Regulation of erythrocyte survival by AMP-activated protein kinase

FASEB Journal

Volumn 23, Issue 4, 2009, Pages 1072-1080

  Föller, Michael ^a   Sopjani, Mentor ^a   Koka, Saisudha ^a   Gu, Shuchen ^a   Mahmud, Hasan ^a   Wang, Kan ^a   Floride, Elisa ^a   Schleicher, Erwin ^a   Schulz, Eberhard ^b   Münzel, Thomas ^b   Lang, Florian ^a  

^a UNIVERSITY OF TÜBINGEN   (Germany)

^b JOHANNES GUTENBERG UNIVERSITY   (Germany)

Author keywords

Annexin; Calcium; Cell volume; Eryptosis; Phosphatidylserine

Indexed keywords

5 AMINO 4 IMIDAZOLECARBOXAMIDE RIBOSIDE; CALCIUM; CALCIUM IONOPHORE; FLUO 3; GLUCOSE; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE INHIBITOR; HYDROXYMETHYLGLUTARYL COENZYME A REDUCTASE KINASE; IONOMYCIN; LIPOCORTIN 5; PHOSPHATIDYLSERINE; (6 (4 (2 PIPERIDIN 1 YLETHOXY)PHENYL)) 3 PYRIDIN 4 YLPYRAZOLO(1,5 A)PYRIMIDINE; (6-(4-(2-PIPERIDIN-1-YLETHOXY)PHENYL))-3-PYRIDIN-4-YLPYRAZOLO(1,5-A)PYRIMIDINE; 5 AMINO 4 IMIDAZOLECARBOXAMIDE; AICA RIBONUCLEOTIDE; DRUG DERIVATIVE; FLUORESCEIN ISOTHIOCYANATE; FLUORESCENT DYE; IONOPHORE; PYRAZOLE DERIVATIVE; PYRIMIDINE DERIVATIVE; RIBONUCLEOTIDE;

ANEMIA; ANIMAL CELL; ARTICLE; CALCIUM TRANSPORT; CELL DEATH; CELL ENERGY; COMPARATIVE STUDY; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DISEASE PREDISPOSITION; ERYPTOSIS; ERYTHROCYTE LIFESPAN; ERYTHROCYTE VOLUME; FLUORESCENCE ACTIVATED CELL SORTING; HUMAN; HUMAN CELL; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; REGULATORY MECHANISM; RETICULOCYTOSIS; SPLENOMEGALY; WESTERN BLOTTING; WILD TYPE; ANIMAL; CELL SIZE; CYTOSOL; DRUG ANTAGONISM; DRUG EFFECT; ERYTHROCYTE; ERYTHROCYTE MEMBRANE; METABOLISM; MOUSE MUTANT; PHYSIOLOGY;

MUS;

AMINOIMIDAZOLE CARBOXAMIDE; AMP-ACTIVATED PROTEIN KINASES; ANIMALS; ANNEXIN A5; CALCIUM; CELL SIZE; CYTOSOL; ERYTHROCYTE AGING; ERYTHROCYTE MEMBRANE; ERYTHROCYTES; FLUORESCEIN-5-ISOTHIOCYANATE; FLUORESCENT DYES; GLUCOSE; HUMANS; IONOMYCIN; IONOPHORES; MALE; MICE; MICE, MUTANT STRAINS; PHOSPHATIDYLSERINES; PYRAZOLES; PYRIMIDINES; RIBONUCLEOTIDES;

EID: 65349138878     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.08-121772     Document Type: Article

References (51)

