Age-dependent memory loss, synaptic pathology and altered brain plasticity in the Drosophila mutant cardinal accumulating 3-hydroxykynurenine

Journal of Neural Transmission

Volumn 107, Issue 5, 2000, Pages 581-601

  Savvateeva, E ^a,b   Popov, A ^c   Kamyshev, N ^b   Bragina, J ^b   Heisenberg, M ^d   Senitz, D ^a   Kornhuber, J ^a,e   Riederer, P ^a  

^a UNIVERSITY OF WÜRZBURG   (Germany)

^b PAVLOV INSTITUTE OF PHYSIOLOGY   (Russian Federation)

^c SECHENOV INSTITUTE OF EVOLUTIONARY PHYSIOLOGY AND BIOCHEMISTRY   (Russian Federation)

^d UNIVERSITY OF WÜRZBURG   (Germany)

^e UNIVERSITY OF GÖTTINGEN   (Germany)

Author keywords

3 hydroxykynurenine; Ageing; Brain plasticity; Conditioned courtship suppression; Drosophila; Glia; Kynurenic acid; Synaptic pathology

Indexed keywords

3 HYDROXYKYNURENINE; CYSTEINE; GLUTAMIC ACID; KYNURENIC ACID; TRYPTOPHAN;

AMNESIA; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; DEGENERATIVE DISEASE; DROSOPHILA; FEMALE; GLIA CELL; LEARNING; MALE; MEMORY; MUTANT; NERVE CELL PLASTICITY; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; SYNAPSE;

EID: 0034021444     PISSN: 03009564     EISSN: None     Source Type: Journal    
DOI: 10.1007/s007020070080     Document Type: Article

References (109)

