Bile acid-induced suicidal erythrocyte death

Cellular Physiology and Biochemistry

Volumn 38, Issue 4, 2016, Pages 1500-1509

  Lang, Elisabeth ^a,b   Pozdeev, Vitaly I ^a   Gatidis, Sergios ^b   Qadri, Syed M ^b,c   Häussinger, Dieter ^a   Kubitz, Ralf ^a   Herebian, Diran ^a   Mayatepek, Ertan ^a   Lang, Florian ^b   Lang, Karl S ^d   Lang, Philipp A ^a,e  

^a HEINRICH HEINE UNIVERSITY   (Germany)

^b UNIVERSITY OF TÜBINGEN   (Germany)

^c MCMASTER UNIVERSITY   (Canada)

^d UNIVERSITY OF DUISBURG ESSEN   (Germany)

^e Department of Molecular Medicine II ^*  (Germany)

Author keywords

Apoptosis; Calcium; Cell volume; Eryptosis; Phosphatidylserine; Scrambling

Indexed keywords

CALCIUM ION; CERAMIDE; GLYCOCHENODEOXYCHOLIC ACID; LIPOCORTIN 5; PHOSPHATIDYLSERINE; TAUROCHENODEOXYCHOLIC ACID; ANILINE DERIVATIVE; BILE ACID; CALCIUM; CHOLAGOGUE; DETERGENT; FLUO 3; XANTHENE DERIVATIVE;

APOPTOSIS; ARTICLE; CALCIUM CELL LEVEL; CELL MEMBRANE; CELL STIMULATION; CELL VOLUME; CONCENTRATION (PARAMETERS); CONTROLLED STUDY; CYTOSOL; ERYPTOSIS; ERYTHROCYTE; ERYTHROCYTE MEMBRANE; GENE TRANSLOCATION; HEMOLYSIS; HUMAN; HUMAN CELL; IN VITRO STUDY; INCUBATION TIME; LIPOGENESIS; PRIORITY JOURNAL; PROTEIN BINDING; CELL CULTURE; CHEMISTRY; CYTOLOGY; DRUG EFFECTS; FLOW CYTOMETRY; METABOLISM;

ANILINE COMPOUNDS; BILE ACIDS AND SALTS; CALCIUM; CELLS, CULTURED; CERAMIDES; CHOLAGOGUES AND CHOLERETICS; DETERGENTS; ERYPTOSIS; ERYTHROCYTES; FLOW CYTOMETRY; GLYCOCHENODEOXYCHOLIC ACID; HEMOLYSIS; HUMANS; PHOSPHATIDYLSERINES; TAUROCHENODEOXYCHOLIC ACID; XANTHENES;

EID: 84964053940     PISSN: 10158987     EISSN: 14219778     Source Type: Journal    
DOI: 10.1159/000443091     Document Type: Article

References (75)

