Sphingosine but not sphingosine-1-phosphate stimulates suicidal erythrocyte death

Cellular Physiology and Biochemistry

Volumn 28, Issue 2, 2011, Pages 339-346

  Qadri, Syed M ^a   Bauer, Julia ^a   Zelenak, Christine ^a   Mahmud, Hasan ^a   Kucherenko, Yuliya ^a   Lee, Seung Hun ^b   Ferlinz, Klaus ^a,c   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b Yonsei University College of Medicine   (South Korea)

^c Oracle Deutschland GmbH   (Germany)

Author keywords

Annexin; Calcium; Cell volume; Eryptosis; Oxidative stress; Phosphatidylserine; Sphingosine; Sphingosine phosphate

Indexed keywords

CALCIUM ION; FLUO 3; LIPOCORTIN 5; PHOSPHATIDYLSERINE; SPHINGOSINE; SPHINGOSINE 1 PHOSPHATE;

ARTICLE; CALCIUM CELL LEVEL; CALCIUM SIGNALING; CELL DEATH; ERYPTOSIS; ERYTHROCYTE; ERYTHROCYTE VOLUME; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN BINDING;

EID: 80052077564     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000331750     Document Type: Article

References (113)

1. Hanel P, Andreani P, Graler MH: Erythrocytes store and release sphingosine 1-phosphate in blood. FASEB J 2007;21:1202-1209. (Pubitemid 46495709)
2. Karliner JS: Mechanisms of cardioprotection by lysophospholipids. J Cell Biochem 2004;92:1095-1103. (Pubitemid 44264221)
3. Ren S, Xin C, Pfeilschifter J, Huwiler A: A novel mode of action of the putative sphingosine kinase inhibitor 2-(phydroxyanilino)-4-(p-chlorophenyl) thiazole (SKI II): induction of lysosomal sphingosine kinase 1 degradation. Cell Physiol Biochem 2010;26:97-104.
4. Takabe K, Paugh SW, Milstien S, Spiegel S: "Inside-out" signaling of sphingosine-1-phosphate: therapeutic targets. Pharmacol Rev 2008;60:181-195. (Pubitemid 351962008)
5. Ito K, Anada Y, Tani M, Ikeda M, Sano T, Kihara A, Igarashi Y: Lack of sphingosine 1-phosphate-degrading enzymes in erythrocytes. Biochem Biophys Res Commun 2007;357:212-217. (Pubitemid 46574517)
6. Yang L, Yatomi Y, Miura Y, Satoh K, Ozaki Y: Metabolism and functional effects of sphingolipids in blood cells. Br J Haematol 1999;107:282-293. (Pubitemid 29530212)
7. Allende ML, Sasaki T, Kawai H, Olivera A, Mi Y, Echten-Deckert G, Hajdu R, Rosenbach M, Keohane CA, Mandala S, Spiegel S, Proia RL: Mice deficient in sphingosine kinase 1 are rendered lymphopenic by FTY720. J Biol Chem 2004;279:52487-52492. (Pubitemid 39656625)
8. Graler MH: Targeting sphingosine 1-phosphate (S1P) levels and S1P receptor functions for therapeutic immune interventions. Cell Physiol Biochem 2010;26:79-86.
9. Lucke S, Levkau B: Endothelial functions of sphingosine-1-phosphate. Cell Physiol Biochem 2010;26:87-96.
10. McVerry BJ, Garcia JG: In vitro and in vivo modulation of vascular barrier integrity by sphingosine 1-phosphate: mechanistic insights. Cell Signal 2005;17:131-139. (Pubitemid 39371042)
11. Potteck H, Nieuwenhuis B, Luth A, van der GM, Kleuser B: Phosphorylation of the immunomodulator FTY720 inhibits programmed cell death of fibroblasts via the S1P3 receptor subtype and Bcl-2 activation. Cell Physiol Biochem 2010;26:67-78.
12. Rosen H, Goetzl EJ: Sphingosine 1-phosphate and its receptors: an autocrine and paracrine network. Nat Rev Immunol 2005;5:560-570. (Pubitemid 40961333)
13. Gulbins E: Regulation of death receptor signaling and apoptosis by ceramide. Pharmacol Res 2003;47:393-399. (Pubitemid 36379201)
14. 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. (Pubitemid 38656358)
15. Nicolay JP, Gatz S, Liebig G, Gulbins E, Lang F: Amyloid induced suicidal erythrocyte death. Cell Physiol Biochem 2007;19:175-184.
