Sulforaphane decreases endothelial cell apoptosis in Fuchs endothelial corneal dystrophy: A novel treatment

Investigative Ophthalmology and Visual Science

Volumn 54, Issue 10, 2013, Pages 6724-6734

  Ziaei, Alireza ^a,b   Schmedt, Thore ^a   Chen, Yuming ^a   Jurkunas, Ula V ^a  

^a SCHEPENS EYE RESEARCH INSTITUTE   (United States)

^b BOSTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

Apoptosis; Corneal endothelial cells; Dj 1; Fuchs endothelial corneal dystrophy; Hmox 1; NQO1; Nrf2; Oxidative stress; Reactive oxygen species; Sulforaphane

Indexed keywords

BETA 2 MICROGLOBULIN; CARBON DIOXIDE; HEME OXYGENASE 1; PROTEIN P53; REACTIVE OXYGEN METABOLITE; SULFORAPHANE; TERT BUTYL HYDROPEROXIDE; TRANSCRIPTION FACTOR NRF2;

AGED; ANTIOXIDANT RESPONSIVE ELEMENT; APOPTOSIS; ARTICLE; CELL PROTECTION; CELL VIABILITY; CLINICAL ARTICLE; CONFOCAL MICROSCOPY; CONGENITAL CORNEA DYSTROPHY; CONTROLLED STUDY; CORNEA; CORNEA ENDOTHELIUM; DENSITOMETRY; EX VIVO STUDY; FEMALE; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOFLUORESCENCE TEST; IMMUNOHISTOCHEMISTRY; MALE; NICK END LABELING; OXIDATIVE STRESS; PRIORITY JOURNAL; REAL TIME POLYMERASE CHAIN REACTION; UPREGULATION; WESTERN BLOTTING;

APOPTOSIS; CORNEAL ENDOTHELIAL CELLS; DJ-1; FUCHS ENDOTHELIAL CORNEAL DYSTROPHY; HMOX-1; NQO1; NRF2; OXIDATIVE STRESS; REACTIVE OXYGEN SPECIES; SULFORAPHANE;

AGED; ANTICARCINOGENIC AGENTS; APOPTOSIS; BLOTTING, WESTERN; CELL LINE; CORNEAL TRANSPLANTATION; ENDOTHELIUM, CORNEAL; FEMALE; FUCHS' ENDOTHELIAL DYSTROPHY; HUMANS; IMMUNOHISTOCHEMISTRY; IN SITU NICK-END LABELING; ISOTHIOCYANATES; MALE; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; REAL-TIME POLYMERASE CHAIN REACTION; RNA; UP-REGULATION;

EID: 84885644985     PISSN: 01460404     EISSN: 15525783     Source Type: Journal    
DOI: 10.1167/iovs.13-12699     Document Type: Article

References (35)

