ATP release from non-excitable cells

All cells release nucleotides and are in one way or another involved in local autocrine and paracrine regulation of organ function via stimulation of purinergic receptors. Significant technical advances have been made in recent years to quantify more precisely resting and stimulated adenosine triphosphate (ATP) concentrations in close proximity to the plasma membrane. These technical advances are reviewed here. However, the mechanisms by which cells release ATP continue to be enigmatic. The current state of knowledge on different suggested mechanisms is also reviewed. Current evidence suggests that two separate regulated modes of ATP release co-exist in non-excitable cells: (1) a conductive pore which in several systems has been found to be the channel pannexin 1 and (2) vesicular release. Modes of stimulation of ATP release are reviewed and indicate that both subtle mechanical stimulation and agonist-triggered release play pivotal roles. The mechano-sensor for ATP release is not yet defined.

[1]  N. C. Melchior.  Sodium and potassium complexes of adenosinetriphosphate: equilibrium studies. , 1954, The Journal of biological chemistry.

[2]  W D McElroy,et al.  Anion inhibition of firefly luciferase. , 1970, Archives of biochemistry and biophysics.

[3]  D. Njus,et al.  Bioenergetics of secretory vesicles. , 1986, Biochimica et biophysica acta.

[4]  S. B. Horowitz,et al.  Intracellular compartmentalization of adenosine triphosphate. , 1986, The Journal of biological chemistry.

[5]  M. Berridge,et al.  Simultaneous measurements of cytosolic calcium and secretion in single bovine adrenal chromaffin cells by fluorescent imaging of fura-2 in cocultured cells , 1989, The Journal of cell biology.

[6]  W. D. Mcelroy,et al.  Introduction to beetle luciferases and their applications. , 1989, Journal of bioluminescence and chemiluminescence.

[7]  G. Burnstock,et al.  Increased flow‐induced ATP release from isolated vascular endothelial cells but not smooth muscle cells , 1991, British journal of pharmacology.

[8]  M. Cahalan,et al.  Cell-to-cell spread of calcium signals mediated by ATP receptors in mast cells , 1992, Nature.

[9]  W. Suki,et al.  ATP inhibits the hydrosmotic effect of AVP in rabbit CCT: evidence for a nucleotide P2u receptor. , 1994, The American journal of physiology.

[10]  榎本 浩一.  The increase in the intracellular Ca[2+] concentration induced by mechanical stimulation is propagated via release of pyrophosphorylated nucleotides in mammary epithelial cells , 1995 .

[11]  G. Burnstock,et al.  Uptake and Flow-induced Release of Uridine Nucleotides from Isolated Vascular Endothelial Cells , 1995 .

[12]  G. Cutting,et al.  CFTR regulates outwardly rectifying chloride channels through an autocrine mechanism involving ATP , 1995, Cell.

[13]  S. Lidofsky,et al.  Autocrine signaling through ATP release represents a novel mechanism for cell volume regulation. , 1996, Proceedings of the National Academy of Sciences of the United States of America.

[14]  K. Gunderson,et al.  Failure of the Cystic Fibrosis Transmembrane Conductance Regulator to Conduct ATP , 1996, Science.

[15]  K. Strange,et al.  Cellular and molecular physiology of volume-sensitive anion channels. , 1996, The American journal of physiology.

[16]  T. K. Harden,et al.  Direct Demonstration of Mechanically Induced Release of Cellular UTP and Its Implication for Uridine Nucleotide Receptor Activation* , 1997, The Journal of Biological Chemistry.

[17]  J. Hanrahan,et al.  CFTR-independent ATP release from epithelial cells triggered by mechanical stimuli. , 1997, The American journal of physiology.

[18]  R. Boucher,et al.  Release, metabolism and interconversion of adenine and uridine nucleotides: implications for G protein-coupled P2 receptor agonist selectivity. , 1997, Trends in pharmacological sciences.

[19]  Sreenivas Devidas,et al.  Cystic Fibrosis Transmembrane Conductance Regulator–associated ATP Release Is Controlled by a Chloride Sensor , 1998, The Journal of cell biology.

