Degradative organelles containing mislocalized α- and β-synuclein proliferate in presenilin-1 null neurons

Journal of Cell Biology

Volumn 165, Issue 3, 2004, Pages 335-346

  Wilson, Christina A ^a   Murphy, Diane D ^a,b   Giasson, Benoit I ^a   Zhang, Bin ^a   Trojanowski, John Q ^a   Lee, Virginia M Y ^a  

^a UNIVERSITY OF PENNSYLVANIA   (United States)

^b Neuroscience Center   (United States)

Author keywords

Autophagy; Calcium dysregulation; Neurodegenerative diseases

Indexed keywords

1 [2 (4 METHOXYPHENYL) 2 [3 (4 METHOXYPHENYL)PROPOXY]ETHYL] 1H IMIDAZOLE; ALPHA SYNUCLEIN; BETA SYNUCLEIN; CALCIUM CHANNEL; GAMMA SECRETASE; L 685458; MEMBRANE PROTEIN; PRESENILIN 1; STAUROSPORINE; SYNUCLEIN; THAPSIGARGIN; UNCLASSIFIED DRUG;

ARTICLE; ASSOCIATION; AUTOPHAGY; BRAIN DEGENERATION; CELL ORGANELLE; CELL PROLIFERATION; CELL STIMULATION; CELL VACUOLE; CLINICAL FEATURE; CONTROLLED STUDY; DEGENERATIVE DISEASE; ENZYME ACTIVITY; HUMAN; HUMAN CELL; LEWY BODY; MICROMORPHOLOGY; NERVE CELL; NULL ALLELE; PERIKARYON; PRESYNAPTIC NERVE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN DEFICIENCY; PROTEIN DEGRADATION; PROTEIN LOCALIZATION;

AGED; AGED, 80 AND OVER; ALPHA-SYNUCLEIN; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; ANTIGENS, CD; ASPARTIC ENDOPEPTIDASES; AUTOPHAGY; BETA-SYNUCLEIN; BRAIN; CALCIUM CHANNELS; CELLS, CULTURED; ENDOPEPTIDASES; FEMALE; HUMANS; INCLUSION BODIES; LYSOSOME-ASSOCIATED MEMBRANE GLYCOPROTEINS; LYSOSOMES; MALE; MEMBRANE PROTEINS; MICE; MICE, KNOCKOUT; MICROSCOPY, ELECTRON; MIDDLE AGED; MUTATION; NERVE TISSUE PROTEINS; NEURODEGENERATIVE DISEASES; NEURONS; PRESENILIN-1; PROTEIN TRANSPORT; SYNUCLEINS; UP-REGULATION; VACUOLES;

EID: 2442421944     PISSN: 00219525     EISSN: None     Source Type: Journal    
DOI: 10.1083/jcb.200403061     Document Type: Article

References (78)