16. Nicolay JP, Bentzen PJ, Ghashghaeinia M, Wieder T, Lang F: Stimulation of erythrocyte cell membrane scrambling by amiodarone. Cell Physiol Biochem 2007;20:1043-1050. (Pubitemid 350059710)
17. Kornhuber J, Tripal P, Reichel M, Muhle C, Rhein C, Muehlbacher M, Groemer TW, Gulbins E: Functional Inhibitors of Acid Sphingomyelinase (FIASMAs): a novel pharmacological group of drugs with broad clinical applications. Cell Physiol Biochem 2010;26:9-20.
18. Walter S, Fassbender K: Spingolipids in Multiple Sclerosis. Cell Physiol Biochem 2010;26:49-56.
19. Contreras FX, Sot J, Alonso A, Goni FM: Sphingosine increases the permeability of model and cell membranes. Biophys J 2006;90:4085-4092. (Pubitemid 43846123)
20. Lang F, Gulbins E, Lerche H, Huber SM, Kempe DS, Foller M: Eryptosis, a window to systemic disease. Cell Physiol Biochem 2008;22:373-380.
21. Lang PA, Kaiser S, Myssina S, Wieder T, Lang F, Huber SM: Role of Ca2+-activated K+ channels in human erythrocyte apoptosis. Am J Physiol Cell Physiol 2003;285:C1553-C1560. (Pubitemid 37429630)
22. Daugas E, Cande C, Kroemer G: Erythrocytes: death of a mummy. Cell Death Differ 2001;8:1131-1133. (Pubitemid 34048467)
23. 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. (Pubitemid 34048470)
24. 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. (Pubitemid 34048474)
25. Duranton C, Huber SM, Lang F: Oxidation induces a Cl-dependent cation conductance in human red blood cells. J Physiol 2002;539:847-855. (Pubitemid 35175434)
26. Bookchin RM, Ortiz OE, Lew VL: Activation of calcium-dependent potassium channels in deoxygenated sickled red cells. Prog Clin Biol Res 1987;240:193-200.
27. Brugnara C, de Franceschi L, Alper SL: Inhibition of Ca2+-dependent K+ transport and cell dehydration in sickle erythrocytes by clotrimazole and other imidazole derivatives. J Clin Invest 1993;92:520-526. (Pubitemid 23209038)
28. Schneider J, Nicolay JP, Foller M, Wieder T, Lang F: Suicidal erythrocyte death following cellular K+ loss. Cell Physiol Biochem 2007;20:35-44. (Pubitemid 46956810)
29. Mandal D, Mazumder A, Das P, Kundu M, Basu J: Fas-, caspase 8-, and caspase 3-dependent signaling regulates the activity of the aminophospholipid translocase and phosphatidylserine externalization in human erythrocytes. J Biol Chem 2005;280:39460-39467. (Pubitemid 41713903)
30. Lang KS, Myssina S, Brand V, Sandu C, Lang PA, Berchtold S, Huber SM, Lang F, Wieder T: Involvement of ceramide in hyperosmotic shock-induced death of erythrocytes. Cell Death Differ 2004;11:231-243. (Pubitemid 38159647)
31. Basu S, Banerjee D, Chandra S, Chakrabarti A: Eryptosis in hereditary spherocytosis and thalassemia: role of glycoconjugates. Glycoconj J 2010;27:717-722.
32. Basu S, Banerjee D, Ghosh M, Chakrabarti A: Erythrocyte membrane defects and asymmetry in paroxysmal nocturnal hemoglobinuria and myelodysplastic syndrome. Hematology 2010;15:236-239.
33. Bhavsar SK, Eberhard M, Bobbala D, Lang F: Monensin induced suicidal erythrocyte death. Cell Physiol Biochem 2010;25:745-752.
34. Bobbala D, Alesutan I, Foller M, Huber SM, Lang F: Effect of anandamide in Plasmodium Berghei-infected mice. Cell Physiol Biochem 2010;26:355-362.
35. Chadebech P, Michel M, Janvier D, Yamada K, Copie-Bergman C, Bodivit G, Bensussan A, Fournie JJ, Godeau B, Bierling P, Izui S, Noizat-Pirenne F: IgAmediated human autoimmune hemolytic anemia as a result of hemagglutination in the spleen, but independently of complement activation and Fc{alpha}RI. Blood 2010;116:4141-4147.
