Abstract. The presented review describes the structure and features of the functioning of the erythrocyte membrane. Its osmotic resistance is characterized as an indicator of the functional activity of the cell membrane. Changes under the influence of various physical and chemical factors are described. The reasons for its decrease are identified and the direction of maintaining metabolic stability under the influence of various pathological factors is indicated.

Article recieved: 25.07.2023

Ключові слова: erythrocyte, cell membrane, osmotic resistance of erythrocytes

Повний текст: PDF (Ukr)

1. 1. De Oliveira S, Saldanha C. An overview about erythrocyte membrane. Clin Hemorheol Microcirc. 2010;44(1):63-74.doi.org/10.3233/CH-2010-1253
2. 2. Daleke DL. Regulation of phospholipid asymmetry in the erythrocyte membrane. Curr Opin Hematol. 2008;15(3):191-5.doi.org/10.1097/MOH.0b013e3282f97af7
3. 3. Op den Kamp JAF, Roelofsen B, van Deenen LLM. Structural and dynamic aspects of phosphatidylcholine in the human erythrocyte membrane. Trends Biochem Sci. 1985;10(8):320-3.doi.org/10.1016/0968-0004(85)90173-2
4. 4. Boegheim JPJ, Van Linde M, Op Den Kamp JAF, Roelofsen B. The sphingomyelin pools in the outer and inner layer of the human erythrocyte membrane are composed of different molecular species. Biochim Biophys Acta Biomembr. 1983;735(3): 438-42.doi.org/10.1016/0005-2736(83)90160-8
5. 5. Belokoneva OS, Villegas E, Corzo G, Dai L, Nakajima T. The hemolytic activity of six arachnid cationic peptides is affected by the phosphatidylcholine-to-sphingomyelin ratio in lipid bilayers. Biochim Biophys Acta Biomembr. 2003;1617(1-2):22-30.doi.org/10.1016/j.bbamem.2003.08.010
6. 6. Aoki Y, Uenaka T, Aoki J, Umeda M, Inoue K. A Novel Peptide Probe for Studying the Transbilayer Movement of Phosphatidylethanolamine. J Biochem. 1994;116(2): 291-7.doi.org/10.1093/oxfordjournals.jbchem.a124522
7. 7. Miljanich GP, Nemes PP, White DL, Dratz EA. The asymmetric transmembrane distribution of phosphatidylethanolamine, phosphatidylserine, and fatty acids of the bovine retinal rod outer segment disk membrane. J Membr Biol. 1981;60(3),249-55.doi.org/10.1007/BF01992562
8. 8. Bütikofer P, Lin ZW, Chiu DT, Lubin B, Kuypers FA. Transbilayer distribution and mobility of phosphatidylinositol in human red blood cells. J Biol Chem. 1990;265(27):16035-8.doi.org/10.1016/S0021-9258(17)46183-7
9. 9. Clarke RJ, Hossain KR, Cao K. Physiological roles of transverse lipid asymmetry of animal membranes. Biochim Biophys Acta Biomembr. 2020;1862(10):183382.doi.org/10.1016/j.bbamem.2020.183382
10. 10. Sherratt SCR, Juliano RA, Mason RP. Eicosapentaenoic acid (EPA) has optimal chain length and degree of unsaturation to inhibit oxidation of small dense LDL and membrane cholesterol domains as compared to related fatty acids in vitro. Biochim Biophys Acta Biomembr. 2020;1862(7):183254.doi.org/10.1016/j.bbamem.2020.183254
11. 11. Ballweg S, Ernst R. Control of membrane fluidity: the OLE pathway in focus. Biol Chem. 2017;398(2):215-28.doi.org/10.1515/hsz-2016-0277
12. 12. Hon GM, Hassan MS, van Rensburg SJ, Abel S, van Jaarsveld P, Erasmus RT, et al. Red blood cell membrane fluidity in the etiology of multiple sclerosis. J Membr Biol. 2009;232(1-3):25-34.doi.org/10.1007/s00232-009-9213-1
13. 13. Suda T, Akamatsu A, Nakaya Y, Masuda Y, Desaki J. Alterations in erythrocyte membrane lipid and its fragility in a patient with familial lecithin: cholesterol acyltrasferase (LCAT) deficiency. J Med Invest. 2002;49(3-4):147-55.
