Nrf2-ARE activator carnosic acid decreases mitochondrial dysfunction, oxidative damage and neuronal cytoskeletal degradation following traumatic brain injury in mice

Experimental Neurology

Volumn 264, Issue , 2015, Pages 103-110

  Miller, Darren M ^a   Singh, Indrapal N ^a   Wang, Juan A ^a   Hall, Edward D ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

4 Hydroxy 2 nonenal; Lipid peroxidation; Mitochondria; Nrf2; Oxidative damage; Traumatic brain injury

Indexed keywords

4 HYDROXYNONENAL; ADENOSINE DIPHOSPHATE; CARNOSIC ACID; MITOCHONDRIAL PROTEIN; PLACEBO; REDUCED NICOTINAMIDE ADENINE DINUCLEOTIDE DEHYDROGENASE (UBIQUINONE); SPECTRIN; SUCCINATE DEHYDROGENASE (UBIQUINONE); SUCCINIC ACID; TRANSCRIPTION FACTOR NRF2; 4-HYDROXY-2-NONENAL; ABIETANE DERIVATIVE; ALDEHYDE; ANTIOXIDANT; PLANT EXTRACT;

ADULT; ANIMAL EXPERIMENT; ANIMAL MODEL; ANTIOXIDANT ACTIVITY; ANTIOXIDANT RESPONSIVE ELEMENT; ARTICLE; BRAIN CORTEX; BRAIN REGION; BRAIN TISSUE; CONTROLLED STUDY; CYTOSKELETON; DISORDERS OF MITOCHONDRIAL FUNCTIONS; DOSE RESPONSE; DRUG DOSE COMPARISON; DRUG EFFICACY; DRUG PROTEIN BINDING; DRUG TARGETING; LIPID PEROXIDATION; MALE; MITOCHONDRIAL RESPIRATION; MOUSE; MOUSE MODEL; NERVE CELL DEGENERATION; NEUROPROTECTION; NITRATION; NONHUMAN; OXIDATIVE STRESS; OXYGEN CONSUMPTION; PROTEIN DETERMINATION; PROTEIN EXPRESSION; PROTEIN LOCALIZATION; TISSUE DISTRIBUTION; TRANSCRIPTION INITIATION; TRAUMATIC BRAIN INJURY; YOUNG ADULT; ANALYSIS OF VARIANCE; ANIMAL; BRAIN; BRAIN INJURIES; COMPLICATION; DISEASE MODEL; DRUG EFFECTS; METABOLISM; MITOCHONDRIAL DISEASES; PATHOLOGY;

ADENOSINE DIPHOSPHATE; ALDEHYDES; ANALYSIS OF VARIANCE; ANIMALS; ANTIOXIDANTS; BRAIN; BRAIN INJURIES; CYTOSKELETON; DISEASE MODELS, ANIMAL; DITERPENES, ABIETANE; DOSE-RESPONSE RELATIONSHIP, DRUG; LIPID PEROXIDATION; MALE; MICE; MITOCHONDRIAL DISEASES; OXIDATIVE STRESS; PLANT EXTRACTS; SUCCINIC ACID;

EID: 84919774511     PISSN: 00144886     EISSN: 10902430     Source Type: Journal    
DOI: 10.1016/j.expneurol.2014.11.008     Document Type: Article

References (41)

