Glucocerebrosidase deficiency accelerates the accumulation of proteinase K-resistant α-synuclein and aggravates neurodegeneration in a Drosophila model of Parkinson’s disease

Human Molecular Genetics

Volumn 24, Issue 23, 2015, Pages 6675-6686

  Suzuki, Mari ^a   Fujikake, Nobuhiro ^a   Takeuchi, Toshihide ^a   Kohyama Koganeya, Ayako ^b   Nakajima, Kazuki ^b   Hirabayashi, Yoshio ^b   Wada, Keiji ^a   Nagai, Yoshitaka ^a  

^a NATIONAL INSTITUTE OF NEUROSCIENCE   (Japan)

^b RIKEN BRAIN SCIENCE INSTITUTE   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; GANGLIOSIDE GM1; GLUCOSYLCERAMIDE; GLYCOSPHINGOLIPID; LIPOSOME; PROTEINASE K; BETA GALACTOSIDASE; DROSOPHILA PROTEIN; GLUCOSYLCERAMIDASE; SNCA PROTEIN, HUMAN;

ANIMAL TISSUE; ARTICLE; ASSAY; CLIMBING ASSAY; CONFORMATIONAL TRANSITION; CONTROLLED STUDY; DISPERSION; DROSOPHILA; GAUCHER DISEASE; GENE KNOCKDOWN; IMMUNOBLOTTING; IMMUNOHISTOCHEMISTRY; LYSOSOME; MALE; NERVE DEGENERATION; NEUROTOXICITY; NONHUMAN; PARKINSON DISEASE; PHENOTYPE; REAL TIME REVERSE TRANSCRIPTION POLYMERASE CHAIN REACTION; RNA INTERFERENCE; RNA ISOLATION; THIN LAYER CHROMATOGRAPHY; ANIMAL; DEFICIENCY; DISEASE MODEL; DROSOPHILA MELANOGASTER; GENE SILENCING; GENETICS; HUMAN; METABOLISM; PARKINSONIAN DISORDERS; PATHOPHYSIOLOGY; PROTEIN FOLDING; PROTEINOSIS;

ALPHA-SYNUCLEIN; ANIMALS; BETA-GALACTOSIDASE; DISEASE MODELS, ANIMAL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENDOPEPTIDASE K; GENE KNOCKDOWN TECHNIQUES; GLUCOSYLCERAMIDASE; GLUCOSYLCERAMIDES; HUMANS; MALE; PARKINSONIAN DISORDERS; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN FOLDING;

EID: 84983539697     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddv372     Document Type: Article

References (54)

