Modulation of innate immunity by adenosine receptor stimulation

Shock

Volumn 36, Issue 3, 2011, Pages 208-215

  Ramakers, Bart P ^a   Riksen, Niels P ^a   Van Der Hoeven, Johannes G ^a   Smits, Paul ^a   Pickkers, Peter ^a  

^a RADBOUD UNIVERSITY MEDICAL CENTER   (Netherlands)

Author keywords

Adenosine; adenosine metabolism; adenosine receptors; inflammation; sepsis

Indexed keywords

5' NUCLEOTIDASE; ADENOSINE A1 RECEPTOR; ADENOSINE A2 RECEPTOR; ADENOSINE DEAMINASE; ADENOSINE KINASE; ADENOSINE PHOSPHATE; ADENOSINE RECEPTOR; ADENOSINE RECEPTOR BLOCKING AGENT; ADENOSINE RECEPTOR STIMULATING AGENT; CAFFEINE; CALCIUM CHANNEL; CXCL3 CHEMOKINE; CYCLIC AMP; EQUILIBRATIVE NUCLEOSIDE TRANSPORTER; G PROTEIN COUPLED RECEPTOR; HOMOCYSTEINE; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; INTERLEUKIN 6; NUCLEOSIDE TRANSPORTER; PHOSPHODIESTERASE INHIBITOR; POTASSIUM CHANNEL;

CELL PROTECTION; CELL TYPE; HUMAN; HYPOXIA; IMMUNOMODULATION; IN VITRO STUDY; INFLAMMATION; INNATE IMMUNITY; KNOCKOUT GENE; NONHUMAN; REVIEW; SEPSIS; SIGNAL TRANSDUCTION;

ADENOSINE; ANIMALS; HUMANS; IMMUNITY, INNATE; RECEPTOR, ADENOSINE A2A; RECEPTOR, ADENOSINE A2B; RECEPTOR, ADENOSINE A3; RECEPTORS, PURINERGIC P1; SEPSIS;

EID: 80052037502     PISSN: 10732322     EISSN: 15400514     Source Type: Journal    
DOI: 10.1097/SHK.0b013e318225aee4     Document Type: Review

References (81)

