Inhibition of suicidal erythrocyte death by nitric oxide

Pflugers Archiv European Journal of Physiology

Volumn 456, Issue 2, 2008, Pages 293-305

  Nicolay, Jan P ^a   Liebig, Gerd ^a   Niemoeller, Olivier M ^a   Koka, Saisudha ^a   Ghashghaeinia, Mehrdad ^a   Wieder, Thomas ^a   Haendeler, Judith ^b   Busse, Rudi ^c   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b HEINRICH HEINE UNIVERSITY   (Germany)

^c GOETHE UNIVERSITY   (Germany)

Author keywords

Apoptosis; Cell volume; cGMP; Erythrocytes; Intracellular calcium; Nitric oxide; Nitroprusside; Osmotic stress; Protein kinase G; Red blood cells

Indexed keywords

CALCIUM ION; CERAMIDE; CYCLIC GMP; IONOMYCIN; LIPOCORTIN 5; NITRIC OXIDE; NITRIC OXIDE DONOR; NITROPRUSSIDE SODIUM; PAPANONOATE; PHOSPHATIDYLSERINE; THIOREDOXIN; UNCLASSIFIED DRUG;

APOPTOSIS; ARTICLE; CELL DEATH; CELL FUNCTION; CELL SIZE; CELL VOLUME; CONTROLLED STUDY; ERYPTOSIS; ERYTHROCYTE; ERYTHROCYTE LIFESPAN; FLOW CYTOMETRY; HUMAN; HUMAN CELL; KNOCKOUT MOUSE; NITROSYLATION; PRIORITY JOURNAL; PROTEIN BINDING;

ANIMALS; ANNEXINS; APOPTOSIS; CALCIUM; CERAMIDES; CYCLIC GMP; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; FLUORESCEINS; FLUORESCENT DYES; HUMANS; IONOMYCIN; IONOPHORES; MICE; MICE, KNOCKOUT; NITRIC OXIDE; NITROPRUSSIDE; PHOSPHATIDYLSERINES; SUCCINIMIDES;

EID: 42049086369     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-007-0393-1     Document Type: Article

References (72)

