Emerging functional cross-talk between the Keap1-Nrf2 system and mitochondria

Journal of Clinical Biochemistry and Nutrition

Volumn 56, Issue 2, 2015, Pages 91-97

  Itoh, Ken ^a   Ye, Peng ^a   Matsumiya, Tomoh ^a   Tanji, Kunikazu ^a   Ozaki, Taku ^a  

^a HIROSAKI UNIVERSITY   (Japan)

Author keywords

Heme oxygenase 1; Mitochondria; NRF 1; Nrf2; P62

Indexed keywords

ANTIOXIDANT; KELCH LIKE ECH ASSOCIATED PROTEIN 1; REACTIVE OXYGEN METABOLITE; TRANSCRIPTION FACTOR NRF2;

BIOGENESIS; CELL FUNCTION; CELL RESPIRATION; CELL STRESS; DETOXIFICATION; DISORDERS OF MITOCHONDRIAL FUNCTIONS; ELECTRON TRANSPORT; GENE TARGETING; HUMAN; MITOCHONDRION; NONHUMAN; OXIDATIVE STRESS; PROTEIN FUNCTION; PROTEIN PROTEIN INTERACTION; QUALITY CONTROL; REVIEW; SIGNAL TRANSDUCTION; TRANSCRIPTION INITIATION;

CAENORHABDITIS ELEGANS; MUS; VASCONCELLEA CANDICANS;

EID: 84924943241     PISSN: 09120009     EISSN: None     Source Type: Journal    
DOI: 10.3164/jcbn.14-134     Document Type: Review

References (69)