1. Alberati-Giani D, Buchli R, Malherbe P, Broger C, Lang G, Köhler C, Lahm H-W, Cesura AM (1996) Isolation and expression of a cDNA clone encoding human kynureninase. Eur J Biochem 239: 460-468
2. Arendt T, Brückner MK, Bigl V, Marcova L (1995a) Dendritic reorganization in the basal forebrain under degenerative conditions and its defects in Alzheimer's disease. I. Dendritic reorganization of the normal human basal forebrain. J Comp Neurol 351: 169-188
3. Arendt T, Brückner MK, Bigl V, Marcova L (1995b) Dendritic reorganization in the basal forebrain under degenerative conditions and its defects in Alzheimer's disease. II. Ageing, Korsakoff's disease, Parkinson's disease, and Alzheimer's disease. J Comp Neurol 351: 189-222
4. Balling A, Technau GM, Heisenberg M (1987) Are the structural changes in adult Drosophila mushroom bodies memory traces? Studies on biochemical learning mutants. J Neurogenet 4: 65-73
5. Banfi S, Borsani G, Rossi E, Bernard L, Guffanti A, Rubboli F, Marchitiello A, Giglio S, Coluccia E, Zollo M, Zuffardi O, Ballabio A (1996) Identification and mapping of human cDNAs homologous to Drosophila mutant genes through EST database searching. Nature Genet 13: 167-174
6. Barth M, Heisenberg M (1997) Vision affect mushroom bodies and central complex in Drosophila melanogaster. Learning and Memory 4(2): 219-229
7. Beal MF (1995) Aging, energy, and oxidative stress in neurodegenerative diseases. Ann Neurol 38: 357-366
8. Betz H, Schuster C, Ultsch A, Schmitt B (1993) Molecular biology of ionotropic glutamate receptors in Drosophila melanogaster. Trends Pharm Sci 14: 428-431
9. Birch PJ, Grossman CJ, Hayes AG (1988) Kynurenate and FG9041 have both competitive and noncompetitive antagonist actions at excitatory amino acid receptors. Eur J Pharmacol 151: 313-315
10. Blennow K, Bogdanovic N, Alafuzoff I, Ekman R, Davidson P (1996) Synaptic pathology in Alzheimer's disease: relation to severity of dementia, but not to senile plaques, neurofibrillary tangles or the ApoE4 allele. J Neural Transm 103: 603-618
11. Bolger G, Michaeli T, Martins T, St John T, Steiner B, Rodgers L, Riggs M, Wigler M, Ferguson K (1993) A family of human phosphodiesterases homologous to the dunce learning and memory gene product of Drosophila melanogaster are potential targets for antidepressant drugs. Mol Cell Biol 13: 6558-6571
12. Boulianne GL, Livne-Bar I, Humphreys JM, Liang Y, Lin C, Rogaev E, George-Hyslop P (1997) Cloning and characterization of the Drosophila presenilin homologue. Neuroreport 8: 1025-1029
13. Buchli R, Alberati-Giani D, Malherbe P, Kohler C, Broger C, Cesura AM (1995) Cloning and functional expression of a soluble form of kynurenine/alpha-aminoadipate aminotransferase from rat kidney. J Biol Chem 270: 29330-29335
14. Buchnan RL, Benzer S (1993) Defective glia in the Drosophila brain degeneration mutant drop dead. Neuron 10: 839-850
15. Buchner E, Gundersen CB (1997) The DnaJ-like cysteine string protein and exocytotic neurotransmitter release. Trends Neurosci 20: 223-227
16. Buchner E, Bader R, Buchner S, Cox J, Emson PC, Flory E, Heizmann CW, Hemm S, Hofbauer A, Oertel WH (1988) Cell-specific immuno-probes for the brain of normal and mutant Drosophila melanogaster. I. Wildtype visual system. Cell Tissue Res 253: 357-370
17. Ceresoli G, Guidetti P, Schwarcz R (1997) Metabolism of [5-(3)H]kynurenine in the developing rat brain in vivo: effect of intrastriatal ibotenate injections. Brain Res Dev Brain Res 100: 73-81
18. Chiarugi A, Carpenedo R, Molina MT, Mattoli L, Pellicciari R, Moroni F (1995) Comparison of the neurochemical and behavioral effects resulting from the inhibition of kynurenine hydroxylase and/or kynureninase. J Neurochem 65: 1176-1183
19. Coppola T, Gundersen CB (1996) Widespread expression of human cysteine string proteins. FEBS Lett 391: 269-272
20. Davidsson P, Blennow K (1998) Neurochemical dissection of synaptic pathology in Alzheimer's disease. Int Psychogeriatr 10: 11-23
21. Davis RL, Dauwalder B (1991) The Drosophila dunce locus: learning and memory genes in the fly. Trends Genet 7: 224-229
22. deBelle JS (1995) Drosophila mushroom body subdomains: innate or learned representations of odor preference and sexual orientation? Neuron 15: 245-247
23. deBelle JS, Heisenberg M (1994) Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263: 692-695
24. DiAntonio A, Burgess RW, Chin AC, Deitcher DL, Scheller RH, Schwarz TL (1993) Identification and characterization of Drosophila genes for synaptic vesicle proteins. J Neurosci 13: 4924-4935
