Erythrocyte signal transduction pathways, their oxygenation dependence and functional significance

Cellular Physiology and Biochemistry

Volumn 15, Issue 1-4, 2005, Pages 1-18

  Barvitenko, Nadezhda N ^a   Adragna, Norma C ^b   Weber, Roy E ^c  

^a SECHENOV INSTITUTE OF EVOLUTIONARY PHYSIOLOGY AND BIOCHEMISTRY   (Russian Federation)

^b WRIGHT STATE UNIVERSITY   (United States)

^c AARHUS UNIVERSITY   (Denmark)

Author keywords

2,3 DPG; Calcium; Erythrocyte; Hemoglobin; Magnesium; Nitric oxide; Oxygen sensors; Oxygenation deoxygenation; Shear stress; Signal transduction; Volume sensors

Indexed keywords

2,3 DIPHOSPHOGLYCERIC ACID; ADENOSINE TRIPHOSPHATE; INOSITOL PENTAKISPHOSPHATE; MAGNESIUM ION; NITRIC OXIDE;

BLOOD RHEOLOGY; CALCIUM SIGNALING; CELL INTERACTION; CYTOSKELETON; ERYTHROCYTE; ERYTHROCYTE MEMBRANE; ERYTHROCYTE VOLUME; HEMOGLOBIN DETERMINATION; HUMAN; ION TRANSPORT; NONHUMAN; OXYGEN AFFINITY; OXYGEN TRANSPORT; OXYGENATION; PRIORITY JOURNAL; PROTEIN FUNCTION; REVIEW; SHEAR STRESS; SIGNAL TRANSDUCTION;

AVES; VERTEBRATA;

EID: 12444257346     PISSN: 10158987     EISSN: None     Source Type: Journal    
DOI: 10.1159/000083634     Document Type: Review

References (214)

