Lysosomal fusion dysfunction as a unifying hypothesis for alzheimers disease pathology

International Journal of Alzheimer's Disease

Volumn , Issue , 2012, Pages

  Funk, Kristen E ^a   Kuret, Jeff ^a  

^a THE OHIO STATE UNIVERSITY COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; TAU PROTEIN;

ALZHEIMER DISEASE; AUTOLYSOSOME; CELL MIGRATION; DEGENERATION; ENDOPLASMIC RETICULUM; GENE CONTROL; GENE MUTATION; GRANULOVACUOLAR DEGENERATION; HUMAN; LYSOSOME; PATHOGENESIS; PRIORITY JOURNAL; REVIEW; UPREGULATION; VESICLE TRAFFICKING DYSFUNCTION;

EID: 84867028097     PISSN: None     EISSN: 20900252     Source Type: Journal    
DOI: 10.1155/2012/752894     Document Type: Review

References (131)

1. Selkoe D. J., The cell biology β -amyloid precursor protein and presenilin in Alzheimer's disease. Trends in Cell Biology 1998 8 11 447 453 2-s2.0-0032211830 10.1016/S0962-8924(98)01363-4 (Pubitemid 28529718)
2. Goedert M., Tau protein and the neurofibrillary pathology of Alzheimer's disease. Trends in Neurosciences 1993 16 11 460 465 2-s2.0-0027420369 (Pubitemid 23313524)
3. Ball M. J., Lo P., Granulovacuolar degeneration in the ageing brain and in dementia. Journal of Neuropathology and Experimental Neurology 1977 36 3 474 487 2-s2.0-0017645498 (Pubitemid 8119548)
4. Holtzman D. M., CSF biomarkers for Alzheimer's disease: current utility and potential future use. Neurobiology of Aging 2011 32 supplement 1 S4 S9
5. Goate A., Chartier-Harlin M. C., Mullan M., Brown J., Crawford F., Fidani L., Giuffra L., Haynes A., Irving N., James L., Mant R., Newton P., Rooke K., Roques P., Talbot C., Pericak-Vance M., Roses A., Williamson R., Hardy J., Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 1991 349 6311 704 706 2-s2.0-0026088977 10.1038/349704a0 (Pubitemid 21912142)
6. Smith M. A., Perry G., Richey P. L., Sayre L. M., Anderson V. E., Beal M. F., Kowall N., Oxidative damage in Alzheimer's. Nature 1996 382 6587 120 121 2-s2.0-0029982815
7. Hasegawa T., Prolonged stress will induce Alzheimer's disease in elderly people by increased release of homocysteic acid. Medical Hypotheses 2007 69 5 1135 1139 2-s2.0-34548772324 10.1016/j.mehy.2007.02.034 (Pubitemid 47432920)
8. Mellman I., Membranes and sorting. Current Opinion in Cell Biology 1996 8 4 497 498 2-s2.0-0030037845 10.1016/S0955-0674(96)80026-3 (Pubitemid 26254045)
9. Vieira A. V., Lamaze C., Schmid S. L., Control of EGF receptor signaling by clathrin-mediated endocytosis. Science 1996 274 5295 2086 2089 2-s2.0-0030461226 10.1126/science.274.5295.2086 (Pubitemid 27020702)
10. Vanlandingham P. A., Ceresa B. P., Rab7 regulates late endocytic trafficking downstream of multivesicular body biogenesis and cargo sequestration. The Journal of Biological Chemistry 2009 284 18 12110 12124 2-s2.0-66449123730 10.1074/jbc.M809277200
11. Hurley J. H., ESCRT complexes and the biogenesis of multivesicular bodies. Current Opinion in Cell Biology 2008 20 1 4 11 2-s2.0-39149132089 10.1016/j.ceb.2007.12.002
12. Saksena S., Sun J., Chu T., Emr S. D., ESCRTing proteins in the endocytic pathway. Trends in Biochemical Sciences 2007 32 12 561 573 2-s2.0-36248991778 10.1016/j.tibs.2007.09.010 (Pubitemid 350123053)
13. Williams R. L., Urbé S., The emerging shape of the ESCRT machinery. Nature Reviews Molecular Cell Biology 2007 8 5 355 368 2-s2.0-34247342216 10.1038/nrm2162 (Pubitemid 46643239)
14. Johnstone R. M., Mathew A., Mason A. B., Teng K., Exosome formation during maturation of mammalian and avian reticulocytes: evidence that exosome release is a major route for externalization of obsolete membrane proteins. Journal of Cellular Physiology 1991 147 1 27 36 2-s2.0-0025890156 (Pubitemid 21910079)
15. Théry C., Zitvogel L., Amigorena S., Exosomes: composition, biogenesis and function. Nature Reviews Immunology 2002 2 8 569 579 2-s2.0-0036676445 (Pubitemid 37328732)
16. Fader C. M., Colombo M. I., Autophagy and multivesicular bodies: two closely related partners. Cell Death and Differentiation 2009 16 1 70 78 2-s2.0-57649195400 10.1038/cdd.2008.168
17. Pankiv S., Clausen T. H., Lamark T., Brech A., Bruun J. A., Outzen H., Overvatn A., Bjorkoy G., Johansen T., p62/SQSTM1 binds directly to Atg8/LC3 to facilitate degradation of ubiquitinated protein aggregates by autophagy. The Journal of Biological Chemistry 2007 282 33 24131 24145 2-s2.0-34548259958 10.1074/jbc.M702824200 (Pubitemid 47328003)
