Blocking ADAM10 synaptic trafficking generates a model of sporadic Alzheimer's disease

Brain

Volumn 133, Issue 11, 2010, Pages 3323-3335

  Epis, Roberta ^a   Marcello, Elena ^a   Gardoni, Fabrizio ^a   Vastagh, Csaba ^a   Malinverno, Matteo ^a   Balducci, Claudia ^b   Colombo, Alessio ^b   Borroni, Barbara ^c   Vara, Hugo ^d,e   Dell'Agli, Mario ^a   Cattabeni, Flamino ^a   Giustetto, Maurizio ^d   Borsello, Tiziana ^b   Forloni, Gianluigi ^b   Padovani, Alessandro ^c   Di Luca, Monica ^a  

^a UNIVERSITY OF MILAN   (Italy)

^b MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

^c UNIVERSITY OF BRESCIA   (Italy)

^d UNIVERSITY OF TURIN   (Italy)

^e MIGUEL HERNÁNDEZ UNIVERSITY   (Spain)

Author keywords

amyloid precursor protein metabolism; animal models; NMDA; SAP97; synaptopathy

Indexed keywords

ADAM10 ENDOPEPTIDASE; ALPHA SECRETASE; AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; DISINTEGRIN; GUANYLATE KINASE; MEMBRANE PROTEIN; METALLOPROTEINASE; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; PEPTIDE; TAU PROTEIN;

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; CELL MEMBRANE PERMEABILITY; CLINICAL ARTICLE; CONTROLLED STUDY; DISEASE COURSE; ELECTROPHYSIOLOGY; HUMAN; MALE; METABOLISM; MOUSE; NEUROPATHOLOGY; NONHUMAN; POSTSYNAPTIC POTENTIAL; PRIORITY JOURNAL; PROTEIN AGGREGATION; PROTEIN DOMAIN; PROTEIN PHOSPHORYLATION; SYNAPSE;

ADAM PROTEINS; ADAPTOR PROTEINS, SIGNAL TRANSDUCING; ALZHEIMER DISEASE; AMINO ACID SEQUENCE; AMYLOID PRECURSOR PROTEIN SECRETASES; ANIMALS; DISEASE MODELS, ANIMAL; GUANYLATE KINASE; MALE; MEMBRANE PROTEINS; MICE; MICE, INBRED C57BL; MOLECULAR SEQUENCE DATA; MULTIPROTEIN COMPLEXES; NERVE TISSUE PROTEINS; NEURAL INHIBITION; PROTEIN TRANSPORT; SYNAPSES; TIME FACTORS;

EID: 78049476184     PISSN: 00068950     EISSN: 14602156     Source Type: Journal    
DOI: 10.1093/brain/awq217     Document Type: Article

References (52)

