Effect of 6-hydroxydopamine on striatal GDNF and nigral GFRα1 and RET mRNAs in the adult rat

Molecular Brain Research

Volumn 117, Issue 2, 2003, Pages 129-138

  Smith, Amanda D ^a   Antion, Marci ^a   Zigmond, Michael J ^a   Austin, Mark C ^a  

^a UNIVERSITY OF PITTSBURGH SCHOOL OF MEDICINE   (United States)

Author keywords

Degenerative disease: Parkinson's; Disorders of the nervous system; Glial cell line derived neurotrophic factor; Neuroprotection; Parkinson's disease

Indexed keywords

BIOLOGICAL MARKER; DOPAMINE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR RECEPTOR ALPHA 1; MESSENGER RNA; OXIDOPAMINE; PROTEIN RET; RECEPTOR PROTEIN; RECEPTOR SUBUNIT; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINE BRAIN LEVEL; DOPAMINERGIC NERVE CELL; ENZYME ACTIVITY; IMMUNOCYTOCHEMISTRY; IMMUNOREACTIVITY; IN SITU HYBRIDIZATION; MALE; NERVE CELL LESION; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DETERMINATION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; RADIOIMMUNOASSAY; RAT; REDUCTION; SUBSTANTIA NIGRA; VENTRAL TEGMENTUM;

ANIMALS; AUTORADIOGRAPHY; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CORPUS STRIATUM; DROSOPHILA PROTEINS; FUNCTIONAL LATERALITY; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; IMAGING, THREE-DIMENSIONAL; IMMUNOHISTOCHEMISTRY; IN SITU HYBRIDIZATION; MALE; MEDIAL FOREBRAIN BUNDLE; NERVE GROWTH FACTORS; OXIDOPAMINE; PROTO-ONCOGENE PROTEINS C-RET; RADIOIMMUNOASSAY; RATS; RATS, SPRAGUE-DAWLEY; RECEPTOR PROTEIN-TYROSINE KINASES; RECEPTORS, GROWTH FACTOR; RNA, MESSENGER; SUBSTANTIA NIGRA; SYMPATHOLYTICS; TIME FACTORS; TYROSINE 3-MONOOXYGENASE; VENTRAL TEGMENTAL AREA;

ANIMALIA;

EID: 1642325875     PISSN: 0169328X     EISSN: None     Source Type: Journal    
DOI: 10.1016/S0169-328X(03)00289-4     Document Type: Article

References (66)

