Induction of serine racemase expression and D-serine release from microglia by secreted amyloid precursor protein (sAPP)

Current Alzheimer Research

Volumn 4, Issue 3, 2007, Pages 243-251

  Wu, Shengzhou ^a   Basile, Anthony S ^b   Barger, Steven W ^c,d,e  

^a WASHINGTON UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b DOV Pharmaceutical Inc   (United States)

^c UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

^d GERIATRIC RESEARCH EDUCATION AND CLINICAL CENTER   (United States)

^e UNIVERSITY OF ARKANSAS FOR MEDICAL SCIENCES   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

AMYLOID PRECURSOR PROTEIN; DEXTRO SERINE; DIMER; GLUTAMIC ACID; MESSENGER RNA; N METHYL DEXTRO ASPARTIC ACID; N METHYL DEXTRO ASPARTIC ACID RECEPTOR; N METHYL DEXTRO ASPARTIC ACID RECEPTOR STIMULATING AGENT; RACEMASE; SERINE;

ALZHEIMER DISEASE; ANIMAL CELL; ARTICLE; BRAIN REGION; CELL LOSS; DEGENERATIVE DISEASE; EXCITOTOXICITY; GENE INDUCTION; MICROGLIA; NONHUMAN; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN EXPRESSION; PROTEIN SECRETION; RAT; REPORTER GENE; STEADY STATE; SYNAPSE; TRANSCRIPTION REGULATION; TRANSLATION REGULATION;

AMYLOID BETA-PROTEIN PRECURSOR; ANIMALS; ANIMALS, NEWBORN; CELLS, CULTURED; CEREBRAL CORTEX; CHROMATOGRAPHY, HIGH PRESSURE LIQUID; DOSE-RESPONSE RELATIONSHIP, DRUG; GENE EXPRESSION; HUMANS; MICROGLIA; RACEMASES AND EPIMERASES; RATS; RATS, SPRAGUE-DAWLEY; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; SERINE; TRANSFECTION;

EID: 34347372591     PISSN: 15672050     EISSN: None     Source Type: Journal    
DOI: 10.2174/156720507781077241     Document Type: Article

References (77)

