Home LiteratureArticle Details
PMID: 9746488 Published · ppublish English Journal Article Research Support, Non-U.S. Gov't Research Support, U.S. Gov't, P.H.S.

Demonstration of an early and a late phase of ischemic preconditioning in mice.

The American journal of physiology ·Vol. 275 ·No. 4 ·1998-00-00 ·Pages H1375-87

Guo Y, Wu WJ, Qiu Y, Tang XL, Yang Z, Bolli R

Abstract

It is unknown whether ischemic preconditioning (PC; either early or late) occurs in the mouse. The goal of this study was to answer this question and to develop a reliable and physiologically relevant murine model of both early and late ischemic PC. A total of 201 mice were used. In nonpreconditioned open-chest animals subjected to 30 min of coronary occlusion followed by 24 h of reperfusion, infarct size (tetrazolium staining) averaged 52% of the region at risk. When the 30-min occlusion was performed 10 min after a PC protocol consisting of six cycles of 4-min occlusion and 4-min reperfusion, infarct size was reduced by 75%, indicating an early PC effect. When the 30-min occlusion was performed 24 h after the same PC protocol, infarct size was reduced by 48%, indicating a late PC effect. In mice in which the 30-min occlusion was followed by 4 h of reperfusion, infarct size was similar to that observed after 24 h of reperfusion, indicating that a 4-h reperfusion interval is sufficient to detect the final extent of cell death in this model. Fundamental physiological variables (body temperature, arterial oxygenation, acid-base balance, heart rate, and arterial pressure) were measured and found to be within normal limits. Taken together, these results demonstrate that, in the mouse, a robust infarct-sparing effect occurs during both the early and the late phases of ischemic PC, although the early phase is more powerful. This murine model is physiologically relevant, provides reliable measurements, and should be useful for elucidating the cellular mechanisms of ischemic PC in genetically engineered animals.

