Triggering of Suicidal Erythrocyte Death by the Antibiotic Ionophore Nigericin

Basic and Clinical Pharmacology and Toxicology

Volumn 118, Issue 5, 2016, Pages 381-389

  Bissinger, Rosi ^a   Malik, Abaid ^a   Bouguerra, Ghada ^a,b   Zhou, Yuetao ^a   Singh, Yogesh ^a   Abbès, Salem ^b   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b PASTEUR INSTITUTE OF TUNIS   (Tunisia)

Author keywords

[No Author keywords available]

Indexed keywords

CALCIUM; CALCIUM CHANNEL; CARIPORIDE; CERAMIDE; IONOPHORE; LIPOCORTIN 5; NIGERICIN; PHOSPHATIDYLSERINE; REACTIVE OXYGEN METABOLITE; ANTIINFECTIVE AGENT; GUANIDINE DERIVATIVE; SODIUM PROTON EXCHANGE PROTEIN; SULFONE;

APOPTOSIS; ARTICLE; CELL MEMBRANE; CELL PH; CELL SURFACE; CELL VOLUME; CONTROLLED STUDY; ERYTHROCYTE; ERYTHROCYTE MEMBRANE; ERYTHROCYTE VOLUME; FLOW CYTOMETRY; FLUORESCENCE; HUMAN; HUMAN CELL; OXIDATIVE STRESS; PH; PRIORITY JOURNAL; CELL DEATH; CELL SIZE; DOSE RESPONSE; DRUG EFFECTS; METABOLISM; PATHOLOGY;

ANNEXIN A5; ANTI-BACTERIAL AGENTS; CALCIUM; CELL DEATH; CELL SIZE; CERAMIDES; DOSE-RESPONSE RELATIONSHIP, DRUG; ERYTHROCYTES; GUANIDINES; HUMANS; HYDROGEN-ION CONCENTRATION; IONOPHORES; NIGERICIN; REACTIVE OXYGEN SPECIES; SODIUM-HYDROGEN ANTIPORTER; SULFONES;

EID: 84962742734     PISSN: 17427835     EISSN: 17427843     Source Type: Journal    
DOI: 10.1111/bcpt.12503     Document Type: Article

References (108)

