A microRNA embedded AAV alpha-synuclein gene silencing vector for dopaminergic neurons

Brain Research

Volumn 1386, Issue , 2011, Pages 15-24

  Han, Ye ^a   Khodr, Christina E ^a   Sapru, Mohan K ^a   Pedapati, Jyothi ^a   Bohn, Martha C ^a  

^a NORTHWESTERN UNIVERSITY   (United States)

Author keywords

Cell death; Gene therapy; Neurodegeneration; Parkinson's disease; Tyrosine hydroxylase; Vesicular monoamine transporter

Indexed keywords

ADENOVIRUS VECTOR; ALPHA SYNUCLEIN; DNA DIRECTED DNA POLYMERASE ALPHA; DNA DIRECTED DNA POLYMERASE GAMMA; DOPAMINE TRANSPORTER; MICRORNA; SHORT HAIRPIN RNA; TYROSINE 3 MONOOXYGENASE; VESICULAR MONOAMINE TRANSPORTER;

ARTICLE; CELL STRAIN; CELL VIABILITY; CONTROLLED STUDY; DOPAMINERGIC NERVE CELL; GENE SILENCING; HUMAN; HUMAN CELL; IN VITRO GENE TRANSFER; PARKINSON DISEASE; PRIORITY JOURNAL; PROMOTER REGION; VIRAL GENE THERAPY;

ALPHA-SYNUCLEIN; ANIMALS; CELL LINE, TUMOR; DEPENDOVIRUS; DOPAMINE; GENE SILENCING; GENETIC VECTORS; HEK293 CELLS; HUMANS; MICE; MICRORNAS; NEURONS; PARKINSON DISEASE; PC12 CELLS; PLASMIDS; RATS;

RATTUS; RODENTIA;

EID: 79953862206     PISSN: 00068993     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.brainres.2011.02.041     Document Type: Article

References (53)

