Neurobiology of Aging
Volume 30, Issue 9 , Pages 1361-1378 , September 2009

Inflammatory priming of the substantia nigra influences the impact of later paraquat exposure: Neuroimmune sensitization of neurodegeneration

  • Emily N. Mangano
    • ,
  • Shawn Hayley

      Affiliations

    • Corresponding Author InformationCorresponding author at: 1125 Colonel By Drive, Ottawa, Ontario, Canada K1S 5B6. Tel.: +1 613 520 2600x6314; fax: +1 613 520 4052.

Received 20 June 2007 ,Revised 4 October 2007 ,Accepted 16 November 2007.

References 

  1. Andersen JK. Paraquat and iron exposure as possible synergistic environmental risk factors in Parkinson's disease. Neurotox. Res. 2003;5(5):307–313
  2. Baba Y, Kuroiwa A, Uitti RJ, Wszolek ZK, Yamada T. Alterations of T-lymphocyte populations in Parkinson's disease. Parkinsonism Relat. Disord. 2005;11(8):985–998
  3. Barone FC. Endogenous brain protection: models, gene expression, and mechanisms. Methods Mol. Med. 2005;104:105–184
  4. Benner EJ, Mosley RL, Destache CJ, Lewis TB, Jackson-Lewis V, Gorantla S, et al. Therapeutic immunization protects dopaminergic neurons in a mouse model of Parkinson's disease. Proc. Natl. Acad. Sci. U.S.A. 2004;101(25):9435–9440
  5. Betarbet R, Sherer TB, MacKenzie G, Garcia-Osuna M, Panov AV, Greenamyre JT. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 2000;(12):1301–1306
  6. Betarbet R, Sherer TB, Di Monte DA, Greenamyre JT. Mechanistic approaches to Parkinson's disease pathogenesis. Brain Pathol. 2002;12(4):499–510
  7. Betarbet R, Canet-Aviles RM, Sherer TB, Mastroberardino PG, McLendon C, Kim JH, et al. Intersecting pathways to neurodegeneration in Parkinson's disease: effects of the pesticide rotenone on DJ-1, alpha-synuclein, and the ubiquitin-proteasome system. Neurobiol. Dis. 2006;22(2):404–420
  8. Bezard E, Jaber M, Gonon F, Boireau A, Bloch B, Gross CE. Adaptive changes in the nigrostriatal pathway in response to increased 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced neurodegeneration in the mouse. Eur. J. Neurosci. 2000;12(8):2892–2900
  9. Blandini F, Nappi G, Tassorelli C, Martignoni E. Functional changes of the basal ganglia circuitry in Parkinson's disease. Prog. Neurobiol. 2000;62(1):63–88
  10. Bolin LM, Strycharska-Orezyk I, Murray R, Langston JW, Di Monte D. Increased vulnerability of dopaminergic neurons in MPTP-lesioned interleukin-6 deficient mice. J. Neurochem. 2002;83(1):167–175
  11. Cardenas H, Bolin LM. Compromised reactive microgliosis in MPTP-lesioned IL-6 KO mice. Brain Res. 2003;985(1):89–97
  12. Carvey PM, Chang Q, Lipton JW, Ling Z. Prenatal exposure to the bacteriotoxin lipopolysaccharide leads to long-term losses of dopamine neurons in offspring: a potential, new model of Parkinson's disease. Front Biosci. 2003;8:s826–s837
  13. Carvey PM, Punati A, Newman MB. Progressive dopamine neuron loss in Parkinson's disease: the multiple hit hypothesis. Cell Transplant. 2006;15(3):239–250
  14. Cassarejos MJ, Menendez J, Solano RM, Rodriguez-Navarro JA, Garcia de Yebenes J, Mena MA. Susceptibility to rotenone is increased in neurons from parkin null mice and is reduced by minocycline. J. Neurochem. 2006;97(4):934–946
  15. Chen PS, Peng GS, Li G, Yang S, Wu X, Wang CC, et al. Valproate protects dopaminergic neurons in midbrain neuron/glia cultures by stimulating the release of neurotrophic factors from astrocytes. Mol. Psychiatry. 2006;11(12):1116–1125
