Did α-Synuclein and glucocerebrosidase coevolve? Implications for Parkinson's disease

PLoS ONE

Volumn 10, Issue 7, 2015, Pages

  Gruschus, James M ^a  

^a NATIONAL HEART LUNG AND BLOOD INSTITUTE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ALPHA SYNUCLEIN; GLUCOSYLCERAMIDASE; HEMOGLOBIN; SNCA PROTEIN, HUMAN;

ALPHA CHAIN; ARTICLE; BETA CHAIN; DISEASE ASSOCIATION; GENE DISRUPTION; GENE FUNCTION; GENE SEQUENCE; GENETIC ASSOCIATION; GENETIC CORRELATION; GENETIC LINKAGE; GLUCOSYLCERAMIDASE GENE; HUMAN; MOLECULAR EVOLUTION; MUTATIONAL ANALYSIS; NONHUMAN; PARKINSON DISEASE; PATHOGENESIS; PHYLOGENETIC TREE; PROTEIN PROTEIN INTERACTION; RISK FACTOR; SEQUENCE HOMOLOGY; X RAY CRYSTALLOGRAPHY; AMINO ACID SUBSTITUTION; BIOLOGICAL MODEL; GENETICS; MISSENSE MUTATION;

ALPHA-SYNUCLEIN; AMINO ACID SUBSTITUTION; EVOLUTION, MOLECULAR; GLUCOSYLCERAMIDASE; HUMANS; MODELS, GENETIC; MUTATION, MISSENSE; PARKINSON DISEASE;

EID: 84941687042     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0133863     Document Type: Article

References (70)

