The DOI matches its Crossref record; 57 of the 57 references it cites were found in a registry or an index.
Ischemic preconditioning alters real-time measure of O2 radicals in intact hearts with ischemia and reperfusion
Abstract
Reactive oxygen species (ROS) are believed to be involved in triggering cardiac ischemic preconditioning (IPC). Decreased formation of ROS on reperfusion after prolonged ischemia may in part underlie protection by IPC. In heart models, these contentions have been based either on the effect of ROS scavengers to abrogate IPC-induced preservation or on a measurement of oxidation products on reperfusion. Using spectrophotofluorometry at the left ventricular wall and the fluorescent probe dihydroethidium (DHE), we measured intracellular ROS superoxide (O[Formula: see text]·) continuously in isolated guinea pig heart and tested the effect of IPC and the O[Formula: see text]· scavenger manganese(III) tetrakis (4-benzoic acid) porphyrin chloride (MnTBAP) on O[Formula: see text]· formation throughout the phases of preconditioning (PC), 30-min ischemia and 60-min reperfusion (I/R). IPC was evidenced by improved contractile function and reduced infarction; MnTBAP abrogated these effects. Brief PC pulses increased O[Formula: see text]· during the ischemic but not the reperfusion phase. O[Formula: see text]· increased by 35% within 1 min of ischemia, increased further to 95% after 20 min of ischemia, and decreased slowly on reperfusion. In the IPC group, O[Formula: see text]· was not elevated over 35% during index ischemia and was not increased at all on reperfusion; these effects were abrogated by MnTBAP. Our results directly demonstrate how intracellular ROS increase in intact hearts during IPC and I/R and clarify the role of ROS in triggering and mediating IPC.
Overview
Integrity signals
Registry
Cites
Statistics
Verification
Claims the paper makes
Claims other papers make about this one
Each is checked against this paper’s own text: does it say what the citing paper says it does?
In the citing paper
“A small class of “uncoupling” proteins, called UCPs 1–4, are believed to induce an inward proton “leak” in charged mitochondria (49, 55, 176, 300).”
From Mitochondrial reactive oxygen species production in excitable cells: Modulators of mitochondrial and cell function (2009) · cites this paper as [176]
Citations
Cites
Preconditioning with ischemia: a delay of lethal cell injury in ischemic myocardium.
Murry, C. E., Jennings, R. B., & Reimer, K. A. (1986) · Circulation · doi:10.1161/01.cir.74.5.1124 · Cited by 7,813
LeBel, C. P., Ischiropoulos, H., & Bondy, S. C. (1992) · Chemical Research in Toxicology · doi:10.1021/tx00026a012 · Cited by 2,694
Vanden Hoek, T. L., Becker, L. B., Shao, Z., Li, C., & Schumacker, P. T. (1998) · Journal of Biological Chemistry · doi:10.1074/jbc.273.29.18092 · Cited by 721
Bolli, R., Patel, B. S., Jeroudi, M. O., Lai, E. K., & McCay, P. B. (1988) · Journal of Clinical Investigation · doi:10.1172/jci113621 · Cited by 685
Pain, T., Yang, X.-M., Critz, S. D., Yue, Y., Nakano, A., Liu, G. S., Heusch, G., Cohen, M. V., & Downey, J. M. (2000) · Circulation Research · doi:10.1161/01.res.87.6.460 · Cited by 662
Critical evaluation of the use of hydroethidine as a measure of superoxide anion radical
Benov, L., Sztejnberg, L., & Fridovich, I. (1998) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(98)00163-4 · Cited by 495
Baines, C. P., Goto, M., & Downey, J. M. (1997) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.1996.0265 · Cited by 484 · cited 6×
“Exogenous administration of H2O2 can induce a preconditioned state in cardiomyocytes (44) and intact hearts (43), and a similar effect can be achieved by endogenous ROS formation by the xanthine/xanthine oxidase reaction (4, 52) or by using the ETC inhibitor menadione (49).”
