The Journal of Thoracic and Cardiovascular Surgery
Volume 138, Issue 3 , Pages 752-759 , September 2009

Apyrase treatment prevents ischemia–reperfusion injury in rat lung isografts

  • Seiichiro Sugimoto, MD, PhD

      Affiliations

    • Division of Cardiothoracic Surgery, Department of Surgery, Washington University School of Medicine, St Louis, Mo
    • ,
  • Xue Lin, MD

      Affiliations

    • Division of Cardiothoracic Surgery, Department of Surgery, Washington University School of Medicine, St Louis, Mo
    • ,
  • Jiaming Lai, MD

      Affiliations

    • Division of Cardiothoracic Surgery, Department of Surgery, Washington University School of Medicine, St Louis, Mo
    • ,
  • Mikio Okazaki, MD, PhD

      Affiliations

    • Division of Cardiothoracic Surgery, Department of Surgery, Washington University School of Medicine, St Louis, Mo
    • ,
  • Nitin A. Das, MD

      Affiliations

    • Division of Cardiothoracic Surgery, Department of Surgery, Washington University School of Medicine, St Louis, Mo
    • ,
  • Wenjun Li, MD

      Affiliations

    • Division of Cardiothoracic Surgery, Department of Surgery, Washington University School of Medicine, St Louis, Mo
    • ,
  • Alexander S. Krupnick, MD

      Affiliations

    • Division of Cardiothoracic Surgery, Department of Surgery, Washington University School of Medicine, St Louis, Mo
    • ,
  • Ridong Chen, PhD

      Affiliations

    • APT Therapeutics Inc, St Louis, Mo
    • ,
  • Soon Seog Jeong, PhD

      Affiliations

    • APT Therapeutics Inc, St Louis, Mo
    • ,
  • G.A. Patterson, MD

      Affiliations

    • Division of Cardiothoracic Surgery, Department of Surgery, Washington University School of Medicine, St Louis, Mo
    • ,
  • Daniel Kreisel, MD, PhD

      Affiliations

    • Division of Cardiothoracic Surgery, Department of Surgery, Washington University School of Medicine, St Louis, Mo
    • ,
  • Andrew E. Gelman, PhD

      Affiliations

    • Division of Cardiothoracic Surgery, Department of Surgery, Washington University School of Medicine, St Louis, Mo
    • Corresponding Author InformationAddress for reprints: Andrew E. Gelman, PhD, Assistant Professor of Surgery, Pathology & Immunology, Campus Box 8234, 660 South Euclid Avenue, Washington University in St Louis, St Louis, MO 63110-1013.

Received 7 November 2008 ,Revised 27 March 2009 ,Accepted 23 April 2009.

