Immuno-spin trapping from biochemistry to medicine: Advances, challenges, and pitfalls. Focus on protein-centered radicals

Biochimica et Biophysica Acta - General Subjects

Volumn 1840, Issue 2, 2014, Pages 722-729

  Gomez Mejiba, Sandra E ^a   Zhai, Zili ^b   Della Vedova, Maria C ^a   Muñoz, Marcos D ^a   Chatterjee, Saurabh ^c   Towner, Rheal A ^d   Hensley, Kenneth ^e   Floyd, Robert A ^d   Mason, Ronald P ^f   Ramirez, Dario C ^a  

^a UNIVERSIDAD NACIONAL DE SAN LUIS   (Argentina)

^b UNIVERSITY OF CHICAGO   (United States)

^c UNIVERSITY OF SOUTH CAROLINA   (United States)

^d OKLAHOMA MEDICAL RESEARCH FOUNDATION   (United States)

^e UNIVERSITY OF TOLEDO MEDICAL CENTER   (United States)

^f NATIONAL INSTITUTE OF ENVIRONMENTAL HEALTH SCIENCES   (United States)

Author keywords

Anti DMPO; Disease exposure model; Immuno spin trapping; Protein radical; Reactive chemical species; Spin trap

Indexed keywords

5,5 DIMETHYL 1 PYRROLINE 1 OXIDE; NITRONE; RADICAL; REACTIVE OXYGEN METABOLITE; ALBUMIN; ALPHA LACTALBUMIN; CATALASE; COPPER ZINC SUPEROXIDE DISMUTASE; CYTOCHROME C; EOSINOPHIL PEROXIDASE; GUANOSINE TRIPHOSPHATASE ACTIVATING PROTEIN; HEMOGLOBIN; LACTOPEROXIDASE; MANGANESE SUPEROXIDE DISMUTASE; MEMBRANE PROTEIN; MYELOPEROXIDASE; MYOGLOBIN; NEUROGLOBIN; THYROID PEROXIDASE;

AGRANULOCYTOSIS; AMYOTROPHIC LATERAL SCLEROSIS; ANALYTIC METHOD; ANTIBODY DETECTION; ANTIOXIDANT ACTIVITY; ASTHMA; BIOCHEMISTRY; CELL ORGANELLE; CELL STRESS; CELLULAR DISTRIBUTION; CONCENTRATION RESPONSE; DIABETES MELLITUS; DISEASE MODEL; ELECTRON SPIN RESONANCE; HOST PARASITE INTERACTION; IMMUNO SPIN TRAPPING; IMMUNODETECTION; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATION; INTERMETHOD COMPARISON; LUNG INJURY; MEDICAL RESEARCH; MICROENVIRONMENT; NONHUMAN; OBESITY; PATHOGENESIS; PRIORITY JOURNAL; PROCESS DESIGN; PROCESS DEVELOPMENT; PROTEIN ANALYSIS; PROTEIN BINDING; PROTEIN INTERACTION; PROTEIN LOCALIZATION; REPRODUCIBILITY; REVIEW; SENSITIVITY AND SPECIFICITY; SEPSIS; SPIN TRAPPING; TISSUE DISTRIBUTION; CARDIOTOXICITY; CHEMICAL REACTION; COMPLEX FORMATION; DNA ADDUCT; ENZYME LINKED IMMUNOSORBENT ASSAY; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; IMMUNOASSAY; LIVER TOXICITY; MASS SPECTROMETRY; NUCLEAR MAGNETIC RESONANCE IMAGING; REPERFUSION INJURY; STEADY STATE; TANDEM MASS SPECTROMETRY; TRYPANOSOMA CRUZI;

ANIMALIA;