BackgroundMethodInfluentialMitochondrial PKCε and MAPK Form Signaling Modules in the Murine Heart
Baines, C. P., Zhang, J., Wang, G.-W., Zheng, Y.-T., Xiu, J. X., Cardwell, E. M., Bolli, R., & Ping, P. (2002) · Circulation Research · doi:10.1161/01.res.0000012702.90501.8d · Cited by 429
Generation of superoxide in cardiomyocytes during ischemia before reperfusion
Becker, L. B., Hoek, T. L. V., Shao, Z., Li, C., & Schumacker, P. T. (1999) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1999.277.6.h2240 · Cited by 413
Hoek, T. L. V., Li, C., Shao, Z., Schumacker, P. T., & Becker, L. B. (1997) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.1997.0497 · Cited by 398
ATP-Sensitive Potassium Channels: A Review of their Cardioprotective Pharmacology
Grover, G. J., & Garlid, K. (2000) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.2000.1111 · Cited by 396
Diazoxide-Induced Cardioprotection Requires Signaling Through a Redox-Sensitive Mechanism
Forbes, R. A., Steenbergen, C., & Murphy, E. (2001) · Circulation Research · doi:10.1161/hh0801.089342 · Cited by 395
The Optimal Efficiency and the Economic Degrees of Coupling of Oxidative Phosphorylation
Stucki, J. W. (1980) · European Journal of Biochemistry · doi:10.1111/j.1432-1033.1980.tb04792.x · Cited by 394
Preconditioning in Cardiomyocytes Protects by Attenuating Oxidant Stress at Reperfusion
Hoek, T. L. V., Becker, L. B., Shao, Z., Li, C., & Schumacker, P. T. (2000) · Circulation Research · doi:10.1161/01.res.86.5.541 · Cited by 312
Oxygen-derived free radicals and myocardial reperfusion injury: An overview
Bolli, R. (1991) · Cardiovascular Drugs and Therapy · doi:10.1007/bf00054747 · Cited by 295
Role of DNA Repair Inhibition in Lead- and Cadmium-Induced Genotoxicity: A Review
Hartwig, A. (1994) · Environmental Health Perspectives · doi:10.1289/ehp.94102s345 · Cited by 287
Day, B. J., Fridovich, I., & Crapo, J. D. (1997) · Archives of Biochemistry and Biophysics · doi:10.1006/abbi.1997.0341 · Cited by 285
Flaherty, J. T., Pitt, B., Gruber, J. W., Heuser, R. R., ROTHBAUM, D. A., Burwell, L. R., George, B. S., Kereiakes, D. J., Deitchman, D., & Gustafson, N. (1994) · Circulation · doi:10.1161/01.cir.89.5.1982 · Cited by 255
Granulocytes cause reperfusion ventricular dysfunction after 15-minute ischemia in the dog.
Engler, R. L., & Covell, J. W. (1987) · Circulation Research · doi:10.1161/01.res.61.1.20 · Cited by 227
Zhou, X., Zhai, X., & Ashraf, M. (1996) · Circulation · doi:10.1161/01.cir.93.6.1177 · Cited by 184
Mitochondrial Generation of Oxygen Radicals During Reoxygenation of Ischemic Tissues
Turrens, J. F., Beconi, M., Barilla, J., Chavez, U. B., & McCord, J. M. (1991) · Free Radical Research Communications · doi:10.3109/10715769109145847 · Cited by 177
Chen, W., Gabel, S. A., Steenbergen, C., & Murphy, E. (1995) · Circulation Research · doi:10.1161/01.res.77.2.424 · Cited by 165
Reactive oxygen species function as second messenger during ischemic preconditioning of heart
Das, D. K., Maulik, N., Sato, M., & Ray, P. S. (1999) · Molecular and Cellular Biochemistry · doi:10.1023/a:1006966128795 · Cited by 164
Nakano, A., Cohen, M. V., & Downey, J. M. (2000) · Pharmacology & Therapeutics · doi:10.1016/s0163-7258(00)00058-9 · Cited by 163
Vanden Hoek, T. L., Shao, Z., Li, C., Schumacker, P. T., & Becker, L. B. (1997) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.1997.0481 · Cited by 161 · cited 1×
“In one study, the mKATP channel opener nicorandil enhanced postischemic supply of high-energy phosphates and decreased oxidant injury (35); both factors are consistent with improved ETC function and with evidence that the mitochondrion is the most likely source of ROS during ischemia (44, 47).”