25. Eastman CL, Guilarte TR (1989) Cytotoxicity of 3-hydroxykynurenine in a neuronal hybrid cell line. Brain Res 495: 225-231
26. Eberle KK, Zinsmaier KE, Buchner S, Gruhn M, Jenni M, Arnold C, Leibold C, Reisch D, Walter N, Hafen E, Hofbauer A, Pflugfelder GO, Buchner E (1998) Wide distribution of the cysteine string proteins in Drosophila tissues revealed by targeted mutagenesis. Cell Tissue Res 294: 203-217
27. Fahrbach SE, Giray T, Robinson GE (1995) Volume changes in the mushroom bodies of adult honey bee queens. Neurobiol Learn Mem 63: 181-191
28. Fahrbach SE, Giray T, Farris SM, Robinson GE (1997) Expansion of the neuropil of the mushroom bodies in male honey bees is coincident with initiation of flight. Neurosci Lett 236: 135-138
29. Feany M, Quinn WG (1995) A neuropeptide gene defined by the Drosophila memory mutant amnesiac. Science 268: 869-873
30. Ferré J (1983) Accumulation of kynurenic acid in the cinnabar mutant of Drosophila melanogaster as revealed by thin-layer chromatography. Insect Biochem 13: 289-294
31. Ferré J, Real MD, Mensua JL, Jacobson KB (1985) Xanthurenic acid 8-O-β-D-glucoside, a novel tryptophan metabolite in eye-color mutants of Drosophila melanogaster. J Biol Chem 260: 7509-7514
32. Ferveur J-F (1997) The pheromomal role of cuticular hydrocarbons in Drosophila melanogaster. BioEssays 19: 353-358
33. Gailey DA, Jackson FR, Siegel RW (1984) Conditioned mutations in Drosophila melanogaster affect an experience-dependent behavioral modification in courting males. Genetics 106: 613-623
34. Gasic G (1995) Systems and molecular genetic approaches converge to tackle learning and memory. Neuron 15: 507-512
35. Gerlach M, Riederer P (1996) Animal models of Parkinson's disease: an empirical comparison with the phenomenology of the disease in man. J Neural Transm 103: 987-1041
36. Ghosh D, Forrest HS (1967) Enzymatic studies on the hydroxylation of kynurenine in Drosophila melanogaster. Genetics 55: 423-431
37. Gramsbergen JB, Schmidt W, Turski WA, Schwarcz R (1992) Age-related changes in kynurenic acid production in rat brain. Brain Res 588: 1-5
38. Gronenberg W, Heeren S, Hölldobler B (1996) Age-dependent and task-related morphological changes in the brain and the mushroom bodies of the ant Camponotus floridanus. J Exp Biol 199: 2011-2019
39. 3H] kynurenine in the rat brain in vivo: evidence for existence of a functional kynurenine pathway. J Neurochem 65: 2621-2632
40. Halter DA, Urban J, Rickert C, Ner SS, Ito K, Travers AA, Technau GM (1995) The homeobox gene repo is required for the differentiation and maintenance of glia function in the embryonic nervous system of Drosophila melanogaster. Development 121: 317-332
41. Hartley D (1996) Drosophila inherit diseases. Nature Genet 13: 133-134
42. Heinonen O, Soininen H, Sorvari H, Kosunen O, Paljärvi L, Koivisto E, Riekkinen PJ Sr (1995) Loss of synaptophysin-like immunoreactivity in the hippocampal formation is an early phenomenon in Alzheimer's disease. Neurosci 64: 375-384
43. Heisenberg M (1994) Central brain function in insects: genetic studies on the mushroom bodies and central complex in Drosophila. Fortschr Zool 39: 30-39
44. Heisenberg M, Böhl K (1979) Isolation of anatomical brain mutants of Drosophila by histological means. Z Naturforsch 34c: 143-147
45. Heisenberg M, Borst A, Wagner S, Byers D (1985) Drosophila mushroom body mutants are deficient in olfactory learning. J Neurogenet 2: 1-30
46. Heisenberg M, Heusipp M, Wanke T (1995) Structural plasticity in the Drosophila brain. J Neurosci 15: 1951-1960
47. Hicks RR, Smith DH, Gennarelli TA, McIntosh T (1994) Kynurenate is neuroprotective following experimental brain injury in the rat. Brain Res 655: 91-96
48. Holmes WR (1989) The role of dendritic diameters in maximizing the effectiveness of synaptic inputs. Brain Res 478: 127-137
49. Hong CS, Koo EH (1997) Isolation and characterization of Drosophila presenilin homolog. Neuroreport 8: 665-668
50. Howells AJ, Summers KM, Ryall RL (1977) Developmental patterns of 3-hydroxykynurenine accumulation in white and various other eye color mutants of Drosophila melanogaster. Biochem Genet 15: 1049-1059
51. Ito K, Awano W, Suzuki K, Hiromi Y, Yamamoto D (1997) The Drosophila mushroom body is a quadruple structure of clonal units each of which contains a virtually identical set of neurons and glial cells. Development 124: 761-771
52. Jaffe K, Blanco ME (1994) Involvement of amino acids, opiods, nitric oxide, and NMDA receptors in learning and memory consolidation in crickets. Pharmacol Biochem Behav 47: 493-496