5,5-DIMETHYL-1-PYRROLINE N-OXIDE; AG; AMINOGLUTETHIMIDE; ANTI-DMPO; BOVINE SERUM ALBUMIN; BSA; DISEASE/EXPOSURE MODEL; DMPO; ELECTRON SPIN RESONANCE; ESR; HIGH PERFORMANCE LIQUID CHROMATOGRAPHY; HOMB; HORSE MYGLOBIN; HPLC; HUHB/MB; HUMAN HEMOGLOBIN/MYOGLOBIN; I/R; IMMUNO-SPIN TRAPPING; ISCHEMIA/REPERFUSION; IST; LC; LIPOPOLYSACCHARIDE; LIQUID CHROMATOGRAPHY; LPS; MAGNETIC RESONANCE IMAGING; MASS SPECTROMETRY; MRI; MS; OA; OCTANOIC ACID; PROTEIN RADICAL; REACTIVE CHEMICAL SPECIES; SOD; SPIN TRAP; SUPEROXIDE DISMUTASE; THYROID PEROXIDASE; TPO;

ANIMALS; BIOCHEMISTRY; FREE RADICALS; HUMANS; IMMUNOGLOBULIN G; NITROGEN OXIDES; PROTEINS; SPIN TRAPPING;

EID: 84890116733     PISSN: 03044165     EISSN: 18728006     Source Type: Journal    
DOI: 10.1016/j.bbagen.2013.04.039     Document Type: Review

References (83)

