A Caenorhabditis elegans Parkin mutant with altered solubility couples α-synuclein aggregation to proteotoxic stress

Human Molecular Genetics

Volumn 14, Issue 22, 2005, Pages 3407-3423

  Springer, Wolfdieter ^a   Hoppe, Thorsten ^a   Schmidt, Enrico ^b   Baumeister, Ralf ^a,b  

^a UNIVERSITY OF MUNICH   (Germany)

^b UNIVERSITY OF FREIBURG   (Germany)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; MUTANT PROTEIN; UBIQUITIN PROTEIN LIGASE E3;

ARTICLE; AUTOSOMAL RECESSIVE DISORDER; CAENORHABDITIS ELEGANS; CELL CULTURE; CELLULAR DISTRIBUTION; CONJUGATION; CONTROLLED STUDY; CYTOSOL; DETOXIFICATION; DEVELOPMENTAL DISORDER; ENDOPLASMIC RETICULUM; GENE DELETION; GENE FUNCTION; GENE MUTATION; IN VIVO STUDY; KNOCKOUT GENE; LETHALITY; NONHUMAN; PARKINSON DISEASE; PARKINSONISM; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DEGRADATION; PROTEIN FOLDING; RNA INTERFERENCE; SEQUENCE HOMOLOGY; SOLUBILITY; STRESS;

ALPHA-SYNUCLEIN; AMINO ACID SEQUENCE; ANIMALS; CAENORHABDITIS ELEGANS PROTEINS; ENDOPLASMIC RETICULUM; LOSS OF HETEROZYGOSITY; MOLECULAR SEQUENCE DATA; OXIDATIVE STRESS; SEQUENCE DELETION; SOLUBILITY; UBIQUITIN; UBIQUITIN-PROTEIN LIGASES;

CAENORHABDITIS ELEGANS;

EID: 27944506923     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddi371     Document Type: Article

References (64)

