Skip to main content

Advertisement

Log in

Taurine prevents myocardial ischemia/reperfusion-induced oxidative stress and apoptosis in prolonged hypothermic rat heart preservation

  • ORIGINAL ARTICLE
  • Published:
Heart and Vessels Aims and scope Submit manuscript

Abstract

Taurine (2-aminoethanesulfonic acid) is a potent antioxidant and inhibits cell apoptosis in ischemic reperfusion injury. In this study we evaluated whether addition of taurine to St. Thomas' cardioplegic solution enhances its myocardial protective effects in prolonged hypothermic heart preservation in rats. Hearts isolated from male Sprague–Dawley rats were mounted on a Langendorff apparatus to estimate baseline cardiac function, then arrested and stored in St. Thomas' cardioplegic solution, with taurine (10 mM; taurine group, n = 8) or without taurine (control group, n = 8), for 6 h at 4°C. After storage, the hearts were reperfused and heart rate (HR), coronary flow (CF), left ventricular developed pressure (LVP), and positive maximum left ventricular developing pressure (max LV dp/dt) were measured. The LV tissue was examined immunohistochemically for determining DNA oxidative stress and cell apoptosis. Compared with control groups, recovery of LVP (P < 0.001), max LV dp/dt (P < 0.001), and coronary flow (P < 0.001) were significantly enhanced, whereas glutamic oxaloacetic transaminase (P < 0.01), lactate dehydrogenase (P < 0.05), creatine phosphate kinase (P < 0.01), 8-hydroxy-2′-deoxyguanosine index (P < 0.01), caspase-3 mRNA expression (P < 0.05), and percentage of TUNEL-positive cardiomyocytes (P < 0.05) were reduced in the taurine group. Addition of taurine to St. Thomas' cardioplegic solution improved cardiac function recovery for prolonged hypothermic rat heart preservation by suppressing DNA oxidative stress and cell apoptosis.

This is a preview of subscription content, log in via an institution to check access.

Access this article

Price excludes VAT (USA)
Tax calculation will be finalised during checkout.

Instant access to the full article PDF.

Similar content being viewed by others

References

  1. S Darracott-Cankovic PG Stovin D Wheeldon J Wallwork F Wells TA English (1989) ArticleTitleEffect of donor heart damage on survival after transplantation Eur J Cardiothorac Surg 3 525–532 Occurrence Handle2635940 Occurrence Handle1:STN:280:By%2BB2MzosVM%3D

    PubMed  CAS  Google Scholar 

  2. DJ Lefer DN Granger (2000) ArticleTitleOxidative stress and cardiac disease Am J Med 109 315–323 Occurrence Handle10996583 Occurrence Handle1:CAS:528:DC%2BD3cXms1Wku7o%3D Occurrence Handle10.1016/S0002-9343(00)00467-8

    Article  PubMed  CAS  Google Scholar 

  3. D Kumar BI Jugdutt (2003) ArticleTitleApoptosis and oxidants in the heart J Lab Clin Med 142 288–297 Occurrence Handle14647032 Occurrence Handle1:CAS:528:DC%2BD3sXpsVSgsLg%3D Occurrence Handle10.1016/S0022-2143(03)00148-3

    Article  PubMed  CAS  Google Scholar 

  4. JP Schmitt J Schroder H Schunkert DE Birnbaum H Aebert (2002) ArticleTitleRole of apoptosis in myocardial stunning after open surgery Ann Thorac Surg 73 1229–1235 Occurrence Handle11996268 Occurrence Handle10.1016/S0003-4975(02)03401-X

    Article  PubMed  Google Scholar 

  5. RJ Huxtable (1992) ArticleTitlePhysiological actions of taurine Physiol Rev 72 101–163 Occurrence Handle1731369 Occurrence Handle1:CAS:528:DyaK38XhsVKhsLw%3D

    PubMed  CAS  Google Scholar 

  6. K Takahashi Y Ohyabu K Takahashi V Solodushko T Takatani T Itoh SW Schaffer J Azuma (2003) ArticleTitleTaurine renders the cell resistant to ischemia-induced injury in cultured neonatal rat cardiomyocytes J Cardiovasc Pharmacol 41 726–733 Occurrence Handle12717103 Occurrence Handle1:CAS:528:DC%2BD3sXjt1Shtr0%3D

