206
Views
1
CrossRef citations to date
0
Altmetric
Review Articles

Free radical imaging of endogenous redox molecules using dynamic nuclear polarization magnetic resonance imaging

, , , , , , & show all
Pages 343-351 | Received 29 Oct 2020, Accepted 30 Nov 2020, Published online: 14 Dec 2020

References

  • Niki E. Free radicals in the 1900’s: from in vitro to in vivo. Free Radic Res. 2000;33(6):693–704.
  • Nolfi-Donegan D, Braganza A, Shiva S. Mitochondrial electron transport chain: oxidative phosphorylation, oxidant production, and methods of measurement. Redox Biol. 2020;104–105:36–43.
  • Sun L, Wang X, Saredy J, et al. Innate-adaptive immunity interplay and redox regulation in immune response. Redox Biol. 2020;37:101759.
  • Yan J, Jiang J, He L, et al. Mitochondrial superoxide/hydrogen peroxide: an emerging therapeutic target for metabolic diseases. Free Radic Biol Med. 2020;152:33–42.
  • Sumida Y, Niki E, Naito Y, et al. Involvement of free radicals and oxidative stress in NAFLD/NASH. Free Radic Res. 2013;47(11):869–880.
  • Panieri E, Santoro MM. ROS homeostasis and metabolism: a dangerous liason in cancer cells. Cell Death Dis. 2016;7(6):e2253.
  • Berkowitz BA, Lenning J, Khetarpal N, et al. In vivo imaging of prodromal hippocampus CA1 subfield oxidative stress in models of Alzheimer disease and Angelman syndrome. Faseb J. 2017;31(9):4179–4186.
  • Niki E. Lipid oxidation in the skin. Free Radic Res. 2015;49(7):827–834.
  • Yin H, Niki E, Uchida K. Special issue on “Recent progress in lipid peroxidation based on novel approaches”. Free Radic Res. 2015;49(7):813–815.
  • Takahashi W, Miyake Y, Hirata H. Artifact suppression in electron paramagnetic resonance imaging of (14)N- and (15)N-labeled nitroxyl radicals with asymmetric absorption spectra. J Magn Reson. 2014;247:31–37.
  • Miyake Y, Wang X, Amasaka M, et al. Simultaneous imaging of an enantiomer pair by electron paramagnetic resonance using isotopic nitrogen labeling. Anal Chem. 2013;85(2):985–990.
  • Gonet M, Epel B, Elas M. Data processing of 3D and 4D in-vivo electron paramagnetic resonance imaging co-registered with ultrasound. 3D printing as a registration tool. Comput Electr Eng. 2019;74:130–137.
  • Emoto MC, Sato-Akaba H, Matsuoka Y, et al. Non-invasive mapping of glutathione levels in mouse brains by in vivo electron paramagnetic resonance (EPR) imaging: applied to a kindling mouse model. Neurosci Lett. 2019;690:6–10.
  • Khramtsov VV. In vivo molecular electron paramagnetic resonance-based spectroscopy and imaging of tumor microenvironment and redox using functional paramagnetic probes. Antioxid Redox Signal. 2018;28(15):1365–1377.
  • Emoto M, Mito F, Yamasaki T, et al. A novel ascorbic acid-resistant nitroxide in fat emulsion is an efficient brain imaging probe for in vivo EPR imaging of mouse. Free Radic Res. 2011;45(11–12):1325–1332.
  • Matsumoto KI, Mitchell JB, Krishna MC. Comparative studies with EPR and MRI on the in vivo tissue redox status estimation using redox-sensitive nitroxyl probes: influence of the choice of the region of interest. Free Radic Res. 2018;52(2):248–255.
  • Uchida T, Togashi H, Kuroda Y, et al. In vivo analysis of redox status in organs – from bench to bedside. Free Radic Res. 2020:1–8.
  • Lazarova D, Shibata S, Ishii I, et al. Nitroxide-enhanced magnetic resonance imaging of kidney dysfunction in vivo based on redox-imbalance and oxidative stress. Gen Physiol Biophys. 2019;38(3):191–204.
  • Hyodo F, Chuang KH, Goloshevsky AG, et al. Brain redox imaging using blood-brain barrier-permeable nitroxide MRI contrast agent. J Cereb Blood Flow Metab. 2008;28(6):1165–1174.
  • Hyodo F, Matsumoto K, Matsumoto A, et al. Probing the intracellular redox status of tumors with magnetic resonance imaging and redox-sensitive contrast agents. Cancer Res. 2006;66(20):9921–9928.
