Disruption of fast axonal transport is a pathogenic mechanism for intraneuronal amyloid beta

Proceedings of the National Academy of Sciences of the United States of America

Volumn 106, Issue 14, 2009, Pages 5907-5912

  Pigino, G ^a,b   Morfini, G ^a,b   Atagi, Y ^a,b   Deshpande, A ^c   Yu, C ^a   Jungbauer, L ^a   LaDu, M ^a   Busciglio, J ^c   Brady, S ^a,b  

^a UNIVERSITY OF ILLINOIS AT CHICAGO   (United States)

^b MARINE BIOLOGICAL LABORATORY   (United States)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Alzheimer's disease; Axonal transport; Beta amyloid oligomer CK2; Kinesin

Indexed keywords

AMYLOID BETA PROTEIN; CASEIN KINASE II; KINESIN 1;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; AXOPLASM; CELL DISRUPTION; CONTROLLED STUDY; HUMAN; NERVE FIBER TRANSPORT; NONHUMAN; PATHOGENESIS; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN PHOSPHORYLATION; SQUID;

ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; ANIMALS; AXONAL TRANSPORT; CASEIN KINASE II; KINESIN; MICE; NEURONS; PHOSPHORYLATION; PROTEIN MULTIMERIZATION;

EID: 65249161745     PISSN: 00278424     EISSN: 10916490     Source Type: Journal    
DOI: 10.1073/pnas.0901229106     Document Type: Article

References (55)

