Signalling mechanisms underlying development and maintenance of dopamine neurons

Current Opinion in Neurobiology

Volumn 18, Issue 3, 2008, Pages 297-306

  Andressoo, Jaan Olle ^a   Saarma, Mart ^a  

^a UNIVERSITY OF HELSINKI   (Finland)

Author keywords

[No Author keywords available]

Indexed keywords

BRAIN DERIVED NEUROTROPHIC FACTOR; DOPAMINE; GLIAL CELL LINE DERIVED NEUROTROPHIC FACTOR; GROWTH FACTOR; NEUROTROPHIC FACTOR; TRANSCRIPTION FACTOR;

CENTRAL NERVOUS SYSTEM; CORPUS STRIATUM; DOPAMINE BRAIN LEVEL; DOPAMINERGIC NERVE CELL; FRONTAL CORTEX; GENE DELIVERY SYSTEM; INVOLUNTARY MOVEMENT; MESENCEPHALON; MICROGLIA; MOOD; MOTIVATION; MOVEMENT (PHYSIOLOGY); MUSCLE RIGIDITY; NERVE CELL DIFFERENTIATION; NERVE FIBER; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; REVIEW; SUBSTANTIA NIGRA;

ANIMALS; BRAIN; DOPAMINE; NEURONS; SIGNAL TRANSDUCTION;

EID: 53949086721     PISSN: 09594388     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.conb.2008.07.005     Document Type: Review

References (54)