1. Akerud P., Alberch J., Eketjall S., Wagner J., Arenas E. Differential effects of glial cell line-derived neurotrophic factor and neurturin on developing and adult substantia nigra dopaminergic neurons. J. Neurochem. 73:1999;70-78.
2. Altar C.A., Cai N., Bliven T., Juhasz M., Conner J.M., Acheson A.L., Lindsay R.M., Wiegand S.J. Anterograde transport of brain-derived neurotrophic factor and its role in the brain. Nature. 389:1997;856-860.
3. Araujo D.M., Hilt D.C., Miller P.J., Wen D., Jiao S., Lapchak P.A. ret receptor tyrosine kinase immunoreactivity is altered in glial cell line-derived neurotrophic factor-responsive neurons following lesions of the nigrostriatal and septohippocampal pathways. Neuroscience. 80:1997;9-16.
4. Austin M.C., Cottingham S.L., Paul S.M., Crawley J.N. Tyrosine hydroxylase and galanin mRNA levels in locus coeruleus neurons are increased following reserpine administration. Synapse. 6:1990;351-357.
5. Arvidsson A., Kokaia Z., Airaksinen M.S., Saarma M., Lindvall O. Stroke induces widespread changes of gene expression for glial cell line-derived neurotrophic factor family receptors in the adult rat brain. Neuroscience. 106:2001;27-41.
6. Batchelor P.E., Liberatore G.T., Porritt M.J., Donnan G.A., Howells D.W. Inhibition of brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor expression reduces dopaminergic sprouting in the injured striatum. Eur. J. Neurosci. 12:2000;3462-3468.
7. Batchelor P.E., Liberatore G.T., Wong J.Y., Porritt M.J., Frerichs F., Donnan G.A., Howells D.W. Activated macrophages and microglia induce dopaminergic sprouting in the injured striatum and express brain-derived neurotrophic factor and glial cell line-derived neurotrophic factor. J. Neurosci. 19:1999;1708-1716.
8. 3H]spiperone binding, dopamine and HVA concentrations in Parkinson's disease and supranuclear palsy. Eur. J. Pharmacol. 99:1984;167-175.
9. Bowenkamp K.E., David D., Lapchak P.L., Henry M.A., Granholm A.C., Hoffer B.J., Mahalik T.J. 6-hydroxydopamine induces the loss of the dopaminergic phenotype in substantia nigra neurons of the rat. A possible mechanism for restoration of the nigrostriatal circuit mediated by glial cell line-derived neurotrophic factor. Exp. Brain Res. 111:1996;1-7.
10. Bowenkamp K.E., Hoffman A.F., Gerhardt G.A., Henry M.A., Biddle P.T., Hoffer B.J., Granholm A.C. Glial cell line-derived neurotrophic factor supports survival of injured midbrain dopaminergic neurons. J. Comp. Neurol. 355:1995;479-489.
11. Bresjanac M., Antauer G. Reactive astrocytes of the quinolinic acid-lesioned rat striatum express GFRalpha1 as well as GDNF in vivo. Exp. Neurol. 164:2000;53-59.
12. Burke R.E., Antonelli M., Sulzer D. Glial cell line-derived neurotrophic growth factor inhibits apoptotic death of postnatal substantia nigra dopamine neurons in primary culture. J. Neurochem. 71:1998;517-525.
13. Canzian F., Ushijima T., Nagao M., Matera I., Romeo G., Ceccherini I. Genetic mapping of the RET protooncogene on rat chromosome 4. Mamm. Genome. 6:1995;433-435.
14. Chauhan N.B., Siegel G.J., Lee J.M. Depletion of glial cell line-derived neurotrophic factor in substantia nigra neurons of Parkinson's disease brain. J. Chem. Neuroanat. 21:2001;277-288.
15. Chen A.C., Eisch A.J., Sakai N., Takahashi M., Nestler E.J., Duman R.S. Regulation of GFRalpha-1 and GFRalpha-2 mRNAs in rat brain by electroconvulsive seizure. Synapse. 39:2001;42-50.
16. Choi-Lundberg D.L., Bohn M.C. Ontogeny and distribution of glial cell line-derived neurotrophic factor (GDNF) mRNA in rat. Dev. Brain Res. 85:1995;80-88.
