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Purinergic Signalling

, Volume 8, Issue 3, pp 343–357 | Cite as

ATP synthesis and storage

  • Massimo Bonora
  • Simone Patergnani
  • Alessandro Rimessi
  • Elena De Marchi
  • Jan M. Suski
  • Angela Bononi
  • Carlotta Giorgi
  • Saverio Marchi
  • Sonia Missiroli
  • Federica Poletti
  • Mariusz R. Wieckowski
  • Paolo PintonEmail author
Original Article

Abstract

Since 1929, when it was discovered that ATP is a substrate for muscle contraction, the knowledge about this purine nucleotide has been greatly expanded. Many aspects of cell metabolism revolve around ATP production and consumption. It is important to understand the concepts of glucose and oxygen consumption in aerobic and anaerobic life and to link bioenergetics with the vast amount of reactions occurring within cells. ATP is universally seen as the energy exchange factor that connects anabolism and catabolism but also fuels processes such as motile contraction, phosphorylations, and active transport. It is also a signalling molecule in the purinergic signalling mechanisms. In this review, we will discuss all the main mechanisms of ATP production linked to ADP phosphorylation as well the regulation of these mechanisms during stress conditions and in connection with calcium signalling events. Recent advances regarding ATP storage and its special significance for purinergic signalling will also be reviewed.

Keywords

ATP synthesis ATP storage Mitochondria Calcium 

Notes

Acknowledgments

The authors apologize for any excessive bias and the inevitable omissions. The authors are also deeply indebted to past collaborators. This research was supported by the Ministry of Science and Higher Education, Poland, grant NN407 075 137 to MRW; the Italian Ministry of Health to A.R.; and the Italian Association for Cancer Research (AIRC), Telethon (GGP09128), local funds from the University of Ferrara, the Italian Ministry of Education, University and Research (COFIN, FIRB and Futuro in Ricerca), the Italian Cystic Fibrosis Research Foundation, and Italian Ministry of Health to P.P.

SM was supported by a FIRC fellowship; AB was supported by a research fellowship Fondazione Italiana Sclerosi Multipla (FISM)-Cod. 2010/B/1; SP was supported by a training fellowship FISM-Cod. 2010/B/13; JMS was supported by PhD fellowship from The Foundation for Polish Science (FNP), UE, European Regional Development Fund and Operational Programme “Innovative economy”.

