Mechanisms and pathophysiological significance of eryptosis, the suicidal erythrocyte death

Seminars in Cell and Developmental Biology

Volumn 39, Issue , 2015, Pages 35-42

  Lang, Elisabeth ^a   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Chronic kidney disease; Diabetes; Eryptosis; Malaria; Sickle cell disease

Indexed keywords

ADENYLATE KINASE; CALCIUM ION; JANUS KINASE 3; MITOGEN ACTIVATED PROTEIN KINASE P38; P21 ACTIVATED KINASE 2; PHOSPHATE; PROTEIN KINASE C;

ANEMIA; CALCIUM TRANSPORT; CELL DEATH; CELL MEMBRANE; CHRONIC KIDNEY FAILURE; DEHYDRATION; DIABETES MELLITUS; ENZYME ACTIVITY; ERYPTOSIS; ERYTHROCYTE; FEVER; GLUCOSE 6 PHOSPHATE DEHYDROGENASE DEFICIENCY; HEMOLYSIS; HEMOLYTIC UREMIC SYNDROME; HUMAN; HYPEROSMOTIC STRESS; INTOXICATION; IRON DEFICIENCY; LIVER FAILURE; MALARIA; MICROCIRCULATION; MOLECULAR MECHANICS; MYCOPLASMOSIS; NEOPLASM; OXIDATIVE STRESS; PATHOPHYSIOLOGY; PHOSPHATE DEFICIENCY; REVIEW; SEPSIS; SICKLE CELL ANEMIA; THALASSEMIA; WILSON DISEASE; ANIMAL; CELL AGING; PATHOLOGY;

MYCOPLASMA;

ANIMALS; CELL AGING; CELL DEATH; CELL MEMBRANE; ERYTHROCYTES; HUMANS; OXIDATIVE STRESS;

EID: 84928208168     PISSN: 10849521     EISSN: 10963634     Source Type: Journal    
DOI: 10.1016/j.semcdb.2015.01.009     Document Type: Review

References (189)

1. Arese P., Turrini F., Schwarzer E. Band 3/complement-mediated recognition and removal of normally senescent and pathological human erythrocytes. Cell Physiol Biochem 2005, 16:133-146.
2. Bosman G.J., Willekens F.L., Werre J.M. Erythrocyte aging: a more than superficial resemblance to apoptosis. Cell Physiol Biochem 2005, 16:1-8.
3. Kiefer C.R., Snyder L.M. Oxidation and erythrocyte senescence. Curr Opin Hematol 2000, 7:113-116.
4. Lutz H.U. Innate immune and non-immune mediators of erythrocyte clearance. Cell Mol Biol (Noisy-le-grand) 2004, 50:107-116.
5. Lang F., Lang K.S., Lang P.A., Huber S.M., Wieder T. Mechanisms and significance of eryptosis. Antioxid Redox Signal 2006, 8:1183-1192.
6. Lang E., Qadri S.M., Lang F. Killing me softly - suicidal erythrocyte death. Int J Biochem Cell Biol 2012, 44:1236-1243.
7. Cimen M.Y. Free radical metabolism in human erythrocytes. Clin Chim Acta 2008, 390:1-11.
8. Foller M., Bobbala D., Koka S., Huber S.M., Gulbins E., Lang F. Suicide for survival - death of infected erythrocytes as a host mechanism to survive malaria. Cell Physiol Biochem 2009, 24:133-140.
9. Nguyen D.B., Wagner-Britz L., Maia S., Steffen P., Wagner C., Kaestner L., et al. Regulation of phosphatidylserine exposure in red blood cells. Cell Physiol Biochem 2011, 28:847-856.
10. Lang F., Qadri S.M. Mechanisms and significance of eryptosis, the suicidal death of erythrocytes. Blood Purif 2012, 33:125-130.
11. Lang F., Abed M., Lang E., Foller M. Oxidative stress and suicidal erythrocyte death. Antioxid Redox Signal 2014, 21:138-153.
12. Lang F., Lang E., Foller M. Physiology and pathophysiology of eryptosis. Transfus Med Hemother 2012, 39:308-314.
13. Lang K.S., Duranton C., Poehlmann H., Myssina S., Bauer C., Lang F., et al. Cation channels trigger apoptotic death of erythrocytes. Cell Death Differ 2003, 10:249-256.
14. Klarl B.A., Lang P.A., Kempe D.S., Niemoeller O.M., Akel A., Sobiesiak M., et al. Protein kinase C mediates erythrocyte programmed cell death following glucose depletion. Am J Physiol Cell Physiol 2006, 290:C244-C253.
15. Kamp D., Sieberg T., Haest C.W.M. Inhibition and stimulation of phospholipid scrambling activity. Consequences for lipid asymmetry, echinocytosis, and microvesiculation of erythrocytes. Biochemistry 2001, 40:9438-9446.
16. Foller M., Mahmud H., Gu S., Wang K., Floride E., Kucherenko Y., et al. Participation of leukotriene C(4) in the regulation of suicidal erythrocyte death. J Physiol Pharmacol 2009, 60:135-143.
17. Foller M., Sopjani M., Koka S., Gu S., Mahmud H., Wang K., et al. Regulation of erythrocyte survival by AMP-activated protein kinase. FASEB J 2009, 23:1072-1080.
18. Duranton C., Huber S.M., Lang F. Oxidation induces a Cl(-)-dependent cation conductance in human red blood cells. J Physiol 2002, 539:847-855.
19. Lang P.A., Kempe D.S., Myssina S., Tanneur V., Birka C., Laufer S., et al. PGE(2) in the regulation of programmed erythrocyte death. Cell Death Differ 2005, 12:415-428.