BackgroundTanaka, M., Fujiwara, H., Yamasaki, K., & Sasayama, S. (1994) · Cardiovascular Research · doi:10.1093/cvr/28.7.980 · Cited by 143
WeinaChen, ScottGabel, CharlesSteenbergen, & ElizabethMurphy (1995) · Circulation Research · Cited by 142
Nakagawa, Y., Ito, H., Kitakaze, M., Kusuoka, H., Hori, M., Kuzuya, T., Higashino, Y., Fujii, K., & Minamino, T. (1995) · Journal of the American College of Cardiology · doi:10.1016/0735-1097(94)00542-x · Cited by 139
Sun, J. Z., Kaur, H., Halliwell, B. B., Li, X. Y., & Bolli, R. (1993) · Circulation Research · doi:10.1161/01.res.73.3.534 · Cited by 126
IWAMOTO, T., Miura, T., Adachi, T., Noto, T., Ogawa, T., Tsuchida, A., & Iimura, O. (1991) · Circulation · doi:10.1161/01.cir.83.3.1015 · Cited by 111
Novalija, E., Varadarajan, S. G., Camara, A. K. S., An, J., Chen, Q., Riess, M. L., Hogg, N., & Stowe, D. F. (2002) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01056.2001 · Cited by 105
Self-citationAn, J., Varadarajan, S. G., Camara, A. K. S., Chen, Q., Novalija, E., Gross, G. J., & Stowe, D. F. (2001) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2001.281.6.h2398 · Cited by 94
Self-citationRiess, M. L., Camara, A. K. S., Chen, Q., Novalija, E., Rhodes, S. S., & Stowe, D. F. (2002) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.01057.2001 · Cited by 93
Self-citationTósaki, Á., Cordis, G. A., Szerdahelyi, P., Engelman, R. M., & Das, D. K. (1994) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-199403000-00002 · Cited by 89
Varadarajan, S. G., An, J., Novalija, E., Smart, S. C., & Stowe, D. F. (2001) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2001.280.1.h280 · Cited by 88
Self-citationOpenings of cardiac KATP channel by oxygen free radicals produced by xanthine oxidase reaction
Tokube, K., Kiyosue, T., & Arita, M. (1996) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1996.271.2.h478 · Cited by 83
An, J., Varadarajan, S. G., Novalija, E., & Stowe, D. F. (2001) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2001.281.4.h1508 · Cited by 77
Self-citationRiess, M. L., Camara, A. K. S., Novalija, E., Chen, Q., Rhodes, S. S., & Stowe, D. F. (2002) · Anesthesia & Analgesia · doi:10.1097/00000539-200212000-00013 · Cited by 76
Self-citationPreconditioning cultured human pediatric myocytes requires adenosine and protein kinase C
Ikonomidis, J. S., Shirai, T., Weisel, R. D., Derylo, B., Rao, V., Whiteside, C. I., Mickle, D. A. G., & Li, R. (1997) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1997.272.3.h1220 · Cited by 74
Tósaki, Á., Cordis, G. A., Szerdahelyi, P., et al. (1994) · Journal of Cardiovascular Pharmacology · doi:10.1097/00005344-199423030-00002 · Cited by 73
Evidence for the involvement of peroxynitrite in ischaemic preconditioning in rat isolated hearts
