Toll-Like Receptor 4-Mediated Nuclear Factor Kappa B Activation Is Essential for Sensing Exogenous Oxidants to Propagate and Maintain Oxidative/Nitrosative Cellular Stress

PLoS ONE

Volumn 8, Issue 9, 2013, Pages

  Karki, Rajendra ^a   Igwe, Orisa J ^a  

^a UNIVERSITY OF MISSOURI KANSAS CITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALKALINE PHOSPHATASE; EBSELEN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; INTERLEUKIN 1BETA; N TERT BUTYL ALPHA PHENYLNITRONE; OXIDIZING AGENT; PEROXYCHROMATE; SCAVENGER; TOLL LIKE RECEPTOR 2; TOLL LIKE RECEPTOR 4; TUMOR NECROSIS FACTOR ALPHA; UNCLASSIFIED DRUG; ANTIOXIDANT; CHROMIC ACID; EUK-134; ORGANOMETALLIC COMPOUND; PEROXIDE; POTASSIUM TETRAPEROXOCHROMATE; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN METABOLITE; SALICYLIC ACID DERIVATIVE; TLR2 PROTEIN, MOUSE; TLR4 PROTEIN, MOUSE;

ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DRUG EFFICACY; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; ENZYME RELEASE; FACE PAIN; GENETIC TRANSFECTION; HUMAN; HUMAN CELL; IN VITRO STUDY; IN VIVO STUDY; INFLAMMATORY PAIN; MALE; MOUSE; NITROSATIVE STRESS; NONHUMAN; OXIDATIVE STRESS; OXYGEN SENSING; PHAGOCYTE; PROTEIN EXPRESSION; REPORTER GENE; SIGNAL TRANSDUCTION; TISSUE LEVEL; TREATMENT RESPONSE; ANIMAL; ANTAGONISTS AND INHIBITORS; CELL ENGINEERING; CELL SURVIVAL; DRUG EFFECTS; GENE EXPRESSION REGULATION; GENETICS; HEK293 CELL LINE; METABOLISM; PAIN; PAIN THRESHOLD; PATHOPHYSIOLOGY; SECRETION (PROCESS);

ALKALINE PHOSPHATASE; ANIMALS; ANTIOXIDANTS; CELL ENGINEERING; CELL SURVIVAL; CHROMATES; GENE EXPRESSION REGULATION; HEK293 CELLS; HUMANS; INTERLEUKIN-1BETA; MALE; MICE; NF-KAPPA B; ORGANOMETALLIC COMPOUNDS; OXIDANTS; OXIDATIVE STRESS; PAIN; PAIN THRESHOLD; PEROXIDES; REACTIVE NITROGEN SPECIES; REACTIVE OXYGEN SPECIES; SALICYLATES; SIGNAL TRANSDUCTION; TOLL-LIKE RECEPTOR 2; TOLL-LIKE RECEPTOR 4;

EID: 84884241348     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0073840     Document Type: Article

References (86)

