Debra, a protein mediating lysosomal degradation, is required for long-term memory in Drosophila

PLoS ONE

Volumn 6, Issue 10, 2011, Pages

  Kottler, Benjamin ^a,b   Aurélie Lampin Saint Amaux, Daniel Comas ^a   Comas, Daniel ^a,c   Preat, Thomas ^a   Goguel, Valérie ^a  

^a CNRS   (France)

^b UNIVERSITY OF QUEENSLAND   (Australia)

^c Galapagos   (France)

Author keywords

[No Author keywords available]

Indexed keywords

DROSOPHILA PROTEIN; SONIC HEDGEHOG PROTEIN; TRANSCRIPTION FACTOR GAL4; DEBRA PROTEIN, DROSOPHILA;

ANIMAL TISSUE; ARTICLE; CONTROLLED STUDY; DEBRA GENE; DROSOPHILA MELANOGASTER; GENE; GENE IDENTIFICATION; GENE INSERTION; GENE OVEREXPRESSION; GENE SILENCING; LONG TERM MEMORY; LYSOSOME; MEMORY DISORDER; MUSHROOM BODY; MUTANT; NERVE CELL PLASTICITY; NONHUMAN; OLFACTORY MEMORY; PROTEIN DEGRADATION; PROTEIN SYNTHESIS; RNA INTERFERENCE; SIGNAL TRANSDUCTION; TRANSGENE; AGING; ANIMAL; ANIMAL BEHAVIOR; CYTOLOGY; ENHANCER REGION; GENE LOCUS; GENETICS; METABOLISM; MUTATION; PHYSIOLOGY;

BASIDIOMYCOTA; ERINACEIDAE; MAMMALIA;

AGING; ANIMALS; BEHAVIOR, ANIMAL; DROSOPHILA MELANOGASTER; DROSOPHILA PROTEINS; ENHANCER ELEMENTS, GENETIC; GENETIC LOCI; HEDGEHOG PROTEINS; LYSOSOMES; MEMORY, LONG-TERM; MUSHROOM BODIES; MUTATION; PROTEOLYSIS; RNA INTERFERENCE;

EID: 80053460836     PISSN: None     EISSN: 19326203     Source Type: Journal    
DOI: 10.1371/journal.pone.0025902     Document Type: Article

References (54)

