Nrf2 activators modulate oxidative stress responses and bioenergetic profiles of human retinal epithelial cells cultured in normal or high glucose conditions

Pharmacological Research

Volumn 99, Issue , 2015, Pages 296-307

  Foresti, Roberta ^a,b   Bucolo, Claudio ^c   Platania, Chiara Maria Bianca ^c   Drago, Filippo ^c   Dubois Randé, Jean Luc ^a,d   Motterlini, Roberto ^a,b  

^a FACULTÉ DE MÉDECINE   (France)

^b INSERM U955   (France)

^c UNIVERSITY OF CATANIA   (Italy)

^d HENRI MONDOR HOSPITAL   (France)

Author keywords

Glucose levels; Heme oxygenase; Mitochondria; Nrf2 activators; Oxygen consumption; Retinal diseases; Retinal pigment epithelial cells; Wound healing

Indexed keywords

ACETYLCYSTEINE; ADENOSINE TRIPHOSPHATE; ANTIOXIDANT; CARNOSOL; FUMARIC ACID DIMETHYL ESTER; GLUCOSE; GLUTATHIONE; HEME OXYGENASE; OXYGEN; REACTIVE OXYGEN METABOLITE; THIOL DERIVATIVE; TRANSCRIPTION FACTOR NRF2; ABIETANE DERIVATIVE; NFE2L2 PROTEIN, HUMAN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARPE 19 CELL LINE; ARTICLE; BIOENERGY; BIOSYNTHESIS; CELL FUNCTION; CELL LINE; CELL MIGRATION; CELL NUCLEUS; CELL RESPIRATION; CELL STRESS; CELL STRUCTURE; CHEMOSENSITIVITY; CONTROLLED STUDY; CORNEA EPITHELIUM; CORNEA INJURY; CULTURE MEDIUM; DIABETIC RETINOPATHY; DISORDERS OF CARBOHYDRATE METABOLISM; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DRUG MECHANISM; ENERGY YIELD; ENZYME ACTIVATION; ENZYME ACTIVITY; GLUTATHIONE METABOLISM; HUMAN; HUMAN CELL; HUMAN CELL CULTURE; HYPERGLYCEMIA; IN VITRO STUDY; IN VIVO STUDY; INTRACELLULAR TRANSPORT; MALE; MOUSE; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PRIORITY JOURNAL; PROTEIN TRANSPORT; RETINA PIGMENT CELL; TRANSCRIPTION INITIATION; WOUND CLOSURE; WOUND HEALING; ANIMAL; ENERGY METABOLISM; EPITHELIUM CELL; METABOLISM; MITOCHONDRION; PHYSIOLOGY; RAT; RETINA; SPRAGUE DAWLEY RAT;

ACETYLCYSTEINE; ANIMALS; ANTIOXIDANTS; CELL LINE; DITERPENES, ABIETANE; ENERGY METABOLISM; EPITHELIAL CELLS; GLUCOSE; HEME OXYGENASE (DECYCLIZING); HUMANS; MALE; MITOCHONDRIA; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; RATS; RATS, SPRAGUE-DAWLEY; REACTIVE OXYGEN SPECIES; RETINA;

EID: 84937960662     PISSN: 10436618     EISSN: 10961186     Source Type: Journal    
DOI: 10.1016/j.phrs.2015.07.006     Document Type: Article

References (34)

