Synaptic vulnerability in neurodegenerative disease

Journal of Neuropathology and Experimental Neurology

Volumn 65, Issue 8, 2006, Pages 733-739

  Wishart, Thomas M ^a   Parson, Simon H ^b   Gillingwater, Thomas H ^a  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF LEEDS   (United Kingdom)

Author keywords

Alzheimer disease; Huntington disease; Motor neuron disease; Neurodegeneration; Prion; Stroke; Synapse

Indexed keywords

ALZHEIMER DISEASE; APOPTOSIS; CELL PROTECTION; CELLULAR DISTRIBUTION; CENTRAL NERVOUS SYSTEM; CEREBROVASCULAR DISEASE; DEGENERATIVE DISEASE; DISEASE COURSE; HUMAN; HUNTINGTON CHOREA; LYSOSOME STORAGE DISEASE; MOTOR NEURON DISEASE; NERVE DEGENERATION; PATHOPHYSIOLOGY; PERIPHERAL NERVOUS SYSTEM; PRION DISEASE; PRIORITY JOURNAL; REVIEW; STROKE; SYMPTOMATOLOGY; SYNAPOPTOSIS; SYNAPTIC MEMBRANE;

ANIMALS; CELL DEATH; CENTRAL NERVOUS SYSTEM; DISEASE MODELS, ANIMAL; GENETIC PREDISPOSITION TO DISEASE; HUMANS; NERVE TISSUE PROTEINS; NEURODEGENERATIVE DISEASES; PRESYNAPTIC TERMINALS; SIGNAL TRANSDUCTION; SYNAPSES;

EID: 33746873734     PISSN: 00223069     EISSN: None     Source Type: Journal    
DOI: 10.1097/01.jnen.0000228202.35163.c4     Document Type: Review

References (98)

