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Improved Myocardial Ischemia/Reperfusion Injury in Mice

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Improved Myocardial Ischemia/Reperfusion Injury in Mice Journal of the American College of Cardiology Vol. 39, No. 7, 2002 © 2002 by the American College of Cardiology Foundation ISSN 0735-1097/02/$22.00 Published by Elsevier Science Inc. PII S0735-1097(02)01738-2 Improved Myocardial Ischemia/Reperfusion Injury in Mice Lacking Tumor Necrosis Factor-␣ Naoya Maekawa, BSC,* Hisayasu Wada, MD, PHD,* Tsugiyasu Kanda, MD, PHD,‡ Tamikazu Niwa, BSC,* Yasuhiro Yamada, MD, PHD,* Kuniaki Saito, PHD,* Hisayoshi Fujiwara, MD, PHD,† Kenji Sekikawa, PHD,§ Mitsuru Seishima, MD, PHD* Gifu, Maebashi and Tsukuba, Japan OBJECTIVES This study sought to assess the role of tumor necrosis factor-␣ (TNF-␣) in myocardial ischemia/reperfusion (I/R) injury using TNF-␣ knockout (KO) mice. BACKGROUND Tumor necrosis factor-␣ is thought to be involved in the pathogenesis of myocardial I/R injury by promoting leukocyte infiltration of the myocardium. However, the precise role of TNF-␣ in I/R injury is still unknown. METHODS The hearts in TNF-␣ KO and wild-type (WT) mice were exposed by left lateral thoracotomy, and the left coronary artery was occluded for 30 min then reperfused for 120 min. RESULTS The infarct size in TNF-␣ KO mice was significantly reduced compared with WT mice. The frequency of arrhythmia was decreased, and cardiac function during reperfusion was significantly improved in TNF-␣ KO mice compared with WT mice. The activation of nuclear factor-␬B (NF-␬B), the expression of chemokines and adhesion molecules and the infiltration of leukocytes were also significantly reduced in TNF-␣ KO mice, compared with WT mice. These findings provide evidence that TNF-␣ aggravates I/R injury. CONCLUSIONS Tumor necrosis factor-␣ exacerbates myocardial I/R injury at an early stage of reperfusion by activating NF-␬B, thereby inducing chemokines and adhesion molecules and facilitating leukocyte infiltration. (J Am Coll Cardiol 2002;39:1229–35) © 2002 by the American College of Cardiology Foundation Recanalization of occluded coronary arteries is a standard tant to reevaluate the effects of TNF-␣ on myocardial I/R method of treatment for acute myocardial infarction. How- injury using TNF-␣ KO. ever, reperfusion itself can cause myocardial damage, which is designated as ischemia/reperfusion (I/R) injury. Numer- METHODS ous studies have demonstrated that leukocyte infiltration Animals. Tumor necrosis factor-␣ KO mice were gener- occurs in the reperfused myocardium (1). Leukocytes, espe- ated by gene targeting, as described previously (6). cially polymorphonuclear neutrophils, mediate the damage C57BL/6J mice were used as wild-type (WT) controls. to endothelial cells and cardiac myocytes during reperfusion. Male mice at 12 to 13 weeks of age were used for this Tumor necrosis factor-␣ (TNF-␣) is known to be a experiment, which was performed according to the “Posi- proinflammatory cytokine. Recent studies have demon- tion of the American Heart Association on Research Ani- strated that TNF-␣ is produced during I/R injury (2,3) and ␬ ␬ mal Use,” adopted by the American Heart Association activates nuclear factor- B (NF- B), which initiates the November 11, 1984. cytokine cascade and facilitates the expression of chemo- ␣ Surgical procedures. Mice were anesthetized with 2% kines and adhesion molecules. Treatment with anti-TNF- halothane (Takeda Pharmaceutical, Osaka, Japan) and 40% antibody has been reported to improve myocardial recovery oxygen, and maintained with 0.5% halothane and 40% after I/R (4). oxygen. Tracheotomy was performed to provide artificial In contrast, beneficial effects of TNF-␣ on acute myo- ␣ ventilation (0.3 ml tidal volume, 120 breaths/min), and the cardial infarction (5) have also been reported, where TNF- left coronary artery was ligated with an 8-0 nylon surgical receptor knockout (KO) mice show accelerated myocardial ␣ suture 1.0 mm distal from tip of the left auricle. apoptosis after ischemia, indicating that TNF- has a Measurements of infarct area and area at risk. After protective action against ischemia. Accordingly, it is impor- 30-min ligation and 120-min reperfusion, the left coronary artery was reoccluded at the same point and Evans blue dye From the *Department of Laboratory Medicine, Gifu University School of was perfused from the left ventricular (LV) cavity. The heart Medicine, Gifu, Japan; †Second Department of Internal Medicine, Gifu University was removed and cut transversely into five sections, which School of Medicine, Gifu, Japan; ‡Department of Laboratory Medicine, Gunma were then incubated in a 1.0% solution of 2,3,5-triphenyl- University School of Medicine, Maebashi, Japan; and §Department of Immunology, National Institute of Animal Health, Tsukuba, Japan. This work was supported in tetrazolium chloride (TTC; Sigma, St. Louis, Missouri) for part by a grant-in-aid for General Scientific Research from the Japanese Ministry of 20 min at 37°C. The area at risk (AAR) and the infarct area Education, Science and Culture (10670641), and Charitable Trust Clinical Pathology (IA) corresponded to the area unstained with Evans blue Research Foundation of Japan. Manuscript received February 28, 2001; revised manuscript received January 2, dye and the area unstained with TTC solution, respectively. 