Modulation of transcription factor Nrf2 in an in vitro model of traumatic brain injury

Journal of Neurotrauma

Volumn 29, Issue 6, 2012, Pages 1188-1196

  Hatic, Haris ^a   Kane, Michael J ^a   Saykally, Jessica N ^a,b   Citron, Bruce A ^a,b  

^a VETERANS AFFAIRS MEDICAL CENTER   (United States)

^b UNIVERSITY OF SOUTH FLORIDA   (United States)

Author keywords

apoptosis; in vitro studies; model of injury; neuronal cell death; traumatic brain injury

Indexed keywords

HEAT SHOCK PROTEIN 70; TERT BUTYLHYDROQUINONE; TRANSCRIPTION FACTOR NRF2;

ARTICLE; CANCER CELL CULTURE; CELL ACTIVATION; CELL DIFFERENTIATION; CELL VIABILITY; CONTROLLED STUDY; HUMAN; HUMAN CELL; IN VITRO STUDY; NEUROBLASTOMA CELL; NUCLEOTIDE SEQUENCE; PROTEIN EXPRESSION; REAL TIME POLYMERASE CHAIN REACTION; TRAUMATIC BRAIN INJURY; UPREGULATION; WESTERN BLOTTING;

ANTIOXIDANTS; BLOTTING, WESTERN; BRAIN INJURIES; CELL LINE; CELL SURVIVAL; ELECTROPHORETIC MOBILITY SHIFT ASSAY; GENE EXPRESSION REGULATION; HSP70 HEAT-SHOCK PROTEINS; HUMANS; HYDROQUINONES; IMMUNOHISTOCHEMISTRY; NEURONS; NF-E2-RELATED FACTOR 2; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; THIOREDOXINS;

EID: 84859890473     PISSN: 08977151     EISSN: 15579042     Source Type: Journal    
DOI: 10.1089/neu.2011.1806     Document Type: Article

References (56)