1. Barger SW. An unconventional hypothesis of oxidation in Alzheimer's disease: intersections with excitotoxicity. Front Biosci 9: 3286-95 (2004).
2. Willard LB, Hauss-Wegrzyniak B, Danysz W and Wenk GL. The cytotoxicity of chronic neuroinflammation upon basal forebrain cholinergic neurons of rats can be attenuated by glutamatergic antagonism or cyclooxygenase-2 inhibition. Exp Brain Res 134: 58-65. (2000).
3. Piani D, Spranger M, Frei K, Schaffner A and Fontana A. Macrophage-induced cytotoxicity of N-methyl-D-aspartate receptor positive neurons involves excitatory amino acids rather than reactive oxygen intermediates and cytokines. Eur J Immunol 22: 2429-2436 (1992).
4. Barger SW. Vascular consequences of passive Aβ immunization for Alzheimer's disease. Is avoidance of "malactivation" of microglia enough? J Neuroinflammation 2: 2 (2005).
5. Barger SW and Basile AS. Activation of microglia by secreted amyloid precursor protein evokes release of glutamate by cystine exchange and attenuates synaptic function. J Neurochem 76: 846-854 (2001).
6. Heyes MP, Achim CL, Wiley CA, Major EO, Saito K and Markey SP. Human microglia convert L-tryptophan into the neurotoxin quinolinic acid. Biochem J 320: 595-597 (1996).
7. Wu S-Z, Bodles AM, Porter MM, Griffin WST, Basile AS and Barger SW. Induction of serine racemase expression and D-serine release from microglia by amyloid β-peptide. J Neuroinflammation 1: 2-12 (2004).
8. Saito K, Elce JS, Hamos JE and Nixon RA. Widespread activation of calcium-activated neutral proteinase (calpain) in the brain in Alzheimer disease: a potential molecular basis for neuronal degeneration. Proc Natl Acad Sci (USA) 90: 2628-2632 (1993).
9. Jansen KL, Faull RL, Dragunow M and Synek BL. Alzheimer's disease: changes in hippocampal N-methyl-D-aspartate, quisqualate, neurotensin, adenosine, benzodiazepine, serotonin and opioid receptors - an autoradiographic study. Neuroscience 39: 613-27 (1990).
10. Penney JB, Maragos WF, Greenamyre JT, Debowey DL, Hollingsworth Z and Young AB. Excitatory amino acid binding sites in the hippocampal region of Alzheimer's disease and other dementias. J Neurol Neurosurg Psychiatry 53: 314-20 (1990).
11. Ulas J, Brunner LC, Geddes JW, Choe W and Cotman CW. N-methyl-D-aspartate receptor complex in the hippocampus of elderly, normal individuals and those with Alzheimer's disease. Neuroscience 49: 45-61 (1992).
12. 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 160: 194-204 (1999).
13. Sze C, Bi H, Kleinschmidt-DeMasters BK, Filley CM and Martin LJ. N-Methyl-D-aspartate receptor subunit proteins and their phosphorylation status are altered selectively in Alzheimer's disease. J Neurol Sci 182: 151-9 (2001).
14. Hynd MR, Scott HL and Dodd PR. Glutamate(NMDA) receptor NR1 subunit mRNA expression in Alzheimer's disease. J Neurochem 78: 175-82 (2001).
15. Bi H and Sze CI. N-methyl-D-aspartate receptor subunit NR2A and NR2B messenger RNA levels are altered in the hippocampus and entorhinal cortex in Alzheimer's disease. J Neurol Sci 200: 11-8 (2002).
16. Hynd MR, Scott HL and Dodd PR. Selective loss of NMDA receptor NR1 subunit isoforms in Alzheimer's disease. J Neurochem 89: 240-7 (2004).
17. Hynd MR, Scott HL and Dodd PR. Differential expression of N-methyl-D-aspartate receptor NR2 isoforms in Alzheimer's disease. J Neurochem 90: 913-9 (2004).
18. Mishizen-Eberz AJ, Rissman RA, Carter TL, Ikonomovic MD, Wolfe BB and Armstrong DM. Biochemical and molecular studies of NMDA receptor subunits NR1/2A/2B in hippocampal subregions throughout progression of Alzheimer's disease pathology. Neurobiol Dis 15: 80-92 (2004).
19. Harkany T, Abraham I, Timmerman W, Laskay G, Toth B, Sasvari M, et al. β-amyloid neurotoxicity is mediated by a glutamatetriggered excitotoxic cascade in rat nucleus basalis. Eur J Neurosci 12: 2735-45. (2000).