  • Aoki I. Nano-theranostics and nitroxyl radical-labeled antitumor agents for magnetic resonance imaging. Yakugaku Zasshi. 2016;136(8):1087–1091.
  • Barros W, Jr., Engelsberg M. Enhanced Overhauser contrast in proton-electron double-resonance imaging of the formation of an alginate hydrogel. J Magn Reson. 2007;184(1):101–107.
  • Utsumi H, Yamada K, Ichikawa K, et al. Simultaneous molecular imaging of redox reactions monitored by Overhauser-enhanced MRI with 14N- and 15N-labeled nitroxyl radicals. Proc Natl Acad Sci USA. 2006;103(5):1463–1468.
  • Lurie DJ, Mader K. Monitoring drug delivery processes by EPR and related techniques-principles and applications. Adv Drug Deliv Rev. 2005;57(8):1171–1190.
  • Lurie DJ, Davies GR, Foster MA, et al. Field-cycled PEDRI imaging of free radicals with detection at 450 mT. Magn Reson Imaging. 2005;23(2):175–181.
  • Li H, Deng Y, He G, et al. Proton electron double resonance imaging of the in vivo distribution and clearance of a triaryl methyl radical in mice. Magn Reson Med. 2002;48(3):530–534.
  • Lurie DJ, Li H, Petryakov S, Zweier JL. Development of a PEDRI free-radical imager using a 0.38 T clinical MRI system. Magn Reson Med. 2002;47(1):181–186.
  • Foster MA, Seimenis I, Lurie DJ. The application of PEDRI to the study of free radicals in vivo. Phys Med Biol. 1998;43(7):1893–1897.
  • Kishimoto S, Krishna MC, Khramtsov VV, et al. In vivo application of proton-electron double-resonance imaging. Antioxid Redox Signal. 2018;28(15):1345–1364.
  • Ahn KH, Scott G, Stang P, et al. Multiparametric imaging of tumor oxygenation, redox status, and anatomical structure using Overhauser-enhanced MRI-prepolarized MRI system. Magn Reson Med. 2011;65(5):1416–1422.
  • Krishna MC, English S, Yamada K, et al. Overhauser enhanced magnetic resonance imaging for tumor oximetry: coregistration of tumor anatomy and tissue oxygen concentration. Proc Natl Acad Sci USA. 2002;99(4):2216–2221.
  • Eto H, Hyodo F, Kosem N, et al. Redox imaging of skeletal muscle using in vivo DNP-MRI and its application to an animal model of local inflammation. Free Radic Biol Med. 2015;89:1097–1104.
  • Eto H, Hyodo F, Nakano K, et al. Selective imaging of malignant ascites in a mouse model of peritoneal metastasis using in vivo dynamic nuclear polarization-magnetic resonance imaging. Anal Chem. 2016;88(4):2021–2027.
  • Eto H, Tsuji G, Chiba T, et al. Non-invasive evaluation of atopic dermatitis based on redox status using in vivo dynamic nuclear polarization magnetic resonance imaging. Free Radic Biol Med. 2017;103:209–215.
  • Kodama Y, Hyodo F, Yamato M, et al. Dynamic nuclear polarization magnetic resonance imaging and the oxygen-sensitive paramagnetic agent OX63 provide a noninvasive quantitative evaluation of kidney hypoxia in diabetic mice. Kidney Int. 2019;96(3):787–792.
  • Hyodo F, Ito S, Yasukawa K, et al. Simultaneous and spectroscopic redox molecular imaging of multiple free radical intermediates using dynamic nuclear polarization-magnetic resonance imaging. Anal Chem. 2014;86(15):7234–7238.
  • Swartz H, Bolton J, Brog D. Biological applications of electron spin resonance. 1972.
  • Bielski B, Gebicki JM. Atlas of electron spin resonance spectra. 1967.
  • Cadenas E, Davies KJ. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med. 2000;29(3–4):222–230.
  • Mailloux RJ. Teaching the fundamentals of electron transfer reactions in mitochondria and the production and detection of reactive oxygen species. Redox Biol. 2015;4:381–398.
  • Miki T, Yu L, Yu CA. Characterization of ubisemiquinone radicals in succinate-ubiquinone reductase. Arch Biochem Biophys. 1992;293(1):61–66.
  • Hyodo F, Ito S, Utsumi H. [Redox molecular imaging using ReMI]. Yakugaku Zasshi. 2015;135(5):725–731.
  • Mueller-Lisse UG, Scherr MK. Proton MR spectroscopy of the prostate. Eur J Radiol. 2007;63(3):351–360.
