Caspase-3 triggers early synaptic dysfunction in a mouse model of Alzheimer's disease

Nature Neuroscience

Volumn 14, Issue 1, 2011, Pages 69-79

  D'Amelio, Marcello ^a,b   Cavallucci, Virve ^a   Middei, Silvia ^c   Marchetti, Cristina ^d   Pacioni, Simone ^d   Ferri, Alberto ^c   Diamantini, Adamo ^a   De Zio, Daniela ^e   Carrara, Paolo ^f   Battistini, Luca ^a   Moreno, Sandra ^f   Bacci, Alberto ^d   Ammassari Teule, Martine ^c   Marie, Hélène ^d,g   Cecconi, Francesco ^a,e  

^a IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^b UNIVERSITY CAMPUS BIO MEDICO   (Italy)

^c CNR   (Italy)

^d EUROPEAN BRAIN RESEARCH INSTITUTE   (Italy)

^e UNIVERSITY OF ROME TOR VERGATA   (Italy)

^f ROMA TRE UNIVERSITY   (Italy)

^g INSTITUT DE PHARMACOLOGIE MOLÉCULAIRE ET CELLULAIRE   (France)

Author keywords

[No Author keywords available]

Indexed keywords

AMPA RECEPTOR; AMYLOID PRECURSOR PROTEIN; CALCINEURIN; CASPASE 3; GLUTAMATE RECEPTOR 1;

ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONDITIONING; CONTROLLED STUDY; DENDRITIC SPINE; ENZYME ACTIVATION; ENZYME ACTIVITY; ENZYME INHIBITION; FEAR; FEMALE; HIPPOCAMPUS; LONG TERM DEPRESSION; MALE; MEMORY DISORDER; MOUSE; NERVE CELL PLASTICITY; NONHUMAN; PHENOTYPE; POSTSYNAPTIC DENSITY; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; PROTEIN DEPHOSPHORYLATION; PYRAMIDAL NERVE CELL; SYNAPTIC TRANSMISSION; WILD TYPE;

ALZHEIMER DISEASE; ANIMALS; CALCINEURIN; CASPASE 3; DENDRITIC SPINES; DIPEPTIDES; DISEASE MODELS, ANIMAL; GENE EXPRESSION REGULATION; HIPPOCAMPUS; LONG-TERM SYNAPTIC DEPRESSION; MEMORY DISORDERS; MICE; MICE, TRANSGENIC; NERVE DEGENERATION; OLIGOPEPTIDES; POLYGLUTAMIC ACID; RECEPTORS, AMPA; SYNAPTIC TRANSMISSION;

EID: 78650659370     PISSN: 10976256     EISSN: None     Source Type: Journal    
DOI: 10.1038/nn.2709     Document Type: Article

References (50)

