Electron paramagnetic resonance monitoring of ischemia-induced myocardial oxygen depletion and acidosis in isolated rat hearts using soluble paramagnetic probes

Magnetic Resonance in Medicine

Volumn 68, Issue 2, 2012, Pages 649-655

  Komarov, Denis A ^a   Dhimitruka, Ilirian ^a   Kirilyuk, Igor A ^b   Trofimiov, Dmitrii G ^c   Grigor'Ev, Igor A ^b   Zweier, Jay L ^a   Khramtsov, Valery V ^a  

^a OHIO STATE UNIVERSITY   (United States)

^b N N VOROZHTSOV NOVOSIBIRSK INSTITUTE OF ORGANIC CHEMISTRY   (Russian Federation)

^c NOVOSIBIRSK STATE UNIVERSITY   (Russian Federation)

Author keywords

electron paramagnetic resonance; electron paramagnetic resonance oximetry; myocardial acidosis; myocardial ischemia; pH sensitive nitroxide; triarylmethyl radical

Indexed keywords

ACIDIFICATION; ELECTRON RESONANCE; ELECTRONS; OXYGEN; PARAMAGNETISM; PH SENSORS; POTENTIOMETRIC SENSORS; PROBES; RATS; TISSUE; TISSUE ENGINEERING;

MYOCARDIAL ACIDOSIS; MYOCARDIAL ISCHEMIA; NITROXIDES; OXIMETRY; TRIARYLMETHYL RADICAL;

PARAMAGNETIC RESONANCE;

NITROXIDE;

ACIDITY; ACIDOSIS; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; CORONARY ARTERY BLOOD FLOW; ELECTRON SPIN RESONANCE; HEART MUSCLE ISCHEMIA; HEART MUSCLE REPERFUSION; ISOLATED HEART; MALE; MYOCARDIAL OXYGEN DEPLETION; NONHUMAN; OXYGEN CONCENTRATION; OXYGEN TENSION; PH; RADIODIAGNOSTIC EQUIPMENT AND SUPPLIES; RAT; REPERFUSION INJURY;

EID: 84863854231     PISSN: 07403194     EISSN: 15222594     Source Type: Journal    
DOI: 10.1002/mrm.23251     Document Type: Article

References (43)