17. Choi-Lundberg D.L., Lin Q., Chang Y.N., L Chiang Y., Hay C.M., Mohajeri H., Davidson B.L., Bohn M.C. Dopaminergic neurons protected from degeneration by GDNF gene therapy. Science. 275:1997;838-841.
18. Conner J.M., lauterborn J.C., Yan Q., Gall C.M., Varon S. Distribution of brain derived neurotrophic factor (BDNF) protein and mRNA in the normal adult rat CNS: evidence for anterograde axonal transport. J. Neurosci. 17:1997;2295-2313.
19. Eggert K., Schegel J., Oertel W., Wurz C., Krieg J.C., Velder H. Glial cell line-derived neurotrophic factor protects dopaminergic neurons from 6-hydroxydopamine toxicity in vitro. Neurosci. lett. 269:1999;178-182.
20. Grunblatt E., Mandel S., Maor G., Youdim M.B. Gene expression analysis in N-methyl-4-phenyl-1,2,3,6-tetrahydropyridine mice model of Parkinson's disease using cDNA microarray: effect of R-apomorphine. J. Neurochem. 78:2001;1-12.
21. Ho A., Gore A.C., Weickert C.S., Blum M. Glutamate regulation of GDNF gene expression in the striatum and primary striatal astrocytes. Neuroreport. 6:1995;1454-1458.
22. Hoffer B.J., Hoffman A., Bowenkamp K., Huettl P., Hudson J., Martin D., Lin L.F., Gerhardt G.A. Glial cell line-derived neurotrophic factor reverses toxin-induced injury to midbrain dopaminergic neurons in vivo. Neurosci. Lett. 182:1994;107-111.
23. Hornykiewicz O. Biochemical aspects of Parkinson's disease. Neurology. 51:1998;S2-S9.
24. Hou J.G., Lin L.F., Mytilineau C. Glial cell line-derived neurotrophic factor exerts neurotrophic effects on dopaminergic neurons in vitro and promotes their survival and regrowth after damage by 1-methyl-4- phenylpyridinium. J. Neurochem. 66:1996;74-82.
25. Humpel C., Hoffer B., Stromberg I., Bektesh S., Collins F., Olson L. Neurons of the hippocampal formation express glial cell line-derived neurotrophic factor messenger RNA in response to kainate-induced excitation. Neuroscience. 59:1994;791-795.
26. 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. Mol. Brain Res. 41:1996;14-26.
27. Hung H.C., Lee E.H. MPTP produces differential oxidative stress and antioxidative responses in the nigrostriatal and mesolimbic dopaminergic pathways. Free Radic. Biol. Med. 24:1998;76-84.
28. Inoue T., Tsui J., Wong N., Wong S.Y., Suzuki F., Kwok Y.N. Expression of glial cell line-derived neurotrophic factor and its mRNA in the nigrostriatal pathway following MPTP treatment. Brain Res. 826:1999;306-308.
29. Jacobowitz D.M., Burns R.S., Chiueh C.C., Kopin I.J. N-methyl-4-phenyl-1, 2,3,6-tetra-hydropyridine (MPTP) causes destruction of the nigrostriatal but not the mesolimbic dopamine system in the monkey. Psychopharmacol. Bull. 20:1984;416-422.
30. Jeon B.S., Jackson-Lewis V., Burke R.E. 6-Hydroxydopamine lesion of the rat substantia nigra: time course and morphology of cell death. Neurodegeneration. 4:1995;131-137.
31. Jing S., Wen D., Yu Y., Holst P.L., Luo Y., Fang M., Tamir R., Antonio L., Hu Z., Cupples R., Louis J.C., Hu S., Altrock B.W., Fox G.M. GDNF-induced activation of the ret protein tyrosine kinase is mediated by GDNFR-alpha, a novel receptor for GDNF. Cell. 85:1996;1113-1124.
32. Kearns C.M., Gash D.M. GDNF protects nigral dopamine neurons against 6-hydroxydopamine in vivo. Brain Res. 672:1995;104-111.
33. Kitagawa H., Sasaki C., Zhang W.R., Sakai K., Shiro Y., Warita H., Mitsumoto Y., Mori T., Abe K. Induction of glial cell line-derived neurotrophic factor receptor proteins in cerebral cortex and striatum after permanent middle cerebral artery occlusion in rats. Brain Res. 834:1999;190-195.
34. Kokaia Z., Airaksinen M.S., Nanobashvili A., Larsson E., Kujamaki E., Lindvall O., Saarma M. GDNF family ligands and receptors are differentially regulated after brain insults in the rat. Eur. J. Neurosci. 11:1999;1202-1216.