36. + leak of human erythrocytes. Cell Physiol Biochem 2008;21:183-192.
37. Foller M, Bobbala D, Koka S, Huber SM, 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.
38. Foller M, Braun M, Qadri SM, Lang E, Mahmud H, Lang F: Temperature sensitivity of suicidal erythrocyte death. Eur J Clin Invest 2010;40:534-540.
39. Ghashghaeinia M, Bobbala D, Wieder T, Koka S, Bruck J, Fehrenbacher B, Rocken M, Schaller M, Lang F, Ghoreschi K: Targeting glutathione by dimethylfumarate protects against experimental malaria by enhancing erythrocyte cell membrane scrambling. Am J Physiol Cell Physiol 2010;299:C791-C804.
40. Koka S, Bobbala D, Lang C, Boini KM, Huber SM, Lang F: Influence of paclitaxel on parasitemia and survival of Plasmodium berghei infected mice. Cell Physiol Biochem 2009;23:191-198.
41. Kucherenko YV, Bhavsar SK, Grischenko VI, Fischer UR, Huber SM, Lang F: Increased cation conductance in human erythrocytes artificially aged by glycation. J Membr Biol 2010;235:177-189.
42. Lang F, Gulbins E, Lang PA, Zappulla D, Foller M: Ceramide in suicidal death of erythrocytes. Cell Physiol Biochem 2010;26:21-28.
43. Mahmud H, Mauro D, Foller M, Lang F: Inhibitory effect of thymol on suicidal erythrocyte death. Cell Physiol Biochem 2009;24:407-414.
44. Mahmud H, Mauro D, Qadri SM, Foller M, Lang F: Triggering of suicidal erythrocyte death by amphotericin B. Cell Physiol Biochem 2009;24:263-270.
45. Siraskar B, Ballal A, Bobbala D, Foller M, Lang F: Effect of amphotericin B on parasitemia and survival of plasmodium berghei-infected mice. Cell Physiol Biochem 2010;26:347-354.
46. Wang K, Mahmud H, Föller M, Biswas R, Lang KS, Bohn E, Goetz F, Lang F: Lipopeptides in the Triggering of Erythrocyte Cell Membrane Scrambling. Cell Physiol Biochem 2008;22:381-386.
47. Foller M, Shumilina E, Lam R, Mohamed W, Kasinathan R, Huber S, Chakraborty T, Lang F: Induction of suicidal erythrocyte death by listeriolysin from Listeria monocytogenes. Cell Physiol Biochem 2007;20:1051-1060. (Pubitemid 350059711)
48. Bartke N, Hannun YA: Bioactive sphingolipids: metabolism and function. J Lipid Res 2009;50:S91-S96.
49. Billich A, Baumruker T: Sphingolipid metabolizing enzymes as novel therapeutic targets. Subcell Biochem 2008;49:487-522.
50. Claus RA, Dorer MJ, Bunck AC, Deigner HP: Inhibition of sphingomyelin hydrolysis: targeting the lipid mediator ceramide as a key regulator of cellular fate. Curr Med Chem 2009;16:1978-2000.
51. Cuvillier O: Downregulating sphingosine kinase-1 for cancer therapy. Expert Opin Ther Targets 2008;12:1009-1020.
52. Duan RD, Nilsson A: Metabolism of sphingolipids in the gut and its relation to inflammation and cancer development. Prog Lipid Res 2009;48:62-72.
53. Ekiz HA, Baran Y: Therapeutic applications of bioactive sphingolipids in hematological malignancies. Int J Cancer 2010;127:1497-1506.
54. Ekiz HA, Baran Y: Bioactive Sphingolipids in Response to Chemotherapy: a Scope on Leukemias. Anticancer Agents Med Chem 2011;11:385-397.
55. Farooqui AA, Ong WY, Farooqui T: Lipid mediators in the nucleus: Their potential contribution to Alzheimer's disease. Biochim Biophys Acta 2010;1801:906-916.
56. Gangoiti P, Camacho L, Arana L, Ouro A, Granado MH, Brizuela L, Casas J, Fabrias G, Abad JL, Delgado A, Gomez-Munoz A: Control of metabolism and signaling of simple bioactive sphingolipids: Implications in disease. Prog Lipid Res 2010;49:316-334.
57. Gulbins E, Kolesnick R: Raft ceramide in molecular medicine. Oncogene 2003;22:7070-7077. (Pubitemid 37386676)