1. Bevensee MO, Bashi E, Boron WF. Effect of trace levels of nigericin on intracellular pH and acid-base transport in rat renal mesangial cells. J Membr Biol 1999;169:131-9.
2. Boyarsky G, Hanssen C, Clyne LA. Inadequacy of high K+/nigericin for calibrating BCECF. II. Intracellular pH dependence of the correction. Am J Physiol 1996;271:C1146-56.
3. Boyarsky G, Hanssen C, Clyne LA. Inadequacy of high K+/nigericin for calibrating BCECF. I. Estimating steady-state intracellular pH. Am J Physiol 1996;271:C1131-45.
4. Canitrot Y, Lautier D, Viallet P, Salmon JM. Modulation of rhodamine 123 uptake by nigericin in sensitive and multidrug resistant leukemic cells. Cancer Lett 1994;84:75-83.
5. Chu CY, Kao YS, Fong JC. Nigericin inhibits insulin-stimulated glucose transport in 3T3-L1 adipocytes. J Cell Biochem 2002;85:83-91.
6. Doebler JA. Studies on the prevention of nigericin action in neuroblastoma X glioma hybrid (NG108-15) cells. Pharmacol Toxicol 2000;87:63-8.
7. Fellner V, Sauer FD, Kramer JK. Effect of nigericin, monensin, and tetronasin on biohydrogenation in continuous flow-through ruminal fermenters. J Dairy Sci 1997;80:921-8.
8. Fruth IA, Arrizabalaga G. Toxoplasma gondii: induction of egress by the potassium ionophore nigericin. Int J Parasitol 2007;37:1559-67.
9. Hamidinia SA, Tan B, Erdahl WL, Chapman CJ, Taylor RW, Pfeiffer DR. The ionophore nigericin transports Pb2 + with high activity and selectivity: a comparison to monensin and ionomycin. Biochemistry 2004;43:15956-65.
10. Harvey BM, Mironenko T, Sun Y, Hong H, Deng Z, Leadlay PF et al. Insights into polyether biosynthesis from analysis of the nigericin biosynthetic gene cluster in Streptomyces sp. DSM4137. Chem Biol 2007;14:703-14.
11. Irurzun A, Nieva JL, Carrasco L. Entry of Semliki forest virus into cells: effects of concanamycin A and nigericin on viral membrane fusion and infection. Virology 1997;227:488-92.
12. King SR, Walsh LP, Stocco DM. Nigericin inhibits accumulation of the steroidogenic acute regulatory protein but not steroidogenesis. Mol Cell Endocrinol 2000;166:147-53.
13. Kucejova B, Kucej M, Petrezselyova S, Abelovska L, Tomaska L. A screen for nigericin-resistant yeast mutants revealed genes controlling mitochondrial volume and mitochondrial cation homeostasis. Genetics 2005;171:517-26.
14. Lim J, Lee Y, Kim HW, Rhyu IJ, Oh MS, Youdim MB et al. Nigericin-induced impairment of autophagic flux in neuronal cells is inhibited by overexpression of Bak. J Biol Chem 2012;287:23271-82.
15. Lin CW, Shulok JR. Enhancement of Nile blue derivative-induced photocytotoxicity by nigericin and low cytoplasmic pH. Photochem Photobiol 1994;60:143-6.
16. Patten GS, Leifert WR, Burnard SL, Head RJ, McMurchie EJ. Stimulation of human cheek cell Na+/H+ antiporter activity by saliva and salivary electrolytes: amplification by nigericin. Mol Cell Biochem 1996;154:133-41.
17. Prabhananda BS, Kombrabail MH. Metal ion specificity in anaesthetic induced increase in the rate of monensin and nigericin mediated H+/M+ exchange across phospholipid vesicular membranes. Indian J Biochem Biophys 1999;36:415-21.
18. Rodriguez R, Sitges M. Nigericin-induced Na+/H+ and K+/H+ exchange in synaptosomes: effect on [3H]GABA release. Neurochem Res 1996;21:889-95.
19. Varnes ME, Bayne MT, Menegay HJ, Tuttle SW. Effect of the K+/H+ ionophore nigericin on response of A549 cells to photodynamic therapy and tert-butylhydroperoxide. Free Radic Biol Med 1993;15:395-405.
20. Wood PJ, Sansom JM, Newell K, Tannock IF, Stratford IJ. Reduction of tumour intracellular pH and enhancement of melphalan cytotoxicity by the ionophore Nigericin. Int J Cancer 1995;60:264-8.
21. Varnes ME, Bayne MT, Bright GR. Reduction of intracellular pH is not the mechanism for the synergistic interaction between photodynamic therapy and nigericin. Photochem Photobiol 1996;64:853-8.
