Severely dystrophic axons at amyloid plaques remain continuous and connected to viable cell bodies

Brain

Volumn 132, Issue 2, 2009, Pages 402-416

  Adalbert, Robert ^a   Nogradi, Antal ^b   Babetto, Elisabetta ^a   Janeckova, Lucie ^a   Walker, Simon A ^a   Kerschensteiner, Martin ^c   Misgeld, Thomas ^d   Coleman, Michael P ^a  

^a BABRAHAM INSTITUTE   (United Kingdom)

^b UNIVERSITY OF SZEGED   (Hungary)

^c UNIVERSITY OF MUNICH   (Germany)

^d TECHNICAL UNIVERSITY OF MUNICH   (Germany)

Author keywords

Alzheimer's disease; Axonal damage signalling; Axonal dystrophy; Synapse dysfunction; TgCRND8

Indexed keywords

AMYLOID; YELLOW FLUORESCENT PROTEIN;

ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ARTICLE; CONTROLLED STUDY; DENDRITE; DISEASE SEVERITY; MALE; MOUSE; NERVE FIBER DEGENERATION; NERVE FIBER TRANSPORT; NONHUMAN; PRIORITY JOURNAL; SYNAPTIC TRANSMISSION;

ALZHEIMER DISEASE; ANIMALS; AXONS; BREEDING; CELL SURVIVAL; IMMUNOHISTOCHEMISTRY; MALE; MICE; MICE, INBRED C57BL; MICROSCOPY, ELECTRON; MODELS, ANIMAL; NERVE DEGENERATION; NEURONS; SENILE PLAQUES; SYNAPTIC TRANSMISSION;

EID: 60149092294     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awn312     Document Type: Article

References (59)

