Nrf2 Is an Attractive Therapeutic Target for Retinal Diseases

Oxidative Medicine and Cellular Longevity

Volumn 2016, Issue , 2016, Pages

  Nakagami, Yasuhiro ^a  

^a DAIICHI SANKYO CO   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ANTIOXIDANTS; CARDIOLOGY; CHEMICAL ACTIVATION; ENZYMES; TRANSCRIPTION;

ANTIOXIDANT RESPONSE ELEMENTS; CHRONIC KIDNEY DISEASE; DETOXIFYING ENZYMES; MITOCHONDRIAL MYOPATHY; NUCLEAR FACTOR ERYTHROID 2-RELATED FACTOR 2; PULMONARY ARTERIAL HYPERTENSION; REACTIVE OXYGEN SPECIES; RETINAL DEGENERATIONS;

OPHTHALMOLOGY;

TRANSCRIPTION FACTOR NRF2; ANTIOXIDANT;

DISEASE ASSOCIATION; HUMAN; NONHUMAN; OXIDATIVE STRESS; PROTEIN TARGETING; RETINA DEGENERATION; RETINA DISEASE; REVIEW; SIGNAL TRANSDUCTION; AGONISTS; ANIMAL; DISEASE MODEL; DRUG DESIGN; DRUG EFFECTS; METABOLISM; MOLECULARLY TARGETED THERAPY; PATHOLOGY; RETINA; RETINAL DISEASES;

ANIMALS; ANTIOXIDANTS; DISEASE MODELS, ANIMAL; DRUG DESIGN; HUMANS; MOLECULAR TARGETED THERAPY; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; RETINA; RETINAL DISEASES; SIGNAL TRANSDUCTION;

EID: 84994031814     PISSN: 19420900     EISSN: 19420994     Source Type: Journal    
DOI: 10.1155/2016/7469326     Document Type: Review

References (68)