18. Kabeya Y., Mizushima N., Ueno T., Yamamoto A., Kirisako T., Noda T., Kominami E., Ohsumi Y., Yoshimori T., LC3, a mammalian homologue of yeast Apg8p, is localized in autophagosome membranes after processing. EMBO Journal 2000 19 21 5720 5728 2-s2.0-0034329418
19. Dunn W. A. Jr., Studies on the mechanisms of autophagy: maturation of the autophagic vacuole. Journal of Cell Biology 1990 110 6 1935 1945 2-s2.0-0025340880 10.1083/jcb.110.6.1935 (Pubitemid 20183151)
20. Eskelinen E. L., Maturation of autophagic vacuoles in Mammalian cells. Autophagy 2005 1 1 1 10 2-s2.0-26844531363
21. Nixon R. A., Cataldo A. M., Lysosomal system pathways: genes to neurodegeneration in Alzheimer's disease. Journal of Alzheimer's Disease 2006 9 3, supplement 277 289 2-s2.0-33747388358 (Pubitemid 44253321)
22. Nixon R. A., Mathews P. M., Cataldo A. M., The neuronal endosomal-lysosomal system in Alzheimer's disease. Journal of Alzheimer's Disease 2001 3 1 97 107 2-s2.0-0035078189 (Pubitemid 32238256)
23. Ginsberg S. D., Alldred M. J., Counts S. E., Cataldo A. M., Neve R. L., Jiang Y., Wuu J., Chao M. V., Mufson E. J., Nixon R. A., Che S., Microarray analysis of hippocampal CA1 neurons implicates early endosomal dysfunction during Alzheimer's disease progression. Biological Psychiatry 2010 68 10 885 893 2-s2.0-78049427173 10.1016/j.biopsych.2010.05.030
24. Ginsberg S. D., Mufson E. J., Counts S. E., Wuu J., Alldred M. J., Nixon R. A., Che S., Regional selectivity of rab5 and rab7 protein upregulation in mild cognitive impairment and Alzheimer's disease. Journal of Alzheimer's Disease 2010 22 2 631 639 2-s2.0-78650803250 10.3233/JAD-2010-101080
25. Ginsberg S. D., Mufson E. J., Alldred M. J., Counts S. E., Wuu J., Nixon R. A., Che S., Upregulation of select rab GTPases in cholinergic basal forebrain neurons in mild cognitive impairment and Alzheimer's disease. Journal of Chemical Neuroanatomy 2011 42 2 102 110 2-s2.0-79959608500 10.1016/j.jchemneu. 2011.05.012
26. Cataldo A. M., Mathews P. M., Boiteau A. B., Hassinger L. C., Peterhoff C. M., Jiang Y., Mullaney K., Neve R. L., Gruenberg J., Nixon R. A., Down syndrome fibroblast model of Alzheimer-related endosome pathology: accelerated endocytosis promotes late endocytic defects. American Journal of Pathology 2008 173 2 370 384 2-s2.0-48249095748 10.2353/ajpath.2008.071053
27. Cataldo A. M., Peterhoff C. M., Troncoso J. C., Gomez-Isla T., Hyman B. T., Nixon R. A., Endocytic pathway abnormalities precede amyloid β deposition in sporadic Alzheimer's disease and down syndrome: differential effects of APOE genotype and presenilin mutations. American Journal of Pathology 2000 157 1 277 286 2-s2.0-0033869715 (Pubitemid 30641743)
28. Zhang Y. W., Thompson R., Zhang H., Xu H., APP processing in Alzheimer's disease. Molecular Brain 2011 4 1, article 3 2-s2.0-78650944520 10.1186/1756-6606-4-3
29. Hook V., Toneff T., Bogyo M., Greenbaum D., Medzihradszky K. F., Neveu J., Lane W., Hook G., Reisine T., Inhibition of cathepsin B reduces β -amyloid production in regulated secretory vesicles of neuronal chromaffin cells: evidence for cathepsin B as a candidate β -secretase of Alzheimer's disease. Biological Chemistry 2005 386 9 931 940 2-s2.0-26844559355 10.1515/BC.2005.108 (Pubitemid 41448149)
30. Hook V. Y. H., Kindy M., Reinheckel T., Peters C., Hook G., Genetic cathepsin B deficiency reduces β -amyloid in transgenic mice expressing human wild-type amyloid precursor protein. Biochemical and Biophysical Research Communications 2009 386 2 284 288 2-s2.0-67649656100 10.1016/j.bbrc.2009.05.131
31. Benilova I., Karran E., De Strooper B., The toxic Abeta oligomer and Alzheimer's disease: an emperor in need of clothes. Nature Neuroscience 2012 15 3 349 357
32. Prvulovic D., Hampel H., Amyloid β (A β) and phospho-tau (p-tau) as diagnostic biomarkers in Alzheimer's disease. Clinical Chemistry and Laboratory Medicine 2011 49 3 367 374 2-s2.0-79952793175 10.1515/CCLM.2011.087
33. Cataldo A. M., Barnett J. L., Pieroni C., Nixon R. A., Increased neuronal endocytosis and protease delivery to early endosomes in sporadic Alzheimer's disease: neuropathologic evidence for a mechanism of increased β -amyloidogenesis. Journal of Neuroscience 1997 17 16 6142 6151 2-s2.0-0030836345 (Pubitemid 27329890)
34. Cataldo A. M., Petanceska S., Terio N. B., Peterhoff C. M., Durham R., Mercken M., Mehta P. D., Buxbaum J., Haroutunian V., Nixon R. A., A β localization in abnormal endosomes: association with earliest A β elevations in AD and Down syndrome. Neurobiology of Aging 2004 25 10 1263 1272 2-s2.0-4644319713 10.1016/j.neurobiolaging.2004.02.027 (Pubitemid 39299162)
