Reduced Ca2+ entry and suicidal death of erythrocytes in PDK1 hypomorphic mice

Pflugers Archiv European Journal of Physiology

Volumn 455, Issue 5, 2008, Pages 939-949

  Föller, Michael ^a   Mahmud, Hasan ^a   Koka, Saisudha ^a   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

Author keywords

Apoptosis; Ca2+ channels; Cell volume; Eryptosis; Phosphatidylserine

Indexed keywords

CALCIUM ION; CALCIUM IONOPHORE; CATION CHANNEL; CHLORIDE; FLUORESCENT DYE; IONOMYCIN; LIPOCORTIN 5; PHOSPHATIDYLSERINE; PHOSPHOINOSITIDE DEPENDENT KINASE 1; PHOSPHOTRANSFERASE; SUCROSE; TERT BUTYL HYDROPEROXIDE; UNCLASSIFIED DRUG; CALCIUM; HEMOGLOBIN; ION CHANNEL; PROTEIN SERINE THREONINE KINASE; PYRUVATE DEHYDROGENASE (ACETYL TRANSFERRING) KINASE; PYRUVATE DEHYDROGENASE (ACETYL-TRANSFERRING) KINASE;

ANIMAL CELL; ARTICLE; CALCIUM CELL LEVEL; CALCIUM TRANSPORT; CELL DEATH; CELL MEMBRANE PERMEABILITY; CONTROLLED STUDY; CYTOSOL; ERYTHROCYTE LIFESPAN; ERYTHROCYTE MEMBRANE; ERYTHROCYTE VOLUME; GENE EXPRESSION; MOUSE; NONHUMAN; OSMOTIC STRESS; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN BINDING; WILD TYPE; ANIMAL; APOPTOSIS; CYTOLOGY; ERYTHROCYTE; ERYTHROCYTE COUNT; FLOW CYTOMETRY; GENETICS; MEAN CORPUSCULAR VOLUME; METABOLISM; MOUSE MUTANT; OSMOTIC PRESSURE; PHYSIOLOGY; RETICULOCYTE COUNT;

ANIMALS; APOPTOSIS; CALCIUM; CHLORIDES; ERYTHROCYTE COUNT; ERYTHROCYTE INDICES; ERYTHROCYTE VOLUME; ERYTHROCYTES; FLOW CYTOMETRY; HEMOGLOBINS; ION CHANNELS; MICE; MICE, MUTANT STRAINS; OSMOTIC PRESSURE; OXIDATIVE STRESS; PROTEIN-SERINE-THREONINE KINASES; RETICULOCYTE COUNT;

EID: 37249031439     PISSN: 00316768     EISSN: 14322013     Source Type: Journal    
DOI: 10.1007/s00424-007-0336-x     Document Type: Article

References (74)

