Yuanlin Cao, Yongsheng Chen, Qian Wan, Jungai Hu, Baolu Zhao. Three-dimensional electron spin resonance imaging of endogenous nitric oxide radicals generated in living plants. Biophysics Reports, 2018, 4(3): 133-142. doi: 10.1007/s41048-018-0051-5
Citation: Yuanlin Cao, Yongsheng Chen, Qian Wan, Jungai Hu, Baolu Zhao. Three-dimensional electron spin resonance imaging of endogenous nitric oxide radicals generated in living plants. Biophysics Reports, 2018, 4(3): 133-142. doi: 10.1007/s41048-018-0051-5

Three-dimensional electron spin resonance imaging of endogenous nitric oxide radicals generated in living plants

doi: 10.1007/s41048-018-0051-5
More Information
  • Corresponding author: Yuanlin Cao, Baolu Zhao
  • Received Date: 28 March 2017
  • Rev Recd Date: 15 May 2017
  • Publish Date: 30 June 2018
  • Electron spin resonance imaging (ESRI) has been developed to detect the spatial contribution of free radicals in recent years, but all of these studies are used in animal systems and almost of them using exogenous spin probes and only a few to study the endogenous free radicals in vivo. However, there is no report about the endogenous free radical three-dimensional (3D) EPRI in plant because of low concentration of endogenous free radicals and low resolution of the L-band ESRI. Recently, we have developed the imaging resolution better than 200 lm which is higher 10 times than L-band (about 1-3 mm) and the sensitivity is higher about 1000 times than that of L-band ESRI. Using this system and spin trapping technique, we studied spatial contribution of the endogenous nitric oxide (NO) radical generation in wheat leaves and got a clear 3D ESRI picture and CT (computed tomography) of NO of a wheat leaf. This imaging picture shows a clear spatial distribution of NO free radicals in the leaf. This is the first 3D ESRI of endogenous NO free radical generated in plant in the world. We have also studied the distributions of NO generation in different plants from different species with different shapes and it is shown that this is a convenient method to study the endogenous free radicals in plants.
  • loading
  • Ahern GP, Hsu SF, Klyachko VA, Jackson MB (2000) Induction of persistent sodium current by exogenous and endogenous nitric oxide. J Biol Chem 275:28810
    Berliner LJ, Fujii H (1985) Magnetic resonance imaging of biological specimens by electron paramagnetic resonance of nitroxide spin labels. Science 227:517
    Berliner LJ, Fujii H, Wang X, Lukiewicz SJ (1987) Feasibility study of imaging a living murine tumor by electron paramagnetic resonance. Magn Reson Med 4:380-384
    Blute TA, Lee MR, Eldred WD (2000) Direct imaging of NMDAstimulated nitric oxide production in the retina. Vis Neurosci 17:557
    Cao Y, Guo P, Zhao B-L (2005) Simultaneous detection of NO and ROS by ESR in biological system. Method Enzymol 396:77-83
    Chandok MR, Ekengren SK, Martin GB, Klessig DF (2004) Suppression of pathogen-inducible NO synthase (iNOS) activity in tomato increases susceptibility to Pseudomonas syringae. Proc Natl Acad Sci USA 101:8239-8244
    Dangl J (1998) Plants just say NO to pathogens. Nature 394:525-526
    Delledonne M, Xia YJ, Dixon RA, Lamb C (1998) Nitric oxide function as a signal in plant disease resistance. Nature 394:585-588
    Durner J, Wendohenne D, Klessing DF (1998) Defense gene induction in tobacco by nitric oxide, cyclic ADP-ribose. Proc Natl Acad Sci USA 95:10328-10333
