The infarct-sparing effect of IB-MECA against myocardial ischemia/reperfusion injury in mice is mediated by sequential activation of adenosine A3 and A2A receptors

Basic Research in Cardiology

Volumn 110, Issue 2, 2015, Pages 1-12

  Tian, Yikui ^a,c   Marshall, Melissa ^a   French, Brent A ^a   Linden, Joel ^a,b   Yang, Zequan ^a  

^a UNIVERSITY OF VIRGINIA HEALTH SYSTEM   (United States)

^b LA JOLLA INSTITUTE FOR ALLERGY AND IMMUNOLOGY   (United States)

^c TIANJIN MEDICAL UNIVERSITY   (China)

Author keywords

Adenosine; Agonist; Knockout; Myocardial infarction; Receptors

Indexed keywords

6 N (3 IODOBENZYL)ADENOSINE 5' N METHYLCARBOXAMIDE; ADENOSINE A1 RECEPTOR; ADENOSINE A2A RECEPTOR; ADENOSINE A3 RECEPTOR; HISTAMINE; ADENOSINE; N(6)-(3-IODOBENZYL)-5'-N-METHYLCARBOXAMIDOADENOSINE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BINDING AFFINITY; BONE MARROW CELL; CHIMERA; CONTROLLED STUDY; DRUG ACTIVATION; DRUG EFFECT; DRUG RECEPTOR BINDING; HEART INFARCTION; HEART INFARCTION SIZE; HEART PROTECTION; HEART RATE VARIABILITY; HISTAMINE BLOOD LEVEL; HISTAMINE RELEASE; KNOCKOUT MOUSE; MALE; MOUSE; NONHUMAN; RECEPTOR BINDING ASSAY; REPERFUSION INJURY; TREATMENT OUTCOME; ANALOGS AND DERIVATIVES; ANIMAL; C57BL MOUSE; DISEASE MODEL; DRUG EFFECTS; HEMODYNAMICS; METABOLISM;

ADENOSINE; ANIMALS; DISEASE MODELS, ANIMAL; HEMODYNAMICS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MYOCARDIAL INFARCTION; MYOCARDIAL REPERFUSION INJURY; RECEPTOR, ADENOSINE A2A; RECEPTOR, ADENOSINE A3;

EID: 84923810907     PISSN: 03008428     EISSN: 14351803     Source Type: Journal    
DOI: 10.1007/s00395-015-0473-x     Document Type: Article

References (53)

