NF-E2-related factor 2 activation in PC12 cells: Its protective role in manganese-induced damage

Archives of Toxicology

Volumn 85, Issue 8, 2011, Pages 901-910

  Li, Huangyuan ^a   Wu, Siying ^a   Shi, Nian ^b   Lin, Wei ^a   You, Junyi ^a   Zhou, Wenhua ^a  

^a FUJIAN MEDICAL UNIVERSITY   (China)

^b HUAZHONG UNIVERSITY OF SCIENCE AND TECHNOLOGY   (China)

Author keywords

Apoptosis; Heme oxygenase 1 (HO 1); Manganese chloride; NF E2 related factor 2 (Nrf2); tert Butylhydroquinone (tBHQ)

Indexed keywords

MANGANESE CHLORIDE; TERT BUTYLHYDROQUINONE; TRANSCRIPTION FACTOR NRF2;

ANTIOXIDANT ACTIVITY; ANTIOXIDANT RESPONSIVE ELEMENT; APOPTOSIS; ARTICLE; BINDING AFFINITY; CELL SURVIVAL; CONTROLLED STUDY; CYTOTOXICITY; DRUG MECHANISM; GENE; GENE ACTIVATION; GENE EXPRESSION REGULATION; GENE FUNCTION; GENE LOCATION; GENE SEQUENCE; HEME OXYGENASE 1 GENE; INTOXICATION; NEUROPROTECTION; NEUROTOXICITY; NF E2 RELATED FACTOR 2 GENE; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHEOCHROMOCYTOMA CELL; PRIORITY JOURNAL; PROTEIN BINDING; REGULATOR GENE;

ANIMALS; APOPTOSIS; CHLORIDES; GENE EXPRESSION REGULATION, ENZYMOLOGIC; HEME OXYGENASE-1; HYDROQUINONES; MANGANESE COMPOUNDS; NEUROPROTECTIVE AGENTS; NEUROTOXICITY SYNDROMES; NF-E2-RELATED FACTOR 2; OXIDATIVE STRESS; PC12 CELLS; RATS; RESPONSE ELEMENTS;

RATTUS;

EID: 80052783408     PISSN: 03405761     EISSN: 14320738     Source Type: Journal    
DOI: 10.1007/s00204-010-0625-6     Document Type: Article

References (50)