20. Kaestner L., Bernhardt I. Ion channels in the human red blood cell membrane: their further investigation and physiological relevance. Bioelectrochemistry 2002, 55:71-74.
21. Foller M., Harris I.S., Elia A., John R., Lang F., Kavanagh T.J., et al. Functional significance of glutamate-cysteine ligase modifier for erythrocyte survival in vitro and in vivo. Cell Death Differ 2013, 20:1350-1358.
22. Bilmen S., Aksu T.A., Gumuslu S., Korgun D.K., Canatan D. Antioxidant capacity of G-6-PD-deficient erythrocytes. Clin Chim Acta 2001, 303:83-86.
23. Mavelli I., Ciriolo M.R., Rossi L., Meloni T., Forteleoni G., De Flora A., et al. Favism: a hemolytic disease associated with increased superoxide dismutase and decreased glutathione peroxidase activities in red blood cells. Eur J Biochem 1984, 139:13-18.
24. Damonte G., Guida L., Sdraffa A., Benatti U., Melloni E., Forteleoni G., et al. Mechanisms of perturbation of erythrocyte calcium homeostasis in favism. Cell Calcium 1992, 13:649-658.
25. Vota D.M., Crisp R.L., Nesse A.B., Vittori D.C. Oxidative stress due to aluminum exposure induces eryptosis which is prevented by erythropoietin. J Cell Biochem 2012, 113:1581-1589.
26. Myssina S., Huber S.M., Birka C., Lang P.A., Lang K.S., Friedrich B., et al. Inhibition of erythrocyte cation channels by erythropoietin. J Am Soc Nephrol 2003, 14:2750-2757.
27. + transport and cell dehydration in sickle erythrocytes by clotrimazole and other imidazole derivatives. J Clin Invest 1993, 92:520-526.
28. + channels in human erythrocyte apoptosis. Am J Physiol Cell Physiol 2003, 285:C1553-C1560.
29. Huber S.M., Uhlemann A.C., Gamper N.L., Duranton C., Kremsner P.G., Lang F. Plasmodium falciparum activates endogenous Cl(-) channels of human erythrocytes by membrane oxidation. EMBO J 2002, 21:22-30.
30. Tanneur V., Duranton C., Brand V.B., Sandu C.D., Akkaya C., Kasinathan R.S., et al. Purinoceptors are involved in the induction of an osmolyte permeability in malaria-infected and oxidized human erythrocytes. FASEB J 2006, 20:133-135.
31. Lang F., Busch G.L., Ritter M., Volkl H., Waldegger S., Gulbins E., et al. Functional significance of cell volume regulatory mechanisms. Physiol Rev 1998, 78:247-306.
32. Berg C.P., Engels I.H., Rothbart A., Lauber K., Renz A., Schlosser S.F., et al. 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.
33. Mandal D., Baudin-Creuza V., Bhattacharyya A., Pathak S., Delaunay J., Kundu M., et al. Caspase 3-mediated proteolysis of the N-terminal cytoplasmic domain of the human erythroid anion exchanger 1 (band 3). J Biol Chem 2003, 278:52551-52558.
34. Bratosin D., Estaquier J., Petit F., Arnoult D., Quatannens B., Tissier J.P., et al. 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.
35. Lau I.P., Chen H., Wang J., Ong H.C., Leung K.C., Ho H.P., et al. In vitro effect of CTAB- and PEG-coated gold nanorods on the induction of eryptosis/erythroptosis in human erythrocytes. Nanotoxicology 2012, 6:847-856.
36. Maellaro E., Leoncini S., Moretti D., Del Bello B., Tanganelli I., De Felice C., et al. Erythrocyte caspase-3 activation and oxidative imbalance in erythrocytes and in plasma of type 2 diabetic patients. Acta Diabetol 2013, 50:489-495.
37. Mandal D., Moitra P.K., Saha S., Basu J. Caspase 3 regulates phosphatidylserine externalization and phagocytosis of oxidatively stressed erythrocytes. FEBS Lett 2002, 513:184-188.
38. Matarrese P., Straface E., Pietraforte D., Gambardella L., Vona R., Maccaglia A., et al. Peroxynitrite induces senescence and apoptosis of red blood cells through the activation of aspartyl and cysteinyl proteases. FASEB J 2005, 19:416-418.
39. Lang K.S., Myssina S., Brand V., Sandu C., Lang P.A., Berchtold S., et al. Involvement of ceramide in hyperosmotic shock-induced death of erythrocytes. Cell Death Differ 2004, 11:231-243.
40. Weil M., Jacobson M.D., Raff M.C. Are caspases involved in the death of cells with a transcriptionally inactive nucleus? Sperm and chicken erythrocytes. J Cell Sci 1998, 111(Pt (18)):2707-2715.
41. Bhavsar S.K., Gu S., Bobbala D., Lang F. Janus kinase 3 is expressed in erythrocytes, phosphorylated upon energy depletion and involved in the regulation of suicidal erythrocyte death. Cell Physiol Biochem 2011, 27:547-556.
42. Zelenak C., Foller M., Velic A., Krug K., Qadri S.M., Viollet B., et al. Proteome analysis of erythrocytes lacking AMP-activated protein kinase reveals a role of PAK2 kinase in eryptosis. J Proteome Res 2011, 10:1690-1697.
43. Zelenak C., Eberhard M., Jilani K., Qadri S.M., Macek B., Lang F. Protein kinase CK1alpha regulates erythrocyte survival. Cell Physiol Biochem 2012, 29:171-180.
