Mutant twinkle increases dopaminergic neurodegeneration, mtDNA deletions and modulates Parkin expression

Human Molecular Genetics

Volumn 21, Issue 23, 2012, Pages 5147-5158

  Song, Lanying ^a   Shan, Yuxi ^a   Kent Lloyd, K C ^a   Cortopassi, Gino A ^a  

^a UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DNA; HELICASE; MITOCHONDRIAL DNA; PARKIN; PROTEASOME; RNA; TWINKLE HELICASE; TYROSINE 3 MONOOXYGENASE; UNCLASSIFIED DRUG;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; BEHAVIOR; BODY WEIGHT; BRAIN MITOCHONDRION; CONFOCAL MICROSCOPY; CONTROLLED STUDY; DEGENERATIVE DISEASE; DOPAMINERGIC NERVE CELL; GENE DELETION; GENE MUTATION; IMMUNOPRECIPITATION; MESENCEPHALON; MITOCHONDRIAL RESPIRATION; MOTOR PERFORMANCE; MOUSE; NERVE CELL; NEUROLOGIC DISEASE; NONHUMAN; PARKINSON DISEASE; PARKINSONISM; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN PROTEIN INTERACTION; REAL TIME POLYMERASE CHAIN REACTION; ROTAROD TEST; SUBSTANTIA NIGRA; TRANSGENE; TRANSGENIC MOUSE;

ANIMALS; AUTOPHAGY; BEHAVIOR, ANIMAL; CELL LINE; CELL RESPIRATION; DNA HELICASES; DNA, MITOCHONDRIAL; DOPAMINERGIC NEURONS; GENE EXPRESSION; GENE ORDER; GENE TARGETING; HUMANS; MICE; MICE, TRANSGENIC; MITOCHONDRIAL PROTEINS; MUTATION; PARKINSON DISEASE; PROMOTER REGIONS, GENETIC; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN BINDING; SUBSTANTIA NIGRA; TYROSINE 3-MONOOXYGENASE; UBIQUITIN-PROTEIN LIGASES;

MAMMALIA; MUS;

EID: 84869048670     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/dds365     Document Type: Article

References (45)