MeSH Terms
Animals Coronary Vessels/physiology Heart/physiology,physiopathology Heart Rate Ischemic Preconditioning/methods Male Mice Mice, Inbred ICR Myocardial Infarction/pathology,physiopathology Myocardial Ischemia/physiopathology Myocardial Reperfusion Myocardium/pathology Time Factors
Authors & Affiliations
6 authors, click to expand affiliations / ORCID
Guo Y
Experimental Research Laboratory, Division of Cardiology, University of Louisville, Louisville, Kentucky 40292, USA.
Wu W J
Qiu Y
Tang X L
Yang Z
Bolli R
References (49)
49 references, click to expand
  1. Salt-sensitive hypertension in transgenic mice overexpressing Na(+)-proton exchanger.
    Circ Res. 1995 Jan;76(1):148-53 PMID: 8001273
  2. Adenosine receptor involvement in a delayed phase of myocardial protection 24 hours after ischemic preconditioning.
    Circulation. 1994 Dec;90(6):2993-3000 PMID: 7994847
  3. The protective effect of late preconditioning against myocardial stunning in conscious rabbits is mediated by nitric oxide synthase. Evidence that nitric oxide acts both as a trigger and as a mediator of the late phase of ischemic preconditioning.
    Circ Res. 1997 Dec;81(6):1094-107 PMID: 9400391
  4. Blood pressure and fluid-electrolyte balance in ANF-transgenic mice on high- and low-salt diets.
    Am J Physiol. 1995 Jul;269(1 Pt 2):R186-92 PMID: 7631892
  5. A comparative study with various anesthetics in mice (pentobarbitone, ketamine-xylazine, carfentanyl-etomidate).
    Res Exp Med (Berl). 1984;184(3):159-69 PMID: 6473905
  6. Direct evidence that protein kinase C plays an essential role in the development of late preconditioning against myocardial stunning in conscious rabbits and that epsilon is the isoform involved.
    J Clin Invest. 1998 May 15;101(10):2182-98 PMID: 9593774
  7. Myocardial adaptation, stress proteins, and the second window of protection.
    Ann N Y Acad Sci. 1996 Sep 30;793:123-41 PMID: 8906161
  8. Generation of transgenic mice with elevated blood pressure by introduction of the rat renin and angiotensinogen genes.
    Proc Natl Acad Sci U S A. 1990 Jul;87(13):5153-7 PMID: 2195550
  9. Nitric oxide synthase is the mediator of late preconditioning against myocardial infarction in conscious rabbits.
    Circulation. 1998 Aug 4;98(5):441-9 PMID: 9714095
  10. "Normothermic range" temperature affects myocardial infarct size.
    Cardiovasc Res. 1994 Jul;28(7):1014-7 PMID: 7954586
  11. Ischemic preconditioning induces selective translocation of protein kinase C isoforms epsilon and eta in the heart of conscious rabbits without subcellular redistribution of total protein kinase C activity.
    Circ Res. 1997 Sep;81(3):404-14 PMID: 9285643
  12. Differences in reperfusion length following 30 minutes of ischemia in the rabbit influence infarct size, as measured by triphenyltetrazolium chloride staining.
    J Mol Cell Cardiol. 1997 Feb;29(2):657-66 PMID: 9140823
  13. Preconditioning protects ischemic rabbit heart by protein kinase C activation.
    Am J Physiol. 1994 Mar;266(3 Pt 2):H1145-52 PMID: 8160817
  14. Selective activation of A3 adenosine receptors with N6-(3-iodobenzyl)adenosine-5'-N-methyluronamide protects against myocardial stunning and infarction without hemodynamic changes in conscious rabbits.
    Circ Res. 1997 Jun;80(6):800-9 PMID: 9168782
  15. Evidence that late preconditioning against myocardial stunning in conscious rabbits is triggered by the generation of nitric oxide.
    Circ Res. 1997 Jul;81(1):42-52 PMID: 9201026
  16. Involvement of protein kinase C in the delayed cytoprotection following sublethal ischaemia in rabbit myocardium.
    Br J Pharmacol. 1995 May;115(2):222-4 PMID: 7545515
  17. Cardiac stress protein elevation 24 hours after brief ischemia or heat stress is associated with resistance to myocardial infarction.
    Circulation. 1993 Sep;88(3):1264-72 PMID: 8353888
  18. Phosphorylation of tyrosine 182 of p38 mitogen-activated protein kinase correlates with the protection of preconditioning in the rabbit heart.
    J Mol Cell Cardiol. 1997 Sep;29(9):2383-91 PMID: 9299362
  19. Effect of human recombinant superoxide dismutase on canine myocardial infarction.
    Am J Physiol. 1990 Feb;258(2 Pt 2):H369-80 PMID: 2309904
  20. Acadesine extends the window of protection afforded by ischaemic preconditioning in conscious rabbits.
    Cardiovasc Res. 1995 May;29(5):653-7 PMID: 7606753
  21. Salt-resistant hypertension in mice lacking the guanylyl cyclase-A receptor for atrial natriuretic peptide.
    Nature. 1995 Nov 2;378(6552):65-8 PMID: 7477288
  22. Characterisation of the infarct-limiting effect of delayed preconditioning: timecourse and dose-dependency studies in rabbit myocardium.
    Basic Res Cardiol. 1997 Jun;92(3):159-67 PMID: 9226101
  23. Time course of late preconditioning against myocardial stunning in conscious pigs.
    Circ Res. 1996 Sep;79(3):424-34 PMID: 8781476
  24. Hypertension in mice lacking the gene for endothelial nitric oxide synthase.