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. Albright CD, da Costa KA, Craciunescu CN, Klem E, Mar MH, Zeisel SH (2005) Regulation of choline deficiency apoptosis by epidermal growth factor in CWSV-1 rat hepatocytes. Cell Physiol Biochem 15:59-68
3. Alessi DR, Andjelkovic M, Caudwell B, Cron P, Morrice N, Cohen P, Hemmings BA (1996) Mechanism of activation of protein kinase B by insulin and IGF-1. EMBO J 15:6541-6551
4. Alessi DR, Cohen P (1998) Mechanism of activation and function of protein kinase B. Curr Opin Genet Dev 8:55-62
5. Alisi A, Demori I, Spagnuolo S, Pierantozzi E, Fugassa E, Leoni S (2005) Thyroid status affects rat liver regeneration after partial hepatectomy by regulating cell cycle and apoptosis. Cell Physiol Biochem 15:69-76
6. Artunc F, Rexhepaj R, Volkl H, Grahammer F, Remy C, Sandulache D, Nasir O, Wagner CA, Alessi DR, Lang F (2006) Impaired intestinal and renal glucose transport in PDK-1 hypomorphic mice. Am J Physiol Regul Integr Comp Physiol 291:R1533-R1538
7. Bankers-Fulbright JL, Kephart GM, Loegering DA, Bradford AL, Okada S, Kita H, Gleich GJ (1998) Sulfonylureas inhibit cytokine-induced eosinophil survival and activation. J Immunol 160:5546-5553
8. Barvitenko NN, Adragna NC, Weber RE (2005) Erythrocyte signal transduction pathways, their oxygenation dependence and functional significance. Cell Physiol Biochem 15:1-18
9. Benson RS, Heer S, Dive C, Watson AJ (1996) Characterization of cell volume loss in CEM-C7A cells during dexamethasone-induced apoptosis. Am J Physiol 270:C1190-C1203
10. Bergamo P, Luongo D, Rossi M (2004) Conjugated linoleic acid-mediated apoptosis in Jurkat T cells involves the production of reactive oxygen species. Cell Physiol Biochem 14:57-64
11. 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
12. Bortner CD, Cidlowski JA (1999) Caspase independent/dependent regulation of K(+), cell shrinkage, and mitochondrial membrane potential during lymphocyte apoptosis. J Biol Chem 274:21953-21962
13. Bosman GJ, Willekens FL, Werre JM (2005) Erythrocyte aging: a more than superficial resemblance to apoptosis? Cell Physiol Biochem 16:1-8
14. 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
15. 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
16. Chin LS, Park CC, Zitnay KM, Sinha M, DiPatri AJ Jr., Perillan P, Simard JM (1997) 4-Aminopyridine causes apoptosis and blocks an outward rectifier K+ channel in malignant astrocytoma cell lines. J Neurosci Res 48:122-127
17. Coffer PJ, Jin J, Woodgett JR (1998) Protein kinase B (c-Akt): a multifunctional mediator of phosphatidylinositol 3-kinase activation. Biochem J 335(Pt 1):1-13
18. Coffer PJ, Woodgett JR (1991) Molecular cloning and characterisation of a novel putative protein-serine kinase related to the cAMP-dependent and protein kinase C families. Eur J Biochem 201:475-481
19. Colom LV, Diaz ME, Beers DR, Neely A, Xie WJ, Appel SH (1998) Role of potassium channels in amyloid-induced cell death. J Neurochem 70:1925-1934
20. Dallaporta B, Hirsch T, Susin SA, Zamzami N, Larochette N, Brenner C, Marzo I, Kroemer G (1998) Potassium leakage during the apoptotic degradation phase. J Immunol 160:5605-5615
21. Dangel GR, Lang F, Lepple-Wienhues A (2005) Effect of sphingosine on Ca2+ entry and mitochondrial potential of Jurkat T cells-interaction with Bcl2. Cell Physiol Biochem 16:9-14
22. Daugas E, Cande C, Kroemer G (2001) Erythrocytes: death of a mummy. Cell Death Differ 8:1131-1133
23. Dekkers DW, Comfurius P, Bevers EM, Zwaal RF (2002) Comparison between Ca2+-induced scrambling of various fluorescently labelled lipid analogues in red blood cells. Biochem J 362:741-747
24. Duranton C, Huber SM, Lang F (2002) Oxidation induces a Cl(-)-dependent cation conductance in human red blood cells. J Physiol 539:847-855
25. 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