1. s mutant mouse. J Physiol 2001;534:627-39
2. Coleman M. Axon degeneration mechanisms: Commonality amid diversity. Nat Rev Neurosci 2005;6:889-98
3. Dewar D, Yam P, McCulloch J. Drug development for stroke: Importance of protecting cerebral white matter. Eur J Pharmacol 1999;375:41-50
4. Selkoe DJ. Alzheimer's disease is a synaptic failure. Science 2002;298:789-91
5. Coleman P, Federoff H, Kurlan R. A focus on the synapse for neuroprotection in Alzheimer disease and other dementias. Neurology 2004;63:1155-62
6. Games D, Adams D, Alessandrini R, et al. Alzheimer-type neuropathology in transgenicmice overexpressing V717F beta-amyloid precursor protein. Nature 1995;373:523-37
7. Mucke L, Masliah E, Yu GQ, et al. High-level neuronal expression of abeta 1-42 in wild-type human amyloid protein precursor transgenic mice: Synaptotoxicity without plaque formation. J Neurosci 2000;20:4050-58
8. Masliah E, Mallory M, Alford M, et al. Altered expression of synaptic proteins occurs early during progression of Alzheimer's disease. Neurology 2001;56:127-29
9. Walsh DM, Klyubin I, Fadeeva JV, et al. Naturally secreted oligomers of amyloid beta protein potently inhibit hippocampal long-term potentiation in vivo. Nature 2002;416:535-39
10. Buttini M, Masliah E, Barbour R, et al. Beta-amyloid immunotherapy prevents synaptic degeneration in a mouse model of Alzheimer's disease. J Neurosci 2005;25:9096-101
11. DeKosky ST, Scheff SW. Synapse loss in frontal cortex biopsies in Alzheimer's disease: Correlation with cognitive severity. Ann Neurol 1990;27:457-64
12. Scheff SW, Price DA. Synaptic pathology in Alzheimer's disease: A review of ultrastructural studies. Neurobiol Aging 2003;24:1029-46
13. Davies CA, Mann DM, Sumpter PQ, et al. A quantitative morphometric analysis of the neuronal and synaptic content of the frontal and temporal cortex in patients with Alzheimer's disease. J Neurol Sci 1987;78:151-64
14. Terry RD, Masliah E, Salmon DP, et al. Physical basis of cognitive alterations in Alzheimer's disease: Synapse loss is the major correlate of cognitive impairment. Ann Neurol 1991;30:572-80
15. Brown DF, Risser RC, Bigio EH, et al. Neocortical synapse density and Braak stage in the Lewy body variant of Alzheimer disease: A comparison with classic Alzheimer disease and normal aging. J Neuropathol Exp Neurol 1998;57:955-60
16. Zhou L, Miller BL, McDaniel CH, et al. Frontotemporal dementia: Neuropil spheroids and presynaptic terminal degeneration. Ann Neurol 1998;44:99-109
17. Lipton AM, Cullum CM, Satumtira S, et al. Contribution of asymmetric synapse loss to lateralizing clinical deficits in frontotemporal dementias. Arch Neurol 2001;58:1233-39
18. Uylings HB, deBrabander JM. Neuronal changes in normal human aging and Alzheimer's disease. Brain Cogn 2002;49:268-76
19. Larson J, Lynch G, Games D, et al. Alterations in synaptic transmission and long-term potentiation in hippocampal slices from young and aged PDAPP mice. Brain Res 1999;840:23-35
20. Chapman PF, White GL, Jones MW, et al. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 1999;2:271-76
21. Li J-Y, Plomann M, Brundin P. Huntington's disease: A synaptopathy? Trends Mol Med 2003;9:414-20
22. Graveland GA, Williams RS, DiFiglia M. Evidence for degenerative and regenerative changes in neostriatal spiny neurons in Huntington's disease. Science 1985;227:770-73
23. Ferrante RJ, Kowall NW, Richardson EP Jr. Proliferative and degenerative changes in striatal spiny neurons in Huntington's disease: A combined study using the section-Golgi method and calbindin D28k immunocytochemistry. J Neurosci 1991;11:3877-87
24. Modregger J, DiProspero NA, Charles V, et al. PACSIN 1 interacts with huntingtin and is absent from synaptic varicosities in presymptomatic Huntington's disease brains. Hum Mol Genet 2002;11:2547-58
25. DiProspero NA, Chen EY, Charles V, et al. Early changes in Huntington's disease patient brains involve alterations in cytoskeletal and synaptic elements. J Neurocytol 2004;33:517-33