35. Kokaia Z., Andsberg G., Yan Q., Lindvall O. Rapid alterations of BDNF protein levels in the rat brain after focal ischemia: evidence for increased synthesis and anterograde axonal transport. Exp. Neurol. 154:1998;289-301.
36. Kozlowski D.A., Connor B., Tillerson J.L., Schallert T., Bohn M.C. Delivery of a GDNF gene into the substantia nigra after a progressive 6-OHDA lesion maintains functional nigrostriatal connections. Exp. Neurol. 166:2000;1-15.
37. Krieglstein K., Suter-Crazzolara C., Fischer W.H., Unsicker K. TGF-beta superfamily members promote survival of midbrain dopaminergic neurons and protect them against MPP+ toxicity. EMBO J. 14:1995;736-742.
38. Liang C.L., Sinton C.M., Sonsalla P.K., German D.C. Midbrain dopaminergic neurons in the mouse that contain calbindin-D28k exhibit reduced vulnerability to MPTP-induced neurodegeneration. Neurodegeneration. 5:1996;313-318.
39. Liberatore G.T., Wong J.Y., Porritt M.J., Donnan G.A., Howells D.W. Expression of glial cell line-derived neurotrophic factor (GDNF) mRNA following mechanical injury to mouse striatum. Neuroreport. 8:1997;3097-3101.
40. Liu Y., Peter D., Roghani A., Schuldiner S., Prive G.G., Eisenberg D., Brecha N., Edwards R.H. A cDNA that suppresses MPP+ toxicity encodes a vesicular amine transporter. Cell. 70:1992;539-551.
41. Liu Y., Schweitzer E.S., Nirenberg M.J., Pickel V.M., Evans C.J., Edwards R.H. Preferential localization of a vesicular monoamine transporter to dense core vesicles in PC12 cells. J. Cell Biol. 127:1994;1419-1433.
42. Ma D., Wang X., Han J. NIH 3T3 cells or engineered NIH 3T3 cells stably expressing GDNF can protect primary dopaminergic neurons. Neurol. Res. 22:2000;538-544.
43. Marco S., Saura J., Perez-Navarro E., Jose Marti M., Tolosa E., Alberch J. Regulation of c-Ret, GFRalpha1, and GFRalpha2 in the substantia nigra pars compacta in a rat model of Parkinson's disease. J. Neurobiol. 52:2002;343-351.
44. Melamed E., Rosenthal J., Globus M., Cohen O., Frucht Y., Uzzan A. Mesolimbic dopaminergic neurons are not spared by MPTP neurotoxicity in mice. Eur. J. Pharmacol. 114:1985;97-100.
45. Nirenberg M.J., Chan J., Liu Y., Edwards R.H., Pickel V.M. Ultrastructural localization of the vesicular monoamine transporter-2 in midbrain dopaminergic neurons: potential sites for somatodendritic storage and release of dopamine. J. Neurosci. 16:1996;4135-4145.
46. Reeben M., Laurikainen A., Hiltunen J.O., Castren E., Saarma M. The messenger RNAs for both glial cell line-derived neurotrophic factor receptors, c-ret and GDNFRalpha, are induced in the rat brain in response to kainate-induced excitation. Neuroscience. 83:1998;151-159.
47. Rind H.B., von Bartheld C.S. Anterograde axonal transport of internalized GDNF in sensory and motor neurons. Neuroreport. 13:2002;659-664.
48. Rodriguez M., Barroso-Chinea P., Abdala P., Obeso J., Gonzalez-Hernandez T. Dopamine cell degeneration induced by intraventricular administration of 6-hydroxydopamine in the rat: similarities with cell loss in parkinson's disease. Exp. Neurol. 169:2001;163-181.
49. Rosenblad C., Kirik D., Devaux B., Moffat B., Phillips H.S., Bjorklund A. Protection and regeneration of nigral dopaminergic neurons by neurturin or GDNF in a partial lesion model of Parkinson's disease after administration into the striatum or the lateral ventricle. Eur. J. Neurosci. 11:1999;1554-1566.
50. Russel F.D., Koishi K., Jiang Y., mcLennan L.S. Anterograde axonal transport of glial cell line-derived neurotrophic factor and its receptors in rat hypoglossal nerve. Neuroscience. 97:2000;575-580.
