Enhanced eryptosis of erythrocytes from gene-targeted mice lacking annexin A7

Pflugers Archiv European Journal of Physiology

Volumn 460, Issue 3, 2010, Pages 667-676

  Lang, Elisabeth ^a   Lang, Philipp A ^a   Shumilina, Ekaterina ^a   Qadri, Syed M ^a   Kucherenko, Yuliya ^a   Kempe, Daniela S ^a   Föller, Michael ^a   Capasso, Anna ^a   Wieder, Thomas ^a   Gulbins, Erich ^b   Clemen, Christoph S ^c   Herr, Claudia ^c   Noegel, Angelika A ^c   Huber, Stephan M ^a   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b UNIVERSITY OF DUISBURG ESSEN   (Germany)

^c UNIVERSITY OF COLOGNE   (Germany)

Author keywords

Annexin; Cell volume; Energy depletion; Osmolarity; Phosphatidylserine

Indexed keywords

LIPOCORTIN 5; SYNEXIN; ANXA7 PROTEIN, MOUSE; CHLORIDE;

ANIMAL CELL; ARTICLE; BASOPHIL; CELL MEMBRANE; CELL MEMBRANE PERMEABILITY; CELL VOLUME; CONTROLLED STUDY; EOSINOPHIL; ERYPTOSIS; ERYTHROCYTE DISORDER; ERYTHROCYTE MEMBRANE; FLUORESCENCE ACTIVATED CELL SORTER; MOUSE; NEUTROPHIL; NONHUMAN; OSMOTIC STRESS; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; SIGNAL TRANSDUCTION; ANIMAL; CELL DEATH; ENERGY METABOLISM; ERYTHROCYTE; KNOCKOUT MOUSE; OSMOTIC PRESSURE; PHYSIOLOGY;

ANIMALS; ANNEXIN A7; CELL DEATH; CHLORIDES; ENERGY METABOLISM; ERYTHROCYTES; MICE; MICE, KNOCKOUT; OSMOTIC PRESSURE;

EID: 77955471995     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-010-0829-x     Document Type: Article

References (56)

