Age and α-synuclein expression interact to reveal a dependence of dopaminergic axons on endogenous Akt/PKB signaling

Neurobiology of Disease

Volumn 44, Issue 2, 2011, Pages 215-222

  Kim, Sang Ryong ^a   Ries, Vincent ^a   Cheng, Hsiao Chun ^a   Kareva, Tatyana ^a   Oo, Tinmarla F ^a   Yu, W Haung ^a,b   Duff, Karen ^a,b   Kholodilov, Nikolai ^a   Burke, Robert E ^a,b  

^a Och Spine at New York Presbyterian Hospitals   (United States)

^b NewYork Presbyterian Hospital   (United States)

Author keywords

Akt; Axon; Dopamine; Parkinson's disease; Substantia nigra; Synuclein

Indexed keywords

ALPHA SYNUCLEIN; PHOSPHATIDYLINOSITOL 3 KINASE; PLECKSTRIN; PROTEIN KINASE B; TYROSINE 3 MONOOXYGENASE;

AGE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; CORPUS STRIATUM; DOPAMINERGIC NERVE CELL; MALE; MOUSE; NONHUMAN; PARKINSON DISEASE; PHENOTYPE; PRIORITY JOURNAL; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; RISK FACTOR; SIGNAL TRANSDUCTION; SUBSTANTIA NIGRA;

AGING; ALPHA-SYNUCLEIN; ANIMALS; AXONS; DISEASE MODELS, ANIMAL; DOPAMINERGIC NEURONS; HUMANS; MALE; MICE; MICE, INBRED C57BL; MICE, KNOCKOUT; MICE, TRANSGENIC; PARKINSONIAN DISORDERS; PROTO-ONCOGENE PROTEINS C-AKT; SIGNAL TRANSDUCTION;

EID: 80052290624     PISSN: 09699961     EISSN: 1095953X     Source Type: Journal    
DOI: 10.1016/j.nbd.2011.07.003     Document Type: Article

References (49)