    PubMed  CAS  Google Scholar 

  7. F Franconi I Stendardi P Failli R Matucci C Baccaro L Montorsi R Bandinelli A Giotti (1985) ArticleTitleThe protective effects of taurine on hypoxia (performed in the absence of glucose) and on reoxygenation (in the presence of glucose) in guinea-pig heart Biochem Pharmacol 34 2611–2615 Occurrence Handle4015703 Occurrence Handle1:CAS:528:DyaL2MXltlCrs70%3D Occurrence Handle10.1016/0006-2952(85)90556-8

    Article  PubMed  CAS  Google Scholar 

  8. M Wettstein D Haussinger (2000) ArticleTitleTaurine attenuates cold ischemia-reoxygenation injury in rat liver Transplantation 69 2290–2296 Occurrence Handle10868628 Occurrence Handle1:CAS:528:DC%2BD3cXksVGhtbk%3D

    PubMed  CAS  Google Scholar 

  9. P Wingenfeld U Gehrmann S Strubind T Minor W Isselhard DV Michalk (1996) ArticleTitleLong-lasting hypoxic preservation of porcine kidney cells. Beneficial effect of taurine on viability and metabolism in a simplified transplantation model Adv Exp Med Biol 403 230–212

    Google Scholar 

  10. T Minor T Yamaguchi W Isselhard (1995) ArticleTitleEffects of taurine on liver preservation in UW solution with consecutive ischemic rewarming in the isolated perfused rat liver Transpl Int 8 174–179 Occurrence Handle7626175 Occurrence Handle1:CAS:528:DyaK2sXjtFKnuw%3D%3D Occurrence Handle10.1007/BF00336533

    Article  PubMed  CAS  Google Scholar 

  11. DV Michalk B Hoffmann T Minor (2003) ArticleTitleTaurine reduces renal ischemia/reperfusion injury in the rat Adv Exp Med Biol 526 49–56 Occurrence Handle12908583 Occurrence Handle1:CAS:528:DC%2BD3sXnsVyhsbs%3D

    PubMed  CAS  Google Scholar 

  12. H Kasai S Nishimura (1984) ArticleTitleHydroxylation of deoxyguanosine at the C-8 position by ascorbic acid and other reducing agents Nucleic Acids Res 12 2137–2145 Occurrence Handle6701097 Occurrence Handle1:CAS:528:DyaL2cXhsFalsb0%3D

    PubMed  CAS  Google Scholar 

  13. S Toyokuni (1999) ArticleTitleReactive oxygen species-induced molecular damage and its application in pathology Pathol Int 49 91–102 Occurrence Handle10355961 Occurrence Handle1:CAS:528:DyaK1MXitFChurk%3D Occurrence Handle10.1046/j.1440-1827.1999.00829.x

    Article  PubMed  CAS  Google Scholar 

  14. C Kishimoto N Tomioka Y Nakayama M Miyamoto (2003) ArticleTitleAnti-oxidant effects of coenzyme Q10 on experimental viral myocarditis in mice J Cardiovasc Pharmacol 42 588–592 Occurrence Handle14576505 Occurrence Handle1:CAS:528:DC%2BD3sXotlaqtLw%3D

    PubMed  CAS  Google Scholar 

  15. K Yamazaki S Miwa K Ueda S Tanaka S Toyokuni O Unimonh K Nishimura M Komeda (2004) ArticleTitlePrevention of myocardial reperfusion injury by poly(ADP-ribose) synthetase inhibitor, 3-aminobenzamide, in cardioplegic solution: in vitro study of isolated rat heart model Eur J Cardiothorac Surg 26 270–275 Occurrence Handle15296882 Occurrence Handle10.1016/j.ejcts.2004.04.044

    Article  PubMed  Google Scholar 

  16. S Toyokuni T Tanaka Y Hattori Y Nishiyama A Yoshida K Uchida H Hiai H Ochi T Osawa (1997) ArticleTitleQuantiative immunohistochemical determination of 8-hydroxy-2′-deoxyguanosine by a monoclonal antibody N45.1: its application to ferric nitrilotriacetate-induced renal carcinogenesis model Lab Invest 76 365–374 Occurrence Handle9121119 Occurrence Handle1:CAS:528:DyaK2sXis1Gru7Y%3D

