MicroRNA-7 activates Nrf2 pathway by targeting Keap1 expression

Free Radical Biology and Medicine

Volumn 89, Issue , 2015, Pages 548-556

  Kabaria, Savan ^a   Choi, Doo Chul ^a   Chaudhuri, Amrita Datta ^a   Jain, Mohit Raja ^b   Li, Hong ^b   Junn, Eunsung ^a  

^a RUTGERS ROBERT WOOD JOHNSON MEDICAL SCHOOL   (United States)

^b The State University of New Jersey   (United States)

Author keywords

Keap1; MicroRNA 7; MPP; Nrf2; Oxidativestress; Parkinson'sdisease

Indexed keywords

1 METHYL 4 PHENYLPYRIDINIUM; GLUTAMATE CYSTEINE LIGASE; GLUTAMATE CYSTEINE LIGASE MODIFIER SUBUNIT; GLUTATHIONE; GLUTATHIONE DISULFIDE; HEME OXYGENASE 1; HYDROPEROXIDE; KELCH LIKE ECH ASSOCIATED PROTEIN 1; MESSENGER RNA; MICRORNA; MICRORNA 7; TRANSCRIPTION FACTOR NRF2; UNCLASSIFIED DRUG; KEAP1 PROTEIN, HUMAN; MIRN7 MICRORNA, HUMAN; NFE2L2 PROTEIN, HUMAN; SIGNAL PEPTIDE;

3' UNTRANSLATED REGION; ARTICLE; CELL PROTECTION; CELL SURVIVAL; CELL VIABILITY; CONTROLLED STUDY; CYTOTOXICITY; GENE EXPRESSION; HUMAN; HUMAN CELL; NERVE FIBER GROWTH; NEURAL STEM CELL; NEUROBLASTOMA CELL LINE; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; BIOSYNTHESIS; CELL LINE; GENE EXPRESSION REGULATION; GENETIC TRANSFECTION; LIQUID CHROMATOGRAPHY; METABOLISM; PHYSIOLOGY; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; WESTERN BLOTTING;

BLOTTING, WESTERN; CELL LINE; CHROMATOGRAPHY, LIQUID; GENE EXPRESSION REGULATION; HUMANS; INTRACELLULAR SIGNALING PEPTIDES AND PROTEINS; KELCH-LIKE ECH-ASSOCIATED PROTEIN 1; MICRORNAS; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; POLYMERASE CHAIN REACTION; SIGNAL TRANSDUCTION; TANDEM MASS SPECTROMETRY; TRANSFECTION;

EID: 84944089083     PISSN: 08915849     EISSN: 18734596     Source Type: Journal    
DOI: 10.1016/j.freeradbiomed.2015.09.010     Document Type: Article

References (50)

