Exploiting oxidative microenvironments in the body as triggers for drug delivery systems

Antioxidants and Redox Signaling

Volumn 21, Issue 5, 2014, Pages 730-754

  Joshi Barr, Shivanjali ^a   De Gracia Lux, Caroline ^a   Mahmoud, Enas ^a   Almutairi, Adah ^a,b  

^a UNIVERSITY OF CALIFORNIA SAN DIEGO   (United States)

^b UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DICHLORODIHYDROFLUORESCEIN DIACETATE; FERROCENE; NANOCARRIER; NANOPARTICLE; POLYMER; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SELENIUM; SILICON; SULFIDE; DRUG CARRIER; NANOMATERIAL;

ATHEROSCLEROSIS; CELL MEMBRANE; CHEMICAL STRUCTURE; CHRONIC OBSTRUCTIVE LUNG DISEASE; DEGENERATIVE DISEASE; DRUG DELIVERY SYSTEM; DRUG RELEASE; ENVIRONMENTAL FACTOR; EXTRACELLULAR SPACE; GENE MUTATION; HUMAN; INFLAMMATION; MICELLE; MICROENVIRONMENT; NEOPLASM; NONHUMAN; OXIDATION; OXIDATIVE STRESS; PEROXISOME; PHAGOSOME; PRIORITY JOURNAL; REVIEW; RHEUMATOID ARTHRITIS; SYSTEMIC INFLAMMATORY RESPONSE SYNDROME; ANIMAL; CHEMISTRY; METABOLISM; OXIDATION REDUCTION REACTION; PROCEDURES; SIGNAL TRANSDUCTION;

ANIMALS; DRUG CARRIERS; DRUG DELIVERY SYSTEMS; HUMANS; NANOSTRUCTURES; OXIDATION-REDUCTION; OXIDATIVE STRESS; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; SIGNAL TRANSDUCTION;

EID: 84904440126     PISSN: 15230864     EISSN: 15577716     Source Type: Journal    
DOI: 10.1089/ars.2013.5754     Document Type: Review

References (206)

1. Ahmed H. Principles and Reactions of Protein Extraction, Purification, and Characterization. Boca Raton, FL: Taylor & Francis, 2004.
2. Albrecht SC, Barata AG, Grosshans J, Teleman AA, and Dick TP. In vivo mapping of hydrogen peroxide and oxidized glutathione reveals chemical and regional specificity of redox homeostasis. Cell Metab 14: 819-829, 2011.
3. Allen BL, Johnson JD, and Walker JP. Encapsulation and enzyme-mediated release of molecular cargo in polysulfide nanoparticles. ACS Nano 5: 5263-5272, 2011.
4. Amici A, Levine RL, Tsai L, and Stadtman ER. Conversion of amino-acid residues in proteins and amino-acid homopolymers to carbonyl derivatives by metal-catalyzed oxidation reactions. J Biol Chem 264: 3341-3346, 1989.
5. Antonenkov VD, Grunau S, Ohlmeier S, and Hiltunen JK. Peroxisomes are oxidative organelles. Antioxid Redox Signal 13: 525-537, 2010.
6. Auger I and Roudier J. A function for the QKRAA amino acid motif: mediating binding of DnaJ to DnaK. Implications for the association of rheumatoid arthritis with HLA-DR4. J Clin Invest 99: 1818-1822, 1997.
7. Avissar N, Slemmon JR, Palmer IS, and Cohen HJ. Partial sequence of human plasma glutathione peroxidase and immunologic identification of milk glutathione peroxidase as the plasma enzyme. J Nutrition 121: 1243-1249, 1991.
8. Barber SC and Shaw PJ. Oxidative stress in ALS: key role in motor neuron injury and therapeutic target. Free Radic Biol Med 48: 629-641, 2010.
9. Barrera G, Pizzimenti S, and Dianzani MU. Lipid peroxidation: control of cell proliferation, cell differentiation and cell death. Mol Aspects Med 29: 1-8, 2008.
10. Beal MF, Ferrante RJ, Browne SE, Matthews RT, Kowall NW, Brown RH, Jr. Increased 3-nitrotyrosine in both sporadic and familial amyotrophic lateral sclerosis. Ann Neurol 42: 644-654, 1997.
11. Belousov VV, Fradkov AF, Lukyanov KA, Staroverov DB, Shakhbazov KS, Terskikh AV, and Lukyanov S. Genetically encoded fluorescent indicator for intracellular hydrogen peroxide. Nat Methods 3: 281-286, 2006.
12. Berisha HI, Pakbaz H, Absood A, and Said SI. Nitric oxide as a mediator of oxidant lung injury due to paraquat. Proc Natl Acad Sci U S A 91: 7445-7449, 1994.
13. Bilski P, Belanger AG, and Chignell CF. Photosensitized oxidation of 2′,7′-dichlorofluorescin: singlet oxygen does not contribute to the formation of fluorescent oxidation product 2′,7′- dichlorofluorescein. Free Radic Biol Med 33: 938-946, 2002.
14. Boveris A. Determination of the production of superoxide radicals and hydrogen-peroxide in mitochondria. Meth Enzymol 105: 429-435, 1984.
15. Boveris A and Chance B. The mitochondrial generation of hydrogen peroxide. General properties and effect of hyperbaric oxygen. Biochem J 134: 707-716, 1973.
16. Briggs RT, Drath DB, Karnovsky ML, and Karnovsky MJ. Localization of NADH oxidase on the surface of human polymorphonuclear leukocytes by a new cytochemical method. J Cell Biol 67: 566-586, 1975.
17. Broaders KE, Grandhe S, and Frechet JMJ. A Biocompatible Oxidation-Triggered Carrier Polymer with Potential in Therapeutics. J Am Chem Soc 133: 756-758, 2011.
18. Brown TP, Rumsby PC, Capleton AC, Rushton L, and Levy LS. Pesticides and Parkinson's disease-is there a link? Environ Health Perspect 114: 156-164, 2006.
19. Budd SL, Castilho RF, and Nicholls DG. Mitochondrial membrane potential and hydroethidine-monitored superoxide generation in cultured cerebellar granule cells. FEBS Lett 415: 21-24, 1997.