26. Erdo S, Michler A, Wolff JR (1991) GABA accelerates excitotoxic cell death in cortical cultures: protection by blockers of GABA-gated chloride channels. Brain Res 542:254-258
27. Firestone GL, Giampaolo JR, OKeeffe BA (2003) Stimulus-dependent regulation of serum and glucocorticoid inducible protein kinase (SGK) transcription, subcellular localization and enzymatic activity. Cell Physiol Biochem 13:1-12
28. Föller M, Kasinathan RS, Koka S, Lang C, Shumilina E, Birnbaumer L, Lang F, Huber SM (2007) TRPC6 contributes to the Ca2+ leak of human erythrocytes. Cell Physiol Biochem (in press)
29. Gantner F, Uhlig S, Wendel A (1995) Quinine inhibits release of tumor necrosis factor, apoptosis, necrosis and mortality in a murine model of septic liver failure. Eur J Pharmacol 294:353-355
30. Gomez-Angelats M, Bortner CD, Cidlowski JA (2000) Protein kinase C (PKC) inhibits fas receptor-induced apoptosis through modulation of the loss of K+ and cell shrinkage. A role for PKC upstream of caspases. J Biol Chem 275:19609-19619
31. Gulbins E, Jekle A, Ferlinz K, Grassme H, Lang F (2000) Physiology of apoptosis. Am J Physiol Renal Physiol 279:F605-F615
32. Kaestner L, Bernhardt I (2002) Ion channels in the human red blood cell membrane: their further investigation and physiological relevance. Bioelectrochemistry 55:71-74
33. Kaestner L, Bollensdorff C, Bernhardt I (1999) Non-selective voltage-activated cation channel in the human red blood cell membrane. Biochim Biophys Acta 1417:9-15
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. Kobayashi T, Deak M, Morrice N, Cohen P (1999) Characterization of the structure and regulation of two novel isoforms of serum- and glucocorticoid-induced protein kinase. Biochem J 344 Pt 1:189-197
38. Lang F, Bohmer C, Palmada M, Seebohm G, Strutz-Seebohm N, Vallon V (2006) (Patho)physiological significance of the serum- and glucocorticoid-inducible kinase isoforms. Physiol Rev 86:1151-1178
39. Lang F, Cohen P (2001) Regulation and physiological roles of serum- and glucocorticoid-induced protein kinase isoforms. Sci STKE 2001:RE17
40. Lang KS, Duranton C, Poehlmann H, Myssina S, Bauer C, Lang F, Wieder T, Huber SM (2003) Cation channels trigger apoptotic death of erythorcytes. Cell Death Differ 10:249-256
41. 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
42. 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
43. 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
44. 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
45. 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
46. 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
47. 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
48. 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
49. 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
50. Lawlor MA, Mora A, Ashby PR, Williams MR, Murray-Tait V, Malone L, Prescott AR, Lucocq JM, Alessi DR (2002) Essential role of PDK1 in regulating cell size and development in mice. EMBO J 21:3728-3738
51. Liu XH, Kirschenbaum A, Yu K, Yao S, Levine AC (2005) Cyclooxygenase-2 suppresses hypoxia-induced apoptosis via a combination of direct and indirect inhibition of p53 activity in a human prostate cancer cell line. J Biol Chem 280:3817-3823
52. Michea L, Ferguson DR, Peters EM, Andrews PM, Kirby MR, Burg MB (2000) Cell cycle delay and apoptosis are induced by high salt and urea in renal medullary cells. Am J Physiol Renal Physiol 278:F209-F218
53. Myssina S, Lang PA, Kempe DS, Kaiser S, Huber SM, Wieder T, Lang F (2004) Cl- channel blockers NPPB and niflumic acid blunt Ca(2+)-induced erythrocyte 'apoptosis'. Cell Physiol Biochem 14:241-248
54. Nicolay JP, Schneider J, Niemoeller OM, Artunc F, Portero-Otin M, Haik G Jr, Thornalley PJ, Schleicher E, Wieder T, Lang F (2006) Stimulation of suicidal erythrocyte death by methylglyoxal. Cell Physiol Biochem 18:223-232
