Nrf2 protects mitochondrial decay by oxidative stress

FASEB Journal

Volumn 30, Issue 1, 2016, Pages 66-80

  Strom, Joshua ^a   Xu, Beibei ^a   Tian, Xiuqing ^a   Chen, Qin M ^a  

^a UNIVERSITY OF ARIZONA COLLEGE OF MEDICINE   (United States)

Author keywords

Cell survival; Loss of mitochondria; Mitochondrial outer membrane; Transcription factor

Indexed keywords

ADENOVIRUS VECTOR; CYTOCHROME B; CYTOCHROME C; DNA; HYDROGEN PEROXIDE; MESSENGER RNA; MITOCHONDRIAL PROTEIN; TRANSCRIPTION FACTOR NRF2; ANTIOXIDANT; NFE2L2 PROTEIN, MOUSE; PROTECTIVE AGENT;

ANIMAL CELL; ARTICLE; CARDIAC MUSCLE CELL; CELL FRACTIONATION; CELL MEMBRANE POTENTIAL; CELL PROTECTION; CELL STRUCTURE; CELL SURVIVAL; CELL VACUOLE; CONTROLLED STUDY; DIMERIZATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DNA BINDING; ELECTRON MICROSCOPY; GENE; GENE OVEREXPRESSION; GENE TRANSFER; HEART HYPERTROPHY; HEART MITOCHONDRION; MEASUREMENT; MITOCHONDRIAL DAMAGE; MITOCHONDRIAL MEMBRANE POTENTIAL; MITOCHONDRIAL RESPIRATION; NEWBORN; NONHUMAN; NONVIRAL GENE THERAPY; OXIDATIVE STRESS; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; RAT; VIRAL GENE DELIVERY SYSTEM; ANIMAL; DRUG EFFECTS; GENETICS; KNOCKOUT MOUSE; METABOLISM; PHYSIOLOGY; SIGNAL TRANSDUCTION;

ANIMALS; ANTIOXIDANTS; HYDROGEN PEROXIDE; MICE, KNOCKOUT; MITOCHONDRIA, HEART; MYOCYTES, CARDIAC; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PROTECTIVE AGENTS; SIGNAL TRANSDUCTION;

EID: 84974777642     PISSN: 08926638     EISSN: 15306860     Source Type: Journal    
DOI: 10.1096/fj.14-268904     Document Type: Article

References (69)