1. Halliwell B, Cross CE, (1994) Oxygen-derived species: their relation to human disease and environmental stress. Environ Health Perspect 102Suppl 10: 5-12.
2. Droge W, (2002) Free radicals in the physiological control of cell function. Physiol. Rev. 82: 47-95.
3. Adler V, Yin Z, Tew KD, Ronai Z, (1999) Role of redox potential and reactive oxygen species in stress signaling. Oncogene 18(45): 6104-6111.
4. Tzortzaki EG, Dimakou K, Neofytou E, Tsikritsaki K, Samara K, et al. (2012) Oxidative DNA damage and somatic mutations: a link to the molecular pathogenesis of chronic inflammatory airway diseases.Chest. 141: 1243-1250.
5. Suzuki YJ, Forman HJ, Sevanian A, (1997) Oxidants as stimulators of signal transduction. Free Radic Biol Med 22 (1-2): 269-285.
6. Gill R, Tsung A, Billiar T, (2010) Linking oxidative stress to inflammation: Toll-like receptors. Free Radic Biol Med 48(9): 1121-1132.
7. Uttara B, Singh AV, Zamboni P, Mahajan RT, (2009) Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options. Curr Neuropharmacol 7: 65-74.
8. Pham-Huy LA, He H, Pham-Huy CP, (2008) Free radicals, antioxidants in disease and health. Int J Biomed Sci 4: 89-96.
9. Dalle-Donne I, Rossi R, Colombo R, Giustarini D, Milzani A, (2006) Biomarkers of oxidative damage in human disease. Clin Chem 52(4): 601-623.
10. Little JW, Doyle T, Salvemini D, (2012) Reactive nitroxidative species and nociceptive processing: determining the roles for nitric oxide, superoxide, and peroxynitrite in pain. Amino Acids 42(1): 75-94.
11. Meyer M, Schreck R, Baeuerle PA, (1993) H2O2 and antioxidants have opposite effects on activation of NF-kappa B and AP-1 in intact cells: AP-1 as secondary antioxidant-responsive factor. EMBO J 12: 2005-2015.
12. Li N, Karin M, (1999) Is NF-kappaB the sensor of oxidative stress? FASEB J 13: 1137-1143.
13. Akira S, Uematsu S, Takeuchi O, (2006) Pathogen recognition and innate immunity. Cell 124: 783-801.
14. Rifkin IR, Leadbetter EA, Busconi L, Viglianti G, Marshak-Rothstein A, (2005) Toll-like receptors, endogenous ligands, and systemic autoimmune disease. Immunol Rev 204: 27-42.
15. Lee H, Lee S, Cho IH, Lee SJ, (2013) Toll-like receptors: sensor molecules for detecting damage to the nervous system. Curr Protein Pept Sci. 14(1): 33-42.
16. McGettrick AF, O'Neill LA, (2004) The expanding family of MyD88-like adaptors in Toll-like receptor signal transduction. Mol Immunol 41(6-7): 577-582.
17. Brown J, Wang H, Hajishengallis GN, Martin M, (2011) TLR-signaling networks: an integration of adaptor molecules, kinases, and cross-talk. J Dent Res 90: 417-427.
18. Hawlisch H, Köhl J, (2006) Complement and Toll-like receptors: key regulators of adaptive immune responses. Mol Immunol 43(1-2): 13-21.
19. Kopp EB, Medzhitov R, (1999) The Toll-receptor family and control of innate immunity. Curr Opin Immunol 11(1): 13-18.
20. O'Neill LA, (2003) Therapeutic targeting of Toll-like receptors for inflammatory and infectious diseases. Curr Opin Pharmacol 3: 396-403.
21. Nicotra L, Loram LC, Watkins LR, Hutchinson MR, (2012) Toll-like receptors in chronic pain Exp Neurol. 234(2): 316-329.
22. Tanga FY, Nutile-McMenemy N, DeLeo JA, (2005) The CNS role of Toll-like receptor 4 in innate neuroimmunity and painful neuropathy. Proc Natl Acad Sci USA 102(16): 5856-5861.
23. Wu FX, Bian JJ, Miao XR, Huang SD, Xu XW, et al. (2010) Intrathecal siRNA against Toll-like receptor 4 reduces nociception in a rat model of neuropathic pain. Int J Med Sci 7(5): 251-259.
24. Benoliel R, Sharav Y, (2010) Chronic orofacial pain. Curr Pain Headache Rep 14(1): 33-40.
25. Graff-Radford SB, (2009) Facial pain. Neurologist 15(4): 171-177.
26. Diogenes A, Ferraz CC, Akopian AN, Henry MA, Hargreaves KM, (2011) LPS sensitizes TRPV1 via activation of TLR4 in trigeminal sensory neurons. J Dent Res 90(6): 759-764.
