Sulforaphane Restores Cellular Glutathione Levels and Reduces Chronic Periodontitis Neutrophil Hyperactivity In Vitro

PLoS ONE

Volumn 8, Issue 6, 2013, Pages

  Dias, Irundika H K ^a   Chapple, Ian L C ^b   Milward, Mike ^b   Grant, Melissa M ^b   Hill, Eric ^a   Brown, James ^a   Griffiths, Helen R ^a  

^a ASTON UNIVERSITY   (United Kingdom)

^b UNIVERSITY OF BIRMINGHAM   (United Kingdom)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; GLUTATHIONE DISULFIDE; MESSENGER RNA; PHORBOL 13 ACETATE 12 MYRISTATE; REACTIVE OXYGEN METABOLITE; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE; SPHINGOMYELIN PHOSPHODIESTERASE; SULFORAPHANE; THIOL; TRANSCRIPTION FACTOR NRF2;

ADULT; ARTICLE; CELL DIFFERENTIATION; CELL STRAIN HL 60; CHRONIC PERIODONTITIS; CLINICAL ARTICLE; CONTROLLED STUDY; DNA BINDING; DRUG MECHANISM; ENZYME ACTIVITY; EX VIVO STUDY; FEMALE; HUMAN; HUMAN CELL; LEUKOCYTE DISORDER; LIPID RAFT; MALE; NEUTROPHIL HYPERACTIVITY; OXIDATION REDUCTION REACTION; OXIDATIVE STRESS; PROTEIN EXPRESSION; RESPIRATORY BURST; STIMULUS RESPONSE; UPREGULATION;

ADULT; CHRONIC DISEASE; FEMALE; GLUTATHIONE; HL-60 CELLS; HUMANS; ISOTHIOCYANATES; MALE; MIDDLE AGED; NADPH OXIDASE; NEUTROPHILS; NF-E2-RELATED FACTOR 2; PERIODONTITIS; RESPIRATORY BURST; TETRADECANOYLPHORBOL ACETATE;

EID: 84879479555     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0066407     Document Type: Article

References (51)