1. J Alam D Stewart C Touchard S Boinapally AM Choi JL Cook 1999 Nrf2, a Cap'n'Collar transcription factor, regulates induction of the heme oxygenase-1 gene J Biol Chem 274 26071 26078 10473555 10.1074/jbc.274.37.26071 1:CAS:528:DyaK1MXmtVKmt7c%3D (Pubitemid 29437049)
2. M Aschner 2000 Manganese: brain transport and emerging research needs Environ Health Perspect 108 429 432 10852840 10.2307/3454532 1:CAS:528:DC%2BD3cXlsF2iu7k%3D (Pubitemid 30466168)
3. M Aschner TR Guilarte JS Schneider W Zheng 2007 Manganese: recent advances in understanding its transport and neurotoxicity Toxicol Appl Pharmacol 221 131 147 17466353 10.1016/j.taap.2007.03.001 1:CAS:528:DC%2BD2sXlvVOltL4%3D (Pubitemid 46779052)
4. S Braun C Hanselmann MG Gassmann U auf dem Keller C Born-Berclaz K Chan YW Kan S Werner 2002 Nrf2 transcription factor, a novel target of keratinocyte growth factor action which regulates gene expression and inflammation in the healing skin wound Mol Cell Biol 22 5492 5505 12101242 10.1128/MCB.22.15.5492- 5505.2002 1:CAS:528:DC%2BD38XltlGntrc%3D (Pubitemid 34755759)
5. ET Brouillet I Shinova U McGarvey F Hochberg MF Beal 1993 Manganese injection into the rat striatum produces excitotoxic lesions by impairing energy metabolism Exp Neurol 120 89 94 8477830 10.1006/exnr.1993.1042 1:CAS:528:DyaK3sXisV2nurw%3D (Pubitemid 23114032)
6. NC Burton TW Kensler TR Guilarte 2006 In vivo modulation of the Parkinsonian phenotype by Nrf2 NeuroToxicology 27 1094 1100 16959318 10.1016/j.neuro.2006.07.019 1:CAS:528:DC%2BD28Xht12rsLnK (Pubitemid 44838961)
7. MJ Calkins DA Johnson JA Townsend MR Vargas JA Dowell TP Williamson AD Kraft JM Lee J Li JA Johnson 2009 The Nrf2/ARE pathway as a potential therapeutic target in neurodegenerative disease Antioxid Redox Signal 11 497 508 18717629 10.1089/ars.2008.2242 1:CAS:528:DC%2BD1MXhtFOrtLg%3D
8. DB Calne NS Chu CC Huang CS Lu W Olanow 1994 Manganism and idiopathic parkinsonism: similarities and differences Neurology 44 1583 1586 7936278 1:STN:280:DyaK2M%2Fit1ansA%3D%3D (Pubitemid 24286629)
9. CY Chen JH Jang MH Li YJ Surh 2005 Resveratrol upregulates heme oxygenase-1 expression via activation of NF-E2-related factor 2 in PC12 cells Biochem Biophys Res Commun 331 993 1000 15882976 10.1016/j.bbrc.2005.03.237 1:CAS:528:DC%2BD2MXjvFemtLg%3D (Pubitemid 40692459)
10. PC Chen MR Vargas AK Pani RJ Smeyne DA Johnson YW Kan JA Johnson 2009 Nrf2-mediated neuroprotection in the MPTP mouse model of Parkinson's disease: critical role for the astrocyte Proc Natl Acad Sci USA 106 2933 2938 19196989 10.1073/pnas.0813361106 1:CAS:528:DC%2BD1MXislSkurg%3D
11. DH Chui W Tang SH Orkin 1995 cDNA cloning of murine Nrf 2 gene, coding for a p45 NF-E2 related transcription factor Biochem Biophys Res Commun 209 40 46 7726861 10.1006/bbrc.1995.1467 1:CAS:528:DyaK2MXkvFOqtbs%3D
12. A Cuadrado P Moreno-Murciano J Pedraza-Chaverri 2009 The transcription factor Nrf2 as a new therapeutic target in Parkinson's disease Expert Opin Ther Targets 13 319 329 19236154 10.1517/13543780802716501 1:CAS:528: DC%2BD1MXitFKnu74%3D
13. HE de Vries M Witte D Hondius AJ Rozemuller B Drukarch J Hoozemans J van Horssen 2008 Nrf2-induced antioxidant protection: a promising target to counteract ROS-mediated damage in neurodegenerative disease? Free Radic Biol Med 45 1375 1383 18824091 10.1016/j.freeradbiomed.2008.09.001