14. 14. Luneva OG, Brazhe NA, Maksimova NV, Rodnenkov OV, Parshina EYu, Bryzgalova NYu, et al. Ion transport, membrane fluidity and haemoglobin conformation in erythrocyte from patients with cardiovascular diseases: Role of augmented plasma cholesterol. Pathophysiology. 2007;14(1):41-6.doi.org/10.1016/j.pathophys.2006.12.001
15. 15. Lin C, Cotton F, Boutique C, Dhermy D, Vertongen F, Gulbis B. Capillary gel electrophoresis: separation of major erythrocyte membrane proteins. J Chromatogr B Biomed. 2000;742(2): 411-9.doi.org/10.1016/S0378-4347(00)00205-X
16. 16. Li H, Lykotrafitis G. Erythrocyte membrane model with explicit description of the lipid bilayer and the spectrin network. Biophys J. 2014;107(3):642-53.doi.org/10.1016/j.bpj.2014.06.031
17. 17. Bennett V. Spectrin: a structural mediator between diverse plasma membrane proteins and the cytoplasm. Curr Opin Cell Biol. 1990;2(1):51-6.doi.org/10.1016/S0955-0674(05)80030-4
18. 18. Cohen CM, Foley SF. Spectrin-dependent and -independent association of F-actin with the erythrocyte membrane. J Cell Biol. 1980;86(2):694-8.doi.org/10.1083/jcb.86.2.694
19. 19. Smith AS, Nowak RB, Zhou S, Giannetto M, Gokhin DS, Papoin G, et al. Myosin IIA interacts with the spectrin-actin membrane skeleton to control red blood cell membrane curvature and deformability. PNAS. 2018;115(19):E4377-85.doi.org/10.1073/pnas.1718285115
20. 20. Antreas KC, Reithmeier RAF. Interaction of the human erythrocyte Band 3 anion exchanger 1 (AE1, SLC4A1) with lipids and glycophorin A: molecular organization of the Wright (Wr) blood group antigen. PLoS Comput Biol. 2018;14(7):e1006284.doi.org/10.1371/journal.pcbi.1006284
21. 21. Паламарчук В. И. Особенности радиационных изменений содержания стеринов и скволена в тканях лимфоидной системы и мембранах эритроцитов крыс. Радиобиология. 1990;30(3):321-7.
22. 22. Hess JR, D'Alessandro A. Red blood cell metabolism and preservation. Rossi's Principles of Transfusion Medicine. John Wiley & Sons Ltd; 2022. 708(143-157).doi.org/10.1002/9781119719809.ch14
23. 23. Jarolim P, Rubin HL, Zakova D, Storry J, Reid ME. Characterization of seven low incidence blood group antigens carried by erythrocyte band 3 protein: presented in part at the 49th annual meeting of the American Association of Blood Banks. Blood. 1998;92(12):4836-43.doi.org/10.1182/blood.V92.12.4836
24. 24. Scozzafava A, Mastrolorenzo A, Supuran CT. Modulation of carbonic anhydrase activity and its applications in therapy. Expert Opin Ther Pat. 2004:14(5):667-702.doi.org/10.1517/13543776.14.5.667
25. 25. Abe Y, Chaen T, Jin XR, Hamasaki T, Hamasaki N. Massspectrometric analyses of transmembrane proteins in human erythrocyte membrane. J Biochem. 2004;136(1):97-106.doi.org/10.1093/jb/mvh100
26. 26. Lew VL. Effect of ouabain on the Ca2+-dependent increase in K+ permeability in depleted guinea-pig red cells. Biochim Biophys Acta Biomembr. 1971;249(1):236-9.doi.org/10.1016/0005-2736(71)90100-3
27. 27. Geering K. Subunit assembly and functional maturation of Na,K-ATPase. J Membrane Biol. 1990;115:109-21.doi.org/10.1007/BF01869450
28. 28. Abed M, Feger M, Alzoubi K, Pakladok T, Frauenfeld L, Geiger C, et al. Sensitization of erythrocytes to suicidal erythrocyte death following water deprivation. Kidney Blood Press Res. 2013;37(6):567-78.doi.org/10.1159/000355737