1. Hansen, L., Salmon, D., Galasko, D., Masliah, E., Katzman, R., DeTeresa, R., Thal, L., Pay, M.M., Hofstetter, R., Klauber, M. et al. (1990) The Lewy body variant of Alzheimer’s disease: a clinical and pathologic entity. Neurology, 40, 1–8.
2. Trinh, J. and Farrer, M. (2013) Advances in the genetics of Parkinson disease. Nat. Rev. Neurol., 9, 445–454.
3. Satake, W., Nakabayashi, Y., Mizuta, I., Hirota, Y., Ito, C., Kubo, M., Kawaguchi, T., Tsunoda, T., Watanabe, M., Takeda, A. et al. (2009) Genome-wide association study identifies common variants at four loci as genetic risk factors for Parkinson’s disease. Nat. Genet., 41, 1303–1307.
4. Simon-Sanchez, J., Schulte, C., Bras, J.M., Sharma, M., Gibbs, J. R., Berg, D., Paisan-Ruiz, C., Lichtner, P., Scholz, S.W., Hernandez, D.G. et al. (2009) Genome-wide association study reveals genetic risk underlying Parkinson’s disease. Nat. Genet., 41, 1308–1312.
5. Uversky, V.N. (2007) Neuropathology, biochemistry, and biophysics of α-synuclein aggregation. J. Neurochem., 103, 17–37.
6. Sidransky, E., Nalls, M.A., Aasly, J.O., Aharon-Peretz, J., Annesi, G., Barbosa, E.R., Bar-Shira, A., Berg, D., Bras, J., Brice, A. et al. (2009) Multicenter analysis of glucocerebrosidase mutations in Parkinson’s disease. N. Engl. J. Med., 361, 1651–1661.
7. Nalls, M.A., Duran, R., Lopez, G., Kurzawa-Akanbi, M., McKeith, I.G., Chinnery, P.F., Morris, C.M., Theuns, J., Crosiers, D., Cras, P. et al. (2013) A multicenter study of glucocerebrosidase mutations in dementia with Lewy bodies. JAMA Neurol., 70, 727–735.
8. Bultron, G., Kacena, K., Pearson, D., Boxer, M., Yang, R., Sathe, S., Pastores, G. and Mistry, P.K. (2010) The risk of Parkinson’s disease in type 1 Gaucher disease. J. Inherit. Metab. Dis., 33, 167–173.
9. Tayebi, N., Walker, J., Stubblefield, B., Orvisky, E., LaMarca, M. E., Wong, K., Rosenbaum, H., Schiffmann, R., Bembi, B. and Sidransky, E. (2003) Gaucher disease with parkinsonian manifestations: does glucocerebrosidase deficiency contribute to a vulnerability to parkinsonism? Mol. Genet. Metab., 79, 104–109.
10. Neumann, J., Bras, J., Deas, E., O’Sullivan, S.S., Parkkinen, L., Lachmann, R.H., Li, A., Holton, J., Guerreiro, R., Paudel, R. et al. (2009) Glucocerebrosidase mutations in clinical and pathologically proven Parkinson’s disease. Brain, 132, 1783–1794.
11. Perry, E.K., Haroutunian, V., Davis, K.L., Levy, R., Lantos, P., Eagger, S., Honavar, M., Dean, A., Griffiths, M., McKeith, I.G. et al. (1994) Neocortical cholinergic activities differentiate Lewy body dementia from classical Alzheimer’s disease. Neuroreport, 5, 747–749.
12. Auluck, P.K., Chan, H.Y., Trojanowski, J.Q., Lee, V.M. and Bonini, N.M. (2002) Chaperone suppression of α-synuclein toxicity in a Drosophila model for Parkinson’s disease. Science, 295, 865–868.
13. Cuervo, A.M., Stefanis, L., Fredenburg, R., Lansbury, P.T. and Sulzer, D. (2004) Impaired degradation of mutant α-synuclein by chaperone-mediated autophagy. Science, 305, 1292–1295.
14. Vogiatzi, T., Xilouri, M., Vekrellis, K. and Stefanis, L. (2008) Wild type α-synuclein is degraded by chaperone-mediated autophagy and macroautophagy in neuronal cells. J. Biol. Chem., 283, 23542–23556.
15. Mak, S.K., McCormack, A.L., Manning-Bog, A.B., Cuervo, A.M. and Di Monte, D.A. (2010) Lysosomal degradation of α-synuclein in vivo. J. Biol. Chem., 285, 13621–13629.
16. Bousset, L., Pieri, L., Ruiz-Arlandis, G., Gath, J., Jensen, P.H., Habenstein, B., Madiona, K., Olieric, V., Bockmann, A., Meier, B.H. et al. (2013) Structural and functional characterization of two α-synuclein strains. Nat. Commun., 4, 2575.
17. Guo, J.L., Covell, D.J., Daniels, J.P., Iba, M., Stieber, A., Zhang, B., Riddle, D.M., Kwong, L.K., Xu, Y., Trojanowski, J.Q. et al. (2013) Distinct α-synuclein strains differentially promote tau inclusions in neurons. Cell, 154, 103–117.
18. Miake, H., Mizusawa, H., Iwatsubo, T. and Hasegawa, M. (2002) Biochemical characterization of the core structure of α-synuclein filaments. J. Biol. Chem., 277, 19213–19219.