1. Aarskog, N.K., and Vedeler, C.A. (2000). Real-time quantitative polymerase chain reaction. A new method that detects both the peripheral myelin protein 22 duplication in Charcot- Marie-Tooth type 1A disease and the peripheral myelin protein 22 deletion in hereditary neuropathy with liability to pressure palsies. Hum. Genet. 107, 494-498. (Pubitemid 32000420)
2. Annegers, J.F., Grabow, J.D., Kurland, L.T., and Laws, E.R., Jr. (1980). The incidence, causes, and secular trends of head trauma in Olmsted County, Minnesota, 1935-1974. Neurology 30, 912-919. (Pubitemid 10059240)
3. Arner, E.S., and Holmgren, A. (2000). Physiological functions of thioredoxin and thioredoxin reductase. Eur. J. Biochem. 267, 6102-6109.
4. Atkins, C.M., Oliva, A.A., Jr., Alonso, O.F., Pearse, D.D., Bramlett, H.M., and Dietrich, W.D. (2007). Modulation of the cAMP signaling pathway after traumatic brain injury. Exp. Neurol. 208, 145-158. (Pubitemid 47600157)
5. Borland, M.K., Trimmer, P.A., Rubinstein, J.D., Keeney, P.M., Mohanakumar, K., Liu, L., and Bennett, J.P., Jr. (2008). Chronic, low-dose rotenone reproduces Lewy neurites found in early stages of Parkinson's disease, reduces mitochondrial movement and slowly kills differentiated SH-SY5Y neural cells. Mol. Neurodegener. 3, 21.
6. Brooks, A.R., Lelkes, P.I., and Rubanyi, G.M. (2002). Gene expression profiling of human aortic endothelial cells exposed to disturbed flow and steady laminar flow. Physiol. Genomics 9, 27-41. (Pubitemid 135707410)
7. Bruns J., Jr. and Hauser, W.A. (2003). The epidemiology of traumatic brain injury: a review. Epilepsia 44(Suppl. 10), 2-10. (Pubitemid 37280386)
8. Bullock, M.R., Lyeth, B.G., and Muizelaar, J.P. (1999). Current status of neuroprotection trials for traumatic brain injury: lessons from animal models and clinical studies. Neurosurgery 45, 207-217; discussion 217-220.
9. Calabrese, V., Signorile, A., Cornelius, C., Mancuso, C., Scapagnini, G., Ventimiglia, B., Ragusa, N., and Dinkova- Kostova, A. (2008). Practical approaches to investigate redox regulation of heat shock protein expression and intracellular glutathione redox state. Methods Enzymol. 441, 83-110.
10. Cha, M.K., Suh, K.H., and Kim, I.H. (2009). Overexpression of peroxiredoxin I and thioredoxin1 in human breast carcinoma. J. Exp. Clin. Cancer Res. 28, 93.
11. Chirgwin, J.M., Przybyla, A.E., MacDonald, R.J., and Rutter, W.J. (1979). Isolation of biologically active ribonucleic acid from sources enriched in ribonuclease. Biochemistry 18, 5294-5299. (Pubitemid 10140274)
12. Dennis, J.S., and Citron, B.A. (2009). Wobbler mice modeling motor neuron disease display elevated transactive response DNA binding protein. Neuroscience 158, 745-750.
13. Echemendia, R.J., and Julian, L.J. (2001). Mild traumatic brain injury in sports: neuropsychology's contribution to a developing field. Neuropsychol. Rev. 11, 69-88. (Pubitemid 33744605)
14. Ellis, E.F., McKinney, J.S., Willoughby, K.A., Liang, S., and Povlishock, J.T. (1995). A new model for rapid stretch-induced injury of cells in culture: characterization of the model using astrocytes. J. Neurotrauma 12, 325-339.
15. Endo, H., Sugioka, Y., Nakagi, Y., Saijo, Y., and Yoshida, T. (2008). A novel role of the NRF2 transcription factor in the regulation of arsenite-mediated keratin 16 gene expression in human keratinocytes. Environ. Health Perspect. 116, 873-879. (Pubitemid 351943893)
16. Ewing-Cobbs, L., Brookshire, B., Scott, M.A., and Fletcher, J.M. (1998). Children's narratives following traumatic brain injury: linguistic structure, cohesion, and thematic recall. Brain Lang. 61, 395-419. (Pubitemid 28268653)
17. Foster, J.A., and Brown, I.R. (1997). Differential induction of heat shock mRNA in oligodendrocytes, microglia, and astrocytes following hyperthermia. Brain Res. Mol. Brain Res. 45, 207-218. (Pubitemid 27170697)
18. Gius, D., Botero, A., Shah, S., and Curry, H.A. (1999). Intracellular oxidation/reduction status in the regulation of transcription factors NF-kappaB and AP-1. Toxicol. Lett. 106, 93-106. (Pubitemid 29257819)