1. Ueda K, Fukushima H, Masliah E, Xia Y, Iwai A, Yoshimoto M, et al. (1993) Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc Natl Acad Sci U S A 90: 11282-11286. PMID: 8248242
2. Breydo L, Wu JW, Uversky VN (2012) Alpha-synuclein misfolding and Parkinson's disease. Biochim Biophys Acta 1822: 261-285. doi: 10.1016/j.bbadis.2011.10.002 PMID: 22024360
3. Stefanis L (2012) alpha-Synuclein in Parkinson's disease. Cold Spring Harb Perspect Med 2: a009399. doi: 10.1101/cshperspect.a009399 PMID: 22355802
4. Cookson MR (2012) Evolution of neurodegeneration. Curr Biol 22: R753-761. doi: 10.1016/j.cub. 2012.07.008 PMID: 22975006
5. Spillantini MG, Schmidt ML, Lee VM, Trojanowski JQ, Jakes R, Goedert M (1997) Alpha-synuclein in Lewy bodies. Nature 388: 839-840. PMID: 9278044
6. Abeliovich A, Schmitz Y, Farinas I, Choi-Lundberg D, Ho WH, Castillo PE, et al. (2000) Mice lacking alpha-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron 25: 239-252. PMID: 10707987
7. Cabin DE, Shimazu K, Murphy D, Cole NB, Gottschalk W, McIlwain KL, et al. (2002) Synaptic vesicle depletion correlates with attenuated synaptic responses to prolonged repetitive stimulation in mice lacking alpha-synuclein. J Neurosci 22: 8797-8807. PMID: 12388586
8. Nemani VM, Lu W, Berge V, Nakamura K, Onoa B, Lee MK, et al. (2010) Increased expression of alpha-synuclein reduces neurotransmitter release by inhibiting synaptic vesicle reclustering after endocytosis. Neuron 65: 66-79. doi: 10.1016/j.neuron.2009.12.023 PMID: 20152114
9. Bellani S, Sousa VL, Ronzitti G, Valtorta F, Meldolesi J, Chieregatti E (2010) The regulation of synaptic function by alpha-synuclein. Commun Integr Biol 3: 106-109. PMID: 20585500
10. Vargas KJ, Makani S, Davis T, Westphal CH, Castillo PE, Chandra SS (2014) Synucleins regulate the kinetics of synaptic vesicle endocytosis. J Neurosci 34: 9364-9376. doi: 10.1523/JNEUROSCI.4787- 13.2014 PMID: 25009269
11. Burre J, Sharma M, Tsetsenis T, Buchman V, Etherton MR, Sudhof TC (2010) Alpha-synuclein promotes SNARE-complex assembly in vivo and in vitro. Science 329: 1663-1667. doi: 10.1126/science. 1195227 PMID: 20798282
12. Diao J, Burre J, Vivona S, Cipriano DJ, Sharma M, Kyoung M, et al. (2013) Native alpha-synuclein induces clustering of synaptic-vesicle mimics via binding to phospholipids and synaptobrevin-2/ VAMP2. Elife 2: e00592. doi: 10.7554/eLife.00592 PMID: 23638301
13. Yin G, Lopes da Fonseca T, Eisbach SE, Anduaga AM, Breda C, Orcellet ML, et al. (2014) alpha-Synuclein interacts with the switch region of Rab8a in a Ser129 phosphorylation-dependent manner. Neurobiol Dis 70: 149-161. doi: 10.1016/j.nbd.2014.06.018 PMID: 24983211
14. Chen RH, Wislet-Gendebien S, Samuel F, Visanji NP, Zhang G, Marsilio D, et al. (2013) alpha-Synuclein membrane association is regulated by the Rab3a recycling machinery and presynaptic activity. J Biol Chem 288: 7438-7449. doi: 10.1074/jbc.M112.439497 PMID: 23344955
15. Gruschus JM, Yap TL, Pistolesi S, Maltsev AS, Lee JC (2013) NMR structure of calmodulin complexed to an N-terminally acetylated alpha-synuclein peptide. Biochemistry 52: 3436-3445. doi: 10.1021/ bi400199p PMID: 23607618
16. Lee FJ, Liu F, Pristupa ZB, Niznik HB (2001) Direct binding and functional coupling of alpha-synuclein to the dopamine transporters accelerate dopamine-induced apoptosis. FASEB J 15: 916-926. PMID: 11292651
17. Choi P, Golts N, Snyder H, Chong M, Petrucelli L, Hardy J, et al. (2001) Co-association of parkin and alpha-synuclein. Neuroreport 12: 2839-2843. PMID: 11588587
18. Ahn BH, Rhim H, Kim SY, Sung YM, Lee MY, Choi JY, et al. (2002) alpha-Synuclein interacts with phospholipase D isozymes and inhibits pervanadate-induced phospholipase D activation in human embryonic kidney-293 cells. J Biol Chem 277: 12334-12342. PMID: 11821392