1. Minetti G, Low PS: Erythrocyte signal transduction pathways and their possible functions. Curr Opin Hematol 1997;4:116-121.
2. Gulbins E, Jekle A, Ferlinz K, Grassme H, Lang F: Physiology of apoptosis. Am J Physiol Renal Physiol 2000;279:F605-F615.
3. Lang F, Busch GL, Ritter M, Volkl H, Waldegger S, Gulbins E, Haussinger D: Functional significance of cell volume regulatory mechanisms. Physiol Rev 1998;78:247-306.
4. Pedersen SF, Hoffmann EK, Mills JW: The cytoskeleton and cell volume regulation. Comp Biochem Physiol A Mol Integr Physiol 2001;130:385-399.
5. Maeno E, Okada Y: Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc Natl Acad Sci U S A 2004;97:9487-9492.
6. Myssina S, Huber SM, Birka C, Lang PA, Lang KS, Friedrich B, Risler T, Wieder T, Lang F: Inhibition of erythrocyte cation channels by erythropoietin. J Am Soc Nephrol 2003;14:2750-2757.
7. Rivera A, Jarolim P, Brugnara C: Modulation of Gardos channel activity by cytokines in sickle erythrocytes. Blood 2002;99:357-603.
8. Buemi M, Marino D, Floccari F, Ruello A, Nostro L, Aloisi C, Marino MT, Di Pasquale G, Corica F, Frisina N: Effect of interleukin 8 and ICAM-1 on calciumdependent outflow of K+ in erythrocytes from subjects with essential hypertension. Curr Med Res Opin 2004;20:19-24.
9. + channels in human erythrocyte apoptosis. Am J Physiol Cell Physiol 2003;285:C1553-C1560.
10. Gibson JS, Cossins AR, Ellory JC: Oxygen-sensitive membrane transporters in vertebrate red cells. J Exp Biol 2000;203:1395-1407.
11. Tuvia S, Levin S, Korenstein R: Oxygenation-deoxygenation cycle of erythrocytes modulates submicron cell membrane fluctuations. Biophys J 1992;63:599-602.
12. Tuvia S, Moses A, Gulayev N, Levin S, Korenstein R: Beta-adrenergic agonists regulate cell membrane fluctuations of human erythrocytes. J Physiol 1999;516:781-792.
13. Barbul A, Zipser Y, Nachles A, Korenstein R: Deoxygenation and elevation of intracellular magnesium induce tyrosine phosphorylation of band 3 in human erythrocytes. FEBS Lett 1999;455:87-91.
14. Low PS, Rathinavelu P, Harrison ML: Regulation of glycolysis via reversible enzyme binding to the membrane protein, band 3. J Biol Chem 1993;268:14627-14631.
15. Weber RE: Adaptations for oxygen transport: Lessons from fish hemoglobins. In: Di Prisco G, Giardina B, Weber RE, editors. Hemoglobin Function in Vertebrates, Molecular Adaptation in Extreme and Temperate Environments. Milano: Springer-Verlag Italia, 2000:23-37.
16. Wenger RH: Mammalian oxygen sensing, signalling and gene regulation. J Exp Biol 2000;203:1253-1263.
17. Hofer T, Spielmann P, Stengel P, Stier B, Katschinski DM, Desbaillets I, Gassmann M, Wenger RH: Mammalian PASKIN, a PAS-serine/threonine kinase related to bacterial oxygen sensors. Biochem Biophys Res Com 2001;288:757-764.
18. + exchange by molecular oxygen in trout erythrocytes. A possible role of hemoglobin as a transducer. J Gen Physiol 1987;90:197-207.
19. + fluxes in trout red cells: the nature of O2 sensing revealed by the affinity, cooperativity and pH dependence of the transport. Journal of Physiology-London 2000;526:69-80.
20. Bogdanova AY, Nikinmaa M: Reactive oxygen species regulate oxygen-sensitive potassium flux in rainbow trout erythrocytes. J Gen Physiol 2001;117:181-190.
21. Burmester T, Weich B, Reinhardt S, Hankeln T: A vertebrate globin expressed in the brain. Nature 2000;407:520-523.
22. Burmester T, Ebner B, Weich B, Hankeln T: Cytoglobin: A novel globin type ubiquitously expressed in vertebrate tissues. Mol Biol Evol 2002;19:416-421.
23. Trent JT, Hargrove MS: A ubiquitously expressed human hexacoordinate hemoglobin. J Biol Chem 2002;277:19538-19545.
24. Roesner A, Fuchs C, Hankeln T, Burmester T: A globin gene of ancient evolutionary origin in lower vertebrates. Evidence for two distinct globin families in animals. Mol Biol Evol 2004;In press.
25. Sun YJ, Jin KL, Mao XO, Zhu YH, Greenberg DA: Neuroglobin is upregulated by and protects neurons from hypoxic-ischemic injury. Proc Natl Acad Sci USA 2001;98:15306-15311.
26. Fordel E, Geuens E, Dewilde S, Rottiers P, Carmeliet P, Grooten J, Moens L: Cytoglobin expression is upregulated in all tissues upon hypoxia: an in vitro and in vivo study by quantitative real-time PCR. Biochem Biophys Res Com 2004;319:342-348.
27. Sun Y, Jin K, Peel A, Mao XO, Xie L, Greenberg DA: Neuroglobin protects the brain from experimental stroke in vivo. PNAS 2003;100:3497-3500.
28. Kriegl JM, Bhattacharyya AJ, Nienhaus K, Deng P, Minkow O, Nienhaus GU: Ligand binding and protein dynamics in neuroglobin. PNAS 2002;99:7992-7997.
29. Arnone A, Perutz MF: Structure of inositol hexaphosphate- human deoxyhaemoglobin complex. Nature 1974;249:34-36.
30. Ellory JC, Gibson JS, Stewart GW: Pathophysiology of abnormal cell volume in human red cells. Contrib Nephrol 1998;123:220-239.
31. Walder JA, Chatterjee R, Steck TL, Low PS, Musso GF, Kaiser ET, Rogers PH, Arnone A: The interaction of hemoglobin with the cytoplasmic domain of Band 3 of the human erythrocyte membrane. J Biol Chem 1984;259:10238-10246.
32. 2+ and hemoglobin. J Biol Chem 1988;263:8544-8550.