[20]  R. Dermietzel,et al.  Visualization and functional blocking of gap junction hemichannels (connexons) with antibodies against external loop domains in astrocytes , 1998, Glia.

[21]  G Burnstock,et al.  Receptors for purines and pyrimidines. , 1998, Pharmacological reviews.

[22]  R. Stone,et al.  A release mechanism for stored ATP in ocular ciliary epithelial cells. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[23]  Corelease of noradrenaline and adenosine triphosphate from sympathetic neurones. , 1998, Advances in pharmacology.

[24]  C. Naus,et al.  Connexins regulate calcium signaling by controlling ATP release. , 1998, Proceedings of the National Academy of Sciences of the United States of America.

[25]  M. L. Ellsworth,et al.  Deformation-induced ATP release from red blood cells requires CFTR activity. , 1998, American journal of physiology. Heart and circulatory physiology.

[26]  T. Jentsch,et al.  Permeation and Block of the Skeletal Muscle Chloride Channel, ClC-1, by Foreign Anions , 1998, The Journal of general physiology.

[27]  J. Hescheler,et al.  Spontaneous calcium oscillations in embryonic stem cell-derived primitive endodermal cells. , 1998, Experimental cell research.

[28]  Y. Okada,et al.  Cell surface measurements of ATP release from single pancreatic β cells using a novel biosensor technique , 1998, Pflügers Archiv.

[29]  W. Watt,et al.  Cystic Fibrosis Transmembrane Regulator-independent Release of ATP , 1998, The Journal of Biological Chemistry.

[30]  T. van der Wijk,et al.  Osmotic cell swelling-induced ATP release mediates the activation of extracellular signal-regulated protein kinase (Erk)-1/2 but not the activation of osmo-sensitive anion channels. , 1999, The Biochemical journal.

[31]  Takahiro Shimizu,et al.  Swelling-Induced, Cftr-Independent Atp Release from a Human Epithelial Cell Line , 1999, The Journal of general physiology.

[32]  G. Dubyak,et al.  Detection of local ATP release from activated platelets using cell surface-attached firefly luciferase , 1998 .

[33]  B. Jena,et al.  Continuous detection of extracellular ATP on living cells by using atomic force microscopy. , 1999, Proceedings of the National Academy of Sciences of the United States of America.

[34]  Z Wang,et al.  Direct observation of calcium-independent intercellular ATP signaling in astrocytes. , 2000, Analytical chemistry.

[35]  P. Insel,et al.  Cellular Release of and Response to ATP as Key Determinants of the Set-Point of Signal Transduction Pathways* , 2000, The Journal of Biological Chemistry.

[36]  M. Knowles,et al.  Basal Nucleotide Levels, Release, and Metabolism in Normal and Cystic Fibrosis Airways , 2000, Molecular medicine.

[37]  G. Dubyak,et al.  Endotoxin Activation of Macrophages Does Not Induce ATP Release and Autocrine Stimulation of P2 Nucleotide Receptors1 , 2000, The Journal of Immunology.

[38]  H. Cantiello.  Electrodiffusional ATP movement through CFTR and other ABC transporters , 2001, Pflügers Archiv.

[39]  Amal K. Dutta,et al.  Volume-Dependent Atp-Conductive Large-Conductance Anion Channel as a Pathway for Swelling-Induced Atp Release , 2001, The Journal of general physiology.

[40]  I. Novak,et al.  Visualization of ATP Release in Pancreatic Acini in Response to Cholinergic Stimulus , 2001, The Journal of Biological Chemistry.

[41]  G Burnstock,et al.  Evidence That Release of Adenosine Triphosphate From Endothelial Cells During Increased Shear Stress Is Vesicular , 2001, Journal of cardiovascular pharmacology.

[42]  G. D. Hunter,et al.  Proteinase-activated receptors. , 2001, Pharmacological reviews.

[43]  K. R. Spring,et al.  Bending the MDCK Cell Primary Cilium Increases Intracellular Calcium , 2001, The Journal of Membrane Biology.

