Erythrocyte programmed cell death

IUBMB Life

Volumn 60, Issue 10, 2008, Pages 661-668

  Föller, Michael ^a   Huber, Stephan M ^a   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Anemia; Apoptosis; Hemolysis; Malaria; Red blood cells; Sepsis

Indexed keywords

ADENOSINE; ALUMINUM; AMYLOID; ANANDAMIDE; CALCIUM ION; CALPAIN; CASPASE; CATECHOLAMINE; CATION CHANNEL; CERAMIDE; CHLORPROMAZINE; COPPER; CURCUMIN; CYCLIC GMP DEPENDENT PROTEIN KINASE; CYCLOSPORIN; ERYTHROPOIETIN; HEMOLYSIN; LEAD; LISTERIOLYSIN; MERCURY; METHYLGLYOXAL; NITRIC OXIDE; PACLITAXEL; PHOSPHATIDYLSERINE; POTASSIUM CHANNEL; POTASSIUM CHLORIDE; PROSTAGLANDIN E2; SPHINGOMYELIN PHOSPHODIESTERASE; THROMBOCYTE ACTIVATING FACTOR; VALINOMYCIN; CALCIUM;

ANEMIA; APOPTOSIS; BETA THALASSEMIA; CELL MEMBRANE; CELL STIMULATION; CELL STRESS; CELL STRUCTURE; CELL SURFACE; CELLULAR STRESS RESPONSE; CELLULAR STRESS SIGNAL; CYTOLYSIS; CYTOSKELETON; ERYTHROCYTE; GLUCOSE 6 PHOSPHATE DEHYDROGENASE DEFICIENCY; HEMOLYSIS; HEMOLYTIC UREMIC SYNDROME; HOMEOSTASIS; HUMAN; IRON DEFICIENCY; MACROPHAGE; MALARIA; OSMOTIC STRESS; OXIDATIVE STRESS; PHOSPHATE DEFICIENCY; PHYSIOLOGY; REVIEW; SEPSIS; SICKLE CELL ANEMIA; SIGNAL TRANSDUCTION; WILSON DISEASE; CELL DEATH; CYTOLOGY; METABOLISM;

CALCIUM; CELL DEATH; ERYTHROCYTES; HUMANS; OXIDATIVE STRESS; SIGNAL TRANSDUCTION;

EID: 55049140968     PISSN: 15216543     EISSN: 15216551     Source Type: Journal    
DOI: 10.1002/iub.106     Document Type: Review

References (139)

1. Bosman G. J., Willekens F. L., and Werre J. M. (2005) Erythrocyte aging: a more than superficial resemblance to apoptosis? Cell. Physiol. Biochem. 16, 1-8.
2. Kiefer C. R. and Snyder L. M. (2000) Oxidation and erythrocyte senescence. Curr. Opin. Hematol. 7, 113-116.
3. Schwarzer E., Kühn H., Valente E., and Arese P. (2005) Band 3/COMPLEMENT-mediated recognition and removal of normally senescent and pathological human erythrocytes. Cell. Physiol. Biochem. 16, 133-146.
4. Green D. R. and Reed J. C. (1998) Mitochondria and apoptosis Science 281, 1309-1312.
5. Gulbins E., Jekle A., Ferlinz K., Grassme H., and Lang F. (2000) Physiology of apoptosis. Am. J. Physiol. Renal. Physiol. 279, F605-F615.
6. Bortner C. D. and Cidlowski J. A. (1999) Caspase independent/dependent regulation of K1, cell shrinkage, and mitochondrial membrane potential during lymphocyte apoptosis. J. Biol. Chem. 274, 21953-21962.
7. Bortner C. D. and Cidlowski J. A. (2002) Apoptotic volume decrease and the incredible shrinking cell. Cell. Death. Differ. 9, 1307-1310.
8. Bortner C. D. and Cidlowski J. A. (2004) The role of apoptotic volume decrease and ionic homeostasis in the activation and repression of apoptosis. Pflugers. Arch. 448, 313-318.
9. Javadov S. and Karmazyn M. (2007) Mitochondrial permeability transition pore opening as an endpoint to initiate cell death and as a putative target for cardioprotection. Cell. Physiol. Biochem. 20, 1-22.
10. Lang F., Busch G. L., Ritter M., Völkl H., Waldegger S., Gulbins E., and Häussinger D. (1998) Functional significance of cell volume regulatory mechanisms. Physiol. Rev. 78, 247-306.