1. Adamec, E., P.S. Mohan, A.M. Cataldo, A.N. Srinivasan, J.P. Vonsattel, and R.A. Nixon. 2000. Upregulation of the lysosomal system in experimental models of neuronal injury: Implications for Alzheimer's disease. Neuroscience. 100: 663-675.
2. Advani, R.J., B. Yang, R. Prekeris, K.C. Lee, J. Klumperman, and R.H. Scheller. 1999. VAMP-7 mediates vesicular transport from endosomes to lysosomes. J. Cell Biol. 146:765-775.
3. Anglade, P., S. Vyas, F. Javoy-Agid, M.T. Herrero, P.P. Michel, J. Marquez, A. Mouatt-Prigent, M. Ruberg, E.C. Hirsch, and Y. Agid. 1997. Apoptosis and autophagy in nigral neurons of patients with Parkinson's disease. Histol. Histopathol 12:25-31.
4. Annaert, W.G., C. Esselens, V. Baert, C. Boeve, G. Snellings, P. Cupers, K. Craessaerts, and B. De Strooper. 2001. Interaction with telencephalin and the amyloid precursor protein predicts a ring structure for presenilins. Neuron. 32:579-589.
5. Bembi, B., M.S. Zambito, E. Sidransky, G. Ciana, M. Carrozzi, C. Martini, M. Giolis, M.G. Pittis, and L. Capus. 2003. Gaucher's disease with Parkinson's disease: Clinical and pathogical aspects. Neurology. 61:99-101.
6. Betarbet, R., T.B. Sherer, G. MacKenzie, M. Garcia-Osuna, A.V. Panov, and J.T. Greenamyre. 2000. Chronic systemic pesticide exposure reproduces features of Parkinson's disease. Nat. Neurosci. 3:1301-1306.
7. Bi, X., J. Zhou, and G. Lynch. 1999. Lysosomal protease inhibitors induce meganeurites and tangle-like structures in entorhinohippocampal regions vulnerable to Alzheimer's disease. Exp. Neurol. 158:312-327.
8. Cabin, D.E., K. Shimazu, D. Murphy, N.B. Cole, W. Gottschalk, K.L. McIlwain, B. Orrison, A. Chen, C.E. Ellis, R. Paylor, 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.
9. Cataldo, A.M., J.L. Barnett, S.A. Berman, J. Li, S. Quarless, S. Bursztajn, C. Lippa, and R.A. Nixon. 1995. Gene expression and cellular content of cathepsin D in Alzheimer's disease brain: evidence for early up-regulation of the endosomal-lysosomal system. Neuron. 14:671-680.
10. Codogno, P., E. Ogier-Denis, and J.J. Houri. 1997. Signal transduction pathways in macroautophagy. Cell. Signal. 9:125-130.
11. Cole, N.B., D.D. Murphy, T. Grider, S. Rueter, D. Brasaemle, and R.L. Nussbaum. 2002. Lipid droplet binding and oligomerization properties of the Parkinson's disease protein alpha-synuclein. J. Biol. Chem. 277:6344-6352.
12. Cuervo, A.M., and J.F. Dice. 2000. Age-related decline in chaperone-mediated autophagy. J. Biol. Chem. 275:31505-31513.
13. Darsow, T., S.E. Rieder, and S.D. Emr. 1997. A multispecificity syntaxin homologue, Vamp3p, essential for autophagic and biosynthetic protein transport to the vacuole. J. Cell Biol. 138:517-529.
14. Davidson, W.S., A. Jonas, D.F. Clayton, and J.M. George. 1998. Stabilization of alpha-synuclein secondary structure upon binding to synthetic membranes. J. Biol. Chem. 273:9443-9449.
15. De Strooper, B., P. Saftig, K. Craessaerts, H. Vanderstichele, G. Guhde, W. Annaert, K. Von Figura, and F. Van Leuven. 1998. Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature. 391:387-390.
16. De Strooper, B., W. Annaert, P. Cupers, P. Saftig, K. Craessaerts, J.S. Mumm, E.H. Schroeter, V. Schrijvers, M.S. Wolfe, W.J. Ray, et al. 1999. A presenilin-1-dependent gamma-secretase-like protease mediates release of Notch intracellular domain. Nature. 398:518-522.