19. Neumann, M., Kahle, P.J., Giasson, B.I., Ozmen, L., Borroni, E., Spooren, W., Muller, V., Odoy, S., Fujiwara, H., Hasegawa, M. et al. (2002) Misfolded proteinase K-resistant hyperphosphorylated α-synuclein in aged transgenic mice with locomotor deterioration and in human α-synucleinopathies. J. Clin. Invest., 110, 1429–1439.
20. Tanji, K., Mori, F., Mimura, J., Itoh, K., Kakita, A., Takahashi, H. and Wakabayashi, K. (2010) Proteinase K-resistant α-synuclein is deposited in presynapses in human Lewy body disease and A53T α-synuclein transgenic mice. Acta Neuropathol., 120, 145–154.
21. Chen, L. and Feany, M.B. (2005) Alpha-synuclein phosphorylation controls neurotoxicity and inclusion formation in a Drosophila model of Parkinson disease. Nat. Neurosci., 8, 657–663.
22. Suzuki, K., Iseki, E., Togo, T., Yamaguchi, A., Katsuse, O., Katsuyama, K., Kanzaki, S., Shiozaki, K., Kawanishi, C., Yamashita, S. et al. (2007) Neuronal and glial accumulation of α- and β-synucleins in human lipidoses. Acta Neuropathol., 114, 481–489.
23. Hamano, K., Hayashi, M., Shioda, K., Fukatsu, R. and Mizutani, S. (2008) Mechanisms of neurodegeneration in mucopolysaccharidoses II and IIIB: analysis of human brain tissue. Acta Neuropathol., 115, 547–559.
24. Tayebi, N., Callahan, M., Madike, V., Stubblefield, B.K., Orvisky, E., Krasnewich, D., Fillano, J.J. and Sidransky, E. (2001) Gaucher disease and parkinsonism: a phenotypic and genotypic characterization. Mol. Genet. Metab., 73, 313–321.
25. Schöndorf, D.C., Aureli, M., McAllister, F.E., Hindley, C.J., Mayer, F., Schmid, B., Sardi, S.P., Valsecchi, M., Hoffmann, S., Schwarz, L.K. et al. (2014) iPSC-derived neurons from GBA1-associated Parkinson’s disease patients show autophagic defects and impaired calcium homeostasis. Nat. Commun., 5, 4028.
26. Cremades, N., Cohen, S.I., Deas, E., Abramov, A.Y., Chen, A.Y., Orte, A., Sandal, M., Clarke, R.W., Dunne, P., Aprile, F.A. et al. (2012) Direct observation of the interconversion of normal and toxic forms of α-synuclein. Cell, 149, 1048–1059.
27. Manning-Bog, A.B., Schule, B. and Langston, J.W. (2009) Alpha-synuclein-glucocerebrosidase interactions in pharmacological Gaucher models: a biological link between Gaucher disease and parkinsonism. Neurotoxicology, 30, 1127–1132.
28. Mazzulli, J.R., Xu, Y.H., Sun, Y., Knight, A.L., McLean, P.J., Caldwell, G.A., Sidransky, E., Grabowski, G.A. and Krainc, D. (2011) Gaucher disease glucocerebrosidase and α-synuclein form a bidirectional pathogenic loop in synucleinopathies. Cell, 146, 37–52.
29. Dermentzaki, G., Dimitriou, E., Xilouri, M., Michelakakis, H. and Stefanis, L. (2013) Loss of β-glucocerebrosidase activity does not affect α-synuclein levels or lysosomal function in neuronal cells. PLoS ONE, 8, e60674.
30. Cullen, V., Sardi, S.P., Ng, J., Xu, Y.H., Sun, Y., Tomlinson, J.J., Kolodziej, P., Kahn, I., Saftig, P., Woulfe, J. et al. (2011) Acid βglucosidase mutants linked to Gaucher disease, Parkinson disease, and Lewy body dementia alter α-synuclein processing. Ann. Neurol., 69, 940–953.
31. Fishbein, I., Kuo, Y.M., Giasson, B.I. and Nussbaum, R.L. (2014) Augmentation of phenotype in a transgenic Parkinson mouse heterozygous for a Gaucher mutation. Brain, 137, 3235–3247.
32. Argyriou, A., Dermentzaki, G., Papasilekas, T., Moraitou, M., Stamboulis, E., Vekrellis, K., Michelakakis, H. and Stefanis, L. (2012) Increased dimerization of α-synuclein in erythrocytes in Gaucher disease and aging. Neurosci. Lett., 528, 205–209.
33. Martinez, Z., Zhu, M., Han, S. and Fink, A.L. (2007) GM1 specifically interacts with α-synuclein and inhibits fibrillation. Biochemistry, 46, 1868–1877.
34. Yanagisawa, K., Odaka, A., Suzuki, N. and Ihara, Y. (1995) GM1 ganglioside-bound amyloid β-protein (Aβ): a possible form of preamyloid in Alzheimer’s disease. Nat. Med., 1, 1062–1066.
35. Desplats, P., Lee, H.J., Bae, E.J., Patrick, C., Rockenstein, E., Crews, L., Spencer, B., Masliah, E. and Lee, S.J. (2009) Inclusion formation and neuronal cell death through neuron-to-neuron transmission of α-synuclein. Proc. Natl Acad. Sci. USA, 106, 13010–13015.