1. Goldhaber, J. I. (1997) Metabolism in normal and ischemic myocardium. In The Myocardium (Langer, G. A., ed.), pp. 325-393, Academic Press, San Diego, CA, USA
2. Babu, G. G., Walker, J. M., Yellon, D. M., and Hausenloy, D. J. (2011) Peri-procedural myocardial injury during percutaneous coronary intervention: an important target for cardioprotection. Eur. Heart J. 32, 23-31
3. Herrmann, J. (2005) Peri-procedural myocardial injury: 2005 update. Eur. Heart J. 26, 2493-2519
4. Kloner, R. A., Przyklenk, K., and Whittaker, P. (1989) Deleterious effects of oxygen radicals in ischemia/reperfusion. Resolved and unresolved issues. Circulation 80, 1115-1127
5. Opie, L. H. (1989) Reperfusion injury and its pharmacologic modification. Circulation 80, 1049-1062
6. Chen, Y. R., and Zweier, J. L. (2014) Cardiac mitochondria and reactive oxygen species generation. Circ. Res. 114, 524-537
7. Chen, Q. M., Tu, V. C., Wu, Y., and Bahl, J. J. (2000) Hydrogen peroxide dose dependent induction of cell death or hypertrophy in cardiomyocytes. Arch. Biochem. Biophys. 373, 242-248
8. Xie, L., Terrand, J., Xu, B., Tsaprailis, G., Boyer, J., and Chen, Q. M. (2010) Cystatin C increases in cardiac injury: a role in extracellular matrix protein modulation. Cardiovasc. Res. 87, 628-635
9. Purdom-Dickinson, S. E., Lin, Y., Dedek, M., Morrissy, S., Johnson, J., and Chen, Q. M. (2007) Induction of antioxidant and detoxification response by oxidants in cardiomyocytes: evidence from gene expression profiling and activation of Nrf2 transcription factor. J. Mol. Cell. Cardiol. 42, 159-176
10. Purdom-Dickinson, S. E., Sheveleva, E. V., Sun, H., and Chen, Q. M. (2007) Translational control of nrf2 protein in activation of antioxidant response by oxidants. Mol. Pharmacol. 72, 1074-1081
11. Lee, J. M., Calkins, M. J., Chan, K., Kan, Y. W., and Johnson, J. A. (2003) Identification of the NF-E2-related factor-2-dependent genes conferring protection against oxidative stress in primary cortical astrocytes using oligonucleotide microarray analysis.J. Biol. Chem. 278, 12029-12038
12. Nguyen, T., Nioi, P., and Pickett, C. B. (2009) The Nrf2-antioxidant response element signaling pathway and its activation by oxidative stress. J. Biol. Chem. 284, 13291-13295
13. Li, W., and Kong, A. N. (2009) Molecular mechanisms of Nrf2-mediated antioxidant response. Mol. Carcinog. 48, 91-104
14. Ma, Q. (2013) Role of nrf2 in oxidative stress and toxicity. Annu. Rev. Pharmacol. Toxicol. 53, 401-426
15. Kensler, T. W., Wakabayashi, N., and Biswal, S. (2007) Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 47, 89-116
16. Barth, E., Stämmler, G., Speiser, B., and Schaper, J. (1992) Ultrastructural quantitation of mitochondria and myofilaments in cardiac muscle from 10 different animal species including man. J. Mol. Cell. Cardiol. 24, 669-681
17. Chen, Q. M., Merrett, J. B., Dilley, T., and Purdom, S. (2002) Down regulation of p53 with HPV E6 delays and modifies cell death in oxidant response of human diploid fibroblasts: an apoptosis-like cell death associated with mitosis. Oncogene 21, 5313-5324
18. Zhang, J., Dinh, T., Kapperler, K., Tsaprailis, G., and Chen, Q. (2012) La autoantigen mediates oxidant induced de novo nrf2 protein translation. Mol. Cell. Proteomics 11, M111.015032
19. Xu, B., Zhang, J., Strom, J., Lee, S., and Chen, Q. M. (2014) Myocardial ischemic reperfusion induces de novo Nrf2 protein translation. Biochim. Biophys. Acta 1842, 1638-1647
20. Alam, J., Stewart, D., Touchard, C., Boinapally, S., Choi, A. M., and Cook, J. L. (1999) Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene. J. Biol. Chem. 274, 26071-26078