1. Gautier, C.A., Kitada, T. and Shen, J. (2008) Loss of PINK1 causes mitochondrial functional defects and increased sensitivity to oxidative stress. Proc. Natl Acad. Sci. USA., 105, 11364-11369.
2. Abou-Sleiman, P.M., Muqit, M.M. and Wood, N.W. (2006) Expanding insights of mitochondrial dysfunction in Parkinson's disease. Nat. Rev. Neurosci., 7, 207-219.
3. Parker, W.D. Jr., Boyson, S.J. and Parks, J.K. (1989) Abnormalities of the electron transport chain in idiopathic Parkinson's disease. Ann. Neurol., 26, 719-723.
4. Valente, E.M., Abou-Sleiman, P.M., Caputo, V., Muqit, M.M., Harvey, K., Gispert, S., Ali, Z., Del Turco, D., Bentivoglio, A.R., Healy, D.G. et al. (2004) Hereditary early-onset Parkinson's disease caused by mutations in PINK1. Science, 304, 1158-1160.
5. Serikawa, T., Shimohata, T., Akashi, M., Yokoseki, A., Tsuchiya, M., Hasegawa, A., Haino, K., Koike, R., Takakuwa, K., Tanaka, K. et al. (2011) Successful twin pregnancy in a patient with parkin-associated autosomal recessive juvenile parkinsonism. BMC Neurol., 11, 72.
6. Betarbet, R., Sherer, T.B., MacKenzie, G., Garcia-Osuna, M., Panov, A.V. and Greenamyre, J.T. (2000) Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci., 3, 1301-1306.
7. Shin, J.H., Ko, H.S., Kang, H., Lee, Y., Lee, Y.I., Pletinkova, O., Troconso, J.C., Dawson, V.L. and Dawson, T.M. (2011) PARIS (ZNF746) repression of PGC-1alpha contributes to neurodegeneration in Parkinson's disease. Cell, 144, 689-702.
8. Bender, A., Krishnan, K.J., Morris, C.M., Taylor, G.A., Reeve, A.K., Perry, R.H., Jaros, E., Hersheson, J.S., Betts, J., Klopstock, T. et al. (2006) High levels of mitochondrial DNA deletions in substantia nigra neurons in aging and Parkinson disease. Nat. Genet., 38, 515-517.
9. Cortopassi, G.A., Shibata, D., Soong, N.W. and Arnheim, N. (1992) A pattern of accumulation of a somatic deletion of mitochondrial DNA in aging human tissues. Proc. Natl Acad. Sci. USA., 89, 7370-7374.
10. Soong, N.W., Hinton, D.R., Cortopassi, G. and Arnheim, N. (1992) Mosaicism for a specific somatic mitochondrial DNA mutation in adult human brain. Nat. Genet., 2, 318-323.
11. Trifunovic, A., Wredenberg, A., Falkenberg, M., Spelbrink, J.N., Rovio, A.T., Bruder, C.E., Bohlooly, Y.M., Gidlof, S., Oldfors, A., Wibom, R. et al. (2004) Premature ageing in mice expressing defective mitochondrial DNA polymerase. Nature, 429, 417-423.
12. Luoma, P., Melberg, A., Rinne, J.O., Kaukonen, J.A., Nupponen, N.N., Chalmers, R.M., Oldfors, A., Rautakorpi, I., Peltonen, L., Majamaa, K. et al. (2004) Parkinsonism, premature menopause, and mitochondrial DNA polymerase gamma mutations: clinical and molecular genetic study. Lancet, 364, 875-882.
13. Spelbrink, J.N., Li, F.Y., Tiranti, V., Nikali, K., Yuan, Q.P., Tariq, M., Wanrooij, S., Garrido, N., Comi, G., Morandi, L. et al. (2001) Human mitochondrial DNA deletions associated with mutations in the gene encoding Twinkle, a phage T7 gene 4-like protein localized in mitochondria. Nat. Genet., 28, 223-231.
14. Tyynismaa, H., Mjosund, K.P., Wanrooij, S., Lappalainen, I., Ylikallio, E., Jalanko, A., Spelbrink, J.N., Paetau, A. and Suomalainen, A. (2005) Mutant mitochondrial helicase Twinkle causes multiple mtDNA deletions and a late-onset mitochondrial disease in mice. Proc. Natl Acad. Sci. USA., 102, 17687-17692.
15. Baloh, R.H., Salavaggione, E., Milbrandt, J. and Pestronk, A. (2007) Familial Parkinsonism and ophthalmoplegia from a mutation in the mitochondrial DNA helicase twinkle. Arch. Neurol., 64, 998-1000.