1. Davis RL, (2005) Olfactory memory formation in Drosophila: from molecular to systems neuroscience. Annu Rev Neurosci 28: 275-302.
2. Tully T, Quinn WG, (1985) Classical conditioning and retention in normal and mutant Drosophila melanogaster. J Comp Physiol A 157: 263-277.
3. Pascual A, Preat T, (2001) Localization of long-term memory within the Drosophila mushroom body. Science 294: 1115-1117.
4. Tully T, Preat T, Boynton SC, Del Vecchio M, (1994) Genetic dissection of consolidated memory in Drosophila. Cell 79: 35-47.
5. Chabaud MA, Isabel G, Kaiser L, Preat T, (2009) Social facilitation of long-lasting memory retrieval in Drosophila. Curr Biol 19: 1654-1659.
6. Bailey CH, Kandel ER, (1993) Structural changes accompanying memory storage. Annu Rev Physiol 55: 397-426.
7. Costa-Mattioli M, Sonenberg N, (2008) Translational control of gene expression: a molecular switch for memory storage. Prog Brain Res 169: 81-95.
8. Yin JC, Tully T, (1996) CREB and the formation of long-term memory. Curr Opin Neurobiol 6: 264-268.
9. Perazzona B, Isabel G, Preat T, Davis RL, (2004) The role of cAMP response element-binding protein in Drosophila long-term memory. J Neurosci 24: 8823-8828.
10. Alberini CM, (2009) Transcription factors in long-term memory and synaptic plasticity. Physiol Rev 89: 121-145.
11. Benito E, Barco A, (2010) CREB's control of intrinsic and synaptic plasticity: implications for CREB-dependent memory models. Trends Neurosci 33: 230-240.
12. DeZazzo J, Sandstrom D, de Belle S, Velinzon K, Smith P, et al. (2000) nalyot, a mutation of the Drosophila myb-related Adf1 transcription factor, disrupts synapse formation and olfactory memory. Neuron 27: 145-158.
13. Copf T, Goguel V, Lampin-Saint-Amaux A, Scaplehorn N, Preat T, (2011) Cytokine signaling through the JAK/STAT pathway is required for long-term memory in Drosophila. Proc Natl Acad Sci U S A 108: 8059-8064.
14. Ge X, Hannan F, Xie Z, Feng C, Tully T, et al. (2004) Notch signaling in Drosophila long-term memory formation. Proc Natl Acad Sci U S A 101: 10172-10176.
15. 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 U S A 101: 1764-1768.
16. Dubnau J, Chiang AS, Grady L, Barditch J, Gossweiler S, et al. (2003) The staufen/pumilio pathway is involved in Drosophila long-term memory. Curr Biol 13: 286-296.
17. Comas D, Petit F, Preat T, (2004) Drosophila long-term memory formation involves regulation of cathepsin activity. Nature 430: 460-463.
18. Didelot G, Molinari F, Tchenio P, Comas D, Milhiet E, et al. (2006) Tequila, a neurotrypsin ortholog, regulates long-term memory formation in Drosophila. Science 313: 851-853.
19. Deshapriya RM, Takeuchi A, Shirao K, Isa K, Watabe S, et al. (2007) Drosophila CTLA-2-like protein (D/CTLA-2) inhibits cysteine proteinase 1 (CP1), a cathepsin L-like enzyme. Zoolog Sci 24: 21-30.
20. Berry J, Krause WC, Davis RL, (2008) Olfactory memory traces in Drosophila. Prog Brain Res 169: 293-304.
21. Heisenberg M, (2003) Mushroom body memoir: from maps to models. Nat Rev Neurosci 4: 266-275.
22. Keene AC, Waddell S, (2007) Drosophila olfactory memory: single genes to complex neural circuits. Nat Rev Neurosci 8: 341-354.
23. Crittenden JR, Skoulakis EM, Han KA, Kalderon D, Davis RL, (1998) Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem 5: 38-51.
24. Ito K, Suzuki K, Estes P, Ramaswami M, Yamamoto D, et al. (1998) The organization of extrinsic neurons and their implications in the functional roles of the mushroom bodies in Drosophila melanogaster Meigen. Learn Mem 5: 52-77.
25. Boquet I, Hitier R, Dumas M, Chaminade M, Preat T, (2000) Central brain postembryonic development in Drosophila: implication of genes expressed at the interhemispheric junction. J Neurobiol 42: 33-48.
26. Dai P, Akimaru H, Ishii S, (2003) A hedgehog-responsive region in the Drosophila wing disc is defined by debra-mediated ubiquitination and lysosomal degradation of Ci. Dev Cell 4: 917-928.
27. Brand AH, Perrimon N, (1993) Targeted gene expression as a means of altering cell fates and generating dominant phenotypes. Development 118: 401-415.
28. Piccin A, Salameh A, Benna C, Sandrelli F, Mazzotta G, et al. (2001) Efficient and heritable functional knock-out of an adult phenotype in Drosophila using a GAL4-driven hairpin RNA incorporating a heterologous spacer. Nucleic Acids Res 29: E55-55.