1. Deng Y., Thompson B.M., Gao X., Hall E.D. Temporal relationship of peroxynitrite-induced oxidative damage, calpain-mediated cytoskeletal degradation and neurodegeneration after traumatic brain injury. Exp. Neurol. 2007, 205(1):154-165. (May).
2. Singh I.N., Sullivan P.G., Deng Y., Mbye L.H., Hall E.D. Time course of post-traumatic mitochondrial oxidative damage and dysfunction in a mouse model of focal traumatic brain injury: implications for neuroprotective therapy. J. Cereb. Blood Flow Metab. 2006, 26(11):1407-1418. (Nov).
3. Thurman D.J., Alverson C., Dunn K.A., Guerrero J., Sniezek J.E. Traumatic brain injury in the United States: a public health perspective. J. Head Trauma Rehabil. 1999, 14(6):602-615. (Dec).
4. Smith S.L., Andrus P.K., Zhang J.R., Hall E.D. Direct measurement of hydroxyl radicals, lipid peroxidation, and blood-brain barrier disruption following unilateral cortical impact head injury in the rat. J. Neurotrauma 1994, 11(4):393-404. (Aug).
5. Ansari M.A., Roberts K.N., Scheff S.W. Oxidative stress and modification of synaptic proteins in hippocampus after traumatic brain injury. Free Radic. Biol. Med. 2008, 45(4):443-452. (Aug 15).
6. Kontos H.A., Wei E.P. Superoxide production in experimental brain injury. J. Neurosurg. 1986, 64(5):803-807. (May).
7. Vaishnav R.A., Singh I.N., Miller D.M., Hall E.D. Lipid peroxidation-derived reactive aldehydes directly and differentially impair spinal cord and brain mitochondrial function. J. Neurotrauma 2010, 27(7):1311-1320. (Jul).
8. Bains M., Hall E.D. Antioxidant therapies in traumatic brain and spinal cord injury. Biochim. Biophys. Acta 2012, 1822(5):675-684. (May).
9. Pandya J.D., Pauly J.R., Nukala V.N., Sebastian A.H., Day K.M., Korde A.S., et al. Post-injury administration of mitochondrial uncouplers increases tissue sparing and improves behavioral outcome following traumatic brain injury in rodents. J. Neurotrauma 2007, 24(5):798-811. (May).
10. Azbill R.D., Mu X., Bruce-Keller A.J., Mattson M.P., Springer J.E. Impaired mitochondrial function, oxidative stress and altered antioxidant enzyme activities following traumatic spinal cord injury. Brain Res. 1997, 765(2):283-290. (Aug 15).
11. Sullivan P.G., Thompson M.B., Scheff S.W. Cyclosporin A attenuates acute mitochondrial dysfunction following traumatic brain injury. Exp. Neurol. 1999, 160(1):226-234. (Nov).
12. Singh I.N., Sullivan P.G., Hall E.D. Peroxynitrite-mediated oxidative damage to brain mitochondria: protective effects of peroxynitrite scavengers. J. Neurosci. Res. 2007, 85(10):2216-2223. (Aug 1).
13. Deng-Bryant Y., Singh I.N., Carrico K.M., Hall E.D. Neuroprotective effects of tempol, a catalytic scavenger of peroxynitrite-derived free radicals, in a mouse traumatic brain injury model. J. Cereb. Blood Flow Metab. 2008, 28(6):1114-1126. (Jun).
14. Kensler T.W., Wakabayashi N., Biswal S. Cell survival responses to environmental stresses via the Keap1-Nrf2-ARE pathway. Annu. Rev. Pharmacol. Toxicol. 2007, 47:89-116.
15. Chan J.Y., Han X.L., Kan Y.W. Isolation of cDNA encoding the human NF-E2 protein. Proc. Natl. Acad. Sci. U. S. A. 1993, 90(23):11366-11370. (Dec 1).
16. Itoh K., Wakabayashi N., Katoh Y., Ishii T., Igarashi K., Engel J.D., et al. Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain. Genes Dev. 1999, 13(1):76-86. (Jan 1).
17. Moi P., Chan K., Asunis I., Cao A., Kan Y.W. 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. 1994, 91(21):9926-9930. (Oct 11).
18. Kobayashi A., Kang M.I., Okawa H., Ohtsuji M., Zenke Y., Chiba T., et al. Oxidative stress sensor Keap1 functions as an adaptor for Cul3-based E3 ligase to regulate proteasomal degradation of Nrf2. Mol. Cell. Biol. 2004, 24(16):7130-7139. (Aug).
19. Tong K.I., Kobayashi A., Katsuoka F., Yamamoto M. Two-site substrate recognition model for the Keap1-Nrf2 system: a hinge and latch mechanism. Biol. Chem. 2006, 387(10-11):1311-1320. (Oct-Nov).
20. Jain A.K., Bloom D.A., Jaiswal A.K. Nuclear import and export signals in control of Nrf2. J. Biol. Chem. 2005, 280(32):29158-29168. (Aug 12).
21. Johnson J.A., Johnson D.A., Kraft A.D., Calkins M.J., Jakel R.J., Vargas M.R., et al. The Nrf2-ARE pathway: an indicator and modulator of oxidative stress in neurodegeneration. Ann. N. Y. Acad. Sci. 2008, 1147:61-69. (Dec).
22. Calkins M.J., Jakel R.J., Johnson D.A., Chan K., Kan Y.W., Johnson J.A. Protection from mitochondrial complex II inhibition in vitro and in vivo by Nrf2-mediated transcription. Proc. Natl. Acad. Sci. U. S. A. 2005, 102(1):244-249. (Jan 4).
