Oxidative stress evaluation of skeletal muscle in ischemia-reperfusion injury using enhanced magnetic resonance imaging.
Journal
Scientific reports
ISSN: 2045-2322
Titre abrégé: Sci Rep
Pays: England
ID NLM: 101563288
Informations de publication
Date de publication:
02 07 2020
02 07 2020
Historique:
received:
01
07
2019
accepted:
03
06
2020
entrez:
4
7
2020
pubmed:
4
7
2020
medline:
16
12
2020
Statut:
epublish
Résumé
Acute extremity arterial occlusion requires prompt revascularization. Delayed revascularization induces ischemia-reperfusion injury in the skeletal muscle. Organ injury-induced oxidative stress is widely reported, and oxidative stress is heavily involved in ischemia-reperfusion injury. This study aimed to evaluate oxidative stress in ischemia-reperfusion rat models using 3-carbamoyl PROXYL enhanced magnetic resonance imaging (3-CP enhanced MRI). Ischemia-reperfusion injury was induced through clamping the right femoral artery in rats, with a 4-h ischemia time in all experiments. 3-CP enhanced MRI was performed to evaluate oxidative stress, and the rats were divided into 3 reperfusion time groups: 0.5, 2, and 24 h. Signal intensity was evaluated using 3-CP enhanced MRI and compared in the ischemia-reperfusion and intact limbs in the same rat. Furthermore, the effect of edaravone (radical scavenger) was evaluated in the 4-h ischemia-24-h reperfusion injury rat model. The signal intensity of the ischemia-reperfusion limb was significantly stronger than that of the intact limb, suggesting that oxidative stress was induced in the ischemia-reperfusion muscle. Edaravone administration reduced the oxidative stress in the ischemia-reperfusion limb. The signal intensity of the ischemia-reperfusion limb was stronger than that of the intact limb, presumably reflecting the oxidative stress in the former. 3-CP MRI examination shows promise for effective assessment of oxidative stress and may facilitate early diagnosis of ischemia-reperfusion injury.
Identifiants
pubmed: 32616815
doi: 10.1038/s41598-020-67336-4
pii: 10.1038/s41598-020-67336-4
pmc: PMC7331576
doi:
Substances chimiques
Free Radical Scavengers
0
Edaravone
S798V6YJRP
Types de publication
Evaluation Study
Journal Article
Langues
eng
Sous-ensembles de citation
IM
Pagination
10863Références
Granger, D. N. & Kvietys, P. R. Reperfusion injury and reactive oxygen species: the evolution of a concept. Redox. Biol. 6, 524–551 (2015).
doi: 10.1016/j.redox.2015.08.020
pubmed: 26484802
pmcid: 4625011
Kalogeris, T., Baines, C. P., Krenz, M. & Korthuis, R. J. Ischemia/reperfusion. Compr. Physiol. 7, 113–170 (2016).
doi: 10.1002/cphy.c160006
pubmed: 28135002
pmcid: 5648017
Farber, A. & Eberhardt, R. T. The current state of critical limb ischemia: a systemic review. JAMA Surg. 151, 1070–1077 (2016).
doi: 10.1001/jamasurg.2016.2018
pubmed: 27551978
Hyodo, F. et al. Assessment of tissue redox status using metabolic responsive contrast agents and magnetic resonance imaging. J. Pharm. Pharmacol. 60, 1049–1060 (2008).
doi: 10.1211/jpp.60.8.0011
pubmed: 18644197
pmcid: 2752670
Uchida, T. et al. In vivo visualization of redox status by high-resolution whole body magnetic resonance imaging using niroxide radicals. J. Clin. Biochem. Nutr. 63, 192–196 (2018).
doi: 10.3164/jcbn.18-18
pubmed: 30487668
pmcid: 6252305
Zhelev, Z., Bakalova, R., Aoki, I., Lazarova, D. & Saga, T. Imaging of superoxide generation in the dopaminergic area of the brain in Parkinson’s disease, using mito-TEMPO. ACS. Chem. Neurosci. 4, 1439–1445 (2013).
doi: 10.1021/cn400159h
pubmed: 24024751
pmcid: 3837371
Kilkenny, C., Browne, W. J., Cuthill, I. C., Emerson, M. & Altman, D. G. Improving bioscience research reporting: the ARRIVE guidelines for reporting animal research. PLoS. Biol. 8, e1000412 (2010).
doi: 10.1371/journal.pbio.1000412
pubmed: 20613859
pmcid: 2893951
McCormack, M. C. et al. Development of reproducible histologic injury severity scores: skeletal muscle reperfusion injury. Surgery 143, 126–133 (2008).