14. MS Desole M Miele G Esposito R Migheli L Fresu G De Natale E Miele 1994 Dopaminergic system activity and cellular defense mechanisms in the striatum and striatal synaptosomes of the rat subchronically exposed to manganese Arch Toxicol 68 566 570 7998823 10.1007/s002040050115 1:CAS:528:DyaK2MXit12qtrc%3D (Pubitemid 24279379)
15. MS Desole L Sciola MR Delogu S Sircana R Migheli 1996 Manganese and 1-methyl-4-(2 V-ethylpheny1)-1,2,3,6-tetrahydropyridine induce apoptosis in PC12 cells Neurosci Lett 209 193 196 8736643 10.1016/0304-3940(96)12645-8 1:CAS:528:DyaK28Xjt1Slsrk%3D
16. JM Gorell CC Johnson BA Rybicki EL Peterson RJ Richardson 1998 The risk of Parkinson's disease with exposure to pesticides, farming, well water, and rural living Neurology 50 1346 1350 9595985 1:STN:280:DyaK1c3lsFChtg%3D%3D (Pubitemid 28240350)
17. JM Gorell BA Rybicki C Johnson EL Cole Peterson 1999 Occupational metal exposures and the risk of Parkinson's disease Neuroepidemiology 18 303 308 10545782 10.1159/000026225 1:STN:280:DC%2BD3c%2FhsFSlsg%3D%3D (Pubitemid 29493517)
18. D HaMai SC Bondy 2004 Oxidative basis of manganese neurotoxicity Ann NY Acad Sci 1012 129 141 15105260 10.1196/annals.1306.010 1:CAS:528: DC%2BD2cXjvVOmsr4%3D (Pubitemid 38453520)
19. JM Hansen YM Go DP Jones 2006 Nuclear and mitochondrial compartmentation of oxidative stress and redox signaling Annu Rev Pharmacol Toxicol 46 215 234 16402904 10.1146/annurev.pharmtox.46.120604.141122 1:CAS:528: DC%2BD28XisFKltb4%3D (Pubitemid 43271189)
20. Y Hirata 2002 Manganese-induced apoptosis in PC12 cells Neurotoxicol Teratol 24 639 653 12200195 10.1016/S0892-0362(02)00215-5 1:CAS:528: DC%2BD38XmsVCit7g%3D (Pubitemid 35013524)
21. Y Hirata K Adachi K Kiuchi 1998 Activation of JNK pathway and induction of apoptosis by manganese in PC12 cells J Neurochem 71 1607 1615 9751194 10.1046/j.1471-4159.1998.71041607.x 1:CAS:528:DyaK1cXmt1Kit7w%3D (Pubitemid 28443033)
22. LS Honig RN Rosenberg 2000 Apoptosis and neurologic disease Am J Med 108 317 330 11014725 10.1016/S0002-9343(00)00291-6 1:CAS:528:DC%2BD3cXit1Gqt7k%3D (Pubitemid 30110461)
23. Imhoff BR, Hansen JM (2010) Tert-butylhydroquinone induces mitochondrial oxidative stress causing Nrf2 activation. Cell Biol Toxicol 29 Apr 2010. [Epub ahead of print]
24. K Itoh N Wakabayashi Y Katoh T Ishii K Igarashi JD Engel M Yamamoto 1999 Keap1 represses nuclear activation of antioxidant responsive elements by Nrf2 through binding to the amino-terminal Neh2 domain Genes Dev 13 76 86 9887101 10.1101/gad.13.1.76 1:CAS:528:DyaK1MXnvF2qsg%3D%3D (Pubitemid 29045117)
25. K Itoh T Ishii N Wakabayashi M Yamamoto 1999 Regulatory mechanisms of cellular response to oxidative stress Free Radic Res 31 319 324 10517536 10.1080/10715769900300881 1:CAS:528:DyaK1MXmslGjsLo%3D (Pubitemid 29452857)
26. JA Johnson DA Johnson AD Kraft MJ Calkins RJ Jakel MR Vargas PC Chen 2008 The Nrf2-ARE pathway: an indicator and modulator of oxidative stress in neurodegeneration Ann N Y Acad Sci 1147 61 69 19076431 10.1196/annals.1427.036 1:CAS:528:DC%2BD1MXhsVaqtbw%3D