1. Bernhardt I, Weiss E, Robinson HC, Wilkins R, Bennekou P. Differential effect of HOE642 on two separate monovalent cation transporters in the human red cell membrane. Cell Physiol Biochem 2007; 20: 601-606
2. Duranton C, Huber S, Tanneur V, Lang K, Brand V, Sandu C, Lang F. Electrophysiological properties of the Plasmodium Falciparum-induced cation conductance of human erythrocytes. Cell Physiol Biochem 2003; 13: 189-198
3. Duranton C, Huber SM, Lang F. Oxidation induces a Cl(-)-dependent cation conductance in human red blood cells. J Physiol 2002; 539: 847-855
4. Huber SM, Gamper N, Lang F. Chloride conductance and volume-regulatory nonselective cation conductance in human red blood cell ghosts. Pflugers Arch 2001; 441: 551-558
5. Kaestner L, Bernhardt I. Ion channels in the human red blood cell membrane: their further investigation and physiological relevance. Bioelectrochemistry 2002; 55: 71-74
6. Kaestner L, Christophersen P, Bernhardt I, Bennekou P. The non-selective voltage-Activated cation channel in the human red blood cell membrane: reconciliation between two conflicting reports and further characterisation. Bioelectrochemistry 2000; 52: 117-125
7. Lang KS, Duranton C, Poehlmann H, Myssina S, Bauer C, Lang F, Wieder T, Huber SM. Cation channels trigger apoptotic death of erythrocytes. Cell Death Differ 2003; 10: 249-256
8. 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
9. Brand VB, Sandu CD, Duranton C, Tanneur V, Lang KS, Huber SM, Lang F. Dependence of Plasmodium falciparum in vitro growth on the cation permeability of the human host erythrocyte. Cell Physiol Biochem 2003; 13: 347-356
10. 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
11. Daugas E, Cande C, Kroemer G. Erythrocytes: death of a mummy. Cell Death Differ 2001; 8: 1131-1133
12. 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
13. Brugnara C, de Franceschi L, Alper SL. Inhibition of Ca(2+)-dependent K+ transport and cell dehydration in sickle erythrocytes by clotrimazole and other imidazole derivatives. J Clin Invest 1993; 92: 520-526
14. 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: C1553-1560
15. 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
16. 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
17. Foller M, Geiger C, Mahmud H, Nicolay J, Lang F. Stimulation of suicidal erythrocyte death by amantadine. Eur J Pharmacol 2008; 581: 13-18
18. Foller M, Sopjani M, Mahmud H, Lang F. Vanadate-induced suicidal erythrocyte death. Kidney Blood Press Res 2008; 31: 87-93
19. Lang E, Gatidis S, Freise NF, Bock H, Kubitz R, Lauermann C, Orth HM, Klindt C, Schuier M, Keitel V, Reich M, Liu G, Schmidt S, Xu HC, Qadri SM, Herebian D, Pandyra AA, Mayatepek E, Gulbins E, Lang F, Haussinger D, Lang KS, Foller M, Lang PA. Conjugated bilirubin triggers anemia by inducing erythrocyte death. Hepatology 2015; 61: 275-284
20. Zollner G, Marschall HU, Wagner M, Trauner M. Role of nuclear receptors in the adaptive response to bile acids and cholestasis: pathogenetic and therapeutic considerations. Mol Pharm 2006; 3: 231-251
21. Voronina SG, Gryshchenko OV, Gerasimenko OV, Green AK, Petersen OH, Tepikin AV. Bile acids induce a cationic current, depolarizing pancreatic acinar cells and increasing the intracellular Na+ concentration. J Biol Chem 2005; 280: 1764-1770
22. Borgognone M, Perez LM, Basiglio CL, Ochoa JE, Roma MG. Signaling modulation of bile salt-induced necrosis in isolated rat hepatocytes. Toxicol Sci 2005; 83: 114-125
23. Petersen OH, Sutton R. Ca2+ signalling and pancreatitis: effects of alcohol, bile and coffee. Trends Pharmacol Sci 2006; 27: 113-120
24. Higuchi H, Bronk SF, Takikawa Y, Werneburg N, Takimoto R, El-Deiry W, Gores GJ. The bile acid glycochenodeoxycholate induces trail-receptor 2/DR5 expression and apoptosis. J Biol Chem 2001; 276: 38610-38618
25. Wang K, Brems JJ, Gamelli RL, Ding J. Reversibility of caspase activation and its role during glycochenodeoxycholate-induced hepatocyte apoptosis. J Biol Chem 2005; 280: 23490-23495
