α-Synuclein overexpression enhances manganese-induced neurotoxicity through the NF-κB-mediated pathway

Toxicology Mechanisms and Methods

Volumn 21, Issue 6, 2011, Pages 435-443

  Prabhakaran, Krishnan ^a   Chapman, Gail D ^a   Gunasekar, Palur G ^a  

^a WRIGHT PATTERSON AIR FORCE BASE   (United States)

Author keywords

Synuclein; Apoptosis; Manganese; NF B; Nitric oxide; Oxidative stress; p38 MAPK

Indexed keywords

4 [4 (4 FLUOROPHENYL) 5 (2 METHOXY 4 PYRIMIDINYL) 1 IMIDAZOLYL]CYCLOHEXANOL; ALPHA SYNUCLEIN; IMMUNOGLOBULIN ENHANCER BINDING PROTEIN; MANGANESE; MITOGEN ACTIVATED PROTEIN KINASE P38; N [3 (AMINOMETHYL)BENZYL]ACETAMIDINE; NITRIC OXIDE; SN 50;

ANIMAL CELL; APOPTOSIS; ARTICLE; CELL DEATH; CELL FUSION; CONTROLLED STUDY; GENE OVEREXPRESSION; GENETIC ASSOCIATION; GLIOMA; HUMAN; HUMAN CELL; MESENCEPHALON; NERVE DEGENERATION; NEUROBLASTOMA; NEUROTOXICITY; NONHUMAN; OXIDATIVE STRESS; PRIORITY JOURNAL; RAT; TUMOR CELL LINE;

ALPHA-SYNUCLEIN; ANIMALS; ANTIOXIDANTS; APOPTOSIS; CELL LINE; CELL NUCLEUS; ENVIRONMENTAL POLLUTANTS; HEAVY METAL POISONING, NERVOUS SYSTEM; HUMANS; HYBRID CELLS; MANGANESE; MESENCEPHALON; MICE; NERVE TISSUE PROTEINS; NEURONS; NF-KAPPA B; NITRIC OXIDE; OXIDATIVE STRESS; P38 MITOGEN-ACTIVATED PROTEIN KINASES; PROTEIN KINASE INHIBITORS; PROTEIN TRANSPORT; RATS; SIGNAL TRANSDUCTION;

RATTUS;

EID: 79958189881     PISSN: 15376516     EISSN: 15376524     Source Type: Journal    
DOI: 10.3109/15376516.2011.560210     Document Type: Article

References (58)

