Region- and age-dependent reductions of hippocampal long-term potentiation and NMDA to AMPA ratio in a genetic model of Alzheimer's disease

Neurobiology of Aging

Volumn 36, Issue 1, 2015, Pages 123-133

  Tozzi, Alessandro ^a,b   Sclip, Alessandra ^c   Tantucci, Michela ^a   de Iure, Antonio ^a   Ghiglieri, Veronica ^b   Costa, Cinzia ^a   Di Filippo, Massimiliano ^a   Borsello, Tiziana ^c   Calabresi, Paolo ^a,b  

^a UNIVERSITY OF PERUGIA   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c MARIO NEGRI INSTITUTE FOR PHARMACOLOGICAL RESEARCH   (Italy)

Author keywords

Beta amyloid; CA1; Dentate gyrus; Long term potentiation

Indexed keywords

ALPHA AMINO 3 HYDROXY 5 METHYL 4 ISOXAZOLEPROPIONIC ACID; AMYLOID BETA PROTEIN; AMYLOID BETA PROTEIN[1-42]; MEMANTINE; N METHYL DEXTRO ASPARTIC ACID; NEOSTIGMINE; AMYLOID PRECURSOR PROTEIN; CHOLINESTERASE INHIBITOR; N METHYLASPARTIC ACID;

AGE; ALZHEIMER DISEASE; AMYLOID PLAQUE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; BRAIN REGION; CONTROLLED STUDY; DENTATE GYRUS; DRUG EFFECT; DRUG SELECTIVITY; GENETIC MODEL; HIPPOCAMPAL CA1 REGION; HIPPOCAMPUS; LONG TERM POTENTIATION; MOUSE; NONHUMAN; AGING; ANIMAL; DISEASE MODEL; DRUG EFFECTS; GENETICS; METABOLISM; MOLECULARLY TARGETED THERAPY; MUTATION; PATHOPHYSIOLOGY; PHYSIOLOGY; TRANSGENIC MOUSE;

AGING; ALPHA-AMINO-3-HYDROXY-5-METHYL-4-ISOXAZOLEPROPIONIC ACID; ALZHEIMER DISEASE; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; CHOLINESTERASE INHIBITORS; DISEASE MODELS, ANIMAL; HIPPOCAMPUS; LONG-TERM POTENTIATION; MICE, TRANSGENIC; MOLECULAR TARGETED THERAPY; MUTATION; N-METHYLASPARTATE; NEOSTIGMINE; PLAQUE, AMYLOID;

EID: 84920573581     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2014.07.002     Document Type: Article

References (44)