    PubMed  CAS  Google Scholar 

  17. T Takatani K Takahashi Y Uozumi E Shikata Y Yamamoto T Itoh T Matsuda SW Schaffer Y Fujio J Azuma (2004) ArticleTitleTurine inhibits apoptosis by preventing formation of the Apaf-1/caspase-9 apoptosome Am J Physiol Cell Physiol 287 949–953 Occurrence Handle10.1152/ajpcell.00042.2004

    Article  Google Scholar 

  18. Q Wu JH Wang F Fennessy HP Redmond D Bouchier-Hayes (1999) ArticleTitleTaurine prevents high-glucose-induced human vascular endothelial cell apoptosis Am J Physiol Cell Physiol 277 1229–1238

    Google Scholar 

  19. E Oz MC Sivrikoz V Halit A Altunkaya G Take (2002) ArticleTitleThe role of taurine added to pulmonary reperfusion solutions is isolated guinea pig lungs Amino Acids 22 391–403 Occurrence Handle12107765 Occurrence Handle1:CAS:528:DC%2BD38XmvFCqt7g%3D

    PubMed  CAS  Google Scholar 

  20. MJ Novotny PM Hogan DM Paley HR Adams (1991) ArticleTitleSystolic and diastolic dysfunction of the left ventricle induced by dietary taurine deficiency in cats Am J Physiol Heart Circ Physiol 261 H121–H127 Occurrence Handle1:CAS:528:DyaK3MXltlCku78%3D

    CAS  Google Scholar 

  21. N Lake (1993) ArticleTitleLoss of cardiac myofibrils: mechanism of contractile deficits induced by taurine deficiency Am J Physiol Heart Circ Physiol 264 H1323–H1326 Occurrence Handle1:CAS:528:DyaK3sXkt1Gkt7g%3D

    CAS  Google Scholar 

  22. PD Pion MD Kittleson OR Rogers JG Morris (1987) ArticleTitleMyocardial failure in cats associated with low plasma taurine: a reversible cardiomyopathy Science 237 764–768 Occurrence Handle3616607 Occurrence Handle1:CAS:528:DyaL2sXltlehs74%3D

    PubMed  CAS  Google Scholar 

  23. Y Yamori L Liu K Ikeda A Miura S Mizushima T Miki Y Nara InstitutionalAuthorNameWHO-Cardiovascular Disease and Alimentary Comparison (CARDIAC) Study Group (2001) ArticleTitleDistribution of twenty-four hour urinary taurine excretion and association with ischemic heart disease mortality in 24 populations of 16 countries: results from the WHO-CARDIAC study Hypertens Res 24 453–457 Occurrence Handle11510759 Occurrence Handle1:CAS:528:DC%2BD3MXmslWns7k%3D Occurrence Handle10.1291/hypres.24.453

    Article  PubMed  CAS  Google Scholar 

  24. J Azuma A Sawamura N Awata H Ohta T Hamaguchi H Harada K Takihara H Hasegawa T Yamagami T Ishiyama (1985) ArticleTitleTherapeutic effect of taurine in congestive heart failure: a double-blind crossover trial Clin Cardiol 8 276–282 Occurrence Handle3888464 Occurrence Handle1:STN:280:BiqB3c3ktFA%3D Occurrence Handle10.1002/clc.4960080507

    Article  PubMed  CAS  Google Scholar 

  25. J Milei R Ferreira S Llesuy P Forcada J Covarrubias A Boveris (1992) ArticleTitleReduction of reperfusion injury with preoperative rapid intravenous infusion of taurine during myocardial revascularization Am Heart J 123 339–345 Occurrence Handle1736568 Occurrence Handle1:STN:280:By2C2c3pvFY%3D