44. Kucherenko Y., Zelenak C., Eberhard M., Qadri S.M., Lang F. Effect of casein kinase 1alpha activator pyrvinium pamoate on erythrocyte ion channels. Cell Physiol Biochem 2012, 30:407-417.
45. Gatidis S., Zelenak C., Fajol A., Lang E., Jilani K., Michael D., et al. p38 MAPK activation and function following osmotic shock of erythrocytes. Cell Physiol Biochem 2011, 28:1279-1286.
46. Lupescu A., Shaik N., Jilani K., Zelenak C., Lang E., Pasham V., et al. Enhanced erythrocyte membrane exposure of phosphatidylserine following sorafenib treatment: an in vivo and in vitro study. Cell Physiol Biochem 2012, 30:876-888.
47. Shaik N., Lupescu A., Lang F. Sunitinib-sensitive suicidal erythrocyte death. Cell Physiol Biochem 2012, 30:512-522.
48. Foller M., Feil S., Ghoreschi K., Koka S., Gerling A., Thunemann M., et al. Anemia and splenomegaly in cGKI-deficient mice. Proc Natl Acad Sci U S A 2008, 105:6771-6776.
49. Das A., Smolenski A., Lohmann S.M., Kukreja R.C. Cyclic GMP-dependent protein kinase I alpha attenuates necrosis and apoptosis following ischemia/reoxygenation in adult cardiomyocyte. J Biol Chem 2006, 281:38644-38652.
50. Li J.R., Billiar T.R. The anti-apoptotic actions of nitric oxide in hepatocytes. Cell Death Differ 1999, 6:952-955.
51. Nagai-Kusuhara A., Nakamura M., Mukuno H., Kanamori A., Negi A., Seigel G.M. cAMP-responsive element binding protein mediates a cGMP/protein kinase G-dependent anti-apoptotic signal induced by nitric oxide in retinal neuro-glial progenitor cells. Exp Eye Res 2007, 84:152-162.
52. Schlossmann J., Feil R., Hofmann F. Insights into cGMP signalling derived from cGMP kinase knockout mice. Front Biosci 2005, 10:1279-1289.
53. Owusu B.Y., Stapley R., Patel R.P. Nitric oxide formation versus scavenging: the red blood cell balancing act. J Physiol (Lond) 2012, 590:4993-5000.
54. Kahn M.J., Maley J.H., Lasker G.F., Kadowitz P.J. Updated role of nitric oxide in disorders of erythrocyte function. Cardiovasc Hematol Disord Drug Targets 2013, 13:83-87.
55. Gow A.J., Luchsinger B.P., Pawloski J.R., Singel D.J., Stamler J.S. The oxyhemoglobin reaction of nitric oxide. Proc Natl Acad Sci U S A 1999, 96:9027-9032.
56. Nicolay J.P., Liebig G., Niemoeller O.M., Koka S., Ghashghaeinia M., Wieder T., et al. Inhibition of suicidal erythrocyte death by nitric oxide. Pflugers Arch 2008, 456:293-305.
57. Malan D., Levi R.C., Alloatti G., Marcantoni A., Bedendi I., Gallo M.P. Cyclic AMP and cyclic GMP independent stimulation of ventricular calcium current by peroxynitrite donors in guinea pig myocytes. J Cell Physiol 2003, 197:284-296.
58. + pump in isolated rabbit cardiac myocytes. J Physiol (Lond) 2005, 565:815-825.
59. Dimmeler S., Haendeler J., Nehls M., Zeiher A.M. Suppression of apoptosis by nitric oxide via inhibition of interleukin-1 beta-converting enzyme (ICE)-like and cysteine protease protein (CPP)-32-like proteases. J Exp Med 1997, 185:601-607.
60. Rossig L., Fichtlscherer B., Breitschopf K., Haendeler J., Zeiher A.M., Mulsch A., et al. Nitric oxide inhibits caspase-3 by S-nitrosation in vivo. J Biol Chem 1999, 274:6823-6826.
61. Benhar M., Stamler J.S. A central role for S-nitrosylation in apoptosis. Nat Cell Biol 2005, 7:645-646.
62. Haendeler J., Hoffmann J., Tischler V., Berk B.C., Zeiher A.M., Dimmeler S. Redox regulatory and anti-apoptotic functions of thioredoxin depend on S-nitrosylation at cysteine 69. Nat Cell Biol 2002, 4:743-749.
63. Hoffmann J., Haendeler J., Zeiher A.M., Dimmeler S. TNF alpha and oxLDL reduce protein S-nitrosylation in endothelial cells. J Biol Chem 2001, 276:41383-41387.
64. Melino G., Bernassola F., Knight R.A., Corasaniti M.T., Nistico G., FinazziAgro A. S-nitrosylation regulates apoptosis. Nature 1997, 388:432-433.
65. Castillo S.S., Levy M., Wang C.B., Thaikoottathil J.V., Khan E., Goldkorn T. Nitric oxide-enhanced caspase-3 and acidic sphingomyelinase interaction: a novel mechanism by which airway epithelial cells escape ceramide-induced apoptosis. Exp Cell Res 2007, 313:816-823.
66. Davidson S.M., Duchen M.R. Endothelial mitochondria - contributing to vascular function and disease. Circ Res 2007, 100:1128-1141.
67. Pacher P., Beckman J.S., Liaudet L. Nitric oxide and peroxynitrite in health and disease. Physiol Rev 2007, 87:315-424.