22. Deng CC, Liang Y, Wu MS, Feng FT, Hu WR, Chen LZ et al. Nigericin selectively targets cancer stem cells in nasopharyngeal carcinoma. Int J Biochem Cell Biol 2013;45:1997-2006.
23. Fang A, Wong GK, Demain AL. Enhancement of the antifungal activity of rapamycin by the coproduced elaiophylin and nigericin. J Antibiot (Tokyo) 2000;53:158-62.
24. Ivanova IV, Khristova KR, Moncheva PA, Miteva VI. [Resistance to its own antibiotic nigericin and macromolecular synthesis in Streptomyces hygroscopicus 155]. Antibiot Khimioter 1995;40:12-6.
25. Moncheva PA, Christova KR, Ivanova IV. Resistance to the polyether ionophore antibiotic pandavir (nigericin) in two producing strains of Streptomyces. J Antibiot (Tokyo) 1995;48:811-4.
26. Mouslim J, Cuer A, David L, Tabet JC. Biosynthetic study on the polyether carboxylic antibiotic, nigericin production and biohydroxylation of grisorixin by nigericin-producing Streptomyces hygroscopicus NRRL B-1865. J Antibiot (Tokyo) 1995;48:1011-4.
27. Adovelande J, Schrevel J. Carboxylic ionophores in malaria chemotherapy: the effects of monensin and nigericin on Plasmodium falciparum in vitro and Plasmodium vinckei petteri in vivo. Life Sci 1996;59:PL309-15.
28. Couzinet S, Dubremetz JF, David L, Prensier G. Toxoplasma gondii: activity of the polyether ionophorous antibiotic nigericin on tachyzoites in cell culture. Exp Parasitol 1994;78:341-51.
29. Irurzun A, Sanchez-Palomino S, Novoa I, Carrasco L. Monensin and nigericin prevent the inhibition of host translation by poliovirus, without affecting p220 cleavage. J Virol 1995;69:7453-60.
30. Myskiw C, Piper J, Huzarewich R, Booth TF, Cao J, He R. Nigericin is a potent inhibitor of the early stage of vaccinia virus replication. Antiviral Res 2010;88:304-10.
31. Hasuda K, Lee C, Tannock IF. Antitumor activity of nigericin and 5-(N-ethyl-N-isopropyl)amiloride: an approach to therapy based on cellular acidification and the inhibition of regulation of intracellular pH. Oncol Res 1994;6:259-68.
32. Zhou HM, Dong TT, Wang LL, Feng B, Zhao HC, Fan XK et al. Suppression of colorectal cancer metastasis by nigericin through inhibition of epithelial-mesenchymal transition. World J Gastroenterol 2012;18:2640-8.
33. Mashima T, Okabe S, Seimiya H. Pharmacological targeting of constitutively active truncated androgen receptor by nigericin and suppression of hormone-refractory prostate cancer cell growth. Mol Pharmacol 2010;78:846-54.
34. Oh JH, O'Malley KL, Krajewski S, Reed JC, Oh YJ. Bax accelerates staurosporine-induced but suppresses nigericin-induced neuronal cell death. NeuroReport 1997;8:1851-6.
35. Watanabe N, Kawaguchi M, Kobayashi Y. Activation of interleukin-1beta-converting enzyme by nigericin is independent of apoptosis. Cytokine 1998;10:645-53.
36. Hentze H, Lin XY, Choi MS, Porter AG. Critical role for cathepsin B in mediating caspase-1-dependent interleukin-18 maturation and caspase-1-independent necrosis triggered by the microbial toxin nigericin. Cell Death Differ 2003;10:956& #x2013;68.
37. Stout-Delgado HW, Vaughan SE, Shirali AC, Jaramillo RJ, Harrod KS. Impaired NLRP3 inflammasome function in elderly mice during influenza infection is rescued by treatment with nigericin. J Immunol 2012;188:2815-24.
38. Xue LY, Agarwal ML, Varnes ME. Elevation of GRP-78 and loss of HSP-70 following photodynamic treatment of V79 cells: sensitization by nigericin. Photochem Photobiol 1995;62:135-43.
39. O'Rourke F, Soons K, Flaumenhauft R, Watras J, Baio-Larue C, Matthews E et al. Ca2 + release by inositol 1, 4, 5-trisphosphate is blocked by the K(+)-channel blockers apamin and tetrapentylammonium ion, and a monoclonal antibody to a 63 kDa membrane protein: reversal of blockade by K+ ionophores nigericin and valinomycin and purification of the 63 kDa antibody-binding protein. Biochem J 1994;300(Pt 3):673-83.