1. Acsady L., Kali S. Models, structure, function: the transformation of cortical signals in the dentate gyrus. Prog. Brain Res. 2007, 163:577-599.
2. Arima-Yoshida F., Watabe A.M., Manabe T. The mechanisms of the strong inhibitory modulation of long-term potentiation in the rat dentate gyrus. Eur. J. Neurosci. 2011, 33:1637-1646.
3. Bagetta V., Sgobio C., Pendolino V., Del Papa G., Tozzi A., Ghiglieri V., Giampa C., Zianni E., Gardoni F., Calabresi P., Picconi B. Rebalance of striatal NMDA/AMPA receptor ratio underlies the reduced emergence of dyskinesia during D2-like dopamine agonist treatment in experimental Parkinson's disease. J.Neurosci. 2012, 32:17921-17931.
4. Bakker A., Kirwan C.B., Miller M., Stark C.E. Pattern separation in the human hippocampal CA3 and dentate gyrus. Science 2008, 319:1640-1642.
5. Bellucci A., Luccarini I., Scali C., Prosperi C., Giovannini M.G., Pepeu G., Casamenti F. Cholinergic dysfunction, neuronal damage and axonal loss in TgCRND8 mice. Neurobiol. Dis. 2006, 23:260-272.
6. Blennow K., de Leon M.J., Zetterberg H. Alzheimer's disease. Lancet Neurol. 2006, 368:387-403.
7. Bobinski M., de Leon M.J., Tarnawski M., Wegiel J., Reisberg B., Miller D.C., Wisniewski H.M. Neuronal and volume loss in CA1 of the hippocampal formation uniquely predicts duration and severity of Alzheimer disease. Brain Res. 1998, 805:267-269.
8. Calabresi P., Castrioto A., Di Filippo M., Picconi B. New experimental and clinical links between the hippocampus and the dopaminergic system in Parkinson's disease. Lancet Neurol. 2013, 12:811-821.
9. Chapman P.F., White G.L., Jones M.W., Cooper-Blacketer D., Marshall V.J., Irizarry M., Younkin L., Good M.A., Bliss T.V., Hyman B.T., Younkin S.G., Hsiao K.K. Impaired synaptic plasticity and learning in aged amyloid precursor protein transgenic mice. Nat. Neurosci. 1999, 2:271-276.
10. Chishti M.A., Yang D.S., Janus C., Phinney A.L., Horne P., Pearson J., Strome R., Zuker N., Loukides J., French J., Turner S., Lozza G., Grilli M., Kunicki S., Morissette C., Paquette J., Gervais F., Bergeron C., Fraser P.E., Carlson G.A., George-Hyslop P.S., Westaway D. Early-onset amyloid deposition and cognitive deficits in transgenic mice expressing a double mutant form of amyloid precursor protein 695. J.Biol. Chem. 2001, 276:21562-21570.
11. 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 M.G., Latagliata E.C., 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.
12. Danysz W., Parsons C.G. The NMDA receptor antagonist memantine as a symptomatological and neuroprotective treatment for Alzheimer's disease: preclinical evidence. Int. J. Geriatr. Psychiatry 2003, 18:S23-S32.
13. Doralp S., Leung L.S. Cholinergic modulation of hippocampal CA1 basal-dendritic long-term potentiation. Neurobiol. Learn Mem. 2008, 90:382-388.
14. Duyckaerts C., Potier M.C., Delatour B. Alzheimer disease models and human neuropathology: similarities and differences. Acta Neuropathol. 2008, 115:5-38.
15. Easton A., Douchamps V., Eacott M., Lever C. Aspecific role for septohippocampal acetylcholine in memory?. Neuropsychologia 2012, 50:3156-3168.
16. Findlay D.J., Connelly P.J. Memantine (Ebixa) in the later stages of dementia. Hosp. Med. 2003, 64:654-657.
17. Fitzjohn S.M., Morton R.A., Kuenzi F., Rosahl T.W., Shearman M., Lewis H., Smith D., Reynolds D.S., Davies C.H., Collingridge G.L., Seabrook G.R. Age-related impairment of synaptic transmission but normal long-term potentiation in transgenic mice that overexpress the human APP695SWE mutant form of amyloid precursor protein. J.Neurosci. 2001, 21:4691-4698.
18. Francis B.M., Kim J., Barakat M.E., Fraenkl S., Yucel Y.H., Peng S., Michalski B., Fahnestock M., McLaurin J., Mount H.T. Object recognition memory and BDNF expression are reduced in young TgCRND8 mice. Neurobiol. Aging 2012, 33:555-563.
19. Hasselmo M.E. What is the function of hippocampal theta rhythm?-Linking behavioral data to phasic properties of field potential and unit recording data. Hippocampus 2005, 15:936-949.
20. Hernandez C.M., Dineley K.T. alpha7 nicotinic acetylcholine receptors in Alzheimer's disease: neuroprotective, neurotrophic or both?. Curr. Drug Targets 2012, 13:613-622.
21. Hunsaker M.R., Kesner R.P. Dissociations across the dorsal-ventral axis of CA3 and CA1 for encoding and retrieval of contextual and auditory-cued fear. Neurobiol. Learn Mem. 2008, 89:61-69.
22. Jacobsen J.S., Wu C.C., Redwine J.M., Comery T.A., Arias R., Bowlby M., Martone R., Morrison J.H., Pangalos M.N., Reinhart P.H., Bloom F.E. Early-onset behavioral and synaptic deficits in a mouse model of Alzheimer's disease. Proc. Natl. Acad. Sci. U.S.A 2006, 103:5161-5166.