20. Burgoyne JR, Oka S, Ale-Agha N, and Eaton P. Hydrogen peroxide sensing and signaling by protein kinases in the cardiovascular system. Antioxid Redox Signal 18: 1042-1052, 2013.
21. Bylund J, Brown KL, Movitz C, Dahlgren C, and Karlsson A. Intracellular generation of superoxide by the phagocyte NADPH oxidase: how, where, and what for? Free Radic Biol Med 49: 1834-1845, 2010.
22. Cadenas E and Davies KJA. Mitochondrial free radical generation, oxidative stress, and aging. Free Radic Biol Med 29: 222-230, 2000.
23. Cannon MB and Remington SJ. Redox-sensitive green fluorescent protein: probes for dynamic intracellular redox responses. A review. Methods Mol Biol 476: 51-65, 2008.
24. Castegna A, Aksenov M, Aksenova M, Thongboonkerd V, Klein JB, Pierce WM, Booze R, Markesbery WR, and Butterfield DA. Proteomic identification of oxidatively modified proteins in Alzheimer's disease brain. Part I: creatine kinase BB, glutamine synthase, and ubiquitin carboxy-terminal hydrolase L-1. Free Radic Biol Med 33: 562-571, 2002.
25. Cedergren J, Forslund T, Sundqvist T, and Skogh T. Intracellular oxidative activation in synovial fluid neutrophils from patients with rheumatoid arthritis but not from other arthritis patients. J Rheumatol 34: 2162-2170, 2007.
26. Chabaud M, Aarvak T, Garnero P, Natvig JB, and Miossec P. Potential contribution of IL-17-producing Th(1)cells to defective repair activity in joint inflammation: partial correction with Th(2)-promoting conditions. Cytokine 13: 113-118, 2001.
27. Chae HZ, Chung SJ, and Rhee SG. Thioredoxindependent peroxide reductase from yeast. J Biol Chem 269: 27670-27678, 1994.
28. Chaiswing L and Oberley TD. Extracellular/microenvironmental redox state. Antioxid Redox Signal 13: 449-465, 2010.
29. Chance B, Sies H, and Boveris A. Hydroperoxide metabolism in mammalian organs. Physiol Rev 59: 527-605, 1979.
30. Chang CH, Schiller B, and Goldfischer S. Small cytoplasmic bodies in the loop of Henle and distal convoluted tubule that resemble peroxisomes. J Histochem Cytochem 19: 56-62, 1971.
31. Chang LY, Slot JW, Geuze HJ, and Crapo JD. Molecular immunocytochemistry of the cuzn superoxide-dismutase in rat hepatocytes. J Cell Biol 107: 2169-2179, 1988.
32. Chatham WW, Swaim R, Frohsin H, Jr., Heck LW, Miller EJ, and Blackburn WD, Jr. Degradation of human articular cartilage by neutrophils in synovial fluid. Arthritis Rheum 36: 51-58, 1993.
33. Chen Q, Vazquez EJ, Moghaddas S, Hoppel CL, and Lesnefsky EJ. Production of reactive oxygen species by mitochondria: central role of complex III. J Biol Chem 278: 36027-36031, 2003.
34. Chen XQ, Tian XZ, Shin I, and Yoon J. Fluorescent and luminescent probes for detection of reactive oxygen and nitrogen species. Chem Soc Rev 40: 4783-4804, 2011.
35. Chu F, Esworthy R, Doroshow J, Doan K, and Liu X. Expression of plasma glutathione peroxidase in human liver in addition to kidney, heart, lung, and breast in humans and rodents. Blood 79: 3233-3238, 1992.
36. Chu FF, Doroshow JH, and Esworthy RS. Expression, characterization, and tissue distribution of a new cellular selenium-dependent glutathione peroxidase, GSHPx-GI. J Biol Chem 268: 2571-2576, 1993.
37. Chu FF, Esworthy RS, Chu PG, Longmate JA, Huycke MM, Wilczynski S, and Doroshow JH. Bacteria-induced intestinal cancer in mice with disrupted Gpx1 and Gpx2 genes. Cancer Res 64: 962-968, 2004.
38. Colton CA, Yao JB, Gilbert D, and Oster-Granite ML. Enhanced production of superoxide anion by microglia from trisomy 16 mice. Brain Res 519: 236-242, 1990.
39. Correia-Ledo D, Arnold AA, and Mauzeroll J. Synthesis of redox active ferrocene-modified phospholipids by transphosphatidylation reaction and chronoamperometry study of the corresponding redox sensitive liposome. J Am Chem Soc 132: 15120-15123, 2010.
40. Crow JP. Dichlorodihydrofluorescein and dihydrorhodamine 123 are sensitive indicators of peroxynitrite in vitro: implications for intracellular measurement of reactive nitrogen and oxygen species. Nitric Oxide 1: 145-157, 1997.
41. D'Aniello A, D'Onofrio G, Pischetola M, D'Aniello G, Vetere A, Petrucelli L, and Fisher GH. Biological role of D-amino acid oxidase and D-aspartate oxidase. Effects of D-amino acids. J Biol Chem 268: 26941-26949, 1993.
42. D'Autreaux B and Toledano MB. ROS as signalling molecules: mechanisms that generate specificity in ROS homeostasis. Nat Rev Mol Cell Biol 8: 813-824, 2007.
43. Daniel KB, Agrawal A, Manchester M, and Cohen SM. Readily accessible fluorescent probes for sensitive biological imaging of hydrogen peroxide. Chembiochem 14: 593-598, 2013.
44. Davies MG and Hagen PO. Systemic inflammatory response syndrome. Br J Surg 84: 920-935, 1997.
45. de Gracia Lux C, Joshi-Barr S, Nguyen T, Mahmoud E, Schopf E, Fomina N, and Almutairi A. Biocompatible polymeric nanoparticles degrade and release cargo in response to biologically relevant levels of hydrogen peroxide. J Am Chem Soc 134: 15758-15764, 2012.
46. de Jong HK, van der Poll T, and Wiersinga WJ. The systemic pro-inflammatory response in sepsis. J Innate Immun 2: 422-430, 2010.
47. Deng C, Jiang YJ, Cheng R, Meng FH, and Zhong ZY. Biodegradable polymeric micelles for targeted and controlled anticancer drug delivery: promises, progress and prospects. Nano Today 7: 467-480, 2012.