1. D. Harman, "Aging: a theory based on free radical and radiation chemistry, " Journal of Gerontology, vol. 11, no. 3, pp. 298-300, 1956.
2. K. L. DeBalsi, K. E. Hoff, W. C. Copeland, "Role of the mitochondrial DNA replication machinery in mitochondrial DNA mutagenesis, aging and age-related diseases, " Ageing Research Reviews, 2016.
3. R. D. Glickman, "Ultraviolet phototoxicity to the retina, " Eye and Contact Lens, vol. 37, no. 4, pp. 196-205, 2011.
4. M. Majdi, B. Y. Milani, A. Movahedan, L. Wasielewski, A. R. Djalilian, "The role of ultraviolet radiation in the ocular system of mammals, " Photonics, vol. 1, no. 4, pp. 347-368, 2014.
5. J. W. Crabb, M. Miyagi, X. Gu et al., "Drusen proteome analysis: an approach to the etiology of age-related macular degeneration, " Proceedings of the National Academy of Sciences of the United States of America, vol. 99, no. 23, pp. 14682-14687, 2002.
6. H.-P. Hammes, H. Hoerauf, A. Alt et al., "N()(carboxymethyl) lysin and the AGE receptor RAGE colocalize in age-related macular degeneration, " Investigative Ophthalmology & Visual Science, vol. 40, no. 8, pp. 1855-1859, 1999.
7. S. R. Kim, S. Jockusch, Y. Itagaki, N. J. Turro, J. R. Sparrow, "Mechanisms involved in A2E oxidation, " Experimental Eye Research, vol. 86, no. 6, pp. 975-982, 2008.
8. J. R. Sparrow, H. R. Vollmer-Snarr, J. Zhou et al., "A2E-epoxides damage DNA in retinal pigment epithelial cells. Vitamin E and other antioxidants inhibit A2E-epoxide formation, " The Journal of Biological Chemistry, vol. 278, no. 20, pp. 18207-18213, 2003.
9. R. A. Radu, N. L. Mata, A. Bagla, G. H. Travis, "Light exposure stimulates formation of A2E oxiranes in a mouse model of Stargardt's macular degeneration, " Proceedings of the National Academy of Sciences of the United States of America, vol. 101, no. 16, pp. 5928-5933, 2004.
10. Y. Kuse, K. Ogawa, K. Tsuruma, M. Shimazawa, H. Hara, "Damage of photoreceptor-derived cells in culture induced by light emitting diode-derived blue light, " Scientific Reports, vol. 4, article 5223, 2014.
11. G. K. Jain, M. H. Warsi, J. Nirmal et al., "Therapeutic stratagems for vascular degenerative disorders of the posterior eye, " Drug Discovery Today, vol. 17, no. 13-14, pp. 748-759, 2012.
12. H. Ahsan, "Diabetic retinopathy-biomolecules and multiple pathophysiology, " Diabetes and Metabolic Syndrome: Clinical Research and Reviews, vol. 9, no. 1, pp. 51-54, 2015.
13. M. P. Cabrera and R. H. Chihuailaf, "Antioxidants and the integrity of ocular tissues, " Veterinary Medicine International, vol. 2011, Article ID 905153, 8 pages, 2011.
14. J. T. Handa, "How does the macula protect itself from oxidative stress" Molecular Aspects of Medicine, vol. 33, no. 4, pp. 418-435, 2012.
15. S. G. Jarrett and M. E. Boulton, "Consequences of oxidative stress in age-related macular degeneration, " Molecular Aspects of Medicine, vol. 33, no. 4, pp. 399-417, 2012.
16. J. G. Hollyfield, V. L. Bonilha, M. E. Rayborn et al., "Oxidative damage-induced inflammation initiates age-related macular degeneration, " Nature Medicine, vol. 14, no. 2, pp. 194-198, 2008.
17. E. Y. Chew, T. E. Clemons, E. Agrón, L. J. Launer, F. Grodstein, P. S. Bernstein, "Effect of omega-3 fatty acids, lutein/zeaxanthin, or other nutrient supplementation on cognitive function: the AREDS2 randomized clinical trial, " The Journal of the American Medical Association, vol. 314, no. 8, pp. 791-801, 2015.
