Noninvasive assessment of the brain redox status after transient middle cerebral artery occlusion using Overhauser-enhanced magnetic resonance imaging

Journal of Cerebral Blood Flow and Metabolism

Volumn 29, Issue 10, 2009, Pages 1655-1664

  Yamato, Mayumi ^a,b   Shiba, Takeshi ^a,b   Yamada, Ken Ichi ^b   Watanabe, Toshiaki ^a   Utsumi, Hideo ^b  

^a KYUSHU UNIVERSITY   (Japan)

^b KYUSHU UNIVERSITY   (Japan)

Author keywords

Brain imaging; Ischemia?reperfusion; Nitroxyl radical; Overhauser enhanced MRI; Oxidative stress; Redox

Indexed keywords

3 METHOXYCARBONYL 2,2,5,5 TETRAMETHYLPYRROLIDINE OXYL; ASCORBIC ACID; CONTRAST MEDIUM; CYSTEINE; GLUTATHIONE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); UNCLASSIFIED DRUG;

ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; ENZYME ACTIVITY; HEMISPHERE; MALE; MIDDLE CEREBRAL ARTERY OCCLUSION; NON INVASIVE MEASUREMENT; NONHUMAN; NUCLEAR MAGNETIC RESONANCE IMAGING; NUCLEAR OVERHAUSER EFFECT; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT;

ANIMALS; ANTIOXIDANTS; ASCORBIC ACID; BRAIN; CONTRAST MEDIA; INFARCTION, MIDDLE CEREBRAL ARTERY; KINETICS; MAGNETIC RESONANCE IMAGING; MALE; MITOCHONDRIAL PROTEINS; OXIDATION-REDUCTION; RATS; RATS, WISTAR; REPERFUSION; TIME FACTORS;

EID: 70349690371     PISSN: 0271678X     EISSN: None     Source Type: Journal    
DOI: 10.1038/jcbfm.2009.84     Document Type: Article

References (40)