35. Grbovic O. M., Mathews P. M., Jiang Y., Schmidt S. D., Dinakar R., Summers-Terio N. B., Ceresa B. P., Nixon R. A., Cataldo A. M., Rab5-stimulated up-regulation of the endocytic pathway increases intracellular β -cleaved amyloid precursor protein carboxyl-terminal fragment levels and A β production. The Journal of Biological Chemistry 2003 278 33 31261 31268 2-s2.0-0042733013 10.1074/jbc.M304122200 (Pubitemid 36994643)
36. Mathews P. M., Guerra C. B., Jiang Y., Grbovic O. M., Kao B. H., Schmidt S. D., Dinakar R., Mercken M., Hille-Rehfeld A., Rohrer J., Mehta P., Cataldo A. M., Nixon R. A., Alzheimer's disease-related overexpression of the cation-dependent mannose 6-phosphate receptor increases A β secretion: role for altered lysosomal hydrolase distribution in β -amyloidogenesis. The Journal of Biological Chemistry 2002 277 7 5299 5307 2-s2.0-0037085458 10.1074/jbc.M108161200 (Pubitemid 34968574)
37. Nixon R. A., Cataldo A. M., Mathews P. M., The endosomal-lysosomal system of neurons in Alzheimer's disease pathogenesis: a review. Neurochemical Research 2000 25 9-10 1161 1172 2-s2.0-0034304390
38. Yu W. H., Cuervo A. M., Kumar A., Peterhoff C. M., Schmidt S. D., Lee J. H., Mohan P. S., Mercken M., Farmery M. R., Tjernberg L. O., Jiang Y., Duff K., Uchiyama Y., Näslund J., Mathews P. M., Cataldo A. M., Nixon R. A., Macroautophagya novel β -amyloid peptide-generating pathway activated in Alzheimer's disease. Journal of Cell Biology 2005 171 1 87 98 2-s2.0-26444587508 10.1083/jcb.200505082 (Pubitemid 41434604)
39. Arbel M., Yacoby I., Solomon B., Inhibition of amyloid precursor protein processing by β -secretase through site-directed antibodies. Proceedings of the National Academy of Sciences of the United States of America 2005 102 21 7718 7723 2-s2.0-19644368873 10.1073/pnas.0502427102 (Pubitemid 40741037)
40. Huse J. T., Pijak D. S., Leslie G. J., Lee V. M. Y., Doms R. W., Maturation and endosomal targeting of β -site amyloid precursor protein-cleaving enzyme. The Alzheimer's disease β -secretase. The Journal of Biological Chemistry 2000 275 43 33729 33737 2-s2.0-0034721842 10.1074/jbc.M004175200
41. Kametaka S., Shibata M., Moroe K., Kanamori S., Ohsawa Y., Waguri S., Sims P. J., Emoto K., Umeda M., Uchiyama Y., Identification of phospholipid scramblase 1 as a novel interacting molecule with β -secretase (β -site amyloid precursor protein (APP) cleaving enzyme (BACE)). The Journal of Biological Chemistry 2003 278 17 15239 15245 2-s2.0-0038350536 10.1074/jbc.M208611200 (Pubitemid 36799860)
42. Kinoshita A., Fukumoto H., Shah T., Whelan C. M., Irizarry M. C., Hyman B. T., Demonstration by FRET of BACE interaction with the amyloid precursor protein at the cell surface and in early endosomes. Journal of Cell Science 2003 116, part 16 3339 3346 2-s2.0-0042887148 10.1242/jcs.00643 (Pubitemid 37038982)
43. Koh Y. H., von Arnim C. A. F., Hyman B. T., Tanzi R. E., Tesco G., BACE is degraded via the lysosomal pathway. The Journal of Biological Chemistry 2005 280 37 32499 32504 2-s2.0-25444482802 10.1074/jbc.M506199200 (Pubitemid 41361863)
44. Friedrich R. P., Tepper K., Rönicke R., Soom M., Westermann M., Reymann K., Kaether C., Fändrich M., Mechanism of amyloid plaque formation suggests an intracellular basis of A β pathogenicity. Proceedings of the National Academy of Sciences of the United States of America 2010 107 5 1942 1947 2-s2.0-76649116890 10.1073/pnas.0904532106
45. Koo E. H., Squazzo S. L., Evidence that production and release of amyloid β -protein involves the endocytic pathway. The Journal of Biological Chemistry 1994 269 26 17386 17389 2-s2.0-0028276801 (Pubitemid 24218009)
46. McConlogue L., Castellano F., deWit C., Schenk D., Maltese W. A., Differential effects of a Rab6 mutant on secretory versus amyloidogenic processing of Alzheimer's β -amyloid precursor protein. The Journal of Biological Chemistry 1996 271 3 1343 1348 2-s2.0-0030064136 10.1074/jbc.271.3. 1343 (Pubitemid 26028615)
47. Schellenberg G. D., Montine T. J., The genetics and neuropathology of Alzheimer's disease. Acta Neuropathologica 2012 124 3 305 323
48. Takasugi N., Tomita T., Hayashi I., Tsuruoka M., Niimura M., Takahashi Y., Thinakaran G., Iwatsubo T., The role of presenilin cofactors in the γ -secratase complex. Nature 2003 422 6930 438 441 2-s2.0-0037468759 10.1038/nature01506 (Pubitemid 36411397)