1. Yellon DM, Hausenloy DJ,. Myocardial reperfusion injury. N Engl J Med 2007; 357: 1121-1135.
2. Kuppusamy P, Chzhan M, Vij K, Shteynbuk M, Lefer DJ, Giannella E, Zweier JL,. Three-dimensional spectral-spatial EPR imaging of free radicals in the heart: a technique for imaging tissue metabolism and oxygenation. Proc Natl Acad Sci USA 1994; 91: 3388-3392. (Pubitemid 24130242)
3. Regan TJ, Effros RM, Haider B, Oldewurtel HA, Ettinger PO, Ahmed SS,. Myocardial ischemia and cell acidosis: modification by alkali and the effects on ventricular function and cation composition. Am J Cardiol 1976; 37: 501-507.
4. Niwano S, Tojo T,. Systemic acidosis in acute myocardial ischemiaa-cause or result of life-threatening ventricular arrhythmia? Circ J 2010; 74: 1794-1795.
5. Mast F, Elzinga G,. Metabolic recovery of acidotic rabbit cardiac muscle: effects of low pH and oxygen shortage. Circ Res 1989; 65: 909-916. (Pubitemid 19242643)
6. Cohen MV, Yang XM, Downey JM,. The pH hypothesis of postconditioning: staccato reperfusion reintroduces oxygen and perpetuates myocardial acidosis. Circulation 2007; 115: 1895-1903. (Pubitemid 46598903)
7. Khramtsov VV, Zweier JL,. Functional in vivo EPR spectroscopy and imaging using nitroxide and trityl radicals. In:, Hicks R, editor. Stable radicals: fundamentals and applied aspects of odd-electron compounds. Chichester, UK: John Wiley & Sons, Ltd.; 2010. pp 537-566.
8. Zweier JL, Kuppusamy P,. Electron paramagnetic resonance measurements of free radicals in the intact beating heart: a technique for detection and characterization of free radicals in whole biological tissues. Proc Natl Acad Sci USA 1988; 85: 5703-5707.
9. Zweier JL, Chzhan M, Ewert U, Schneider G, Kuppusamy P,. Development of a highly sensitive probe for measuring oxygen in biological tissues. J Magn Reson B 1994; 105: 52-57.
10. Vahidi N, Clarkson RB, Liu KJ, Norby SW, Wu M, Swartz HM,. In vivo and in vitro EPR oximetry with fusinite: a new coal-derived, particulate EPR probe. Magn Reson Med 1994; 31: 139-146. (Pubitemid 24044084)
11. Liu KJ, Gast P, Moussavi M, Norby SW, Vahidi N, Walczak T, Wu M, Swartz HM,. Lithium phthalocyanine: a probe for electron paramagnetic resonance oximetry in viable biological systems. Proc Natl Acad Sci USA 1993; 90: 5438-5442. (Pubitemid 23176175)
12. Ilangovan G, Manivannan A, Li H, Yanagi H, Zweier JL, Kuppusamy P,. A naphthalocyanine-based EPR probe for localized measurements of tissue oxygenation. Free Radical Biol Med 2002; 32: 139-147. (Pubitemid 34127703)
13. Pandian RP, Dolgos M, Dang V, Sostaric JZ, Woodward PM, Kuppusamy P,. Structure and oxygen-sensing paramagnetic properties of a new lithium 1,8,15,22-tetraphenoxyphthalocyanine radical probe for biological oximetry. Chem Mater 2007; 19: 3545-3552. (Pubitemid 47160943)
14. Ardenkjaer-Larsen JH, Laursen I, Leunbach I, Ehnholm G, Wistrand LG, Petersson JS, Golman K,. EPR and DNP properties of certain novel single electron contrast agents intended for oximetric imaging. J Magn Reson 1998; 133: 1-12. (Pubitemid 128450605)
15. Elas M, Williams BB, Parasca A, Mailer C, Pelizzari CA, Lewis MA, River JN, Karczmar GS, Barth ED, Halpern HJ,. Quantitative tumor oxymetric images from 4D electron paramagnetic resonance imaging (EPRI): methodology and comparison with blood oxygen level-dependent (BOLD) MRI. Magn Reson Med 2003; 49: 682-691. (Pubitemid 36389978)
16. Krishna MC, English S, Yamada K, Yoo J, Murugesan R, Devasahayam N, Cook JA, Golman K, Ardenkjaer-Larsen JH, Subramanian S, Mitchell JB,. Overhauser enhanced magnetic resonance imaging for tumor oximetry: coregistration of tumor anatomy and tissue oxygen concentration. Proc Natl Acad Sci USA 2002; 99: 2216-2221. (Pubitemid 34169041)
17. Dhimitruka I, Grigorieva O, Zweier JL, Khramtsov VV,. Synthesis, structure and EPR characterization of deuterated derivatives of Finland trityl radical. Bioorg Med Chem Lett 2010; 20: 3946-3949.
18. Khramtsov VV, Weiner LM, Grigor'ev IA, Volodarsky LB,. Proton exchange in stable nitroxyl radicals. EPR studies of the pH of aqueous solutions. Chem Phys Lett 1982; 91: 69-72.
19. N with pH. J Am Chem Soc 1982; 104: 827-830.
20. Khramtsov VV,. Biological imaging and spectroscopy of pH. Curr Org Chem 2005; 9: 909-923. (Pubitemid 40753872)
21. Potapenko DI, Foster MA, Lurie DJ, Kirilyuk IA, Hutchison JM, Grigor'ev IA, Bagryanskaya EG, Khramtsov VV,. Real-time monitoring of drug-induced changes in the stomach acidity of living rats using improved pH-sensitive nitroxides and low-field EPR techniques. J Magn Reson 2006; 182: 1-11. (Pubitemid 44293435)