1. Tonetti MS, VanDyke TE, (2013) Cardiovascular disease and periodontal disease. Consensus report of the joint EFP/AAP Worhshop. J Clin Periodontol 40Ahead of print.
2. Chapple IL, Genco RJ, (2013) Diabetes and periodontal disease: Consensus report of the joint EFP/AAP Worhshop. J Clin Periodontol 40Ahead of print.
3. Chapple ILC, Matthews JB, (2007) The role of reactive oxygen and antioxidant species in periodontal tissue destruction. Periodontol 2000 43: 160-232. doi:10.1111/j.1600-0757.2006.00178.x. PubMed: 17214840.
4. Matthews JB, Wright HJ, Roberts A, Cooper PR, Chapple ILC, (2007) Hyperactivity and reactivity of peripheral blood neutrophils in chronic periodontitis. Clin Exp Immunol 147: 255-264. PubMed: 17223966.
5. Dias IH, Matthews JB, Chapple IL, Wright HJ, Dunston CR, et al. (2011) Activation of the neutrophil respiratory burst by plasma from periodontitis patients is mediated by pro-inflammatory cytokines. J Clin Periodontol 38: 1-7. doi:10.1111/j.1600-051X.2010.01692.x. PubMed: 20964702.
6. Dias IHK, Marshall L, Lambert PA, Chapple ILC, Matthews JB, et al. (2008) Gingipains from Porphyromonas gingivalis Increase the Chemotactic and Respiratory Burst-Priming Properties of the 77-Amino-Acid Interleukin-8 Variant. Infect Immun 76: 317-323. doi:10.1128/IAI.00618-07. PubMed: 18025101.
7. Grant MM, Brock GR, Matthews JB, Chapple IL, (2010) Crevicular fluid glutathione levels in periodontitis and the effect of non-surgical therapy. J Clin Periodontol 37: 17-23. doi:10.1111/j.1600-051X.2009.01504.x. PubMed: 19968740.
8. Griffiths H, (2000) Antioxidants and protein oxidation. Free Radic Res 33: 47-58.
9. Griffiths HR, (2005) ROS as signalling molecules in T cells--evidence for abnormal redox signalling in the autoimmune disease, rheumatoid arthritis. Redox Rep 10: 273-280. doi:10.1179/135100005X83680. PubMed: 16438798.
10. Hancock JT, (2008) The role of redox in signal transduction. Methods Mol Biol 476: 1-9. doi:10.1007/978-1-59745-129-1_1. PubMed: 19157005.
11. Schissel SL, Keesler GA, Schuchman EH, Williams KJ, Tabas I, (1998) The Cellular Trafficking and Zinc Dependence of Secretory and Lysosomal Sphingomyelinase, Two Products of the Acid Sphingomyelinase Gene. J Biol Chem 273: 18250-18259. doi:10.1074/jbc.273.29.18250. PubMed: 9660788.
12. Holopainen JM, Subramanian M, Kinnunen PKJ, (1998) Sphingomyelinase Induces Lipid Microdomain Formation in a Fluid Phosphatidylcholine/Sphingomyelin Membrane. Biochem 37: 17562-17570. doi:10.1021/bi980915e.
13. Grassmé H, Jendrossek V, Riehle A, Kurthy Gv, Berger J, et al. (2003) Host defense against Pseudomonas aeruginosa requires ceramide-rich membrane rafts. Nat Med 9: 322-330. doi:10.1038/nm823. PubMed: 12563314.
14. Li P, Zhang Y, Yi F, (2007) Lipid Raft Rodox Signaling Platforms in Endothelial Dysfunction. Antiox Redox 9: 1457-1470. doi:10.1089/ars.2007.1667.
15. Shao D, Segal AW, Dekker LV, (2003) Lipid rafts determine eficiency of NADPH oxidase activation in neutrophils. FEBS Lett 550: 101-106. doi:10.1016/S0014-5793(03)00845-7. PubMed: 12935894.
16. David A, Fridlich R, Aviram I, (2005) The presence of membrane Proteinase 3 in neutrophil lipid rafts and its colocalization with FcgRIIIb and cytochrome b558. Exp Cell Res 308: 156-165. doi:10.1016/j.yexcr.2005.03.034. PubMed: 15916759.
17. Vilhardt F, Deurs Bv, (2004) The phagocyte NADPH oxidase depends on cholesterol-enriched membrane microdomains for assembly. EMBO J 23: 739-748. doi:10.1038/sj.emboj.7600066. PubMed: 14765128.
18. Guichard C, Pedruzzi E, Dewas C, Fay M, Pouzet C, et al. (2005) Interleukin-8-induced Priming of Neutrophil Oxidative Burst Requires Sequential Recruitment of NADPH Oxidase Components into Lipid Rafts. J Biol Chem 280: 37021-37032. doi:10.1074/jbc.M506594200. PubMed: 16115878.