23. Kamenetz F., Tomita T., Hsieh H., Seabrook G., Borchelt D., Iwatsubo T., Sisodia S., Malinow R. APP processing and synaptic function. Neuron 2003, 37:925-937.
24. Kesner R.P., Hunsaker M.R. The temporal attributes of episodic memory. Behav. Brain Res. 2010, 215:299-309.
25. Kleschevnikov A.M., Belichenko P.V., Villar A.J., Epstein C.J., Malenka R.C., Mobley W.C. Hippocampal long-term potentiation suppressed by increased inhibition in the Ts65Dn mouse, a genetic model of Down syndrome. J.Neurosci. 2004, 24:8153-8160.
26. Klyubin I., Wang Q., Reed M.N., Irving E.A., Upton N., Hofmeister J., Cleary J.P., Anwyl R., Rowan M.J. Protection against Abeta-mediated rapid disruption of synaptic plasticity and memory by memantine. Neurobiol. Aging 2011, 32:614-623.
27. LaFerla F.M., Oddo S. Alzheimer's disease: abeta, tau and synaptic dysfunction. Trends Mol. Med. 2005, 11:170-176.
28. Luo L., Chen W.H., Wang M., Zhu D.M., She J.Q., Ruan D.Y. Modulation of long-term potentiation by individual subtypes of muscarinic acetylcholine receptor in the rat dentate gyrus. Hippocampus 2008, 18:989-995.
29. Luscher C., Malenka R.C. NMDA receptor-dependent long-term potentiation and long-term depression (LTP/LTD). Cold Spring Harb Perspect. Biol. 2012, 4.
30. Matsuyama S., Matsumoto A., Enomoto T., Nishizaki T. Activation of nicotinic acetylcholine receptors induces long-term potentiation invivo in the intact mouse dentate gyrus. Eur. J. Neurosci. 2000, 12:3741-3747.
31. McGleenon B.M., Dynan K.B., Passmore A.P. Acetylcholinesterase inhibitors in Alzheimer's disease. Br. J. Clin. Pharmacol. 1999, 48:471-480.
32. Nakauchi S., Sumikawa K. Endogenously released ACh and exogenous nicotine differentially facilitate long-term potentiation induction in the hippocampal CA1 region of mice. Eur. J. Neurosci. 2012, 35:1381-1395.
33. Ovsepian S.V., Anwyl R., Rowan M.J. Endogenous acetylcholine lowers the threshold for long-term potentiation induction in the CA1 area through muscarinic receptor activation: invivo study. Eur. J. Neurosci. 2004, 20:1267-1275.
34. Palop J.J., Chin J., Roberson E.D., Wang J., Thwin M.T., Bien-Ly N., Yoo J., Ho K.O., Yu G.Q., Kreitzer A., Finkbeiner S., Noebels J.L., Mucke L. Aberrant excitatory neuronal activity and compensatory remodeling of inhibitory hippocampal circuits in mouse models of Alzheimer's disease. Neuron 2007, 55:697-711.
35. Parsons C.G., Stoffler A., Danysz W. Memantine: a NMDA receptor antagonist that improves memory by restoration of homeostasis in the glutamatergic system-too little activation is bad, too much is even worse. Neuropharmacology 2007, 53:699-723.
36. Rammes G., Hasenjager A., Sroka-Saidi K., Deussing J.M., Parsons C.G. Therapeutic significance of NR2B-containing NMDA receptors and mGluR5 metabotropic glutamate receptors in mediating the synaptotoxic effects of beta-amyloid oligomers on long-term potentiation (LTP) in murine hippocampal slices. Neuropharmacology 2011, 60:982-990.
37. Reisberg B., Doody R., Stoffler A., Schmitt F., Ferris S., Mobius H.J. Memantine in moderate-to-severe Alzheimer's disease. N.Engl. J. Med. 2003, 348:1333-1341.
38. Rossler M., Zarski R., Bohl J., Ohm T.G. Stage-dependent and sector-specific neuronal loss in hippocampus during Alzheimer's disease. Acta Neuropathol. 2002, 103:363-369.
39. Sclip A., Antoniou X., Colombo A., Camici G.G., Pozzi L., Cardinetti D., Feligioni M., Veglianese P., Bahlmann F.H., Cervo L., Balducci C., Costa C., Tozzi A., Calabresi P., Forloni G., Borsello T. c-Jun N-terminal kinase regulates soluble Abeta oligomers and cognitive impairment in AD mouse model. J.Biol. Chem. 2011, 286:43871-43880.
40. Selkoe D.J. Resolving controversies on the path to Alzheimer's therapeutics. Nat. Med. 2011, 17:1060-1065.
41. Styren S.D., Hamilton R.L., Styren G.C., Klunk W.E. X-34, a fluorescent derivative of Congo red: a novel histochemical stain for Alzheimer's disease pathology. J.Histochem. Cytochem. 2000, 48:1223-1232.
42. Suthana N.A., Ekstrom A.D., Moshirvaziri S., Knowlton B., Bookheimer S.Y. Human hippocampal CA1 involvement during allocentric encoding of spatial information. J.Neurosci. 2009, 29:10512-10519.
43. Tanzi R.E., Bertram L. Twenty years of the Alzheimer's disease amyloid hypothesis: a genetic perspective. Cell 2005, 120:545-555.
44. Tronci E., Fidalgo C., Zianni E., Collu M., Stancampiano R., Morelli M., Gardoni F., Carta M. Effect of memantine on L-DOPA-induced dyskinesia in the 6-OHDA-lesioned rat model of Parkinson's disease. Neuroscience 2014, 265:245-252.