Mechanisms underlying synaptic vulnerability and degeneration in neurodegenerative disease

Neuropathology and Applied Neurobiology

Volumn 39, Issue 4, 2013, Pages 320-334

  Gillingwater, T H ^a   Wishart, T M ^a,b  

^a UNIVERSITY OF EDINBURGH   (United Kingdom)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

Alzheimer's disease; Huntington's disease; Mitochondria; Neurodegeneration; Synaptic vulnerability; Ubiquitin

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE TRIPHOSPHATE; APOPTOSIS INDUCING FACTOR; CALRETININ; CYSTEINE STRING PROTEIN; MITOCHONDRIAL PROTEIN; PROTEASOME; REACTIVE OXYGEN METABOLITE; SPECTRIN; UBIQUITIN; UBIQUITIN CONJUGATING ENZYME;

ALZHEIMER DISEASE; CAENORHABDITIS ELEGANS; DEGENERATIVE DISEASE; DISEASE ASSOCIATION; DISEASE COURSE; DROSOPHILA; ENDOCYTOSIS; FRAGILE X SYNDROME; HUNTINGTON CHOREA; MITOCHONDRIAL ENERGY TRANSFER; MITOCHONDRION; MOTOR DYSFUNCTION; NERVE DEGENERATION; NERVE FIBER DEGENERATION; NONHUMAN; PARKINSON DISEASE; PRIORITY JOURNAL; PROTEIN PROCESSING; REVIEW; SPASTIC PARAPLEGIA; SPINOCEREBELLAR DEGENERATION; SYNAPSE VESICLE; SYNAPTIC TRANSMISSION; SYNAPTIC VULNERABILITY; UBIQUITINATION;

ANIMALS; HUMANS; MITOCHONDRIA; NEURODEGENERATIVE DISEASES; PROTEASOME ENDOPEPTIDASE COMPLEX; PROTEIN PROCESSING, POST-TRANSLATIONAL; SIGNAL TRANSDUCTION; SYNAPSES; UBIQUITIN;

EID: 84876883390     PISSN: 03051846     EISSN: 13652990     Source Type: Journal    
DOI: 10.1111/nan.12014     Document Type: Review

References (195)

1. National Institute of Health Statistics. 2010. Alzheimer's Disease. Accessed at: http://report.nih.gov/nihfactsheets/ViewFactSheet.aspx?csid=107 (last accessed 18 October 2012).
2. Hay JW, Ernst RL. The economic costs of Alzheimer's disease. Am J Public Health 1987; 77: 1169-1175. PMID: 3113273.
3. Wishart TM, Parson SH, Gillingwater TH. Synaptic vulnerability in neurodegenerative disease. J Neuropathol Exp Neurol 2006; 65: 733-739. PMID: 16896307.
4. Marcello E, Epis R, Saraceno C, Di Luca M. Synaptic dysfunction in Alzheimer's disease. Adv Exp Med Biol 2012; 970: 573-601. PMID: 22351073.
5. Picconi B, Piccoli G, Calabresi P. Synaptic dysfunction in Parkinson's disease. Adv Exp Med Biol 2012; 970: 553-572. PMID: 22351072.
6. Yin DM, Chen YJ, Sathyamurthy A, Xiong WC, Mei L. Synaptic dysfunction in schizophrenia. Adv Exp Med Biol 2012; 970: 493-516. PMID: 22351070.
7. Chiesa R, Piccardo P, Dossena S, Nowoslawski L, Roth KA, Ghetti B, Harris DA. 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: 238-243. PMID: 15618403.
8. Koike T, Yang Y, Suzuki K, Zheng X. Axon & dendrite degeneration: its mechanisms and protective experimental paradigms. Neurochem Int 2007; 52: 751-760. PMID: 18029056.
9. Bachstetter AD, Norris CM, Sompol P, Wilcock DM, Goulding D, Neltner JH, St Clair D, Watterson DM, Van Eldik LJ. Early stage drug treatment that normalizes proinflammatory cytokine production attenuates synaptic dysfunction in a mouse model that exhibits age-dependent progression of Alzheimer's disease-related pathology. J Neurosci 2012; 32: 10201-10210. PMID: 22836255.
10. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, Hansen LA, Katzman R. Physical basis of cognitive alterations in Alzheimer's disease: synapse loss is the major correlate of cognitive impairment. Ann Neurol 1991; 30: 572-580. PMID: 1789684.
11. Lee SH, Kim KR, Ryu SY, Son S, Hong HS, Mook-Jung I, Lee SH, Ho WK. Impaired short-term plasticity in mossy fiber synapses caused by mitochondrial dysfunction of dentate granule cells is the earliest synaptic deficit in a mouse model of Alzheimer's disease. J Neurosci 2012; 32: 5953-5963. PMID: 22539855.
12. Balietti M, Tamagnini F, Fattoretti P, Burattini C, Casoli T, Platano D, Lattanzio F, Aicardi G. Impairments of synaptic plasticity in aged animals and in animal models of Alzheimer's disease. Rejuvenation Res 2012; 15: 235-238. PMID: 22533439.
13. Sheng M, Sabatini BL, Südhof TC. Synapses and Alzheimer's disease. Cold Spring Harb Perspect Biol 2012; 4: a005777. PMID: 22491782.
14. Ferrer I, López-Gonzalez I, Carmona M, Dalfó E, Pujol A, Martínez A. Neurochemistry and the non-motor aspects of PD. Neurobiol Dis 2012; 46: 508-526. PMID: 22737710.
15. Cunningham C, Deacon R, Wells H, Boche D, Waters S, Diniz CP, Scott H, Rawlins JN, Perry VH. Synaptic changes characterize early behavioural signs in the ME7 model of murine prion disease. Eur J Neurosci 2003; 17: 2147-2155. PMID: 12786981.
16. Bate C, Williams A. Clustering of sialylated glycosylphosphatidylinositol anchors mediates prp-induced activation of cytoplasmic phospholipase A 2 and synapse damage. Prion 2012; 6: 350-353. PMID: 22895089.
17. Caleo M, Restani L, Vannini E, Siskova Z, Al-Malki H, Morgan R, O'Connor V, Perry VH. The role of activity in synaptic degeneration in a protein misfolding disease, prion disease. PLoS ONE 2012; 7: e41182. PMID: 22815961.
18. Perkins EM, Clarkson YL, Sabatier N, Longhurst DM, Millward CP, Jack J, Toraiwa J, Watanabe M, Rothstein JD, Lyndon AR, Wyllie DJ, Dutia MB, Jackson M. Loss of beta-iii spectrin leads to purkinje cell dysfunction recapitulating the behavior and neuropathology of spinocerebellar ataxia type 5 in humans. J Neurosci 2010; 30: 4857-4867. PMID: 20371805.