  16. Cicchetti F, Lapointe N, Roberge-Tremblay A, Saint-Pierre M, Jimenez L, Ficke BW, et al. Systemic exposure to paraquat and maneb models early Parkinson's disease in young adult rats. Neurobiol. Dis. 2005;20(2):360–371
  17. Collier TJ, Lipton J, Daley BF, Palfi S, Chu Y, Sortwell C, et al. Aging-related changes in the nigrostriatal dopamine system and the response to MPTP in nonhuman primates: diminished compensatory mechanisms as a prelude to parkinsonism. Neurobiol. Dis. 2007;26(1):56–65
  18. Cunningham C, Wilcockson DC, Campion S, Lunnon K, Perry VH. Central and systemic endotoxin challenges exacerbate the local inflammatory response and increase neuronal death during chronic neurodegeneration. J. Neurosci. 2005;25(40):9245–9284
  19. Czlonkowska A, Kurkowska-Jastrzebska I, Czlonkowski A, Peter D, Stefano G. Immune processes in the pathogenesis of Parkinson's disease: a potential role for microglia and nitric oxide. Med. Sci. Monit. 2002;8(8):RA165–RA177
  20. Dawson TM, Dawson VL. Rare genetic mutations shed light on the pathogenesis of Parkinson disease. J. Clin. Invest. 2003;111(2):145–151
  21. Depino AM, Earl C, Kaczmarczyk E, Ferrari C, Besedovsky H, del Rey A, et al. Microglial activation with atypical proinflammatory cytokine expression in a rat model of Parkinson's disease. Eur. J. Neurosci. 2003;18(10):2731–2742
  22. Di Monte DA. The environment and Parkinson's disease: is the nigrostriatal system preferentially targeted by neurotoxins?. Lancet Neurol. 2003;2(9):531–538
  23. Díaz-Hernández M, Hernández F, Martín-Aparicio E, Gómez-Ramos P, Morán MA, Castaño JG, et al. Neuronal induction of the immunoproteasome in Huntington's disease. J. Neurosci. 2003;23(37):11653–11661
  24. Dickman MS. Von economo enchephalitis. Arch. Neurol. 2001;(58):10
  25. Doherty FJ, Dawson S, Mayer RJ. The ubiquitin-proteasome pathway of intracellular proteolysis. Essays Biochem. 2002;38:51–63
  26. Eberling JL, Bankiewicz KS, Jordan S, VanBrocklin HF, Jagust WJ. PET studies of functional compensation in a primate model of Parkinson's disease. Neuroreport. 1997;8(12):2727–2733
  27. Farkas IG, Czigner A, Farkas E, Dobo E, Soos K, Penke B, et al. Beta-amyloid peptide-induced blood-brain barrier disruption facilitates T-cell entry into the rat brain. Acta Histochem. 2003;105(2):115–125
  28. Faulkner JR, Herrmann JE, Woo MJ, Tansey KE, Doan NB, Sofroniew MV. Reactive astrocytes protect tissue and preserve function after spinal cord injury. J. Neurosci. 2004;24(9):2143–2155
  29. Fehling HJ, Swat W, Laplace C, Kuhn R, Rajewsky K, Muller U, et al. MHC class I expression in mice lacking the proteasome subunit LMP-7. Science. 1994;265(5176):1234–1237
  30. Fawcett JW, Asher RA. The glial scar and central nervous system repair. Brain Res. Bull. 1999;49(6):377–391
  31. Ferger B, Leng A, Mura A, Hengerer B, Feldon J. Genetic ablation of tumor necrosis factor-alpha (TNF-α) and pharmacological inhibition of TNF-α synthesis attenuates MPTP toxicity in mouse striatum. J. Neurochem. 2004;89(4):822–833
  32. Forno LS, DeLanney LE, Irwin I, Langston JW. Evolution of nerve fiber degeneration in the striatum in the MPTP-treated squirrel monkey. Mol. Neurobiol. 1994;9(13):163–170
  33. Gao HM, Hong JS, Zhang W, Liu B. Distinct role for microglia in rotenone-induced degeneration of dopaminergic neurons. J. Neurosci. 2002;22:782–790