68. Dasgupta T., Fabry M.E., Kaul D.K. Antisickling property of fetal hemoglobin enhances nitric oxide bioavailability and ameliorates organ oxidative stress in transgenic-knockout sickle mice. Am J Physiol Reg Int Comp Physiol 2010, 298:R394-R402.
69. Salhany J.M. The oxidative denitrosylation mechanism and nitric oxide release from human fetal and adult hemoglobin, an experimentally based model simulation study. Blood Cells Mol Dis 2013, 50:8-19.
70. Kaul D.K., Liu X.D., Chang H.Y., Nagel R.L., Fabry M.E. Effect of fetal hemoglobin on microvascular regulation in sickle transgenic-knockout mice. J Clin Invest 2004, 114:1136-1145.
71. Hermle T., Shumilina E., Attanasio P., Akel A., Kempe D.S., Lang P.A., et al. Decreased cation channel activity and blunted channel-dependent eryptosis in neonatal erythrocytes. Am J Physiol Cell Physiol 2006, 291:C710-C717.
72. Jain S.K. Presence of phosphatidylserine in the outer membrane bilayer of newborn human erythrocytes. Biochem Biophys Res Commun 1986, 136:914-920.
73. Setty B.N., Kulkarni S., Rao A.K., Stuart M.J. Fetal hemoglobin in sickle cell disease: relationship to erythrocyte phosphatidylserine exposure and coagulation activation. Blood 2000, 96:1119-1124.
74. Bell S.G. An introduction to hemoglobin physiology. Neonatal Netw 1999, 18:9-15.
75. Ghashghaeinia M., Cluitmans J.C., Akel A., Dreischer P., Toulany M., Koberle M., et al. The impact of erythrocyte age on eryptosis. Br J Haematol 2012, 157:606-614.
76. Rice L., Alfrey C.P. The negative regulation of red cell mass by neocytolysis: physiologic and pathophysiologic manifestations. Cell Physiol Biochem 2005, 15:245-250.
77. Kempe D.S., Lang P.A., Duranton C., Akel A., Lang K.S., Huber S.M., et al. Enhanced programmed cell death of iron-deficient erythrocytes. FASEB J 2006, 20:368-370.
78. Borst O., Abed M., Alesutan I., Towhid S.T., Qadri S.M., Foller M., et al. Dynamic adhesion of eryptotic erythrocytes to endothelial cells via CXCL16/SR-PSOX. Am J Physiol Cell Physiol 2012, 302:C644-C651.
79. Betal S.G., Setty B.N.Y. Phosphatidylserine-positive erythrocytes bind to immobilized and soluble thrombospondin-1 via its heparin-binding domain. Transl Res 2008, 152:165-177.
80. Manodori A.B., Barabino G.A., Lubin B.H., Kuypers F.A. Adherence of phosphatidylserine-exposing erythrocytes to endothelial matrix thrombospondin. Blood 2000, 95:1293-1300.
81. Fadok V.A., Bratton D.L., Rose D.M., Pearson A., Ezekewitz R.A.B., Henson P.M. A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 2000, 405:85-90.
82. Walker B., Towhid S.T., Schmid E., Hoffmann S.M., Abed M., Munzer P., et al. Dynamic adhesion of eryptotic erythrocytes to immobilized platelets via platelet phosphatidylserine receptors. Am J Physiol Cell Physiol 2014, 306:C291-C297.
83. Andrews D.A., Low P.S. Role of red blood cells in thrombosis. Curr Opin Hematol 1999, 6:76-82.
84. Abed M., Herrmann T., Alzoubi K., Pakladok T., Lang F. Tannic acid induced suicidal erythrocyte death. Cell Physiol Biochem 2013, 32:1106-1116.
85. Abed M., Towhid S.T., Mia S., Pakladok T., Alesutan I., Borst O., et al. Sphingomyelinase-induced adhesion of eryptotic erythrocytes to endothelial cells. Am J Physiol Cell Physiol 2012, 303:C991-C999.
86. Ahmed M.S., Langer H., Abed M., Voelkl J., Lang F. The uremic toxin acrolein promotes suicidal erythrocyte death. Kidney Blood Press Res 2013, 37:158-167.
87. Alzoubi K., Alktifan B., Oswald G., Fezai M., Abed M., Lang F. Breakdown of phosphatidylserine asymmetry following treatment of erythrocytes with lumefantrine. Toxins (Basel) 2014, 6:650-664.
88. Arnold M., Lang E., Modicano P., Bissinger R., Faggio C., Abed M., et al. Effect of nitazoxanide on erythrocytes. Basic Clin Pharmacol Toxicol 2014, 114:421-426.
89. Bissinger R., Malik A., Jilani K., Lang F. Triggering of erythrocyte cell membrane scrambling by salinomycin. Basic Clin Pharmacol Toxicol 2014.
90. Bottger E., Multhoff G., Kun J.F., Esen M. Plasmodium falciparum-infected erythrocytes induce granzyme B by NK cells through expression of host-Hsp70. PLoS ONE 2012, 7:e33774.
91. Firat U., Kaya S., Cim A., Buyukbayram H., Gokalp O., Dal M.S., et al. Increased caspase-3 immunoreactivity of erythrocytes in STZ diabetic rats. Exp Diabetes Res 2012, 2012:316384.
92. Frauenfeld L., Alzoubi K., Abed M., Lang F. Stimulation of erythrocyte cell membrane scrambling by mushroom tyrosinase. Toxins (Basel) 2014, 6:1096-1108.
93. Ganesan S., Chaurasiya N.D., Sahu R., Walker L.A., Tekwani B.L. Understanding the mechanisms for metabolism-linked hemolytic toxicity of primaquine against glucose 6-phosphate dehydrogenase deficient human erythrocytes: evaluation of eryptotic pathway. Toxicology 2012, 294:54-60.