References

  1. 1.
    Pollard-Knight D, Cornish-Bowden A (1982) Mechanism of liver glucokinase. Mol Cell Biochem 44(2):71–80PubMedGoogle Scholar
  2. 2.
    Robey RB, Hay N (2005) Mitochondrial hexokinases: guardians of the mitochondria. Cell Cycle 4(5):654–658PubMedGoogle Scholar
  3. 3.
    Sirover MA (1999) New insights into an old protein: the functional diversity of mammalian glyceraldehyde-3-phosphate dehydrogenase. Biochim Biophys Acta 1432(2):159–184PubMedGoogle Scholar
  4. 4.
    Jurica MS et al (1998) The allosteric regulation of pyruvate kinase by fructose-1,6-bisphosphate. Structure 6(2):195–210PubMedGoogle Scholar
  5. 5.
    Mazurek S (2011) Pyruvate kinase type M2: A key regulator of the metabolic budget system in tumor cells. Int J Biochem Cell Biol 43:969–980Google Scholar
  6. 6.
    Christofk HR et al (2008) The M2 splice isoform of pyruvate kinase is important for cancer metabolism and tumour growth. Nature 452(7184):230–233PubMedGoogle Scholar
  7. 7.
    Warburg O, Wind F, Negelein E (1927) The metabolism of tumors in the body. J Gen Physiol 8(6):519–530PubMedGoogle Scholar
  8. 8.
    Krebs HA (1940) The citric acid cycle and the Szent-Gyorgyi cycle in pigeon breast muscle. Biochem J 34(5):775–779PubMedGoogle Scholar
  9. 9.
    Kennedy EP, Lehninger AL (1949) Oxidation of fatty acids and tricarboxylic acid cycle intermediates by isolated rat liver mitochondria. J Biol Chem 179(2):957–972PubMedGoogle Scholar
  10. 10.
    Lambeth DO et al (2004) Expression of two succinyl–CoA synthetases with different nucleotide specificities in mammalian tissues. J Biol Chem 279(35):36621–36624PubMedGoogle Scholar
  11. 11.
    King A, Selak MA, Gottlieb E (2006) Succinate dehydrogenase and fumarate hydratase: linking mitochondrial dysfunction and cancer. Oncogene 25(34):4675–4682PubMedGoogle Scholar
  12. 12.
    Quinn PJ, Dawson RM (1969) Interactions of cytochrome c and [14C]. Biochem J 115(1):65–75PubMedGoogle Scholar
  13. 13.
    Lenaz G, Genova ML (2010) Structure and organization of mitochondrial respiratory complexes: a new understanding of an old subject. Antioxid Redox Signal 12(8):961–1008PubMedGoogle Scholar
  14. 14.
    Boyer PD (2000) Catalytic site forms and controls in ATP synthase catalysis. Biochim Biophys Acta 1458(2–3):252–262PubMedGoogle Scholar
  15. 15.
    Ferguson SJ (2010) ATP synthase: from sequence to ring size to the P/O ratio. Proc Natl Acad Sci USA 107(39):16755–16756PubMedGoogle Scholar
  16. 16.
    Ramaiah A, Hathaway JA, Atkinson DE (1964) Adenylate as a metabolic regulator. Effect on yeast phosphofructokinase kinetics. J Biol Chem 239:3619–3622PubMedGoogle Scholar
  17. 17.
    Hardie DG, Carling D (1997) The AMP-activated protein kinase–fuel gauge of the mammalian cell? Eur J Biochem 246(2):259–273PubMedGoogle Scholar
  18. 18.
    Carling D et al (1989) Purification and characterization of the AMP-activated protein kinase. Copurification of acetyl-CoA carboxylase kinase and 3-hydroxy-3-methylglutaryl-CoA reductase kinase activities. Eur J Biochem 186(1–2):129–136PubMedGoogle Scholar
  19. 19.
    Hardie DG (2007) AMPK and SNF1: snuffing out stress. Cell Metab 6(5):339–340PubMedGoogle Scholar
  20. 20.
    Crute BE et al (1998) Functional domains of the alpha1 catalytic subunit of the AMP-activated protein kinase. J Biol Chem 273(52):35347–35354PubMedGoogle Scholar
  21. 21.
    Hudson ER et al (2003) A novel domain in AMP-activated protein kinase causes glycogen storage bodies similar to those seen in hereditary cardiac arrhythmias. Curr Biol 13(10):861–866PubMedGoogle Scholar
  22. 22.
    Scott JW et al (2004) CBS domains form energy-sensing modules whose binding of adenosine ligands is disrupted by disease mutations. J Clin Invest 113(2):274–284PubMedGoogle Scholar