1. Auluck PK, Chan HY, Trojanowski JQ, Lee VM, Bonini NM. 2002. Chaperone suppression of α-synuclein toxicity in a Drosophila model for Parkinsons disease. Science 295:865-868. (Pubitemid 34118369)
2. Baichwal VR, Baeuerie PA. 1997. Activate NF-κB or die? Curr Biol 7:R94-R96
3. Calabrese V, Ravagna A, Colombrita C, Scapagnini G, Guagliano E, Calvani M, Butterfield DA, Giuffrida Stella AM. 2005. Acetylcarnitine induces heme oxygenase in rat astrocytes and protects against oxidative stress: involvement of the transcription factor Nrf2. J Neurosci Res 79:509-521. (Pubitemid 40283351)
4. Chae HJ, Kim SC, Han KS, Chae SW, An NH, Kim HM, Kim HH, Lee ZH, Kim HR. 2001. Hypoxia induces apoptosis by caspase activation accompanying cytochrome C release from mitochondria in MC3T3E1 osteoblasts. p38 MAPK is related in hypoxia-induced apoptosis. Immunopharmacol Immunotoxicol 23:133-152.
5. Chang JY, Liu LZ. 1999. Manganese potentiates nitric oxide production by microglia. Brain Res Mol Brain Res 68:22-28. (Pubitemid 29243991)
6. Choi-Lundberg DL, Lin Q, Chang YN, Chiang YL, Hay CM, Mohajeri H, Davidson BL, Bohn MC. 1997. Dopaminergic neurons protected from degeneration by GDNF gene therapy. Science 275:838-841. (Pubitemid 27074886)
7. Cookson MR. 2005. The biochemistry of Parkinsons disease. Annu Rev Biochem 74:29-52.
8. Cookson MR. 2009. α-Synuclein and neuronal cell death. Mol Neurodegener 4:9.
9. Crossgrove J, Zheng W. 2004. Manganese toxicity upon overexposure. NMR Biomed 17:544-553. (Pubitemid 40124780)
10. De Zutter GS, Davis RJ. 2001. Pro-apoptotic gene expression mediated by the p38 mitogen-activated protein kinase signal transduction pathway. Proc Natl Acad Sci USA 98:6168-6173. (Pubitemid 32488211)
11. Dawson TM, Dawson VL. 2003. Molecular pathways of neurodegeneration in Parkinsons disease. Science 302:819-822. (Pubitemid 37339614)
12. Dobson AW, Erikson KM, Aschner M. 2004. Manganese neurotoxicity. Ann N Y Acad Sci 1012:115-128. (Pubitemid 38453519)
13. Di Monte DA, Lavasani M, Manning-Bog AB. 2002. Environmental factors in Parkinsons disease. Neurotoxicology 23:487-502.
14. Dauer W, Kholodilov N, Vila M, Trillat AC, Goodchild R, Larsen KE, Staal R, Tieu K, Schmitz Y, Yuan CA, Rocha M, Jackson-Lewis V, Hersch S, Sulzer D, Przedborski S, Burke R, Hen R. 2002. Resistance of α-synuclein null mice to the parkinsonian neurotoxin MPTP. Proc Natl Acad Sci USA 99:14524-14529. (Pubitemid 35257704)
15. El Mchichi B, Hadji A, Vazquez A, Leca G. 2007. p38 MAPK and MSK1 mediate caspase-8 activation in manganese-induced mitochondriadependent cell death. Cell Death Differ 14:1826-1836. (Pubitemid 47430433)
16. Forno LS. 1996. Neuropathology of Parkinsons disease. J Neuropathol Exp Neurol 55:259-272.
17. Feany MB, Bender WW. 2000. A Drosophila model of Parkinsons disease. Nature 404:394-398.
18. Gitler AD, Chesi A, Geddie ML, Strathearn KE, Hamamichi S, Hill KJ, Caldwell KA, Caldwell GA, Cooper AA, Rochet JC, Lindquist S. 2009. α-Synuclein is part of a diverse and highly conserved interaction network that includes PARK9 and manganese toxicity. Nat Genet 41:308-315.
19. Gonzalez LE, Juknat AA, Venosa AJ, Verrengia N, Kotler ML. 2008. Manganese activates the mitochondrial apoptotic pathway in rat astrocytes by modulating the expression of proteins of the Bcl-2 family. Neurochem Int 53:408-415.
20. Guilarte TR, Chen MK, McGlothan JL, Verina T, Wong DF, Zhou Y, Alexander M, Rohde CA, Syversen T, Decamp E, Koser AJ, Fritz S, Gonczi H, Anderson DW, Schneider JS. 2006. Nigrostriatal dopamine system dysfunction and subtle motor deficits in manganeseexposed non-human primates. Exp Neurol 202:381-390. (Pubitemid 44692681)
21. Halvorsen EM, Dennis J, Keeney P, Sturgill TW, Tuttle JB, Bennett JB Jr. 2002. Methylpyridinium (MPP(+))- and nerve growth factorinduced changes in pro- and anti-apoptotic signaling pathways in SH-SY5Y neuroblastoma cells. Brain Res 952:98-110. (Pubitemid 35279492)