[44]  M. Oike,et al.  Involvement of Rho‐kinase and tyrosine kinase in hypotonic stress‐induced ATP release in bovine aortic endothelial cells , 2001, The Journal of physiology.

[45]  Ronald M. Welch,et al.  Climatic Impact of Tropical Lowland Deforestation on Nearby Montane Cloud Forests , 2001, Science.

[46]  E. Newman,et al.  Propagation of Intercellular Calcium Waves in Retinal Astrocytes and Müller Cells , 2001, The Journal of Neuroscience.

[47]  M. Sanderson,et al.  Propagation of intercellular calcium waves in C6 glioma cells transfected with connexins 43 or 32 , 2001, Microscopy research and technique.

[48]  O. Hamill,et al.  Brefeldin A Block of Integrin-dependent Mechanosensitive ATP Release from Xenopus Oocytes Reveals a Novel Mechanism of Mechanotransduction* , 2001, The Journal of Biological Chemistry.

[49]  久留 和成.  Volume-regulated anion channels serve as an auto/paracrine nucleotide release pathway in aortic endothelial cells , 2002 .

[50]  R. North.  Molecular physiology of P2X receptors. , 2002, Physiological reviews.

[51]  V. Stein,et al.  Molecular structure and physiological function of chloride channels. , 2002, Physiological reviews.

[52]  R. Grygorczyk,et al.  Cell swelling-induced ATP release and gadolinium-sensitive channels. , 2002, American journal of physiology. Cell physiology.

[53]  T. Takano,et al.  Intercellular calcium signaling mediated by point-source burst release of ATP , 2002, Proceedings of the National Academy of Sciences of the United States of America.

[54]  Sung Joon Kim,et al.  Luminal P2Y2 receptor-mediated inhibition of Na+ absorption in isolated perfused mouse CCD. , 2002, Journal of the American Society of Nephrology : JASN.

[55]  D. Jagger,et al.  Purinergic Regulation of Sound Transduction and Auditory Neurotransmission , 2002, Audiology and Neurotology.

[56]  R. Dutzler,et al.  X-ray structure of a ClC chloride channel at 3.0 Å reveals the molecular basis of anion selectivity , 2002, Nature.

[57]  S. Jalkanen,et al.  The evidence for two opposite, ATP-generating and ATP-consuming, extracellular pathways on endothelial and lymphoid cells. , 2002, The Biochemical journal.

[58]  N. Dale,et al.  Spike‐independent release of ATP from Xenopus spinal neurons evoked by activation of glutamate receptors , 2002, The Journal of physiology.

[59]  Amal K. Dutta,et al.  Regulation of an ATP‐conductive large‐conductance anion channel and swelling‐induced ATP release by arachidonic acid , 2002, The Journal of physiology.

[60]  M. Lucero,et al.  Activation of Purinergic Receptor Subtypes Modulates Odor Sensitivity , 2003, The Journal of Neuroscience.

[61]  E. Schwiebert,et al.  Extracellular ATP as a signaling molecule for epithelial cells. , 2003, Biochimica et biophysica acta.

[62]  M. Valverde,et al.  Plasma Membrane Voltage-dependent Anion Channel Mediates Antiestrogen-activated Maxi Cl– Currents in C1300 Neuroblastoma Cells* , 2003, Journal of Biological Chemistry.

[63]  K. Spring,et al.  Removal of the MDCK Cell Primary Cilium Abolishes Flow Sensing , 2003, The Journal of Membrane Biology.

[64]  P. D. Bell,et al.  Macula densa cell signaling involves ATP release through a maxi anion channel , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[65]  G. Dubyak,et al.  Colocalization of ATP Release Sites and Ecto-ATPase Activity at the Extracellular Surface of Human Astrocytes* , 2003, Journal of Biological Chemistry.

[66]  M. Matteoli,et al.  Storage and Release of ATP from Astrocytes in Culture* , 2003, The Journal of Biological Chemistry.

[67]  A. Houtsmuller,et al.  Increased Vesicle Recycling in Response to Osmotic Cell Swelling , 2003, Journal of Biological Chemistry.