1. Tschopp J. Mitochondria: Sovereign of inflammation? Eur J Immunol 2011; 41: 1196-1202.
2. Indo HP, Davidson M, Yen HC, et al. Evidence of ROS generation by mitochondria in cells with impaired electron transport chain and mitochondrial DNA damage. Mitochondrion 2007; 7: 106-118.
3. Haynes CM, Fiorese CJ, Lin YF. Evaluating and responding to mitochondrial dysfunction: The mitochondrial unfolded-protein response and beyond. Trends Cell Biol 2013; 23: 311-318.
4. Yun J, Finkel T. Mitohormesis. Cell Metab 2014; 19: 757-766.
5. Itoh K, Mimura J, Yamamoto M. Discovery of the negative regulator of Nrf2, Keap1: A historical overview. Antioxid Redox Signal 2010; 13: 1665-1678.
6. Chan K, Lu R, Chang JC, Kan YW. NRF2, a member of the NFE2 family of transcription factors, is not essential for murine erythropoiesis, growth, and development. Proc Natl Acad Sci USA 1966; 93: 13943-13948.
7. Itoh K, Wakabayashi N, Katoh Y, et al. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the aminoterminal Neh2 domain. Genes Dev 1999; 13: 76-86.
8. Kobayashi M, Itoh K, Suzuki T, et al. Identification of the interactive interface and phylogenic conservation of the Nrf2-Keap1 system. Genes Cells 2002; 7: 807-820.
9. Katoh Y, Iida K, Kang MI, et al. Evolutionary conserved N-terminal domain of Nrf2 is essential for the Keap1-mediated degradation of the protein by proteasome. Arch Biochem Biophys 2005; 433: 342-350.
10. Karapetian RN, Evstafieva AG, Abaeva IS, et al. Nuclear oncoprotein prothymosin alpha is a partner of Keap1: implications for expression of oxidative stress-protecting genes. Mol Cell Biol 2005; 25: 1089-1099.
11. Niture SK, Jaiswal AK. Inhibitor of Nrf2 (INrf2 or Keap1) protein degrades Bcl-xL via phosphoglyceratemutase 5 and controls cellular apoptosis. J Biol Chem 2011; 286: 44542-44556.
12. Xu Y, Fang F, Miriyala S, et al. KEAP1 is a redox sensitive target that arbitrates the opposing radiosensitive effects of parthenolide in normal and cancer cells. Cancer Res 2013; 73: 4406-4417.
13. Lee DF, Kuo HP, Liu M, et al. KEAP1 E3 ligase-mediated downregulation of NF-B signaling by targeting IKK?. Mol Cell 2009; 36: 131-140.
14. Komatsu M, Kurokawa H, Waguri S, et al. The selective autophagy substrate p62 activates the stress responsive transcription factor Nrf2 through inactivation of Keap1. Nat Cell Biol 2010; 12: 213-223.
15. Niture SK, Jaiswal AK. INrf2 (Keap1) targets Bcl-2 degradation and controls cellular apoptosis. Cell Death Differ 2011; 18: 439-451.
16. Ishii T, Yanagawa T, Kawane T, et al. Murine peritoneal macrophages induce a novel 60-kDa protein with structural similarity to a tyrosine kinase p56lck-associated protein in response to oxidative stress. Biochem Biophys Res Commun 1996; 226: 456-460.
17. Ishii T, Itoh K, Takahashi S, et al. Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J Biol Chem 2000; 275: 16023-16029.
18. Yoshikawa Y, Ogawa M, Hain T, et al. Listeria monocytogenes ActAmediated escape from autophagic recognition. Nat Cell Biol 2009; 11: 1233-1240.
19. Geisler S, Holmström KM, Skujat D, et al. PINK1/Parkin-mediated mitophagy is dependent on VDAC1 and p62/SQSTM1. Nat Cell Biol 2010; 12: 119-131.
20. Kosaka K, Mimura J, Itoh K, et al. Role of Nrf2 and p62/ZIP in the neurite outgrowth by carnosic acid in PC12h cells. J Biochem 2010; 147: 73-81.
21. Hancock R, Bertrand HC, Tsujita T, et al. Peptide inhibitors of the Keap1-Nrf2 protein-protein interaction. Free Radic Biol Med 2012; 52: 444-451.
22. Ichimura Y, Waguri S, Sou YS, et al. Phosphorylation of p62 activates the Keap1-Nrf2 pathway during selective autophagy. Mol Cell 2013; 51: 618-631.
23. Kwon J, Han E, Bui CB, et al. Assurance of mitochondrial integrity and mammalian longevity by the p62-Keap1-Nrf2-Nqo1 cascade. EMBO Rep 2012; 13: 150-156.
24. Seibenhener ML, Du Y, Diaz-Meco MT, Moscat J, Wooten MC, Wooten MW. A role for sequestosome 1/p62 in mitochondrial dynamics, import and genome integrity. Biochim Biophys Acta 2013; 1833: 452-459.
25. Seibenhener ML, Zhao T, Du Y, et al. Behavioral effects of SQSTM1/p62 overexpression in mice: support for a mitochondrial role in depression and anxiety. Behav Brain Res 2013; 248: 94-103.