1. Arendt, T. Synaptic degeneration in Alzheimer′s disease. Acta Neuropathol. 118, 167-179 (2009).
2. Morrison, J.H. & Hof, P.R. Life and death of neurons in the aging brain. Science 278, 412-419 (1997).
3. Bookheimer, S.Y. et al. Patterns of brain activation in people at risk for Alzheimer′s disease. N. Engl. J. Med. 343, 450-456 (2000).
4. Elias, M.F. et al. The preclinical phase of Alzheimer disease: a 22-year prospective study of the Framingham cohort. Arch. Neurol. 57, 808-813 (2000).
5. Zhou, Y. et al. Abnormal connectivity in the posterior cingulate and hippocampus in early Alzheimer's disease and mild cognitive impairment. Alzheimers Dement. 4, 265-270 (2008).
6. Scheff, S.W., Price, D.A., Schmitt, F.A., DeKosky, S.T. & Mufson, E.J. Synaptic alterations in CA1 in mild Alzheimer disease and mild cognitive impairment. Neurology 68, 1501-1508 (2007).
7. Bourne, J.N. & Harris, K.M. Balancing structure and function at hippocampal dendritic spines. Annu. Rev. Neurosci. 31, 47-67 (2008).
8. Ferrer, I., Guionnet, N., Cruz-Sánchez, F. & Tuñón, T. Neuronal alterations in patients with dementia: a Golgi study on biopsy samples. Neurosci. Lett. 114, 11-16 (1990).
9. Lanz, T.A., Carter, D.B. & Merchant, K.M. Dendritic spine loss in the hippocampus of young PDAPP and Tg2576 mice and its prevention by the ApoE2 genotype. Neurobiol. Dis. 13, 246-253 (2003).
10. Mattson, M.P., Keller, J.N. & Begley, J.G. Evidence for synaptic apoptosis. Exp. Neurol. 153, 35-48 (1998).
11. Hsiao, K. et al. Correlative memory defcits, Abeta elevation, and amyloid plaques in transgenic mice. Science 274, 99-102 (1996).
12. Jacobsen, J.S. et al. Early-onset behavioral and synaptic defcits in a mouse model of Alzheimer′s disease. Proc. Natl. Acad. Sci. USA 103, 5161-5166 (2006).
13. Kawarabayashi, T. et al. Age-dependent changes in brain, CSF, and plasma amyloid (beta) protein in the Tg2576 transgenic mouse model of Alzheimer′s disease. J. Neurosci. 21, 372-381 (2001).
14. Irizarry, M.C., McNamara, M., Fedorchak, K., Hsiao, K. & Hyman, B.T. APPSw transgenic mice develop age-related A beta deposits and neuropil abnormalities, but no neuronal loss in CA1. J. Neuropathol. Exp. Neurol. 56, 965-973 (1997).
15. Westerman, M.A. et al. The relationship between Abeta and memory in the Tg2576 mouse model of Alzheimer′s disease. J. Neurosci. 22, 1858-1867 (2002).
16. Janus, C. et al. A beta peptide immunization reduces behavioural impairment and plaques in a model of Alzheimer′s disease. Nature 408, 979-982 (2000).
17. Chen, G. et al. A learning defcit related to age and beta-amyloid plaques in a mouse model of Alzheimer′s disease. Nature 408, 975-979 (2000).
18. Phillips, R.G. & LeDoux, J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behav. Neurosci. 106, 274-285 (1992).
19. Lee, I. & Kesner, R.P. Differential contributions of dorsal hippocampal subregions to memory acquisition and retrieval in contextual fear-conditioning. Hippocampus 14, 301-310 (2004).
20. Lajtha, A., Perez-Polo, J.R. & Rossner, S. Handbook of Neurochemistry and Molecular Neurobiology (Springer, New York, 2008).
21. Li, S. et al. Soluble oligomers of amyloid Beta protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron 62, 788-801 (2009).
22. Almeida, C.G. et al. Beta-amyloid accumulation in APP mutant neurons reduces PSD-95 and GluR1 in synapses. Neurobiol. Dis. 20, 187-198 (2005).
23. Malinow, R. & Malenka, R.C. AMPA receptor traffcking and synaptic plasticity. Annu. Rev. Neurosci. 25, 103-126 (2002).
24. Chapman, P. F. et al. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat. Neurosci. 2, 271-276 (1999).
25. Lee, H.K., Kameyama, K., Huganir, R.L. & Bear, M.F. NMDA induces long-term synaptic depression and dephosphorylation of the GluR1 subunit of AMPA receptors in hippocampus. Neuron 21, 1151-1162 (1998).
26. van Engeland, M., Nieland, L.J., Ramaekers, F.C., Schutte, B. & Reutelingsperger, C.P. Annexin V-affnity assay: a review on an apoptosis detection system based on phosphatidylserine exposure. Cytometry 31, 1-9 (1998).