27. AD Kraft DA Johnson JA Johnson 2004 Nuclear factor E2-related factor 2-dependent antioxidant response element activation by tert-butylhydroquinone and sulforaphane occurring preferentially in astrocytes conditions neurons against oxidative insult J Neurosci 24 1101 1112 14762128 10.1523/JNEUROSCI. 3817-03.2004 1:CAS:528:DC%2BD2cXhsFKlsL0%3D (Pubitemid 38177017)
28. JM Lee JD Moehlenkamp JM Hanson JA Johnson 2001 Nrf2-dependent activation of the antioxidant responsive element by tert-butylhydroquinone is independent of oxidative stress in IMR-32 human neuroblastoma cells Biochem Biophys Res Commun 280 286 292 11162512 10.1006/bbrc.2000.4106 1:CAS:528: DC%2BD3MXivVeltQ%3D%3D (Pubitemid 32917509)
29. JM Lee AY Shih TH Murphy JA Johnson 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 12842875 10.1074/jbc.M305204200 1:CAS:528:DC%2BD3sXnsV2ltbs%3D (Pubitemid 37175325)
30. J Li JM Lee JA Johnson 2002 Microarray analysis reveals an antioxidant responsive element-driven gene set involved in conferring protection from an oxidative stress-induced apoptosis in IMR-32 cells J Biol Chem 277 388 394 11687587 10.1074/jbc.M109380200 1:CAS:528:DC%2BD38XjslGhsA%3D%3D (Pubitemid 34952070)
31. J Li D Johnson M Calkins L Wright C Svendsen J Johnson 2005 Stabilization of Nrf2 by tBHQ confers protection against oxidative stress-induced cell death in human neural stem cells Toxicol Sci 83 313 328 15525690 10.1093/toxsci/kfi027 1:CAS:528:DC%2BD2MXisVWluw%3D%3D (Pubitemid 40227901)
32. HY Li YF Zhong SY Wu N Shi 2007 NF-E2 related factor 2 activation and Heme oxygenase-1 induction by tert-butylhydroquinone protect against deltamethrin mediated oxidative stress in PC12 cells Chem Res Toxicol 20 1242 1251 17676812 10.1021/tx700076q 1:CAS:528:DC%2BD2sXos1Kkt7w%3D (Pubitemid 47548292)
33. HY Li SY Wu N Shi 2007 Transcription factor Nrf2 activation by deltamethrin in PC12 cells: involvement of ROS Toxicol Lett 171 87 98 17540521 10.1016/j.toxlet.2007.04.007 1:CAS:528:DC%2BD2sXntFaqu7c%3D (Pubitemid 46994730)
34. MH Li JH Jang HK Na YN Cha YJ Surh 2007 Carbon monoxide produced by heme oxygenase-1 in response to nitrosative stress induces expression of glutamate-cysteine ligase in PC12 cells via activation of phosphatidylinositol 3-kinase and Nrf2 signaling J Biol Chem 282 28577 28586 17681938 10.1074/jbc.M701916200 1:CAS:528:DC%2BD2sXhtVOmtbzL (Pubitemid 47606059)
35. A Menegon PG Board AC Blackburn GD Mellick DG Le Couteur 1998 Parkinson's disease, pesticides, and glutathione transferase polymorphisms Lancet 352 1344 1346 9802272 10.1016/S0140-6736(98)03453-9 1:STN:280:DyaK1M%2Fhslamug%3D%3D (Pubitemid 28510915)
36. N Morito K Yoh K Itoh A Hirayama A Koyama M Yamamoto S Takahashi 2003 Nrf2 regulates the sensitivity of death receptor signals by affecting intracellular glutathione levels Oncogene 22 9275 9281 14681686 10.1038/sj.onc.1207024 1:CAS:528:DC%2BD3sXpvVGgsbw%3D (Pubitemid 38122039)
37. T Nguyen PJ Sherratt HC Huang CS Yang CB Pickett 2003 Increased protein stability as a mechanism that enhances Nrf2-mediated transcriptional activation of the antioxidant response element: degradation of Nrf2 by the 26S proteasome J Biol Chem 278 4536 4541 12446695 10.1074/jbc.M207293200 1:CAS:528: DC%2BD3sXhtVKmurs%3D (Pubitemid 36800950)