1. Auchampach JA, Ge ZD, Wan TC, Moore J, Gross GJ (2003) A3 adenosine receptor agonist IB-MECA reduces myocardial ischemia-reperfusion injury in dogs. Am J Physiol Heart Circ Physiol 285:H607–H613. doi:10.1152/ajpheart.01001.2002
2. Auchampach JA, Rizvi A, Qiu Y, Tang XL, Maldonado C, Teschner S, Bolli R (1997) Selective activation of A3 adenosine receptors with N6-(3-iodobenzyl)adenosine-5′-N-methyluronamide protects against myocardial stunning and infarction without hemodynamic changes in conscious rabbits. Circ Res 80:800–809. doi:10.1161/01.RES.80.6.800
3. Black RG Jr, Guo Y, Ge ZD, Murphree SS, Prabhu SD, Jones WK, Bolli R, Auchampach JA (2002) Gene dosage-dependent effects of cardiac-specific overexpression of the A3 adenosine receptor. Circ Res 91:165–172. doi:10.1161/01.RES.0000028007.91385.EE
4. Boucher M, Pesant S, Falcao S, de Montigny C, Schampaert E, Cardinal R, Rousseau G (2004) Post-ischemic cardioprotection by A2A adenosine receptors: dependent of phosphatidylinositol 3-kinase pathway. J Cardiovasc Pharmacol 43:416–422. doi:10.1097/00005344-200403000-00013
5. Bouma MG, Jeunhomme TM, Boyle DL, Dentener MA, Voitenok NN, van den Wildenberg FA, Buurman WA (1997) Adenosine inhibits neutrophil degranulation in activated human whole blood: involvement of adenosine A2 and A3 receptors. J Immunol 158:5400–5408
6. Bowlin TL, Borcherding DR, Edwards CK 3rd, McWhinney CD (1997) Adenosine A3 receptor agonists inhibit murine macrophage tumor necrosis factor-alpha production in vitro and in vivo. Cell Mol Biol (Noisy-le-grand) 43:345–349
7. Cerniway RJ, Yang Z, Jacobson MA, Linden J, Matherne GP (2001) Targeted deletion of A(3) adenosine receptors improves tolerance to ischemia-reperfusion injury in mouse myocardium. Am J Physiol Heart Circ Physiol 281:H1751–H1758
8. Day YJ, Huang L, McDuffie MJ, Rosin DL, Ye H, Chen JF, Schwarzschild MA, Fink JS, Linden J, Okusa MD (2003) Renal protection from ischemia mediated by A2A adenosine receptors on bone marrow-derived cells. J Clin Invest 112:883–891. doi:10.1172/JCI15483
9. Du L, Gao ZG, Nithipatikom K, Ijzerman AP, Veldhoven JP, Jacobson KA, Gross GJ, Auchampach JA (2012) Protection from myocardial ischemia/reperfusion injury by a positive allosteric modulator of the A(3) adenosine receptor. J Pharmacol Exp Ther 340:210–217. doi:10.1124/jpet.111.187559
10. Fenster MS, Shepherd RK, Linden J, Duling BR (2000) Activation of adenosine A2 alpha receptors inhibits mast cell degranulation and mast cell-dependent vasoconstriction. Microcirculation 7:129–135. doi:10.1038/sj.mn.7300101
11. Ge ZD, Peart JN, Kreckler LM, Wan TC, Jacobson MA, Gross GJ, Auchampach JA (2006) Cl-IB-MECA [2-chloro-N6-(3-iodobenzyl)adenosine-5′-N-methylcarboxamide] reduces ischemia/reperfusion injury in mice by activating the A3 adenosine receptor. J Pharmacol Exp Ther 319:1200–1210. doi:10.1124/jpet.106.111351
12. Ge ZD, van der Hoeven D, Maas JE, Wan TC, Auchampach JA (2010) A(3) adenosine receptor activation during reperfusion reduces infarct size through actions on bone marrow-derived cells. J Mol Cell Cardiol 49:280–286. doi:10.1016/j.yjmcc.2010.01.018
13. Gomez G, Sitkovsky MV (2003) Differential requirement for A2a and A3 adenosine receptors for the protective effect of inosine in vivo. Blood 102:4472–4478. doi:10.1182/blood-2002-11-3624
14. Grandoch M, Hoffmann J, Rock K, Wenzel F, Oberhuber A, Schelzig H, Fischer JW (2013) Novel effects of adenosine receptors on pericellular hyaluronan matrix: implications for human smooth muscle cell phenotype and interactions with monocytes during atherosclerosis. Basic Res Cardiol 108:340. doi:10.1007/s00395-013-0340-6
15. Guo Y, Bolli R, Bao W, Wu WJ, Black RG Jr, Murphree SS, Salvatore CA, Jacobson MA, Auchampach JA (2001) Targeted deletion of the A3 adenosine receptor confers resistance to myocardial ischemic injury and does not prevent early preconditioning. J Mol Cell Cardiol 33:825–830. doi:10.1182/blood-2002-11-3624
16. Harrison GJ, Cerniway RJ, Peart J, Berr SS, Ashton K, Regan S, Paul Matherne G, Headrick JP (2002) Effects of A(3) adenosine receptor activation and gene knock-out in ischemic-reperfused mouse heart. Cardiovasc Res 53:147–155. doi:10.1016/S0008-6363(01)00424-2
17. Heusch G, Boengler K, Schulz R (2008) Cardioprotection: nitric oxide, protein kinases, and mitochondria. Circulation 118:1915–1919. doi:10.1161/CIRCULATIONAHA.108.805242