1. Akel A, Hermle T, Niemoeller OM, Kempe DS, Lang PA, Attanasio P, Podolski M, Wieder T, Lang F (2006) Stimulation of erythrocyte phosphatidylserine exposure by chlorpromazine. Eur J Pharmacol 532:11-17
2. Andrews DA, Low PS (1999) Role of red blood cells in thrombosis. Curr Opin Hematol 6:76-82
3. Bao X, Cui J, Wu Y, Han X, Gao C, Hua Z, Shen P (2007) The roles of endogenous reactive oxygen species and nitric oxide in triptolide-induced apoptotic cell death in macrophages. J Mol Med 85:85-98
4. Barvitenko NN, Adragna NC, Weber RE (2005) Erythrocyte signal transduction pathways, their oxygenation dependence and functional significance. Cell Physiol Biochem 15:1-18
5. Benhar M, Stamler JS (2005) A central role for S-nitrosylation in apoptosis. Nat Cell Biol 7:645-646
6. Berg CP, Engels IH, Rothbart A, Lauber K, Renz A, Schlosser SF, Schulze-Osthoff K, Wesselborg S (2001) Human mature red blood cells express caspase-3 and caspase-8, but are devoid of mitochondrial regulators of apoptosis. Cell Death Differ 8:1197-1206
7. 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 (2004) Enhanced susceptibility to erythrocyte "apoptosis" following phosphate depletion. Pflugers Arch 448:471-477
8. Boas FE, Forman L, Beutler E (1998) Phosphatidylserine exposure and red cell viability in red cell aging and in hemolytic anemia. Proc Natl Acad Sci U S A 95:3077-3081
9. Bosman GJ, Willekens FL, Werre JM (2005) Erythrocyte aging: a more than superficial resemblance to apoptosis? Cell Physiol Biochem 16:1-8
10. Brand VB, Sandu CD, Duranton C, Tanneur V, Lang KS, Huber SM, Lang F (2003) Dependence of Plasmodium falciparum in vitro growth on the cation permeability of the human host erythrocyte. Cell Physiol Biochem 13:347-356
11. Brandes RP, Schmitz-Winnenthal FH, Feletou M, Godecke A, Huang PL, Vanhoutte PM, Fleming I, Busse R (2000) An endothelium-derived hyperpolarizing factor distinct from NO and prostacyclin is a major endothelium-dependent vasodilator in resistance vessels of wild-type and endothelial NO synthase knockout mice. Proc Natl Acad Sci U S A 97:9747-9752
12. Bratosin D, Estaquier J, Petit F, Arnoult D, Quatannens B, Tissier JP, Slomianny C, Sartiaux C, Alonso C, Huart JJ, Montreuil J, Ameisen JC (2001) Programmed cell death in mature erythrocytes: a model for investigating death effector pathways operating in the absence of mitochondria. Cell Death Differ 8:1143-1156
13. Brugnara C, de Franceschi L, Alper SL (1993) Inhibition of Ca(2+)-dependent K+ transport and cell dehydration in sickle erythrocytes by clotrimazole and other imidazole derivatives. J Clin Invest 92:520-526
14. Castillo SS, Levy M, Wang C, Thaikoottathil JV, Khan E, Goldkorn T (2007) Nitric oxide-enhanced caspase-3 and acidic sphingomyelinase interaction: a novel mechanism by which airway epithelial cells escape ceramide-induced apoptosis. Exp Cell Res 313:816-823
15. Chung SM, Bae ON, Lim KM, Noh JY, Lee MY, Jung YS, Chung JH (2007) Lysophosphatidic acid induces thrombogenic activity through phosphatidylserine exposure and procoagulant microvesicle generation in human erythrocytes. Arterioscler Thromb Vasc Biol 27:414-421
16. Closse C, Dachary-Prigent J, Boisseau MR (1999) Phosphatidylserine- related adhesion of human erythrocytes to vascular endothelium. Br J Haematol 107:300-302
17. Cosby K, Partovi KS, Crawford JH, Patel RP, Reiter CD, Martyr S, Yang BK, Waclawiw MA, Zalos G, Xu X, Huang KT, Shields H, Kim-Shapiro DB, Schechter AN, Cannon RO III, Gladwin MT (2003) Nitrite reduction to nitric oxide by deoxyhemoglobin vasodilates the human circulation. Nat Med 9:1498-1505
18. Crawford JH, Isbell TS, Huang Z, Shiva S, Chacko BK, Schechter AN, Darley-Usmar VM, Kerby JD, Lang JD Jr., Kraus D, Ho C, Gladwin MT, Patel RP (2006) Hypoxia, red blood cells, and nitrite regulate NO-dependent hypoxic vasodilation. Blood 107:566-574
19. Das A, Smolenski A, Lohmann SM, Kukreja RC (2006) Cyclic GMP-dependent protein kinase Ialpha attenuates necrosis and apoptosis following ischemia/reoxygenation in adult cardiomyocyte. J Biol Chem 281:38644-38652
20. Davidson SM, Duchen MR (2007) Endothelial mitochondria: contributing to vascular function and disease. Circ Res 100:1128-1141
21. Dejam A, Hunter CJ, Pelletier MM, Hsu LL, Machado RF, Shiva S, Power GG, Kelm M, Gladwin MT, Schechter AN (2005) Erythrocytes are the major intravascular storage sites of nitrite in human blood. Blood 106:734-739