1. B. Uttara, A.V. Singh, P. Zamboni, and R.T. Mahajan Oxidative stress and neurodegenerative diseases: a review of upstream and downstream antioxidant therapeutic options Curr Neuropharmacol 7 2009 65 74
2. P. Moi, K. Chan, I. Asunis, A. Cao, and Y.W. Kan Isolation of NF-E2-related factor 2 (Nrf2), a NF-E2-like basic leucine zipper transcriptional activator that binds to the tandem NF-E2/AP1 repeat of the beta-globin locus control region Proc Natl Acad Sci U S A 91 1994 9926 9930
3. A.K. Jaiswal Nrf2 signaling in coordinated activation of antioxidant gene expression Free Radic Biol Med 36 2004 1199 1207
4. T. Nguyen, P. Nioi, and C.B. Pickett The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress J Biol Chem 284 2009 13291 13295
5. K. Itoh, N. Wakabayashi, Y. Katoh, T. Ishii, K. Igarashi, J.D. Engel, and M. Yamamoto Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain Genes Dev 13 1999 76 86
6. L. He, and G.J. Hannon MicroRNAs: small RNAs with a big role in gene regulation Nat Rev Genet 5 2004 522 531
7. E. Junn, and M.M. Mouradian MicroRNAs in neurodegenerative diseases and their therapeutic potential Pharmacol Ther 133 2012 142 150
8. J. Kim, K. Inoue, J. Ishii, W.B. Vanti, S.V. Voronov, E. Murchison, G. Hannon, and A. Abeliovich A MicroRNA feedback circuit in midbrain dopamine neurons Science 317 2007 1220 1224
9. J. Bilen, N. Liu, B.G. Burnett, R.N. Pittman, and N.M. Bonini MicroRNA pathways modulate polyglutamine-induced neurodegeneration Mol Cell 24 2006 157 163
10. S.M. Eacker, T.M. Dawson, and V.L. Dawson Understanding microRNAs in neurodegeneration Nat Rev Neurosci 10 2009 837 841
11. E. Junn, K.W. Lee, B.S. Jeong, T.W. Chan, J.Y. Im, and M.M. Mouradian Repression of alpha-synuclein expression and toxicity by microRNA-7 Proc Natl Acad Sci U S A 106 2009 13052 13057
12. D.C. Choi, Y.J. Chae, S. Kabaria, A.D. Chaudhuri, M.R. Jain, H. Li, M.M. Mouradian, and E. Junn MicroRNA-7 protects against 1-methyl-4-phenylpyridinium-induced cell death by targeting RelA J Neurosci 34 2014 12725 12737
13. A.D. Chaudhuri, S. Kabaria, D.C. Choi, M.M. Mouradian, and E. Junn MicroRNA-7 Promotes Glycolysis to Protect against 1-Methyl-4-phenylpyridinium-induced Cell Death J Biol Chem 290 2015 12425 12434
14. J. Zhang, T. Ohta, A. Maruyama, T. Hosoya, K. Nishikawa, J.M. Maher, S. Shibahara, K. Itoh, and M. Yamamoto BRG1 interacts with Nrf2 to selectively mediate HO-1 induction in response to oxidative stress Mol Cell Biol 26 2006 7942 7952
15. R. Donato, E.A. Miljan, S.J. Hines, S. Aouabdi, K. Pollock, S. Patel, F.A. Edwards, and J.D. Sinden Differential development of neuronal physiological responsiveness in two human neural stem cell lines BMC Neurosci 8 2007 36
16. E. Meijering, M. Jacob, J.C. Sarria, P. Steiner, H. Hirling, and M. Unser Design and validation of a tool for neurite tracing and analysis in fluorescence microscopy images Cytometry A 58 2004 167 176
17. B. Kalyanaraman, V. Darley-Usmar, K.J. Davies, P.A. Dennery, H.J. Forman, M.B. Grisham, G.E. Mann, K. Moore, and L.J. Roberts 2nd; Ischiropoulos, H. Measuring reactive oxygen and nitrogen species with fluorescent probes: challenges and limitations Free Radic Biol Med 52 2012 1 6
18. J. Zielonka, A. Sikora, M. Hardy, J. Joseph, B.P. Dranka, and B. Kalyanaraman Boronate probes as diagnostic tools for real time monitoring of peroxynitrite and hydroperoxides Chem Res Toxicol 25 2012 1793 1799
19. M. Rehmsmeier, P. Steffen, M. Hochsmann, and R. Giegerich Fast and effective prediction of microRNA/target duplexes RNA 10 2004 1507 1517