    Feng Y, Wang HY, Zhao BL, Lu ZB (2016) Protective effect of a new formula based on nitric oxide and natural antioxidants on myocardium. J Univ Chin Acad Sci 33:625-631
    Ferrer MA, Ros Bareclo A (1999) Differential effects of nitric oxide on peroxidase and H2O2 production by the xylem of Zinnia elegans. Plant Cell Environ 22:891-897
    Fu G, Liu W, Li Y, Jin Y, Jiang L, Liang X, Feng S, Dai Z (2014) Magnetic prussian blue nanoparticles for targeted photothermal therapy under magnetic resonance imaging guidance. Bioconjugate Chem 25:1655-1663
    Gao M, Zhang J, Zhao BL (2016) Protective effect of nitric oxide and natural antioxidants on stability of blood. Hans journal of food and nutrition. Science 5(1):1-11
    Gorbunov NV, Pogue-Geile KL, Epperly MW, Bigbee WL, Draviam R, Day BW, Wald N, Watkins SC, Greenberger JS (2000) Activation of the nitric oxide synthase 2 pathway in the response of bone marrow stromal cells to high doses of ionizing radiation. Radiat Res 154:73-86
    Gouvea CMCP, Souza JF, Magalhacs ACN, Martins IS (1997) NOreleasing substance that induce growth elongation in maize root segments. Plant Growth Regul 21:183-187
    Guo P, Cao Y-L, Li Z-Q, Zhao B-L (2004) Role of an endogenous nitric oxide burst in the resistance of wheat to stripe rust. Plant Cell Environ 27(4):473-477
    Guo SH, Bezard E, Zhao B-L (2005) Protective effect of green tea polyphenols on the SH-SY5Y cells against 6-OHDA induced apoptosis through ROS-NO pathway. Free Radic Biol Med 39:682-695
    Hiramatsu M, Oikawa K, Noda H, Mori A, Ogata T, Kamada H (1995) Free radical imaging by electron spin resonance computed tomography in rat brain. Brain Res 697:44-47
    Hou H, Khan N, O'Hara JA, Grinberg OY, Dunn JF, Abajian MA, Wilmot CM, Demidenko E, Lu S, Steffen RP, Swartz HM (2005) Increased oxygenation of intracranial tumors by efaproxyn (efaproxiral), an allosteric hemoglobin modifier:in vivo EPR oximetry study. Int J Radiat Oncol Biol Phys 61:1503-1509
    Itoh Y, Ma FH, Hoshi H, Oka M, Noda K, Ukai Y, Kojima H, Nagano T, Toda N (2000) Determination and bioimaging method for nitric oxide in biological specimens by diaminofluorescein fluorometry. Anal Biochem 287:203-209
    Kobayashi H, Watanabe R, Choyke P (2014) Improving conventional enhanced permeability and retention (EPR) effects; what is the appropriate target? Theranostics 4(1):81-89
    Kojima H, Hashimoto H, Yoda K (2014) Interaction among the Subunits of Golgi membrane Mannosyltransferase complexes of the yeast. Biosci Biotechnol Biochem 63(11):1970-1976
    Kojima H, Nakatsubo N, Kikuchi K, Urano Y, Higuchi T, Tanaka J, Kudo Y, Nagano T (1998a) Direct evidence of NO production in rat hippocampus and cortex using a new fluorescent indicator:DAF-2 DA. NeuroReport 9:3345
    Kojima H, Nakatsubo N, Kikuchi K, Kawahara S, Kirino Y, Nagoshi H, Hirata Y, Nagano T (1998b) Detection and imaging of nitric oxide with novel fluorescent indicators:diaminofluoresceins. Anal Chem 70:2446
    Kuppusamy P, Chzhan M, Vij K, Shteynbuk M, Lefer DJ, Giannella E, Zweier JL (1994) 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 91:3388-3392
    Kuppusamy P, Wang P, Zweier JL (1995a) Three-dimensional spatial EPR imaging of the rat heart. Magn Reson Med 34:99-105
