The intranigral injection of tissue plasminogen activator induced blood-brain barrier disruption, inflammatory process and degeneration of the dopaminergic system of the rat

NeuroToxicology

Volumn 30, Issue 3, 2009, Pages 403-413

  Villarán, Ruth F ^a   de Pablos, Rocío M ^a   Argüelles, Sandro ^a   Espinosa Oliva, Ana M ^a   Tomás Camardiel, Mayka ^a   Herrera, Antonio J ^a   Cano, Josefina ^a   Machado, Alberto ^a  

^a UNIVERSITY OF SEVILLE   (Spain)

Author keywords

BDNF; Disruption of BBB; Dopaminergic neurodegeneration; Excitotoxicity; Microglial activation; tPA

Indexed keywords

4 AMINOBUTYRIC ACID RECEPTOR; AQUAPORIN 4; BRAIN DERIVED NEUROTROPHIC FACTOR; CYCLIC AMP RESPONSIVE ELEMENT BINDING PROTEIN; INDUCIBLE NITRIC OXIDE SYNTHASE; MITOGEN ACTIVATED PROTEIN KINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; NEURONAL NITRIC OXIDE SYNTHASE; NITRIC OXIDE SYNTHASE; TISSUE PLASMINOGEN ACTIVATOR;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; BLOOD BRAIN BARRIER; CELL ACTIVATION; CELL LOSS; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; DOPAMINERGIC SYSTEM; ENZYME PHOSPHORYLATION; EXCITOTOXICITY; GABAERGIC SYSTEM; INFLAMMATION; MACROGLIA; MALE; MICROGLIA; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PRIORITY JOURNAL; PROTEIN EXPRESSION; RAT; SUBSTANTIA NIGRA;

ALPHA-SYNUCLEIN; ANIMALS; ASTROCYTES; BLOOD-BRAIN BARRIER; BRAIN-DERIVED NEUROTROPHIC FACTOR; DOPAMINE; GAMMA-AMINOBUTYRIC ACID; INFLAMMATION MEDIATORS; MALE; MAP KINASE SIGNALING SYSTEM; MICROGLIA; MICROINJECTIONS; NEURONS; NITRIC OXIDE SYNTHASE TYPE I; NITRIC OXIDE SYNTHASE TYPE II; RATS; RATS, WISTAR; SUBSTANTIA NIGRA; TISSUE PLASMINOGEN ACTIVATOR;

RATTUS;

EID: 67349260743     PISSN: 0161813X     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuro.2009.02.011     Document Type: Article

References (87)