1. Riess, O., Berg, D., Kruger, R. and Schulz, J.B. (2003) Therapeutic strategies for Parkinson's disease based on data derived from genetic research. J. Neurol., 250 (Suppl. 1), I3-I10.
2. Lykkebo, S. and Jensen, P.H. (2002) Alpha-synuclein and presynaptic function: Implications for Parkinson's disease. Neuromol. Med., 2, 115-129.
3. Polymeropoulos, M.H., Lavedan, C., Leroy, E., Ide, S.E., Dehejia, A., Dutra, A., Pike, B., Root, H., Rubenstein, J., Boyer, R. et al. (1997) Mutation in the α-synuclein gene identified in families with Parkinson's disease. Science, 276, 2045-2047.
4. Kruger, R., Kuhn, W., Muller, T., Woitalla, D., Graeber, M., Kosel, S., Przuntek, H., Epplen, J.T., Schols, L. and Riess, O. (1998) Ala30Pro mutation in the gene encoding α-synuclein in Parkinson's disease. Nat. Genet., 18, 106-108.
5. Zarranz, J.J., Alegre, J., Gomez-Esteban, J.C., Lezcano, E., Ros, R., Ampuero, I., Vidal, L., Hoenicka, J., Rodriguez, O., Atares, B. et al. (2004) The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann. Neurol., 55, 164-173.
6. Chartier-Harlin, M.C., Kachergus, J., Roumier, C., Mouroux, V., Douay, X., Lincoln, S., Levecque, C., Larvor, L., Andrieux, J., Hulihan, M. et al. (2004) α-Synuclein locus duplication as a cause of familial Parkinson's disease. Lancet, 364, 1167-1169.
7. Singleton, A.B., Farrer, M., Johnson, J., Singleton, A., Hague, S., Kachergus, J., Hulihan, M., Peuralinna, T., Dutra, A., Nussbaum, R. et al. (2003) α-Synuclein locus triplication causes Parkinson's disease. Science, 302, 841.
8. Ibanez, P., Bonnet, A.M., Debarges, B., Lohmann, E., Tison, F., Pollak, P., Agid, Y., Durr, A. and Brice, A. (2004) Causal relation between α-synuclein gene duplication and familial Parkinson's disease. Lancet, 364, 1169-1171.
9. Maries, E., Dass, B., Collier, T.J., Kordower, J.H. and Steece-Collier, K. (2003) The role of α-synuclein in Parkinson's disease: Insights from animal models. Nat. Rev. Neurosci., 4, 727-738.
10. Lakso, M., Vartiainen, S., Moilanen, A.M., Sirvio, J., Thomas, J.H., Nass, R., Blakely, R.D. and Wong, G. (2003) Dopaminergic neuronal loss and motor deficits in Caenorhabditis elegans overexpressing human alpha-synuclein. J. Neurochem., 86, 165-172.
11. Kitada, T., Asakawa, S., Hattori, N., Matsumine, H., Yamamura, Y., Minoshima, S., Yokochi, M., Mizuno, Y. and Shimizu, N. (1998) Mutations in the Parkin gene cause autosomal recessive juvenile Parkinsonism. Nature, 392, 605-608.
12. Sakata, E., Yamaguchi, Y., Kurimoto, E., Kikuchi, J., Yokoyama, S., Yamada, S., Kawahara, H., Yokosawa, H., Hattori, N., Mizuno, Y. et al. (2003) Parkin binds the Rpn10 subunit of 26S proteasomes through its ubiquitin-like domain. EMBO Rep., 4, 301-306.
13. Shimura, H., Schlossmacher, M.G., Hattori, N., Frosch, M.P., Trockenbacher, A., Schneider, R., Mizuno, Y., Kosik, K.S. and Selkoe, D.J. (2001) Ubiquitination of a new form of alpha-synuclein by parkin from human brain: Implications for Parkinson's disease. Science, 293, 263-269.
14. Finney, N., Walther, F., Mantel, P.Y., Stauffer, D., Rovelli, G. and Dev, K.K. (2003) The cellular protein level of parkin is regulated by its ubiquitin-like domain. J. Biol. Chem., 278, 16054-16058.
15. Shimura, H., Hattori, N., Kubo, S., Mizuno, Y., Asakawa, S., Minoshima, S., Shimizu, N., Iwai, K., Chiba, T., Tanaka, K. et al. (2000) Familial Parkinson disease gene product, parkin, is a ubiquitin-protein ligase. Nat. Genet., 25, 302-305.
16. Pickart, C.M. (2001) Mechanisms underlying ubiquitination. Annu. Rev. Biochem., 70, 503-533.