1. Bernard GR, Vincent JL, Laterre PF, LaRosa SP, Dhainaut JF, Lopez-Rodriguez A, Steingrub JS, Garber GE, Helterbrand JD, Ely EW, et al.: Efficacy and safety of recombinant human activated protein C for severe sepsis. N Engl J Med 344: 699-709, 2001. (Pubitemid 32204987)
2. Annane D, Sebille V, Charpentier C, Bollaert PE, Francois B, Korach JM, Capellier G, Cohen Y, Azoulay E, Troche G, et al.: Effect of treatment with low doses of hydrocortisone and fludrocortisone on mortality in patients with septic shock. JAMA 288:862-871, 2002.
3. Webster NR, Galley HF: Immunomodulation in the critically ill. Br J Anaesth 103:70-81, 2009.
4. JungerWG: Immune cell regulation by autocrine purinergic signalling. Nat Rev Immunol 11:201-212, 2011.
5. Drury AN, Szent-Gyorgyi A: The physiological activity of adenine compounds with especial reference to their action upon the mammalian heart. J Physiol 68:213-237, 1929.
6. Martin C, Leone M, Viviand X, Ayem ML, Guieu R: High adenosine plasma concentration as a prognostic index for outcome in patients with septic shock. Crit Care Med 28:3198-3202, 2000.
7. Hasko G, Linden J, Cronstein B, Pacher P: Adenosine receptors: therapeutic aspects for inflammatory and immune diseases. Nat Rev Drug Discov 7:759-770, 2008.
8. Ohta A, Sitkovsky M: Role of G-proteinYcoupled adenosine receptors in downregulation of inflammation and protection from tissue damage. Nature 414:916-920, 2001. (Pubitemid 34024743)
9. Newby AC: Adenosine and the concept of Fretaliatory metabolites. Trends Biochem Sci 9:42-44, 1984.
10. Fredholm BB, IJzerman AP, Jacobson KA, Klotz KN, Linden J: International Union of Pharmacology. XXV. Nomenclature and classification of adenosine receptors. Pharmacol Rev 53:527-552, 2001. (Pubitemid 33136237)
11. Rongen GA, Floras JS, Lenders JW, Thien T, Smits P: Cardiovascular pharmacology of purines. Clin Sci (Lond) 92:13-24, 1997. (Pubitemid 27033006)
12. Deussen A: Metabolic flux rates of adenosine in the heart. Naunyn Schmiedebergs Arch Pharmacol 362:351-363, 2000.
13. Gorlach A: Control of adenosine transport by hypoxia. Circ Res 97:1-3, 2005. (Pubitemid 40982315)
14. Kobayashi S, Zimmermann H, Millhorn DE: Chronic hypoxia enhances adenosine release in rat PC12 cells by altering adenosine metabolism and membrane transport. J Neurochem 74:621-632, 2000. (Pubitemid 30053734)
15. Decking UK, Schlieper G, Kroll K, Schrader J: Hypoxia-induced inhibition of adenosine kinase potentiates cardiac adenosine release. Circ Res 81: 154-164, 1997. (Pubitemid 27342482)
16. Nakav S, Naamani O, Chaimovitz C, Shaked G, Czeiger D, Zlotnik M, Douvdevani A: Regulation of adenosine system at the onset of peritonitis. Nephrol Dial Transplant 25:931-939, 2010.
17. Ramakers BP, Riksen NP, van den Broek P, Franke B, Peters WH, van der Hoeven JG, Smits P, Pickkers P: Circulating adenosine increases during human experimental endotoxemia but blockade of its receptor does not influence the immune response and subsequent organ injury. Crit Care 15(1):R3, 2011. [Epub ahead of print].
18. Fredholm BB, Battig K, Holmen J, Nehlig A, Zvartau EE: Actions of caffeine in the brain with special reference to factors that contribute to its widespread use. Pharmacol Rev 51:83-133, 1999. (Pubitemid 29113867)
19. Jacobson KA, Gao ZG: Adenosine receptors as therapeutic targets. Nat Rev Drug Discov 5:247-264, 2006. (Pubitemid 43336037)