20. Reisberg B, Doody R, Stoffler A, Schmitt F, Ferris S, Mobius HJ, et al. Memantine in moderate-to-severe Alzheimer's disease. N Engl J Med 348: 1333-1341 (2003).
21. Abele AE, Scholz KP, Scholz WK and Miller RJ. Excitotoxicity induced by enhanced excitatory neurotransmission in cultured hippocampal pyramidal neurons. Neuron 4: 413-419 (1990).
22. Laube B, Hirai H, Sturgess M, Betz H and Kuhse J. Molecular determinants of agonist discrimination by NMDA receptor subunits: analysis of the glutamate binding site on the NR2B subunit. Neuron 18: 493-503 (1997).
23. Panizzutti R, De Miranda J, Ribeiro CS, Engelender S and 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 98: 5294-9 (2001).
24. Furukawa H and Gouaux E. Mechanisms of activation, inhibition and specificity: crystal structures of the NMDA receptor NR1 ligand-binding core. EMBO J 22: 2873-85 (2003).
25. Schell MJ, Molliver ME and Snyder SH. D-serine, an endogenous synaptic modulator: localization to astrocytes and glutamate-stimulated release. Proc Natl Acad Sci USA 92: 3948-52. (1995).
26. Mothet JP, Parent AT, Wolosker H, Brady RO, Jr., Linden DJ, Ferris CD, et al. D-serine is an endogenous ligand for the glycine site of the N-methyl-D- aspartate receptor. Proc Natl Acad Sci USA 97: 4926-31. (2000).
27. Koh J-Y, Yang LL and Cotman CW. β-amyloid protein increases the vulnerability of cultured cortical neurons to excitotoxic damage. Brain Res 533: 315-320 (1990).
28. Mattson MP, Cheng B, Davis D, Bryant K, Lieberburg I and Rydel RE. β-Amyloid peptides destabilize calcium homeostasis and render human cortical neurons vulnerable to excitotoxicity. J. Neurosci. 12: 379-389 (1992).
29. Gray CW and Patel AJ. Neurodegeneration mediated by glutamate and beta-amyloid peptide: a comparison and possible interaction. Brain Res 691: 169-79 (1995).
30. Qiu Z and Gruol DL. Interleukin-6, beta-amyloid peptide and NMDA interactions in rat cortical neurons. J Neuroimmunol 139: 51-7 (2003).
31. Fisher G, 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 15: 263-9 (1998).
32. Barger SW and Harmon AD. Microglial activation by secreted Alzheimer amyloid precursor protein and modulation by apolipoprotein E. Nature 388: 878-881 (1997).
33. Li Y, Liu L, Kang J, Sheng JG, Barger SW, Mrak RE, et al. Neuronal-glial interactions mediated by interleukin-1 enhance neuronal acetylcholinesterase activity and mRNA expression. J Neurosci 20: 149-155 (2000).
34. Ikezu T, Luo X, Weber GA, Zhao J, McCabe L, Buescher JL, et al. Amyloid precursor protein-processing products affect mononuclear phagocyte activation: pathways for sAPP- and Abeta-mediated neurotoxicity. J Neurochem 85: 925-34 (2003).
35. Li Y, Liu L, Barger SW and Griffin WS. Interleukin-1 mediates pathological effects of microglia on tau phosphorylation and on synaptophysin synthesis in cortical neurons through a p38-MAPK pathway. J Neurosci 23: 1605-1611 (2003).
36. Xiong H, McCabe L, Costello J, Anderson E, Weber G and Ikezu T. Activation of NR1a/NR2B receptors by soluble factors from APP-stimulated monocyte-derived macrophages: implications for the pathogenesis of Alzheimer's disease. Neurobiol Aging 25: 905-11 (2004).
37. Griffin WS, Liu L, Li Y, Mrak RE and Barger SW. Interleukin-1 mediates Alzheimer and Lewy body pathologies. J Neuroinflammation 3: 5 (2006).
38. Wu S-Z and Barger SW. Serine racemase induction by inflammatory stimuli is dependent on AP-1. Ann N Y Acad Sci 1035: 133-146 (2004).
39. Yamada K, Ohnishi T, Hashimoto K, Ohba H, Iwayama-Shigeno Y, Toyoshima M, et al. Identification of multiple serine racemase (SRR) mRNA isoforms and genetic analyses of SRR and DAO in schizophrenia and D-serine levels. Biol Psychiatry 57: 1493-503 (2005).
40. Cook SP, Galve-Roperh I, Martinez Del Pozo A and Rodriguez-Crespo I. Direct calcium binding results in activation of brain Serine Racemase. J Biol Chem 20: 27782-27792 (2002).