18. M. A. Babizhayev, "New concept in nutrition for the maintenance of the aging eye redox regulation and therapeutic treatment of cataract disease; Synergism of natural antioxidant imidazole-containing amino acid-based compounds, chaperone, glutathione boosting agents: a systemic perspective on aging and longevity emerged from studies in humans, " American Journal of Therapeutics, vol. 17, no. 4, pp. 373-389, 2010.
19. E. L. Berson, B. Rosner, M. A. Sandberg et al., "Clinical trial of lutein in patientswith retinitis pigmentosa receiving vitamin A, " Archives of Ophthalmology, vol. 128, no. 4, pp. 403-411, 2010.
20. W. T. Wong, W. Kam, D. Cunningham et al., "Treatment of geographic atrophy by the topical administration of OT-551: results of a phase II clinical trial, " Investigative Ophthalmology & Visual Science, vol. 51, no. 12, pp. 6131-6139, 2010.
21. K. Itoh, J. Mimura, M. Yamamoto, "Discovery of the negative regulator ofNrf2, keap1: a historical overview, " Antioxidants and Redox Signaling, vol. 13, no. 11, pp. 1665-1678, 2010.
22. T. Suzuki, H. Motohashi, M. Yamamoto, "Toward clinical application of the Keap1-Nrf2 pathway, " Trends in Pharmacological Sciences, vol. 34, no. 6, pp. 340-346, 2013.
23. S. Ruiz, P. E. Pergola, R. A. Zager, N. D. Vaziri, "Targeting the transcription factor Nrf2 to ameliorate oxidative stress and inflammation in chronic kidney disease, " Kidney International, vol. 83, no. 6, pp. 1029-1041, 2013.
24. J. D. Wardyn, A. H. Ponsford, C. M. Sanderson, "Dissecting molecular cross-talk between Nrf2 and NF-B response pathways, " Biochemical Society Transactions, vol. 43, pp. 621-626, 2015.
25. I. Rahman, "Antioxidant therapies in COPD, " International Journal of Chronic Obstructive Pulmonary Disease, vol. 1, no. 1, pp. 15-29, 2006.
26. M. Suzuki, T. Betsuyaku, Y. Ito et al., "Down-regulated NF-E2-related factor 2 in pulmonarymacrophages of aged smokers and patients with chronic obstructive pulmonary disease, "American Journal of Respiratory Cell and Molecular Biology, vol. 39, no. 6, pp. 673-682, 2008.
27. Q. Zhong, M. Mishra, R. A. Kowluru, "Transcription factor Nrf2-mediated antioxidant defense system in the development of diabetic retinopathy, " Investigative Ophthalmology & Visual Science, vol. 54, no. 6, pp. 3941-3948, 2013.
28. M. L. Lambros and S. M. Plafker, "Oxidative stress and the Nrf2 anti-oxidant transcription factor in age-related macular degeneration, " Advances in Experimental Medicine and Biology, vol. 854, pp. 67-72, 2016.
29. K. Itoh, T. Chiba, S. Takahashi et al., "An Nrf2/small Maf heterodimer mediates the induction of phase II detoxifying enzyme genes through antioxidant response elements, " Biochemical and Biophysical Research Communications, vol. 236, no. 2, pp. 313-322, 1997.
30. K. Chan, R. Lu, J. C. Chang, Y. W. Kan, "NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, development, " Proceedings of the National Academy of Sciences of the United States of America, vol. 93, no. 24, pp. 13943-13948, 1996.
31. Z. Zhao, Y. Chen, J. Wang et al., "Age-related retinopathy in NRF2-deficient mice, " PLoS ONE, vol. 6, no. 4, article e19456, 2011.
32. M. Cano, R. Thimmalappula, M. Fujihara et al., "Cigarette smoking, oxidative stress, the anti-oxidant response through Nrf2 signaling, Age-related Macular Degeneration, " Vision Research, vol. 50, no. 7, pp. 652-664, 2010.
33. K. Uno, T. W. Prow, I. A. Bhutto et al., "Role of Nrf2 in retinal vascular development and the vaso-obliterative phase of oxygen-induced retinopathy, " Experimental Eye Research, vol. 90, no. 4, pp. 493-500, 2010.
34. N. Himori, K. Yamamoto, K. Maruyama et al., "Critical role of Nrf2 in oxidative stress-induced retinal ganglion cell death, " Journal of Neurochemistry, vol. 127, no. 5, pp. 669-680, 2013.