1. Adalbert R, Gilley J, Coleman MP. Abeta, tau and ApoE4 in Alzheimer's disease: the axonal connection. Trends Mol Med 2007; 13: 135-42.
2. Beirowski B, Adalbert R, Wagner D, Grumme D, Addicks K, Ribchester RR, et al. The progressive nature of Wallerian degeneration in wild-type and slow Wallerian degeneration (WldS) nerves. BMC Neurosci 2005; 6: 6.
3. Beirowski B, Berek L, Adalbert R, Wagner D, Grumme DS, Addicks K, et al. Quantitative and qualitative analysis of Wallerian degeneration using restricted axonal labelling in YFP-H mice. J Neurosci Meth 2004; 134: 23-35.
4. Bellucci A, Luccarini I, Scali C, Prosperi C, Giovannini MG, Pepeu G, et al. Cholinergic dysfunction, neuronal damage and axonal loss in TgCRND8 mice. Neurobiol Dis 2006; 23: 260-72.
5. Berkelaar M, Clarke DB, Wang YC, Bray GM, Aguayo AJ. Axotomy results in delayed death and apoptosis of retinal ganglion cells in adult rats. J Neurosci 1994; 14: 4368-74.
6. Blennow K, Zetterberg H. Pinpointing plaques with PIB. Nat Med 2006; 12: 753-4.
7. Boutajangout A, Authelet M, Blanchard V, Touchet N, Tremp G, Pradier L, et al. 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 2004; 15: 47-60.
8. Braak H, Braak E, Grundke-Iqbal I, Iqbal K. Occurrence of neuropil threads in the senile human brain and in Alzheimer's disease: a third location of paired helical filaments outside of neurofibrillary tangles and neuritic plaques. Neurosci Lett 1986; 65: 351-5.
9. Brendza RP, Bacskai BJ, Cirrito JR, Simmons KA, Skoch JM, Klunk WE, et al. Anti-Abeta antibody treatment promotes the rapid recovery of amyloid-associated neuritic dystrophy in PDAPP transgenic mice. J Clin Invest 2005; 115: 428-33.
10. Brendza RP, O'Brien C, Simmons K, McKeel DW, Bales KR, Paul SM, et al. PDAPP; YFP double transgenic mice: a tool to study amyloid-beta associated changes in axonal, dendritic, and synaptic structures. J Comp Neurol 2003a; 456: 375-83.
11. Brendza RP, Simmons K, Bales KR, Paul SM, Goldberg MP, Holtzman DM. Use of YFP to study amyloid-beta associated neurite alterations in live brain slices. Neurobiol Aging 2003b; 24: 1071-7.
12. Bridge K, Berg N, Adalbert R, Babetto E, Dias T, Spillantini MG, et al. Late onset distal axonal swelling in YFP-H transgenic mice. Neurobiol Aging 2007 [Epub ahead of print, doi:10.1016/j.neurobiolaging.2007.06.002].
13. Capetillo-Zarate E, Staufenbiel M, Abramowski D, Haass C, Escher A, Stadelmann C, et al. Selective vulnerability of different types of commissural neurons for amyloid beta-protein-induced neurodegeneration in APP23 mice correlates with dendritic tree morphology. Brain 2006; 129: 2992-3005.
14. Chishti MA, Yang DS, Janus C, Phinney AL, Horne P, Pearson J, et al. Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J Biol Chem 2001; 276: 21562-70.
15. Coleman M. Axon degeneration mechanisms: commonality amid diversity. Nat Rev Neurosci 2005; 6: 889-98.
16. Coleman MP, Adalbert R, Beirowski B. Neuroprotective strategies in MS: lessons from C57BL/Wld (S) mice. J Neurol Sci 2005; 233: 133-8.
17. Conforti L, Adalbert R, Coleman MP. Neuronal death: where does the end begin? Trends Neurosci 2007; 30: 159-66.
18. Dickson TC, King CE, McCormack GH, Vickers JC. Neurochemical diversity of dystrophic neurites in the early and late stages of Alzheimer's disease. Exp Neurol 1999; 156: 100-10.
19. Dong H, Martin MV, Chambers S, Csernansky JG. Spatial relationship between synapse loss and beta-amyloid deposition in Tg2576 mice. J Comp Neurol 2007; 500: 311-21.
20. Edgar JM, McLaughlin M, Yool D, Zhang SC, Fowler JH, Montague P, et al. Oligodendroglial modulation of fast axonal transport in a mouse model of hereditary spastic paraplegia. J Cell Biol 2004; 166: 121-31.
21. Enright LE, Zhang S, Murphy TH. Fine mapping of the spatial relationship between acute ischemia and dendritic structure indicates selective vulnerability of layer V neuron dendritic tufts within single neurons in vivo. J Cereb Blood Flow Metab 2007; 27: 1185-200.
22. Feng G, Mellor RH, Bernstein M, Keller-Peck C, Nguyen QT, Wallace M, et al. Imaging neuronal subsets in transgenic mice expressing multiple spectral variants of GFP. Neuron 2000; 28: 41-51.
23. Ferguson B, Matyszak MK, Esiri MM, Perry VH. Axonal damage in acute multiple sclerosis lesions. Brain 1997; 120: 393-9.
24. Ferri A, Sanes JR, Coleman MP, Cunningham JM, Kato AC. Inhibiting axon degeneration and synapse loss attenuates apoptosis and disease progression in a mouse model of motoneuron disease. Curr Biol 2003; 13: 669-73.
25. Fiala JC. Mechanisms of amyloid plaque pathogenesis. Acta Neuropathol 2007; 114: 551-71.
26. Fiala JC, Feinberg M, Peters A, Barbas H. Mitochondrial degeneration in dystrophic neurites of senile plaques may lead to extracellular deposition of fine filaments. Brain Struct Funct 2007; 212: 195-207.
27. Fiala JC, Spacek J, Harris KM. Dendritic spine pathology: cause or consequence of neurological disorders? Brain Res Brain Res Rev 2002; 39: 29-54.
28. Fischer O. Miliare Nekrosen mit drusigen Wucherungen der Neurofibrillen, eine regelmabe Veränderung der Hirnrinde bei seniler Demenz. Monatsschr Psychiatr Neuro 1907; 2: 361-72.
29. Fishman PS, Parks DA. Death of transcallosal neurons after close axotomy. Brain Res 1998; 779: 231-9.