  34. Gao HM, Hong JS, Zhang W, Liu B. Synergistic dopaminergic neurotoxicity of the pesticide rotenone and inflammation lipopolysaccharide: relevance to the etiology of Parkinson's disease. J. Neurosci. 2003;23(4):1228–1236
  35. Gao HM, Liu B, Zhang W, Hong JS. Synergistic dopaminergic neurotoxicity of MPTP and inflammogen lipopolysaccharide: relevance to the etiology of Parkinson's disease. FASEB J. 2003;17(13):1957–1959
  36. Gómez-Pinilla F, Lee JW, Cotman CW. Basic FGF in adult rat brain: cellular distribution and response to entorhinal lesion and fimbria-fornix transaction. J. Neurosci. 1992;12(1):345–355
  37. Gordon MN, Schreier WA, Ou X, Holcomb LA, Morgan DG. Exaggerated astrocyte reactivity after nigrostriatal deafferentation in the aged rat. J. Comp. Neurol. 1997;388(1):106–119
  38. Gottlieb M, Matute C. Expression of nerve growth factor in astrocytes of the hippocampal CA1 area following transient forebrain ischemia. Neuroscience. 1994;91(3):1027–1034
  39. Groettrup M, Khan S, Schwarz K, Schmidtke G. Interferon-gamma inducible exchanges of 20S proteasome active site subunits: why?. Biochimie. 2001;83(3–4):367–372
  40. Hanisch UK. Microglia as a source and target of cytokines. Glia. 2002;40(2):140–155
  41. Hartz AM, Bauer B, Fricker G, Miller DS. Rapid modulation of P-glycoprotein-mediated transport at the blood-brain barrier by tumor necrosis factor-alpha and lipopolysaccharide. Mol. Pharmacol. 2006;69(2):462–470
  42. Hayley S, Anisman H. Multiple mechanisms of cytokine action in neurodegenerative and psychiatric states: neurochemical and molecular substrates. Curr. Pharm. Des. 2005;11(8):947–962
  43. Hayley S, Brebner K, Lacosta S, Merali Z, Anisman H. Sensitization effects of Tumor Necrosis Factor-a: neuroendocrine, central monoamine and behavioral variations. J. Neurosci. 1999;19(13):5654–5665
  44. Hayley S, Lacosta S, Merali Z, van Rooijen N, Anisman H. Central monoamine and plasma corticosterone changes induced by a bacterial endotoxin: sensitization and cross-sensitization effects. Eur. J. Neurosci. 2001;13:1155–1165
  45. Hayley S, Crocker SJ, Smith P, Shree T, Park DS. Mice lacking the tumor necrosis factor-α or Fas receptors are resistant to MPTP induced death of dopaminergic neurons. J. Neurosci. 2004;24:2045–2053
  46. Herrera AJ, Tomas-Camardiel M, Venero JL, Cano J, Machado A. Inflammatory process as a determinant factor for the degeneration of substantia nigra dopaminergic neurons. J. Neural. Transm. 2005;112(1):111–119
  47. Hirsch E, Graybiel AM, Agid YA. Melanized dopaminergic neurons are differentially susceptible to degeneration in Parkinson's disease. Nature. 1998;334(6180):345–348
  48. Ho A, Blum M. Induction of interleukin-1 associated with compensatory dopaminergic sprouting in the denervated striatum of young mice: of aging and neurodegenerative disease. J. Neurosci. 1998;18(15):5614–5629
  49. Hulse RE, Kunkler PE, Fedynshyn JP, Kraig RP. Optimization of multiplexed bead-based cytokine immunoassays for rat serum and brain tissue. J. Neurosci. Methods. 2004;136(1):87–98
  50. Kawahara K, Hosoya R, Sato H, Tanaka M, Nakajima T, Iwabuchi S. Selective blockade of astrocytic glutamate transporter GLT-1 with dihydrokainate prevents neuronal death during ouabain treatment of astrocyte/neuron cocultures. Glia. 2002;40(3):337–349
