Granulocyte macrophage-colony stimulating factor protects against substantia nigra dopaminergic cell loss in an environmental toxin model of Parkinson's disease

Neurobiology of Disease

Volumn 43, Issue 1, 2011, Pages 99-112

  Mangano, E N ^a   Peters, S ^a   Litteljohn, D ^a   So, R ^a   Bethune, C ^a   Bobyn, J ^a   Clarke, M ^a   Hayley, S ^a  

^a CARLETON UNIVERSITY   (Canada)

Author keywords

Cytokine; GM CSF; Inflammatory; Neurodegeneration; Paraquat; Parkinson's disease; Pesticide; Toxin; Trophic factor

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; GRANULOCYTE MACROPHAGE COLONY STIMULATING FACTOR; LIPOPOLYSACCHARIDE; NEURITE PROMOTING FACTOR; PARAQUAT; PROTEIN BCL 2;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; ASTROCYTE; BLOOD BRAIN BARRIER; BRAIN LEVEL; BRAIN TISSUE; CELL LOSS; CELL SURVIVAL; COMORBIDITY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DRUG EFFICACY; DRUG PENETRATION; HIPPOCAMPUS; HISTOPATHOLOGY; IMMUNOREACTIVITY; MALE; MESENCEPHALON; MICROGLIA; MOUSE; NERVE CELL PLASTICITY; NEUROPROTECTION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN ANALYSIS; SUBSTANTIA NIGRA PARS COMPACTA;

ANIMALS; CELL DEATH; DISEASE MODELS, ANIMAL; DOPAMINE; GRANULOCYTE-MACROPHAGE COLONY-STIMULATING FACTOR; HERBICIDES; INJECTIONS, INTRALESIONAL; LIPOPOLYSACCHARIDES; MALE; MICE; MICE, INBRED C57BL; NEURONS; NEUROPROTECTIVE AGENTS; PARAQUAT; PARKINSONIAN DISORDERS; SUBSTANTIA NIGRA;

EID: 79955945545     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.02.011     Document Type: Article

References (90)