17. Imai, Y., Soda, M. and Takahashi, R. (2000) Parkin suppresses unfolded protein stress-induced cell death through its E3 ubiquitin-protein ligase activity. J. Biol. Chem., 275, 35661-35664.
18. Rutkowski, D.T. and Kaufman, R.J. (2004) A trip to the ER: Coping with stress. Trends Cell Biol., 14, 20-28.
19. Kostova, Z. and Wolf, D.H. (2003) For whom the bell tolls: Protein quality control of the endoplasmic reticulum and the ubiquitin-proteasome connection. EMBO J., 22, 2309-2317.
20. Friedlander, R., Jarosch, E., Urban, J., Volkwein, C. and Sommer, T. (2000) A regulatory link between ER-associated protein degradation and the unfolded-protein response. Nat. Cell Biol., 2, 379-384.
21. Travers, K.J., Patil, C.K., Wodicka, L., Lockhart, D.J., Weissman, J.S. and Walter, P. (2000) Functional and genomic analyses reveal an essential coordination between the unfolded protein response and ER-associated degradation. Cell, 101, 249-258.
22. Imai, Y., Soda, M., Hatakeyama, S., Akagi, T., Hashikawa, T., Nakayama, K.I. and Takahashi, R. (2002) CHIP is associated with Parkin, a gene responsible for familial Parkinson's disease, and enhances its ubiquitin ligase activity. Mol. Cell, 10, 55-67.
23. Kahle, P.J. and Haass, C. (2004) How does parkin ligate ubiquitin to Parkinson's disease? EMBO Rep., 5, 681-685.
24. Petrucelli, L., O'Farrell, C., Lockhart, P.J., Baptista, M., Kehoe, K., Vink, L., Choi, P., Wolozin, B., Farrer, M., Hardy, J. et al. (2002) Parkin protects against the toxicity associated with mutant α-synuclein: Proteasome dysfunction selectively affects catecholaminergic neurons. Neuron, 36, 1007-1019.
25. Yang, Y., Nishimura, I., Imai, Y., Takahashi, R. and Lu, B. (2003) Parkin suppresses dopaminergic neuron-selective neurotoxicity induced by Pael-R in Drosophila. Neuron, 37, 911-924.
26. Mata, I.F., Lockhart, P.J. and Farrer, M.J. (2004) Parkin genetics: One model for Parkinson's disease. Hum. Mol. Genet, 13, R127-R133.
27. Sriram, S.R., Li, X., Ko, H.S., Chung, K.K., Wong, E., Lim, K.L., Dawson, V.L. and Dawson, T.M. (2005) Familial-associated mutations differentially disrupt the solubility, localization, binding and ubiquitination properties of Parkin. Hum. Mol. Genet., in press.
28. Imai, Y., Soda, M., Inoue, H., Hattori, N., Mizuno, Y. and Takahashi, R. (2001) An unfolded putative transmembrane polypeptide, which can lead to endoplasmic reticulum stress, is a substrate of Parkin. Cell, 105, 891-902.
29. Chung, K.K., Zhang, Y., Lim, K.L., Tanaka, Y., Huang, H., Gao, J., Ross, C.A., Dawson, V.L. and Dawson, T.M. (2001) Parkin ubiquitinates the alpha-synuclein-interacting protein, synphilin-1: Implications for Lewy-body formation in Parkinson disease. Nat. Med., 7, 1144-1150.
30. Corti, O., Hampe, C., Koutnikova, H., Darios, F., Jacquier, S., Prigent, A., Robinson, J.C., Pradier, L., Ruberg, M., Mirande, M. et al. (2003) The p38 subunit of the aminoacyl-tRNA synthetase complex is a Parkin substrate: Linking protein biosynthesis and neurodegeneration. Hum. Mol. Genet., 12, 1427-1437.
31. Hyun, D.H., Lee, M., Hattori, N., Kubo, S., Mizuno, Y., Halliwell, B. and Jenner, P. (2002) Effect of wild-type or mutant Parkin on oxidative damage, nitric oxide, antioxidant defenses, and the proteasome. J. Biol. Chem., 277, 28572-28577.
32. Gu, W.J., Corti, O., Araujo, F., Hampe, C., Jacquier, S., Lucking, C.B., Abbas, N., Duyckaerts, C., Rooney, T., Pradier, L. et al. (2003) The C289G and C418R missense mutations cause rapid sequestration of human Parkin into insoluble aggregates. Neurobiol. Dis., 14, 357-364.