1. Bignami A., Eng L.F., Dahl D., and Uyeda C.T. Localization of glial fibrillary acid protein in astrocytes by immunofluorescence. Brain Res 43 (1972) 429-435
2. Bignami A., and Dahl D. The astroglial response to stabbing. Immunofluorescence studies with antibodies to astrocyte-specific protein (GFAP) in mammalian and submammalian vertebrates. Neuropathol Appl Neurobiol 2 (1976) 99-100
3. Binder D.K., and Scharfman H.E. Brain-derived neurotrophic factor. Growth Factors 22 (2004) 123-131
4. Carreño-Müller E., Herrera A.J., de Pablos R.M., Tomás-Camardiel M., Venero J.L., Cano J., et al. Thrombin induces in vivo degeneration of nigral dopaminergic neurones along with the activation of microglia. J Neurochem 84 (2003) 1201-1214
5. Castaño A., Herrera A.J., Cano J., and Machado A. Effects of a short period of vitamin E-deficient diet in the turnover of different neurotransmitters in substantia nigra and striatum of the rat. Neuroscience 53 (1993) 179-185
6. Castaño A., Herrera A.J., Cano J., and Machado A. Lipopolysaccharide intranigral injection induces inflammatory reaction and damage in nigrostriatal dopaminergic system. J Neurochem 70 (1998) 1584-1592
7. Castellino F.J. Plasmin. In: Barrett A.J., Rawlings N.D., and Woessner J.F. (Eds). Handbook of Proteolytic Enzymes (1998), Academic Press, San Diego 190-199
8. Choi S.H., Lee D.Y., Ryu J.K., Kim J., Joe E.H., and Jin B.K. Thrombin induces nigral dopaminergic neurodegeneration in vivo by altering expression of death-related proteins. Neurobiol Dis 14 (2003) 181-193
9. Chun H.S., Gibson G.E., DeGiorgio L.A., Zhang H., Kidd V.J., and Son J.H. Dopaminergic cell death induced by MPP(+), oxidant and specific neurotoxicants shares the common molecular mechanism. J Neurochem 76 (2001) 1010-1021
10. Cinelli P., Madani R., Tsuzuki N., Vallet P., Arras M., Zhao C.N., et al. Neuroserpin, a neuroprotective factor in focal ischemic stroke. Mol Cell Neurosci 18 (2001) 443-457
11. Cross D.A., Alessi D.R., Cohen P., Andjelkovich M., and Hemmings B.A. Inhibition of glycogen synthase kinase-3 by insulin mediated by protein kinase B. Nature 378 (1995) 785-789
12. Dahl D., and Bignami A. Heterogeneity of the glial fibrillary acid protein in gliosed human brain. J Neurol Sci 23 (1974) 551-563
13. de Pablos R.M., Herrera A.J., Villarán R.F., Cano J., and Machado A. Dopamine-dependent neurotoxicity of lipopolysaccharide in substantia nigra. FASEB J 19 (2005) 407-409
14. de Pablos R.M., Villaran R.F., Argüelles S., Herrera A.J., Venero J.L., Ayala A., et al. Stress increases vulnerability to inflammation in the rat prefrontal cortex. J Neurosci 26 (2006) 5709-5719
15. Erlander M.G., Tillakaratne N.J., Feldblum S., Patel N., and Tobin A.J. Two genes encode distinct glutamate decarboxylases. Neuron 7 (1991) 91-100
16. Fenton II J.W. Thrombin specificity. Ann N Y Acad Sci 370 (1981) 468-495
17. Fernández-Monreal M., López-Atalaya J.P., Benchenane K., Cacquevel M., Dulin F., Le Caer J.P., et al. Arginine 260 of the amino-terminal domain of NR1 subunit is critical for tissue-type plasminogen activator-mediated enhancement of NMDA receptor signalling. J Biol Chem 279 (2004) 50850-50856
18. Fryer H.J., Davis G.E., Manthorpe M., and Varon S. Lowry protein assay using an automatic microtiter plate spectrophotometer. Anal Biochem 153 (1986) 262-266
19. Gabriel C., Ali C., Lesné S., Fernández-Monreal M., Docagne F., Plawinski L., et al. Transforming growth factor alpha-induced expression of type 1 plasminogen activator inhibitor in astrocytes rescues neurons from excitotoxicity. FASEB J 17 (2003) 277-279
20. Gardoni F., and Di Luca M. New targets for pharmacological intervention in the glutamatergic synapse. Eur J Pharmacol 545 (2006) 2-10
21. Ghabriel M.N., Zhu C., Hermanis G., and Allt G. Immunological targeting of the endothelial barrier antigen (EBA) in vivo leads to opening of the blood-brain barrier. Brain Res 878 (2000) 127-135
22. Goto H., Fujisawa H., Oka F., Nomura S., Kajiwara K., Kato S., et al. Neurotoxic effects of exogenous recombinant tissue-type plasminogen activator on the normal rat brain. J Neurotrauma 24 (2007) 745-752
23. Graeber M.B., Bise K., and Mehrain P. CR3/43, a marker foractvated human microglia: application to diagnostic neuropathology. Neuropathol Appl Neurobiol 20 (1994) 406-408