References 

  1. Thabut G, Mal H, Cerrina J, Dartevelle P, Dromer C, Velly JF, et al. Graft ischemic time and outcome of lung transplantation: a multicenter analysis. Am J Respir Crit Care Med. 2005;171:786
  2. de Perrot M, Liu M, Waddell TK, Keshavjee S. Ischemia-reperfusion-induced lung injury. Am J Respir Crit Care Med. 2003;167:490
  3. Morrell CN, Sun H, Swaim AM, Baldwin WM. Platelets an inflammatory force in transplantation. Am J Transplant. 2007;7:2447
  4. De Perrot M, Sekine Y, Fischer S, Waddell TK, McRae K, Liu M, et al. Interleukin-8 release during early reperfusion predicts graft function in human lung transplantation. Am J Respir Crit Care Med. 2002;165:211
  5. Robson SC, Wu Y, Sun X, Knosalla C, Dwyer K, Enjyoji K. Ectonucleotidases of CD39 family modulate vascular inflammation and thrombosis in transplantation. Semin Thromb Hemost. 2005;31:217
  6. Gayle RB, Maliszewski CR, Gimpel SD, Schoenborn MA, Caspary RG, Richards C, et al. Inhibition of platelet function by recombinant soluble ecto-ADPase/CD39. J Clin Invest. 1998;101:1851
  7. Koziak K, Sevigny J, Robson SC, Siegel JB, Kaczmarek E. Analysis of CD39/ATP diphosphohydrolase (ATPDase) expression in endothelial cells, platelets and leukocytes. Thromb Haemost. 1999;82:1538
  8. Labasi JM, Petrushova N, Donovan C, McCurdy S, Lira P, Payette MM, et al. Absence of the P2X7 receptor alters leukocyte function and attenuates an inflammatory response. J Immunol. 2002;168:6436
  9. Suh BC, Kim JS, Namgung U, Ha H, Kim KT. P2X7 nucleotide receptor mediation of membrane pore formation and superoxide generation in human promyelocytes and neutrophils. J Immunol. 2001;166:6754
  10. Robson SC, Kaczmarek E, Siegel JB, Candinas D, Koziak K, Millan M, et al. Loss of ATP diphosphohydrolase activity with endothelial cell activation. J Exp Med. 1997;185:153
  11. Marcus AJ, Broekman MJ, Drosopoulos JH, Islam N, Alyonycheva TN, Safier LB, et al. The endothelial cell ecto-ADPase responsible for inhibition of platelet function is CD39. J Clin Invest. 1997;99:1351
  12. Guckelberger O, Sun XF, Sevigny J, Imai M, Kaczmarek E, Enjyoji K, et al. Beneficial effects of CD39/ecto-nucleoside triphosphate diphosphohydrolase-1 in murine intestinal ischemia-reperfusion injury. Thromb Haemost. 2004;91:576
  13. Grenz A, Zhang H, Hermes M, Eckle T, Klingel K, Huang DY, et al. Contribution of E-NTPDase1 (CD39) to renal protection from ischemia-reperfusion injury. Faseb J. 2007;21:2863
  14. Kohler D, Eckle T, Faigle M, Grenz A, Mittelbronn M, Laucher S, et al. CD39/ectonucleoside triphosphate diphosphohydrolase 1 provides myocardial protection during cardiac ischemia/reperfusion injury. Circulation. 2007;116:1784
  15. Mizuta T, Kawaguchi A, Nakahara K, Kawashima Y. Simplified rat lung transplantation using a cuff technique. J Thorac Cardiovasc Surg. 1989;97:578
  16. Krawisz JE, Sharon P, Stenson WF. Quantitative assay for acute intestinal inflammation based on myeloperoxidase activity. Assessment of inflammation in rat and hamster models. Gastroenterology. 1984;87:1344
  17. Katayama Y, Hidalgo A, Chang J, Peired A, Frenette PS. CD44 is a physiological E-selectin ligand on neutrophils. J Exp Med. 2005;201:1183
  18. Okazaki M, Kreisel F, Richardson SB, Kreisel D, Krupnick AS, Patterson GA, et al. Sphingosine 1-phosphate inhibits ischemia reperfusion injury following experimental lung transplantation. Am J Transplant. 2007;7:751
  19. Okazaki M, Gelman AE, Tietjens JR, Ibricevic A, Kornfeld CG, Huang HJ, et al. Maintenance of airway epithelium in acutely rejected orthotopic vascularized mouse lung transplants. Am J Respir Cell Mol Biol. 2007;37:625
  20. Quadri SM, Segall L, de Perrot M, Han B, Edwards V, Jones N, et al. Caspase inhibition improves ischemia-reperfusion injury after lung transplantation. Am J Transplant. 2005;5:292
  21. Ishiyama T, Dharmarajan S, Hayama M, Moriya H, Grapperhaus K, Patterson GA. Inhibition of nuclear factor kappaB by IkappaB superrepressor gene transfer ameliorates ischemia-reperfusion injury after experimental lung transplantation. J Thorac Cardiovasc Surg. 2005;130:194
  22. von Albertini M, Palmetshofer A, Kaczmarek E, Koziak K, Stroka D, Grey ST, et al. Extracellular ATP and ADP activate transcription factor NF-kappa B and induce endothelial cell apoptosis. Biochem Biophys Res Commun. 1998;248:822
  23. Goepfert C, Imai M, Brouard S, Csizmadia E, Kaczmarek E, Robson SC. CD39 modulates endothelial cell activation and apoptosis. Mol Med. 2000;6:591
  24. Demertzis S, Langer F, Graeter T, Dwenger A, Georg T, Schafers HJ. Amelioration of lung reperfusion injury by L- and E- selectin blockade. Eur J Cardiothorac Surg. 1999;16:174
  25. Sternberg DI, Shimbo D, Kawut SM, Sarkar J, Hurlitz G, D'Ovidio F, et al. Platelet activation in the postoperative period after lung transplantation. J Thorac Cardiovasc Surg. 2008;135:679
  26. Shargall Y, Guenther G, Ahya VN, Ardehali A, Singhal A, Keshavjee S. Report of the ISHLT Working Group on Primary Lung Graft Dysfunction part VI: treatment. J Heart Lung Transplant. 2005;24:1489
  27. Okada Y, Marchevsky AM, Zuo XJ, Pass JA, Kass RM, Matloff JM, et al. Accumulation of platelets in rat syngeneic lung transplants: a potential factor responsible for preservation-reperfusion injury. Transplantation. 1997;64:801
  28. Uluckan O, Eagleton MC, Floyd DH, Morgan EA, Hirbe AC, Kramer M, et al. APT102, a novel adpase, cooperates with aspirin to disrupt bone metastasis in mice. J Cell Biochem. 2008;104:1311
  29. Cypel M, Yeung JC, Hirayama S, Rubacha M, Fischer S, Anraku M, et al. Technique for prolonged normothermic ex vivo lung perfusion. J Heart Lung Transplant. 2008;27:1319
  30. Griffiths RJ, Stam EJ, Downs JT, Otterness IG. ATP induces the release of IL-1 from LPS-primed cells in vivo. J Immunol. 1995;154:2821
  31. Sipka S, Kovacs I, Szanto S, Szegedi G, Brugos L, Bruckner G, et al. Adenosine inhibits the release of interleukin-1beta in activated human peripheral mononuclear cells. Cytokine. 2005;31:258
  32. Linden J. New insights into the regulation of inflammation by adenosine. J Clin Invest. 2006;116:1835
  33. Kopp E, Medzhitov R. Recognition of microbial infection by Toll-like receptors. Curr Opin Immunol. 2003;15:396

 This work was sponsored by a NIH SBIR grant (1R42HL087456) from the National Heart, Lung and Blood Institute.

 S. Sugimoto and X. Lin have contributed equally to this work.

PII: S0022-5223(09)00780-6

doi: 10.1016/j.jtcvs.2009.04.049

The Journal of Thoracic and Cardiovascular Surgery
Volume 138, Issue 3 , Pages 752-759 , September 2009

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