22. Hancock JT, Desikan R, Neill SJ. 2001. Role of reactive oxygen species in cell signalling pathways. Biochem Soc Trans 29:345-350.
23. Hornykiewicz O. 1998. Biochemical aspects of Parkinsons disease. Neurology 51:S2-S9.
24. Hong Z, Shi M, Chung KA, Quinn JF, Peskind ER, Galasko D, Jankovic J, Zabetian CP, Leverenz JB, Baird G, Montine TJ, Hancock AM, Hwang H, Pan C, Bradner J, Kang UJ, Jensen PH, Zhang J. 2010. DJ-1 and α-synuclein in human cerebrospinal fluid as biomarkers of Parkinsons disease. Brain 133:713-726.
25. Hashimoto M, Hsu LJ, Rockenstein E, Takenouchi T, Mallory M, Masliah E. 2002. α-Synuclein protects against oxidative stress via inactivation of the c-Jun N-terminal kinase stress-signaling pathway in neuronal cells. J Biol Chem 277:11465-11472. (Pubitemid 34952915)
26. Hensley K, Robinson KA, Gabbita SP, Salsman S, Floyd RA. 2000. Reactive oxygen species, cell signaling, and cell injury. Free Radic Biol Med 28:1456-1462. (Pubitemid 30604227)
27. Hornykiewicz O. 1998. Biochemical aspects of Parkinsons disease. Neurology Suppl 2:S2-S9.
28. Hsu LJ, Sagara Y, Arroyo A, Rockenstein E, Sisk A, Mallory M, Wong J, Takenouchi T, Hashimoto M, Masliah E. 2000. α-synuclein promotes mitochondrial deficit and oxidative stress. Am J Pathol 157:401-410. (Pubitemid 30627559)
29. Iregren A. 1999. Manganese neurotoxicity in industrial exposures: proof of effects, critical exposure level, and sensitive tests. Neurotoxicology 20:315-323.
30. Karin M. 1999. How NF-κB is activated: the role of the IκB kinase (IKK) complex. Oncogene 18:6867-6874.
31. Le W, Rowe D, Xie W, Ortiz I, He Y, Appel SH. 2001. Microglial activation and dopaminergic cell injury: an in vitro model relevant to Parkinsons disease. J Neurosci 21:8447-8455. (Pubitemid 33051443)
32. Li Y, Sun L, Cai T, Zhang Y, Lv S, Wang Y, Ye L. 2010. α-Synuclein overexpression during manganese-induced apoptosis in SH-SY5Y neuroblastoma cells. Brain Res Bull 81:428-433.
33. Masliah E, Rockenstein E, Veinbergs I, Mallory M, Hashimoto M, Takeda A, Sagara Y, Sisk A, Mucke L. 2000. Dopaminergic loss and inclusion body formation in α-synuclein mice: implications for neurodegenerative disorders. Science 287:1265-1269. (Pubitemid 30112148)
34. Matsuoka Y, Vila M, Lincoln S, McCormack A, Picciano M, LaFrancois J, Yu X, Dickson D, Langston WJ, McGowan E, Farrer M, Hardy J, Duff K, Przedborski S, Di Monte DA. 2001. Lack of nigral pathology in transgenic mice expressing human ?-synuclein driven by the tyrosine hydroxylase promoter. Neurobiol Dis 8:535-539. (Pubitemid 32566143)
35. Manning-Bog AB, McCormack AL, Li J, Uversky VN, Fink AL, Di Monte DA. 2002. The herbicide paraquat causes up-regulation and aggregation of α-synuclein in mice: paraquat and α-synuclein. J Biol Chem 277:1641-1644. (Pubitemid 34968732)
36. Mergler D, Baldwin M. 1997. Early manifestations of manganese neurotoxicity in humans: an update. Environ Res 73:92-100. (Pubitemid 27406570)
37. Olanow CW. 2004. Manganese-induced parkinsonism and Parkinsons disease. Ann N Y Acad Sci 1012:209-223.
38. Ostrerova-Golts N, Petrucelli L, Hardy J, Lee JM, Farer M, Wolozin B. 2000. The A53T α-synuclein mutation increases iron-dependent aggregation and toxicity. J Neurosci 20:6048-6054. (Pubitemid 30658398)
39. Perl DP, Olanow CW. 2007. The neuropathology of manganeseinduced Parkinsonism. J Neuropathol Exp Neurol 66:675-682.
40. Ponzoni S, Gaziri LC, Britto LR, Barreto WJ, Blum D. 2002. Clearance of manganese from the rat substantia nigra following intra-nigral microinjections. Neurosci Lett 328:170-174. (Pubitemid 34804736)
41. Prabhakaran K, Ghosh D, Chapman GD, Gunasekar PG. 2008. Molecular mechanism of manganese exposure-induced dopaminergic toxicity. Brain Res Bull 76:361-367.