35. Z. Xu, Y. Wei, J. Gong et al., "NRF2 plays a protective role in diabetic retinopathy in mice, " Diabetologia, vol. 57, no. 1, pp. 204-213, 2014.
36. N. Nagai, R. K. Thimmulappa, M. Cano et al., "Nrf2 is a critical modulator of the innate immune response in amodel of uveitis, " Free Radical Biology and Medicine, vol. 47, no. 3, pp. 300-306, 2009.
37. Y. Wei, J. Gong, T. Yoshida et al., "Nrf2 has a protective role against neuronal and capillary degeneration in retinal ischemiareperfusion injury, " Free Radical Biology and Medicine, vol. 51, no. 1, pp. 216-224, 2011.
38. N. Wakabayashi, K. Itoh, J. Wakabayashi et al., "Keap1-null mutation leads to postnatal lethality due to constitutive Nrf2 activation, " Nature Genetics, vol. 35, no. 3, pp. 238-245, 2003.
39. H. Okawa, H. Motohashi, A. Kobayashi, H. Aburatani, T. W. Kensler, M. Yamamoto, "Hepatocyte-specific deletion of the keap1 gene activates Nrf2 and confers potent resistance against acute drug toxicity, " Biochemical and Biophysical Research Communications, vol. 339, no. 1, pp. 79-88, 2006.
40. T. W. Kensler, P. A. Egner, A. S. Agyeman et al., "Keap1-Nrf2 signaling: a target for cancer prevention by sulforaphane, " Topics in Current Chemistry, vol. 329, pp. 163-178, 2013.
41. K. Takaya, T. Suzuki, H. Motohashi et al., "Validation of the multiple sensor mechanism of the Keap1-Nrf2 system, " Free Radical Biology and Medicine, vol. 53, no. 4, pp. 817-827, 2012.
42. M. C. Lu, J. A. Ji, Z. Y. Jiang, Q. D. You, "The Keap1-Nrf2-ARE pathway as a potential preventive and therapeutic target: an update, "Medicinal Research Reviews, vol. 36, no. 5, pp. 924-963, 2016.
43. C. A. Houghton, R. G. Fassett, J. S. Coombes, "Sulforaphane and other nutrigenomic Nrf2 activators: can the clinician's expectation bematched by the reality" OxidativeMedicine and Cellular Longevity, vol. 2016, Article ID 7857186, 17 pages, 2016.
44. E. D. Deeks, "Dimethyl fumarate: a review in relapsingremitting MS, " Drugs, vol. 76, no. 2, pp. 243-254, 2016.
45. K. T. Liby and M. B. Sporn, "Synthetic oleanane triterpenoids: multifunctional drugs with a broad range of applications for prevention and treatment of chronic disease, " Pharmacological Reviews, vol. 64, no. 4, pp. 972-1003, 2012.
46. K. T. Liby, M. M. Yore, M. B. Sporn, "Triterpenoids and rexinoids as multifunctional agents for the prevention and treatment of cancer, " Nature Reviews Cancer, vol. 7, no. 5, pp. 357-369, 2007.
47. P. E. Pergola, P. Raskin, R. D. Toto et al., "Bardoxolone methyl and kidney function in CKD with type 2 diabetes, " The New England Journal of Medicine, vol. 365, no. 4, pp. 327-336, 2011.
48. D. de Zeeuw, T. Akizawa, P. Audhya et al., "Bardoxolone methyl in type 2 diabetes and stage 4 chronic kidney disease, " The New England Journal of Medicine, vol. 369, no. 26, pp. 2492-2503, 2013.
49. M. P. Chin, S. A. Reisman, G. L. Bakris et al., "Mechanisms contributing to adverse cardiovascular events in patients with type 2 diabetes mellitus and stage 4 chronic kidney disease treated with bardoxolonemethyl, " American Journal of Nephrology, vol. 39, no. 6, pp. 499-508, 2014.
50. H. E. Abboud, "Synthetic oleanane triterpenoids: magic bullets or not" Kidney International, vol. 83, no. 5, pp. 785-787, 2013.
51. I. Pitha-Rowe, K. Liby, D. Royce, M. Sporn, "Synthetic triterpenoids attenuate cytotoxic retinal injury: cross-talk between Nrf2 and PI3K/AKT signaling through inhibition of the lipid phosphatase PTEN, " Investigative Ophthalmology and Visual Science, vol. 50, no. 11, pp. 5339-5347, 2009.