    PubMed  CAS  Google Scholar 

  26. SW Schaffer V Pastukh V Solodushko J Kramer J Azuma (2002) ArticleTitleEffect of ischemia, calcium depletion and repletion, acidosis and hypoxia on cellular taurine content Amino Acids 23 395–400 Occurrence Handle12436206 Occurrence Handle1:CAS:528:DC%2BD38XoslOrtb0%3D Occurrence Handle10.1007/s00726-002-0201-3

    Article  PubMed  CAS  Google Scholar 

  27. MF Crass JB Lombardini (1977) ArticleTitleLoss of cardiac muscle taurine after acute left ventricular ischemia Life Sci 21 951–958 Occurrence Handle927022 Occurrence Handle1:CAS:528:DyaE1cXkt12l Occurrence Handle10.1016/0024-3205(77)90261-2

    Article  PubMed  CAS  Google Scholar 

  28. H Harada T Tsjino Y Watari H Nonaka N Emoto M Yokoyama (2004) ArticleTitleOral taurine supplementation prevents fructose-induced hypertention in rats Heart Vessels 19 132–136 Occurrence Handle15168061 Occurrence Handle10.1007/s00380-003-0757-1

    Article  PubMed  Google Scholar 

  29. GY Oudit MG Trivieri N Khaper T Husain GJ Wilson P Liu MJ Sole PH Backx (2004) ArticleTitleTaurine supplementation reduces oxidative stress and improves cardiovascular function in an iron-overload murine model Circulation 109 1877–1885 Occurrence Handle15037530 Occurrence Handle1:CAS:528:DC%2BD2cXivFKmsbg%3D Occurrence Handle10.1161/01.CIR.0000124229.40424.80

    Article  PubMed  CAS  Google Scholar 

  30. JM McCord (1988) ArticleTitleFree radicals and myocardial ischemia: overview and outlook J Free Radic Biol Med 4 9–14 Occurrence Handle1:CAS:528:DyaL1cXhtFSit7g%3D

    CAS  Google Scholar 

  31. JL Zeweier JT Flaherty ML Weisfeldt (1987) ArticleTitleDirect measurement of free radical generation following reperfusion of ischemic myocardium Proc Natl Acad Sci USA 84 1404–1408

    Google Scholar 

  32. SA Messina RJ Dawson (2000) ArticleTitleAttenuation of oxidative damage to DNA by taurine and taurine analogs Adv Exp Med Biol 483 355–367 Occurrence Handle11787620 Occurrence Handle1:CAS:528:DC%2BD3MXitFaht7g%3D

    PubMed  CAS  Google Scholar 

  33. S Miwa S Toyokuni T Nishina T Nomoto M Hiroyasu K Nishimura M Komeda (2002) ArticleTitleSpatiotemporal alteration of 8-hydroxy-2′-deoxyguanosine levels in cardiomyocytes after myocardial infarction in rats Free Radic Res 36 853–858 Occurrence Handle12420743 Occurrence Handle1:CAS:528:DC%2BD3sXitlSlsrs%3D

    PubMed  CAS  Google Scholar 

  34. CE Wright HH Tallan YY Lin (1986) ArticleTitleTaurine: biological update Annu Rev Biochem 55 427–453 Occurrence Handle3527049 Occurrence Handle1:CAS:528:DyaL28XlsVyhsbs%3D

    PubMed  CAS  Google Scholar 

  35. JA Timbrell V Seabra CJ Waterfield (1995) ArticleTitleThe in vivo and in vitro protective properties of taurine Gen Pharmacol 26 453–462 Occurrence Handle7789717 Occurrence Handle1:CAS:528:DyaK2MXkslyltLk%3D

    PubMed  CAS  Google Scholar 

  36. HP Redmond JH Wang D Bouchier-Hayes (1996) ArticleTitleTaurine attenuates nitric oxide- and reactive oxygen intermediate-dependent hepatocyte injury Arch Surg 131 1287–1288

    Google Scholar 

  37. R Cozzi R Ricordy F Bartolini L Ramadori P Perticone RD Salvia (1995) ArticleTitleTaurine and ellagic acid: two differently-acting natural antioxidants Environ Mol Mutagen 26 248–254 Occurrence Handle7588651 Occurrence Handle1:CAS:528:DyaK2MXptlehu7o%3D