  23. 23.
    Witczak CA, Sharoff CG, Goodyear LJ (2008) AMP-activated protein kinase in skeletal muscle: from structure and localization to its role as a master regulator of cellular metabolism. Cell Mol Life Sci 65(23):3737–3755PubMedGoogle Scholar
  24. 24.
    Jansen M et al (2009) LKB1 and AMPK family signaling: the intimate link between cell polarity and energy metabolism. Physiol Rev 89(3):777–798PubMedGoogle Scholar
  25. 25.
    Shaw RJ et al (2004) The tumor suppressor LKB1 kinase directly activates AMP-activated kinase and regulates apoptosis in response to energy stress. Proc Natl Acad Sci USA 101(10):3329–3335PubMedGoogle Scholar
  26. 26.
    Woods A et al (2003) LKB1 is the upstream kinase in the AMP-activated protein kinase cascade. Curr Biol 13(22):2004–2008PubMedGoogle Scholar
  27. 27.
    Hawley SA et al (2005) Calmodulin-dependent protein kinase kinase-beta is an alternative upstream kinase for AMP-activated protein kinase. Cell Metab 2(1):9–19PubMedGoogle Scholar
  28. 28.
    Zhang BB, Zhou G, Li C (2009) AMPK: an emerging drug target for diabetes and the metabolic syndrome. Cell Metab 9(5):407–416PubMedGoogle Scholar
  29. 29.
    Dennis PB et al (2001) Mammalian TOR: a homeostatic ATP sensor. Science 294(5544):1102–1105PubMedGoogle Scholar
  30. 30.
    Rosner M et al (2008) The mTOR pathway and its role in human genetic diseases. Mutat Res 659(3):284–292PubMedGoogle Scholar
  31. 31.
    Gwinn DM et al (2008) AMPK phosphorylation of raptor mediates a metabolic checkpoint. Mol Cell 30(2):214–226PubMedGoogle Scholar
  32. 32.
    Hardie DG (2008) AMPK and Raptor: matching cell growth to energy supply. Mol Cell 30(3):263–265PubMedGoogle Scholar
  33. 33.
    Zeng PY, Berger SL (2006) LKB1 is recruited to the p21/WAF1 promoter by p53 to mediate transcriptional activation. Cancer Res 66(22):10701–10708PubMedGoogle Scholar
  34. 34.
    Budanov AV, Karin M (2008) p53 Target genes sestrin1 and sestrin2 connect genotoxic stress and mTOR signaling. Cell 134(3):451–460PubMedGoogle Scholar
  35. 35.
    Zhang WB et al (2010) Activation of AMP-activated protein kinase by temozolomide contributes to apoptosis in glioblastoma cells via p53 activation and mTORC1 inhibition. J Biol Chem 285(52):40461–40471PubMedGoogle Scholar
  36. 36.
    Beffy P et al (2010) Altered signal transduction pathways and induction of autophagy in human myotonic dystrophy type 1 myoblasts. Int J Biochem Cell Biol 42(12):1973–1983PubMedGoogle Scholar
  37. 37.
    Arnold S, Kadenbach B (1997) Cell respiration is controlled by ATP, an allosteric inhibitor of cytochrome-c oxidase. Eur J Biochem 249(1):350–354PubMedGoogle Scholar
  38. 38.
    Bender E, Kadenbach B (2000) The allosteric ATP-inhibition of cytochrome c oxidase activity is reversibly switched on by cAMP-dependent phosphorylation. FEBS Lett 466(1):130–134PubMedGoogle Scholar
  39. 39.
    Lee I et al (2005) cAMP-dependent tyrosine phosphorylation of subunit I inhibits cytochrome c oxidase activity. J Biol Chem 280(7):6094–6100PubMedGoogle Scholar
  40. 40.
    Acin-Perez R et al (2011) Protein phosphorylation and prevention of cytochrome oxidase inhibition by ATP: coupled mechanisms of energy metabolism regulation. Cell Metab 13(6):712–719PubMedGoogle Scholar
  41. 41.
    Ashcroft FM, Gribble FM (1998) Correlating structure and function in ATP-sensitive K+ channels. Trends Neurosci 21(7):288–294PubMedGoogle Scholar
  42. 42.
    Ashford ML, Boden PR, Treherne JM (1990) Glucose-induced excitation of hypothalamic neurones is mediated by ATP-sensitive K+ channels. Pflugers Arch 415(4):479–483PubMedGoogle Scholar
  43. 43.
    Duchen MR, Biscoe TJ (1992) Mitochondrial function in type I cells isolated from rabbit arterial chemoreceptors. J Physiol 450:13–31PubMedGoogle Scholar