19. Gao Y, Perkins EM, Clarkson YL, Tobia S, Lyndon AR, Jackson M, Rothstein JD. β-III spectrin is critical for development of purkinje cell dendritic tree and spine morphogenesis. J Neurosci 2011; 31: 16581-16590. PMID: 22090485.
20. Hourez R, Servais L, Orduz D, Gall D, Millard I, de Kerchove d'Exaerde A, Cheron G, Orr HT, Pandolfo M, Schiffmann SN. Aminopyridines correct early dysfunction and delay neurodegeneration in a mouse model of spinocerebellar ataxia type 1. J Neurosci 2011; 31: 11795-11807. PMID: 21849540.
21. Gunčová I, Látr I, Mazurová Y. The neurodegenerative process in a neurotoxic rat model and in patients with Huntington's disease: histopathological parallels and differences. Acta Histochem 2011; 113: 783-792. PMID: 21193226.
22. Milnerwood AJ, Kaufman AM, Sepers MD, Gladding CM, Zhang L, Wang L, Fan J, Coquinco A, Qiao JY, Lee H, Wang YT, Cynader M, Raymond LA. Mitigation of augmented extrasynaptic NMDAR signaling and apoptosis in cortico-striatal co-cultures from Huntington's disease mice. Neurobiol Dis 2012; 48: 40-51. PMID: 22668780.
23. Nithianantharajah J, Hannan AJ. Dysregulation of synaptic proteins, dendritic spine abnormalities and pathological plasticity of synapses as experience-dependent mediators of cognitive and psychiatric symptoms in Huntington's disease. Neuroscience 2012; http://dx.doi.org/10.1016/j.neuroscience.2012.05.043. PMID: 22633949.
24. Raymond LA, André VM, Cepeda C, Gladding CM, Milnerwood AJ, Levine MS. Pathophysiology of Huntington's disease: time-dependent alterations in synaptic and receptor function. Neuroscience 2011; 198: 252-273. PMID: 21907762.
25. Virmani T, Gupta P, Liu X, Kavalali ET, Hofmann SL. Progressively reduced synaptic vesicle pool size in cultured neurons derived from neuronal ceroid lipofuscinosis-1 knockout mice. Neurobiol Dis 2005; 20: 314-323. PMID: 16242638.
26. Kielar C, Wishart TM, Palmer A, Dihanich S, Wong AM, Macauley SL, Chan CH, Sands MS, Pearce DA, Cooper JD, Gillingwater TH. Molecular correlates of axonal and synaptic pathology in mouse models of Batten disease. Hum Mol Genet 2009; 18: 4066-4080. PMID: 19640925.
27. Luiro K, Kopra O, Blom T, Gentile M, Mitchison HM, Hovatta I, Törnquist K, Jalanko A. Batten disease (JNCL) is linked to disturbances in mitochondrial, cytoskeletal, and synaptic compartments. J Neurosci Res 2006; 84: 1124-1138. PMID: 16941499.
28. Pressey SN, Smith DA, Wong AM, Platt FM, Cooper JD. Early glial activation, synaptic changes and axonal pathology in the thalamocortical system of niemann-pick type C1 mice. Neurobiol Dis 2012; 45: 1086-1100. PMID: 22198570.
29. Fischer LR, Culver DG, Tennant P, Davis AA, Wang M, Castellano-Sanchez A, Khan J, Polak MA, Glass JD. Amyotrophic lateral sclerosis is a distal axonopathy: evidence in mice and man. Exp Neurol 2004; 185: 232-240. PMID: 14736504.
30. Murray LM, Comley LH, Thomson D, Parkinson N, Talbot K, Gillingwater TH. Selective vulnerability of motor neurons and dissociation of pre- and post-synaptic pathology at the neuromuscular junction in mouse models of spinal muscular atrophy. Hum Mol Genet 2008; 17: 949-962. PMID: 18065780.
31. Martinez TL, Kong L, Wang X, Osborne MA, Crowder ME, Van Meerbeke JP, Xu X, Davis C, Wooley J, Goldhamer DJ, Lutz CM, Rich MM, Sumner CJ. Survival motor neuron protein in motor neurons determines synaptic integrity in spinal muscular atrophy. J Neurosci 2012; 32: 8703-8715. PMID: 22723710.
32. Coleman P, Federoff H, Kurlan R. A focus on the synapse for neuroprotection in Alzheimer disease and other dementias. Neurology 2004; 63: 1155-1162. PMID: 15477531.
33. Larson J, Lynch G, Games D, Seubert P. Alterations in synaptic transmission and long-term potentiation in hippocampal slices from young and aged PDAPP mice. Brain Res 1999; 840: 23-35. PMID: 10517949.
34. Chapman PF, White GL, Jones MW, Cooper-Blacketer D, Marshall VJ, Irizarry M, Younkin L, Good MA, Bliss TV, Hyman BT, Younkin SG, Hsiao KK. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat Neurosci 1999; 2: 271-276. PMID: 10195221.
35. DeKosky ST, Davies SW. Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann Neurol 1990; 27: 457-464. PMID: 2360787.
36. Scheff SW, Price DA. Synaptic pathology in Alzheimer's disease: a review of ultrastructural studies. Neurobiol Aging 2003; 24: 1029-1046. PMID: 14643375.
37. Davies CA, Mann DM, Sumpter PQ, Yates PO. 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: 151-164. PMID: 3572454.
38. Graveland GA, Williams RS, DiFiglia M. Evidence for degenerative and regenerative changes in neostriatal spiny neurons in Huntington's disease. Science 1985; 227: 770-773. PMID: 3155875.
39. 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: 3877-3887. PMID: 1836019.
40. Modregger J, DiProspero NA, Charles V, Tagle DA, Plomann M. PACSIN 1 interacts with huntingtin and is absent from synaptic varicosities in presymptomatic Huntington's disease brains. Hum Mol Genet 2002; 11: 2547-2558. PMID: 12354780.
41. DiProspero NA, Chen EY, Charles V, Plomann M, Kordower JH, Tagle DA. Early changes in Huntington's disease patient brains involve alterations in cytoskeletal and synaptic elements. J Neurocytol 2004; 33: 517-533. PMID: 15906159.
42. Li J-Y, Plomann M, Brundin P. Huntington's disease: a synaptopathy? Trends Mol Med 2003; 9: 414-420. PMID: 14557053.
43. Partanen S, Haapanen A, Kielar C, Pontikis C, Alexander N, Inkinen T, Saftig P, Gillingwater TH, Cooper JD, Tyynelä J. Synaptic changes in the thalamocortical system of cathepsin D-deficient mice: a model of human congenital neuronal ceroid-lipofuscinosis. J Neuropathol Exp Neurol 2008; 67: 16-29. PMID: 18091563.