19. Neystat M, Rzhetskaya M, Kholodilov N, Burke RE (2002) Analysis of synphilin-1 and synuclein interactions by yeast two-hybrid beta-galactosidase liquid assay. Neurosci Lett 325: 119-123. PMID: 12044636
20. Jensen PH, Hager H, Nielsen MS, Hojrup P, Gliemann J, Jakes R (1999) alpha-synuclein binds to Tau and stimulates the protein kinase A-catalyzed tau phosphorylation of serine residues 262 and 356. J Biol Chem 274: 25481-25489. PMID: 10464279
21. Yap TL, Gruschus JM, Velayati A, WestbroekW, Goldin E, Moaven N, et al. (2011) Alpha-synuclein interacts with Glucocerebrosidase providing a molecular link between Parkinson and Gaucher diseases. J Biol Chem 286: 28080-28088. doi: 10.1074/jbc.M111.237859 PMID: 21653695
22. Uemura N, Koike M, Ansai S, Kinoshita M, Ishikawa-Fujiwara T, Matsui H, et al. (2015) Viable Neuronopathic Gaucher Disease Model in Medaka (Oryzias latipes) Displays Axonal Accumulation of Alpha- Synuclein. PLoS Genet 11: e1005065. doi: 10.1371/journal.pgen.1005065 PMID: 25835295
23. El-Agnaf OM, Bodles AM, Guthrie DJ, Harriott P, Irvine GB (1998) The N-terminal region of non-A beta component of Alzheimer's disease amyloid is responsible for its tendency to assume beta-sheet and aggregate to form fibrils. Eur J Biochem 258: 157-163. PMID: 9851705
24. Vilar M, Chou HT, Luhrs T, Maji SK, Riek-Loher D, Verel R, et al. (2008) The fold of alpha-synuclein fibrils. Proc Natl Acad Sci U S A 105: 8637-8642. doi: 10.1073/pnas.0712179105 PMID: 18550842
25. Hashimoto M, Rockenstein E, Mante M, Mallory M, Masliah E (2001) beta-Synuclein inhibits alphasynuclein aggregation: a possible role as an anti-parkinsonian factor. Neuron 32: 213-223. PMID: 11683992
26. Klein C, Westenberger A (2012) Genetics of Parkinson's disease. Cold Spring Harb Perspect Med 2: a008888. doi: 10.1101/cshperspect.a008888 PMID: 22315721
27. Hruska KS, LaMarca ME, Scott CR, Sidransky E (2008) Gaucher disease: mutation and polymorphism spectrum in the glucocerebrosidase gene (GBA). Hum Mutat 29: 567-583. doi: 10.1002/humu.20676 PMID: 18338393
28. Sidransky E, Nalls MA, Aasly JO, Aharon-Peretz J, Annesi G, Barbosa ER, et al. (2009) Multicenter analysis of glucocerebrosidase mutations in Parkinson's disease. N Engl J Med 361: 1651-1661. doi: 10.1056/NEJMoa0901281 PMID: 19846850
29. Sardi SP, Clarke J, Kinnecom C, Tamsett TJ, Li L, Stanek LM, et al. (2011) CNS expression of glucocerebrosidase corrects alpha-synuclein pathology and memory in a mouse model of Gaucher-related synucleinopathy. Proc Natl Acad Sci U S A 108: 12101-12106. doi: 10.1073/pnas.1108197108 PMID: 21730160
30. Sybertz E, Krainc D (2014) Development of targeted therapies for Parkinson's disease and related synucleinopathies. J Lipid Res 55: 1996-2003. doi: 10.1194/jlr.R047381 PMID: 24668939
31. Mak SK, McCormack AL, Manning-Bog AB, Cuervo AM, Di Monte DA (2010) Lysosomal degradation of alpha-synuclein in vivo. J Biol Chem 285: 13621-13629. doi: 10.1074/jbc.M109.074617 PMID: 20200163
32. de Juan D, Pazos F, Valencia A (2013) Emerging methods in protein co-evolution. Nat Rev Genet 14: 249-261. doi: 10.1038/nrg3414 PMID: 23458856
33. Marks DS, Colwell LJ, Sheridan R, Hopf TA, Pagnani A, Zecchina R, et al. (2011) Protein 3D structure computed from evolutionary sequence variation. PLoS One 6: e28766. doi: 10.1371/journal.pone. 0028766 PMID: 22163331
34. Kosciolek T, Jones DT (2014) De novo structure prediction of globular proteins aided by sequence variation- derived contacts. PLoS One 9: e92197. doi: 10.1371/journal.pone.0092197 PMID: 24637808