16. Rothfuss, O., Fischer, H., Hasegawa, T., Maisel, M., Leitner, P., Miesel, F., Sharma, M., Bornemann, A., Berg, D., Gasser, T. et al. (2009) Parkin protects mitochondrial genome integrity and supports mitochondrial DNA repair. Hum. Mol. Genet., 18, 3832-3850.
17. Glauser, L., Sonnay, S., Stafa, K. and Moore, D.J. (2011) Parkin promotes the ubiquitination and degradation of the mitochondrial fusion factor mitofusin 1. J. Neurochem., 118, 636-645.
18. Um, J.W., Im, E., Lee, H.J., Min, B., Yoo, L., Yoo, J., Lubbert, H., Stichel-Gunkel, C., Cho, H.S., Yoon, J.B. et al. (2010) Parkin directly modulates 26S proteasome activity. J. Neurosci., 30, 11805-11814.
19. Alemi, M., Prigione, A., Wong, A., Schoenfeld, R., DiMauro, S., Hirano, M., Taroni, F. and Cortopassi, G. (2007) Mitochondrial DNA deletions inhibit proteasomal activity and stimulate an autophagic transcript. Free Radic. Biol. Med., 42, 32-43.
20. Hara, T., Nakamura, K., Matsui, M., Yamamoto, A., Nakahara, Y., Suzuki-Migishima, R., Yokoyama, M., Mishima, K., Saito, I., Okano, H. et al. (2006) Suppression of basal autophagy in neural cells causes neurodegenerative disease in mice. Nature, 441, 885-889.
21. Cotan, D., Cordero, M.D., Garrido-Maraver, J., Oropesa-Avila, M., Rodriguez-Hernandez, A., Gomez Izquierdo, L., De la Mata, M., De Miguel, M., Bautista Lorite, J., Rivas Infante, E. et al. (2011) Secondary coenzyme Q10 deficiency triggers mitochondria degradation by mitophagy in MELAS fibroblasts. FASEB J., 25, 2669-87.
22. Archer, C.R., Koomoa, D.L., Mitsunaga, E.M., Clerc, J., Shimizu, M., Kaiser, M., Schellenberg, B., Dudler, R. and Bachmann, A.S. (2010) Syrbactin class proteasome inhibitor-induced apoptosis and autophagy occurs in association with p53 accumulation and Akt/PKB activation in neuroblastoma. Biochem. Pharmacol., 80, 170-178.
23. Casarejos, M.J., Solano, R.M., Rodriguez-Navarro, J.A., Gomez, A., Perucho, J., Castano, J.G., Garcia de Yebenes, J. and Mena, M.A. (2009) Parkin deficiency increases the resistance of midbrain neurons and glia to mild proteasome inhibition: the role of autophagy and glutathione homeostasis. J. Neurochem., 110, 1523-1537.
24. Fukui, H. and Moraes, C.T. (2009) Mechanisms of formation and accumulation of mitochondrial DNA deletions in aging neurons. Hum. Mol. Genet., 18, 1028-1036.
25. Ekstrand, M.I., Terzioglu, M., Galter, D., Zhu, S., Hofstetter, C., Lindqvist, E., Thams, S., Bergstrand, A., Hansson, F.S., Trifunovic, A. et al. (2007) Progressive Parkinsonism in mice with respiratory-chain-deficient dopamine neurons. Proc. Natl Acad. Sci. USA., 104, 1325-1330.
26. Park, J., Lee, S.B., Lee, S., Kim, Y., Song, S., Kim, S., Bae, E., Kim, J., Shong, M., Kim, J.M. et al. (2006) Mitochondrial dysfunction in Drosophila PINK1 mutants is complemented by Parkin. Nature, 441, 1157-1161.
27. Deng, H., Dodson, M.W., Huang, H. and Guo, M. (2008) The Parkinson's disease genes pink1 and parkin promote mitochondrial fission and/or inhibit fusion in Drosophila. Proc. Natl Acad. Sci. USA., 105, 14503-14508.
28. Yang, H., Zhou, X., Liu, X., Yang, L., Chen, Q., Zhao, D., Zuo, J. and Liu, W. (2011) Mitochondrial dysfunction induced by knockdown of mortalin is rescued by Parkin. Biochem. Biophys. Res. Commun., 410, 114-120.
29. Greenwood, S.M. and Bushell, T.J. (2010) Astrocytic activation and an inhibition of MAP kinases are required for proteinase-activated receptor-2-mediated protection from neurotoxicity. J. Neurochem., 113, 1471-1480.
