Levels of kinesin light chain and dynein intermediate chain are reduced in the frontal cortex in Alzheimer's disease: Implications for axoplasmic transport

Acta Neuropathologica

Volumn 123, Issue 1, 2012, Pages 71-84

  Morel, Marina ^a   Héraud, Céline ^a   Nicaise, Charles ^a   Suain, Valérie ^a   Brion, Jean Pierre ^a  

^a UNIVERSITÉ LIBRE DE BRUXELLES   (Belgium)

Author keywords

Alzheimer's disease; Dynein intermediate chain; GSK 3 ; Kinesin light chain; Neurofibrillary tangles

Indexed keywords

AMYLOID BETA PROTEIN; BETA TUBULIN; DYNEIN ADENOSINE TRIPHOSPHATASE; DYNEIN INTERMEDIATE CHAIN; GLYCOGEN SYNTHASE KINASE 3BETA; KINESIN; KINESIN LIGHT CHAIN 1; KINESIN LIGHT CHAIN 2; MESSENGER RNA; SYNAPTOPHYSIN; TAU PROTEIN; TUBULIN BETA3; UNCLASSIFIED DRUG;

AGED; ALZHEIMER DISEASE; ARTICLE; AXOPLASM FLOW; CEREBELLUM CORTEX; CONTROLLED STUDY; FEMALE; FRONTAL CORTEX; GENE EXPRESSION; HUMAN; HUMAN CELL; HUMAN TISSUE; IMMUNOBLOTTING; IMMUNOREACTIVITY; MALE; NEUROFIBRILLARY TANGLE; NEUROPATHOLOGY; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PHOSPHORYLATION;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AXONAL TRANSPORT; CELL LINE; CEREBELLAR CORTEX; DYNEINS; FEMALE; FRONTAL LOBE; GLYCOGEN SYNTHASE KINASE 3; HUMANS; KINESIN; MALE; NEUROFIBRILLARY TANGLES; SYNAPTOPHYSIN; TAU PROTEINS;

EID: 84857034149     PISSN: 00016322     EISSN: 14320533     Source Type: Journal    
DOI: 10.1007/s00401-011-0901-4     Document Type: Article

References (52)