26. Wang K, Brems JJ, Gamelli RL, Holterman AX. Survivin signaling is regulated through nuclear factor-kappa B pathway during glycochenodeoxycholate-induced hepatocyte apoptosis. Biochim Biophys Acta 2010; 1803: 1368-1375
27. Wang K, Brems JJ, Gamelli RL, Holterman AX. iNOS/NO signaling regulates apoptosis induced by glycochenodeoxycholate in hepatocytes. Cell Signal 2011; 23: 1677-1685
28. Chieco P, Romagnoli E, Aicardi G, Suozzi A, Forti GC, Roda A. Apoptosis induced in rat hepatocytes by in vivo exposure to taurochenodeoxycholate. Histochem J 1997; 29: 875-883
29. Rust C, Karnitz LM, Paya CV, Moscat J, Simari RD, Gores GJ. The bile acid taurochenodeoxycholate activates a phosphatidylinositol 3-kinase-dependent survival signaling cascade. J Biol Chem 2000; 275: 20210-20216
30. Lang E, Lang F. Mechanisms and pathophysiological significance of eryptosis, the suicidal erythrocyte death. Semin Cell Dev Biol 2015; 39: 35-42
31. Abed M, Artunc F, Alzoubi K, Honisch S, Baumann D, Foller M, Lang F. Suicidal erythrocyte death in end-stage renal disease. J Mol Med (Berl) 2014; 92: 871-879
32. Ahmed MS, Langer H, Abed M, Voelkl J, Lang F. The uremic toxin acrolein promotes suicidal erythrocyte death. Kidney Blood Press Res 2013; 37: 158-167
33. Calderon-Salinas JV, Munoz-Reyes EG, Guerrero-Romero JF, Rodriguez-Moran M, Bracho-Riquelme RL, Carrera-Gracia MA, Quintanar-Escorza MA. Eryptosis and oxidative damage in type 2 diabetic mellitus patients with chronic kidney disease. Mol Cell Biochem 2011; 357: 171-179
34. Polak-Jonkisz D, Purzyc L. Ca(2+) influx versus efflux during eryptosis in uremic erythrocytes. Blood Purif 2012; 34: 209-210; author reply 210
35. Lang PA, Beringer O, Nicolay JP, Amon O, Kempe DS, Hermle T, Attanasio P, Akel A, Schafer R, Friedrich B, Risler T, Baur M, Olbricht CJ, Zimmerhackl LB, Zipfel PF, Wieder T, Lang F. Suicidal death of erythrocytes in recurrent hemolytic uremic syndrome. J Mol Med (Berl) 2006; 84: 378-388
36. Abed M, Feger M, Alzoubi K, Pakladok T, Frauenfeld L, Geiger C, Towhid ST, Lang F. Sensitization of erythrocytes to suicidal erythrocyte death following water deprivation. Kidney Blood Press Res 2013; 37: 567-578
37. 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
38. Birka C, Lang PA, Kempe DS, Hoefling L, Tanneur V, Duranton C, Nammi S, Henke G, Myssina S, Krikov M, Huber SM, Wieder T, Lang F. Enhanced susceptibility to erythrocyte apoptosis following phosphate depletion. Pflugers Arch 2004; 448: 471-477
39. Nicolay JP, Schneider J, Niemoeller OM, Artunc F, Portero-Otin M, Haik G Jr, Thornalley PJ, Schleicher E, Wieder T, Lang F. Stimulation of suicidal erythrocyte death by methylglyoxal. Cell Physiol Biochem 2006; 18: 223-232
40. Kempe DS, Akel A, Lang PA, Hermle T, Biswas R, Muresanu J, Friedrich B, Dreischer P, Wolz C, Schumacher U, Peschel A, Gotz F, Doring G, Wieder T, Gulbins E, Lang F. Suicidal erythrocyte death in sepsis. J Mol Med (Berl) 2007; 85: 273-281
41. Brand V, Koka S, Lang C, Jendrossek V, Huber SM, Gulbins E, Lang F. Influence of amitriptyline on eryptosis, parasitemia and survival of Plasmodium berghei-infected mice. Cell Physiol Biochem 2008; 22: 405-412
42. Koka S, Lang C, Boini KM, Bobbala D, Huber SM, Lang F. Influence of chlorpromazine on eryptosis, parasitemia and survival of Plasmodium berghe infected mice. Cell Physiol Biochem 2008; 22: 261-268
43. Koka S, Lang C, Niemoeller OM, Boini KM, Nicolay JP, Huber SM, Lang F. Influence of NO synthase inhibitor L-NAME on parasitemia and survival of Plasmodium berghei infected mice. Cell Physiol Biochem 2008; 21: 481-488
44. 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
45. Alzoubi K, Egler J, Abed M, Lang F. Enhanced Eryptosis Following Auranofin Exposure. Cell Physiol Biochem 2015; 37: 1018-1028
46. Bissinger R, Barking S, Alzoubi K, Liu G, Liu G, Lang F. Stimulation of Suicidal Erythrocyte Death by the Antimalarial Drug Mefloquine. Cell Physiol Biochem 2015; 36: 1395-1405