41. Mothet JP, Pollegioni L, Ouanounou G, Martineau M, Fossier P and Baux G. Glutamate receptor activation triggers a calcium-dependent and SNARE protein-dependent release of the gliotransmitter D-serine. Proc Natl Acad Sci USA 102: 5606-11 (2005).
42. Kartvelishvily E, Shleper M, Balan L, Dumin E and Wolosker H. Neuron-derived D-serine release provides a novel means to activate N-methyl-D-aspartate receptors. J Biol Chem 281: 14151-62 (2006).
43. De Miranda J, Santoro A, Engelender S and Wolosker H. Human serine racemase: moleular cloning, genomic organization and functional analysis. Gene 256: 183-8 (2000).
44. Katsuki H, Nonaka M, Shirakawa H, Kume T and Akaike A. Endogenous D-serine is involved in induction of neuronal death by N-methyl-D-aspartate and simulated ischemia in rat cerebrocortical slices. J Pharmacol Exp Ther 311: 836-44 (2004).
45. Shleper M, Kartvelishvily E and Wolosker H. D-serine is the dominant endogenous coagonist for NMDA receptor neurotoxicity in organotypic hippocampal slices. J Neurosci 25: 9413-7 (2005).
46. Wu SZ, Jiang S, Sims TJ and Barger SW. Schwann cells exhibit excitotoxicity consistent with release of NMDA receptor agonists. J Neurosci Res 79: 638-643 (2005).
47. Chumakov I, Blumenfeld M, Guerassimenko O, Cavarec L, Palicio M, Abderrahim H, et al. Genetic and physiological data implicating the new human gene G72 and the gene for D-amino acid oxidase in schizophrenia. Proc Natl Acad Sci USA 99: 13675-80 (2002).
48. Tsai G and Coyle JT. Glutamatergic mechanisms in schizophrenia. Annu Rev Pharmacol Toxicol 42: 165-79 (2002).
49. Casanova MF, Carosella NW, Gold JM, Kleinman JE, Weinberger DR and Powers RE. A topographical study of senile plaques and neurofibrillary tangles in the hippocampi of patients with Alzheimer's disease and cognitively impaired patients with schizophrenia. Psychiatry Res 49: 41-62 (1993).
50. Purohit DP, Davidson M, Perl DP, Powchik P, Haroutunian VH, Bierer LM, et al. Severe cognitive impairment in elderly schizophrenic patients: a clinicopathological study. Biol Psychiatry 33: 255-60 (1993).
51. Arnold SE, Trojanowski JQ, Gur RE, Blackwell P, Han LY and Choi C. Absence of neurodegeneration and neural injury in the cerebral cortex in a sample of elderly patients with schizophrenia. Arch Gen Psychiatry 55: 225-32 (1998).
52. Miyoshi R, Kito S, Doudou N and Nomoto T. Age-related changes of strychnine-insensitive glycine receptors in rat brain as studied by in vitro autoradiography. Synapse 6: 338-43 (1990).
53. Nagata Y, Uehara T, Kitamura Y, Nomura Y and Horiike K. Dserine content and D-[3H]serine binding in the brain regions of the senescence-accelerated mouse. Mech Ageing Dev 104: 115-24. (1998).
54. Fitzjohn SM, Morton RA, Kuenzi F, Rosahl TW, Shearman M, Lewis H, et al. 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 21: 4691-8. (2001).
55. Doble A. The role of excitotoxicity in neurodegenerative disease: implications for therapy. Pharmacol Ther 81: 163-221 (1999).
56. Breitner JC, Gau BA, Welsh KA, Plassman BL, McDonald WM, Helms MJ, et al. Inverse association of anti-inflammatory treatments and Alzheimer's disease: initial results of a co-twin control study. Neurology 44: 227-232 (1994).
57. Lindsay J, Laurin D, Verreault R, Hebert R, Helliwell B, Hill GB, et al. Risk factors for Alzheimer's disease: a prospective analysis from the Canadian Study of Health and Aging. Am J Epidemiol 156: 445-53 (2002).
58. in 't Veld BA, Launer LJ, Hoes AW, Ott A, Hofman A, Breteler MM, et al. NSAIDs and incident Alzheimer's disease. The Rotterdam Study. Neurobiol Aging 19: 607-11. (1998).
59. Zandi PP, Anthony JC, Hayden KM, Mehta K, Mayer L and Breitner JC. Reduced incidence of AD with NSAID but not H2 receptor antagonists: the Cache County Study. Neurology 59: 880-6. (2002).
60. Wilcock GK, Black SE, Haworth J, Hendrix S, Laughlin M, Zavitz K, et al. Efficacy and Safety of MPC-7869, a Selective Aß42-Lowering Agent, in Alzheimer's Disease (AD): Results of a 12-Month Phase 2 Trial and 1-year Follow-on Study. In: ICAD 2006; 2006; Madrid, Spain; 2006.