33. Jensen FB, Brahm J: Kinetics of chloride transport across fish red blood cell membranes. J Exp Biol 1995;198:2237-2244.
34. Jensen FB, Wang T, Jones DR, Brahm J: Carbon dioxide transport in alligator blood and its erythrocyte permeability to anions and water. Am J Physiol 1998;274:R661-71.
35. Galtieri A, Tellone E, Romano L, Misiti F, Bellocco E, Ficarra S, Russo A, Di Rosa D, Castagnola M, Giardina B, Messana I: Band-3 protein function in human erythrocytes: effect of oxygenationdeoxygenation. Biochim Biophys Acta-Biomembranes 2002;1564:214-218.
36. Drew C, Ball V, Robinson H, Clive Ellory J, Gibson JS: Oxygen sensitivity of red cell membrane transporters revisited. Bioelectrochemistry 2004;62:153-158.
37. Murphy JR: Erythrocyte metabolism .2. Glucose metabolism and pathways. J Lab & Clin Med 1960;55:286-302.
38. Rapoport I, Berger H, Rapoport SM, Elsner R, Gerber G: Response of glycolysis of human erythrocytes to transition from oxygenated to deoxygenated state at constant intracellular pH. Biochim Biophys Acta 1976;428:193-204.
39. 2 -linked transition of hemoglobin. FEBS Lett 1996;390:25-28.
40. Hamasaki N, Asakura T, Minakami S: Effect of oxygen tension on glycolysis in human erythrocytes. J Biochem Tokyo 1970;68:157-161.
41. 2 delivery mediated by hemoglobin oxygenation. Am J Physiol Heart Circ Physiol 2001;280:H2833-H2839.
42. 2 Weber RE, Voelter W, Fago A, Echner H, Campanella E, Low PS: Modulation of red cell glycolysis: interactions between vertebrate hemoglobins and cytoplasmic domains of band 3 red cell membrane proteins. Am J Physiol Regul Integr Comp Physiol 2004;287:R454-R464.
43. Rauenbuehler PB, Cordes KA, Salhany JM: Identification of the hemoglobin binding sites on the inner surface of the erythrocyte membrane. Biochim Biophys Acta 1982;692:361-370.
44. Lebbar I, Stetzkowski-Marden F, Mauffret O, Cassoly R: Interactions of actin and tubulin with human deoxyhemoglobin. Their possible occurrence within erythrocytes. Eur J Biochem 1987;170:273-277.
45. Tuvia S, Levin S, Bitler A, Korenstein R: Mechanical fluctuations of the membrane-skeleton are dependent on Factin ATPase in human erythrocytes. J Cell Biol 1998;141:1551-1561.
46. Cossins AR, Weaver YR, Lykkeboe G, Nielsen OB: Role of protein phosphorylation in control of K flux pathways of trout red blood cells. Am J Physiol 1994;267(36):C1641-C1650.
47. Sørensen B, Weber RE: Effects of oxygenation and the stress hormones adrenaline and cortisol on the viscosity of blood from trout, Oncorhynchus mykiss. J Exp Biol 1995;198:953-959.
48. Jensen FB, Jakobsen MH, Weber RE: Interaction between haemoglobin and synthetic peptides of the N- terminal cytoplasmic fragment of trout band 3 (AE1) protein. J Exp Biol 1998;201:2685-2690.
49. + fluxes in sheep red cells. J Physiol (London) 1998;506:679-688.
50. Chaimanee P, Yuthavong Y: Binding of haemoglobin to spectrin of human erythrocytes. FEBS Lett 1977;78:119-123.
51. Devogel M, Leonis J, Vincentelli J: The alteration of the functional properties of human haemoglobin by spectrin. Experientia 1977;33:1429-1450.
52. Liu SC, Palek J: Hemoglobin enhances the self-association of spectrin heterodimers in human erythrocytes. J Biol Chem 1984;259:11556-11562.
53. Vincentelli J, Fraboni A, Paul C, Schnek AG: The influence of experimental conditions on the spectrin-hemoglobin interaction. Biol Chem Hoppe Seyler 1989;370:63-66.
54. Cassoly R: Evidence against the binding of native hemoglobin to spectrin of human erythrocytes. FEBS Lett 1978;85:357-360.
55. Shaklai N, Frayman B, Fortier N, Snyder M: Crosslinking of isolated cytoskeletal proteins with hemoglobin: a possible damage inflicted to the red cell membrane. Biochim Biophys Acta 1987;915:406-414.
56. Datta P, Chakrabarty SB, Chakrabarty A, Chakrabarti A: Interaction of erythroid spectrin with hemoglobin variants: implications in betathalassemia. Blood Cells Molecules and Diseases 2003;30:248-253.
57. Marttila ONT, Nikinmaa M: Binding of b-adrenergic antagonists 3H-DHA and 3H-CGP 12177 to intact rainbow trout (Salmo gairdneri) and carp (Cyprinus carpio) red blood cells. Gen Comp Endocrinol 1988;70:429-435.
58. Chang SH, Low PS: Regulation of the glycophorin C-protein 4.1 membraneto-skeleton bridge and evaluation of its contribution to erythrocyte membrane stability. J Biol Chem 2001;276:22223-22230.
59. Bunn HF, Ransil BJ, Chao A: The interaction between erythrocyte organic phosphates, magnesium ion, and hemoglobin. J Biol Chem 1971;246:5273-5279.
60. Janmey PA: The cytoskeleton and cell signaling: Component localization and mechanical coupling. Physiol Rev 1998;78:763-781.
61. Papakonstanti EA, Vardaki EA, Stournaras C: Actin cytoskeleton: a signaling sensor in cell volume regulation. Cell Physiol Biochem 2000;10:257-264.
62. Weaver YR, Cossins AR: Protein tyrosine phosphorylation and the regulation of KCl cotransport in trout erythrocytes. Pflugers Arch 1996;432:727-734.
63. + sheep and goat erythrocytes. Biochem Biophys Res Com 1980;92:1422-1428.
64. + Cl- cotransport - sulfhydryls, divalent-cations, and the mechanism of volume activation in a red-cell. J Membr Biol 1985;88:1-13.