  44. 44.
    Duchen MR, Biscoe TJ (1992) Relative mitochondrial membrane potential and [Ca2+]i in type I cells isolated from the rabbit carotid body. J Physiol 450:33–61PubMedGoogle Scholar
  45. 45.
    Rimessi A et al (2008) The versatility of mitochondrial calcium signals: from stimulation of cell metabolism to induction of cell death. Biochim Biophys Acta 1777(7–8):808–816PubMedGoogle Scholar
  46. 46.
    Pozzan T, Rizzuto R (2000) High tide of calcium in mitochondria. Nat Cell Biol 2(2):E25–E27PubMedGoogle Scholar
  47. 47.
    Jouaville LS et al (1999) Regulation of mitochondrial ATP synthesis by calcium: evidence for a long-term metabolic priming. Proc Natl Acad Sci USA 96(24):13807–13812PubMedGoogle Scholar
  48. 48.
    Matlib MA et al (1998) Oxygen-bridged dinuclear ruthenium amine complex specifically inhibits Ca2+ uptake into mitochondria in vitro and in situ in single cardiac myocytes. J Biol Chem 273(17):10223–10231PubMedGoogle Scholar
  49. 49.
    De Stefani D et al (2011) A forty-kilodalton protein of the inner membrane is the mitochondrial calcium uniporter. Nature 476:336–340Google Scholar
  50. 50.
    Sparagna GC et al (1995) Mitochondrial calcium uptake from physiological-type pulses of calcium. A description of the rapid uptake mode. J Biol Chem 270(46):27510–27515PubMedGoogle Scholar
  51. 51.
    Rizzuto R et al (1992) Rapid changes of mitochondrial Ca2+ revealed by specifically targeted recombinant aequorin. Nature 358(6384):325–327PubMedGoogle Scholar
  52. 52.
    Carafoli E et al (1974) The release of calcium from heart mitochondria by sodium. J Mol Cell Cardiol 6(4):361–371PubMedGoogle Scholar
  53. 53.
    Fiskum G, Lehninger AL (1979) Regulated release of Ca2+ from respiring mitochondria by Ca2+/2H+ antiport. J Biol Chem 254(14):6236–6239PubMedGoogle Scholar
  54. 54.
    Baumgartner HK et al (2009) Calcium elevation in mitochondria is the main Ca2+ requirement for mitochondrial permeability transition pore (mPTP) opening. J Biol Chem 284(31):20796–20803PubMedGoogle Scholar
  55. 55.
    Denton RM, Randle PJ, Martin BR (1972) Stimulation by calcium ions of pyruvate dehydrogenase phosphate phosphatase. Biochem J 128(1):161–163PubMedGoogle Scholar
  56. 56.
    McCormack JG, Halestrap AP, Denton RM (1990) Role of calcium ions in regulation of mammalian intramitochondrial metabolism. Physiol Rev 70(2):391–425PubMedGoogle Scholar
  57. 57.
    Denton RM, Richards DA, Chin JG (1978) Calcium ions and the regulation of NAD+-linked isocitrate dehydrogenase from the mitochondria of rat heart and other tissues. Biochem J 176(3):899–906PubMedGoogle Scholar
  58. 58.
    McCormack JG, Denton RM (1979) The effects of calcium ions and adenine nucleotides on the activity of pig heart 2-oxoglutarate dehydrogenase complex. Biochem J 180(3):533–544PubMedGoogle Scholar
  59. 59.
    Kerbey AL et al (1976) Regulation of pyruvate dehydrogenase in rat heart. Mechanism of regulation of proportions of dephosphorylated and phosphorylated enzyme by oxidation of fatty acids and ketone bodies and of effects of diabetes: role of coenzyme A, acetyl-coenzyme A and reduced and oxidized nicotinamide-adenine dinucleotide. Biochem J 154(2):327–348PubMedGoogle Scholar
  60. 60.
    Rutter GA, Denton RM (1989) The binding of Ca2+ ions to pig heart NAD+−isocitrate dehydrogenase and the 2-oxoglutarate dehydrogenase complex. Biochem J 263(2):453–462PubMedGoogle Scholar
  61. 61.
    Lawlis VB, Roche TE (1980) Effect of micromolar Ca2+ on NADH inhibition of bovine kidney alpha-ketoglutarate dehydrogenase complex and possible role of Ca2+ in signal amplification. Mol Cell Biochem 32(3):147–152PubMedGoogle Scholar
  62. 62.
    Harris DA (1993) Regulation of the mitochondrial ATP synthase in rat heart. Biochem Soc Trans 21(Pt 3(3)):778–781PubMedGoogle Scholar