53. Kamyshev NG (1980) Longevity and its relation to the locomotor activity in tryptophan-xanthommatin metabolic pathway mutants of Drosophila. Dokl Akad Nauk USSR 253: 1476-1480
54. Kamyshev NG, Iliadi KG, Bragina JV (1999) Drosophila conditioned courtship: two approaches to test memory. Learning and Memory 6: 1-20
55. Kandel E, Abel T (1995) Neuropeptides, adenylyl cyclase, and memory storage. Science 268: 825-826
56. Kemp JA, Leeson PD (1993) The glycine site of the NMDA receptor - five years on. Trends Pharm Sci 14: 20-25
57. Kucharczyk R, Zagulski M, Rytka J, Herbert CJ (1998) The yeast gene YJR025c encodes a 3-hydroxyanthranilic acid dioxygenase and is involved in nicotinic acid biosynthesis. FEBS Lett 424: 127-130
58. Li J, Li G (1997) Transamination of 3-hydroxykynurenine to produce xanthurenic acid: a major branch pathway of tryptophan metabolism in the mosquito, Aedes aegypti, during larval development. Insect Biochem Mol Biol 27: 859-867
59. Lints FA (1988) Aim and scope of Drosophila ageing research. In: Lints FA, Soliman MH (eds) Drosophila as a model organism for ageing studies. Blakie, Glasgow London pp3-16
60. Linzen B (1974) Tryptophan - ommochrome pathway in insects. Adv Insect Physiol 10: 117-246
61. Liu X, Erikson C, Brun A (1996) Cortical synaptic changes and gliosis in normal aging, Alzheimer's disease and frontal lobe degeneration. Dementia 7: 128-134
62. Lopatina NG, Ponomarenko VV, Chesnokova EG (1992) The conditioned reflex in biology and genetics of behavior. Sechenov Physiol J 79: 36-47
63. Luo L, Tully T, White K (1992) Human amyloid precusor protein ameliorates behavioral deficit of flies deleted for Appl gene. Neuron 9: 595-605
64. Maher P, Davis JB (1996) The role of monoamine metabolism in oxidative glutamate toxicity. J Neurosci 16: 6394-6401
65. Masliah E (1995) Mechanisms of synaptic dysfunction in Alzheimer's disease. Histol Histopathol 10: 509-519
66. Masliah E, Mallory M, Hansen L, DeTeresa R, Alford M, Terry R (1994) Synaptic and neuritic alterations during the progression of Alzheimer's disease. Neurosci Lett 174: 67-72
67. Min KT, Benzer S (1997) Spongecake and eggroll: two hereditary diseases in Drosophila resemble patterns of human brain degeneration. Curr Biol 7: 885-888
68. Mirmiran M, van Someren EJ, Swaab DF (1996) Is brain plasticity preserved during aging and in Alzheimer's disease? Behav Brain Res 78: 43-48
69. Moroni F (1999) Tryptophan metabolism and brain function: focus on kynurenine and other indole metabolites. Eur J Pharmacol 375: 87-100
70. Moroni F, Alesiani M, Facci L, Fadda E, Skarper SD, Galli A, Lombardi G, Mori F, Ciuffi M, Natalini P, Pellicciari R (1992) Thiokynuranates prevent excitotoxic neuronal death in vitro and in vivo by acting as glycine antagonists and as inhibitors of lipid peroxidation. Eur J Pharmacol 218: 145-151
71. Morrison JH, Hof HR (1997) Life and death of neurons in the aging brain. Science 278: 412-419
72. Nakagami Y, Saito H, Katsuki H (1996) 3-Hydroxylkynurenine toxicity on the rat striatum in vivo. Jpn J Pharmacol 71: 183-186
73. O'Dell KM, Armstrong JD, Yang MY, Kaiser K (1995) Functional dissection of the Drosophila mushroom bodies by selective feminization of genetically defined subcompartments. Neuron 15: 55-61
74. Orr WC (1996) Senescence: in search of casualty. Dev Genet 18: 93-98
75. Okuda S, Nishiyama N, Saito H, Katsuki H (1996) Hydrogen peroxide-mediated neuronal cell death induced by an endogenous neurotoxin, 3-hydroxykynurenine. Proc Natl Acad Sci USA 93: 12553-12558
76. Okuda S, Nishiyama N, Saito H, Katsuki H (1998) 3-Hydroxykynurenine, an endogenous oxidative stress generator, causes neuronal cell death with apoptotic features and region selectivity. J Neurochem 70: 299-307
77. Pearson SJ, Reynolds GP (1992) Increased brain concentrations of a neurotoxin, 3-hydroxykynurenine, in Huntington's disease. Neurosci Lett 144: 199-201
78. Pellegrini-Giampietro DE, Cozzi A, Moroni F (1994) The glycine antagonist and free radical scavenger 7-Cl-thio-kynuranate reduces CA1 ischemic damage in the gerbil. Neurosci 63: 701-709
79. Pfrieger F, Barres BA (1995) What the fly's glia tell the fly's brain. Cell 83: 671-674
80. Pfrieger F, Barres BA (1997) Synaptic efficacy enhanced by glial cells in vitro. Science 277: 1684-1687
81. Phillips JP, Forrest HS, Kulkarni AD (1973) Terminal synthesis of xanthommatin in Drosophila melanogaster. III. Mutational pleiotropy and pigment granule association of phenoxazinone synthetase. Genetics 73: 45-56
82. Quinn WG, Harris WA, Benzer S (1974) Conditioned behavior in Drosophila melanogaster. Proc Natl Acad Sci USA 71: 708-712