48. DeYulia GJ, Jr., Carcamo JM, Borquez-Ojeda O, Shelton CC, and Golde DW. Hydrogen peroxide generated extracellularly by receptor-ligand interaction facilitates cell signaling. Proc Natl Acad Sci U S A 102: 5044-5049, 2005.
49. Dickinson BC, Huynh C, and Chang CJ. A palette of fluorescent probes with varying emission colors for imaging hydrogen peroxide signaling in living cells. J Am Chem Soc 132: 5906-5915, 2010.
50. Dikalov S, Griendling KK, and Harrison DG. Measurement of reactive oxygen species in cardiovascular studies. Hypertension 49: 717-727, 2007.
51. Dooley CT, Dore TM, Hanson GT, Jackson WC, Remington SJ, and Tsien RY. Imaging dynamic redox changes in mammalian cells with green fluorescent protein indicators. J Biol Chem 279: 22284-22293, 2004.
52. ED J, C G, G B, HW H, TW K, and WW F. Localization of xanthine oxidase in mammary-gland epithelium and capillary. Cell 25: 67-82, 1981.
53. Eiserich JP, van der Vliet A, Handelman GJ, Halliwell B, and Cross CE. Dietary antioxidants and cigarette smokeinduced biomolecular damage: a complex interaction. Am J Clin Nutr 62: 1490S-1500S, 1995.
54. Elchuri S, Oberley TD, Qi W, Eisenstein RS, Jackson Roberts L, Van Remmen H, Epstein CJ, and Huang TT. CuZnSOD deficiency leads to persistent and widespread oxidative damage and hepatocarcinogenesis later in life. Oncogene 24: 367-380, 2005.
55. Eruslanov E and Kusmartsev S. Identification of ROS using oxidized DCFDA and flow-cytometry. In: T Advanced Protocols in Oxidative Stress II. 2009, pp. 57-72.
56. Esworthy RS, Ho YS, and Chu FF. The Gpx1 gene encodes mitochondrial glutathione peroxidase in the mouse liver. Arch Biochem Biophys 340: 59-63, 1997.
57. Finkel T. Signal transduction by reactive oxygen species. J Cell Biol 194: 7-15, 2011.
58. Finn AV, Nakano M, Narula J, Kolodgie FD, and Virmani R. Concept of vulnerable/unstable plaque. Arterioscler Thromb Vasc Biol 30: 1282-1292, 2010.
59. Finocchietto PV, Franco MC, Holod S, Gonzalez AS, Converso DP, Antico Arciuch VG, Serra MP, Poderoso JJ, and Carreras MC. Mitochondrial nitric oxide synthase: a masterpiece of metabolic adaptation, cell growth, transformation, and death. Exp Biol Med (Maywood) 234: 1020-1028, 2009.
60. Forman HJ and Boveris A. Chapter 3-Superoxide radical and hydrogen peroxide in mitochondria. In: Free Radicals in Biology, edited by William Pryor. London: Academic Press, 1982, pp. 65-90.
61. Freitas M, Lima JLFC, and Fernandes E. Optical probes for detection and quantification of neutrophils' oxidative burst. A review. Analyt Chim Acta 649: 8-23, 2009.
62. Fransen M, Nordgren M, Wang B, and Apanasets O. Role of peroxisomes in ROS/RNS-metabolism: implications for human disease. Biochim Biophys Acta 1822: 1363-1373, 2012.
63. Fridovich I. Superoxide dismutases. Ann Rev Biochem 44: 147-159, 1975.
64. Friedman M and Van den Bovenkamp GJ. The pathogenesis of a coronary thrombus. Am J Pathol 48: 19-44, 1966.
65. Fukai T, Folz RJ, Landmesser U, and Harrison DG. Extracellular superoxide dismutase and cardiovascular disease. Cardiovasc Res 55: 239-249, 2002.
66. Gaeta A and Hider RC. The crucial role of metal ions in neurodegeneration: the basis for a promising therapeutic strategy. Br J Pharmacol 146: 1041-1059, 2005.
67. Gaetani GF, Galiano S, Canepa L, Ferraris AM, and Kirkman HN. Catalase and glutathione peroxidase are equally active in detoxification of hydrogen peroxide in human erythrocytes. Blood 73: 334-339, 1989.
68. Gasser G, Ott I, and Metzler-Nolte N. Organometallic anticancer compounds. J Med Chem 54: 3-25, 2011.
69. Gaunt GL and Deduve C. Subcellular-distribution of D-amino-acid oxidase and catalase in rat-brain. J Neurochem 26: 749, 1976.
70. Gehrmann W and Elsner M. A specific fluorescence probe for hydrogen peroxide detection in peroxisomes. Free Rad Res 45: 501-506, 2011.
71. Giulivi C, Boveris A, and Cadenas E. Hydroxyl radical generation during mitochondrial electron transfer and the formation of 8-hydroxydesoxyguanosine in mitochondrial DNA. Arch Biochem Biophys 316: 909-916, 1995.
72. Glass CK, Saijo K, Winner B, Marchetto MC, and Gage FH. Mechanisms underlying inflammation in neurodegeneration. Cell 140: 918-934, 2010.
73. Goldstein IM, Cerqueira M, Lind S, and Kaplan HB. Evidence that the superoxide-generating system of human leukocytes is associated with the cell surface. J Clin Invest 59: 249-254, 1977.
74. Graves JA, Metukuri M, Scott D, Rothermund K, and Prochownik EV. Regulation of reactive oxygen species homeostasis by peroxiredoxins and c-Myc. J Biol Chem 284: 6520-6529, 2009.
75. Grisham MB. Methods to detect hydrogen peroxide in living cells: possibilities and pitfalls. Comp Biochem Physiol A Mol Integr Physiol 165: 429-438, 2013.
76. Gupta MK, Meyer TA, Nelson CE, and Duvall CL. Poly(PS-b-DMA) micelles for reactive oxygen species triggered drug release. J Controlled Release 162: 591-598, 2012.
77. Gutscher M, Pauleau AL, Marty L, Brach T, Wabnitz GH, Samstag Y, Meyer AJ, and Dick TP. Real-time imaging of the intracellular glutathione redox potential. Nat Methods 5: 553-559, 2008.