26. Guidetti P, Charles V, Chen EY, et al. Early degenerative changes in transgenic mice expressing mutant huntingtin involve dendritic abnormalities but no impairment of mitochondrial energy production. Exp Neurol 2001;169:340-50
27. Klapstein GJ, Fisher RS, Zanjani H, et al. Electrophysiological and morphological changes in striatal spiny neurons in R6/2 Huntington's disease transgenic mice. J Neurophysiol 2001;86:2667-77
28. Ribchester RR, Thomson D, Wood NI, et al. Progressive abnormalities in skeletal muscle and neuromuscular junctions of transgenic mice expressing the Huntington's disease mutation. Eur J Neurosci 2004;20:3092-114
29. Sasaki S, Maruyama S. Synapse loss in anterior horn neurons in amyotrophic lateral sclerosis. Acta Neuropathol (Berl) 1994;88:222-27
30. Nagao M, Misawa H, Kato S, et al. Loss of cholinergic synapses on the spinal motor neurons of amyotrophic lateral sclerosis. J Neuropathol Exp Neurol 1998;57:329-33
31. Sasaki S, Iwata M. Ultrastructural changes of synapses of Betz cells in patients with amyotrophic lateral sclerosis. Neurosci Lett 1999;268:29-32
32. Zang DW, Lopes EC, Cheema SS. Loss of synaptophysin-positive boutons on lumbar motor neurons innervating the medial gastrocnemius muscle of the SOD1G93A G1H transgenic mouse model of ALS. J Neurosci Res 2005;79:694-99
33. Maselli RA, Wollman RL, Leung C, et al. Neuromuscular transmission in amyotrophic lateral sclerosis. Muscle Nerve 1993;16:1193-203
34. Fischer LR, Culver DG, Tennant P, et al. Amyotrophic lateral sclerosis is a distal axonopathy: Evidence in mice and man. Exp Neurol 2004;185:232-40
35. Balice-Gordon RJ, Smith DB, Goldman J, et al. Functional motor unit failure precedes neuromuscular degeneration in canine motor neuron disease. Ann Neurol 2000;47:596-605
36. Frey D, Schneider C, Xu L, et al. Early and selective loss of neuromuscular synapse subtypes with low sprouting competence in motor neuron diseases. J Neurosci 2000;20:2534-42
37. Cifuentes-Diaz C, Nicole S, Velasco ME, et al. Neurofilament accumulation at the motor endplate and lack of axonal sprouting in a spinal muscular atrophy mouse model. Hum Mol Genet 2002;11:1439-47
38. Chan YB, Miguel-Aliaga I, Franks C, et al. Neuromuscular defects in a Drosophila survival motor neuron gene mutant. Hum Mol Genet 2003;12:1367-76
39. Newbery HJ, Gillingwater TH, Dharmasaroja P, et al. Progressive loss of motor neuron function in Wasted mice: Effects of a spontaneous null mutation in the gene for the eEF1A2 translation factor. J Neuropathol Exp Neurol 2005;64:295-303
40. Storkebaum E, Lambrechts D, Dewerchin M, et al. Treatment of motoneuron degeneration by intracerebroventricular delivery of VEGF in a rat model of ALS. Nat Neurosci 2005;8:85-92
41. Ikemoto A, Nakamura S, Akiguchi I, et al. Differential expression between synaptic vesicle proteins and presynaptic plasma membrane proteins in the anterior horn of amyotrophic lateral sclerosis. Acta Neuropathol 2002;103:179-87
42. Brown MR, Sullivan PG, Geddes JW. Synaptic mitochondria are more susceptible to Ca2+ overload than non-synaptic mitochondria. J Biol Chem 2006;281:11658-68
43. Ironside JW, Dearmond S. Human prion diseases. Brain Pathol 1994;4:313-14
44. Kitamoto T, Shin RW, Doh-ura K, et al. Abnormal isoform of prion proteins accumulates in the synaptic structures of the central nervous system in patients with Creutzfeldt-Jakob disease. Am J Pathol 1992;140:1285-94
45. Clinton J, Forsyth C, Royston MC, et al. Synaptic degeneration is the primary neuropathological feature in prion disease: A preliminary study. Neuroreport 1993;4:65-68
46. Jeffrey M, Halliday WG, Bell J, et al. Synapse loss associated with abnormal PrP precedes neuronal degeneration in the scrapie-infected murine hippocampus. Neuropathol Appl Neurobiol 2000;26:41-54
47. Cunningham C, Deacon R, Wells H, et al. Synaptic changes characterize early behavioural signs in the ME7 model of murine prion disease. Eur J Neurosci 2003;17:2147-55