11. Maeno E., Ishizaki Y., Kanaseki T., Hazama A., and Okada Y. (2000) Normotonic cell shrinkage because of disordered volume regulation is an early prerequisite to apoptosis. Proc. Natl. Acad. Sci. USA 97, 9487-9492.
12. Okada Y., Maeno E., Shimizu T., Dezaki K., Wang J., and Morishima S. (2001) Receptor-mediated control of regulatory volume decrease (RVD) and apoptotic volume decrease (AVD). J. Physiol. 532, 3-16.
13. Yu S. P., Canzoniero L. M., and Choi D. W. (2001) Ion homeostasis and apoptosis. Curr. Opin. Cell. Biol. 13, 405-411.
14. Daniel P. T., Wieder T., Sturm I., and Schulze-Osthoff K. (2001) The kiss of death: promises and failures of death receptors and ligands in cancer therapy. Leukemia 15, 1022-1032.
15. Grassme H., Kirschnek S., Riethmueller J., Riehle A., von Kurthy G., Lang F., Weller M., and Gulbins E. (2000) CD95/CD95 ligand interactions on epithelial cells in host defense to Pseudomonas aeruginosa. Science 290, 527-530.
16. Lang F., Szabo I., Lepple-Wienhues A., Siemen D., and Gulbins E. (1999) Physiology of receptor-mediated lymphocyte apoptosis, news. Physiol. Sci. 14, 194-200.
17. Rieger J., Frank B., Weller M., and Wick W. (2007) Mechanisms of resistance of human glioma cells to Apo2 ligand/TNF-related apoptosis-inducing ligand. Cell. Physiol. Biochem. 20, 23-34.
18. Han H., Wang J., Zhang Y., Long H., Wang H., Xu D., and Wang Z. (2004) HERG K channel conductance promotes H2O2-induced apoptosis in HEK293 cells: cellular mechanisms. Cell. Physiol. Biochem. 14, 121-134.
19. 2+ mobilisation. Cell. Physiol. Biochem. 20, 773-780.
20. Bachmeier B., Nerlich A. G., Iancu C. M., Cilli M., Schleicher E., Vene R., Dell'Eva R., Jochum M., Albini A., and Pfeffer U. (2007) The chemopreventive polyphenol Curcumin prevents hematogenous breast cancer metastases in immunodeficient mice. Cell. Physiol. Biochem. 19, 137-152.
21. Rosette C. and Karin M. (1996) Ultraviolet light and osmotic stress: activation of the JNK cascade through multiple growth factor and cytokine receptors. Science 274, 1194-1197.
22. Shimizu T., Wehner F., and Okada Y. (2006) Inhibition of hypertonicity-induced cation channels sensitizes HeLa cells to shrinkage-induced apoptosis. Cell. Physiol. Biochem. 18, 295-302.
23. Chen T., Wang J., Xing D., and Chen W. R. (2007) Spatio-temporal dynamic analysis of bid activation and apoptosis induced by alkaline condition in human lung adenocarcinoma cell. Cell. Physiol. Biochem. 20, 569-578.
24. + exchanger isoform-1 and the extracellular signal-regulated kinase induces apoptosis: a time course of events. Cell. Physiol. Biochem. 18, 211-222.
25. Becker S., Reinehr R., Graf D., Vom D. S., and Haussinger D. (2007) Hydrophobic bile salts induce hepatocyte shrinkage via NADPH oxidase activation. Cell. Physiol. Biochem. 19, 89-98.
26. Fadok V. A., Bratton D. L., Rose D. M., Pearson A., Ezekewitz R. A., and Henson P. M. (2000) A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405, 85-90.
27. Boas F. E., Forman L., and Beutler E. (1998) Phosphatidylserine exposure and red cell viability in red cell aging and in hemolytic anemia. Proc. Natl. Acad. Sci. USA 95, 3077-3081.
28. Berg C. P., Engels I. H., Rothbart A., Lauber K., Renz A., Schlosser S. F., Schulze-Osthoff K., and Wesselborg S. (2001) Human mature red blood cells express caspase-3 and caspase-8, but are devoid of mitochondrial regulators of apoptosis Cell. Death Differ. 8, 1197-1206.
29. Bratosin D., Estaquier J., Petit F., Arnoult D., Quatannens B., Tissier J. P., Slomianny C., Sartiaux C., Alonso C., Huart J. J., Montreuil J., and Ameisen J. C. (2001) Programmed cell death in mature erythrocytes: a model for investigating death effector pathways operating in the absence of mitochondria. Cell. Death Differ. 8, 1143-1156.