24. Gravanis I., and Tsirka S.E. Tissue plasminogen activator and glial function. Glia 49 (2005) 177-183
25. Gundersen H.G.J., Bagger P., Bendtsen T.F., Evans S.M., Korbo L., Marcussen N., et al. The new stereological tools: dissector, fractionator, nucleator, and point sampled intercepts and their use in pathological research and diagnosis. Acta Pathol Microbiol Immunol Scand 96 (1988) 857-881
26. Hadj Tahar A., Grégoire L., Darré A., Bélanger N., Meltzer L., and Bédard P.J. Effect of a selective glutamate antagonist on L-dopa-induced dyskinesias in drug-naive parkinsonian monkeys. Neurobiol Dis 15 (2004) 171-176
27. Han I.O., Kim K.W., Ryu J.H., and Kim W.K. p38 mitogen-activated protein kinase mediates lipopolysaccharide, not interferon-gamma, -induced inducible nitric oxide synthase expression in mouse BV2 microglial cells. Neurosci Lett 325 (2002) 9-12
28. Hayden S.M., and Seeds N.W. Modulated expression of plasminogen activator system components in cultured cells from dissociated mouse dorsal root ganglia. J Neurosci 16 (1996) 2307-2317
29. Herrera A.J., Castaño A., Venero J.L., Cano J., and 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 7 (2000) 429-447
30. Herrera A.J., de Pablos R.M., Carreño-Müller E., Villarán R.F., Venero J.L., Tomás-Camardiel M., et al. The intrastriatal injection of thrombin in rat induced a retrograde apoptotic degeneration of nigral dopaminergic neurons through synaptic elimination. J Neurochem 105 (2008) 750-762
31. Herrera A.J., Tomás-Camardiel M., Venrro J.L., Cano J., and Machado A. Inflammatory process as a determinant factor for the degeneration of substantia nigra dopaminergic neurons. J Neural Transm 112 (2005) 111-119
32. Hetman M., Cavanaugh J.E., Kimelman D., and Xia Z. Role of glycogen synthase kinase-3beta in neuronal apoptosis induced by trophic withdrawal. J Neurosci 20 (2000) 2567-2574
33. Kaytor M.D., and Orr H.T. The GSK3 beta signaling cascade and neurodegenerative disease. Curr Opin Neurobiol 12 (2002) 275-278
34. Kim Y.H., Park J.H., Hong S.H., and Koh J.Y. Nonproteolytic neuroprotection by human recombinant tissue plasminogen activator. Science 284 (1999) 647-650
35. Kim S.H., Won S.J., Sohn S., Kwon H.J., Lee J.Y., Park J.H., et al. Brain-derived neurotrophic factor can act as a pronecrotic factor through transcriptional and translational activation of NADPH oxidase. J Cell Biol 159 (2002) 821-831
36. Kim W.G., Mohney R.P., Wilson B., Jeohn G.H., Liu B., and Hong J.S. Regional difference in susceptibility to lipopolysaccharide-induced neuroxicity in TH rat brain: role of microglia. J Neurosci 20 (2000) 6309-6316
37. Koh J.Y., Gwag B.J., Lobner D., and Choi D.W. Potentiated necrosis of cultured cortical neurons by neurotrophins. Science 268 (1995) 573-575
38. Lee R., Kermani P., Teng K.K., and Hempstead B.L. Regulation of cell survival by secreted proneurotrophins. Science 294 (2001) 1945-1948
39. Lijnen H.R., and Collen D. t-Plasminogen activator. In: Barrett A.J., Rawlings N.D., and Woessner J.F. (Eds). Handbook of Proteolytic Enzymes (1998), Academic Press, San Diego 184-190
40. Löschmann P.A., De Groote C., Smith L., Wüllner U., Fischer G., Kemp J.A., et al. Antiparkinsonian activity of Ro 25-6981, a NR2B subunit specific NMDA receptor antagonist, in animal models of Parkinson's disease. Exp Neurol 187 (2004) 86-93
41. Martin D.L., and Rimvall K. Regulation of gamma-aminobutyric acid synthesis in the brain. J. Neurochem 60 (1993) 395-407
42. Mataga N., Nagai N., and Hensch T.K. Permissive proteolytic activity for visual cortical plasticity. Proc Natl Acad Sci USA 99 (2002) 7717-7721
43. Matute C., Alberdi E., Domercq M., Sánchez-Gómez M.V., Pérez-Samartín A., Rodríguez-Antigüedad A., et al. Excitotoxic damage to white matter. J Anat 210 (2007) 693-702
44. Medina M.G., Ledesma M.D., Domínguez J.E., Medina M., Zafra D., Alameda F., et al. Tissue plasminogen activator mediates amyloid-induced neurotoxicity via Erk1/2 activation. EMBO J 24 (2005) 1706-1716
45. Möller T., Hanisch U.K., and Ransom B.R. Thrombin-induced activation of cultured rodent microglia. J Neurochem 75 (2000) 1539-1547
