Presynaptic plasticity and associative learning are impaired in a Drosophila presenilin null mutant

Developmental Neurobiology

Volumn 67, Issue 12, 2007, Pages 1598-1613

  Knight, David ^a   Iliadi, Konstantin ^a   Charlton, Milton P ^b   Atwood, Harold L ^b   Boulianne, Gabrielle L ^a,c  

^a HOSPITAL FOR SICK CHILDREN   (Canada)

^b UNIVERSITY OF TORONTO   (Canada)

^c UNIVERSITY OF TORONTO   (Canada)

Author keywords

Alzheimer's disease; Behavior; Drosophila melanogaster; Larvae; Motor neurons; Neuromuscular junction

Indexed keywords

ALZHEIMER DISEASE; ANIMAL EXPERIMENT; ANIMAL MODEL; ANIMAL TISSUE; ARTICLE; COGNITIVE DEFECT; CONTROLLED STUDY; DROSOPHILA; GENE; GENE MUTATION; MEMORY DISORDER; MOTONEURON; NERVE CELL PLASTICITY; NEUROMUSCULAR SYNAPSE; NONHUMAN; POST TETANIC POTENTIATION; PRIORITY JOURNAL; PROTEIN FUNCTION; PSN GENE; SMELLING; STATE DEPENDENT LEARNING; SYNAPSE VESICLE; TRANSGENE; VISION;

ACTION POTENTIALS; ANIMALS; ANIMALS, GENETICALLY MODIFIED; ASSOCIATION LEARNING; BLOTTING, WESTERN; DROSOPHILA; ELECTROPHYSIOLOGY; FEMALE; GENE EXPRESSION; IMMUNOHISTOCHEMISTRY; MALE; MUTATION; NEUROMUSCULAR JUNCTION; NEURONAL PLASTICITY; NEUROTRANSMITTER AGENTS; PRESENILINS; PRESYNAPTIC TERMINALS; SYNAPTIC TRANSMISSION; SYNAPTIC VESICLES;

EID: 34848875120     PISSN: 19328451     EISSN: 1932846X     Source Type: Journal    
DOI: 10.1002/dneu.20532     Document Type: Article

References (59)