1. Abeliovich, A., Schmitz, Y., Farinas, I., Choi-Lundberg, D., Ho, W.H., Castillo, P.E., Shinsky, N., Verdugo, J.M., Armanini, M., Ryan, A., Hynes, M., Phillips, H., Sulzer, D., Rosenthal, A., 2000. Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25, 239-252. (Pubitemid 30316525)
2. Alerte, T.N., Akinfolarin, A.A., Friedrich, E.E., Mader, S.A., Hong, C.S., Perez, R.G., 2008. Alpha-synuclein aggregation alters tyrosine hydroxylase phosphorylation and immunoreactivity: lessons from viral transduction of knockout mice. Neurosci. Lett. 435, 24-29.
3. Auluck, P.K., Caraveo, G., Lindquist, S., 2010. Membrane interactions and toxicity in Parkinson's disease. Annu. Rev. Cell Dev. Biol. 26, 211-233.
4. Boudreau, R.L., Martins, I., Davidson, B.L., 2009. Artificial microRNAs as siRNA shuttles: improved safety as compared to shRNAs in vitro and in vivo. Mol. Ther. 17, 169-175.
5. Boudreau, R.L., Davidson, B.L., 2010. RNAi therapeutics for CNS disorders. Brain Res. 1338, 112-121.
6. Chang, K., Elledge, S.J., Hannon, G.J., 2006. Lessons from nature: microRNA-based shRNA libraries. Nat. Methods 3, 707-714. (Pubitemid 44275738)
7. Chu, Y., Kordower, J.H., 2007. Age-associated increases of alpha-synuclein in monkeys and humans are associated with nigrostriatal dopamine depletion: is this the target for Parkinson's disease? Neurobiol. Dis. 25, 134-149. (Pubitemid 44765223)
8. Chung, C.Y., Koprich, J.B., Siddiqi, H., Isacson, O., 2009. Dynamic changes in presynaptic and axonal transport proteins combined with striatal neuroinflammation precede dopaminergic neuronal loss in a rat model of AAV alpha-synucleinopathy. J. Neurosci. 29, 3365-3373.
9. Cookson, M.R., van der Brug, M., 2008. Cell systems and the toxic mechanism(s) of alpha-synuclein. Exp. Neurol. 209, 5-11.
10. Cookson, M.R., 2009. alpha-Synuclein and neuronal cell death. Mol. Neurodegener. 4, 9.
11. Davidson, B.L., Boudreau, R.L., 2007. RNA interference: a tool for querying nervous system function and an emerging therapy. Neuron 53, 781-788. (Pubitemid 46367555)
12. Ehlert, E.M., Eggers, R., Niclou, S.P., Verhaagen, J., 2010. Cellular toxicity following application of adeno-associated viral vector-mediated RNA interference in the nervous system. BMC Neurosci. 11, 20-31.
13. Feany, M.B., Bender, W.W., 2000. A Drosophila model of Parkinson's disease. Nature 404, 394-398. (Pubitemid 30164341)
14. Fernagut, P.O., Chesselet, M.F., 2004. alpha-Synuclein and transgenic mouse models. Neurobiol. Dis. 17, 123-130.
15. Fishman-Jacob, T., Reznichenko, L., Youdim, M.B., Mandel, S.A., 2009. A sporadic Parkinson disease model via silencing of the ubiquitin-proteasome/E3 ligase component SKP1A. J. Biol. Chem. 284, 32835-32845.
16. Fountaine, T.M., Wade-Martins, R., 2007. RNA interference-mediated knockdown of alpha-synuclein protects human dopaminergic neuroblastoma cells from MPP(+) toxicity and reduces dopamine transport. J. Neurosci. Res. 85, 351-363.
17. Giasson, B.I., Duda, J.E., Quinn, S.M., Zhang, B., Trojanowski, J.Q., Lee, V.M., 2002. Neuronal alpha-synucleinopathy with severe movement disorder in mice expressing A53T human alpha-synuclein. Neuron 34, 521-533. (Pubitemid 34628750)
18. Giering, J.C., Grimm, D., Storm, T.A., Kay, M.A., 2008. Expression of shRNA from a tissue-specific pol II promoter is an effective and safe RNAi therapeutic. Mol. Ther. 16, 1630-1636.
19. Gorbatyuk, O.S., Li, S., Nash, K., Gorbatyuk, M., Lewin, A.S., Sullivan, L.F., Mandel, R.J., Chen, W., Meyers, C., Manfredsson, F.P., Muzyczka, N., 2010. In vivo RNAi-mediated alpha-synuclein silencing induces nigrostriatal degeneration. Mol. Ther. 18, 1450-1457.
20. Grimm, D., Streetz, K.L., Jopling, C.L., Storm, T.A., Pandey, K., Davis, C.R., Marion, P., Salazar, F., Kay, M.A., 2006. Fatality in mice due to oversaturation of cellular microRNA/short hairpin RNA pathways. Nature 441, 537-541. (Pubitemid 44050158)
21. Harper, S.Q., Staber, P.D., He, X., Eliason, S.L., Martins, I.H., Mao, Q., Yang, L., Kotin, R.M., Paulson, H.L., Davidson, B.L., 2005. RNA interference improves motor and neuropathological abnormalities in a Huntington's disease mouse model. Proc. Natl Acad. Sci. USA 102, 5820-5825.