20. F.Q. Schafer, and G.R. Buettner Redox environment of the cell as viewed through the redox state of the glutathione disulfide/glutathione couple Free Radic Biol Med 30 2001 1191 1212
21. A.H. Stokes, T.G. Hastings, and K.E. Vrana Cytotoxic and genotoxic potential of dopamine J Neurosci Res 55 1999 659 665
22. M. Komatsu, H. Kurokawa, S. Waguri, K. Taguchi, A. Kobayashi, Y. Ichimura, Y.S. Sou, I. Ueno, A. Sakamoto, K.I. Tong, M. Kim, Y. Nishito, S. Iemura, T. Natsume, T. Ueno, E. Kominami, H. Motohashi, K. Tanaka, and M. Yamamoto The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1 Nat Cell Biol 12 2010 213 223
23. C.H. He, P. Gong, B. Hu, D. Stewart, M.E. Choi, A.M. Choi, and J. Alam Identification of activating transcription factor 4 (ATF4) as an Nrf2-interacting protein. Implication for heme oxygenase-1 gene regulation J Biol Chem 276 2001 20858 20865
24. J. Jeyapaul, and A.K. Jaiswal Nrf2 and c-Jun regulation of antioxidant response element (ARE)-mediated expression and induction of gamma-glutamylcysteine synthetase heavy subunit gene Biochem Pharmacol 59 2000 1433 1439
25. H. Motohashi, F. Katsuoka, J.D. Engel, and M. Yamamoto Small Maf proteins serve as transcriptional cofactors for keratinocyte differentiation in the Keap1-Nrf2 regulatory pathway Proc Natl Acad Sci U S A 101 2004 6379 6384
26. C. Gorrini, P.S. Baniasadi, I.S. Harris, J. Silvester, S. Inoue, B. Snow, P.A. Joshi, A. Wakeham, S.D. Molyneux, B. Martin, P. Bouwman, D.W. Cescon, A.J. Elia, Z. Winterton-Perks, J. Cruickshank, D. Brenner, A. Tseng, M. Musgrave, H.K. Berman, R. Khokha, J. Jonkers, T.W. Mak, and M.L. Gauthier BRCA1 interacts with Nrf2 to regulate antioxidant signaling and cell survival J Exp Med 210 2013 1529 1544
27. M. Narasimhan, D. Patel, D. Vedpathak, M. Rathinam, G. Henderson, and L. Mahimainathan Identification of novel microRNAs in post-transcriptional control of Nrf2 expression and redox homeostasis in neuronal SH-SY5Y cells. PLoS One 7 2012 e51111
28. G. Eades, M. Yang, Y. Yao, Y. Zhang, and Q. Zhou miR-200a regulates Nrf2 activation by targeting Keap1 mRNA in breast cancer cells J Biol Chem 286 2011 40725 40733
29. R.L. Boudreau, P. Jiang, B.L. Gilmore, R.M. Spengler, R. Tirabassi, J.A. Nelson, C.A. Ross, Y. Xing, and B.L. Davidson Transcriptome-wide discovery of microRNA binding sites in human brain Neuron 81 2014 294 305
30. H. Chen, R. Shalom-Feuerstein, J. Riley, S.D. Zhang, P. Tucci, M. Agostini, D. Aberdam, R.A. Knight, G. Genchi, P. Nicotera, G. Melino, and M. Vasa-Nicotera miR-7 and miR-214 are specifically expressed during neuroblastoma differentiation, cortical development and embryonic stem cells differentiation, and control neurite outgrowth in vitro Biochem Biophys Res Commun 394 2010 921 927
31. J. Krutzfeldt, N. Rajewsky, R. Braich, K.G. Rajeev, T. Tuschl, M. Manoharan, and M. Stoffel Silencing of microRNAs in vivo with''antagomirs' Nature 438 2005 685 689
32. G.H. Liu, J. Qu, and X. Shen NF-kappaB/p65 antagonizes Nrf2-ARE pathway by depriving CBP from Nrf2 and facilitating recruitment of HDAC3 to MafK Biochim Biophys Acta 1783 2008 713 727
33. M. Yu, H. Li, Q. Liu, F. Liu, L. Tang, C. Li, Y. Yuan, Y. Zhan, W. Xu, W. Li, H. Chen, C. Ge, J. Wang, and X. Yang Nuclear factor p65 interacts with Keap1 to repress the Nrf2-ARE pathway Cell Signal 23 2011 883 892
34. C.P. Ramsey, C.A. Glass, M.B. Montgomery, K.A. Lindl, G.P. Ritson, L.A. Chia, R.L. Hamilton, C.T. Chu, and K.L. Jordan-Sciutto Expression of Nrf2 in neurodegenerative diseases J Neuropathol Exp Neurol 66 2007 75 85