78. Guzman JN, Sanchez-Padilla J, Wokosin D, Kondapalli J, Ilijic E, Schumacker PT, and Surmeier DJ. Oxidant stress evoked by pacemaking in dopaminergic neurons is attenuated by DJ-1. Nature 468: 696-700, 2010.
79. Haber F and Weiss J. The catalytic decomposition of hydrogen peroxide by iron salts. Proc Royal Soc London A Math Phys Sci 147: 332-351, 1934.
80. Halliwell B, Clement MV, and Long LH. Hydrogen peroxide in the human body. FEBS Lett 486: 10-13, 2000.
81. Han P, Ma N, Ren HF, Xu HP, Li ZB, Wang ZQ, and Zhang X. Oxidation-Responsive Micelles Based on a Selenium-Containing Polymeric Superamphiphile. Langmuir 26: 14414-14418, 2010.
82. Hanson GT, Aggeler R, Oglesbee D, Cannon M, Capaldi RA, Tsien RY, and Remington SJ. Investigating mitochondrial redox potential with redox-sensitive green fluorescent protein indicators. J Biol Chem 279: 13044-13053, 2004.
83. Hauptmann N, Grimsby J, Shih JC, and Cadenas E. The metabolism of tyramine by monoamine oxidase A/B causes oxidative damage to mitochondrial DNA. Arch Biochem Biophys 335: 295-304, 1996.
84. Hodge S, Hodge G, Holmes M, and Reynolds PN. Increased airway epithelial and T-cell apoptosis in COPD remains despite smoking cessation. Eur Respir J 25: 447-454, 2005.
85. Horoz M, Bolukbas C, Bolukbas FF, Aslan M, Koylu AO, Selek S, and Erel O. Oxidative stress in hepatitis C infected end-stage renal disease subjects. BMC Infect Dis 6, 2006.
86. Hruban Z, Hopkins E, Slesers A, and Vigil EL. Microbodies- constituent organelles of animal cells. Lab Invest 27: 184-191, 1972.
87. Ivashchenko O, Van Veldhoven PP, Brees C, Ho YS, Terlecky SR, and Fransen M. Intraperoxisomal redox balance in mammalian cells: oxidative stress and interorganellar cross-talk. Mol Biol Cell 22: 1440-1451, 2011.
88. Janczewski D, Song J, Csanyi E, Kiss L, Blazso P, Katona RL, Deli MA, Gros G, Xu JW, and Vancso GJ. Organometallic polymeric carriers for redox triggered release of molecular payloads. J Mater Chem 22: 6429-6435, 2012.
89. Kan W, Zhao K-s, Jiang Y, Yan W, Huang Q, Wang J, Qin Q, Huang X, and Wang S. Lung, spleen, and kidney are the major places for inducible nitric oxide synthase expression in endotoxic shock: role of p38 mitogenactivated protein kinase in signal transduction of inducible nitric oxide synthase expression. Shock 21: 281-287, 2004.
90. Karin M. Nuclear factor-kappaB in cancer development and progression. Nature 441: 431-436, 2006.
91. Keatings VM and Barnes PJ. Granulocyte activation markers in induced sputum: comparison between chronic obstructive pulmonary disease, asthma, and normal subjects. Am J Respir Crit Care Med 155: 449-453, 1997.
92. Keele BB, Mccord JM, and Fridovic I. Superoxide dismutase from Escherichia-coli-B -a new manganesecontaining enzyme. J Biol Chem 245: 6176-6181, 1970.
93. Keller A, Mohamed A, Drose S, Brandt U, Fleming I, and Brandes RP. Analysis of dichlorodihydrofluorescein and dihydrocalcein as probes for the detection of intracellular reactive oxygen species. Free Radic Res 38: 1257-1267, 2004.
94. Kim JH, Chu SC, Gramlich JL, Pride YB, Babendreier E, Chauhan D, Salgia R, Podar K, Griffin JD, and Sattler M. Activation of the PI3K/mTOR pathway by BCR-ABL contributes to increased production of reactive oxygen species. Blood 105: 1717-1723, 2005.
95. Kim JY, Il Choi W, Kim YH, and Tae G. Highly selective in-vivo imaging of tumor as an inflammation site by ROS detection using hydrocyanine-conjugated, functional nano-carriers. J Controlled Release 156: 398-405, 2011.
96. Kinkade Jr JM, Pember SO, Barnes KC, Shapira R, Spitznagel JK, and Martin LE. Differential distribution of distinct forms of myeloperoxidase in different azurophilic granule subpopulations from human neutrophils. Biochem Biophys Res Comm 114: 296-303, 1983.
97. Kirkinezos IG and Moraes CT. Reactive oxygen species and mitochondrial diseases. Semin Cell Dev Biol 12: 449-457, 2001.
98. Kitazawa M, Anantharam V, and Kanthasamy AG. Dieldrin-induced oxidative stress and neurochemical changes contribute to apoptopic cell death in dopaminergic cells. Free Radic Biol Med 31: 1473-1485, 2001.
99. Klebanoff SJ. Myeloperoxidase: friend and foe. J Leukocyte Biol 77: 598-625, 2005.
100. Knowles RG and Moncada S. Nitric-oxide synthases in mammals. Biochem J 298: 249-258, 1994.
101. Kostikas K, Papatheodorou G, Psathakis K, Panagou P, and Loukides S. Oxidative stress in expired breath condensate of patients with COPD. Chest 124: 1373-1380, 2003.
102. Kotake S, Udagawa N, Takahashi N, Matsuzaki K, Itoh K, Ishiyama S, Saito S, Inoue K, Kamatani N, Gillespie MT, Martin TJ, and Suda T. IL-17 in synovial fluids from patients with rheumatoid arthritis is a potent stimulator of osteoclastogenesis. J Clin Invest 103: 1345-1352, 1999.
103. Kruth HS, Jones NL, Huang W, Zhao B, Ishii I, Chang J, Combs CA, Malide D, and Zhang WY. Macropinocytosis is the endocytic pathway that mediates macrophage foam cell formation with native low density lipoprotein. J Biol Chem 280: 2352-2360, 2005.
104. Kulbaba K, MacLachlan MJ, Evans CEB, and Manners I. Organometallic gels: Characterization and electrochemical studies of swellable, thermally crosslinked poly(ferrocenylsilane)s. Macromol Chem Phys 202: 1768-1775, 2001.