  51. Kelada SN, Checkoway H, Kardia SL, Carlson CS, Costa-Mallen P, Eaton DL, et al. 5′ and 3′ region variability in the dopamine transporter gene (SLC6A3), pesticide exposure and Parkinson's disease risk: a hypothesis-generating study. Hum. Mol. Genet. 2006;15(20):3055–3062
  52. Kim WG, Mohney RP, Wilson B, Jeohn GH, Hong JS. Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J. Neurosci. 2000;20:6309–6316
  53. Koustilieri E, Sopper S, Scheller C, ter Meulen V, Riederer P. Parkinsonism in HIV dementia. J. Neural. Transm. 2002;109(5–6):767–775
  54. Krum JM, Phillips TM, Rosenstein JM. Changes in astroglial GLT-1 expression after neural transplantation or stab wounds. Exp. Neurol. 2002;174(2):137–149
  55. Kurkowska-Jastrzebska I, Wronska A, Kohutnicka M, Czlonkowski A, Czlonkowska A. MHC class II positive microglia and lymphocytic infiltration are present in the substantia nigra and striatum and in mouse model of Parkinson's disease. Acta Neurobiol. Exp. 1999;59(1):1–8
  56. Langston JW. Parkinson's complex: Parkinsonism is just the tip of the iceberg. Ann. Neurol. 2006;59(4):591–596
  57. Laurie C, Reynolds A, Coskun O, Bowman E, Gendelman HE, Mosley RL. CD4+ T cells from Copolymer-1 immunized mice protect dopaminergic neurons in the 1-methy-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. J. Neuroimmunol. 2007;183(1–2):60–68
  58. Le W, Rowe D, Xie W, Ortiz I, He Y, Appel SH. Microglial activation and dopaminergic cell injury: an in vitro model relevant to Parkinson's disease. J. Neurosci. 2001;21:8447–8455
  59. Lee da Y, Oh YJ, Jin BK. Thrombin-activated microglia contributes to death of dopaminergic neurons in rat mesencephalic cultures: dual roles of mitogen-activated protein kinase signaling pathways. Glia. 2005;51(2):98–110
  60. Lehnardt S, Massillon L, Follett P, Jensen FE, Ratan R, Rosenberg PA, et al. Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc. Natl. Acad. Sci. 2003;100(14):8514–8519
  61. Ling Z, Zhu Y, Tong CW, Snyder JA, Carvey PM. Progressive dopamine neurons loss following supra-nigral lipopolysaccharide (LPS) infusion into rats exposed to LPS prenatally. Exp. Neurol. 2006;24
  62. Liu B, Gao HM, Hong JS. Parkinson's disease and exposure to infectious agents and pesticides and the occurrence of brain injuries: role of neuroinflammation. Environ. Health Perspect. 2003;111(8):1065–1073
  63. Mandel S, Grunblatt E, Youdim M. cDNA microarray to study gene expression of dopaminergic neurodegeneration and neuroprotection in MPTP and 6-hydroxydopamine models: implications for idiopathic Parkinson's disease. J. Neural. Transm. Suppl. 2000;60:117–124
  64. Marques L, Brucet M, Lloberas J, Celada A. STAT1 regulates lipopolysaccharide and TNF-alpha-dependent expression of transport associated with antigen processing 1 and low molecular mass polypeptide 2 genes in macrophages by distinct mechanisms. J. Immunol. 2004;173(2):1103–1110
  65. Martin S, Gee JR, Bruce-Keller AJ, Keller JN. Loss of an individual proteasome subunit alters motor function but not cognitive function or ambulation in mice. Neurosci. Lett. 2004;357(1):76–78
  66. McCormack AL, Thiruchelvam M, Manning-Bog AB, Thiffault C, Langston JW, Cory-Slechta DA, et al. Environmental risk factors and Parkinson's disease: selective degeneration of nigral dopaminergic neurons caused by the herbicide paraquat. Neurobiol. Dis. 2002;10(2):119–127