17. Duda, J.E., V.M.-Y. Lee, and J.Q. Trojanowski. 2000. Neuropathology of synuclein aggregates. J. Neurosci. Res. 61:121-127.
18. Duda, J.E., B.I. Giasson, M.E. Mabon, V.M. Lee, and J.Q. Trojanowski. 2002. Novel antibodies to synuclein show abundant striatal pathology in Lewy body diseases. Ann. Neurol. 52:205-210.
19. Esler, W.P., W.T. Kimberly, B.L. Ostaszewski, W. Ye, T.S. Diehl, D.J. Selkoe, and M.S. Wolfe. 2002. Activity-dependent isolation of the presenilin-gamma-secretase complex reveals nicastrin and a gamma substrate. Proc. Natl. Acad. Sci. USA. 99:2720-2725.
20. Galvin, J.E., K. Uryu, V.M.-Y. Lee, and J.Q. Trojanowski. 1999. Axon pathology in Parkinson's disease and Lewy body dementia hippocampus contains alpha-, beta-, and gamma-synuclein. Proc. Natl. Acad. Sci. USA. 96:13450-13455.
21. Georgakopoulos, A., P. Marambaud, S. Efthimiopoulos, J. Shioi, W. Cui, H.C. Li, M. Schutte, R. Gordon, G.R. Holstein, G. Martinelli, et al. 1999. Presenilin-1 forms complexes with the cadherin/catenin cell-cell adhesion system and is recruited to intercellular and synaptic contacts. Mol. Cell. 4:893-902.
22. George, J.M. 2002. The synucleins. Genome Biol. 3:reviews3002.1-3002.6.
23. George, J.M., H. Jin, W.S. Woods, and D.F. Clayton. 1995. Characterization of a novel protein regulated during the critical period for song learning in the zebra finch. Neuron. 15:361-372.
24. Giasson, B.I., R. Jakes, M. Goedert, J.E. Duda, S. Leight, J.Q. Trojanowski, and V.M.-Y. Lee. 2000. A panel of epitope-specific antibodies detects protein domains distributed throughout human alpha-synuclein in Lewy bodies of Parkinson's disease. J. Neurosci. Res. 59:528-533.
25. Gomez-Santos, C., I. Ferrer, A.F. Santidrian, M. Barrachina, and J. Gil. 2003. Dopamine induces autophagic cell death and alpha-synuclein increase in human neuroblastoma SH-SY5Y cells. J. Neurosci. Res. 73:341-350.
26. Hornung, J.P., H. Koppel, and P.G. Clarke. 1989. Endocytosis and autophagy in dying neurons: an ultrastructural study in chick embryos. J. Comp. Neurol. 283:425-437.
27. Hsu, L.J., Y. Sagara, A. Arroyo, E. Rockenstein, A. Sisk, M. Mallory, J. Wong, T. Takenouchi, M. Hashimoto, and E. Masliah. 2000. alpha-synuclein promotes mitochondrial deficit and oxidative stress. Am. J. Pathol. 157:401-410.
28. Ishimaru, H., K. Ueda, A. Takahashi, and Y. Maruyama. 1998. Changes in presynaptic protein NACP/alpha-synuclein in an ischemic gerbil hippocampus. Brain Res. 788:311-314.
29. Iwai, A., E. Masliah, M. Yoshimoto, N. Ge, L. Flanagan, H. A.de Silva, A. Kittel, and T. Saitoh. 1995. The precursor protein of non-A beta component of Alzheimer's disease amyloid is a presynaptic protein of the central nervous system. Neuron. 14:467-475.
30. Iwata, A., S. Miura, I. Kanazawa, M. Sawada, and N. Nukina. 2001. alpha-synuclein forms a complex with transcription factor Elk-1. J. Neurochem. 77: 239-252.
31. Jakes, R., M.G. Spillantini, and M. Goedert. 1994. Identification of two distinct synucleins from human brain. FEBS Lett. 345:27-32.
32. Jensen, P.H., J.Y. Li, A. Dahlstrom, and C.G. Dotti. 1999. Axonal transport of synucleins is mediated by all rate components. Eur. J. Neurosci. 11:3369-3376.