[68]  D. Levine,et al.  Paracrine factors in tubuloglomerular feedback: adenosine, ATP, and nitric oxide. , 2003, Annual review of physiology.

[69]  N. Dale,et al.  A three-enzyme microelectrode sensor for detecting purine release from central nervous system. , 2003, Biosensors & bioelectronics.

[70]  Jing Zhou,et al.  Polycystins 1 and 2 mediate mechanosensation in the primary cilium of kidney cells , 2003, Nature Genetics.

[71]  Sheldon Weinbaum,et al.  Effect of flow and stretch on the [Ca2+]i response of principal and intercalated cells in cortical collecting duct. , 2003, American journal of physiology. Renal physiology.

[72]  S. Koizumi,et al.  P2X4 receptors induced in spinal microglia gate tactile allodynia after nerve injury , 2003, Nature.

[73]  T Kendall Harden,et al.  Mechanisms of release of nucleotides and integration of their action as P2X- and P2Y-receptor activating molecules. , 2003, Molecular pharmacology.

[74]  B. Nilius,et al.  TRPs Make Sense , 2003, The Journal of Membrane Biology.

[75]  I. Novak.  ATP as a signaling molecule: the exocrine focus. , 2003, News in physiological sciences : an international journal of physiology produced jointly by the International Union of Physiological Sciences and the American Physiological Society.

[76]  J. Leipziger.  Control of epithelial transport via luminal P2 receptors. , 2003, American journal of physiology. Renal physiology.

[77]  Hannah Monyer,et al.  Pannexins, a family of gap junction proteins expressed in brain , 2003, Proceedings of the National Academy of Sciences of the United States of America.

[78]  B. Hellman,et al.  Pancreatic beta-cells communicate via intermittent release of ATP. , 2004, American journal of physiology. Endocrinology and metabolism.

[79]  B. Mizaikoff,et al.  Amperometric ATP biosensor based on polymer entrapped enzymes. , 2004, Biosensors & bioelectronics.

[80]  T. Maéno,et al.  The increase in the intracellular Ca2+ concentration induced by mechanical stimulation is propagated via release of pyrophosphorylated nucleotides in mammary epithelial cells , 1994, Pflügers Archiv.

[81]  G. Dahl,et al.  Pannexin membrane channels are mechanosensitive conduits for ATP , 2004, FEBS letters.

[82]  Alessandra Fabbro,et al.  Quantal release of ATP from clusters of PC12 cells , 2004, The Journal of physiology.

[83]  P. D. Bell,et al.  Macula densa basolateral ATP release is regulated by luminal [NaCl] and dietary salt intake. , 2004, American journal of physiology. Renal physiology.

[84]  Seiko F. Okada,et al.  Voltage-dependent Anion Channel-1 (VDAC-1) Contributes to ATP Release and Cell Volume Regulation in Murine Cells , 2004, The Journal of general physiology.

[85]  Geoffrey Burnstock,et al.  Purinergic Signalling: ATP Release , 2001, Neurochemical Research.

[86]  B. Hellman,et al.  Pancreatic β-cells communicate via intermittent release of ATP , 2004 .

[87]  E. Yeung,et al.  Investigation of G protein-initiated, Ca2+-dependent release of ATP from endothelial cells. , 2004, Biochimica et biophysica acta.

[88]  E. Yeung,et al.  Monitoring real-time release of ATP from the molluscan central nervous system , 2004, Journal of Neuroscience Methods.

[89]  Amal K. Dutta,et al.  Detecting ATP Release by a Biosensor Method , 2004, Science's STKE.

[90]  G. Dubyak,et al.  Methylene ATP analogs as modulators of extracellular ATP metabolism and accumulation , 2004, British journal of pharmacology.

[91]  N. Dale,et al.  ATP is a key mediator of central and peripheral chemosensory transduction , 2004, Experimental physiology.

[92]  R. Grygorczyk,et al.  Cell swelling‐induced ATP release is tightly dependent on intracellular calcium elevations , 2004, The Journal of physiology.