20. Csoka B, Hasko G: Adenosine, inflammation pathways and therapeutic challenges. Joint Bone Spine 78:4-6, 2011.
21. Murphree LJ, Sullivan GW, Marshall MA, Linden J: Lipopolysaccharide rapidly modifies adenosine receptor transcripts in murine and human macrophages: role of NF-kappaB in A(2A) adenosine receptor induction. Biochem J 391:575-580, 2005. (Pubitemid 41634783)
22. Kreth S, Kaufmann I, Ledderose C, Luchting B, Thiel M: Reduced ligand affinity leads to an impaired function of the adenosine A2A receptor of human granulocytes in sepsis. J Cell Mol Med 13:985-994, 2009.
23. Hasko G, Cronstein BN: Adenosine: an endogenous regulator of innate immunity. Trends Immunol 25:33-39, 2004. (Pubitemid 38032805)
24. Fredholm BB: Adenosine, an endogenous distress signal, modulates tissue damage and repair. Cell Death Differ 14:1315-1323, 2007. (Pubitemid 46965261)
25. Cronstein BN, Daguma L, Nichols D, Hutchison AJ, Williams M: The adenosine/neutrophil paradox resolved: human neutrophils possess both A1 and A2 receptors that promote chemotaxis and inhibit O2 generation, respectively. J Clin Invest 85:1150-1157, 1990. (Pubitemid 20123757)
26. Gallos G, Ruyle TD, Emala CW, Lee HT: A1 adenosine receptor knockout mice exhibit increased mortality, renal dysfunction, and hepatic injury in murine septic peritonitis. Am J Physiol Renal Physiol 289:F369-F376, 2005. (Pubitemid 41003666)
27. Nemeth ZH, Csoka B, Wilmanski J, Xu D, Lu Q, Ledent C, Deitch EA, Pacher P, Spolarics Z, Hasko G: Adenosine A2A receptor inactivation increases survival in polymicrobial sepsis. J Immunol 176:5616-5626, 2006.
28. Belikoff B, Hatfield S, Sitkovsky M, Remick DG: Adenosine negative feedback on A2A adenosine receptors mediates hypo-responsiveness in chronically septic mice. Shock 35:382-387, 2011.
29. Yang D, Zhang Y, Nguyen HG, Koupenova M, Chauhan AK, Makitalo M, Jones MR, St HC, Seldin DC, Toselli P, et al.: The A2B adenosine receptor protects against inflammation and excessive vascular adhesion. J Clin Invest 116:1913-1923, 2006. (Pubitemid 44033315)
30. Csoka B, Nemeth ZH, Rosenberger P, Eltzschig HK, Spolarics Z, Pacher P, Selmeczy Z, Koscso B, Himer L, Vizi ES, et al.: A(2B) adenosine receptors protect against sepsis-induced mortality by dampening excessive inflammation. J Immunol 185:542-550, 2010.
31. Belikoff BG, Hatfield S, Georgiev P, Ohta A, Lukashev D, Buras JA, Remick DG, Sitkovsky M: A2B adenosine receptor blockade enhances macrophagemediated bacterial phagocytosis and improves polymicrobial sepsis survival in mice. J Immunol 186:2444-2453, 2011.
32. Salvatore CA, Tilley SL, Latour AM, Fletcher DS, Koller BH, Jacobson MA: Disruption of the A(3) adenosine receptor gene in mice and its effect on stimulated inflammatory cells. J Biol Chem 275:4429-4434, 2000. (Pubitemid 30094686)
33. Lee HT, Kim M, Joo JD, Gallos G, Chen JF, Emala CW: A3 adenosine receptor activation decreases mortality and renal and hepatic injury in murine septic peritonitis. Am J Physiol Regul Integr Comp Physiol 291:R959-R969, 2006. (Pubitemid 44498436)
34. Kumar V, Sharma A: Adenosine: an endogenous modulator of innate immune system with therapeutic potential. Eur J Pharmacol 616:7-15, 2009.
35. Nakav S, Chaimovitz C, Sufaro Y, Lewis EC, Shaked G, Czeiger D, Zlotnik M, Douvdevani A: Anti-inflammatory preconditioning by agonists of adenosine A1 receptor. PLoS One 3:e2107, 2008.