44. Koch S, Molchanova SM, Wright AK, Edwards A, Cooper JD, Taira T, Gillingwater TH, Tyynelä J. Morphologic and functional correlates of synaptic pathology in the cathepsin D knockout mouse model of congenital neuronal ceroid lipofuscinosis. J Neuropathol Exp Neurol 2011; 70: 1089-1096. PMID: 22082660.
45. Harris KM, Weinberg RJ. Ultrastructure of synapses in the mammalian brain. Cold Spring Harb Perspect Biol 2012; 4: a005587. PMID: 22357909.
46. Reddy PH, Shirendeb UP. Mutant huntingtin, abnormal mitochondrial dynamics, defective axonal transport of mitochondria, and selective synaptic degeneration in Huntington's disease. Biochim Biophys Acta 2012; 1822: 101-110. PMID: 22080977.
47. Manji H, Kato T, Di Prospero NA, Ness S, Beal MF, Krams M, Chen G. Impaired mitochondrial function in psychiatric disorders. Nat Rev Neurosci 2012; 13: 293-307. PMID: 22510887.
48. Shetty PK, Galeffi F, Turner DA. Cellular links between neuronal activity and energy homeostasis. Front Pharmacol 2012; 3: 43. PMID: 22470340.
49. Breuer ME, Koopman WJ, Koene S, Nooteboom M, Rodenburg RJ, Willems PH, Smeitink JA. The role of mitochondrial OXPHOS dysfunction in the development of neurologic diseases. Neurobiol Dis 2012; http://dx.doi.org/10.1016/j.nbd.2012.03.007. PMID: 22426394.
50. Perluigi M, Di Domenico F, Giorgi A, Schininà ME, Coccia R, Cini C, Bellia F, Cambria MT, Cornelius C, Butterfield DA, Calabrese V. Redox proteomics in aging rat brain: involvement of mitochondrial reduced glutathione status and mitochondrial protein oxidation in the aging process. J Neurosci Res 2010; 88: 3498-3507. PMID: 20936692.
51. Lee CW, Peng HB. The function of mitochondria in presynaptic development at the neuromuscular junction. Mol Biol Cell 2008; 19: 150-158. PMID: 17942598.
52. Attwell D, Laughlin SB. An energy budget for signaling in the grey matter of the brain. J Cereb Blood Flow Metab 2001; 21: 1133-1145. PMID: 11598490.
53. Verstreken P, Ly CV, Venken KJ, Koh TW, Zhou Y, Bellen HJ. Synaptic mitochondria are critical for mobilization of reserve pool vesicles at drosophila neuromuscular junctions. Neuron 2005; 47: 365-378. PMID: 16055061.
54. Raimondo JV, Irkle A, Wefelmeyer W, Newey SE, Akerman CJ. Genetically encoded proton sensors reveal activity-dependent ph changes in neurons. Front Mol Neurosci 2012; 5: 68. PMID: 22666186.
55. Huang WC, Xiao S, Huang F, Harfe BD, Jan YN, Jan LY. Calcium-activated chloride channels (caccs) regulate action potential and synaptic response in hippocampal neurons. Neuron 2012; 74: 179-192. PMID: 22500639.
56. Billups B, Forsythe ID. Presynaptic mitochondrial calcium sequestration influences transmission at mammalian central synapses. J Neurosci 2002; 22: 5840-5847. PMID: 12122046.
57. Talbot JD, David G, Barrett EF. Inhibition of mitochondrial ca2+ uptake affects phasic release from motor terminals differently depending on external [ca2+]. J Neurophysiol 2003; 90: 491-502. PMID: 12672777.
58. Avery MA, Rooney TM, Pandya JD, Wishart TM, Gillingwater TH, Geddes JW, Sullivan PG, Freeman MR. WldS prevents axon degeneration through increased mitochondrial flux and enhanced mitochondrial ca2+ buffering. Curr Biol 2012; 22: 596-600. PMID: 22425157.
59. George EB, Glass JD, Griffin JW. Axotomy-induced axonal degeneration is mediated by calcium influx through ion-specific channels. J Neurosci 1995; 15: 6445-6452. PMID: 7472407.
60. Yi M, Weaver D, Hajnóczky G. Control of mitochondrial motility and distribution by the calcium signal: a homeostatic circuit. J Cell Biol 2004; 167: 661-672. PMID: 15545319.
61. Wang X, Schwarz TL. The mechanism of Ca2+-dependent regulation of kinesin-mediated mitochondrial motility. Cell 2009; 136: 163-174. PMID: 19135897.
62. Du H, Guo L, Yan S, Sosunov AA, McKhann GM, Yan SS. Early deficits in synaptic mitochondria in an Alzheimer's disease mouse model. Proc Natl Acad Sci U S A 2010; 107: 18670-18675. PMID: 20937894.
63. Sisková Z, Mahad DJ, Pudney C, Campbell G, Cadogan M, Asuni A, O'Connor V, Perry VH. Morphological and functional abnormalities in mitochondria associated with synaptic degeneration in prion disease. Am J Pathol 2010; 177: 1411-1421. PMID: 20651247.
64. Sharma AK, Searfoss GH, Reams RY, Jordan WH, Snyder PW, Chiang AY, Jolly RA, Ryan TP. Kainic acid-induced F-344 rat model of mesial temporal lobe epilepsy: gene expression and canonical pathways. Toxicol Pathol 2009; 37: 776-789. PMID: 19700661.
65. Maycotte P, Blancas S, Morán J. Role of inhibitor of apoptosis proteins and Smac/DIABLO in staurosporine-induced cerebellar granule neurons death. Neurochem Res 2008; 33: 1534-1540. PMID: 18338251.
66. Oxler EM, Dolga A, Culmsee C. AIF depletion provides neuroprotection through a preconditioning effect. Apoptosis 2012; 17: 1027-1038. PMID: 22865232.
67. Lee JH, Cheon YH, Woo RS, Song DY, Moon C, Baik TK. Evidence of early involvement of apoptosis inducing factor-induced neuronal death in Alzheimer brain. Anat Cell Biol 2012; 45: 26-37. PMID: 22536549.
68. Liu W, Fan Z, Han Y, Zhang D, Li J, Wang H. Intranuclear localization of apoptosis-inducing factor and endonuclease G involves in peroxynitrite-induced apoptosis of spiral ganglion neurons. Neurol Res 2012; 34: 915-922. PMID: 23006905.
69. Zhao ST, Chen M, Li SJ, Zhang MH, Li BX, Das M, Bean JC, Kong JM, Zhu XH, Gao TM. Mitochondrial BNIP3 upregulation precedes endonuclease G translocation in hippocampal neuronal death following oxygen-glucose deprivation. BMC Neurosci 2009; 10: 113. PMID: 19737385.