65. Zipser Y, Piade A, Kosower NS: Erythrocyte thiol status regulates band 3 phosphotyrosine level via oxidation/ reduction of band 3-associated phosphotyrosine phosphatase. FEBS Lett 1997;406:126-130.
66. Bordin L, Brunati AM, Donella-Deana A, Baggio B, Toninello A, Clari G: Band 3 is an anchor protein and a target for SHP-2 tyrosine phosphatase in human erythrocytes. Blood 2002;100:276-282.
67. - cotransport in equine red blood cells. Exp Physiol 1994;79:997-1009.
68. Honess NA, Gibson JS, Cossins AR: The effects of oxygenation upon the Cl dependent K flux pathway in equine red cells. Pflügers Arch-Eur J Physiol 1996;432:270-277.
69. Tyuma I, kamigawara Y, Imai K: pH dependence of the shape of the hemoglobin-oxygen equilibrium curve. Biochim Biophys Acta 1973;310:317-320.
70. Weber RE, Jensen FB, Cox RP: Analysis of teleost hemoglobin by Adair and Monod-Wyman-Changeux models. Effects of nucleoside triphosphates and pH on oxygenation of tench hemoglobin. J Comp Physiol 1987;157B:145-152.
71. Merciris P, Hardy-Dessources MD, Sauvage M, Giraud F: Involvement of deoxygenation-induced increase in tyrosine kinase activity in sickle cell dehydration. Pflügers Arch-Eur J Physiol 1998;436:315-322.
72. Merciris P, Hardy-Dessources MD, Giraud F: Deoxygenation of sickle cells stimulates Syk tyrosine kinase and inhibits a membrane tyrosine phosphatase. Blood 2001;98:3121-3127.
73. Fathallah H, Coezy E, Deneef RS, Hardydessources MD, Giraud F: Inhibition of deoxygenation-induced membrane-protein dephosphorylation and cell dehydration by phorbol esters and okadaic acid in sickle cells. Blood 1995;86:1999-2007.
74. 4 Salama A, Nikinmaa M: Effect of oxygen tension on catecholamine-induced formation of cAMP and on swelling of carp red blood cells. Am J Physiol 1990;259:C723-C726.
75. + exchanger - Evidence that the cytoplasmic domain mediates hormonal regulation. Proc Natl Acad Sci USA 1992;89:6765-6769.
76. Prat AG, Cunningham CC, Jackson GR, Jr., Borkan SC, Wang Y, Ausiello DA, Cantiello HF: Actin filament organization is required for proper cAMP-dependent activation of CFTR. Am J Physiol 1999;277:C1160-C1169.
77. + exchanger NHE3. J Biol Chem 2001;276:40761-40768.
78. + exchanger, NHE1: structure, regulation, and cellular actions. Annu Rev Pharmacol Toxicol 2002;42:527-552.
79. Nikinmaa M, Cech JJ, Jr., Ryhanen EL, Salama A: Red cell function of carp (Cyprinus carpio) in acute hypoxia. Exp Biol 1987;47:53-58.
80. Jensen FB: Nitrite and red cell function in carp: control factors for nitrite entry, membrane potassium ion permeation, oxygen affinity and methaemoglobin formation. J Exp Biol 1990;152:149-166.
81. Nielsen OB, Lykkeboe G, Cossins AR: Oxygenation-activated K-fluxes in trout red-blood-cells. Am J Physiol 1992;263:C1057-C1064.
82. Jensen FB: Red blood cell pH, the Bohr effect, and other oxygenation-linked phenomena in blood O2 and CO2 transport. Acta Physiol Scand 2004;182:215-227.
83. Muto S, Ebata S, Okada K, Saito T, Asano Y: Glucocorticoid modulates Na+/H+ exchange activity in vascular smooth muscle cells by nongenomic and genomic mechanisms. Kidney Int 2000;57:2319-2333.
84. Ullrich V, Bachschmid M: Superoxide as a messenger of endothelial function. Biochem Biophys Res Comm 2000;278:1-8.
85. Stuhlmeier KM, Kao JJ, Wallbrandt P, Lindberg M, Hammarstrom B, Broell H, Paigen B: Antioxidant protein 2 prevents methemoglobin formation in erythrocyte hemolysates. Eur J Biochem 2003;270:334-341.
86. Nikinmaa M, Bogdanova A, Lecklin T: Oxygen dependency of the adrenergic Na/H exchange in rainbow trout erythrocytes is diminished by a hydroxyl radical scavenger. Acta Physiol Scand 2003;178:149-154.
87. Gibson JS, Muzyamba MC: Modulation of Gardos channel activity by oxidants and oxygen tension: effects of 1-chloro-2,4-dinitrobenzene and phenazine methosulphate. Bioelectrochemistry 2004;62:147-152.
88. Guillemette G, Favreau I, Lamontagne S, Boulay G: 2,3-Diphosphoglycerate is a nonselective inhibitor of inositol 1,4,5-trisphosphate action and metabolism. Eur J Pharmacol , Mol Pharmacol Sect 1990;188:251-260.
89. McConnel FM, Goldstein L: Intracellular signals and volume regulatory response in skate erythrocytes. Am J Physiol , Regul Integr Comp Physiol 1988;255:R982-R987.
90. 2+ influx into human red cells. Cell Calcium 1999;26:131-137.
91. Ferrell CM, Lauf PK, Wilson BA, Adragna NC: Lithium and protein kinase C modulators regulate swelling-activated K-Cl cotransport and reveal a complete phosphatidylinositol cycle in low K sheep erythrocytes. J Membr Biol 2000;177:81-93.
92. Piacentini MP, Piatti E, Bucchini A, Fazi A, Accorsi A: Modification of inositol 1,4,5-trisphosphate concentration of human erythrocytes under "in vivo" physiological conditions. Biochem Mol Biol Int 1996;38:1265-1269.
93. 2+ -adenosine triphosphatase activity in vitro by a guanine nucleotide regulatory protein. Metabolism 1995;44:865-868.
94. Shiffer KA, Rood L, Emerson RK, Kuypers FA: Effects of phosphatidylinositol diphosphate on phospholipid asymmetry in the human erythrocyte membrane. Biochemistry 1998;37:3449-3458.