49. Kimberly W. T., LaVoie M. J., Ostaszewski B. L., Ye W., Wolfe M. S., Selkoe D. J., γ -Secretase is a membrane protein complex comprised of presenilin, nicastrin, aph-1, and pen-2. Proceedings of the National Academy of Sciences of the United States of America 2003 100 11 6382 6387 2-s2.0-0038652102 10.1073/pnas.1037392100 (Pubitemid 36666590)
50. Cupers P., Bentahir M., Craessaerts K., Orlans I., Vanderstichele H., Saftig P., De Strooper B., Annaert W., The discrepancy between presenilin subcellular localization and γ -secretase processing of amyloid precursor protein. Journal of Cell Biology 2001 154 4 731 740 2-s2.0-0035921427 10.1083/jcb.200104045 (Pubitemid 34292955)
51. Kovacs D. M., Fausett H. J., Page K. J., Kim T. W., Moir R. D., Merriam D. E., Hollister R. D., Hallmark' O. G., Mancini R., Felsenstein K. M., Hyman B. T., Tanzi R. E., Wasco W., Alzheimer-associated presenilins 1 and 2: neuronal expression in brain and localization to intracellular membranes in mammalian cells. Nature Medicine 1996 2 2 224 229 2-s2.0-13344282063 10.1038/nm0296-224 (Pubitemid 26057557)
52. Scheuner D., Eckman C., Jensen M., Song X., Citron M., Suzuki N., Bird T. D., Hardy J., Hutton M., Kukull W., Larson E., Levy-Lahad E., Viitanen M., Peskind E., Poorkaj P., Schellenberg G., Tanzi R., Wasco W., Lannfelt L., Selkoe D., Younkin S., Secreted amyloid β -protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease. Nature Medicine 1996 2 8 864 870 2-s2.0-16044373524 10.1038/nm0896-864 (Pubitemid 26296755)
53. Borchelt D. R., Thinakaran G., Eckman C. B., Lee M. K., Davenport F., Ratovitsky T., Prada C. M., Kim G., Seekins S., Yager D., Slunt H. H., Wang R., Seeger M., Levey A. I., Gandy S. E., Copeland N. G., Jenkins N. A., Price D. L., Younkin S. G., Sisodia S. S., Familial Alzheimer's disease-linked presenilin I variants elevate a β 1- 42/1-40 ratio in vitro and in vivo. Neuron 1996 17 5 1005 1013 2-s2.0-0030293676 10.1016/S0896-6273(00)80230-5 (Pubitemid 26424026)
54. Cai D., Leem J. Y., Greenfield J. P., Wang P., Kim B. S., Wang R., Lopes K. O., Kim S. H., Zheng H., Greengard P., Sisodia S. S., Thinakaran G., Xu H., Presenilin-1 regulates intracellular trafficking and cell surface delivery of β -amyloid precursor protein. The Journal of Biological Chemistry 2003 278 5 3446 3454 2-s2.0-0037474287 10.1074/jbc.M209065200 (Pubitemid 36801261)
55. Dumanchin C., Czech C., Campion D., Cuif M. H., Poyot T., Martin C., Charbonnier F., Goud B., Pradier L., Frebourg T., Presenilins interact with Rab11, a small GTPase involved in the regulation of vesicular transport. Human Molecular Genetics 1999 8 7 1263 1269 2-s2.0-0032787598 10.1093/hmg/8.7.1263 (Pubitemid 29328995)
56. Scheper W., Zwart R., Baas F., Rab6 membrane association is dependent of Presenilin 1 and cellular phosphorylation events. Molecular Brain Research 2004 122 1 17 23 2-s2.0-1342306722 10.1016/j.molbrainres.2003.11.013 (Pubitemid 38264543)
57. Scheper W., Zwart R., van der Sluijs P., Annaert W., van Gool W. A., Baas F., Alzheimer's presenilin 1 is a putative membrane receptor for rab GDP dissociation inhibitor. Human Molecular Genetics 2000 9 2 303 310 2-s2.0-0033958665 (Pubitemid 30052754)
58. Lee J. H., Yu W. H., Kumar A., Lee S., Mohan P. S., Peterhoff C. M., Wolfe D. M., Martinez-Vicente M., Massey A. C., Sovak G., Uchiyama Y., Westaway D., Cuervo A. M., Nixon R. A., Lysosomal proteolysis and autophagy require presenilin 1 and are disrupted by Alzheimer-related PS1 mutations. Cell 2010 141 7 1146 1158 2-s2.0-77953913051 10.1016/j.cell.2010.05.008
59. Yamamoto A., Tagawa Y., Yoshimori T., Moriyama Y., Masaki R., Tashiro Y., Bafilomycin A1 prevents maturation of autophagic vacuoles by inhibiting fusion between autophagosomes and lysosomes in rat hepatoma cell line, H-4-II-E cells. Cell Structure and Function 1998 23 1 33 42 2-s2.0-0031593675 (Pubitemid 28223394)
60. Zhang X., Garbett K., Veeraraghavalu K., A role for presenilins in autophagy revisited: normal acidification of Lysosomes in cells lacking PSEN1 and PSEN2. Journal of Neuroscience 2012 32 25 8633 8648
61. Coen K., Flannagan R. S., Baron S., Lysosomal calcium homeostasis defects, not proton pump defects, cause endo-lysosomal dysfunction in PSEN-deficient cells. Journal of Cell Biology 2012 198 1 23 35
62. 2+ in late endosome-lysosome heterotypic fusion and in the reformation of lysosomes from hybrid organelles. Journal of Cell Biology 2000 149 5 1053 1062 2-s2.0-0034729167 10.1083/jcb.149.5.1053 (Pubitemid 30354255)