1. SM Ali MJ Geisow RD Burgoyne 1989 A role for calpactin in calcium-dependent exocytosis in adrenal chromaffin cells Nature 340 313 315 10.1038/340313a0 1:CAS:528:DyaL1MXlt1Omt7w%3D 2526299 (Pubitemid 19189693)
2. HA Andree CP Reutelingsperger R Hauptmann HC Hemker WT Hermens GM Willems 1990 Binding of vascular anticoagulant alpha (VAC alpha) to planar phospholipid bilayers J Biol Chem 265 4923 4928 1:CAS:528:DyaK3cXhvFCjtbw%3D 2138622
3. DA Andrews L Yang PS Low 2002 Phorbol ester stimulates a protein kinase C-mediated agatoxin-TK-sensitive calcium permeability pathway in human red blood cells Blood 100 3392 3399 10.1182/blood.V100.9.3392 1:CAS:528: DC%2BD38XosVSit70%3D 12384442 (Pubitemid 35217092)
4. CP Berg IH Engels A Rothbart K Lauber A Renz SF Schlosser K Schulze-Osthoff S Wesselborg 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 10.1038/sj.cdd.4400905 1:CAS:528:DC%2BD38XmtVKlug%3D%3D 11753567 (Pubitemid 34048474)
5. FE Boas L Forman E Beutler 1998 Phosphatidylserine exposure and red cell viability in red cell aging and in hemolytic anemia Proc Natl Acad Sci USA 95 3077 3081 10.1073/pnas.95.6.3077 1:CAS:528:DyaK1cXitV2itrg%3D 9501218 (Pubitemid 28135857)
6. RM Bookchin OE Ortiz VL Lew 1987 Activation of calcium-dependent potassium channels in deoxygenated sickled red cells Prog Clin Biol Res 240 193 200 1:STN:280:DyaL2s3ovF2huw%3D%3D 2441414
7. V Brand S Koka C Lang V Jendrossek SM Huber E Gulbins F Lang 2008 Influence of amitriptyline on eryptosis, parasitemia and survival of Plasmodium berghei-infected mice Cell Physiol Biochem 22 405 412 10.1159/000185482 1:CAS:528:DC%2BD1cXhsV2lt7bM 19088422
8. D Bratosin J Estaquier F Petit D Arnoult B Quatannens JP Tissier C Slomianny C Sartiaux C Alonso JJ Huart J Montreuil JC Ameisen 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 10.1038/sj.cdd.4400946 1:CAS:528:DC%2BD38XmtVKltg%3D%3D 11753563 (Pubitemid 34048470)
9. C Brugnara L de Franceschi SL Alper 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 10.1172/JCI116597 1:CAS:528:DyaK3sXlsleru70%3D 8326017
10. H Caohuy M Srivastava HB Pollard 1996 Membrane fusion protein synexin (annexin VII) as a Ca2+/GTP sensor in exocytotic secretion Proc Natl Acad Sci USA 93 10797 10802 10.1073/pnas.93.20.10797 1:CAS:528:DyaK28XmtVOltbs%3D 8855260 (Pubitemid 26333069)
11. CS Clemen C Herr N Hovelmeyer AA Noegel 2003 The lack of annexin A7 affects functions of primary astrocytes Exp Cell Res 291 406 414 10.1016/j.yexcr.2003.07.012 1:CAS:528:DC%2BD3sXpsVSht70%3D 14644162 (Pubitemid 37485728)
12. CS Clemen A Hofmann C Zamparelli AA Noegel 1999 Expression and localisation of annexin VII (synexin) isoforms in differentiating myoblasts J Muscle Res Cell Motil 20 669 679 10.1023/A:1005524623337 1:CAS:528: DC%2BD3cXht1Cmurg%3D 10672515 (Pubitemid 30068172)
13. E Daugas C Cande G Kroemer 2001 Erythrocytes: death of a mummy Cell Death Differ 8 1131 1133 10.1038/sj.cdd.4400953 1:STN:280:DC%2BD38%2Fgt1WitQ%3D%3D 11753560 (Pubitemid 34048467)
14. DW Dekkers P Comfurius EM Bevers RF Zwaal 2002 Comparison between Ca2+-induced scrambling of various fluorescently labelled lipid analogues in red blood cells Biochem J 362 741 747 10.1042/0264-6021:3620741 1:CAS:528:DC%2BD2cXit1Kg 11879203 (Pubitemid 34242327)
15. DS Drust CE Creutz 1988 Aggregation of chromaffin granules by calpactin at micromolar levels of calcium Nature 331 88 91 10.1038/331088a0 1:CAS:528:DyaL1cXht1KqtbY%3D 2963226 (Pubitemid 18053425)