36. Gessi S, Varani K, Merighi S, Ongini E, Borea PA: A(2A) adenosine receptors in human peripheral blood cells. Br J Pharmacol 129:2-11, 2000. (Pubitemid 30072665)
37. Bouma MG, Stad RK, van den Wildenberg FA, Buurman WA: Differential regulatory effects of adenosine on cytokine release by activated human monocytes. J Immunol 153:4159-4168, 1994. (Pubitemid 24322583)
38. Hamano R, Takahashi HK, Iwagaki H, Kanke T, Liu K, Yoshino T, Sendo T, Nishibori M, Tanaka N: Stimulation of adenosine A2A receptor inhibits LPSinduced expression of intercellular adhesion molecule 1 and production of TNF-alpha in human peripheral blood mononuclear cells. Shock 29: 154-159, 2008.
39. Le MO, Stordeur P, Schandene L, Marchant A, de GD, Goldman M, Deviere J: Adenosine enhances IL-10 secretion by human monocytes. J Immunol 156:4408-4414, 1996. (Pubitemid 26165841)
40. Kaufmann I, Hoelzl A, Schliephake F, Hummel T, Chouker A, Lysenko L, Peter K, Thiel M: Effects of adenosine on functions of polymorphonuclear leukocytes from patients with septic shock. Shock 27:25-31, 2007. (Pubitemid 44968006)
41. Kreckler LM, Wan TC, Ge ZD, Auchampach JA: Adenosine inhibits tumor necrosis factor-alpha release from mouse peritoneal macrophages via A2A and A2B but not the A3 adenosine receptor. J Pharmacol Exp Ther 317:172-180, 2006.
42. Nemeth ZH, Lutz CS, Csoka B, Deitch EA, Leibovich SJ, Gause WC, Tone M, Pacher P, Vizi ES, Hasko G: Adenosine augments IL-10 production by macrophages through an A2B receptor-mediated posttranscriptional mechanism. J Immunol 175:8260-8270, 2005. (Pubitemid 41798391)
43. Wakai A, Wang JH, Winter DC, Street JT, O'Sullivan RG, Redmond HP: Adenosine inhibits neutrophil vascular endothelial growth factor release and transendothelial migration via A2B receptor activation. Shock 15: 297-301, 2001. (Pubitemid 33596722)
44. Sun CX, Zhong H, Mohsenin A, Morschl E, Chunn JL, Molina JG, Belardinelli L, Zeng D, Blackburn MR: Role of A2B adenosine receptor signaling in adenosine-dependent pulmonary inflammation and injury. J Clin Invest 116: 2173-2182, 2006. (Pubitemid 44162326)
45. Martin L, Pingle SC, Hallam DM, Rybak LP, Ramkumar V: Activation of the adenosine A3 receptor in RAW 264.7 cells inhibits lipopolysaccharidestimulated tumor necrosis factor-alpha release by reducing calcium-dependent activation of nuclear factor-kappaB and extracellular signal-regulated kinase 1/2. J Pharmacol Exp Ther 316:71-78, 2006. (Pubitemid 41832582)
46. van der HD, Wan TC, Auchampach JA: Activation of the A(3) adenosine receptor suppresses superoxide production and chemotaxis of mouse bone marrow neutrophils. Mol Pharmacol 74:685-696, 2008.
47. Gessi S, Varani K, Merighi S, Cattabriga E, Iannotta V, Leung E, Baraldi PG, Borea PA: A(3) adenosine receptors in human neutrophils and promyelocytic HL60 cells: a pharmacological and biochemical study. Mol Pharmacol 61:415-424, 2002. (Pubitemid 34112817)
48. Inoue Y, Chen Y, Hirsh MI, Yip L, Junger WG: A3 and P2-2 receptors control the recruitment of neutrophils to the lungs in a mouse model of sepsis. Shock 30:173-177, 2008.
49. Chen Y, Hashiguchi N, Yip L, Junger WG: Hypertonic saline enhances neutrophil elastase release through activation of P2 and A3 receptors. Am J Physiol Cell Physiol 290:C1051-C1059, 2006.
50. Inoue Y, Tanaka H, Sumi Y, Woehrle T, Chen Y, Hirsh MI, Junger WG: A3 adenosine receptor inhibition improves the efficacy of hypertonic saline resuscitation. Shock 35:178-183, 2011.