30. Daugas E., Cande C., and Kroemer G. (2001) Erythrocytes: death of a mummy. Cell. Death Differ. 8, 1131-1133.
31. + channels in human erythrocyte apoptosis. Am. J. Physiol. Cell. Physiol. 285, C1553-C1560.
32. 2+-induced scrambling of various fluorescently labelled lipid analogues in red blood cells. Biochem. J. 362, 741-747.
33. 2+ sensitivity of phospholipid scrambling in human red cell ghosts. Cell Calcium 25, 313-320.
34. Zhou Q., Zhao J., Wiedmer T., and Sims P. J. (2002) Normal hemostasis but defective hematopoietic response to growth factors in mice deficient in phospholipid scramblase 1. Blood 99, 4030-4038.
35. Seigneuret M. and Devaux P. F. (1984) ATP-dependent asymmetric distribution of spin-labeled phospholipids in the erythrocyte membrane: relation to shape changes. Proc. Natl. Acad. Sci USA 81, 3751-3755.
36. Lang K. S., Lang P. A., Bauer C., Duranton C., Wieder T., Huber S. M., and Lang F. (2005) Mechanisms of suicidal erythrocyte death. Cell. Physiol. Biochem. 15, 195-202.
37. Lang K. S., Duranton C., Poehlmann H., Myssina S., Bauer C., Lang F., Wieder T., and Huber S. M. (2003) Cation channels trigger apoptotic death of erythrocytes. Cell. Death. Differ. 10, 249-256.
38. Barvitenko N. N., Adragna N. C., and Weber R. E. (2005) Erythrocyte signal transduction pathways, their oxygenation dependence and functional significance. Cell. Physiol. Biochem. 15, 1-18.
39. Bracci R., Perrone S., and Buonocore G. (2002) Oxidant injury in neonatal erythrocytes during the perinatal period. Acta. Paediatr. Suppl. 91, 130-134.
40. Lang K. S., Roll B., Myssina S., Schittenhelm M., Scheel-Walter H. G., Kanz L., Fritz J., Lang F., Huber S. M., and Wieder T. (2002) Enhanced erythrocyte apoptosis in sickle cell anemia, thalassemia and glucose-6-phosphate dehydrogenase deficiency. Cell. Physiol. Biochem. 12, 365-372.
41. Head D. J., Lee Z. E., Poole J., and Avent N. D. (2005) Expression of phosphatidylserine (PS) on wild-type and Gerbich variant erythrocytes following glycophorin-C (GPC) ligation. Br. J. Haematol. 129, 130-137.
42. Head D. J., Lee Z. E., Swallah M. M., and Avent N. D. (2005) Ligation of CD47 mediates phosphatidylserine expression on erythrocytes and a concomitant loss of viability in vitro. Br. J. Haematol. 130, 788-790.
43. Mandal D., Mazumder A., Das P., Kundu M., and Basu J. (2005) FAS-,caspase 8-and caspase 3-dependent signaling regulates the activity of the aminophospholipid translocase and phosphatidylserine externalization in human erythrocytes. J. Biol. Chem. 280, 39460-39467.
44. Lang K. S., Myssina S., Brand V., Sandu C., Lang P. A., Berchtold S., Huber S. M., Lang F., and Wieder T. (2004) Involvement of ceramide in hyperosmotic shock-induced death of erythrocytes. Cell. Death. Differ. 11, 231-243.
45. 2 in the regulation of programmed erythrocyte death. Cell. Death. Differ. 12, 415-428.
46. Lang P. A., Kempe D. S., Tanneur V., Eisele K., Klarl B. A., Myssina S., Jendrossek V., Ishii S., Shimizu T., Waidmann M., Hessler G., Huber S. M., Lang F., and Wieder T. (2005) Stimulation of erythrocyte ceramide formation by platelet-activating factor. J. Cell. Sci. 118, 1233-1243.
47. Attanasio P., Shumilina E., Hermle T., Kiedaisch V., Lang P. A., Huber S. M., Wieder T., and Lang F. (2007) Stimulation of eryptosis by anti-A IgG antibodies. Cell. Physiol. Biochem. 20, 591-600.
48. Lang P. A., Kaiser S., Myssina S., Birka C., Weinstock C., Northoff H., Wieder T., Lang F., and Huber S. M. (2004) Effect of Vibrio parahaemolyticus haemolysin on human erythrocytes. Cell. Microbiol. 6, 391-400.
49. Foller M., Shumilina E., Lam R., Mohamed W., Kasinathan R., Huber S., Chakraborty T., and Lang F. (2007) Induction of suicidal erythrocyte death by listeriolysin from Listeria monocytogenes. Cell. Physiol. Biochem. 20, 1051-1060.