1. R.P. Mason Assay of in situ radicals by electron spin resonance Methods Enzymol. 105 1984 416 422
2. R.P. Mason In vivo spin trapping - from chemistry to toxicology C.J. Rhodes, Toxicology of the Human Environment The Critical Role of Free Radicals 2000 Taylor and Francis London 49 70
3. O. Augusto, J. Schreiber, and R.P. Mason Direct ESR detection of a free radical intermediate during the peroxidase-catalyzed oxidation of the antimalarial drug primaquine Biochem. Pharmacol. 37 1988 2791 2797
4. L.J. Berliner From spin-labeled proteins to in vivo EPR applications Eur. Biophys. J. 39 2010 579 588
5. M.J. Davies, and T.F. Slater The use of electron-spin-resonance techniques to detect free-radical formation and tissue damage Proc. Nutr. Soc. 47 1988 397 405
6. E.G. Janzen Spin trapping Methods Enzymol. 105 1984 188 198
7. M.J. Davies, and C.L. Hawkins EPR spin trapping of protein radicals Free Radic. Biol. Med. 36 2004 1072 1086 (Pubitemid 38479861)
8. O. Augusto, and S. Muntz Vaz EPR spin-trapping of protein radicals to investigate biological oxidative mechanisms Amino Acids 32 2007 535 542 (Pubitemid 46790935)
9. M.J. Davies, B.C. Gilbert, and R.M. Haywood Radical-induced damage to proteins: e.s.r. spin-trapping studies Free Radic. Res. Commun. 15 1991 111 127
10. E.G. Janzen, M.S. West, Y. Kotake, and C.M. DuBose Biological spin trapping methodology. III. Octanol-water partition coefficients of spin-trapping compounds J. Biochem. Biophys. Methods 32 1996 183 190 (Pubitemid 26238461)
11. K. Anzai, T. Aikawa, Y. Furukawa, Y. Matsushima, S. Urano, and T. Ozawa ESR measurement of rapid penetration of DMPO and DEPMPO spin traps through lipid bilayer membranes Arch. Biochem. Biophys. 415 2003 251 256 (Pubitemid 36794139)
12. E.G. Janzen, J.L. Poyer, C.F. Schaefer, P.E. Downs, and C.M. DuBose Biological spin trapping. II. Toxicity of nitrone spin traps: dose-ranging in the rat J. Biochem. Biophys. Methods 30 1995 239 247
13. F.A. Villamena, A. Das, and K.M. Nash Potential implication of the chemical properties and bioactivity of nitrone spin traps for therapeutics Future Med. Chem. 4 2012 1171 1207
14. R.A. Floyd, R.D. Kopke, C.H. Choi, S.B. Foster, S. Doblas, and R.A. Towner Nitrones as therapeutics Free Radic. Biol. Med. 45 2008 1361 1374
15. E.G. Janzen, L.T. Jandrisits, R.V. Shetty, D.L. Haire, and J.W. Hilborn Synthesis and purification of 5,5-dimethyl-1-pyrroline-N-oxide for biological applications Chem. Biol. Interact. 70 1989 167 172 (Pubitemid 19161223)
16. K. Ranguelova, and R.P. Mason The fidelity of spin trapping with DMPO in biological systems Magn. Reson. Chem. 49 2011 152 158
17. K.M. Nash, A. Rockenbauer, and F.A. Villamena Reactive nitrogen species reactivities with nitrones: theoretical and experimental studies Chem. Res. Toxicol. 25 2012 1581 1597
18. F. Leinisch, K. Ranguelova, E.F. Derose, J. Jiang, and R.P. Mason Evaluation of the Forrester-Hepburn mechanism as an artifact source in ESR spin-trapping Chem. Res. Toxicol. 24 2011 2217 2226
19. C.L. Hawkins, P.E. Morgan, and M.J. Davies Quantification of protein modification by oxidants Free Radic. Biol. Med. 46 2009 965 988
20. R.P. Mason Using anti-5,5-dimethyl-1-pyrroline N-oxide (anti-DMPO) to detect protein radicals in time and space with immuno-spin trapping Free Radic. Biol. Med. 36 2004 1214 1223 (Pubitemid 38526315)
21. S.E. Gomez-Mejiba, Z. Zhai, H. Akram, L.J. Deterding, K. Hensley, N. Smith, R.A. Towner, K.B. Tomer, R.P. Mason, and D.C. Ramirez Immuno-spin trapping of protein and DNA radicals: "tagging" free radicals to locate and understand the redox process Free Radic. Biol. Med. 46 2009 853 865
