The detection of micromolar pericellular ATP pool on lymphocyte surface by using lymphoid ecto-adenylate kinase as intrinsic ATP sensor

Molecular Biology of the Cell

Volumn 17, Issue 8, 2006, Pages 3378-3385

  Yegutkin, Gennady G ^a   Mikhailov, Andrey ^b   Samburski, Sergei S ^a   Jalkanen, Sirpa ^a  

^a NATIONAL PUBLIC HEALTH INSTITUTE   (Finland)

^b UNIVERSITY OF TURKU   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; APYRASE; INOSITOL PHOSPHATE; LYMPHOID ECTO ADENYLATE KINASE; MEPACRINE; NUCLEOTIDE; PHOSPHATE; PURINE P2Y RECEPTOR; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; AUTOCRINE EFFECT; B LYMPHOCYTE; BLOOD; CELL GRANULE; CELL SURFACE; CELL TRANSPORT; CHEMICAL REACTION; CONCENTRATION RESPONSE; CONFOCAL MICROSCOPY; CONTROLLED STUDY; ENZYME ACTIVITY; ENZYMIC BIOSENSOR; EXTRACELLULAR SPACE; HUMAN; HUMAN CELL; LEUKEMIA CELL; LYMPHOCYTE; MEMBRANE STRUCTURE; MOLECULAR IMAGING; MOLECULAR PROBE; NONHUMAN; PARACRINE SIGNALING; PHOSPHORYLATION; PRIORITY JOURNAL; PROTEIN ANALYSIS; SIGNAL TRANSDUCTION; SYNAPSE; T LYMPHOCYTE;

ADENOSINE MONOPHOSPHATE; ADENOSINE TRIPHOSPHATE; ADENYLATE KINASE; ANIMALS; CELL MEMBRANE; CHO CELLS; CRICETINAE; CRICETULUS; CYTOPLASMIC GRANULES; HUMANS; JURKAT CELLS; KINETICS; LYMPHOCYTES; PHOSPHATES; PHOSPHORYLATION; RADIOACTIVE TRACERS; RECEPTORS, PURINERGIC; TUMOR CELLS, CULTURED;

EID: 33746616390     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.E05-10-0993     Document Type: Article

References (40)