1. Maeda S, et al. (2006) Increased levels of granular tau oligomers: An early sign of brain aging and Alzheimer's disease. Neurosci Res 54:197-201.
2. Terry RD, Davies P (1980) Dementia of the Alzheimer type. Annu Rev Neurosci 3:77-95.
3. Masliah E, Terry RD, DeTeresa RM, Hansen LA (1989) Immunohistochemical quantification of the synapse-related protein synaptophys in in Alzheimerdisease. Neurosci Lett 103:234-239.
4. Hardy JA, Higgins GA (1992) Alzheimer's disease: The amyloid cascade hypothesis. Science 256:184-185.
5. Lambert MP et al. (1998) Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 95:6448-6453.
6. Dahlgren KN et al. (2002) Oligomeric and fibrillar species of amyloid-beta peptides differentially affect neuronal viability. J Biol Chem 277:32046-32053.
7. Deshpande A, Mina E, Glabe C, Busciglio J (2006) Different conformations of amyloid beta induce neurotoxicity by distinct mechanisms in human cortical neurons. J Neurosci 26:6011-6018.
8. Lacor PN et al. (2007) Abeta oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J Neurosci 27:796-807.
9. Lesne S et al. (2006) A specific amyloid-beta protein assembly in the brain impairs memory. Nature 440:352-357.
10. Cleary JP et al. (2005) Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 8:79-84.
11. Wertkin AM et al. (1993) Human neurons derived from a teratocarcinoma cell line express solely the 695-amino acid amyloid precursor protein and produce intracellular betaamyloid or A4 peptides. Proc Natl Acad Sci USA 90:9513-9517.
12. Gouras GK et al. (2000) Intraneuronal Abeta42 accumulation in human brain. Am J Pathol 156:15-20.
13. Takahashi RH et al. (2004) Oligomerization of Alzheimer's beta-amyloid within processes and synapses of cultured neurons and brain. J Neurosci 24:3592-3599.
14. Takahashi RH et al. (2002) Intraneuronal Alzheimer abeta42 accumulates in multivesicular bodies and is associated with synaptic pathology. Am J Pathol 161:1869-1879.
15. Gyure KA, Durham R, Stewart WF, Smialek JE, Troncoso JC (2001) Intraneuronal abetaamyloid precedes development of amyloid plaques in Down syndrome. Arch Pathol Lab Med 125:489-492.
16. LaFerla FM, Tinkle BT, Bieberich CJ, Haudenschild CC, Jay G (1995) The Alzheimer's A beta peptide induces neurodegeneration and apoptotic cell death in transgenic mice. Nat Genet 9:21-30.
17. Crowther DC et al. (2005) Intraneuronal Abeta, non-amyloid aggregates and neurodegeneration in a Drosophila model of Alzheimer's disease. Neuroscience 132:123-135.
18. Zhang Y, McLaughlin R, Goodyer C, LeBlanc A (2002) Selective cytotoxicity of intracellular amyloid beta peptide1-42 through p53 and Bax in cultured primary human neurons. J Cell Biol 156:519-529.
19. Joachim CL, Mori H, Selkoe DJ (1989) Amyloidbeta-proteindeposition in tissuesother than brain in Alzheimer's disease. Nature 341:226-230.
20. Hafezparast M, et al. (2003) Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science 300:808-812.
21. Reid E, et al. (2002) A Kinesin Heavy Chain (KIF5A) Mutation in Hereditary Spastic Paraplegia (SPG10). Am J Hum Genet 71:1189-1194.
22. Morfini G, Szebenyi G, Elluru R, Ratner N, Brady ST (2002) Glycogen synthase kinase 3 phosphorylateskinesin light chains andnegatively regulates kinesin-basedmotility. EMBO J 23:281-293.
23. Pigino G, Morfini G, Mattson MP, Brady ST, Busciglio J (2003) Alzheimer's presenilin 1 mutations impair kinesin-based axonal transport. J Neurosci 23:4499-4508.
24. Morfini G, et al. (2006) JNK mediates pathogenic effects of polyglutamine-expanded androgen receptor on fast axonal transport. Nat Neurosci 9:907-916.
25. Szebenyi G, et al. (2003) Neuropathogenic forms of Huntingtin and androgen receptor inhibit fast axonal transport. Neuron 40:41-52.
26. Morfini G, et al. (2007) 1-Methyl-4-phenylpyridinium affects fast axonal transport by activation of caspase and protein kinase C. Proc Natl Acad Sci USA 104:2442-2447.
27. Stine WB, Jr., Dahlgren KN, Krafft GA, LaDu MJ (2003) In vitro characterization of conditions for amyloid-beta peptide oligomerization and fibrillogenesis. J Biol Chem 278:11612-11622.
28. Morfini G, Szebenyi G, Richards B, Brady ST (2001) Regulation of kinesin: Implications for neuronal development. Dev Neurosci 23:364-376.
29. Morfini G, Pigino G, Beffert U, Busciglio J, Brady ST (2002) Fastaxonal transport misregulation and Alzheimer's disease. Neuromol Med 2:89-99.
30. Pei JJ et al. (1997) Distribution, levels, and activity of glycogen synthase kinase-3 in the Alzheimer disease brain. J Neuropathol Exp Neurol 56:70-78.
31. Pei JJ et al. (2001) Localization of active forms of C-jun kinase (JNK) and p38 kinase in Alzheimer's disease brains at different stages of neurofibrillary degeneration. J Alzheimers Dis 3:41-48.
32. Lee MS, Tsai LH (2003) Cdk5: One of the links between senile plaques and neurofibrillary tangles? J Alzheimers Dis 5:127-137.
33. Morfini Getal. (2004) A novel CDK5-dependent pathway for regulating GSK3 activity and kinesin-driven motility in neurons. EMBO J 23:2235-2245.
34. Masliah E et al. (1992) Casein kinase II alteration precedes tau accumulation in tangle formation. Am J Pathol 140:263-268.
35. Chauhan A, Chauhan VP, Murakami N, Brockerhoff H, Wisniewski HM (1993) Amyloid beta-protein stimulates casein kinase I and casein kinase II activities. Brain Res 629:47-52.
36. PaganoMAetal. (2004) 2-Dimethylamino-4,5,6,7-tetrabromo-1H-benzimidazole: Anovel powerful and selective inhibitor of protein kinase CK2. Biochem Biophys Res Commun 321:1040-1044.
37. Pagano MAetal. (2007) Tetrabromocinnamicacid (TBCA) and related compounds represent a new class of specific protein kinase CK2 inhibitors. Chembiochem 8:129-139.
38. Stenoien DS, Brady ST (1997) Immunochemical analysis of kinesin light chain function. Molec Biol Cell 8:675-689.
39. Donelan MJ et al. (2002) Ca2+-dependent dephosphorylation of kinesin heavy chain on beta-granules in pancreatic beta-cells. Implications for regulated beta-granule transport and insulin exocytosis. J Biol Chem 277:24232-24242.
40. Lapointe NE et al. (2009) The amino terminus of tau inhibits kinesin-dependent axonal transport: Implications for filament toxicity. J Neurosci Res 87:440-451.
41. Moreno H et al. (1998) Nerve growth factor acutely reduces chemical transmission by means of postsynaptic TrkA-like receptors in squid giant synapse. Proc Natl Acad Sci USA 95:14997-15002.
42. Klein WL (2002) Abeta toxicity in Alzheimer's disease: Globular oligomers (ADDLs) as new vaccine and drug targets. Neurochem Int 41:345-352.
43. Busciglio J et al. (2002) Altered metabolism of the amyloid beta precursor protein is associated with mitochondrial dysfunction in Down's syndrome. Neuron 33:677-688.
44. LaFerla FM, Green KN, OddoS (2007) Intracellular amyloid-beta in Alzheimer's disease. Nat Rev Neurosci 8:499-509.
45. Selkoe DJ (2002) Alzheimer's disease is a synaptic failure. Science 298:789-791.
46. Wishart TM, Parson SH, Gillingwater TH (2006) Synaptic vulnerability in neurodegenerative disease. J Neuropathol Exp Neurol 65:733-739.
47. Coleman M (2005) Axon degeneration mechanisms: Commonality amid diversity. Nat Rev Neurosci 6:889-898.
48. Meggio F, Pinna LA (2003) One-thousand-and-one substrates of protein kinase CK2? FASEB J 17:349-368.
49. Moreno HH, et al. (2009) Synaptic transmission block by pre-synaptic injection of oligomeric amyloid beta. Proc Natl Acad Sci USA, 10.1073.0900944106.
50. Shata A, Saisu H, Odani S, Abe T (2007) Phosphorylated synaphin/complexin found in the brain exhibits enhanced SNARE complex binding. Biochem Biophys Res Commun 354:808-813.
51. Deboer SR et al. (2008) Conventional kinesin holoenzymes are composed of heavy and light chain homodimers. Biochemistry 47:4535-4543.
52. Pigino G, Pelsman A, Mori H, Busciglio J (2001) Presenilin-1 mutations reduce cytoskeletal association, deregulate neurite growth, and potentiate neuronal dystrophy and tau phosphorylation. J Neurosci 21:834-842.
53. Brady ST, Lasek RJ, Allen RD (1985) Video microscopy of fast axonal transport in isolated axoplasm: A new model for study of molecular mechanisms. Cell Motility 5:81-101.
54. Brady ST, Richards BW, Leopold PL (1993) Assay of vesicle motility in squid axoplasm. Meth Cell Biol 39:191-202.
55. Morfini G, Pigino G, Brady ST (2006) Approaches to kinesin-1 phosphorylation. Molecular Motors: Methods and Protocols, Methods in Molecular Biology, ed Sperry A (Humana Press, Clifton, NJ), Vol 392, pp 51-70.