18. Hussain A, Gharanei AM, Nagra AS, Maddock HL (2014) Caspase inhibition via A3 adenosine receptors: a new cardioprotective mechanism against myocardial infarction. Cardiovasc Drugs Ther 28:19–32. doi:10.1007/s10557-013-6500-y
19. Jacobson KA, Nikodijevic O, Shi D, Gallo-Rodriguez C, Olah ME, Stiles GL, Daly JW (1993) A role for central A3-adenosine receptors. Mediation of behavioral depressant effects. FEBS Lett 336:57–60. doi:10.1016/0014-5793(93)81608-3
20. Jin X, Shepherd RK, Duling BR, Linden J (1997) Inosine binds to A3 adenosine receptors and stimulates mast cell degranulation. J Clin Invest 100:2849–2857. doi:10.1172/JCI119833
21. Kilpatrick EL, Narayan P, Mentzer RM Jr, Lasley RD (2001) Adenosine A3 agonist cardioprotection in isolated rat and rabbit hearts is blocked by the A1 antagonist DPCPX. Am J Physiol Heart Circ Physiol 281:H847–H853
22. Kleinbongard P, Heusch G (2014) Extracellular signalling molecules in the ischaemic/reperfused heart—druggable and translatable for cardioprotection? Br J Pharmacol. doi:10.1111/bph.12902
23. Lasley RD, Narayan P, Jahania MS, Partin EL, Kraft KR, Mentzer RM Jr (1999) Species-dependent hemodynamic effects of adenosine A3-receptor agonists IB-MECA and Cl-IB-MECA. Am J Physiol 276:H2076–H2084
24. Leung CT, Li A, Banerjee J, Gao ZG, Kambayashi T, Jacobson KA, Civan MM (2014) The role of activated adenosine receptors in degranulation of human LAD2 mast cells. Purinergic Signal 10:465–475. doi:10.1007/s11302-014-9409-4
25. Maddock HL, Mocanu MM, Yellon DM (2002) Adenosine A(3) receptor activation protects the myocardium from reperfusion/reoxygenation injury. Am J Physiol Heart Circ Physiol 283:H1307–H1313. doi:10.1152/ajpheart.00851.2001
26. McWhinney CD, Dudley MW, Bowlin TL, Peet NP, Schook L, Bradshaw M, De M, Borcherding DR, Edwards CK 3rd (1996) Activation of adenosine A3 receptors on macrophages inhibits tumor necrosis factor-alpha. Eur J Pharmacol 310:209–216. doi:10.1016/0014-2999(96)00272-5
27. Murphree LJ, Marshall MA, Rieger JM, MacDonald TL, Linden J (2002) Human A(2A) adenosine receptors: high-affinity agonist binding to receptor-G protein complexes containing Gbeta(4). Mol Pharmacol 61:455–462. doi:10.1016/0014-2999(96)00272-5
28. Nieri P, Martinotti E, Calderone V, Breschi MC (2001) Adenosine-mediated hypotension in in vivo guinea-pig: receptors involved and role of NO. Br J Pharmacol 134:745–752. doi:10.1038/sj.bjp.0704301
29. Osipchuk Y, Cahalan M (1992) Cell-to-cell spread of calcium signals mediated by ATP receptors in mast cells. Nature 359:241–244. doi:10.1038/359241a0
30. Palmer TM, Poucher SM, Jacobson KA, Stiles GL (1995) 125I-4-(2-[7-amino-2-[2-furyl][1,2,4]triazolo[2,3-a][1,3,5] triazin-5-yl-amino]ethyl)phenol, a high affinity antagonist radioligand selective for the A2a adenosine receptor. Mol Pharmacol 48:970–974
31. Park KS, Hoffmann C, Kim HO, Padgett WL, Daly JW, Brambilla R, Motta C, Abbracchio MP, Jacobson KA (1998) Activation and Desensitization of Rat A-Adenosine Receptors by Selective Adenosine Derivatives and Xanthine-7-Ribosides. Drug Dev Res 44:97–105. doi:10.1002/(SICI)1098-2299(199806/07)44:2/3<97:AID-DDR7>3.0.CO;2-5
32. Pelleg A, Burnstock G (1990) Physiological importance of ATP released from nerve terminals and its degradation to adenosine in humans. Circulation 82:2269–2272. doi:10.1161/01.CIR.82.6.2269
33. Ramkumar V, Stiles GL, Beaven MA, Ali H (1993) The A3 adenosine receptor is the unique adenosine receptor which facilitates release of allergic mediators in mast cells. J Biol Chem 268:16887–16890
34. Rork TH, Wallace KL, Kennedy DP, Marshall MA, Lankford AR, Linden J (2008) Adenosine A2A receptor activation reduces infarct size in the isolated, perfused mouse heart by inhibiting resident cardiac mast cell degranulation. Am J Physiol Heart Circ Physiol 295:H1825–H1833. doi:10.1152/ajpheart.495.2008
35. Salvatore CA, Tilley SL, Latour AM, Fletcher DS, Koller BH, Jacobson MA (2000) Disruption of the A(3) adenosine receptor gene in mice and its effect on stimulated inflammatory cells. J Biol Chem 275:4429–4434. doi:10.1074/jbc.275.6.4429
36. Schulz R, Post H, Vahlhaus C, Heusch G (1998) Ischemic preconditioning in pigs: a graded phenomenon: its relation to adenosine and bradykinin. Circulation 98:1022–1029. doi:10.1161/01.CIR.98.10.1022