16. C Duranton S Huber V Tanneur K Lang V Brand C Sandu F Lang 2003 Electrophysiological properties of the Plasmodium falciparum-induced cation conductance of human erythrocytes Cell Physiol Biochem 13 189 198 10.1159/000072421 1:CAS:528:DC%2BD3sXls1ajur4%3D 12876376 (Pubitemid 36921037)
17. C Duranton SM Huber F Lang 2002 Oxidation induces a Cl(-)-dependent cation conductance in human red blood cells J Physiol 539 847 855 10.1113/jphysiol.2001.013040 1:CAS:528:DC%2BD38Xjt1ejs7o%3D 11897854 (Pubitemid 35175434)
18. S Eda IW Sherman 2002 Cytoadherence of malaria-infected red blood cells involves exposure of phosphatidylserine Cell Physiol Biochem 12 373 384 10.1159/000067908 1:CAS:528:DC%2BD38XoslOqs7Y%3D 12438774 (Pubitemid 35356713)
19. N Emans JP Gorvel C Walter V Gerke R Kellner G Griffiths J Gruenberg 1993 Annexin II is a major component of fusogenic endosomal vesicles J Cell Biol 120 1357 1369 10.1083/jcb.120.6.1357 1:CAS:528:DyaK3sXps1Cisw%3D%3D 8449982
20. VA Fadok DL Bratton DM Rose A Pearson RA Ezekewitz PM Henson 2000 A receptor for phosphatidylserine-specific clearance of apoptotic cells Nature 405 85 90 10.1038/35011084 1:CAS:528:DC%2BD3cXjt1yitb0%3D 10811223 (Pubitemid 30321820)
21. M Foller D Bobbala S Koka SM Huber E Gulbins F Lang 2009 Suicide for survival-death of infected erythrocytes as a host mechanism to survive malaria Cell Physiol Biochem 24 133 140 10.1159/000233238 19710527
22. M Foller RS Kasinathan S Koka C Lang E Shumilina L Birnbaumer F Lang SM Huber 2008 TRPC6 contributes to the Ca(2+) leak of human erythrocytes Cell Physiol Biochem 21 183 192 10.1159/000113760 18209485
23. JR Glenney Jr 1987 Calpactins: calcium-regulated membrane-skeletal proteins Biochem Soc Trans 15 798 800 1:CAS:528:DyaL2sXkvFajsro%3D 2961637
24. DR Green JC Reed 1998 Mitochondria and apoptosis Science 281 1309 1312 10.1126/science.281.5381.1309 1:CAS:528:DyaK1cXlvVegsLo%3D 9721092
25. E Gulbins A Jekle K Ferlinz H Grassme F Lang 2000 Physiology of apoptosis Am J Physiol Renal Physiol 279 F605 F615 1:CAS:528:DC%2BD3cXns1egurs%3D 10997910
26. PM Henson DL Bratton VA Fadok 2001 The phosphatidylserine receptor: a crucial molecular switch? Nat Rev Mol Cell Biol 2 627 633 10.1038/35085094 1:CAS:528:DC%2BD3MXlvVOqsLs%3D 11483996 (Pubitemid 33674014)
27. C Herr CS Clemen G Lehnert R Kutschkow SM Picker BS Gathof C Zamparelli M Schleicher AA Noegel 2003 Function, expression and localization of annexin A7 in platelets and red blood cells: insights derived from an annexin A7 mutant mouse BMC Biochem 4 8 10.1186/1471-2091-4-8 12925238
28. C Herr N Smyth S Ullrich F Yun P Sasse J Hescheler B Fleischmann K Lasek K Brixius RH Schwinger R Fassler R Schroder AA Noegel 2001 Loss of annexin A7 leads to alterations in frequency-induced shortening of isolated murine cardiomyocytes Mol Cell Biol 21 4119 4128 10.1128/MCB.21.13.4119-4128.2001 1:CAS:528:DC%2BD3MXksVOrtr8%3D 11390641 (Pubitemid 32565294)
29. R Huber J Romisch EP Paques 1990 The crystal and molecular structure of human annexin V, an anticoagulant protein that binds to calcium and membranes EMBO J 9 3867 3874 1:CAS:528:DyaK3MXnslamsA%3D%3D 2147412