70. Ly CV, Verstreken P. Mitochondria at the synapse. Neuroscientist 2006; 12: 291-299. PMID: 16840705.
71. Bertoni-Freddari C, Fattoretti P, Casoli T, Spagna C, Meier-Ruge W, Ulrich J. Morphological plasticity of synaptic mitochondria during aging. Brain Res 1993; 628: 193-200. PMID: 8313147.
72. Lai JC, Walsh JM, Dennis SC, Clark JB. Synaptic and non-synaptic mitochondria from rat brain: isolation and characterization. J Neurochem 1977; 28: 625-631. PMID: 16086.
73. Friberg H, Connern C, Halestrap AP, Wieloch T. Differences in the activation of the mitochondrial permeability transition among brain regions in the rat correlate with selective vulnerability. J Neurochem 1999; 72: 2488-2497. PMID: 10349859.
74. Yarana C, Sanit J, Chattipakorn N, Chattipakorn S. Synaptic and nonsynaptic mitochondria demonstrate a different degree of calcium-induced mitochondrial dysfunction. Life Sci 2012; 90: 808-814. PMID: 22525373.
75. Brown MR, Sullivan PG, Geddes JW. Synaptic mitochondria are more susceptible to ca2+overload than nonsynaptic mitochondria. J Biol Chem 2006; 281: 11658-11668. PMID: 16517608.
76. Ligon LA, Steward O. Role of microtubules and actin filaments in the movement of mitochondria in the axons and dendrites of cultured hippocampal neurons. J Comp Neurol 2000; 427: 351-361. PMID: 11054698.
77. Menzies RA, Gold PH. The turnover of mitochondria in a variety of tissues of young adult and aged rats. J Biol Chem 1971; 246: 2425-2429. PMID: 5553400.
78. Amiri M, Hollenbeck PJ. Mitochondrial biogenesis in the axons of vertebrate peripheral neurons. Dev Neurobiol 2008; 68: 1348-1361. PMID: 18666204.
79. Mironov SL. ADP regulates movements of mitochondria in neurons. Biophys J 2007; 92: 2944-2952. PMID: 17277190.
80. Macaskill AF, Rinholm JE, Twelvetrees AE, Arancibia-Carcamo IL, Muir J, Fransson A, Aspenstrom P, Attwell D, Kittler JT. Miro1 is a calcium sensor for glutamate receptor-dependent localization of mitochondria at synapses. Neuron 2009; 61: 541-555. PMID: 19249275.
81. Kang JS, Tian JH, Pan PY, Zald P, Li C, Deng C, Sheng ZH. Docking of axonal mitochondria by syntaphilin controls their mobility and affects short-term facilitation. Cell 2008; 132: 137-148. PMID: 18191227.
82. Misgeld T, Kerschensteiner M, Bareyre FM, Burgess RW, Lichtman JW. Imaging axonal transport of mitochondria in vivo. Nat Methods 2007; 4: 559-561. PMID: 17558414.
83. Sheng ZH, Cai Q. Mitochondrial transport in neurons: impact on synaptic homeostasis and neurodegeneration. Nat Rev Neurosci 2012; 13: 77-93. PMID: 22218207.
84. Court FA, Coleman MP. Mitochondria as a central sensor for axonal degenerative stimuli. Trends Neurosci 2012; 35: 364-372. PMID: 22578891.
85. Tanaka Y, Kanai Y, Okada Y, Nonaka S, Takeda S, Harada A, Hirokawa N. Targeted disruption of mouse conventional kinesin heavy chain, kif5b, results in abnormal perinuclear clustering of mitochondria. Cell 1998; 93: 1147-1158. PMID: 9657148.
86. 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: 2057-2068. PMID: 16467387.
87. Chang DT, Reynolds IJ. Mitochondrial trafficking and morphology in healthy and injured neurons. Prog Neurobiol 2006; 80: 241-268. PMID: 17188795.
88. Chan DC. Mitochondria: dynamic organelles in disease, aging, and development. Cell 2006; 125: 1241-1252. PMID: 16814712.
89. Itoh K, Nakamura K, Iijima M, Sesaki H. Mitochondrial dynamics in neurodegeneration. Trends Cell Biol 2012; pii: S0962-8924(12)00184-5. PMID: 23159640.
90. Wang X, Su B, Siedlak SL, Moreira PI, Fujioka H, Wang Y, Casadesus G, Zhu X. Amyloid beta overproduction causes abnormal mitochondrial dynamics via differential modulation of mitochondrial fission/fusion proteins. Proc Natl Acad Sci U S A 2008; 105: 19318-19323. PMID: 19050078.
91. Kanaan NM, Pigino GF, Brady ST, Lazarov O, Binder LI, Morfini GA. Axonal degeneration in Alzheimer's disease: when signaling abnormalities meet the axonal transport system. Exp Neurol 2012; http://dx.doi.org/10.1016/j.expneurol.2012.06.003. PMID: 22721767.
92. Santos RX, Correia SC, Wang X, Perry G, Smith MA, Moreira PI, Zhu X. Alzheimer's disease: diverse aspects of mitochondrial malfunctioning. Int J Clin Exp Pathol 2010; 3: 570-581. PMID: 20661404.
93. Caviston JP, Ross JL, Antony SM, Tokito M, Holzbaur EL. Huntingtin facilitates dynein/dynactin-mediated vesicle transport. Proc Natl Acad Sci U S A 2007; 104: 10045-10050. PMID: 17548833.
94. Trushina E, Dyer RB, Badger JD, Ure D, Eide L, Tran DD, Vrieze BT, Legendre-Guillemin V, McPherson PS, Mandavilli BS, Van Houten B, Zeitlin S, McNiven M, Aebersold R, Hayden M, Parisi JE, Seeberg E, Dragatsis I, Doyle K, Bender A, Chacko C, McMurray CT. Mutant huntingtin impairs axonal trafficking in mammalian neurons in vivo and in vitro. Mol Cell Biol 2004; 24: 8195-8209. PMID: 15340079.
95. Weihofen A, Thomas KJ, Ostaszewski BL, Cookson MR, Selkoe DJ. Pink1 forms a multiprotein complex with miro and milton, linking pink1 function to mitochondrial trafficking. Biochemistry 2009; 48: 2045-2052. PMID: 19152501.
96. Yang F, Jiang Q, Zhao J, Ren Y, Sutton MD, Feng J. Parkin stabilizes microtubules through strong binding mediated by three independent domains. J Biol Chem 2005; 280: 17154-17162. PMID: 15737990.