1. Aarts M, Liu Y, Liu L, Besshoh S, Arundine M, Gurd JW, et al. Treatment of ischemic brain damage by perturbing NMDA receptor-PSD-95 protein interactions. Science 2002; 298: 846-50.
2. Alvarez VA, Sabatini BL. Anatomical and physiological plasticity of dendritic spines. Annu Rev Neurosci 2007; 30: 79-97.
3. Billings LM, Oddo S, Green KN, McGaugh JL, LaFerla FM. Intraneuronal Abeta causes the onset of early Alzheimer's disease-related cognitive deficits in transgenic mice. Neuron 2005; 45: 675-88.
4. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991; 82: 239-59.
5. Cleary JP, Walsh DM, Hofmeister JJ, Shankar GM, Kuskowski MA, Selkoe DJ, et al. Natural oligomers of the amyloid-beta protein specifically disrupt cognitive function. Nat Neurosci 2005; 8: 79-84.
6. Colledge M, Dean RA, Scott GK, Langeberg LK, Huganir RL, Scott JD. Targeting of PKA to glutamate receptors through a MAGUK-AKAP complex. Neuron 2000; 27: 107-19.
7. De Strooper B, Saftig P, Craessaerts K, Vanderstichele H, Guhde G, Annaert W, et al. Deficiency of presenilin-1 inhibits the normal cleavage of amyloid precursor protein. Nature 1998; 391: 387-90.
8. DeKosky ST, Scheff SW. Synapse loss in frontal cortex biopsies in Alzheimer's disease: correlation with cognitive severity. Ann Neurol 1990; 27: 457-64.
9. Epis R, Gardoni F, Marcello E, Genazzani A, Canonico PL, Di Luca M. Searching for new animal models of Alzheimer's disease. Eur J Pharmacol 2010; 626: 57-63.
10. Gamblin TC, Chen F, Zambrano A, Abraha A, Lagalwar S, Guillozet AL, et al. Caspase cleavage of tau: linking amyloid and neurofibrillary tangles in Alzheimer's disease. Proc Natl Acad Sci USA 2003; 100: 10032-7.
11. Gan WB, Grutzendler J, Wong WT, Wong RO, Lichtman JW. Multicolor "DiOlistic" labeling of the nervous system using lipophilic dye combinations. Neuron 2000; 27: 219-25.
12. Gardoni F, Bellone C, Cattabeni F, Di Luca M. Protein kinase C activation modulates alpha-calmodulin kinase II binding to NR2A subunit of N-methyl-D-aspartate receptor complex. J Biol Chem 2001; 276: 7609-13.
13. Gardoni F, Mauceri D, Fiorentini C, Bellone C, Missale C, Cattabeni F, et al. CaMKII-dependent phosphorylation regulates SAP97/NR2A interaction. J Biol Chem 2003; 278: 44745-52.
14. Gerlai R. Gene-targeting studies of mammalian behavior: is it the mutation or the background genotype? Trends Neurosci 1996; 19: 177-81.
15. Goate A, Chartier-Harlin MC, Mullan M, Brown J, Crawford F, Fidani L, et al. Segregation of a missense mutation in the amyloid precursor protein gene with familial Alzheimer's disease. Nature 1991; 349: 704-6.
16. Hardy JA, Higgins GA. Alzheimer's disease: the amyloid cascade hypothesis. Science 1992; 256: 184-5.
17. Hauptmann S, Scherping I, Drose S, Brandt U, Schulz KL, Jendrach M, et al. Mitochondrial dysfunction: an early event in Alzheimer pathology accumulates with age in AD transgenic mice. Neurobiol Aging 2009; 30: 1574-86.
18. Holcomb L, Gordon MN, McGowan E, Yu X, Benkovic S, Jantzen P, et al. Accelerated Alzheimer-type phenotype in transgenic mice carrying both mutant amyloid precursor protein and presenilin 1 transgenes. Nat Med 1998; 4: 97-100.
19. Jacobsen JS, Wu CC, Redwine JM, Comery TA, Arias R, Bowlby M, et al. Early-onset behavioral and synaptic deficits in a mouse model of Alzheimer's disease. Proc Natl Acad Sci USA 2006; 103: 5161-6.
20. Kim M, Suh J, Romano D, Truong MH, Mullin K, Hooli B, et al. Potential late-onset Alzheimer's disease-associated mutations in the ADAM10 gene attenuate {alpha}-secretase activity. Hum Mol Genet 2009; 18: 3987-96.
21. Klein WL, Krafft GA, Finch CE. Targeting small Abeta oligomers: the solution to an Alzheimer's disease conundrum? Trends Neurosci 2001; 24: 219-24.
22. Knobloch M, Konietzko U, Krebs DC, Nitsch RM. Intracellular Abeta and cognitive deficits precede beta-amyloid deposition in transgenic arcAbeta mice. Neurobiol Aging 2007; 28: 1297-306.
23. Lacor PN, Buniel MC, Chang L, Fernandez SJ, Gong Y, Viola KL, et al. Synaptic targeting by Alzheimer's-related amyloid beta oligomers. J Neurosci 2004; 24: 10191-200.
24. 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.
25. Lammich S, Kojro E, Postina R, Gilbert S, Pfeiffer R, Jasionowski M, et al. Constitutive and regulated alpha-secretase cleavage of Alzheimer's amyloid precursor protein by a disintegrin metalloprotease. Proc Natl Acad Sci USA 1999; 96: 3922-7.
26. Lau CG, Zukin RS. NMDA receptor trafficking in synaptic plasticity and neuropsychiatric disorders. Nat Rev Neurosci 2007; 8: 413-26.
27. Leonard AS, Davare MA, Horne MC, Garner CC, Hell JW. SAP97 is associated with the alpha-amino-3-hydroxy-5-methylisoxazole-4-propionic acid receptor GluR1 subunit. J Biol Chem 1998; 273: 19518-24.