22. Hayashita-Kinoh, H., Yamada, M., Yokota, T., Mizuno, Y., Mochizuki, H., 2006. Down-regulation of alpha-synuclein expression can rescue dopaminergic cells from cell death in the substantia nigra of Parkinson's disease rat model. Biochem. Biophys. Res. Commun. 341, 1088-1095.
23. Kahle, P.J., Neumann, M., Ozmen, L., Muller, V., Jacobsen, H., Schindzielorz, A., Okochi, M., Leimer, U., van Der Putten, H., Probst, A., Kremmer, E., Kretzschmar, H.A., Haass, C., 2000. Subcellular localization of wild-type and Parkinson's disease-associated mutant alpha-synuclein in human and transgenic mouse brain. J. Neurosci. 20, 6365-6373.
24. Kaplan, B., Ratner, V., Haas, E., 2003. Alpha-synuclein: its biological function and role in neurodegenerative diseases. J. Mol. Neurosci. 20, 83-92.
25. Kesireddy, V., van der Ven, P.F., Furst, D.O., 2010. Multipurpose modular lentiviral vectors for RNA interference and transgene expression. Mol Biol Rep. 37, 2863-2870.
26. Kirik, D., Rosenblad, C., Burger, C., Lundberg, C., Johansen, T.E., Muzyczka, N., Mandel, R.J., Bjorklund, A., 2002. Parkinson-like neurodegeneration induced by targeted overexpression of alpha-synuclein in the nigrostriatal system. J. Neurosci. 22, 2780-2791. (Pubitemid 37465827)
27. Kirik, D., Annett, L.E., Burger, C., Muzyczka, N., Mandel, R.J., Bjorklund, A., 2003. Nigrostriatal alpha-synucleinopathy induced by viral vector-mediated overexpression of human alpha-synuclein: a new primate model of Parkinson's disease. Proc. Natl Acad. Sci. USA 100, 2884-2889.
28. Kruger, R., Kuhn, W., Muller, T., Woitalla, D., Graeber, M., Kosel, S., Przuntek, H., Epplen, J.T., Schols, L., Riess, O., 1998. Ala30Pro mutation in the gene encoding alpha-synuclein in Parkinson's disease. Nat. Genet. 18, 106-108.
29. Kuhn, K., Wellen, J., Link, N., Maskri, L., Lubbert, H., Stichel, C.C., 2003. The mouse MPTP model: gene expression changes in dopaminergic neurons. Eur. J. Neurosci. 17, 1-12.
30. Liu, D.M., Jin, L., Wang, H., Zhao, H.Y., Zhao, C.L., Yang, H., 2008. RNA interference mediated silencing of alpha-synuclein in MN9D cells and its effects on cell viability. Neurosci. Bull. 24, 96-104.
31. Maraganore, D.M., de Andrade, M., Elbaz, A., Farrer, M.J., Ioannidis, J.P., Kruger, R., Rocca, W.A., Schneider, N.K., Lesnick, T.G., Lincoln, S.J., Hulihan, M.M., Aasly, J.O., Ashizawa, T., Chartier-Harlin, M.C., Checkoway, H., Ferrarese, C., Hadjigeorgiou, G., Hattori, N., Kawakami, H., Lambert, J.C., Lynch, T., Mellick, G.D., Papapetropoulos, S., Parsian, A., Quattrone, A., Riess, O., Tan, E.K., Van Broeckhoven, C., 2006. Collaborative analysis of alpha-synuclein gene promoter variability and Parkinson disease. JAMA 296, 661-670. (Pubitemid 44200637)
32. McBride, J.L., Boudreau, R.L., Harper, S.Q., Staber, P.D., Monteys, A.M., Martins, I., Gilmore, B.L., Burstein, H., Peluso, R.W., Polisky, B., Carter, B.J., Davidson, B.L., 2008. Artificial miRNAs mitigate shRNA-mediated toxicity in the brain: implications for the therapeutic development of RNAi. Proc. Natl Acad. Sci. USA 105, 5868-5873.
33. McCormack, A.L., Mak, S.K., Henderson, J.M., Bumcrot, D., Farrer, M.J., Di Monte, D.A., 2010. Alpha-synuclein suppression by targeted small interfering RNA in the primate substantia nigra. PLoS ONE 5, e12122.
34. Murphy, D.D., Rueter, S.M., Trojanowski, J.Q., Lee, V.M., 2000. Synucleins are developmentally expressed, and alpha-synuclein regulates the size of the presynaptic vesicular pool in primary hippocampal neurons. J. Neurosci. 20, 3214-3220. (Pubitemid 30263139)
35. Nielsen, T.T., Marion, I., Hasholt, L., Lundberg, C., 2009. Neuron-specific RNA interference using lentiviral vectors. J. Gene Med. 11, 559-569.
36. Perez, R.G., Hastings, T.G., 2004. Could a loss of alpha-synuclein function put dopaminergic neurons at risk? J. Neurochem. 89, 1318-1324. (Pubitemid 38802653)