22. D.C. Ramirez, Y.R. Chen, J. Corbett, and R.P. Mason Detection of hemoglobin-tyrosyl-radical derived nitrone adducts by immuno-spin trapping. A first application to in vivo toxicology Free Radic. Biol. Med. 33 2002 434
23. C.D. Detweiler, L.J. Deterding, K.B. Tomer, C.F. Chignell, D. Germolec, and R.P. Mason Immunological identification of the heart myoglobin radical formed by hydrogen peroxide Free Radic. Biol. Med. 33 2002 364 369 (Pubitemid 34786275)
24. L. Zhang, C.L. Chen, P.T. Kang, V. Garg, K. Hu, K.B. Green-Church, and Y.R. Chen Peroxynitrite-mediated oxidative modifications of complex II: relevance in myocardial infarction Biochem. 49 2010 2529 2539
25. M. Ehrenshaft, and R.P. Mason Protein radical formation on thyroid peroxidase during turnover as detected by immuno-spin trapping Free Radic. Biol. Med. 41 2006 422 430 (Pubitemid 44056010)
26. F.A. Summers, R.P. Mason, and M. Ehrenshaft Development of immunoblotting techniques for DNA radical detection Free Radic. Biol. Med. 56 2013 64 71
27. A.S. Domazou, W.H. Koppenol, and J.M. Gebicki Efficient repair of protein radicals by ascorbate Free Radic. Biol. Med. 46 2009 1049 1057
28. J.M. Gebicki, T. Nauser, A. Domazou, D. Steinmann, P.L. Bounds, and W.H. Koppenol Reduction of protein radicals by GSH and ascorbate: potential biological significance Amino Acids 39 2010 1131 1137
29. Z. Zhai, S.E. Gomez-Mejiba, M.S. Gimenez, L.J. Deterding, K.B. Tomer, R.P. Mason, M.T. Ashby, and D.C. Ramirez Free radical-operated proteotoxic stress in macrophages primed with lipopolysaccharide Free Radic. Biol. Med. 53 2012 172 181
30. N. Khan, C.M. Wilmot, G.M. Rosen, E. Demidenko, J. Sun, J. Joseph, J. O'Hara, B. Kalyanaraman, and H.M. Swartz Spin traps: in vitro toxicity and stability of radical adducts Free Radic. Biol. Med. 34 2003 1473 1481 (Pubitemid 36570419)
31. D.C. Ramirez, S.E. Gomez-Mejiba, and R.P. Mason Immuno-spin trapping analyses of DNA radicals Nat. Protoc. 2 2007 512 522 (Pubitemid 47040015)
32. D.C. Ramirez, and R.P. Mason Immuno-spin trapping: detection of protein-centered radicals Curr. Protoc. Toxicol. 2005 24:17.7.1 24:17.7.18
33. M.G. Bonini, A.G. Siraki, B.S. Atanassov, and R.P. Mason Immunolocalization of hypochlorite-induced, catalase-bound free radical formation in mouse hepatocytes Free Radic. Biol. Med. 42 2007 530 540 (Pubitemid 46162122)
34. C.D. Detweiler, O.M. Lardinois, L.J. Deterding, P.R. de Montellano, K.B. Tomer, and R.P. Mason Identification of the myoglobin tyrosyl radical by immuno-spin trapping and its dimerization Free Radic. Biol. Med. 38 2005 969 976 (Pubitemid 40321088)
35. S. Bhattacharjee, L.J. Deterding, J. Jiang, M.G. Bonini, K.B. Tomer, D.C. Ramirez, and R.P. Mason Electron transfer between a tyrosyl radical and a cysteine residue in hemoproteins: spin trapping analysis J. Am. Chem. Soc. 129 2007 13493 13501 (Pubitemid 350071777)
36. O.M. Lardinois, C.D. Detweiler, K.B. Tomer, R.P. Mason, and L.J. Deterding Identifying the site of spin trapping in proteins by a combination of liquid chromatography, ELISA, and off-line tandem mass spectrometry Free Radic. Biol. Med. 44 2008 893 906
37. D.C. Ramirez, Y.R. Chen, and R.P. Mason Immunochemical detection of hemoglobin-derived radicals formed by reaction with hydrogen peroxide: involvement of a protein-tyrosyl radical Free Radic. Biol. Med. 34 2003 830 839 (Pubitemid 36316067)
38. L.J. Deterding, D.C. Ramirez, J.R. Dubin, R.P. Mason, and K.B. Tomer Identification of free radicals on hemoglobin from its self-peroxidation using mass spectrometry and immuno-spin trapping: observation of a histidinyl radical J. Biol. Chem. 279 2004 11600 11607 (Pubitemid 38401661)