83. Real MD, Ferré J (1989) Distribution of xanthurenic acid glucoside in species of the genus Drosophila. Insect Biochem 19: 111-115
84. Real MD, Ferré J (1991) Analysis of kynurenine transaminase activity in Drosophila by high performance liquid chromatography. Insect Biochem 6: 647-652
85. Ryall RL, Howells AJ (1974) Ommochrome biosynthetic pathway of Drosophila melanogaster: variations in levels of enzyme activities and intermediates during adult development. Insect Biochem 4: 47-61
86. Sardar AM, Bell JE, Reynolds GP (1995) Increased concentrations of the neurotoxin 3-hydroxykynurenine in the frontal cortex of HIV-1-positive patients. J Neurochem 64: 932-935
87. Sagara Y, Dargusch R, Chambers D, Davis J, Schubert D, Maher P (1998) Cellular mechanisms of resistance to chronic oxidative stress. Free Radic Biol Med 24: 1375-1389
88. Savvateeva E (1977) Comparative study of learning ability in Drosophila strains selected on neurophysiologic characters and in mutants. Dokl Acad Nauk USSR 235: 1430-1432
89. Savvateeva E (1991) Kynurenines in the regulation of behavior in insects. Adv Exp Med Biol 294: 319-328
90. Savvateeva EV, Popov AV, Kamyshev NG, Iliadi KG, Bragina JV, Heisenberg M, Kornhuber J, Riederer P (1999) Age-dependent changes in memory and mushroom bodies in the Drosophila mutant vermilion deficient in the kynurenine pathway of tryptophan metabolism. Ross Fiziol Zh Im I M Sechenova 85: 167-183
91. Siegel RW, Hall JC (1979) Conditioned responses in courtship behavior of normal and mutant Drosophila. Proc Natl Acad Sci USA 76: 3430-3434
92. Smith DH, Okiyama K, Thomas MJ, McIntosh TK (1993) Effects of the excitatory amino acid receptor antagonists kynurenate and indole-2-carboxylic acid on behavioral and neurochemical outcome following experimental brain injury. J Neurosci 13: 5383-5392
93. Sokal RR, Rohlf FJ (1995) Biometry, 3rd edn. Freeman WH & Co, New York, pp 803-820
94. StatSoft 5.0 (1995) STATISTICA for Windows [Computer program manual]. StatSoft, Inc, Tulsa, OK
95. Stone TW, Connick JH (1985) Quinolinic acid and other kynurenines in the central nervous system. Neurosci 15: 597-617
96. Südhof TC, Baumert M, Perin MS, Jahn R (1989) A synaptic vesicle membrane protein is conserved from mammals to Drosophila. Neuron 2: 1475-1481
97. Sullivan DT, Grillo SL, Kitos RJ (1974) Subcellular localization of the first free enzymes of the ommochrome synthetic pathway in Drosophila melanogaster. J Exp Zool 188: 225-233
98. Summers KM, Howells AJ, Pyliotis NA (1982) Biology of eye pigmentation in insects. Adv Insect Physiol 16: 119-167
99. Technau GM (1984) Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience. J Neurogenet 1: 113-126
100. Tohgi H, Abe T, Takahashi S, Kimura M, Takahashi J, Kikuchi T (1992) Concentrations of serotonin and its related substances in the cerebrospinal fluid in patients with Alzheimer type dementia. Neurosci Lett 141: 9-12
101. Tohgi H, Abe T, Takahashi S, Takahashi J, Hamato H (1993) Concentration of serotonin and its related substances in the cerebrospinal fluid of Parkinsonian patients and their relations to the severity of symptoms. Neurosci Lett 150: 71-74
102. Tully T, Quinn WG (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A Sens Neural Behav Physiol 157: 263-277
103. Ultsch A, Schuster CM, Laube B, Schloss P, Schmitt B, Betz H (1992) Glutamate receptors of Drosophila melanogaster: cloning of a kainate-selective subunit expressed in the central nervous system. Proc Natl Acad Sci USA 89: 10484-10488
104. Ultsch A, Schuster C, Laube B, Betz H, Schmitt B (1993) Glutamate receptors of Drosophila melanogaster. Primary structure of a putative NMDA receptor protein expressed in the head of the adult fly. FEBS 324: 171-177
105. Umbach JA, Zinsmaier KE, Eberle KK, Buchner E, Benzer S, Gundersen CB (1994) Presynaptic dysfunction in Drosophila csp mutants. Neuron 13: 899-907
106. Warren WD, Palmer S, Howells AJ (1996) Molecular characterization of the cinnabar region of Drosophila melanogaster: identification of the cinnabar transcription unit. Genetica 98: 249-262
107. Zawistowski S (1988) A replication demonstrating reduced courtship of Drosophila melanogaster by associative learning. J Comp Psychol 102: 174-176
108. Zhan SS, Beyruether K, Schmitt HP (1993) Quantitative assessment of the synaptophysin immuno-reactivity of the cortical neuropil in various neurodegenerative disorders with dementia. Dementia 4: 66-74
109. Zinsmaier KE, Hofbauer A, Heimbeck G, Pflugfelder GO, Buchner S, Buchner E (1990) A cysteine string protein is expressed in retina and brain of Drosophila. J Neurogenet 7: 15-29