The Journal of Heart and Lung Transplantation
Volume 29, Issue 5 , Pages 544-553 , May 2010

Amelioration of rat cardiac cold ischemia/reperfusion injury with inhaled hydrogen or carbon monoxide, or both

  • Atsunori Nakao, MD

      Affiliations

    • Thomas E. Starzl Transplantation Institute, University of Pittsburgh, Pittburgh, Pennsylvania
    • Heart, Lung and Esophageal Surgery Institute, University of Pittsburgh, Pittburgh, Pennsylvania
    • Corresponding Author InformationReprint requests: Atsunori Nakao, MD, Thomas E. Starzl Transplantation Institute, Department of Surgery, University of Pittsburgh, E1551, Biomedical Science Tower, 200 Lothrop Street, Pittsburgh, PA 15213. Telephone: 412-648-9547. Fax: 412-624-6666
    • ,
  • David J. Kaczorowski, MD

      Affiliations

    • Departments of Surgery, Division of Gastroenterology, Hepatology and Nutrition, University of Pittsburgh Medical Center, Pittburgh, Pennsylvania
    • ,
  • Yinna Wang, MD

      Affiliations

    • Heart, Lung and Esophageal Surgery Institute, University of Pittsburgh, Pittburgh, Pennsylvania
    • ,
  • Jon S. Cardinal, MD

      Affiliations

    • Departments of Surgery, Division of Gastroenterology, Hepatology and Nutrition, University of Pittsburgh Medical Center, Pittburgh, Pennsylvania
    • ,
  • Bettina M. Buchholz, MD

      Affiliations

    • Department of Medicine, Division of Gastroenterology, Hepatology and Nutrition, University of Pittsburgh Medical Center, Pittburgh, Pennsylvania
    • ,
  • Ryujiro Sugimoto, MD

      Affiliations

    • Thomas E. Starzl Transplantation Institute, University of Pittsburgh, Pittburgh, Pennsylvania
    • Heart, Lung and Esophageal Surgery Institute, University of Pittsburgh, Pittburgh, Pennsylvania
    • ,
  • Kimimasa Tobita, MD

      Affiliations

    • Department of Pediatrics, McGowan Institute for Regenerative Medicine, University of Pittsburgh, Pittburgh, Pennsylvania
    • ,
  • Sungsoo Lee, MD

      Affiliations

    • Thomas E. Starzl Transplantation Institute, University of Pittsburgh, Pittburgh, Pennsylvania
    • Heart, Lung and Esophageal Surgery Institute, University of Pittsburgh, Pittburgh, Pennsylvania
    • ,
  • Yoshiya Toyoda, MD, PhD

      Affiliations

    • Thomas E. Starzl Transplantation Institute, University of Pittsburgh, Pittburgh, Pennsylvania
    • Heart, Lung and Esophageal Surgery Institute, University of Pittsburgh, Pittburgh, Pennsylvania
    • ,
  • Timothy R. Billiar, MD

      Affiliations

    • Departments of Surgery, Division of Gastroenterology, Hepatology and Nutrition, University of Pittsburgh Medical Center, Pittburgh, Pennsylvania
    • ,
  • Kenneth R. McCurry, MD

      Affiliations

    • Thomas E. Starzl Transplantation Institute, University of Pittsburgh, Pittburgh, Pennsylvania
    • Heart, Lung and Esophageal Surgery Institute, University of Pittsburgh, Pittburgh, Pennsylvania
    • Heart and Vascular Institute, Cleveland Clinic, Cleveland, Ohio