Altuǧ, S., Demiryürek, A. T., Kane, K. A., & Kanzık, İ. (2000) · British Journal of Pharmacology · doi:10.1038/sj.bjp.0703280 · Cited by 72
Zhang, H., McPherson, B. C., Liu, H., Baman, T. S., Rock, P., & Yao, Z. (2002) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.00683.2001 · Cited by 66
Bogoyevitch, M. A., Ng, D. C. H., Court, N. W., Draper, K. A., Dhillon, A. S., & Abas, L. (2000) · Journal of Molecular and Cellular Cardiology · doi:10.1006/jmcc.2000.1187 · Cited by 62
Park, J.-W., Chun, Y.-S., Kim, Y., Kim, C., & Kim, M. (1997) · Life Sciences · doi:10.1016/s0024-3205(97)00236-1 · Cited by 55
Inhibition of DNA-ethidium bromide intercalation due to free radical attack upon DNA
Pr�tz, W. A. (1984) · Radiation and Environmental Biophysics · doi:10.1007/bf01326731 · Cited by 54
Inhibition of DNA-ethidium bromide intercalation due to free radical attack upon DNA
Pr�tz, W. A. (1984) · Radiation and Environmental Biophysics · doi:10.1007/bf01326732 · Cited by 49
Stowe, D. F., Varadarajan, S. G., An, J., & Smart, S. C. (2000) · Circulation · doi:10.1161/01.cir.102.10.1172 · Cited by 45
Self-citationIschaemic preconditioning is not mediated by oxygen derived free radicals in rats
Richard, V. J., Tron, C., & Thuillez, C. (1993) · Cardiovascular Research · doi:10.1093/cvr/27.11.2016 · Cited by 44
Hydroxyl radical production during myocardial ischemia and reperfusion in cats
O’Neill, C., Fu, L., Halliwell, B. B., & Longhurst, J. C. (1996) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.1996.271.2.h660 · Cited by 42
Osada, M., Sato, T., Komori, S., & Tamura, K. (1991) · Cardiovascular Research · doi:10.1093/cvr/25.6.441 · Cited by 41
Menadione mimics the infarct-limiting effect of preconditioning in isolated rat hearts
Yue, Y., Krenz, M., Cohen, M. V., Downey, J. M., & Critz, S. D. (2001) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2001.281.2.h590 · Cited by 41
Preconditioning with hydrogen peroxide (H2O2) or ischemia in H2O2-induced cardiac dysfunction
Valen, G., Starkopf, J., Takeshima, S., Kullisaar, T., Vihalemm, T., Kengsepp, A., Löwbeer, C., Vaage, J., & Zilmer, M. (1998) · Free Radical Research · doi:10.1080/10715769800300271 · Cited by 39
Ischemic Preconditioning Decreases Oxidative Stress during Reperfusion: A Chemiluminescence Study
Crestanello, J. A., Lingle, D. M., Kamelgard, J. I., Millili, J. J., & Whitman, G. J. R. (1996) · Journal of Surgical Research · doi:10.1006/jsre.1996.0342 · Cited by 37
Horobin, R. W., & Rashid‐Doubell, F. (1990) · Histochemistry and Cell Biology · doi:10.1007/bf02440189 · Cited by 36
Nicorandil decreases postischemic actin oxidation
Schwalb, H., Olivson, A., Li, J., Houminer, E., Wahezi, S. E., Opie, L. H., Maulik, D., Borman, J. B., & Powell, S. R. (2001) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(01)00620-7 · Cited by 19
In vivo EPR spectroscopy of free radicals in the heart.