48. Chiesa R, Piccardo P, Dossena S, et al. Bax deletion prevents neuronal loss but not neurological symptoms in a transgenic model of inherited prion disease. Proc Natl Acad Sci U S A 2005;102:238-43
49. Aguzzi A, Haass C. Games played by rogue proteins in prion disorders and Alzheimer's disease. Science 2003;302:814-18
50. Jeyakumar M, Dwek RA, Butters TD, et al. Storage solutions: Treating lysosomal disorders of the brain. Nat Rev Neurosci 2005;6:713-25
51. Patel SC, Suresh S, Kumar U, et al. Localization of Niemann-Pick C1 protein in astrocytes: Implications for neuronal degeneration in Niemann- Pick type C disease. Proc Natl Acad Sci U S A 1999;96:1657-62
52. Luiro K, Kopra O, Lehtovirta M, et al. CLN3 protein is targeted to neuronal synapses but excluded from synaptic vesicles: New clues to Batten disease. Hum Mol Genet 2001;10:2123-31
53. Lehtovirta M, Kyttala A, Eskelinen EL, et al. Palmitoyl protein thioesterase (PPT) localizes into synaptosomes and synaptic vesicles in neurons: Implications for infantile neuronal ceroid lipofuscinosis (INCL). Hum Mol Genet 2001;10:69-75
54. Virmani T, Gupta P, Liu X, et al. Progressively reduced synaptic vesicle pool size in cultured neurons derived from neuronal ceroid lipofuscinosis-1 knockout mice. Neurobiol Dis 2005;20:314-23
55. Mitter D, Reisinger C, Hinz B, et al. The synaptophysin/synaptobrevin interaction critically depends on the cholesterol content. J Neurochem 2003;84:35-42
56. Ohara S, Ukita Y, Ninomiya H, et al. Axonal dystrophy of dorsal root ganglion sensory neurons in a mouse model of Niemann-Pick disease type C. Exp Neurol 2004;187:289-98
57. s mutant mice. J Cereb Blood Flow Metab 2004;24:62-66
58. Ishimaru H, Casamenti F, Ueda K, et al. Changes in presynaptic proteins, SNAP-25 and synaptophysin, in the hippocampal CA1 area in ischemic gerbils. Brain Res 2001;903:94-101
59. Jourdain P, Nikonenko I, Alberi S, et al. Remodeling of hippocampal synaptic networks by a brief anoxia-hypoglycemia. J Neurosci 2002;22:3108-16
60. Zhang S, Boyd J, Delaney K, et al. Rapid reversible changes in dendritic spine structure in vivo gated by the degree of ischemia. J Neurosci 2005;25:5333-38
61. Willison HJ. The immunobiology of Guillain-Barré syndromes. J Peripher Nerv Syst 2005;10:94-112
62. Prasarnpun S, Walsh J, Awad SS, et al. Envenoming bites by kraits: The biological basis of treatment-resistant neuromuscular paralysis. Brain 2005;128:2987-96
63. s and other mutant mice. J Neurocytol 2003;32:863-81
64. s mutant and Ube4b/Nmnat transgenic mice. J Physiol 2002;543:739-55
65. Parson SH, Ribchester RR, Davie N, et al. Axotomy-dependent and -independent synapse elimination in organ cultures of Wld(s) mutant mouse skeletal muscle. J Neurosci Res 2004;76:64-75
66. Gillingwater TH, Ingham CA, Parry KE, et al. Delayed synaptic degeneration in the CNS of Wlds mice after cortical lesion. Brain 2006;129:1546-56
67. Mi W, Beirowski B, Gillingwater TH, et al. The slow Wallerian degeneration gene, WldS, inhibits axonal spheroid pathology in gracile axonal dystrophy mice. Brain 2005;128:405-16
68. s gene regulates expression of PTTG1 and erythroid differentiation regulator 1-like gene in mice and human cells. Hum Mol Genet 2006;15:625-35
69. Mattson MP, Keller JN, Begley JG. Evidence for synaptic apoptosis. Exp Neurol 1998;153:35-48
70. Gilman CP, Chan SL, Guo Z, et al. p53 is present in synapses where it mediates mitochondrial dysfunction and synaptic degeneration in response to DNA damage, and oxidative and excitotoxic insults. Neuromolecular Med 2003;3:159-72
71. Gylys KH, Fein JA, Wiley DJ, et al. Rapid annexin-V labeling in synaptosomes. Neurochem Int 2004;44:125-31
72. Chan SL, Mattson MP. Caspase and calpain substrates: Roles in synaptic plasticity and cell death. J Neurosci Res 1999;58:167-90
73. Mattson MP. Apoptotic and anti-apoptotic synaptic signaling mechanisms. Brain Pathol 2000;10:300-12
