D-serine levels in Alzheimer's disease: Implications for novel biomarker development

Translational Psychiatry

Volumn 5, Issue , 2015, Pages

  Madeira, C ^a   Lourenco, M V ^a   Vargas Lopes, C ^a   Suemoto, C K ^b   Brandao C O ^a   Reis, T ^a   Leite, R E P ^b   Laks, J ^a   Jacob Filho, W ^b   Pasqualucci, C A ^b   Grinberg, L T ^b,c   Ferreira, S T ^a   Panizzutti, R ^a  

^a FEDERAL UNIVERSITY OF RIO DE JANEIRO   (Brazil)

^b UNIVERSITY OF SÃO PAULO   (Brazil)

^c UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID BETA PROTEIN; AMYLOID PRECURSOR PROTEIN; BIOLOGICAL MARKER; DEXTRO SERINE; OLIGOMER; RACEMASE; SERINE; TAU PROTEIN;

AGED; ALZHEIMER DISEASE; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; CEREBROSPINAL FLUID LEVEL; CONTROLLED STUDY; FEMALE; HIPPOCAMPAL NEURONAL CULTURE; HIPPOCAMPUS; HUMAN; HUMAN TISSUE; MAJOR DEPRESSION; MALE; MENTAL HEALTH; MILD COGNITIVE IMPAIRMENT; MOUSE; NONHUMAN; NORMOTENSIVE HYDROCEPHALUS; OCCIPITAL CORTEX; PARIETAL CORTEX; RAT; UPREGULATION; WILD TYPE RAT; ANIMAL; BRAIN CORTEX; CASE CONTROL STUDY; CEREBROSPINAL FLUID; DISEASE MODEL; GENETICS; METABOLISM; MIDDLE AGED; TRANSGENIC MOUSE; VERY ELDERLY;

AGED; AGED, 80 AND OVER; ALZHEIMER DISEASE; AMYLOID BETA-PEPTIDES; AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; BIOMARKERS; CASE-CONTROL STUDIES; CEREBRAL CORTEX; DEPRESSIVE DISORDER, MAJOR; DISEASE MODELS, ANIMAL; FEMALE; HIPPOCAMPUS; HUMANS; HYDROCEPHALUS, NORMAL PRESSURE; MALE; MICE; MICE, TRANSGENIC; MIDDLE AGED; RATS; SERINE;

EID: 84929159607     PISSN: None     EISSN: 21583188     Source Type: Journal    
DOI: 10.1038/tp.2015.52     Document Type: Article

References (77)