23. Rojo A.I., Innamorato N.G., Martin-Moreno A.M., De Ceballos M.L., Yamamoto M., Cuadrado A. Nrf2 regulates microglial dynamics and neuroinflammation in experimental Parkinson's disease. Glia 2010, 58(5):588-598. (Apr).
24. Li J., Johnson D., Calkins M., Wright L., Svendsen C., Johnson J. Stabilization of Nrf2 by tBHQ confers protection against oxidative stress-induced cell death in human neural stem cells. Toxicol. Sci. 2005, 83(2):313-328. (Feb).
25. Vargas M.R., Johnson D.A., Sirkis D.W., Messing A., Johnson J.A. Nrf2 activation in astrocytes protects against neurodegeneration in mouse models of familial amyotrophic lateral sclerosis. J. Neurosci. 2008, 28(50):13574-13581. (Dec 10).
26. Zhao X., Sun G., Zhang J., Strong R., Dash P.K., Kan Y.W., et al. Transcription factor Nrf2 protects the brain from damage produced by intracerebral hemorrhage. Stroke 2007, 38(12):3280-3286. (Dec).
27. Son T.G., Camandola S., Arumugam T.V., Cutler R.G., Telljohann R.S., Mughal M.R., et al. Plumbagin, a novel Nrf2/ARE activator, protects against cerebral ischemia. J. Neurochem. 2010, 112(5):1316-1326. (Mar).
28. Jin W., Wang H., Yan W., Zhu L., Hu Z., Ding Y., et al. Role of Nrf2 in protection against traumatic brain injury in mice. J. Neurotrauma 2009, 26(1):131-139. (Jan).
29. Zhao J., Moore A.N., Redell J.B., Dash P.K. Enhancing expression of Nrf2-driven genes protects the blood brain barrier after brain injury. J. Neurosci. 2007, 27(38):10240-10248. (Sep 19).
30. Zhao J., Moore A.N., Clifton G.L., Dash P.K. Sulforaphane enhances aquaporin-4 expression and decreases cerebral edema following traumatic brain injury. J. Neurosci. Res. 2005, 82(4):499-506. (Nov 15).
31. Dash P.K., Zhao J., Orsi S.A., Zhang M., Moore A.N. Sulforaphane improves cognitive function administered following traumatic brain injury. Neurosci. Lett. 2009, 460(2):103-107. (Aug 28).
32. Satoh T., Kosaka K., Itoh K., Kobayashi A., Yamamoto M., Shimojo Y., et al. Carnosic acid, a catechol-type electrophilic compound, protects neurons both in vitro and in vivo through activation of the Keap1/Nrf2 pathway via S-alkylation of targeted cysteines on Keap1. J. Neurochem. 2008, 104(4):1116-1131. (Feb).
33. Greco T., Fiskum G. Brain mitochondria from rats treated with sulforaphane are resistant to redox-regulated permeability transition. J. Bioenerg. Biomembr. 2010, 42(6):491-497. (Dec).
34. Miller D.M., Singh I.N., Wang J.A., Hall E.D. Administration of the Nrf2-ARE activators sulforaphane and carnosic acid attenuates 4-hydroxy-2-nonenal-induced mitochondrial dysfunction ex vivo. Free Radic. Biol. Med. 2013, 57:1-9. (Apr).
35. Hall E.D., Wang J.A., Miller D.M. Relationship of nitric oxide synthase induction to peroxynitrite-mediated oxidative damage during the first week after experimental traumatic brain injury. Exp. Neurol. 2012, 238(2):176-182. (Dec).
36. Marshall L.F., Maas A.I., Marshall S.B., Bricolo A., Fearnside M., Iannotti F., et al. A multicenter trial on the efficacy of using tirilazad mesylate in cases of head injury. J. Neurosurg. 1998, 89(4):519-525. (Oct).
37. Miller D.M., Wang J.A., Buchanan A.K., Hall E.D. Temporal and spatial dynamics of Nrf2-ARE mediated gene targets in cortex and hippocampus following controlled cortical impact traumatic brain injury in mice. J. Neurotrauma 2014, 31:1194-1201. (Mar 14).
38. Wang K.K. Calpain and caspase: can you tell the difference?. Trends Neurosci. 2000, 23(1):20-26. (Jan).
39. Thompson S.N., Gibson T.R., Thompson B.M., Deng Y., Hall E.D. Relationship of calpain-mediated proteolysis to the expression of axonal and synaptic plasticity markers following traumatic brain injury in mice. Exp. Neurol. 2006, 201(1):253-265. (Sep).
40. Mustafa A.G., Wang J.A., Carrico K.M., Hall E.D. Pharmacological inhibition of lipid peroxidation attenuates calpain-mediated cytoskeletal degradation after traumatic brain injury. J. Neurochem. 2011, 117(3):579-588. (May).
41. Mbye L.H., Singh I.N., Carrico K.M., Saatman K.E., Hall E.D. Comparative neuroprotective effects of cyclosporin A and NIM811, a nonimmunosuppressive cyclosporin A analog, following traumatic brain injury. J. Cereb. Blood Flow Metab. 2009, 29(1):PMC2755489-PMC2755497. (Jan, Epub 2008 Aug 20. PubMed PMID: 18714331; PubMed Central PMCID). 10.1038/jcbfm.2008.93.