94. Gao M., Cheung K.L., Lau I.P., Yu W.S., Fung K.P., Yu B., et al. Polyphyllin D induces apoptosis in human erythrocytes through Ca(2)(+) rise and membrane permeabilization. Arch Toxicol 2012, 86:741-752.
95. Gao M., Lau P.M., Kong S.K. Mitochondrial toxin betulinic acid induces in vitro eryptosis in human red blood cells through membrane permeabilization. Arch Toxicol 2014, 88:755-768.
96. Ghashghaeinia M., Cluitmans J.C., Toulany M., Saki M., Koberle M., Lang E., et al. Age sensitivity of NFkappaB abundance and programmed cell death in erythrocytes induced by NFkappaB inhibitors. Cell Physiol Biochem 2013, 32:801-813.
97. Jacobi J., Lang E., Bissinger R., Frauenfeld L., Modicano P., Faggio C., et al. Stimulation of erythrocyte cell membrane scrambling by mitotane. Cell Physiol Biochem 2014, 33:1516-1526.
98. Jilani K., Lupescu A., Zbidah M., Abed M., Shaik N., Lang F. Enhanced apoptotic death of erythrocytes induced by the mycotoxin ochratoxin A. Kidney Blood Press Res 2012, 36:107-118.
99. Jilani K., Lupescu A., Zbidah M., Shaik N., Lang F. Withaferin A-stimulated Ca(2+) entry, ceramide formation and suicidal death of erythrocytes. Toxicol In Vitro 2013, 27:52-58.
100. Kucherenko Y.V., Lang F. Inhibitory effect of furosemide on non-selective voltage-independent cation channels in human erythrocytes. Cell Physiol Biochem 2012, 30:863-875.
101. Lang E., Qadri S.M., Jilani K., Zelenak C., Lupescu A., Schleicher E., et al. Carbon monoxide-sensitive apoptotic death of erythrocytes. Basic Clin Pharmacol Toxicol 2012, 111:348-355.
102. Lupescu A., Bissinger R., Herrmann T., Oswald G., Jilani K., Lang F. Induction of suicidal erythrocyte death by novobiocin. Cell Physiol Biochem 2014, 33:670-680.
103. Lupescu A., Bissinger R., Jilani K., Lang F. In vitro induction of erythrocyte phosphatidylserine translocation by the natural naphthoquinone shikonin. Toxins (Basel) 2014, 6:1559-1574.
104. Lupescu A., Jilani K., Zbidah M., Lang F. Patulin-induced suicidal erythrocyte death. Cell Physiol Biochem 2013, 32:291-299.
105. Malik A., Bissinger R., Jilani K., Lang F. Stimulation of erythrocyte cell membrane scrambling by nystatin. Basic Clin Pharmacol Toxicol 2015, 116:47-52.
106. Oswald G., Alzoubi K., Abed M., Lang F. Stimulation of suicidal erythrocyte death by ribavirin. Basic Clin Pharmacol Toxicol 2014, 114:311-317.
107. Polak-Jonkisz D., Purzyc L. Ca influx versus efflux during eryptosis in uremic erythrocytes. Blood Purif 2012, 34:209-210.
108. Qian E.W., Ge D.T., Kong S.K. Salidroside protects human erythrocytes against hydrogen peroxide-induced apoptosis. J Nat Prod 2012, 75:531-537.
109. Shaik N., Zbidah M., Lang F. Inhibition of Ca(2+) entry and suicidal erythrocyte death by naringin. Cell Physiol Biochem 2012, 30:678-686.
110. Voelkl J., Alzoubi K., Mamar A.K., Ahmed M.S., Abed M., Lang F. Stimulation of suicidal erythrocyte death by increased extracellular phosphate concentrations. Kidney Blood Press Res 2013, 38:42-51.
111. Vota D.M., Maltaneri R.E., Wenker S.D., Nesse A.B., Vittori D.C. Differential erythropoietin action upon cells induced to eryptosis by different agents. Cell Biochem Biophys 2013, 65:145-157.
112. Weiss E., Cytlak U.M., Rees D.C., Osei A., Gibson J.S. Deoxygenation-induced and Ca(2+) dependent phosphatidylserine externalisation in red blood cells from normal individuals and sickle cell patients. Cell Calcium 2012, 51:51-56.
113. Zbidah M., Lupescu A., Jilani K., Lang F. Stimulation of suicidal erythrocyte death by fumagillin. Basic Clin Pharmacol Toxicol 2013, 112:346-351.
114. Zelenak C., Pasham V., Jilani K., Tripodi P.M., Rosaclerio L., Pathare G., et al. Tanshinone IIA stimulates erythrocyte phosphatidylserine exposure. Cell Physiol Biochem 2012, 30:282-294.
115. Lupescu A., Bissinger R., Warsi J., Jilani K., Lang F. Stimulation of erythrocyte cell membrane scrambling by gedunin. Cell Physiol Biochem 2014, 33:1838-1848.
116. Bissinger R., Modicano P., Alzoubi K., Honisch S., Faggio C., Abed M., et al. Effect of saponin on erythrocytes. Int J Hematol 2014, 100:51-59.
117. 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, 37:567-578.
118. Alzoubi K., Calabro S., Bissinger R., Abed M., Faggio C., Lang F. Stimulation of suicidal erythrocyte death by artesunate. Cell Physiol Biochem 2014, 34:2232-2244.
119. Arnold M., Bissinger R., Lang F. Mitoxantrone-induced suicidal erythrocyte death. Cell Physiol Biochem 2014, 34:1756-1767.