21. Petit, P. X., Goubern, M., Diolez, P., Susin, S. A., Zamzami, N., and Kroemer, G. (1998) Disruption of the outer mitochondrial membrane as a result of large amplitude swelling: the impact of irreversible permeability transition. FEBS Lett. 426, 111-116
22. Baines, C. P., Kaiser, R. A., Purcell, N. H., Blair, N. S., Osinska, H., Hambleton, M. A., Brunskill, E. W., Sayen, M. R., Gottlieb, R. A., Dorn, G. W., Robbins, J., and Molkentin, J. D. (2005) Loss of cyclophilin D reveals a critical role for mitochondrial permeability transition in cell death. Nature 434, 658-662
23. Borillo, G. A., Mason, M., Quijada, P., Völkers, M., Cottage, C., McGregor, M., Din, S., Fischer, K., Gude, N., Avitabile, D., Barlow, S., Alvarez, R., Truffa, S., Whittaker, R., Glassy, M. S., Gustafsson, A. B., Miyamoto, S., Glembotski, C. C., Gottlieb, R. A., Brown, J. H., and Sussman, M. A. (2010) Pim-1 kinase protects mitochondrial integrity in cardiomyocytes. Circ. Res. 106, 1265-1274
24. Lee, J. M., Shih, A. Y., Murphy, T. H., and Johnson, J. A. (2003) 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, 37948-37956
25. He, X., Kan, H., Cai, L., and Ma, Q. (2009) Nrf2 is critical in defense against high glucose-induced oxidative damage in cardiomyocytes. J. Mol. Cell. Cardiol. 46, 47-58
26. Kovac, S., Angelova, P. R., Holmström, K. M., Zhang, Y., Dinkova-Kostova, A. T., and Abramov, A. Y. (2015) Nrf2 regulates ROS production by mitochondria and NADPH oxidase. Biochim. Biophys. Acta 1850, 794-801
27. Piantadosi, C. A., Carraway, M. S., Babiker, A., and Suliman, H. B. (2008) Heme oxygenase-1 regulates cardiac mitochondrial biogenesis via Nrf2-mediated transcriptional control of nuclear respiratory factor-1. Circ. Res. 103, 1232-1240
28. Kwon, J., Han, E., Bui, C. B., Shin, W., Lee, J., Lee, S., Choi, Y. B., Lee, A. H., Lee, K. H., Park, C., Obin, M. S., Park, S. K., Seo, Y. J., Oh, G. T., Lee, H. W., and Shin, J. (2012) Assurance of mitochondrial integrity and mammalian longevity by the p62-Keap1-Nrf2-Nqo1 cascade. EMBO Rep. 13, 150-156
29. Athale, J., Ulrich, A., MacGarvey, N. C., Bartz, R. R., Welty-Wolf, K. E., Suliman, H. B., and Piantadosi, C. A. (2012) Nrf2 promotes alveolar mitochondrial biogenesis and resolution of lung injury in Staphylococcus aureus pneumonia in mice. Free Radic. Biol. Med. 53, 1584-1594
30. Bindu, S., Pal, C., Dey, S., Goyal, M., Alam, A., Iqbal, M. S., Dutta, S., Sarkar, S., Kumar, R., Maity, P., and Bandyopadhyay, U. (2011) Translocation of heme oxygenase-1 to mitochondria is a novel cytoprotective mechanism against non-steroidal anti-inflammatory drug-induced mitochondrial oxidative stress, apoptosis, and gastric mucosal injury. J. Biol. Chem. 286, 39387-39402
31. Bolisetty, S., Traylor, A., Zarjou, A., Johnson, M. S., Benavides, G. A., Ricart, K., Boddu, R., Moore, R. D., Landar, A., Barnes, S., Darley-Usmar, V., and Agarwal, A. (2013) Mitochondria-targeted heme oxygenase-1 decreases oxidative stress in renal epithelial cells. Am. J. Physiol. Renal Physiol. 305, F255-F264
32. Slebos, D. J., Ryter, S. W., van der Toorn, M., Liu, F., Guo, F., Baty, C. J., Karlsson, J. M., Watkins, S. C., Kim, H. P., Wang, X., Lee, J. S., Postma, D. S., Kauffman, H. F., and Choi, A. M. (2007) Mitochondrial localization and function of heme oxygenase-1 in cigarette smoke-induced cell death. Am. J. Respir. Cell Mol. Biol. 36, 409-417
33. Holmström, K. M., Baird, L., Zhang, Y., Hargreaves, I., Chalasani, A., Land, J. M., Stanyer, L., Yamamoto, M., Dinkova-Kostova, A. T., and Abramov, A. Y. (2013) Nrf2 impacts cellular bioenergetics by controlling substrate availability for mitochondrial respiration. Biol. Open 2, 761-770
34. Ludtmann, M. H., Angelova, P. R., Zhang, Y., Abramov, A. Y., and Dinkova-Kostova, A. T. (2014) Nrf2 affects the efficiency of mitochondrial fatty acid oxidation. Biochem. J. 457, 415-424
