan K, Dasari RR, Feld MS, Kuriabova T, Henie ML, Levine AJ, Popescu G (2010) Measurement of red blood cell mechanics during morphological changes. PNAS 107(15):6731–6736 Peker S, Akar N, Demiralp DO (2012) Proteomic identification of erythrocyte membrane protein deficiency in hereditary spherocytosis. Mol Biol Rep 39:3161–3167 Peng Z, Zhu Q (2013) Deformation of the erythrocyte cytoskeleton in tank treading motions. Soft Matter 9(31):7617–7627 Peng Z, Asaro RJ, Zhu Q (2010) Multiscale simulation of erythrocyte membrane. Phys Rev E 81:031904 Peng Z, Asaro RJ, Zhu Q (2011) Multiscale modeling of erythrocytes in Stokes flow. J Fluid Mech 686:299–337 Peng Z, Li X, Pivkin IV, Dao M, Karniadakis GE, Suresh S (2013) Lipid bilayer and cytoskeletal interactions in a red blood cell. PNAS 110(33):13356–13361 Perrotta S, Gallagher PG, Mohandas N (2008) Hereditary spherocytosis. Lancet 372:1411–1426 Pesciotta EN, Sriswasdi S, Tang HY, Mason PJ, Speicher M (2012) A label-free proteome anaqlysis strategy for identifying quantitative changes in erythrocyte membranes induced by red cell disorders. J Proteom 76:194–202 Picart C, Discher DE (1999) Actin protofilament orientation at the erythrocyte membrane. Biophys J 77(2):865–878 Picart C, Dalhaimer P, Discher DE (2000) Actin protofilament orientation of the erythrocyte membrane skeleton. Biophys J 79:2987–3000 Picot J, Ndour PA, Lefevre SD, El Nemer W, Tawfik H, Gallimand J, Da Costa L, Ribeil JA, de Montalembert M, Brousse V, Le Pioufle B, Buffet P, Le Van KC, Francais O (2015) A biomimetic microfluidic chip to study the circulation and mechanical retention of red blood cells in the spleen. Am J Hematol 90:339–345 Pielak GJ (2005) A model of intracellular organization. PNAS 102:5901–5902 Pozrikidis C (2003) Modeling and simulation of capsules and biological cells. Chapman & Hall/CRC, Boca Raton Pratt AG, Xiao Y-F, Ausiello DA, Cantiello HF (1995) cAMP-independent regulation CFTR by the actin cytoskeleton. Am J Physiol 268:C1552–1561 Rachmilewitz EA (1974) Denaturation of the normal and abnormal hemoglobin molecule. Semin Hemotol 11:441–462 Reid ME, Takakuwa Y, Conboy J, Tchernia G, Mohandas N (1990) Glycophorin C content of human erythrocyte membrane is regulated by protein 4.1. Blood 75:2229–2234 Ridger VC, Boulanger CM, Angelillo-Scherrer A, Badimon L, Blanc-Brude O, Bochaton-Piallat ML, Boilard E, Buzas EI, Caporali A et al (2017) Microvesicles in vascular homeostatis and diseases. Thromb Haemost 117:1296–1316 Rief MJ, Pascual J, Saraste M, Gaub HE (1999) Single molecule force spectroscopy of spectrin repeats: low unfolding forces in helix bundles. J Mol Biol 286:553–561 Rifkind JM, Nagababu E (2013) Hemoglobin redox reactions and red blood cell aging. Antioxid Redox Signal 18:2274–2283 Rifkind JM, Ramasamy S, Manoharan PT, Nagababu E, Mohanty JG (2004) Antioxid Redox Signal 6:657–666 Rigat-Brugarolas LG, Bernabeu M, Elizalde A, de Niz M, Martin-Jaular L, Fernandez-Becerra C, Homs-Corbera A, del Portillo HA, Samitier J (2013) Human splenon-on-a-chip: design and validation of a microfluidic model resembling the interstitial slits and the fast and slow microcirculations. In: International conference on miniturized systems for chemistry and life sciences, pp 27–31 Rigat-Brugarolas A, Elizalde-Torrent M, Bernabeu MD, Niz LM-J, Fernandez-Becerra C, Homs-Corbera A, Samiter J, del Portillo HA (2014) A functional microengineered model of the human spleen-on-a-chip. Lab Chip 14:1715–1724 Rous P, Robertson OH (1917) The normal fate of erythrocytes: the findings in healthy animals. J Exp Med 25:651–673 Rybicki AC, Heath R, Lubin B, Schwartz RS (1988) Human erythrocyte protein 4.1 ia a phosphatidylserine binding protein. J Clin Investig 81:255–260 Safeukui I, Correas JM, Brousse V, Hirt D, Deplaine G, Buffert PA (2008) Retention of Plasmodium falciparum ring-infected erythrocytes in the slow, open microcirculation