Synergistic dopaminergic neurotoxicity of manganese and lipopolysaccharide: Differential involvement of microglia and astroglia

Journal of Neurochemistry

Volumn 112, Issue 2, 2010, Pages 434-443

  Zhang, Ping ^a   Lokuta, Kyle M ^a   Turner, Deanne E ^a   Liu, Bin ^a,b  

^a UNIVERSITY OF FLORIDA HEALTH   (United States)

^b UNIVERSITY OF FLORIDA   (United States)

Author keywords

Astroglia; Dopamine; Free radical; Microglia; Neuroinflammation; Neurotoxicity

Indexed keywords

ENDOTOXIN; FREE RADICAL; INTERLEUKIN 1BETA; LIPOPOLYSACCHARIDE; MANGANESE CHLORIDE; MINOCYCLINE; NALOXONE; NITRIC OXIDE; REACTIVE OXYGEN METABOLITE; TUMOR NECROSIS FACTOR ALPHA;

ANIMAL CELL; ARTICLE; CELL DAMAGE; CONTROLLED STUDY; CYTOKINE RELEASE; DOPAMINERGIC ACTIVITY; DOPAMINERGIC NERVE CELL; GLIA CELL; INFLAMMATION; MACROGLIA; MICROGLIA; NERVE CELL CULTURE; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT;

ANIMALS; ANIMALS, NEWBORN; ASTROCYTES; CELLS, CULTURED; CHLORIDES; DOPAMINE; DOSE-RESPONSE RELATIONSHIP, DRUG; DRUG SYNERGISM; INTERLEUKIN-1BETA; LIPOPOLYSACCHARIDES; MANGANESE COMPOUNDS; MICROGLIA; MINOCYCLINE; NALOXONE; NARCOTIC ANTAGONISTS; NEURONS; NEUROTOXINS; NITRIC OXIDE; RATS; RATS, INBRED F344; REACTIVE OXYGEN SPECIES; TIME FACTORS; TRITIUM; TUMOR NECROSIS FACTOR-ALPHA; TYROSINE 3-MONOOXYGENASE;

RATTUS;

EID: 72849138642     PISSN: 00223042     EISSN: 14714159     Source Type: Journal    
DOI: 10.1111/j.1471-4159.2009.06477.x     Document Type: Article

References (65)