40. Erecinska M, Nelson D, Dagani F, Deas J, Silver IA. Relations between intracellular ions and energy metabolism under acidotic conditions: a study with nigericin in synaptosomes, neurons, and C6 glioma cells. J Neurochem 1993;61:1356-68.
41. Cheneval D, Ramage P, Kastelic T, Szelestenyi T, Niggli H, Hemmig R et al. Increased mature interleukin-1beta (IL-1beta) secretion from THP-1 cells induced by nigericin is a result of activation of p45 IL-1beta-converting enzyme processing. J Biol Chem 1998;273:17846-51.
42. Perregaux D, Gabel CA. Interleukin-1 beta maturation and release in response to ATP and nigericin. Evidence that potassium depletion mediated by these agents is a necessary and common feature of their activity. J Biol Chem 1994;269:15195-203.
43. Le Petit-Thevenin J, Nobili O, Verine A, Boyer J. Selective modulation of membrane sphingomyelin fatty acid turnover by nigericin. A study in the rat reticulocyte. Life Sci 1996;59:PL289-94.
44. Parfenova H, Haffner J, Leffler CW. Phosphorylation-dependent stimulation of prostanoid synthesis by nigericin in cerebral endothelial cells. Am J Physiol 1999;277:C728-38.
45. 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:C1553-60.
46. Lang F, Qadri SM. Mechanisms and significance of eryptosis, the suicidal death of erythrocytes. Blood Purif 2012;33:125-30.
47. Abed M, Towhid ST, 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:C991-9.
48. Lau IP, Chen H, Wang J, Ong HC, Leung KC, Ho HP et al. In vitro effect of CTAB- and PEG-coated gold nanorods on the induction of eryptosis/erythroptosis in human erythrocytes. Nanotoxicology 2012;6:847-56.
49. 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;50:489-95.
50. Jilani K, Lang F. Carmustine-induced phosphatidylserine translocation in the erythrocyte membrane. Toxins (Basel) 2013;5:703-16.
51. Vota DM, Maltaneri RE, Wenker SD, Nesse AB, Vittori DC. Differential erythropoietin action upon cells induced to eryptosis by different agents. Cell Biochem Biophys 2013;65:145-57.
52. Zappulla D. Environmental stress, erythrocyte dysfunctions, inflammation, and the metabolic syndrome: adaptations to CO2 increases? J Cardiometab Syndr 2008;3:30-4.
53. Lupescu A, Jilani K, Zbidah M, Lang F. Patulin-induced suicidal erythrocyte death. Cell Physiol Biochem 2013;32:291-9.
54. Abed M, Zoubi KA, Theurer M, Lang F. Effect of dermaseptin on erythrocytes. Basic Clin Pharmacol Toxicol 2013;113:347-52.
55. Ahmed MS, Langer H, Abed M, Voelkl J, Lang F. The uremic toxin acrolein promotes suicidal erythrocyte death. Kidney Blood Press Res 2013;37:158-67.
56. Ghashghaeinia M, Cluitmans JC, 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;32:801-13.
57. Alzoubi K, Honisch S, Abed M, Lang F. Triggering of suicidal erythrocyte death by Penta-O-galloyl-beta-d-glucose. Toxins (Basel) 2014;6:54-65.
58. Jilani K, Enkel S, Bissinger R, Almilaji A, Abed M, Lang F. Fluoxetine induced suicidal erythrocyte death. Toxins (Basel) 2013;5:1230-43.
59. Lupescu A, Bissinger R, Jilani K, Lang F. Triggering of suicidal erythrocyte death by celecoxib. Toxins (Basel) 2013;5:1543-54.
60. Arnold M, Lang E, Modicano P, Bissinger R, Faggio C, Abed M et al. Effect of nitazoxanide on erythrocytes. Basic Clin Pharmacol Toxicol 2014;114:421-6.
61. Oswald G, Alzoubi K, Abed M, Lang F. Stimulation of suicidal erythrocyte death by ribavirin. Basic Clin Pharmacol Toxicol 2014;114:311-7.
62. Lupescu A, Bissinger R, Herrmann T, Oswald G, Jilani K, Lang F. Induction of suicidal erythrocyte death by novobiocin. Cell Physiol Biochem 2014;33:670-80.
63. 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;37:567-78.