1. Tarawneh R, Holtzman DM. The clinical problem of symptomatic Alzheimer disease and mild cognitive impairment. Cold Spring Harb Perspect Med 2012; 2: 1-17.
2. Mattson MP. Pathways towards and away from Alzheimer's disease. Nature 2004; 430: 631-639.
3. Ferreira ST, Klein WL. The A? oligomer hypothesis for synapse failure and memory loss in Alzheimer's disease. Neurobiol Learn Mem 2011; 96: 529-543.
4. Mucke L, Selkoe DJ. Neurotoxicity of amyloid-beta protein: Synaptic and network dysfunction. Cold Spring Harb Perspect Med 2012; 2: 1-17.
5. Jack CR, Albert MS, Knopman DS, McKhann GM, Sperling RA, Carrillo MC et al. Introduction to the recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 2011; 7: 257-262.
6. McKhann GM, Knopman DS, Chertkow H, Hyman BT, Jack CR, Kawas CH et al. The diagnosis of dementia due to Alzheimer's disease: Recommendations from the National Institute on Aging-Alzheimer's Association workgroups on diagnostic guidelines for Alzheimer's disease. Alzheimers Dement 2011; 7: 263-269.
7. McKhann GM. Changing concepts of Alzheimer's disease. JAMA 2011; 305: 2458-2459.
8. Selkoe DJ. Preventing Alzheimer's disease. Science 2012; 337: 1488-1492.
9. DeKosky ST, Carrillo MC, Phelps C, Knopman D, Petersen RC, Frank R et al. Revision of the criteria for Alzheimer's disease: A symposium. Alzheimers Dement 2011; 7: E1-e12.
10. Blennow K, Hampel H, Weiner M, Zetterberg H. Cerebrospinal fluid and plasma biomarkers in Alzheimer disease. Nat Rev Neurol 2010; 6: 131-144.
11. Hampel H, Bürger K, Teipel SJ, Bokde ALW, Zetterberg H, Blennow K. Core candidate neurochemical and imaging biomarkers of Alzheimer's disease. Alzheimers Dement 2008; 4: 38-48.
12. Paula-Lima AC, Brito-Moreira J, Ferreira ST. Deregulation of excitatory neurotransmission underlying synapse failure in Alzheimer's disease. J Neurochem 2013; 126: 191-202.
13. Li S, Jin M, Koeglsperger T, Shepardson NE, Shankar GM, Selkoe DJ. Soluble A? oligomers inhibit long-term potentiation through a mechanism involving excessive activation of extrasynaptic NR2B-containing NMDA receptors. J Neurosci 2011; 31: 6627-6638.
14. Li S, Hong S, Shepardson NE, Walsh DM, Shankar GM, Selkoe D. Soluble oligomers of amyloid-? protein facilitate hippocampal long-term depression by disrupting neuronal glutamate uptake. Neuron 2009; 62: 788-801.
15. Shankar GM, Bloodgood BL, Townsend M, Walsh DM, Selkoe DJ, Sabatini BL. Natural oligomers of the Alzheimer amyloid-? protein induce reversible synapse loss by modulating an NMDA-type glutamate receptor-dependent signaling pathway. J Neurosci 2007; 27: 2866-2875.
16. De Felice FG, Velasco PT, Lambert MP, Viola K, Fernandez SJ, Ferreira ST et al. A? oligomers induce neuronal oxidative stress through an N-methyl-D-aspartate receptor-dependent mechanism that is blocked by the Alzheimer drug memantine. J Biol Chem 2007; 282: 11590-11601.
17. Talantova M, Sanz-Blasco S, Zhang X, Xia P, Akhtar MW, Okamoto S et al. A? induces astrocytic glutamate release, extrasynaptic NMDA receptor activation, and synaptic loss. Proc Natl Acad Sci USA 2013; 110: E2518-E2527.
18. Parsons CG, Danysz W, Dekundy A, Pulte I. Memantine and cholinesterase inhibitors: Complementary mechanisms in the treatment of Alzheimer's Disease. Neurotox Res 2013; 24: 358-369.
19. Wolosker H, Radzishevsky I. The serine shuttle between glia and neurons: Implications for neurotransmission and neurodegeneration. Biochem Soc Trans 2013; 41: 1546-1550.
20. Radzishevsky I, Sason H, Wolosker H. D-Serine: Physiology and pathology. Curr Opin Clin Nutr Metab Care 2013; 16: 72-75.
21. Wolosker H, Dumin E, Balan L, Foltyn VN. d-Amino acids in the brain: D-serine in neurotransmission and neurodegeneration. FEBS J 2008; 275: 3514-3526.