19. Greve, M.W., and Zink, B.J. (2009). Pathophysiology of traumatic brain injury. Mt. Sinai J. Med. 76, 97-104.
20. Hattori, I., Takagi, Y., Nozaki, K., Kondo, N., Bai, J., Nakamura, H., Hashimoto, N., and Yodoi, J. (2002). Hypoxia-ischemia induces thioredoxin expression and nitrotyrosine formation in new-born rat brain. Redox Rep. 7, 256-259. (Pubitemid 36032909)
21. Heneka, M.T., Sharp, A., Murphy, P., Lyons, J.A., Dumitrescu, L., and Feinstein, D.L. (2001). The heat shock response reduces myelin oligodendrocyte glycoprotein-induced experimental autoimmune encephalomyelitis in mice. J. Neurochem. 77, 568-579. (Pubitemid 32298751)
22. Hirota, K., Murata, M., Sachi, Y., Nakamura, H., Takeuchi, J., Mori, K., and Yodoi, J. (1999). Distinct roles of thioredoxin in the cytoplasm and in the nucleus. A two-step mechanism of redox regulation of transcription factor NF-kappaB. J. Biol. Chem. 274, 27891-27897.
23. Hoge, C.W., McGurk, D., Thomas, J.L., Cox, A.L., Engel, C.C., and Castro, C.A. (2008). Mild traumatic brain injury in U.S. Soldiers returning from Iraq. N. Engl. J. Med. 358, 453-463. (Pubitemid 351185801)
24. Holmgren, A. (1985). Thioredoxin. Annu. Rev. Biochem. 54, 237-271.
25. Inglese, M., Makani, S., Johnson, G., Cohen, B.A., Silver, J.A., Gonen, O., and Grossman, R.I. (2005). Diffuse axonal injury in mild traumatic brain injury: a diffusion tensor imaging study. J. Neurosurg. 103, 298-303. (Pubitemid 43193906)
26. Ishii, T., Itoh, K., Takahashi, S., Sato, H., Yanagawa, T., Katoh, Y., Bannai, S., and Yamamoto, M. (2000). Transcription factor Nrf2 coordinately regulates a group of oxidative stress-inducible genes in macrophages. J. Biological Chem. 275, 16023-16029. (Pubitemid 30366908)
27. Jaiswal, A.K. (2004). Nrf2 signaling in coordinated activation of antioxidant gene expression. Free Rad. Biol. Mede. 36, 1199-1207. (Pubitemid 38526313)
28. Jakel, R.J., Townsend, J.A., Kraft, A.D., and Johnson, J.A. (2007). Nrf2-mediated protection against 6-hydroxydopamine. Brain Res. 1144, 192-201. (Pubitemid 46440842)
29. Jin, W., Wang, H., Yan, W., Zhu, L., Hu, Z., Ding, Y., and Tang, K. (2009). Role of Nrf2 in protection against traumatic brain injury in mice. J. Neurotrauma 26, 131-139.
30. Kahle, K.T., Simard, J.M., Staley, K.J., Nahed, B.V., Jones, P.S., and Sun, D. (2009). Molecular mechanisms of ischemic cerebral edema: role of electroneutral ion transport. Physiology (Bethesda) 24, 257-265.
31. Kane, M.J., and Citron, B.A. (2009). Transcription factors as therapeutic targets in CNS disorders. Recent Pat. CNS Drug Discov. 4, 190-199.
32. Kane, M.J., Hatic, H., Delic, V., Dennis, J.S., Butler, C.L., Saykally, J.N., and Citron, B.A. (2011). Modeling the pathobiology of repetitive traumatic brain injury in immortalized neuronal cell lines. Brain Res. 1425, 122-130.
33. Kaspar, J.W., Niture, S.K., and Jaiswal, A.K. (2009). Nrf2:INrf2 (Keap1) signaling in oxidative stress. Free Radic. Biol. Med. 47, 1304-1309.
34. Kelly, S., and Yenari, M.A. (2002). Neuroprotection: heat shock proteins. Curr. Med. Res. Opin. 18 (Suppl. 2), s55-s60.
35. Kim, Y.C., Masutani, H., Yamaguchi, Y., Itoh, K., Yamamoto, M., and Yodoi, J. (2001). Hemin-induced activation of the thioredoxin gene by Nrf2. A differential regulation of the antioxidant responsive element by a switch of its binding factors. J. Biol. Chem. 276, 18399-18406.
36. Langlois, J.A., Rutland-Brown, W., and Wald, M.M. (2006). The epidemiology and impact of traumatic brain injury: a brief overview. J. Head Trauma Rehabil. 21, 375-378. (Pubitemid 44413110)
37. Lee, J.M., Li, J., Johnson, D.A., Stein, T.D., Kraft, A.D., Calkins, M.J., Jakel, R.J., and Johnson, J.A. (2005). Nrf2, a multi-organ protector? FASEB J. 19, 1061-1066. (Pubitemid 40946431)
38. Li, C.Q., Kim, M.Y., Godoy, L.C., Thiantanawat, A., Trudel, L.J., and Wogan, G.N. (2009). Nitric oxide activation of Keap1/Nrf2 signaling in human colon carcinoma cells. Proc. Natl. Acad. Sci. USA 106, 14547-14551.
