Persistent increase of d-aspartate in d-aspartate oxidase mutant mice induces a precocious hippocampal age-dependent synaptic plasticity and spatial memory decay

Neurobiology of Aging

Volumn 32, Issue 11, 2011, Pages 2061-2074

  Errico, Francesco ^a   Nisticò, Robert ^b,c   Napolitano, Francesco ^a   Oliva, Alessandra Bonito ^a   Romano, Rosaria ^a   Barbieri, Federica ^d   Florio, Tullio ^d   Russo, Claudio ^d,e   Mercuri, Nicola B ^b   Usiello, Alessandro ^a,e  

^a CEINGE BIOTECNOLOGIE AVANZATE   (Italy)

^b IRCCS FONDAZIONE SANTA LUCIA   (Italy)

^c UNIVERSITY OF CALABRIA   (Italy)

^d UNIVERSITY OF GENOA   (Italy)

^e UNIVERSITY OF MOLISE   (Italy)

Author keywords

Brain aging; D Aspartate; Hippocampus; NMDA receptors; Reference memory; Synaptic plasticity

Indexed keywords

ASPARTATE OXIDASE; CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; CHLORPHENIRAMINE MALEATE PLUS PHENYLEPHRINE; DEXTRO ASPARTIC ACID; GLUTAMATE RECEPTOR; MITOGEN ACTIVATED PROTEIN KINASE 3; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR 2B; SERINE; THREONINE;

AGING; ANIMAL CELL; ANIMAL EXPERIMENT; ARTICLE; BRAIN FUNCTION; CALCIUM CURRENT; CONTROLLED STUDY; DOWN REGULATION; ENZYME ACTIVATION; ENZYME PHOSPHORYLATION; GENOTYPE; HIPPOCAMPAL CA1 REGION; HIPPOCAMPAL CA3 REGION; IMMUNOHISTOCHEMISTRY; LIFESPAN; LONG TERM POTENTIATION; MAZE TEST; MOUSE; NERVE CELL PLASTICITY; NEUROTRANSMISSION; NONHUMAN; PATCH CLAMP; PRIORITY JOURNAL; PROTEIN EXPRESSION; REFERENCE MEMORY; SPATIAL MEMORY; UPREGULATION;

AGE FACTORS; ANIMALS; CONDITIONING (PSYCHOLOGY); D-ASPARTATE OXIDASE; D-ASPARTIC ACID; FEAR; FREEZING REACTION, CATALEPTIC; HIPPOCAMPUS; MAZE LEARNING; MEMORY; MICE; MICE, KNOCKOUT; NEURONAL PLASTICITY; SYNAPSES;

EID: 80052624160     PISSN: 01974580     EISSN: 15581497     Source Type: Journal    
DOI: 10.1016/j.neurobiolaging.2009.12.007     Document Type: Article

References (47)