29. Roman G, Endo K, Zong L, Davis RL, (2001) P[Switch], a system for spatial and temporal control of gene expression in Drosophila melanogaster. Proc Natl Acad Sci U S A 98: 12602-12607.
30. Mao Z, Roman G, Zong L, Davis RL, (2004) Pharmacogenetic rescue in time and space of the rutabaga memory impairment by using Gene-Switch. Proc Natl Acad Sci U S A 101: 198-203.
31. Schwaerzel M, Heisenberg M, Zars T, (2002) Extinction antagonizes olfactory memory at the subcellular level. Neuron 35: 951-960.
32. Isabel G, Pascual A, Preat T, (2004) Exclusive consolidated memory phases in Drosophila. Science 304: 1024-1027.
33. Yu D, Akalal DB, Davis RL, (2006) Drosophila alpha/beta mushroom body neurons form a branch-specific, long-term cellular memory trace after spaced olfactory conditioning. Neuron 52: 845-855.
34. Akalal DB, Yu D, Davis RL, (2010) A late-phase, long-term memory trace forms in the gamma neurons of Drosophila mushroom bodies after olfactory classical conditioning. J Neurosci 30: 16699-16708.
35. Tseng AS, Hariharan IK, (2002) An overexpression screen in Drosophila for genes that restrict growth or cell-cycle progression in the developing eye. Genetics 162: 229-243.
36. Abdelilah-Seyfried S, Chan YM, Zeng C, Justice NJ, Younger-Shepherd S, et al. (2000) A gain-of-function screen for genes that affect the development of the Drosophila adult external sensory organ. Genetics 155: 733-752.
37. Szuperak M, Zvara A, Erdelyi M, (2005) Identification of germ plasm-enriched mRNAs in Drosophila melanogaster by the cDNA microarray technique. Gene Expr Patterns 5: 717-723.
38. Khokhar A, Chen N, Yuan JP, Li Y, Landis GN, et al. (2008) Conditional switches for extracellular matrix patterning in Drosophila melanogaster. Genetics 178: 1283-1293.
39. Pavlopoulos E, Anezaki M, Skoulakis EM, (2008) Neuralized is expressed in the alpha/beta lobes of adult Drosophila mushroom bodies and facilitates olfactory long-term memory formation. Proc Natl Acad Sci U S A 105: 14674-14679.
40. Bingol B, Sheng M, (2011) Deconstruction for reconstruction: the role of proteolysis in neural plasticity and disease. Neuron 69: 22-32.
41. Tai HC, Schuman EM, (2008) Ubiquitin, the proteasome and protein degradation in neuronal function and dysfunction. Nat Rev Neurosci 9: 826-838.
42. Hegde AN, Goldberg AL, Schwartz JH, (1993) Regulatory subunits of cAMP-dependent protein kinases are degraded after conjugation to ubiquitin: a molecular mechanism underlying long-term synaptic plasticity. Proc Natl Acad Sci U S A 90: 7436-7440.
43. Hegde AN, Inokuchi K, Pei W, Casadio A, Ghirardi M, et al. (1997) Ubiquitin C-terminal hydrolase is an immediate-early gene essential for long-term facilitation in Aplysia. Cell 89: 115-126.
44. Chain DG, Schwartz JH, Hegde AN, (1999) Ubiquitin-mediated proteolysis in learning and memory. Mol Neurobiol 20: 125-142.
45. Merlo E, Romano A, (2007) Long-term memory consolidation depends on proteasome activity in the crab Chasmagnathus. Neuroscience 147: 46-52.
46. Lopez-Salon M, Alonso M, Vianna MR, Viola H, Mello e Souza T, et al. (2001) The ubiquitin-proteasome cascade is required for mammalian long-term memory formation. Eur J Neurosci 14: 1820-1826.
47. Artinian J, McGauran AM, De Jaeger X, Mouledous L, Frances B, et al. (2008) Protein degradation, as with protein synthesis, is required during not only long-term spatial memory consolidation but also reconsolidation. Eur J Neurosci 27: 3009-3019.
48. Rodriguez-Ortiz CJ, Balderas I, Saucedo-Alquicira F, Cruz-Castaneda P, Bermudez-Rattoni F, (2011) Long-term aversive taste memory requires insular and amygdala protein degradation. Neurobiol Learn Mem 95: 311-315.
49. Lai EC, Deblandre GA, Kintner C, Rubin GM, (2001) Drosophila neuralized is a ubiquitin ligase that promotes the internalization and degradation of delta. Dev Cell 1: 783-794.
50. Bilen J, Bonini NM, (2007) Genome-wide screen for modifiers of ataxin-3 neurodegeneration in Drosophila. PLoS Genet 3: 1950-1964.
51. Piper RC, Katzmann DJ, (2007) Biogenesis and function of multivesicular bodies. Annu Rev Cell Dev Biol 23: 519-547.
52. Preat T, (1998) Decreased odor avoidance after electric shock in Drosophila mutants biases learning and memory tests. J Neurosci 18: 8534-8538.
53. Lee YS, Carthew RW, (2003) Making a better RNAi vector for Drosophila: use of intron spacers. Methods 30: 322-329.
54. Wu JS, Luo L, (2006) A protocol for dissecting Drosophila melanogaster brains for live imaging or immunostaining. Nat Protoc 1: 2110-2115.