52. T. E. Sussan, T. Rangasamy, D. J. Blake et al., "Targeting Nrf2 with the triterpenoid CDDO-imidazolide attenuates cigarette smoke-induced emphysema and cardiac dysfunction in mice, " Proceedings of the National Academy of Sciences of the United States of America, vol. 106, no. 1, pp. 250-255, 2009.
53. Y. Nakagami, K. Masuda, E. Hatano et al., "NovelNrf2 activators from microbial transformation products inhibit blood-retinal barrier permeability in rabbits, " British Journal of Pharmacology, vol. 172, no. 5, pp. 1237-1249, 2015.
54. Y. Nakagami, E. Hatano, T. Inoue, K. Yoshida, M. Kondo, H. Terasaki, "Cytoprotective effects of a novel Nrf2 activator, RS9, in rhodopsin Pro347Leu rabbits, " Current Eye Research, vol. 41, no. 8, pp. 1123-1126, 2016.
55. H.-H. Shen, E. C. Chan, J. H. Lee et al., "Nanocarriers for treatment of ocular neovascularization in the back of the eye: new vehicles for ophthalmic drug delivery, " Nanomedicine, vol. 10, no. 13, pp. 2093-2107, 2015.
56. N. Kuno and S. Fujii, "Biodegradable intraocular therapies for retinal disorders: progress to date, " Drugs and Aging, vol. 27, no. 2, pp. 117-134, 2010.
57. G. Wells, "Peptide and small molecule inhibitors of the Keap1-Nrf2 protein-protein interaction, " Biochemical Society Transactions, vol. 43, pp. 674-679, 2015.
58. D. A. Abed, M. Goldstein, H. Albanyan, H. Jin, L. Hu, "Discovery of direct inhibitors of Keap1-Nrf2 protein-protein interaction as potential therapeutic and preventive agents, " Acta Pharmaceutica Sinica B, vol. 5, no. 4, pp. 285-299, 2015.
59. K. I. Tong, B. Padmanabhan, A. Kobayashi et al., "Different electrostatic potentials define ETGE and DLG motifs as hinge and latch in oxidative stress response, " Molecular and Cellular Biology, vol. 27, no. 21, pp. 7511-7521, 2007.
60. L. Hu, S. Magesh, L. Chen et al., "Discovery of a small-molecule inhibitor and cellular probe of Keap1-Nrf2 protein-protein interaction, " Bioorganic and Medicinal Chemistry Letters, vol. 23, no. 10, pp. 3039-3043, 2013.
61. R. Shimozono, Y. Asaoka, Y. Yoshizawa et al., "Nrf2 activators attenuate the progression of nonalcoholic steatohepatitisrelated fibrosis in a dietary rat models, " Molecular Pharmacology, vol. 84, no. 1, pp. 62-70, 2013.
62. P. Canning and A. N. Bullock, "New strategies to inhibit KEAP1 and the Cul3-based E3 ubiquitin ligases, " Biochemical Society Transactions, vol. 42, no. 1, pp. 103-107, 2014.
63. A. Kobayashi, M.-I. Kang, H. Okawa et al., "Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2, " Molecular and Cellular Biology, vol. 24, no. 16, pp. 7130-7139, 2004.
64. M. Furukawa and Y. Xiong, "BTB protein keap1 targets antioxidant transcription factor Nrf2 for ubiquitination by the cullin 3-Roc1 ligase, " Molecular and Cellular Biology, vol. 25, no. 1, pp. 162-171, 2005.
65. K. Itoh, N. Wakabayashi, Y. Katoh, T. Ishii, T. O'Connor, M. Yamamoto, "Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles, " Genes to Cells, vol. 8, no. 4, pp. 379-391, 2003.
66. E. C. R. Solano, D. J. Kornbrust, A. Beaudry, J. W.-D. Foy, D. J. Schneider, J. D. Thompson, "Toxicological and pharmacokinetic properties of QPI-1007, a chemically modified synthetic siRNA targeting caspase 2 mRNA, following intravitreal injection, " Nucleic AcidTherapeutics, vol. 24, no. 4, pp. 258-266, 2014.
67. P. J. Morgan-Warren, J. O'Neill, F. De Cogan et al., "SiRNAmediated knockdown of themTOR inhibitor RTP801 promotes retinal ganglion cell survival and axon elongation by direct and indirect mechanisms, " Investigative Ophthalmology and Visual Science, vol. 57, no. 2, pp. 429-443, 2016.
68. J. D. Hayes and M. McMahon, "NRF2 and KEAP1 mutations: permanent activation of an adaptive response in cancer, " Trends in Biochemical Sciences, vol. 34, no. 4, pp. 176-188, 2009.