42. Prabhakaran K, Chapman GD, Gunasekar PG. 2009. BNIP3 up-regulation and mitochondrial dysfunction in manganeseinduced neurotoxicity. Neurotoxicology 30:414-422.
43. Prasad JE, Kumar B, Andreatta C, Nahreini P, Hanson AJ, Yan XD, Prasad KN. 2004. Overexpression of α-synuclein decreased viability and enhanced sensitivity to prostaglandin E(2), hydrogen peroxide, and a nitric oxide donor in differentiated neuroblastoma cells. J Neurosci Res 76:415-422. (Pubitemid 38580137)
44. Pulido MD, Parrish AR. 2003. Metal-induced apoptosis: mechanisms. Mutat Res 533:227-241. (Pubitemid 37487871)
45. Roth JA, Garrick MD. 2003. Iron interactions and other biological reactions mediating the physiological and toxic actions of manganese. Biochem Pharmacol 66:1-13. (Pubitemid 36724894)
46. Ruan Q, Harrington AJ, Caldwell KA, Caldwell GA, Standaert DG. 2010. VPS41, a protein involved in lysosomal trafficking, is protective in Caenorhabditis elegans and mammalian cellular models of Parkinsons disease. Neurobiol Dis 37:330-338.
47. Saha AR, Ninkina NN, Hanger DP, Anderton BH, Davies AM, Buchman VL. 2000. Induction of neuronal death by α-synuclein. Eur J Neurosci 12:3073-3077.
48. Shavali S, Combs CK, Ebadi M. 2006. Reactive macrophages increase oxidative stress and α-synuclein nitration during death of dopaminergic neuronal cells in co-culture: relevance to Parkinsons disease. Neurochem Res 31:85-94. (Pubitemid 43234549)
49. Shuto T, Xu H, Wang B, Han J, Kai H, Gu XX, Murphy TF, Lim DJ, Li JD. 2001. Activation of NF-κB by nontypeable Hemophilus influenzae is mediated by toll-like receptor 2-TAK1-dependent NIK-IKK α/β- IκBα and MKK3/6-p38 MAP kinase signaling pathways in epithelial cells. Proc Natl Acad Sci USA 98:8774-8779. (Pubitemid 32678103)
50. Singleton AB, Farrer M, Johnson J, Singleton A, Hague S, Kachergus J, Hulihan M, Peuralinna T, Dutra A, Nussbaum R, Lincoln S, Crawley A, Hanson M, Maraganore D, Adler C, Cookson MR, Muenter M, Baptista M, Miller D, Blancato J, Hardy J, Gwinn-Hardy K. 2003. α-Synuclein locus triplication causes Parkinsons disease. Science 302:841. (Pubitemid 37339619)
51. Spillantini MG, Goedert M. 2000. The α-synucleinopathies: Parkinsons disease, dementia with Lewy bodies, and multiple system atrophy. Ann N Y Acad Sci 920:16-27. (Pubitemid 32056547)
52. Tong M, Dong M, de la Monte SM. 2009. Brain insulin-like growth factor and neurotrophin resistance in Parkinsons disease and dementia with Lewy bodies: potential role of manganese neurotoxicity. J Alzheimers Dis 16:585-599.
53. U.S. Army Center for Health Promotion and Preventive Medicine. 2008. Micro-particulate surveillance reports.
54. Uversky VN, Li J, Fink AL. 2001. Pesticides directly accelerate the rate of α-synuclein fibril formation: a possible factor in Parkinsons disease. FEBS Lett 500:105-108. (Pubitemid 32607541)
55. Wang CY, Guttridge DC, Mayo MW, Baldwin AS Jr. 1999. NF-κB induces expression of the Bcl-2 homologue A1/Bfl-1 to preferentially suppress chemotherapy-induced apoptosis. Mol Cell Biol 19:5923-5929. (Pubitemid 29399297)
56. Whitmarsh AJ, Davis RJ. 1996. Transcription factor AP-1 regulation by mitogen-activated protein kinase signal transduction pathways. J Mol Med 74:589-607. (Pubitemid 26343761)
57. Yamagishi S, Yamada M, Ishikawa Y, Matsumoto T, Ikeuchi T, Hatanaka H. 2001. p38 mitogen-activated protein kinase regulates low potassium-induced c-Jun phosphorylation and apoptosis in cultured cerebellar granule neurons. J Biol Chem 276:5129-5133.
58. Zhou W, Hurlbert MS, Schaack J, Prasad KN, Freed CR. 2000. Overexpression of human α-synuclein causes dopamine neuron death in rat primary culture and immortalized mesencephalonderived cells. Brain Res 866:33-43. (Pubitemid 30313005)