  67. McKinnon PJ, Margolskee RF. SC1: a marker for astrocytes in the adult rodent brain is upregulated during reactive astrocytosis.. Brain Res. 1996;709(1):27–36
  68. McLay RN, Freeman SM, Zadina JE. Administration of FGF-1 through transfected cells alleviates MPTP toxicity in mice. Neurotox Res. 2001;3(3):249–253
  69. McNaught KS, Belizaire R, Jenner P, Olanow CW, Isacson O. Selective loss of 20S proteasome alpha-subunits in the substantia nigra pars compacta in Parkinson's disease. Neurosci. Lett. 2002;326(3):155–158
  70. Mishto M, Bellavista E, Santoro A, Stolzing A, Ligorio C, Ohm T, et al. Immunoproteasome and LMP2 polymorphism in aged and Alzheimer's disease brains. Neurobiol. Aging. 2006;27(1):54–66
  71. Mogi M, Harada M, Riederer P, Narabayashi H, Fuitia K, Nagatsu T. Tumor necrosis factor-alpha (TNF-α) increases both in the brain and in the cerebrospinal fluid from Parkinsonian patients. Neurosci. Lett. 1994;165(1–2):208–210
  72. Mogi M, Harada M, Narabayashi H, Inagaki H, Minami M, Nagatsu T. Interleukin (IL)-1beta, IL-2, IL-4, IL-6 and transforming growth factor-alpha levels are elevated in ventricular cerebrospinal fluid in juvenile parkinsonism and Parkinson's disease. Neurosci. Lett. 1996;211(1):13–16
  73. Montero-Menei CN, Sindji L, Garcion E, Mege M, Couez D, Gamelin E, et al. Early events of the inflammatory reaction induced in rat brain by lipopolysaccharide intracerebral injection: relative contribution of peripheral monocytes and activated microglia. Brain Res. 1996;724(1):55–66
  74. Montine TJ, Milatovic D, Gupta RC, Valyi-Nagy T, Morrow JD, Breyer RM. Neuronal oxidative damage from activated innate immunity is EP2 receptor-dependent. J. Neurochem. 2002;83(2):463–470
  75. Nagatsu T, Swada M. Inflammatory process in Parkinson's disease: role for cytokines. Curr. Pharm. Des. 2005;11(8):999–1016
  76. Nagatsu T, Mogi M, Ichinose H, Togari A. Changes in cytokine and neurotrophinsin Parkinson's disease. J. Neural Transm. Suppl. 2000;60:277–290
  77. Nakamura A, Kitami T, Mori H, Mizuno Y, Hattori N. Nuclear localization of the 20S proteasome subunit in Parkinson's disease. Neurosci. Lett. 2006;406(1–2):43–48
  78. Ossowska K, Wardas J, Smiałowska M, Kuter K, Lenda T, Wierońska JM, et al. A slowly developing dysfunction of dopaminergic nigrostriatal neurons induced by long-term paraquat administration in rats: an animal model of preclinical stages of Parkinson's disease?. Eur. J. Neurosci. 2005;22(6):1294–1304
  79. Ossowska K, Wardas J, Kuter K, Nowak P, Dabrowska J, Bortel A, et al. Influence of paraquat on dopaminergic transporter in the rat brain. Pharmacol. Rep. 2005;57(3):330–335
  80. Peng J, Mao XO, Stevenson FF, Hsu M, Andersen JK. The herbicide paraquat induces dopaminergic nigral apoptosis through sustained activation of the JNK pathway. J. Biol. Chem. 2004;279(31):23626–23632
  81. Peng GS, Li G, Tzeng NS, Chen PS, Chuang DM, Hsu YD, et al. Valproate pretreatment protects dopaminergic neurons from LPS-induced neurotoxicity in rat primary midbrain cultures: role of microglia.. Brain Res. Mol. Brain Res. 2005;134(1):162–169
  82. Peng J, Stevenson FF, Doctrow SR, Andersen JK. Superoxide dismutase/catalase mimetics are neuroprotective against selective paraquat-mediated dopaminergic neuron death in the substantia nigra: implications for Parkinson disease. J. Biol. Chem. 2005;280(32):29194–29198