1. Towler, M. C., and Hardie, D. G. (2007) AMP-activated protein kinase in metabolic control and insulin signaling. Circ. Res. 100, 328-341 (Pubitemid 46272405)
2. Winder, W. W., and Thomson, D. M. (2007) Cellular energy sensing and signaling by AMP-activated protein kinase. Cell Biochem. Biophys. 47, 332-347 (Pubitemid 47339850)
3. Carling, D. (2007) The role of the AMP-activated protein kinase in the regulation of energy homeostasis. Novartis Found. Symp. 286, 72-81
4. Horie, T., Ono, K., Nagao, K., Nishi, H., Kinoshita, M., Kawamura, T., Wada, H., Shimatsu, A., Kita, T., and Hasegawa, K. (2008) Oxidative stress induces GLUT4 translocation by activation of PI3-K/Akt and dual AMPK kinase in cardiac myocytes. J. Cell. Physiol. 215, 733-742 (Pubitemid 351632695)
5. Jensen, T. E., Rose, A. J., Hellsten, Y., Wojtaszewski, J. F., and Richter, E. A. (2007) Caffeine-induced Ca(2+) release increases AMPK-dependent glucose uptake in rodent soleus muscle. Am. J. Physiol. Endocrinol. Metab. 293, E286-E292
6. McGee, S. L., and Hargreaves, M. (2008) AMPK and transcriptional regulation. Front. Biosci. 13, 3022-3033
7. Hardie, D. G. (2004) The AMP-activated protein kinase pathway- new players upstream and downstream. J. Cell Sci. 117, 5479-5487
8. Lang, K. S., Lang, P. A., Bauer, C., Duranton, C., Wieder, T., Huber, S. M., and Lang, F. (2005) Mechanisms of suicidal erythrocyte death. Cell Physiol. Biochem. 15, 195-202
9. Berg, C. P., Engels, I. H., Rothbart, A., Lauber, K., Renz, A., Schlosser, S. F., Schulze-Osthoff, K., and 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 (Pubitemid 34048474)
10. Brand, V. B., Sandu, C. D., Duranton, C., Tanneur, V., Lang, K. S., Huber, S. M., and 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 (Pubitemid 37465150)
11. Bratosin, D., Estaquier, J., Petit, F., Arnoult, D., Quatannens, B., Tissier, J. P., Slomianny, C., Sartiaux, C., Alonso, C., Huart, J. J., Montreuil, J., and Ameisen, J. C. (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 (Pubitemid 34048470)
12. Daugas, E., Cande, C., and Kroemer, G. (2001) Erythrocytes: death of a mummy. Cell Death Differ. 8, 1131-1133
13. Lang, P. A., Warskulat, U., Heller-Stilb, B., Huang, D. Y., Grenz, A., Myssina, S., Duszenko, M., Lang, F., Haussinger, D., Vallon, V., and Wieder, T. (2003) Blunted apoptosis of erythrocytes from taurine transporter deficient mice. Cell Physiol. Biochem. 13, 337-346 (Pubitemid 37465149)
14. Duranton, C., Huber, S. M., and Lang, F. (2002) Oxidation induces a Cl(-)-dependent cation conductance in human red blood cells. J. Physiol. 539, 847-855 (Pubitemid 35175434)
15. Duranton, C., Huber, S., Tanneur, V., Lang, K., Brand, V., Sandu, C., and Lang, F. (2003) Electrophysiological properties of the Plasmodium Falciparum-induced cation conductance of human erythrocytes. Cell Physiol. Biochem. 13, 189-198 (Pubitemid 36921037)
16. Huber, S. M., Gamper, N., and Lang, F. (2001) Chloride conductance and volume-regulatory nonselective cation conductance in human red blood cell ghosts. Pflügers Arch. 441, 551-558 (Pubitemid 32128152)
17. Lang, K. S., Duranton, C., Poehlmann, H., Myssina, S., Bauer, C., Lang, F., Wieder, T., and Huber, S. M. (2003) Cation channels trigger apoptotic death of erythrocytes. Cell Death Differ. 10, 249-256 (Pubitemid 36553467)
18. Kaestner, L., Tabellion, W., Lipp, P., and Bernhardt, I. (2004) Prostaglandin E2 activates channel-mediated calcium entry in human erythrocytes: an indication for a blood clot formation supporting process. Thromb. Haemost. 92, 1269-1272 (Pubitemid 39642535)