    Kuppusamy P, Chzhan M, Zweier JL (1995b) Developement and optimization of three-dimensional spatial EPR imaging for biological organs and tissues. J Magn Reson 106:122-130
    Kuppusamy P, Ohnishi ST, Numagami Y, Ohnishi T, Zweier JL (1996) Res Chem Intermed 22:605
    Lancaster JR Jr (1994) Simulation of the diffusion and reaction of endogenously produced nitric oxide. Proc Natl Acad Sci USA 91:8137-8141
    Laxalt A, Beligni MV, Lamattina L (1997) Nitric oxide preserves the level of chlorophyll in potato leaves infected by Phytophthora infestans. Eur J Plant Pathol 73:643-651
    Leshem YY, Haramaty E (1996) The charaterization and contrasting effects of the nitricoxide free radical in vegetative stress and senescence of Pisum sativum Linn. foliage. J Plant Physiol 148:258-263
    Leshem YY, Pinchasov Y (2000) Non-invasive photoacoustic spectroscopic determination of relative endogenous nitric oxide and ethylene content stoichiometry during the ripening of strawberries Fragaria anannasa (duch) and avocados Persea amaricana (Mill). J Exp Bot 51:1471-1473
    Leshem YY, Wills RBH, Ku VVV (1998) Evidence for the function of free radical gas-nitric oxide (NO.) as an endogenous maturation and senescence regulation factor in higher plants. Plant Phys Biochem 36:825-833
    Li H-T, Hu J-G, Xin W-J, Zhao B-L (2000) Production and interaction of oxygen and nitric oxide free radicals in PMA stimulated macrophages during the respiratory. Redox Rep 5:353-358
    Lin W, Liu J, Jeffries C, Yang L, Lu Y, Lee RE, Chen T (2014) Development of BODIPY FL vindoline as a novel and highaffinity pregnane X receptor fluorescent probe. Bioconjugate Chem 25(9):1664-1677
    Lopez-Figueroa MO, Day HEW, River C, Akil H, Watson SJ (2000a) Temporal and anatomical distribution of nitric oxide synthase mRNA expression and nitric oxide production during central nervous system inflammation. Brain Res 852:239-246
    Lopez-Figueroa MO, Caamano C, Morano MI, Ronn LC, Akil H, Watson SJ (2000b) Direct evidence of nitric oxide presence within mitochondria. Biochem Biophys Res Commun 272:129
    Maeda H (2012) Macromolecular therapeutics in cancer treatment:the EPR effect and beyond. J Control Release 164:138-144
    Maeda H (2013) The link between infection and cancer:tumor vasculature, free radicals, and drug delivery to tumors via the EPR effect. Cancer Sci 104:779-789
    Matsumoto K, Hyodo F, Matsumoto A, Koretsky AP, Sowers AL, Mitchell JB, Krishna MC (2006) High-resolution mapping of tumor redox status by magnetic resonance imaging using nitroxides as redox-sensitive contrast agents. Clin Cancer Res 12:2455-2462
    Mikuni T, He G, Petryakov S, Fallouh MM, Deng Y, Ishihara R, Kuppusamy P, Tatsuta M, Zweier JL (2004) In vivo detection of gastric cancer in rats by electron paramagnetic resonance imaging. Cancer Res 64:6495-6502
    Millar AH, Day DA (1997) Alternative solution to radical problems. Trend Plant Sci 2:289-290
    Morosan DE, Gallagher PT, Zucca P, O'Flannagain A, Fallows R, Reid H, Magdalenic J, Mann G, Bisi MM, Kerdraon A, Konovalenko AA, MacKinnon AL, Rucker HO, Thide B, Vocks C, Alexov A, Anderson J, Asgekar A, Avruch IM, Bentum MJ, Bernardi G, Bonafede A, Breitling F, Broderick JW, Brouw WN, Butcher HR, Ciardi B, de Geus E, Eisloffel J, Falcke H, Frieswijk W, Garrett MA, Griessmeier J, Gunst AW, Hessels JWT, Hoeft M, Karastergiou A, Kondratiev VI, Kuper G, van Leeuwen J, McKay-Bukowski D, McKean JP, Munk H, Orru E, Paas H, Pizzo R, Polatidis AG, Scaife AMM, Sluman J, Tasse C, Toribio MC, Vermeulen R, Zarka P (2015) LOFAR tied-array imaging and spectroscopy of solar S bursts. Astron. Astrophys 580:A65