1. Smidt M.P., and Burbach J.P. How to make a mesodiencephalic dopaminergic neuron. Nat Rev Neurosci 8 (2007) 21-32
2. Smits S.M., Burbach J.P., and Smidt M.P. Developmental origin and fate of meso-diencephalic dopamine neurons. Prog Neurobiol 78 (2006) 1-16
3. Pasterkamp R.J., and Kolodkin A.L. Semaphorin junction: making tracks toward neural connectivity. Curr Opin Neurobiol 13 (2003) 79-89
4. Huber A.B., Kolodkin A.L., Ginty D.D., and Cloutier J.F. Signaling at the growth cone: ligand-receptor complexes and the control of axon growth and guidance. Annu Rev Neurosci 26 (2003) 509-563
5. Holt C.E., and Dickson B.J. Sugar codes for axons?. Neuron 46 (2005) 169-172
6. Lin L.F., Doherty D.H., Lile J.D., Bektesh S., and Collins F. GDNF: a glial cell line-derived neurotrophic factor for midbrain dopaminergic neurons. Science 260 (1993) 1130-1132
7. Oo T.F., Kholodilov N., and Burke R.E. Regulation of natural cell death in dopaminergic neurons of the substantia nigra by striatal glial cell line-derived neurotrophic factor in vivo. J Neurosci 23 (2003) 5141-5148
8. Bespalov M.M., and Saarma M. GDNF family receptor complexes are emerging drug targets. Trends Pharmacol Sci 28 (2007) 68-74
9. Lindholm P., Voutilainen M.H., Lauren J., Peranen J., Leppanen V.M., Andressoo J.O., Lindahl M., Janhunen S., Kalkkinen N., Timmusk T., et al. Novel neurotrophic factor CDNF protects and rescues midbrain dopamine neurons in vivo. Nature 448 (2007) 73-77. The study describes the discovery of the novel conserved dopamine neurotrophic factor CDNF which effectively protects and repairs the dopamine neurons in the rat 6-OHDA model of PD at least as effectively as GDNF, a known protein which has reached clinical trials. Unlike GDNF, CDNF has no effect on peripheral neurons in vitro, raising hopes that CDNF may have fewer side effects than GDNF.
10. Burke R.E. GDNF as a candidate striatal target-derived neurotrophic factor for the development of substantia nigra dopamine neurons. J Neural Transm Suppl (2006) 41-45
11. Krieglstein K. Factors promoting survival of mesencephalic dopaminergic neurons. Cell Tissue Res 318 (2004) 73-80
12. Granholm A.C., Reyland M., Albeck D., Sanders L., Gerhardt G., Hoernig G., Shen L., Westphal H., and Hoffer B. Glial cell line-derived neurotrophic factor is essential for postnatal survival of midbrain dopamine neurons. J Neurosci 20 (2000) 3182-3190
13. Jain S., Golden J.P., Wozniak D., Pehek E., Johnson Jr. E.M., and Milbrandt J. RET is dispensable for maintenance of midbrain dopaminergic neurons in adult mice. J Neurosci 26 (2006) 11230-11238
14. Kramer E.R., Aron L., Ramakers G.M., Seitz S., Zhuang X., Beyer K., Smidt M.P., and Klein R. Absence of Ret signaling in mice causes progressive and late degeneration of the nigrostriatal system. PLoS Biol 5 (2007) e39. An excellent effort where researchers provide first in vivo evidence that the lack of trophic support mediated by GDNF receptor RET but not BDNF receptor TrkB specifically in dopamineric neurons result in age-associated dopaminergic loss and microglial activation. This result rise hopes that conversely, stimulation with GDNF may result in an increased and long-lasting protection in vivo.
15. Mijatovic J., Airavaara M., Planken A., Auvinen P., Raasmaja A., Piepponen T.P., Costantini F., Ahtee L., and Saarma M. Constitutive Ret activity in knockin multiple endocrine neoplasia type B mice induces profound elevation of brain dopamine concentration via enhanced synthesis and increases the number of TH-positive cells in the substantia nigra. J Neurosci 27 (2007) 4799-4809
16. Airaksinen M.S., and Saarma M. The GDNF family: signalling, biological functions and therapeutic value. Nat Rev Neurosci 3 (2002) 383-394
17. Pascual A., Hidalgo-Figueroa M., Piruat J.I., Pintado C.O., Gomez-Diaz R., and Lopez-Barneo J. Absolute requirement of GDNF for adult catecholaminergic neuron survival. Nat Neurosci 7 (2008) 755-761. An exciting study, where GDNF protein levels were decreased 40-60% in postnatal mice using Cre-Lox and tamoxifen-inducible Cre recombination system. They show pronounced decrease of DA neuronal numbers in SNpc, VTA and almost complete loss of DA neurons in locus coeruleus. These data significantly differ from those obtained with GDNF heterozygous mice or by deleting RET from DA neurons, suggesting that the levels and timing of GDNF expression are critically important.