  83. Purisai MG, McCormack AL, Cumine S, Li J, Isla MZ, Di Monte DA. Microglial activation as a priming event leading to paraquat-induced dopaminergic cell degeneration. Neurobiol. Dis. 2007;25(2):392–400
  84. Qian L, Block ML, Wei SJ, Lin CF, Reece J, Pang H, et al. Interleukin-10 protects lipopolysaccharide-induced neurotoxicity in primary midbrain cultures by inhibiting the function of NADPH oxidase. J. Pharmacol. Exp. Ther. 2006;319(1):44–52
  85. Qin L, Liu Y, Wang T, Wei SJ, Block ML, Wilson B, et al. NADPH oxidase mediates lipopolysaccharide-induced neurotoxicity and pro-inflammatory gene expression in activated microglia. J. Biol. Chem. 2004;279(2):1415–1421
  86. Robertson DC, Schmidt O, Ninkina N, Jones PA, Sharkey J, Buchman VL. Developmental loss and resistance to MPTP toxicity of dopaminergic neurons in substantia nigra pars compacta of gamma-synuclein, alpha-synuclein and double alpha/gamma-synuclein null mutant mice. J. Neurochem. 2004;89(5):1126–1136
  87. Rosenzweig HL, Lessov NS, Henshall DC, Minami M, Simon RP, Stenzel-Poore MP. Endotoxin preconditioning prevents cellular inflammatory response during ischemic neuroprotection in mice. Stroke. 2004;35(11):2576–2581
  88. Rossini M, Cheunsuchon B, Donnert E, Ma LJ, Thomas JW, Neilson EG, et al. Immunolocalization of fibroblast growth factor-1 (FGF-1), its receptor (FGFR-1), and fibroblast-specific protein-1 (FSP-1) in inflammatory renal disease. Kidney Int. 2005;68(6):2621–2628
  89. Saint-Pierre M, Tremblay ME, Sik A, Gross RE, Cicchetti F. Temporal effects of paraquat/maneb on microglia activation and dopamine neuronal loss in older rats. J. Biol. Chem. 2006;98(3):760–772
  90. Saporito MS, Brown EM, Miller MS, Carswell S. CEP-1347/KT-7515, an inhibitor of c-jun N-terminal kinase activation, attenuates the 1-methyl-4-phenyl tetrahydropyridine-mediated loss of nigrostriatal dopaminergic neurons In vivo. J. Pharmacol. Exp. Ther. 1999;288(2):421–427
  91. Schmidt ED, Janszen AW, Wouterlood FG, Tilders FJ. Interleukin-1 induced long-lasting changes in hypothalamic corticotropin-releasing hormone (CRH) neurons and hyper-responsiveness of the hypothalamic-pituitary-adrenal axis. J. Neurosci. 1995;15:7417–7426
  92. Sherer TB, Richardson JR, Testa CM, Seo BB, Panov AV, Yagi T, et al. Mechanism of toxicity of pesticides acting at complex 1: relevance to environmental etiologies of Parkinson's disease. J. Neurochem. 2007;100(6):1469–1479
  93. Shie FS, Montine KS, Breyer RM, Montine TJ. Microglial EP2 is critical to neurotoxicity from activated cerebral innate immunity. Glia. 2005;52(1):70–77
  94. Smith WW, Pei Z, Jiang H, Moore DJ, Liang Y, West AB, et al. Leucine-rich repeat kinase 2 (LRRK2) interacts with parkin, and mutant LRRK2 induces neuronal degeneration. Proc. Natl. Acad. Sci. U.S.A. 2005;102(51):18676–18681
  95. Sriram K, Matheson JM, Benkovic SA, Miller DB, Luster MI, O’Callaghan JP. Mice deficient in TNF receptors are protected against dopaminergic neurotoxicity: implications for Parkinson's disease. FASEB J. 2002;16(11):1474–1476
  96. Sriram K, Matheson JM, Benkovic SA, Miller DB, Luster MI, O’Callaghan JP. Deficiency of TNF receptors suppresses microglial activation and alters the susceptibility of brain regions to MPTP-induced neurotoxicity: role of TNF-α. FASEB J. 2006;20(6):670–682