38. J Pi W Qu JM Reece Y Kumagai MP Waalkesa 2003 Transcription factor Nrf2 activation by inorganic arsenic in cultured keratinocytes: involvement of hydrogen peroxide Exp Cell Res 290 234 245 14567983 10.1016/S0014-4827(03)00341- 0 1:CAS:528:DC%2BD3sXotVCitL8%3D (Pubitemid 37272168)
39. K Prabhakaran D Ghosh GD Chapman PG Gunasekar 2008 Molecular mechanism of manganese exposure-induced dopaminergic toxicity Brain Res Bull 76 361 367 18502311 10.1016/j.brainresbull.2008.03.004 1:CAS:528:DC%2BD1cXmtlWht7Y%3D
40. K Prabhakaran GD Chapman PG Gunasekar 2009 BNIP3 up-regulation and mitochondrial dysfunction in manganese-induced neurotoxicity Neurotoxicology 30 414 422 19442826 10.1016/j.neuro.2009.02.012 1:CAS:528:DC%2BD1MXmtFCjt74%3D
41. V Radjendirane P Joseph YH Lee S Kimura AJ Klein-Szanto FJ Gonzalez AK Jaiswal 1998 Disruption of the DT diaphorase (NQO1) gene in mice leads to increased menadione toxicity J Biol Chem 273 7382 7389 9516435 10.1074/jbc.273.13.7382 1:CAS:528:DyaK1cXit1emurg%3D (Pubitemid 28152759)
42. GT Ramesh D Ghosh PG Gunasekar 2002 Early activation of transcription factor, NF-κB following low-level manganese exposure Toxcol Lett 136 151 158 10.1016/S0378-4274(02)00332-6 1:CAS:528:DC%2BD38Xotl2jsLY%3D (Pubitemid 35345150)
43. A Roth L Feng J Walowitz RW Browne 2000 Manganese-induced rat pheochromocytoma (PC12) cell death is independent of caspase activation J Neurosci Res 61 162 171 10878589 10.1002/1097-4547(20000715)61:2<162::AID- JNR7>3.0.CO;2-G 1:CAS:528:DC%2BD3cXkslOgtrs%3D (Pubitemid 30451804)
44. AY Shih DA Johnson G Wong AD Kraft L Jiang H Erb JA Johnson TH Murphy 2003 Coordinate regulation of glutathione biosynthesis and release by Nrf2-expressing glia potently protects neurons from oxidative stress J Neurosci 23 3394 3406 12716947 1:CAS:528:DC%2BD3sXjsFSkt7o%3D (Pubitemid 36531981)
45. K Sriram GX Lin AM Jefferson JR Roberts RS Chapman BT Chen JM Soukup AJ Ghio JM Antonini 2010 Dopaminergic neurotoxicity following pulmonary exposure to manganese-containing welding fumes Arch Toxicol 84 521 540 20224926 10.1007/s00204-010-0525-9 1:CAS:528:DC%2BC3cXjtFWltLk%3D
46. JS Timothy DA William 1991 Transmitter, ion channel and receptor properties of pheochromocytoma (PC12) cells: a model for neurotoxicological studies Neuro Toxicol 12 473 492
47. FL van Muiswinkel HB Kuiperij 2005 The Nrf2-ARE signalling pathway: promising drug target to combat oxidative stress in neurodegenerative disorders Curr Drug Targets CNS Neurol Disord 4 267 281 15975029 10.2174/1568007054038238 (Pubitemid 40754162)
48. J Wang MF Rahman HM Duhart GD Newport TA Patterson RC Murdock SM Hussain JJ Schlager SF Ali 2009 Expression changes of dopaminergic system-related genes in PC12 cells induced by manganese, silver, or copper nanoparticles Neuro Toxicol 30 926 933
49. AC Wild HR Moinova RT Mulcahy 1999 Regulation of gamma-glutamylcysteine synthetase subunit gene expression by the transcription factor Nrf2 J Biol Chem 274 33627 33636 10559251 10.1074/jbc.274.47.33627 1:CAS:528:DyaK1MXns1ejsLk%3D (Pubitemid 129511675)
50. K Wise S Manna J Barr P Gunasekar G Ramesh 2004 Activation of activator protein-1 DNA binding activity due to low level manganese exposure in pheochromocytoma cells Toxicol Lett 147 237 244 15104115 10.1016/j.toxlet.2003. 11.007 1:CAS:528:DC%2BD2cXhtV2lu7k%3D (Pubitemid 38177545)