50. Lang P. A., Huober J., Bachmann C., Kempe D. S., Sobiesiak M., Akel A., Niemoeller O. M., Dreischer P., Eisele K., Klarl B. A., Gulbins E., Lang F., and Wieder T. (2006) Stimulation of erythrocyte phosphatidylserine exposure by paclitaxel. Cell. Physiol. Biochem. 18, 151-164.
51. Föller M., Geiger C., Mahmud H., Nicolay J. P., and Lang F. (2008) Stimulation of suicidal erythrocyte death by amantadine. Eur. J. Pharmacol. 581, 13-18.
52. Geiger C., Föller M., Herrlinger K. R., and Lang F. (2008) Azathioprine-induced suicidal erythrocyte death. Inflamm. Bowel Diseases, in press.
53. Niemoeller O. M., Foller M., Lang C., Huber S. M., and Lang F. (2008) Retinoic acid induced suicidal erythrocyte death. Cell. Physiol. Biochem. 21, 193-202.
54. Akel A., Hermle T., Niemoeller O. M., Kempe D. S., Lang P. A., Attanasio P., Podolski M., Wieder T., and Lang F. (2006) Stimulation of erythrocyte phosphatidylserine exposure by chlorpromazine. Eur. J. Pharmacol. 532, 11-17.
55. Niemoeller O. M., Akel A., Lang P. A., Attanasio P., Kempe D. S., Hermle T., Sobiesiak M., Wieder T., and Lang F. (2006) Induction of eryptosis by cyclosporine. Naunyn Schmiedebergs Arch. Pharmacol. 374, 41-49.
56. Nicolay J. P., Schneider J., Niemoeller O. M., Artunc F., Portero-Otin M., Haik G., Jr., Thornalley P. J., Schleicher E., Wieder T., and Lang F. (2006) Stimulation of suicidal erythrocyte death by methylglyoxal. Cell. Physiol. Biochem. 18, 223-232.
57. Nicolay J. P., Gatz S., Liebig G., Gulbins E., and Lang F. (2007) Amyloid induced suicidal erythrocyte death. Cell. Physiol. Biochem. 19, 175-184.
58. Bentzen P. J. and Lang F. (2007) Effect of anandamide on erythrocyte survival. Cell. Physiol. Biochem. 20, 1033-1042.
59. Shumilina E., Kiedaisch V., Akkel A., Lang P., Hermle T., Kempe D. S., Huber S. M., Wieder T., Laufer S. and Lang F. (2006) Stimulation of suicidal erythrocyte death by lipoxygenase inhibitor Bay-Y5884. Cell. Physiol. Biochem. 18, 233-242.
60. Bentzen P. J., Lang E., and Lang F. (2007) Curcumin induced suicidal erythrocyte death. Cell. Physiol. Biochem. 19, 153-164.
61. + loss. Cell. Physiol. Biochem. 20, 35-44.
62. Niemoeller O. M., Kiedaisch V., Dreischer P., Wieder T., and Lang F. (2006) Stimulation of eryptosis by aluminium ions. Toxicol. Appl. Pharmacol. 217, 168-175.
63. Eisele K., Lang P. A., Kempe D. S., Klarl B. A., Niemoller O., Wieder T., Huber S. M., Duranton C., and Lang F. (2006) Stimulation of erythrocyte phosphatidylserine exposure by mercury ions. Toxicol. Appl. Pharmacol. 210, 116-122.
64. Kempe D. S., Lang P. A., Eisele K., Klarl B. A., Wieder T., Huber S. M., Duranton C., and Lang F. (2005) Stimulation of erythrocyte phosphatidylserine exposure by lead ions. Am. J. Physiol. Cell. Physiol. 288, C396-C402.
65. 2+ entry into and subsequent suicidal death of erythrocytes. Toxicology 244, 271-279.
66. Föller M., Sopjani M., Mahmud H., and Lang F. (2008) Vanadate induced suicidal erythrocyte death. Kidney Blood Pres. Res. 31, 87-93.
67. Lang P. A., Schenck M., Nicolay J. P., Becker J. U., Kempe D. S., Lupescu A., Koka S., Eisele K., Klarl B. A., Rubben H., Schmid K. W., Mann K., Hildenbrand S., Hefter H., Huber S. M., Wieder T., Erhardt A., Haussinger D., Gulbins E., and Lang F. (2007) Liver cell death and anemia in Wilson disease involve acid sphingomyelinase and ceramide. Nat. Med. 13, 164-170.