1. Agus DB, Gambhir SS, Pardridge WM, Spielholz C, Baselga J, Vera JC, Golde DW (1997) Vitamin C crosses the bloodbrain barrier in the oxidized form through the glucose transporters. J Clin Invest 100:2842-2848
2. Anzai K, Saito K, Takeshita K, Takahashi S, Miyazaki H, Shoji H, Lee MC, Masumizu T, Ozawa T (2003) Assessment of ESR-CT imaging by comparison with autoradiography for the distribution of a blood-brainbarrier permeable spin probe, MC-PROXYL, to rodent brain. Magn Reson Imaging 21:765-772
3. Bobko AA, Kirilyuk IA, Grigor'ev IA, Zweier JL, Khramtsov VV (2007) Reversible reduction of nitroxides to hydroxylamines: roles for ascorbate and glutathione. Free Radic Biol Med 42:404-412
4. Chen K, Morse PD, II, Swartz HM (1988) Kinetics of enzyme-mediated reduction of lipid soluble nitroxide spin labels by living cells. Biochim Biophys Acta 943:477-484
5. Chen YR, Chen CL, Pfeiffer DR, Zweier JL (2007) Mitochondrial complex II in the post-ischemic heart: oxidative injury and the role of protein S-glutathionylation. J Biol Chem 282:32640-32654
6. Cohen G (1994) Enzymatic/nonenzymatic sources of oxyradicals and regulation of antioxidant defenses. Ann NY Acad Sci 738:8-14
7. Hanes CS, Hird FJ, Isherwood FA (1952) Enzymic transpeptidation reactions involving gamma-glutamyl peptides and alpha-amino-acyl peptides. Biochem J 51:25-35
8. Huang J, Agus DB, Winfree CJ, Kiss S, Mack WJ, McTaggart RA, Choudhri TF, Kim LJ, Mocco J, Pinsky DJ, Fox WD, Israel RJ, Boyd TA, Golde DW, Connolly ES, Jr (2001) Dehydroascorbic acid, a blood-brain barrier transportable form of vitamin C, mediates potent cerebroprotection in experimental stroke. Proc Natl Acad Sci USA 98:11720-11724
9. Hyodo F, Chuang KH, Goloshevsky AG, Sulima A, Griffiths GL, Mitchell JB, Koretsky AP, Krishna MC (2008) Brain redox imaging using blood-brain barrier-permeable nitroxide MRI contrast agent. J Cereb Blood Flow Metab 28:1165-1174
10. Krishna MC, English S, Yamada K, Yoo J, Murugesan R, Devasahayam N, Cook JA, Golman K, Ardenkjaer-Larsen JH, Subramanian S, Mitchell JB (2002) Overhauser enhanced magnetic resonance imaging for tumor oximetry: coregistration of tumor anatomy and tissue oxygen concentration. Proc Natl Acad Sci USA 99:2216-2221
11. Krishna MC, Grahame DA, Samuni A, Mitchell JB, Russo A (1992) Oxoammonium cation intermediate in the nitroxide- catalyzed dismutation of superoxide. Proc Natl Acad Sci USA 89:5537-5541
12. Kudo W, Yamato M, Yamada K, Kinoshita Y, Shiba T, Watanabe T, Utsumi H (2008) Formation of TEMPOLhydroxylamine during reaction between TEMPOL and hydroxyl radical: HPLC/ECD study. Free Radic Res 42:505-512
13. Kuroda S, Katsura K, Hillered L, Bates TE, Siesjo BK (1996) Delayed treatment with alpha-phenyl-N-tert-butyl nitrone (PBN) attenuates secondary mitochondrial dysfunction after transient focal cerebral ischemia in the rat. Neurobiol Dis 3:149-157
14. Lee MC, Shoji H, Miyazaki H, Yoshino F, Hori N, Toyoda M, Ikeda Y, Anzai K, Ikota N, Ozawa T (2004) Assessment of oxidative stress in the spontaneously hypertensive rat brain using electron spin resonance (ESR) imaging and in vivo L-Band ESR. Hypertens Res 27:485-492
15. Lei B, Adachi N, Nagaro T, Arai T (1997) The effect of dopamine depletion on the H2O2 production in the rat striatum following transient middle cerebral artery occlusion. Brain Res 764:299-302
16. Li H, He G, Deng Y, Kuppusamy P, Zweier JL (2006) In vivo proton electron double resonance imaging of the distribution and clearance of nitroxide radicals in mice. Magn Reson Med 55:669-675
17. Liebgott T, Li H, Deng Y, Zweier JL (2003) Proton electron double resonance imaging (PEDRI) of the isolated beating rat heart. Magn Reson Med 50:391-399
18. Liu S, Liu M, Peterson S, Miyake M, Vallyathan V, Liu KJ (2003) Hydroxyl radical formation is greater in striatal core than in penumbra in a rat model of ischemic stroke. J Neurosci Res 71:882-888
19. Lurie DJ, Bussell DM, Bell LH, Mallard JR (1988) Protonelectron double magnetic resonance imaging of free radical solutions. J Magn Reson 76:366-370