46. Moriyoshi K., Masu M., Ishii T., Shigemoto R., Mizuno N., and Nakanishi S. Molecular cloning and characterization of the rat NMDA receptor. Nature 354 (1991) 31-37
47. Nagai N., De Mol M., Lijnen H.R., Carmeliet P., and Collen D. Role of plasminogen system components in focal cerebral ischemic infarction: a gene targeting and gene transfer study in mice. Circulation 99 (1999) 2440-2444
48. Nash J.E., Fox S.H., Henry B., Hill M.P., Peggs D., McGuire S., et al. Antiparkinsonian actions of ifenprodil in the MPTP-lesioned marmoset model of Parkinson's disease. Exp Neurol 165 (2000) 136-142
49. Nicole O., Docagne F., Ali C., Margaill I., Carmeliet P., MacKenzie E.T., et al. The proteolytic activity of tissue-plasminogen activator enhances NMDA receptor-mediated signaling. Nat Med 7 (2001) 59-64
50. NINDS and rt-PA Stroke Study Group. Tissue plasminogen activator for acute ischemic stroke. N Engl J Med 333 (1995) 1581-1587
51. Pang P.T., Teng H.K., Zaitsev E., Woo N.T., Sakata K., Zhen S., et al. Cleavage of proBDNF by tPA/plasmin is essential for long-term hippocampal plasticity. Science 306 (2004) 487-491
52. Pap M., and Cooper G.M. Role of glycogen synthase kinase-3 in the phosphatidylinositol 3-kinase/Akt cell survival pathway. J Biol Chem 273 (1998) 19929-19932
53. Park C., Lee S., Cho I.H., Lee H.K., Kim D., Choi S.Y., et al. TLR3-mediated signal induces proinflammatory cytokine and chemokine gene expression in astrocytes: differential signaling mechanisms of TLR3-induced IP-10 and IL-8 gene expression. Glia 53 (2006) 248-256
54. Pasinetti G.M., Lerner S.P., Johnson S.A., Morgan D.G., Telford N.A., and Finch C.E. Chronic lesions differentially decrease tyrosine hydroxylase messenger RNA in dopaminergic neurons of the substantia nigra. Brain Res 5 (1989) 203-209
55. Paxinos G., and Watson C. The Rat Brain in Stereotaxic Coordinates. 2nd ed. (1986), Academic Press, San Diego
56. Polavarapu R., Gongora M.C., Yi H., Ranganthan S., Lawrence D.A., Strickland D., et al. Tissue-type plasminogen activator-mediated shedding of astrocytic low-density lipoprotein receptor-related protein increases the permeability of the neurovascular unit. Blood 109 (2007) 3270-3278
57. Pyo H., Jou I., Jung S., Hong S., and Joe E.H. Mitogen-activated protein kinases activated by lipopolysaccharide and beta-amyloid in cultured rat microglia. Neuroreport 9 (1998) 871-874
58. Qian Z., Gilbert M.E., Colicos M.A., Kandel E.R., and Kuhl D. Tissue-plasminogen activator is induced as an immediate-early gene during seizure, kindling and long-term potentiation. Nature 361 (1993) 453-457
59. Rite I., Machado A., Cano J., and Venero J.L. Blood-brain barrier disruption induces in vivo degeneration of nigral dopaminergic neurons. J Neurochem 101 (2007) 1567-1582
60. Ryu J.K., Shin W.H., Kim J., Joe E.H., Lee Y.B., Cho K.G., et al. Trisialoganglioside GT1b induces in vivo degeneration of nigral dopaminergic neurons: role of microglia. Glia 38 (2002) 15-23
61. Samdani A.F., Newcamp C., Resink A., Facchinetti F., Hoffman B.E., Dawson V.L., et al. Differential susceptibility to neurotoxicity mediated by neurotrophins and neuronal nitric oxide synthase. J Neurosci 17 (1997) 4633-4641
62. Saporito M.S., Thomas B.A., and Scott R.W. MPTP activates c-Jun NH(2)-terminal kinase (JNK) and its upstream regulatory kinase MKK4 in nigrostriatal neurons in vivo. J Neurochem 75 (2000) 1200-1208
63. Sawada M., Imamura K., and Nagatsu T. Role of cytokines in inflammatory process in Parkinson's disease. J Neural Transm Suppl 70 (2006) 373-381
64. Scarisbrick I.A., Isackson P.J., Ciric B., Windebank A.J., and Rodriguez M. MSP, a trypsin-like serine protease, is abundantly expressed in the human nervous system. J Comp Neurol 431 (2001) 347-361
65. Seeds N.W., Williams B.L., and Bickford P.C. Tissue plasminogen activator induction in Purkinje neurons after cerebellar motor learning. Science 270 (1995) 1992-1994
66. Siao C.J., and Tsirka S.E. Tissue plasminogen activator mediates microglial activation via its finger domain through annexin II. J Neurosci 22 (2002) 3352-3358
67. Sternberger N.H., and Sternberger L.A. Blood-brain barrier protein recognized by monoclonal antibody. Proc Natl Acad Sci USA 84 (1987) 8169-8173