29. 29. Quintanar-Escorza MA, González-Martínez MT, Navarro L, Maldonado M, Arévalo B, Calderón-Salinas JV. Intracellular free calcium concentration and calcium transport in human erythrocytes of lead-exposed workers. Toxicol Appl Pharmacol. 2007;220(1):1-8.doi.org/10.1016/j.taap.2006.10.016
30. 30. Shan F, Yang R, Ji T, Jiao F. Vitamin C inhibits aggravated eryptosis by hydrogen peroxide in glucose-6-phosphated dehydrogenase deficiency. Cell Physiol Biochem. 2016; 39(4):1453-62.doi.org/10.1159/000447848
31. 31. Wieschhaus A, Khan A, Zaidi A, Rogalin H, Hanada T, Liu F, et al. Calpain-1 knockout reveals broad effects on erythrocyte deformability and physiology. Biochem J. 2012;448(1):141-52.doi.org/10.1042/BJ20121008
32. 32. Bennett V. The membrane skeleton of human erythrocytes and its implications for more complex cells. Annu Rev Biochem. 1985;54(1):273-304.doi.org/10.1146/annurev.bi.54.070185.001421
33. 33. Rabuazzo AM, Buscema M, Vinci C, Caltabiano V, Anello M, Vigneri R, et al. Inhibition of the high-affinity glucose transporter GLUT 1 affects the sensitivity to glucose in a hamster-derived pancreatic beta cell line (HIT). Diabetologia. 1993; 36(11):1204-7.doi.org/10.1007/BF00401067
34. 34. Benga G. The first discovered water channel protein, later called aquaporin 1: Molecular characteristics, functions and medical implications. Mol Aspects Med. 2012;33(5-6):518-34.doi.org/10.1016/j.mam.2012.06.001
35. 35. Geyer R, Musa-Aziz R, Qin X, Boron WF. Relative CO2/NH3 selectivities of mammalian aquaporins 0-9 R. Am J Physiol Cell Physiol. 2013;304(10):C985-94.doi.org/10.1152/ajpcell.00033.2013
36. 36. Zhang D, Kiyatkin A, Bolin JT, Low PS. Crystallographic structure and functional interpretation of the cytoplasmic domain of erythrocyte membrane band 3. Blood. 2000;96(9):2925-33.doi.org/10.1182/blood.V96.9.2925
37. 37. White PH, Plishker GA. Calcium-dependent association of glutathione S-transferase with the human erythrocyte membrane. BBRC. 1983;114(2):488-92.doi.org/10.1016/0006-291X(83)90806-9
38. 38. Olszewska M, Wiatrow J, Bober J, Stachowska E, Gołembiewska E, Jakubowska K, et al. Oxidative stress modulates the organization of erythrocyte membrane cytoskeleton. Advances in Hygiene and Experimental Medicine. 2012;66: 534-42. doi.org/10.5604/17322693.1005677
39. 39. Cooper GM. The Cell: A Molecular Approach. Structure of the Plasma Membrane. 2nd edition. Sunderland (MA): Sinauer Associates; 2000.
40. 40. Kumar D, Rizvi SI. Erythrocyte membrane bound and plasma sialic acid during aging. Biologia. 2013;68(4):762-5.doi.org/10.2478/s11756-013-0207-1
41. 41. Lisowska E, Messeter L, Duk M, Czerwiński M, Lundblad A. A monoclonal antiglycophorin a antibody recognizing the blood group M determinant: Studies on the subspecificity. Mol Immunol. 1987;24(6):605-13.doi.org/10.1016/0161-5890(87)90041-1
42. 42. Klei TRL, de Back DZ, Asif PJ, Verkuijlen PJJH, Veldthuis M, Ligthart PC, et al. Glycophorin-C sialylation regulates Lu/BCAM adhesive capacity during erythrocyte aging. Blood Adv. 2018;2(1):14-24.doi.org/10.1182/bloodadvances.2017013094
43. 43. Salomao M, Chen K, Villalobos J, Mohandas N, An X, Chasis JA. Hereditary spherocytosis and hereditary elliptocytosis: aberrant protein sorting during erythroblast enucleation. Blood. 2010;116(2):267-9.doi.org/10.1182/blood-2010-02-264127
44. 44. Lawicki S, Covin RB, Powers AA. The Kidd (JK) blood group system. Transfus Med Rev. 2017;31(3):165-72.doi.org/10.1016/j.tmrv.2016.10.003
45. 45. Höher G, Fiegenbaum M, Almeida S. Molecular basis of the Duffy blood group system. Blood Transfus. 2018;16(1):93-100.
