Endothelial nitric oxide synthase mediates the first and inducible nitric oxide synthase mediates the second window of desflurane-induced preconditioning

Journal of Cardiothoracic and Vascular Anesthesia

Volumn 27, Issue 3, 2013, Pages 494-501

  Redel, Andreas ^a,b   Stumpner, Jan ^a   Smul, Thorsten M ^a   Lange, Markus ^a   Jazbutyte, Virginija ^c   Ridyard, Douglas G ^d   Roewer, Norbert ^b   Kehl, Franz ^e  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c HANNOVER MEDICAL SCHOOL   (Germany)

^d UNIVERSITY OF COLORADO SCHOOL OF MEDICINE   (United States)

^e Department of Anesthesiology Klinikum   (Germany)

Author keywords

anesthetic induced preconditioning; endothelial nitric oxide synthase; inducible nitric oxide synthase; mouse; myocardial infarction

Indexed keywords

DESFLURANE; ENDOTHELIAL NITRIC OXIDE SYNTHASE; EVANS BLUE; INDUCIBLE NITRIC OXIDE SYNTHASE; TRIPHENYLTETRAZOLIUM;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CORONARY REPERFUSION; HEART INFARCTION; HEART INFARCTION SIZE; ISCHEMIC PRECONDITIONING; LABORATORY TEST; MALE; MOUSE; NONHUMAN; PRIORITY JOURNAL; PROSPECTIVE STUDY; RESPIRATORY TRACT PARAMETERS; STAINING; WILD TYPE;

ANESTHETICS, INHALATION; ANIMALS; ARTERIAL PRESSURE; BODY WEIGHT; CORONARY VESSELS; HEART RATE; HEMODYNAMICS; ISCHEMIC PRECONDITIONING, MYOCARDIAL; ISOFLURANE; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE III;

EID: 84877775305     PISSN: 10530770     EISSN: 15328422     Source Type: Journal    
DOI: 10.1053/j.jvca.2012.04.015     Document Type: Article

References (51)