of the human spleen. Blood 112:2520–2528 Safeukui I, Buffet PA, Deplaine G, Perrot S, Brousse V, Ndour A, Nguyen M, Mercereau-Puijalon O, David PH, Milon G, Mohandas N (2012) Quantitative assessment of sensing and sequestration of spherocytic erythrocytes by the human spleen. Blood 120(2):424–430 Salas-Burgos A, Iserovich P, Zuniga F, Vera JC, Fishbarg J (2004) Predicting the three-dimimentional structure of the human faciliative glucose transporter GLIY1 by a novel evollutionary homology strategy: insights on the molecular mechanism of substrate migration, and binding sites for glucose and inhibitory molecules. Biophys J 87:2990–2999 Salehyar S, Zhu Q (2016) Deformation and internal stress in a red blood cell as it is driven through a slit by an incoming flow. Soft Matter 12:3156–3164 Salehyar S, Zhu Q (2017) Effects of stiffness and volume on the transit time of an erythrocyte through a slit. Biomech Model Mechanobiol 16(3):921–931 Salzer U, Zhu R, Luten M, Isobe H, Pastushenko V, Perkmann T et al (2008) Transfusion 48:451–462 Saxtion M, Jacobson K (1997) Single particle tracking: applications to membrane dynamics. Biophys J 26:373–399 Saxton M (1995) Single-particle tracking: effects of corrals. Biophys J 69:389–398 Saxton M (1996) Anomalous diffusion due to binding: a monte carlo study. Biophys J 70:250–1262 Saxton M (1997) Single-particle tracking: the distribution of diffusion coefficients. Biophys J 72:1744–1753 Schwartz HP, Dorner F (2003) Karl Landsteiner and his major contributions to haematology. Br J Haematol 121:556–565 Schwartz RS, Madsen JW, Rybicki AC, Nagel NL (1991) Oxidation of spectrin and deformability in diabetic erythrocytes. Diabetes 40(6):701–708 Sheetz MP, Singer SJ (1974) Biological membranes as bilayer couples. A molecular mechanism of drug-erythrocyte interactions. PNAS 71:4457–4461 Shin S, Ku Y, Babu N, Singh M (2007) Erythrocyte deformability and its variation in diabetes mettilus. Indian J Exp Biol 45:121–128 Shotton D, Thompson K, Wofsy L, Branton D (1978) Appearance and distribution of surface proteins of the human erythrocyte membrane. An electron microscope and immunochemical labeling study. J Cell Biol 76:512–531 Shviro Y, Zibler I, Shaklai N (1982) The interaction of hemoglobin with phosphatidyserine vesicles. Biochim Biophys Acta 687:63–70 Speicher DW (1986) The present status of erythrocyte spectrin structure: the 106-residue repetitive structure is a basic feature of an entire class of proteins. J Cell Biochem 30:245–258 Sprague RS, Ellsworth ML (2012) Erythrocyte-derived ATP and perfusion distribution: Role of intracellular and intercellular comminication. Microcirculation 19(5):430–439 Sprague RS, Ellsworth ML, Stephenson AH, Lonigro AH (1996) ATP: the red blood cell link to NO and local control of the pulmonary circulation. Am J Physiol 271:H2717–2722 Sprague RS, Ellsworth ML, Stephenson AH, Kleinhenz ME, Lonigro AJ (1998) deformation-induced ATP release from red blood cells requires CFTR activity. Am J Physiol Heart C 275:H1726–171732 Sridharan M, Adderley SP, Bowles EA, Egan TM, Stephenson AH, Ellsworth ML, Sprague RS (2010) Pannexin is the conduit for low oxygen tension-induced ATP release from human erythrocytes. Am J Physiol Heart Circ Phusiol 299(4):H1146–H1152 Sriswasdi S, Harper SL, Tang HY, Gallagher PG, Speicher DW (2014) Probing large conformational rearrangements in wild-type and nutant spectrin using structural mass spectrometry. PNAS 111(5):1801–1806 Stauber H, Waisman D, Netanel K, Sznitman J (2017) Red blood cell dynamics in biomimetic microfluidic networks of pulmonary alveolar capillaries. Biomicrofluidics 11:014103 Steck T, Fairbanks G, Wallach DFH (1971) Disposition of the major proteins in the isolated erythrocytes erythrocyte membrane. Proteolytic dissection. Biochemistry 10:2617–2624 Strey H, Peterson M, Sackmann E (1995) Measurement of erythrocyte membrane elasticity by