105. Kundu K, Knight SF, Willett N, Lee S, Taylor WR, and Murthy N. Hydrocyanines: A class of fluorescent sensors that can image reactive oxygen species in cell culture, tissue, and in vivo. Angew Chem Int Edit 48: 299-303, 2009.
106. Kuwana Y, Takei M, Yajima M, Imadome K, Inomata H, Shiozaki M, Ikumi N, Nozaki T, Shiraiwa H, Kitamura N, Takeuchi J, Sawada S, Yamamoto N, Shimizu N, Ito M, and Fujiwara S. Epstein-Barr virus induces erosive arthritis in humanized mice. PLoS One 6: e26630, 2011.
107. Kwon NS, Nathan CF, Gilker C, Griffith OW, Matthews DE, and Stuehr DJ. L-citrulline production from Larginine by macrophage nitric oxide synthase. The ureido oxygen derives from dioxygen. J Biol Chem 265: 13442-13445, 1990.
108. Labunskyy VM and Gladyshev VN. Role of reactive oxygen species-mediated signaling in aging. Antioxid Redox Signal 19: 1362-1372, 2012.
109. Lacy F, Gough DA, and Schmid-Schonbein GW. Role of xanthine oxidase in hydrogen peroxide production. Free Radic Biol Med 25: 720-727, 1998.
110. Lee D, Bae S, Hong D, Lim H, Yoon JH, Hwang O, Park S, Ke Q, Khang G, and Kang PM. H2O2-responsive molecularly engineered polymer nanoparticles as ischemia/ reperfusion-targeted nanotherapeutic agents. Sci Rep 3: 2233, 2013.
111. Lee D, Khaja S, Velasquez-Castano JC, Dasari M, Sun C, Petros J, Taylor WR, and Murthy N. In vivo imaging of hydrogen peroxide with chemiluminescent nanoparticles. Nat Mater 6: 765-769, 2007.
112. Lee SH, Gupta MK, Bang JB, Bae H, and Sung HJ. Current progress in reactive oxygen species (ROS)-responsive materials for biomedical applications. Adv Healthcare Mater 2: 908-915, 2013.
113. Li DW, Qin LX, Li Y, Nia RP, Long YT, and Chen HY. CdSe/ZnS quantum dot-Cytochrome c bioconjugates for selective intracellular O2 (-) sensing. Chem Commun (Camb) 47: 8539-8541, 2011.
114. Li X and Makarov SS. An essential role of NF-kappaB in the "tumor-like" phenotype of arthritic synoviocytes. Proc Natl Acad Sci U S A 103: 17432-17437, 2006.
115. Lim CK, Lee YD, Na J, Oh JM, Her S, Kim K, Choi K, Kim S, and Kwon IC. Chemiluminescence-generating nanoreactor formulation for near-infrared imaging of hydrogen peroxide and glucose level in vivo. Adv Funct Mater 20: 2644-2648, 2010.
116. Ling LU, Tan KB, Lin H, and Chiu GN. The role of reactive oxygen species and autophagy in safingolinduced cell death. Cell Death Dis 2: e129, 2011.
117. Liou GY and Storz P. Reactive oxygen species in cancer. Free Radic Res 44: 479-496, 2010.
118. Liu Q, Berchner-Pfannschmidt U, Möller U, Brecht M, Wotzlaw C, Acker H, Jungermann K, and Kietzmann T. A Fenton reaction at the endoplasmic reticulum is involved in the redox control of hypoxia-inducible gene expression. Proc Natl Acad Sci USA 101: 4302-4307, 2004.
119. Liu W, Vives-Bauza C, Acin-Perez R, Yamamoto A, Tan Y, Li Y, Magrane J, Stavarache MA, Shaffer S, Chang S, Kaplitt MG, Huang XY, Beal MF, Manfredi G, and Li C. PINK1 defect causes mitochondrial dysfunction, proteasomal deficit and alpha-synuclein aggregation in cell culture models of Parkinson's disease. PLoS One 4: e4597, 2009.
120. Lu C, Song G, and Lin J-M. Reactive oxygen species and their chemiluminescence-detection methods. TrAC Trends Anal Chem 25: 985-995, 2006.
121. Ma N, Li Y, Ren HF, Xu HP, Li ZB, and Zhang X. Selenium-containing block copolymers and their oxidationresponsive aggregates. Polymer Chem 1: 1609-1614, 2010.
122. Ma N, Li Y, Xu HP, Wang ZQ, and Zhang X. Dual redox responsive assemblies formed from diselenide block copolymers. J Am Che Soc 132: 442-443, 2010.
123. Ma N, Xu HP, An LP, Li J, Sun ZW, and Zhang X. Radiation-sensitive diselenide block co-polymer micellar aggregates: toward the combination of radiotherapy and chemotherapy. Langmuir 27: 5874-5878, 2011.
124. Mahdi H, Fisher BA, Kallberg H, Plant D, Malmstrom V, Ronnelid J, Charles P, Ding B, Alfredsson L, Padyukov L, Symmons DP, Venables PJ, Klareskog L, and Lundberg K. Specific interaction between genotype, smoking and autoimmunity to citrullinated alpha-enolase in the etiology of rheumatoid arthritis. Nat Genet 41: 1319-1324, 2009.
125. Mahmoud EA, Sankaranarayanan J, Morachis JM, Kim G, and Almutairi A. Inflammation responsive logic gate nanoparticles for the delivery of proteins. Bioconj Chem 22: 1416-1421, 2011.
126. Malerba M, Ricciardolo F, Radaeli A, Torregiani C, Ceriani L, Mori E, Bontempelli M, Tantucci C, and Grassi V. Neutrophilic inflammation and IL-8 levels in induced sputum of alpha-1-antitrypsin PiMZ subjects. Thorax 61: 129-133, 2006.
127. Malinouski M, Zhou Y, Belousov VV, Hatfield DL, and Gladyshev VN. Hydrogen peroxide probes directed to different cellular compartments. PLoS One 6, 2011.
128. Martinez-Ruiz A and Lamas S. Signalling by NO-induced protein S-nitrosylation and S-glutathionylation: convergences and divergences. Cardiovasc Res 75: 220-228, 2007.
