Further characterisation of the LPS model of Parkinson's disease: A comparison of intra-nigral and intra-striatal lipopolysaccharide administration on motor function, microgliosis and nigrostriatal neurodegeneration in the rat

Brain, Behavior, and Immunity

Volumn 27, Issue 1, 2013, Pages 91-100

  Hoban, Deirdre B ^a   Connaughton, Emer ^a   Connaughton, Catherine ^a   Hogan, Grace ^a   Thornton, Chloe ^a   Mulcahy, Padraig ^a   Moloney, Teresa C ^a   Dowd, Eilis ^a  

^a NATIONAL UNIVERSITY OF IRELAND   (Ireland)

Author keywords

Animal models; Behaviour; LPS; Neuroinflammation; Parkinson's disease

Indexed keywords

LIPOPOLYSACCHARIDE; TYROSINE 3 MONOOXYGENASE;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AUTOPSY; CONTROLLED STUDY; GLIOSIS; IMMUNOHISTOCHEMISTRY; MALE; MOTOR PERFORMANCE; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; RAT; STRIATONIGRAL DEGENERATION; SUBSTANTIA NIGRA;

ANIMALS; ANTIGENS, CD11B; BEHAVIOR, ANIMAL; CORPUS STRIATUM; DISEASE MODELS, ANIMAL; GLIOSIS; IMMUNOHISTOCHEMISTRY; LIPOPOLYSACCHARIDES; MALE; MOTOR ACTIVITY; MOTOR SKILLS; PARKINSON DISEASE; RATS; RATS, SPRAGUE-DAWLEY; SUBSTANTIA NIGRA; TYROSINE 3-MONOOXYGENASE;

EID: 84870733873     PISSN: 08891591     EISSN: 10902139     Source Type: Journal    
DOI: 10.1016/j.bbi.2012.10.001     Document Type: Article

References (67)