30. Stichel, C.C., Zhu, X.R., Bader, V., Linnartz, B., Schmidt, S. and Lubbert, H. (2007) Mono- and double-mutant mouse models of Parkinson's disease display severe mitochondrial damage. Hum. Mol. Genet., 16, 2377-2393.
31. Komatsu, M., Waguri, S., Chiba, T., Murata, S., Iwata, J., Tanida, I., Ueno, T., Koike, M., Uchiyama, Y., Kominami, E. et al. (2006) Loss of autophagy in the central nervous system causes neurodegeneration in mice. Nature, 441, 880-884.
32. Pan, T., Kondo, S., Le, W. and Jankovic, J. (2008) The role of autophagy-lysosome pathway in neurodegeneration associated with Parkinson's disease. Brain, 131, 1969-1978.
33. Takacs-Vellai, K., Bayci, A. and Vellai, T. (2006) Autophagy in neuronal cell loss: a road to death. Bioessays, 28, 1126-1131.
34. Apostolova, N., Gomez-Sucerquia, L.J., Gortat, A., Blas-Garcia, A. and Esplugues, J.V. (2011) Compromising mitochondrial function with the antiretroviral drug efavirenz induces cell survival-promoting autophagy. Hepatology, 54, 1009-19.
35. Iwata, A., Riley, B.E., Johnston, J.A. and Kopito, R.R. (2005) HDAC6 and microtubules are required for autophagic degradation of aggregated huntingtin. J. Biol. Chem., 280, 40282-40292.
36. Massey, A.C., Kaushik, S., Sovak, G., Kiffin, R. and Cuervo, A.M. (2006) Consequences of the selective blockage of chaperone-mediated autophagy. Proc. Natl Acad. Sci. USA., 103, 5805-5810.
37. Lee, J.Y., Nagano, Y., Taylor, J.P., Lim, K.L. and Yao, T.P. (2010) Disease-causing mutations in parkin impair mitochondrial ubiquitination, aggregation, and HDAC6-dependent mitophagy. J. Cell Biol., 189, 671-679.
38. Matsushita, N., Okada, H., Yasoshima, Y., Takahashi, K., Kiuchi, K. and Kobayashi, K. (2002) Dynamics of tyrosine hydroxylase promoter activity during midbrain dopaminergic neuron development. J. Neurochem., 82, 295-304.
39. Fleming, S.M., Salcedo, J., Fernagut, P.O., Rockenstein, E., Masliah, E., Levine, M.S. and Chesselet, M.F. (2004) Early and progressive sensorimotor anomalies in mice overexpressing wild-type human alpha-synuclein. J. Neurosci., 24, 9434-9440.
40. Song, L., Fassler, R., Mishina, Y., Jiao, K. and Baldwin, H.S. (2007) Essential functions of Alk3 during AV cushion morphogenesis in mouse embryonic hearts. Dev. Biol., 301, 276-286.
41. Zhang, Y., Gao, J., Chung, K.K., Huang, H., Dawson, V.L. and Dawson, T.M. (2000) Parkin functions as an E2-dependent ubiquitin- protein ligase and promotes the degradation of the synaptic vesicle-associated protein, CDCrel-1. Proc. Natl Acad. Sci. USA., 97, 13354-13359.
42. Schoenfeld, R., Wong, A., Silva, J., Li, M., Itoh, A., Horiuchi, M., Itoh, T., Pleasure, D. and Cortopassi, G. (2010) Oligodendroglial differentiation induces mitochondrial genes and inhibition of mitochondrial function represses oligodendroglial differentiation. Mitochondrion, 10, 143-150.
43. Goydos, J.S. and Gorski, D.H. (2003) Vascular endothelial growth factor C mRNA expression correlates with stage of progression in patients with melanoma. Clin. Cancer Res., 9, 5962-5967.
44. Sims, N.R. and Anderson, M.F. (2008) Isolation of mitochondria from rat brain using Percoll density gradient centrifugation. Nat. Protoc., 3, 1228-1239.
45. Shan, Y., Napoli, E. and Cortopassi, G. (2007) Mitochondrial frataxin interacts with ISD11 of the NFS1/ISCU complex and multiple mitochondrial chaperones. Hum. Mol. Genet., 16, 929-941.