68. Allan D. and Michell R. H. (1977) Calcium ion-dependent diacylglycerol accumulation in erythrocytes is associated with microvesiculation but not with efflux of potassium ions. Biochem. J. 166, 495-499.
69. Pant H. C., Virmani M. and Gallant P. E. (1983) Calcium-induced proteolysis of spectrin and band 3 protein in rat erythrocyte membranes. Biochem. Biophys. Res. Commun. 117, 372-377.
70. Kaestner L. and Bernhardt I. (2002) Ion channels in the human red blood cell membrane: their further investigation and physiological relevance. Bioelectrochemistry 55, 71-74.
71. Kaestner L., Tabellion W., Lipp P., and Bernhardt I. (2004) Prostaglandin E2 activates channel-mediated calcium entry in human erythrocytes: an indication for a blood clot formation supporting process. Thromb. Haemost. 92, 1269-1272.
72. 2+ leak of human erythrocytes. Cell. Physiol. Biochem. 21, 183-192.
73. Huber S. M., Gamper N., and Lang F. (2001) Chloride conductance and volume-regulatory nonselective cation conductance in human red blood cell ghosts. Pflugers. Arch. 441, 551-558.
74. --dependent cation conductance in human red blood cells. J. Physiol. 539, 847-855.
75. Bookchin R. M., Ortiz O. E., and Lew V. L. (1987) Activation of calcium-dependent potassium channels in deoxygenated sickled red cells. Prog. Clin. Biol. Res. 240, 193-200.
76. + transport and cell dehydration in sickle erythrocytes by clotrimazole and other imidazole derivatives. J. Clin. Invest. 92, 520-526.
77. Franco R. S., Palascak M., Thompson H., Rucknagel D. L., and Joiner C. H. (1996) Dehydration of transferrin receptor-positive sickle reticulocytes during continuous or cyclic deoxygenation: role of KCl cotransport and extracellular calcium. Blood 88, 4359-4365
78. Lang P. A., Warskulat U., Heller-Stilb B., Huang D. Y., Grenz A., Myssina S., Duszenko M., Lang F., Haussinger D., Vallon V., and Wieder T. (2003) Blunted apoptosis of erythrocytes from taurine transporter deficient mice. Cell. Physiol. Biochem. 13, 337-346.
79. + movements in the membrane signal induced by PAF-acether. Biochem. Pharmacol. 35, 2811-2815.
80. Rivera A., Jarolim P., and Brugnara C. (2002) Modulation of Gardos channel activity by cytokines in sickle erythrocytes. Blood 99, 357-603.
81. Dupuis F., Levasseur S., Jean-Louis F., Dulery C., Praloran V., Denizot Y., and Michel L. (1997) Production, metabolism and effect of platelet-activating factor on the growth of the human K562 erythroid cell line. Biochim. Biophys. Acta. 1359, 241-249.
82. Klarl B. A., Lang P. A., Kempe D. S., Niemoeller O. M., Akel A., Sobiesiak M., Eisele K., Podolski M., Huber S. M., Wieder T., and Lang F. (2006) Protein kinase C mediates erythrocyte "programmed cell death" following glucose depletion. Am. J. Physiol. Cell. Physiol. 290, C244-C253.
83. Andrews D. A., Yang L., and Low P. S. (2002) Phorbol ester stimulates a protein kinase C-mediated agatoxin-TK-sensitive calcium permeability pathway in human red blood cells. Blood 100, 3392-3399.
84. deJong K., Rettig M. P., Low P. S., and Kuypers F. A. (2002) Protein kinase C activation induces phosphatidylserine exposure on red blood cells. Biochemistry 41, 12562-12567.
85. Govekar R. B. and Zingde S. M. (2001) Protein kinase C isoforms in human erythrocytes. Ann. Hematol. 80, 531-534.
86. Danilov Y. N. and Cohen C. M. (1989) Wheat germ agglutinin but not concanavalin A modulates protein kinase C-mediated phosphorylation of red cell skeletal proteins. FEBS Lett. 257, 431-434.
87. + antiport activity by adrenaline on erythrocytes from normal and obese individuals. Mol. Cell. Endocrinol. 205, 141-150.
88. Bilmen S., Aksu T. A., Gumuslu S., Korgun D. K., and Canatan D. (2001) Antioxidant capacity of G-6-PD-deficient erythrocytes. Clin. Chim. Acta. 303, 83-86.
89. Damonte G., Guida L., Sdraffa A., Benatti U., Melloni E., Forteleoni G., Meloni T., Carafoli E., and De Flora A. (1992) Mechanisms of perturbation of erythrocyte calcium homeostasis in favism. Cell. Calcium. 13, 649-658.
