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The adenosine/neutrophil paradox resolved: human neutrophils possess both A1 and A2 receptors that promote chemotaxis and inhibit O2 generation, respectively.

B N Cronstein, … , A J Hutchison, M Williams

Published April 1, 1990
Citation Information: J Clin Invest. 1990;85(4):1150-1157. https://doi.org/10.1172/JCI114547.

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Research Article

The adenosine/neutrophil paradox resolved: human neutrophils possess both A1 and A2 receptors that promote chemotaxis and inhibit O2 generation, respectively.

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Abstract

Occupancy of specific receptors on neutrophils by adenosine or its analogues diminishes the stimulated release of toxic oxygen metabolites from neutrophils, while paradoxically promoting chemotaxis. We now report evidence that two distinct adenosine receptors are found on neutrophils (presumably the A1 and A2 receptors of other cell types). These adenosine receptors modulate chemotaxis and O2- generation, respectively. N6-Cyclopentyladenosine (CPA), a selective A1 agonist, promoted neutrophil chemotaxis to the chemoattractant FMLP as well as or better than 5'N-ethylcarboxamidoadenosine (NECA). In contrast, CPA did not inhibit O2- generation stimulated by FMLP. Pertussis toxin completely abolished promotion of chemotaxis by CPA but enhanced inhibition by NECA of O2- generation. Disruption of microtubules by colchicine or vinblastine also abrogated the enhancement by NECA of chemotaxis whereas these agents did not markedly interfere with inhibition by NECA of O2- generation. FMLP receptors, once they have bound ligand, shift to a high affinity state and become associated with the cytoskeleton. NECA significantly increased association of [3H]FMLP with cytoskeletal preparations as it inhibited O2-. Disruption of microtubules did not prevent NECA from increasing association of [3H]FMLP with cytoskeletal preparations. Additionally, CPA (A1 agonist) did not increase binding of [3H]FMLP to the cytoskeleton as well as NECA (A2 agonist). These studies indicate that occupancy of one class of adenosine receptors (A1) promotes chemotaxis by a mechanism requiring intact microtubules and G proteins whereas engagement of a second class of receptors (A2) inhibits O2- generation. Signalling via A2 receptors is independent of microtubules, insensitive to pertussis toxin and is associated with binding of [3H]FMLP to cytoskeletal preparations.

Authors

B N Cronstein, L Daguma, D Nichols, A J Hutchison, M Williams

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Citations to this article (317)

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Adenosine 5′-triphosphate and adenosine as endogenous signaling molecules in immunity and inflammation MJ Bours, EL Swennen, FD Virgilio, BN Cronstein, PC Dagnelie	Pharmacology & Therapeutics	2006
Adenosine A1 receptor antagonist versus montelukast on airway reactivity and inflammation A Nadeem, PC Obiefuna, CN Wilson, SJ Mustafa	European Journal of Pharmacology	2006
Adenosine A2a receptors induce heterologous desensitization of chemokine receptors N Zhang, D Yang, H Dong, Q Chen, DI Dimitrova, TJ Rogers, M Sitkovsky, JJ Oppenheim	Blood	2006
Suppression of inflammation by low-dose methotrexate is mediated by adenosine A2A receptor but not A3 receptor activation in thioglycollate-induced peritonitis MC Montesinos, A Desai, BN Cronstein	Arthritis Research & Therapy	2006
Adenosine in the airways: Implications and applications L Spicuzza, GD Maria, R Polosa	European Journal of Pharmacology	2006
Taurine 6 SS Oja, P Saransaari		2006
Regulation of immune cells by local-tissue oxygen tension: HIF1α and adenosine receptors M Sitkovsky, D Lukashev	Nature Reviews Immunology	2005