33. Winklhofer, K.F., Henn, I.H., Kay-Jackson, P.C., Heller, U. and Tatzelt, J. (2003) Inactivation of Parkin by oxidative stress and C-terminal truncations: A protective role of molecular chaperones. J. Biol. Chem., 278, 47199-47208.
34. Henn, I.H., Gostner, J.M., Lackner, P., Tatzelt, J. and Winklhofer, K.F. (2005) Pathogenic mutations inactivate Parkin by distinct mechanisms. J. Neurochem., 92, 114-122.
35. Jones, D., Crowe, E., Stevens, T.A. and Candido, E.P. (2002) Functional and phylogenetic analysis of the ubiquitylation system in Caenorhabditis elegans: Ubiquitin-conjugating enzymes, ubiquitin-activating enzymes, and ubiquitin-like proteins. Genome Biol., 3, RESEARCH0002.1-0002.15
36. Hoppe, T., Cassata, G., Barral, J.M., Springer, W., Hutagalung, A.H., Epstein, H.F. and Baumeister, R. (2004) Regulation of the myosin-directed chaperone UNC-45 by a novel E3/E4-multiubiquitylation complex in C. elegans. Cell, 118, 337-349.
37. Hoppe, T. (2005) Multiubiquitylation by E4 enzymes: 'one size' doesn't fit all. Trends Biochem. Sci., 30, 183-187.
38. Lorick, K.L., Jensen, J.P., Fang, S., Ong, A.M., Hatakeyama, S. and Weissman, A.M. (1999) RING fingers mediate ubiquitin-conjugating enzyme (E2)-dependent ubiquitination. Proc. Natl Acad. Sci. USA, 96, 11364-11369.
39. Cookson, M.R., Lockhart, P.J., McLendon, C., O'Farrell, C., Schlossmacher, M. and Farrer, M.J. (2003) RING finger 1 mutations in Parkin produce altered localization of the protein. Hum. Mol. Genet., 12, 2957-2965.
40. Wang, C., Tan, J.M., Ho, M.W., Zaiden, N., Wong, S.H., Chew, C.L., Eng, P.W., Lim, T.M., Dawson, T.M. and Lim, K.L. (2005) Alterations in the solubility and intracellular localization of Parkin by several familial Parkinson's disease-linked point mutations. J. Neurochem., 93, 422-431.
41. Nass, R., Hall, D.H., Miller, D.M., III and Blakely, R.D. (2002) Neurotoxin-induced degeneration of dopamine neurons in Caenorhabditis elegans. Proc. Natl Acad. Sci. USA, 99, 3264-3269.
42. Shen, X., Ellis, R.E., Lee, K., Liu, C.Y., Yang, K., Solomon, A., Yoshida, H., Morimoto, R., Kurnit, D.M., Mori, K. et al. (2001) Complementary signaling pathways regulate the unfolded protein response and are required for C. elegans development. Cell, 107, 893-903.
43. Calfon, M., Zeng, H., Urano, F., Till, J.H., Hubbard, S.R., Harding, H.P., Clark, S.G. and Ron, D. (2002) IRE1 couples endoplasmic reticulum load to secretory capacity by processing the XBP-1 mRNA. Nature, 415, 92-96.
44. Urano, F., Calfon, M., Yoneda, T., Yun, C., Kiraly, M., Clark, S.G. and Ron, D. (2002) A survival pathway for Caenorhabditis elegans with a blocked unfolded protein response. J. Cell. Biol., 158, 639-646.
45. Cao, S., Gelwix, C.C., Caldwell, K.A. and Caldwell, G.A. (2005) Torsin-mediated protection from cellular stress in the dopaminergic neurons of Caenorhabditis elegans. J. Neurosci., 25, 3801-3812.
46. 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.
47. Palacino, J.J., Sagi, D., Goldberg, M.S., Krauss, S., Motz, C., Wacker, M., Klose, J. and Shen, J. (2004) Mitochondrial dysfunction and oxidative damage in Parkin-deficient mice. J. Biol. Chem., 279, 18614- 18622.
48. Goldberg, M.S., Fleming, S.M., Palacino, J.J., Cepeda, C., Lam, H.A., Bhatnagar, A., Meloni, E.G., Wu, N., Ackerson, L.C., Klapstein, G.J. et al. (2003) Parkin-deficient mice exhibit nigrostriatal deficits but not loss of dopaminergic neurons. J. Biol. Chem., 278, 43628-43635.