  97. Takeuchi H, Jin S, Wang J, Zhang G, Kawanokuchi J, Kuno R, et al. Tumor necrosis factor-α induces neurotoxicity via glutamate release from hemichannels of activated microglia in an autocrine manner. J. Biol. Chem. 2006;281(30):21362–21368
  98. Tanaka SK, Sugiura S, Matsuoka-Omura E, Sasaki T, Yagita Y, Hori M. Infiltrating macrophages as in vivo targets for intravenous gene delivery in cerebral infarction. Stroke. 2004;35(8):1968–1973
  99. Teismann P, Tieu K, Cohen O, Choi DK, Wu du C, Marks D, et al. Pathogenic role of glial cells in Parkinson's disease. Mov. Disord. 2003;18(2):121–129
  100. Thiruchelvam M, Richfield EK, Baggs RB, Tank AW, Cory-Slechta DA. The nigrostriatal dopaminergic system as a preferential target of repeated exposures to combined paraquat and maneb: implications for Parkinson's disease. J. Neurosci. 2000;20(24):9207–9214
  101. Timmer M, Cesnulevicius K, Winkler C, Kolb J, Lipokatic-Takacs E, Jungnickel J. Fibroblast growth factor (FGF)-2 and FGF receptor 3 are required for the development of the substantia nigra, and FGF-2 plays a crucial role for the rescue of dopaminergic neurons after 6-hydroxydopamine lesion. J. Neurosci. 2007;27(3):459–471
  102. Van Kaer L, Ashton-Rickardt PG, Eichelberger M, Gaczynska M, Nagashima K, Rock KL, et al. Altered peptidase and viral-specific T cell response in LMP2 mutant mice. Immunity. 1994;1(7):533–541
  103. Walker DG, Terai K, Matsuo A, Beach TG, McGeer EG, McGeer PL. Immunohistochemical analyses of fibroblast growth factor receptor-1 in the human substantia nigra. Comparison between normal and Parkinson's disease cases. Brain Res. 1998;794(2):181–187
  104. Wang X, Li X, Erhardt JA, Barone FC, Feuerstein GZ. Detection of tumor necrosis factor-alpha mRNA induction in ischemic brain tolerance by means of real-time polymerase chain reaction. J. Cereb. Blood Flow Metab. 2000;20(1):15–20
  105. Wang V, Chia LG, Ni DR, Cheng LJ, Ho YP, Cheng FC, et al. Effects of the combined treatment of naloxone and indomethacin on catecholamines and behavior after intranigral lipopolysaccharide injection. Neurochem. Res. 2004;29(4):341–346
  106. Wu DC, Jackson-Lewis V, Vila M, Tieu K, Teismann P, Vadseth C, et al. Blockade of microglial activation is neuroprotection in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mouse model of Parkinson disease. J. Neurosci. 2002;22(5):1763–1771
  107. Wu DC, Teismann P, Tieu K, Vila M, Jackson-Lewis V, Ischiropoulos H, et al. NADPH oxidase mediates oxidative stress in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. Proc. Natl. Acad. Sci. U.S.A. 2003;100(10):6145–6150
  108. Xiao H, Banks WA, Niehoff ML, Morley JE. Effect of LPS on the permeability of the blood-brain barrier to insulin. Brain Res. 2001;896(1–2):36–42
  109. Zhang W, Qin L, Wang T, Wei SJ, Gao HM, Liu J, et al. 3-hydroxymorphinan is neurotrophic to dopaminergic neurons and is also neuroprotective against LPS-induced neurotoxicity. FASEB J. 2005;19(3):395–397
  110. Zhou HF, Liu XY, Niu DB, Li FQ, He OH, Wang XM. Triptolide protects dopaminergic neurons from inflammation-mediated damage induced by lipopolysaccharide intranigral injection. Neurobiol. Dis. 2005;18(3):441–449

PII: S0197-4580(07)00449-6

doi: 10.1016/j.neurobiolaging.2007.11.020

Neurobiology of Aging
Volume 30, Issue 9 , Pages 1361-1378 , September 2009

Article Tools

* Image Usage & Resolution