64. Alzoubi K, Calabròa S, Bissinger R, Abed M, Faggio C, Lang F. Stimulation of suicidal erythrocyte death by artesunate. Cell Physiol Biochem 2014;34:2232-44.
65. Arnold M, Bissinger R, Lang F. Mitoxantrone-induced suicidal erythrocyte death. Cell Physiol Biochem 2014;34:1756-67.
66. Bissinger R, Fischer S, Jilani K, Lang F. Stimulation of erythrocyte death by phloretin. Cell Physiol Biochem 2014;34:2256-65.
67. Bissinger R, Lupescu A, Zelenak C, Jilani K, Lang F. Stimulation of eryptosis by cryptotanshinone. Cell Physiol Biochem 2014;34:432-42.
68. Bissinger R, Modicano P, Frauenfeld L, Lang E, Jacobi J, Faggio C et al. Estramustine-induced suicidal erythrocyte death. Cell Physiol Biochem 2013;32:1426-36.
69. 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;33:1516-26.
70. Lupescu A, Bissinger R, Warsi J, Jilani K, Lang F. Stimulation of erythrocyte cell membrane scrambling by gedunin. Cell Physiol Biochem 2014;33:1838-48.
71. Malik A, Bissinger R, Calabro S, Faggio C, Jilani K, Lang F. Aristolochic acid induced suicidal erythrocyte death. Kidney Blood Press Res 2014;39:408-19.
72. Tesoriere L, Attanzio A, Allegra M, Cilla A, Gentile C, Livrea MA. Oxysterol mixture in hypercholesterolemia-relevant proportion causes oxidative stress-dependent eryptosis. Cell Physiol Biochem 2014;34:1075-89.
73. Voelkl J, Alzoubi K, Mamar AK, Ahmed MS, Abed M, Lang F. Stimulation of suicidal erythrocyte death by increased extracellular phosphate concentrations. Kidney Blood Press Res 2013;38:42-51.
74. 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;34:1780-91.
75. Qadri SM, Kucherenko Y, Lang F. Beauvericin induced erythrocyte cell membrane scrambling. Toxicology 2011;283:24-31.
76. Abed M, Artunc F, Alzoubi K, Honisch S, Baumann D, Foller M et al. Suicidal erythrocyte death in end-stage renal disease. J Mol Med (Berl) 2014;92:871-9.
77. Polak-Jonkisz D, Purzyc L. Ca(2 + ) influx versus efflux during eryptosis in uremic erythrocytes. Blood Purif 2012;34:209-10; author reply 10.
78. Calderon-Salinas JV, Munoz-Reyes EG, Guerrero-Romero JF, Rodriguez-Moran M, Bracho-Riquelme RL, Carrera-Gracia MA et al. Eryptosis and oxidative damage in type 2 diabetic mellitus patients with chronic kidney disease. Mol Cell Biochem 2011;357:171-9.
79. Lang PA, Beringer O, Nicolay JP, Amon O, Kempe DS, Hermle T et al. Suicidal death of erythrocytes in recurrent hemolytic uremic syndrome. J Mol Med (Berl) 2006;84:378-88.
80. Nicolay JP, Schneider J, Niemoeller OM, Artunc F, Portero-Otin M, Haik G Jr et al. Stimulation of suicidal erythrocyte death by methylglyoxal. Cell Physiol Biochem 2006;18:223-32.
81. Lang E, Gatidis S, Freise NF, Bock H, Kubitz R, Lauermann C et al. Conjugated bilirubin triggers anemia by inducing erythrocyte death. Hepatology 2015;61:275-84.
82. Kempe DS, Akel A, Lang PA, Hermle T, Biswas R, Muresanu J et al. Suicidal erythrocyte death in sepsis. J Mol Med (Berl) 2007;85:273-81.
83. Lang PA, Schenck M, Nicolay JP, Becker JU, Kempe DS, Lupescu A et al. Liver cell death and anemia in Wilson disease involve acid sphingomyelinase and ceramide. Nat Med 2007;13:164-70.
84. Bernstein RL, Hyun WC, Davis JH, Fulwyler MJ, Pershadsingh HA. Flow cytometric analysis of mature adipocytes. Cytometry 1989;10:469-74.
85. Wooden JM, Finney GL, Rynes E, Maccoss MJ, Lambert AJ, Robledo RF et al. Comparative proteomics reveals deficiency of SLC9A1 (sodium/hydrogen exchanger NHE1) in beta-adducin null red cells. Br J Haematol 2011;154:492-501.
86. Aharonovitz O, Demaurex N, Woodside M, Grinstein S. ATP dependence is not an intrinsic property of Na+/H+ exchanger NHE1: requirement for an ancillary factor. Am J Physiol 1999;276:C1303-11.
87. Lang F, Hoffmann EK. Role of ion transport in control of apoptotic cell death. Compr Physiol 2012;2:2037-61.