26. Alam J, Cook JL. How many transcription factors does it take to turn on the heme oxygenase-1 gene? Am J Respir Cell Mol Biol 2007; 36: 166-174.
27. Piantadosi CA. Biological chemistry of carbon monoxide. Antioxid Redox Signal 2002; 4: 259-270.
28. D'Amico G, Lam F, Hagen T, Moncada S. Inhibition of cellular respiration by endogenously produced carbon monoxide. J Cell Sci 2006; 119: 2291-2298.
29. Suliman HB, Carraway MS, Tatro LG, Piantadosi CA. A new activating role for CO in cardiac mitochondrial biogenesis. J Cell Sci 2007; 120: 299-308.
30. Zhu H, Li Y. NAD(P)H: quinoneoxidoreductase 1 and its potential protective role in cardiovascular diseases and related conditions. Cardiovasc Toxicol 2012; 12: 39-45.
31. Dominy JE, Puigserver P. Mitochondrial biogenesis through activation of nuclear signaling proteins. Cold Spring Harb Perspect Biol 2013; 5. DOI: 10.1101/cshperspect.a015008
32. Piantadosi CA, Carraway MS, Babiker A, Suliman HB. Heme oxygenase-1 regulates cardiac mitochondrial biogenesis via Nrf2-mediated transcriptional control of nuclear respiratory factor-1. Circ Res 2008; 103: 1232-1240.
33. Piantadosi CA, Suliman HB. Mitochondrial transcription factor A induction by redox activation of nuclear respiratory factor 1. J Biol Chem 2006; 281: 324-333.
34. Athale J, Ulrich A, Macgarvey NC, et al. Nrf2 promotes alveolar mitochondrial biogenesis and resolution of lung injury in Staphylococcus aureus pneumonia in mice. Free Radic Biol Med 2012; 53: 1584-1594.
35. MacGarvey NC, Suliman HB, Bartz RR, et al. Activation of mitochondrial biogenesis by heme oxygenase-1-mediated NF-E2-related factor-2 induction rescues mice from lethal Staphylococcus aureus sepsis. Am J Respir Crit Care Med 2012; 185: 851-861.
36. Hota SK, Barhwal K, Singh SB, Sairam M, Ilavazhagan G. NR1 and GluR2 expression mediates excitotoxicity in chronic hypobaric hypoxia. J Neurosci Res 2008; 86: 1142-1152.
37. Barhwal K, Hota SK, Jain V, Prasad D, Singh SB, Ilavazhagan G. Acetyl-lcarnitine (ALCAR) prevents hypobaric hypoxia-induced spatial memory impairment through extracellular related kinase-mediated nuclear factor erythroid 2-related factor 2 phosphorylation. Neuroscience 2009; 161: 501-514.
38. Kosaka K, Mimura J, Itoh K, et al. Role of Nrf2 and p62/ZIP in the neurite outgrowth by carnosic acid in PC12h cells. J Biochem 2010; 147: 73-81.
39. Hota KB, Hota SK, Chaurasia OP, Singh SB. Acetyl-L-carnitine-mediated neuroprotection during hypoxia is attributed to ERK1/2-Nrf2-regulated mitochondrial biosynthesis. Hippocampus 2012; 22: 723-736.
40. Kim SK, Joe Y, Zheng M, et al. Resveratrol induces hepatic mitochondrial biogenesis through the sequential activation of nitric oxide and carbon monoxide production. Antioxid Redox Signal 2014; 20: 2589-2605.
41. Kim TH, Hur EG, Kang SJ, et al. NRF2 blockade suppresses colon tumor angiogenesis by inhibiting hypoxia-induced activation of HIF-1. Cancer Res 2011; 71: 2260-2275.
42. Holmström KM, Baird L, Zhang Y, et al. Nrf2 impacts cellular bioenergetics by controlling substrate availability for mitochondrial respiration. Biol Open 2013; 2: 761-770.
43. Ludtmann MH, Angelova PR, Zhang Y, Abramov AY, Dinkova-Kostova AT. Nrf2 affects the efficiency of mitochondrial fatty acid oxidation. Biochem J 2014; 457: 415-424.
44. Ricart KC, Bolisetty S, Johnson MS, et al. The permissive role of mitochondria in the induction of haem oxygenase-1 in endothelial cells. Biochem J 2009; 419: 427-436.
45. Scarffe LA, Stevens DA, Dawson VL, Dawson TM. Parkin and PINK1: much more than mitophagy. Trends Neurosci 2014; 37: 315-324.
46. Koh H, Chung J. PINK1 as a molecular checkpoint in the maintenance of mitochondrial function and integrity. Mol Cells 2012; 34: 7-13.
47. Pridgeon JW, Olzmann JA, Chin LS, Li L. PINK1 protects against oxidative stress by phosphorylating mitochondrial chaperone TRAP1. PLoS Biol 2007; 5: e172.
48. Chien WL, Lee TR, Hung SY, Kang KH, Lee MJ, Fu WM. Impairment of oxidative stress-induced heme oxygenase-1 expression by the defect of Parkinson-related gene of PINK1. J Neurochem 2011; 117: 643-653.