1. R Adalbert A Nogradi E Babetto, et al. 2009 Severely dystrophic axons at amyloid plaques remain continuous and connected to viable cell bodies Brain 132 402 416 19059977 10.1093/brain/awn312
2. ME Andersson A Sjolander N Andreasen, et al. 2007 Kinesin gene variability may affect tau phosphorylation in early Alzheimer's disease Int J Mol Med 20 233 239 17611642 1:CAS:528:DC%2BD2sXpt1egsr0%3D
3. J Bain L Plater M Elliott, et al. 2007 The selectivity of protein kinase inhibitors: a further update Biochem J 408 297 315 17850214 10.1042/BJ20070797 1:CAS:528:DC%2BD2sXhtlGmtbjE
4. KL Barrett JM Willingham AJ Garvin MC Willingham 2001 Advances in cytochemical methods for detection of apoptosis J Histochem Cytochem 49 821 832 11410607 10.1177/002215540104900703 1:CAS:528:DC%2BD3MXltVWks7w%3D (Pubitemid 32565976)
5. A Boutajangout M Authelet V Blanchard, et al. 2004 Characterisation of cytoskeletal abnormalities in mice transgenic for wild-type human tau and familial Alzheimer's disease mutants of APP and presenilin-1 Neurobiol Dis 15 47 60 14751770 10.1016/j.nbd.2003.09.007 1:CAS:528:DC%2BD2cXntVOhsg%3D%3D (Pubitemid 38134380)
6. H Braak E Braak 1991 Neuropathological stageing of Alzheimer-related changes Acta Neuropathol (Berl) 82 239 259 10.1007/BF00308809 1:STN:280:DyaK387gtFOiug%3D%3D
7. ST Brady 1985 A novel brain ATPase with properties expected for the fast axonal transport motor Nature 317 73 75 2412134 10.1038/317073a0 1:CAS:528:DyaL2MXlvFWqsbk%3D (Pubitemid 15016692)
8. Brion JP (2006) Cellular changes in Alzheimer's disease, Chap 92. In: Pathy MSJ, Sinclair AJ, Morley JE (eds) Principles and practice of geriatric medicine. Wiley, Chicester, pp 1073-1081
9. JP Brion DP Hanger AM Couck BH Anderton 1991 A68 proteins in Alzheimer's disease are composed of several tau isoforms in a phosphorylated state which affects their electrophoretic mobilities Biochem.J. 279 831 836 1953678 1:CAS:528:DyaK3MXmsFehur0%3D
10. JP Brion DP Hanger MT Bruce AM Couck J Flament-Durand BH Anderton 1991 Tau in Alzheimer neurofibrillary tangles. N- and C-terminal regions are differentially associated with paired helical filaments and the location of a putative abnormal phosphorylation site Biochem J 273 Pt 1 127 133 1899184 1:CAS:528:DyaK3MXktVelsg%3D%3D
11. M Coleman 2005 Axon degeneration mechanisms: commonality amid diversity Nat Rev Neurosci 6 889 898 16224497 10.1038/nrn1788 1:CAS:528:DC%2BD2MXhtFKls7bN (Pubitemid 41568730)
12. I Cuchillo-Ibanez A Seereeram HL Byers, et al. 2008 Phosphorylation of tau regulates its axonal transport by controlling its binding to kinesin FASEB J 22 3186 3195 18511549 10.1096/fj.08-109181 1:CAS:528:DC%2BD1cXhtV2rurrL
13. KJ De Vos AJ Grierson S Ackerley CC Miller 2008 Role of axonal transport in neurodegenerative diseases Annu Rev Neurosci 31 151 173 18558852 10.1146/annurev.neuro.31.061307.090711
14. CM Dhaenens E Van Brussel S Schraen-Maschke F Pasquier A Delacourte B Sablonniere 2004 Association study of three polymorphisms of kinesin light-chain 1 gene with Alzheimer's disease Neurosci Lett 368 290 292 15364413 10.1016/j.neulet.2004.07.040 1:CAS:528:DC%2BD2cXnsFGmtbg%3D (Pubitemid 39214970)
15. R Dixit JL Ross YE Goldman EL Holzbaur 2008 Differential regulation of dynein and kinesin motor proteins by tau Science 319 1086 1089 18202255 10.1126/science.1152993 1:CAS:528:DC%2BD1cXit1yhsbo%3D (Pubitemid 351300789)
16. BW Doble S Patel GA Wood LK Kockeritz JR Woodgett 2007 Functional redundancy of GSK-3alpha and GSK-3beta in Wnt/beta-catenin signaling shown by using an allelic series of embryonic stem cell lines Dev Cell 12 957 971 17543867 10.1016/j.devcel.2007.04.001 1:CAS:528:DC%2BD2sXmsFentrg%3D (Pubitemid 46805920)
17. J Du Y Wei L Liu, et al. 2010 A kinesin signaling complex mediates the ability of GSK-3beta to affect mood-associated behaviors Proc Natl Acad Sci USA 107 11573 11578 20534517 10.1073/pnas.0913138107 1:CAS:528:DC%2BC3cXot1eksL0%3D
18. Dustin P, Flament-Durand J (1982) Disturbances of axoplasmic transport in Alzheimer's disease. In: Weiss DG, Gorio A (eds) Axoplasmic transport in physiology and pathology. Springer, Berlin, pp 131-136