51. Sarabi A., Hoffer B.J., Olson L., Morales M. GFRalpha-1 mRNA in dopaminergic and nondopaminergic neurons in the substantia nigra and ventral tegmental area. J. Comp. Neurol. 441:2001;106-117.
52. Sauer H., Oertel W.H. Progressive degeneration of nigrostriatal dopamine neurons following intrastriatal terminal lesions with 6-hydroxydopamine: a combined retrograde tracing and immunocytochemical study in the rat. Neuroscience. 59:1994;401-415.
53. Siegel G.J., Chauhan N.B. Neurotrophic factors in Alzheimer's and Parkinson's disease brain. Brain Res. Rev. 33:2000;199-227.
54. Smith A.D., Antion M.D., Zigmond M.J., Austin M.C. Expression of GDNF, GFRα1, and RET in 6-OHDA-lesioned midbrain dopamine neurons. SFN Abstract. 2000.
55. Smith A.D., Kozlowski D.A., Bohn M.C., Zigmond M.J. Delivery of a GDNF gene into the substantia nigra 1 week after 6-OHDA enhances dopamine neurotransmission of remaining terminals in the striatum. SFN Abstract. 2001;. 198.7.
56. Staal R.G., Sonsalla P.K. Inhibition of brain vesicular monoamine transporter (VMAT2) enhances 1-methyl-4-phenylpyridinium neurotoxicity in vivo in rat striata. J. Pharmacol. Exp. Ther. 293:2000;336-342.
57. Stern-Bach Y., Keen J.N., Bejerano M., Steiner-Mordoch S., Wallach M., Findlay J.B., Schuldiner S. Homology of a vesicular amine transporter to a gene conferring resistance to 1-methyl-4-phenylpyridinium. Proc. Natl. Acad. Sci. USA. 89:1992;9730-9733.
58. Strömberg I., Bjorklund L., Johansson M., Tomac A., Collins F., Olson L., Hoffer B., Humpel C. Glial cell line-derived neurotrophic factor is expressed in the developing but not adult striatum and stimulates developing dopamine neurons in vivo. Exp. Neurol. 124:1993;401-412.
59. Takahashi N., Miner L.L., Sora I., Ujike H., Revay R.S., Kostic V., Jackson-Lewis V., Przedborski S., Uhl G.R. VMAT2 knockout mice: heterozygotes display reduced amphetamine-conditioned reward, enhanced amphetamine locomotion, and enhanced MPTP toxicity. Proc. Natl. Acad. Sci. USA. 94:1997;9938-9943.
60. Tan Y., Williams E.A., Zahm D.S. Calbindin-D 28 kDa immunofluorescence in ventral mesencephalic neurons labeled following injections of Fluoro-Gold in nucleus accumbens subterritories: inverse relationship relative to known neurotoxin vulnerabilities. Brain Res. 844:1999;67-77.
61. Tan Y., Williams E.A., Lancia A.J., Zahm D.S. On the altered expression of tyrosine hydroxylase and calbindin-D 28 kDa immunoreactivities and viability of neurons in the ventral tegmental area of Tsai following injections of 6-hydroxydopamine in the medial forebrain bundle in the rat. Brain Res. 869:2000;56-68.
62. Tang Y.P., Ma Y.L., Chao C.C., Chen K.Y., Lee E.H. Enhanced glial cell line-derived neurotrophic factor mRNA expression upon (-)-deprenyl and melatonin treatments. J. Neurosci. Res. 53:1998;593-604.
63. Trupp M., Arenas E., Fainzilber M., Nilsson A.S., Sieber B.A., Grigoriou M., Kilkenny C., Salazar-Grueso E., Pachnis V., Arumae U. Functional receptor for GDNF encoded by the c-ret proto-oncogene. Nature. 381:1996;785-789.
64. Wei G., Wu G., Cao X. Dynamic expression of glial cell line-derived neurotrophic factor after cerebral ischemia. Neuroreport. 11:2000;1177-1183.
65. Yurek D.M., Fletcher-Turner A. Differential expression of GDNF, BDNF, and NT-3 in the aging nigrostriatal system following a neurotoxic lesion. Brain Res. 891:2001;228-235.
66. Zhou J., Yu Y., Tang Z., Shen Y., Xu L. Differential expression of mRNAs of GDNF family in the striatum following 6-OHDA-induced lesion. Neuroreport. 11:2000;3289-3293.