[93]  Yushi Ito,et al.  Sequential activation of RhoA and FAK/paxillin leads to ATP release and actin reorganization in human endothelium , 2004, The Journal of physiology.

[94]  D. Klenerman,et al.  Aldosterone acts via an ATP autocrine/paracrine system: the Edelman ATP hypothesis revisited. , 2005, Proceedings of the National Academy of Sciences of the United States of America.

[95]  K. Strange,et al.  Oscillatory Ca2+ Signaling in the Isolated Caenorhabditis elegans Intestine , 2005, The Journal of general physiology.

[96]  Richard C Boucher,et al.  Normal and Cystic Fibrosis Airway Surface Liquid Homeostasis , 2005, Journal of Biological Chemistry.

[97]  C. Mitchell,et al.  Release of ATP from retinal pigment epithelial cells involves both CFTR and vesicular transport. , 2005, American journal of physiology. Cell physiology.

[98]  Alexander V. Gourine,et al.  ATP is a mediator of chemosensory transduction in the central nervous system , 2005, Nature.

[99]  J. Frøkiaer,et al.  Transepithelial pressure pulses induce nucleotide release in polarized MDCK cells. , 2005, American journal of physiology. Renal physiology.

[100]  B. Mizaikoff,et al.  AFM-tip-integrated amperometric microbiosensors: high-resolution imaging of membrane transport. , 2005, Angewandte Chemie.

[101]  Sonja Hatz,et al.  Microelectrode biosensor for real-time measurement of ATP in biological tissue. , 2005, Analytical chemistry.

[102]  H. Monyer,et al.  Pharmacological properties of homomeric and heteromeric pannexin hemichannels expressed in Xenopus oocytes , 2005, Journal of neurochemistry.

[103]  N. Dale,et al.  Release of ATP in the Ventral Medulla during Hypoxia in Rats: Role in Hypoxic Ventilatory Response , 2005, The Journal of Neuroscience.

[104]  F. Di Virgilio,et al.  A novel recombinant plasma membrane-targeted luciferase reveals a new pathway for ATP secretion. , 2005, Molecular biology of the cell.

[105]  S. Korn,et al.  Potassium channels , 2005, IEEE Transactions on NanoBioscience.

[106]  G. J. Liu,et al.  Secretion of ATP from Schwann cells in response to uridine triphosphate , 2005, The European journal of neuroscience.

[107]  T. Finger,et al.  ATP Signaling Is Crucial for Communication from Taste Buds to Gustatory Nerves , 2005, Science.

[108]  Cathryn L. Kubera,et al.  Astrocytic Purinergic Signaling Coordinates Synaptic Networks , 2005, Science.

[109]  Kenneth R Spring,et al.  A physiological view of the primary cilium. , 2005, Annual review of physiology.

[110]  Jiliang Li,et al.  The P2X7 Nucleotide Receptor Mediates Skeletal Mechanotransduction* , 2005, Journal of Biological Chemistry.

[111]  B. Mizaikoff,et al.  Imaging of ATP membrane transport with dual micro-disk electrodes and scanning electrochemical microscopy. , 2005, Biosensors & bioelectronics.

[112]  P. Rorsman,et al.  Selective nucleotide-release from dense-core granules in insulin-secreting cells , 2005, Journal of Cell Science.

[113]  J. Ando,et al.  Cell-surface-localized ATP detection with immobilized firefly luciferase. , 2006, Analytical biochemistry.

[114]  G. Dahl,et al.  Pannexin 1 in erythrocytes: Function without a gap , 2006, Proceedings of the National Academy of Sciences of the United States of America.

[115]  Seiko F. Okada,et al.  Physiological Regulation of ATP Release at the Apical Surface of Human Airway Epithelia*♦ , 2006, Journal of Biological Chemistry.

[116]  R. North,et al.  Vesicular release of ATP at central synapses , 2006, Pflügers Archiv.

[117]  Linda Yip,et al.  ATP Release Guides Neutrophil Chemotaxis via P2Y2 and A3 Receptors , 2006, Science.