39. Li, J., Johnson, D., Calkins, M., Wright, L., Svendsen, C., and Johnson, J. (2005). Stabilization of Nrf2 by tBHQ confers protection against oxidative stress-induced cell death in human neural stem cells. Toxicol. Sci. 83, 313-328. (Pubitemid 40227901)
40. Masutani, H., Ueda, S., and Yodoi, J. (2005). The thioredoxin system in retroviral infection and apoptosis. Cell Death Differ. 12(Suppl. 1), 991-998. (Pubitemid 41030612)
41. Meaney, D.F., and Smith, D.H. (2011). Biomechanics of concussion. Clin. Sports Med. 30, 19-31, vii.
42. Niso-Santano, M., Gonzalez-Polo, R.A., Bravo-San Pedro, J.M., Gomez-Sanchez, R., Lastres-Becker, I., Ortiz-Ortiz, M.A., Soler, G., Moran, J.M., Cuadrado, A., and Fuentes, J.M. (2010). Activation of apoptosis signal-regulating kinase 1 is a key factor in paraquat-induced cell death: modulation by the Nrf2/Trx axis. Free Radic. Biol. Med. 48, 1370-1381.
43. Powis, G., and Montfort, W.R. (2001). Properties and biological activities of thioredoxins. Annu. Rev. Biophys. Biomol. Struct. 30, 421-455. (Pubitemid 32566170)
44. Saitoh, M., Nishitoh, H., Fujii, M., Takeda, K., Tobiume, K., Sawada, Y., Kawabata, M., Miyazono, K., and Ichijo, H. (1998). Mammalian thioredoxin is a direct inhibitor of apoptosis signalregulating kinase (ASK) 1. EMBO J. 17, 2596-2606. (Pubitemid 28221195)
45. Shah, Z.A., Li, R.C., Thimmulappa, R.K., Kensler, T.W., Yamamoto, M., Biswal, S., and Dore, S. (2007). Role of reactive oxygen species in modulation of Nrf2 following ischemic reperfusion injury. Neuroscience 147, 53-59. (Pubitemid 46881103)
46. Shih, A.Y., Erb, H., and Murphy, T.H. (2007). Dopamine activates Nrf2-regulated neuroprotective pathways in astrocytes and meningeal cells. J. Neurochem. 101, 109-119. (Pubitemid 46426469)
47. Shih, A.Y., Li, P., and Murphy, T.H. (2005). A small-moleculeinducible Nrf2-mediated antioxidant response provides effective prophylaxis against cerebral ischemia in vivo. J. Neurosci. 25, 10321-10335. (Pubitemid 41636229)
48. Soundararajan, R., Wishart, A.D., Rupasinghe, H.P., Arcellana- Panlilio, M., Nelson, C.M., Mayne, M., and Robertson, G.S. (2008). Quercetin 3-glucoside protects neuroblastoma (SHSY5Y) cells in vitro against oxidative damage by inducing sterol regulatory element-binding protein-2-mediated cholesterol biosynthesis. J. Biol. Chem. 283, 2231-2245.
49. Tavaria, M., Gabriele, T., Anderson, R.L., Mirault, M.E., Baker, E., Sutherland, G., and Kola, I. (1995). Localization of the gene encoding the human heat shock cognate protein, HSP73, to chromosome 11. Genomics 29, 266-268.
50. Thurman, D., and Guerrero, J. (1999). Trends in hospitalization associated with traumatic brain injury. JAMA 282, 954-957. (Pubitemid 29420314)
51. Turturici, G., Sconzo, G., and Geraci, F. (2011). Hsp70 and its molecular role in nervous system diseases. Biochem. Res. Int. 2011, 618127.
52. Ueno, M., Masutani, H., Arai, R.J., Yamauchi, A., Hirota, K., Sakai, T., Inamoto, T., Yamaoka, Y., Yodoi, J., and Nikaido. T. (1999). Thioredoxin-dependent redox regulation of p53- mediated p21 activation. J. Biol. Chem. 274, 35809-35815. (Pubitemid 129512885)
53. Venugopal, R., and Jaiswal, A.K. (1998). Nrf2 and Nrf1 in association with Jun proteins regulate antioxidant response element-mediated expression and coordinated induction of genes encoding detoxifying enzymes. Oncogene 17, 3145-3156. (Pubitemid 29020810)
54. Watson, W.H., Yang, X., Choi, Y.E., Jones, D.P., and Kehrer, J.P. (2004). Thioredoxin and its role in toxicology. Toxicol. Sci. 78, 3-14. (Pubitemid 38401016)
55. Werner, C., and Engelhard, K. (2007). Pathophysiology of traumatic brain injury. Br. J. Anaesth. 99, 4-9. (Pubitemid 47072553)
56. Zhang, Y., Ba, Y., Liu, C., Sun, G., Ding, L., Gao, S., Hao, J., Yu, Z., Zhang, J., Zen, K., Tong, Z., Xiang, Y., and Zhang, C.Y. (2007). PGC-1alpha induces apoptosis in human epithelial ovarian cancer cells through a PPARgamma-dependent pathway. Cell Res. 17, 363-373. (Pubitemid 46639941)