58. Gulbins E, Li PL: Physiological and pathophysiological aspects of ceramide. Am J Physiol Regul Integr Comp Physiol 2006;290:R11-R26.
59. Jana A, Pahan K: Sphingolipids in multiple sclerosis. Neuromolecular Med 2010;12:351-361.
60. Kolesnick RN, Goni FM, Alonso A: Compartmentalization of ceramide signaling: physical foundations and biological effects. J Cell Physiol 2000;184:285-300. (Pubitemid 30625491)
61. Lai WQ, Wong WS, Leung BP: Sphingosine kinase and sphingosine 1-phosphate in asthma. Biosci Rep 2011;31:145-150.
62. Leong WI, Saba JD: S1P metabolism in cancer and other pathological conditions. Biochimie 2010;92:716-723.
63. Perrotta C, De Palma C, Clementi E: Nitric oxide and sphingolipids: mechanisms of interaction and role in cellular pathophysiology. Biol Chem 2008;389:1391-1397.
64. Ponnusamy S, Meyers-Needham M, Senkal CE, Saddoughi SA, Sentelle D, Selvam SP, Salas A, Ogretmen B: Sphingolipids and cancer: ceramide and sphingosine-1-phosphate in the regulation of cell death and drug resistance. Future Oncol 2010;6:1603-1624.
65. Stancevic B, Kolesnick R: Ceramide-rich platforms in transmembrane signaling. FEBS Lett 2010;584:1728-1740.
66. Weigert A, Weis N, Brune B: Regulation of macrophage function by sphingosine-1-phosphate. Immunobiology 2009;214:748-760.
67. Arboleda G, Huang TJ, Waters C, Verkhratsky A, Fernyhough P, Gibson RM: Insulin-like growth factor-1-dependent maintenance of neuronal metabolism through the phosphatidylinositol 3-kinase-Akt pathway is inhibited by C2-ceramide in CAD cells. Eur J Neurosci 2007;25:3030-3038. (Pubitemid 46888810)
68. Arboleda G, Cardenas Y, Rodriguez Y, Morales LC, Matheus L, Arboleda H: Differential regulation of AKT, MAPK and GSK3beta during C2-ceramide-induced neuronal death. Neurotoxicology 2010;31:687-693.
69. Costantini C, Scrable H, Puglielli L: An aging pathway controls the TrkA to p75NTR receptor switch and amyloid beta-peptide generation. EMBO J 2006;25:1997-2006.
70. Gulbins E, Szabo I, Baltzer K, Lang F: Ceramide-induced inhibition of T lymphocyte voltage-gated potassium channel is mediated by tyrosine kinases. Proc Natl Acad Sci USA 1997;94:7661-7666. (Pubitemid 27345373)
71. Lang PA, Schenck M, Nicolay JP, Becker JU, Kempe DS, Lupescu A, Koka S, Eisele K, Klarl BA, Rubben H, Schmid KW, Mann K, Hildenbrand S, Hefter H, Huber SM, Wieder T, Erhardt A, Haussinger D, Gulbins E, Lang F: Liver cell death and anemia in Wilson disease involve acid sphingomyelinase and ceramide. Nat Med 2007;13:164-170.
72. Teichgraber V, Ulrich M, Endlich N, Riethmuller J, Wilker B, Oliveira-Munding CC, van Heeckeren AM, Barr ML, von Kurthy G, Schmid KW, Weller M, Tummler B, Lang F, Grassme H, Doring G, Gulbins E: Ceramide accumulation mediates inflammation, cell death and infection susceptibility in cystic fibrosis. Nat Med 2008;14:382-391. (Pubitemid 351499396)
73. Eberhard M, Ferlinz K, Alizzi K, Cacciato PM, Faggio C, Foller M, Lang F: FTY720-induced suicidal erythrocyte death. Cell Physiol Biochem 2010;26:761-766.
74. Beckham TH, Elojeimy S, Cheng JC, Turner LS, Hoffman SR, Norris JS, Liu X: Targeting sphingolipid metabolism in head and neck cancer: rational therapeutic potentials. Expert Opin Ther Targets 2010;14:529-539.
75. Liu X, Cheng JC, Turner LS, Elojeimy S, Beckham TH, Bielawska A, Keane TE, Hannun YA, Norris JS: Acid ceramidase upregulation in prostate cancer: role in tumor development and implications for therapy. Expert Opin Ther Targets 2009;13:1449-1458.