129. Mccord JM and Fridovic I. Superoxide dismutase an enzymic function for erythrocuprein (Hemocuprein). J Biol Chem 244: 6049-6055, 1969.
130. Meyer AJ, Brach T, Marty L, Kreye S, Rouhier N, Jacquot JP, and Hell R. Redox-sensitive GFP in Arabidopsis thaliana is a quantitative biosensor for the redox potential of the cellular glutathione redox buffer. Plant J 52: 973-986, 2007.
131. Michiko Sukenobu H, Horiike K, Tojo H, Katagiri M, and Yamano T. Kinetic properties of rat kidney d-amino acid oxidase associated with peroxisomes. Comp Biochem Physiol B Comp Biochem 80: 425-430, 1985.
132. Miller EW, Albers AE, Pralle A, Isacoff EY, and Chang CJ. Boronate-based fluorescent probes for imaging cellular hydrogen peroxide. J Am Chem Soc 127: 16652-16659, 2005.
133. Mills GC. Hemoglobin catabolism: I. glutathione peroxidase, an erythrocyte enzyme which protects hemoglobin from oxidative breakdown. J Biol Chem 229: 189-197, 1957.
134. Mohanty JG, Jaffe JS, Schulman ES, and Raible DG. A highly sensitive fluorescent micro-assay of H2O2 release from activated human leukocytes using a dihydroxyphenoxazine derivative. J Immunol Methods 202: 133-141, 1997.
135. Morgan EJ. The distribution of xanthine oxidase I. Biochem J 20: 1282-1291, 1926.
136. Moss DW and Bates TE. Activation of murine microglial cell lines by lipopolysaccharide and interferon-gamma causes NO-mediated decreases in mitochondrial and cellular function. Eur J Neurosci 13: 529-538, 2001.
137. Nadel JA. Role of neutrophil elastase in hypersecretion during COPD exacerbations, and proposed therapies. Chest 117: 386S-389S, 2000.
138. Nakahata M, Takashima Y, Yamaguchi H, and Harada A. Redox-responsive self-healing materials formed from host-guest polymers. Nat Comm 2, 2011.
139. Napoli A, Valentini M, Tirelli N, Muller M, and Hubbell JA. Oxidation-responsive polymeric vesicles. Nat Mat 3: 183-189, 2004.
140. Nathan C and Shiloh MU. Reactive oxygen and nitrogen intermediates in the relationship between mammalian hosts and microbial pathogens. Proc Natl Acad Sci U S A 97: 8841-8848, 2000.
141. Ohashi T, Mizutani A, Murakami A, Kojo S, Ishii T, and Taketani S. Rapid oxidation of dichlorodihydrofluorescin with heme and hemoproteins: formation of the fluorescein is independent of the generation of reactive oxygen species. FEBS Lett 511: 21-27, 2002.
142. Ostergaard H, Henriksen A, Hansen FG, and Winther JR. Shedding light on disulfide bond formation: engineering a redox switch in green fluorescent protein. EMBO J 20: 5853-5862, 2001.
143. Oushiki D, Kojima H, Terai T, Arita M, Hanaoka K, Urano Y, and Nagano T. Development and application of a near-infrared fluorescence probe for oxidative stress based on differential reactivity of linked cyanine dyes. J Am Chem Soc 132: 2795-2801, 2010.
144. Owusu-Ansah E, Yavari A, and Banerjee U. A protocol for in vivo detection of reactive oxygen species. Protocol Exchange 2008. [Epub ahead of print]; DOI:10.1038/nprot.2008.23.
145. Page G, Lebecque S, and Miossec P. Anatomic localization of immature and mature dendritic cells in an ectopic lymphoid organ: correlation with selective chemokine expression in rheumatoid synovium. J Immunol 168: 5333-5341, 2002.
146. Palacino JJ, Sagi D, Goldberg MS, Krauss S, Motz C, Wacker M, Klose J, and Shen J. Mitochondrial dysfunction and oxidative damage in parkin-deficient mice. J Biol Chem 279: 18614-18622, 2004.
147. Parge HE, Hallewell RA, and Tainer JA. Atomic structures of wild-type and thermostable mutant recombinant human Cu,Zn superoxide-dismutase. Proc Natl Acad Sci U S A 89: 6109-6113, 1992.
148. Rajagopalan S, Meng XP, Ramasamy S, Harrison DG, and Galis ZS. Reactive oxygen species produced by macrophage-derived foam cells regulate the activity of vascular matrix metalloproteinases in vitro. Implications for atherosclerotic plaque stability. J Clin Invest 98: 2572-2579, 1996.
149. Rehor A, Hubbell JA, and Tirelli N. Oxidation-sensitive polymeric nanoparticles. Langmuir 21: 411-417, 2005.
150. Ren HF, Wu YT, Ma N, Xu HP, and Zhang X. Side-chain selenium-containing amphiphilic block copolymers: redoxcontrolled self-assembly and disassembly. Soft Matter 8: 1460-1466, 2012.
151. Robertson RP. Chronic oxidative stress as a central mechanism for glucose toxicity in pancreatic islet beta cells in diabetes. J Biol Chem 279: 42351-42354, 2004.
152. Rohnstock A and Lehmann L. Evaluation of the probe dihydrocalcein acetoxymethylester as an indicator of reactive oxygen species formation and comparison with oxidative DNA base modification determined by modified alkaline elution technique. Toxicol In Vitro 21: 1552-1562, 2007.
153. Rosen DR, Siddique T, Patterson D, Figlewicz DA, Sapp P, Hentati A, Donaldson D, Goto J, O'Regan JP, Deng HX, et al. Mutations in Cu/Zn superoxide dismutase gene are associated with familial amyotrophic lateral sclerosis. Nature 362: 59-62, 1993.
154. Royall JA and Ischiropoulos H. Evaluation of 2′,7′- dichlorofluorescin and dihydrorhodamine 123 as fluorescent probes for intracellular H2O2 in cultured endothelial cells. Arch Biochem Biophys 302: 348-355, 1993.
155. Saetta M, Baraldo S, Corbino L, Turato G, Braccioni F, Rea F, Cavallesco G, Tropeano G, Mapp CE, Maestrelli P, Ciaccia A, and Fabbri LM. CD8 + ve cells in the lungs of smokers with chronic obstructive pulmonary disease. Am J Respir Crit Care Med 160: 711-717, 1999.
