Neurturin protects against 6-hydroxydopamine-induced reductions in evoked dopamine overflow in rat striatum

Neurochemistry International

Volumn 57, Issue 5, 2010, Pages 540-546

  Cass, Wayne A ^a   Peters, Laura E ^a  

^a UNIVERSITY OF KENTUCKY   (United States)

Author keywords

6 OHDA; Dopamine; GDNF; Microdialysis; Neurturin; Striatum; Substantia Nigra

Indexed keywords

3,4 DIHYDROXYPHENYLACETIC ACID; AMPHETAMINE; DOPAMINE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; HOMOVANILLIC ACID; NEURTURIN; OXIDOPAMINE; POTASSIUM;

ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DIALYSATE LEVEL; DOPAMINE BRAIN LEVEL; DOPAMINE RELEASE; MALE; MICRODIALYSIS; NEUROPROTECTION; NONHUMAN; PRIORITY JOURNAL; RAT; SINGLE DRUG DOSE; SUBSTANTIA NIGRA;

3,4-DIHYDROXYPHENYLACETIC ACID; AMPHETAMINE; ANIMALS; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; CORPUS STRIATUM; DOPAMINE; DOPAMINE UPTAKE INHIBITORS; FUNCTIONAL LATERALITY; GLIAL CELL LINE-DERIVED NEUROTROPHIC FACTOR; HOMOVANILLIC ACID; MALE; MICRODIALYSIS; NERVE GROWTH FACTORS; NEUROPROTECTIVE AGENTS; NEURTURIN; OXIDOPAMINE; POTASSIUM CHLORIDE; RATS; RATS, INBRED F344; SUBSTANTIA NIGRA; SYMPATHOLYTICS;

ANIMALIA; RATTUS;

EID: 77956227043     PISSN: 01970186     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.neuint.2010.06.019     Document Type: Article

References (62)