90. Mavelli I., Ciriolo M. R., Rossi L., Meloni T., Forteleoni G., De Flora A., Benatti U., Morelli A., and Rotilio G. (1984) Favism: a hemolytic disease associated with increased superoxide dismutase and decreased glutathione peroxidase activities in red blood cells. Eur. J. Biochem. 139, 13-18.
91. - channels of human erythrocytes by membrane oxidation. EMBO J. 21, 22-30.
92. Tanneur V., Duranton C., Brand V. B., Sandu C. D., Akkaya C., Kasinathan R. S., Gachet C., Sluyter R., Barden J. A., Wiley J. S., Lang F., and Huber S. M. (2006) Purinoceptors are involved in the induction of an osmolyte permeability in malaria-infected and oxidized human erythrocytes. FASEB J. 20, 133-135.
93. 2+-induced Erythrocyte 'Apoptosis.' Cell. Physiol. Biochem. 14, 241-248.
94. Matarrese P., Straface E., Pietraforte D., Gambardella L., Vona R., Maccaglia A., Minetti M., and Malorni W. (2005) Peroxynitrite induces senescence and apoptosis of red blood cells through the activation of aspartyl and cysteinyl proteases. FASEB J. 19, 416-418.
95. Mandal D., Baudin-Creuza V., Bhattacharyya A., Pathak S., Delaunay J., Kundu M., and Basu J. (2003) Caspase 3-mediated proteolysis of the N-terminal cytoplasmic domain of the human erythroid anion exchanger 1 (band 3). J. Biol. Chem. 278, 52551-52558.
96. Mandal D., Moitra P. K., Saha S., and Basu J. (2002) Caspase 3 regulates phosphatidylserine externalization and phagocytosis of oxidatively stressed erythrocytes. FEBS Lett. 513, 184-188.
97. Weil M., Jacobson M. D., and Raff M. C. (1998) Are caspases involved in the death of cells with a transcriptionally inactive nucleus? Sperm and chicken erythrocytes. J. Cell. Sci. 111 (Pt 18), 2707-2715.
98. Myssina S., Huber S. M., Birka C., Lang P. A., Lang K. S., Friedrich B., Risler T., Wieder T., and Lang F. (2003) Inhibition of erythrocyte cation channels by erythropoietin. J. Am. Soc. Nephrol. 14, 2750-2757.
99. Jelkmann W. (1992) Erythropoietin: structure, control of production, and function. Physiol. Rev. 72, 449-489.
100. Polenakovic M. and Sikole A. (1996) Is erythropoietin a survival factor for red blood cells? J. Am. Soc. Nephrol. 7, 1178-1182.
101. Lang P. A., Kempe D. S., Akel A., Klarl B. A., Eisele K., Podolski M., Hermle T., Niemoeller O. M., Attanasio P., Huber S. M., Wieder T., Lang F., and Duranton C. (2005) Inhibition of erythrocyte "apoptosis" by catecholamines. Naunyn Schmiedebergs Arch. Pharmacol. 372, 228-235.
102. Lakshmi C., Deb C., Ray C., and Ray M. R. (2005) Reduction of hematotoxicity and augmentation of antitumor efficacy of cyclophosphamide by dopamine. Neoplasma 52, 68-73.
103. Lang K. S., Myssina S., Tanneur V., Wieder T., Huber S. M., Lang F., and Duranton C. (2003) Inhibition of erythrocyte cation channels and apoptosis by ethylisopropylamiloride. Naunyn Schmiedebergs Arch. Pharmacol. 367, 391-396.
104. Kasinathan R. S., Föller M., Koka S., Huber S. M., and Lang F. (2007) Inhibition of eryptosis and intraerythrocytic growth of Plasmodium falciparum by flufenamic acid. Naunyn Schmiedebergs Arch. Pharmacol. 374, 255-264.
105. Niemoeller O. M., Bentzen P. J., Lang E., and Lang F. (2007) Adenosine protects against suicidal erythrocyte death. Pflugers. Arch. 454, 427-439.
106. Nicolay J. P., Liebig G., Niemoeller O. M., Koka S., Ghashghaeinia M., Wieder T., Haendeler J., Busse R., and Lang F. (2008) Inhibition of suicidal erythrocyte death by nitric oxide. Pflugers Arch. 456, 293-305.
107. Das A., Smolenski A., Lohmann S. M., and Kukreja R. C. (2006) Cyclic GMP-dependent protein kinase Iα attenuates necrosis and apoptosis following ischemia/reoxygenation in adult cardiomyocyte. J. Biol. Chem. 281, 38644-38652.