1. Aschner M., Guilarte T. s. R., Schneider J. S. Zheng W. (2007) Manganese: recent advances in understanding its transport and neurotoxicity. Toxicol. Appl. Pharmacol. 221, 131 147.
2. Bae J. H., Jang B. C., Suh S. I., Ha E., Baik H. H., Kim S. S., Lee M. Y. Shin D. H. (2006) Manganese induces inducible nitric oxide synthase (iNOS) expression via activation of both MAP kinase and PI3KAkt pathways in BV2 microglial cells. Neurosci. Lett. 398, 151 154.
3. Barhoumi R., Faske J., Liu X. Tjalkens R. B. (2004) Manganese potentiates lipopolysaccharide-induced expression of NOS2 in C6 glioma cells through mitochondrial-dependent activation of nuclear factor kappaB. Brain Res. Mol. Brain Res. 122, 167 179.
4. Brydon L., Harrison N. A., Walker C., Steptoe A. Critchley H. D. (2008) Peripheral inflammation is associated with altered substantia nigra activity and psychomotor slowing in humans. Biol. Psychiatry 63, 1022 1029.
5. Calne D. B., Chu N. S., Huang C. C., Lu C. S. Olanow W. (1994) Manganism and idiopathic parkinsonism: similarities and differences. Neurology 44, 1583 1586.
6. Cersosimo M. G. Koller W. C. (2006) The diagnosis of manganese-induced Parkinsonism. Neurotoxicology 27, 340 346.
7. Chang J. Y. Liu L. Z. (1999) Manganese potentiates nitric oxide production by microglia. Brain Res. Mol. Brain Res. 68, 22 28.
8. Chen H., Jacobs E., Schwarzschild M. A., McCullough M. L., Calle E. E., Thun M. J. Ascherio A. (2005) Nonsteroidal antiinflammatory drug use and the risk for Parkinson's disease. Ann. Neurol. 58, 963 967. (Pubitemid 41746889)
9. Crittenden P. L. Filipov N. M. (2008) Manganese-induced potentiation of in vitro proinflammatory cytokine production by activated microglial cells is associated with persistent activation of p38 MAPK. Toxicol. In Vitro 22, 18 27.
10. Di Monte D. A. (2003) The environment and Parkinson's disease: is the nigrostriatal system preferentially targeted by neurotoxins? Lancet Neurol. 2, 531 538.
11. Dutta G., Zhang P. Liu B. (2008) The lipopolysaccharide Parkinson's disease animal model: mechanistic studies and drug discovery. Fundam. Clin. Pharmacol. 22, 453 464.
12. Erikson K. M., Dobson A. W., Dorman D. C. Aschner M. (2004) Manganese exposure and induced oxidative stress in the rat brain. Sci. Total Environ. 334-335, 409 416.
13. Filipov N. M., Seegal R. F. Lawrence D. A. (2005) Manganese potentiates in vitro production of proinflammatory cytokines and nitric oxide by microglia through a nuclear factor kappa B-dependent mechanism. Toxicol. Sci. 84, 139 148.
14. Finkelstein M. M. Jerrett M. (2007) A study of the relationships between Parkinson's disease and markers of traffic-derived and environmental manganese air pollution in two Canadian cities. Environ. Res. 104, 420 432.
15. Fleckenstein A. E., Volz T. J., Riddle E. L., Gibb J. W. Hanson G. R. (2007) New insights into the mechanism of action of amphetamines. Annu. Rev. Pharmacol. Toxicol. 47, 681 698.
16. Fored C. M., Fryzek J. P., Brandt L., Nise G., Sjogren B., McLaughlin J. K., Blot W. J. Ekbom A. (2006) Parkinson's disease and other basal ganglia or movement disorders in a large nationwide cohort of Swedish welders. Occup. Environ. Med. 63, 135 140.
17. Frank-Cannon T. C., Tran T., Ruhn K. A. et al. (2008) Parkin deficiency increases vulnerability to inflammation-related nigral degeneration. J. Neurosci. 28, 10825 10834.
18. Gao H. M., Hong J. S., Zhang W. Liu B. (2002a) Distinct role for microglia in rotenone-induced degeneration of dopaminergic neurons. J. Neurosci. 22, 782 790.
19. Gao H. M., Jiang J., Wilson B., Zhang W., Hong J. S. Liu B. (2002b) Microglial activation-mediated delayed and progressive degeneration of rat nigral dopaminergic neurons: relevance to Parkinson's disease. J. Neurochem. 81, 1285 1297.
20. Gao H. M., Hong J. S., Zhang W. Liu B. (2003a) Synergistic dopaminergic neurotoxicity of the pesticide rotenone and inflammogen lipopolysaccharide: relevance to the etiology of Parkinson's disease. J. Neurosci. 23, 1228 1236.
21. Gao H. M., Liu B., Zhang W. Hong J. S. (2003b) Synergistic dopaminergic neurotoxicity of MPTP and inflammogen lipopolysaccharide: relevance to the etiology of Parkinson's disease. FASEB J. 17, 1957 1959.