doi: 10.1016/j.surg.2007.06.005
pubmed: 18154940
Zhelev, Z. et al. Nitroxyl radicals for labeling of conventional therapeutics and noninvasive magnetic resonance imaging of their permeability for blood-brain barrier: relationship between structure, blood clearance, and MRI signal dynamic in the brain. Mol. Pharm. 6, 504–512 (2009).
doi: 10.1021/mp800175k
pubmed: 19718801
Jittapiromsak, N. et al. Dynamic contrast-enhanced MRI of orbital and anterior visual pathway lesions. Magn. Reason. Imaging 51, 44–50 (2018).
doi: 10.1016/j.mri.2018.04.016
Lee, X. R. & Xiang, G. L. Effects of edaravone, the free radical scavenger, on outcomes in acute cerebral infarction patients treated with ultra-early thrombolysis of recombinant tissue plasminogen activator. Clin. Neurol. Neurosurg. 67, 157–161 (2018).
doi: 10.1016/j.clineuro.2018.02.026
Yamamura, M., Miyamoto, Y., Mitsuno, M., Tanaka, H. & Ryomoto, M. Edaravone injected at the start of reperfusion suppresses myonephropathic metabolic syndrome in rats. Int. J. Angiol. 23, 193–196 (2014).
doi: 10.1055/s-0034-1387825
pubmed: 25317032
pmcid: 4169098
McLeish, M. J. & Kenyon, G. L. Relating structure to mechanism in creatine kinase. Crit. Rev. Biochem. Mol. Biol. 40, 1–20 (2005).
doi: 10.1080/10409230590918577
pubmed: 15804623
Blaisdell, F. W. The pathophysiology of skeletal muscle ischemia and the reperfusion syndrome: a review. Cardiovasc. Surg. 10, 620–630 (2002).
doi: 10.1016/S0967-2109(02)00070-4
pubmed: 12453699
Steven, S., Daiber, A., Dopheide, J. F., Münzel, T. & Espinola-Klein, C. Peripheral artery disease, redox signaling, oxidative stress—basic and clinical aspects. Redox. Biol. 12, 787–797 (2017).
doi: 10.1016/j.redox.2017.04.017
pubmed: 28437655
pmcid: 5403804
Nakano, H. et al. Reactive oxygen species mediate crosstalk between NF-kappaB and JNK. Cell Death Differ. 13, 730–737 (2006).
doi: 10.1038/sj.cdd.4401830
pubmed: 16341124
Paradis, S. et al. Chronology of mitochondrial and cellular events during skeletal muscle ischemia-reperfusion. Am. J. Physiol Cell Physiol. 310, C968–C982 (2016).
doi: 10.1152/ajpcell.00356.2015
pubmed: 27076618
pmcid: 4935201
Togashi, H., Aoyama, M. & Oikawa, K. Imaging of reactive oxygen species generated in vivo. Magn. Reason. Med. 75, 1375–1379 (2016).
doi: 10.1002/mrm.25582
Takeshita, K., Chi, C., Hirata, H., Ono, M. & Ozawa, T. In vivo generation of free radicals in the skin of live mice under ultraviolet light, measured by L-band EPR spectroscopy. Free Radic. Biol. Med. 40, 876–885 (2006).
doi: 10.1016/j.freeradbiomed.2005.10.049
pubmed: 16520239
Zhang, H. 3-Carbamoyl-2,2,5,5-tetramethyl-1-pyrrolidinyl-N-oxyl. 2008 Apr 30. Molecular Imaging and Contrast Agent Database (MICAD). Bethesda (MD): National Center for Biotechnology Information (US); 2004–2013; https://www.ncbi.nlm.nih.gov/books/NBK23323/ . Accessed 9 June 2008
Matsumoto, K., Narazaki, M., Ikehira, H., Anzai, K. & Ikota, N. Comparisons of EPR imaging and T1-weighted MRI for efficient imaging of nitroxyl contrast agents. J. Magn. Reason. 187, 155–162 (2007).
doi: 10.1016/j.jmr.2007.03.013
Davis, R. M. et al. Magnetic resonance imaging of organic contrast agents in mice: capturing the whole-body redox landscape. Free Radic. Biol. Med. 50, 459–468 (2011).
doi: 10.1016/j.freeradbiomed.2010.11.028
pubmed: 21130158
Matsumoto, K. et al. High-resolution mapping of tumor redox status by magnetic resonance imaging using nitroxides as redox-sensitive contrast agents. Clin. Cancer Res. 12, 2455–2462 (2006).
doi: 10.1158/1078-0432.CCR-05-2747
pubmed: 16638852
Dick, F. et al. Basic control of reperfusion effectively protects against reperfusion injury in a realistic rodent model of acute limb ischemia. Circulation 118, 1920–1928 (2008).
doi: 10.1161/CIRCULATIONAHA.108.787754
pubmed: 18936330