1. Anisman H., et al. Neurotransmitter, peptide and cytokine processes in relation to depressive disorder: comorbidity between depression and neurodegenerative disorders. Prog. Neurobiol. 2008, 85:1-74.
2. Baquet Z.C., et al. Brain-derived neurotrophic factor is required for the establishment of the proper number of dopaminergic neurons in the substantia nigra pars compacta. J. Neurosci. 2005, 25:6251-6259.
3. Bertrand E., et al. Degenerative axonal changes in the hippocampus and amygdala in Parkinson's disease. Folia Neuropathol. 2003, 41:197-207.
4. Bossers K., et al. Analysis of gene expression in Parkinson's disease: possible involvement of neurotrophic support and axon guidance in dopaminergic cell death. Brain Pathol. 2009, 19:91-107.
5. Bouhy D., et al. Delayed GM-CSF treatment stimulates axonal regeneration and functional recovery in paraplegic rats via an increased BDNF expression by endogenous macrophages. FASEB J. 2006, 20:1239-1241.
6. Bruck A., et al. Hippocampal and prefrontal atrophy in patients with early non-demented Parkinson's disease is related to cognitive impairment. J. Neurol. Neurosurg. Psychiatry 2004, 75:1467-1469.
7. Cannon J.R., et al. A highly reproducible rotenone model of Parkinson's disease. Neurobiol. Dis. 2009, 34:279-290.
8. Carvey P.M., et al. Progressive dopamine neuron loss in Parkinon's disease: the multiple hit hypothesis. Cell Transplant. 2006, 15:239-250.
9. Chauhan N.B., et al. Depletion of glial cell line-derived neurotrophic factor in substantia nigra neurons of Parkinson's disease brain. J. Chem. Neuroanat. 2001, 21:277-288.
10. Chen P.S., et al. Valproate protects dopaminergic neurons in midbrain neuron/glia cultures by stimulating the release of neurotrophic factors from astrocytes. Mol. Psychiatry 2006, 11:1116-1125.
11. Cicchetti F., et al. Environmental toxins and Parkinson's disease: what have we learned from pesticide-induced animal models?. Trends Pharmacol. Sci. 2009, 30:475-483.
12. Davignon J.L., et al. Selective production of interleukin 3 (IL3) and granulocyte-macrophage colony-stimulating factor (GM-CSF) in vitro by murine L3T4+ T cells: lack of spontaneous IL3 and GM-CSF production by Ly-2-/L3T4- lpr subset. Eur. J. Immunol. 1988, 18:1367-1372.
13. Di Monte D.A. The environment and Parkinson's disease: is the nigrostriatal system preferentially targeted by neurotoxins?. Lancet Neurol. 2003, 2:531-538.
14. Eslamboli A. Assessment of GDNF in primate models of Parkinson's disease: comparison with human studies. Rev. Neurosci. 2005, 16:303-310.
15. Farabaugh A.H., et al. Pattern of depressive symptoms in Parkinson's disease. Psychosomatics 2009, 50:448-454.
16. Fischer H.G., Reichmann G. Brain dendritic cells and macrophages/microglia in central nervous system inflammation. J. Immunol. 2001, 166:2717-2726.
17. Fitzmaurice P.S., et al. Nigral glutathione deficiency is not specific for idiopathic Parkinson's disease. Mov. Disord. 2003, 18:969-976.
18. Franzen R., et al. Nervous system injury: focus on the inflammatory cytokine 'granulocyte-macrophage colony stimulating factor'. Neurosci. Lett. 2004, 361:76-78.
19. Galvin J.E., et al. Axon pathology in Parkinson's disease and Lewy body dementia hippocampus contains alpha-, beta-, and gamma-synuclein. Proc. Natl. Acad. Sci. U. S. A. 1999, 96:13450-13455.
20. Gao H.M., et al. Critical role for microglial NADPH oxidase in rotenone-induced degeneration of dopaminergic neurons. J. Neurosci. 2003, 23:6181-6187.
21. Gash D.M., et al. Functional recovery in parkinsonian monkeys treated with GDNF. Nature 1996, 380:252-255.
22. Gourley S.L., et al. Acute hippocampal brain-derived neurotrophic factor restores motivational and forced swim performance after corticosterone. Biol. Psychiatry 2008, 64:884-890.
23. Grondin R., et al. Chronic, controlled GDNF infusion promotes structural and functional recovery in advanced parkinsonian monkeys. Brain 2002, 125:2191-2201.
24. Guerini F.R., et al. BDNF Val66Met polymorphism is associated with cognitive impairment in Italian patients with Parkinson's disease. Eur. J. Neurol. 2009, 16:1240-1245.
25. Guillemin G., et al. Granulocyte macrophage colony stimulating factor stimulates in vitro proliferation of astrocytes derived from simian mature brains. Glia 1996, 16:71-80.
26. Ha Y., et al. Synthes Award for Resident Research on Spinal Cord and Spinal Column Injury: granulocyte macrophage colony stimulating factor (GM-CSF) prevents apoptosis and improves functional outcome in experimental spinal cord contusion injury. Clin. Neurosurg. 2005, 52:341-347.
27. Hartmann A., et al. FADD: A link between TNF family receptors and caspases in Parkinson's disease. Neurology 2002, 58:308-310.
28. Hayashi M., et al. Granulocyte-macrophage colony stimulating factor inhibits class II major histocompatibility complex expression and antigen presentation by microglia. J. Neuroimmunol. 1993, 48:23-32.
29. Hayashi K., et al. Activation of dendritic-like cells and neural stem/progenitor cells in injured spinal cord by GM-CSF. Neurosci. Res. 2009, 64:96-103.