22. Dimmeler S, Haendeler J, Nehls M, Zeiher AM (1997) Suppression of apoptosis by nitric oxide via inhibition of interleukin-1beta-converting enzyme (ICE)-like and cysteine protease protein (CPP)-32-like proteases. J Exp Med 185:601-607
23. Dimmeler S, Zeiher AM (1999) Nitric oxide-an endothelial cell survival factor. Cell Death Differ 6:964-968
24. Eisele K, Lang PA, Kempe DS, Klarl BA, Niemoller O, Wieder T, Huber SM, Duranton C, Lang F (2006) Stimulation of erythrocyte phosphatidylserine exposure by mercury ions. Toxicol Appl Pharmacol 210:116-122
25. Fadok VA, Bratton DL, Rose DM, Pearson A, Ezekewitz RA, Henson PM (2000) A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405:85-90
26. Frasch SC, Henson PM, Kailey JM, Richter DA, Janes MS, Fadok VA, Bratton DL (2000) Regulation of phospholipid scramblase activity during apoptosis and cell activation by protein kinase Cdelta. J Biol Chem 275:23065-23073
27. Gallagher PG, Chang SH, Rettig MP, Neely JE, Hillery CA, Smith BD, Low PS (2003) Altered erythrocyte endothelial adherence and membrane phospholipid asymmetry in hereditary hydrocytosis. Blood 101:4625-4627
28. Grubina R, Huang Z, Shiva S, Joshi MS, Azarov I, Basu S, Ringwood LA, Jiang A, Hogg N, Kim-Shapiro DB, Gladwin MT (2007) Concerted nitric oxide formation and release from the simultaneous reactions of nitrite with deoxy- and oxyhemoglobin. J Biol Chem 282:12916-12927
29. Haendeler J, Hoffmann J, Tischler V, Berk BC, Zeiher AM, Dimmeler S (2002) Redox regulatory and anti-apoptotic functions of thioredoxin depend on S-nitrosylation at cysteine 69. Nat Cell Biol 4:743-749
30. Haendeler J, Hoffmann J, Zeiher AM, Dimmeler S (2004) Antioxidant effects of statins via S-nitrosylation and activation of thioredoxin in endothelial cells: a novel vasculoprotective function of statins. Circulation 110:856-861
31. Haendeler J, Zeiher AM, Dimmeler S (1999) Nitric oxide and apoptosis. Vitam Horm 57:49-77
32. Hoffmann J, Haendeler J, Zeiher AM, Dimmeler S (2001) TNFalpha and oxLDL reduce protein S-nitrosylation in endothelial cells. J Biol Chem 276:41383-41387
33. Kamp D, Sieberg T, Haest CW (2001) Inhibition and stimulation of phospholipid scrambling activity. Consequences for lipid asymmetry, echinocytosis, and microvesiculation of erythrocytes. Biochemistry 40:9438-9446
34. 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 (2007) Suicidal erythrocyte death in sepsis. J Mol Med 85:269-277
35. Kempe DS, Lang PA, Duranton C, Akel A, Lang KS, Huber SM, Wieder T, Lang F (2006) Enhanced programmed cell death of iron-deficient erythrocytes. FASEB J 20:368-370
36. Kempe DS, Lang PA, Eisele K, Klarl BA, Wieder T, Huber SM, Duranton C, Lang F (2005) Stimulation of erythrocyte phosphatidylserine exposure by lead ions. Am J Physiol Cell Physiol 288:C396-C402
37. Klarl BA, Lang PA, Kempe DS, Niemoeller OM, Akel A, Sobiesiak M, Eisele K, Podolski M, Huber SM, Wieder T, Lang F (2006) Protein kinase C mediates erythrocyte "programmed cell death" following glucose depletion. Am J Physiol Cell Physiol 290:C244-C253
38. Kolesnick RN, Kronke M (1998) Regulation of ceramide production and apoptosis. Annu Rev Physiol 60:643-665
39. Lang KS, Duranton C, Poehlmann H, Myssina S, Bauer C, Lang F, Wieder T, Huber SM (2003) Cation channels trigger apoptotic death of erythrocytes. Cell Death Differ 10:249-256
40. Lang KS, Lang PA, Bauer C, Duranton C, Wieder T, Huber SM, Lang F (2005) Mechanisms of suicidal erythrocyte death. Cell Physiol Biochem 15:195-202
41. Lang KS, Myssina S, Brand V, Sandu C, Lang PA, Berchtold S, Huber SM, Lang F, Wieder T (2004) Involvement of ceramide in hyperosmotic shock-induced death of erythrocytes. Cell Death Differ 11:231-243
42. -. Am J Physiol Renal Physiol 286:F1046-F1053
43. Lang KS, Roll B, Myssina S, Schittenhelm M, Scheel-Walter HG, Kanz L, Fritz J, Lang F, Huber SM, Wieder T (2002) Enhanced erythrocyte apoptosis in sickle cell anemia, thalassemia and glucose-6-phosphate dehydrogenase deficiency. Cell Physiol Biochem 12:365-372
44. 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 (2006) Suicidal death of erythrocytes in recurrent hemolytic uremic syndrome. J Mol Med 84:378-388
45. Lang PA, Huober J, Bachmann C, Kempe DS, Sobiesiak M, Akel A, Niemoeller OM, Dreischer P, Eisele K, Klarl BA, Gulbins E, Lang F, Wieder T (2006) Stimulation of erythrocyte phosphatidylserine exposure by paclitaxel. Cell Physiol Biochem 18:151-164
46. Lang PA, Kaiser S, Myssina S, Birka C, Weinstock C, Northoff H, Wieder T, Lang F, Huber SM (2004) Effect of Vibrio parahaemolyticus haemolysin on human erythrocytes. Cell Microbiol 6:391-400