Zweier, J. L., & Kuppusamy, P. (1994) · Environmental Health Perspectives · doi:10.1289/ehp.94102s1045 · Cited by 17
Flumazenil preconditions cardiomyocytes via oxygen radicals and KATPchannels
Zhang, Q., & Yao, Z. (2000) · American Journal of Physiology-Heart and Circulatory Physiology · doi:10.1152/ajpheart.2000.279.4.h1858 · Cited by 14
Cited by
Sorted by citations
Mechanisms Underlying Acute Protection From Cardiac Ischemia-Reperfusion Injury
Murphy, E., & Steenbergen, C. (2008) · Physiological Reviews · doi:10.1152/physrev.00024.2007 · Cited by 1,504
ROS and redox signaling in myocardial ischemia-reperfusion injury and cardioprotection
Cadenas, S. (2018) · Free Radical Biology and Medicine · doi:10.1016/j.freeradbiomed.2018.01.024 · Cited by 832
Zhao, H., Kalivendi, S., Zhang, H., Joseph, J., Nithipatikom, K., Vásquez-Vivar, J., & Kalyanaraman, B. (2003) · Free Radical Biology and Medicine · doi:10.1016/s0891-5849(03)00142-4 · Cited by 803
New concepts in reactive oxygen species and cardiovascular reperfusion physiology
Becker, L. C. (2003) · Cardiovascular Research · doi:10.1016/j.cardiores.2003.10.025 · Cited by 703
Involvement of neutrophils in the pathogenesis of lethal myocardial reperfusion injury
Vinten-Johansen, J. (2003) · Cardiovascular Research · doi:10.1016/j.cardiores.2003.10.011 · Cited by 695
Metadata
- Authors
- Kevin, L. G., Camara, A. K. S., Riess, M. L., Novalija, E., & Stowe, D. F.
- Affiliations
- Anesthesiology Research Laboratories, Departments ofAnesthesiology and
- Medical College of Wisconsin (US)
- Venue
- American Journal of Physiology-Heart and Circulatory Physiology
- Publisher
- American Physiological Society
- Published
- 2003-02-01
- Volume
- 284
- Issue
- 2
- Pages
- H566-H574
- ISSN
- 0363-6135 (ISSN-L)
- 1522-1539
- OpenAlex
- W2079438155
- Cited by
- 272
- References
- 56
- Citations by year
- 2026: 1 · 2025: 7 · 2024: 4 · 2023: 1 · 2022: 3 · 2021: 4 · 2020: 4 · 2019: 9 · 2018: 9 · 2017: 15 · 2016: 7 · 2015: 15 · 2014: 15 · 2013: 9 · 2012: 12
- FWCI
- 11.37
- Type
- journal article
- Language
- en
- Open access
- closed
- Locations
- American Journal of Physiology-Heart and Circulatory Physiology (publishedVersion)
- PubMed (publishedVersion)
- Funders
- National Heart, Lung, and Blood Institute (HL 58691, R01HL058691)
- National Institute of General Medical Sciences (GM-8204-06)
- Topics
- Health Sciences › Medicine › Cardiology and Cardiovascular Medicine › Cardiac Ischemia and Reperfusion
- Health Sciences › Medicine › Physiology (medical) › Nitric Oxide and Endothelin Effects
- Health Sciences › Medicine › Surgery › Organ Transplantation Techniques and Outcomes
- Keywords
- ischemic preconditioning, reactive oxygen species, superoxide, myocardial ischemia-reperfusion injury, MnTBAP, dihydroethidium, cardioprotection, myocardial infarction, guinea pig heart
- MeSH terms
- Animals, Computer Systems, Ethidium, Guinea Pigs, Myocardial Infarction, Myocardium, Spectrometry, Fluorescence, Myocardial Reperfusion Injury, Myocardial Ischemia, Reactive Oxygen Species, Ischemic Preconditioning, Myocardial, In Vitro Techniques
About these checks
Registry, retraction, Cites and statistics results are computed, not judged, with one exception: a printed reference that no index lists is read once by a model before it counts as a citation error. Claims are extracted by a model and kept only when their quote appears verbatim in the text; each cited source is then checked, with a model’s help, for whether it says what the claim relies on. Those verdicts can be wrong — read the claim’s quote and the cited source before relying on one.
Statistics and arithmetic are recomputed, not judged.
Confidence bands are shown only for fields calibrated on our annotated test set. None is calibrated yet, so no band is shown.
What counts as a claim ›How we measure confidence ›How we check this ›
Are you an author, or do you see a problem with this page? Request a review