1. S.M. Plafker, G.B. O'Mealey, and L.I. Szweda Mechanisms for countering oxidative stress and damage in retinal pigment epithelium Int. Rev. Cell Mol. Biol. 298 2012 135 177
2. G.A. Lutty Effects of diabetes on the eye Invest. Ophthalmol. Vision Sci. 54 2013 ORSF81 ORSF87
3. K. Trudeau, A.J. Molina, and S. Roy High glucose induces mitochondrial morphology and metabolic changes in retinal pericytes Invest. Ophthalmol. Vision Sci. 52 2011 8657 8664
4. Y.H. Ahn, Y. Hwang, H. Liu, X.J. Wang, Y. Zhang, K.K. Stephenson, T.N. Boronina, R.N. Cole, A.T. Dinkova-Kostova, P. Talalay, and P.A. Cole Electrophilic tuning of the chemoprotective natural product sulforaphane Proc. Natl. Acad. Sci. U.S.A. 107 2010 9590 9595
5. X. Gao, and P. Talalay Induction of phase 2 genes by sulforaphane protects retinal pigment epithelial cells against photooxidative damage Proc. Natl. Acad. Sci. U.S.A. 101 2004 10446 10451
6. L. Wang, N. Kondo, M. Cano, K. Ebrahimi, T. Yoshida, B.P. Barnett, S. Biswal, and J.T. Handa Nrf2 signaling modulates cigarette smoke-induced complement activation in retinal pigmented epithelial cells Free Radic. Biol. Med. 70 2014 155 166
7. R. Motterlini, and R. Foresti Heme oxygenase-1 as a target for drug discovery Antioxid. Redox Signal. 20 2014 1810 1826
8. K. Patil, L. Bellner, G. Cullaro, K.H. Gotlinger, M.W. Dunn, and M.L. Schwartzman Heme oxygenase-1 induction attenuates corneal inflammation and accelerates wound healing after epithelial injury Invest. Ophthalmol. Vision Sci. 49 2008 3379 3386
9. J. Fan, G. Xu, T. Jiang, and Y. Qin Pharmacologic induction of heme oxygenase-1 plays a protective role in diabetic retinopathy in rats Invest. Ophthalmol. Vision Sci. 53 2012 6541 6556
10. R. Foresti, S.K. Bains, T.S. Pitchumony, L.E. de Castro Bras, F. Drago, J.L. Dubois-Rande, C. Bucolo, and R. Motterlini Small molecule activators of the Nrf2-HO-1 antioxidant axis modulate heme metabolism and inflammation in BV2 microglia cells Pharmacol. Res. 76 2013 132 148
11. B. Haas, S. Chrusciel, S. Fayad-Kobeissi, J.L. Dubois-Rande, F. Azuaje, J. Boczkowski, R. Motterlini, and R. Foresti Permanent culture of macrophages at physiological oxygen attenuates the antioxidant and immunomodulatory properties of dimethyl fumarate J. Cell Physiol. 230 2015 1128 1138
12. J.L. Wilson, S. Fayad Kobeissi, S. Oudir, B. Haas, B.W. Michel, J.L. Dubois-Rande, A. Ollivier, T. Martens, M. Rivard, R. Motterlini, and R. Foresti Design and synthesis of novel hybrid molecules that activate the transcription factor Nrf2 and simultaneously release carbon monoxide Chemistry 20 2014 14698 14704
13. H. Abuarqoub, R. Foresti, C.J. Green, and R. Motterlini Heme oxygenase-1 mediates the anti-inflammatory actions of 2'-hydroxychalcone in RAW 264. 7 murine macrophages Am. J. Physiol. Cell Physiol. 290 2006 C1092 C1099
14. E. Balogun, M. Hoque, P. Gong, E. Killeen, C.J. Green, R. Foresti, J. Alam, and R. Motterlini Curcumin activates the heme oxygenase-1 gene via regulation of Nrf2 and the antioxidant responsive element Biochem. J. 371 2003 887 895
15. C. Bucolo, G. Marrazzo, C.B. Platania, F. Drago, G.M. Leggio, and S. Salomone Fortified extract of red berry, Ginkgo biloba, and white willow bark in experimental early diabetic retinopathy J. Diabetes Res. 2013 2013 432695
16. C. Bucolo, G.M. Leggio, F. Drago, and S. Salomone Eriodictyol prevents early retinal and plasma abnormalities in streptozotocin-induced diabetic rats Biochem. Pharmacol. 84 2012 88 92
17. M.J.J. Vesely, D.J. Exon, J.E. Clark, R. Foresti, C.J. Green, and R. Motterlini Heme oxygenase-1 induction in skeletal muscle cells: hemin and sodium nitroprusside are regulators in vitro Am. J. Physiol. 275 1998 C1087 C1094
18. J.E. Clark, C.J. Green, and R. Motterlini Involvement of the heme oxygenase-carbon monoxide pathway in keratinocyte proliferation Biochem. Biophys. Res. Commun. 241 1997 215 220