1. J.R. Kersten, T.J. Schmeling, P.S. Pagel Isoflurane mimics ischemic preconditioning via activation of K(ATP) channels: Reduction of myocardial infarct size with an acute memory phase Anesthesiology 87 1997 361 370
2. M. Tonkovic-Capin, G.J. Gross, Z.J. Bosnjak Delayed cardioprotection by isoflurane: Role of K(ATP) channels Am J Physiol Heart Circ Physiol 283 2002 H61 H68
3. H. Horimoto, G.R. Gaudette, A.E. Saltman The role of nitric oxide, K(+)(ATP) channels, and cGMP in the preconditioning response of the rabbit J Surg Res 92 2000 56 63
4. A. Nakano, G.S. Liu, G. Heusch Exogenous nitric oxide can trigger a preconditioned state through a free radical mechanism, but endogenous nitric oxide is not a trigger of classical ischemic preconditioning J Mol Cell Cardiol 32 2000 1159 1167
5. R.M. Bell, D.M. Yellon The contribution of endothelial nitric oxide synthase to early ischaemic preconditioning: The lowering of the preconditioning threshold An investigation in eNOS knockout mice Cardiovasc Res 52 2001 274 280
6. H. Post, R. Schulz, M. Behrends No involvement of endogenous nitric oxide in classical ischemic preconditioning in swine J Mol Cell Cardiol 32 2000 725 733
7. E.O. Weselcouch, A.J. Baird, P. Sleph Inhibition of nitric oxide synthesis does not affect ischemic preconditioning in isolated perfused rat hearts Am J Physiol Heart Circ Physiol 268 1995 H242 H249
8. R.G. Woolfson, V.C. Patel, G.H. Neild Inhibition of nitric oxide synthesis reduces infarct size by an adenosine-dependent mechanism Circulation 91 1995 1545 1551
9. R. Bolli Cardioprotective function of inducible nitric oxide synthase and role of nitric oxide in myocardial ischemia and preconditioning: An overview of a decade of research J Mol Cell Cardiol 33 2001 1897 1918
10. Y.T. Xuan, X.L. Tang, Y. Qiu Biphasic response of cardiac NO synthase isoforms to ischemic preconditioning in conscious rabbits Am J Physiol Heart Circ Physiol 279 2000 H2360 H2371
11. T.M. Smul, M. Lange, A. Redel Desflurane-induced preconditioning against myocardial infarction is mediated by nitric oxide Anesthesiology 105 2006 719 725
12. C.H. Chen, J.H. Chuang, K. Liu Nitric oxide triggers delayed anesthetic preconditioning-induced cardiac protection via activation of nuclear factor-kappaB and upregulation of inducible nitric oxide synthase Shock 30 2008 241 249
13. Y. Guo, W.K. Jones, Y.T. Xuan The late phase of ischemic preconditioning is abrogated by targeted disruption of the inducible NO synthase gene Proc Natl Acad Sci U S A 96 1999 11507 11512
14. R. Bolli, B. Dawn, X.L. Tang The nitric oxide hypothesis of late preconditioning Basic Res Cardiol 93 1998 325 338
15. P.L. Huang, Z. Huang, H. Mashimo Hypertension in mice lacking the gene for endothelial nitric oxide synthase Nature 377 1995 239 242
16. V.E. Laubach, E.G. Shesely, O. Smithies Mice lacking inducible nitric oxide synthase are not resistant to lipopolysaccharide-induced death Proc Natl Acad Sci U S A 92 1995 10688 10692
17. K. Bayne Revised guide for the care and use of laboratory animals available American Physiological Society Physiologist 39 1996 208 211
18. A. Redel, V. Jazbutyte, T.M. Smul Impact of ischemia and reperfusion times on myocardial infarct size in mice in vivo Exp Biol Med (Maywood) 233 2008 84 93
19. T. Grenz, A. Köhler, D. Eckle Systematic evaluation of a novel model for cardiac ischemic preconditioning in mice Am J Physiol Heart Circ Physiol 291 2006 H2533 H2540
20. J.M. Sonner, D. Gong, E.I. Eger II Naturally occurring variability in anesthetic potency among inbred mouse strains Anesth Analg 91 2000 720 726
21. A. Redel, J. Stumpner, T. Tischer-Zeitz Comparison of isoflurane-, sevoflurane-, and desflurane-induced pre- and postconditioning against myocardial infarction in mice in vivo Exp Biol Med (Maywood) 234 2009 1186 1191
22. L.H. Michael, M.L. Entman, C.J. Hartley Myocardial ischemia and reperfusion: A murine model Am J Physiol Heart Circ Physiol 269 1995 H2147 H2154
23. J. Stumpner, A. Redel, A. Kellermann Differential role of Pim-1 kinase in anesthetic-induced and ischemic preconditioning against myocardial infarction Anesthesiology 111 2009 1257 1264
24. A. Redel, M. Lange, V. Jazbutyte Activation of mitochondrial large-conductance calcium-activated K+ channels via protein kinase A mediates desflurane-induced preconditioning Anesth Analg 106 2008 384 391
25. K. Tanaka, L.M. Ludwig, J.G. Krolikowski Isoflurane produces delayed preconditioning against myocardial ischemia and reperfusion injury: Role of cyclooxygenase-2 Anesthesiology 100 2004 525 531
