Loss of glucocerebrosidase 1 activity causes lysosomal dysfunction and α-synuclein aggregation

Experimental and Molecular Medicine

Volumn 47, Issue 3, 2015, Pages

  Bae, Eun Jin ^a,b   Yang, Na Young ^a,b,f   Lee, Cheolsoon ^b,c   Lee, He Jin ^b,c   Kim, Seokjoong ^d   Sardi, Sergio Pablo ^e   Lee, Seung Jae ^a,b  

^a Konkuk University   (South Korea)

^b Konkuk University   (South Korea)

^c Konkuk University School of Medicine   (South Korea)

^d Seoul National University   (South Korea)

^e Genzyme   (United States)

^f NONE   (South Korea)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; DEXTRAN; GLUCOSYLCERAMIDASE; GLUCOSYLCERAMIDASE 1; UNCLASSIFIED DRUG; ZINC FINGER NUCLEASE; PROTEIN BINDING; ZINC FINGER PROTEIN;

ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL FUNCTION; CELL VACUOLE; ENZYME ACTIVITY; ENZYME MODIFICATION; GBA1 GENE; GENE; HUMAN; HUMAN CELL; LYSOSOMAL DYSFUNCTION; LYSOSOME; NEUROBLASTOMA CELL LINE; NONSENSE MUTATION; PROTEIN AGGREGATION; PROTEIN EXPRESSION; SH SY5Y CELL LINE; CELL LINE; CHEMISTRY; ENZYME ACTIVATION; GENE INACTIVATION; GENE LOCUS; GENE ORDER; GENETICS; METABOLISM; MUTATION; PROTEINOSIS;

ALPHA-SYNUCLEIN; CELL LINE; ENZYME ACTIVATION; GENE KNOCKOUT TECHNIQUES; GENE ORDER; GENETIC LOCI; GLUCOSYLCERAMIDASE; HUMANS; LYSOSOMES; MUTATION; PROTEIN AGGREGATION, PATHOLOGICAL; PROTEIN BINDING; ZINC FINGERS;

EID: 84965185844     PISSN: 12263613     EISSN: 20926413     Source Type: Journal    
DOI: 10.1038/emm.2014.128     Document Type: Article

References (42)