    Nature. 1995 Sep 21;377(6546):239-42 PMID: 7545787
  25. Overexpression of heat shock protein 72 in transgenic mice decreases infarct size in vivo.
    Circulation. 1996 Sep 15;94(6):1408-11 PMID: 8823000
  26. The early and late phases of ischemic preconditioning: a comparative analysis of their effects on infarct size, myocardial stunning, and arrhythmias in conscious pigs undergoing a 40-minute coronary occlusion.
    Circ Res. 1997 May;80(5):730-42 PMID: 9130454
  27. Role of adenosine receptors in late preconditioning against myocardial stunning in conscious rabbits.
    Am J Physiol. 1997 Sep;273(3 Pt 2):H1324-32 PMID: 9321822
  28. Selection for blood pressure levels in mice.
    Genetics. 1974 Mar;76(3):537-49 PMID: 4833575
  29. The early and late phases of preconditioning against myocardial stunning and the essential role of oxyradicals in the late phase: an overview.
    Basic Res Cardiol. 1996 Jan-Feb;91(1):57-63 PMID: 8660262
  30. Effect of temperature on myocardial infarction in swine.
    Am J Physiol. 1996 Apr;270(4 Pt 2):H1189-99 PMID: 8967356
  31. Adenosine A1 receptors, KATP channels, and ischemic preconditioning in dogs.
    Am J Physiol. 1993 May;264(5 Pt 2):H1327-36 PMID: 8498546
  32. Species-specific kinetics of mouse renin contribute to maintenance of normal blood pressure in transgenic mice with overexpressed human angiotensinogen.
    J Vet Med Sci. 1992 Dec;54(6):1191-3 PMID: 1477169
  33. Ischemic preconditioning Nature's own cardioprotective intervention.
    Trends Cardiovasc Med. 1992 Sep-Dec;2(5):170-6 PMID: 21239250
  34. Preconditioning potentiates molecular signaling for myocardial adaptation to ischemia.
    Ann N Y Acad Sci. 1996 Sep 30;793:191-209 PMID: 8906166
  35. Late preconditioning against myocardial stunning. An endogenous protective mechanism that confers resistance to postischemic dysfunction 24 h after brief ischemia in conscious pigs.
    J Clin Invest. 1995 Jan;95(1):388-403 PMID: 7814639
  36. Genistein, a tyrosine kinase inhibitor, blocks the "second window of protection" 48 h after ischemic preconditioning in the rabbit.
    J Mol Cell Cardiol. 1997 Jul;29(7):1885-93 PMID: 9236142
  37. Epicardial temperature is a major predictor of myocardial infarct size in dogs.
    J Mol Cell Cardiol. 1997 Jun;29(6):1577-83 PMID: 9220343
  38. Myocardial ischemia and reperfusion: a murine model.
    Am J Physiol. 1995 Dec;269(6 Pt 2):H2147-54 PMID: 8594926
  39. Infarct limitation of the second window of protection in a conscious rabbit model.
    Cardiovasc Res. 1996 May;31(5):777-83 PMID: 8763407
  40. Evidence for an essential role of reactive oxygen species in the genesis of late preconditioning against myocardial stunning in conscious pigs.
    J Clin Invest. 1996 Jan 15;97(2):562-76 PMID: 8567981
  41. Delayed effects of sublethal ischemia on the acquisition of tolerance to ischemia.
    Circ Res. 1993 Jun;72(6):1293-9 PMID: 8495557
  42. Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium.
    Circulation. 1986 Nov;74(5):1124-36 PMID: 3769170
  43. Some statistical methods useful in circulation research.
    Circ Res. 1980 Jul;47(1):1-9 PMID: 7379260
  44. Human tissue kallikrein induces hypotension in transgenic mice.
    Hypertension. 1994 Feb;23(2):236-43 PMID: 7508423
  45. Attenuation of myocardial ischaemic injury 24 h after diacylglycerol treatment in vivo.
    J Mol Cell Cardiol. 1997 Jul;29(7):1967-75 PMID: 9236150
  46. Myocardial temperature in acute myocardial infarction: protection with mild regional hypothermia.
    Am J Physiol. 1997 Jul;273(1 Pt 2):H220-7 PMID: 9249493
  47. Chimeric renin-angiotensin system demonstrates sustained increase in blood pressure of transgenic mice carrying both human renin and human angiotensinogen genes.
    J Biol Chem. 1993 Jun 5;268(16):11617-21 PMID: 8505294
  48. Nitric oxide triggers late preconditioning against myocardial infarction in conscious rabbits.
    Am J Physiol. 1997 Dec;273(6 Pt 2):H2931-6 PMID: 9435634
  49. Conscious rabbits become tolerant to multiple episodes of ischemic preconditioning.
    Circ Res. 1994 May;74(5):998-1004 PMID: 8156647
Article Info
Journal
The American journal of physiology
Abbr.
Am J Physiol
ISSN
0002-9513
Published
1998-00-00
Pages
H1375-87
Language
English
Region
United States
NLM ID
0370511
PMCID
PMC3701297
Subset
IM
Grants
NHLBI NIH HHS · R37 HL055757 · United States
NHLBI NIH HHS · R01 HL055757 · United States
NHLBI NIH HHS · R01 HL043151 · United States
NHLBI NIH HHS · R01 HL-43151 · United States
NHLBI NIH HHS · HL-55757 · United States
Analysis Services
Analysis Services

Contact

No. 2 Wenbo Road, Zhangqiu District, Jinan, Shandong

Qilu Normal University · Genelibs Bioinformatics Lab

750 Shunhua Rd, Jinan

2F, Bldg F, University Science Park

Tel: 0531-88819269

WeChat Official Account

Follow our WeChat subscription account for real-time updates and the latest in medical and biological research.


Business Email

E-mail: [email protected]