35. Estaquier, J., and Arnoult, D. (2007) Inhibiting Drp1-mediated mitochondrial fission selectively prevents the release of cytochrome c during apoptosis. Cell Death Differ. 14, 1086-1094
36. Hoppins, S., Lackner, L., and Nunnari, J. (2007) The machines that divide and fuse mitochondria. Annu. Rev. Biochem. 76, 751-780
37. Youle, R. J., and van der Bliek, A. M. (2012) Mitochondrial fission, fusion, and stress. Science 337, 1062-1065
38. Ong, S. B., and Hausenloy, D. J. (2010) Mitochondrial morphology and cardiovascular disease. Cardiovasc. Res. 88, 16-29
39. Brady, N. R., Hamacher-Brady, A., and Gottlieb, R. A. (2006) Proapoptotic BCL-2 family members and mitochondrial dysfunction during ischemia/reperfusion injury, a study employing cardiac HL-1 cells and GFP biosensors. Biochim. Biophys. Acta 1757, 667-678
40. Dominic, E. A., Ramezani, A., Anker, S. D., Verma, M., Mehta, N., and Rao, M. (2014) Mitochondrial cytopathies and cardiovascular disease. Heart 100, 611-618
41. Dagda, R. K., Cherra III, S. J., Kulich, S. M., Tandon, A., Park, D., and Chu, C. T. (2009) Loss of PINK1 function promotes mitophagy through effects on oxidative stress and mitochondrial fission. J. Biol. Chem. 284, 13843-13855
42. Wu, S., Zhou, F., Zhang, Z., and Xing, D. (2011) Mitochondrial oxidative stress causes mitochondrial fragmentation via differential modulation of mitochondrial fission-fusion proteins. FEBS J. 278, 941-954
43. Chan, D. C. (2012) Fusion and fission: interlinked processes critical for mitochondrial health. Annu. Rev. Genet. 46, 265-287
44. Scarpulla, R. C., Vega, R. B., and Kelly, D. P. (2012) Transcriptional integration of mitochondrial biogenesis. Trends Endocrinol. Metab. 23, 459-466
45. Elmore, S. P., Qian, T., Grissom, S. F., and Lemasters, J. J. (2001) The mitochondrial permeability transition initiates autophagy in rat hepatocytes. FASEB J. 15, 2286-2287
46. Kim, I., Rodriguez-Enriquez, S., and Lemasters, J. J. (2007) Selective degradation of mitochondria by mitophagy. Arch. Biochem. Biophys. 462, 245-253
47. Kubli, D. A., and Gustafsson, A. B. (2012) Mitochondria and mitophagy: the yin and yang of cell death control. Circ. Res. 111, 1208-1221
48. Lau, A., Wang, X. J., Zhao, F., Villeneuve, N. F., Wu, T., Jiang, T., Sun, Z., White, E., and Zhang, D. D. (2010) A noncanonical mechanism of Nrf2 activation by autophagy deficiency: direct interaction between Keap1 and p62. Mol. Cell. Biol. 30, 3275-3285
49. Komatsu, M., Kurokawa, H., Waguri, S., Taguchi, K., Kobayashi, A., Ichimura, Y., Sou, Y. S., Ueno, I., Sakamoto, A., Tong, K. I., Kim, M., Nishito, Y., Iemura, S., Natsume, T., Ueno, T., Kominami, E., Motohashi, H., Tanaka, K., and Yamamoto, M. (2010) The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat. Cell Biol. 12, 213-223
50. Ichimura, Y., Waguri, S., Sou, Y. S., Kageyama, S., Hasegawa, J., Ishimura, R., Saito, T., Yang, Y., Kouno, T., Fukutomi, T., Hoshii, T., Hirao, A., Takagi, K., Mizushima, T., Motohashi, H., Lee, M. S., Yoshimori, T., Tanaka, K., Yamamoto, M., and Komatsu, M. (2013) Phosphorylation of p62 activates the Keap1-Nrf2 pathway during selective autophagy. Mol. Cell 51, 618-631
51. Jo, C., Gundemir, S., Pritchard, S., Jin, Y. N., Rahman, I., and Johnson, G. V. (2014) Nrf2 reduces levels of phosphorylated tau protein by inducing autophagy adaptor protein NDP52. Nat. Commun. 5
52. Rao, V. A., Klein, S. R., Bonar, S. J., Zielonka, J., Mizuno, N., Dickey, J. S., Keller, P. W., Joseph, J., Kalyanaraman, B., and Shacter, E. (2010) The antioxidant transcription factor Nrf2 negatively regulates autophagy and growth arrest induced by the anticancer redox agent mitoquinone. J. Biol. Chem. 285, 34447-34459