46. 46. Minetti G, Low PS. Erythrocyte signal transduction pathways and their possible functions. Curr Opin Hematol. 1997;4(2):116-21.doi.org/10.1097/00062752-199704020-00007
47. 47. Geekiyanage NM, Balanant MA, Sauret E, Saha S, Flower R, Lim CT, et al. A coarsegrained red blood cell membrane model to study stomatocyte-discocyte-echinocyte morphologies. PLOS One. 2019;14(4):e0215447.doi.org/10.1371/journal.pone.0215447
48. 48. Smith JE. Erythrocyte membrane: structure, function, and pathophysiology. Veterinary Pathology. 1987;24(6):471-6.doi.org/10.1177/030098588702400601
49. 49. Gevi F, D'Alessandro A, Rinalducci S, Zolla L. Alterations of red blood cell metabolome during cold liquid storage of erythrocyte concentrates in CPD-SAGM. J Proteomics. 2012;76:168-80.doi.org/10.1016/j.jprot.2012.03.012
50. 50. Möller MN, Orrico F, Villar SF, López AC, Silva N, Donzé M, et al. Oxidants and antioxidants in the redox biochemistry of human red blood cells. ACS Omega. 2023;8(1):147-68.doi.org/10.1021/acsomega.2c06768
51. 51. Çimen MYB. Free radical metabolism in human erythrocytes. Clin Chim Acta. 2008;390(1-2):1-11.doi.org/10.1016/j.cca.2007.12.025
52. 52. Tziakas D, Chalikias G, Grapsa A, Gioka T, Tentes I, Konstantinides S. Red blood cell distribution width - a strong prognostic marker in cardiovascular disease - is associated with cholesterol content of erythrocyte membrane. Clin Hemorheol Microcirc. 2012;51(4):243-54.doi.org/10.3233/CH-2012-1530
53. 53. Yammine A, Auezova L, Lizard G, Greige-Gerges H. Activity of Na+/K+- and Ca2+-ATPases in human erythrocyte membranes: protocol improvement, relation to cholesterol content, and effects of polyphenols. Biochimie. 2023;212:95-105.doi.org/10.1016/j.biochi.2023.04.010
54. 54. Muro SM, Lee JH, Stokes JV, Ross MK, Archer TM, Wills RW, et al. Effects of leukoreduction and storage on erythrocyte phosphatidylserine expression and eicosanoid concentrations in units of canine packed red blood cells. J Vet Intern Med. 2017;31(2):410-418.doi.org/10.1111/jvim.14664
55. 55. Zhbanov A, Lee YS, Son M, Jung MH, Eom K, Yang S. Effect of hemoglobin hydration on the physical properties of erythrocyte cytoplasm and whole blood. Electrochim Acta. 2023;438:141560.doi.org/10.1016/j.electacta.2022.141560
56. 56. Kaczmarska M, Fornal M, Messerli FH, et al. Erythrocyte membrane properties in patients with essential hypertension. Cell Biochem Biophys. 2013;67(3):1089-102.doi.org/10.1007/s12013-013-9613-9
57. 57. Burris SM, Eaton JW, White JG. Evaluation of the role of diacylglycerol in calciuminduced erythrocyte shape change and rigidity. J Lab Clin Med. 1980;86(4):749-56.
58. 58. Rechsteiner MC. Uptake of proteins by red blood cells. Exp Cell Res. 1975;93(2):487-92.doi.org/10.1016/0014-4827(75)90478-4
59. 59. Lominadze D, Dean WL, Tyagi SC, Roberts AM. Mechanisms of fibrinogen-induced microvascular dysfunction during cardiovascular disease. Acta Physiol. 2010;198(1):1-13.doi.org/10.1111/j.1748-1716.2009.02037.x
60. 60. Bogner P, Sipos K, Ludány A, Somogyi B, Miseta A. Steady-state volumes and metabolism-independent osmotic adaptation in mammalian erythrocytes. Eur Biophys J. 2002;31(2):145-152.doi.org/10.1007/s00249-001-0198-7
61. 61. Igbokwe NA. A review of the factors that influence erythrocyte osmotic fragility. Sokoto J Vet Sci. 2018;16(4):1-23.doi.org/10.4314/sokjvs.v16i4.1
62. 62. King MJ, Zanella A. Hereditary red cell membrane disorders and laboratory diagnostic testing. Int J Lab Hem. 2013;35(3):237-43.doi.org/10.1111/ijlh.12070
63. 63. Oto G, Arihan O, Celikezen F, Basbugan Y, Sen S. Effect of doxorubicin and some boron compounds on erythrocyte fragility in rats. Natural Science and Discovery. 2015;1(2):50-3.doi.org/10.20863/nsd.27011