20. Matsumoto K, Hyodo F, Matsumoto A, Koretsky AP, Sowers AL, Mitchell JB, Krishna MC (2006) Highresolution mapping of tumor redox status by magnetic resonance imaging using nitroxides as redox-sensitive contrast agents. Clin Cancer Res 12:2455-2462
21. Matsumoto S, Yamada K, Hirata H, Yasukawa K, Hyodo F, Ichikawa K, Utsumi H (2007) Advantageous application of a surface coil to EPR irradiation in overhauserenhanced MRI. Magn Reson Med 57:806-811
22. Mehlhorn RJ (1991) Ascorbate- and dehydroascorbic acidmediated reduction of free radicals in the human erythrocyte. J Biol Chem 266:2724-2731
23. Meister A (1994) Glutathione-ascorbic acid antioxidant system in animals. J Biol Chem 269:9397-9400
24. Meister A, Tate SS (1976) Glutathione and related gammaglutamyl compounds: biosynthesis and utilization. Annu Rev Biochem 45:559-604
25. Ohtaki H, Takeda T, Dohi K, Yofu S, Nakamachi T, Satoh K, Hiraizumi Y, Miyaoka H, Matsunaga M, Shioda S (2007) Increased mitochondrial DNA oxidative damage after transient middle cerebral artery occlusion in mice. Neurosci Res 58:349-355
26. Olney JW, Zorumski C, Price MT, Labruyere J (1990) Lcysteine, a bicarbonate-sensitive endogenous excitotoxin. Science 248:596-599
27. Piantadosi CA, Zhang J (1996) Mitochondrial generation of reactive oxygen species after brain ischemia in the rat. Stroke 27:327-31; discussion 332
28. Quintanilha AT, Packer L (1977) Surface localization of sites of reduction of nitroxide spin-labeled molecules in mitochondria. Proc Natl Acad Sci USA 74:570-574
29. Sano H, Matsumoto K, Utsumi H (1997) Synthesis and imaging of blood-brain-barrier permeable nitroxylprobes for free radical reactions in brain of living mice. Biochem Mol Biol Int 42:641-647
30. Sano H, Naruse M, Matsumoto K, Oi T, Utsumi H (2000) A new nitroxyl-probe with high retention in the brain and its application for brain imaging. Free Radic Biol Med 28:959-969
31. Sato-Akaba H, Fujii H, Hirata H (2008) Development and testing of a CW-EPR apparatus for imaging of shortlifetime nitroxyl radicals in mouse head. J Magn Reson 193:191-198
32. Shiba T, Yamato M, Kudou W, Ichikawa K, Yamada K, Watanabe T, Utsumi H (2008) Analysis of nitroxyl spin probes in mouse brain by X-band ESR with microdialysis technique. J Pharm Sci 97:4101-4107
33. Slivka A, Cohen G (1993) Brain ischemia markedly elevates levels of the neurotoxic amino acid, cysteine. Brain Res 608:33-37
34. Trounce IA, Kim YL, Jun AS, Wallace DC (1996) Assessment of mitochondrial oxidative phosphorylation in patient muscle biopsies, lymphoblasts, and transmitochondrial cell lines. Methods Enzymol 264:484-509
35. Utsumi H, Yamada K, Ichikawa K, Sakai K, Kinoshita Y, Matsumoto S, Nagai M (2006) Simultaneous molecular imaging of redox reactions monitored by Overhauserenhanced MRI with 14N- and 15N-labeled nitroxyl radicals. Proc Natl Acad Sci USA 103:1463-1468
36. Winkler BS, Orselli SM, Rex TS (1994) The redox couple between glutathione and ascorbic acid: a chemical and physiological perspective. Free Radic Biol Med 17:333-349
37. Xu L, Voloboueva LA, Ouyang Y, Emery JF, Giffard RG (2009) Overexpression of mitochondrial Hsp70/Hsp75 in rat brain protects mitochondria, reduces oxidative stress, and protects from focal ischemia. J Cereb Blood Flow Metab 29:365-374
38. Yamato M, Egashira T, Utsumi H (2003) Application of in vivo ESR spectroscopy to measurement of cerebrovascular ROS generation in stroke. Free Radic Biol Med 35:1619-1631
39. Yokoyama H, Lin Y, Itoh O, Ueda Y, Nakajima A, Ogata T, Sato T, Ohya-Nishiguchi H, Kamada H (1999) EPR imaging for in vivo analysis of the half-life of a nitroxide radical in the hippocampus and cerebral cortex of rats after epileptic seizures. Free Radic Biol Med 27:442-448
40. Zhang M, Liu K, Gong K, Su L, Chen Y, Mao L (2005) Continuous on-line monitoring of extracellular ascorbate depletion in the rat striatum induced by global ischemia with carbon nanotube-modified glassy carbon electrode integrated into a thin-layer radial flow cell. Anal Chem 77:6234-6242