28. Lesne S, Koh MT, Kotilinek L, Kayed R, Glabe CG, Yang A, et al. A specific amyloid-beta protein assembly in the brain impairs memory. Nature 2006; 440: 352-7.
29. Ludwig A, Hundhausen C, Lambert MH, Broadway N, Andrews RC, Bickett DM, et al. Metalloproteinase inhibitors for the disintegrin-like metalloproteinases ADAM10 and ADAM17 that differentially block constitutive and phorbol ester-inducible shedding of cell surface molecules. Comb Chem High Throughput Screen 2005; 8: 161-71.
30. Marcello E, Gardoni F, Mauceri D, Romorini S, Jeromin A, Epis R, et al. Synapse-associated protein-97 mediates alpha-secretase ADAM10 trafficking and promotes its activity. J Neurosci 2007; 27: 1682-91.
31. Morrissette DA, Parachikova A, Green KN, LaFerla FM. Relevance of transgenic mouse models to human Alzheimer disease. J Biol Chem 2009; 284: 6033-7.
32. Nash JE, Johnston TH, Collingridge GL, Garner CC, Brotchie JM. Subcellular redistribution of the synapse-associated proteins PSD-95 and SAP97 in animal models of Parkinson's disease and L-DOPA-induced dyskinesia. FASEB J 2005; 19: 583-5.
33. Oddo S, Caccamo A, Kitazawa M, Tseng BP, LaFerla FM. Amyloid deposition precedes tangle formation in a triple transgenic model of Alzheimer's disease. Neurobiol Aging 2003a; 24: 1063-70.
34. Oddo S, Caccamo A, Shepherd JD, Murphy MP, Golde TE, Kayed R, et al. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 2003b; 39: 409-21.
35. Oddo S, Caccamo A, Tran L, Lambert MP, Glabe CG, Klein WL, et al. Temporal profile of amyloid-beta (Abeta) oligomerization in an in vivo model of Alzheimer disease. A link between Abeta and tau pathology. J Biol Chem 2006; 281: 1599-604.
36. Postina R, Schroeder A, Dewachter I, Bohl J, Schmitt U, Kojro E, et al. A disintegrin-metalloproteinase prevents amyloid plaque formation and hippocampal defects in an Alzheimer disease mouse model. J Clin Invest 2004; 113: 1456-64.
37. Reiss K, Maretzky T, Ludwig A, Tousseyn T, de Strooper B, Hartmann D, et al. ADAM10 cleavage of N-cadherin and regulation of cell-cell adhesion and beta-catenin nuclear signalling. EMBO J 2005; 24: 742-52.
38. Sans N, Racca C, Petralia RS, Wang YX, McCallum J, Wenthold RJ. Synapse-associated protein 97 selectively associates with a subset of AMPA receptors early in their biosynthetic pathway. J Neurosci 2001; 21: 7506-16.
39. Scheff SW, Price DA, Schmitt FA, DeKosky ST, Mufson EJ. Synaptic alterations in CA1 in mild Alzheimer disease and mild cognitive impairment. Neurology 2007; 68: 1501-8.
40. Scheuner D, Eckman C, Jensen M, Song X, Citron M, Suzuki N, et al. Secreted amyloid beta-protein similar to that in the senile plaques of Alzheimer's disease is increased in vivo by the presenilin 1 and 2 and APP mutations linked to familial Alzheimer's disease. Nat Med 1996; 2: 864-70.
41. Seabold GK, Burette A, Lim IA, Weinberg RJ, Hell JW. Interaction of the tyrosine kinase Pyk2 with the N-methyl-D-aspartate receptor complex via the Src homology 3 domains of PSD-95 and SAP102. J Biol Chem 2003; 278: 15040-8.
42. Selkoe DJ. Alzheimer's disease: genes, proteins, and therapy. Physiol Rev 2001; 81: 741-66.
43. Selkoe DJ. Alzheimer's disease is a synaptic failure. Science 2002; 298: 789-91.
44. Selkoe DJ. Soluble oligomers of the amyloid beta-protein impair synaptic plasticity and behavior. Behav Brain Res 2008; 192: 106-13.
45. Shankar GM, Li S, Mehta TH, Garcia-Munoz A, Shepardson NE, Smith I, et al. Amyloid-beta protein dimers isolated directly from Alzheimer's brains impair synaptic plasticity and memory. Nat Med 2008; 14: 837-42.
46. Snyder EM, Nong Y, Almeida CG, Paul S, Moran T, Choi EY, et al. Regulation of NMDA receptor trafficking by amyloid-beta. Nat Neurosci 2005; 8: 1051-8.
47. Terry RD, Masliah E, Salmon DP, Butters N, DeTeresa R, Hill R, 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.
48. Vassar R, Bennett BD, Babu-Khan S, Kahn S, Mendiaz EA, Denis P, et al. Beta-secretase cleavage of Alzheimer's amyloid precursor protein by the transmembrane aspartic protease BACE. Science 1999; 286: 735-41.
49. Venkitaramani DV, Chin J, Netzer WJ, Gouras GK, Lesne S, Malinow R, et al. Beta-amyloid modulation of synaptic transmission and plasticity. J Neurosci 2007; 27: 11832-7.
50. Wei W, Nguyen LN, Kessels HW, Hagiwara H, Sisodia S, Malinow R. Amyloid beta from axons and dendrites reduces local spine number and plasticity. Nat Neurosci 2010; 13: 190-6.
51. Zhang H, Gong B, Liu S, Fa M, Ninan I, Staniszewski A, et al. Synaptic fatigue is more pronounced in the APP/PS1 transgenic mouse model of Alzheimer's disease. Curr Alzheimer Res 2005; 2: 137-40.
52. Zucker RS, Regehr WG. Short-term synaptic plasticity. Annu Rev Physiol 2002; 64: 355-405.