1. Andersson P.B., Perry V.H., Gordon S. The acute inflammatory response to lipopolysaccharide in CNS parenchyma differs from that in other body tissues. Neuroscience 1992, 48:169-186.
2. Arai H., Furuya T., Yasuda T., Miura M., Mizuno Y., Mochizuki H. Neurotoxic effects of lipopolysaccharide on nigral dopaminergic neurons are mediated by microglial activation, interleukin-1beta, and expression of caspase-11 in mice. J. Biol. Chem. 2004, 279:51647-51653.
3. Arimoto T., Choi D.Y., Lu X., Liu M., Nguyen X.V., Zheng N., Stewart C.A., Kim H.C., Bing G. Interleukin-10 protects against inflammation-mediated degeneration of dopaminergic neurons in substantia nigra. Neurobiol. Aging 2007, 28:894-906.
4. Bing G.Y., Lu X., Zheng N.Y., Jin L., Floyd R.A., Kim H.C. Microglia mediated dopaminergic cell death in the substantia nigra: a new animal model for Parkinson's disease. Free Radical Biol. Med. 1998, 25:S44.
5. Block M.L., Hong J.S. Microglia and inflammation-mediated neurodegeneration: multiple triggers with a common mechanism. Prog. Neurobiol. 2005, 76:77-98.
6. Bourdiol F., Toulmond S., Serrano A., Benavides J., Scatton B. Increase in omega 3 (peripheral type benzodiazepine) binding sites in the rat cortex and striatum after local injection of interleukin-1 tumour necrosis factor-alpha and lipopolysaccharide. Brain Res. 1991, 543:194-200.
7. Byler S.L., Boehm G.W., Karp J.D., Kohman R.A., Tarr A.J., Schallert T., Barth T.M. Systemic lipopolysaccharide plus MPTP as a model of dopamine loss and gait instability in C57Bl/6J mice. Behav. Brain Res. 2009, 198:434-439.
8. Castano A., Herrera A.J., Cano J., Machado A. Lipopolysaccharide intranigral injection induces inflammatory reaction and damage in nigrostriatal dopaminergic system. J. Neurochem. 1998, 70:1584-1592.
9. Castano A., Herrera A.J., Cano J., Machado A. The degenerative effect of a single intranigral injection of LPS on the dopaminergic system is prevented by dexamethasone, and not mimicked by rh-TNF-alpha, IL-1beta and IFN-gamma. J. Neurochem. 2002, 81:150-157.
10. Choi D.Y., Liu M., Hunter R.L., Cass W.A., Pandya J.D., Sullivan P.G., Shin E.J., Kim H.C., Gash D.M., Bing G. Striatal neuroinflammation promotes Parkinsonism in rats. PLoS ONE 2009, 4:e5482.
11. Collins L.M., Toulouse A., Connor T.J., Nolan Y.M. Contributions of central and systemic inflammation to the pathophysiology of Parkinson's disease. Neuropharmacology 2012, 62:2154-2168.
12. De Pablos R.M., Herrera A.J., Villaran R.F., Cano J., Machado A. Dopamine-dependent neurotoxicity of lipopolysaccharide in substantia nigra. Faseb J. 2005, 19:407-409.
13. Dowd E., Monville C., Torres E.M., Dunnett S.B. The Corridor task: a simple test of lateralised response selection sensitive to unilateral dopamine deafferentation and graft-derived dopamine replacement in the striatum. Brain Res. Bull. 2005, 68:24-30.
14. Dutta G., Zhang P., Liu B. The lipopolysaccharide Parkinson's disease animal model: mechanistic studies and drug discovery. Fundam. Clin. Pharmacol. 2008, 22:453-464.
15. Fan L.W., Tien L.T., Zheng B., Pang Y., Lin R.C., Simpson K.L., Ma T., Rhodes P.G., Cai Z. Dopaminergic neuronal injury in the adult rat brain following neonatal exposure to lipopolysaccharide and the silent neurotoxicity. Brain Behav. Immun. 2011, 25:286-297.
16. Fitzsimmons D.F., Moloney T.C., Dowd E. Further validation of the corridor task for assessing deficit and recovery in the hemi-Parkinsonian rat: restoration of bilateral food retrieval by dopamine receptor agonism. Behav. Brain Res. 2006, 169:352-355.
17. Fortier M.E., Joober R., Luheshi G.N., Boksa P. Maternal exposure to bacterial endotoxin during pregnancy enhances amphetamine-induced locomotion and startle responses in adult rat offspring. J. Psychiatr. Res. 2004, 38:335-345.
18. Frank-Cannon T.C., Alto L.T., McAlpine F.E., Tansey M.G. Does neuroinflammation fan the flame in neurodegenerative diseases?. Mol. Neurodegener. 2009, 4:447.
19. Gonzalez-Hernandez T., Cruz-Muros I., Afonso-Oramas D., Salas-Hernandez J., Castro-Hernandez J. Vulnerability of mesostriatal dopaminergic neurons in Parkinson's disease. Front Neuroanat. 2010, 4:140.
20. Grealish S., Mattsson B., Draxler P., Bjorklund A. Characterisation of behavioural and neurodegenerative changes induced by intranigral 6-hydroxydopamine lesions in a mouse model of Parkinson's disease. Eur. J. Neurosci. 2010, 31:2266-2278.
21. Grealish S., Xie L., Kelly M., Dowd E. Unilateral axonal or terminal injection of 6-hydroxydopamine causes rapid-onset nigrostriatal degeneration and contralateral motor impairments in the rat. Brain Res. Bull. 2008, 77:312-319.