95. + pump. Adv Exp Med Biol 2004;536:231-238.
96. Hoffmann EK, Pedersen SF: Sensors and signal transduction in the activation of cell volume regulatory ion transport systems. Contrib Nephrol 1988;123:58-78.
97. Mongin AA, Orlov SN: Mechanisms of cell volume regulation and possible nature of the cell volume sensor. Pathophysiology 2001;8:77-88.
98. Jensen FB: Regulatory volume decrease in carp red blood cells: mechanisms and oxygenation-dependency of volumeactivated potassium and amino acid transport. J Exp Biol 1995;198:155-165.
99. - cotransport in rat erythrocytes. Biochim Biophys Acta 1993;1151:186-192.
100. Estevez AY, Bond T, Strange K: Regulation of ICl,swell in neuroblastoma cells by G protein signaling pathways. Am J Physiol Cell Physiol 2001;281:C89-C98.
101. Lominadze D, Dean WL: Involvement of fibrinogen specific binding in erythrocyte aggregation. FEBS Lett 2002;517:41-44.
102. Dahl Sv, Schliess F, Reissmann R, Gorg B, Weiergraber O, Kocalkova M, Dombrowski F, Haussinger D: Involvement of integrins in osmosensing and signaling toward autophagic proteolysis in rat liver. J Biol Chem 2003;278:27088-27095.
103. Lepple-Wienhues A, Szabo I, Laun T, Kaba NK, Gulbins E, Lang F: The tyrosine kinase p56(lck) mediates activation of swelling-induced chloride channels in lymphocytes. J Cell Biol 1998;141:281-286.
104. Arias-Salgado EG, Lizano S, Sarkar S, Brugge JS, Ginsberg MH, Shattil SJ: Src kinase activation by direct interaction with the integrin beta cytoplasmic domain. Proc Natl Acad Sci USA 2003;100:13298-13302.
105. Colclasure GC, Parker JC: Cytosolic protein concentration is the primary volume signal for swelling-induced [KCl] cotransport in dog red cells. J Gen Physiol 1992;100:1-10.
106. Minton AP, Colclasure GC, Parker JC: Model for the role of macromolecular crowding in regulation of cellular-volume. Proc Natl Acad Sci USA 1992;89:10504-10506.
107. Vitoux D, Beuzard Y, Brugnara C: The effect of hemoglobin A and S on the volume- and pH-dependence of K-Cl cotranport in human erythrocytic ghosts. J Membr Biol 1999;167:233-240.
108. Sachs JR, Martin DW: The role of ATP in swelling-stimulated K-Cl cotransport in human red cell ghosts. Phosphorylation-dephosphorylation events are not in the signal transduction pathway. J Gen Physiol 1993;102:551-573.
109. - cotransport in human red cell ghosts and sickle cells. Bioelectrochemistry 2004;62:141-146.
110. - ) cotransport system in human erythrocytes. Blood 1992;79:793-797.
111. OARAB . Br J Haematol 1999;107:516-521.
112. Dunham PB: Effects of urea on K-Cl cotransport in sheep red-blood-cells - Evidence for 2 signals of swelling. Am J Physiol Cell Physiol 1995;37:C1026-C1032.
113. Bard H, Fouron JC, Robillard JE, Cornet A, Soukini MA: Red-cell oxygen-affinity in fetal sheep - role of 2,3-DPG and adult hemoglobin. J Appl Physiol 1978;45:7-10.
114. Holland RA, Tibben EA, Hallam JF: Interaction between organic phosphates and sheep hemoglobins Interaction between organic phosphates and sheep hemoglobins. Adv Exp Med Biol 1990;277:191-197.
115. Chien S: Red cell deformability and its relevance to blood flow. Annu Rev Physiol 1987;49:177-192.
116. Cicha I, Suzuki Y, Tateishi N, Maeda N: Changes of RBC aggregation in oxygenation-deoxygenation: pH dependency and cell morphology. Am J Physiol Heart Circ Physiol 2003;284:H2335-H2342.
117. Speake PF, Gibson JS: Urea-stimulated K-Cl cotransport in equine red blood cells. Pflugers Arch 1997;434:104-112.
118. Friederichs E, Meiselman HJ: Effects of calcium permeabilization on RBC rheologic behavior. Biorheology 1994;31:207-215.
119. Bordin L, Clari G, Moro I, Dallavecchia F, Moret V: Functional-link between phosphorylation state of membraneproteins and morphological-changes of human erythrocytes. Biochem Biophys Res Comm 1995;213:249-257.
120. Manno S, Takakuwa Y, Nagao K, Mohandas N: Modulation of erythrocytemembrane mechanical function by betaspectrin phosphorylation and dephosphorylation. J Biol Chem 1995;270:5659-5665.
121. 2 on hemoglobinoxygen affinity. J Comp Physiol 1978;128B:127-137.
122. Murphy E: Mysteries of magnesium homeostasis. Circ Res 2000;86:245-248.
123. Mairbaurl H, Hoffman JF: Internal magnesium, 2,3-diphosphoglycerate, and the regulation of the steady-state volume of human red blood cells by the Na/K/2Cl cotransport system. J Gen Physiol 1992;99:721-746.
124. Bennet V: The spectrin-actin junction of erythrocyte-membrane skeletons. Biochim Biophys Acta 1989;988:107-121.
125. Beaven GH, Parmar J, Nash GB, Bennett PM, Gratzer WB: Effect of magnesium ions on red cell membrane properties. J Membr Biol 1990;118:251-257.
126. Wallis CJ, Babitch JA, Wenegieme EF: Divalent cation binding to erythrocyte spectrin. Biochemistry 1993;32:5045-5050.
127. Kay FR: 2,3-Diphosphoglycerate, bloodoxygen dissociation and biology of mammals. Comp Biochem Physiol A Physiol 1977;57:309-316.
128. Bunn HF: Evolution of mammalian hemoglobin function. Blood 1981;58:189-197.