1. Joyce NC. Proliferative capacity of the corneal endothelium. Prog Retin Eye Res. 2003;22:359-389.
2. Waring GO 3rd, Rodrigues MM, Laibson PR. Corneal dystrophies. II. Endothelial dystrophies. Surv Ophthalmol. 1978;23: 147-168.
3. Bergstrom P, Andersson HC, Gao Y et al. Repeated transient sulforaphane stimulation in astrocytes leads to prolonged Nrf2-mediated gene expression and protection from superoxideinduced damage. Neuropharmacology. 2011;60:343-353.
4. Jurkunas UV, Bitar MS, Funaki T, Azizi B. Evidence of oxidative stress in the pathogenesis of Fuchs endothelial corneal dystrophy. Am J Pathol. 2010;177:2278-2289.
5. McMahon M, Itoh K, Yamamoto M, Hayes JD. Keap1-dependent proteasomal degradation of transcription factor Nrf2 contributes to the negative regulation of antioxidant response element-driven gene expression. J Biol Chem. 2003; 278:21592-21600.
6. Itoh K, Chiba T, Takahashi S, et al. An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements. Biochem Biophys Res Commun. 1997;236:313-322.
7. Bitar MS, Liu C, Ziaei A, Chen Y, Schmedt T, Jurkunas UV. Decline in DJ-1 and decreased nuclear translocation of Nrf2 in Fuchs endothelial corneal dystrophy. Invest Ophthalmol Vis Sci. 2012;53:5806-5813.
8. Azizi B, Ziaei A, Fuchsluger T, Schmedt T, Chen Y, Jurkunas UV. p53-regulated increase in oxidative-stress-induced apoptosis in Fuchs endothelial corneal dystrophy: a native tissue model. Invest Ophthalmol Vis Sci. 2011;52:9291-9297.
9. Cook AL, Vitale AM, Ravishankar S, et al. NRF2 activation restores disease related metabolic deficiencies in olfactory neurosphere-derived cells from patients with sporadic Parkinson's disease. PLoS One. 2011;6:e21907.
10. Zheng H, Whitman SA, Wu W, et al. Therapeutic potential of Nrf2 activators in streptozotocin-induced diabetic nephropathy. Diabetes. 2011;60:3055-3066.
11. Evans PC. The influence of sulforaphane on vascular health and its relevance to nutritional approaches to prevent cardiovascular disease. Epma J. 2011;2:9-14.
12. de Haan JB. Nrf2 activators as attractive therapeutics for diabetic nephropathy. Diabetes. 2011;60:2683-2684.
13. Cui W, Bai Y, Luo P, Miao L, Cai L. Preventive and therapeutic effects of MG132 by activating Nrf2-ARE signaling pathway on IOVS j October 2013 j Vol. 54 j No. 10 j 6733 oxidative stress-induced cardiovascular and renal injury. Oxid Med Cell Longev. 2013;2013:306073.
14. Shapiro TA, Fahey JW, Wade KL, Stephenson KK, Talalay P. Human metabolism and excretion of cancer chemoprotective glucosinolates and isothiocyanates of cruciferous vegetables. Cancer Epidemiol Biomarkers Prev. 1998;7:1091-1100.
15. Dinkova-Kostova AT, Massiah MA, Bozak RE, Hicks RJ, Talalay P. Potency of Michael reaction acceptors as inducers of enzymes that protect against carcinogenesis depends on their reactivity with sulfhydryl groups. Proc Natl Acad Sci U S A. 2001;98: 3404-3409.
16. Keum YS, Yu S, Chang PP, et al. Mechanism of action of sulforaphane: inhibition of p38 mitogen-activated protein kinase isoforms contributing to the induction of antioxidant response element-mediated heme oxygenase-1 in human hepatoma HepG2 cells. Cancer Res. 2006;66:8804-8813.
17. Manandhar S, Cho JM, Kim JA, Kensler TW, Kwak MK. Induction of Nrf2-regulated genes by 3H-1, 2-dithiole-3-thione through the ERK signaling pathway in murine keratinocytes. Eur J Pharmacol. 2007;577:17-27.
18. Soriano FX, Leveille F, Papadia S, et al. Induction of sulfiredoxin expression and reduction of peroxiredoxin hyperoxidation by the neuroprotective Nrf2 activator 3H-1,2dithiole-3-thione. J Neurochem. 2008;107:533-543.
19. Higdon JV, Delage B, Williams DE, Dashwood RH. Cruciferous vegetables and human cancer risk: epidemiologic evidence and mechanistic basis. Pharmacol Res. 2007;55: 224-236.
20. Clarke JD, Dashwood RH, Ho E. Multi-targeted prevention of cancer by sulforaphane. Cancer Lett. 2008;269:291-304.
21. Cheung KL, Kong AN. Molecular targets of dietary phenethyl isothiocyanate and sulforaphane for cancer chemoprevention. Aaps J. 2010;12:87-97.
22. Zhu C, Joyce NC. Proliferative response of corneal endothelial cells from young and older donors. Invest Ophthalmol Vis Sci. 2004;45:1743-1751.
23. Friis MB, Friborg CR, Schneider L, et al. Cell shrinkage as a signal to apoptosis in NIH 3T3 fibroblasts. J Physiol. 2005;567:427-443.
24. Theodore M, Kawai Y, Yang J, et al. Multiple nuclear localization signals function in the nuclear import of the transcription factor Nrf2. J Biol Chem. 2008;283:8984-8994.
25. Lee JM, Shih AY, Murphy TH, Johnson JA. NF-E2-related factor-2 mediates neuroprotection against mitochondrial complex I inhibitors and increased concentrations of intracellular calcium in primary cortical neurons. J Biol Chem. 2003;278: 37948-37956.
26. Li J, Johnson D, Calkins M, Wright L, Svendsen C, Johnson J. Stabilization of Nrf2 by tBHQ confers protection against oxidative stress-induced cell death in human neural stem cells. Toxicol Sci. 2005;83:313-328.
27. Xue M, Qian Q, Adaikalakoteswari A, Rabbani N, Babaei-Jadidi R, Thornalley PJ. Activation of NF-E2-related factor-2 reverses biochemical dysfunction of endothelial cells induced by hyperglycemia linked to vascular disease. Diabetes. 2008;57: 2809-2817.
28. Gao X, Talalay P. Induction of phase 2 genes by sulforaphane protects retinal pigment epithelial cells against photooxidative damage. Proc Natl Acad Sci U S A. 2004;101:10446-10451.
29. del VCM, Reyes JM, Park CY, et al. Demonstration by redox fluorometry that sulforaphane protects retinal pigment epithelial cells against oxidative stress. Invest Ophthalmol Vis Sci. 2008;49:2606-2612.
30. Zhu H, Jia Z, Strobl JS, Ehrich M, Misra HP, Li Y. Potent induction of total cellular and mitochondrial antioxidants and phase 2 enzymes by cruciferous sulforaphane in rat aortic smooth muscle cells: cytoprotection against oxidative and electrophilic stress. Cardiovasc Toxicol. 2008;8:115-125.
31. Miller DM, Singh IN, Wang JA, Hall ED. Administration of the Nrf2-ARE activators sulforaphane and carnosic acid attenuates 4-hydroxy-2-nonenal-induced mitochondrial dysfunction ex vivo. Free Radic Biol Med. 2013;57:1-9.
32. Thimmulappa RK, Mai KH, Srisuma S, Kensler TW, Yamamoto M, Biswal S. Identification of Nrf2-regulated genes induced by the chemopreventive agent sulforaphane by oligonucleotide microarray. Cancer Res. 2002;62:5196-5203.
33. Kim HJ, Barajas B, Wang M, Nel AE. Nrf2 activation by sulforaphane restores the age-related decrease of T(H)1 immunity: role of dendritic cells. J Allergy Clin Immunol. 2008;121:1255-1261. e1257.
34. Vasseur S, Afzal S, Tomasini R, et al. Consequences of DJ-1 upregulation following p53 loss and cell transformation. Oncogene. 2012;31:664-670.
35. Jung KA, Kwak MK. The Nrf2 system as a potential target for the development of indirect antioxidants. Molecules. 2010;15: 7266-7291.