18. Takagi Y., Takahashi J., Saiki H., Morizane A., Hayashi T., Kishi Y., Fukuda H., Okamoto Y., Koyanagi M., Ideguchi M., et al. Dopaminergic neurons generated from monkey embryonic stem cells function in a Parkinson primate model. J Clin Invest 115 (2005) 102-109
19. Lindvall O., and Kokaia Z. Stem cells for the treatment of neurological disorders. Nature 441 (2006) 1094-1096
20. Dodson M.W., and Guo M. Pink1, Parkin, DJ-1 and mitochondrial dysfunction in Parkinson's disease. Curr Opin Neurobiol 17 (2007) 331-337
21. 2+-based pace making in adult dopamine neurons renders them susceptible to stressors and that a drug induced switch to a pacemaking system normally used by neurons not affected in PD can halt this specific sensitivity both in vivo and in vitro. These results may open a new avenue in PD drug discovery.
22. Block M.L., Zecca L., and Hong J.S. Microglia-mediated neurotoxicity: uncovering the molecular mechanisms. Nat Rev Neurosci 8 (2007) 57-69
23. Griffin III W.C., Boger H.A., Granholm A.C., and Middaugh L.D. Partial deletion of glial cell line-derived neurotrophic factor (GDNF) in mice: effects on sucrose reward and striatal GDNF concentrations. Brain Res 1068 (2006) 257-260
24. Boger H.A., Middaugh L.D., Huang P., Zaman V., Smith A.C., Hoffer B.J., Tomac A.C., and Granholm A.C. A partial GDNF depletion leads to earlier age-related deterioration of motor function and tyrosine hydroxylase expression in the substantia nigra. Exp Neurol 202 (2006) 336-347
25. Kowsky S., Poppelmeyer C., Kramer E.R., Falkenburger B.H., Kruse A., Klein R., and Schulz J.B. RET signaling does not modulate MPTP toxicity but is required for regeneration of dopaminergic axon terminals. Proc Natl Acad Sci U S A 104 (2007) 20049-20054
26. Boger H.A., Middaugh L.D., Patrick K.S., Ramamoorthy S., Denehy E.D., Zhu H., Pacchioni A.M., Granholm A.C., and McGinty J.F. Long-term consequences of methamphetamine exposure in young adults are exacerbated in glial cell line-derived neurotrophic factor heterozygous mice. J Neurosci 27 (2007) 8816-8825
27. von Bohlen und Halbach O., Minichiello L., and Unsicker K. Haploinsufficiency for trkB and trkC receptors induces cell loss and accumulation of alpha-synuclein in the substantia nigra. FASEB J 19 (2005) 1740-1742
28. Zaman V., Nelson M.E., Gerhardt G.A., and Rohrer B. Neurodegenerative alterations in the nigrostriatal system of trkB hypomorphic mice. Exp Neurol 190 (2004) 337-346
29. Hennigan A., O'Callaghan R.M., and Kelly A.M. Neurotrophins and their receptors: roles in plasticity, neurodegeneration and neuroprotection. Biochem Soc Trans 35 (2007) 424-427
30. Maswood N., Young J., Tilmont E., Zhang Z., Gash D.M., Gerhardt G.A., Grondin R., Roth G.S., Mattison J., Lane M.A., et al. Caloric restriction increases neurotrophic factor levels and attenuates neurochemical and behavioral deficits in a primate model of Parkinson's disease. Proc Natl Acad Sci U S A 101 (2004) 18171-18176
31. Martin B., Mattson M.P., and Maudsley S. Caloric restriction and intermittent fasting: two potential diets for successful brain aging. Ageing Res Rev 5 (2006) 332-353
32. Encinas M, Rozen EJ, Dolcet X, Jain S, Comella JX, Milbrandt J, Johnson EM Jr: Analysis of Ret knockin mice reveals a critical role for IKKs, but not PI 3-K, in neurotrophic factor-induced survival of sympathetic neurons. Cell Death Differ 2008, May 23. [Epub ahead of print]; doi:10.1038/cdd.2008.76.
33. Ries V., Henchcliffe C., Kareva T., Rzhetskaya M., Bland R., During M.J., Kholodilov N., and Burke R.E. Oncoprotein Akt/PKB induces trophic effects in murine models of Parkinson's disease. Proc Natl Acad Sci U S A 103 (2006) 18757-18762
34. Chen X., Rzhetskaya M., Kareva T., Bland R., During M.J., Tank A.W., Kholodilov N., and Burke R.E. Antiapoptotic and trophic effects of dominant-negative forms of dual leucine zipper kinase in dopamine neurons of the substantia nigra in vivo. J Neurosci 28 (2008) 672-680
35. Paratcha G., Ledda F., and Ibáñez C.F. The neural cell adhesion molecule NCAM is an alternative signaling receptor for GDNF family ligands. Cell 113 (2003) 867-879
36. Ledda F., Paratcha G., Sandoval-Guzman T., and Ibáñez C.F. GDNF and GFRalpha1 promote formation of neuronal synapses by ligand-induced cell adhesion. Nat Neurosci 10 (2007) 293-300
37. Chao C.C., Ma Y.L., Chu K.Y., and Lee E.H. Integrin alphav and NCAM mediate the effects of GDNF on DA neuron survival, outgrowth, DA turnover and motor activity in rats. Neurobiol Aging 24 (2003) 105-116
