Alzheimer-associated mutant ubiquitin impairs spatial reference memory

Physiology and Behavior

Volumn 102, Issue 2, 2011, Pages 193-200

  van Tijn, Paula ^a   Hobo, Barbara ^a   Verhage, Marian C ^a   Oitzl, Melly S ^b   van Leeuwen, Fred W ^a,c   Fischer, David F ^a,d  

^a NETHERLANDS INSTITUTE FOR NEUROSCIENCE   (Netherlands)

^b LEIDEN UNIVERSITY   (Netherlands)

^c MAASTRICHT UNIVERSITY   (Netherlands)

^d BioFocus DPI   (United Kingdom)

Author keywords

Behavior; Mutant ubiquitin; Neurodegeneration; Transgenic mouse model; Ubiquitin proteasome system

Indexed keywords

MUTANT PROTEIN; UBIQUITIN;

AGING; ANIMAL TISSUE; ARTICLE; BEHAVIOR; COGNITION; CONTROLLED STUDY; FOREBRAIN; GROUPS BY AGE; LEARNING DISORDER; MALE; MEMORY DISORDER; MOTOR COORDINATION; MOUSE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; REFERENCE MEMORY; TRANSGENIC MOUSE; WILD TYPE;

AGE FACTORS; ANALYSIS OF VARIANCE; ANIMALS; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HUMANS; MALE; MAZE LEARNING; MEMORY DISORDERS; MICE; MICE, INBRED C57BL; MICE, TRANSGENIC; MOTOR ACTIVITY; MUTATION; NEUROLOGIC EXAMINATION; PROSENCEPHALON; PROTEASOME ENDOPEPTIDASE COMPLEX; PSYCHOMOTOR PERFORMANCE; ROTAROD PERFORMANCE TEST; SPATIAL BEHAVIOR; UBIQUITIN;

EID: 78649344625     PISSN: 00319384     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.physbeh.2010.11.001     Document Type: Article

References (43)