49. Clements CM, McNally RS, Conti BJ, Mak TW, Ting JP. DJ-1, a cancer-and Parkinson's disease-associated protein, stabilizes the antioxidant transcriptional master regulator Nrf2. Proc Natl Acad Sci USA 2006; 103: 15091-15096.
50. Malhotra D, Thimmulappa R, Navas-Acien A, et al. Decline in NRF2-regulated antioxidants in chronic obstructive pulmonary disease lungs due to loss of its positive regulator, DJ-1. Am J Respir Crit Care Med 2008; 178: 592-604.
51. Kim RH, Smith PD, Aleyasin H, et al. Hypersensitivity of DJ-1-deficient mice to 1-methyl-4-phenyl-1,2,3,6-tetrahydropyrindine (MPTP) and oxidative stress. Proc Natl Acad Sci USA 2005; 102: 5215-5220.
52. Canet-Avilés RM, Wilson MA, Miller DW, et al. The Parkinson's disease protein DJ-1 is neuroprotective due to cysteine-sulfinic acid-driven mitochondrial localization. Proc Natl Acad Sci U S A 2004; 101: 9103-9108.
53. Thomas KJ, McCoy MK, Blackinton J, et al. DJ-1 acts in parallel to the PINK1/parkin pathway to control mitochondrial function and autophagy. Hum Mol Genet 2011; 20: 40-50.
54. Aleyasin H, Rousseaux MW, Marcogliese PC. DJ-1 protects the nigrostriatal axis from the neurotoxin MPTP by modulation of the AKT pathway. Proc Natl Acad Sci U S A 2010; 107: 3186-3191.
55. Tanti GK, Goswami SK. SG2NA recruits DJ-1 and Akt into the mitochondria and membrane to protect cells from oxidative damage. Free Radic Biol Med 2014; 75: 1-13.
56. Gan L, Johnson DA, Johnson JA. Keap1-Nrf2 activation in the presence and absence of DJ-1. Eur J Neurosci 2010; 31: 967-977.
57. Pulliam DA, Bhattacharya A, Van Remmen H. Mitochondrial dysfunction in aging and longevity: A causal or protective role? Antioxid Redox Signal 2013; 19: 1373-1387.
58. Pulliam DA, Deepa SS, Liu Y, et al. Complex IV-deficient Surf1(-/-) mice initiate mitochondrial stress responses. Biochem J 2014; 462: 359-371.
59. Dassa EP, Paupe V, Gonçalves S, Rustin P. The mtDNA NARP mutation activates the actin-Nrf2 signaling of antioxidant defenses. Biochem Biophys Res Commun 2008; 368: 620-624.
60. Matigian, Abrahamsen G, Sutharsan R, et al. Disease-specific, neurospherederived cells as models for brain disorders. Dis Model Mech 2010; 3: 785-798.
61. Abrahamsen G, Fan Y, Matigian N, et al. A patient-derived stem cell model of hereditary spastic paraplegia with SPAST mutations. Dis Model Mech 2013; 6: 489-502.
62. Paupe V, Dassa EP, Goncalves S, et al. Impaired nuclear Nrf2 translocation undermines the oxidative stress response in Friedreich ataxia. PLoS One 2009; 4: e4253.
63. D'Oria V, Petrini S, Travaglini L, et al. Frataxin deficiency leads to reduced expression and impaired translocation of NF-E2-related factor 2 (Nrf2) in cultured motor neurons. Int J Mol Sci 2013; 14: 7853-7865.
64. Shan Y, Schoenfeld RA, Hayashi G, et al. Frataxin deficiency leads to defects in expression of antioxidants and Nrf2 expression in dorsal root ganglia of the Friedreich's ataxia YG8R mouse model. Antioxid Redox Signal 2013; 19: 1481-1493.
65. Sahdeo S, Scott BD, McMackin MZ, et al. Dyclonine rescues frataxin deficiency in animal models and buccal cells of patients with Friedreich's ataxia. Hum Mol Genet 2014; 23: 6848-6862.
66. Brand MD, Couture P, Else PL, Withers KW, Hulbert AJ. Evolution of energy metabolism. Proton permeability of the inner membrane of liver mitochondria is greater in a mammal than in a reptile. Biochem J 1991; 275: 81-86.
67. Anedda A, López-Bernardo E, Acosta-Iborra B, Saadeh Suleiman M, Landázuri MO, Cadenas S. The transcription factor Nrf2 promotes survival by enhancing the expression of uncouplingprotein 3 under conditions of oxidative stress. Free Radic Biol Med 2013; 61: 395-407.
68. Rada P, Rojo AI, Chowdhry S, McMahon M, Hayes JD, Cuadrado A. SCF/-TrCP promotes glycogen synthase kinase 3-dependent degradation of the Nrf2 transcription factor in a Keap1-independent manner. Mol Cell Biol 2011; 31: 1121-1133.
69. Jain AK, Jaiswal AK. GSK-3beta acts upstream of Fyn kinase in regulation of nuclear export and degradation of NF-E2 related factor 2. J Biol Chem 2007; 282: 16502-16510.