1. Airaksinen M.S., Saarma M. The GDNF family: signaling, biological functions and therapeutic value. Nat. Rev. Neurosci. 2002, 3:383-394.
2. 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. 1999, 73:70-78.
3. Andersson D.R., Nissbrandt H., Bergquist F. Partial depletion of dopamine in substantia nigra impairs motor performance without altering striatal dopamine neurotransmission. Eur. J. Neurosci. 2006, 24:617-624.
4. Aoi M., Date I., Tomita S., Ohmoto T. Single administration of GDNF into the striatum induced protection and repair of the nigrostriatal dopaminergic system in the intrastriatal 6-hydroxydopamine injection model of hemiparkinsonism. Restor. Neurol. Neurosci. 2000, 17:31-38.
5. Baloh R.H., Enomoto H., Johnson E.M., Milbrandt J. The GDNF family ligands and receptors - implications for neural development. Curr. Opin. Neurobiol. 2000, 10:103-110.
6. Bjorklund A., Kirik D., Rosenblad C., Georgievska B., Lundberg C., Mandel R.J. Towards a neuroprotective gene therapy for Parkinson's disease: use of adenovirus, AAV and lentivirus vectors for gene transfer of GDNF to the nigrostriatal system in the rat Parkinson model. Brain Res. 2000, 886:82-98.
7. Bourque M.-J., Trudeau L.-E. GDNF enhances the synaptic efficacy of dopaminergic neurons in culture. Eur. J. Neurosci. 2000, 12:3172-3180.
8. Burazin T.C.D., Gundlach A.L. Localization of GDNF /neurturin receptor (c-ret, GFRα-1 and α-2) mRNAs in postnatal rat brain: differential regional and temporal expression in hippocampus, cortex and cerebellum. Mol. Brain Res. 1999, 73:151-171.
9. Cass W.A. GDNF selectively protects dopamine neurons over serotonin neurons against the neurotoxic effects of methamphetamine. J. Neurosci. 1996, 16:8132-8139.
10. Cass W.A., Manning M.W. GDNF protection against 6-OHDA-induced reductions in potassium-evoked overflow of striatal dopamine. J. Neurosci. 1999, 19:1416-1423.
11. Cass W.A., Peters L.E. Neurturin effects on nigrostriatal dopamine release and content: comparison with GDNF. Neurochem. Res. 2010, 35:727-734.
12. Cass W.A., Kearns C.M., Gash D.M. Protective and regenerative properties of GDNF in the central nervous system. Neuroprotective Signal Transduction 1998, 145-161. Humana Press, Totowa, NJ. M.P. Mattson (Ed.).
13. Cass W.A., Harned M.E., Peters L.E., Nath A., Maragos W.F. HIV-1 protein Tat potentiation of methamphetamine-induced decreases in evoked overflow of dopamine in the striatum of the rat. Brain Res. 2003, 984:133-142.
14. Cass W.A., Peters L.E., Smith M.P. Neuroprotective effects of a single injection of GDNF in a rat model of early Parkinson's disease. Exp. Neurol. 2004, 187:205.
15. Fjord-Larsen L., Johansen J.L., Kusk P., Tornoe J., Gronborg M., Rosenblad C., Wahlberg L.U. Efficient in vivo protection of nigral dopaminergic neurons by lentiviral gene transfer of a modified neurturin construct. Exp. Neurol. 2005, 195:49-60.
16. Gash D.M., Zhang Z., Gerhardt G.A. Neuroprotective and neurorestorative properties of GDNF. Ann. Neurol. 1998, 44(Suppl. 1):S121-S125.
17. Gasmi M., Brandon E.P., Herzog C.D., Wilson A., Bishop K.M., Hofer E.K., Cunningham J.J., Printz M.A., Kordower J.H., Bartus R.T. AAV2-mediated delivery of human neurturin to the rat nigrostriatal system: long-term efficacy and tolerability of CERE-120 for Parkinson's disease. Neurobiol. Dis. 2007, 27:67-76.
18. Gasmi M., Herzog C.D., Brandon E.P., Cunningham J.J., Ramirez G.A., Ketchum E.T., Bartus R.T. Striatal delivery of neurturin by CERE-120, an AAV2 vector for the treatment of dopaminergic neuron degeneration in Parkinson's disease. Mol. Ther. 2007, 15:62-68.
19. Gerhardt G.A., Cass W.A., Yi A., Zhang Z., Gash D.M. Changes in somatodendritic but not terminal dopamine regulation in aged rhesus monkeys. J. Neurochem. 2002, 80:168-177.
20. Gerin C. Behavioral improvement and dopamine release in a parkinsonian rat model. Neurosci. Lett. 2002, 330:5-8.
21. Gill S.S., Patel N.K., Hotton G.R., O'Sullivan K., McCarter R., Bunnage M., Brooks D.J., Svendsen C.N., Heywood P. Direct brain infusion of glial cell line-derived neurotrophic factor in Parkinson disease. Nat. Med. 2003, 9:589-595.
22. Glick S.D., Dong N., Keller R.W., Carlson J.N. Estimating extracellular concentrations of dopamine and 3,4-dihydroxyphenylacetic acid in nucleus accumbens and striatum using microdialysis: relationships between in vitro and in vivo recoveries. J. Neurochem. 1994, 62:2017-2021.
23. Golden J.P., Baloh R.H., Kotzbauer P.T., Lampe P.A., Osborne P.A., Milbrandt J., Johnson E.M. Expression of neurturin, GDNF, and their receptors in the adult mouse CNS. J. Comp. Neurol. 1998, 398:139-150.