30. Hayley S., et al. Sensitization to the effects of tumor necrosis factor-alpha: neuroendocrine, central monoamine, and behavioral variations. J. Neurosci. 1999, 19:5654-5665.
31. Hayley S., et al. Regulation of dopaminergic loss by Fas in a 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine model of Parkinson's disease. J. Neurosci. 2004, 24:2045-2053.
32. Heldt S.A., et al. Hippocampus-specific deletion of BDNF in adult mice impairs spatial memory and extinction of aversive memories. Mol. Psychiatry 2007, 12:656-670.
33. Hercus T.R., et al. The granulocyte-macrophage colony-stimulating factor receptor: linking its structure to cell signaling and its role in disease. Blood 2009, 114:1289-1298.
34. Hirsch E.C., Hunot S. Neuroinflammation in Parkinson's disease: a target for neuroprotection?. Lancet Neurol. 2009, 8:382-397.
35. Howells D.W., et al. Reduced BDNF mRNA expression in the Parkinson's disease substantia nigra. Exp. Neurol. 2000, 166:127-135.
36. Huang X., et al. GM-CSF inhibits apoptosis of neural cells via regulating the expression of apoptosis-related proteins. Neurosci. Res. 2007, 58:50-57.
37. Huang X., et al. GM-CSF inhibits glial scar formation and shows long-term protective effect after spinal cord injury. J. Neurol. Sci. 2009, 277:87-97.
38. Huang R., et al. Gene therapy using lactoferrin-modified nanoparticles in a rotenone-induced chronic Parkinson model. J. Neurol. Sci. 2010, 290:123-130.
39. Hung H.C., Lee E.H. The mesolimbic dopaminergic pathway is more resistant than the nigrostriatal dopaminergic pathway to MPTP and MPP+toxicity: role of BDNF gene expression. Brain Res. Mol. Brain Res. 1996, 41:14-26.
40. Hunot S., et al. JNK-mediated induction of cyclooxygenase 2 is required for neurodegeneration in a mouse model of Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 2004, 101:665-670.
41. Jenner P. Oxidative mechanisms in nigral cell death in Parkinson's disease. Mov. Disord. 1998, 13(Suppl 1):24-34.
42. Jokinen P., et al. Impaired cognitive performance in Parkinson's disease is related to caudate dopaminergic hypofunction and hippocampal atrophy. Parkinsonism Relat. Disord. 2009, 15:88-93.
43. Juillerat-Jeanneret L., Schmitt F. Chemical modification of therapeutic drugs or drug vector systems to achieve targeted therapy: looking for the grail. Med. Res. Rev. 2007, 27:574-590.
44. Kearns C.M., Gash D.M. GDNF protects nigral dopamine neurons against 6-hydroxydopamine in vivo. Brain Res. 1995, 672:104-111.
45. Kim N.K., et al. Granulocyte-macrophage colony-stimulating factor promotes survival of dopaminergic neurons in the 1-methyl-4-phenyl-1,2,3,6-tetrahydropyridine-induced murine Parkinson's disease model. Eur. J. Neurosci. 2009, 29:891-900.
46. Kirik D., et al. Localized striatal delivery of GDNF as a treatment for Parkinson disease. Nat. Neurosci. 2004, 7:105-110.
47. Knott C., et al. Inflammatory regulators in Parkinson's disease: iNOS, lipocortin-1, and cyclooxygenases-1 and ?2. Mol. Cell. Neurosci. 2000, 16:724-739.
48. Kordower J.H., et al. Clinicopathological findings following intraventricular glial-derived neurotrophic factor treatment in a patient with Parkinson's disease. Ann. Neurol. 1999, 46:419-424.
49. Lang A.E., et al. Randomized controlled trial of intraputamenal glial cell line-derived neurotrophic factor infusion in Parkinson disease. Ann. Neurol. 2006, 59:459-466.
50. Levivier M., et al. Intrastriatal implantation of fibroblasts genetically engineered to produce brain-derived neurotrophic factor prevents degeneration of dopaminergic neurons in a rat model of Parkinson's disease. J. Neurosci. 1995, 15:7810-7820.
51. Lin L.F., et al. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 1993, 260:1130-1132.
52. Litteljohn D., et al. Interferon-gamma deficiency modifies the motor and co-morbid behavioral pathology and neurochemical changes provoked by the pesticide paraquat. Neuroscience 2009, 164:1894-1906.
53. Liu B., et al. Parkinson's disease and exposure to infectious agents and pesticides and the occurrence of brain injuries: role of neuroinflammation. Environ. Health Perspect. 2003, 111:1065-1073.
54. Malipiero U.V., et al. Production of hemopoietic colony-stimulating factors by astrocytes. J. Immunol. 1990, 144:3816-3821.
55. Mangano E.N., Hayley S. Inflammatory priming of the substantia nigra influences the impact of later paraquat exposure: Neuroimmune sensitization of neurodegeneration. Neurobiol. Aging 2009, 30:1361-1378.
56. Masaki T., et al. Association between a polymorphism of brain-derived neurotrophic factor gene and sporadic Parkinson's disease. Ann. Neurol. 2003, 54:276-277.
57. Maswood N., et al. Effects of chronic intraputamenal infusion of glial cell line-derived neurotrophic factor (GDNF) in aged Rhesus monkeys. Neurobiol. Aging 2002, 23:881-889.
58. McCoy M.K., et al. Intranigral lentiviral delivery of dominant-negative TNF attenuates neurodegeneration and behavioral deficits in hemiparkinsonian rats. Mol. Ther. 2008, 16:1572-1579.
59. McLay R.N., et al. Granulocyte-macrophage colony-stimulating factor crosses the blood-brain and blood-spinal cord barriers. Brain 1997, 120(Pt 11):2083-2091.