97. Xie W, Chung KK. Alpha-synuclein impairs normal dynamics of mitochondria in cell and animal models of Parkinson's disease. J Neurochem 2012; 122: 404-414. PMID: 22537068.
98. Yao A, Jin S, Li X, Liu Z, Ma X, Tang J, Zhang YQ. Drosophila FMRP regulates microtubule network formation and axonal transport of mitochondria. Hum Mol Genet 2011; 20: 51-63. PMID: 20935173.
99. Baloh RH. Mitochondrial dynamics and peripheral neuropathy. Neuroscientist 2008; 14: 12-18. PMID: 17911220.
100. Wang J, He Z. NAD and axon degeneration: from the wlds gene to neurochemistry. Cell Adh Migr 2009; 3: 77-87. PMID: 19372760.
101. Wishart TM, Paterson JM, Short DM, Meredith S, Robertson KA, Sutherland C, Cousin MA, Dutia MB, Gillingwater TH. Differential proteomics analysis of synaptic proteins identifies potential cellular targets and protein mediators of synaptic neuroprotection conferred by the slow wallerian degeneration (wlds) gene. Mol Cell Proteomics 2007; 6: 1318-1330. PMID: 17470424.
102. Gillingwater TH, Ingham CA, Parry KE, Wright AK, Haley JE, Wishart TM, Arbuthnott GW, Ribchester RR. Delayed synaptic degeneration in the CNS of wlds mice after cortical lesion. Brain 2006; 129: 1546-1556. PMID: 16738060.
103. Wright AK, Wishart TM, Ingham CA, Gillingwater TH. Synaptic protection in the brain of wlds mice occurs independently of age but is sensitive to gene-dose. PLoS ONE 2010; 5: e15108. PMID: 21124744.
104. Osterloh JM, Yang J, Rooney TM, Fox AN, Adalbert R, Powell EH, Sheehan AE, Avery MA, Hackett R, Logan MA, MacDonald JM, Ziegenfuss JS, Milde S, Hou YJ, Nathan C, Ding A, Brown RH Jr, Conforti L, Coleman M, Tessier-Lavigne M, Züchner S, Freeman MR. DSarm/sarm1 is required for activation of an injury-induced axon death pathway. Science 2012; 337: 481-484. PMID: 22678360.
105. Chang C, Hsieh YW, Lesch BJ, Bargmann CI, Chuang CF. Microtubule-based localization of a synaptic calcium-signaling complex is required for left-right neuronal asymmetry in C. elegans. Development 2011; 138: 3509-3518. PMID: 21771813.
106. van Zundert B, Izaurieta P, Fritz E, Alvarez FJ. Early pathogenesis in the adult-onset neurodegenerative disease amyotrophic lateral sclerosis. J Cell Biochem 2012; 113: 3301-3312. PMID: 22740507.
107. Chakroborty S, Kim J, Schneider C, Jacobson C, Molgó J, Stutzmann GE. Early presynaptic and postsynaptic calcium signaling abnormalities mask underlying synaptic depression in presymptomatic Alzheimer's disease mice. J Neurosci 2012; 32: 8341-8353. PMID: 22699914.
108. Costa C, Sgobio C, Siliquini S, Tozzi A, Tantucci M, Ghiglieri V, Di Filippo M, Pendolino V, de Iure A, Marti M, Morari M, Spillantini MG, Latagliata EC, Pascucci T, Puglisi-Allegra S, Gardoni F, Di Luca M, Picconi B, Calabresi P. Mechanisms underlying the impairment of hippocampal long-term potentiation and memory in experimental Parkinson's disease. Brain 2012; 135: 1884-1899. PMID: 22561640.
109. Flavell SW, Greenberg ME. Signaling mechanisms linking neuronal activity to gene expression and plasticity of the nervous system. Annu Rev Neurosci 2008; 31: 563-590. PMID: 18558867.
110. Buchner E, Gundersen CB. The dnaj-like cysteine string protein and exocytotic neurotransmitter release. Trends Neurosci 1997; 20: 223-227. PMID: 9141199.
111. Chamberlain LH, Burgoyne RD. Cysteine-string protein: the chaperone at the synapse. J Neurochem 2000; 74: 1781-1789. PMID: 10800920.
112. Fernández-Chacón R, Wölfel M, Nishimune H, Tabares L, Schmitz F, Castellano-Muñoz M, Rosenmund C, Montesinos ML, Sanes JR, Schneggenburger R, Südhof TC. The synaptic vesicle protein CSP alpha prevents presynaptic degeneration. Neuron 2004; 42: 237-251. PMID: 15091340.
113. Schmitz F, Tabares L, Khimich D, Strenzke N, de la Villa-Polo P, Castellano-Muñoz M, Bulankina A, Moser T, Fernández-Chacón R, Südhof TC. CSPalpha-deficiency causes massive and rapid photoreceptor degeneration. Proc Natl Acad Sci U S A 2006; 103: 2926-2931. PMID: 16477021.
114. García-Junco-Clemente P, Cantero G, Gómez-Sánchez L, Linares-Clemente P, Martínez-López JA, Luján R, Fernández-Chacón R. Cysteine string protein-alpha prevents activity-dependent degeneration in gabaergic synapses. J Neurosci 2010; 30: 7377-7391. PMID: 20505105.
115. Velinov M, Dolzhanskaya N, Gonzalez M, Powell E, Konidari I, Hulme W, Staropoli JF, Xin W, Wen GY, Barone R, Coppel SH, Sims K, Brown WT, Züchner S. Mutations in the gene DNAJC5 cause autosomal dominant kufs disease in a proportion of cases: study of the parry family and 8 other families. PLoS ONE 2012; 7: e29729. PMID: 22235333.
116. Scott D, Roy S. A-synuclein inhibits intersynaptic vesicle mobility and maintains recycling-pool homeostasis. J Neurosci 2012; 32: 10129-10135. PMID: 22836248.
117. Singleton AB. Altered alpha-synuclein homeostasis causing Parkinson's disease: the potential roles of dardarin. Trends Neurosci 2005; 28: 416-421. PMID: 15955578.
118. Lim Y, Kehm VM, Lee EB, Soper JH, Li C, Trojanowski JQ, Lee VM. A-Syn suppression reverses synaptic and memory defects in a mouse model of dementia with Lewy bodies. J Neurosci 2011; 31: 10076-10087. PMID: 21734300.
119. Volpicelli-Daley LA, Luk KC, Patel TP, Tanik SA, Riddle DM, Stieber A, Meaney DF, Trojanowski JQ, Lee VM. Exogenous α-synuclein fibrils induce Lewy body pathology leading to synaptic dysfunction and neuron death. Neuron 2011; 72: 57-71. PMID: 21982369.