    Nagano T, Yoshimura T (2002) Bioimaging of nitric oxide. Chem Rev 102:1235-1269
    Neill SJ, Desikan R, Hancock JT (2003) Nitric oxide signalling in plants. New Phytol 159:11
    Noritake T, Kawakita K, Doke N (1996) Nitric oxide induces phytoalexin accumulation in potato tuber tissue. Plant Cell Physiol 37:113-116
    Pedroso MC, Magalhaes JR, Durzan D (2000a) A nitric oxide burst precedes apoptosis in angiosperm and gymnosperm callus cells and foliar tissues. J Exp Bot 51:1027
    Pedroso MC, Magalhaes JR, Durzan D (2000b) Nitric oxide induces cell death in Taxus cells. Plant Sci 157:173-180
    Shen J-G, Wang J, Zhao B-L, Hou J-W, Gao T-L, Xin W-J (1998) Effects of EGb-761 on nitric oxide, oxygen free radicals, myocardial damage and arrhythmias in ischemia-reperfusion injury in vivo. Biochim Biophys Acta 1406:228-236
    Shen J-G, Li M, Xin W-J, Zhao B-L (2000) Effects of Chinonin on nitric oxide free radical, myocardial damage and arrhythmia in ischemia-reperfusion injury in vivo. Appl Magn Reson 19:9-19
    Stohr C, Ullrich WR (2002) Generation and possible roles of NO in plant roots and their apoplastic space. J Exp Bot 53:2293
    Suzuki Y, Fujii S, Tominaga T, Yoshimoto T, Fujii S, Akaike T, Maeda H, Yoshimura TJ (1999) Direct evidence of in vivo nitric oxide production and inducible nitric oxide synthase mRNA expression in the brain of living rat during experimental meningitis. Cereb Blood Flow Metab 19:175
    Ueda Y, Yokoyama H, Ohya-Nishiguchi H, Kamada H (1997) ESR Imaging of the rat brain with a nitroxide radical perfused by in vivo microdialysis. Magn Reson Imaging 15:355-360
    Van Camp W, Inze D, Van Montagu M (1998) H2O2 and NO:redox signals in disease resistance. Trends Plant Sci 3:330-334
    Velayutham M, Li HH, Kuppusamy P, Zweier JL (2003) Mapping ischemic risk region and necrosis in the isolated heart using EPR imaging. Magn Reson Med 49:1181-1187
    Wendehenne D, Pugin A, Klessig DF, Durner J (2001) Nitric oxide:comparative synthesis and signaling in animal and plant cells. Trends Plant Sci 6:177-183
    Wink DA, Hanbauer L, Krishna MC, Graeff R, Lee HC, Foster R, Chua N-H (1997) Abscisic acid signaling through cyclic ADPribose in plant. Science 282:226-230
    Wu K, Huang C, Cong J, Xian H, Wang C, Gao S (2005) Plate form three-dimensional gradient coils for L-band ESR imaging experiment. J Magn Reson 175:256-263
    Wu K, Huang C, Cao Y, Zheng Y, Cong J, Xian HG, Wang CN, Gao S, Zhao B-L (2007) Plate form three-dimensional gradient coils for L-band ESR imaging experiment. J Magn Reson 184:357
    Xu Y-C, Zhao B-L (2003) The main origin of endogenous NO in higher non-leguminous plant. Plant Physiol Biochem 41:833-838
    Xu Y-C, Cao Y-L, Guo P, Zhao B-L (2004) Detection of nitric oxide in plants by electron spin resonance. Phytopath 94:402-407
    Xu Y-C, Cao Y-L, Guo P, Zhao B-L (2005) Technique of detection of NO in plants by ESR spin trapping. Method Enzym 396:84-92
    Yermolaieva O, Brot N, Weissbach H, Heinemann SH, Hoshi T (2000) Reactive oxygen species and nitric oxide mediate plasticity of neuronal calcium signaling. Proc Natl Acad Sci USA 97:448