1. Bach M.E., Barad M., Son H., Zhuo M., Lu Y.F., Shih R., Mansuy I., Hawkins R.D., Kandel E.R. 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. Proceedings of the National Academy of Sciences of the United States of America 1999, 96(9):5280-5285.
2. Banbury Conference on genetic background in mice Mutant mice and neuroscience: recommendations concerning genetic background. Neuron 1997, 19(4):755-759.
3. Barbour B., Brew H., Attwell D. Electrogenic uptake of glutamate and aspartate into glial cells isolated from the salamander (Ambystoma) retina. The Journal of Physiology 1991, 436:169-193.
4. Barnes C.A. Long-term potentiation and the ageing brain. Philosophical Transactions of the Royal Society of London. Series B, Biological Sciences 2003, 358(1432):765-772.
5. Bevins R.A., Besheer J. Object recognition in rats and mice: a one-trial non-matching-to-sample learning task to study 'recognition memory'. Nature Protocols 2006, 1(3):1306-1311.
6. Coba M.P., Valor L.M., Kopanitsa M.V., Afinowi N.O., Grant S.G. Kinase networks integrate profiles of N-methyl-d-aspartate receptor-mediated gene expression in hippocampus. The Journal of Biological Chemistry 2008, 283(49):34101-34107.
7. D'Aniello A. d-Aspartic acid: an endogenous amino acid with an important neuroendocrine role. Brain Research Reviews 2007, 53(2):215-234.
8. D'Aniello A., D'Onofrio G., Pischetola M., D'Aniello G., Vetere A., Petrucelli L., Fisher G.H. Biological role of d-amino acid oxidase and d-aspartate oxidase. Effects of d-amino acids. The Journal of Biological Chemistry 1993, 268(36):26941-26949.
9. D'Aniello A., Di Fiore M.M., Fisher G.H., Milone A., Seleni A., D'Aniello S., Perna A.F., Ingrosso D. Occurrence of d-aspartic acid and N-methyl-d-aspartic acid in rat neuroendocrine tissues and their role in the modulation of luteinizing hormone and growth hormone release. The FASEB Journal 2000, 14(5):699-714.
10. Davis S., Laroche S. Mitogen-activated protein kinase/extracellular regulated kinase signalling and memory stabilization: a review. Genes, Brain, and Behavior 2006, 5(Suppl. 2):61-72.
11. Dewachter I., Reverse D., Caluwaerts N., Ris L., Kuiperi C., Van den Haute C., Spittaels K., Umans L., Serneels L., Thiry E., Moechars D., Mercken M., Godaux E., Van Leuven F. Neuronal deficiency of presenilin 1 inhibits amyloid plaque formation and corrects hippocampal long-term potentiation but not a cognitive defect of amyloid precursor protein [V717I] transgenic mice. The Journal of Neuroscience 2002, 22(9):3445-3453.
12. Errico F., Nistico R., Palma G., Federici M., Affuso A., Brilli E., Topo E., Centonze D., Bernardi G., Bozzi Y., D'Aniello A., Di Lauro R., Mercuri N.B., Usiello A. Increased levels of d-aspartate in the hippocampus enhance LTP but do not facilitate cognitive flexibility. Molecular and Cellular Neurosciences 2008, 37(2):236-246.
13. Errico F., Pirro M.T., Affuso A., Spinelli P., De Felice M., D'Aniello A., Di Lauro R. A physiological mechanism to regulate d-aspartic acid and NMDA levels in mammals revealed by d-aspartate oxidase deficient mice. Gene 2006, 374:50-57.
14. Errico F., Rossi S., Napolitano F., Catuogno V., Topo E., Fisone G., D'Aniello A., Centonze D., Usiello A. D-aspartate prevents corticostriatal long-term depression and attenuates schizophrenia-like symptoms induced by amphetamine and MK-801. The Journal of Neuroscience 2008, 28(41):10404-10414.
15. Errico F., Santini E., Migliarini S., Borgkvist A., Centonze D., Nasti V., Carta M., De Chiara V., Prosperetti C., Spano D., Herve D., Pasqualetti M., Di Lauro R., Fisone G., Usiello A. The GTP-binding protein Rhes modulates dopamine signalling in striatal medium spiny neurons. Molecular and Cellular Neurosciences 2008, 37(2):335-345.
16. Fagg G.E., Matus A. Selective association of N-methyl aspartate and quisqualate types of l-glutamate receptor with brain postsynaptic densities. Proceedings of the National Academy of Sciences of the United States of America 1984, 81(21):6876-6880.
17. Fukunaga K., Muller D., Miyamoto E. Increased phosphorylation of Ca2+/calmodulin-dependent protein kinase II and its endogenous substrates in the induction of long-term potentiation. The Journal of Biological Chemistry 1995, 270(11):6119-6124.
18. Guatteo E., Mercuri N.B., Bernardi G., Knopfel T. Intracellular sodium and calcium homeostasis during hypoxia in dopamine neurons of rat substantia nigra pars compacta. Journal of Neurophysiology 1998, 80(5):2237-2243.
19. Hardingham G.E., Bading H. The Yin and Yang of NMDA receptor signalling. Trends in Neurosciences 2003, 26(2):81-89.
20. Hashimoto A., Kumashiro S., Nishikawa T., Oka T., Takahashi K., Mito T., Takashima S., Doi N., Mizutani Y., Yamazaki T., et al. Embryonic development and postnatal changes in free d-aspartate and d-serine in the human prefrontal cortex. Journal of Neurochemistry 1993, 61(1):348-351.
21. Huang A.S., Beigneux A., Weil Z.M., Kim P.M., Molliver M.E., Blackshaw S., Nelson R.J., Young S.G., Snyder S.H. d-Aspartate regulates melanocortin formation and function: behavioral alterations in d-aspartate oxidase-deficient mice. The Journal of Neuroscience 2006, 26(10):2814-2819.
22. Huang Y. Apolipoprotein E and Alzheimer disease. Neurology 2006, 66(2 Suppl. 1):S79-S85.