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Adenosine A2Aagonists in development for the treatment of inflammation CM Lappas, GW Sullivan, J Linden	Expert Opinion on Investigational Drugs	2005
Adenosine A 2A agonists in development for the treatment of inflammation CM Lappas, GW Sullivan, J Linden	Expert Opinion on Investigational Drugs	2005
International Review of Neurobiology ZT Bloomgarden	International review of neurobiology	2005
Adenosine A2A receptor activation reduces inflammation and preserves pulmonary function in an in vivo model of lung transplantation TB Reece, PI Ellman, TS Maxey, IK Crosby, PS Warren, TW Chong, RD LeGallo, J Linden, JA Kern, CG Tribble, IL Kron	The Journal of Thoracic and Cardiovascular Surgery	2005
Differential expression of adenosine receptors in human neutrophils: up-regulation by specific Th1 cytokines and lipopolysaccharide A Fortin, D Harbour, M Fernandes, P Borgeat, S Bourgoin	Journal of leukocyte biology	2005
A Novel A 1 Adenosine Receptor Antagonist, L-97-1 [3-[2-(4-Aminophenyl)-ethyl]-8-benzyl-7-{2-ethyl-(2-hydroxy-ethyl)-amino]-ethyl}-1-propyl-3,7-dihydro-purine-2,6-dione], Reduces Allergic Responses to House Dust Mite in an Allergic Rabbit Model of Asthma PC Obiefuna, VK Batra, A Nadeem, P Borron, CN Wilson, SJ Mustafa	The Journal of pharmacology and experimental therapeutics	2005
A putative osmoreceptor system that controls neutrophil function through the release of ATP, its conversion to adenosine, and activation of A2 adenosine and P2 receptors Y Chen, A Shukla, S Namiki, PA Insel, WG Junger	Journal of leukocyte biology	2004
Endogenous adenosine produced during hypoxia attenuates neutrophil accumulation: coordination by extracellular nucleotide metabolism HK Eltzschig, LF Thompson, J Karhausen, RJ Cotta, JC Ibla, SC Robson, SP Colgan	Blood	2004
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Animal models for the study of adenosine receptor function R Yaar, MR Jones, JF Chen, K Ravid	Journal of Cellular Physiology	2004
Provocation with adenosine 5'-monophosphate, but not methacholine, induces sputum eosinophilia MV berge, HA Kerstjens, DM de reus, GH Koeter, HF Kauffman, DS Postma	Clinical & Experimental Allergy	2004
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Protection from ischemic liver injury by activation of A 2A adenosine receptors during reperfusion: inhibition of chemokine induction YJ Day, MA Marshall, L Huang, MJ McDuffie, MD Okusa, J Linden	AJP Gastrointestinal and Liver Physiology	2004
Thyroid hormone stimulates 5′-ecto-nucleotidase of neonatal rat ventricular myocytes MS Carneiro-Ramos, VB da Silva, MB Júnior, AM Battastini, JJ Sarkis, ML Barreto-Chaves	Molecular and Cellular Biochemistry	2004
Low-dose adenosine stress echocardiography: detection of myocardial viability A Djordjevic-Dikic, M Ostojic, B Beleslin, I Nedeljkovic, J Stepanovic, S Stojkovic, Z Petrasinovic, M Nedeljkovic, J Saponjski, V Giga	Cardiovascular ultrasound	2003
The critical role of adenosine A2A receptors in downregulation of inflammation and immunity in the pathogenesis of infectious diseases M Thiel, CC Caldwell, MV Sitkovsky	Microbes and Infection	2003
Use of the A2A adenosine receptor as a physiological immunosuppressor and to engineer inflammation in vivo MV Sitkovsky	Biochemical Pharmacology	2003
Functional expression of adenosine A2A and A3 receptors in the mouse dendritic cell line XS-106 JM Dickenson, S Reeder, B Rees, S Alexander, D Kendall	European Journal of Pharmacology	2003
Inhibition of the neutrophil NADPH oxidase by adenosine is associated with increased movement of flavocytochrome b between subcellular fractions Steve D Swain, Daniel W Siemsen, Laura K Nelson, Karen M Sipes, Angela J Hanson, Mark T Quinn	Inflammation	2003
Adenosine Promotes Wound Healing and Mediates Angiogenesis in Response to Tissue Injury Via Occupancy of A2A Receptors MC Montesinos, A Desai, JF Chen, H Yee, MA Schwarzschild, JS Fink, BN Cronstein	The American Journal of Pathology	2002