39. Y.-R. Chen, C.-L. Chen, X. Liu, H. Li, J.L. Zweier, and R.P. Mason Involvement of protein radical, protein aggregation, and effects on NO metabolism in the hypochlorite-mediated oxidation of mitochondrial cytochrome c Free Radic. Biol. Med. 37 2004 1591 1603 (Pubitemid 39349805)
40. 2 reaction using immuno-spin trapping and mass spectrometry Biochemistry 47 2008 10440 10448
41. D.C. Ramirez, S.E. Gomez Mejiba, and R.P. Mason Mechanism of hydrogen peroxide-induced Cu, Zn-superoxide dismutase-centered radical formation as explored by immuno-spin trapping: the role of copper- and carbonate radical anion-mediated oxidations Free Radic. Biol. Med. 38 2005 201 214 (Pubitemid 39656131)
42. D.C. Ramirez, S.E. Gomez-Mejiba, J.T. Corbett, L.J. Deterding, K.B. Tomer, and R.P. Mason Cu, Zn-superoxide dismutase-driven free radical modifications: copper- and carbonate radical anion-initiated protein radical chemistry Biochem. J. 417 2009 341 353
43. K. Ranguelova, M.G. Bonini, and R.P. Mason (Bi) sulfite oxidation by copper, zinc-superoxide dismutase: sulfite-derived, radical-initiated protein radical formation Environ. Heal. Perspect. 118 2010 970 975
44. K. Ansenberger-Fricano, D. Ganini, M. Mao, S. Chatterjee, S. Dallas, R.P. Mason, K. Stadler, J.H. Santos, and M.G. Bonini The peroxidase activity of mitochondrial superoxide dismutase Free Radic. Biol. Med. 54 2013 116 124
45. A.G. Siraki, M.G. Bonini, J. Jiang, M. Ehrenshaft, and R.P. Mason Aminoglutethimide-induced protein free radical formation on myeloperoxidase: a potential mechanism of agranulocytosis Chem. Res. Toxicol. 20 2007 1038 1045 (Pubitemid 47204817)
46. A.G. Siraki, L.J. Deterding, M.G. Bonini, J. Jiang, M. Ehrenshaft, K.B. Tomer, and R.P. Mason Procainamide, but not N-acetylprocainamide, induces protein free radical formation on myeloperoxidase: a potential mechanism of agranulocytosis Chem. Res. Toxicol. 21 2008 1143 1153
47. K. Ranguelova, S. Chatterjee, M. Ehrenshaft, D.C. Ramirez, F.A. Summers, M. Kadiiska, and R.P. Mason Protein radical formation resulting from eosinophil peroxidase-catalyzed oxidation of sulfite J. Biol. Chem. 285 2010 24195 24205
48. Q. Guo, C.D. Detweiler, and R.P. Mason Protein radical formation during lactoperoxidase-mediated oxidation of the suicide substrate glutathione: immunochemical detection of a lactoperoxidase radical-derived 5,5-dimethyl-1-pyrroline N-oxide nitrone adduct J. Biol. Chem. 279 2004 13272 13283 (Pubitemid 38445907)
49. M.G. Bonini, A.G. Siraki, S. Bhattacharjee, and R.P. Mason Glutathione-induced radical formation on lactoperoxidase does not correlate with the enzyme's peroxidase activity Free Radic. Biol. Med. 42 2007 985 992 (Pubitemid 46371366)
50. Q. Guo, G.H. Gao, S.Y. Qian, and R.P. Mason Novel identification of a sulfur-centered, radical-derived 5,5-dimethyl-1-pyrroline N-oxide nitrone adduct formed from the oxidation of DTT by LC/ELISA, LC/electrospray ionization-MS, and LC/tandem MS Chem. Res. Toxicol. 17 2004 1481 1490 (Pubitemid 39532317)
51. D.C. Ramirez, S.E. Gomez-Mejiba, and R.P. Mason Copper-catalyzed protein oxidation and its modulation by carbon dioxide: enhancement of protein radicals in cells J. Biol. Chem. 280 2005 27402 27411 (Pubitemid 41040782)
52. T.K. Dalsgaard, M. Triquigneaux, L. Deterding, F. Summers, K. Ranguelova, G. Mortensen, and R.P. Mason Site-specific detection of radicals on alpha-lactalbumin after a riboflavin-sensitized reaction, detected by immuno-spin trapping, ESR, and MS J. Agric. Food Chem. 61 2013 418 426
53. M.F. Davis, L. Zhou, M. Ehrenshaft, K. Ranguelova, H.P. Gunawardena, X. Chen, M.G. Bonini, R.P. Mason, and S.L. Campbell Detection of Ras GTPase protein radicals through immuno-spin trapping Free Radic. Biol. Med. 53 2012 1339 1345