26. Y. Shi, W.C. Hutchins, J. Su Delayed cardioprotection with isoflurane: Role of reactive oxygen and nitrogen Am J Physiol Heart Circ Physiol 288 2005 H175 H184
27. T.M. Smul, A. Redel, J. Stumpner Time course of desflurane-induced preconditioning in rabbits J Cardiothorac Vasc Anesth 24 2010 91 98
28. M. Wakeno-Takahashi, H. Otani, S. Nakao Isoflurane induces second window of preconditioning through upregulation of inducible nitric oxide synthase in rat heart Am J Physiol Heart Circ Physiol 289 2005 H2585 H2591
29. Y.M. Tsutsumi, H.H. Patel, D. Huang Role of 12-lipoxygenase in volatile anesthetic-induced delayed preconditioning in mice Am J Physiol Heart Circ Physiol 291 2006 H979 H983
30. J.G. Krolikowski, D. Weihrauch, M. Bienengraeber Role of ERK1/2, p70s6k, and eNOS in isoflurane-induced cardioprotection during early reperfusion in vivo Can J Anaesth 53 2006 174 182
31. Z.D. Ge, D. Pravdic, M. Bienengraeber Isoflurane postconditioning protects against reperfusion injury by preventing mitochondrial permeability transition by an endothelial nitric oxide synthase-dependent mechanism Anesthesiology 112 2010 73 85
32. T. Smul, M. Lange, A. Redel Desflurane-induced cardioprotection against ischemia-reperfusion injury depends on timing J Cardiothorac Vasc Anesth 23 2009 600 606
33. Y. Guo, Q. Li, W.J. Wu Endothelial nitric oxide synthase is not necessary for the early phase of ischemic preconditioning in the mouse J Mol Cell Cardiol 44 2008 496 501
34. P.C. Chiari, M.W. Bienengraeber, D. Weihrauch Role of endothelial nitric oxide synthase as a trigger and mediator of isoflurane-induced delayed preconditioning in rabbit myocardium Anesthesiology 103 2005 74 83
35. W.K. Alderton, C.E. Cooper, R.G. Knowles Nitric oxide synthases: Structure, function and inhibition Biochem J 357 2001 593 615
36. R. Schulz, M. Kelm, G. Heusch Nitric oxide in myocardial ischemia/reperfusion injury Cardiovasc Res 61 2004 402 413
37. L.S. Burwell, P.S. Brookes Mitochondria as a target for the cardioprotective effects of nitric oxide in ischemia-reperfusion injury Antioxid Redox Signal 10 2008 579 599
38. B. Dawn, R. Bolli Role of nitric oxide in myocardial preconditioning Ann N Y Acad Sci 962 2002 18 41
39. G. Landoni, G.G. Biondi-Zoccai, A. Zangrillo Desflurane and sevoflurane in cardiac surgery: A meta-analysis of randomized clinical trials J Cardiothorac Vasc Anesth 21 2007 502 511
40. C.H. Yu, W.S. Beattie The effects of volatile anesthetics on cardiac ischemic complications and mortality in CABG: A meta-analysis Can J Anaesth 53 2006 906 918
41. J.A. Symons, P.S. Myles Myocardial protection with volatile anaesthetic agents during coronary artery bypass surgery: A meta-analysis Br J Anaesth 97 2006 127 136
42. M. Lange, T.M. Smul, C.A. Blomeyer Role of the beta1-adrenergic pathway in anesthetic and ischemic preconditioning against myocardial infarction in the rabbit heart in vivo Anesthesiology 105 2006 503 510
43. F. Kehl, J.G. Krolikowski, B. Mraovic Hyperglycemia prevents isoflurane-induced preconditioning against myocardial infarction Anesthesiology 96 2002 183 188
44. K. Tanaka, F. Kehl, W. Gu Isoflurane-induced preconditioning is attenuated by diabetes Am J Physiol Heart Circ Physiol 282 2002 H2018 H2023
45. K. Boengler, R. Schulz, G. Heusch Loss of cardioprotection with ageing Cardiovasc Res 83 2009 247 261
46. H. Brunner, J.R. Cockcroft, J. Deanfield Endothelial function and dysfunction. part II: Association with cardiovascular risk factors and diseases A statement by the Working Group on Endothelins and Endothelial Factors of the European Society of Hypertension J Hypertens 23 2005 233 246
47. B.R. Sharp, S.P. Jones, D.M. Rimmer Differential response to myocardial reperfusion injury in eNOS-deficient mice Am J Physiol Heart Circ Physiol 282 2002 H2422 H2426
48. M.V. Brahmajothi, D.L. Campbell Heterogeneous basal expression of nitric oxide synthase and superoxide dismutase isoforms in mammalian heart: Implications for mechanisms governing indirect and direct nitric oxide-related effects Circ Res 85 1999 575 587
49. C. Martin, R. Schulz, H. Post Microdialysis-based analysis of interstitial NO in situ: NO synthase-independent NO formation during myocardial ischemia Cardiovasc Res 74 2007 46 55
50. M.P. Maxwell, D.J. Hearse, D.M. Yellon Species variation in the coronary collateral circulation during regional myocardial ischaemia: A critical determinant of the rate of evolution and extent of myocardial infarction Cardiovasc Res 21 1987 737 746
51. M.S. Sumeray, D.D. Rees, D.M. Yellon Infarct size and nitric oxide synthase in murine myocardium J Mol Cell Cardiol 32 2000 35 42