55. Offen D, Ziv I, Gorodin S, Barzilai A, Malik Z, Melamed E (1995) Dopamine-induced programmed cell death in mouse thymocytes. Biochim Biophys Acta 1268:171-177
56. Okada Y, Maeno E, Shimizu T, Dezaki K, Wang J, Morishima S (2001) Receptor-mediated control of regulatory volume decrease (RVD) and apoptotic volume decrease (AVD). J Physiol 532:3-16
57. Pal S, He K, Aizenman E (2004) Nitrosative stress and potassium channel-mediated neuronal apoptosis: is zinc the link? Pflugers Arch 448:296-303
58. Palmada M, Poppendieck S, Embark HM, van de Graaf SF, Boehmer C, Bindels RJ, Lang F (2005) Requirement of PDZ domains for the stimulation of the epithelial Ca2+ channel TRPV5 by the NHE regulating factor NHERF2 and the serum and glucocorticoid inducible kinase SGK1. Cell Physiol Biochem 15:175-182
59. Prehn JH, Jordan J, Ghadge GD, Preis E, Galindo MF, Roos RP, Krieglstein J, Miller RJ (1997) Ca2+ and reactive oxygen species in staurosporine-induced neuronal apoptosis. J Neurochem 68:1679-1685
60. Rexhepaj R, Grahammer F, Volkl H, Remy C, Wagner CA, Sandulache D, Artunc F, Henke G, Nammi S, Capasso G, Alessi DR, Lang F (2006) Reduced intestinal and renal amino acid transport in PDK1 hypomorphic mice. FASEB J 20:2214-2222
61. Rice L, Alfrey CP (2005) The negative regulation of red cell mass by neocytolysis: physiologic and pathophysiologic manifestations. Cell Physiol Biochem 15:245-250
62. Rosette C, Karin M (1996) Ultraviolet light and osmotic stress: activation of the JNK cascade through multiple growth factor and cytokine receptors. Science 274:1194-1197
63. Rotoli BM, Uggeri J, Dall'Asta V, Visigalli R, Barilli A, Gatti R, Orlandini G, Gazzola GC, Bussolati O (2005) Inhibition of glutamine synthetase triggers apoptosis in asparaginase-resistant cells. Cell Physiol Biochem 15:281-292
64. Salido M, Vilches J, Lopez A, Roomans GM (2001) X-ray microanalysis of etoposide-induced apoptosis in the PC-3 prostatic cancer cell line. Cell Biol Int 25:499-508
65. Sandu C, Artunc F, Palmada M, Rexhepaj R, Grahammer F, Hussain A, Yun C, Alessi DR, Lang F (2006) Impaired intestinal NHE3 activity in the PDK1 hypomorphic mouse. Am J Physiol Gastrointest Liver Physiol 291:G868-G876
66. 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
67. Storey NM, Gomez-Angelats M, Bortner CD, Armstrong DL, Cidlowski JA (2003) Stimulation of Kv1.3 potassium channels by death receptors during apoptosis in Jurkat T lymphocytes. J Biol Chem 278:33319-33326
68. Sturm JW, Zhang H, Magdeburg R, Hasenberg T, Bonninghoff R, Oulmi J, Keese M, McCuskey R (2004) Altered apoptotic response and different liver structure during liver regeneration in FGF-2-deficient mice. Cell Physiol Biochem 14:249-260
69. Takahashi N, Wang X, Tanabe S, Uramoto H, Jishage K, Uchida S, Sasaki S, Okada Y (2005) ClC-3-independent sensitivity of apoptosis to Cl- channel blockers in mouse cardiomyocytes. Cell Physiol Biochem 15:263-270
70. Wang Z (2004) Roles of K+ channels in regulating tumour cell proliferation and apoptosis. Pflugers Arch 448:274-286
71. Wenzel U, Daniel H (2004) Early and late apoptosis events in human transformed and non-transformed colonocytes are independent on intracellular acidification. Cell Physiol Biochem 14:65-76
72. Woon LA, Holland JW, Kable EP, Roufogalis BD (1999) Ca2+ sensitivity of phospholipid scrambling in human red cell ghosts. Cell Calcium 25:313-320
73. Yurinskaya V, Goryachaya T, Guzhova I, Moshkov A, Rozanov Y, Sakuta G, Shirokova A, Shumilina E, Vassilieva I, Lang F, Vereninov A (2005) Potassium and sodium balance in U937 cells during apoptosis with and without cell shrinkage. Cell Physiol Biochem 16:155-162
74. Yurinskaya VE, Moshkov AV, Rozanov YM, Shirokova AV, Vassilieva IO, Shumilina EV, Lang F, Volgareva EV, Vereninov AA (2005) Thymocyte K+, Na+ and water balance during dexamethasone- and etoposide-induced apoptosis. Cell Physiol Biochem 16:15-22