Abnormal α-synuclein interactions with rab3a and rabphilin in diffuse Lewy body disease

Neurobiology of Disease

Volumn 16, Issue 1, 2004, Pages 92-97

  Dalfo E ^a   Barrachina, M ^a   Rosa, J L ^b   Ambrosio, S ^b   Ferrer, I ^a  

^a HOSPITAL UNIVERSITARI DE BELLVITGE   (Spain)

^b UNIVERSITY OF BARCELONA   (Spain)

Author keywords

Synuclein; Lewy body disease; rab3a; rab5; rab8; Rabphilin

Indexed keywords

ALPHA SYNUCLEIN; NEUROPEPTIDE; RAB PROTEIN; RABPHILIN; UNCLASSIFIED DRUG;

AGED; ARTICLE; BINDING AFFINITY; CASE REPORT; CONTROLLED STUDY; DIFFUSE LEWY BODY DISEASE; ENTORHINAL CORTEX; FEMALE; HUMAN; IMMUNOBLOTTING; IMMUNOPRECIPITATION; IMMUNOREACTIVITY; MALE; MOLECULAR WEIGHT; PRIORITY JOURNAL; PROTEIN INTERACTION; SYNAPSE VESICLE;

ADAPTOR PROTEINS, SIGNAL TRANSDUCING; AGED; ALPHA-SYNUCLEIN; FEMALE; HUMANS; LEWY BODY DISEASE; MALE; NERVE TISSUE PROTEINS; RAB GTP-BINDING PROTEINS; RAB3 GTP-BINDING PROTEINS; RAB3A GTP-BINDING PROTEIN; SYNUCLEINS; VESICULAR TRANSPORT PROTEINS;

EID: 2342457804     PISSN: 09699961     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.nbd.2004.01.001     Document Type: Article

References (64)