22. Gorell J. M., Johnson C. C., Rybicki B. A., Peterson E. L., Kortsha G. X., Brown G. G. Richardson R. J. (1997) Occupational exposures to metals as risk factors for Parkinson's disease. Neurology 48, 650 658.
23. Gorell J. M., Johnson C. C., Rybicki B. A., Peterson E. L., Kortsha G. X., Brown G. G. Richardson R. J. (1999) Occupational exposure to manganese, copper, lead, iron, mercury and zinc and the risk of Parkinson's disease. Neurotoxicology 20, 239 247.
24. Huang C. C. (2007) Parkinsonism induced by chronic manganese intoxication - an experience in Taiwan. Chang Gung Med. J. 30, 385 395.
25. Jenner P. Olanow C. W. (1996) Oxidative stress and the pathogenesis of Parkinson's disease. Neurology 47, S161 S170.
26. Kim H. S. Suh Y. H. (2009) Minocycline and neurodegenerative diseases. Behav. Brain Res. 196, 168 179.
27. Klein C. Schlossmacher M. G. (2007) Parkinson disease, 10 years after its genetic revolution: multiple clues to a complex disorder. Neurology 69, 2093 2104.
28. Ling Z., Chang Q. A., Tong C. W., Leurgans S. E., Lipton J. W. Carvey P. M. (2004a) Rotenone potentiates dopamine neuron loss in animals exposed to lipopolysaccharide prenatally. Exp. Neurol. 190, 373 383.
29. Ling Z. D., Chang Q., Lipton J. W., Tong C. W., Landers T. M. Carvey P. M. (2004b) Combined toxicity of prenatal bacterial endotoxin exposure and postnatal 6-hydroxydopamine in the adult rat midbrain. Neuroscience 124, 619 628.
30. Liu B 2006) Modulation of microglial pro-inflammatory and neurotoxic activity for the treatment of Parkinson's disease. Aaps J. 8, E606 E621.
31. Liu B. Hong J. S. (2003a) Neuroprotective effect of naloxone in inflammation-mediated dopaminergic neurodegeneration. Dissociation from the involvement of opioid receptors. Methods Mol Med 79, 43 54.
32. Liu B. Hong J. S. (2003b) Primary rat mesencephalic neuron-glia, neuron-enriched, microglia-enriched, and astroglia-enriched cultures. Methods Mol. Med. 79, 387 395.
33. Liu B. Hong J. S. (2003c) Role of microglia in inflammation-mediated neurodegenerative diseases: mechanisms and strategies for therapeutic intervention. J. Pharmacol. Exp. Ther. 304, 1 7.
34. Liu B., Du L. Hong J. S. (2000) Naloxone protects rat dopaminergic neurons against inflammatory damage through inhibition of microglia activation and superoxide generation. J. Pharmacol. Exp. Ther. 293, 607 617.
35. Liu B., Wang K., Gao H. M., Mandavilli B., Wang J. Y. Hong J. S. (2001) Molecular consequences of activated microglia in the brain: overactivation induces apoptosis. J. Neurochem. 77, 182 189.
36. Liu B., Gao H. M., Wang J. Y., Jeohn G. H., Cooper C. L. Hong J. S. (2002) Role of nitric oxide in inflammation-mediated neurodegeneration. Ann. NY Acad. Sci. 962, 318 331.
37. Liu B., Gao H. M. Hong J. S. (2003) Parkinson's disease and exposure to infectious agents and pesticides and the occurrence of brain injuries: role of neuroinflammation. Environ. Health Perspect. 111, 1065 1073.
38. Logroscino G. (2005) The role of early life environmental risk factors in Parkinson disease: what is the evidence? Environ. Health Perspect. 113, 1234 1238.
39. Lucchini R. G., Albini E., Benedetti L. et al. (2007) High prevalence of Parkinsonian disorders associated to manganese exposure in the vicinities of ferroalloy industries. Am. J. Ind. Med. 50, 788 800.
40. Manning-Bog A. B. Langston J. W. (2007) Model fusion, the next phase in developing animal models for Parkinson's disease. Neurotox. Res. 11, 219 240.
41. Marsh G. M. Gula M. J. (2006) Employment as a welder and Parkinson disease among heavy equipment manufacturing workers. J. Occup. Environ. Med. 48, 1031 1046.
42. McCoy M. K., Martinez T. N., Ruhn K. A., Szymkowski D. E., Smith C. G., Botterman B. R., Tansey K. E. Tansey M. G. (2006) Blocking soluble tumor necrosis factor signaling with dominant-negative tumor necrosis factor inhibitor attenuates loss of dopaminergic neurons in models of Parkinson's disease. J. Neurosci. 26, 9365 9375.
43. McGeer P. L. McGeer E. G. (2008) Glial reactions in Parkinson's disease. Mov. Disord. 23, 474 483.
44. Mergler D., Huel G., Bowler R., Iregren A., Belanger S., Baldwin M., Tardif R., Smargiassi A. Martin L. (1994) Nervous system dysfunction among workers with long-term exposure to manganese. Environ. Res. 64, 151 180.