51. Hasko G, Szabo C, Nemeth ZH, Kvetan V, Pastores SM, Vizi ES: Adenosine receptor agonists differentially regulate IL-10, TNF-alpha, and nitric oxide production in RAW 264.7 macrophages and in endotoxemic mice. J Immunol 157:4634-4640, 1996. (Pubitemid 126449386)
52. Sullivan GW, Fang G, Linden J, Scheld WM: A2A adenosine receptor activation improves survival in mouse models of endotoxemia and sepsis. J Infect Dis 189:1897-1904, 2004. (Pubitemid 38657226)
53. Moore CC, Martin EN, Lee GH, Obrig T, Linden J, Scheld WM: An A2A adenosine receptor agonist, ATL313, reduces inflammation and improves survival in murine sepsis models. BMC Infect Dis 8:141, 2008.
54. Lukashev D, Ohta A, Apasov S, Chen JF, Sitkovsky M: Cutting edge: physiologic attenuation of proinflammatory transcription by the Gs proteinYcoupled A2A adenosine receptor in vivo. J Immunol 173:21-24, 2004. (Pubitemid 38797321)
55. Ryzhov S, Zaynagetdinov R, Goldstein AE, Novitskiy SV, Blackburn MR, Biaggioni I, Feoktistov I: Effect of A2B adenosine receptor gene ablation on adenosine-dependent regulation of proinflammatory cytokines. J Pharmacol Exp Ther 324:694-700, 2008. (Pubitemid 351185857)
56. Hasko G, Nemeth ZH, Vizi ES, Salzman AL, Szabo C: An agonist of adenosine A3 receptors decreases interleukin-12 and interferon-gamma production and prevents lethality in endotoxemic mice. Eur J Pharmacol 358:261-268, 1998. (Pubitemid 28498186)
57. Horrigan LA, Kelly JP, Connor TJ: Caffeine suppresses TNF-alpha production via activation of the cyclic AMP/protein kinase A pathway. Int Immunopharmacol 4:1409-1417, 2004. (Pubitemid 39094414)
58. Horrigan LA, Kelly JP, Connor TJ: Immunomodulatory effects of caffeine: friend or foe? Pharmacol Ther 111:877-892, 2006. (Pubitemid 44118438)
59. Ohta A, Lukashev D, Jackson EK, Fredholm BB, Sitkovsky M: 1,3,7-Trimethylxanthine (caffeine) may exacerbate acute inflammatory liver injury by weakening the physiological immunosuppressive mechanism. J Immunol 179:7431-7438, 2007.
60. Verma R, Huang Z, Deutschman CS, Levy RJ: Caffeine restores myocardial cytochrome oxidase activity and improves cardiac function during sepsis. Crit Care Med 37:1397-1402, 2009.
61. Firestein GS, Boyle D, Bullough DA, Gruber HE, Sajjadi FG, Montag A, Sambol B, Mullane KM: Protective effect of an adenosine kinase inhibitor in septic shock. J Immunol 152:5853-5859, 1994. (Pubitemid 24174165)
62. Firestein GS: Anti-inflammatory effects of adenosine kinase inhibitors in acute and chronic inflammation. Drug Dev Res 39:371-376, 1996. (Pubitemid 27199347)
63. Adanin S, Yalovetskiy IV, Nardulli BA, Sam AD, Jonjev ZS, Law WR: Inhibiting adenosine deaminase modulates the systemic inflammatory response syndrome in endotoxemia and sepsis. Am J Physiol Regul Integr Comp Physiol 282:R1324-R1332, 2002. (Pubitemid 34664516)
64. Tofovic SP, Zacharia L, Carcillo JA, Jackson EK: Inhibition of adenosine deaminase attenuates endotoxin-induced release of cytokines in vivo in rats. Shock 16:196-202, 2001. (Pubitemid 33598197)
65. Noji T, Takayama M, Mizutani M, Okamura Y, Takai H, Karasawa A, Kusaka H: KF24345, an adenosine uptake inhibitor, suppresses lipopolysaccharideinduced tumor necrosis factor-alpha production and leukopenia via endogenous adenosine in mice. J Pharmacol Exp Ther 300:200-205, 2002. (Pubitemid 34028528)