68. Stone S.R., and le Bonniec B.F. Thrombin. In: Barrett A.J., Rawlings N.D., and Woessner J.F. (Eds). Handbook of Proteolytic Enzymes (1998), Academic Press, San Diego 168-174
69. Tapia-Arancibia L., Rage F., Givalois L., and Arancibia S. Physiology of BDNF: focus on hypothalamic function. Front Neuroendocrinol 25 (2004) 77-107
70. Tomás-Camardiel M., Herrera Aj, Venero J.L., Cano J., and Machado A. Inflammatory process as a determinat factor for the degeneration of Substantia nigra dopaminergic neurons: possible relevance to the etiology of Parkinson's disease. Curr Med Chem-CNS Agents 4 (2004) 223-233
71. Tomás-Camardiel M., Rite I., Herrera A.J., de Pablos R.M., Cano J., Machado A., et al. Minocycline reduces the lipopolysaccharide-induced inflammatory reaction, peroxynitrite-mediated nitration of proteins, disruption of the blood-brain barrier, and damage in the nigral dopaminergic system. Neurobiol Dis 16 (2004) 190-201
72. Tomás-Camardiel M., Venero J.L., Herrera A.J., de Pablos R.M., Pintor-Toro J.A., Machado A., et al. Blood-brain barrier disruption highly induces aquaporin-4 mRNA and protein in perivascular and parenchymal astrocytes: protective effect by estradiol treatment in ovariectomized animals. J Neurosci Res 80 (2005) 235-246
73. Tsai S.-J. Statins may enhance the proteolytic cleavage of proBDNF: implications for the treatment of depression. Med Hypotheses 68 (2007) 1296-1299
74. Tsirka S., Rogove A., Bugge T., Degen J., and Strickland S. An extracellular proteolytic cascade promotes neuronal degeneration in the mouse hippocampus. J Neurosci 17 (1997) 543-552
75. Venero J.L., Machado A., and Cano J. Importance of aquaporins in the physiopathology of brain edema. Curr Pharm Des 10 (2004) 2153-2161
76. Vizuete M.L., Merino M., Venero J.L., Santiago M., Cano J., and Machado A. Histamine infusion induces a selective dopaminergic neuronal death along with an inflammatory reaction in rat substantia nigra. J Neurochem 75 (2000) 540-552
77. Waetzig V., Czeloth K., Hidding U., Mielke K., Kanzow M., Brecht S., et al. c-Jun N-terminal kinases (JNKs) mediate pro-inflammatory actions of microglia. Glia 50 (2005) 235-246
78. Walton K.M., DiRocco R., Bartlett B.A., Koury E., Marcy V.R., Jarvis B., et al. Activation of p38MAPK in microglia after ischemia. J Neurochem 70 (1998) 1764-1767
79. Wang Y.F., Tsirka S.E., Strickland S., Stieg P.E., Soriano S.G., and Lipton S.A. Tissue plasminogen activator (tPA) increases neuronal damage after focal cerebral ischemia in wild-type and tPA-deficient mice. Nat Med 4 (1998) 228-231
80. Wedzony K., Czepiel K., and Fijał K. Immunohistochemical evidence for localization of NMDAR1 receptor subunit on dopaminergic neurons of the rat substantia nigra, pars compacta. Pol J Pharmacol 53 (2001) 675-679
81. Weiss S., Tzavara E.T., Davis R.J., Nomikos G.G., Michael McIntosh J., Giros B., et al. Functional alterations of nicotinic neurotransmission in dopamine transporter knock-out mice. Neuropharmacology 52 (2007) 1496-1508
82. Wessell R.H., Ahmed S.M., Menniti F.S., Dunbar G.L., Chase T.N., and Oh J.D. NR2B selective NMDA receptor antagonist CP-101,606 prevents levodopa-induced motor response alterations in hemi-parkinsonian rats. Neuropharmacology 47 (2004) 184-194
83. Xie Z., Smith C.J., and Van Eldik L.J. Activated glia induce neuron death via MAP kinase signaling pathways involving JNK and p38. Glia 45 (2004) 170-179
84. Yatsushige H., Calvert J.W., Cahill J., and Zhang J.H. Limited role of inducible nitric oxide synthase in blood-brain barrier function after experimental subarachnoid hemorrhage. J Neurotrauma 23 (2006) 1874-1882
85. Yepes M., Sandkvist M., Wong M.K., Coleman T.A., Smith E., Cohan S.L., et al. Neuroserpin reduces cerebral infarct volume and protects neurons from ischemia-induced apoptosis. Blood 96 (2000) 569-576
86. Yepes M., Sandkvist M., Coleman T.A., Moore E., Wu J.Y., Mitola D., et al. Regulation of seizure spreading by neuroserpin and tissue-type plasminogen activator is plasminogen-independent. J Clin Invest 109 (2002) 1571-1578
87. Yepes M., Sandkvist M., Moore E.G., Bugge T.H., Strickland D.K., and Lawrence D.A. Tissue-type plasminogen activator induces opening of the blood-brain barrier via the LDL receptor-related protein. J Clin Invest 112 (2003) 1533-1540