References 

  1. Slater JP, Amirhamzeh MM, Yano OJ, et al. Discriminating between preservation and reperfusion injury in human cardiac allografts using heart weight and left ventricular mass. Circulation. 1995;92:II-223-7
  2. Tanaka M, Mokhtari GK, Terry RD, et al. Prolonged cold ischemia in rat cardiac allografts promotes ischemia–reperfusion injury and the development of graft coronary artery disease in a linear fashion. J Heart Lung Transplant. 2005;24:1906–1914
  3. Knight RJ, Dikman S, Liu H, et al. Cold ischemic injury accelerates the progression to chronic rejection in a rat cardiac allograft model. Transplantation. 1997;64:1102–1107
  4. Yamani MH, Tuzcu EM, Starling RC, et al. Myocardial ischemic injury after heart transplantation is associated with upregulation of vitronectin receptor (alpha(v)beta3), activation of the matrix metalloproteinase induction system, and subsequent development of coronary vasculopathy. Circulation. 2002;105:1955–1961
  5. Ohsawa I, Ishikawa M, Takahashi K, et al. Hydrogen acts as a therapeutic antioxidant by selectively reducing cytotoxic oxygen radicals. Nat Med. 2007;13:688–694
  6. Nakao A, Choi AM, Murase N. Protective effect of carbon monoxide in transplantation. J Cell Mol Med. 2006;10:650–671
  7. Akamatsu Y, Haga M, Tyagi S, et al. Heme oxygenase-1-derived carbon monoxide protects hearts from transplant associated ischemia reperfusion injury. FASEB J. 2004;18:771–772
  8. Clark JE, Naughton P, Shurey S, et al. Cardioprotective actions by a water-soluble carbon monoxide-releasing molecule. Circ Res. 2003;93:e2–e8
  9. Faleo G, Neto JS, Kohmoto J, et al. Carbon monoxide ameliorates renal cold ischemia-reperfusion injury with an upregulation of vascular endothelial growth factor by activation of hypoxia-inducible factor. Transplantation. 2008;85:1833–1840
  10. Nakao A, Sugimoto R, Billiar TR, et al. Therapeutic antioxidant medical gas. J Clin Biochem Nutr. 2009;44:1–13
  11. Nakao A, Toyokawa H, Abe M, et al. Heart allograft protection with low-dose carbon monoxide inhalation: effects on inflammatory mediators and alloreactive T-cell responses. Transplantation. 2006;81:220–230
  12. Otterbein LE, Zuckerbraun BS, Haga M, et al. Carbon monoxide suppresses arteriosclerotic lesions associated with chronic graft rejection and with balloon injury. Nat Med. 2003;9:183–190
  13. Nakao A, Kimizuka K, Stolz DB, et al. Carbon monoxide inhalation protects rat intestinal grafts from ischemia/reperfusion injury. Am J Pathol. 2003;163:1587–1598
  14. Buchholz BM, Kaczorowski DJ, Sugimoto R, et al. Hydrogen inhalation ameliorates oxidative stress in transplantation induced intestinal graft injury. Am J Transplant. 2008;8:2015–2024
  15. Nakao A, Neto JS, Kanno S, et al. Protection against ischemia/reperfusion injury in cardiac and renal transplantation with carbon monoxide, biliverdin and both. Am J Transplant. 2005;5:282–291
  16. Pinsky DJ, Oz MC, Koga S, et al. Cardiac preservation is enhanced in a heterotopic rat transplant model by supplementing the nitric oxide pathway. J Clin Invest. 1994;93:2291–2297
  17. Wang CY, Naka Y, Liao H, et al. Cardiac graft intercellular adhesion molecule-1 (ICAM-1) and interleukin-1 expression mediate primary isograft failure and induction of ICAM-1 in organs remote from the site of transplantation. Circ Res. 1998;82:762–772
  18. Kaizu T, Ikeda A, Nakao A, et al. Protection of transplant-induced hepatic ischemia/reperfusion injury with carbon monoxide via MEK/ERK1/2 pathway downregulation. Am J Physiol Gastrointest Liver Physiol. 2008;294:G236–G244
  19. Baxter K, Howden BO, Jablonski P. Heart preservation with Celsior solution improved by the addition of nitroglycerine. Transplantation. 2001;71:1380–1384
  20. Tsung A, Sahai R, Tanaka H, et al. The nuclear factor HMGB1 mediates hepatic injury after murine liver ischemia–reperfusion. J Exp Med. 2005;201:1135–1143
  21. Taylor DO, Edwards LB, Boucek MM, et al. Registry of the International Society for Heart and Lung Transplantation: twenty-fourth official adult heart transplant report—2007. J Heart Lung Transplant. 2007;26:769–781
  22. Hayashida K, Sano M, Ohsawa I, et al. Inhalation of hydrogen gas reduces infarct size in the rat model of myocardial ischemia–reperfusion injury. Biochem Biophys Res Commun. 2008;373:30–35
  23. Fukuda KI, Asoh S, Ishikawa M, et al. Inhalation of hydrogen gas suppresses hepatic injury caused by ischemia/reperfusion through reducing oxidative stress. Biochem Biophys Res Commun. 2007;361:670–674
  24. Cai J, Kang Z, Liu WW, et al. Hydrogen therapy reduces apoptosis in neonatal hypoxia–ischemia rat model. Neurosci Lett. 2008;441:167–172
  25. Levitt MD. Production and excretion of hydrogen gas in man. N Engl J Med. 1969;281:122–127
  26. Abraini JH, Gardette-Chauffour MC, Martinez E, et al. Psychophysiological reactions in humans during an open sea dive to 500 m with a hydrogen–helium–oxygen mixture. J Appl Physiol. 1994;76:1113–1118
  27. Otterbein LE. Carbon monoxide: innovative anti-inflammatory properties of an age-old gas molecule. Antioxid Redox Signal. 2002;4:309–319
  28. Ryter SW, Otterbein LE. Carbon monoxide in biology and medicine. Bioessays. 2004;26:270–280

PII: S1053-2498(09)00823-7

doi: 10.1016/j.healun.2009.10.011

The Journal of Heart and Lung Transplantation
Volume 29, Issue 5 , Pages 544-553 , May 2010

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