30. SM Huber N Gamper F Lang 2001 Chloride conductance and volume-regulatory nonselective cation conductance in human red blood cell ghosts Pflugers Arch 441 551 558 10.1007/s004240000456 1:CAS:528:DC%2BD3MXlt1Ogtw%3D%3D 11212220 (Pubitemid 32128152)
31. BA Klarl PA Lang DS Kempe OM Niemoeller A Akel M Sobiesiak K Eisele M Podolski SM Huber T Wieder F Lang 2006 Protein kinase C mediates erythrocyte "programmed cell death" following glucose depletion Am J Physiol Cell Physiol 290 C244 C253 10.1152/ajpcell.00283.2005 1:CAS:528:DC%2BD28XhsVSju7Y%3D 16338977
32. S Koka D Bobbala C Lang KM Boini SM Huber F Lang 2009 Influence of paclitaxel on parasitemia and survival of Plasmodium berghei infected mice Cell Physiol Biochem 23 191 198 10.1159/000204107 1:CAS:528:DC%2BD1MXitVGjtbY%3D 19255513
33. S Koka C Lang KM Boini D Bobbala SM Huber F Lang 2008 Influence of chlorpromazine on eryptosis, parasitemia and survival of Plasmodium berghe infected mice Cell Physiol Biochem 22 261 268 10.1159/000149804 1:CAS:528:DC%2BD1cXhtVKlsL7L 18769053
34. S Koka C Lang OM Niemoeller KM Boini JP Nicolay SM Huber F Lang 2008 Influence of NO synthase inhibitor L-NAME on parasitemia and survival of Plasmodium berghei infected mice Cell Physiol Biochem 21 481 488 10.1159/000129641 1:CAS:528:DC%2BD1cXltFOrtL4%3D 18453756 (Pubitemid 351620302)
35. GA Kuijpers G Lee HB Pollard 1992 Immunolocalization of synexin (annexin VII) in adrenal chromaffin granules and chromaffin cells: evidence for a dynamic role in the secretory process Cell Tissue Res 269 323 330 10.1007/BF00319624 1:CAS:528:DyaK38XlsVOktb0%3D 1423500
36. F Lang E Gulbins H Lerche SM Huber DS Kempe M Foller 2008 Eryptosis, a window to systemic disease Cell Physiol Biochem 22 373 380 10.1159/000185448 1:CAS:528:DC%2BD1cXhsV2lt7nK 19088418
37. KS Lang C Duranton H Poehlmann S Myssina C Bauer F Lang T Wieder SM Huber 2003 Cation channels trigger apoptotic death of erythrocytes Cell Death Differ 10 249 256 10.1038/sj.cdd.4401144 1:CAS:528:DC%2BD3sXivFGhtrY%3D 12700653 (Pubitemid 36553467)
38. KS Lang S Myssina V Brand C Sandu PA Lang S Berchtold SM Huber F Lang T Wieder 2004 Involvement of ceramide in hyperosmotic shock-induced death of erythrocytes Cell Death Differ 11 231 243 10.1038/sj.cdd.4401311 1:CAS:528:DC%2BD2cXkt1KmtA%3D%3D 14615798 (Pubitemid 38159647)
39. KS Lang B Roll S Myssina M Schittenhelm HG Scheel-Walter L Kanz J Fritz F Lang SM Huber T Wieder 2002 Enhanced erythrocyte apoptosis in sickle cell anemia, thalassemia and glucose-6-phosphate dehydrogenase deficiency Cell Physiol Biochem 12 365 372 10.1159/000067907 1:CAS:528:DC%2BD38XoslOqs7k%3D 12438773 (Pubitemid 35356712)
40. PA Lang RS Kasinathan VB Brand C Duranton C Lang S Koka E Shumilina DS Kempe V Tanneur A Akel KS Lang M Föller JFJ Kun PG Kremsner S Wesselborg S Laufer CS Clemen C Herr AA Noegel T Wieder E Gulbins F Lang SM Huber 2009 Accelerated clearance of Plasmodium-infected erythrocytes in sickle cell trait and annexin-A7 deficiency Cell Physiol Biochem 24 5-6 415 428 10.1159/000257529 1:CAS:528:DC%2BD1MXhsVSktrzE 19910682
41. PA Lang S Kaiser S Myssina T Wieder F Lang SM Huber 2003 Role of Ca2+-activated K+ channels in human erythrocyte apoptosis Am J Physiol Cell Physiol 285 C1553 C1560 1:CAS:528:DC%2BD2cXhtlWh 14600080
42. PA Lang DS Kempe S Myssina V Tanneur C Birka S Laufer F Lang T Wieder SM Huber 2005 PGE(2) in the regulation of programmed erythrocyte death Cell Death Differ 12 415 428 10.1038/sj.cdd.4401561 1:CAS:528:DC%2BD2MXkvVSrt7s%3D 15746942 (Pubitemid 40662840)