2002, accepted January 11, 2002. Each slice of the ventricle was weighed, and the AAR to LV 1230 Maekawa et al. JACC Vol. 39, No. 7, 2002 Ischemia/Reperfusion in TNF-␣ Knockout Mice April 3, 2002:1229–35 Abbreviations and Acronyms AAR ϭ area at risk IA ϭ infarct area ICAM ϭ intercellular adhesion molecule IL ϭ interleukin I/R ϭ ischemia/reperfusion KO ϭ knockout LV ϭ left ventricle MCP ϭ monocyte chemoattractant protein MIP ϭ macrophage inflammatory protein NF-␬B ϭ nuclear factor-␬B RT-PCR ϭ reverse transcription and polymerase chain reaction TNF-␣ ϭ tumor necrosis factor-␣ WT ϭ wild-type ratio and IA to LV ratio of each slice were determined using National Institutes of Health Image version 1.62. Neutralization of TNF-␣ with a selective antibody. To neutralize the action of TNF-␣ in WT mice, 10 ␮g of goat anti-mouse TNF-␣ polyclonal antibody (AF-410-NA; R&D Systems Inc., Minneapolis, Minnesota) dissolved in 0.1 ml of saline was injected through the tail vein 30 min before left coronary artery ligation. Figure 2. Hemodynamic parameters measured just before the end of reperfusion. Summarized data on peak left ventricular systolic pressure (LVSP) (A) and maximal positive rate of the first derivative of left ventricular pressure (dP/dtmax) (B) in the sham-operated wild-type mice (solid bars) (n ϭ 5), tumor necrosis factor (TNF)-␣ knockout (KO) mice (light bars) (n ϭ 5), reperfused wild-type (n ϭ 6) and TNF-␣ KO (n ϭ 5) mice. *p Ͻ 0.05. I/R ϭ ischemia/reperfusion. Electrocardiogram monitoring of arrhythmia. Electro- cardiogram recording started 10 min before occlusion and continued until the end of reperfusion (160 min total). Data were sampled at a rate of 10 kHz and analyzed using MacLab/8s (AD Instruments, Castle Hill, Australia). Hemodynamic study. A 1.4 French high-fidelity catheter tip micromanometer (SPR-671; Millar Instruments, Hous- ton, Texas) was inserted through the right carotid artery into the LV cavity to measure LV pressure. First derivative of LV pressure (dP/dt) was analyzed using MacLab/8s. Electrophoretic gel mobility shift assay. Nuclear extract was prepared from the entire LV of the reperfused heart according to the method described by Morishita et al. (7). Nuclear extract was incubated with 1 ϫ 105 cpm 32P- labeled oligonucleotide containing the NF-␬B consensus sequences (Promega Corp., Madison, Wisconsin). The protein content was measured, and 10 ␮g of protein was applied to each lane. RNA extraction, reverse transcription and polymerase chain reaction analysis. Total RNA was extracted from ischemic and nonischemic regions. Reverse transcription Figure 1. Arrhythmia observed during myocardial ischemia/reperfusion. (RT) and real-time quantitative polymerase chain reaction (A) Summarized data on the arrhythmia during reperfusion in wild-type (PCR) were performed using a Light Cycler (F. Hoffmann- (n ϭ 11) and tumor necrosis factor (TNF)-␣ knockout (KO) (n ϭ 9) mice. LaRoche Ltd., Basel, Switzerland). The expression levels of (B) Summarized data on the arrhythmia during reperfusion in wild-type ␣ mice receiving nonimmune IgG (n ϭ 5) and anti-TNF-␣ antibody (n ϭ TNF- , interleukin (IL)-6, intercellular adhesion molecule 5). **p Ͻ 0.01. (ICAM)-1, vascular cell adhesion molecule-1, macrophage JACC Vol. 39, No. 7, 2002 Maekawa et al. 1231 April 3, 2002:1229–35 Ischemia/Reperfusion in TNF-␣ Knockout Mice Figure 3. Infarct area (IA) and area at risk (AAR) of the left ventricle (LV) after 30-min ligation and 120-min reperfusion. Representative photographs of midventricular myocardium from wild-type mice (A), tumor necrosis factor (TNF)-␣ knockout (KO) mice (B), wild-type mice receiving nonimmune IgG (C) and wild-type mice receiving anti-TNF-␣ antibody (D). (E) Summarized data on infarct area to area at risk ratio (IA/AAR), IA to left ventricle ratio (IA/LV) and AAR to LV ratio (AAR/LV) in wild-type (n ϭ 11) and TNF-␣ KO (n ϭ 9) mice. (F) Summarized data on IA/AAR, IA/LV and AAR/LV in wild-type mice receiving nonimmune IgG (n ϭ 5) and anti-TNF-␣ antibody (n ϭ 5). **p Ͻ 0.01. inflammatory protein (MIP)-1-␣, MIP-2 and monocyte Scheffe’s post-hoc test. Stat View 5.0 was used for statistical chemoattractant protein (MCP)-1 were investigated. The analyses. Results were considered statistically significant at fluorescence intensity of each target gene was normalized p Ͻ 0.05. with that of ␤-actin amplified under identical conditions. Ϫ Histopathological study. The heart embedded in 20°C RESULTS cryostat compound (Miles Laboratory, Elkhart, Indiana) was snap frozen in 2-methylbutane prechilled with liquid Arrhythmia. The frequency of arrhythmia observed during nitrogen and cut into sections 5 ␮m thick. Sections were reperfusion was significantly less in TNF-␣ KO mice (1.2 Ϯ stained with May-Giemsa (Muto Pure Chemicals, Tokyo, 0.5 beats/2 h) than in WT mice (31.8 Ϯ 10.1 beats/2 h) Japan).
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