35. Hopf TA, Scharfe CP, Rodrigues JP, Green AG, Kohlbacher O, Sander C, et al. (2014) Sequence coevolution gives 3D contacts and structures of protein complexes. Elife 3.
36. Skerker JM, Perchuk BS, Siryaporn A, Lubin EA, Ashenberg O, Goulian M, et al. (2008) Rewiring the specificity of two-component signal transduction systems. Cell 133: 1043-1054. doi: 10.1016/j.cell. 2008.04.040 PMID: 18555780
37. Weigt M, White RA, Szurmant H, Hoch JA, Hwa T (2009) Identification of direct residue contacts in protein- protein interaction by message passing. Proceedings of the National Academy of Sciences of the United States of America 106: 67-72. doi: 10.1073/pnas.0805923106 PMID: 19116270
38. Ovchinnikov S, Kamisetty H, Baker D (2014) Robust and accurate prediction of residue-residue interactions across protein interfaces using evolutionary information. Elife 3.
39. Jeong CS, Kim D (2012) Reliable and robust detection of coevolving protein residues. Protein Eng Des Sel 25: 705-713. doi: 10.1093/protein/gzs081 PMID: 23077274
40. Pazos F, HelmerCitterich M, Ausiello G, Valencia A (1997) Correlated mutations contain information about protein-protein interaction. Journal of Molecular Biology 271: 511-523. PMID: 9281423
41. Morcos F, Pagnani A, Lunt B, Bertolino A, Marks DS, Sander C, et al. (2011) Direct-coupling analysis of residue coevolution captures native contacts across many protein families. Proc Natl Acad Sci U S A 108: E1293-1301. doi: 10.1073/pnas.1111471108 PMID: 22106262
42. Brown CA, Brown KS (2010) Validation of coevolving residue algorithms via pipeline sensitivity analysis: ELSC and OMES and ZNMI, oh my! PLoS One 5: e10779. doi: 10.1371/journal.pone.0010779 PMID: 20531955
43. Ashenberg O, Laub MT (2013) Using analyses of amino Acid coevolution to understand protein structure and function. Methods Enzymol 523: 191-212. doi: 10.1016/B978-0-12-394292-0.00009-6 PMID: 23422431
44. Martin LC, Gloor GB, Dunn SD, Wahl LM (2005) Using information theory to search for co-evolving residues in proteins. Bioinformatics 21: 4116-4124. PMID: 16159918
45. Sievers F, Wilm A, Dineen D, Gibson TJ, Karplus K, Li W, et al. (2011) Fast, scalable generation of high-quality protein multiple sequence alignments using Clustal Omega. Mol Syst Biol 7: 539. doi: 10. 1038/msb.2011.75 PMID: 21988835
46. Altschul SF, Gish W, Miller W, Myers EW, Lipman DJ (1990) Basic local alignment search tool. J Mol Biol 215: 403-410. PMID: 2231712
47. Di Lena P, Nagata K, Baldi P (2012) Deep architectures for protein contact map prediction. Bioinformatics 28: 2449-2457. PMID: 22847931
48. Halabi N, Rivoire O, Leibler S, Ranganathan R (2009) Protein sectors: evolutionary units of threedimensional structure. Cell 138: 774-786. doi: 10.1016/j.cell.2009.07.038 PMID: 19703402
49. Polymeropoulos MH, Lavedan C, Leroy E, Ide SE, Dehejia A, Dutra A, et al. (1997) Mutation in the alpha-synuclein gene identified in families with Parkinson's disease. Science 276: 2045-2047. PMID: 9197268
50. Pasanen P, Myllykangas L, Siitonen M, Raunio A, Kaakkola S, Lyytinen J, et al. (2014) A novel alphasynuclein mutation A53E associated with atypical multiple system atrophy and Parkinson's diseasetype pathology. Neurobiol Aging 35: 2180 e2181-2185.
51. Dvir H, Harel M, McCarthy AA, Toker L, Silman I, Futerman AH, et al. (2003) X-ray structure of human acid-beta-glucosidase, the defective enzyme in Gaucher disease. EMBO Rep 4: 704-709. PMID: 12792654
52. Knaggs MH, Salsbury FR, Edgell MH, Fetrow JS (2007) Insights into correlated motions and longrange interactions in CheY derived from molecular dynamics simulations. Biophysical Journal 92: 2062-2079. PMID: 17172298