49. Lorenzetti, D., Antalffy, B., Vogel, H., Noveroske, J., Armstrong, D. and Justice, M. (2004) The neurological mutant quaking (viable) is Parkin deficient. Mamm. Genome, 15, 210-217.
50. Lim, K.L., Chew, K.C., Tan, J.M., Wang, C., Chung, K.K., Zhang, Y., Tanaka, Y., Smith, W., Engelender, S., Ross, C.A. et al. (2005) Parkin mediates nonclassical, proteasomal-independent ubiquitination of synphilin-1: Implications for Lewy body formation. J. Neurosci., 25, 2002-2009.
51. Liani, E., Eyal, A., Avraham, E., Shemer, R., Szargel, R., Berg, D., Bornemann, A., Riess, O., Ross, C.A., Rott, R. et al. (2004) Ubiquitylation of synphilin-1 and alpha-synuclein by SIAH and its presence in cellular inclusions and Lewy bodies imply a role in Parkinson's disease. Proc. Natl Acad. Sci. USA, 101, 5500-5505.
52. Nagano, Y., Yamashita, H., Takahashi, T., Kishida, S., Nakamura, T., Iseki, E., Hattori, N., Mizuno, Y., Kikuchi, A. and Matsumoto, M. (2003) Siah-1 facilitates ubiquitination and degradation of synphilin-1. J. Biol. Chem., 278, 51504-51514.
53. Ito, T., Niwa, J., Hishikawa, N., Ishigaki, S., Doyu, M. and Sobue, G. (2003) Dorfin localizes to Lewy bodies and ubiquitylates synphilin-1. J. Biol. Chem., 278, 29106-29114.
54. Sherman, M.Y. and Goldberg, A.L. (2001) Cellular defenses against unfolded proteins: A cell biologist thinks about neurodegenerative diseases. Neuron, 29, 15-32.
55. Forman, M.S., Lee, V.M. and Trojanowski, J.Q. (2003) 'Unfolding' pathways in neurodegenerative disease. Trends Neurosci., 26, 407-410.
56. Ryu, E.J., Harding, H.P., Angelastro, J.M., Vitolo, O.V., Ron, D. and Greene, L.A. (2002) Endoplasmic reticulum stress and the unfolded protein response in cellular models of Parkinson's disease. J. Neurosci., 22, 10690-10698.
57. Braungart, E., Gerlach, M., Riederer, P., Baumeister, R. and Höner, M. (2004) Caenorhabditis elegans MPP+ model of Parkinson's disease for high-throughput drug screenings. Neurodegenerative Dis., 1, 175-183.
58. Eriksen, J.L., Dawson, T.M., Dickson, D.W. and Petrucelli, L. (2003) Caught in the act: α-synuclein is the culprit in Parkinson's disease. Neuron, 40, 453-456.
59. Giasson, B.I., Duda, J.E., Quinn, S.M., Zhang, B., Trojanowski, J.Q. and Lee, V.M. (2002) Neuronal alpha-synucleinopathy with severe movement disorder in mice expressing A53T human alpha-synuclein. Neuron, 34, 521-533.
60. Greene, J.C., Whitworth, A.J., Kuo, I., Andrews, L.A., Feany, M.B. and Pallanck, L.J. (2003) Mitochondrial pathology and apoptotic muscle degeneration in Drosophila parkin mutants. Proc. Natl Acad. Sci. USA, 100, 4078-4083.
61. Pesah, Y., Pham, T., Burgess, H., Middlebrooks, B., Verstreken, P., Zhou, Y., Harding, M., Bellen, H. and Mardon, G. (2004) Drosophila parkin mutants have decreased mass and cell size and increased sensitivity to oxygen radical stress. Development, 131, 2183-2194.
62. Itier, J.M., Ibanez, P., Mena, M.A., Abbas, N., Cohen-Salmon, C., Bohme, G.A., Laville, M., Pratt, J., Corti, O., Pradier, L. et al. (2003) Parkin gene inactivation alters behaviour and dopamine neurotransmission in the mouse. Hum. Mol. Genet., 12, 2277-2291.
63. Von Coelln, R., Thomas, B., Savitt, J.M., Lim, K.L., Sasaki, M., Hess, E.J., Dawson, V.L. and Dawson, T.M. (2004) Loss of locus coeruleus neurons and reduced startle in parkin null mice. Proc. Natl Acad. Sci. USA, 101, 10744-10749.
64. Brenner, S. (1974) The genetics of Caenorhabditis elegans. Genetics, 77, 71-94.