63. 2+ signalling in health and disease. Biochemical Journal 2011 439 3 349 374
64. Harold D., Abraham R., Hollingworth P., Genome-wide association study identifies variants at CLU and PICALM associated with Alzheimer's disease. Nature Genetics 2009 41 10 1088 1093 2-s2.0-70349558631
65. Lambert J. C., Heath S., Even G., Genome-wide association study identifies variants at CLU and CR1 associated with Alzheimer's disease. Nature Genetics 2009 41 10 1094 1099
66. Mahley R. W., Rall S. C. Jr., Apolipoprotein E: far more than a lipid transport protein. Annual Review of Genomics and Human Genetics 2000 1 2000 507 537 2-s2.0-0034575124
67. Mahley R. W., Weisgraber K. H., Huang Y., Apolipoprotein E: structure determines function, from atherosclerosis to Alzheimer's disease to AIDS. Journal of Lipid Research 2009 50, supplement S183 S188 2-s2.0-66349085616 10.1194/jlr.R800069-JLR200
68. Rogaeva E., Meng Y., Lee J. H., Gu Y., Kawarai T., Zou F., Katayama T., Baldwin C. T., Cheng R., Hasegawa H., Chen F., Shibata N., Lunetta K. L., Pardossi-Piquard R., Bohm C., Wakutani Y., Cupples L. A., Cuenco K. T., Green R. C., Pinessi L., Rainero I., Sorbi S., Bruni A., Duara R., Friedland R. P., Inzelberg R., Hampe W., Bujo H., Song Y. Q., Andersen O. M., Willnow T. E., Graff-Radford N., Petersen R. C., Dickson D., Der S. D., Fraser P. E., Schmitt-Ulms G., Younkin S., Mayeux R., Farrer L. A., George -. P. S., The neuronal sortilin-related receptor SORL1 is genetically associated with Alzheimer disease. Nature Genetics 2007 39 2 168 177 2-s2.0-33846613222 10.1038/ng1943 (Pubitemid 46184347)
69. Seshadri S., Fitzpatrick A. L., Ikram M. A., Genome-wide analysis of genetic loci associated with Alzheimer disease. The Journal of the American Medical Association 2010 303 18 1832 1840
70. Jones L., Harold D., Williams J., Genetic evidence for the involvement of lipid metabolism in Alzheimer's disease. Biochimica et Biophysica Acta 2010 1801 8 754 761 2-s2.0-77953283403 10.1016/j.bbalip.2010.04.005
71. Nuutinen T., Suuronen T., Kauppinen A., Salminen A., Clusterin: a forgotten player in Alzheimer's disease. Brain Research Reviews 2009 61 2 89 104 2-s2.0-70349557788 10.1016/j.brainresrev.2009.05.007
72. Kim W., Lee S., Hall G. F., Secretion of human tau fragments resembling CSF-tau in Alzheimer's disease is modulated by the presence of the exon 2 insert. FEBS Letters 2010 584 14 3085 3088 2-s2.0-77954176744 10.1016/j.febslet.2010.05.042
73. Kim W., Lee S., Jung C., Ahmed A., Lee G., Hall G. F., Interneuronal transfer of human tau between lamprey central neurons in situ. Journal of Alzheimer's Disease 2010 19 2 647 664 2-s2.0-77049123465 10.3233/JAD-2010-1273
74. Emmanouilidou E., Melachroinou K., Roumeliotis T., Garbis S. D., Ntzouni M., Margaritis L. H., Stefanis L., Vekrellis K., Cell-produced α -synuclein is secreted in a calcium-dependent manner by exosomes and impacts neuronal survival. Journal of Neuroscience 2010 30 20 6838 6851 2-s2.0-77952648551 10.1523/JNEUROSCI.5699-09.2010
75. Fevrier B., Vilette D., Archer F., Loew D., Faigle W., Vidal M., Laude H., Raposo G., Cells release prions in association with exosomes. Proceedings of the National Academy of Sciences of the United States of America 2004 101 26 9683 9688 2-s2.0-3042788972 10.1073/pnas.0308413101 (Pubitemid 38869296)
76. Rajendran L., Honsho M., Zahn T. R., Keller P., Geiger K. D., Verkade P., Simons K., Alzheimer's disease β -amyloid peptides are released in association with exosomes. Proceedings of the National Academy of Sciences of the United States of America 2006 103 30 11172 11177 2-s2.0-33746593662 10.1073/pnas.0603838103 (Pubitemid 44156491)
77. Saman S., Kim W., Raya M., Exosome-associated tau is secreted in tauopathy models and is selectively phosphorylated in cerebrospinal fluid in early Alzheimer disease. The Journal of Biological Chemistry 2012 287 6 3842 3849
78. Braak H., Alafuzoff I., Arzberger T., Kretzschmar H., Del Tredici K., Staging of Alzheimer disease-associated neurofibrillary pathology using paraffin sections and immunocytochemistry. Acta Neuropathologica 2006 112 4 389 404 2-s2.0-33749150163 10.1007/s00401-006-0127-z (Pubitemid 44469160)
79. Lee S., Kim W., Li Z., Hall G. F., Accumulation of vesicle-associated human tau in distal dendrites drives degeneration and tau secretion in an in situ cellular tauopathy model. International Journal of Alzheimer's Disease 2012 2012 16 172837 10.1155/2012/172837