Activation of Adenosine A2a Receptor Pathway Reduces Leukocyte Infiltration but Enhances Edema Formation in Rat Caerulein Pancreatitis A Satoh, K Satoh, A Masamune, T Yamagiwa, T Shimosegawa	Pancreas	2002
Provocation with adenosine 5'-monophosphate as a marker of inflammation in asthma, allergic rhinitis and chronic obstructive pulmonary disease M Berge, HA Kerstjens, DS Postma	Clinical & Experimental Allergy	2002
Purine, kynurenine, neopterin and lipid peroxidation levels in inflammatory bowel disease CM Forrest, P Youd, A Kennedy, SR Gould, LG Darlington, TW Stone	Journal of Biomedical Science	2002
Effects of adenosine pretreatment on detection of free radicals in ischemic and reperfused canine gracilis muscle flaps by use of spin-trapping electron paramagnetic resonance spectroscopy BA Brisson, CW Miller, G Chen, LJ McCutcheon, EG Janzen	American Journal of Veterinary Research	2002
Targeting Adenosine Receptors: Novel Therapeutic Targets in Asthma and Chronic Obstructive Pulmonary Disease S Rorke, ST Holgate	American Journal of Respiratory Medicine	2002
Adenosine Deaminase Inhibition Attenuates Microvascular Dysfunction and Improves Survival in Sepsis ES Cohen, WR Law, CR Easington, KQ Cruz, BA Nardulli, RA Balk, JE Parrillo, SM Hollenberg	American journal of respiratory and critical care medicine	2002
Adenosine A2A receptor activation decreases reperfusion injury associated with high-flow reperfusion SM Fiser, CG Tribble, AK Kaza, SM Long, JA Kern, DC Cassada, J Linden, J Rieger, VE Laubach, A Matisoff, IL Kron	The Journal of Thoracic and Cardiovascular Surgery	2002
A 2A adenosine receptor: a novel therapeutic target in renal disease MD Okusa	American journal of physiology. Renal physiology	2002
Molecular and Cellular Biology of Neuroprotection in the CNS C Alzheimer		2002
Cyclic AMP-dependent inhibition of human neutrophil oxidative activity by substituted 2-propynylcyclohexyl adenosine A2Areceptor agonists GW Sullivan, JM Rieger, WM Scheld, TL Macdonald, J Linden	British Journal of Pharmacology	2001
New clinical applications of xanthine derivatives: Modulatory actions on leukocyte survival and function K Yasui, A Komiyama	International Journal of Hematology	2001
Systemic adenosine A2A agonist ameliorates ischemic reperfusion injury in the rabbit spinal cord DC Cassada, JJ Gangemi, JM Rieger, J Linden, AK Kaza, SM Long, IL Kron, CG Tribble, JA Kern	The Annals of Thoracic Surgery	2001
A3 receptors mediate rapid inflammatory cell influx into the lungs of sensitized guinea-pigs LM Spruntulis, KJ Broadley	Clinical & Experimental Allergy	2001
Combined use of adenosine and amrinone inhibits reperfusion injury of rat liver K Katsuragi, S Takemura, Y Minamiyama, H Tanaka, K Hirohashi, M Inoue, H Kinoshita	Pathophysiology	2001
Adenosine analogue reduces spinal cord reperfusion injury in a time-dependent fashion DC Cassada, CG Tribble, AK Kaza, SM Fiser, SM Long, J Linden, JM Rieger, IL Kron, JA Kern	Surgery	2001
Selective A 2A adenosine receptor activation reduces skin pressure ulcer formation and inflammation SM Peirce, TC Skalak, JM Rieger, TL Macdonald, J Linden	American journal of physiology. Heart and circulatory physiology	2001
Effects of adenosine on ischaemia-reperfusion injury associated with rat pancreas transplantation F Pi, F Badosa, A Sola, JR Catafau, C Xaus, N Prats, E Gelpi, G Hotter	The British journal of surgery	2001
Purinergic and Pyrimidinergic Signalling II MP Abbracchio, M Williams		2001
Adenosine and cardioprotection during ischaemia and reperfusion - an overview HT Sommerschild, KA Kirkeboen	Acta Anaesthesiologica Scandinavica	2000
A2Aadenosine receptors in human peripheral blood cells S Gessi, K Varani, S Merighi, E Ongini, PA Borea	British Journal of Pharmacology	2000