19. Panjamurthy K, Manoharan S, CR R (2005) Lipid peroxidation and antioxidant status in patients with periodontitis. Cell Mol Biol Lett 10: 255-264.
20. Allen EM, Matthews JB, O' Halloran DJ, Griffiths HR, Chapple IL, (2011) Oxidative and inflammatory status in type-2 diabetes patients with periodontitis. J Clin Periodontol 38: 894-901. doi:10.1111/j.1600-051X.2011.01764.x. PubMed: 21883360.
21. Go YM, Jones DP, (2010) Redox clamp model for study of extracellular thiols and disulfides in redox signaling. Methods Enzymol 474: 165-179. doi:10.1016/S0076-6879(10)74010-6. PubMed: 20609910.
22. Phillips DC, Dias HK, Kitas GD, Griffiths HR, (2010) Aberrant reactive oxygen and nitrogen species generation in rheumatoid arthritis (RA): causes and consequences for immune function, cell survival, and therapeutic intervention. Antioxid Redox Signal. Antioxid Redox Signal 12: 743-785. doi:10.1089/ars.2009.2607. PubMed: 19686039.
23. Jaiswal A, (2004) Nrf2 signaling in coordinated activation of antioxidant gene expression FRBM 36: 1199-1207.
24. Zhang DD, Hannink M, (2003) Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. Mol Cell Biol 23: 8137-8151. doi:10.1128/MCB.23.22.8137-8151.2003. PubMed: 14585973.
25. Taguchi K, Fujikawa N, Komatsu M, Ishii T, Unno M, et al. (2012) Keap1 degradation by autophagy for the maintenance of redox homeostasis. PNAS 109: 13561-13566. doi:10.1073/pnas.1121572109. PubMed: 22872865.
26. Myzak MC, Karplus PA, Chung F-L, Dashwood RH, (2004) A Novel Mechanism of Chemoprotection by Sulforaphane: Inhibition of Histone Deacetylase. Cancer Res 64: 5767-5774. doi:10.1158/0008-5472.CAN-04-1326. PubMed: 15313918.
27. Starrett W, Blake DJ, (2011) Sulforaphane inhibits de novo synthesis of IL-8 and MCP-1 in human epithelial cells generated by cigarette smoke extract. J Immunotoxicol 8: 150-158. doi:10.3109/1547691X.2011.558529. PubMed: 21401388.
28. Sun X, Mi L, Liu J, Song L, Chung FL, et al. (2011) Sulforaphane prevents microcystin-LR-induced oxidative damage and apoptosis in BALB/c mice Toxicol Appl Pharmacol 255: 9-17. doi:10.1016/j.taap.2011.05.011. PubMed: 21684301.
29. Kong X, Thimmulappa R, Craciun F, Harvey C, Singh A, et al. (2011) Enhancing Nrf2 pathway by disruption of Keap1 in myeloid leukocytes protects against sepsis. Am J Respir Crit Care Med 184: 928-938. doi:10.1164/rccm.201102-0271OC. PubMed: 21799073.
30. Chapple ILC, Milward MR, Ling-Mountford N, Weston P, Carter K, et al. (2012) Adjunctive daily supplementation with encapsulated fruit, vegetable and berry juice powder concentrates and clinical periodontal outcomes: a double blind RCT. J Clin Periodontol 39: 62-72. doi:10.1111/j.1600-051X.2011.01793.x. PubMed: 22093005.
31. Gherghel D, Griffiths HR, Hilton EJ, Cunliffe IA, Hosking SL, (2005) Systemic Reduction in Glutathione Levels Occurs in Patients with Primary Open-Angle Glaucoma. Invest Ophthalmol Vis Sci 46: 877-883. doi:10.1167/iovs.04-0777. PubMed: 15728543.
32. Soeda S, Tsuji Y, Ochiai T, Mishima K, Iwasaki K, et al. (2004) Inhibition of sphingomyelinase activity helps to prevent neuron death caused by ischemic stress. Neurochem Int 45: 619-626. doi:10.1016/j.neuint.2004.04.001. PubMed: 15234103.
33. McMahon M, Itoh K, Yamamoto M, Hayes JD, (2003) Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression. J Biol Chem 278: 21592-21600. doi:10.1074/jbc.M300931200. PubMed: 12682069.
34. Hancock JT, Desikan R, Neill SJ, (2003) Cytochrome c, Glutathione, and the Possible Role of Redox Potentials in Apoptosis. Ann N Y Acad Sci 1010: 446-448. doi:10.1196/annals.1299.081. PubMed: 15033768.
35. Kemp M, Go Y-M, Jones DP, (2008) Non-equilibrium thermodynamics of thiol/disulfide redox systems: A perspective on redox systems biology. Free Radic Biol Med 44: 921-937. doi:10.1016/j.freeradbiomed.2007.11.008. PubMed: 18155672.