  • Tognarelli JM, Dawood M, Shariff MI, et al. Magnetic resonance spectroscopy: principles and techniques: lessons for clinicians. J Clin Exp Hepatol. 2015;5(4):320–328.
  • Fukuda T, Wengler K, de Carvalho R, et al. MRI biomarkers in osseous tumors. J Magn Reson Imaging. 2019;50(3):702–718.
  • Ding XQ, Lanfermann H. Whole brain ¹H-spectroscopy: a developing technique for advanced analysis of cerebral metabolism. Clin Neuroradiol. 2015;25(Suppl 2):245–250.
  • Njus D, Kelley PM, Tu YJ, et al. Ascorbic acid: the chemistry underlying its antioxidant properties. Free Radic Biol Med. 2020;159:37–43.
  • Keshari KR, Kurhanewicz J, Bok R, et al. Hyperpolarized 13C dehydroascorbate as an endogenous redox sensor for in vivo metabolic imaging. Proc Natl Acad Sci USA. 2011;108(46):18606–18611.
  • Bohndiek SE, Kettunen MI, Hu DE, et al. Hyperpolarized [1–13C]-ascorbic and dehydroascorbic acid: vitamin C as a probe for imaging redox status in vivo. J Am Chem Soc. 2011;133(30):11795–11801.
  • Buettner GR, Jurkiewicz BA. Ascorbate free radical as a marker of oxidative stress: an EPR study. Free Radic Biol Med. 1993;14(1):49–55.
  • Sharma MK, Buettner GR, Spencer KT, et al. Ascorbyl free radical as a real-time marker of free radical generation in briefly ischemic and reperfused hearts. An electron paramagnetic resonance study. Circ Res. 1994;74(4):650–658.
  • Ito S, Hyodo F. Dynamic nuclear polarization-magnetic resonance imaging at low ESR irradiation frequency for ascorbyl free radicals. Sci Rep. 2016;6:21407.
  • Verrax J, Delvaux M, Beghein N, et al. Buc Calderon P. Enhancement of quinone redox cycling by ascorbate induces a caspase-3 independent cell death in human leukaemia cells. An in vitro comparative study. Free Radic Res. 2005;39(6):649–657.
  • Puehringer S, Metlitzky M, Schwarzenbacher R. The pyrroloquinoline quinone biosynthesis pathway revisited: a structural approach. BMC Biochem. 2008;9:8.
  • He K, Nukada H, Urakami T, et al. Antioxidant and pro-oxidant properties of pyrroloquinoline quinone (PQQ): implications for its function in biological systems. Biochem Pharmacol. 2003;65(1):67–74.
  • Vanea E, Charlier N, Dewever J, et al. Molecular electron paramagnetic resonance imaging of melanin in melanomas: a proof-of-concept. NMR Biomed. 2008;21(3):296–300.
  • Nakagawa K, Minakawa S, Itabashi C, et al. Investigation of paraffin-embedded basal cell carcinoma using electron paramagnetic resonance. Anal Sci. 2019;35(3):265–269.
  • Zdybel M, Chodurek E, Pilawa B. EPR studies of free radicals in A-2058 human melanoma cells treated by valproic acid and 5,7-dimethoxycoumarin. Acta Pol Pharm. 2014;71(6):1066–1072.
  • Plonka PM. Electron paramagnetic resonance as a unique tool for skin and hair research. Exp Dermatol. 2009;18(5):472–484.
  • Collins B, Poehler TO, Bryden WA. EPR persistence measurements of UV-induced melanin free radicals in whole skin. Photochem Photobiol. 1995;62(3):557–560.
  • Hyodo F, Naganuma T, Eto H, et al. In vivo melanoma imaging based on dynamic nuclear polarization enhancement in melanin pigment of living mice using in vivo dynamic nuclear polarization magnetic resonance imaging. Free Radic Biol Med. 2019;134:99–105.

Reprints and Corporate Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

To request a reprint or corporate permissions for this article, please click on the relevant link below:

Academic Permissions

Please note: Selecting permissions does not provide access to the full text of the article, please see our help page How do I view content?

Obtain permissions instantly via Rightslink by clicking on the button below:

If you are unable to obtain permissions via Rightslink, please complete and submit this Permissions form. For more information, please visit our Permissions help page.