66. Noji T, Nan-ya K, Mizutani M, Katagiri C, Sano J, Takada C, Nishikawa S, Karasawa A, Kusaka H: KF24345, an adenosine uptake inhibitor, ameliorates the severity and mortality of lethal acute pancreatitis via endogenous adenosine in mice. Eur J Pharmacol 454:85-93, 2002. (Pubitemid 35284370)
67. Noji T, Sato H, Sano J, Nishikawa S, Kusaka H, Karasawa A: Treatment with an adenosine uptake inhibitor attenuates glomerulonephritis in mice. Eur J Pharmacol 449:293-300, 2002.
68. Law WR, Conlon BA, Ross JD: The extracellular cardiac purine metabolome in sepsis. Shock 28:259-264, 2007. (Pubitemid 47282015)
69. Jabs CM, Sigurdsson GH, Neglen P: Plasma levels of high-energy compounds compared with severity of illness in critically ill patients in the intensive care unit. Surgery 124:65-72, 1998. (Pubitemid 28354687)
70. Soop A, Johansson C, Hjemdahl P, Kristiansson M, Gyllenhammar H, Li N, Sollevi A: Adenosine treatment attenuates cytokine interleukin-6 responses to endotoxin challenge in healthy volunteers. Shock 19:503-507, 2003.
71. Soop A, Sunden-Cullberg J, Albert J, Hallstrom L, Treutiger CJ, Sollevi A: Adenosine infusion attenuates soluble RAGE in endotoxin-induced inflammation in human volunteers. Acta Physiol (Oxf) 197:47-53, 2009.
72. Ramakers BP, Pickkers P, Deussen A, Rongen GA, van den BP, van der Hoeven JG, Smits P, Riksen NP: Measurement of the endogenous adenosine concentration in humans in vivo: methodological considerations. Curr Drug Metab 9:679-685, 2008.
73. Schmidt WM, Spiel AO, Jilma B, Wolzt M, Muller M: In-vivo effects of simvastatin and rosuvastatin on global gene expression in peripheral blood leucocytes in a human inflammation model. Pharmacogenet Genomics 18: 109-120, 2008.
74. Chavez VR, Ahlawat R, Wills-Karp M, Nathan A, Ezell T, Gauda EB: Correlation between serum caffeine levels and changes in cytokine profile in a cohort of preterm infants. J Pediatr 158:57-64, 64.e1, 2011.
75. Clementina M, Giuseppe S: A2A receptor ligands: past, present and future trends. Curr Top Med Chem 10:902-922, 2010.
76. Gemignani AS, Abbott BG: The emerging role of the selective A2A agonist in pharmacologic stress testing. J Nucl Cardiol 17:494-497, 2010.
77. Mantell SJ, Stephenson PT, Monaghan SM, Maw GN, Trevethick MA, Yeadon M, Keir RF, Walker DK, Jones RM, Selby MD, et al.: Inhaled adenosine A(2A) receptor agonists for the treatment of chronic obstructive pulmonary disease. Bioorg Med Chem Lett 18:1284-1287, 2008. (Pubitemid 351226550)
78. Cerqueira MD: The future of pharmacologic stress: selective A2A adenosine receptor agonists. Am J Cardiol 94:33D-40D, 2004.
79. Silverman MH, Strand V, Markovits D, Nahir M, Reitblat T, Molad Y, Rosner I, Rozenbaum M, Mader R, Adawi M, et al.: Clinical evidence for utilization of the A3 adenosine receptor as a target to treat rheumatoid arthritis: data from a phase II clinical trial. J Rheumatol 35:41-48, 2008.
80. Zhao L, Gray L, Leonardi-Bee J, Weaver CS, Heptinstall S, Bath PM: Effect of aspirin, clopidogrel and dipyridamole on soluble markers of vascular function in normal volunteers and patients with prior ischaemic stroke. Platelets 17: 100-104, 2006. (Pubitemid 43155616)
81. Forrest CM, Stoy N, Stone TW, Harman G, Mackay GM, Oxford L, Darlington LG: Adenosine and cytokine levels following treatment of rheumatoid arthritis with dipyridamole. Rheumatol Int 27:11-17, 2006. (Pubitemid 44655744)