In vivo hypoxic preconditioning protects from warm liver ischemia-reperfusion injury through the adenosine A2B receptor

Transplantation

Volumn 94, Issue 9, 2012, Pages 894-902

  Choukèr, Alexander ^a,b   Ohta, Akio ^b,c   Martignoni, André ^a   Lukashev, Dmitriy ^b,c   Zacharia, Lefteris C ^d   Jackson, Edwin K ^e   Schnermann, Jürgen ^f   Ward, Jerrold M ^b   Kaufmann, Ines ^a   Klaunberg, Brenda ^g   Sitkovsky, Michail V ^b,c   Thiel, Manfred ^h  

^a UNIVERSITY OF MUNICH   (Germany)

^b NATIONAL INSTITUTE OF ALLERGY AND INFECTIOUS DISEASES   (United States)

^c NORTHEASTERN UNIVERSITY   (United States)

^d FAME Laboratory   (Greece)

^e UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

^f NATIONAL INSTITUTE OF DIABETES AND DIGESTIVE AND KIDNEY DISEASES   (United States)

^g NATIONAL INSTITUTE OF NEUROLOGICAL DISORDERS AND STROKE   (United States)

^h UNIVERSITY OF HEIDELBERG   (Germany)

Author keywords

Hepatoprotection; Hypoxia; Murine liver ischemia; Preconditioning

Indexed keywords

4 [2 [7 AMINO 2 (2 FURYL) 1,2,4 TRIAZOLO[2,3 A][1,3,5]TRIAZIN 5 YLAMINO]ETHYL]PHENOL; ADENOSINE; ADENOSINE A1 RECEPTOR; ADENOSINE A2A RECEPTOR; ADENOSINE A2B RECEPTOR; ADENOSINE A3 RECEPTOR; ADENOSINE PHOSPHATE; ADENOSINE RECEPTOR; ALANINE AMINOTRANSFERASE; ASPARTATE AMINOTRANSFERASE; HYPOXANTHINE; INOSINE; INTERLEUKIN 6; LACTATE DEHYDROGENASE; MESSENGER RNA; MYELOPEROXIDASE; N (4 CYANOPHENYL) 2 [4 (2,3,6,7 TETRAHYDRO 2,6 DIOXO 1,3 DIPROPYL 1H PURIN 8 YL)PHENOXY]ACETAMIDE; OXYGEN; PURINE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; GENE DELETION; HEPATITIS; ISCHEMIC PRECONDITIONING; KNOCKOUT MOUSE; LIVER CELL DAMAGE; LIVER ISCHEMIA; LIVER METABOLISM; LIVER PROTECTION; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; QUANTITATIVE ANALYSIS; RECEPTOR BLOCKING; REPERFUSION; REPERFUSION INJURY; WILD TYPE;

ACETAMIDES; ADENOSINE; ANIMALS; ANOXIA; HEPATOCYTES; ISCHEMIC PRECONDITIONING; LIVER; LIVER TRANSPLANTATION; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MODELS, ANIMAL; PURINES; RECEPTOR, ADENOSINE A2B; REPERFUSION INJURY; SIGNAL TRANSDUCTION; WARM ISCHEMIA;

EID: 84869503883     PISSN: 00411337     EISSN: None     Source Type: Journal    
DOI: 10.1097/TP.0b013e31826a9a46     Document Type: Article

References (46)