27. Green, D.R. & Kroemer, G. The pathophysiology of mitochondrial cell death. Science 305, 626-629 (2004).
28. Schulze-Osthoff, K., Ferrari, D., Los, M., Wesselborg, S. & Peter, M.E. Apoptosis signaling by death receptors. Eur. J. Biochem. 254, 439-459 (1998).
29. Hsieh, H. et al. AMPAR removal underlies Abeta-induced synaptic depression and dendritic spine loss. Neuron 52, 831-843 (2006).
30. Mukerjee, N., McGinnis, K.M., Park, Y.H., Gnegy, M.E. & Wang, K.K. Caspase-mediated proteolytic activation of calcineurin in thapsigargin-mediated apoptosis in SH-SY5Y neuroblastoma cells. Arch. Biochem. Biophys. 379, 337-343 (2000).
31. Vicent, M.J. & Pérez-Payá, E. Poly-L-glutamic acid (PGA) aided inhibitors of apoptotic protease activating factor 1 (Apaf-1): an antiapoptotic polymeric nanomedicine. J. Med. Chem. 49, 3763-3765 (2006).
32. Santamaría, B. et al. A nanoconjugate Apaf-1 inhibitor protects mesothelial cells from cytokine-induced injury. PLoS ONE 4, e6634 (2009).
33. Salvesen, G.S. & Dixit, V.M. Caspases: intracellular signaling by proteolysis. Cell 91, 443-446 (1997).
34. Bravarenko, N.I. et al. Caspase-like activity is essential for long-term synaptic plasticity in the terrestrial snail Helix. Eur. J. Neurosci. 23, 129-140 (2006).
35. Huesmann, G.R. & Clayton, D.F. Dynamic role of postsynaptic caspase-3 and BIRC4 in zebra fnch song-response habituation. Neuron 52, 1061-1072 (2006).
36. Li, Z. et al. Caspase-3 activation via mitochondria is required for long-term depression and AMPA receptor internalization. Cell 141, 859-871 (2010).
37. Marín, N. et al. Beta-amyloid-induced activation of caspase-3 in primary cultures of rat neurons. Mech. Ageing Dev. 119, 63-67 (2000).
38. Gervais, F.G. et al. Involvement of caspases in proteolytic cleavage of Alzheimer's amyloid-beta precursor protein and amyloidogenic A beta peptide formation. Cell 97, 395-406 (1999).
39. Stadelmann, C. et al. Activation of caspase-3 in single neurons and autophagic granules of granulovacuolar degeneration in Alzheimer's disease. Evidence for apoptotic cell death. Am. J. Pathol. 155, 1459-1466 (1999).
40. Louneva, N. et al. Caspase-3 is enriched in postsynaptic densities and increased in Alzheimer′s disease. Am. J. Pathol. 173, 1488-1495 (2008).
41. Kuida, K. et al. Decreased apoptosis in the brain and premature lethality in CPP32-defcient mice. Nature 384, 368-372 (1996).
42. Hakem, R. et al. Differential requirement for caspase 9 in apoptotic pathways in vivo. Cell 94, 339-352 (1998).
43. Kuida, K. et al. Reduced apoptosis and cytochrome c-mediated caspase activation in mice lacking caspase 9. Cell 94, 325-337 (1998).
44. Cecconi, F., Alvarez-Bolado, G., Meyer, B.I., Roth, K.A. & Gruss, P. Apaf1 (CED-4 homolog) regulates programmed cell death in mammalian development. Cell 94, 727-737 (1998).
45. Takahashi, R.H. et al. Oligomerization of Alzheimer's beta-amyloid within processes and synapses of cultured neurons and brain. J. Neurosci. 24, 3592-3599 (2004).
46. Manczak, M. et al. Mitochondria are a direct site of A beta accumulation in Alzheimer's disease neurons: implications for free radical generation and oxidative damage in disease progression. Hum. Mol. Genet. 15, 1437-1449 (2006).
47. Cho, D.H. et al. S-nytrosylation of Drp1 mediates beta-amyloid-related mitochondrial fssion and neuronal injury. Science 324, 102-105 (2009).
48. Marie, H., Morishita, W., Yu, X., Calakos, N. & Malenka, R.C. Generation of silent synapses by acute in vivo expression of CaMKIV and CREB. Neuron 45, 741-752 (2005).
49. Gylys, K.H., Fein, J.A., Wiley, D.J. & Cole, G.M. Rapid annexin-V labeling in synaptosomes. Neurochem. Int. 44, 125-131 (2004).
50. Ferri, A. et al. Calcineurin activity is regulated both by redox compounds and by mutant familial amyotrophic lateral sclerosis-superoxide dismutase. J. Neurochem. 75, 606-613 (2000).