23. 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. Proceedings of the National Academy of Sciences of the United States of America 2006, 103(13):5161-5166.
24. Katsuki H., Ishihara K., Shimada A., Takeda T., Satoh M. Age-related deterioration of long-term potentiation in the CA3 and CA1 regions of hippocampal slices from the senescence-accelerated mouse. Archives of Gerontology and Geriatrics 1990, 11(1):77-83.
25. Krapivinsky G., Krapivinsky L., Manasian Y., Ivanov A., Tyzio R., Pellegrino C., Ben-Ari Y., Clapham D.E., Medina I. The NMDA receptor is coupled to the ERK pathway by a direct interaction between NR2B and RasGRF1. Neuron 2003, 40(4):775-784.
26. Lisman J., Schulman H., Cline H. The molecular basis of CaMKII function in synaptic and behavioural memory. Nature Reviews 2002, 3(3):175-190.
27. Liu J., Fukunaga K., Yamamoto H., Nishi K., Miyamoto E. Differential roles of Ca(2+)/calmodulin-dependent protein kinase II and mitogen-activated protein kinase activation in hippocampal long-term potentiation. The Journal of Neuroscience 1999, 19(19):8292-8299.
28. Maekawa M., Watanabe M., Yamaguchi S., Konno R., Hori Y. Spatial learning and long-term potentiation of mutant mice lacking d-amino-acid oxidase. Neuroscience Research 2005, 53(1):34-38.
29. Mammen A.L., Kameyama K., Roche K.W., Huganir R.L. Phosphorylation of the alpha-amino-3-hydroxy-5-methylisoxazole4-propionic acid receptor GluR1 subunit by calcium/calmodulin-dependent kinase II. The Journal of Biological Chemistry 1997, 272(51):32528-32533.
30. McIlwain K.L., Merriweather M.Y., Yuva-Paylor L.A., Paylor R. The use of behavioral test batteries: effects of training history. Physiology & Behavior 2001, 73(5):705-717.
31. Oddo S., Caccamo A., Shepherd J.D., Murphy M.P., Golde T.E., Kayed R., Metherate R., Mattson M.P., Akbari Y., LaFerla F.M. Triple-transgenic model of Alzheimer's disease with plaques and tangles: intracellular Abeta and synaptic dysfunction. Neuron 2003, 39(3):409-421.
32. Olverman H.J., Jones A.W., Mewett K.N., Watkins J.C. Structure/activity relations of N-methyl-d-aspartate receptor ligands as studied by their inhibition of [3H]d-2-amino-5-phosphonopentanoic acid binding in rat brain membranes. Neuroscience 1988, 26(1):17-31.
33. Omkumar R.V., Kiely M.J., Rosenstein A.J., Min K.T., Kennedy M.B. Identification of a phosphorylation site for calcium/calmodulindependent protein kinase II in the NR2B subunit of the N-methyl-d-aspartate receptor. The Journal of Biological Chemistry 1996, 271(49):31670-31678.
34. Paul S., Nairn A.C., Wang P., Lombroso P.J. NMDA-mediated activation of the tyrosine phosphatase STEP regulates the duration of ERK signaling. Nature Neuroscience 2003, 6(1):34-42.
35. Phillips R.G., LeDoux J.E. Differential contribution of amygdala and hippocampus to cued and contextual fear conditioning. Behavioral Neuroscience 1992, 106(2):274-285.
36. Rosenzweig E.S., Barnes C.A. Impact of aging on hippocampal function: plasticity, network dynamics, and cognition. Progress in Neurobiology 2003, 69(3):143-179.
37. Sakai K., Homma H., Lee J.A., Fukushima T., Santa T., Tashiro K., Iwatsubo T., Imai K. Emergence of d-aspartic acid in the differentiating neurons of the rat central nervous system. Brain Research 1998, 808(1):65-71.
38. Santini E., Heiman M., Greengard P., Valjent E., Fisone G. Inhibition of mTOR signaling in Parkinson's disease prevents L-DOPA-induced dyskinesia. Science Signaling 2009, 2(80):ra36.
39. Schell M.J., Cooper O.B., Snyder S.H. d-Aspartate localizations imply neuronal and neuroendocrine roles. Proceedings of the National Academy of Sciences of the United States of America 1997, 94(5):2013-2018.
40. Shumyatsky G.P., Tsvetkov E., Malleret G., Vronskaya S., Hatton M., Hampton L., Battey J.F., Dulac C., Kandel E.R., Bolshakov V.Y. Identification of a signaling network in lateral nucleus of amygdala important for inhibiting memory specifically related to learned fear. Cell 2002, 111(6):905-918.
41. Svenningsson P., Lindskog M., Ledent C., Parmentier M., Greengard P., Fredholm B.B., Fisone G. Regulation of the phosphorylation of the dopamine- and cAMP-regulated phosphoprotein of 32 kDa in vivo by dopamine D1, dopamine D2, and adenosine A2A receptors. Proceedings of the National Academy of Sciences of the United States of America 2000, 97(4):1856-1860.
42. Tang Y.P., Shimizu E., Dube G.R., Rampon C., Kerchner G.A., Zhuo M., Liu G., Tsien J.Z. Genetic enhancement of learning and memory in mice. Nature 1999, 401(6748):63-69.
43. Thomas G.M., Huganir R.L. MAPK cascade signalling and synaptic plasticity. Nature Reviews 2004, 5(3):173-183.
44. Tsien J.Z., Huerta P.T., Tonegawa S. The essential role of hippocampal CA1 NMDA receptor-dependent synaptic plasticity in spatial memory. Cell 1996, 87(7):1327-1338.
45. Van Veldhoven P.P., Brees C., Mannaerts G.P. d-Aspartate oxidase, a peroxisomal enzyme in liver of rat and man. Biochimica et Biophysica Acta 1991, 1073(1):203-208.
46. Winters B.D., Saksida L.M., Bussey T.J. Object recognition memory: neurobiological mechanisms of encoding, consolidation and retrieval. Neuroscience and Biobehavioral Reviews 2008, 32(5):1055-1070.
47. Wolosker H., D'Aniello A., Snyder S.H. d-Aspartate disposition in neuronal and endocrine tissues: ontogeny, biosynthesis and release. Neuroscience 2000, 100(1):183-189.