22. Mustafa AK, Ahmad AS, Zeynalov E, Gazi SK, Sikka G, Ehmsen JT et al. Serine racemase deletion protects against cerebral ischemia and excitotoxicity. J Neurosci 2010; 30: 1413-1416.
23. Wu S-Z, Bodles AM, Porter MM, Griffin WS, Basile AS, Barger SW. Induction of serine racemase expression and D-serine release from microglia by amyloid-? peptide. J Neuroinflammation 2004; 1: 1-11.
24. Brito-Moreira J, Paula-Lima AC, Bomfim TR, Oliveira FF, Sepúlveda FJ, Mello FG et al. A? oligomers induce glutamate release from hippocampal neurons. Curr Alzheimer Res 2011; 8: 552-562.
25. Bado P, Madeira C, Vargas-Lopes C, Moulin TC, Wasilewska-Sampaio AP, Maretti L et al. Effects of low-dose d-serine on recognition and working memory in mice. Psychopharmacology 2011; 218: 461-470.
26. Guercio GD, Bevictori L, Vargas-Lopes C, Madeira C, Oliveira A, Carvalho VF et al. D-serine prevents cognitive deficits induced by acute stress. Neuropharmacology 2014; 86: 1-8.
27. Di Prisco GV, Huang W, Buffington SA, Hsu CC, Bonnen PE, Placzek AN et al. Translational control of mGluR-dependent long-term depression and object-place learning by eIF2alpha. Nat Neurosci 2014; 17: 1073-1082.
28. Kumashiro S, Hashimoto A, Nishikawa T. Free D-serine in post-mortem brains and spinal cords of individuals with or without neuropsychiatric diseases. Brain Res 1995; 681: 117-125.
29. Nagata Y, Borghi M, Fisher GH, D'Aniello A. Free D-serine concentration in normal and Alzheimer human brain. Brain Res Bull 1995; 38: 181-183.
30. Chouinard ML, Gaitan D, Wood PL. Presence of the N-methyl-D-aspartate-associated glycine receptor agonist, d-serine, in human temporal cortex: Comparison of normal, Parkinson, and Alzheimer tissues. J Neurochem 1993; 61: 1561-1564.
31. Fisher GH, Lorenzo N, Abe H, Fujita E, Frey WH, Emory C et al. Free D-and L-amino acids in ventricular cerebrospinal fluid from Alzheimer and normal subjects. Amino Acids 1998; 15: 263-269.
32. Grinberg LT, Lucena Ferretti RE, Farfel JM, Leite R, Pasqualucci CA, Rosemberg S et al. Brain bank of the Brazilian aging brain study group-a milestone reached and more than 1,600 collected brains. Cell Tissue Bank 2007; 8: 151-162.
33. Ferreti R, Damin AE, Brucki SM, Morillo LS, Perroco TR, Campora F et al. Postmortem diagnosis of dementia by informant interview. Dement Neuropsychol 2010; 4: 138-1441.
34. Morris JC. The Clinical Dementia Rating (CDR): Current version and scoring rules. Neurology 1993; 43: 2412-2412a.
35. Reis T, Brandão CO, Freire Coutinho ES, Engelhardt E, Laks J. Cerebrospinal fluid biomarkers in Alzheimer's disease and geriatric depression: Preliminary findings from Brazil. CNS Neurosci Ther 2012; 18: 524-529.
36. Calcia MA, Madeira C, Alheira FV, TCS Silva, Tannos FM, Vargas-Lopes C et al. Plasma levels of D-serine in Brazilian individuals with schizophrenia. Schizophr Res 2012; 142: 83-87.
37. Hashimoto A, Nishikawa T, Hayashi T, Fujii N, Harada K, Oka T et al. The presence of free D-serine in rat brain. FEBS Lett 1992; 296: 33-36.
38. Sebollela A, Freitas-Correa L, Oliveira FF, Paula-Lima AC, Saraiva LM, Martins SM et al. Amyloid-? oligomers induce differential gene expression in adult human brain slices. J Biol Chem 2012; 287: 7436-7445.
39. Jurgensen S, Antonio LL, Mussi GE, Brito-Moreira J, Bomfim TR, De Felice FG et al. Activation of D1/D5 dopamine receptors protects neurons from synapse dysfunction induced by amyloid-? oligomers. J Biol Chem 2011; 286: 3270-3276.
40. Ledo JH, Azevedo EP, Clarke JR, Ribeiro FC, Figueiredo CP, Foguel D et al. Amyloid-? oligomers link depressive-like behavior and cognitive deficits in mice. Mol Psychiatry 2013; 18: 1053-1054.