Therapeutic targeting of adenosine receptors in inflammatory diseases TP Shanley, K Bshesh	Expert Opinion on Therapeutic Targets	2000
Potential of adenosine receptor agonists for the prevention and treatment of coronary artery disease and acute myocardial infarction KL Clark, L Merkel	Expert Opinion on Emerging Drugs	2000
AMP 579, a Novel Adenosine Agonist for the Treatment of Acute Myocardial Infarction KL Clark, L Merkel, P Zannikos, MF Kelley, B Boutouyrie, MH Perrone	Cardiovascular Drug Reviews	2000
Activation of adenosine A1–receptor pathway induces edema formation in the pancreas of rats A Satoh, T Shimosegawa, K Satoh, H Ito, Y Kohno, A Masamune, M Fujita, T Toyota	Gastroenterology	2000
Adenosine and chronic ischemia of the lower limbs FL Pasini, PL Capecchi, TD Perri	Vascular medicine (London, England)	2000
Ketamine Modulates the Stimulated Adhesion Molecule Expression on Human Neutrophils In Vitro: MA Weigand, H Schmidt, Q Zhao, K Plaschke, E Martin, HJ Bardenheuer	Anesthesia & Analgesia	2000
Brief Antecedent Ischemia Enhances Recombinant Tissue Plasminogen Activator–Induced Coronary Thrombolysis by Adenosine-Mediated Mechanism K Przyklenk, P Whittaker	Circulation	2000
Methotrexate BN Cronstein, JR Bertino		2000
Adenosine receptor occupancy suppresses chemoattractant-induced phospholipase D activity by diminishing membrane recruitment of small GTPases N Thibault, D Harbour, P Borgeat, PH Naccache, SG Bourgoin	Blood	2000
Plasma and rectal adenosine in inflammatory bowel disease: Effect of methotrexate LJ Egan, WJ Sandborn, DC Mays, WJ Tremaine, JJ Lipsky	Inflammatory Bowel Diseases	1999
A1 adenosine receptors in human neutrophils: Direct binding and electron microscope visualization A Falleni, ML Trincavelli, M Macchia, F Salvetti, M Hamdan, F Calvani, V Gremigni, A Lucacchini, C Martini	Journal of Cellular Biochemistry	1999
Selective adenosine-A2A activation reduces lung reperfusion injury following transplantation SD Ross, CG Tribble, J Linden, JJ Gangemi, BC Lanpher, AY Wang, IL Kron	The Journal of Heart and Lung Transplantation	1999
Acute paw oedema induced by local injection of adenosine A1, A2 and A3 receptor agonists J Sawynok, A Reid, XJ Liu	European Journal of Pharmacology	1999
Exogenous cyclic AMP, cholera toxin, and endotoxin induce expression of the lipopolysaccharide receptor CD14 in murine bone marrow cells: role of purinoreceptors T Pedron, R Girard, R Chaby	Clinical and diagnostic laboratory immunology	1999
Plasma and Rectal Adenosine in Inflammatory Bowel Disease: Effect of Methotrexate: LJ Egan, WJ Sandborn, DC Mays, WJ Tremaine, JJ Lipsky	Inflammatory Bowel Diseases	1999
Taurine Potentiates the Efficacy of Hypothermia N Ohno, KJ Miyamoto, TA Miyamoto	Asian Cardiovascular and Thoracic Annals	1999
Molecular and Cellular Basis of Inflammation CN Serhan, PA Ward		1999
Lipoxygenases and their Metabolites S Nigam, CR Pace-Asciak		1999
Endogenous adenosine inhibits P-selectin-dependent formation of coronary thromboemboli during hypoperfusion in dogs T Minamino, M Kitakaze, H Asanuma, Y Tomiyama, M Shiraga, H Sato, Y Ueda, H Funaya, T Kuzuya, Y Matsuzawa, M Hori	Journal of Clinical Investigation	1998
Alternative Therapies for Vasculitis and Proliferative Nephritides: The Role of Cyclic AMP Elevating Agents EN Wardle	Renal Failure	1998
Role of A2A adenosine receptors in inflammation GW Sullivan, J Linden	Drug Development Research	1998
Pharmacological characterization of AMP 579, a novel adenosine A1/A2 receptor agonist and cardioprotective L Merkel, CJ Rojas, MF Jarvis, BF Cox, C Fink, GJ Smits, AP Spada, MH Perrone, KL Clark	Drug Development Research	1998
Modulation of the chemotactic peptide- and immunoglobulin G-triggered respiratory burst in human neutrophils by exogenous and endogenous adenosine S Zalavary, T Bengtsson	European Journal of Pharmacology	1998