19. Bookchin, R. M., Ortiz, O. E., and Lew, V. L. (1987) Activation of calcium-dependent potassium channels in deoxygenated sickled red cells. Prog. Clin. Biol. Res. 240, 193-200
20. Brugnara, C., de Franceschi, L., and Alper, S. L. (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 (Pubitemid 23209038)
21. Lang, P. A., Kaiser, S., Myssina, S., Wieder, T., Lang, F., and Huber, S. M. (2003) Role of Ca2+-activated K+ channels in human erythrocyte apoptosis. Am. J. Physiol. Cell. Physiol. 285, C1553-C1560
22. Schneider, J., Nicolay, J. P., Foller, M., Wieder, T., and Lang, F. (2007) Suicidal erythrocyte death following cellular K+ loss. Cell Physiol. Biochem. 20, 35-44 (Pubitemid 46956810)
23. Gulbins, E. (2003) Regulation of death receptor signaling and apoptosis by ceramide. Pharmacol. Res. 47, 393-399 (Pubitemid 36379201)
24. Lang, K. S., Myssina, S., Brand, V., Sandu, C., Lang, P. A., Berchtold, S., Huber, S. M., Lang, F., and Wieder, T. (2004) Involvement of ceramide in hyperosmotic shock-induced death of erythrocytes. Cell Death Differ. 11, 231-243 (Pubitemid 38159647)
25. Nicolay, J. P., Schneider, J., Niemoeller, O. M., Artunc, F., Portero-Otin, M., Haik, G., Jr., Thornalley, P. J., Schleicher, E., Wieder, T., and Lang, F. (2006) Stimulation of suicidal erythrocyte death by methylglyoxal. Cell Physiol. Biochem. 18, 223-232 (Pubitemid 44946977)
26. Nicolay, J. P., Gatz, S., Liebig, G., Gulbins, E., and Lang, F. (2007) Amyloid induced suicidal erythrocyte death. Cell Physiol. Biochem. 19, 175-184 (Pubitemid 46270900)
27. Viollet, B., Andreelli, F., Jorgensen, S. B., Perrin, C., Flamez, D., Mu, J., Wojtaszewski, J. F., Schuit, F. C., Birnbaum, M., Richter, E., Burcelin, R., and Vaulont, S. (2003) Physiological role of AMP-activated protein kinase (AMPK): insights from knockout mouse models. Biochem. Soc. Trans. 31, 216-219 (Pubitemid 36241431)
28. Lang, P. A., Huober, J., Bachmann, C., Kempe, D. S., Sobiesiak, M., Akel, A., Niemoeller, O. M., Dreischer, P., Eisele, K., Klarl, B. A., Gulbins, E., Lang, F., and Wieder, T. (2006) Stimulation of erythrocyte phosphatidylserine exposure by paclitaxel. Cell Physiol. Biochem. 18, 151-164 (Pubitemid 43295509)
29. Foller, M., Shumilina, E., Lam, R., Mohamed, W., Kasinathan, R., Huber, S., Chakraborty, T., and Lang, F. (2007) Induction of suicidal erythrocyte death by listeriolysin from Listeria monocytogenes. Cell Physiol. Biochem. 20, 1051-1060 (Pubitemid 350059711)
30. Klarl, B. A., Lang, P. A., Kempe, D. S., Niemoeller, O. M., Akel, A., Sobiesiak, M., Eisele, K., Podolski, M., Huber, S. M., Wieder, T., and Lang, F. (2006) Protein kinase C mediates erythrocyte "programmed cell death" following glucose depletion. Am. J. Physiol. Cell. Physiol. 290, C244-C253
31. Lira, V. A., Soltow, Q. A., Long, J. H., Betters, J. L., Sellman, J. E., and Criswell, D. S. (2007) Nitric oxide increases GLUT4 expression and regulates AMPK signaling in skeletal muscle. Am. J. Physiol. Endocrinol. Metab. 293, E1062-E1068
32. Chuang, D. M. (2004) Neuroprotective and neurotrophic actions of the mood stabilizer lithium: can it be used to treat neurodegenerative diseases? Crit. Rev. Neurobiol. 16, 83-90
33. Gaskin, F. S., Kamada, K., Yusof, M., and Korthuis, R. J. (2007) 5-AMP-activated protein kinase activation prevents postischemic leukocyte-endothelial cell adhesive interactions. Am. J. Physiol. Heart. Circ. Physiol. 292, H326-H332 (Pubitemid 46105194)
34. Sell, H., Dietze-Schroeder, D., Eckardt, K., and Eckel, J. (2006) Cytokine secretion by human adipocytes is differentially regulated by adiponectin, AICAR, and troglitazone. Biochem. Biophys. Res. Commun. 343, 700-706