1. Hoehn MM, Yahr MD. Parkinsonism: onset, progression and mortality. Neurology 1967; 17: 427-442.
2. Dauer W, Przedborski S. Parkinson's disease: mechanisms and models. Neuron 2003; 39: 889-909.
3. Bahr BA, Bendiske J. The neuropathogenic contributions of lysosomal dysfunction. J Neurochem 2002; 83: 481-489.
4. Trinh J, Farrer M. Advances in the genetics of Parkinson disease. Nat Rev Neurol 2013; 9: 445-454.
5. Pankratz N, Wilk JB, Latourelle JC, DeStefano AL, Halter C, Pugh EW et al. Genomewide association study for susceptibility genes contributing to familial Parkinson disease. Hum Genet 2009; 124: 593-605.
6. Satake W, Nakabayashi Y, Mizuta I, Hirota Y, Ito C, Kubo M et al. Genome-wide association study identifies common variants at four loci as genetic risk factors for Parkinson's disease. Nat Genet 2009; 41: 1303-1307.
7. Simon-Sanchez J, Schulte C, Bras JM, Sharma M, Gibbs JR, Berg D et al. Genome-wide association study reveals genetic risk underlying Parkinson's disease. Nat Genet 2009; 41: 1308-1312.
8. Edwards TL, Scott WK, Almonte C, Burt A, Powell EH, Beecham GW et al. Genome-wide association study confirms SNPs in SNCA and the MAPT region as common risk factors for Parkinson disease. Ann Hum Genet 2010; 74: 97-109.
9. Daher JP, Pletnikova O, Biskup S, Musso A, Gellhaar S, Galter D et al. Neurodegenerative phenotypes in an A53T alpha-synuclein transgenic mouse model are independent of LRRK2. Hum Mol Genet 2012; 21: 2420-2431.
10. Brady RO, Kanfer J, Shapiro D. The metabolism of glucocerebrosides. I. purification and properties of a glucocerebroside-cleaving enzyme from spleen tissue. J Biol Chem 1965; 240: 39-43.
11. Hruska KS, LaMarca ME, Scott CR, Sidransky E. Gaucher disease: mutation and polymorphism spectrum in the glucocerebrosidase gene (GBA). Hum Mutat 2008; 29: 567-583.
12. Yang NY, Lee YN, Lee HJ, Kim YS, Lee SJ. Glucocerebrosidase, a new player changing the old rules in Lewy body diseases. Biol Chem 2013; 394: 807-818.
13. Sidransky E, Nalls MA, Aasly JO, Aharon-Peretz J, Annesi G, Barbosa ER et al. Multicenter analysis of glucocerebrosidase mutations in Parkinson's disease. N Engl J Med 2009; 361: 1651-1661.
14. Rosenbloom B, Balwani M, Bronstein JM, Kolodny E, Sathe S, Gwosdow AR et al. The incidence of Parkinsonism in patients with type 1 Gaucher disease: data from the ICGG Gaucher Registry. Blood Cells Mol Dis 2011; 46: 95-102.
15. Goker-Alpan O, Stubblefield BK, Giasson BI, Sidransky E. Glucocerebrosi-dase is present in alpha-synuclein inclusions in Lewy body disorders. Acta Neuropathol 2010; 120: 641-649.
16. Clark LN, Kartsaklis LA, Wolf Gilbert R, Dorado B, Ross BM, Kisselev S et al. Association of glucocerebrosidase mutations with dementia with lewy bodies. Arch Neurol 2009; 66: 578-583.
17. Lee HJ, Bae EJ, Jang A, Ho DH, Cho ED, Suk JE et al. Enzyme-linked immunosorbent assays for alpha-synuclein with species and multimeric state specificities. J Neurosci Methods 2011; 199: 249-257.
18. Lee H-J, Khoshaghideh F, Patel S, Lee S-J. Clearance of alpha-synuclein oligomeric intermediates via the lysosomal degradation pathway. J Neurosci 2004; 24: 1888-1896.
19. Sardi SP, Clarke J, Kinnecom C, Tamsett TJ, Li L, Stanek LM et al. CNS expression of glucocerebrosidase corrects alpha-synuclein pathology and memory in a mouse model of Gaucher-related synucleinopathy. Proc Natl Acad Sci USA 2011; 108: 12101-12106.
20. Lee H-J, Shin SY, Choi C, Lee YH, Lee S-J. Formation and removal of alpha-synuclein aggregates in cells exposed to mitochondrial inhibitors. J Biol Chem 2002; 277: 5411-5417.
21. Atrian S, Lopez-Vinas E, Gomez-Puertas P, Chabas A, Vilageliu L, Grinberg D. An evolutionary and structure-based docking model for glucocerebrosidase-saposin C and glucocerebrosidase-substrate interactions - relevance for Gaucher disease. Proteins 2008; 70: 882-891.