76. Oskouian B, Saba JD: Cancer treatment strategies targeting sphingolipid metabolism. Adv Exp Med Biol 2010;688:185-205.
77. Patwardhan GA, Liu YY: Sphingolipids and expression regulation of genes in cancer. Prog Lipid Res 2011;50:104-114.
78. Saddoughi SA, Song P, Ogretmen B: Roles of bioactive sphingolipids in cancer biology and therapeutics. Subcell Biochem 2008;49:413-440.
79. Vadas M, Xia P, McCaughan G, Gamble J: The role of sphingosine kinase 1 in cancer: oncogene or non-oncogene addiction? Biochim Biophys Acta 2008;1781:442-447.
80. Nixon GF: Sphingolipids in inflammation: pathological implications and potential therapeutic targets. Br J Pharmacol 2009;158:982-993.
81. Schuchardt M, Tolle M, Prufer J, van der Giet M: Pharmacological relevance and potential of sphingosine 1-phosphate in the vascular system. Br J Pharmacol 2011;163:1140-1162.
82. Dhami R, He X, Schuchman EH: Acid sphingomyelinase deficiency attenuates bleomycin-induced lung inflammation and fibrosis in mice. Cell Physiol Biochem 2010;26:749-760.
83. Becker KA, Grassme H, Zhang Y, Gulbins E: Ceramide in Pseudomonas aeruginosa infections and cystic fibrosis. Cell Physiol Biochem 2010;26:57-66.
84. Kuebler WM, Yang Y, Samapati R, Uhlig S: Vascular barrier regulation by PAF, ceramide, caveolae, and NO-an intricate signaling network with discrepant effects in the pulmonary and systemic vasculature. Cell Physiol Biochem 2010;26:29-40.
85. Li X, Becker KA, Zhang Y: Ceramide in redox signaling and cardiovascular diseases. Cell Physiol Biochem 2010;26:41-48.
86. Tolle M, Schuchardt M, van der Giet M: Relevance of sphingolipids in the pleiotropic protective effects of high-density lipoproteins. Curr Pharm Des 2010;16:1468-1479.
87. Holland WL, Summers SA: Sphingolipids, insulin resistance, and metabolic disease: new insights from in vivo manipulation of sphingolipid metabolism. Endocr Rev 2008;29:381-402. (Pubitemid 351831506)
88. Lang F, Ullrich S, Gulbins E: Ceramide formation as a target in beta cell survival and function. Expert Opin Ther Targets 2011;in press.
89. Zhao H, Przybylska M, Wu IH, Zhang J, Siegel C, Komarnitsky S, Yew NS, Cheng SH: Inhibiting glycosphingolipid synthesis improves glycemic control and insulin sensitivity in animal models of type diabetes. Diabetes 2007;56:1210-1218. (Pubitemid 46715599)
90. Zigmond E, Zangen SW, Pappo O, Sklair-Levy M, Lalazar G, Zolotaryova L, Raz I, Ilan Y: Beta-glycosphingolipids improve glucose intolerance and hepatic steatosis of the Cohen diabetic rat. Am J Physiol Endocrinol Metab 2009;296:E72-E78.
91. de la Monte SM: Insulin resistance and Alzheimer's disease. BMB Rep 2009;42:475-481.
92. Li H, Costantini C, Scrable H, Weindruch R, Puglielli L: Egr-1 and Hipk2 are required for the TrkA to p75(NTR) switch that occurs downstream of IGF1-R. Neurobiol Aging 2009;30:2010-2020.
93. Okada T, Kajimoto T, Jahangeer S, Nakamura S: Sphingosine kinase/sphingosine 1-phosphate signalling in central nervous system. Cell Signal 2009;21:7-13.
94. Tong M, Neusner A, Longato L, Lawton M, Wands JR, de la Monte SM: Nitrosamine exposure causes insulin resistance diseases: relevance to type 2 diabetes mellitus, non-alcoholic steatohepatitis, and Alzheimer's disease. J Alzheimers Dis 2009;17:827-844.
95. Morris AJ, Panchatcharam M, Cheng HY, Federico L, Fulkerson Z, Selim S, Miriyala S, Escalante-Alcalde D, Smyth SS: Regulation of blood and vascular cell function by bioactive lysophospholipids. J Thromb Haemost 2009;7:S38-43.