Adhesion of neutrophils to cultured human endothelial cells is enhanced by stimulation of adenosine A1-receptors S Zahler, BF Becker	Drug Development Research	1998
Adenosine A2A receptors of human circulating blood elements K Varani, S Gessi, S Merighi, E Ongini, PA Borea	Drug Development Research	1998
Further pharmacological characterization of the adenosine receptor subtype mediating inhibition of oxidative burst in human isolated neutrophils JP Hannon, KM Bray-French, RM Phillips, JR Fozard	Drug Development Research	1998
[3H]-SCH 58261 labelling of functional A2Aadenosine receptors in human neutrophil membranes K Varani, S Gessi, S Dionisotti, E Ongini, PA Borea	British Journal of Pharmacology	1998
Effects of cyclosporine A and methotrexate on CD18 expression in recipients of rat cardiac allografts CJ Ciesielski, J Mei, LA Piccinini	Transplant Immunology	1998
Adenosine Receptor Mediates Motility in Human Melanoma Cells EC Woodhouse, DF Amanatullah, JA Schetz, LA Liotta, ML Stracke, T Clair	Biochemical and Biophysical Research Communications	1998
Adenosine receptors: new opportunities for future drugs SA Poulsen, RJ Quinn	Bioorganic & Medicinal Chemistry	1998
Differential Regulation of Human Neutrophil FcγRIIa (CD32) and FcγRIIIb (CD16)-induced Ca 2+ Transients JC Edberg, JJ Moon, DJ Chang, RP Kimberly	The Journal of biological chemistry	1998
Preconditioning and adenosine in I/R-induced leukocyte-endothelial cell interactions P Kubes, D Payne, L Ostrovsky	American journal of physiology. Heart and circulatory physiology	1998
Cardiovascular Biology of Purines G Burnstock, JG Dobson, BT Liang, J Linden		1998
Purine and Pyrimidine Metabolism in Man IX A Griesmacher, MM Müller, P Chiba		1998
Chemical modifications of striatal A2A adenosine receptors: a possible role for tyrosine at the ligand binding sites C Martini, L Trincavelli, A Lucacchini	Biochimica et Biophysica Acta (BBA) - Biomembranes	1997
Making sense of asthma PJ Richardson	Expert Opinion on Investigational Drugs	1997
Purines and neutrophil leukocytes BB Fredholm	General Pharmacology: The Vascular System	1997
Nucleotide Binding to Autotaxin: Crosslinking of Bound Substrate Followed by lysC Digestion Identifies Two Labeled Peptides T Clair, HC Krutzsch, LA Liotta, ML Stracke	Biochemical and Biophysical Research Communications	1997
Cardioprotection with a novel adenosine regulating agent mediated by intravascular adenosine MA Kurz, DA Bullough, CJ Buggé, KM Mullane, MA Young	European Journal of Pharmacology	1997
Adenosine, Cardioprotection and Its Clinical Application RM Mentzer, M Kitakaze, JM Downey, M Hori		1997
Neutrophil migration, oxidative metabolism, and adhesion in elderly and young subjects D Biasi, A Carletto, C Dell'agnola, P Caramaschi, F Montesanti, G Zavateri, S Zeminian, P Bellavite, LM Bambara	Inflammation	1996
Purinergic mechanisms in inflammation BN Cronstein, MG Bouma, BF Becker	Drug Development Research	1996
Molecular therapeutics. Methotrexate and its mechanism of action BN Cronstein	Arthritis & Rheumatism	1996
Effect of Cyclic AMP Level Reduction on Human Neutrophil Responses to Formylated Peptides S Spisani, M Pareschi, M Buzzi, M Colamussi, C Biondi, S Traniello, G Zecchini, M Paradisi, I Torrini, M Ferretti	Cellular Signalling	1996
Anti-inflammatory effects of adenosine kinase inhibitors in acute and chronic inflammation GS Firestein	Drug Development Research	1996
Adenosine physiology and pharmacology: How about A2 receptors? JL Daval, F Nicolas, JF Doriat	Pharmacology & Therapeutics	1996
Inhibition of glycolysis and enhanced mechanical function of working rat hearts as a result of adenosine A1 receptor stimulation during reperfusion following ischaemia BA Finegan, GD Lopaschuk, M Gandhi, AS Clanachan	British Journal of Pharmacology	1996