19. TL Falzone GB Stokin C Lillo, et al. 2009 Axonal stress kinase activation and Tau misbehavior induced by Kinesin-1 transport defects J Neurosci 29 5758 5767 19420244 10.1523/JNEUROSCI.0780-09.2009 1:CAS:528:DC%2BD1MXlvVGnsbo%3D
20. JE Hamos LJ DeGennaro DA Drachman 1989 Synaptic loss in Alzheimer's disease and other dementias Neurology 39 355 361 2927643 1:STN:280: DyaL1M7ot1Ckug%3D%3D (Pubitemid 19094725)
21. PJ Hollenbeck WM Saxton 2005 The axonal transport of mitochondria J Cell Sci 118 5411 5419 16306220 10.1242/jcs.02745 1:CAS:528:DC%2BD28XjvFOitw%3D%3D (Pubitemid 43079283)
22. C Hooper R Killick S Lovestone 2008 The GSK3 hypothesis of Alzheimer's disease J Neurochem 104 1433 1439 18088381 10.1111/j.1471-4159.2007.05194.x 1:CAS:528:DC%2BD1cXkt1Citbw%3D (Pubitemid 351316776)
23. NM Kanaan GA Morfini NE LaPointe, et al. 2011 Pathogenic forms of tau inhibit kinesin-dependent axonal transport through a mechanism involving activation of axonal phosphotransferases J Neurosci 31 9858 9868 21734277 10.1523/JNEUROSCI.0560-11.2011 1:CAS:528:DC%2BC3MXptFWruro%3D
24. N Kimura O Imamura F Ono K Terao 2007 Aging attenuates dynactin-dynein interaction: down-regulation of dynein causes accumulation of endogenous tau and amyloid precursor protein in human neuroblastoma cells J Neurosci Res 85 2909 2916 17628503 10.1002/jnr.21408 1:CAS:528:DC%2BD2sXht1eis7fP (Pubitemid 47523575)
25. NE LaPointe G Morfini G Pigino, et al. 2009 The aminoterminus of Tau inhibits kinesin-dependent axonal transport: implications for filament toxicity J Neurosci Res 87 440 451 18798283 10.1002/jnr.21850 1:CAS:528: DC%2BD1MXhvFCrsLs%3D
26. K Leroy Z Yilmaz JP Brion 2007 Increased level of active GSK-3beta in Alzheimer's disease and accumulation in argyrophilic grains and in neurones at different stages of neurofibrillary degeneration Neuropathol Appl Neurobiol 33 43 55 17239007 10.1111/j.1365-2990.2006.00795.x 1:CAS:528:DC%2BD2sXjtlemuro%3D (Pubitemid 46090309)
27. K Leroy A Bretteville K Schindowski, et al. 2007 Early axonopathy preceding neurofibrillary tangles in mutant tau transgenic mice Am J Pathol 171 976 992 17690183 10.2353/ajpath.2007.070345 1:CAS:528:DC%2BD2sXhtV2murbF (Pubitemid 47440995)
28. S Lovestone CL Hartley J Pearce BH Anderton 1996 Phosphorylation of tau by glycogen synthase kinase-3β in intact mammalian cells: The effects on the organization and stability of microtubules Neurosci. 73 1145 1157 10.1016/0306-4522(96)00126-1 1:CAS:528:DyaK28XktFWiur8%3D (Pubitemid 26194338)
29. E Masliah M Mallory M Alford, et al. 2001 Altered expression of synaptic proteins occurs early during progression of Alzheimer's disease Neurology 56 127 129 11148253 1:STN:280:DC%2BD3MzmvFWguw%3D%3D (Pubitemid 32059669)
30. AE McCart D Mahony JA Rothnagel 2003 Alternatively spliced products of the human kinesin light chain 1 (KNS2) gene Traffic 4 576 580 12839500 10.1034/j.1600-0854.2003.00113.x 1:CAS:528:DC%2BD3sXlvVyjtLs%3D (Pubitemid 36896549)
31. SS Mirra A Heyman D McKeel, et al. 1991 The Consortium to Establish a Registry for Alzheimer's Disease (CERAD). Part II. Standardization of the neuropathologic assessment of Alzheimer's disease Neurology 41 479 486 2011243 1:STN:280:DyaK3M7oslajsQ%3D%3D
32. M Morel M Authelet R Dedecker JP Brion 2010 Glycogen synthase kinase-3beta and the p25 activator of cyclin dependent kinase 5 increase pausing of mitochondria in neurons Neuroscience 167 1044 1056 20211702 10.1016/j.neuroscience.2010.02.077 1:CAS:528:DC%2BC3cXlsFOiu7Y%3D
33. G Morfini G Szebenyi R Elluru N Ratner ST Brady 2002 Glycogen synthase kinase 3 phosphorylates kinesin light chains and negatively regulates kinesin-based motility EMBO J 21 281 293 11823421 10.1093/emboj/21.3.281 1:CAS:528:DC%2BD38XhsVSnsro%3D (Pubitemid 34137290)
34. G Morfini G Pigino N Mizuno M Kikkawa ST Brady 2007 tau binding to microtubules does not directly affect microtubule-based vesicle motility J Neurosci Res 85 2620 2630 17265463 10.1002/jnr.21154 1:CAS:528: DC%2BD2sXht1Wntr%2FI (Pubitemid 47344564)
35. GA Morfini M Burns LI Binder, et al. 2009 Axonal transport defects in neurodegenerative diseases J Neurosci 29 12776 12786 19828789 10.1523/JNEUROSCI.3463-09.2009 1:CAS:528:DC%2BD1MXhtlSit7bO