37. Shin Y, Daly JW, Jacobson KA (1996) Activation of phosphoinositide breakdown and elevation of intracellular calcium in a rat RBL-2H3 mast cell line by adenosine analogs: involvement of A(3)-adenosine receptors? Drug Dev Res 39:36–46. doi:10.1002/(SICI)1098-2299(19960901)39:1<36:AID-DDR5>3.0.CO;2-L
38. Smith SR, Denhardt G, Terminelli C (2002) A role for histamine in cytokine modulation by the adenosine A(3) receptor agonist, 2-Cl-IB-MECA. Eur J Pharmacol 457:57–69. doi:10.1016/S0014-2999(02)02645-6
39. Sullivan GW, Linden J (1998) Role of A2A adenosine receptors in inflammation. Drug Dev Res 45:103–112. doi:10.1002/(SICI)1098-2299(199811/12)45:3/4<103:AID-DDR4>3.0.CO;2-W
40. Suzuki R, Furuno T, Okamoto K, Teshima R, Nakanishi M (2007) ATP plays a role in neurite stimulation with activated mast cells. J Neuroimmunol 192:49–56. doi:10.1016/j.jneuroim.2007.09.013
41. Takano H, Bolli R, Black RG Jr, Kodani E, Tang XL, Yang Z, Bhattacharya S, Auchampach JA (2001) A(1) or A(3) adenosine receptors induce late preconditioning against infarction in conscious rabbits by different mechanisms. Circ Res 88:520–528. doi:10.1161/01.RES.88.5.520
42. Tilley SL, Wagoner VA, Salvatore CA, Jacobson MA, Koller BH (2000) Adenosine and inosine increase cutaneous vasopermeability by activating A(3) receptors on mast cells. J Clin Invest 105:361–367. doi:10.1161/01.RES.88.5.520
43. Tracey WR, Magee W, Masamune H, Kennedy SP, Knight DR, Buchholz RA, Hill RJ (1997) Selective adenosine A3 receptor stimulation reduces ischemic myocardial injury in the rabbit heart. Cardiovasc Res 33:410–415. doi:10.1016/S0008-6363(96)00240-4
44. van der Putten C, Zuiderwijk-Sick EA, van Straalen L, de Geus ED, Boven LA, Kondova I, Ijzerman AP, Bajramovic JJ (2009) Differential expression of adenosine A3 receptors controls adenosine A2A receptor-mediated inhibition of TLR responses in microglia. J Immunol 182:7603–7612. doi:10.4049/jimmunol.0803383
45. Van Schaick EA, Jacobson KA, Kim HO, Ijzerman AP, Danhof M (1996) Hemodynamic effects and histamine release elicited by the selective adenosine A3 receptor agonist 2-Cl-IB-MECA in conscious rats. Eur J Pharmacol 308:311–314. doi:10.1016/S0008-6363(96)00240-4
46. Vigorito C, Russo P, Picotti GB, Chiariello M, Poto S, Marone G (1983) Cardiovascular effects of histamine infusion in man. J Cardiovasc Pharmacol 5:531–537. doi:10.1016/S0008-6363(96)00240-4
47. Wan TC, Ge ZD, Tampo A, Mio Y, Bienengraeber MW, Tracey WR, Gross GJ, Kwok WM, Auchampach JA (2008) The A3 adenosine receptor agonist CP-532,903 [N6-(2,5-dichlorobenzyl)-3′-aminoadenosine-5′-N-methylcarboxamide] protects against myocardial ischemia/reperfusion injury via the sarcolemmal ATP-sensitive potassium channel. J Pharmacol Exp Ther 324:234–243. doi:10.1124/jpet.107.127480
48. Yang Z, Berr SS, Gilson WD, Toufektsian MC, French BA (2004) Simultaneous evaluation of infarct size and cardiac function in intact mice by contrast-enhanced cardiac magnetic resonance imaging reveals contractile dysfunction in noninfarcted regions early after myocardial infarction. Circulation 109:1161–1167. doi:10.1161/01.CIR.0000118495.88442.32
49. Yang Z, Cerniway RJ, Byford AM, Berr SS, French BA, Matherne GP (2002) Cardiac overexpression of A1-adenosine receptor protects intact mice against myocardial infarction. Am J Physiol Heart Circ Physiol 282:H949–H955
50. Yang Z, Day YJ, Toufektsian MC, Ramos SI, Marshall M, Wang XQ, French BA, Linden J (2005) Infarct-sparing effect of A2A-adenosine receptor activation is due primarily to its action on lymphocytes. Circulation 111:2190–2197. doi:10.1161/01.CIR.0000163586.62253.A5
51. Yang Z, Day YJ, Toufektsian MC, Xu Y, Ramos SI, Marshall MA, French BA, Linden J (2006) Myocardial infarct-sparing effect of adenosine A2A receptor activation is due to its action on CD4+ T lymphocytes. Circulation 114:2056–2064. doi:10.1161/CIRCULATIONAHA.106.649244
52. Yang Z, Linden J, Berr SS, Kron IL, Beller GA, French BA (2008) Timing of adenosine 2A receptor stimulation relative to reperfusion has differential effects on infarct size and cardiac function as assessed in mice by MRI. Am J Physiol Heart Circ Physiol 295:H2328–H2335. doi:10.1152/ajpheart.00091.2008
53. Zhong H, Shlykov SG, Molina JG, Sanborn BM, Jacobson MA, Tilley SL, Blackburn MR (2003) Activation of murine lung mast cells by the adenosine A3 receptor. J Immunol 171:338–345. doi:10.4049/jimmunol.171.1.338