22. Woldman YY, Semenov SV, Bobko AA, Kirilyuk IA, Polienko JF, Voinov MA, Bagryanskaya EG, Khramtsov VV,. Design of liposome-based pH sensitive nanoSPIN probes: nano-sized particles with incorporated nitroxides. Analyst 2009; 134: 904-910.
23. Hui AK, Armstrong BH, Wray AA,. Rapid computation of Voigt and complex error functions. J Quant Spectrosc Radiat Transfer 1978; 19: 509-516.
24. Decroos C, Li Y, Bertho G, Frapart Y, Mansuy D, Boucher JL,. Oxidative and reductive metabolism of tris(p-carboxyltetrathiaaryl)methyl radicals by liver microsomes. Chem Res Toxicol 2009; 22: 1342-1350.
25. Baker JE, Froncisz W, Joseph J, Kalyanaraman B,. Spin label oximetry to assess extracellular oxygen during myocardial ischemia. Free Radical Biol Med 1997; 22: 109-115. (Pubitemid 26399316)
26. Friedman BJ, Grinberg OY, Isaacs KA, Walczak TM, Swartz HM,. Myocardial oxygen tension and relative capillary density in isolated perfused rat hearts. J Mol Cell Cardiol 1995; 27: 2551-2558. (Pubitemid 26003184)
27. Friedman BJ, Grinberg OY, Isaacs KA, Ruuge EK, Swartz HM,. Effect of repetitive ischemia on myocardial oxygen tension in isolated perfused and hypoperfused rat hearts. Magn Reson Med 1996; 35: 214-220. (Pubitemid 26044389)
28. Ilangovan G, Liebgott T, Kutala VK, Petryakov S, Zweier JL, Kuppusamy P,. EPR oximetry in the beating heart: myocardial oxygen consumption rate as an index of postischemic recovery. Magn Reson Med 2004; 51: 835-842. (Pubitemid 38420462)
29. Zhu X, Zuo L, Cardounel AJ, Zweier JL, He G,. Characterization of in vivo tissue redox status, oxygenation, and formation of reactive oxygen species in postischemic myocardium. Antioxid Redox Signal 2007; 9: 447-455. (Pubitemid 46331759)
30. Zhu X, Liu B, Zhou S, Chen YR, Deng Y, Zweier JL, He G,. Ischemic preconditioning prevents in vivo hyperoxygenation in postischemic myocardium with preservation of mitochondrial oxygen consumption. Am J Physiol Heart Circ Physiol 2007; 293: H1442-H1450. (Pubitemid 47367187)
31. Khan M, Mohan IK, Kutala VK, Kotha SR, Parinandi NL, Hamlin RL, Kuppusamy P,. Sulfaphenazole protects heart against ischemia-reperfusion injury and cardiac dysfunction by overexpression of iNOS, leading to enhancement of nitric oxide bioavailability and tissue oxygenation. Antioxid Redox Signal 2009; 11: 725-738.
32. Li Y, Cai M, Xu Y, Swartz HM, He G,. Late phase ischemic preconditioning preserves mitochondrial oxygen metabolism and attenuates post-ischemic myocardial tissue hyperoxygenation. Life Sci 2011; 88: 57-64.
33. Angelos MG, Kutala VK, Torres CA, He G, Stoner JD, Mohammad M, Kuppusamy P,. Hypoxic reperfusion of the ischemic heart and oxygen radical generation. Am J Physiol Heart Circ Physiol 2006; 290: H341-H347.
34. Zweier JL, Kuppusamy P, Williams R, Rayburn BK, Smith D, Weisfeldt ML, Flaherty JT,. Measurement and characterization of postischemic free radical generation in the isolated perfused heart. J Biol Chem 1989; 264: 18890-18895. (Pubitemid 19285787)
35. Becker LB,. New concepts in reactive oxygen species and cardiovascular reperfusion physiology. Cardiovasc Res 2004; 61: 461-470. (Pubitemid 38210152)
36. Kutala VK, Khan M, Angelos MG, Kuppusamy P,. Role of oxygen in postischemic myocardial injury. Antioxid Redox Signal 2007; 9: 1193-1206. (Pubitemid 47080829)
37. 31P NMR pH indicator in isolated organs. Direct NMR evidence of acidic compartments in the ischemic and reperfused rat liver. J Biol Chem 2001; 276: 1750-1758. (Pubitemid 32109646)
38. Kirilyuk IA, Bobko AA, Grigor'ev IA, Khramtsov VV,. Synthesis of the tetraethyl substituted pH-sensitive nitroxides of imidazole series with enhanced stability towards reduction. Org Biomol Chem 2004; 2: 1025-1030.
39. 31P NMR spectroscopic study of the isovolumic rat heart. NMR Biomed 1993; 6: 278-286.
40. Asimakis GK, Inners-McBride K, Medellin G, Conti VR,. Ischemic preconditioning attenuates acidosis and postischemic dysfunction in isolated rat heart. Am J Physiol 1992; 263 (3 Pt 2): H887-H894.
41. Lundmark JA, Trueblood N, Wang LF, Ramasamy R, Schaefer S,. Repetitive acidosis protects the ischemic heart: implications for mechanisms in preconditioned hearts. J Mol Cell Cardiol 1999; 31: 907-917. (Pubitemid 29201559)
42. Khramtsov VV, Caia GL, Shet K, Kesselring E, Petryakov S, Zweier JL, Samouilov A,. Variable field proton-electron double-resonance imaging: application to pH mapping of aqueous samples. J Magn Reson 2010; 202: 267-273.
43. Efimova OV, Sun Z, Petryakov S, Kesselring E, Caia GL, Johnson D, Zweier JL, Khramtsov VV, Samouilov A,. Variable radio frequency proton-electron double-resonance imaging: application to pH mapping of aqueous samples. J Magn Reson 2011; 209: 227-232.