22. Lieberman RL. A guided tour of the structural biology of gaucher disease: acid-beta-glucosidase and saposin C. Enzyme Res 2011; 2011: 973231.
23. Cabrera-Salazar MA, Bercury SD, Ziegler RJ, Marshall J, Hodges BL, Chuang WL et al. Intracerebroventricular delivery of glucocerebrosidase reduces substrates and increases lifespan in a mouse model of neurono-pathic Gaucher disease. Exp Neurol 2010; 225: 436-444.
24. Butler D, Nixon RA, Bahr BA. Potential compensatory responses through autophagic/lysosomal pathways in neurodegenerative diseases. Autophagy 2006; 2: 234-237.
25. Meikle PJ, Brooks DA, Ravenscroft EM, Yan M, Williams RE, Jaunzems AE et al. Diagnosis of lysosomal storage disorders: evaluation of lysosome-associated membrane protein LAMP-1 as a diagnostic marker. Clin Chem 1997; 43: 1325-1335.
26. Webb JL, Ravikumar B, Atkins J, Skepper JN, Rubinsztein DC. Alpha-Synuclein is degraded by both autophagy and the proteasome. J Biol Chem 2003; 278: 25009-25013.
27. Cuervo AM, Stefanis L, Fredenburg R, Lansbury PT, Sulzer D. Impaired degradation of mutant alpha-synuclein by chaperone-mediated autophagy. Science 2004; 305: 1292-1295.
28. Lee H-J, Patel S, Lee S-J. Intravesicular localization and exocytosis of alpha-synuclein and its aggregates. J Neurosci 2005; 25: 6016-6024.
29. Jang A, Lee HJ, Suk JE, Jung JW, Kim KP, Lee SJ. Non-classical exocytosis of alpha-synuclein is sensitive to folding states and promoted under stress conditions. J Neurochem 2010; 113: 1263-1274.
30. Lee HJ, Cho ED, Lee KW, Kim JH, Cho SG, Lee SJ. Autophagic failure promotes the exocytosis and intercellular transfer of alpha-synuclein. Exp Mol Med 2013; 45: e22.
31. Mazzulli JR, Xu YH, Sun Y, Knight AL, McLean PJ, Caldwell GA et al. Gaucher disease glucocerebrosidase and alpha-synuclein form a bidirectional pathogenic loop in synucleinopathies. Cell 2011; 146: 37-52.
32. Schondorf DC, Aureli M, McAllister FE, Hindley CJ, Mayer F, Schmid B et al. iPSC-derived neurons from GBA1-associated Parkinson's disease patients show autophagic defects and impaired calcium homeostasis. Nat Commun 2014; 5: 4028.
33. Gegg ME, Burke D, Heales SJ, Cooper JM, Hardy J, Wood NW et al. Glucocerebrosidase deficiency in substantia nigra of parkinson disease brains. Ann Neurol 2012; 72: 455-463.
34. Murphy KE, Gysbers AM, Abbott SK, Tayebi N, Kim WS, Sidransky E et al. Reduced glucocerebrosidase is associated with increased alpha-synuclein in sporadic Parkinson's disease. Brain 2014; 137: 834-848.
35. Orvisky E, Park JK, LaMarca ME, Ginns EI, Martin BM, Tayebi N et al. Glucosylsphingosine accumulation in tissues from patients with Gaucher disease: correlation with phenotype and genotype. Mol Genet Metab 2002; 76: 262-270.
36. Hein LK, Meikle PJ, Hopwood JJ, Fuller M. Secondary sphingolipid accumulation in a macrophage model of Gaucher disease. Mol Genet Metab 2007; 92: 336-345.
37. Ron I, Horowitz M. ER retention and degradation as the molecular basis underlying Gaucher disease heterogeneity. Hum Mol Genet 2005; 14: 2387-2398.
38. Bendikov-Bar I, Ron I, Filocamo M, Horowitz M. Characterization of the ERAD process of the L444P mutant glucocerebrosidase variant. Blood Cells Mol Dis 2011; 46: 4-10.
39. Tsuang D, Leverenz JB, Lopez OL, Hamilton RL, Bennett DA, Schneider JA et al. GBA mutations increase risk for Lewy body disease with and without Alzheimer disease pathology. Neurology 2012; 79: 1944-1950.
40. Balducci C, Pierguidi L, Persichetti E, Parnetti L, Sbaragli M, Tassi C et al. Lysosomal hydrolases in cerebrospinal fluid from subjects with Parkinson's disease. Mov Disord 2007; 22: 1481-1484.
41. Parnetti L, Balducci C, Pierguidi L, De Carlo C, Peducci M, D'Amore C et al. Cerebrospinal fluid beta-glucocerebrosidase activity is reduced in Dementia with Lewy Bodies. Neurobiol Dis 2009; 34: 484-486.
42. Xu YH, Xu K, Sun Y, Liou B, Quinn B, Li RH et al. Multiple pathogenic proteins implicated in neuronopathic Gaucher disease mice. Hum Mol Genet 2014; 23: 3943-3957.