60. Mogi M., et al. Brain-derived growth factor and nerve growth factor concentrations are decreased in the substantia nigra in Parkinson's disease. Neurosci. Lett. 1999, 270:45-48.
61. Mount M.P., et al. Involvement of interferon-gamma in microglial-mediated loss of dopaminergic neurons. J. Neurosci. 2007, 27:3328-3337.
62. Murer M.G., et al. Brain-derived neurotrophic factor in the control human brain, and in Alzheimer's disease and Parkinson's disease. Prog. Neurobiol. 2001, 63:71-124.
63. Nagatsu T., Sawada M. Biochemistry of postmortem brains in Parkinson's disease: historical overview and future prospects. J. Neural Transm. 2007, 113-120. (Suppl.).
64. Nakagawa T., et al. Intracarotid injection of granulocyte-macrophage colony-stimulating factor induces neuroprotection in a rat transient middle cerebral artery occlusion model. Brain Res. 2006, 1089:179-185.
65. Nimmerjahn A., et al. Resting microglial cells are highly dynamic surveillants of brain parenchyma in vivo. Science 2005, 308:1314-1318.
66. Nutt J.G., et al. Randomized, double-blind trial of glial cell line-derived neurotrophic factor (GDNF) in PD. Neurology 2003, 60:69-73.
67. Pardridge W.M. Targeting neurotherapeutic agents through the blood-brain barrier. Arch. Neurol. 2002, 59:35-40.
68. Peleshok J., Saragovi H.U. Functional mimetics of neurotrophins and their receptors. Biochem. Soc. Trans. 2006, 34:612-617.
69. Peterson A.L., Nutt J.G. Treatment of Parkinson's disease with trophic factors. Neurotherapeutics 2008, 5:270-280.
70. Porritt M.J., et al. Inhibiting BDNF expression by antisense oligonucleotide infusion causes loss of nigral dopaminergic neurons. Exp. Neurol. 2005, 192:226-234.
71. Purisai M.G., et al. Microglial activation as a priming event leading to paraquat-induced dopaminergic cell degeneration. Neurobiol. Dis. 2007, 25:392-400.
72. Re F., et al. Granulocyte-macrophage colony-stimulating factor induces an expression program in neonatal microglia that primes them for antigen presentation. J. Immunol. 2002, 169:2264-2273.
73. Reddy P.H., et al. Granulocyte-macrophage colony-stimulating factor antibody suppresses microglial activity: implications for anti-inflammatory effects in Alzheimer's disease and multiple sclerosis. J. Neurochem. 2009, 111:1514-1528.
74. Salehi Z., Mashayekhi F. Brain-derived neurotrophic factor concentrations in the cerebrospinal fluid of patients with Parkinson's disease. J. Clin. Neurosci. 2009, 16:90-93.
75. Salvatore M.F., et al. Point source concentration of GDNF may explain failure of phase II clinical trial. Exp. Neurol. 2006, 202:497-505.
76. Santambrogio L., et al. Developmental plasticity of CNS microglia. Proc. Natl. Acad. Sci. U. S. A. 2001, 98:6295-6300.
77. Schabitz W.R., et al. A neuroprotective function for the hematopoietic protein granulocyte-macrophage colony stimulating factor (GM-CSF). J. Cereb. Blood Flow Metab. 2008, 28:29-43.
78. Schermer C., Humpel C. Granulocyte macrophage-colony stimulating factor activates microglia in rat cortex organotypic brain slices. Neurosci. Lett. 2002, 328:180-184.
79. Schmidt H.D., Duman R.S. The role of neurotrophic factors in adult hippocampal neurogenesis, antidepressant treatments and animal models of depressive-like behavior. Behav. Pharmacol. 2007, 18:391-418.
80. Schmidt H.D., Duman R.S. Peripheral BDNF Produces Antidepressant-Like Effects in Cellular and Behavioral Models. Neuropsychopharmacology 2010, 35:2378-2391.
81. Sherer T.B., et al. Mechanism of toxicity of pesticides acting at complex I: relevance to environmental etiologies of Parkinson's disease. J. Neurochem. 2007, 100:1469-1479.
82. Shults C.W., et al. BDNF attenuates the effects of intrastriatal injection of 6-hydroxydopamine. NeuroReport 1995, 6:1109-1112.
83. Somayajulu-Nitu M., et al. Paraquat induces oxidative stress, neuronal loss in substantia nigra region and parkinsonism in adult rats: neuroprotection and amelioration of symptoms by water-soluble formulation of coenzyme Q10. BMC Neurosci. 2009, 10:88.
84. Taliaz D., Stall N., Dar D.E., Zangen A. Knockdown of brain-derived neurotrophic factor in specific brain sites precipitates behaviors associated with depression and reduces neurogenesis. Mol. Psychiatry 2010, 15(1):80-92.
85. Tatton W.G., et al. Apoptosis in Parkinson's disease: signals for neuronal degradation. Ann. Neurol. 2003, 53(Suppl. 3):S61-S70. (discussion S70-2).
86. The Cytokine Handbook 2003, Academic Press, London. A.W. Thomson, M.T. Lotze (Eds.).
87. Tomac A., et al. Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature 1995, 373:335-339.
88. Whitton P.S. Inflammation as a causative factor in the aetiology of Parkinson's disease. Br. J. Pharmacol. 2007, 150:963-976.
89. Yasuhara T., et al. Glial cell line-derived neurotrophic factor (GDNF) therapy for Parkinson's disease. Acta Med. Okayama 2007, 61:51-56.
90. Zhang H.T., et al. Immunohistochemical distribution of NGF, BDNF, NT-3, and NT-4 in adult rhesus monkey brains. J. Histochem. Cytochem. 2007, 55:1-19.