36. Luk, K.C., Kehm, V., Carroll, J., Zhang, B., O’Brien, P., Trojanowski, J.Q. and Lee, V.M. (2012) Pathological α-synuclein transmission initiates Parkinson-like neurodegeneration in nontransgenic mice. Science, 338, 949–953.
37. Nilsson, O. and Svennerholm, L. (1982) Accumulation of glucosylceramide and glucosylsphingosine (psychosine) in cerebrum and cerebellum in infantile and juvenile Gaucher disease. J. Neurochem., 39, 709–718.
38. Farfel-Becker, T., Vitner, E.B., Kelly, S.L., Bame, J.R., Duan, J., Shinder, V., Merrill, A.H. Jr, Dobrenis, K. and Futerman, A.H. (2014) Neuronal accumulation of glucosylceramide in a mouse model of neuronopathic Gaucher disease leads to neurodegeneration. Hum. Mol. Genet., 23, 843–854.
39. Daniels, L., Coyie, P., Glew, R., Radin, N. and Labow, R. (1982) Brain glucocerebrosidase in Gaucher’s disease. Arch. Neurol., 39, 550–556.
40. Svennerholm, L., Mansson, J. and Rosengren, B. (1986) Cerebroside-β-glucosidase activity in Gaucher brain. Clin. Genet., 30, 131–135.
41. Gegg, M.E., Burke, D., Heales, S.J., Cooper, J.M., Hardy, J., Wood, N.W. and Schapira, A.H. (2012) Glucocerebrosidase deficiency in substantia nigra of parkinson disease brains. Ann. Neurol., 72, 455–463.
42. Kurzawa-Akanbi, M., Hanson, P.S., Blain, P.G., Lett, D.J., McKeith, I.G., Chinnery, P.F. and Morris, C.M. (2012) Glucocerebrosidase mutations alter the endoplasmic reticulum and lysosomes in Lewy body disease. J. Neurochem., 123, 298–309.
43. Maor, G., Rencus-Lazar, S., Filocamo, M., Steller, H., Segal, D. and Horowitz, M. (2013) Unfolded protein response in Gaucher disease: from human to Drosophila. Orphanet J. Rare Dis., 8, 140.
44. Suzuki, T., Shimoda, M., Ito, K., Hanai, S., Aizawa, H., Kato, T., Kawasaki, K., Yamaguchi, T., Ryoo, H.D., Goto-Inoue, N. et al. (2013) Expression of human Gaucher disease gene GBA generates neurodevelopmental defects and ER stress in Drosophila eye. PLoS ONE, 8, e69147.
45. Bendikov-Bar, I., Maor, G., Filocamo, M. and Horowitz, M. (2013) Ambroxol as a pharmacological chaperone for mutant glucocerebrosidase. Blood Cells Mol. Dis., 50, 141–145.
46. Colla, E., Coune, P., Liu, Y., Pletnikova, O., Troncoso, J.C., Iwatsubo, T., Schneider, B.L. and Lee, M.K. (2012) Endoplasmic reticulum stress is important for the manifestations of αsynucleinopathy in vivo. J. Neurosci., 32, 3306–3320.
47. Colla, E., Jensen, P.H., Pletnikova, O., Troncoso, J.C., Glabe, C. and Lee, M.K. (2012) Accumulation of toxic α-synuclein oligomer within endoplasmic reticulum occurs in α-synucleinopathy in vivo. J. Neurosci., 32, 3301–3305.
48. Bellucci, A., Navarria, L., Zaltieri, M., Falarti, E., Bodei, S., Sigala, S., Battistin, L., Spillantini, M., Missale, C. and Spano, P. (2011) Induction of the unfolded protein response by α-synuclein in experimental models of Parkinson’s disease. J. Neurochem., 116, 588–605.
49. Yamaguchi, M., Hirose, F., Inoue, Y.H., Shiraki, M., Hayashi, Y., Nishi, Y. and Matsukage, A. (1999) Ectopic expression of human p53 inhibits entry into S phase and induces apoptosis in the Drosophila eye imaginal disc. Oncogene, 18, 6767–6775.
50. Suzuki, M., Setsuie, R. and Wada, K. (2009) Ubiquitin carboxylterminal hydrolase l3 promotes insulin signaling and adipogenesis. Endocrinology, 150, 5230–5239.
51. Feany, M.B. and Bender, W.W. (2000) A Drosophila model of Parkinson’s disease. Nature, 404, 394–398.
52. Lee, B.R. and Kamitani, T. (2011) Improved immunodetection of endogenous α-synuclein. PLoS ONE, 6, e23939.
53. Nakajima, K., Kohyama-Koganeya, A. and Hirabayashi, Y. (2014) Profiling of glucosylceramides by liquid chromatography–tandem mass spectrometry. In Taniguchi, N., Endo, T., Hart, G.W., Seeberger, P.H. and Wong, C.-H. (eds), Glycoscience: Biology and Medicine, Springer Japan, Tokyo, Japan, pp. 1–7.
54. Kohyama-Koganeya, A., Nabetani, T., Miura, M. and Hirabayashi, Y. (2011) Glucosylceramide synthase in the fat body controls energy metabolism in Drosophila. J. Lipid Res., 52, 1392–1399.