61. Lim GP, Yang F, Chu T, Chen P, Beech W, Teter B, et al. Ibuprofen suppresses plaque pathology and inflammation in a mouse model for Alzheimer's disease. J Neurosci 20: 5709-14. (2000).
62. Jantzen PT, Connor KE, DiCarlo G, Wenk GL, Wallace JL, Rojiani AM, et al. Microglial activation and beta -amyloid deposit reduction caused by a nitric oxide-releasing nonsteroidal antiinflammatory drug in amyloid precursor protein plus presenilin-1 transgenic mice. J Neurosci 22: 2246-54. (2002).
63. Yan Q, Zhang J, Liu H, Babu-Khan S, Vassar R, Biere AL, et al. Anti-inflammatory drug therapy alters beta-amyloid processing and deposition in an animal model of Alzheimer's disease. J Neurosci 23: 7504-9 (2003).
64. McCusker SM, Curran MD, Dynan KB, McCullagh CD, Urquhart DD, Middleton D, et al. Association between polymorphism in regulatory region of gene encoding tumour necrosis factor alpha and risk of Alzheimer's disease and vascular dementia: a case-control study. Lancet 357: 436-9 (2001).
65. Griffin WS, Nicoll JA, Grimaldi LM, Sheng JG and Mrak RE. The pervasiveness of interleukin-1 in alzheimer pathogenesis: a role for specific polymorphisms in disease risk. Exp Gerontol 35: 481-7 (2000).
66. Espey MG, Kustova Y, Sei Y and Basile AS. Extracellular glutamate levels are chronically elevated in the brains of LP-BM5-infected mice: a mechanism of retrovirus-induced encephalopathy. J. Neurochem. 71: 2079-2087 (1998).
67. Bossuet C, Vaufrey F, Conde F, Chretien F, Pichon J, Hantraye P, et al. Up-regulation of glutamate concentration in the putamen and in the prefrontal cortex of asymptomatic SIVmac251-infected macaques without major brain involvement. J Neurochem 88: 928-38 (2004).
68. Mascarucci P, Perego C, Terrazzino S and De Simoni MG. Glutamate release in the nucleus tractus solitarius induced by peripheral lipopolysaccharide and interleukin-1 beta. Neuroscience 86: 1285-90 (1998).
69. Lipton SA. Similarity of neuronal cell injury and death in AIDS dementia and focal cerebral ischemia: potential treatment with NMDA open-channel blockers and nitric oxide-related species. Brain Pathol 6: 507-17 (1996).
70. Groom AJ, Smith T and Turski L. Multiple sclerosis and glutamate. Ann N Y Acad Sci 993: 229-75; discussion 287-8 (2003).
71. Griffin WS, Sheng JG, Roberts GW and Mrak RE. Interleukin-1 expression in different plaque types in Alzheimer's disease: significance in plaque evolution. J Neuropathol Exp Neurol 54: 276-281 (1995).
72. Mayeux R, Ottman R, Maestre G, Ngai C, Tang MX, Ginsberg H, et al. Synergistic effects of traumatic head injury and apolipoprotein-ε4 in patients with Alzheimer's disease. Neurology 45: 555-557 (1995).
73. Nicoll JR, Roberts GW and Graham DI. Apolipoprotein E ε4 allele is associated with deposition of amyloid β-protein following head injury. Nat Med 1: 135-137 (1995).
74. Sheng JG, Boop FA, Mrak RE and Griffin WS. Increased neuronal β-amyloid precursor protein expression in human temporal lobe epilepsy: association with interleukin-1α immunoreactivity. J Neurochem 63: 1872-1879 (1994).
75. Giometto B, An SF, Groves M, Scaravilli T, Geddes JF, Miller R, et al. Accumulation of beta-amyloid precursor protein in HIV encephalitis: relationship with neuropsychological abnormalities. Ann Neurol 42: 34-40 (1997).
76. Stanley LC, Mrak RE, Woody RC, Perrot LJ, Zhang S, Marshak DR, et al. Glial cytokines as neuropathogenic factors in HIV infection: pathogenic similarities to Alzheimer's disease. J Neuropathol Exp Neurol 53: 231-8. (1994).
77. Furukawa K, Sopher BL, Rydel RE, Begley JG, Pham DG, Martin GM, et al. Increased activity-regulating and neuroprotective efficacy of α-secretase-derived secreted amyloid precursor protein conferred by a c-terminal heparin-binding domain. J. Neurochem. 67: 1882-1896 (1996).