129. Mulquiney PJ, Kuchel PW: Model of 2,3-bisphosphoglycerate metabolism in the human erythrocyte based on detailed enzyme kinetic equations: computer simulation and metabolic control analysis. Biochem J 1999;342 Pt 3:597-604.
130. Mulquiney PJ, Bubb WA, Kuchel PW: Model of 2,3-bisphosphoglycerate metabolism in the human erythrocyte based on detailed enzyme kinetic equations in vivo kinetic characterization of 2,3-bisphosphoglycerate synthase/phosphatase using C-13 and P-31 NMR. Biochem J 1999;342:567-580.
131. Mulquiney PJ, Kuchel PW: Model of 2,3-bisphosphoglycerate metabolism in the human erythrocyte based on detailed enzyme kinetic equations: equations and parameter refinement. Biochem J 1999;342:581-596.
132. Waugh RE: Effects of 2,3-diphosphoglycerate on the mechanical properties of erythrocyte membrane. Blood 1986;68:231-238.
133. Mentzer WC, Jr., Iarocci TA, Mohandas N, Lane PA, Smith B, Lazerson J, Hays T: Modulation of erythrocyte membrane mechanical stability by 2,3-diphosphoglycerate in the neonatal poikilocytosis/elliptocytosis syndrome. J Clin Invest 1987;79:943-949.
134. Chasis JA, Mohandas N: Erythrocyte membrane deformability and stability: two distinct membrane properties that are independently regulated by skeletal protein associations. J Cell Biol 1986;103:343-350.
135. Suzuki Y, Nakajima T, Shiga T, Maeda N: Influence of 2,3- diphosphoglycerate on the deformability of human erythrocytes. Biochim Biophys Acta 1990;1029:85-90.
136. Le Devehat C, Lemoine A, Cirette B, Ramet M: Pharmacological influences of pentoxifylline on red cell filterability and 2-3 diphosphoglycerate. Scand J Clin Lab Invest Suppl 1981;156:301-303.
137. Lee I, Kim JH, Levitt SH, Song CW: Increases in tumour response by pentoxifylline alone or in combination with nicotinamide. Int J Radiat Oncol Biol Phys 1992;22:425-429.
138. Yamamoto N, Yokota K, Yamashita A, Oda M: The effects of KBT-3022, a new anti-platelet agent, on hemorheological properties in guinea pigs. Thromb Haemost 1995;73:118-121.
139. Fernandes PR, Dewey MJ: Genetic control of erythrocyte volume regulation: effect of a single gene (rol) on cation metabolism. Am J Physiol 1994;267:C211-C219.
140. Adragna NC, White RE, Orlov SN, Lauf PK: K-Cl cotransport in vascular smooth muscle and erythrocytes: possible implication in vasodilation. Am J Physiol Cell Physiol 2000;278:C381-C390.
141. Ortiz-Carranza O, Adragna NC, Lauf PK: Modulation of K-Cl cotransport in volume-clamped low-K sheep erythrocytes by pH, magnesium, and ATP. Am J Physiol 1996;271:C1049-C1058.
142. Haley BE, Hoffman JF: Interactions of a photo-affinity ATP analog with cationstimulated adenosine triphosphatases of human red-cell membranes. Proc Natl Acad Sci USA 1974;71:3367-3371.
143. Shaklai N, Benitez L, Ranney HM: Binding of 2,3-diphosphoglycerate by spectrin and its effect on oxygen affinity of hemoglobin. Am J Physiol 1978;234:C36-C40.
144. Sheetz MP, Casaly J: 2,3-Diphosphoglycerate and ATP dissociate erythrocyte membrane skeletons. J Biol Chem 1980;255:9955-9960.
145. Moriyama R, Lombardo CR, Workman RF, Low PS: Regulation of linkages between the erythrocyte membrane and its skeleton by 2,3-diphosphoglycerate. J Biol Chem 1993;268:10990-10996.
146. Clari G, Ferrari S: Kinetic behaviour of human erythrocyte casein kinases. Effect of 2, 3- bisphosphoglycerate and heparin. Ital J Biochem 1983;32:174-188.
147. Chao TS, Tao M: Effect of 2,3-diphosphoglycerate on the phosphorylation of protein 4.1 by protein kinase C. Arch Biochem Biophys 1991;285:221-226.
148. An XL, Takakuwa Y, Nunomura W, Manno S, Mohandas N: Modulation of band 3-ankyrin interaction by protein 4.1 - Functional implications in regulation of erythrocyte membrane mechanical properties. J Biol Chem 1996;271:33187-33191.
149. Sakashita K, Oonishi T, Ishioka N, Uyesaka N: Endothelin-1 improves the impaired filterability of red blood cells through the activation of protein kinase C. Jpn J Physiol 1999;49:113-120.
150. Oonishi T, Sakashita K: Ethanol improves decreased filterability of human red blood cells through modulation of intracellular signaling pathways. Alcohol Clin Exp Res 2000;24:352-356.
151. Ellsworth ML, Forrester T, Ellis CG, Dietrich HH: The erythrocyte as a regulator of vascular tone. Am J Physiol Heart Circ Physiol 1995;269:H2155- H2161.
152. Sprague RS, Ellsworth ML, Stephenson AH, Lonigro AJ: ATP: the red blood cell link to NO and local control of the pulmonary circulation. Am J Physiol Heart Circ Physiol 1996;271:H2717-H2722.
153. Stamler JS, Jia L, Eu JP, McMahon TJ, Demchenko IT, Bonaventura J, Gernert K, Piantadosi CA: Blood flow regulation by S-nitrosohemoglobin in the physiological oxygen gradient. Science 1997;276:2034-2037.
154. Pawloski JR, Hess DT, Stamler JS: Export by red blood cells of nitric oxide bioactivity. Nature 2001;409:622-626.
155. Bonaventura C, Taboy CH, Low PS, Stevens RD, Lafon C, Crumbliss AL: Heme redox properties of S-nitrosated hemoglobin A(0) and hemoglobin S - Implications for interactions of nitric oxide with normal and sickle red blood cells. J Biol Chem 2002;277:14557-14563.