1. Selzner N, Rudiger H, Graf R, et al. Protective strategies against ischemic injury of the liver. Gastroenterology 2003; 125: 917.
2. Singhal AK, Sheng X, Drakos SG, et al. Impact of donor cause of death on transplant outcomes: UNOS registry analysis. Transplant Proc 2009; 41: 3539.
3. Dong JW, Zhu HF, Zhu WZ, et al. Intermittent hypoxia attenuates ischemia/reperfusion induced apoptosis in cardiac myocytes via regulating Bcl-2/Bax expression. Cell Res 2003; 13: 385.
4. Liu X, Wu X, Cai L, et al. Hypoxic preconditioning of cardiomyocytes and cardioprotection: phophorylation of HIF-1alpha induced by p42/p44 mitogen-activated protein kinases is involved. Pathophysiology 2003; 9: 201.
5. Uchiyama T, Engelman RM, Maulik N, et al. Role of Akt signaling in mitochondrial survival pathway triggered by hypoxic preconditioning. Circulation 2004; 109: 3042.
6. Chouker A, Martignoni A, Schauer R, et al. Beneficial effects of ischemic preconditioning in patients undergoing hepatectomy: the role of neutrophils. Arch Surg 2005; 140: 129.
7. Chouker A, Martignoni A, Schauer RJ, et al. Ischemic preconditioning attenuates portal venous plasma concentrations of purines following warm liver ischemia in man. Eur Surg Res 2005; 37: 144.
8. Chouker A, Schachtner T, Schauer R, et al. Effects of Pringle manoeuvre and ischaemic preconditioning on haemodynamic stability in patients undergoing elective hepatectomy: a randomized trial. Br J Anaesth 2004; 93: 204.
9. Franchello A, Gilbo N, David E, et al. Ischemic preconditioning (IP) of the liver as a safe and protective technique against ischemia/reperfusion injury (IRI). Am J Transplant 2009; 9: 1629.
10. Jassem W, Fuggle SV, Cerundolo L, et al. Ischemic preconditioning of cadaver donor livers protects allografts following transplantation. Transplantation 2006; 81: 169.
11. Mei DA, Nithipatikom K, Lasley RD, et al. Myocardial preconditioning produced by ischemia, hypoxia, and a KATP channel opener: effects on interstitial adenosine in dogs. J Mol Cell Cardiol 1998; 30: 1225.
12. Zhang WL, Lu GW. Changes of adenosine and its A(1) receptor in hypoxic preconditioning. Biol Signals Recept 1999; 8: 275.
13. Cherqui D, Benoist S, Malassagne B, et al. Major liver resection for carcinoma in jaundiced patients without preoperative biliary drainage. Arch Surg 2000; 135: 302.
14. Thiel M, Caldwell CC, Sitkovsky MV. The critical role of adenosine A2A receptors in downregulation of inflammation and immunity in the pathogenesis of infectious diseases. Microbes Infect 2003; 5: 515.
15. OlahME, Stiles GL. Adenosine receptor subtypes: characterization and therapeutic regulation. Annu Rev Pharmacol Toxicol 1995; 35: 581.
16. Sitkovsky MV, Lukashev D, Apasov S, et al. Physiological control of immune response and inflammatory tissue damage by hypoxiainducible factors and adenosine A2A receptors. Annu Rev Immunol 2004; 22: 657.
17. Itoh R. Regulation of cytosol 5¶-nucleotidase by adenylate energy charge. Biochim Biophys Acta 1981; 659: 31.
18. Itoh R, Oka J, Ozasa H. Regulation of rat heart cytosol 5¶-nucleotidase by adenylate energy charge. Biochem J 1986; 235: 847.
19. Paugam-Burtz C, Albuquerque M, Baron G, et al. Plasma proteome to look for diagnostic biomarkers of early bacterial sepsis after liver transplantation: a preliminary study. Anesthesiology 2010; 112: 926.
20. Clavien PA, Selzner M, Rudiger HA, et al. A prospective randomized study in 100 consecutive patients undergoing major liver resection with versus without ischemic preconditioning. Ann Surg 2003; 238: 843.
21. Selzner N, Selzner M, Jochum W, et al. Ischemic preconditioning protects the steatotic mouse liver against reperfusion injury: an ATP dependent mechanism. J Hepatol 2003; 39: 55.
22. Jassem W, Fuggle S, Thompson R, et al. Effect of ischemic preconditioning on the genomic response to reperfusion injury in deceased donor liver transplantation. Liver Transpl 2009; 15: 1750.