36. JH Morrison PR Hof 1997 Life and death of neurons in the aging brain Science 278 412 419 9334292 10.1126/science.278.5337.412 1:CAS:528: DyaK2sXmslGlt70%3D (Pubitemid 27454417)
37. L Otvos Jr L Feiner E Lang GI Szendrei M Goedert VM-Y Lee 1994 Monoclonal antibody PHF-1 recognizes tau protein phosphorylated at serine residues 396 and 404 J.Neurosci.Res. 39 669 673 7534834 10.1002/jnr.490390607 1:CAS:528:DyaK2MXislahtLk%3D
38. JJ Pei T Tanaka YC Tung E Braak K Iqbal I Grundke-Iqbal 1997 Distribution, levels, and activity of glycogen synthase kinase-3 in the Alzheimer disease brain J.Neuropathol.Exp.Neurol. 56 70 78 8990130 10.1097/00005072-199701000-00007 1:STN:280:DyaK2s7ksVelsQ%3D%3D (Pubitemid 127470328)
39. KK Pfister EM Fisher IR Gibbons, et al. 2005 Cytoplasmic dynein nomenclature J Cell Biol 171 411 413 16260502 10.1083/jcb.200508078 1:CAS:528:DC%2BD2MXht1ShsrnK (Pubitemid 41586928)
40. G Pigino G Morfini A Pelsman MP Mattson ST Brady J Busciglio 2003 Alzheimer's presenilin 1 mutations impair kinesin-based axonal transport J Neurosci 23 4499 4508 12805290 1:CAS:528:DC%2BD3sXkslOksrw%3D (Pubitemid 36706180)
41. G Pigino G Morfini Y Atagi, et al. 2009 Disruption of fast axonal transport is a pathogenic mechanism for intraneuronal amyloid beta Proc Natl Acad Sci USA 106 5907 5912 19321417 10.1073/pnas.0901229106 1:CAS:528: DC%2BD1MXkvFehtro%3D
42. A Rahman DS Friedman LS Goldstein 1998 Two kinesin light chain genes in mice. Identification and characterization of the encoded proteins J Biol Chem 273 15395 15403 9624122 10.1074/jbc.273.25.15395 1:CAS:528:DyaK1cXktVSmt70%3D (Pubitemid 28298144)
43. S Richard JP Brion AM Couck J Flament-Durand 1989 Accumulation of smooth endoplasmic reticulum in Alzheimer's disease: new morphological evidence of axoplasmic flow disturbances J Submicrosc Cytol Pathol 21 461 467 2477140 1:STN:280:DyaK3c%2Fgt1yhug%3D%3D (Pubitemid 19185026)
44. SW Scheff DA Price FA Schmitt EJ Mufson 2006 Hippocampal synaptic loss in early Alzheimer's disease and mild cognitive impairment Neurobiol Aging 27 1372 1384 16289476 10.1016/j.neurobiolaging.2005.09.012 1:CAS:528: DC%2BD28XoslKrs7s%3D (Pubitemid 44279897)
45. K Spittaels C Van den Haute J Van Dorpe, et al. 1999 Prominent axonopathy in the brain and spinal cord of transgenic mice overexpressing four-repeat human tau protein Am J Pathol 155 2153 2165 10595944 10.1016/S0002-9440(10) 65533-2 1:CAS:528:DC%2BD3cXit1KntQ%3D%3D
46. M Stagi P Gorlovoy S Larionov K Takahashi H Neumann 2006 Unloading kinesin transported cargoes from the tubulin track via the inflammatory c-Jun N-terminal kinase pathway FASEB J 20 2573 2575 17068110 10.1096/fj.06-6679fje 1:CAS:528:DC%2BD28Xht1yls77M (Pubitemid 44953784)
47. K Stamer R Vogel E Thies E Mandelkow EM Mandelkow 2002 Tau blocks traffic of organelles, neurofilaments, and APP vesicles in neurons and enhances oxidative stress J Cell Biol 156 1051 1063 11901170 10.1083/jcb.200108057 1:CAS:528:DC%2BD38Xit1KisL4%3D (Pubitemid 34839854)
48. GB Stokin C Lillo TL Falzone, et al. 2005 Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease Science 307 1282 1288 15731448 10.1126/science.1105681 1:CAS:528:DC%2BD2MXhsFOqt7c%3D (Pubitemid 40299973)
49. A Takashima K Noguchi K Sato T Hoshino K Imahori 1993 Tau protein kinase I is essential for amyloid beta-protein-induced neurotoxicity Proc Natl Acad Sci USA 90 7789 7793 8356085 10.1073/pnas.90.16.7789 1:CAS:528:DyaK3sXlsFOmtrk%3D (Pubitemid 23250036)
50. RD Vale TS Reese MP Sheetz 1985 Identification of a novel force-generating protein, kinesin, involved in microtubule-based motility Cell 42 39 50 3926325 10.1016/S0092-8674(85)80099-4 1:CAS:528:DyaL2MXlslChs7s%3D (Pubitemid 16237554)
51. A Yuan A Kumar C Peterhoff K Duff RA Nixon 2008 Axonal transport rates in vivo are unaffected by tau deletion or overexpression in mice J Neurosci 28 1682 1687 18272688 10.1523/JNEUROSCI.5242-07.2008 1:CAS:528:DC%2BD1cXnvVSrt7s%3D (Pubitemid 351287026)
52. C Zhao J Takita Y Tanaka, et al. 2001 Charcot-Marie-Tooth disease type 2A caused by mutation in a microtubule motor KIF1Bbeta Cell 105 587 597 11389829 10.1016/S0092-8674(01)00363-4 1:CAS:528:DC%2BD3MXktlSqtrw%3D (Pubitemid 32524112)