156. Chen LY, Mehta JL: Evidence for the presence of L-arginine-nitric oxide pathway in human red blood cells: relevance in the effects of red blood cells on platelet function. J Cardiovasc Pharmacol 1998;32:57-61.
157. Kang ES, Ford K, Grokulsky G, Wang YB, Chiang TM, Acchiardo SR: Normal circulating adult human red blood cells contain inactive NOS proteins. J Lab & Clin Med 2000;135:444-451.
158. Bor-Kucukatay M, Wenby RB, Meiselman HJ, Baskurt OK: Effects of nitric oxide on red blood cell deformability. Am J Physiol Heart Circ Physiol 2003;284:H1577-H1584.
159. + exchange by soluble and particulate guanylate cyclase. Am J Physiol 1996;271:C1556-C1564.
160. Hassid A, Yao J, Huang SL: NO alters cell shape and motility in aortic smooth muscle cells via protein tyrosine phosphatase 1B activation. Am J Physiol Heart Circ Physiol 1999;277:H1014-H1026.
161. Brown C, Lin Y, Hassid A: Requirement of protein tyrosine phosphatase SHP2 for NO-stimulated vascular smooth muscle cell motility. Am J Physiol Heart Circ Physiol 2001;281:H1598-H1605.
162. Zipser Y, Kosower NS: Phosphotyrosine phosphatase associated with band 3 protein in the human erythrocyte membrane. Biochem J 1996;314:881-887.
163. Adragna NC, Lauf PK: Role of nitrite, a nitric oxide derivative, in K-Cl cotransport activation of low-potassium sheep red blood cells. J Membr Biol 1998;166:157-167.
164. Caramelo C, Riesco A, Outeirino J, Millas I, Blum G, Monzu B, Casado V, Sanchez L, Mosquera JR, Casado S, Farre AL: Effects of nitric oxide on red-blood-cells - Changes in erythrocyte resistance to hypotonic hemolysis and potassium efflux by experimental maneuvers that decrease nitric oxide. Biochem Biophys Res Com 1994;199:447-454.
165. Tsuda K, Kimura K, Nishio I, Masuyama Y: Nitric oxide improves membrane fluidity of erythrocytes in essential hypertension: An electron paramagnetic resonance investigation. Biochem Biophys Res Comm 2000;275:946-954.
166. Korbut R, Gryglewski RJ: Nitric-oxide from polymorphonuclear leukocytes modulates red-blood-cell deformability in vitro. Eur J Pharmacol 1993;234:17-22.
167. Bateman RM, Jagger JE, Sharpe MD, Ellsworth ML, Mehta S, Ellis CG: Erythrocyte deformability is a nitric oxide-mediated factor in decreased capillary density during sepsis. Am J Physiol Heart Circ Physiol 2001;280:H2848-H2856.
168. Zamir N, Tuvia S, Riven-Kreitman R, Levin S, Korenstein R: Atrial natriuretic peptide: direct effects on human red blood cell dynamics. Biochem Biophys Res Comm 1992;188:1003-1009.
169. Ko KS, McCulloch CAG: Partners in protection: Interdependence of cytoskeleton and plasma membrane in adaptations to applied forces. J Membr Biol 2000;174:85-95.
170. Davies PF: Flow-mediated endothelial mechanotransduction. Physiol Rev 1995;75:519-560.
171. Shyy JY, Chien S: Role of integrins in endothelial mechanosensing of shear stress. Circ Res 2002;91:769-775.
172. Gudi SRP, Clark CB, Frangos JA: Fluid flow rapidly activates G proteins in human endothelial cells - Involvement of G proteins in mechanochemical signal transduction. Circ Res 1996;79:834-839.
173. Olearczyk JJ, Stephenson AH, Lonigro AJ, Sprague RS: Heterotrimeric G protein G(i) is involved in a signal transduction pathway for ATP release from erythrocytes. Am J Physiol Heart Circ Physiol 2004;286:H940-H945.
174. Sprague RS, Ellsworth ML, Stephenson AH, Lonigro AJ: Participation of cAMP in a signal-transduction pathway relating erythrocyte deformation to ATP release. Am J Physiol Cell Physiol 2001;281:C1158-C1164.
175. Sprague RS, Ellsworth ML, Stephenson AH, Kleinhenz ME, Lonigro AJ: Deformation-induced ATP release from red blood cells requires CFTR activity. Am J Physiol Heart Circ Physiol 1998;44:H1726-H1732.
176. Ney PA, Christopher MM, Hebbel RP: Synergistic effects of oxidation and deformation on erythrocyte monovalent cation leak. Blood 1990;75:1192-1198.
177. 2+ permeability of human erythrocytes. Nature 1981;294:667-668.
178. Huber SM, Gamper N, Lang F: Chloride conductance and volume-regulatory nonselective cation conductance in human red blood cell ghosts. Pflugers Arch 2001;441:551-558.
179. Egee S, Lapaix F, Decherf G, Staines HM, Ellory JC, Doerig C, Thomas SL: A stretch-activated anion channel is upregulated by the malaria parasite Plasmodium falciparum. J Physiol 2002;542:795-801.
180. 2+ and calmodulin. Implications for their role in regulation of skeletal protein interactions. J Clin Invest 1988;82:394-400.
181. 2+ -dependent regulation of the spectrin/actin interaction by calmodulin and protein 4.1. J Biol Chem 1991;266:1134-1140.
182. 2+ and calmodulin. Implications for modulation of CD44-ankyrin interaction. J Biol Chem 1997;272:30322-30328.
183. Romero PJ, Romero EA: The role of calcium metabolism in human red blood cell ageing: a proposal. Blood Cells Mol Dis 1999;25:9-19.
184. 2+ pumping activity between subpopulations of human red cells. Cell Calcium 1997;21:353-358.
185. Daugas E, Cande C, Kroemer G: Erythrocytes: death of a mummy. Cell Death Differ 2001;8:1131-1133.
186. Berg CP, Engels IH, Rothbart A, Lauber K, Renz A, Schlosser SF, Schulze-Osthoff K, Wesselborg S: Human mature red blood cells express caspase-3 and caspase-8, but are devoid of mitochondrial regulators of apoptosis. Cell Death Differ 2001;8:1197-1206.