1. Beglopoulos V, Sun X, Saura CA, Lemere CA, Kim RD, Shen J. 2004. Reduced β-amyloid production and increased inflammatory responses in presenilin conditional knock-out mice. J Biol Chem 279:46907-46914.
2. Boulianne GL, Livne-Bar I, Humphreys JM, Liang Y, Lin C, Rogaev E, St George-Hyslop P. 1997. Cloning and characterization of the Drosophila presenilin homologue. Neuroreport 8:1025-1029.
3. Brand AH, Perrimon N. 1993. Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118:401-415.
4. Brumback AC, Lieber JL, Angleson JK, Betz WJ. 2004. Using FM1-43 to study neuropeptide granule dynamics and exocytosis. Methods 33:287-294.
5. Cavener DR. 1987. Comparison of the consensus sequence flanking translational start sites in Drosophila and vertebrates. Nucleic Acids Res 15:1353-1361.
6. de Belle JS, Heisenberg M. 1994. Associative odor learning in Drosophila abolished by chemical ablation of mushroom bodies. Science 263:692-695.
7. Durand J, Kojic L, Wang Y, Lee P, Cynader MS, Gu Q. 2000. Confocal imaging of N-methyl-D-aspartate receptors in living cortical neurons. Neuroscience 97:11-23.
8. Feeney CJ, Karunanithi S, Pearce J, Govind CK, Atwood HL. 1998. Motor nerve terminals on abdominal muscles in larval flesh flies, Sarcophaga bullata: Comparisons with Drosophila. J Comp Neurol 402:197-209.
9. Francis YI, Stephanou A, Latchman DS. 2006. CREB-binding protein activation by presenilin 1 but not by its M146L mutant. Neuroreport 17:917-921.
10. Gerber B, Scherer S, Neuser K, Michels B, Hendel T, Stocker RF, Heisenberg M. 2004. Visual learning in individually assayed Drosophila larvae. J Exp Biol 207:179-188.
11. Golde TE. 2005. The Abeta hypothesis: Leading us to rationally-designed therapeutic strategies for the treatment or prevention of Alzheimer disease. Brain Pathol 15:84-87.
12. Gong B, Cao Z, Zheng P, Vitolo OV, Liu S, Staniszewski A, Moolman D, et al. 2006. Ubiquitin hydrolase Uch-L1 rescues β-amyloid-induced decreases in synaptic function and contextual memory. Cell 126:775-788.
13. Guo Y, Livne-Bar I, Zhou L, Boulianne GL. 1999. Drosophila presenilin is required for neuronal differentiation and affects notch subcellular localization and signaling. J Neurosci 19:8435-8442.
14. Hardy J, Selkoe DJ. 2002. The amyloid hypothesis of Alzheimer's disease: Progress and problems on the road to therapeutics. Science 297:353-356.
15. Hoang B, Chiba A. 2001. Single-cell analysis of Drosophila larval neuromuscular synapses. Dev Biol 229:55-70.
16. Hong CS, Koo EH. 1997. Isolation and characterization of Drosophila presenilin homolog. Neuroreport 8:665-668.
17. Hutton M, Hardy J. 1997. The presenilins and Alzheimer's disease. Hum Mol Genet 6:1639-1646.
18. Hwang DY, Chae KR, Kang TS, Hwang JH, Lim CH, Kang HK, Goo JS, et al. 2002. Alterations in behavior, amyloid β-42, caspase-3, and Cox-2 in mutant PS2 transgenic mouse model of Alzheimer's disease. FASEB J 16:805-813.
19. Jan LY, Jan YN. 1976. L-glutamate as an excitatory transmitter at the Drosophila larval neuromuscular junction. J Physiol 262:215-236.
20. Karunanithi S, Marin L, Wong K, Atwood HL. 2002. Quantal size and variation determined by vesicle size in normal and mutant Drosophila glutamatergic synapses. J Neurosci 22:10267-10276.
21. Kasa P, Papp H, Pakaski M. 2001. Presenilin-1 and its N-terminal and C-terminal fragments are transported in the sciatic nerve of rat. Brain Res 909:159-169.
22. Kuromi H, Kidokoro Y. 1998. Two distinct pools of synaptic vesicles in single presynaptic boutons in a temperature-sensitive Drosophila mutant, shibire. Neuron 20:917-925.
23. Kuromi H, Kidokoro Y. 2000. Tetanic stimulation recruits vesicles from reserve pool via a cAMP- mediated process in Drosophila synapses. Neuron 27:133-143.
24. Kuromi H, Kidokoro Y. 2002. Selective replenishment of two vesicle pools depends on the source of Ca2+ at the Drosophila synapse. Neuron 35:333-343.
25. Lalonde R, Qian S, Strazielle C. 2003. Transgenic mice expressing the PS1-A246E mutation: Effects on spatial learning, exploration, anxiety, and motor coordination. Behav Brain Res 138:71-79.
26. Lnenicka GA, Keshishian H. 2000. Identified motor terminals in Drosophila larvae show distinct differences in morphology and physiology. J Neurobiol 43:186-197.
27. Lukinova NI, Roussakova VV, Fortini ME. 1999. Genetic characterization of cytological region 77A-D harboring the presenilin gene of Drosophila melanogaster. Genetics 153:1789-1797.
28. Macleod GT, Hegstrom-Wojtowicz M, Charlton MP, Atwood HL. 2002. Fast calcium signals in Drosophila motor neuron terminals. J Neurophysiol 88:2659-2663.
29. Marjaux E, Hartmann D, De Strooper B. 2004. Presenilins in memory, Alzheimer's disease, and therapy. Neuron 42:189-192.
30. McLachlan EM, Martin AR. 1981. Non-linear summation of end-plate potentials in the frog and mouse. J Physiol 311:307-324.