19. J.E. Clark, R. Foresti, C.J. Green, and R. Motterlini Dynamics of haem oxygenase-1 expression and bilirubin production in cellular protection against oxidative stress Biochem. J. 348 2000 615 619
20. F. Seta, L. Bellner, R. Rezzani, R.F. Regan, M.W. Dunn, N.G. Abraham, K. Gronert, and M. Laniado-Schwartzman Heme oxygenase-2 is a critical determinant for execution of an acute inflammatory and reparative response Am. J. Pathol. 169 2006 1612 1623
21. K.M. Holmstrom, L. Baird, Y. Zhang, I. Hargreaves, A. Chalasani, J.M. Land, L. Stanyer, M. Yamamoto, A.T. Dinkova-Kostova, and A.Y. Abramov Nrf2 impacts cellular bioenergetics by controlling substrate availability for mitochondrial respiration Biol. Open 2 2013 761 770
22. J. Deshane, S. Chen, S. Caballero, A. Grochot-Przeczek, H. Was, C.S. Li, R. Lach, T.D. Hock, B. Chen, N. Hill-Kapturczak, G.P. Siegal, J. Dulak, A. Jozkowicz, M.B. Grant, and A. Agarwal Stromal cell-derived factor 1 promotes angiogenesis via a heme oxygenase 1-dependent mechanism J. Exp. Med. 204 2007 605 618
23. A. Halilovic, K.A. Patil, L. Bellner, G. Marrazzo, K. Castellano, G. Cullaro, M.W. Dunn, and M.L. Schwartzman Knockdown of heme oxygenase-2 impairs corneal epithelial cell wound healing J. Cell Physiol. 226 2011 1732 1740
24. L. Bellner, L. Martinelli, A. Halilovic, K. Patil, N. Puri, M.W. Dunn, R.F. Regan, and M.L. Schwartzman Heme oxygenase-2 deletion causes endothelial cell activation marked by oxidative stress, inflammation, and angiogenesis J. Pharmacol. Exp. Ther. 331 2009 925 932
25. R. Hayashi, N. Himori, K. Taguchi, Y. Ishikawa, K. Uesugi, M. Ito, T. Duncan, M. Tsujikawa, T. Nakazawa, M. Yamamoto, and K. Nishida The role of the Nrf2-mediated defense system in corneal epithelial wound healing Free Radic. Biol. Med. 61 2013 333 342
26. R.J. Fox, M. Kita, S.L. Cohan, L.J. Henson, J. Zambrano, R.H. Scannevin, J. O'Gorman, M. Novas, K.T. Dawson, and J.T. Phillips BG-12 (dimethyl fumarate): a review of mechanism of action, efficacy, and safety Curr. Med. Res. Opin. 30 2014 251 262
27. P.J. Altmeyer, U. Matthes, F. Pawlak, K. Hoffmann, P.J. Frosch, P. Ruppert, S.W. Wassilew, T. Horn, H.W. Kreysel, and G. Lutz Antipsoriatic effect of fumaric acid derivatives. Results of a multicenter double-blind study in 100 patients J. Am. Acad. Dermatol. 30 1994 977 981
28. T. Satoh, S.R. McKercher, and S.A. Lipton Nrf2/ARE-mediated antioxidant actions of pro-electrophilic drugs Free Radic. Biol. Med. 65 2013 645 657
29. X. Li, Y. Cai, Y.S. Wang, Y.Y. Shi, W. Hou, C.S. Xu, H.Y. Wang, Z. Ye, L.B. Yao, and J. Zhang Hyperglycaemia exacerbates choroidal neovascularisation in mice via the oxidative stress-induced activation of STAT3 signalling in RPE cells PLoS One 7 2012 e47600
30. A. Castilho, C.A. Aveleira, E.C. Leal, N.F. Simoes, C.R. Fernandes, R.I. Meirinhos, F.I. Baptista, and A.F. Ambrosio Heme oxygenase-1 protects retinal endothelial cells against high glucose- and oxidative/nitrosative stress-induced toxicity PLoS One 7 2012 e42428
31. K. Trudeau, A.J. Molina, W. Guo, and S. Roy High glucose disrupts mitochondrial morphology in retinal endothelial cells: implications for diabetic retinopathy Am. J. Pathol. 177 2010 447 455
32. J.M. Santos, M. Mishra, and R.A. Kowluru Posttranslational modification of mitochondrial transcription factor A in impaired mitochondria biogenesis: implications in diabetic retinopathy and metabolic memory phenomenon Exp. Eye Res. 121 2014 168 177
33. S. Roy, K. Trudeau, S. Roy, T. Tien, and K.F. Barrette Mitochondrial dysfunction and endoplasmic reticulum stress in diabetic retinopathy: mechanistic insights into high glucose-induced retinal cell death Curr. Clin. Pharmacol. 8 2013 278 284
34. Z. Chen, G. Liu, Y. Xiao, and P. Lu Adrenomedullin22-52 suppresses high-glucose-induced migration, proliferation, and tube formation of human retinal endothelial cells Mol. Vision 20 2014 259 269