33. Kaether, C., S. Lammich, D. Edbauer, M. Ertl, J. Rietdorf, A. Capell, H. Steiner, and C. Haass. 2002. Presenilin-1 affects trafficking and processing of βAPP and is targeted in a complex with nicastrin to the plasma membrane. J. Cell Biol 158:551-561.
34. Kamal, A., A. Almenar-Queralt, J.F. LeBlanc, E.A. Roberts, and L.S. Goldstein. 2001. Kinesin-mediated axonal transport of a membrane compartment containing β-secretase and presenilin-1 requires APP. Nature. 414:643-648.
35. Kang, D.E., S. Soriano, M.P. Frosch, T. Collins, S. Naruse, S.S. Sisodia, G. Leibowitz, F. Levine, and E.H. Koo. 1999. Presenilin 1 facilitates the constitutive turnover of beta-catenin: differential activity of Alzheimer's disease-linked PSI mutants in the beta-catenin-signaling pathway. J. Neurosci. 19: 4229-4237.
36. Kholodilov, N.G., M. Neystat, T.F. Oo, S.E. Lo, K.E. Larsen, D. Sulzer, and R.E. Burke. 1999. Increased expression of rat synuclein in the substantia nigra pars compacta identified by mRNA differential display in a model of developmental target injury. J. Neurochem. 73:2586-2599.
37. Kosik, K., L.D. Orecchio, L. Binder, J.Q. Trojanowski, V.M.-Y. Lee, and G. Lee. 1988. Epitopes that span the tau molecule are shared with paired helical filaments. Neuron. 1:817-825.
38. Leissring, M.A., Y. Akbari, C.M. Fanger, M.D. Cahalan, M.P. Mattson, and F.M. LaFerla. 2000. Capacitative calcium entry deficits and elevated luminal calcium content in mutant presenilin-1 knockin mice. J. Cell Biol. 149:793-798.
39. Li, W., P.N. Hoffman, W. Stirling, D.L. Price, and M.K. Lee. 2004. Axonal transport of human α-synuclein slows with aging but is not affected by familial Parkinson's disease-linked mutations. J. Neurochem. 88:401-410.
40. Lippa, C.F., H. Fujiwara, D.M. Mann, B. Giasson, M. Baba, M.L. Schmidt, L.E. Nee, B. O'Connell, D.A. Pollen, P. George-Hyslop, et al. 1998. Lewy bodies contain altered alpha-synuclein in brains of many familial Alzheimer's disease patients with mutations in presenilin and amyloid precursor protein genes. Am. J. Pathol. 153:1365-1370.
41. Maroteaux, L., and R.H. Scheller. 1991. The rat brain synucleins; family of proteins transiently associated with neuronal membrane. Brain Res. Mol. Brain Res. 11:335-343.
42. Maroteaux, L., J.T. Campanelli, and R.H. Scheller. 1988. Synuclein: a neuron-specific protein localized to the nucleus and presynaptic nerve terminal. J. Neurosci. 8:2804-2815.
43. Martinez, I., S. Chakrabarti, T. Hellevik, J. Morehead, K. Fowler, and N.W. Andrews. 2000. Synaptotagmin VII regulates calcium-dependent exocytosis of lysosomes in fibroblasts. J. Cell Biol. 148:1141-1149.
44. Meredith, G.E., S. Totterdell, E. Petroske, K. Santa Cruz, R.C.J. Callison, and Y.S. Lau. 2002. Lysosomal malfunction accompanies alpha-synuclein aggregation in a progressive mouse model of Parkinson's disease. Brain Res. 956: 156-165.
45. Mishizen-Eberz, A.J., R.P. Guttmann, B.I. Giasson, G.A. Day, R. Hodara, H. Ischiropoulos, V.M.-Y. Lee, J.Q. Trojanowski, and D.R. Lynch. 2003. Distinct cleavage patterns of normal and pathologic forms of α-synuclein by calpain I in vitro. J. Neurochem. 86:836-847.
46. Moran, L.B., S. Kosel, C. Spitzer, F.W. Schwaiger, O. Riess, G.W. Kreutzberg, and M.B. Graeber. 2001. Expression of alpha-synuclein in non-apoptotic, slowly degenerating facial motoneurones. J. Neurocytol. 30:515-521.