156. Schirmer RH, Schulz GE, and Untuchtgrau R. On the geometry of leukocyte nadph-oxidase, a membrane flavoenzyme-inferences from the structure of glutathione-reductase. FEBS Lett 154: 1-4, 1983.
157. Schrijvers DM, De Meyer GR, Kockx MM, Herman AG, and Martinet W. Phagocytosis of apoptotic cells by macrophages is impaired in atherosclerosis. Arterioscler Thromb Vasc Biol 25: 1256-1261, 2005.
158. Seifried HE, Anderson DE, Fisher EI, and Milner JA. A review of the interaction among dietary antioxidants and reactive oxygen species. J Nutr Biochem 18: 567-579, 2007.
159. Seimon TA, Nadolski MJ, Liao X, Magallon J, Nguyen M, Feric NT, Koschinsky ML, Harkewicz R, Witztum JL, Tsimikas S, Golenbock D, Moore KJ, and Tabas I. Atherogenic lipids and lipoproteins trigger CD36-TLR2-dependent apoptosis in macrophages undergoing endoplasmic reticulum stress. Cell Metab 12: 467-482, 2010.
160. Sem X and Rhen M. Pathogenicity of Salmonella enterica in Caenorhabditis elegans relies on disseminated oxidative stress in the infected host. PLoS One 7: e45417, 2012.
161. Shigenaga MK, Hagen TM, and Ames BN. Oxidative damage and mitochondrial decay in aging. Proc Natl Acad Sci U S A 91: 10771-10778, 1994.
162. Shim MS and Xia Y. A reactive oxygen species (ROS)-responsive polymer for safe, efficient, and targeted gene delivery in cancer cells. Angew Chem Int Ed Engl 52: 6926-6929, 2013.
163. Simonson SG, Zhang J, Canada AT, Jr., Su YF, Benveniste H, and Piantadosi CA. Hydrogen peroxide production by monoamine oxidase during ischemia-reperfusion in the rat brain. J Cereb Blood Flow Metab 13: 125-134, 1993.
164. Slot JW, Geuze HJ, Freeman BA, and Crapo JD. Intracellular localization of the copper-zinc and manganese superoxide dismutases in rat liver parenchymal cells. Lab Invest 55: 363-371, 1986.
165. Snir O, Widhe M, von Spee C, Lindberg J, Padyukov L, Lundberg K, Engstrom A, Venables PJ, Lundeberg J, Holmdahl R, Klareskog L, and Malmstrom V. Multiple antibody reactivities to citrullinated antigens in sera from patients with rheumatoid arthritis: association with HLADRB1 alleles. Ann Rheum Dis 68: 736-743, 2009.
166. Stadtman ER and Levine RL. Free radical-mediated oxidation of free amino acids and amino acid residues in proteins. Amino Acids 25: 207-218, 2003.
167. Staff RH, Gallei M, Mazurowski M, Rehahn M, Berger R, Landfester K, and Crespy D. Patchy nanocapsules of poly(vinylferrocene)-based block copolymers for redoxresponsive release. ACS Nano 6: 9042-9049, 2012.
168. Starkov AA, Fiskum G, Chinopoulos C, Lorenzo BJ, Browne SE, Patel MS, and Beal MF. Mitochondrial alphaketoglutarate dehydrogenase complex generates reactive oxygen species. J Neurosci 24: 7779-7788, 2004.
169. Stolz DB, Zamora R, Vodovotz Y, Loughran PA, Billiar TR, Kim Y-M, Simmons RL, and Watkins SC. Perox-isomal localization of inducible nitric oxide synthase in hepatocytes. Hepatology 36: 81-93, 2002.
170. Stralin P, Karlsson K, Johansson BO, and Marklund SL. The interstitium of the human arterial wall contains very large amounts of extracellular superoxide dismutase. Arterioscler Thromb Vasc Biol 15: 2032-2036, 1995.
171. Szatrowski TP and Nathan CF. Production of Large Amounts of Hydrogen-Peroxide by Human Tumor-Cells. Cancer Res 51: 794-798, 1991.
172. Tabor CW, Tabor H, and Rosenthal SM. Purification of Amine Oxidase From Beef Plasma. J Biol Chem 208: 645-662, 1954.
173. Takahashi K, Avissar N, Whitin J, and Cohen H. Purification and characterization of human-plasma glutathione-peroxidase -a selenoglycoprotein distinct from the known cellular enzyme. Arch Biochem Biophys 256: 677-686, 1987.
174. Taylor RW and Turnbull DM. Mitochondrial DNA mutations in human disease. Nat Rev Genet 6: 389-402, 2005.
175. Tedgui A and Mallat Z. Cytokines in atherosclerosis: pathogenic and regulatory pathways. Physiol Rev 86: 515-581, 2006.
176. Teitelbaum SL. Bone resorption by osteoclasts. Science 289: 1504-1508, 2000.
177. Teoh ML, Fitzgerald MP, Oberley LW, and Domann FE. Overexpression of extracellular superoxide dismutase attenuates heparanase expression and inhibits breast carcinoma cell growth and invasion. Cancer Res 69: 6355-6363, 2009.
178. Test ST and Weiss SJ. Quantitative and temporal characterization of the extracellular H2O2 pool generated by human neutrophils. J Biol Chem 259: 399-405, 1984.
179. Thomas C, Mackey MM, Diaz AA, and Cox DP. Hydroxyl radical is produced via the Fenton reaction in submitochondrial particles under oxidative stress: implications for diseases associated with iron accumulation. Redox Report 14: 102-108, 2009.
180. Thomas DD, Ridnour LA, Isenberg JS, Flores-Santana W, Switzer CH, Donzelli S, Hussain P, Vecoli C, Paolocci N, Ambs S, Colton CA, Harris CC, Roberts DD, and Wink DA. The chemical biology of nitric oxide: implications in cellular signaling. Free Radic Biol Med 45: 18-31, 2008.
181. Turrens JF and Boveris A. Generation of superoxide anion by the NADH dehydrogenase of bovine heart mitochondria. Biochem J 191: 421-427, 1980.
182. Urao N and Ushio-Fukai M. Redox regulation of stem/ progenitor cells and bone marrow niche. Free Radic Biol Med 54: 26-39, 2013.