45. Milatovic D., Zaja-Milatovic S., Gupta R. C., Yu Y. Aschner M. (2009) Oxidative damage and neurodegeneration in manganese-induced neurotoxicity. Toxicol. Appl. Pharmacol. 240, 219 225.
46. Moreno J. A., Sullivan K. A., Carbone D. L., Hanneman W. H. Tjalkens R. B. (2008) Manganese potentiates nuclear factor-kappaB-dependent expression of nitric oxide synthase 2 in astrocytes by activating soluble guanylate cyclase and extracellular responsive kinase signaling pathways. J. Neurosci. Res. 86, 2028 2038.
47. Pal P. K., Samii A. Calne D. B. (1999) Manganese neurotoxicity: a review of clinical features, imaging and pathology. Neurotoxicology 20, 227 238.
48. Perl D. P. Olanow C. W. (2007) The neuropathology of manganese-induced Parkinsonism. J. Neuropathol. Exp. Neurol. 66, 675 682.
49. Powers K. M., Smith-Weller T., Franklin G. M., Longstreth W. T., Jr., Swanson P. D. Checkoway H. (2003) Parkinson's disease risks associated with dietary iron, manganese, and other nutrient intakes. Neurology, 60 1761 1766.
50. Przedborski S. (2007) Neuroinflammation and Parkinson's disease. Handb. Clin. Neurol. 83, 535 551.
51. Qin L., Block M. L., Liu Y. et al. (2005) Microglial NADPH oxidase is a novel target for femtomolar neuroprotection against oxidative stress. FASEB J. 19, 550 557.
52. Racette B. A., McGee-Minnich L., Moerlein S. M., Mink J. W., Videen T. O. Perlmutter J. S. (2001) Welding-related parkinsonism: clinical features, treatment, and pathophysiology. Neurology 56, 8 13.
53. Racette B. A., Tabbal S. D., Jennings D., Good L., Perlmutter J. S. Evanoff B. (2005) Prevalence of parkinsonism and relationship to exposure in a large sample of Alabama welders. Neurology 64, 230 235.
54. Rempe S., Hayden J. M., Robbins R. A. Hoyt J. C. (2007) Tetracyclines and pulmonary inflammation. Endocr. Metab. Immune Disord. Drug Targets 7, 232 236.
55. Richardson J. R., Caudle W. M., Wang M., Dean E. D., Pennell K. D. Miller G. W. (2006) Developmental exposure to the pesticide dieldrin alters the dopamine system and increases neurotoxicity in an animal model of Parkinson's disease. FASEB J. 20, 1695 1697.
56. Spranger M., Schwab S., Desiderato S., Bonmann E., Krieger D. Fandrey J. (1998) Manganese augments nitric oxide synthesis in murine astrocytes: a new pathogenetic mechanism in manganism? Exp. Neurol. 149, 277 283.
57. Stanwood G. D., Leitch D. B., Savchenko V., Wu J., Fitsanakis V. A., Anderson D. J., Stankowski J. N., Aschner M. McLaughlin B. (2009) Manganese exposure is cytotoxic and alters dopaminergic and GABAergic neurons within the basal ganglia. J. Neurochem 110, 378 389.
58. Sulzer D. (2007) Multiple hit hypotheses for dopamine neuron loss in Parkinson's disease. Trends Neurosci. 30, 244 250.
59. Tan E. K., Tan C., Fook-Chong S. M. et al. (2003) Dose-dependent protective effect of coffee, tea, and smoking in Parkinson's disease: a study in ethnic Chinese. J. Neurol. Sci. 216, 163 167.
60. Teeling J. L. Perry V. H. (2009) Systemic infection and inflammation in acute CNS injury and chronic neurodegeneration: underlying mechanisms. Neuroscience 158, 1062 1073.
61. Thiruchelvam M., Richfield E. K., Baggs R. B., Tank A. W. Cory-Slechta D. A. (2000) The nigrostriatal dopaminergic system as a preferential target of repeated exposures to combined paraquat and maneb: implications for Parkinson's disease. J. Neurosci. 20, 9207 9214. (Pubitemid 32042923)
62. Wu D. C., Jackson-Lewis V., Vila M., Tieu K., Teismann P., Vadseth C., Choi D. K., Ischiropoulos H. Przedborski S. (2002) Blockade of microglial activation is neuroprotective in the 1-methyl-4-phenyl-1,2,3,6- tetrahydropyridine mouse model of Parkinson disease. J. Neurosci. 22, 1763 1771.
63. Zhang P., Hatter A. Liu B. (2007) Manganese chloride stimulates rat microglia to release hydrogen peroxide. Toxicol. Lett. 173, 88 100.
64. Zhang P., Wong T. A., Lokuta K. M., Turner D. E., Vujisic K. Liu B. (2009) Microglia enhance manganese chloride-induced dopaminergic neurodegeneration: role of free radical generation. Exp. Neurol. 217, 219 230.
65. Zheng W., Ren S. Graziano J. H. (1998) Manganese inhibits mitochondrial aconitase: a mechanism of manganese neurotoxicity. Brain Res. 799, 334 342.