1. Aleyasin H., Rousseaux M.W., Marcogliese P.C., Hewitt S.J., Irrcher I., Joselin A.P., Parsanejad M., Kim R.H., Rizzu P., Callaghan S.M., Slack R.S., Mak T.W., Park D.S. DJ-1 protects the nigrostriatal axis from the neurotoxin MPTP by modulation of the AKT pathway. Proc. Natl. Acad. Sci. U. S. A. 2010, 107:3186-3191.
2. Altar C.A., Dugich-Djordjevic M., Armanini M., Bakhit C. Medial-to-lateral gradient of neostriatal NGF receptors: relationship to cholinergic neurons and NGF-like immunoreactivity. J. Neurosci. 1991, 11:828-836.
3. Besset V., Scott R.P., Ibanez C.F. Signaling complexes and protein-protein interactions involved in the activation of the Ras and phosphatidylinositol 3-kinase pathways by the c-Ret receptor tyrosine kinase. J. Biol. Chem. 2000, 275:39159-39166.
4. Bower J.H., Maraganore D.M., McDonnell S.K., Rocca W.A. Influence of strict, intermediate, and broad diagnostic criteria on the age- and sex-specific incidence of Parkinson's disease. Mov. Disord. 2000, 15:819-825.
5. Burke R.E. Programmed cell death and new discoveries in the genetics of parkinsonism. J. Neurochem. 2008, 104:875-890.
6. Burke R.E., Karanas A.L. Demonstration of a medial to lateral gradient in the density of cholinergic neuropil in the rat striatum. Neurosci. Lett. 1990, 108:58-64.
7. Chen Z., Chai Y., Cao L., Huang A., Cui R., Lu C., He C. Glial cell line-derived neurotrophic factor promotes survival and induces differentiation through the phosphatidylinositol 3-kinase and mitogen-activated protein kinase pathway respectively in PC12 cells. Neuroscience 2001, 104:593-598.
8. Chen X., Rzhetskaya M., Kareva T., Bland R., During M.J., Tank A.W., Kholodilov N., 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. 2008, 28:672-680.
9. Chen X., Kareva T., Kholodilov N., Burke R.E. SGK has neurotrophic and neuroprotective effects on the nigrostriatal dopaminergic system in vivo. Abstr. Soc. Neurosci. 2009, (2009-S-8157-SfN).
10. Cookson M.R., Bandmann O. Parkinson's disease: insights from pathways. Hum. Mol. Genet. 2010, 19:R21-R27.
11. Coulpier M., Ibanez C.F. Retrograde propagation of GDNF-mediated signals in sympathetic neurons. Mol. Cell. Neurosci. 2004, 27:132-139.
12. Dauer W.T., Kholodilov N., Vila M., Trillat A., Goodchild R., Larsen K.E., Staal R., Tieu K., Schmitz Y., Yuan C.A., Rocha M., Jackson-Lewis V., Hersch S., Sulzer D., Przedborski S., Burke R.E., Hen R. Resistance of α-synuclein null mice to the parkinsonian neurotoxin MPTP. Proc. Natl. Acad. Sci. U. S. A. 2002, 99:14524-14529.
13. De Vita G., Melillo R.M., Carlomagno F., Visconti R., Castellone M.D., Bellacosa A., Billaud M., Fusco A., Tsichlis P.N., Santoro M. Tyrosine 1062 of RET-MEN2A mediates activation of Akt (protein kinase B) and mitogen-activated protein kinase pathways leading to PC12 cell survival. Cancer Res. 2000, 60:3727-3731.
14. Dudek H., Datta S.R., Franke T.F., Birnbaum M.J., Yao R., Cooper G.M., Segal R.A., Kaplan D.R., Greenberg M.E. Regulation of neuronal survival by the serine-threonine protein kinase Akt. Science 1997, 275:661-665.
15. El-Khodor B.F., Burke R.E. Medial forebrain bundle axotomy during development induces apoptosis in dopamine neurons of the substantia nigra and activation of caspases in their degenerating axons. J. Comp. Neurol. 2002, 452:65-79.
16. Gerfen C.R., Herkenham M., Thibault J. The neostriatal mosaic: II. Patch- and matrix-directed mesostriatal dopaminergic and non-dopaminergic systems. J. Neurosci. 1987, 7:3915-3934.
17. Greene, L.A., Levy, O., Malagelada, C., in press. Akt as a victim, villain and potential hero in Parkinson's disease pathophysiology and treatment. Cell. Mol. Neurobiol. doi:. doi:10.1007/s10571-011-9671-8.
18. Hanada M., Feng J., Hemmings B.A. Structure, regulation and function of PKB/AKT-a major therapeutic target. Biochim. Biophys. Acta 2004, 1697:3-16.
19. Kadkhodaei B., Ito T., Joodmardi E., Mattsson B., Rouillard C., Carta M., Muramatsu S., Sumi-Ichinose C., Nomura T., Metzger D., Chambon P., Lindqvist E., Larsson N.G., Olson L., Bjorklund A., Ichinose H., Perlmann T. Nurr1 is required for maintenance of maturing and adult midbrain dopamine neurons. J. Neurosci. 2009, 29:15923-15932.
20. Kramer E.R., Aron L., Ramakers G.M., Seitz S., Zhuang X., Beyer K., Smidt M.P., Klein R. Absence of Ret signaling in mice causes progressive and late degeneration of the nigrostriatal system. PLoS Biol. 2007, 5:e39.
21. Kwon C.H., Luikart B.W., Powell C.M., Zhou J., Matheny S.A., Zhang W., Li Y., Baker S.J., Parada L.F. Pten regulates neuronal arborization and social interaction in mice. Neuron 2006, 50:377-388.
22. Lees A.J., Hardy J., Revesz T. Parkinson's disease. Lancet 2009, 373:2055-2066.
23. Li Y., Liu W., Oo T.F., Wang L., Tang Y., Jackson-Lewis V., Zhou C., Geghman K., Bogdanov M., Przedborski S., Beal M.F., Burke R.E., Li C. Mutant LRRK2(R1441G) BAC transgenic mice recapitulate cardinal features of Parkinson's disease. Nat. Neurosci. 2009, 12:826-828.
24. Lin M.T., Beal M.F. Mitochondrial dysfunction and oxidative stress in neurodegenerative diseases. Nature 2006, 443:787-795.
25. Malagelada C., Jin Z.H., Greene L.A. RTP801 is induced in Parkinson's disease and mediates neuron death by inhibiting Akt phosphorylation/activation. J. Neurosci. 2008, 28:14363-14371.