Adenosine A2 receptor-induced inhibition of leukotriene B4 synthesis in whole blood ex vivo E Krump, G Lemay, P Borgeat	British Journal of Pharmacology	1996
Biomembranes: A Multi-Volume Treatise KJ Clemetson	Biomembranes: A Multi-Volume Treatise	1996
G-Protein-coupled receptors in HL-60 human leukemia cells JF Klinker, K Wenzel-Seifert, R Seifert	General Pharmacology: The Vascular System	1996
Sulfatide-induced L-selectin activation generates intracellular oxygen radicals in human neutrophils: modulation by extracellular adenosine T Bengtsson, M Grenegård, A Olsson, F Sjögren, O Stendahl, S Zalavary	Biochimica et Biophysica Acta	1996
Adenosine A 2 Receptor Occupancy Regulates Stimulated Neutrophil Function via Activation of a Serine/Threonine Protein Phosphatase S Revan, MC Montesinos, D Naime, S Landau, BN Cronstein	The Journal of biological chemistry	1996
Identification of a Bacterial Inhibitor of Protein Kinases: MECHANISM AND ROLE IN HOST CELL INVASION SA Berger, K Rowan, HD Morrison, HJ Ziltener	The Journal of biological chemistry	1996
Purines and Myocardial Protection AS Abd-Elfattah, AS Wechsler		1996
Effects of adenosine on guinea pig pulmonary eosinophils BA Walker	Inflammation	1996
Adenosine A2A receptors mediate the inhibitory effect of adenosine on formyl-Met-Leu-Phe-stimulated respiratory burst in neutrophil leucocytes BB Fredholm, Y Zhang, I van der Ploeg	Naunyn-Schmiedeberg's Archives of Pharmacology	1996
Auranofin and its combination with LTB4 influences ATP level and migration of human polymorphonuclear cells in vitro G Partsch, M Matucci-Cerinic	Inflammation	1995
Methylxanthines with adenosine alter TNFα-primed PMN activation GW Sullivan, LS Luong, HT Carper, RC Barnes, GL Mandell	Immunopharmacology	1995
Adenosine modulation of tumor necrosis factor-α-induced neutrophil activation CR Barnes, GL Mandell, HT Carper, S Luong, GW Sullivan	Biochemical Pharmacology	1995
Heterogeneity of circulating and exudated polymorphonuclear leukocytes in superoxide-generating response to cyclic AMP and cyclic AMP-elevating agents LY Al-Essa, M Niwa, KI Kohno, M Nozaki, K Tsurumi	Biochemical Pharmacology	1995
Human neutrophil (PMN) oxygen radical production and the cytoskeleton ME Wilesαβ, JA Dykensα, CD Wrightαγ	Life Sciences	1995
The A Adenosine Receptor Mediates cAMP Responses to Adenosine Receptor Agonists in Human Intestinal Epithelia GR Strohmeier, SM Reppert, WI Lencer, JL Madara	The Journal of biological chemistry	1995
Activation of Protein Kinase C Increases Adenosine Production in the Hypoxic Canine Coronary Artery Through the Extracellular Pathway T Minamino, M Kitakaze, K Komamura, K Node, H Takeda, M Inoue, M Hori, T Kamada	Arteriosclerosis, thrombosis, and vascular biology	1995
α 1 -Adrenoceptor Activation Increases Ecto-5′-Nucleotidase Activity and Adenosine Release in Rat Cardiomyocytes by Activating Protein Kinase C M Kitakaze, M Hori, T Morioka, T Minamino, S Takashima, Y Okazaki, K Node, K Komamura, K Iwakura, T Itoh, M Inoue, T Kamada	Circulation	1995
Adenosine and Adenine Nucleotides: From Molecular Biology to Integrative Physiology L Belardinelli, A Pelleg		1995
Airways Smooth Muscle: Neurotransmitters, Amines, Lipid Mediators and Signal Transduction D Raeburn, MA Giembycz		1995
3H-NECA Binding to Polymorphonuclear Membrane: Effect of Sera from Patients with Hodgkin's Disease R Polidori, P Tacchi, A Azrará, C Martini, A Lucacchini, MP Ferrara, F Ambrogi	Cancer Investigation	1994
Cloning and characterization of a pharmacologically distinct A1 adenosine receptor from guinea pig brain FM Xie, D Chalmers, C Morgan, SJ Watson, H Akil	Molecular Brain Research	1994
Propentofylline enhancement of the actions of adenosine on neutrophil leukocytes Y Zhang, BB Fredholm	Biochemical Pharmacology	1994
Adenosine modulation of primed human neutrophils C Dianzani, S Brunelleschi, I Viano, R Fantozzi	European Journal of Pharmacology	1994