41. Lourenco Mychael V, Clarke Julia R, Frozza Rudimar L, Bomfim Theresa R, Forny-Germano L, Batista André F et al. TNF-? mediates PKR-dependent memory impairment and brain IRS-1 inhibition induced by Alzheimer's ?-amyloid oligomers in mice and monkeys. Cell Metab 2013; 18: 831-843.
42. Jankowsky JL, Slunt HH, Ratovitski T, Jenkins NA, Copeland NG, Borchelt DR. Coexpression of multiple transgenes in mouse CNS: A comparison of strategies. Biomol Eng 2001; 17: 157-165.
43. Vargas-Lopes C, Madeira C, Kahn SA, Albino do Couto I, Bado P, Houzel JC et al. Protein kinase C activity regulates d-serine availability in the brain. J Neurochem 2011; 116: 281-290.
44. Panizzutti R, De Miranda J, Ribeiro CS, Engelender S, Wolosker H. A new strategy to decrease N-methyl-D-aspartate (NMDA) receptor coactivation: Inhibition of D-serine synthesis by converting serine racemase into an eliminase. Proc Natl Acad Sci USA 2001; 98: 5294-5299.
45. Livak KJ, Schmittgen TD. Analysis of relative gene expression data using real-time quantitative PCR and the 2(-Delta Delta C(T)) Method. Methods 2001; 25: 402-408.
46. Faul F, Erdfelder E, Buchner A, Lang AG. Statistical power analyses using G∗Power 3.1: Tests for correlation and regression analyses. Behav Res Methods 2009; 41: 1149-1160.
47. Wolosker H, Mori H. Serine racemase: An unconventional enzyme for an unconventional transmitter. Amino Acids 2012; 43: 1895-1904.
48. Wolosker H, Sheth KN, Takahashi M, Mothet J-P, Brady RO, Ferris CD et al. Purification of serine racemase: Biosynthesis of the neuromodulator D-serine. Proc Natl Acad Sci USA 1999; 96: 721-725.
49. Smith DL, Pozueta J, Gong B, Arancio O, Shelanski M. Reversal of long-term dendritic spine alterations in Alzheimer disease models. Proc Natl Acad Sci USA 2009; 106: 16877-16882.
50. Puzzo D, Staniszewski A, Deng SX, Privitera L, Leznik E, Liu S et al. Phosphodiesterase inhibition improves synaptic function, memory, and amyloid-load in an Alzheimer's disease mouse model. J Neurosci 2009; 29: 8075-8086.
51. Hulstaert F, Blennow K, Ivanolu A, Schoonderwaldt HC, Riemenschneider M, De Deyn P et al. Improved discrimination of AD patients using ?-amyloid(1-42) and tau levels in CSF. Neurology 1999; 52: 1555-1562.
52. Dauvilliers YA, Lehmann S, Jaussent I, Gabelle A. Hypocretin and brain betaamyloid peptide interactions in cognitive disorders and narcolepsy. Front Aging Neurosci 2014; 6: 119.
53. Lehmann S, Schraen S, Quadrio I, Paquet C, Bombois S, Delaby C et al. Impact of harmonization of collection tubes on Alzheimer's disease diagnosis. Alzheimers Dement 2014; 10: E392.
54. Tabaraud F, Leman JP, Milor AM, Roussie JM, Barriere G, Tartary M et al. Alzheimer CSF biomarkers in routine clinical setting. Acta Neurol Scand 2012; 125: 416-423.
55. Lehmann S, Dumurgier J, Schraen S, Wallon D, Blanc F, Magnin E et al. A diagnostic scale for Alzheimer's disease based on cerebrospinal fluid biomarker profiles. Alzheimers Res Ther 2014; 6: 1-9.
56. Braak H, Braak E. Neuropathological stageing of Alzheimer-related changes. Acta Neuropathol 1991; 82: 239-259.
57. Armstrong RA, Nochlin D, Bird TD. Neuropathological heterogeneity in Alzheimer's disease: A study of 80 cases using principal components analysis. Neuropathology 2000; 1: 31-37.
58. Xia W, Yang T, Shankar GM, Smith IM, Shen Y, Walsh D et al. A specific enzymelinked immunosorbent assay for measuring ?-amyloid protein oligomers in human plasma and brain tissue of patients with Alzheimer disease. Arch Neurol 2009; 66: 190-199.
59. Gong Y, Chang L, Viola KL, Lacor PN, Lambert MP, Finch CE et al. Alzheimer's disease-affected brain: Presence of oligomeric A? ligands (ADDLs) suggests a molecular basis for reversible memory loss. Proc Natl Acad Sci USA 2003; 100: 10417-10422.