120. Bissinger R., Fischer S., Jilani K., Lang F. Stimulation of erythrocyte death by phloretin. Cell Physiol Biochem 2014, 34:2256-2265.
121. Bissinger R., Lupescu A., Zelenak C., Jilani K., Lang F. Stimulation of eryptosis by cryptotanshinone. Cell Physiol Biochem 2014, 34:432-442.
122. Bissinger R., Modicano P., Frauenfeld L., Lang E., Jacobi J., Faggio C., et al. Estramustine-induced suicidal erythrocyte death. Cell Physiol Biochem 2013, 32:1426-1436.
123. Jilani K., Qadri S.M., Lang F. Geldanamycin-induced phosphatidylserine translocation in the erythrocyte membrane. Cell Physiol Biochem 2013, 32:1600-1609.
124. Malik A., Bissinger R., Calabro S., Faggio C., Jilani K., Lang F. Aristolochic acid induced suicidal erythrocyte death. Kidney Blood Press Res 2014, 39:408-419.
125. Tesoriere L., Attanzio A., Allegra M., Cilla A., Gentile C., Livrea M.A. Oxysterol mixture in hypercholesterolemia-relevant proportion causes oxidative stress-dependent eryptosis. Cell Physiol Biochem 2014, 34:1075-1089.
126. Zhang R., Xiang Y., Ran Q., Deng X., Xiao Y., Xiang L., et al. Involvement of calcium, reactive oxygen species, and ATP in hexavalent chromium-induced damage in red blood cells. Cell Physiol Biochem 2014, 34:1780-1791.
127. Banerjee S., Zhao Y., Sarkar P.S., Rosenblatt K.P., Tilton R.G., Choudhary S. Klotho ameliorates chemically induced endoplasmic reticulum (ER) stress signaling. Cell Physiol Biochem 2013, 31:659-672.
128. Kuro-o M. Klotho, phosphate and FGF-23 in ageing and disturbed mineral metabolism. Nat Rev Nephrol 2013, 9:650-660.
129. Abed M., Towhid S.T., Feger M., Schmidt S., Kuro O.M., Gawaz M., et al. Adhesion of klotho-deficient eryptotic erythrocytes to endothelial cells. Acta Physiol (Oxf) 2013, 207:485-493.
130. Kempe D.S., Ackermann T.F., Fischer S.S., Koka S., Boini K.M., Mahmud H., et al. Accelerated suicidal erythrocyte death in Klotho-deficient mice. Pflugers Arch 2009, 458:503-512.
131. Birka C., Lang P.A., Kempe D.S., Hoefling L., Tanneur V., Duranton C., et al. Enhanced susceptibility to erythrocyte apoptosis following phosphate depletion. Pflugers Arch 2004, 448:471-477.
132. Nagababu E., Gulyani S., Earley C.J., Cutler R.G., Mattson M.P., Rifkind J.M. Iron-deficiency anaemia enhances red blood cell oxidative stress. Free Radic Res 2008, 42:824-829.
133. Qadri S.M., Mahmud H., Lang E., Gu S., Bobbala D., Zelenak C., et al. Enhanced suicidal erythrocyte death in mice carrying a loss-of-function mutation of the adenomatous polyposis coli gene. J Cell Mol Med 2012, 16:1085-1093.
134. 2 increases. J Cardiometab Syndr 2008, 3:30-34.
135. Calderon-Salinas J.V., Munoz-Reyes E.G., Guerrero-Romero J.F., Rodriguez-Moran M., Bracho-Riquelme R.L., Carrera-Gracia M.A., et al. Eryptosis and oxidative damage in type 2 diabetic mellitus patients with chronic kidney disease. Mol Cell Biochem 2011, 357:171-179.
136. Nicolay J.P., Schneider J., Niemoeller O.M., Artunc F., Portero-Otin M., Haik G., et al. Stimulation of suicidal erythrocyte death by methylglyoxal. Cell Physiol Biochem 2006, 18:223-232.
137. Thornalley P.J. Modification of the glyoxalase system in human red blood cells by glucose in vitro. Biochem J 1988, 254:751-755.
138. Nwose E.U., Jelinek H.F., Richards R.S., Kerr P.G. Erythrocyte oxidative stress in clinical management of diabetes and its cardiovascular complications. Br J Biomed Sci 2007, 64:35-43.
139. Bandeira S.D., Guedes G.D., da Fonseca L.J.S., Pires A.S., Gelain D.P., Moreira J.C.F., et al. Characterization of blood oxidative stress in Type 2 diabetes mellitus patients: increase in lipid peroxidation and SOD activity. Oxid Med Cell Longev 2012, 2012:819310.
140. Dmitrieva O., de Lusignan S., Macdougall I.C., Gallagher H., Tomson C., Harris K., et al. Association of anaemia in primary care patients with chronic kidney disease: cross sectional study of quality improvement in chronic kidney disease (QICKD) trial data. BMC Nephrol 2013, 14.
141. Yang M., Fox C.H., Vassalotti J., Choi M. Complications of progression of CKD. Adv Chronic Kidney Dis 2011, 18:400-405.
142. Adamson J.W. Hyporesponsiveness to erythropoiesis stimulating agents in chronic kidney disease: the many faces of inflammation. Adv Chronic Kidney Dis 2009, 16:76-82.
143. Atkinson M.A., Furth S.L. Anemia in children with chronic kidney disease. Nat Rev Nephrol 2011, 7:635-641.
144. Besarab A., Coyne D.W. Iron supplementation to treat anemia in patients with chronic kidney disease. Nat Rev Nephrol 2010, 6:699-710.