80. Sverdlov M., Shajahan A. N., Minshall R. D., Tyrosine phosphorylation-dependence of caveolae-mediated endocytosis. Journal of Cellular and Molecular Medicine 2007 11 6 1239 1250 2-s2.0-38149085899 10.1111/j.1582-4934.2007.00127.x
81. Nickel W., Unconventional secretory routes: direct protein export across the plasma membrane of mammalian cells. Traffic 2005 6 8 607 614 2-s2.0-21844468743 10.1111/j.1600-0854.2005.00302.x (Pubitemid 40959689)
82. Fang Y., Wu N., Gan X., Yan W., Morrell J. C., Gould S. J., Higher-order oligomerization targets plasma membrane proteins and HIV gag to exosomes. PLoS Biology 2007 5 6, article e158 2-s2.0-38449122190 10.1371/journal.pbio.0050158 (Pubitemid 46919948)
83. Dolan P. J., Johnson G. V. W., A caspase cleaved form of tau is preferentially degraded through the autophagy pathway. The Journal of Biological Chemistry 2010 285 29 21978 21987 2-s2.0-77954571538 10.1074/jbc.M110.110940
84. Armstrong R. A., Cairns N. J., Lantos P. L., Clustering of Pick bodies in patients with Pick's disease. Neuroscience Letters 1998 242 2 81 84 2-s2.0-0032512868 10.1016/S0304-3940(98)00052-4 (Pubitemid 28082998)
85. Armstrong R. A., Cairns N. J., Lantos P. L., Clustering of cerebral cortical lesions in patients with corticobasal degeneration. Neuroscience Letters 1999 268 1 5 8 2-s2.0-0033546079 10.1016/S0304-3940(99)00309-2 (Pubitemid 29292531)
86. Braak H., Braak E., Neuropathological stageing of Alzheimer-related changes. Acta Neuropathologica 1991 82 4 239 259 2-s2.0-0025863618
87. Gómez-Ramos A., Díaz-Hernández M., Cuadros R., Hernández F., Avila J., Extracellular tau is toxic to neuronal cells. FEBS Letters 2006 580 20 4842 4850 2-s2.0-33747862732 10.1016/j.febslet.2006.07. 078 (Pubitemid 44286844)
88. Gómez-Ramos A., Díaz-Hernández M., Rubio A., Miras-Portugal M. T., Avila J., Extracellular tau promotes intracellular calcium increase through M1 and M3 muscarinic receptors in neuronal cells. Molecular and Cellular Neuroscience 2008 37 4 673 681 2-s2.0-41149111293 10.1016/j.mcn.2007.12.010
89. Strauss K., Goebel C., Runz H., Möbius W., Weiss S., Feussner I., Simons M., Schneider A., Exosome secretion ameliorates lysosomal storage of cholesterol in Niemann-Pick type C disease. The Journal of Biological Chemistry 2010 285 34 26279 26288 2-s2.0-77956193128 10.1074/jbc.M110.134775
90. Bednarski E., Lynch G., Cytosolic proteolysis of τ by cathepsin D in hippocampus following suppression of cathepsins B and L. Journal of Neurochemistry 1996 67 5 1846 1855 2-s2.0-0029845397 (Pubitemid 26349657)
91. Kenessey A., Nacharaju P., Ko L. W., Yen S. H., Degradation of tau by lysosomal enzyme cathepsin D: implication for Alzheimer neurofibrillary degeneration. Journal of Neurochemistry 1997 69 5 2026 2038 2-s2.0-0030774852 (Pubitemid 27452750)
92. Bendiske J., Bahr B. A., Lysosomal activation is a compensatory response against protein accumulation and associated synaptopathogenesisan approach for slowing Alzheimer disease? Journal of Neuropathology and Experimental Neurology 2003 62 5 451 463 2-s2.0-0037989761 (Pubitemid 36560187)
93. Ii K., Ito H., Kominami E., Hirano A., Abnormal distribution of cathepsin proteinases and endogenous inhibitors (cystatins) in the hippocampus of patients with Alzheimer's disease, parkinsonism-dementia complex on Guam, and senile dementia and in the aged. Virchows Archiv A 1993 423 3 185 194 2-s2.0-0027378622 (Pubitemid 23309333)
94. Ikeda K., Akiyama H., Arai T., Kondo H., Haga C., Iritani S., Tsuchiya K., Alz-50/Gallyas-positive lysosome-like intraneuronal granules in Alzheimer's disease and control brains. Neuroscience Letters 1998 258 2 113 116 2-s2.0-0032545149 10.1016/S0304-3940(98)00867-2 (Pubitemid 28566187)
95. Congdon E. E., Kim S., Bonchak J., Songrug T., Matzavinos A., Kuret J., Nucleation-dependent tau filament formation: the importance of dimerization and an estimation of elementary rate constants. The Journal of Biological Chemistry 2008 283 20 13806 13816 2-s2.0-46649101161 10.1074/jbc.M800247200
96. Zhong Q., Congdon E. E., Nagaraja H. N., Kuret J., Tau isoform composition influences rate and extent of filament formation. The Journal of Biological Chemistry 2012 287 24 20711 20719
97. Dickey C. A., Kamal A., Lundgren K., Klosak N., Bailey R. M., Dunmore J., Ash P., Shoraka S., Zlatkovic J., Eckman C. B., Patterson C., Dickson D. W., Nahman N. S., Hutton M., Burrows F., Petrucelli L., The high-affinity HSP90-CHIP complex recognizes and selectively degrades phosphorylated tau client proteins. The Journal of Clinical Investigation 2007 117 3 648 658 2-s2.0-33847369469 10.1172/JCI29715 (Pubitemid 46348523)