47. Murphy, D.D., S.M. Rueter, J.Q. Trojanowski, and V.M.-Y. Lee. 2000. Synucleins are developmentally expressed, and alpha-synuclein regulates the size of the presynaptic vesicular pool in primary hippocampal neurons. J. Neurosci. 20:3214-3220.
48. Nakajo, S., K. Tsukada, K. Omata, Y. Nakamura, and K. Nakaya. 1993. A new brain-specific 14-kDa protein is a phosphoprotein. Its complete amino acid sequence and evidence for phosphorylation. Eur. J. Biochem. 217:1057-1063.
49. Nakamura, N., A. Yamamoto, Y. Wada, and M. Futai. 2000. Syntaxin 7 mediates endocytic trafficking to late endosomes. J. Biol. Chem. 275: 6523-6529.
50. Naruse, S., G. Thinakaran, J.J. Luo, J.W. Kusiak, T. Tomita, T. Iwatsubo, X. Qian, D.D. Ginry, D.L. Price, D.R. Borchelt, et al. 1998. Effects of PS1 deficiency on membrane protein trafficking in neurons. Neuron. 21:1213-1221.
51. Okochi, M., J. Walter, A. Koyama, S. Nakajo, M. Baba, T. Iwatsubo, L. Meijer, P.J. Kahle, and C. Haass. 2000. Constitutive phosphorylation of the Parkinson's disease associated α-synuclein. J. Biol. Chem. 275:390-397.
52. Ostrerova, N., L. Petrucelli, M. Farrer, N. Mehta, P. Choi, J. Hardy, and B. Wolozin. 1999. alpha-Synuclein shares physical and functional homology with 14-3-3 proteins. J. Neurosci. 19:5782-5791.
53. Pasternak, S.H., R.D. Bagshaw, M. Guiral, S. Zhang, C.A. Ackerley, B.J. Pak, J.W. Callahan, and D.J. Mahuran. 2003. Presenilin-1, nicastrin, amyloid precursor protein, and gamma-secretase activity are co-localized in the lysosomal membrane. J. Biol. Chem. 278:26687-26694.
54. Paxinou, E., Q. Chen, M. Weisse, B.I. Giasson, E.H. Norris, S.M. Rueter, J.Q. Trojanowski, V.M.-Y. Lee, and H. Ischiropoulos. 2001. Induction of alpha-synuclein aggregation by intracellular nitrative insult. J. Neurosci. 21:8053-8061.
55. Petersen, K., O.F. Olesen, and J.D. Mikkelsen. 1999. Developmental expression of alpha-synuclein in rat hippocampus and cerebral cortex. Neuroscience. 91:651-659.
56. Phiel, C.J., C.A. Wilson, V.M.-Y. Lee, and P.S. Klein. 2003. GSK-3 α regulates production of Alzheimer's disease amyloid-β peptides. Nature. 423:435-439.
57. Pigino, G., G. Morfino, A. Pelsman, M.P. Mattson, S.T. Brady, and J. Busciglio. 2003. Alzheimer's presenilin 1 mutations impair kinesin-based axonal transport. J. Neurosci. 23:4499-4508.
58. Putney, J.W., and R.R. McKay. 1999. Capacitative calcium entry channels. Bioessays. 21:38-46.
59. Qian, S., P. Jiang, X.M. Guan, G. Singh, M.E. Trumbauer, H. Yu, H.Y. Chen, L.H. Van de Ploeg, and H. Zheng. 1998. Mutant human presenilin 1 protects presenilin 1 null mouse against embryonic lethality and elevates Abeta 1-42/43 expression. Neuron. 20:611-617.
60. Selkoe, D.J., and R. Kopan. 2003. Notch and Presenilin: regulated intramembrane proteolysis links development and degeneration. Annu. Rev. Neurosci. 26: 565-597.
61. Shearman, M.S., D. Beher, E.E. Clarke, H.D. Lewis, T. Harrison, P. Hunt, A. Nadin, A.L. Smith, G. Stevenson, and J.L. Castro. 2000. L-685,458, an aspartyl protease transition state mimic, is a potent inhibitor of amyloid beta-protein precursor gamma-secretase activity. Biochemistry. 39:8698-8704.
62. Shibayama-Imazu, T., I. Okahashi, K. Omata, S. Nakajo, H. Ochiai, Y. Nakai, T. Hama, Y. Nakamura, and K. Nakaya. 1993. Cell and tissue distribution and developmental change of neuron specific 14 kDa protein (phosphoneuroprotein 14). Brain Res. 622:17-25.