22. Grota L.J., Bienen T., Felten D.L. Corticosterone responses of adult Lewis and Fischer rats. J. Neuroimmunol. 1997, 74:95-101.
23. Harkavyi A., Abuirmeileh A., Lever R., Kingsbury A.E., Biggs C.S., Whitton P.S. Glucagon-like peptide 1 receptor stimulation reverses key deficits in distinct rodent models of Parkinson's disease. J. Neuroinflamm. 2008, 5:119.
24. Hart B.L. Biological basis of the behavior of sick animals. Neurosci. Biobehav. Rev. 1988, 12:123-137.
25. Herrera A.J., Castano A., Venero J.L., Cano J., Machado A. The single intranigral injection of LPS as a new model for studying the selective effects of inflammatory reactions on dopaminergic system. Neurobiol. Dis. 2000, 7:429-447.
26. Hirsch E.C., Hunot S. Neuroinflammation in Parkinson's disease: a target for neuroprotection?. Lancet Neurol. 2009, 8:382-397.
27. Hornykiewicz O. Brain monoamines and parkinsonism. Natl. Inst. Drug Abuse Res. Monogr. Ser. 1975, 13-21.
28. Hoshino K., Takeuchi O., Kawai T., Sanjo H., Ogawa T., Takeda Y., Takeda K., Akira S. Cutting edge Toll-like receptor 4 (TLR4)-deficient mice are hyporesponsive to lipopolysaccharide: evidence for TLR4 as the Lps gene product. J. Immunol. 1999, 162:3749-3752.
29. Hsieh P.F., Chia L.G., Ni D.R., Cheng L.J., Ho Y.P., Tzeng S.F., Chang M.H., Hong J.S. Behavior, neurochemistry and histology after intranigral lipopolysaccharide injection. NeuroReport 2002, 13:277-280.
30. Hunter R.L., Cheng B., Choi D.Y., Liu M., Liu S., Cass W.A., Bing G. Intrastriatal lipopolysaccharide injection induces parkinsonism in C57/B6 mice. J. Neurosci. Res. 2009, 87:1913-1921.
31. Hunter R.L., Choi D.Y., Kincer J.F., Cass W.A., Bing G., Gash D.M. Fenbendazole treatment may influence lipopolysaccharide effects in rat brain. Comp. Med. 2007, 57:487-492.
32. Hunter R.L., Dragicevic N., Seifert K., Choi D.Y., Liu M., Kim H.C., Cass W.A., Sullivan P.G., Bing G. Inflammation induces mitochondrial dysfunction and dopaminergic neurodegeneration in the nigrostriatal system. J. Neurochem. 2007, 100:1375-1386.
33. Iravani M.M., Leung C.C., Sadeghian M., Haddon C.O., Rose S., Jenner P. The acute and the long-term effects of nigral lipopolysaccharide administration on dopaminergic dysfunction and glial cell activation. Eur. J. Neurosci. 2005, 22:317-330.
34. Iravani M.M., Sadeghian M., Leung C.C., Tel B.C., Rose S., Schapira A.H., Jenner P. Continuous subcutaneous infusion of pramipexole protects against lipopolysaccharide-induced dopaminergic cell death without affecting the inflammatory response. Exp. Neurol. 2008, 212:522-531.
35. Jankovic J. Parkinson's disease: clinical features and diagnosis. J. Neurol. Neurosurg. Psychiatry 2008, 79:368-376.
36. Kim W.G., Mohney R.P., Wilson B., Jeohn G.H., Liu B., Hong J.S. Regional difference in susceptibility to lipopolysaccharide-induced neurotoxicity in the rat brain: role of microglia. J. Neurosci. 2000, 20:6309-6316.
37. Koprich J.B., Reske-Nielsen C., Mithal P., Isacson O. Neuroinflammation mediated by IL-1beta increases susceptibility of dopamine neurons to degeneration in an animal model of Parkinson's disease. J. Neuroinflamm. 2008, 5:88.
38. Kortekaas R., Leenders K.L., van Oostrom J.C., Vaalburg W., Bart J., Willemsen A.T., Hendrikse N.H. Blood-brain barrier dysfunction in parkinsonian midbrain in vivo. Ann. Neurol. 2005, 57:176-179.
39. Lees A.J., Hardy J., Revesz T. Parkinson's disease. Lancet 2009, 373:2055-2066.
40. Lehnardt S., Massillon L., Follett P., Jensen F.E., Ratan R., Rosenberg P.A., Volpe J.J., Vartanian T. Activation of innate immunity in the CNS triggers neurodegeneration through a Toll-like receptor 4-dependent pathway. Proc. Natl. Acad. Sci. USA 2003, 100:8514-8519.
41. Ling Z., Chang Q.A., Tong C.W., Leurgans S.E., Lipton J.W., Carvey P.M. Rotenone potentiates dopamine neuron loss in animals exposed to lipopolysaccharide prenatally. Exp. Neurol. 2004, 190:373-383.
42. Ling Z.D., Chang Q., Lipton J.W., Tong C.W., Landers T.M., Carvey P.M. Combined toxicity of prenatal bacterial endotoxin exposure and postnatal 6-hydroxydopamine in the adult rat midbrain. Neuroscience 2004, 124:619-628.
43. Liu M., Bing G. Lipopolysaccharide animal models for Parkinson's disease. Parkinsons Dis. 2011, 327089.
44. Long-Smith C.M., Collins L., Toulouse A., Sullivan A.M., Nolan Y.M. Interleukin-1 beta contributes to dopaminergic neuronal death induced by lipopolysaccharide-stimulated rat glia in vitro. J. Neuroimmunol. 2010, 226:20-26.