  63. 63.
    Scholz TD, Balaban RS (1994) Mitochondrial F1-ATPase activity of canine myocardium: effects of hypoxia and stimulation. Am J Physiol 266(6 Pt 2):H2396–H2403PubMedGoogle Scholar
  64. 64.
    Territo PR et al (2000) Ca(2+) activation of heart mitochondrial oxidative phosphorylation: role of the F(0)/F(1)-ATPase. Am J Physiol Cell Physiol 278(2):C423–C435PubMedGoogle Scholar
  65. 65.
    Hubbard MJ, McHugh NJ (1996) Mitochondrial ATP synthase F1-beta-subunit is a calcium-binding protein. FEBS Lett 391(3):323–329PubMedGoogle Scholar
  66. 66.
    Sun J et al (2007) Preconditioning results in S-nitrosylation of proteins involved in regulation of mitochondrial energetics and calcium transport. Circ Res 101(11):1155–1163PubMedGoogle Scholar
  67. 67.
    Azarashvili TS et al (2002) Phosphorylation of a peptide related to subunit c of the F0F1-ATPase/ATP synthase and relationship to permeability transition pore opening in mitochondria. J Bioenerg Biomembr 34(4):279–284PubMedGoogle Scholar
  68. 68.
    Taylor SW et al (2003) Oxidative post-translational modification of tryptophan residues in cardiac mitochondrial proteins. J Biol Chem 278(22):19587–19590PubMedGoogle Scholar
  69. 69.
    Anello M et al (2004) Glucosamine-induced alterations of mitochondrial function in pancreatic beta-cells: possible role of protein glycosylation. Am J Physiol Endocrinol Metab 287(4):E602–E608PubMedGoogle Scholar
  70. 70.
    del Arco A, Satrustegui J (1998) Molecular cloning of Aralar, a new member of the mitochondrial carrier superfamily that binds calcium and is present in human muscle and brain. J Biol Chem 273(36):23327–23334PubMedGoogle Scholar
  71. 71.
    Lasorsa FM et al (2003) Recombinant expression of the Ca(2+)-sensitive aspartate/glutamate carrier increases mitochondrial ATP production in agonist-stimulated Chinese hamster ovary cells. J Biol Chem 278(40):38686–38692PubMedGoogle Scholar
  72. 72.
    Jo H, Noma A, Matsuoka S (2006) Calcium-mediated coupling between mitochondrial substrate dehydrogenation and cardiac workload in single guinea-pig ventricular myocytes. J Mol Cell Cardiol 40(3):394–404PubMedGoogle Scholar
  73. 73.
    Collins TJ et al (2001) Mitochondrial Ca(2+) uptake depends on the spatial and temporal profile of cytosolic Ca(2+) signals. J Biol Chem 276(28):26411–26420PubMedGoogle Scholar
  74. 74.
    Maechler P et al (1998) Desensitization of mitochondrial Ca2+ and insulin secretion responses in the beta cell. J Biol Chem 273(33):20770–20778PubMedGoogle Scholar
  75. 75.
    Moreau B, Parekh AB (2008) Ca2+-dependent inactivation of the mitochondrial Ca2+ uniporter involves proton flux through the ATP synthase. Curr Biol 18(11):855–859PubMedGoogle Scholar
  76. 76.
    Cardenas C et al (2010) Essential regulation of cell bioenergetics by constitutive InsP3 receptor Ca2+ transfer to mitochondria. Cell 142(2):270–283PubMedGoogle Scholar
  77. 77.
    Kaasik A et al (2001) Energetic crosstalk between organelles: architectural integration of energy production and utilization. Circ Res 89(2):153–159PubMedGoogle Scholar
  78. 78.
    Crozatier B et al (2002) Role of creatine kinase in cardiac excitation-contraction coupling: studies in creatine kinase-deficient mice. FASEB J 16(7):653–660PubMedGoogle Scholar
  79. 79.
    Whittaker VP et al (1974) Proteins of cholinergic synaptic vesicles from the electric organ of Torpedo: characterization of a low molecular weight acidic protein. Brain Res 75(1):115–131PubMedGoogle Scholar
  80. 80.
    Pablo Huidobro-Toro J, Veronica Donoso M (2004) Sympathetic co-transmission: the coordinated action of ATP and noradrenaline and their modulation by neuropeptide Y in human vascular neuroeffector junctions. Eur J Pharmacol 500(1–3):27–35PubMedGoogle Scholar