145. Kwack C., Balakrishnan V.S. Managing erythropoietin hyporesponsiveness. Semin Dial 2006, 19:146-151.
146. Abed M., Artunc F., Alzoubi K., Honisch S., Baumann D., Foller M. Suicidal erythrocyte death in end-stage renal disease. J Mol Med (Berl) 2014.
147. Vos F.E., Schollum J.B., Coulter C.V., Doyle T.C.A., Duffull S.B., Walker R.J. Red blood cell survival in long-term dialysis patients. Am J Kidney Dis 2011, 58:591-598.
148. Antonelou M.H., Kriebardis A.G., Velentzas A.D., Kokkalis A.C., Georgakopoulou S.C., Papassideri I.S. Oxidative stress-associated shape transformation and membrane proteome remodeling in erythrocytes of end stage renal disease patients on hemodialysis. J Proteom 2011, 74:2441-2452.
149. Foller M., Sopjani M., Mahmud H., Lang F. Vanadate-induced suicidal erythrocyte death. Kidney Blood Press Res 2008, 31:87-93.
150. Ahmed M.S., Abed M., Voelkl J., Lang F. Triggering of suicidal erythrocyte death by uremic toxin indoxyl sulfate. BMC Nephrol 2013, 14:244.
151. Zhu Q., Sun Z., Jiang Y., Chen F., Wang M.F. Acrolein scavengers: reactivity, mechanism and impact on health. Mol Nutr Food Res 2011, 55:1375-1390.
152. Lang P.A., Beringer O., Nicolay J.P., Amon O., Kempe D.S., Hermle T., et al. Suicidal death of erythrocytes in recurrent hemolytic uremic syndrome. J Mol Med 2006, 84:378-388.
153. Gomez S.A., Abrey-Recalde M.J., Panek C.A., Ferrarotti N.F., Repetto M.G., Mejias M.P., et al. The oxidative stress induced in vivo by Shiga toxin-2 contributes to the pathogenicity of haemolytic uraemic syndrome. Clin Exp Immunol 2013, 173:463-472.
154. Facorro G., Aguirre F., Florentin L., Diaz M., De Paoli T., Ihlo J.E., et al. Oxidative stress and membrane fluidity in erythrocytes from patients with hemolytic uremic syndrome. Acta Physiol Pharmacol Ther Latinoam 1997, 47:137-146.
155. Kempe D.S., Akel A., Lang P.A., Hermle T., Biswas R., Muresanu J., et al. Suicidal erythrocyte death in sepsis. J Mol Med 2007, 85:269-277.
156. Lang E., Gatidis S., Freise N.F., Bock H., Kubitz R., Lauermann C., et al. Conjugated bilirubin triggers anemia by inducing erythrocyte death. Hepatology 2014, 61:275-284.
157. Lang P.A., Schenck M., Nicolay J.P., Becker J.U., Kempe D.S., Lupescu A., et al. Liver cell death and anemia in Wilson disease involve acid sphingomyelinase and ceramide. Nat Med 2007, 13:164-170.
158. Gitlin J.D. Wilson disease. Gastroenterology 2003, 125:1868-1877.
159. Attri S., Sharma N., Jahagirdar S., Thapa B.R.T., Prasad R. Erythrocyte metabolism and antioxidant status of patients with Wilson disease with hemolytic anemia. Pediatr Res 2006, 59:593-597.
160. Nagasaka H., Inoue I., Inui A., Komatsu H., Sogo T., Murayama K., et al. Relationship between oxidative stress and antioxidant systems in the liver of patients with Wilson disease: hepatic manifestation in Wilson disease as a consequence of augmented oxidative stress. Pediatr Res 2006, 60:472-477.
161. Bruce L.J., Robinson H.C., Guizouarn H., Borgese F., Harrison P., King M.J., et al. Monovalent cation leaks in human red cells caused by single amino-acid substitutions in the transport domain of the band 3 chloride-bicarbonate exchanger, AE1. Nat Genet 2005, 37:1258-1263.
162. Akel A., Wagner C.A., Kovacikova J., Kasinathan R.S., Kiedaisch V., Koka S., et al. Enhanced suicidal death of erythrocytes from gene-targeted mice lacking the Cl-/HCO(3)(-) exchanger AE1. Am J Physiol Cell Physiol 2007, 292:C1759-C1767.
163. Weber Y.G., Storch A., Wuttke T.V., Brockmann K., Kempfle J., Maljevic S., et al. GLUT1 mutations are a cause of paroxysmal exertion-induced dyskinesias and induce hemolytic anemia by a cation leak. J Clin Invest 2008, 118:2157-2168.
164. Lang P.A., Kasinathan R.S., Brand V.B., Duranton C., Lang C., Koka S., et al. Accelerated clearance of Plasmodium-infected erythrocytes in sickle cell trait and annexin-A7 deficiency. Cell Physiol Biochem 2009, 24:415-428.
165. Lang K.S., Roll B., Myssina S., Schittenhelm M., Scheel-Walter H.G., Kanz L., et al. Enhanced erythrocyte apoptosis in sickle cell anemia, thalassemia and glucose-6-phosphate dehydrogenase deficiency. Cell Physiol Biochem 2002, 12:365-372.
166. Basu S., Banerjee D., Chandra S., Chakrabarti A. Loss of phospholipid membrane asymmetry and sialylated glycoconjugates from erythrocyte surface in haemoglobin E beta-thalassaemia. Br J Haematol 2008, 141:92-99.