38. Gill S.S., Patel N.K., Hotton G.R., O'Sullivan K., McCarter R., Bunnage M., Brooks D.J., Svendsen C.N., and Heywood P. Direct brain infusion of glial cell line-derived neurotrophic factor in Parkinson disease. Nat Med 9 (2003) 589-595
39. Slevin J.T., Gerhardt G.A., Smith C.D., Gash D.M., Kryscio R., and 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 102 (2005) 216-222
40. Lang A.E., Gill S., Patel N.K., Lozano A., Nutt J.G., Penn R., Brooks D.J., Hotton G., Moro E., Heywood P., et al. Randomized controlled trial of intraputamenal glial cell line-derived neurotrophic factor infusion in Parkinson disease. Ann Neurol 59 (2006) 459-466
41. Sherer T.B., Fiske B.K., Svendsen C.N., Lang A.E., and Langston J.W. Crossroads in GDNF therapy for Parkinson's disease. Mov Disord 21 (2006) 136-141
42. Chebrolu H., Slevin J.T., Gash D.A., Gerhardt G.A., Young B., Given C.A., and Smith C.D. MRI volumetric and intensity analysis of the cerebellum in Parkinson's disease patients infused with glial-derived neurotrophic factor (GDNF). Exp Neurol 198 (2006) 450-456
43. Lindvall O., and Wahlberg L.U. Encapsulated cell biodelivery of GDNF: a novel clinical strategy for neuroprotection and neuroregeneration in Parkinson's disease?. Exp Neurol 209 (2008) 82-88
44. Herzog C.D., Dass B., Holden J.E., Stansell III J., Gasmi M., Tuszynski M.H., Bartus R.T., and 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 22 (2007) 1124-1132. A study demonstrating safety and beneficial effects of AAV2-based neurturin intrastriatal delivery on dopaminergic neurites and cell numbers in aged monkeys showing green light for the approach to enter clinical trials.
45. Check E. Second chance. Nat Med 13 (2007) 770-771
46. Petrova P., Raibekas A., Pevsner J., Vigo N., Anafi M., Moore M.K., Peaire A.E., Shridhar V., Smith D.I., Kelly J., et al. MANF: a new mesencephalic, astrocyte-derived neurotrophic factor with selectivity for dopaminergic neurons. J Mol Neurosci 20 (2003) 173-188
47. Apostolou A., Shen Y., Liang Y., Luo J., and Fang S. Armet, a UPR-upregulated protein, inhibits cell proliferation and ER stress-induced cell death. Exp Cell Res 13 (2008) 2454-2467
48. •].
49. Qin L., Block M.L., Liu Y., Bienstock R.J., Pei Z., Zhang W., Wu X., Wilson B., Burka T., and Hong J.S. Microglial NADPH oxidase is a novel target for femtomolar neuroprotection against oxidative stress. FASEB J 19 (2005) 550-557
50. Sriram K., Miller D.B., and O'Callaghan J.P. Minocycline attenuates microglial activation but fails to mitigate striatal dopaminergic neurotoxicity: role of tumor necrosis factor-alpha. J Neurochem 96 (2006) 706-718
51. Outeiro T.F., Kontopoulos E., Altmann S.M., Kufareva I., Strathearn K.E., Amore A.M., Volk C.B., Maxwell M.M., Rochet J.C., McLean P.J., et al. Sirtuin 2 inhibitors rescue alpha-synuclein-mediated toxicity in models of Parkinson's disease. Science 317 (2007) 516-519. An exciting study showing that small molecule mediated Sirt2 inhibition eases α-synuclein inclusion (Lewy body) formation and toxicity in vitro and in Drosophila model of PD opening another avenue for drug development in PD. However, the precise nature of the observed beneficial effect remains uncovered.
52. Schober A., Peterziel H., von Bartheld C.S., Simon H., Krieglstein K., and Unsicker K. GDNF applied to the MPTP-lesioned nigrostriatal system requires TGF-beta for its neuroprotective action. Neurobiol Dis 25 (2007) 378-391. Using mouse MPTP model of PD this work confirms in vivo the earlier observations that GDNF can deliver stronger dopaminergic effects in the presence of TGF-ß and highlights the point that combination of NTFs may have stronger therapeutic effect than each NTF alone.
53. Farkas L.M., Dunker N., Roussa E., Unsicker K., and Krieglstein K. Transforming growth factor-beta(s) are essential for the development of midbrain dopaminergic neurons in vitro and in vivo. J Neurosci 23 (2003) 5178-5186
54. Qin L., Wu X., Block M.L., Liu Y., Breese G.R., Hong J.S., Knapp D.J., and Crews F.T. Systemic LPS causes chronic neuroinflammation and progressive neurodegeneration. Glia 55 (2007) 453-462. Here researchers perform a single peripheral i.p. injection of LPS into wt and TNFα receptor1/2 double knock out mice and show that inflammatory response in the brain is mediated via TNF-α. Importantly, they also find that microglia remains activated as long as 10 months post LPS injection resulting (as shown in earlier studies) in progressive loss of dopaminergic neurons. These results suggest a link between peripheral inflammation and neuroinflammation.