23. Astarcioglu I, Cursio R, Reynes M, et al. Increased risk of antibodymediated rejection of reduced-size liver allografts. J Surg Res 1999; 87: 258.
24. Howell JG, Zibari GB, Brown MF, et al. Both ischemic and pharmacological preconditioning decrease hepatic leukocyte/endothelial cell interactions. Transplantation 2000; 69: 300.
25. Jones NM, Bergeron M. Hypoxia-induced ischemic tolerance in neonatal rat brain involves enhanced ERK1/2 signaling. J Neurochem 2004; 89: 157.
26. Lu GW, Yu S, Li RH, et al. Hypoxic preconditioning: a novel intrinsic cytoprotective strategy. Mol Neurobiol 2005; 31: 255.
27. Wang CH, Chang A, Tsai MJ, et al. Kainic acid-induced oxidative injury is attenuated by hypoxic preconditioning. Ann N Y Acad Sci 2005; 1042: 314.
28. Lemasters JJ, Thurman RG. Reperfusion injury after liver preservation for transplantation. Annu Rev Pharmacol Toxicol 1997; 37: 327.
29. Ishii D, Schenk AD, Baba S, et al. Role of TNFalpha in early chemokine production and leukocyte infiltration into heart allografts. Am J Transplant 2010; 10: 59.
30. Wang F, Birch SE, He R, et al. Remote ischemic preconditioning by hindlimb occlusion prevents liver ischemic/reperfusion injury: the role of High Mobility Group-Box 1. Ann Surg 2010; 251: 292.
31. Decking UK, Schlieper G, Kroll K, et al. Hypoxia-induced inhibition of adenosine kinase potentiates cardiac adenosine release. Circ Res 1997; 81: 154.
32. Carini R, De Cesaris MG, Splendore R, et al. Signal pathway involved in the development of hypoxic preconditioning in rat hepatocytes. Hepatology 2001; 33: 131.
33. Day YJ, Marshall MA, Huang L, et al. Protection from ischemic liver injury by activation of A2A adenosine receptors during reperfusion: inhibition of chemokine induction. Am J Physiol Gastrointest Liver Physiol 2004; 286: G285.
34. Harada N, Okajima K, Murakami K, et al. Adenosine and selective A(2A) receptor agonists reduce ischemia/reperfusion injury of rat liver mainly by inhibiting leukocyte activation. J Pharmacol Exp Ther 2000; 294: 1034.
35. Poucher SM, Keddie JR, Singh P, et al. The in vitro pharmacology of ZM 241385, a potent, non-xanthine A2a selective adenosine receptor antagonist. Br J Pharmacol 1995; 115: 1096.
36. Klotz KN. Adenosine receptors and their ligands. Naunyn Schmiedebergs Arch Pharmacol 2000; 362: 382.
37. Ji X, Kim YC, Ahern DG, et al. [3H]MRS 1754, a selective antagonist radioligand for A(2B) adenosine receptors. Biochem Pharmacol 2001; 61: 657.
38. Eckle T, Faigle M, Grenz A, et al. A2B adenosine receptor dampens hypoxia-induced vascular leak. Blood 2008; 111: 2024.
39. Yang D, Zhang Y, Nguyen HG, et al. The A2B adenosine receptor protects against inflammation and excessive vascular adhesion. J Clin Invest 2006; 116: 1913.
40. Mullane K, Bullough D. Harnessing an endogenous cardioprotective mechanism: cellular sources and sites of action of adenosine. J Mol Cell Cardiol 1995; 27: 1041.
41. Takano H, Bolli R, Black RG Jr, et al. A(1) or A(3) adenosine receptors induce late preconditioning against infarction in conscious rabbits by different mechanisms. Circ Res 2001; 88: 520.
42. Joo JD, Kim M, Horst P, et al. Acute and delayed renal protection against renal ischemia and reperfusion injury with A1 adenosine receptors. Am J Physiol Renal Physiol 2007; 293: F1847.
43. Thiel M, Holzer K, Kreimeier U, et al. Effects of adenosine on the functions of circulating polymorphonuclear leukocytes during hyperdynamic endotoxemia. Infect Immun 1997; 65: 2136.
44. Lukashev DE, Smith PT, Caldwell CC, et al. Analysis of A2a receptordeficient mice reveals no significant compensatory increases in the expression of A2b, A1, and A3 adenosine receptors in lymphoid organs. Biochem Pharmacol 2003; 65: 2081.
45. Martignoni A, Tschop J, Goetzman HS, et al. CD4-expressing cells are early mediators of the innate immune system during sepsis. Shock 2008; 29: 591.
46. Jackson EK, Zacharia LC, Zhang M, et al. cAMP-adenosine pathway in the proximal tubule. J Pharmacol Exp Ther 2006; 317: 1219.