54. M.J. Davies Detection of myoglobin-derived radicals on reaction of metmyoglobin with hydrogen peroxide and other peroxidic compounds Free Radic. Res. Commun. 10 1990 361 370
55. M.R. Gunther, R.A. Tschirret-Guth, H.E. Witkowska, Y.C. Fann, D.P. Barr, P.R. Ortiz De Montellano, and R.P. Mason Site-specific spin trapping of tyrosine radicals in the oxidation of metmyoglobin by hydrogen peroxide Biochem. J. 330 Pt 3 1998 1293 1299 (Pubitemid 28162008)
56. M.J. Davies The oxidative environment and protein damage Biochim. Biophys. Acta 1703 2005 93 109 (Pubitemid 40170433)
57. P. Cassina, A. Cassina, M. Pehar, R. Castellanos, M. Gandelman, A. de Leon, K.M. Robinson, R.P. Mason, J.S. Beckman, L. Barbeito, and R. Radi Mitochondrial dysfunction in SOD1G93A-bearing astrocytes promotes motor neuron degeneration: prevention by mitochondrial-targeted antioxidants J. Neurosci. 28 2008 4115 4122
58. A.G. Siraki, J. Jiang, and R.P. Mason Investigating the mechanisms of aromatic amine-induced protein free radical formation by quantitative structure-activity relationships: implications for drug-induced agranulocytosis Chem. Res. Toxicol. 23 2010 880 887
59. K. Ranguelova, A.B. Rice, A. Khajo, M. Triquigneaux, S. Garantziotis, R.S. Magliozzo, and R.P. Mason Formation of reactive sulfite-derived free radicals by the activation of human neutrophils: an ESR study Free Radic. Biol. Med. 52 2012 1264 1271
60. K. Ranguelova, A.B. Rice, O.M. Lardinois, M. Triquigneaux, N. Steinckwich, L.J. Deterding, S. Garantziotis, and R.P. Mason Sulfite-mediated oxidation of myeloperoxidase to a free radical: immuno-spin trapping detection in human neutrophils Free Radic. Biol. Med. 60C 2013 98 106
61. K. Ranguelova, J. Suarez, R.S. Magliozzo, and R.P. Mason Spin trapping investigation of peroxide- and isoniazid-induced radicals in Mycobacterium tuberculosis catalase-peroxidase Biochemistry 47 2008 11377 11385
62. M.N. Alvarez, G. Peluffo, L. Piacenza, and R. Radi Intraphagosomal peroxynitrite as a macrophage-derived cytotoxin against internalized Trypanosoma cruzi: consequences for oxidative killing and role of microbial peroxiredoxins in infectivity J. Biol. Chem. 286 2011 6627 6640
63. S.E. Gomez-Mejiba, M.S. Gimenez, Z. Zhai, and D.C. Ramirez Trapping of protein-centered radicals with a nitrone spin trap prevents endotoxin-induced experimental acute respiratory distress syndrome mouse model Free Radic. Biol. Med. 49 2010 S184
64. S. Chatterjee, M. Ehrenshaft, S. Bhattacharjee, L.J. Deterding, M.G. Bonini, J. Corbett, M.B. Kadiiska, K.B. Tomer, and R.P. Mason Immuno-spin trapping of a post-translational carboxypeptidase B1 radical formed by a dual role of xanthine oxidase and endothelial nitric oxide synthase in acute septic mice Free Radic. Biol. Med. 46 2009 454 461
65. S. Chatterjee, O. Lardinois, M.G. Bonini, S. Bhattacharjee, K. Stadler, J. Corbett, L.J. Deterding, K.B. Tomer, M. Kadiiska, and R.P. Mason Site-specific carboxypeptidase B1 tyrosine nitration and pathophysiological implications following its physical association with nitric oxide synthase-3 in experimental sepsis J. Immunol. 183 2009 4055 4066
66. Y.R. Chen, C.L. Chen, L. Zhang, K.B. Green-Church, and J.L. Zweier Superoxide generation from mitochondrial NADH dehydrogenase induces self-inactivation with specific protein radical formation J. Biol. Chem. 280 2005 37339 37348 (Pubitemid 41642339)
67. L. Zuo, Y.R. Chen, L.A. Reyes, H.L. Lee, C.L. Chen, F.A. Villamena, and J.L. Zweier The radical trap 5,5-dimethyl-1-pyrroline N-oxide exerts dose-dependent protection against myocardial ischemia-reperfusion injury through preservation of mitochondrial electron transport J. Pharmacol. Exp. Ther. 329 2009 515 523