Myocardial infarction and purine transport inhibition in anaesthetised ferrets SM Poucher, R Brooks, RM Pleeth, AR Conant, MG Collis	European Journal of Pharmacology	1994
The role of cyclic AMP, calcium and filamentous actin in adenosine modulation of Fc receptor-mediated phagocytosis in human neutrophils S Zalavary, O Stendahl, T Bengtsson	Biochimica et Biophysica Acta (BBA) - Molecular Cell Research	1994
Purine and Pyrimidine Metabolism in Man VIII A Sahota, MW Taylor		1994
A1 adenosine receptors. Two amino acids are responsible for species differences in ligand recognition AL Tucker, AS Robeva, HE Taylor, D Holeton, M Bockner, KR Lynch, J Linden	The Journal of biological chemistry	1994
Complete prevention of postischemic spinal cord injury by means of regional infusion with hypothermic saline and adenosine JA Herold, IL Kron, SE Langenburg, LH Blackbourne, CG Tribble	The Journal of Thoracic and Cardiovascular Surgery	1994
Nonsteroidal antiinflammatory agents inhibit stimulated neutrophil adhesion to endothelium: Adenosine dependent and independent mechanisms BN Cronstein, MV Stouwe, L Druska, RI Levin, G Weissmann	Inflammation	1994
The antiinflammatory mechanism of methotrexate. Increased adenosine release at inflamed sites diminishes leukocyte accumulation in an in vivo model of inflammation BN Cronstein, D Naime, E Ostad	Journal of Clinical Investigation	1993
Brief myocardial ischemia affects free radical generating and scavenging systems in dogs S Hoshida, T Kuzuya, N Yamashita, H Oe, H Fuji, M Hori, M Tada, T Kamada	Heart and Vessels	1993
Adenosine inhibits platelet-activating factor, but not tumour necrosis factor-alpha-induced priming of human neutrophils AG Stewart, T Harris	Immunology	1993
The antiarrhythmic effects of the nucleoside transporter inhibitor, R75231, in anaesthetized pigs CL Wainwright, JR Parratt, HV Belle	British Journal of Pharmacology	1993
Immunophysiology of the Gut EB Chang, MW Musch	Immunophysiology of the Gut	1993
Airway Responsiveness to Adenosine 5′-Monophosphate in Chronic Obstructive Pulmonary Disease Is Determined by Smoking Y Oosterhoff, JW de Jong, MA Jansen, GH Koëter, DS Postma	American journal of respiratory and critical care medicine	1993
Acting via A2 Receptors, Adenosine Inhibits the Upregulation of Mac-1 (CD11b/CD18) Expression on FMLP-stimulated Neutrophils A Wollner, S Wollner, JB Smith	American journal of respiratory cell and molecular biology	1993
Inhibition of human monocyte TNF production by adenosine receptor agonists VL Vraux, YL Chen, I Masson, MD Sousa, JP Giroud, I Florentin, L Chauvelot-Moachon	Life Sciences	1993
Cardioplegia Solution J Golembiewski, N Bourtsos	Journal of Pharmacy Practice	1993
Leukocyte adherence in rat mesenteric venules: Effects of adenosine and methotrexate H Asako, RE Wolf, DN Granger	Gastroenterology	1993
Signal transduction via P2-purinergic receptors for extracellular ATP and other nucleotides GR Dubyak, C el-Moatassim	American journal of physiology. Cell physiology	1993
Adenosine inhibits fMLP-stimulated adherence and superoxide anion generation by human neutrophils at an early step in signal transduction TH Burkey, RO Webster	Biochimica et Biophysica Acta (BBA) - Molecular Cell Research	1993
Attenuation of ecto-5'-nucleotidase activity and adenosine release in activated human polymorphonuclear leukocytes M Kitakaze, M Hori, T Morioka, S Takashima, T Minamino, H Sato, M Inoue, T Kamada	Circulation research	1993
Adenosine alters glucose use during ischemia and reperfusion in isolated rat hearts BA Finegan, GD Lopaschuk, CS Coulson, AS Clanachan	Circulation	1993
GTPases in Biology II BF Dickey, L Birnbaumer		1993
Chirurgisches Forum ’93 für experimentelle und klinische Forschung HM Becker, HG Beger, W Hartel		1993
Is granulocyte or endothelial cell activation responsible for the initiation of granulocyte recruitment during acute inflammation CJ Whelan	Agents and Actions	1992