98. Luo W., Dou F., Rodina A., Chip S., Kim J., Zhao Q., Moulick K., Aguirre J., Wu N., Greengard P., Chiosis G., Roles of heat-shock protein 90 in maintaining and facilitating the neurodegenerative phenotype in tauopathies. Proceedings of the National Academy of Sciences of the United States of America 2007 104 22 9511 9516 2-s2.0-34547183507 10.1073/pnas.0701055104 (Pubitemid 47185810)
99. Wang Y., Martinez-Vicente M., Krüger U., Kaushik S., Wong E., Mandelkow E. M., Cuervo A. M., Mandelkow E., Tau fragmentation, aggregation and clearance: the dual role of lysosomal processing. Human Molecular Genetics 2009 18 21 4153 4170 2-s2.0-70349987102 10.1093/hmg/ddp367
100. Wang Y. P., Biernat J., Pickhardt M., Mandelkow E., Mandelkow E. M., Stepwise proteolysis liberates tau fragments that nucleate the Alzheimer-like aggregation of full-length tau in a neuronal cell model. Proceedings of the National Academy of Sciences of the United States of America 2007 104 24 10252 10257 2-s2.0-34547203592 10.1073/pnas.0703676104 (Pubitemid 47175295)
101. Samsonov A., Yu J. Z., Rasenick M., Popov S. V., Tau interaction with microtubules in vivo. Journal of Cell Science 2004 117, part 25 6129 6141 2-s2.0-12344301460 10.1242/jcs.01531 (Pubitemid 40123977)
102. Dixit R., Ross J. L., Goldman Y. E., Holzbaur E. L. F., Differential regulation of dynein and kinesin motor proteins by tau. Science 2008 319 5866 1086 1089 2-s2.0-39749165656 10.1126/science.1152993 (Pubitemid 351300789)
103. Kapitein L. C., Schlager M. A., Kuijpers M., Wulf P. S., van Spronsen M., MacKintosh F. C., Hoogenraad C. C., Mixed microtubules steer dynein-driven cargo transport into dendrites. Current Biology 2010 20 4 290 299 2-s2.0-76749162221 10.1016/j.cub.2009.12.052
104. Love S., Bridges L. R., Case C. P., Neurofibrillary tangles in Niemann-Pick disease type C. Brain 1995 118, part 1 119 129 2-s2.0-0028929548
105. Almos P. Z., Horvath S., Czibula A., H1 tau haplotype-related genomic variation at 17q21.3 as an Asian heritage of the European Gypsy population. Heredity 2008 101 5 416 419 2-s2.0-54349094729 10.1038/hdy.2008.70
106. Neve R. L., Harris P., Kosik K. S., Kurnit D. M., Donlon T. A., Identification of cDNA clones for the human microtubule-associated protein tau and chromosomal localization of the genes for tau and microtubule-associated protein 2. Brain Research 1986 387 3 271 280 2-s2.0-0022827447 (Pubitemid 17220131)
107. Brandt R., Léger J., Lee G., Interaction of tau with the neural plasma membrane mediated by tau's amino-terminal projection domain. Journal of Cell Biology 1995 131 5 1327 1340 2-s2.0-0028785525 10.1083/jcb.131.5.1327
108. Abraha A., Ghoshal N., Gamblin T. C., Cryns V., Berry R. W., Kuret J., Binder L. I., C-terminal inhibition of tau assembly in vitro and in Alzheimer's disease. Journal of Cell Science 2000 113, 3737 3745 2-s2.0-0033677809
109. Haase C., Stieler J. T., Arendt T., Holzer M., Pseudophosphorylation of tau protein alters its ability for self-aggregation. Journal of Neurochemistry 2004 88 6 1509 1520 2-s2.0-1642280378 (Pubitemid 38366927)
110. Liu F., Li B., Tung E. J., Grundke-Iqbal I., Iqbal K., Gong C. X., Site-specific effects of tau phosphorylation on its microtubule assembly activity and self-aggregation. European Journal of Neuroscience 2007 26 12 3429 3436 2-s2.0-36949040819 10.1111/j.1460-9568.2007.05955.x (Pubitemid 350243526)
111. Vanderstichele H., De Vreese K., Blennow K., Andreasen N., Sindic C., Ivanoiu A., Hampel H., Bürger K., Parnetti L., Lanari A., Padovani A., DiLuca M., Bläser M., Ohrfelt Olsson A., Pottel H., Hulstaert F., Vanmechelen E., Analytical performance and clinical utility of the INNOTEST PHOSPHO-TAU(181P) assay for discrimination between Alzheimer's disease and dementia with Lewy bodies. Clinical Chemistry and Laboratory Medicine 2006 44 12 1472 1480 2-s2.0-33845713197 10.1515/CCLM.2006.258 (Pubitemid 44967698)
112. Smith D. H., Meaney D. F., Shull W. H., Diffuse axonal injury in head trauma. Journal of Head Trauma Rehabilitation 2003 18 4 307 316 2-s2.0-0041807587 (Pubitemid 36899043)
113. Buée L., Bussière T., Buée-Scherrer V., Delacourte A., Hof P. R., Tau protein isoforms, phosphorylation and role in neurodegenerative disorders. Brain Research Reviews 2000 33 1 95 130 2-s2.0-0033850407 10.1016/S0165-0173(00)00019-9