88. Pasham V, Rotte A, Yang W, Zelenak C, Bhandaru M, Foller M et al. OSR1-sensitive regulation of Na+/H+ exchanger activity in dendritic cells. Am J Physiol Cell Physiol 2012;303:C416-26.
89. Rotte A, Pasham V, Eichenmuller M, Yang W, Bhandaru M, Lang F. Influence of dexamethasone on na+/h+ exchanger activity in dendritic cells. Cell Physiol Biochem 2011;28:305-14.
90. Rotte A, Pasham V, Eichenmuller M, Mahmud H, Xuan NT, Shumilina E et al. Effect of bacterial lipopolysaccharide on Na(+)/H(+) exchanger activity in dendritic cells. Cell Physiol Biochem 2010;26:553-62.
91. Rotte A, Pasham V, Eichenmuller M, Bhandaru M, Foller M, Lang F. Upregulation of Na+/H+ exchanger by the AMP-activated protein kinase. Biochem Biophys Res Commun 2010;398:677-82.
92. Kawamoto T, Kimura H, Kusumoto K, Fukumoto S, Shiraishi M, Watanabe T et al. Potent and selective inhibition of the human Na+/H+ exchanger isoform NHE1 by a novel aminoguanidine derivative T-162559. Eur J Pharmacol 2001;420:1-8.
93. Harguindey S, Arranz JL, Polo Orozco JD, Rauch C, Fais S, Cardone RA et al. Cariporide and other new and powerful NHE1 inhibitors as potentially selective anticancer drugs-an integral molecular/biochemical/metabolic/clinical approach after one hundred years of cancer research. J Transl Med 2013;11:282.
94. Harrison HE, Bunting H, Ordway NK, Albrink WS. The pathogenesis of the renal injury produced in the dog by hemoglobin or methemoglobin. J Exp Med 1947;86:339-56.
95. Kirk K. Membrane transport in the malaria-infected erythrocyte. Physiol Rev 2001;81:495-537.
96. Ayi K, Giribaldi G, Skorokhod A, Schwarzer E, Prendergast PT, 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;46:3180-4.
97. 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;104:3364-71.
98. Cappadoro M, Giribaldi G, O'Brien E, Turrini F, Mannu F, Ulliers D et al. Early phagocytosis of glucose-6-phosphate dehydrogenase (G6PD)-deficient erythrocytes parasitized by Plasmodium falciparum may explain malaria protection in G6PD deficiency. Blood 1998;92:2527-34.
99. Koka S, Huber SM, Boini KM, Lang C, Foller M, Lang F. Lead decreases parasitemia and enhances survival of Plasmodium berghei-infected mice. Biochem Biophys Res Commun 2007;363:484-9.
100. Koka S, Lang C, Niemoeller OM, Boini KM, Nicolay JP, Huber SM et al. Influence of NO synthase inhibitor L-NAME on parasitemia and survival of Plasmodium berghei infected mice. Cell Physiol Biochem 2008;21:481-8.
101. Borst O, Abed M, Alesutan I, Towhid ST, Qadri SM, Foller M et al. Dynamic adhesion of eryptotic erythrocytes to endothelial cells via CXCL16/SR-PSOX. Am J Physiol Cell Physiol 2012;302:C644-51.
102. Andrews DA, Low PS. Role of red blood cells in thrombosis. Curr Opin Hematol 1999;6:76-82.
103. Chung SM, Bae ON, Lim KM, Noh JY, Lee MY, Jung YS et al. Lysophosphatidic acid induces thrombogenic activity through phosphatidylserine exposure and procoagulant microvesicle generation in human erythrocytes. Arterioscler Thromb Vasc Biol 2007;27:414-21.
104. Zwaal RF, Comfurius P, Bevers EM. Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 2005;62:971-88.
105. Closse C, Dachary-Prigent J, Boisseau MR. Phosphatidylserine-related adhesion of human erythrocytes to vascular endothelium. Br J Haematol 1999;107:300-2.
106. Gallagher PG, Chang SH, Rettig MP, Neely JE, Hillery CA, Smith BD et al. Altered erythrocyte endothelial adherence and membrane phospholipid asymmetry in hereditary hydrocytosis. Blood 2003;101:4625-7.
107. Pandolfi A, Di Pietro N, Sirolli V, Giardinelli A, Di Silvestre S, Amoroso L et al. Mechanisms of uremic erythrocyte-induced adhesion of human monocytes to cultured endothelial cells. J Cell Physiol 2007;213:699-709.
108. Wood BL, Gibson DF, Tait JF. Increased erythrocyte phosphatidylserine exposure in sickle cell disease: flow-cytometric measurement and clinical associations. Blood 1996;88:1873-80.