    PubMed  CAS  Google Scholar 

  38. T Nakashima T Taniko K Kuriyama (1982) ArticleTitleTherapeutic effect of taurine administration on carbon tetrachloride-induced hepatic injury Jpn J Pharmacol 32 583–589 Occurrence Handle7131945 Occurrence Handle1:CAS:528:DyaL38XltVGiu7c%3D

    PubMed  CAS  Google Scholar 

  39. H Gurer H Ozgunes E Saygin N Ercal (2001) ArticleTitleAntioxidant effect of taurine against lead-induced oxidative stress Arch Environ Contam Toxicol 41 397–402 Occurrence Handle11598776 Occurrence Handle1:CAS:528:DC%2BD3MXovFKktbc%3D

    PubMed  CAS  Google Scholar 

  40. BP Vohra X Hui (2001) ArticleTitleTaurine protects against carbon tetrachloride toxicity in the cultured neurons and in vivo Arch Physiol Biochem 109 90–94 Occurrence Handle11471076 Occurrence Handle1:CAS:528:DC%2BD3MXlsVCiu74%3D Occurrence Handle10.1076/apab.109.1.90.4287

    Article  PubMed  CAS  Google Scholar 

  41. BO Ahn KH Kim G Lee HS Lee CD Kim YS Kim MW Son WB Kim TY Oh JH Hyun (2001) ArticleTitleEffects of taurine on cerulein-induced acute pancreatitis in the rat Pharmacology 63 1–7 Occurrence Handle11408826 Occurrence Handle1:CAS:528:DC%2BD3MXlt1ais70%3D Occurrence Handle10.1159/000056106

    Article  PubMed  CAS  Google Scholar 

  42. H Ha MR Yu KH Kim (1999) ArticleTitleMelatonin and taurine reduce early glomerulopathy in diabetic rats Free Radic Biol Med 26 944–950 Occurrence Handle10232838 Occurrence Handle1:CAS:528:DyaK1MXislGksbw%3D Occurrence Handle10.1016/S0891-5849(98)00276-7

    Article  PubMed  CAS  Google Scholar 

  43. RA Gottlib RL Engler (1999) ArticleTitleApoptosis in myocardial ischemia-reperfusion Ann NY Acad Sci 874 412–426

    Google Scholar 

  44. CA Beltrami N Finato M Rocco GA Feruglio C Puricelli E Cigola F Quaini EH Sonnenblick G Olivetti P Anversa (1994) ArticleTitleStructural basis of end-stage failure in ischemic cardiomyopathy in humans Circulation 89 151–163 Occurrence Handle8281642 Occurrence Handle1:STN:280:ByuC3cbgtV0%3D

    PubMed  CAS  Google Scholar 

  45. DW Nicholson A Ali NA Thornberry JP Vaillancourt CK Ding M Gallant Y Gareau PR Griffin M Labelle YA Lazebnik (1995) ArticleTitleIdentification and inhibition of the ICE/CED-3 protease necessary for mammalian apoptosis Nature 376 37–43 Occurrence Handle7596430 Occurrence Handle1:CAS:528:DyaK2MXmvVGqu7k%3D Occurrence Handle10.1038/376037a0

    Article  PubMed  CAS  Google Scholar 

  46. J Li B Zhang Z Huang S Wang C Tang J Du (2004) ArticleTitleTaurine prevents ß-glycerophosphate-induced calcification in cultured rat vascular smooth cells Heart Vessels 19 125–131 Occurrence Handle15168060 Occurrence Handle10.1007/s00380-003-0733-9

    Article  PubMed  Google Scholar 

Download references

Author information

Authors and Affiliations

Authors

Corresponding author

Correspondence to Masashi Komeda.

Rights and permissions

Reprints and permissions

About this article

Cite this article

Oriyanhan, W., Yamazaki, K., Miwa, S. et al. Taurine prevents myocardial ischemia/reperfusion-induced oxidative stress and apoptosis in prolonged hypothermic rat heart preservation. Heart Vessels 20, 278–285 (2005). https://doi.org/10.1007/s00380-005-0841-9

Download citation

  • Received:

  • Accepted:

  • Issue Date:

  • DOI: https://doi.org/10.1007/s00380-005-0841-9

Key words

Navigation