27. Miesel R, Kroger H, Kurpisz M, Weser U, (1995) Induction of arthritis in mice and rats by potassium peroxochromate and assessment of disease activity by whole blood chemiluminescence and 99mpertechnetate-imaging. Free Radic Res 23: 213-227.
28. Miesel R, Weser U, (1989) Reactivity of active center analogues of Cu2Zn2 superoxide dismutase during aqueous decay of K3CrO8. Inorg Chim Acta 160: 119-121.
29. Rong Y, Doctrow SR, Tocco G, Baudry M, (1999) EUK-134, a synthetic superoxide dismutase and catalase mimetic, prevents oxidative stress and attenuates kainate-induced neuropathology. Proc Natl Acad Sci USA 96(17): 9897-9902.
30. Imbe H, Iwata K, Zhou QQ, Zou S, Dubner R, et al. (2001) Orofacial deep and cutaneous tissue inflammation and trigeminal neuronal activation. Implications for persistent temporomandibular pain. Cells Tissues Organs 169: 238-247.
31. Miyamoto M, Tsuboi Y, Takamiya K, Huganir RL, Kondo M, et al. (2011) Involvement of GluR2 and GluR3 subunit C-termini in the trigeminal spinal subnucleus caudalis and C1-C2 neurons in trigeminal neuropathic pain. Neurosci Lett 491(1): 8-12.
32. Wegner HE, Knispel HH, Meier T, Klän R, Miller K, (1995) Nitric oxide donor, linsidomine chloride (SIN-1), in the diagnosis and treatment of erectile dysfunction: critical appraisal and review of the literature. Int Urol Nephrol 27(5): 621-628.
33. Edwards JC, Quinn PJ, (1982) Decomposing potassium peroxychromate produces hydroxyl radical (.OH) that can peroxidize the unsaturated fatty acids of phospholipid dispersions. J Lipid Res 23 (7): 994-1000.
34. Baird MB, Massie HR, Piekielniak MJ, (1977) Formation of lipid peroxides in isolated rat liver microsomes by singlet molecular oxygen. Chem Biol Interact 16 (2): 145-153.
35. Hodgson EK, Fridovich I, (1974) The production of superoxide radical during decomposition of potassium peroxochromate (V). Biochemistry 13 (18): 3811-3815.
36. Miesel R, Ehrlich W, Wohlert H, Kurpisz M, Kröger H, (1995) The effects of interleukin-1 receptor antagonist on oxidant-induced arthritis in mice. Clin Exp Rheumatol 13(5): 595-601.
37. Miesel R, Haas R, (1993) Reactivity of an active center analog of Cu2Zn2superoxide dismutase in murine model of acute and chronic inflammation. Inflammation 17 (5): 595-611.
38. Lorne E, Zmijewski JW, Zhao X, Liu G, Tsuruta Y, et al. (2008) Role of extracellular superoxide in neutrophil activation: interactions between xanthine oxidase and TLR4 induce proinflammatory cytokine production. Am J Physiol Cell Physiol 294 (4): 985-993.
39. Beckman JS, Koppenol WH, (1996) Nitric oxide, superoxide, and peroxynitrite: the good, the bad, and ugly. Am J Physiol 271(5 Pt 1): C1424-C1437.
40. Afanas'ev IB, (2007) Signaling functions of free radicals superoxide & nitric oxide under physiological & pathological conditions. Mol Biotechnol 37(1): 2-4.
41. Szabo C, Ischiropoulos H, Radi R, (2007) Peroxynitrite: biochemistry, pathophysiology and development of therapeutics. Nat Rev Drug Discov 6: 662-680.
42. Pacher P, Beckman JS, Liaudet L, (2007) Nitric oxide and peroxynitrite in health and disease. Physiol Rev 87(1): 315-424.
43. Altug S, Uludag O, Tunctan B, Cakici I, Zengil H, et al. (2006) Biological time-dependent difference in effect of peroxynitrite demonstrated by the mouse hot plate pain model. Chronobiol Int 23 (3): 583-591.
44. Khattab MM, (2006) TEMPOL, a membrane-permeable radical scavenger, attenuates peroxynitrite- and superoxide anion-enhanced carrageenan-induced paw edema and hyperalgesia: a key role for superoxide anion. Eur J Pharmacol 548 (1-3): 167-173.
45. Salvemini D, Doyle TM, Cuzzocrea S, (2006) Superoxide, peroxynitrite and oxidative/nitrative stress in inflammation. Biochem Soc Trans 34 (Pt 5): 965-970.
46. Dedon PC, Tannenbaum SR, (2004) Reactive nitrogen species in the chemical biology of inflammation. Arch Biochem Biophys 423 (1): 12-22.