45. Lu X., Bing G., Hagg T. Naloxone prevents microglia-induced degeneration of dopaminergic substantia nigra neurons in adult rats. Neuroscience 2000, 97:285-291.
46. McCoy M.K., Martinez T.N., Ruhn K.A., Szymkowski D.E., Smith C.G., Botterman B.R., Tansey K.E., Tansey M.G. 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. 2006, 26:9365-9375.
47. McGeer P.L., Itagaki S., Boyes B.E., McGeer E.G. Reactive microglia are positive for HLA-DR in the substantia nigra of Parkinson's and Alzheimer's disease brains. Neurology 1988, 38:1285-1291.
48. Metz G.A., Whishaw I.Q. Drug-induced rotation intensity in unilateral dopamine-depleted rats is not correlated with end point or qualitative measures of forelimb or hindlimb motor performance. Neuroscience 2002, 111:325-336.
49. Moloney T.C., Dockery P., Windebank A.J., Barry F.P., Howard L., Dowd E. Survival and immunogenicity of mesenchymal stem cells from the green fluorescent protein transgenic rat in the adult rat brain. Neurorehabil. Neural Repair 2010, 24:645-656.
50. Moloney T.C., Rooney G.E., Barry F.P., Howard L., Dowd E. Potential of rat bone marrow-derived mesenchymal stem cells as vehicles for delivery of neurotrophins to the Parkinsonian rat brain 2010, Brain Res.
51. Montero-Menei C.N., Sindji L., Garcion E., Mege M., Couez D., Gamelin E., Darcy F. 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, 724:55-66.
52. Montero-Menei C.N., Sindji L., Pouplard-Barthelaix A., Jehan F., Denechaud L., Darcy F. Lipopolysaccharide intracerebral administration induces minimal inflammatory reaction in rat brain. Brain Res. 1994, 653:101-111.
53. Mosley R.L., Benner E.J., Kadiu I., Thomas M., Boska M.D., Hasan K., Laurie C., Gendelman H.E. Neuroinflammation, oxidative stress and the pathogenesis of Parkinson's disease. Clin. Neurosci. Res. 2006, 6:261-281.
54. Mulcahy P., O'Doherty A., Paucard A., O'Brien T., Kirik D., Dowd E. Development and characterisation of a novel rat model of Parkinson's disease induced by sequential intranigral administration of AAV-alpha-synuclein and the pesticide, rotenone. Neuroscience 2012, 203:170-179.
55. Mulcahy P., Walsh S., Paucard A., Rea K., Dowd E. Characterisation of a novel model of Parkinson's disease by intra-striatal infusion of the pesticide rotenone. Neuroscience 2011, 181:234-242.
56. Olsson M., Nikkhah G., Bentlage C., Bjorklund A. Forelimb akinesia in the rat Parkinson model: differential effects of dopamine agonists and nigral transplants as assessed by a new stepping test. J. Neurosci. 1995, 15:3863-3875.
57. Paxinos G., Watson C. The Rat Brain in Stereotaxic Coordinates 2007, Springer Academic Press.
58. Qin L., Wu X., Block M.L., Liu Y., Breese G.R., Hong J.S., Knapp D.J., Crews F.T. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 2007, 55:453-462.
59. Schallert T., Fleming S.M., Leasure J.L., Tillerson J.L., Bland S.T. CNS plasticity and assessment of forelimb sensorimotor outcome in unilateral rat models of stroke, cortical ablation, parkinsonism and spinal cord injury. Neuropharmacology 2000, 39:777-787.
60. Szczepanik A.M., Fishkin R.J., Rush D.K., Wilmot C.A. Effects of chronic intrahippocampal infusion of lipopolysaccharide in the rat. Neuroscience 1996, 70:57-65.
61. Tansey M.G., Goldberg M.S. Neuroinflammation in Parkinson's disease: its role in neuronal death and implications for therapeutic intervention. Neurobiol. Dis. 2010, 37:510-518.
62. Taylor A.N., Tio D.L., Romeo H.E. The febrile response to intraperitoneal lipopolysaccharide: strain and gender differences in rats. J. Neuroimmunol. 2005, 158:86-93.
63. Tonelli L., Webster J.I., Rapp K.L., Sternberg E. Neuroendocrine responses regulating susceptibility and resistance to autoimmune/inflammatory disease in inbred rat strains. Immunol. Rev. 2001, 184:203-211.
64. Turnbull A.V., Rivier C.L. Sprague-Dawley rats obtained from different vendors exhibit distinct adrenocorticotropin responses to inflammatory stimuli. Neuroendocrinology 1999, 70:186-195.
65. Ungerstedt U., Arbuthnott G.W. Quantitative recording of rotational behavior in rats after 6-hydroxy-dopamine lesions of the nigrostriatal dopamine system. Brain Res. 1970, 24:4485.
66. Walsh S., Finn D.P., Dowd E. Time-course of nigrostriatal neurodegeneration and neuroinflammation in the 6-hydroxydopamine-induced axonal and terminal lesion models of Parkinson's disease in the rat. Neuroscience 2011, 175:251-261.
67. Zhang J., Stanton D.M., Nguyen X.V., Liu M., Zhang Z., Gash D., Bing G. Intrapallidal lipopolysaccharide injection increases iron and ferritin levels in glia of the rat substantia nigra and induces locomotor deficits. Neuroscience 2005, 135:829-838.