  81. 81.
    Coco S et al (2003) Storage and release of ATP from astrocytes in culture. J Biol Chem 278(2):1354–1362PubMedGoogle Scholar
  82. 82.
    Zimmermann H (2008) ATP and acetylcholine, equal brethren. Neurochem Int 52(4–5):634–648PubMedGoogle Scholar
  83. 83.
    Bankston LA, Guidotti G (1996) Characterization of ATP transport into chromaffin granule ghosts. Synergy of ATP and serotonin accumulation in chromaffin granule ghosts. J Biol Chem 271(29):17132–17138PubMedGoogle Scholar
  84. 84.
    Haanes KA, Novak I (2010) ATP storage and uptake by isolated pancreatic zymogen granules. Biochem J 429(2):303–311PubMedGoogle Scholar
  85. 85.
    Yamboliev IA et al (2009) Storage and secretion of beta-NAD, ATP and dopamine in NGF-differentiated rat pheochromocytoma PC12 cells. Eur J Neurosci 30(5):756–768PubMedGoogle Scholar
  86. 86.
    Cotrina ML et al (2000) ATP-mediated glia signaling. J Neurosci 20(8):2835–2844PubMedGoogle Scholar
  87. 87.
    Guthrie PB et al (1999) ATP released from astrocytes mediates glial calcium waves. J Neurosci 19(2):520–528PubMedGoogle Scholar
  88. 88.
    Giorgi C et al (2010) PML regulates apoptosis at endoplasmic reticulum by modulating calcium release. Science 330(6008):1247–1251PubMedGoogle Scholar
  89. 89.
    Newman EA (2001) Propagation of intercellular calcium waves in retinal astrocytes and Muller cells. J Neurosci 21(7):2215–2223PubMedGoogle Scholar
  90. 90.
    Bodin P, Burnstock G (2001) Evidence that release of adenosine triphosphate from endothelial cells during increased shear stress is vesicular. J Cardiovasc Pharmacol 38(6):900–908PubMedGoogle Scholar
  91. 91.
    Hillarp NA (1958) Adenosinephosphates and inorganic phosphate in the adrenaline and noradrenaline containing granules of the adrenal medulla. Acta Physiol Scand 42(3–4):321–332PubMedGoogle Scholar
  92. 92.
    Sawada K et al (2008) Identification of a vesicular nucleotide transporter. Proc Natl Acad Sci USA 105(15):5683–5686PubMedGoogle Scholar
  93. 93.
    Landolfi B et al (1998) Ca2+ homeostasis in the agonist-sensitive internal store: functional interactions between mitochondria and the ER measured in situ in intact cells. J Cell Biol 142(5):1235–1243PubMedGoogle Scholar
  94. 94.
    Luqmani YA (1981) Nucleotide uptake by isolated cholinergic synaptic vesicles: evidence for a carrier of adenosine 5′-triphosphate. Neuroscience 6(6):1011–1021PubMedGoogle Scholar
  95. 95.
    Champagne E et al (2006) Ecto-F1F0 ATP synthase/F1 ATPase: metabolic and immunological functions. Curr Opin Lipidol 17(3):279–284PubMedGoogle Scholar
  96. 96.
    Yegutkin GG (2008) Nucleotide- and nucleoside-converting ectoenzymes: important modulators of purinergic signalling cascade. Biochim Biophys Acta 1783(5):673–694PubMedGoogle Scholar
  97. 97.
    Wang T et al (2006) Cholesterol loading increases the translocation of ATP synthase beta chain into membrane caveolae in vascular endothelial cells. Biochim Biophys Acta 1761(10):1182–1190PubMedGoogle Scholar
  98. 98.
    Ma Z et al (2010) Mitochondrial F1Fo-ATP synthase translocates to cell surface in hepatocytes and has high activity in tumor-like acidic and hypoxic environment. Acta Biochim Biophys Sin (Shanghai) 42(8):530–537Google Scholar
  99. 99.
    Yegutkin GG, Henttinen T, Jalkanen S (2001) Extracellular ATP formation on vascular endothelial cells is mediated by ecto-nucleotide kinase activities via phosphotransfer reactions. FASEB J 15(1):251–260PubMedGoogle Scholar
  100. 100.
    Dzeja PP, Terzic A (2003) Phosphotransfer networks and cellular energetics. J Exp Biol 206(Pt 12):2039–2047PubMedGoogle Scholar
  101. 101.
    Cui J et al (2011) Prevention of extracellular ADP-induced ATP accumulation of the cultured rat spinal astrocytes via P2Y(1)-mediated inhibition of AMPK. Neurosci Lett 503(3):244–249PubMedGoogle Scholar