30. Gillingwater TH, Ribchester RR. Compartmental neurodegeneration and synaptic plasticity in the Wld (s) mutant mouse. J Physiol 2001; 534: 627-39.
31. Gonatas NK, Anderson W, Evangelista I. The contribution of altered synapses in the senile plaque: an electron microscopic study in Alzheimer's dementia. J Neuropath Exp Neurol 1967; 26: 25-39.
32. Grutzendler J, Helmin K, Tsai J, Gan WB. Various dendritic abnormalities are associated with fibrillar amyloid deposits in Alzheimer's disease. Ann N Y Acad Sci 2007; 1097: 30-9.
33. Hafezparast M, Klocke R, Ruhrberg C, Marquardt A, Ahmad-Annuar A, Bowen S, et al. Mutations in dynein link motor neuron degeneration to defects in retrograde transport. Science 2003; 300: 808-12.
34. Hardy J. A hundred years of Alzheimer's disease research. Neuron 2006; 52: 3-13.
35. Hudson CS, Deshpande SS, Albuquerque EX. Consequences of axonal transport blockade by batrachotoxin on mammalian neuromuscular junction. III. An ultrastructural study. Brain Res 1984; 296: 319-32.
36. Koliatsos VE, Price WL, Pardo CA, Price DL. Ventral root avulsion: an experimental model of death of adult motor neurons. J Comp Neurol 1994; 342: 35-44.
37. Lacor PN, Buniel MC, Furlow PW, Clemente AS, Velasco PT, Wood M, et al. Abeta oligomer-induced aberrations in synapse composition, shape, and density provide a molecular basis for loss of connectivity in Alzheimer's disease. J Neurosci 2007; 27: 796-807.
38. LaMonte BH, Wallace KE, Holloway BA, Shelly SS, Ascano J, Tokito M, et al. Disruption of dynein/dynactin inhibits axonal transport in motor neurons causing late-onset progressive degeneration. Neuron 2002; 34: 715-27.
39. Lazarov O, Lee M, Peterson DA, Sisodia SS. Evidence that synaptically released beta-amyloid accumulates as extracellular deposits in the hippocampus of transgenic mice. J Neurosci 2002; 22: 9785-93.
40. Martin KR, Quigley HA, Valenta D, Kielczewski J, Pease ME. Optic nerve dynein motor protein distribution changes with intraocular pressure elevation in a rat model of glaucoma. Exp Eye Res 2006; 83: 255-62.
41. Medana IM, Esiri MM. Axonal damage: a key predictor of outcome in human CNS diseases. Brain 2003; 126: 515-30.
42. Meyer-Luehmann M, Spires-Jones TL, Prada C, Garcia-Alloza M, de Calignon A, Rozkalne A, et al. Rapid appearance and local toxicity of amyloid-beta plaques in a mouse model of Alzheimer's disease. Nature 2008; 451: 720-5.
43. Miledi R, Slater CR. On the degeneration of rat neuromuscular junctions after nerve section. J Physiol 1970; 207: 507-28.
44. Misgeld T, Kerschensteiner M, Bareyre FM, Burgess RW, Lichtman JW. Imaging axonal transport of mitochondria in vivo. Nat Methods 2007; 4: 559-61.
45. Nicoll JA, Wilkinson D, Holmes C, Steart P, Markham H, Weller RO. Neuropathology of human Alzheimer disease after immunization with amyloid-beta peptide: a case report. Nat Med 2003; 9: 448-52.
46. Onorato M, Mulvihill P, Connolly J, Galloway P, Whitehouse P, Perry G. Alteration of neuritic cytoarchitecture in Alzheimer disease. Prog Clin Biol Res 1989; 317: 781-9.
47. Park JH, Gimbel DA, GrandPre T, Lee JK, Kim JE, Li W, et al. Alzheimer precursor protein interaction with the Nogo-66 receptor reduces amyloid-beta plaque deposition. J Neurosci 2006; 26: 1386-95.
48. Phinney AL, Deller T, Stalder M, Calhoun ME, Frotscher M, Sommer B, et al. Cerebral amyloid induces aberrant axonal sprouting and ectopic terminal formation in amyloid precursor protein transgenic mice. J Neurosci 1999; 19: 8552-9.
49. Pilling AD, Horiuchi D, Lively CM, Saxton WM. Kinesin-1 and Dynein are the primary motors for fast transport of mitochondria in Drosophila motor axons. Mol Biol Cell 2006; 17: 2057-68.
50. Pun S, Santos AF, Saxena S, Xu L, Caroni P. Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat Neurosci 2006; 9: 408-19.
51. Rui Y, Tiwari P, Xie Z, Zheng JQ. Acute impairment of mitochondrial trafficking by beta-amyloid peptides in hippocampal neurons. J Neurosci 2006; 26: 10480-7.
52. Selkoe DJ. Alzheimer's disease is a synaptic failure. Science 2002; 298: 789-91.
53. Sheng JG, Price DL, Koliatsos VE. Disruption of corticocortical connections ameliorates amyloid burden in terminal fields in a transgenic model of Abeta amyloidosis. J Neurosci 2002; 22: 9794-9.
54. Spires TL, Meyer-Luehmann M, Stern EA, McLean PJ, Skoch J, Nguyen PT, et al. Dendritic spine abnormalities in amyloid precursor protein transgenic mice demonstrated by gene transfer and intravital multiphoton microscopy. J Neurosci 2005; 25: 7278-87.
55. Stokin GB, Lillo C, Falzone TL, Brusch RG, Rockenstein E, Mount SL, et al. Axonopathy and transport deficits early in the pathogenesis of Alzheimer's disease. Science 2005; 307: 1282-8.
56. Teipel SJ, Bayer W, Alexander GE, Zebuhr Y, Teichberg D, Kulic L, et al. Progression of corpus callosum atrophy in Alzheimer disease. Arch Neurol 2002; 59: 243-8.
57. Tsai J, Grutzendler J, Duff K, Gan WB. Fibrillar amyloid deposition leads to local synaptic abnormalities and breakage of neuronal branches. Nat Neurosci 2004; 7: 1181-3.
58. Wirths O, Weis J, Kayed R, Saido TC, Bayer TA. Age-dependent axonal degeneration in an Alzheimer mouse model. Neurobiol Aging 2006; 28: 1689-99.
59. Wisniewski HM, Ghetti B, Terry RD. Neuritic (senile) plaques and filamentous changes in aged rhesus monkeys. Exp Neurol 1973; 32: 566-84.