167. Ibrahim H.A., Fouda M.I., Yahya R.S., Abousamra N.K., Abd Elazim R.A. Erythrocyte phosphatidylserine exposure in beta-thalassemia. Int J Lab Hematol 2014, 20:9-14.
168. Haynes J., Obiako B., King J.A., Hester R.B., Ofori-Acquah S. Activated neutrophil-mediated sickle red blood cell adhesion to lung vascular endothelium: role of phosphatidylserine-exposed sickle red blood cells. Am J Physiol Heart Circ Physiol 2006, 291:H1679-H1685.
169. Kaul D.K., Tsai H.M., Liu X.D., Nakada M.T., Nagel R.L., Coller B.S. Monoclonal antibodies to alpha V beta 3 (7E3 and LM609) inhibit sickle red blood cell-endothelium interactions induced by platelet-activating factor. Blood 2000, 95:368-374.
170. Kumar A., Eckman J.R., Wick T.M. Inhibition of plasma-mediated adherence of sickle erythrocytes to microvascular endothelium by conformationally constrained RGD-containing peptides. Am J Hematol 1996, 53:92-98.
171. Setty B.N.Y., Kulkarni S., Stuart M.J. Role of erythrocyte phosphatidylserine in sickle red cell-endothelial adhesion. Blood 2002, 99:1564-1571.
172. Haynes J., Obiako B., Hester R.B., Baliga B.S., Stevens T. Hydroxyurea attenuates activated neutrophil-mediated sickle erythrocyte membrane phosphatidylserine exposure and adhesion to pulmonary vascular endothelium. Am J Physiol Heart Circ Physiol 2008, 294:H379-H385.
173. Hillery C.A., Du M.C., Wang W.C., Scott J.P. Hydroxyurea therapy decreases the in vitro adhesion of sickle erythrocytes to thrombospondin and laminin. Br J Haematol 2000, 109:322-327.
174. Yasin Z., Witting S., Palascak M.B., Joiner C.H., Rucknagel D.L., Franco R.S. Phosphatidylserine externalization in sickle red blood cells: associations with cell age, density, and hemoglobin F. Blood 2003, 102:365-370.
175. Charache S., Terrin M.L., Moore R.D., Dover G.J., Barton F.B., Eckert S.V., et al. Effect of hydroxyurea on the frequency of painful crises in sickle-cell-anemia. N Engl J Med 1995, 332:1317-1322.
176. Totino P.R., Daniel-Ribeiro C.T., Ferreira-da-Cruz Mde F. Refractoriness of eryptotic red blood cells to Plasmodium falciparum infection: a putative host defense mechanism limiting parasitaemia. PLoS ONE 2011, 6:e26575.
177. Koka S., Lang C., Niemoeller O.M., Boini K.M., Nicolay J.P., Huber S.M., et al. Influence of NO synthase inhibitor L-NAME on parasitemia and survival of Plasmodium berghei infected mice. Cell Physiol Biochem 2008, 21:481-488.
178. Kirk K. Membrane transport in the malaria-infected erythrocyte. Physiol Rev 2001, 81:495-537.
179. Lang F., Lang P.A., Lang K.S., Brand V., Tanneur V., Duranton C., et al. Channel-induced apoptosis of infected host cells-the case of malaria. Pflugers Arch 2004, 448:319-324.
180. Huber S.M., Duranton C., Lang F. Patch-clamp analysis of the new permeability pathways in malaria-infected erythrocytes. Int Rev Cytol 2005, 246:59-134.
181. Lew V.L., Tiffert T., Ginsburg H. Excess hemoglobin digestion and the osmotic stability of Plasmodium falciparum-infected red blood cells. Blood 2003, 101:4189-4194.
182. Joshi P., Gupta C.M. Abnormal membrane phospholipid organization in Plasmodium falciparum-infected human erythrocytes. Br J Haematol 1988, 68:255-259.
183. Schwartz R.S., Olson J.A., Raventos-Suarez C., Yee M., Heath R.H., Lubin B., et al. Altered plasma membrane phospholipid organization in Plasmodium falciparum-infected human erythrocytes. Blood 1987, 69:401-407.
184. Ayi K., Giribaldi G., Skorokhod A., Schwarzer E., Prendergast P.T., Arese P. 16alpha-bromoepiandrosterone, an antimalarial analogue of the hormone dehydroepiandrosterone, enhances phagocytosis of ring stage parasitized erythrocytes: a novel mechanism for antimalarial activity. Antimicrob Agents Chemother 2002, 46:3180-3184.
185. Turrini F., Ginsburg H., Bussolino F., Pescarmona G.P., Serra M.V., Arese P. Phagocytosis of Plasmodium falciparum-infected human red blood cells by human monocytes: involvement of immune and nonimmune determinants and dependence on parasite developmental stage. Blood 1992, 80:801-808.
186. Sherman I.W., Eda S., Winograd E. Erythrocyte aging and malaria. Cell Mol Biol (Noisy-le-grand) 2004, 50:159-169.
187. Sherman I.W., Eda S., Winograd E. Cytoadherence and sequestration in Plasmodium falciparum: defining the ties that bind. Microbes Infect 2003, 5:897-909.
188. Ayi K., Turrini F., Piga A., Arese P. Enhanced phagocytosis of ring-parasitized mutant erythrocytes: a common mechanism that may explain protection against falciparum malaria in sickle trait and beta-thalassemia trait. Blood 2004, 104:3364-3371.
189. de Jong K., Emerson R.K., Butler J., Bastacky J., Mohandas N., Kuypers F.A. Short survival of phosphatidylserine-exposing red blood cells in murine sickle cell anemia. Blood 2001, 98:1577-1584.