flicker eigenmode decomposition. Biophys J 69(2):478–488 Tipping E, Ketterer B, Christodoulides L (1979) Interactions of small molecules with phospholipid bilayers. Biochem J 180:327–337 Tissot JD, Rubin O, Canellini G (2010) Analaysis and clinical relevance of microparticlea from red blood cells. Curr Opin Hematol 17:571–577 Tsubota K, Wada S, Liu H (2014) Elastic behavior of a red blood cell with the membrane’s nonuniform natural state: equilibrium shape, motion transition under shear flow, and elongation during tank-treading motion. Biomech Model Mechanobiol 13:735–746 Tuvia S, Almagor A, Bitler A, Levin S, Korenstein R, Yedgar S (1997) Cell membrane fluctuations are regulated by nedium macroviscosity: evidence for a metabolic drivibg force. PNAS 94:5045–5049 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 van Leeuwenhoek A (1675) Letter dated March 26, 1675 to the Royal Society, London Verldeij AJ, Zwaal RF, Roelofsen B, Comfurius P, Kastelijn D, van Deenen LL (1973) The assymmetric distribution of phospholipids in the human red cell membrane. A combined study using phospholipases and freeze-etch electron microsccopy. Biochim Biophys Acta 323:178–193 Vrhovac I, Breljak D, Sabolic̀ I (2014) Glucose transporters in the mammalian blood cells. Peridicum Biologorum 116:131–138 Waugh RE, Hochmuth RM (1987) Mechanical equilibrium of thick, hollow, liquid membrane cylinders. Biophys J 52:391–400 Willekens FLA, Bregt-Roerdinkholder B, Groenen-döpp YA, Bos HJ, Bosman GJCGM, van den Bos AG, Verkeij AJ, Weere JM (2003) Haemoglobin loss from erythrocytes in vivo results from spleen-facilitated vesiculation. Blood 101:747–751 Willekens FLA, Weere JM, Groenen-döpp YA, Bregt-Roerdinkholder B, de Pauw B, Bosman GJCGM (2003) Erythrocyte vesiculation: a self-protective mechanism? Br J Haematol 141:549–556 Yan Y, Winograd E, Viel A, Cronin T, Harrison SC, Branton D (1993) Crystal structure of the repetitive segments of spectrin. Science 262:2027–2030 Yazdani A, Kalluri R, Bagchi P (2011) Tank-treading and tumbling frequencies of capsules and red blood cells. Phys Rev E 83:046305 Young LE, Platzer RF, Ervin DM, Ozzo MJ (1951) Hereditary spherocytosis. II Observations on the role of the spleen. Blood 6:1099–1113 Yu J, Branton D (1976) Reconstitution of intramembrane particles in recombinants of erythrocyte protein band 3 and lipid: effects of spectrin-actin association. PNAS 73:3591–3595 Zarà M, Guidetti GF, Camera M, Canobbio I, Amadio P, Torti M, Tremoli E, Barbieri SS (2019) Biology and role of extracellular vesicles (EVs) in the pathogenesis of thrombosis. Int J Mol Sci 20(11):2840–2872 Zhang R, Brown FL (2008) Cytoskeleton mediated effective elastic properties of model red blood cell membranea. J Chem Phys 129(6):065101 Zhang Y, Huang C, Kim S, Golkaram M, Dixon MA, Tilley L, Li J, Ahang S, Suresh S (2015) Multiple stiffening effects of nanoscale knobs on human red blood cells infected with Plasmofium falciparum malaria parasite. PNAS 112(19):6068–6073 Zhao H, Isfahani AHG, Olson LN, Freund JB (2010) A spectral boundary integral method for flowing blood cells. J Comput Phys 229:3726–3744 Zhu Q, Asaro R (2008) Spectrin folding vs. unfolding reactions and RBC membrane stiffness. Biophys J 94:2529–2545 Zhu Q, Asaro RJ (2019) Response modes of erythrocytes in high-frequency oscillatory shear flows. Phys Fluids 31(5):051901 Zhu Q, Vera C, Asaro R, Sche P, Sung LA (2007) A hybrid model for erythrocyte membrane: a single unit of protein network coupled with lipid bilayer. Biophys J 93:386–400 Zhu Q, Salehyar S, Cabrales P, Asaro R (2017) Prospects of human erythrocyte skeleton-bilayer dissociation during splenic flow. Biophy J 113(4):900–912 Zwaal RF, Schroit AJ (1997) Pathological implications of membrane asymmetry in blood cells. Blood 89:1121–1132 Zwaal RFA, Comfurius P, Bevers EM (2005) Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 62:971–988