47. Bissinger R, Bouguerra G, Stockinger K, Abbes S, Lang F. Triggering of Suicidal Erythrocyte Death by Topotecan. Cell Physiol Biochem 2015; 37: 1607-1618
48. Bouguerra G, Aljanadi O, Bissinger R, Abbes S, Lang F. Embelin-Induced Phosphatidylserine Translocation in the Erythrocyte Cell Membrane. Cell Physiol Biochem 2015; 37: 1629-1640
49. Bouguerra G, Bissinger R, Abbes S, Lang F. Stimulation of Eryptosis by Narasin. Cell Physiol Biochem 2015; 37: 1807-1816
50. Bouguerra G, Bissinger R, Abbes S, Lang F. Zopolrestat Induced Suicidal Death of Human Erythrocytes. Cell Physiol Biochem 2015; 37: 1537-1546
51. Briglia M, Fazio A, Faggio C, Laufer S, Alzoubi K, Lang F. Triggering of Suicidal Erythrocyte Death by Ruxolitinib. Cell Physiol Biochem 2015; 37: 768-778
52. Briglia M, Fazio A, Signoretto E, Faggio C, Lang F. Edelfosine Induced Suicidal Death of Human Erythrocytes. Cell Physiol Biochem 2015; 37: 2221-2230
53. Calabro S, Alzoubi K, Faggio C, Laufer S, Lang F. Triggering of Suicidal Erythrocyte Death Following Boswellic Acid Exposure. Cell Physiol Biochem 2015; 37: 131-142
54. Egler J, Lang F. Licochalcone A Induced Suicidal Death of Human Erythrocytes. Cell Physiol Biochem 2015; 37: 2060-2070
55. Faggio C, Alzoubi K, Calabro S, Lang F. Stimulation of suicidal erythrocyte death by PRIMA-1. Cell Physiol Biochem 2015; 35: 529-540
56. Fazio A, Briglia M, Faggio C, Alzoubi K, Lang F. Stimulation of Suicidal Erythrocyte Death by Garcinol. Cell Physiol Biochem 2015; 37: 805-815
57. Lang E, Zelenak C, Eberhard M, Bissinger R, Rotte A, Ghashghaeinia M, Lupescu A, Lang F, Qadri SM. Impact of Cyclin-Dependent Kinase CDK4 Inhibition on Eryptosis. Cell Physiol Biochem 2015; 37: 1178-1186
58. Lupescu A, Bissinger R, Goebel T, Salker MS, Alzoubi K, Liu G, Chirigiu L, Mack AF, Qadri SM, Lang F. Enhanced suicidal erythrocyte death contributing to anemia in the elderly. Cell Physiol Biochem 2015; 36: 773-783
59. Officioso A, Alzoubi K, Manna C, Lang F. Clofazimine Induced Suicidal Death of Human Erythrocytes. Cell Physiol Biochem 2015; 37: 331-341
60. Peter T, Bissinger R, Enkel S, Alzoubi K, Oswald G, Lang F. Programmed erythrocyte death following in vitro Treosulfan treatment. Cell Physiol Biochem 2015; 35: 1372-1380
61. Stockinger K, Bissinger R, Bouguerra G, Abbes S, Lang F. Enhanced Eryptosis Following Exposure to Carnosic Acid. Cell Physiol Biochem 2015; 37: 1779-1791
62. Waibel S, Bissinger R, Bouguerra G, Abbes S, Lang F. Saquinavir Induced Suicidal Death of Human Erythrocytes. Cell Physiol Biochem 2015; 37: 1973-1982
63. Zierle J, Bissinger R, Egler J, Lang F. Lapatinib Induced Suicidal Death of Human Erythrocytes. Cell Physiol Biochem 2015; 37: 2275-2287
64. Lang E, Jilani K, Bissinger R, Rexhepaj R, Zelenak C, Lupescu A, Lang F, Qadri SM. Vitamin D-Rich Diet in Mice Modulates Erythrocyte Survival. Kidney Blood Press Res 2015; 40: 403-412
65. 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
66. 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
67. Boas FE, Forman L, Beutler E. Phosphatidylserine exposure and red cell viability in red cell aging and in hemolytic anemia. Proc Natl Acad Sci U S A 1998; 95: 3077-3081
68. Andrews DA, Low PS. Role of red blood cells in thrombosis. Curr Opin Hematol 1999; 6: 76-82
69. Closse C, Dachary-Prigent J, Boisseau MR. Phosphatidylserine-related adhesion of human erythrocytes to vascular endothelium. Br J Haematol 1999; 107: 300-302
70. 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
71. 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
72. 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
73. 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
74. Zwaal RF, Comfurius P, Bevers EM. Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 2005; 62: 971-988
75. Zappulla D. Environmental stress, erythrocyte dysfunctions, inflammation, and the metabolic syndrome: adaptations to CO2 increases?. J Cardiometab Syndr 2008; 3: 30-34