53. Darvekar, S. R., Elvenes, J., Brenne, H. B., Johansen, T., and Sjøttem, E. (2014) SPBP is a sulforaphane induced transcriptional coactivator of NRF2 regulating expression of the autophagy receptor p62/SQSTM1. PLoS One 9, e85262
54. Chung, S. D., Lai, T. Y., Chien, C. T., and Yu, H. J. (2012) Activating Nrf-2 signaling depresses unilateral ureteral obstruction-evoked mitochondrial stress-related autophagy, apoptosis and pyroptosis in kidney. PLoS One 7, e47299
55. Joshi, G., Gan, K. A., Johnson, D. A., and Johnson, J. A. (2015) Increased Alzheimer's disease-like pathology in the APP/ PS1DE9 mouse model lacking Nrf2 through modulation of autophagy. Neurobiol. Aging 36, 664-679
56. Dutta, D., Calvani, R., Bernabei, R., Leeuwenburgh, C., and Marzetti, E. (2012) Contribution of impaired mitochondrial autophagy to cardiac aging: mechanisms and therapeutic opportunities. Circ. Res. 110, 1125-1138
57. Hoshino, A., Mita, Y., Okawa, Y., Ariyoshi, M., Iwai-Kanai, E., Ueyama, T., Ikeda, K., Ogata, T., and Matoba, S. (2013) Cytosolic p53 inhibits Parkin-mediated mitophagy and promotes mitochondrial dysfunction in the mouse heart. Nat. Commun. 4
58. Cooper, M. P. (2013) Interplay of mitochondrial biogenesis and oxidative stress in heart failure. Circulation 127, 1932-1934
59. LeBleu, V. S., O'Connell, J. T., Gonzalez Herrera, K. N., Wikman, H., Pantel, K., Haigis, M. C., de Carvalho, F. M., Damascena, A., Domingos Chinen, L. T., Rocha, R. M., Asara, J. M., and Kalluri, R. (2014) PGC-1α mediates mitochondrial biogenesis and oxidative phosphorylation in cancer cells to promote metastasis. Nat. Cell Biol. 16, 992-1003, 1-15
60. Rasbach, K. A., and Schnellmann, R. G. (2007) Signaling of mitochondrial biogenesis following oxidant injury. J. Biol. Chem. 282, 2355-2362
61. Tu, V., and Chen, Q. (2003) Distinct roles of ERKs and p38 MAPK in oxidant induced cardiomyocyte hypertrophy. Cardiovasc. Toxicol. 3, 119-133
62. Purdom, S., and Chen, Q. M. (2005) Epidermal growth factor receptor-dependent and -independent pathways in hydrogen peroxide-induced mitogen-activated protein kinase activation in cardiomyocytes and heart fibroblasts. J. Pharmacol. Exp. Ther. 312, 1179-1186
63. Lo, S. C., and Hannink, M. (2008) PGAM5 tethers a ternary complex containing Keap1 and Nrf2 to mitochondria. Exp. Cell Res. 314, 1789-1803
64. Caballero-Caballero, A., Engel, T., Martinez-Villarreal, J., Sanz-Rodriguez, A., Chang, P., Dunleavy, M., Mooney, C. M., Jimenez-Mateos, E. M., Schindler, C. K., and Henshall, D. C. (2013) Mitochondrial localization of the forkhead box class O transcription factor FOXO3a in brain. J. Neurochem. 124, 749-756
65. Tammineni, P., Anugula, C., Mohammed, F., Anjaneyulu, M., Larner, A. C., and Sepuri, N. B. (2013) The import of the transcription factor STAT3 into mitochondria depends on GRIM-19, a component of the electron transport chain. J. Biol. Chem. 288, 4723-4732
66. Dement, G. A., Treff, N. R., Magnuson, N. S., Franceschi, V., and Reeves, R. (2005) Dynamic mitochondrial localization of nuclear transcription factor HMGA1. Exp. Cell Res. 307, 388-401
67. Ogita, K., Fujinami, Y., Kitano, M., and Yoneda, Y. (2003) Transcription factor activator protein-1 expressed by kainate treatment can bind tothenon-coding regionof mitochondrial genome in murine hippocampus. J. Neurosci. Res. 73, 794-802
68. Achanta, G., Sasaki, R., Feng, L., Carew, J. S., Lu, W., Pelicano, H., Keating, M. J., and Huang, P. (2005) Novel role of p53 in maintaining mitochondrial genetic stability through interaction with DNA Pol gamma. EMBO J. 24, 3482-3492
69. Bakhanashvili, M., Grinberg, S., Bonda, E., Simon, A. J., Moshitch-Moshkovitz, S., and Rahav, G. (2008) p53 in mitochondria enhances the accuracy of DNA synthesis. Cell Death Differ. 15, 1865-1874