  102. 102.
    da Silva CG et al (2006) Extracellular nucleotides and adenosine independently activate AMP-activated protein kinase in endothelial cells: involvement of P2 receptors and adenosine transporters. Circ Res 98(5):e39–e47PubMedGoogle Scholar
  103. 103.
    Scheuplein F et al (2009) NAD+ and ATP released from injured cells induce P2X7-dependent shedding of CD62L and externalization of phosphatidylserine by murine T cells. J Immunol 182(5):2898–2908PubMedGoogle Scholar
  104. 104.
    Koch-Nolte F et al (2011) Compartmentation of NAD+-dependent signalling. FEBS Lett 585(11):1651–1656PubMedGoogle Scholar
  105. 105.
    Hubert S et al (2010) Extracellular NAD+ shapes the Foxp3+ regulatory T cell compartment through the ART2–P2X7 pathway. J Exp Med 207(12):2561–2568PubMedGoogle Scholar
  106. 106.
    Heiss K et al (2008) High sensitivity of intestinal CD8+ T cells to nucleotides indicates P2X7 as a regulator for intestinal T cell responses. J Immunol 181(6):3861–3869PubMedGoogle Scholar
  107. 107.
    Klein C et al (2009) Extracellular NAD(+) induces a rise in [Ca(2+)](i) in activated human monocytes via engagement of P2Y(1) and P2Y(11) receptors. Cell Calcium 46(4):263–272PubMedGoogle Scholar
  108. 108.
    Haag F et al (2007) Extracellular NAD and ATP: partners in immune cell modulation. Purinergic Signal 3(1–2):71–81PubMedGoogle Scholar
  109. 109.
    Di Virgilio F (2007) Liaisons dangereuses: P2X(7) and the inflammasome. Trends Pharmacol Sci 28(9):465–472PubMedGoogle Scholar
  110. 110.
    Zhou R et al (2011) A role for mitochondria in NLRP3 inflammasome activation. Nature 469(7329):221–225PubMedGoogle Scholar
  111. 111.
    Li H, Ambade A, Re F (2009) Cutting edge: necrosis activates the NLRP3 inflammasome. J Immunol 183(3):1528–1532PubMedGoogle Scholar
  112. 112.
    Iyer SS et al (2009) Necrotic cells trigger a sterile inflammatory response through the Nlrp3 inflammasome. Proc Natl Acad Sci USA 106(48):20388–20393PubMedGoogle Scholar
  113. 113.
    Zheng LM et al (1991) Extracellular ATP as a trigger for apoptosis or programmed cell death. J Cell Biol 112(2):279–288PubMedGoogle Scholar
  114. 114.
    Schulze-Lohoff E et al (1998) Extracellular ATP causes apoptosis and necrosis of cultured mesangial cells via P2Z/P2X7 receptors. Am J Physiol 275(6 Pt 2):F962–F971PubMedGoogle Scholar
  115. 115.
    Jun DJ et al (2007) Extracellular ATP mediates necrotic cell swelling in SN4741 dopaminergic neurons through P2X7 receptors. J Biol Chem 282(52):37350–37358PubMedGoogle Scholar
  116. 116.
    Leist M et al (1997) Intracellular adenosine triphosphate (ATP) concentration: a switch in the decision between apoptosis and necrosis. J Exp Med 185(8):1481–1486PubMedGoogle Scholar
  117. 117.
    Brovko L, Romanova NA, Ugarova NN (1994) Bioluminescent assay of bacterial intracellular AMP, ADP, and ATP with the use of a coimmobilized three-enzyme reagent (adenylate kinase, pyruvate kinase, and firefly luciferase). Anal Biochem 220(2):410–414PubMedGoogle Scholar
  118. 118.
    Bowers KC, Allshire AP, Cobbold PH (1992) Bioluminescent measurement in single cardiomyocytes of sudden cytosolic ATP depletion coincident with rigor. J Mol Cell Cardiol 24(3):213–218PubMedGoogle Scholar
  119. 119.
    de Wet JR et al (1987) Firefly luciferase gene: structure and expression in mammalian cells. Mol Cell Biol 7(2):725–737PubMedGoogle Scholar
  120. 120.
    Rizzuto R et al (1998) Close contacts with the endoplasmic reticulum as determinants of mitochondrial Ca2+ responses. Science 280(5370):1763–1766PubMedGoogle Scholar
  121. 121.