183. Uusitalo LM and Hempel N. Recent advances in intracellular and in vivo ROS sensing: focus on nanoparticle and nanotube applications. Int J Mol Sci 13: 10660-10679, 2012.
184. Vafa O, Wade M, Kern S, Beeche M, Pandita TK, Hampton GM, and Wahl GM. c-Myc can induce DNA damage, increase reactive oxygen species, and mitigate p53 function: a mechanism for oncogene-induced genetic instability. Mol Cell 9: 1031-1044, 2002.
185. Van de Bittner GC, Dubikovskaya EA, Bertozzi CR, and Chang CJ. In vivo imaging of hydrogen peroxide production in a murine tumor model with a chemoselective bioluminescent reporter. Proc Natl Acad Sci U S A, 107: 21316-21321, 2010.
186. van Lith M, Tiwari S, Pediani J, Milligan G, and Bulleid NJ. Real-time monitoring of redox changes in the mammalian endoplasmic reticulum. J Cell Sci 124: 2349-2356.
187. Van Remmen H, Ikeno Y, Hamilton M, Pahlavani M, Wolf N, Thorpe SR, Alderson NL, Baynes JW, Epstein CJ, Huang TT, Nelson J, Strong R, and Richardson A. Lifelong reduction in MnSOD activity results in increased DNA damage and higher incidence of cancer but does not accelerate aging. Physiol Genomics 16: 29-37, 2003.
188. Viger ML, Sankaranarayanan J, de Gracia Lux C, Chan M, and Almutairi A. Collective activation of MRI agents via encapsulation and disease-triggered release. J Am Chem Soc 135: 7847-7850, 2013.
189. Villela GG, Mitidieri E, and Affonso OR. Intracellular Distribution of Xanthine Oxidase in the Rat Liver. Nature 175: 1087-1087, 1955.
190. Vong LB, Tomita T, Yoshitomi T, Matsui H, and Nagasaki Y. An orally administered redox nanoparticle that accumulates in the colonic mucosa and reduces colitis in mice. Gastroenterology 143: 1027-1036 e3, 2012.
191. Votyakova TV and Reynolds IJ. Detection of hydrogen peroxide with Amplex Red: interference by NADH and reduced glutathione auto-oxidation. Arch Biochem Biophys 431: 138-144, 2004.
192. Wegner N, Wait R, Sroka A, Eick S, Nguyen KA, Lundberg K, Kinloch A, Culshaw S, Potempa J, and Venables PJ. Peptidylarginine deiminase from Porphyromonas gingivalis citrullinates human fibrinogen and alpha-enolase: implications for autoimmunity in rheumatoid arthritis. Arthritis Rheum 62: 2662-2672, 2010.
193. Weisiger RA and Fridovich I. Superoxide dismutase. Organelle specificity. J Biol Chem 248: 3582-3592, 1973.
194. Wheeler MD, Smutney OM, and Samulski RJ. Secretion of extracellular superoxide dismutase from muscle transduced with recombinant adenovirus inhibits the growth of B16 melanomas in mice. Mol Cancer Res 1: 871-881, 2003.
195. Williams KJ and Tabas I. The response-to-retention hypothesis of early atherogenesis. Arterioscler Thromb Vasc Biol 15: 551-561, 1995.
196. Wilson DS, Dalmasso G, Wang LX, Sitaraman SV, Merlin D, and Murthy N. Orally delivered thioketal nanoparticles loaded with TNF-alpha-siRNA target inflammation and inhibit gene expression in the intestines. Nat Mater 9: 923-928, 2010.
197. Wong A, Yang J, Cavadini P, Gellera C, Lonnerdal B, Taroni F, and Cortopassi G. The Friedreich's ataxia mutation confers cellular sensitivity to oxidant stress which is rescued by chelators of iron and calcium and inhibitors of apoptosis. Hum Mol Genet 8: 425-430, 1999.
198. Wu EC, Park JH, Park J, Segal E, Cunin F, and Sailor MJ. Oxidation-triggered release of fluorescent molecules or drugs from mesoporous Si microparticles. ACS Nano 2: 2401-2409, 2008.
199. Yamada H and Yasunobu KT. Monoamine oxidase -purification, crystallization, and properties of plasma monoamine oxidase. J Biol Chem 237: 1511-1516, 1962.
200. Yan Q, Yuan JY, Cai ZN, Xin Y, Kang Y, and Yin YW. Voltage-Responsive Vesicles Based on Orthogonal Assembly of Two Homopolymers. J Am Chem Soc 132: 9268-9270, 2010.
201. Yano T, Oku M, Akeyama N, Itoyama A, Yurimoto H, Kuge S, Fujiki Y, and Sakai Y. A novel fluorescent sensor protein for visualization of redox states in the cytoplasm and in peroxisomes. Mol Cell Biol 30: 3758-3766, 2010.
202. Yu SS, Koblin RL, Zachman AL, Perrien DS, Hofmeister LH, Giorgio TD, and Sung HJ. Physiologically relevant oxidative degradation of oligo(proline) cross-linked polymeric scaffolds. Biomacromolecules 12: 4357-4366, 2011.
203. Zhang J, Fitsanakis VA, Gu G, Jing D, Ao M, Amarnath V, and Montine TJ. Manganese ethylene-bis-dithiocarbamate and selective dopaminergic neurodegeneration in rat: a link through mitochondrial dysfunction. J Neurochem 84: 336-346, 2003.
204. Zhao H, Joseph J, Fales HM, Sokoloski EA, Levine RL, Vasquez-Vivar J, and Kalyanaraman B. Detection and characterization of the product of hydroethidine and intracellular superoxide by HPLC and limitations of fluorescence. Proc Natl Acad Sci U S A 102: 5727-5732, 2005.
205. ZhouMJ, Diwu ZJ, PanchukVoloshina N, and Haugland RP. A stable nonfluorescent derivative of resorufin for the fluorometric determination of trace hydrogen peroxide: applications in detecting the activity of phagocyte NADPH oxidase and other oxidases. Anal Biochem 253: 162-168, 1997.
206. Zhu MT, Nie GJ, Meng H, Xia T, Nel A, and Zhao YL. Physicochemical properties determine nanomaterial cellular uptake, transport, and fate. Acc Chem Res 46: 622-631, 2013.