24. Grondin R., Zhang Z., Yi A., Cass W.A., Maswood N., Andersen A.H., Elsberry D.D., Klein M.C., Gerhardt G.A., Gash D.M. Chronic, controlled GDNF infusion promotes structural and functional recovery in advanced parkinsonian monkeys. Brain 2002, 2191-2201.
25. Grondin R., Zhang Z., Ai Y., Ding F., Walton A.A., Surgener S.P., Gerhardt G.A., Gash D.M. Intraputamenal infusion of exogenous neurturin protein restores motor and dopaminergic function in the globus pallidus of MPTP-lesioned rhesus monkeys. Cell Transplant. 2008, 17:373-381.
26. Hadaczek P., Johnston L., Forsayeth J., Bankiewicz K.S. Pharmacokinetics and bioactivity of glial cell line-derived factor (GDNF) and neurturin (NTN) infused into the rat brain. Neuropharmacology 2010, 58:1114-1121.
27. Hamilton J.F., Morrison P.F., Chen M.Y., Harvey-White J., Pernaute R.S., Phillips H., Oldfield E., Bankiewicz K.S. Heparin coinfusion during convection-enhanced delivery (CED) increases the distribution of the glial-derived neurotrophic factor (GDNF) ligand family in rat striatum and enhances the pharmacological activity of neurturin. Exp. Neurol. 2001, 168:155-161.
28. Hebert M.A., Van Horne C.G., Hoffer B.J., Gerhardt G.A. Functional effects of GDNF in normal rat striatum: presynaptic studies using in vivo electrochemistry and microdialysis. J. Pharmacol. Exp. Ther. 1996, 279:1181-1190.
29. Herzog C.D., Dass B., Holden J.E., Stansell J., Gasmi M., Tuszynski M.H., Bartus R.T., Kordower J.H. Striatal delivery of CERE-120, an AAV2 vector encoding human neurturin, enhances activity of the dopaminergic nigrostriatal system in aged monkeys. Mov. Disord. 2007, 22:1124-1132.
30. Hoane M.R., Gulwadi A.G., Morrison S., Hovanesian G., Lindner M.D., Tao W. Differential in vivo effects of neurturin and glial cell-line-derived neurotrophic factor. Exp. Neurol. 1999, 160:235-243.
31. Hoffman A.F., Van Horne C.G., Eken S., Hoffer B.J., Gerhardt G.A. In vivo microdialysis studies of somatodendritic dopamine release in the rat substantia nigra: effects of unilateral 6-OHDA lesions and GDNF. Exp. Neurol. 1997, 147:130-141.
32. Horger B.A., Nishimura M.C., Armanini M.P., Wang L.-C., Poulsen K.T., Rosenblad C., Kirik D., Moffat B., Simmons L., Johnson E., Milbrandt J., Rosenthal A., Bjorklund A., Vandlen R.A., Hynes M.A., Phillips H.S. Neurturin exerts potent actions on survival and function of midbrain dopaminergic neurons. J. Neurosci. 1998, 18:4929-4937.
33. Hudson J., Granholm A.-C., Gerhardt G.A., Henry M.A., Hoffman A., Biddle P., Leela N.S., Mackerlova L., Lile J.D., Collins F., Hoffer B.J. Glial cell line-derived neurotrophic factor augments midbrain dopaminergic circuits in vivo. Brain Res. Bull. 1995, 36:425-432.
34. Jenkins R., O'Shea R., Thomas K.L., Hunt S.P. c-jun expression in substantia nigra neurons following striatal 6-hydroxydopamine lesions in the rat. Neuroscience 1993, 53:447-455.
35. Kirik D., Rosenblad C., Bjorklund A. Characterization of behavioral and neurodegenerative changes following partial lesions of the nigrostriatal dopamine system induced by intrastriatal 6-hydroxydopamine in the rat. Exp. Neurol. 1998, 152:259-277.
36. Kobayashi S., Ogren S.O., Hoffer B.J., Olson L. Dopamine D1 and D2 receptor-mediated acute and long-lasting behavioral effects of glial cell line-derived neurotrophic factor administered into the striatum. Exp. Neurol. 1998, 154:302-314.
37. Kordower J.H., Emborg M.E., Bloch J., Ma S.Y., Chu Y., Leventhal L., McBride J., Chen E.-Y., Palfi S., Roitberg B.Z., Brown W.D., Holden J.E., Pyzalski R., Taylor M.D., Carvey P., Ling Z., Trono D., Hantraye P., Deglon N., Aebisher P. Neurodegeneration prevented by lentiviral vector delivery of GDNF in primate models of Parkinson's disease. Science 2000, 290:767-773.
38. Kordower J.H., Herzog C.D., Dass B., Bakay R.A.E., Stansell J., Gasmi M., Bartus R.T. Delivery of neurturin by AAV2 (CERE-120)-mediated gene transfer provides structural and functional neuroprotection and neurorestoration in MPTP-treated monkeys. Ann. Neurol. 2006, 60:706-715.
39. Kotzbauer P.T., Lampe P.A., Heuckeroth R.O., Golden J.P., Creedon D.J., Johnson E.M., Milbrandt J. Neurturin, a relative of glial-cell-line-derived neurotrophic factor. Nature 1996, 384:467-470.
40. Kozlowski D.A., Miljan E.A., Bremer E.G., Harrod C.G., Gerin C., Connor B., George D., Larson B., Bohn M.C. Quantitative analysis of GFRα-1 and GFRα-2 mRNAs and tyrosine hydroxylase protein in the nigrostriatal system reveal bilateral compensatory changes following unilateral 6-OHDA lesions in the rat. Brain Res. 2004, 1016:170-181.