120. Ellucci A, Zaltieri M, Navarria L, Grigoletto J, Missale C, Spano P. From α-synuclein to synaptic dysfunctions: new insights into the pathophysiology of Parkinson's disease. Brain Res 2012; 1476: 183-202. PMID: 22560500.
121. Rozas JL, Gómez-Sánchez L, Mircheski J, Linares-Clemente P, Nieto-González JL, Vázquez ME, Luján R, Fernández-Chacón R. Motorneurons require cysteine string protein-α to maintain the readily releasable vesicular pool and synaptic vesicle recycling. Neuron 2012; 74: 151-165. PMID: 22500637.
122. Burgoyne RD, Morgan A. Chaperoning the snares: a role in preventing neurodegeneration? Nat Cell Biol 2011; 13: 8. PMID: 21173802.
123. Bennett V, Healy J. Membrane domains based on ankyrin and spectrin associated with cell-cell interactions. Cold Spring Harb Perspect Biol 2009; 1: a003012. PMID: 20457566.
124. Lorenzo DN, Li MG, Mische SE, Armbrust KR, Ranum LP, Hays TS. Spectrin mutations that cause spinocerebellar ataxia type 5 impair axonal transport and induce neurodegeneration in drosophila. J Cell Biol 2010; 189: 143-158. PMID: 20368622.
125. Stankewich MC, Gwynn B, Ardito T, Ji L, Kim J, Robledo RF, Lux SE, Peters LL, Morrow JS. Targeted deletion of betaiii spectrin impairs synaptogenesis and generates ataxic and seizure phenotypes. Proc Natl Acad Sci U S A 2010; 107: 6022-6027. PMID: 20231455.
126. Jacob FD, Ho ES, Martinez-Ojeda M, Darras BT, Khwaja OS. Case of infantile onset spinocerebellar ataxia type 5. J Child Neurol 2012; doi:10.1177/0883073812454331. PMID: 22914369.
127. Cho E, Fogel BL. A family with spinocerebellar ataxia type 5 found to have a novel missense mutation within a SPTBN2 spectrin repeat. Cerebellum 2012; doi:10.1007/s12311-012-0408-0. PMID: 22843192.
128. Lee M, Paik SK, Lee MJ, Kim YJ, Kim S, Nahm M, Oh SJ, Kim HM, Yim J, Lee CJ, Bae YC, Lee S. Drosophila atlastin regulates the stability of muscle microtubules and is required for synapse development. Dev Biol 2009; 330: 250-262. PMID: 19341724.
129. Valdmanis PN, Meijer IA, Reynolds A, Lei A, MacLeod P, Schlesinger D, Zatz M, Reid E, Dion PA, Drapeau P, Rouleau GA. Mutations in the KIAA0196 gene at the SPG8 locus cause hereditary spastic paraplegia. Am J Hum Genet 2007; 80: 152-161. PMID: 17160902.
130. Debili N, Kieffer N, Mitjavila MT, Villeval JL, Guichard J, Teillet F, Henri A, Clemetson KJ, Vainchenker W, Breton-Gorius J. Expression of platelet glycoproteins by erythroid blasts in four cases of trisomy 21. Leukemia 1989; 3: 669-678. PMID: 2527326.
131. Wishart TM, Rooney TM, Lamont DJ, Wright AK, Morton AJ, Jackson M, Freeman MR, Gillingwater TH. Combining comparative proteomics and molecular genetics uncovers regulators of synaptic and axonal stability and degeneration in vivo. PLoS Genet 2012; 8: e1002936. PMID: 22952455.
132. Flynn JM, Czerwieniec GA, Choi SW, Day NU, Gibson BW, Hubbard A, Melov S. Proteogenomics of synaptosomal mitochondrial oxidative stress. Free Radic Biol Med 2012; 53: 1048-1060. PMID: 22796328.
133. Martins-de-Souza D, Guest PC, Mann DM, Roeber S, Rahmoune H, Bauder C, Kretzschmar H, Volk B, Baborie A, Bahn S. Proteomic analysis identifies dysfunction in cellular transport, energy, and protein metabolism in different brain regions of atypical frontotemporal lobar degeneration. J Proteome Res 2012; 11: 2533-2543. PMID: 22360420.
134. Végh MJ, de Waard MC, van der Pluijm I, Ridwan Y, Sassen MJ, van Nierop P, van der Schors RC, Li KW, Hoeijmakers JH, Smit AB, van Kesteren RE. Synaptic proteome changes in a DNA repair deficient ercc1 mouse model of accelerated aging. J Proteome Res 2012; 11: 1855-1867. PMID: 22289077.
135. Abe K, Yamaguchi S, Sugiura M, Saito H. The ethanol metabolite acetaldehyde inhibits the induction of long-term potentiation in the rat dentate gyrus in vivo. Br J Pharmacol 1999; 127: 1805-1810. PMID: 10482910.
136. Zhou Z, Meng Y, Asrar S, Todorovski Z, Jia Z. A critical role of rho-kinase ROCK2 in the regulation of spine and synaptic function. Neuropharmacology 2009; 56: 81-89. PMID: 18718479.
137. Wey MC, Fernandez E, Martinez PA, Sullivan P, Goldstein DS, Strong R. Neurodegeneration and motor dysfunction in mice lacking cytosolic and mitochondrial aldehyde dehydrogenases: implications for Parkinson's disease. PLoS ONE 2012; 7: e31522. PMID: 22384032.
138. Fotin A, Cheng Y, Grigorieff N, Walz T, Harrison SC, Kirchhausen T. Structure of an auxilin-bound clathrin coat and its implications for the mechanism of uncoating. Nature 2004; 432: 649-653. PMID: 15502813.
139. Maycox PR, Link E, Reetz A, Morris SA, Jahn R. Clathrin-coated vesicles in nervous tissue are involved primarily in synaptic vesicle recycling. J Cell Biol 1992; 118: 1379-1388. PMID: 1325974.
140. Morgan JR, Prasad K, Jin S, Augustine GJ, Lafer EM. Uncoating of clathrin-coated vesicles in presynaptic terminals: roles for hsc70 and auxilin. Neuron 2001; 32: 289-300. PMID: 11683998.
141. Van Eldik LJ, Zendegui JG, Marshak DR, Watterson DM. Calcium-binding proteins and the molecular basis of calcium action. Int Rev Cytol 1982; 77: 1-61. PMID: 6757171.
142. Pascual ML, Luchelli L, Habif M, Boccaccio GL. Synaptic activity regulated mRNA-silencing foci for the fine tuning of local protein synthesis at the synapse. Commun Integr Biol 2012; 5: 388-392. PMID: 23060966.
143. Craig TJ, Jaafari N, Petrovic MM, Rubin PP, Mellor JR, Henley JM. Homeostatic synaptic scaling is regulated by protein sumoylation. J Biol Chem 2012; 287: 22781-22788. PMID: 22582390.