74. Culmsee C, Mattson MP. p53 in neuronal apoptosis. Biochem Biophys Res Commun 2005;331:761-77
75. Duan W, Rangnekar VM, Mattson MP. Prostate apoptosis response-4 production in synaptic compartments following apoptotic and excitotoxic insults: Evidence for a pivotal role in mitochondrial dysfunction and neuronal degeneration. J Neurochem 1999;72:2312-22
76. Xie J, Awad KS, Guo Q. RNAi knockdown of Par-4 inhibits neurosynaptic degeneration in ALS-linked mice. J Neurochem 2005;92:59-71
77. Wang LJ, Lu YY, Muramatsu S, et al. Neuroprotective effects of glial cell line-derived neurotrophic factor mediated by an adeno-associated virus vector in a transgenic animal model of amyotrophic lateral sclerosis. J Neurosci 2002;22:6920-28
78. Lesbordes JC, Cifuentes-Diaz C, Miroglio A, et al. Therapeutic benefits of cardiotrophin-1 gene transfer in a mouse model of spinal muscular atrophy. Hum Mol Genet 2003;12:1233-39
79. Haddad H, Cifuentes-Diaz C, Miroglio A, et al. Riluzole attenuates spinal muscular atrophy disease progression in a mouse model. Muscle Nerve 2003;28:432-37
80. Kaspar BK, Llado J, Sherkat N, et al. Retrograde viral delivery of IGF-1 prolongs survival in a mouse ALS model. Science 2003;301:839-42
81. Dobrowolny G, Giacinti C, Pelosi L, et al. Muscle expression of a local Igf-1 isoform protects motor neurons in an ALS mouse model. J Cell Biol 2005;168:193-99
82. Pun S, Santos AF, Saxena S, et al. Selective vulnerability and pruning of phasic motoneuron axons in motoneuron disease alleviated by CNTF. Nat Neurosci 2006;9:408-19
83. Yi JJ, Ehlers MD. Ubiquitin and protein turnover in synapse function. Neuron 2005;47:629-32
84. Wilson SM, Bhattacharyya B, Rachel RA, et al. Synaptic defects in ataxia mice result from a mutation in Usp14, encoding a ubiquitin-specific protease. Nat Genet 2002;32:420-25
85. Coleman MP, Ribchester RR. Programmed axon death, synaptic dysfunction and the ubiquitin proteasome system. Curr Drug Targets CNS Neurol Disord 2004;3:227-38
86. Fernández-Chacón R, Wolfel M, Nishimune H, et al. The synaptic vesicle protein CSP alpha prevents presynaptic degeneration. Neuron 2004;42:237-51
87. Chandra S, Gallardo G, Fernandez-Chacon R, et al. Alpha-synuclein cooperates with CSPalpha in preventing neurodegeneration. Cell 2005;123:383-96
88. Singleton AB. Altered alpha-synuclein homeostasis causing Parkinson's disease: The potential roles of dardarin. Trends Neurosci 2005;28:416-21
89. Pielage J, Fetter RD, Davis GW. Presynaptic spectrin is essential for synapse stabilization. Curr Biol 2005;15:918-28
90. Sieburth D, Ch'ng Q, Dybbs M, et al. Systematic analysis of genes required for synapse structure and function. Nature 2005;436:510-17
91. Panzer JA, Gibbs SM, Dosch R, et al. Neuromuscular synaptogenesis in wild-type and mutant zebrafish. Dev Biol 2005;285:340-57
92. Schenk D, Barbour R, Dunn W, et al. Immunization with amyloid-beta attenuates Alzheimer-disease-like pathology in the PDAPP mouse. Nature 1999;400:173-77
93. Klyubin I, Walsh DM, Lemere CA, et al. Amyloid beta protein immunotherapy neutralizes Abeta oligomers that disrupt synaptic plasticity in vivo. Nat Med 2005;11:556-61
94. Trachtenberg JT, Chen BE, Knott GW, et al. Long-term in vivo imaging of experience-dependent synaptic plasticity in adult cortex. Nature 2002;420:788-94
95. Kasthuri N, Lichtman JW. Structural dynamics of synapses in living animals. Curr Opin Neurobiol 2004;14:105-11
96. Kumar A, Mann S, Sossi V, et al. [11C]DTBZ-PET correlates of levodopa responses in asymmetric Parkinson's disease. Brain 2003;126:2648-55
97. Sjoholm H, Bratlid T, Sundsfjord J. 123I-beta-CIT SPECT demonstrates increased presynaptic dopamine transporter binding sites in basal ganglia in vivo in schizophrenia. Psychopharmacology (Berl) 2004;173:27-31
98. Rapoport SI. In vivo imaging for evaluating synaptic integrity in Alzheimer disease. Psychol Neuropsychiatr Vieil 2005;3:97-106