60. Kayed R, Head E, Thompson JL, McIntire TM, Milton SX, Cotman CW et al. Common structure of soluble amyloid oligomers implies common mechanism of pathogenesis. Science 2003; 300: 486-489.
61. Lambert MP, Barlow AK, Chromy BA, Edwards C, Freed R, Liosatos M et al. Diffusible, nonfibrillar ligands derived from Abeta1-42 are potent central nervous system neurotoxins. Proc Natl Acad Sci USA 1998; 95: 6448-6453.
62. Decker H, Jürgensen S, Adrover MF, Brito-Moreira J, Bomfim TR, Klein WL et al. Nmethyl-D-aspartate receptors are required for synaptic targeting of Alzheimer's toxic A? oligomers. J Neurochem 2010; 115: 1520-1529.
63. Hardingham GE, Bading H. Synaptic versus extrasynaptic NMDA receptor signalling: Implications for neurodegenerative disorders. Nat Rev Neurosci 2010; 11: 682-696.
64. Roselli F, Tirard M, Lu J, Hutzler P, Lamberti P, Livrea P et al. Soluble ?-amyloid 1- induces NMDA-dependent degradation of postsynaptic density-95 at glutamatergic synapses. J Neurosci 2005; 25: 11061-11070.
65. Hynd MR, Scott HL, Dodd PR. Selective loss of NMDA receptor NR1 subunit isoforms in Alzheimer's disease. J Neurochem 2004; 89: 240-247.
66. Mishizen-Eberz AJ, Rissman RA, Carter TL, Ikonomovic MD, Wolfe BB, Armstrong DM. Biochemical and molecular studies of NMDA receptor subunits NR1/2 A/2B in hippocampal subregions throughout progression of Alzheimer's disease pathology. Neurobiol Dis 2004; 15: 80-92.
67. Ikonomovic MD, Mizukami K, Warde D, Sheffield R, Hamilton R, Wenthold RJ et al. Distribution of glutamate receptor subunit NMDAR1 in the hippocampus of normal elderly and patients with Alzheimer's disease. Exp Neurol 1999; 160: 194-204.
68. Filali M, Lalonde R. The effects of subchronic d-serine on left-right discrimination learning, social interaction, and exploratory activity in APPswe/PS1 mice. Eur J Pharmacol 2013; 701: 152-158.
69. Diniz LP, Almeida JC, Tortelli V, Vargas Lopes C, Setti-Perdigao P, Stipursky J et al. Astrocyte-induced synaptogenesis is mediated by transforming growth factor ? signaling through modulation of D-serine levels in cerebral cortex neurons. J Biol Chem 2012; 287: 41432-41445.
70. Esposito S, Pristerà A, Maresca G, Cavallaro S, Felsani A, Florenzano F et al. Contribution of Serine racemase/D-serine pathway to neuronal apoptosis. Aging Cell 2012; 11: 588-98.
71. Wilson RS, Barnes LL, Mendes De Leon CF, Aggarwal NT, Schneider JS, Bach J et al. Depressive symptoms, cognitive decline, and risk of AD in older persons. Neurology 2002; 59: 364-370.
72. Ownby RL, Crocco E, Acevedo A, John V, Loewenstein D. Depression and risk for Alzheimer disease: Systematic review, meta-analysis and metaregression analysis. Arch Gen Psychiatry 2006; 63: 530-538.
73. Savage MJ, Kalinina J, Wolfe A, Tugusheva K, Korn R, Cash-Mason T et al. A sensitive a oligomer assay discriminates alzheimer's and aged control cerebrospinal fluid. J Neurosci 2014; 34: 2884-2897.
74. Mouton-Liger F, Paquet C, Dumurgier J, Lapalus P, Gray F, Laplanche J-L et al. Increased cerebrospinal fluid levels of double-stranded RNA-dependant protein kinase in Alzheimer's disease. Biol Psychiatry 2012; 71: 829-835.
75. Dumurgier J, Mouton-Liger F, Lapalus P, Prevot V, Laplanche J-L, Hugon J et al. Cerebrospinal fluid PKR level predicts cognitive decline in Alzheimer's disease. PLoS One 2013; 8: E53587.
76. Harari O, Cruchaga C, Kauwe JSK, Ainscough BJ, Bales K, Pickering EH et al. Phosphorylated Tau-A?42 ratio as a continuous trait for biomarker discovery for early-stage Alzheimer's disease in multiplex immunoassay panels of cerebrospinal fluid. Biol Psychiatry 2014; 75: 723-731.
77. Fagan AM, Xiong C, Jasielec MS, Bateman RJ, Goate AM, Benzinger TLS et al. Longitudinal change in CSF biomarkers in autosomal-dominant Alzheimer's disease. Sci Transl Med 2014; 6: 226ra230-226ra230.