[118]  H. Monyer,et al.  Cell-cell communication beyond connexins: the pannexin channels. , 2006, Physiology.

[119]  G. J. Liu,et al.  Purine Release from Spinal Cord Microglia after Elevation of Calcium by Glutamate , 2006, Molecular Pharmacology.

[120]  A. Surprenant,et al.  Pannexin‐1 mediates large pore formation and interleukin‐1β release by the ATP‐gated P2X7 receptor , 2006, The EMBO journal.

[121]  E. Newman.  A purinergic dialogue between glia and neurons in the retina. , 2006, Novartis Foundation symposium.

[122]  Roger J. Thompson,et al.  Ischemia Opens Neuronal Gap Junction Hemichannels , 2006, Science.

[123]  Eric A. Barnard,et al.  International Union of Pharmacology LVIII: Update on the P2Y G Protein-Coupled Nucleotide Receptors: From Molecular Mechanisms and Pathophysiology to Therapy , 2006, Pharmacological Reviews.

[124]  K. Mikoshiba,et al.  ATP autocrine/paracrine signaling induces calcium oscillations and NFAT activation in human mesenchymal stem cells. , 2006, Cell calcium.

[125]  A. Ikari,et al.  P2X7 Receptor-Dependent Cell Death Is Modulated during Murine T Cell Maturation and Mediated by Dual Signaling Pathways1 , 2006, The Journal of Immunology.

[126]  G. Dahl,et al.  Activation of pannexin 1 channels by ATP through P2Y receptors and by cytoplasmic calcium , 2006, FEBS letters.

[127]  S. Jalkanen,et al.  The detection of micromolar pericellular ATP pool on lymphocyte surface by using lymphoid ecto-adenylate kinase as intrinsic ATP sensor. , 2006, Molecular biology of the cell.

[128]  J. Ando,et al.  Impaired flow-dependent control of vascular tone and remodeling in P2X4-deficient mice , 2006, Nature Medicine.

[129]  R. North,et al.  Purinergic transmission in the central nervous system , 2006, Pflügers Archiv.

[130]  C. Gachet.  Regulation of platelet functions by P2 receptors. , 2006, Annual review of pharmacology and toxicology.

[131]  H. Praetorius,et al.  Slow spontaneous [Ca2+]i oscillations reflect nucleotide release from renal epithelia , 2008, Pflügers Archiv - European Journal of Physiology.

[132]  N. Chaudhari,et al.  The role of pannexin 1 hemichannels in ATP release and cell–cell communication in mouse taste buds , 2007, Proceedings of the National Academy of Sciences.

[133]  H. Praetorius,et al.  Flow-induced [Ca2+]i increase depends on nucleotide release and subsequent purinergic signaling in the intact nephron. , 2007, Journal of the American Society of Nephrology : JASN.

[134]  河野 大助,et al.  Spontaneous oscillation and mechanically induced calcium waves in chondrocytes , 2007 .

[135]  P. Insel,et al.  Mice lacking P2Y2 receptors have salt‐resistant hypertension and facilitated renal Na+ and water reabsorption , 2007, FASEB journal : official publication of the Federation of American Societies for Experimental Biology.

[136]  B. Khakh,et al.  Vesicular ATP Is the Predominant Cause of Intercellular Calcium Waves in Astrocytes , 2007, The Journal of General Physiology.

[137]  D. Spray,et al.  Pannexin1 is part of the pore forming unit of the P2X7 receptor death complex , 2007, FEBS letters.

[138]  R. North,et al.  Spontaneous autocrine release of protons activates ASIC‐mediated currents in HEK293 cells , 2007, Journal of cellular physiology.

[139]  Paul A Insel,et al.  A novel method using fluorescence microscopy for real-time assessment of ATP release from individual cells. , 2007, American journal of physiology. Cell physiology.

[140]  E. Meacci,et al.  Pannexin 1 Is Part of the Pore Forming Unit of the P 2 x 7 Receptor Death Complex , 2008 .

[141]  John M. Walker,et al.  Potassium Channels , 2009, Methods in Molecular Biology.