1. Abeliovich A., Schmitz Y., Farinas I., Choi-Lundberg D., Ho W.H., Castillo P.H., Shinsky N., Verdugo J.M., Armanini M., Ryan A., Inés M., Phillips H., Sulzer D., Rosenthal A. Mice lacking α-synuclein display functional deficits in the nigrostriatal dopamine system. Neuron. 25:2000;239-252
2. Alim M.A., Hossain M.S., Arima K., Takeda K., Izumiyama Y., Nakamura M., Kaji H., Shinoda T., Hisanaga S., Ueda K. Tubulin seeds alpha-synuclein formation. J. Biol. Chem. 18:2002;2112-2117
3. Baba M., Nakajo S., Tu P., Tomita T., Nakaya K., Lee V.M.Y., Trojanowski J.Q., Iwatsubo T. Aggregation of α-synuclein in Lewy bodies of sporadic Parkinson's disease and dementia with Lewy bodies. Am. J. Pathol. 152:1998;879-884
4. Bennet M.K., Scheller R.H. The molecular machinery for secretion is conserved from yeast to neurons. Proc. Natl. Acad. Sci. U. S. A. 90:1993;2559-2563
5. Cabin D.E., Shimazu K., Murphy D., Cole N.B., Gottschalk W., Mcllwain K.L., Orrison B., Chen A., Ellis C.E., Paylor R., Lu B., Nussbaum R.L. Synaptic vesicle depletion correlates with attenuated synaptic responses to prolonged repetitive stimulation in mice lacking α-synuclein. J. Neurosci. 22:2002;8797-8807
6. Campbell B.C.V., Li Q.-X., Culvenor J.G., Jäkäla P., Cappai R., Beyreuther K., Masters C.L., McLean C.A. Accumulation of insoluble α-synuclein in dementia with Lewy bodies. Neurobiol. Dis. 7:2000;192-200
7. Chung S.H., Takai Y., Holz R.W. Evidence that the rab3a-binding protein, rabphilin 3a, enhances regulated secretion. Studies in adrenal cromaffin cells. J. Biol. Chem. 270:1995;16714-16719
8. Clayton D.F., George J.M. The synucleins: a family of proteins involved in synaptic function, plasticity, neurodegeneration and disease. Trends Neurosci. 21:1998;249-254
9. Clayton D.F., George J.M. Synucleins in synaptic plasticity and neurodegenerative disorders. J. Neurosci. Res. 8:1999;120-129
10. D'Andrea M.R., Illyin S., Plata-Salaman C.R. Abnormal patterns of microtubule-associated protein-2 (MAP-2) immunolabeling in neuronal nuclei and Lewy bodies in Parkinson's disease substantia nigra brain tissues. Neurosci. Lett. 306:2001;137-140
11. Davidson W.S., Jonas D.F., Clayton D.F., George J.M. Stabilization of α-synuclein secondary structure upon binding to synthetic membranes. J. Biol. Chem. 273:1998;9443-9449
12. Engelender S., Kaminski Z., Guo X., Sharp A.H., Amaravi R.K., Kleirderlein J.J., Margolis R.L., Troncoso A.A., Lanahan P.F., Worley V.L., Dawson T.M., Dawson C.A., Ross C.A. Synphilin-1 associates with alpha-synuclein and promotes the formation of cytosolic inclusions. Nat. Genet. 22:1999;110-114
13. Ferrer I., Blanco R., Carmona M., Puig B., Borrachina M., Gömez C., Ambrosio S. Active, phosphorylation-dependent mitogen-activated protein kinase (MAPK/ERK), stress-activated protein kinase/c-Jun N-terminal kinase (SAPK/JNK), and p38 kinase expression in Parkinson's disease and dementia with Lewy bodies. J. Neural Transm. 108:2001;1383-1396
14. Fischer von Mollard G., Südhof T.C., Jan R. A small GTP-binding protein dissociates from synaptic vesicles during exocytosis. Nature. 349:1991;79-81
15. Fischer von Mollard G., Stahl B., Li C., Südhof T.C., Jan R. Rab proteins in regulated exocytosis. Trends Biochem. 19:1994;164-169
16. Fujiwara H., Hasegawa M., Dohmae N., Kawashima A., Masliah E., Goldberg M.S., Shen J., Takio K., Iwatsubo T. α-Synuclein is phosphorylated in synucleinopathy lesions. Nat. Cell. Biol. 4:2002;160-164
17. Geppert M., Bolshakov V.Y., Siegelbaum S.A., Takei K., De Camilli P., Hammer R.E., Südhof T.C. The role of Rab3A in neurotransmitter release. Nature. 369:1994;493-497
18. Geppert M., Goda Y., Stevens C.F., Südhof T.C. The small GTP-binding protein Rab3A regulates a late step in synaptic vesicle fusion. Nature. 387:1997;810-814
19. Harding A.J., Hallyday G.M. Cortical Lewy body pathology in the diagnosis of dementia. Acta Neuropathol. 102:2001;355-363
20. Hashimoto M., Masliah E. Alpha-synuclein in Lewy body disease and Alzheimer's disease. Brain Pathol. 9:1999;707-720