144. Catarino T, Ribeiro L, Santos SD, Carvalho AL. Regulation of synapse composition by protein acetylation: the role of acetylated cortactin. J Cell Sci 2012; doi:10.1242/jcs.110742. PMID: 23038781.
145. Cajigas IJ, Will T, Schuman EM. Protein homeostasis and synaptic plasticity. EMBO J 2010; 29: 2746-2752. PMID: 20717144.
146. Schwarz LA, Patrick GN. Ubiquitin-dependent endocytosis, trafficking and turnover of neuronal membrane proteins. Mol Cell Neurosci 2012; 49: 387-393. PMID: 21884797.
147. Ding M, Shen K. The role of the ubiquitin proteasome system in synapse remodeling and neurodegenerative diseases. Bioessays 2008; 30: 1075-1083. PMID: 18937340.
148. Schlesinger DH, Goldstein G. Molecular conservation of 74 amino acid sequence of ubiquitin between cattle and man. Nature 1975; 255: 42304. PMID: 1128706.
149. Turowski G, Zak Z, Gałka M. The ubiquitin system as a balance between monomers and polymers in polypeptide structure. Folia Biol (Krakow) 1977; 25: 429-433. PMID: 606569.
150. Kim I, Rao H. What's ub chain linkage got to do with it? Sci STKE 2006; 2006: pe18. PMID: 16608998.
151. Pickart CM, Fushman D. Polyubiquitin chains: polymeric protein signals. Curr Opin Chem Biol 2004; 8: 610-616. PMID: 15556404.
152. d'Azzo A, Bongiovanni A, Nastasi T. E3 ubiquitin ligases as regulators of membrane protein trafficking and degradation. Traffic 2005; 6: 429-441. PMID: 21884797.
153. Speese SD, Trotta N, Rodesch CK, Aravamudan B, Broadie K. The ubiquitin proteasome system acutely regulates presynaptic protein turnover and synaptic efficacy. Curr Biol 2003; 13: 899-910. PMID: 12781128.
154. Dreier L, Burbea M, Kaplan JM. LIN-23-mediated degradation of beta-catenin regulates the abundance of GLR-1 glutamate receptors in the ventral nerve cord of C. elegans. Neuron 2005; 46: 51-64. PMID: 15820693.
155. Zhai Q, Wang J, Kim A, Liu Q, Watts R, Hoopfer E, Mitchison T, Luo L, He Z. Involvement of the ubiquitin-proteasome system in the early stages of wallerian degeneration. Neuron 2003; 39: 217-225. PMID: 12873380.
156. Kuo CT, Zhu S, Younger S, Jan LY, Jan YN. Identification of E2/E3 ubiquitinating enzymes and caspase activity regulating drosophila sensory neuron dendrite pruning. Neuron 2006; 51: 283-290. PMID: 16880123.
157. Ikeda F, Dikic I. Atypical ubiquitin chains: new molecular signals. 'Protein modifications: beyond the usual suspects' review series. EMBO Rep 2008; 9: 536-542. PMID: 16608998.
158. Ramser J, Ahearn ME, Lenski C, Yariz KO, Hellebrand H, von Rhein M, Clark RD, Schmutzler RK, Lichtner P, Hoffman EP, Meindl A, Baumbach-Reardon L. Rare missense and synonymous variants in UBE1 are associated with X-linked infantile spinal muscular atrophy. Am J Hum Genet 2008; 82: 188-193. PMID: 18179898.
159. Wilson RC, Hughes RC, Flatt JW, Meehan EJ, Ng JD, Twigg PD. Structure of full-length ubiquitin-conjugating enzyme E2-25K (huntingtin-interacting protein 2). Acta Crystallogr Sect F Struct Biol Cryst Commun 2009; 65: 440-444. PMID: 19407372.
160. Song S, Jung YK. Alzheimer's disease meets the ubiquitin-proteasome system. Trends Mol Med 2004; 10: 565-570. PMID: 15519283.
161. Rosen KM, Moussa CE, Lee HK, Kumar P, Kitada T, Qin G, Fu Q, Querfurth HW. Parkin reverses intracellular beta-amyloid accumulation and its negative effects on proteasome function. J Neurosci Res 2010; 88: 167-178. PMID: 19610108.
162. Kumar P, Pradhan K, Karunya R, Ambasta RK, Querfurth HW. Cross-functional E3 ligases parkin and c-terminus hsp70-interacting protein in neurodegenerative disorders. J Neurochem 2012; 120: 350-370. PMID: 22098618.
163. Narendra DP, Youle RJ. Targeting mitochondrial dysfunction: role for PINK1 and Parkin in mitochondrial quality control. Antioxid Redox Signal 2011; 14: 1929-1938. PMID: 21194381.
164. Springer W, Kahle PJ. Regulation of pink1-parkin-mediated mitophagy. Autophagy 2011; 7: 266-278. PMID: 21187721.
165. Liu S, Sawada T, Lee S, Yu W, Silverio G, Alapatt P, Millan I, Shen A, Saxton W, Kanao T, Takahashi R, Hattori N, Imai Y, Lu B. Parkinson's disease-associated kinase PINK1 regulates Miro protein level and axonal transport of mitochondria. PLoS Genet 2012; 8: e1002537. PMID: 22396657.
166. Yi JJ, Ehlers MD. Emerging roles for ubiquitin and protein degradation in neuronal function. Pharmacol Rev 2007; 59: 14-39. PMID: 17329546.
167. Helton TD, Otsuka T, Lee MC, Mu Y, Ehlers MD. Pruning and loss of excitatory synapses by the parkin ubiquitin ligase. Proc Natl Acad Sci U S A 2008; 105: 19492-19497. PMID: 19033459.
168. Greer PL, Hanayama R, Bloodgood BL, Mardinly AR, Lipton DM, Flavell SW, Kim TK, Griffith EC, Waldon Z, Maehr R, Ploegh HL, Chowdhury S, Worley PF, Steen J, Greenberg ME. The angelman syndrome protein ube3a regulates synapse development by ubiquitinating arc. Cell 2010; 140: 704-716. PMID: 20211139.
169. Lu Y, Wang F, Li Y, Ferris J, Lee JA, Gao FB. The drosophila homologue of the angelman syndrome ubiquitin ligase regulates the formation of terminal dendritic branches. Hum Mol Genet 2009; 18: 454-462. PMID: 18996915.
170. Wallace ML, Burette AC, Weinberg RJ, Philpot BD. Maternal loss of ube3a produces an excitatory/inhibitory imbalance through neuron type-specific synaptic defects. Neuron 2012; 74: 793-800. PMID: 22681684.