108. Li J. and Billiar T. R. (1999) The anti-apoptotic actions of nitric oxide in hepatocytes. Cell. Death Differ. 6, 952-955.
109. Föller M., Feil S., Ghoreschi K., Koka S., Gerling A., Thunemann M., Hofmann F., Schuler B., Vogel J., Pichler B., Kasinathan R. S., Nicolay J. P., Huber S. M., Lang F., and Feil R. (2008) Anemia and splenomegaly in cGKI-deficient mice. Proc. Natl. Acad. Sci. USA. 105, 6771-6776.
110. Crawford J. H., Isbell T. S., Huang Z., Shiva S., Chacko B. K., Schechter A. N., Darley-Usmar V. M., Kerby J. D., Lang J. D., Jr., Kraus D., Ho C., Gladwin M. T., and Patel R. P. (2006) Hypoxia, red blood cells, and nitrite regulate NO-dependent hypoxic vasodilation. Blood 107, 566-574.
111. Dejam A., Hunter C. J., Pelletier M. M., Hsu L. L., Machado R. F., Shiva S., Power G. G., Kelm M., Gladwin M. T., and Schechter A. N. (2005) Erythrocytes are the major intravascular storage sites of nitrite in human blood. Blood 106, 734-739.
112. Grubina R., Huang Z., Shiva S., Joshi M. S., Azarov I., Basu S., Ringwood L. A., Jiang A., Hogg N., Kim-Shapiro D. B., and Gladwin M. T. (2007) Concerted nitric oxide formation and release from the simultaneous reactions of nitrite with deoxy- and oxyhemoglobin. J. Biol. Chem. 282, 12916-12927.
113. McMahon T. J., Moon R. E., Luschinger B. P., Carraway M. S., Stone A. E., Stolp B. W., Gow A. J., Pawloski J. R., Watke P., Singel D. J., Piantadosi C. A., and Stamler J. S. (2002) Nitric oxide in the human respiratory cycle. Nat. Med. 8, 711-717.
114. Angelo M., Singel D. J., and Stamler J. S. (2006) An S-nitrosothiol (SNO) synthase function of hemoglobin that utilizes nitrite as a substrate. Proc. Natl. Acad. Sci. USA 103, 8366-8371.
115. Diesen D. and Stamler J. S. (2007) S-Nitrosylation and PEGylation of hemoglobin: toward a blood substitute that recapitulates blood. J. Mol. Cell. Cardiol. 42, 921-923.
116. Power G. G., Bragg S. L., Oshiro B. T., Dejam A., Hunter C. J., and Blood A. B. (2007) A novel method of measuring reduction of nitrite-induced methemoglobin applied to fetal and adult blood of humans and sheep. J. Appl. Physiol. 103, 1359-1365.
117. Reynolds J. D., Ahearn G. S., Angelo M., Zhang J., Cobb F., and Stamler J. S. (2007) S-nitrosohemoglobin deficiency: a mechanism for loss of physiological activity in banked blood. Proc. Natl. Acad. Sci. USA 104, 17058-17062.
118. Yang B. C., Nichols W. W., and Mehta J. L. (1996) Cardioprotective Effects of Red Blood Cells on Ischemia and Reperfusion Injury in Isolated Rat Heart: Release of Nitric Oxide as a Potential Mechanism. J. Cardiovasc. Pharmacol. Ther. 1, 297-306.
119. Pawloski J. R., Hess D. T., and Stamler J. S. (2005) Impaired vasodilation by red blood cells in sickle cell disease. Proc. Natl. Acad. Sci. USA 102, 2531-2536.
120. Lang F., Lang P. A., Lang K. S., Brand V., Tanneur V., Duranton C., Wieder T., and Huber S. M. (2004) Channel-induced apoptosis of infected host cells -the case of malaria. Pflugers Arch. 448, 319-324.
121. Duranton C., Huber S., Tanneur V., Lang K., Brand V., Sandu C., and Lang F. (2003) Electrophysiological properties of the Plasmodium Falciparum-induced cation conductance of human erythrocytes. Cell. Physiol. Biochem. 13, 189-198.
122. Kirk K. (2001) Membrane transport in the malaria-infected erythrocyte. Physiol. Rev. 81, 495-537.
123. Brand V. B., Sandu C. D., Duranton C., Tanneur V., Lang K. S., Huber S. M., and Lang F. (2003) Dependence of plasmodium falciparum in vitro growth on the cation permeability of the human host erythrocyte. Cell. Physiol. Biochem. 13, 347-356.