64. 64. Lektib I, Bargaâ R, Chakir Y, Belhouari A, Hammoumi A, El Khasmi M. Study of incubation conditions for erythrocytes osmotic fragility testing in dromedary camel (Camelus dromedarius). Int J Res Env Sci. 2016;2:22-32.doi.org/10.20431/2454-9444.0202004
65. 65. Wagner C, Walski T, Chludzińska L, Komorowska M, Witkiewicz W. Individual osmotic fragility distribution: a new parameter for determination of the osmotic properties of human red blood cells. BioMed Res Int. 2014;162102.doi.org/10.1155/2014/162102
66. 66. Pretorius E. Erythrocyte deformability and eryptosis during inflammation, and impaired blood rheology. Clin Hemorheol Microcirc. 2018;69(4):545-50.doi.org/10.3233/CH-189205
67. 67. Schultheiss TM, Xydas S, Lassar AB. Induction of avian cardiac myogenesis by anterior endoderm. Development. 1995;121(12):4203-14.doi.org/10.1242/dev.121.12.4203
68. 68. Linsalata M, Amati L, Caradonna L, Caccavo D, JirilloE, Di Leo A. Relationship among red blood cell polyamine content, phagocytic activities and plasma endotoxins in untreated colorectal cancer patients. Oncol Rep. 1999;6(6):1411-6.doi.org/10.3892/or.6.6.1411
69. 69. De Souza Gonçalves B, Toledo MM, Colodette NM, Freitas Chaves AL, Munoz LV, De A Ribeiro RIM, et al. Evaluation of the erythrocyte membrane in head and neck cancer patients. J Membrane Biol. 2020;253(6):617-29.doi.org/10.1007/s00232-020-00147-w
70. 70. Smolanka II, Bagmut IY, Sheremet MI, Movchan OV, Oleksandrovich LA, Smolanka II Jr, et al. Phosphorus metabolism disorders in erythrocytes and lymphocytes among patients with inflammatory breast cancer, infiltrative stomach and colorectal cancer. J Med Life. 2022;15(6):747-50.doi.org/10.25122/jml-2022-0048
71. 71. Golovanov MV, Bauer J. Electron microscopic characterization of gels formed by blood cells of leukemia patients at hypertonicity. Colloids Surf B. 2005;44(4):167-71.doi.org/10.1016/j.colsurfb.2005.05.016
72. 72. Andolfo I, Russo R, Gambale A, Iolascon A. New insights on hereditary erythrocyte membrane defects. Haematologica. 2016;101(11):1284-94.doi.org/10.3324/haematol.2016.142463
73. 73. Sam R, Haghighat L, Kjellstrand CM, Ing TS. Hemolysis during hemodialysis. Handbook of Dialysis Therapy. 2008;457-66.doi.org/10.1016/B978-1-4160-4197-9.50035-1
74. 74. Ziemba R. Acute radiation syndrome. Mil Pharm Med. 2011;9:66-71.
75. 75. Ushakov IB, Vasin MV. Radiation protective agents in the radiation safety system for long-term exploration missions. Hum Physiol. 2014;40:695-703.doi.org/10.1134/S0362119714070251
76. 76. Joudoh HJ, Al-Kaysi AM, Kadhim NF. Effects of external radiation exposure on some hematological parameters of hospitals workers staff. Biol Appl Environ Res. 2018;2(2):171-9.
77. 77. Zhirnov VV, Iakovenko IN. The osmotic resistance, and zeta potential responses of human erythrocytes to transmembrane modification of Ca2+ fluxes in the presence of the imposed low rate radiation field of 90 Sr. Int J Radiat Biol. 2015;91(1):117-26.doi.org/10.3109/09553002.2014.950716
78. 78. Alkhalaf AA, Alrusayni SA, Khalid A, Aloraifi A, AL-Shammari OA, Dhanarasu S. Efficacy of parsley (Petroselinum crispum) leaves extract and decoction on status of lipid profile and osmotic fragility in gentamicin-induced nephrotoxicity in rats. J Chem Pharm Res.2016;8(3):948-57.
79. 79. Candan F, Gültekin F, Candan F. Effect of vitamin C and zinc on osmotic fragility and lipid peroxidation in zinc-deficient haemodialysis patients. Cell Biochem Funct. 2002;20(2):95-8.doi.org/10.1002/cbf.947
80. 80. Etlik O, Tomur A, Tuncer M, Ridvanağaoğlu AY, Andac O. Protective effect of antioxidant vitamins on red blood cell lipoperoxidation induced by SO 2 inhalation. J Basic Clin Physiol Pharmacol. 1997;8(1-2):31-44.doi.org/10.1515/JBCPP.1997.8.1-2.31