    Gandelman O et al (1994) Cytoplasmic factors that affect the intensity and stability of bioluminescence from firefly luciferase in living mammalian cells. J Biolumin Chemilumin 9(6):363–371PubMedGoogle Scholar
  122. 122.
    Denton RM, McCormack JG, Edgell NJ (1980) Role of calcium ions in the regulation of intramitochondrial metabolism. Effects of Na+, Mg2+ and ruthenium red on the Ca2+-stimulated oxidation of oxoglutarate and on pyruvate dehydrogenase activity in intact rat heart mitochondria. Biochem J 190(1):107–117PubMedGoogle Scholar
  123. 123.
    Rutter GA (1990) Ca2(+)-binding to citrate cycle dehydrogenases. Int J Biochem 22(10):1081–1088PubMedGoogle Scholar
  124. 124.
    White RL, Wittenberg BA (1993) NADH fluorescence of isolated ventricular myocytes: effects of pacing, myoglobin, and oxygen supply. Biophys J 65(1):196–204PubMedGoogle Scholar
  125. 125.
    Brandes R, Bers DM (1996) Increased work in cardiac trabeculae causes decreased mitochondrial NADH fluorescence followed by slow recovery. Biophys J 71(2):1024–1035PubMedGoogle Scholar
  126. 126.
    Katz LA et al (1989) Relation between phosphate metabolites and oxygen consumption of heart in vivo. Am J Physiol 256(1 Pt 2):H265–H274PubMedGoogle Scholar
  127. 127.
    Burnstock G et al (1978) Purinergic innervation of the guinea-pig urinary bladder. Br J Pharmacol 63(1):125–138PubMedGoogle Scholar
  128. 128.
    Bock P (1980) Identification of paraneurons by labelling with quinacrine (Atebrin). Arch Histol Jpn 43(1):35–44PubMedGoogle Scholar
  129. 129.
    Pryazhnikov E, Khiroug L (2008) Sub-micromolar increase in [Ca(2+)](i) triggers delayed exocytosis of ATP in cultured astrocytes. Glia 56(1):38–49PubMedGoogle Scholar
  130. 130.
    Sorensen CE, 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(35):32925–32932PubMedGoogle Scholar
  131. 131.
    Yegutkin GG et al (2006) The detection of micromolar pericellular ATP pool on lymphocyte surface by using lymphoid ecto-adenylate kinase as intrinsic ATP sensor. Mol Biol Cell 17(8):3378–3385PubMedGoogle Scholar
  132. 132.
    Crowe R, Burnstock G (1981) Comparative studies of quinacrine-positive neurones in the myenteric plexus of stomach and intestine of guinea-pig, rabbit and rat. Cell Tissue Res 221(1):93–107PubMedGoogle Scholar
  133. 133.
    White PN et al (1995) Quinacrine staining of marginal cells in the stria vascularis of the guinea-pig cochlea: a possible source of extracellular ATP? Hear Res 90(1–2):97–105PubMedGoogle Scholar
  134. 134.
    Alund M, Olson L (1979) Quinacrine affinity of endocrine cell systems containing dense core vesicles as visualized by fluorescence microscopy. Cell Tissue Res 204(2):171–186PubMedGoogle Scholar
  135. 135.
    Savran CA et al (2004) Micromechanical detection of proteins using aptamer-based receptor molecules. Anal Chem 76(11):3194–3198PubMedGoogle Scholar
  136. 136.
    Wang Y, Liu B (2008) ATP detection using a label-free DNA aptamer and a cationic tetrahedralfluorene. Analyst 133(11):1593–1598PubMedGoogle Scholar

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© Springer Science+Business Media B.V. 2012

Authors and Affiliations

  • Massimo Bonora
    • 1
  • Simone Patergnani
    • 1
  • Alessandro Rimessi
    • 1
  • Elena De Marchi
    • 1
  • Jan M. Suski
    • 1
    • 2
  • Angela Bononi
    • 1
  • Carlotta Giorgi
    • 1
  • Saverio Marchi
    • 1
  • Sonia Missiroli
    • 1
  • Federica Poletti
    • 1
  • Mariusz R. Wieckowski
    • 2
  • Paolo Pinton
    • 1
    Email author
  1. 1.Department of Experimental and Diagnostic Medicine, Section of General Pathology, Interdisciplinary Center for the Study of Inflammation (ICSI), Laboratory for Technologies of Advanced Therapies (LTTA)University of FerraraFerraraItaly
  2. 2.Nencki Institute of Experimental BiologyWarsawPoland

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