68. Y.-R. Chen, C.-L. Chen, D.R. Pfeiffer, and J.L. Zweier Mitochondrial complex II in the post-ischemic heart. Oxidative injury and the role of protein S-glutathionylation J. Biol. Chem. 45 2007 32640 32654 (Pubitemid 350159288)
69. P.T. Kang, L. Zhang, C.L. Chen, J. Chen, K.B. Green, and Y.R. Chen Protein thiyl radical mediates S-glutathionylation of complex I Free Radic. Biol. Med. 53 2012 962 973
70. S. Dogan, G. Ozlem Elpek, E. Kirimlioglu Konuk, N. Demir, and M. Aslan Measurement of intracellular biomolecular oxidation in liver ischemia-reperfusion injury via immuno-spin trapping Free Radic. Biol. Med. 53 2012 406 414
71. K. Stadler, M.G. Bonini, S. Dallas, J. Jiang, R. Radi, R.P. Mason, and M.B. Kadiiska Involvement of inducible nitric oxide synthase in hydroxyl radical-mediated lipid peroxidation in streptozotocin-induced diabetes Free Radic. Biol. Med. 45 2008 866 874
72. K. Stadler, M.G. Bonini, S. Dallas, D. Duma, R.P. Mason, and M.B. Kadiiska Direct evidence of iNOS-mediated in vivo free radical production and protein oxidation in acetone-induced ketosis Am. J. Physiol. Endocrinol. Metab. 295 2008 E456 E462
73. N.K. Khoo, N. Cantu-Medellin, J.E. Devlin, C.M. St Croix, S.C. Watkins, A.M. Fleming, H.C. Champion, R.P. Mason, B.A. Freeman, and E.E. Kelley Obesity-induced tissue free radical generation: an in vivo immuno-spin trapping study Free Radic. Biol. Med. 52 2012 2312 2319
74. S. Chatterjee, R. Rana, J. Corbett, M.B. Kadiiska, J. Goldstein, and R.P. Mason P2X7 receptor-NADPH oxidase axis mediates protein radical formation and Kupffer cell activation in carbon tetrachloride-mediated steatohepatitis in obese mice Free Radic. Biol. Med. 52 2012 1666 1679
75. Z. Zhai, S.E. Gomez-Mejiba, H. Zhu, F. Lupu, and D.C. Ramirez The spin trap 5,5-dimethyl-1-pyrroline N-oxide inhibits lipopolysaccharide-induced inflammatory response in RAW 264.7 cells Life Sci. 90 2012 432 439
76. Z. Zhai, S.E. Gomez-Mejiba, and D.C. Ramirez The nitrone spin trap 5,5-dimethyl-1-pyrroline n-oxide affects stress response and fate of lipopolysaccharide-primed RAW 264.7 macrophage cells Inflammation 36 2012 346 354
77. S.Y. Qian, H.P. Wang, F.Q. Schafer, and G.R. Buettner EPR detection of lipid-derived free radicals from PUFA, LDL, and cell oxidations Free Radic. Biol. Med. 29 2000 568 579
78. R.A. Towner, N. Smith, D. Saunders, M. Henderson, K. Downum, F. Lupu, R. Silasi-Mansat, D.C. Ramirez, S.E. Gomez-Mejiba, M.G. Bonini, M. Ehrenshaft, and R.P. Mason In vivo imaging of immuno-spin trapped radicals with molecular magnetic resonance imaging in a diabetic mouse model Diabetes 61 2012 2405 2413
79. C.C. Winterbourn, and I.H. Buss Protein carbonyl measurement by enzyme-linked immunosorbent assay Methods Enzymol. 300 1999 106 111
80. M.A. Baraibar, R. Ladouce, and B. Friguet Proteomic quantification and identification of carbonylated proteins upon oxidative stress and during cellular aging J. Proteomics 2013 10.1016/j.jprot.2013.05.008 (in press)
81. S.E. Gomez-Mejiba, Z. Zhai, M.S. Gimenez, M.T. Ashby, J. Chilakapati, K. Kitchin, R.P. Mason, and D.C. Ramirez Myeloperoxidase-induced genomic DNA-centered radicals J. Biol. Chem. 285 2010 20062 20071
82. D.C. Ramirez, S.E. Gomez-Mejiba, and R.P. Mason Immuno-spin trapping of DNA radicals Nat. Methods 3 2006 123 127 (Pubitemid 43173311)
83. C.L. Hawkins, and M.J. Davies Detection of intermediates formed on reaction of hyaluronic acid and related materials with the hydroxyl radical Biochem. Soc. Trans. 23 1995 248S