31. Medina M, Dotti CG. 2003. RIPped out by presenilin-dependent γ-secretase. Cell Signal 15:829-841.
32. Morton RA, Kuenzi FM, Fitzjohn SM, Rosahl TW, Smith D, Zheng H, Shearman M, et al. 2002. Impairment in hippocampal long-term potentiation in mice under-expressing the Alzheimer's disease related gene presenilin-1. Neurosci Lett 319:37-40.
33. Nowotny P, Gorski SM, Han SW, Philips K, Ray WJ, Nowotny V, Jones CJ, et al. 2000. Posttranslational modification and plasma membrane localization of the Drosophila melanogaster presenilin. Mol Cell Neurosci 15:88-98.
34. Parent A, Linden DJ, Sisodia SS, Borchelt DR. 1999. Synaptic transmission and hippocampal long-term potentiation in transgenic mice expressing FAD-linked presenilin 1. Neurobiol Dis 6:56-62.
35. Presente A, Boyles RS, Serway CN, de Belle JS, Andres AJ. 2004. Notch is required for long-term memory in Drosophila. Proc Natl Acad Sci USA 101:1764-1768.
36. Richards JG, Higgins GA, Ouagazzal AM, Ozmen L, Kew JN, Bohrmann B, Malherbe P, et al. 2003. PS2APP transgenic mice, coexpressing hPS2mut and hAPPswe, show age-related cognitive deficits associated with discrete brain amyloid deposition and inflammation. J Neurosci 23:8989-9003.
37. Rocchi A, Pellegrini S, Siciliano G, Murri L. 2003. Causative and susceptibility genes for Alzheimer's disease: A review. Brain Res Bull 61:1-24.
38. Roche JP, Westenbroek R, Sorom AJ, Hille B, Mackie K, Shapiro MS. 2002. Antibodies and a cysteine-modifying reagent show correspondence of M current in neurons to KCNQ2 and KCNQ3 K+ channels. Br J Pharmacol 137:1173-1186.
39. Rosen DR, Martin-Morris L, Luo LQ, White K. 1989. A Drosophila gene encoding a protein resembling the human beta-amyloid protein precursor. Proc Natl Acad Sci USA 86:2478-2482.
40. Rubin GM, Spradling AC. 1982. Genetic transformation of Drosophila with transposable element vectors. Science 218:348-353.
41. Saura CA, Choi SY, Beglopoulos V, Malkani S, Zhang D, Shankaranarayana Rao BS, Chattarji S, et al. 2004. Loss of presenilin function causes impairments of memory and synaptic plasticity followed by age-dependent neurodegeneration. Neuron 42:23-36.
42. Sawin-McCormack EP, Sokolowski MB, Campos AR. 1995. Characterization and genetic analysis of Drosophila melanogaster photobehavior during larval development. J Neurogenet 10:119-135.
43. Scherer S, Stocker RF, Gerber B. 2003. Olfactory learning in individually assayed Drosophila larvae. Learn Mem 10:217-225.
44. Selkoe DJ. 2001. Alzheimer's disease: Genes, proteins, and therapy. Physiol Rev 81:741-766.
45. Siwicki KK, Ladewski L. 2003. Associative learning and memory in Drosophila: Beyond olfactory conditioning. Behav Processes 64:225-238.
46. Sokolowski MB, Kent C, Wong J. 1984. Drosophila larval foraging behavior: Developmental stages. Animal Behav 32:645-651.
47. Tanzi RE, Bertram L. 2005. Twenty years of the Alzheimer's disease amyloid hypothesis: A genetic perspective. Cell 120:545-555.
48. Trinchese F, Liu S, Battaglia F, Walter S, Mathews PM, Arancio O. 2004. Progressive age-related development of Alzheimer-like pathology in APP/PS1 mice. Ann Neurol 55:801-814.
49. Vautrin J, Barker JL. 2003. Presynaptic quantal plasticity: Katz's original hypothesis revisited. Synapse 47:184-199.
50. Verdile G, Fuller S, Atwood CS, Laws SM, Gandy SE, Martins RN. 2004. The role of beta amyloid in Alzheimer's disease: Still a cause of everything or the only one who got caught? Pharmacol Res 50:397-409.
51. Wang R, Dineley KT, Sweatt JD, Zheng H. 2004. Presenilin 1 familial Alzheimer's disease mutation leads to defective associative learning and impaired adult neurogenesis. Neuroscience 126:305-312.
52. Wolf R, Wittig T, Liu L, Wustmann G, Eyding D, Heisenberg M. 1998. Drosophila mushroom bodies are dispensable for visual, tactile, and motor learning. Learn Mem 5:166-178.
53. Ye Y, Fortini ME. 1998. Characterization of Drosophila Presenilin and its colocalization with Notch during development. Mech Dev 79:199-211.
54. Ye Y, Lukinova N, Fortini ME. 1999. Neurogenic phenotypes and altered Notch processing in Drosophila Presenilin mutants. Nature 398:525-529.
55. Yeh E, Gustafson K, Boulianne GL. 1995. Green fluorescent protein as a vital marker and reporter of gene expression in Drosophila. Proc Natl Acad Sci USA 92:7036-7040.
56. Yu H, Saura CA, Choi SY, Sun LD, Yang X, Handler M, Kawarabayashi T, et al. 2001. APP processing and synaptic plasticity in presenilin-1 conditional knockout mice. Neuron 31:713-726.
57. Zaman SH, Parent A, Laskey A, Lee MK, Borchelt DR, Sisodia SS, Malinow R. 2000. Enhanced synaptic potentiation in transgenic mice expressing presenilin 1 familial Alzheimer's disease mutation is normalized with a benzodiazepine. Neurobiol Dis 7:54-63.
58. Zars T. 2000. Behavioral functions of the insect mushroom bodies. Curr Opin Neurobiol 10:790-795.
59. Zucker RS. 1989. Short-term synaptic plasticity. Annu Rev Neurosci 12:13-31.