    Yokoyama H, Yoshimura T, Fujii S, Takayama F, Oikawa K, Kamada H (1996) In vivo EPR detection and imaging of endogenous nitric oxide in lipopolysaccharide-treated mice. Nat Biotechnol 14:992-994
    Yokoyama H, Fujii S, Yoshimura T, Ohya-Nishiguchi H, Kamada H (1997) In vivo ESR-CT imaging of the liver in mice receiving subcutaneous injection of nitric oxide-bound iron complex.
    Magn Reson Imaging 15:249-253
    Yokoyama H, Itoh O, Aoyama M, Obara H, Ohya H, Kamada H (2000) In vivo EPR imaging by using an acyl-protected hydroxylamine to analyze intracerebral oxidative stress in rats after epileptic seizures. Magn Reson Imaging 18:875-879
    Yokoyama H, Itoh O, Aoyama M, Obara H, Kamada H (2002) In vivo temporal EPR imaging of the brain of rats by using two types of blood-brain barrier-permeable nitroxide radicals. Magn Reson Imaging 20:277-284
    Yoshimura T, Fujii S, Yokoyama H, Kamada H (1995) In vivo electron paramagnetic resonance imaging of NO-bound iron complex in a rat head. Chem Lett 24(4):309-310
    Zeidler D, Zähringer U, Gerber I, Dubery I, Hartung T, Bors W, Hutzler P, Durner J (2004) Innate immunity in Arabidopsis thaliana:lipopolysaccharides activate nitric oxide synthase(NOS) and induce defense genes. Proc Natl Acad Sci USA 101:15811-15816
    Zhang DJ, Xiong J, Hu Y, Li Y, Zhao B (2001) Improved method to detect nitric oxide in biological systems. Appl Magn Reson 20:345-356
    Zhang Y-T, Zhang D-L, Cao Y-L, Zhao B-L (2002) Developmental experession and activity variation of nitric oxide synthesase in the brain of golden hamster. Brain Res Bull 58:385-389
    Zhang YT, Zhang J, Zhao B-L (2004a) Nitric oxide synthase inhibition prevents neuronal death in the developing visual cortex. Eur J Neurosci 20:2251-2259
    Zhang D-L, Yin J-J, Zhao B-L (2004b) Oral administration of Crataegus extraction protects against ischemia/reperfusion brain damage in the Mongolian gerbils. J Neurochem 90:211-219
    Zhao B-L (2005) Nitric oxide in neurodegenarative diseases. Front Biosci 10:454-461
    Zhao BL (2015) "ouble Edge" effects of nitric oxide free radical in cardio-brain-vascular diseases and health studied by ESR. Chin J Magn Reson 32:195-207
    Zhao B-L, Wang J-C, Hou J-W, Xin W-J (1996a) Studies on the mechanism of generation of NO free radicals from polymorphonuclear leukocytes stimulated by PMA. Cell Biol Int Rep 20:343-350
    Zhao B-L, Shen J-G, Li M, Xin W-J (1996b) Scavenging effect of Chinonin on NO and oxygen free radicals generated from ischemia reperfusion myocardium. Biochem Biophys Acta 1317:131-137
    Zhou GY, Zhao BL, Hou JW, Li MF, Chen C, Xin WJ (1999) Detect of nitric oxide in tissue by spin trapping EPR spectroscopy and triacetylglycerol extraction. Biotechnol Tech 13:507-511
    Zou J, Zhang H (2017) Super-resolution reconstruction of color image based on microarray lens. In:2017 international conference on applied system innovation (ICASI), pp. 830-833
    Zweier JL, Chzhan M, Samouilov A (1998) Electron paramagnetic resonance imaging of the rat heart. Phys Med Biol 43:1823-1835
  • 加载中

Catalog

    通讯作者: 陈斌, bchen63@163.com
    • 1. 

      沈阳化工大学材料科学与工程学院 沈阳 110142

    1. 本站搜索
    2. 百度学术搜索
    3. 万方数据库搜索
    4. CNKI搜索

    Article Metrics

    Article views (126) PDF downloads(168) Cited by()
    Proportional views
    Related

    /

    DownLoad:  Full-Size Img  PowerPoint
    Return
    Return