171. Maheshwari M, Samanta A, Godavarthi SK, Mukherjee R, Jana NR. Dysfunction of the ubiquitin ligase ube3a may be associated with synaptic pathophysiology in a mouse model of Huntington disease. J Biol Chem 2012; 287: 29949-29957. PMID: 22787151.
172. Matsumoto M, Yada M, Hatakeyama S, Ishimoto H, Tanimura T, Tsuji S, Kakizuka A, Kitagawa M, Nakayama KI. Molecular clearance of ataxin-3 is regulated by a mammalian E4. EMBO J 2004; 23: 659-669. PMID: 14749733.
173. Conforti L, Tarlton A, Mack TG, Mi W, Buckmaster EA, Wagner D, Perry VH, Coleman MP. A ufd2/d4cole1e chimeric protein and overexpression of rbp7 in the slow wallerian degeneration (wlds) mouse. Proc Natl Acad Sci U S A 2000; 97: 11377-11382. PMID: 11027338.
174. Böhm S, Lamberti G, Fernández-Sáiz V, Stapf C, Buchberger A. Cellular functions of Ufd2 and Ufd3 in proteasomal protein degradation depend on Cdc48 binding. Mol Cell Biol 2011; 3: 1528-1539. PMID: 21282470.
175. Kaneko C, Hatakeyama S, Matsumoto M, Yada M, Nakayama K, Nakayama KI. Characterization of the mouse gene for the U-box-type ubiquitin ligase UFD2a. Biochem Biophys Res Commun 2003; 300: 297-304. PMID: 12504083.
176. Kaneko-Oshikawa C, Nakagawa T, Yamada M, Yoshikawa H, Matsumoto M, Yada M, Hatakeyama S, Nakayama K, Nakayama KI. Mammalian E4 is required for cardiac development and maintenance of the nervous system. Mol Cell Biol 2005; 25: 10953-10964. PMID: 16314518.
177. Mammen AL, Mahoney JA, St Germain A, Badders N, Taylor JP, Rosen A, Spinette S. A novel conserved isoform of the ubiquitin ligase ufd2a/UBE4B is expressed exclusively in mature striated muscle cells. PLoS ONE 2011; 6: e28861. PMID: 22174917.
178. Ge P, Zhang F, Zhao J, Liu C, Sun L, Hu B. Protein degradation pathways after brain ischemia. Curr Drug Targets 2012; 13: 159-165. PMID: 22204315.
179. Dimant H, Ebrahimi-Fakhari D, McLean PJ. Molecular chaperones and co-chaperones in Parkinson disease. Neuroscientist 2012; 18: 589-601. PMID: 22829394.
180. DiFiglia M, Sapp E, Chase KO, Davies SW, Bates GP, Vonsattel JP, Aronin N. Aggregation of huntingtin in neuronal intranuclear inclusions and dystrophic neurites in brain. Science 1997; 277: 1990-1993. PMID: 9302293.
181. Tai HC, Serrano-Pozo A, Hashimoto T, Frosch MP, Spires-Jones TL, Hyman BT. The synaptic accumulation of hyperphosphorylated tau oligomers in Alzheimer disease is associated with dysfunction of the ubiquitin-proteasome system. Am J Pathol 2012; 18: 1426-1435. PMID: 22867711.
182. Seo H, Sonntag KC, Isacson O. Generalized brain and skin proteasome inhibition in Huntington's disease. Ann Neurol 2004; 56: 319-328. PMID: 15349858.
183. Schipper-Krom S, Juenemann K, Reits EA. The ubiquitin-proteasome system in Huntington's disease: are proteasomes impaired, initiators of disease, or coming to the rescue? Biochem Res Int 2012; 2012: 837015. PMID: 23050151.
184. Ono S, Takahashi K, Fukuoka Y, Jinnai K, Kanda F, Kurisaki H, Mitake S, Inagaki T, Nagao K. Intracytoplasmic inclusion bodies of the substantia nigra in myotonic dystrophy. Immunohistochemical observations. J Neurol Sci 1997; 148: 193-198. PMID: 9129116.
185. Rozas JL, Gómez-Sánchez L, Tomás-Zapico C, Lucas JJ, Fernández-Chacón R. Presynaptic dysfunction in Huntington's disease. Biochem Soc Trans 2010; 38: 488-492. PMID: 20298208.
186. Martins-Branco D, Esteves AR, Santos D, Arduino DM, Swerdlow RH, Oliveira CR, Januario C, Cardoso SM. Ubiquitin proteasome system in Parkinson's disease: a keeper or a witness? Exp Neurol 2012; 238: 89-99. PMID: 22921536.
187. Ebrahimi-Fakhari D, Wahlster L, McLean PJ. Protein degradation pathways in Parkinson's disease: curse or blessing. Acta Neuropathol 2012; 124: 153-172. PMID: 22744791.
188. Huang Q, Figueiredo-Pereira ME. Ubiquitin/proteasome pathway impairment in neurodegeneration: therapeutic implications. Apoptosis 2010; 15: 1292-1311. PMID: 20131003.
189. Wang J, Wang CE, Orr A, Tydlacka S, Li SH, Li XJ. Impaired ubiquitin-proteasome system activity in the synapses of Huntington's disease mice. J Cell Biol 2008; 180: 1177-1189. PMID: 18362179.
190. Bajic N, Jenner P, Ballard CG, Francis PT. Proteasome inhibition leads to early loss of synaptic proteins in neuronal culture. J Neural Transm 2012; 119: 1467-1476. PMID: 22592936.
191. Upadhya SC, Hegde AN. Ubiquitin-proteasome pathway components as therapeutic targets for CNS maladies. Curr Pharm Des 2005; 11: 3807-3828. PMID: 16305513.
192. Malinow R, Malenka RC. AMPA receptor trafficking and synaptic plasticity. Annu Rev Neurosci 2002; 25: 103-126. PMID: 12052905.
193. Gal-Ben-Ari S, Kenney JW, Ounalla-Saad H, Taha E, David O, Levitan D, Gildish I, Panja D, Pai B, Wibrand K, Simpson TI, Proud CG, Bramham CR, Armstrong JD, Rosenblum K. Consolidation and translation regulation. Learn Mem 2012; 19: 410-422. PMID: 22904372.
194. Hughes CG, Patel MB, Pandharipande PP. Pathophysiology of acute brain dysfunction: what's the cause of all this confusion? Curr Opin Crit Care 2012; 18: 518-526. PMID: 22941208.
195. Calabresi P, Di Filippo M, Gallina A, Wang Y, Stankowski JN, Picconi B, Dawson VL, Dawson TM. New synaptic and molecular targets for neuroprotection in Parkinson's disease. Mov Disord 2012; doi:10.1002/mds.25096. PMID: 22927178.