35. Boas, F. E., Forman, L., and 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 (Pubitemid 28135857)
36. i via AMPK in hypothalamic arcuate nucleus NPY neurons. Biochem. Biophys. Res. Commun. 366, 388-392
37. Evans, A. M., Mustard, K. J., Wyatt, C. N., Peers, C., Dipp, M., Kumar, P., Kinnear, N. P., and Hardie, D. G. (2005) Does AMP-activated protein kinase couple inhibition of mitochondrial oxidative phosphorylation by hypoxia to calcium signaling in O2-sensing cells? J. Biol. Chem. 280, 41504-41511 (Pubitemid 41832211)
38. Low, P. S., Rathinavelu, P., and Harrison, M. L. (1993) Regulation of glycolysis via reversible enzyme binding to the membrane protein, band 3. J. Biol. Chem. 268, 14627-14631 (Pubitemid 23206598)
39. Zappulla, D. (2008) Environmental stress, erythrocyte dysfunctions, inflammation, and the metabolic syndrome: adaptations to CO2 increases? J. Cardiometab. Syndr. 3, 30-34
40. Nicolay, J. P., Liebig, G., Niemoeller, O. M., Koka, S., Ghashghaeinia, M., Wieder, T., Haendeler, J., Busse, R., and Lang, F. (2008) Inhibition of suicidal erythrocyte death by nitric oxide. Pflügers Arch. 456, 293-305
41. Fadok, V. A., Bratton, D. L., Rose, D. M., Pearson, A., Ezekewitz, R. A., and Henson, P. M. (2000) A receptor for phosphatidylserine-specific clearance of apoptotic cells. Nature 405, 85-90 (Pubitemid 30321820)
42. Kempe, D. S., Lang, P. A., Duranton, C., Akel, A., Lang, K. S., Huber, S. M., Wieder, T., and Lang, F. (2006) Enhanced programmed cell death of iron-deficient erythrocytes. FASEB J. 20, 368-370 (Pubitemid 46671174)
43. Mayer, A., Denanglaire, S., Viollet, B., Leo, O., and Andris, F. (2008) AMP-activated protein kinase regulates lymphocyte responses to metabolic stress but is largely dispensable for immune cell development and function. Eur. J. Immunol. 38, 948-956
44. Andrews, D. A., and Low, P. S. (1999) Role of red blood cells in thrombosis. Curr. Opin. Hematol. 6, 76-82 (Pubitemid 29342520)
45. Closse, C., Dachary-Prigent, J., and Boisseau, M. R. (1999) Phosphatidylserine-related adhesion of human erythrocytes to vascular endothelium. Br. J. Haematol. 107, 300-302 (Pubitemid 29530214)
46. Gallagher, P. G., Chang, S. H., Rettig, M. P., Neely, J. E., Hillery, C. A., Smith, B. D., and Low, P. S. (2003) Altered erythrocyte endothelial adherence and membrane phospholipid asymmetry in hereditary hydrocytosis. Blood 101, 4625-4627
47. Pandolfi, A., Di Pietro, N., Sirolli, V., Giardinelli, A., Di Silvestre, S., Amoroso, L., Di Tomo, P., Capani, F., Consoli, A., and Bonomini, M. (2007) Mechanisms of uremic erythrocyte-induced adhesion of human monocytes to cultured endothelial cells. J. Cell. Physiol. 213, 699-709 (Pubitemid 350058263)
48. Wood, B. L., Gibson, D. F., and Tait, J. F. (1996) Increased erythrocyte phosphatidylserine exposure in sickle cell disease: flow-cytometric measurement and clinical associations. Blood 88, 1873-1880
49. Chung, S. M., Bae, O. N., Lim, K. M., Noh, J. Y., Lee, M. Y., Jung, Y. S., and Chung, J. H. (2007) Lysophosphatidic acid induces thrombogenic activity through phosphatidylserine exposure and procoagulant microvesicle generation in human erythrocytes. Arterioscler. Thromb. Vasc. Biol. 27, 414-421
50. Zwaal, R. F., Comfurius, P., and Bevers, E. M. (2005) Surface exposure of phosphatidylserine in pathological cells. Cell. Mol. Life. Sci. 62, 971-988 (Pubitemid 40655614)
51. Lang, K. S., Myssina, S., Lang, P. A., Tanneur, V., Kempe, D. S., Mack, A. F., Huber, S. M., Wieder, T., Lang, F., and Duranton, C. (2004) Inhibition of erythrocyte phosphatidylserine exposure by urea and Cl-. Am. J. Physiol. Renal. Physiol. 286, F1046-F1053 (Pubitemid 38656358)