47. Beal MF, (2002) Oxidatively modified proteins in aging and disease. Free Radic Biol Med 32 (9): 797-803.
48. Drew B, Leeuwenburgh C, (2002) Aging and the role of reactive nitrogen species. Ann N Y Acad Sci 959: 66-81.
49. Cuddy LK, Gordon AC, Black SA, Jaworski E, Ferguson SS, et al. (2012) Peroxynitrite donor SIN-1 alters high-affinity choline transporter activity by modifying its intracellular trafficking. J Neurosci 32(16): 5573-5584.
50. Qureshi N, Jarvis BW, Takayama K (1999) Nontoxic RsDPLA as a potent antagonist of toxic lipopolysaccharide. In: Brade H, Opal SM, Vogel SN, Morrison DC, editors. Endotoxin in Health and Disease. New York: Marcel Dekker. 687-698.
51. Coats SR, Pham TT, Bainbridge BW, Reife RA, Darveau RP, (2005) MD-2 mediates the ability of tetra-acylated and penta-acylated lipopolysaccharides to antagonize Escherichia coli lipopolysaccharide at the TLR4 signaling complex. J Immunol 175: 4490-4498.
52. Saitoh S, Akashi S, Yamada T, Tanimura N, Kobayashi M, et al. (2004) MD-2 mediates the ability of tetra-acylated and penta-acylated lipopolysaccharides to antagonize Escherichia coli lipopolysaccharide at the TLR4 signaling complex. Int Immunol 16: 961-969.
53. Park BS, Song DH, Kim HM, Choi BS, Lee H, et al. (2009) The structural basis of lipopolysaccharide recognition by the TLR4-MD-2 complex. Nature 458(7242): 1191-1195.
54. Jin MS, Lee JO, (2008) Structures of the toll-like receptor family and its ligand complexes. Immunity 29(2): 182-191.
55. Horng T, Barton GM, Medzhitov R, (2001) TIRAP: an adapter molecule in the Toll signaling pathway. Nat Immunol 2(9): 835-841.
56. Horng T, Barton GM, Flavell RA, Medzhitov R, (2002) The adaptor molecule TIRAP provides signalling specificity for Toll-like receptors. Nature 420: 329-333.
57. Sha T, Sunamoto M, Kitazaki T, Sato J, Ii M, et al. (2007) Therapeutic effects of TAK-242, a novel selective Toll-like receptor 4 signal transduction inhibitor, in mouse endotoxin shock model. Eur J Pharmacol 571(2-3): 231-239.
58. Li M, Matsunaga N, Hazeki K, Nakamura K, Takashima K, et al. (2006) A novel cyclohexene derivative, ethyl (6R)-6-[N-(2-Chloro-4-fluorophenyl)sulfamoyl]cyclohex-1-ene-1-carboxylate (TAK-242), selectively inhibits toll-like receptor 4-mediated cytokine production through suppression of intracellular signaling. Mol Pharmacol 69(4): 1288-1295.
59. Matsunaga N, Tsuchimori N, Matsumoto T, Ii M, (2011) TAK-242 (resatorvid), a small-molecule inhibitor of Toll-like receptor (TLR) 4 signaling, binds selectively to TLR4 and interferes with interactions between TLR4 and its adaptor molecules. Mol Pharmacol 79(1): 34-41.
60. Pierce JW, Schoenleber R, Jesmok G, Best J, Moore SA, et al. (1997) Novel inhibitors of cytokine-induced IkappaB alpha phosphorylation and endothelial cell adhesion molecule expression show anti-inflammatory effects in vivo. J Biol Chem 272(34): 21096-21103.
61. Nakamura Y, Feng Q, Kumagai T, Torikai K, Ohigashi H, et al. (2002) Ebselen, a glutathione peroxidase mimetic seleno-organic compound, as a multifunctional antioxidant. Implication for inflammation-associated carcinogenesis. J Biol Chem 277(4): 2687-2694.
62. Lass A, Witting P, Stocker R, Esterbauer H, (1996) Inhibition of copper- and peroxyl radical-induced LDL lipid oxidation by ebselen: antioxidant actions in addition to hydroperoxide-reducing activity. Biochim Biophys Acta 1303(2): 111-118.
63. Parnham MJ, Leyck S, Graf E, Dowling EJ, Blake DR, (1991) The pharmacology of ebselen. Agents Actions 32(1-2): 4-9.
64. Hensley K, Carney JM, Stewart CA, Tabatabaie T, Pye Q, et al. (1997) Nitrons-based free radical traps as neuroprotective agents in cerebral ischaemia and other pathologies. Int Rev Neurobiol 40: 299-317.
65. Paul-Clark MJ, McMaster SK, Sorrentino R, Sriskandan S, Bailey LK, et al. (2009) Toll-like receptor 2 is essential for the sensing of oxidants during inflammation. Am J Respir Crit Care Med 179(4): 299-306.