1. Glickman M.H., Ciechanover A. The ubiquitin-proteasome proteolytic pathway: destruction for the sake of construction. Physiol Rev 2002, 82:373-428.
2. DiAntonio A., Hicke L. Ubiquitin-dependent regulation of the synapse. Annu Rev Neurosci 2004, 27:223-246.
3. Lopez-Salon M., Alonso M., Vianna M.R., Viola H., Mello e Souza T., Izquierdo I., et al. The ubiquitin-proteasome cascade is required for mammalian long-term memory formation. Eur J Neurosci 2001, 14:1820-1826.
4. Lee S.H., Choi J.H., Lee N., Lee H.R., Kim J.I., Yu N.K., et al. Synaptic protein degradation underlies destabilization of retrieved fear memory. Science 2008, 319:1253-1256.
5. Artinian J., McGauran A.M., De Jaeger X., Mouledous L., Frances B., Roullet P. Protein degradation, as with protein synthesis, is required during not only long-term spatial memory consolidation but also reconsolidation. Eur J Neurosci 2008, 27:3009-3019.
6. Gong B., Cao Z., Zheng P., Vitolo O.V., Liu S., Staniszewski A., et al. Ubiquitin hydrolase Uch-L1 rescues beta-amyloid-induced decreases in synaptic function and contextual memory. Cell 2006, 126:775-788.
7. Wood M.A., Kaplan M.P., Brensinger C.M., Guo W., Abel T. Ubiquitin C-terminal hydrolase L3 (Uchl3) is involved in working memory. Hippocampus 2005, 15:610-621.
8. van Tijn P., Hol E.M., van Leeuwen F.W., Fischer D.F. The neuronal ubiquitin-proteasome system: murine models and their neurological phenotype. Prog Neurobiol 2008, 85:176-193.
9. Ciechanover A., Brundin P. The ubiquitin proteasome system in neurodegenerative diseases: sometimes the chicken, sometimes the egg. Neuron 2003, 40:427-446.
10. van Leeuwen F.W., de Kleijn D.P., van den Hurk H.H., Neubauer A., Sonnemans M.A., Sluijs J.A., et al. Frameshift mutants of beta amyloid precursor protein and ubiquitin-B in Alzheimer's and Down patients. Science 1998, 279:242-247.
11. Fischer D.F., De Vos R.A., Van Dijk R., De Vrij F.M., Proper E.A., Sonnemans M.A., et al. Disease-specific accumulation of mutant ubiquitin as a marker for proteasomal dysfunction in the brain. FASEB J 2003, 17:2014-2024.
12. De Pril R., Fischer D.F., Maat-Schieman M.L., Hobo B., De Vos R.A., Brunt E.R., et al. Accumulation of aberrant ubiquitin induces aggregate formation and cell death in polyglutamine diseases. Hum Mol Genet 2004, 13:1803-1813.
13. Lindsten K., de Vrij F.M., Verhoef L.G., Fischer D.F., van Leeuwen F.W., Hol E.M., et al. Mutant ubiquitin found in neurodegenerative disorders is a ubiquitin fusion degradation substrate that blocks proteasomal degradation. J Cell Biol 2002, 157:417-427.
14. van Tijn P., de Vrij F.M., Schuurman K.G., Dantuma N.P., Fischer D.F., van Leeuwen F.W., et al. Dose-dependent inhibition of proteasome activity by a mutant ubiquitin associated with neurodegenerative disease. J Cell Sci 2007, 120:1615-1623.
15. Fischer D.F., van Dijk R., van Tijn P., Hobo B., Verhage M.C., van der Schors R.C., et al. Long-term proteasome dysfunction in the mouse brain by expression of aberrant ubiquitin. Neurobiol Aging 2009, 30:847-863.
16. Nicklas W., Baneux P., Boot R., Decelle T., Deeny A.A., Fumanelli M., et al. Recommendations for the health monitoring of rodent and rabbit colonies in breeding and experimental units. Lab Anim 2002, 36:20-42.
17. Rogers D.C., Fisher E.M., Brown S.D., Peters J., Hunter A.J., Martin J.E. Behavioral and functional analysis of mouse phenotype: SHIRPA, a proposed protocol for comprehensive phenotype assessment. Mamm Genome 1997, 8:711-713.
18. Crawley J.N. Behavioral phenotyping of transgenic and knockout mice: experimental design and evaluation of general health, sensory functions, motor abilities, and specific behavioral tests. Brain Res 1999, 835:18-26.
19. Lewis J., McGowan E., Rockwood J., Melrose H., Nacharaju P., Van Slegtenhorst M., et al. Neurofibrillary tangles, amyotrophy and progressive motor disturbance in mice expressing mutant (P301L) tau protein. Nat Genet 2000, 25:402-405.
20. Mayford M., Bach M.E., Huang Y.Y., Wang L., Hawkins R.D., Kandel E.R. Control of memory formation through regulated expression of a CaMKII transgene. Science 1996, 274:1678-1683.
21. Bach M.E., Barad M., Son H., Zhuo M., Lu Y.F., Shih R., et al. Age-related defects in spatial memory are correlated with defects in the late phase of hippocampal long-term potentiation in vitro and are attenuated by drugs that enhance the cAMP signaling pathway. Proc Natl Acad Sci USA 1999, 96:5280-5285.
22. von Bohlen und Halbach O., Zacher C., Gass P., Unsicker K. Age-related alterations in hippocampal spines and deficiencies in spatial memory in mice. J Neurosci Res 2006, 83:525-531.
23. Rustay N.R., Wahlsten D., Crabbe J.C. Influence of task parameters on rotarod performance and sensitivity to ethanol in mice. Behav Brain Res 2003, 141:237-249.
24. Hikosaka O., Nakamura K., Sakai K., Nakahara H. Central mechanisms of motor skill learning. Curr Opin Neurobiol 2002, 12:217-222.
25. Goddyn H., Leo S., Meert T., D'Hooge R. Differences in behavioural test battery performance between mice with hippocampal and cerebellar lesions. Behav Brain Res 2006, 173:138-147.
26. Costa R.M., Cohen D., Nicolelis M.A. Differential corticostriatal plasticity during fast and slow motor skill learning in mice. Curr Biol 2004, 14:1124-1134.
27. Fetsko L.A., Xu R., Wang Y. Effects of age and dopamine D2L receptor-deficiency on motor and learning functions. Neurobiol Aging 2005, 26:521-530.
28. Serradj N., Jamon M. Age-related changes in the motricity of the inbred mice strains 129/sv and C57BL/6j. Behav Brain Res 2007, 177:80-89.
29. Nicolle M.M., Prescott S., Bizon J.L. Emergence of a cue strategy preference on the water maze task in aged C57B6×SJL F1 hybrid mice. Learn Mem 2003, 10:520-524.
30. Costa R.M., Honjo T., Silva A.J. Learning and memory deficits in Notch mutant mice. Curr Biol 2003, 13:1348-1354.
31. Gordon J.A., Cioffi D., Silva A.J., Stryker M.P. Deficient plasticity in the primary visual cortex of alpha-calcium/calmodulin-dependent protein kinase II mutant mice. Neuron 1996, 17:491-499.
32. Walsh D.M., Selkoe D.J. Deciphering the molecular basis of memory failure in Alzheimer's disease. Neuron 2004, 44:181-193.
33. Emre M. Dementia associated with Parkinson's disease. Lancet Neurol 2003, 2:229-237.
34. Ashe K.H. Learning and memory in transgenic mice modeling Alzheimer's disease. Learn Mem 2001, 8:301-308.
35. Fleming S.M., Chesselet M.F. Behavioral phenotypes and pharmacology in genetic mouse models of parkinsonism. Behav Pharmacol 2006, 17:383-391.
36. Freichel C., Neumann M., Ballard T., Muller V., Woolley M., Ozmen L., et al. Age-dependent cognitive decline and amygdala pathology in alpha-synuclein transgenic mice. Neurobiol Aging 2007, 28:1421-1435.
37. Keller J.N., Hanni K.B., Markesbery W.R. Impaired proteasome function in Alzheimer's disease. J Neurochem 2000, 75:436-439.
38. Lopez Salon M., Morelli L., Castano E.M., Soto E.F., Pasquini J.M. Defective ubiquitination of cerebral proteins in Alzheimer's disease. J Neurosci Res 2000, 62:302-310.
39. McNaught K.S., Jenner P. Proteasomal function is impaired in substantia nigra in Parkinson's disease. Neurosci Lett 2001, 297:191-194.
40. Garbis S., Lubec G., Fountoulakis M. Limitations of current proteomics technologies. J Chromatogr A 2005, 1077:1-18.
41. Pfeiffer B.E., Huber K.M. Current advances in local protein synthesis and synaptic plasticity. J Neurosci 2006, 26:7147-7150.
42. Fonseca R., Vabulas R.M., Hartl F.U., Bonhoeffer T., Nagerl U.V. A balance of protein synthesis and proteasome-dependent degradation determines the maintenance of LTP. Neuron 2006, 52:239-245.
43. Ding Q., Dimayuga E., Markesbery W.R., Keller J.N. Proteasome inhibition induces reversible impairments in protein synthesis. FASEB J 2006, 20:1055-1063.