36. Samiec PS, Drews-Botsch C, Flagg EW, Kurtz JC, Sternberg PJ, et al. (1998) Glutathione in human plasma: decline in association with aging, age-related macular degeneration, and diabetes. Free Radic Biol Med 24: 699-704. doi:10.1016/S0891-5849(97)00286-4. PubMed: 9586798.
37. Hansen JM, Watson WH, Jones DP, (2004) Compartmentation of Nrf-2 Redox Control: Regulation of Cytoplasmic Activation by Glutathione and DNA Binding by Thioredoxin-1. Toxicol Sci 82: 308-317. doi:10.1093/toxsci/kfh231. PubMed: 15282410.
38. Seçkin S, Alptekin N, Doǧru-Abbasoǧlu S, Koçak-Toker N, Toker G, et al. (1997) The effect of chronic stress on heptic and gastric lipid peroxidation in long-term depletion of glutathione in rats. Pharmacol Res 36: 55-57. doi:10.1006/phrs.1997.0204. PubMed: 9368915.
39. Jacob C, Leport M, Szilagyi C, Allen JM, Bertrand C, et al. (2002) DMSO-treated HL60 cells: a model of neutrophil-like cells mainly expressing PDE4B subtype. Int Immunopharmacol 2: 1647-1656. doi:10.1016/S1567-5769(02)00141-8. PubMed: 12469939.
40. Hauert AB, Martinelli S, Marone C, Niggli V, (2002) Differentiated HL-60 cells are a valid model system for the analysis of human neutrophil migration and chemotaxis. Int J Biochem Cell Biol 34: 838-854. doi:10.1016/S1357-2725(02)00010-9. PubMed: 11950599.
41. Guerra BA, Bolin AP, Morandi AC, Otton R, (2012) Glycolaldehyde impairs neutrophil biochemical parameters by an oxidative and calcium-dependent mechanism-Protective role of antioxidants astaxanthin and vitamin C. Diabetes Res Clin Practice 98: 108-118. doi:10.1016/j.diabres.2012.07.004.
42. Yeligar SM, Machida K, Kalra VK, (2010) Ethanol-induced HO-1 and NQO1 are differentially regulated by HIF-1alpha and Nrf2 to attenuate inflammatory cytokine expression. J Biol Chem 285: 35359-35373. doi:10.1074/jbc.M110.138636. PubMed: 20833713.
43. Fitzpatrick AM, Stephenson ST, Hadley GR, Burwell L, Penugonda M, et al. (2011) Thiol redox disturbances in children with severe asthma are associated with posttranslational modification of the transcription factor nuclear factor (erythroid-derived 2)-like 2. J Allergy Clin Immunol 127: 1604-1611. doi:10.1016/j.jaci.2011.03.031. PubMed: 21514635.
44. Cui W, Bai Y, Miao X, Luo P, Chen Q, et al. (2012) Prevention of Diabetic Nephropathy by Sulforaphane: Possible Role of Nrf2 Upregulation and Activation. Oxidative Med Cell Longevity: 12: 821936. PubMed: 23050040.
45. Petri S, Korner S, Kiaei M, (2012) Nrf2/ARE Signaling Pathway: Key Mediator in Oxidative Stress and Potential Therapeutic Target in ALS. Neurology Research International 2012: 7.
46. Sun Z, Chin YE, DD Z (2009) Acetylation of Nrf2 by p300/CBP augments promoter-specific DNA binding of Nrf2 during the antioxidant response. Mol Cell Biol 29: 2658-2672.
47. Huang HC, Nguyen T, Pickett CB, (2002) Phosphorylation of Nrf2 at Ser-40 by protein kinase C regulates antioxidant response element-mediated transcription. J Biol Chem 277: 42769-42774. doi:10.1074/jbc.M206911200. PubMed: 12198130.
48. Chapple ILC, Brock G, Eftimiadi C, Matthews JB, (2002) Glutathione in gingival crevicular fluid and its relation to local antioxidant capacity in periodontal health and disease. J Clin Pathol Mol Pathol 55: 367-373. doi:10.1136/jcp.55.5.367. PubMed: 12456773.
49. Martín SF, Sawai H, Villalba JM, Hannun YA, (2007) Redox regulation of neutral sphingomyelinase-1 activity in HEK293 cells through a GSH-dependant mechanism. Arch Biochem Biophys 459: 295-300. doi:10.1016/j.abb.2006.11.007. PubMed: 17169322.
50. Evans WEIV, Coyer RL, Sandusky MF, Van Fleet MJ, Moore JG, et al. (2003) Characterization of Membrane Rafts Isolated From Rat Sertoli Cell Cultures: Caveolin and Flotillin-1 Content. J Androl 24: 812-821. PubMed: 14581507.
51. Foster LJ, Hoog C,. Mann M (2003) Unbiased quantitative proteomics of lipid rafts reveals high specificity for signaling factors. Cell Biology 100: 5813-5818.