96. Nicolay JP, Liebig G, Niemoeller OM, Koka S, Ghashghaeinia M, Wieder T, Haendeler J, Busse R, Lang F: Inhibition of suicidal erythrocyte death by nitric oxide. Pflugers Arch 2008;456:293-305.
97. Hofmann LP, Ren S, Schwalm S, Pfeilschifter J, Huwiler A: Sphingosine kinase 1 and 2 regulate the capacity of mesangial cells to resist apoptotic stimuli in an opposing manner. Biol Chem 2008;389:1399-1407.
98. You B, Ren A, Yan G, Sun J: Activation of sphingosine kinase-1 mediates inhibition of vascular smooth muscle cell apoptosis by hyperglycemia. Diabetes 2007;56:1445-1453. (Pubitemid 46715619)
99. Wang L, Xing XP, Holmes A, Wadham C, Gamble JR, Vadas MA, Xia P: Activation of the sphingosine kinase-signaling pathway by high glucose mediates the proinflammatory phenotype of endothelial cells. Circ Res 2005;97:891-899. (Pubitemid 41552674)
100. Cuvillier O, Ader I, Bouquerel P, Brizuela L, Malavaud B, Mazerolles C, Rischmann P: Activation of sphingosine kinase-1 in cancer: implications for therapeutic targeting. Curr Mol Pharmacol 2010;3:53-65.
101. Rotstein NP, Miranda GE, Abrahan CE, German OL: Regulating survival and development in the retina: key roles for simple sphingolipids. J Lipid Res 2010;51:1247-1262.
102. Shida D, Takabe K, Kapitonov D, Milstien S, Spiegel S: Targeting SphK1 as a new strategy against cancer. Curr Drug Targets 2008;9:662-673.
103. Fadok VA, Bratton DL, Rose DM, Pearson A, Ezekewitz RA, Henson PM: A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 2000;405:85-90. (Pubitemid 30321820)
104. Boas FE, Forman L, Beutler E: Phosphatidylserine exposure and red cell viability in red cell aging and in hemolytic anemia. Proc Natl Acad Sci USA 1998;95:3077-3081. (Pubitemid 28135857)
105. Kempe DS, Lang PA, Duranton C, Akel A, Lang KS, Huber SM, Wieder T, Lang F: Enhanced programmed cell death of iron-deficient erythrocytes. FASEB J 2006;20:368-370. (Pubitemid 46671174)
106. Andrews DA, Low PS: Role of red blood cells in thrombosis. Curr Opin Hematol 1999;6:76-82. (Pubitemid 29342520)
107. Closse C, Dachary-Prigent J, Boisseau MR: Phosphatidylserine-related adhesion of human erythrocytes to vascular endothelium. Br J Haematol 1999;107:300-302. (Pubitemid 29530214)
108. Gallagher PG, Chang SH, Rettig MP, Neely JE, Hillery CA, Smith BD, Low PS: Altered erythrocyte endothelial adherence and membrane phospholipid asymmetry in hereditary hydrocytosis. Blood 2003;101:4625-4627. (Pubitemid 36857838)
109. Pandolfi A, Di Pietro N, Sirolli V, Giardinelli A, Di Silvestre S, Amoroso L, Di Tomo P, Capani F, Consoli A, Bonomini M: Mechanisms of uremic erythrocyte-induced adhesion of human monocytes to cultured endothelial cells. J Cell Physiol 2007;213:699-709. (Pubitemid 350058263)
110. Wood BL, Gibson DF, Tait JF: Increased erythrocyte phosphatidylserine exposure in sickle cell disease: flow-cytometric measurement and clinical associations. Blood 1996;88:1873-1880. (Pubitemid 26307087)
111. Chung SM, Bae ON, Lim KM, Noh JY, Lee MY, Jung YS, Chung JH: Lysophosphatidic acid induces thrombogenic activity through phosphatidylserine exposure and procoagulant microvesicle generation in human erythrocytes. Arterioscler Thromb Vasc Biol 2007;27:414-421.
112. Zwaal RF, Comfurius P, Bevers EM: Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 2005;62:971-988. (Pubitemid 40655614)
113. Zappulla D: Environmental stress, erythrocyte dysfunctions, inflammation, and the metabolic syndrome: adaptations to CO2 increases? J Cardiometab Syndr 2008;3:30-34.