CGS 21680: A Potent Selective Adenosine A2Receptor Agonist RL Webb, MA Sills, JP Chovan, JL Balwierczak, JE Francis	Cardiovascular Drug Reviews	1992
Adenosine receptors on human leukocytes IV. characterization of an A1/Ri receptor G Marone, R Petracca, S Vigorita, A Genovese, V Casolaro	International Journal of Clinical & Laboratory Research	1992
Neutrophils from asthmatics exhibit diminished responsiveness to 2-chloroadenosine which is reversed by theophylline BZ Joseph, AM Sustiel, L Borish	Inflammation	1992
Release of adenosine from human neutrophils stimulated by platelet activating factor, leukotriene B(4) and opsonized zymosan S Sipka, Z Dinya, M Koltai, P Braquet, G Szegedi	Mediators of Inflammation	1992
Stimulus-response uncoupling in the neutrophil. Adenosine A2-receptor occupancy inhibits the sustained, but not the early, events of stimulus transduction in human neutrophils by a mechanism independent of actin-filament formation BN Cronstein, KA Haines	Biochemical Journal	1992
Neutrophils from asthmatics exhibit diminished responsiveness to 2-chloroadenosine which is reversed by theophylline: Evidence for a cyclic-AMP-independent pathway on human neutrophils BZ Joseph, AM Sustiel, L Borish	Inflammation	1992
Chemical Modification and Irreversible Inhibition of Striatal A2a Adenosine Receptors KA Jacobson, GL Stiles, XD Ji	Molecular pharmacology	1992
Ca2+-Dependent and Ca2+-independent mechanisms modulate whole-cell cationic currents in human neutrophils MA Schumann, T Tanigaki, DN Heller, TA Raffin	Biochemical and Biophysical Research Communications	1992
Adenosine receptors: pharmacology, structure-activity relationships, and therapeutic potential KA Jacobson, PJ van Galen, M Williams	Journal of Medicinal Chemistry	1992
Adenosine Receptors: Pharmacology, Structure–Activity Relationships, and Therapeutic Potential KA Jacobson, PJ van Galen, M Williams	Journal of Medicinal Chemistry	1992
Protective effects of adenosine in myocardial ischemia SW Ely, RM Berne	Circulation	1992
Modulation of neutrophil functions by activated platelet release factors S Spisani, AL Giuliani, T Cavalletti, M Zaccarini, L Milani, R Gavioli, S Traniello	Inflammation	1992
Asthma Treatment D Olivieri, PJ Barnes, SS Hurd, GC Folco		1992
Biochemistry of Inflammation JT Whicher, SW Evans		1992
Dual regulation of arachidonic acid release by P2U purinergic receptors in dibutyryl cyclic AMP-differentiated HL60 cells M Xing, F Thévenod, R Mattera	The Journal of biological chemistry	1992
The cell biology of ischemic renal injury JM Weinberg	Kidney International	1991
Inhibition of Neutrophil Superoxide Production by Adenosine Released from Vascular Endothelial Cells G Gunther, M Herring	Annals of Vascular Surgery	1991
Purinergic regulation of bradykinin-induced plasma extravasation and adjuvant-induced arthritis in the rat PG Green, AI Basbaum, C Helms, JD Levine	Proceedings of the National Academy of Sciences	1991
Role of Uric Acid as an Endogenous Radical Scavenger and Antioxidant BF Becker, N Reinholz, B Leipert, P Ruschke, B Permanetter, E Gerlach	Chest	1991
Microcirculatory dysfunction following perfusion with hyperkalemic, hypothermic, cardioplegic solutions and blood reperfusion. Effects of adenosine MW Keller, L Geddes, W Spotnitz, S Kaul, BR Duling	Circulation	1991
Drug Antioxidant Effects: A Basis for Drug Selection? B Halliwell	Drugs	1991

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The adenosine/neutrophil paradox resolved: human neutrophils possess both A1 and A2 receptors that promote chemotaxis and inhibit O2 generation, respectively.

The adenosine/neutrophil paradox resolved: human neutrophils possess both A1 and A2 receptors that promote chemotaxis and inhibit O2 generation, respectively.

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