124. Ayi K., Turrini F., Piga A., and Arese P. (2004) Enhanced phagocytosis of ring-parasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and β-thalassemia trait. Blood 104, 3364-3371.
125. Cappadoro M., Giribaldi G., O'Brien E., Turrini F., Mannu F., Ulliers D., Simula G., Luzzatto L., and Arese P. (1998) Early phagocytosis of glucose-6-phosphate dehydrogenase (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency. Blood 92, 2527-2534.
126. deJong K., Emerson R. K., Butler J., Bastacky J., Mohandas N., and Kuypers F. A. (2001) Short survival of phosphatidylserine-exposing red blood cells in murine sickle cell anemia. Blood 98, 1577-1584.
127. Kean L. S., Brown L. E., Nichols J. W., Mohandas N., Archer D. R., and Hsu L. L. (2002) Comparison of mechanisms of anemia in mice with sickle cell disease and β-thalassemia: peripheral destruction, ineffective erythropoiesis, and phospholipid scramblase-mediated phosphatidylserine exposure. Exp. Hematol. 30, 394-402.
128. Kuypers F. A., Yuan J., Lewis R. A., Snyder L. M., Kiefer C. R., Bunyaratvej A., Fucharoen S., Ma L., Styles L., de Jong K., and Schrier S. L. (1998) Membrane phospholipid asymmetry in human thalassemia. Blood 91, 3044-3051.
129. Koka S., Foller M., Lamprecht G., Boini K. M., Lang C., Huber S. M., and Lang F. (2007) Iron deficiency influences the course of malaria in Plasmodium berghei infected mice. Biochem. Biophys. Res. Commun. 357, 608-614.
130. Koka S., Huber S. M., Boini K. M., Lang C., Foller M., and Lang F. (2007) Lead decreases parasitemia and enhances survival of Plasmodium berghei-infected mice. Biochem. Biophys. Res. Commun. 363, 484-489.
131. Egberts J. and Van Pelt J. (2004) Evaluation of the blood analyzer ABL 735 radiometer for determination of the percentage of fetal hemoglobin in fetal and neonatal blood. Scand. J Clin. Lab. Invest. 64, 128-131.
132. Hermle T., Shumilina E., Attanasio P., Akel A., Kempe D. S., Lang P. A., Podolski M., Gatz S., Bachmann R., Bachmann C., Abele H., Huber S., Wieder T., and Lang F. (2006) Decreased cation channel activity and blunted channel-dependent eryptosis in neonatal erythrocytes. Am. J. Physiol. Cell. Physiol. 291, C710-C717.
133. Rice L. and Alfrey C. P. (2005) The negative regulation of red cell mass by neocytolysis: physiologic and pathophysiologic manifestations. Cell. Physiol. Biochem. 15, 245-250.
134. Foller M., Kasinathan R. S., Koka S., Huber S. M., Schuler B., Vogel J., Gassmann M., and Lang F. (2007) Enhanced susceptibility to suicidal death of erythrocytes from transgenic mice overexpressing erythropoietin. Am. J. Physiol. Regul. Integr. Comp. Physiol. 293, R1127-R1134.
135. Kempe D. S., Akel A., Lang P. A., Hermle T., Biswas R., Muresanu J., Friedrich B., Dreischer P., Wolz C., Schumacher U., Peschel A., Gotz F., Doring G., Wieder T., Gulbins E., and Lang F. (2007) Suicidal erythrocyte death in sepsis. J. Mol. Med. 85, 269-277.
136. Lang P. A., Beringer O., Nicolay J. P., Amon O., Kempe D. S., Hermle T., Attanasio P., Akel A., Schafer R., Friedrich B., Risler T., Baur M., Olbricht C. J., Zimmerhackl L. B., Zipfel P. F., Wieder T., and Lang F. (2006) Suicidal death of erythrocytes in recurrent hemolytic uremic syndrome. J. Mol. Med. 84, 378-388.
137. Wood B. L., Gibson D. F., and Tait J. F. (1996) Increased erythrocyte phosphatidylserine exposure in sickle cell disease: flow-cytometric measurement and clinical associations. Blood 88, 1873-1880.
138. Birka C., Lang P. A., Kempe D. S., Hoefling L., Tanneur V., Duranton C., Nammi S., Henke G., Myssina S., Krikov M., Huber S. M., Wieder T., and Lang F. (2004) Enhanced susceptibility to erythrocyte "apoptosis" following phosphate depletion. Pflugers Arch. 448, 471-477.
139. Gitlin J. D. (2003) Wilson disease. Gastroenterology 125, 1868-1877.