21. Irizarry M.C., Growdon W., Gómez-Isla T., Newell K., George J.M., Clayton D.F., Hyman B.T. Nigral and cortical Lewy bodies in dystrophic nigral neurites in Parkinson's disease and cortical Lewy body disease contain α-synuclein immunoreactivity. J. Neuropathol. Exp. Neurol. 57:1998;334-337
22. Iwatsubo T., Yamaguchi H., Fujimuro M., Yokosawa H., Ihara Y., Trojanowski J.Q., Lee V.M. Purification and characterization of Lewy bodies from the brains of patients with diffuse Lewy body disease. Am. J. Pathol. 148:1996;1517-1529
23. Jähn R., Südhof T.C. Synaptic vesicles and exocytosis. Annu. Rev. Neurosci. 17:1994;219-246
24. Jakes R., Spillantini M.G., Goedert M. Identification of two distinct synucleins from human brain. FEBS Lett. 345:1994;27-32
25. Jensen P.H., Hager H., Nielsen M.S., Hojrup P., Gliemann J., Jakes R. α-Synuclein binds to tau and stimulates the protein kinase A-catalyzed tau phosphorylation of serine residues 263 and 356. J. Biol. Chem. 36:1999;25481-25489
26. Jensen P.H., Islam K., Kenney J., Nielsen M.S., Power J., Gai W.P. Microtubule-associated protein 1B is a component of cortical Lewy bodies and binds α-synuclein filaments. J. Biol. Chem. 275:2000;21500-21507
27. Khale P.J., Haass C., Kretschmar H.A., Neumann M. Structure/function of α-synuclein in health and disease: rational development of animal models for Parkinson's and related diseases. J. Neurochem. 82:2002;449-457
28. Krüger R., Kuhn W., Müller T., Woitalia D., Graber M., Kosel S., Przuntek H., Epplen J.T., Schols L., Reiss O. Ala30Pro mutation in the gene encoding α-synuclein in Parkinson's disease. Nat. Genet. 18:1998;106-108
29. Krüger R., Müller T., Riess O. Involvement of synuclein in Parkinson's disease and other neurodegenerative disorders. J. Neural Transm. 107:2000;31-40
30. Lavedan C. The synuclein family. Genome Res. 8:1998;871-880
31. Lee F.S.J., Liu Z.B., Pristupa H.B., Niznik H.B. Direct binding and functional coupling of α-synuclein to the dopamine transporters accelerate dopamine-induced apoptosis. FASEB J. 15:2001;916-926
32. Leenders M.A.G., Lopes da Silva F.H., Ghijsen E.J.M.W., Verhage M. Rab3A is involved in transport of synaptic vesicles to the active zone in mouse brain nerve terminals. Mol. Biol. Cell. 12:2001;3095-3102
33. 2+/phospholipid-binding protein, depends on Rab3A/C. Neuron. 13:1994;885-898
34. Lledó P.M., Johannes L., Vernier P., Zorec R., Darchen F., Vincent J.D., Henry J.P., Mason W.T. Rab3 proteins: key players in the control of exocytosis. Trends Neurosci. 17:1994;426-432
35. Lotharius J., Brundin P. Pathogenesis of Parkinson's disease: dopamine, vesicles and α-synuclein. Nat. Rev. 3:2002;1-11
36. Lücking C.B., Brice A. Alpha-synuclein and Parkinson's disease. Cell. Mol. Life Sci. 57:2000;1894-1908
37. Murphy D.D., Rueter S.M., Trojanowski J.Q., Lee V.M. Synucleins are developmentally expressed, and α-synuclein regulates the size of presynaptic vesicular pool in primary hippocampal neurons. FEBS Lett. 470:2000;93-95
38. Nagano F., Kawabe H., Nakanishi H., Shinoara M., Deguchi-Tawarada M., Takeuchi M., Sasaki T., Takai Y. Rabconnectin-3, a novel protein that binds both GDP/GTP exchange protein and GTPases-activating protein for rab3 small G protein family. J. Biol. Chem. 277:2002;9629-9632
39. Nonet M.L., Stauton J.E., Kilgard M.P., Fergestad T., Hartwieg E., Horvitz H.R., Jorgersen E.M., Meyer B.J. Caenorhabditis elegans rab-3 mutant synapses exhibit impaired function and are partially depleted of vesicles. J. Neurosci. 17:1997;8061-8063
40. Ostermeier C., Brunger T.A. Structural basis of Rab effector specificity: crystal structure of the small G protein Rab3a complexed with the effector domain of rabphilin-3A. Cell. 96:1999;363-374
41. Payton J.E., Perrin R.J., Clayton D.F., George J.M. Protein-protein interactions of α-synuclein in brain homogenates and transfected cells. Mol. Brain Res. 95:2001;138-145
42. Pfeffer S.R. Rab GTPases: master regulators of membrane trafficking. Curr. Opin. Cell Biol. 6:1994;522-526