53. Noivirt-Brik O, Unger R, Horovitz A (2009) Analysing the origin of long-range interactions in proteins using lattice models. Bmc Structural Biology 9.
54. Dunn SD, Wahl LM, Gloor GB (2008) Mutual information without the influence of phylogeny or entropy dramatically improves residue contact prediction. Bioinformatics 24: 333-340. PMID: 18057019
55. Ashkenazy H, Kliger Y (2010) Reducing phylogenetic bias in correlated mutation analysis. Protein Eng Des Sel 23: 321-326. doi: 10.1093/protein/gzp078 PMID: 20067922
56. Lee BC, Kim D (2009) A new method for revealing correlated mutations under the structural and functional constraints in proteins. Bioinformatics 25: 2506-2513. doi: 10.1093/bioinformatics/btp455 PMID: 19628501
57. Wollenberg KR, Atchley WR (2000) Separation of phylogenetic and functional associations in biological sequences by using the parametric bootstrap. Proc Natl Acad Sci U S A 97: 3288-3291. PMID: 10725404
58. Fares MA, Travers SA (2006) A novel method for detecting intramolecular coevolution: adding a further dimension to selective constraints analyses. Genetics 173: 9-23. PMID: 16547113
59. Beutler E, Gelbart T, Balicki D, Demina A, Adusumalli J, Elsas L 2nd, et al. (1996) Gaucher disease: four families with previously undescribed mutations. Proc Assoc Am Physicians 108: 179-184. PMID: 8774051
60. Caffrey DR, Somaroo S, Hughes JD, Mintseris J, Huang ES (2004) Are protein-protein interfaces more conserved in sequence than the rest of the protein surface? Protein Sci 13: 190-202. PMID: 14691234
61. Cho MK, Nodet G, Kim HY, Jensen MR, Bernado P, Fernandez CO, et al. (2009) Structural characterization of alpha-synuclein in an aggregation prone state. Protein Sci 18: 1840-1846. doi: 10.1002/pro. 194 PMID: 19554627
62. Gruschus JM, Jiang Z, Yap TL, Hill SA, Grishaev A, Piszczek G, et al. (2015) Dissociation of glucocerebrosidase dimer in solution by its co-factor, saposin C. Biochem Biophys Res Commun 457: 561-566. doi: 10.1016/j.bbrc.2015.01.024 PMID: 25600808
63. Yap TL, Velayati A, Sidransky E, Lee JC (2013) Membrane-bound alpha-synuclein interacts with glucocerebrosidase and inhibits enzyme activity. Mol Genet Metab 108: 56-64. doi: 10.1016/j.ymgme.2012. 11.010 PMID: 23266198
64. Pele J, Moreau M, Abdi H, Rodien P, Castel H, Chabbert M (2014) Comparative analysis of sequence covariation methods to mine evolutionary hubs: examples from selected GPCR families. Proteins 82: 2141-2156. doi: 10.1002/prot.24570 PMID: 24677372
65. Wei RR, Hughes H, Boucher S, Bird JJ, Guziewicz N, Van Patten SM, et al. (2011) X-ray and biochemical analysis of N370S mutant human acid beta-glucosidase. J Biol Chem 286: 299-308. doi: 10.1074/ jbc.M110.150433 PMID: 20980263
66. Zarranz JJ, Alegre J, Gomez-Esteban JC, Lezcano E, Ros R, Ampuero I, et al. (2004) The new mutation, E46K, of alpha-synuclein causes Parkinson and Lewy body dementia. Ann Neurol 55: 164-173. PMID: 14755719
67. Appel-Cresswell S, Vilarino-Guell C, Encarnacion M, Sherman H, Yu I, Shah B, et al. (2013) Alphasynuclein p.H50Q, a novel pathogenic mutation for Parkinson's disease. Mov Disord 28: 811-813. doi: 10.1002/mds.25421 PMID: 23457019
68. Kowarsch A, Fuchs A, Frishman D, Pagel P (2010) Correlated Mutations: A Hallmark of Phenotypic Amino Acid Substitutions. Plos Computational Biology 6.
69. Yap TL, Gruschus JM, Velayati A, Sidransky E, Lee JC (2013) Saposin C protects glucocerebrosidase against alpha-synuclein inhibition. Biochemistry 52: 7161-7163. doi: 10.1021/bi401191v PMID: 24070323
70. Brighina L, Okubadejo NU, Schneider NK, Lesnick TG, de Andrade M, Cunningham JM, et al. (2007) Beta-synuclein gene variants and Parkinson's disease: a preliminary case-control study. Neurosci Lett 420: 229-234. PMID: 17556099