66. Flohé L, Brigelius-Flohé R, Saliou C, Traber MG, Packer L, (1997) Redox regulation of NF-kappa B activation. Free Radic Biol Med 22(6): 1115-1126.
67. Meyer M, Pahl HL, Baeuerle PA, (1994) Regulation of the transcription factors NF-kappa B and AP-1 by redox changes. Chem Biol Interact 91(2-3): 91-100.
68. Fan J, Frey RS, Malik AB, (2003) TLR4 signaling induces TLR2 expression in endothelial cells via neutrophil NADPH oxidase. J Clin Invest 112: 1234-1243.
69. Xiang M, Fan J, Fan J (2010) Association of Toll-like receptor signaling and reactive oxygen species: a potential therapeutic target for posttrauma acute lung injury. Mediators Inflamm doi:pii: 916425. 10.1155/2010/916425.
70. Minard KI, McAlister-Henn L, (2010) Pnc1p supports increases in cellular NAD(H) levels in response to internal or external oxidative stress. Biochemistry 49: 6299-6301.
71. Frantz S, Kelly RA, Bourcier T, (2001) Role of TLR-2 in the activation of nuclear factor kappaB by oxidative stress in cardiac myocytes. J Biol Chem 276(7): 5197-5203.
72. Shoenfelt J, Mitkus RJ, Zeisler R, Spatz RO, Powell J, et al. (2009) Involvement of TLR2 and TLR4 in inflammatory immune responses induced by fine and coarse ambient air particulate matter. J Leukoc Biol 86(2): 303-312.
73. Milam SB, Zardeneta G, Schmitz JP, (1998) Oxidative stress and degenerative temporomandibular joint disease: a proposed hypothesis. J Oral Maxillofac Surg 56(2): 214-223.
74. Chen GY, Nuñez G, (2010) Sterile inflammation: sensing and reacting to damage. Nat Rev Immunol 10(12): 826-837.
75. Schalkwijk J, van den Berg WB, van de Putte LB, Joosten LA, (1987) An experimental model for hydrogen peroxide induced tissue damage: effect on cartilage and other articular tissues. Int J Tissue React 9(1): 39-43.
76. Atsü SS, Ayhan-Ardic F, (2006) Temporomandibular disorders seen in rheumatology practices: A review. Rheumatol Int 26(9): 781-787.
77. Saperstein S, Chen L, Oakes D, Pryhuber G, Finkelstein J, (2009) IL-1beta augments TNF-alpha-mediated inflammatory responses from lung epithelial cells. J Interferon Cytokine Res 29(5): 273-284.
78. Hakim AW, Dong XD, Svensson P, Kumar U, Cairns BE, (2009) TNFalpha mechanically sensitizes masseter muscle afferent fibers of male rats. J Neurophysiol 102(3): 1551-1559.
79. Kopp S, (2001) Neuroendocrine, immune, and local responses related to temporomandibular disorders. J Orofac Pain 15(1): 9-28.
80. Hamada Y, Kondoh T, Holmlund AB, Yamamoto M, Horie A, et al. (2006) Inflammatory cytokines correlated with clinical outcome of temporomandibular joint irrigation in patients with chronic closed lock. Oral Surg Oral Med Oral Pathol Oral Radiol Endod. 102(5): 596-601.
81. Ambalavanar R, Moutanni A, Dessem D, (2006) Inflammation of craniofacial muscle induces widespread mechanical allodynia. Neurosci Lett 399(3): 249-254.
82. Mitchell JA, Paul-Clark MJ, Clarke GW, McMaster SK, Cartwright N, (2007) Critical role of toll-like receptors and nucleotide oligomerisation domain in the regulation of health and disease. J Endocrinol 193(3): 323-330.
83. Paul-Clark MJ, Sorrentino R, Bailey LK, Sriskandan S, Mitchell JA, (2008) Gram-positive and Gram-negative bacteria synergize with oxidants to release CXCL8 from innate immune cells. Mol Med 14(5-6): 238-246.
84. Peri F, Piazza M, (2012) Therapeutic targeting of innate immunity with Toll-like receptor 4 (TLR4) antagonists. Biotechnol Adv 30(1): 251-260.
85. Ze-Jun J, Fei-Xiang W, Qing-Hai H, Jian-Min L, (2012) Toll-like Receptor 4: The Potential Therapeutic Target for Neuropathic Pain. Zhongguo Yi Xue Ke Xue Yuan Xue Bao 34(2): 168-173.
86. Bettoni I, Comelli F, Rossini C, Granucci F, Giagnoni G, et al. (2008) Glial TLR4 receptor as new target to treat neuropathic pain: efficacy of a new receptor antagonist in a model of peripheral nerve injury in mice. Glia 56(12): 1312-1319.