114. Martin L., Latypova X., Terro F., Post-translational modifications of tau protein: implications for Alzheimer's disease. Neurochemistry International 2011 58 4 458 471 2-s2.0-79952105548 10.1016/j.neuint.2010.12.023
115. Morishima-Kawashima M., Hasegawa M., Takio K., Suzuki M., Titani K., Ihara Y., Ubiquitin is conjugated with amino-terminally processed tau in paired helical filaments. Neuron 1993 10 6 1151 1160 2-s2.0-0027193036 10.1016/0896-6273(93)90063-W (Pubitemid 23194405)
116. Cripps D., Thomas S. N., Jeng Y., Yang F., Davies P., Yang A. J., Alzheimer disease-specific conformation of hyperphosphorylated paired helical filament-Tau is polyubiquitinated through Lys-48, Lys-11, and Lys-6 ubiquitin conjugation. The Journal of Biological Chemistry 2006 281 16 10825 10838 2-s2.0-33744950091 10.1074/jbc.M512786200 (Pubitemid 43855505)
117. Thomas S. N., Funk K. E., Wan Y., Dual modification of Alzheimer's disease PHF-tau protein by lysine methylation and ubiquitylation: a mass spectrometry approach. Acta Neuropathologica 2012 123 1 105 117
118. Raiborg C., Rusten T. E., Stenmark H., Protein sorting into multivesicular endosomes. Current Opinion in Cell Biology 2003 15 4 446 455 2-s2.0-0042174019 10.1016/S0955-0674(03)00080-2 (Pubitemid 36928047)
119. Chau V., Tobias J. W., Bachmair A., Marriott D., Ecker D. J., Gonda D. K., Varshavsky A., A multiubiquitin chain is confined to specific lysine in a targeted short-lived protein. Science 1989 243 4898 1576 1583 2-s2.0-0024514688 (Pubitemid 19090506)
120. Cohen T. J., Guo J. L., Hurtado D. E., Kwong L. K., Mills I. P., Trojanowski J. Q., Lee V. M. Y., The acetylation of tau inhibits its function and promotes pathological tau aggregation. Nature Communications 2011 2 1, article 252 2-s2.0-79953087890 10.1038/ncomms1255
121. Min S. W., Cho S. H., Zhou Y., Schroeder S., Haroutunian V., Seeley W. W., Huang E. J., Shen Y., Masliah E., Mukherjee C., Meyers D., Cole P. A., Ott M., Gan L., Acetylation of tau inhibits its degradation and contributes to tauopathy. Neuron 2010 67 6 953 966 2-s2.0-77957001697 10.1016/j.neuron.2010.08. 044
122. Latham J. A., Dent S. Y. R., Cross-regulation of histone modifications. Nature Structural and Molecular Biology 2007 14 11 1017 1024 2-s2.0-35848936709 10.1038/nsmb1307 (Pubitemid 350060331)
123. Ball M. J., Neuronal loss, neurofibrillary tangles and granulovacuolar degeneration in the hippocampus with ageing and dementia. A quantitative study. Acta Neuropathologica 1977 37 2 111 118 2-s2.0-0017358355 (Pubitemid 8047060)
124. Ghoshal N., García-Sierra F., Wuu J., Leurgans S., Bennett D. A.,
125. Okamoto K., Hirai S., Iizuka T., Yanagisawa T., Watanabe M., Reexamination of granulovacuolar degeneration. Acta Neuropathologica 1991 82 5 340 345 2-s2.0-0026051511 10.1007/BF00296544
126. Funk K. E., Mrak R. E., Kuret J., Granulovacuolar degeneration (GVD) bodies of Alzheimer's disease (AD) resemble late-stage autophagic organelles. Neuropathology and Applied Neurobiology 2011 37 3 295 306 2-s2.0-79951790558 10.1111/j.1365-2990.2010.01135.x
127. Yamazaki Y., Takahashi T., Hiji M., Kurashige T., Izumi Y., Yamawaki T., Matsumoto M., Immunopositivity for ESCRT-III subunit CHMP2B in granulovacuolar degeneration of neurons in the Alzheimer's disease hippocampus. Neuroscience Letters 2010 477 2 86 90 2-s2.0-77953293462 10.1016/j.neulet.2010.04.038
128. Boland B., Kumar A., Lee S., Platt F. M., Wegiel J., Yu W. H., Nixon R. A., Autophagy induction and autophagosome clearance in neurons: relationship to autophagic pathology in Alzheimer's disease. Journal of Neuroscience 2008 28 27 6926 6937 2-s2.0-49049096562 10.1523/JNEUROSCI.0800-08.2008
129. Chen L. Q., Wei J. S., Lei Z. N., Zhang L. M., Liu Y., Sun F. Y., Induction of Bcl-2 and Bax was related to hyperphosphorylation of tau and neuronal death induced by okadaic acid in rat brain. Anatomical Record A 2005 287 2 1236 1245 2-s2.0-29444446905 10.1002/ar.a.20241 (Pubitemid 43010434)
130. Díaz-Troya S., Pérez-Pérez M. E., Florencio F. J., Crespo J. L., The role of TOR in autophagy regulation from yeast to plants and mammals. Autophagy 2008 4 7 851 865 2-s2.0-53549113031
131. Soliman G. A., Acosta-Jaquez H. A., Dunlop E. A., Ekim B., Maj N. E., Tee A. R., Fingar D. C., mTOR Ser-2481 autophosphorylation monitors mTORC-specific catalytic activity and clarifies rapamycin mechanism of action. The Journal of Biological Chemistry 2010 285 11 7866 7879 2-s2.0-77950900079 10.1074/jbc.M109.096222