43. Polymeropulos M.H., Lavedant C., Leroy E., Ide S.E., Dehejia A., Dutra A., Pike B., Root H., Rubenstein J., Boyer R., Stenroos E.S., Chandrasekharappa S., Athanassiadou A., Papapetropoulos T., Johnson W.G., Lazzani A.M., Duvoisin R.C., Di Iorio G., Golbe Ll., Nussbaum R.L. Mutations in the α-synuclein gene identified in families with Parkinson's disease. Science. 276:1997;2045-2047
44. Rosa J.L., Casaroli-Marano R.P., Buckler A.J., Vilaró S., Barbacid M. p619, a giant protein related to the chromosome condensation regulator RCC1, stimulates guanine nucleotide exchange on ARF1 and Rab proteins. EMBO J. 15:1996;4262-4273
45. Schlüter O.M., Schnell E., Verhage M., Tzonopoulos T., Nicoll R.A., Janz R., Malenka R.C., Geppert M., Südhof T.C. Rabphilin knock-out mice reveal that rabphilin is not required for rab3 function in regulating neurotransmitter release. J. Neurosci. 19:1999;5834-5846
46. Sharma N., McLean P.J., Kawamata H., Irizarry M.C., Hyman B.D. Alpha-synuclein has an altered conformation and shows a tight intermolecular interaction with ubiquitin in Lewy bodies. Acta Neuropathol. 102:2001;329-334
47. Sharon R., Goldberg M.S., Bar-Josef I., Betensky R.A., Shen J., Selkoe D.J. α-Synuclein occurs in lipid-rich high molecular weight component, binds fatty acids, and shows homology to the fatty acid-binding proteins. Proc. Natl. Acad. Sci. U. S. A. 98:2001;9110-9115
48. Shirataki H., Yamamoto T., Hagi S., Miura H., Oishi H., Jin-no Y., Senbonmatsu T., Takai Y. Rabphilin-3a is associated with synaptic vesicles in a manner independent of Rab3a. J. Biol. Chem. 269:1994;32717-32720
49. Simons K., Zerial M. Rab proteins and the road maps for intracellular transport. Neuron. 11:1993;789-799
50. Söllner T., Rothman J.E. Neurotransmission: harnessing fusion machinery at the synapse. Trends Neurosci. 17:1994;3444-3447
51. Spillantini M.G., Schmidt M.L., Lee V.M.Y., Trojanowski J.Q., Jakes R., Goedert M. α-Synuclein in Lewy bodies. Nature. 388:1997;839-840
52. Spillantini M.G., Growther R.A., Jakes R., Hasegawa M., Goedert M. α-Synuclein in filamentous inclusions of Lewy bodies from Parkinson's disease and dementia with Lewy bodies. Proc. Natl. Acad. Sci. U. S. A. 95:1998;6469-6473
53. Stahl B., Chou J.H., Li C., Südhof C., Jahn R. Rab3 reversibly recruits rabphilin to synaptic vesicles by a mechanism analogous to raf recruitment by ras. EMBO J. 15:1996;1799-1809
54. Südhof T.C. The synaptic vesicle cycle: a cascade of protein interactions. Nature. 375:1995;645-653
55. Südhof T.C. Function of Rab3 GTP-GDP exchange. Neuron. 18:1997;519-522
56. Sulzer D. α-Synuclein and cytosolic dopamine: stabilizing a bad situation. Nat. Med. 7:2001;1280-1282
57. Sung J.Y., Kim J., Paik S.R., Park J.H., Ahn Y.S., Chung K.C. Induction of neuronal death by Rab5A-dependent endocytosis of α-synuclein. J. Biol. Chem. 276:2001;27441-27448
58. Takeda A., Hashimoto M., Mallory M., Sundsumo M., Hioner W., Hansen L., Masliah E. Abnormal accumulation of NACP/α-synuclein in neurodegenerative disorders. Am. J. Pathol. 152:1998;367-372
59. Trojanowski J.Q., Lee V.M.Y. Aggregation of neurofilament and α-synuclein in Lewy bodies: implications for the pathogenesis of Parkinson disease and Lewy body dementia. Arch. Neurol. 55:1998;151-152
60. Ueda K., Fukushima H., Masliah E. Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc. Natl. Acad. Sci. U. S. A. 90:1993;11282-11286
61. Wakabayashi K., Engelender S., Tanaka Y., Yoshimoto M., Mori F., Tsuji S., Ross C.A., Takahashi H. Immunocytochemical localization of synphilin-1, an α-synuclein-associated protein, in neurodegenerative disorders. Acta Neuropathol. 103:2002;209-214
62. Wang Y., Liu X., Biederer T., Südhof T.C. A family of RIM-binding proteins regulated by alternative splicing. Implications for the genesis of synaptic active zones. Proc. Natl. Acad. Sci. U. S. A. 99:2002;14464-14469
63. Wirdefeldt K., Bogdanovic N., Westerberg L., Payami H., Schalling M., Murdoch G. Expression of α-synuclein in the human brain: relation to Lewy body disease. Mol. Brain Res. 92:2001;58-65
64. Zerial M., McBride H. Rab proteins as membrane organizers. Nat. Rev. 2:2001;107-119