47. Lang PA, Kaiser S, Myssina S, Wieder T, Lang F, Huber SM (2003) Role of Ca2+ -activated K+ channels in human erythrocyte apoptosis. Am J Physiol Cell Physiol 285:C1553-C1560
48. Lang PA, Kempe DS, Myssina S, Tanneur V, Birka C, Laufer S, Lang F, Wieder T, Huber SM (2005) PGE(2) in the regulation of programmed erythrocyte death. Cell Death Differ 12:415-428
49. Lang PA, Kempe DS, Tanneur V, Eisele K, Klarl BA, Myssina S, Jendrossek V, Ishii S, Shimizu T, Waidmann M, Hessler G, Huber SM, Lang F, Wieder T (2005) Stimulation of erythrocyte ceramide formation by platelet-activating factor. J Cell Sci 118:1233-1243
50. 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 (2007) Liver cell death and anemia in Wilson disease involve acid sphingomyelinase and ceramide. Nat Med 13:164-170
51. Li J, Billiar TR (1999) The anti-apoptotic actions of nitric oxide in hepatocytes. Cell Death Differ 6:952-955
52. Malan D, Levi RC, Alloatti G, Marcantoni A, Bedendi I, Gallo MP (2003) Cyclic AMP and cyclic GMP independent stimulation of ventricular calcium current by peroxynitrite donors in guinea pig myocytes. J Cell Physiol 197:284-296
53. Mannick JB, Hausladen A, Liu L, Hess DT, Zeng M, Miao QX, Kane LS, Gow AJ, Stamler JS (1999) Fas-induced caspase denitrosylation. Science 284:651-654
54. McMahon TJ, Moon RE, Luschinger BP, Carraway MS, Stone AE, Stolp BW, Gow AJ, Pawloski JR, Watke P, Singel DJ, Piantadosi CA, Stamler JS (2002) Nitric oxide in the human respiratory cycle. Nat Med 8:711-717
55. Melino G, Bernassola F, Knight RA, Corasaniti MT, Nistico G, Finazzi-Agro A (1997) S-nitrosylation regulates apoptosis. Nature 388:432-433
56. - channel blockers NPPB and niflumic acid blunt Ca(2+)-induced erythrocyte 'apoptosis'. Cell Physiol Biochem 14:241-248
57. Nagai-Kusuhara A, Nakamura M, Mukuno H, Kanamori A, Negi A, Seigel GM (2007) 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 84:152-162
58. Pacher P, Beckman JS, Liaudet L (2007) Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87:315-424
59. Pandolfi A, Di Pietro N, Sirolli V, Giardinelli A, Di Silvestre S, Amoroso L, Di Tomo P, Capani F, Consoli A, Bonomini M (2007) Mechanisms of uremic erythrocyte-induced adhesion of human monocytes to cultured endothelial cells. J Cell Physiol 213:699-709
60. Perretti M, Solito E (2004) Annexin 1 and neutrophil apoptosis. Biochem Soc Trans 32:507-510
61. Power GG, Bragg SL, Oshiro BT, Dejam A, Hunter CJ, Blood AB (2007) A novel method of measuring reduction of nitrite-induced methemoglobin applied to fetal and adult blood of humans and sheep. J Appl Physiol 103:1359-1365
62. Rice L, Alfrey CP (2005) The negative regulation of red cell mass by neocytolysis: physiologic and pathophysiologic manifestations. Cell Physiol Biochem 15:245-250
63. Rossig L, Fichtlscherer B, Breitschopf K, Haendeler J, Zeiher AM, Mulsch A, Dimmeler S (1999) Nitric oxide inhibits caspase-3 by S-nitrosation in vivo. J Biol Chem 274:6823-6826
64. Schwarzer E, Kühn H, Valente E, Arese P (2005) Band 3/complement-mediated recognition and removal of normally senescent and pathological human erythrocytes. Cell Physiol Biochem 16:133-146
65. Taylor EL, Megson IL, Haslett C, Rossi AG (2003) Nitric oxide: a key regulator of myeloid inflammatory cell apoptosis. Cell Death Differ 10:418-430
66. Unger RH (2002) Lipotoxic diseases. Annu Rev Med 53:319-336
67. William M, Vien J, Hamilton E, Garcia A, Bundgaard H, Clarke RJ, Rasmussen HH (2005) The nitric oxide donor sodium nitroprusside stimulates the Na+ -K+ pump in isolated rabbit cardiac myocytes. J Physiol 565:815-825
68. Wood BL, Gibson DF, Tait JF (1996) Increased erythrocyte phosphatidylserine exposure in sickle cell disease: flow-cytometric measurement and clinical associations. Blood 88:1873-1880
69. Woon LA, Holland JW, Kable EP, Roufogalis BD (1999) Ca2+ sensitivity of phospholipid scrambling in human red cell ghosts. Cell Calcium 25:313-320
70. Yang BC, Nichols WW, Mehta JL (1996) Cardioprotective effects of red blood cells on ischemia and reperfusion injury in isolated rat heart: release of nitric oxide as a potential mechanism. J Cardiovasc Pharmacol Ther 1:297-306
71. Zhuravliova E, Barbakadze T, Narmania N, Ramsden J, Mikeladze D (2007) Inhibition of nitric oxide synthase and farnesyltransferase change the activities of several transcription factors. J Mol Neurosci 31:281-287
72. Zwaal RF, Comfurius P, Bevers EM (2005) Surface exposure of phosphatidylserine in pathological cells. Cell Mol Life Sci 62:971-988