187. Bratosin D, Estaquier J, Petit F, Arnoult D, Quatannens B, Tissier JP, Slomianny C, Sartiaux C, Alonso C, Huart JJ, Montreuil J, Ameisen JC: Programmed cell death in mature erythrocytes: a model for investigating death effector pathways operating in the absence of mitochondria. Cell Death Differ 2001;8:1143-1156.
188. Bratosin D, Estaquier J, Slomianny C, Tissier JP, Quatannens B, Bulai T, Mitrofan L, Marinescu A, Trandaburu I, Ameisen JC, Montreuil J: On the evolution of erythrocyte programmed cell death: apoptosis of Rana esculenta nucleated red blood cells involves cysteine proteinase activation and mitochondrion permeabilization. Biochimie 2004;86:183-192.
189. Walsh M, Lutz RJ, Cotter TG, O'Connor R: Erythrocyte survival is promoted by plasma and suppressed by a Bak-derived BH3 peptide that interacts with membrane-associated Bcl-X(L). Blood 2002;99:3439-3448.
190. Lang KS, Myssina S, Lang PA, Tanneur V, Kempe DS, Mack AF, Huber SM, Wieder T, Lang F, Duranton C: Inhibition of erythrocyte phosphatidylserine exposure by urea and Cl-. Am J Physiol Renal Physiol 2004;286:F1046-F1053.
191. Lang F, Lang KS, Wieder T, Myssina S, Birka C, Lang PA, Kaiser S, Kempe D, Duranton C, Huber SM: Cation channels, cell volume and the death of an erythrocyte. Pflügers Arch-Eur J Physiol 2003;447:121-125.
192. Zhou Q, Zhao J, Stout JG, Luhm RA, Wiedmer T, Sims PJ: Molecular cloning of human plasma membrane phospholipid scramblase. A protein mediating transbilayer movement of plasma membrane phospholipids. J Biol Chem 1997;272:18240-18244.
193. Connor J, Pak CC, Schroit AJ: Exposure of phosphatidylserine in the outer leaflet of human red blood cells. Relationship to cell density, cell age, and clearance by mononuclear cells. J Biol Chem 1994;269:2399-2404.
194. + channel in human erythrocytes by mechanical stress. Biochim Biophys Acta 1992;1107:314-318.
195. Manno S, Takakuwa Y, Mohandas N: Identification of a functional role for lipid asymmetry in biological membranes: Phosphatidylserine-skeletal protein interactions modulate membrane stability. Proc Natl Acad Sci U S A 2002;99:1943-1948.
196. ++ -dependent vesicle release from erythrocytes involves stomatin-specific lipid rafts, synexin (annexin VII), and sorcin. Blood 2002;99:2569-2577.
197. Inomata M, Hayashi M, Nakamura M, Saito Y, Kawashima S: Properties of erythrocyte membrane binding and autolytic activation of calcium-activated neutral protease. J Biol Chem 1989;264:18838-18843.
198. Boivin P, Galand C, Dhermy D: In vitro digestion of spectrin, protein 4.1 and ankyrin by erythrocyte calcium dependent neutral protease (calpain I). Int J Biochem 1990;22:1479-1489.
199. Al Z, Cohen CM: Phorbol 12-myristate 13-acetate-stimulated phosphorylation of erythrocyte membrane skeletal proteins is blocked by calpain inhibitors: possible role of protein kinase M. Biochem J 1993;296 ( Pt 3):675-683.
200. Ciana A, Minetti G, Balduini C: Phosphotyrosine phosphatases acting on band 3 in human erythrocytes of different age: PTP1B processing during cell ageing. Bioelectrochemistry 2004;62:169-173.
201. Romero PJ, Salas, V., Hernández, C.: Calcium pump phosphoenzyme from young and old human red cells. Cell Biol Int 2002;26:945-949.
202. Cibert C, Pruliere G, Lacombe C, Deprette C, Cassoly R: Calculation of a Gap restoration in the membrane skeleton of the red blood cell: possible role for myosin II in local repair. Biophys J 1999;76:1153-1165.
203. Johnson RM, Taylor G, Meyer DB: Shape and volume changes in erythrocyte ghosts and spectrin-actin networks. J Cell Biol 1980;86:371-376.
204. 2+ and Mg-ATP. Nature 1984;307:376-378.
205. Berridge MJ, Dupont G: Spatial and temporal signalling by calcium. Curr Opin Cell Biol 1994;6:267-274.
206. 2+ signaling over different time and distance scales - Commentary. J Gen Physiol 2000;116:691-695.
207. Allbritton NL, Meyer T, Stryer L: Range of messenger action of calcium-ion and inositol 1,4,5-trisphosphate. Science 1992;258:1812-1815.
208. 2+ influx and cAMP-mediated signaling pathways. Am J Physiol Cell Physiol 1997;42:C1828-C1834.
209. 2+ homeostasis. Biochem Pharmacol 1998;55:713-718.
210. Fukuda S, Yasu T, Predescu DN, Schmid-Schonbein GW: Mechanisms for regulation of fluid shear stress response in circulating leukocytes. Circ Res 2000;86:E13-E18.
211. Dimmeler S, Hermann C, Galle J, Zeiher AM: Upregulation of superoxide dismutase and nitric oxide synthase mediates the apoptosis-suppressive effects of shear stress on endothelial cells. Arterioscler Thromb Vasc Biol 1999;19:656-664.
212. 2+ /A23187-treated human erythrocytes. Biochem J 1996;320:445-450.
213. 2+ promotes erythrocyte band 3 tyrosine phosphorylation via dissociation of phosphotyrosine phosphatase from band 3. Biochem J 2002;368:137-144.
214. Glogauer M, Arora P, Yao G, Sokholov I, Ferrier J, McCulloch CAG: Calcium ions and tyrosine phosphorylation interact coordinately with actin to regulate cytoprotective responses to stretching. J Cell Sci 1997;110:11-21.