41. Lang A.E., Gill S., Patel N.K., Lozano A., Nutt J.G., Penn R., Brooks D.J., Hotton G., Moro E., Heywood P., Brodsky M.A., Burchiel K., Kelly P., Dalvi A., Scott B., Stacy M., Turner D., Wooten V.G.F., Elias W.J., Laws E.R., Dhawan V., Stoessl A.J., Matcham J., Coffey R.J., Traub M. Randomized controlled trial of intraputamenal glial cell line-derived neurotrophic factor infusion in Parkinson disease. Ann. Neurol. 2006, 59:459-466.
42. Lin L.-F.H., Doherty D.H., Lile J.D., Bektesh S., Collins F. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 1993, 260:1130-1132.
43. Martin D., Miller G., Cullen T., Fischer N., Dix D., Russell D. Intranigral or intrastriatal injections of GDNF: effects on monoamine levels and behavior in rats. Eur. J. Pharmacol. 1996, 317:247-256.
44. Mladenovic A., Perovic M., Raicevic N., Kanazir S., Rakic L., Ruzdijic S. 6-Hydroxydopamine increases the level of TNFα and bax mRNA in the striatum and induces apoptosis of dopaminergic neurons in hemiparkinsonian rats. Brain Res. 2004, 996:237-245.
45. Oiwa Y., Yoshimura R., Nakai K., Itakura T. Dopaminergic neuroprotection and regeneration by neurturin assessed by using behavioral, biochemical and histochemical measurements in a model of progressive Parkinson's disease. Brain Res. 2002, 947:271-283.
46. Opacka-Juffry J., Ashworth S., Hume S.P., Martin D., Brooks D.J., Blunt S.B. GDNF protects against 6-OHDA nigrostriatal lesion: in vivo study with microdialysis and PET. NeuroReport 1995, 7:348-352.
47. Pothos E.N., Davila V., Sulzer D. Presynaptic recording of quanta from midbrain dopamine neurons and modulation of the quantal size. J. Neurosci. 1998, 18:4106-4118.
48. Robertson G.S., Robertson H.A. Evidence that l-dopa-induced rotational behavior is dependent on both striatal and nigral mechanisms. J. Neurosci. 1989, 9:3326-3331.
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. 1999, 11:1554-1566.
50. Rosenblad C., Georgievska B., Kirik D. Long-term striatal overexpression of GDNF selectively downregulates tyrosine hydroxylase in the intact nigrostriatal dopamine system. Eur. J. Neurosci. 2003, 17:260-270.
51. Salvatore M.F., Zhang J.-L., Large D.M., Wilson P.E., Gash C.R., Thomas T.C., Haycock J.W., Bing G., Stanford J.A., Gash D.M., Gerhardt G.A. Striatal GDNF administration increases tyrosine hydroxylase phosphorylation in the rat striatum and substantia nigra. J. Neurochem. 2004, 90:245-254.
52. Salvatore M.F., Gerhardt G.A., Dayton R.D., Klien R.L., Stanford J.A. Bilateral effects of unilateral GDNF administration on dopamine- and GABA-regulating proteins in the rat nigrostriatal system. Exp. Neurol. 2009, 219:197-207.
53. Salvatore M.F., Pruett B.S., Spann S.L., Dempsey C. Aging reveals a role for nigral tyrosine hydroxylase ser31 phosphorylation in locomotor activity generation. PLoS One 2009, 4:e8466.
54. 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 1994, 59:401-415.
55. Slevin J.T., Gerhardt G.A., Smith C.D., Gash D.M., Kryscio R., Young B. Improvement of bilateral motor functions in patients with Parkinson disease through the unilateral intraputaminal infusion of glial cell line-derived neurotrophic factor. J. Neurosurg. 2005, 102:216-222.
56. Smith M.P., Cass W.A. Oxidative stress and dopamine depletion in an intrastriatal 6-hydroxydopamine model of Parkinson's disease. Neuroscience 2007, 144:1057-1066.
57. Smith A.D., Kozlowski D.A., Bohn M.C., Zigmond M.J. Effect of AdGDNF on dopaminergic neurotransmission in the striatum of 6-OHDA-treated rats. Exp. Neurol. 2005, 193:420-426.
58. Tomac A., Lindqvist E., Lin L.-F.H., Ogren S.O., Young D., Hoffer B.J., Olson L. Protection and repair of the nigrostriatal dopaminergic system by GDNF in vivo. Nature 1995, 373:335-339.
59. Trevitt J.T., Carlson B.B., Nowend K., Salamone J.D. Substantia nigra pars reticulata is a highly potent site of action for the behavioral effects of the D1 antagonist SCH 23390 in the rat. Psychopharmacology 2001, 156:32-41.
60. Tseng J.L., Baetge E.E., Zurn A.D., Aebischer P. GDNF reduces drug-induced rotation behavior after medial forebrain bundle transection by a mechanism not involving striatal dopamine. J. Neurosci. 1997, 17:325-333.
61. Tseng J.L., Bruhn S.L., Zurn A.D., Aebischer P. Neurturin protects dopaminergic neurons following medial forebrain bundle axotomy. NeuroReport 1998, 9:1817-1822.
62. Widenfalk J., Nosrat C., Tomac A., Westphal H., Hoffer B., Olson L. Neurturin and glial cell line-derived neurotrophic factor receptor-ß (GDNFR-ß), novel proteins related to GDNF and GDNFR-α with specific cellular patterns of expression suggesting roles in the developing and adult nervous system and in peripheral organs. J. Neurosci. 1997, 17:8506-8519.