37. Polymeropoulos, M.H., Lavedan, C., Leroy, E., Ide, S.E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R., Stenroos, E.S., Chandrasekharappa, S., Athanassiadou, A., Papapetropoulos, T., Johnson, W.G., Lazzarini, A.M., Duvoisin, R.C., Di Iorio, G., Golbe, L.I., Nussbaum, R.L., 1997. Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276, 2045-2047. (Pubitemid 27443610)
38. Richfield, E.K., Thiruchelvam, M.J., Cory-Slechta, D.A., Wuertzer, C., Gainetdinov, R.R., Caron, M.G., Di Monte, D.A., Federoff, H.J., 2002. Behavioral and neurochemical effects of wild-type and mutated human alpha-synuclein in transgenic mice. Exp. Neurol. 175, 35-48.
39. Rodriguez-Lebron, E., Paulson, H.L., 2006. Allele-specific RNA interference for neurological disease. Gene Ther. 13, 576-581.
40. Saha, A.R., Hill, J., Utton, M.A., Asuni, A.A., Ackerley, S., Grierson, A.J., Miller, C.C., Davies, A.M., Buchman, V.L., Anderton, B.H., Hanger, D.P., 2004. Parkinson's disease alpha-synuclein mutations exhibit defective axonal transport in cultured neurons. J. Cell Sci. 117, 1017-1024. (Pubitemid 38456084)
41. Sapru, M.K., Yates, J.W., Hogan, S., Jiang, L., Halter, J., Bohn, M.C., 2006. Silencing of human alpha-synuclein in vitro and in rat brain using lentiviral-mediated RNAi. Exp. Neurol. 198, 382-390.
42. Scott, D.A., Tabarean, I., Tang, Y., Cartier, A., Masliah, E., Roy, S., 2010. A pathologic cascade leading to synaptic dysfunction in alpha-synuclein-induced neurodegeneration. J. Neurosci. 30, 8083-8095.
43. Spillantini, M.G., Crowther, R.A., Jakes, R., Hasegawa, M., Goedert, M., 1998. alpha-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with lewy bodies. Proc. Natl Acad. Sci. USA 95, 6469-6473.
44. Stegmeier, F., Hu, G., Rickles, R.J., Hannon, G.J., Elledge, S.J., 2005. A lentiviral microRNA-based system for single-copy polymerase II-regulated RNA interference in mammalian cells. Proc. Natl Acad. Sci. USA 102, 13212-13217.
45. Trojanowski, J.Q., Lee, V.M., 1998. Aggregation of neurofilament and alpha-synuclein proteins in Lewy bodies: implications for the pathogenesis of Parkinson disease and Lewy body dementia. Arch. Neurol. 55, 151-152.
46. Ueda, K., Fukushima, H., Masliah, E., Xia, Y., Iwai, A., Yoshimoto, M., Otero, D.A., Kondo, J., Ihara, Y., Saitoh, T., 1993. Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc. Natl Acad. Sci. USA 90, 11282-11286.
47. Ulusoy, A., Sahin, G., Bjorklund, T., Aebischer, P., Kirik, D., 2009. Dose optimization for long-term rAAV-mediated RNA interference in the nigrostriatal projection neurons. Mol. Ther. 17, 1574-1584.
48. van der Putten, H., Wiederhold, K.H., Probst, A., Barbieri, S., Mistl, C., Danner, S., Kauffmann, S., Hofele, K., Spooren, W.P., Ruegg, M.A., Lin, S., Caroni, P., Sommer, B., Tolnay, M., Bilbe, G., 2000. Neuropathology in mice expressing human alpha-synuclein. J. Neurosci. 20, 6021-6029. (Pubitemid 30658395)
49. Volles, M.J., Lee, S.J., Rochet, J.C., Shtilerman, M.D., Ding, T.T., Kessler, J.C., Lansbury Jr., P.T., 2001. Vesicle permeabilization by protofibrillar alpha-synuclein: implications for the pathogenesis and treatment of Parkinson's disease. Biochemistry 40, 7812-7819.
50. Wersinger, C., Prou, D., Vernier, P., Niznik, H.B., Sidhu, A., 2003. Mutations in the lipid-binding domain of alpha-synuclein confer overlapping, yet distinct, functional properties in the regulation of dopamine transporter activity. Mol. Cell. Neurosci. 24, 91-105.
51. Wood, S.J., Wypych, J., Steavenson, S., Louis, J.C., Citron, M., Biere, A.L., 1999. Alpha-synuclein fibrillogenesis is nucleation-dependent. Implications for the pathogenesis of Parkinson's disease. J. Biol. Chem. 274, 19509-19512.
52. Wood-Kaczmar, A., Gandhi, S., Wood, N.W., 2006. Understanding the molecular causes of Parkinson's disease. Trends Mol. Med. 12, 521-528.
53. Zarranz, J.J., Alegre, J., Gomez-Esteban, J.C., Lezcano, E., Ros, R., Ampuero, I., Vidal, L., Hoenicka, J., Rodriguez, O., Atares, B., Llorens, V., Gomez Tortosa, E., del Ser, T., Munoz, D.G., de Yebenes, J.G., 2004. The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann. Neurol. 55, 164-173.