35. M. Bogdanov, W.R. Matson, L. Wang, T. Matson, R. Saunders-Pullman, S.S. Bressman, and M. Flint Beal Metabolomic profiling to develop blood biomarkers for Parkinson's disease Brain 131 2008 389 396
36. H. Hara, M. Ohta, and T. Adachi Apomorphine protects against 6-hydroxydopamine-induced neuronal cell death through activation of the Nrf2-ARE pathway J Neurosci Res 84 2006 860 866
37. Y.P. Hwang, and H.G. Jeong The coffee diterpene kahweol induces heme oxygenase-1 via the PI3K and p38/Nrf2 pathway to protect human dopaminergic neurons from 6-hydroxydopamine-derived oxidative stress FEBS Lett 582 2008 2655 2662
38. T.T. Cao, L. Ma, G. Kandpal, L. Warren, J.F. Hess, and G.R. Seabrook Increased nuclear factor-erythroid 2 p45-related factor 2 activity protects SH-SY5Y cells against oxidative damage J Neurochem 95 2005 406 417
39. R.J. Jakel, J.A. Townsend, A.D. Kraft, and J.A. Johnson Nrf2-mediated protection against 6-hydroxydopamine Brain Res 1144 2007 192 201
40. C.J. Wruck, M. Claussen, G. Fuhrmann, L. Romer, A. Schulz, T. Pufe, V. Waetzig, M. Peipp, T. Herdegen, and M.E. Gotz Luteolin protects rat PC12 and C6 cells against MPP+ induced toxicity via an ERK dependent Keap1-Nrf2-ARE pathway J Neural Transm Suppl 2007 57 67
41. J.M. Lee, A.Y. Shih, T.H. Murphy, and J.A. Johnson 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 278 2003 37948 37956
42. T. Satoh, N. Harada, T. Hosoya, K. Tohyama, M. Yamamoto, and K. Itoh Keap1/Nrf2 system regulates neuronal survival as revealed through study of keap1 gene-knockout mice Biochem Biophys Res Commun 380 2009 298 302
43. E.L. MacKenzie, P.D. Ray, and Y. Tsuji Role and regulation of ferritin H in rotenone-mediated mitochondrial oxidative stress Free Radic Biol Med 44 2008 1762 1771
44. P.C. Chen, M.R. Vargas, A.K. Pani, R.J. Smeyne, D.A. Johnson, Y.W. Kan, and J.A. Johnson Nrf2-mediated neuroprotection in the MPTP mouse model of Parkinson's disease: Critical role for the astrocyte Proc Natl Acad Sci U S A 106 2009 2933 2938
45. M.D. Maines, B. Polevoda, T. Coban, K. Johnson, S. Stoliar, T.J. Huang, N. Panahian, D.A. Cory-Slechta, and W.K. McCoubrey Jr. Neuronal overexpression of heme oxygenase-1 correlates with an attenuated exploratory behavior and causes an increase in neuronal NADPH diaphorase staining J Neurochem 70 1998 2057 2069
46. K. Fukuda, J.D. Richmon, M. Sato, F.R. Sharp, S.S. Panter, and L.J. Noble Induction of heme oxygenase-1 (HO-1) in glia after traumatic brain injury Brain Res 736 1996 68 75
47. R. Beschorner, D. Adjodah, J.M. Schwab, M. Mittelbronn, I. Pedal, R. Mattern, H.J. Schluesener, and R. Meyermann Long-term expression of heme oxygenase-1 (HO-1, HSP-32) following focal cerebral infarctions and traumatic brain injury in humans Acta Neuropathol 100 2000 377 384
48. E. Huang, W.Y. Ong, M.L. Go, and L.J. Garey Heme oxygenase-1 activity after excitotoxic injury: immunohistochemical localization of bilirubin in neurons and astrocytes and deleterious effects of heme oxygenase inhibition on neuronal survival after kainate treatment J Neurosci Res 80 2005 268 278
49. A.S. Ahmad, H. Zhuang, and S. Dore Heme oxygenase-1 protects brain from acute excitotoxicity Neuroscience 141 2006 1703 1708
50. Y. Lin, H.J. Vreman, R.J. Wong, T. Tjoa, T. Yamauchi, and L.J. Noble-Haeusslein Heme oxygenase-1 stabilizes the blood-spinal cord barrier and limits oxidative stress and white matter damage in the acutely injured murine spinal cord J Cereb Blood Flow Metab 27 2007 1010 1021