1. Alonso, M. A., and Millan, J. (2001). The role of lipid rafts in signalling and membrane trafficking in T lymphocytes. J. Cell Sci. 124, 3957-3965.
2. Beigi, R., Kobatake, E., Aizawa, M., and Dubyak, G. R. (1999). Detection of local ATP release from activated platelets using cell surface-attached firefly luciferase. Am. J. Physiol. 276, C267-C278.
3. Bodin, P., and Burnstock, G. (2001). Evidence that release of adenosine triphosphate from endothelial cells during increased shear stress is vesicular. J. Cardiovasc. Pharmacol. 38, 900-908.
4. Carrasco, A. J., et al. (2001). Adenylate kinase phosphotransfer communicates cellular energetic signals to ATP-sensitive potassium channels. Proc. Natl. Acad. Sci. USA 98, 7623-7628.
5. Collavin, L., Lazarevic, D., Utrera, R., Marzinotto, S., Monte, M., and Schneider, C. (1999). wt p53 dependent expression of a membrane-associated isoform of adenylate kinase. Oncogene 18, 5879-5888.
6. Di Virgilio, F., Chiozzi, P., Ferrari, D., Falzoni, S., Sanz, J. M., Morelli, A., Torboli, M., Bolognesi, G., and Baricordi, O. R. (2001). Nucleotide receptors: an emerging family of regulatory molecules in blood cells. Blood 97, 587-600.
7. Dzeja, P. P., and Terzic, A. (2003). Phosphotransfer networks and cellular energetics. J. Exp. Biol. 206, 2039-2047.
8. Griffith, D. A., and Jarvis, S. M. (1996). Nucleoside and nucleobase transport systems of mammalian cells. Biochim. Biophys. Acta 1286, 153-181.
9. Harder, T., Scheiffele, P., Verkade, P., and Simons, K. (1998). Lipid domain structure of the plasma membrane revealed by patching of membrane components. J. Cell Biol. 141, 929-942.
10. Harder, T., and Simons, K. (1999). Clusters of glycolipid and glycosylphosphatidylinositol-anchored proteins in lymphoid cells: accumulation of actin regulated by local tyrosine phosphorylation. Eur. J. Immunol. 29, 556-562.
11. Hayashi, S., Hazama, A., Dutta, A. K., Sabirov, R. Z., and Okada, Y. (2004). Detecting ATP release by a biosensor method. Sci. STKE 2004, p114.
12. Hazama, A., Hayashi, S., and Okada, Y. (1998). Cell surface measurements of ATP release from single pancreatic beta cells using a novel biosensor technique. Pfluegers Arch. 437, 31-35.
13. Helenius, A., and Simons, K. (1975). Solubilization of membranes by detergents. Biochim. Biophys. Acta 415, 29-79.
14. Henttinen, T., Jalkanen, S., and Yegutkin, G. G. (2003). Adherent leukocytes prevent adenosine formation and impair endothelial barrier function by ecto-5′-nucleotidase/CD73-dependent mechanism. J. Biol. Chem. 278, 24888-24895.
15. Janes, P. W., Ley, S. C., and Magee, A. I. (1999). Aggregation of lipid rafts accompanies signaling via the T cell antigen receptor. J. Cell Biol. 147, 447-461.
16. Joseph, S. M., Buchakjian, M. R., and Dubyak, G. R. (2003). Colocalization of ATP release sites and ecto-ATPase activity at the extracellular surface of human astrocytes. J. Biol. Chem. 278, 23331-23342.
17. Kaiser, R. A., Oxhorn, B. C., Andrews, G., and Buxton, I. L. (2002). Functional compartmentation of endothelial P2Y receptor signaling. Circ. Res. 91, 292-299.
18. Koziak, K., et al. (2000). Palmitoylation targets CD39/endothelial ATP diphosphohydrolase to caveolae. J. Biol. Chem. 275, 2057-2062.
19. Lazarowski, E. R., Boucher, R. C., and Harden, T. K. (2000). Constitutive release of ATP and evidence for major contribution of ecto-nucleotide pyrophosphatase and nucleoside diphosphokinase to extracellular nucleotide concentrations. J. Biol. Chem. 275, 31061-31068.
20. Lazarowski, E. R., Boucher, R. C., and Harden, T. K. (2003). Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. Mol. Pharmacol. 64, 785-795.
21. Lazarowski, E. R., Watt, W. C., Stutts, M. J., Boucher, R. C., and Harden, T. K. (1995). Pharmacological selectivity of the cloned human P2U-purinoceptor: potent activation by diadenosine tetraphosphate. Br. J. Pharmacol. 116, 1619-1627.
22. Mitchell, C. H., Carre, D. A., McGlinn, A. M., Stone, R. A., and Civan, M. M. (1998). A release mechanism for stored ATP in ocular ciliary epithelial cells. Proc. Natl. Acad. Sci. USA 95, 7174-7178.
23. Norman, G. A., Follett, M. J., and Hector, D. A. (1974). Quantitative thin-layer chromatography of ATP and the products of its degradation in meat tissue. J. Chromatogr. 90, 105-111.
24. Parr, C. E., Sullivan, D. M., Paradiso, A. M., Lazarowski, E. R., Burch, L. H., Olsen, J. C., Erb, L., Weisman, G. A., Boucher, R. C., and Turner, J. T. (1994). Cloning and expression of a human P2U nucleotide receptor, a target for cystic fibrosis pharmacotherapy. Proc. Natl. Acad. Sci. USA 91, 3275-3279.
25. Pellegatti, P., Falzoni, S., Pinton, P., Rizzuto, R., and Di Virgilio, F. (2005). A novel recombinant plasma membrane-targeted luciferase reveals a new pathway for ATP secretion. Mol. Biol. Cell 16, 3659-3665.
26. Picher, M., and Boucher, R. C. (2003). Human airway ecto-adenylate kinase. A mechanism to propagate ATP signaling on airway surfaces. J. Biol. Chem. 278, 11256-11264.
27. Ralevic, V., and Burnstock, G. (1998). Receptors for purines and pyrimidines. Pharmacol. Rev. 50, 413-492.
28. Randak, C., and Welsh, M. J. (2003). An intrinsic adenylate kinase activity regulates gating of the ABC transporter CFTR. Cell 115, 837-850.
29. Resta, R., Hooker, S. W., Laurent, A. B., Shuck, J. K., Misumi, Y., Ikehara, Y., Koretzky, G. A., and Thompson, L. F. (1994). Glycosyl phosphatidylinositol membrane anchor is not required for T cell activation through CD73. J. Immunol. 153, 1046-1053.
30. Ruan, Q., Chen, Y., Gratton, E., Glaser, M., and Mantalin, W. W. (2002). Cellular characterization of adenylate kinase and its isoform: two-photon excitation fluorescence imaging and fluorescence correlation spectroscopy. Biophys. J. 83, 3177-3187.
31. Schneider, S. W., Egan, M. E., Jena, B. P., Guggino, W. B., Oberleithner, H., and Geibel, J. P. (1999). Continuous detection of extracellular ATP on living cells by using atomic force microscopy. Proc. Natl. Acad. Sci. USA 96, 12180-12185.
32. Schwiebert, E. M., and Zsembery, A. (2003). Extracellular ATP as a signaling molecule for epithelial cells. Biochim. Biophys. Acta 1615, 7-32.
33. Sorensen, C. E., and Novak, I. (2001). Visualization of ATP release in pancreatic acini in response to cholinergic stimulus. Use of fluorescent probes and confocal microscopy. J. Biol. Chem. 276, 32925-32932.
34. Stulnig, T. M. (2003). Immunomodulation by polyunsaturated fatty acids: mechanisms and effects. Int. Arch. Allergy Immunol. 132, 310-321.
35. Stulnig, T. M., Huber, J., Leitinger, N., Imre, E. M., Angelisova, P., Nowotny, P., and Waldhausl, W. (2001). Polyunsaturated eicosapentaenoic acid displaces proteins from membrane rafts by altering raft lipid composition. J. Biol. Chem. 276, 37335-37340.
36. Vacca, F., Amadio, S., Sancesario, G., Bernardi, G., and Volonte, C. (2004). P2X3 receptor localizes into lipid rafts in neuronal cells. J. Neurosci. Res. 76, 653-661.
37. Yan, H., and Tsai, M.-D. (1999). Nucleoside monophosphate kinases: structure, mechanism, and substrate specificity. Adv. Enzymol. Relat. Areas Mol. Biol. 73, 103-134.
38. Yegutkin, G. G., Henttinen, T., and Jalkanen, S. (2001). Extracellular ATP formation on vascular endothelial cells is mediated by ecto-nucleotide kinase activities via phosphotransfer reactions. FASEB J. 15, 251-260.
39. Yegutkin, G. G., Henttinen, T., Samburski, S. S., Spychala, J., and Jalkanen, S. (2002). The evidence for two opposite, ATP-generating and ATP-consuming, extracellular pathways on endothelial and lymphoid cells. Biochem. J. 367, 121-128.
40. Zimmermann, H. (2000). Extracellular metabolism of ATP and other nucleotides. Naunyn Schmiedebergs Arch Pharmacol. 362, 299-309.