63. Sinha, S., and I. Lieberburg. 1999. Cellular mechanisms of beta-amyloid production and secretion. Proc. Natl. Acad. Sci. USA. 96:11049-11053.
64. Souza, J.M., B.I. Giasson, V.M.-Y. Lee, and H. Ischiropoulos. 2000. Chaperone-like activity of synucleins. FEBS Lett. 474:116-119.
65. Stefanis, L., K.E. Larsen, H.J. Rideout, D. Sulzer, and L.A. Greene. 2001. Expression of A53T mutant but not wild-type alpha-synuclein in PC12 cells induces alterations of the ubiquitin-dependent degradation system, loss of dopamine release, and autophagic cell death. J. Neurosci. 21:9549-9560.
66. Suzuki, K., E. Iseki, O. Katsuse, A. Yamaguchi, K. Katsuyama, I. Aoki, S. Yamanaka, and K. Kosaka. 2003. Neuronal accumulation of alpha- and beta-synucleins in the brain of a GM2 gangliosidosis mouse model. Neuroreport. 14:551-554.
67. Teclemariam-Mesbah, R., J. Wortel, H.J. Romijn, and R.M. Buijs. 1997. A simple silver-gold intensification procedure for double DAB labeling studies in electron microscopy. J. Histochem. Cytochem. 45:619-621.
68. Trojanowski, J.Q., T. Schuck, M.L. Schmidt, and V.M.-Y. Lee. 1989. Distribution of phosphate-independent MAP2 epitopes revealed with monoclonal antibodies in microwave-denatured human nervous system tissues. J. Neurosci. Methods. 29:171-180.
69. Tu, P.H., G. Elder, R.A. Lazzarini, D. Nelson, J.Q. Trojanowski, and V.M.-Y. Lee. 1995. Overexpression of the human NFM subunit in transgenic mice modifies the level of endogenous NFL and the phosphorylation state of NFH subunits. J. Cell Biol. 129:1629-1640.
70. Ueda, K., H. Fukushima, E. Masliah, Y. Xia, A. Iwai, M. Yoshimoto, DA. Otero, J. Kondo, Y. Ihara, and T. Saitoh. 1993. Molecular cloning of cDNA encoding an unrecognized component of amyloid in Alzheimer disease. Proc. Natl. Acad. Sci. USA. 90:11282-11286.
71. Vila, M., S. Vukosavic, V. Jackson-Lewis, M. Neystat, M. Jakowec, and S. Przedborski. 2000. Alpha-synuclein up-regulation in substantia nigra dopaminergic neurons following administration of the parkinsonian toxin MPTP. J. Neurochem. 74:721-729.
72. Walkley, S.U. 1998. Cellular pathology of lysosomal storage disorders. Brain Pathol. 8:175-193.
73. Webb, J.L., B. Ravikumar, J. Atkins, J.N. Skepper, and D.C. Rubinsztein. 2003. Alpha-synuclein is degraded by both autophagy and the proteasome. J. Biol. Chem. 278:25009-25013.
74. Wilson, C.A., R.W. Doms, H. Zheng, and V.M.-Y. Lee. 2002. Presenilins are not required for A beta 42 production in the early secretory pathway. Nat Neurosci. 5:849-855.
75. Withers, G.S., J.M. George, G.A. Banker, and D.F. Clayton. 1997. Delayed localization of synelfin (synuclein, NACP) to presynaptic terminals in cultured rat hippocampal neurons. Brain Res. Dev. Brain Res. 99:87-94.
76. Wolfe, M.S., M. Citron, T. Diehl, W. Xia, I.O. Donkor, and D.J. Selkoe. 1998. Cellular mechanisms of beta-amyloid production and secretion. J. Med. Chem. 41:6-9.
77. Wong, P.C., H. Zheng, H. Chen, M.W. Becher, D.J. Sirinathsinghji, M.E. Trumbauer, H.Y. Chen, D.L. Price, L.H. Van der Ploeg, and S.S. Sisodia. 1997. Presenilin 1 is required for Notch1 and DII1 expression in the paraxial mesoderm. Nature. 387:288-292.
78. Yoo, A.S., I. Cheng, S. Chung, T.Z. Grenfell, H. Lee, E. Pack-Chung, M. Handler, J. Shen, W. Xia, G. Tesco, et al. 2000. Presenilin-mediated modulation of capacitative calcium entry. Neuron. 27:561-572.