43. PA Lang U Warskulat B Heller-Stilb DY Huang A Grenz S Myssina M Duszenko F Lang D Haussinger V Vallon T Wieder 2003 Blunted apoptosis of erythrocytes from taurine transporter deficient mice Cell Physiol Biochem 13 337 346 10.1159/000075121 1:CAS:528:DC%2BD3sXptV2ksr0%3D 14631140 (Pubitemid 37465149)
44. H Mahmud D Mauro SM Qadri M Foller F Lang 2009 Triggering of suicidal erythrocyte death by amphotericin B Cell Physiol Biochem 24 263 270 10.1159/000233251 1:CAS:528:DC%2BD1MXpsVaks7s%3D 19710541
45. UK Messmer J Pfeilschifter 2000 New insights into the mechanism for clearance of apoptotic cells Bioessays 22 878 881 10.1002/1521-1878(200010)22: 10<878::AID-BIES2>3.0.CO;2-J 1:CAS:528:DC%2BD3MXmslShsb8%3D 10984713
46. K Monastyrskaya EB Babiychuk A Draeger 2009 The annexins: spatial and temporal coordination of signaling events during cellular stress Cell Mol Life Sci 66 2623 2642 10.1007/s00018-009-0027-1 1:CAS:528:DC%2BD1MXovFOks70%3D 19381436
47. K Monastyrskaya EB Babiychuk A Hostettler P Wood T Grewal A Draeger 2009 Plasma membrane-associated annexin A6 reduces Ca2+ entry by stabilizing the cortical actin cytoskeleton J Biol Chem 284 17227 17242 10.1074/jbc.M109.004457 1:CAS:528:DC%2BD1MXntFCjtb8%3D 19386597
48. OM Niemoeller M Foller C Lang SM Huber F Lang 2008 Retinoic acid induced suicidal erythrocyte death Cell Physiol Biochem 21 193 202 10.1159/000113761 1:CAS:528:DC%2BD1cXps1ajtQ%3D%3D 18209486
49. OM Niemoeller H Mahmud M Foller T Wieder F Lang 2008 Ciglitazone and 15d-PGJ2 induced suicidal erythrocyte death Cell Physiol Biochem 22 237 244 10.1159/000149801 1:CAS:528:DC%2BD1cXhtVKlsL7I 18769050
50. P Raynal HB Pollard 1994 Annexins: the problem of assessing the biological role for a gene family of multifunctional calcium- and phospholipid-binding proteins Biochim Biophys Acta 1197 63 93 1:CAS:528:DyaK2cXivFahsro%3D 8155692
51. F Russo-Marie 1992 Macrophages and the glucocorticoids J Neuroimmunol 40 281 286 10.1016/0165-5728(92)90144-A 1:CAS:528:DyaK3sXhs1ektA%3D%3D 1430158
52. M Sopjani M Foller P Dreischer F Lang 2008 Stimulation of eryptosis by cadmium ions Cell Physiol Biochem 22 245 252 10.1159/000149802 1:CAS:528:DC%2BD1cXhtVKlsL7J 18769051
53. M Srivastava I Atwater M Glasman X Leighton G Goping H Caohuy G Miller J Pichel H Westphal D Mears E Rojas HB Pollard 1999 Defects in inositol 1,4,5-trisphosphate receptor expression, Ca(2+) signaling, and insulin secretion in the anx7(+/-) knockout mouse Proc Natl Acad Sci USA 96 13783 13788 10.1073/pnas.96.24.13783 1:CAS:528:DyaK1MXns1Oqt78%3D 10570150
54. K Wang H Mahmud M Foller R Biswas KS Lang E Bohn F Gotz F Lang 2008 Lipopeptides in the triggering of erythrocyte cell membrane scrambling Cell Physiol Biochem 22 381 386 10.1159/000187116 1:CAS:528:DC%2BD1cXhsV2lt7nL 19088419
55. LA Woon JW Holland EP Kable BD Roufogalis 1999 Ca2+ sensitivity of phospholipid scrambling in human red cell ghosts Cell Calcium 25 313 320 10.1054/ceca.1999.0029 1:CAS:528:DyaK1MXks1Krt7o%3D 10456228 (Pubitemid 29353720)
56. H Yoshizaki S Tanabe K Arai A Murakami Y Wada M Ohkuchi Y Hashimoto M Maki 1992 Effects of calphobindin II (annexin VI) on procoagulant and anticoagulant activities of cultured endothelial cells Chem Pharm Bull (Tokyo) 40 1860 1863 1:CAS:528:DyaK38XmsVGhur0%3D