26. Malagelada C., Jin Z.H., Jackson-Lewis V., Przedborski S., Greene L.A. Rapamycin protects against neuron death in in vitro and in vivo models of Parkinson's disease. J. Neurosci. 2010, 30:1166-1175.
27. Manning B.D., Cantley L.C. AKT/PKB signaling: navigating downstream. Cell 2007, 129:1261-1274.
28. Matsuoka Y., Vila M., Lincoln S., McCormack A., Picciano M., LaFrancois J., Yu X., Dickson D., Langston W.J., McGowan E., Farrer M., Hardy J., Duff K., Przedborski S., Di Monte D.A. Lack of nigral pathology in transgenic mice expressing human alpha-synuclein driven by the tyrosine hydroxylase promoter. Neurobiol. Dis. 2001, 8:535-539.
29. Maurin Y., Banrezes B., Menetrey A., Mailly P., Deniau J.M. Three-dimensional distribution of nigrostriatal neurons in the rat: relation to the topography of striatonigral projections. Neuroscience 1999, 91:891-909.
30. Namikawa K., Honma M., Abe K., Takeda M., Mansur K., Obata T., Miwa A., Okado H., Kiyama H. Akt/protein kinase B prevents injury-induced motoneuron death and accelerates axonal regeneration. J. Neurosci. 2000, 20:2875-2886.
31. Olson V.G., Heusner C.L., Bland R.J., During M.J., Weinshenker D., Palmiter R.D. Role of noradrenergic signaling by the nucleus tractus solitarius in mediating opiate reward. Science 2006, 311:1017-1020.
32. Oo T.F., Kholodilov N., Burke R.E. Regulation of natural cell death in dopaminergic neurons of the substantia nigra by striatal GDNF in vivo. J. Neurosci. 2003, 23:5141-5148.
33. Pals P., Lincoln S., Manning J., Heckman M., Skipper L., Hulihan M., Van den, B.M., De Pooter T., Cras P., Crook J., Van Broeckhoven C., Farrer M.J. alpha-Synuclein promoter confers susceptibility to Parkinson's disease. Ann. Neurol. 2004, 56:591-595.
34. Park K.K., Liu K., Hu Y., Smith P.D., Wang C., Cai B., Xu B., Connolly L., Kramvis I., Sahin M., He Z. Promoting axon regeneration in the adult CNS by modulation of the PTEN/mTOR pathway. Science 2008, 322:963-966.
35. Pascual A., Hidalgo-Figueroa M., Piruat J.I., Pintado C.O., Gomez-Diaz R., Lopez-Barneo J. Absolute requirement of GDNF for adult catecholaminergic neuron survival. Nat. Neurosci. 2008, 11:755-761.
36. Paxinos G., Franklin K.B.J. The Mouse Brain in Stereotaxic Coordinates 2001, Academic Press, New York.
37. Pong K., Xu R.Y., Baron W.F., Louis J.C., Beck K.D. Inhibition of phosphatidylinositol 3-kinase activity blocks cellular differentiation mediated by glial cell line-derived neurotrophic factor in dopaminergic neurons. J. Neurochem. 1998, 71:1912-1919.
38. Rieker C., Engblom D., Kreiner G., Domanskyi A., Schober A., Stotz S., Neumann M., Yuan X., Grummt I., Schutz G., Parlato R. Nucleolar disruption in dopaminergic neurons leads to oxidative damage and parkinsonism through repression of mammalian target of rapamycin signaling. J. Neurosci. 2011, 31:453-460.
39. Ries V., Henchcliffe C., Kareva T., Rzhetskaya M., Bland R.J., During M.J., Kholodilov N., Burke R.E. Oncoprotein Akt/PKB: trophic effects in murine models of Parkinson's disease. Proc. Natl. Acad. Sci. U. S. A. 2006, 103:18757-18762.
40. Ries V., Silva R.M., Oo T.F., Cheng H.C., Rzhetskaya M., Kholodilov N., Flavell R.A., Kuan C.Y., Rakic P., Burke R.E. JNK2 and JNK3 combined are essential for apoptosis in dopamine neurons of the substantia nigra, but are not required for axon degeneration. J. Neurochem. 2008, 107:1578-1588.
41. Ries V., Cheng H.C., Baohan A., Kareva T., Oo T.F., Rzhetskaya M., Bland R.J., During M.J., Kholodilov N., Burke R.E. Regulation of the postnatal development of dopamine neurons of the substantia nigra in vivo by Akt/protein kinase B. J. Neurochem. 2009, 110:23-33.
42. Sawada H., Ibi M., Kihara T., Urushitani M., Nakanishi M., Akaike A., Shimohama S. Neuroprotective mechanism of glial cell line-derived neurotrophic factor in mesencephalic neurons. J. Neurochem. 2000, 74:1175-1184.
43. Schnabel J. Secrets of the shaking palsy. Nature 2010, 466:S2-S5.
44. Singleton A.B., Farrer M., Johnson J., Singleton A., Hague S., Kachergus J., Hulihan M., Peuralinna T., Dutra A., Nussbaum R., Lincoln S., Crawley A., Hanson M., Maraganore D., Adler C., Cookson M.R., Muenter M., Baptista M., Miller D., Blancato J., Hardy J., Gwinn-Hardy K. alpha-Synuclein locus triplication causes Parkinson's disease. Science 2003, 302:841.
45. Soler R.M., Dolcet X., Encinas M., Egea J., Bayascas J.R., Comella J.X. Receptors of the glial cell line-derived neurotrophic factor family of neurotrophic factors signal cell survival through the phosphatidylinositol 3-kinase pathway in spinal cord motoneurons. J. Neurosci. 1999, 19:9160-9169.
46. Songyang Z., Baltimore D., Cantley L.C., Kaplan D.R., Franke T.F. Interleukin 3-dependent survival by the Akt protein kinase. Proc. Natl. Acad. Sci. U. S. A. 1997, 94:11345-11350.
47. Timmons S., Coakley M.F., Moloney A.M., O'Neill C. Akt signal transduction dysfunction in Parkinson's disease. Neurosci. Lett. 2009, 467:30-35.
48. Voorn P., Vanderschuren L.J., Groenewegen H.J., Robbins T.W., Pennartz C.M. Putting a spin on the dorsal-ventral divide of the striatum. Trends Neurosci. 2004, 27:468-474.
49. Wang Q., Liu L., Pei L., Ju W., Ahmadian G., Lu J., Wang Y., Liu F., Wang Y.T. Control of synaptic strength, a novel function of Akt. Neuron 2003, 38:915-928.