Defective neuronal development in the mushroom bodies of Drosophila fragile X mental retardation 1 mutants

Journal of Neuroscience

Volumn 24, Issue 25, 2004, Pages 5789-5809

  Michel, Carlos I ^a,c   Kraft, Robert ^a   Restifo, Linda L ^a,b  

^a UNIVERSITY OF ARIZONA   (United States)

^b UNIVERSITY OF ARIZONA   (United States)

^c WASHINGTON UNIVERSITY   (United States)

Author keywords

Cognition; Genetic model system; Learning; Memory; Metamorphosis; Neurogenetics

Indexed keywords

FMRP PROTEIN; GENE PRODUCT; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; DROSOPHILA PROTEIN; FMR1 PROTEIN, DROSOPHILA; FRAGILE X MENTAL RETARDATION PROTEIN;

ADOLESCENT; ARTICLE; BRAIN DEVELOPMENT; CELL MATURATION; CIRCADIAN RHYTHM; COGNITION; COGNITIVE DEFECT; CONTROLLED STUDY; DEVELOPMENTAL DISORDER; DEVELOPMENTAL STAGE; DFMR1 GENE; DROSOPHILA FRAGILE X MENTAL RETARDATION 1 GENE; FRAGILE X SYNDROME; GENE; GENE FUNCTION; GENE MUTATION; GENETIC DISORDER; GENETIC MODEL; GENETICS; INTERNEURON; LARVA; LEARNING; LINOTTE GENE; MEMORY; METAMORPHOSIS; MORPHOGENESIS; MUSHROOM BODY; NERVE CELL DIFFERENTIATION; NERVE CELL PLASTICITY; NERVE ENDING; NEUROBIOLOGY; NEUROMUSCULAR SYNAPSE; NONHUMAN; ORTHOLOGY; PHENOTYPE; POSTSYNAPTIC MEMBRANE; PRIORITY JOURNAL; TRANSCRIPTION REGULATION; ANIMAL; ANIMAL MODEL; CHROMOSOME; CONGENITAL MALFORMATION; DROSOPHILA; GROWTH, DEVELOPMENT AND AGING; MUTATION; NERVE CELL; PATHOLOGY; PRENATAL DEVELOPMENT;

ANIMALS; CHROMOSOMES; DROSOPHILA; DROSOPHILA PROTEINS; FRAGILE X MENTAL RETARDATION PROTEIN; METAMORPHOSIS, BIOLOGICAL; MODELS, ANIMAL; MORPHOGENESIS; MUSHROOM BODIES; MUTATION; NEURONS; PHENOTYPE; RNA-BINDING PROTEINS;

EID: 3042735950     PISSN: 02706474     EISSN: None     Source Type: Journal    
DOI: 10.1523/JNEUROSCI.0450-04.2004     Document Type: Article

References (97)

1. Antar LN, Bassell GJ (2003) Sunrise at the synapse: the FMRP mRNP shaping the synaptic interface. Neuron 37:555-558.
2. Bainbridge SP, Bownes M (1981) Staging the metamorphosis of drosophila melanogaster. J Embryol Exp Morphol 66:57-80.
3. Barth M, Heisenberg M (1997) Vision affects mushroom bodies and central complex in Drosophila melanogaster. Learn Mem 4:219-229.
4. Bennetto L, Pennington BF (2002) Neuropsychology. In: Fragile X syndrome: diagnosis, treatment, and research, Ed 3 (Hagermann PJ, ed), pp 206-250. Baltimore: Johns Hopkins UP.
5. Bolwig GM, Del Vecchio M, Hannon G, Tully T (1995) Molecular cloning of linotte in Drosophila: a novel gene that functions in adults during associative learning. Neuron 15:829-842.
6. Bonini NM (2000) Drosophila as a genetic tool to define vertebrate pathway players. Methods Mol Biol 136:7-14.
7. Bonkowsky JL, Yoshikawa S, O'Keefe DD, Scully AL, Thomas JB (1999) Axon routing across the midline controlled by the Drosophila Derailed receptor. Nature 402:540-544.
8. Boquet I, Boujemaa R, Carlier M-F, Préat T (2000) Ciboulot regulated actin assembly during Drosophila brain metamorphosis. Cell 102:797-808.
9. Brand AH, Dormand E-L (1995) The GAL4 system as a tool for unravelling the mysteries of the Drosophila nervous system. Curr Opin Neurobiol 5:572-578.
10. Braun K, Segal M (2000) FMRP involvement in formation of synapses among cultured hippocampal neurons. Cereb Cortex 10:1045-1052.
11. Brown V, Jin P, Ceman S, Darnell JC, O'Donnell WT, Tenenbaum SA, Jin X, Feng Y, Wilkinson KD, Keene JD, Darnell RB, Warren ST (2001) Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell 107:477-487.
12. Budnik V, Martin-Morris L, White K (1986) Perturbed pattern of catecholamine-containing neurons in mutant Drosophila deficient in the enzyme dopa decarboxylase. J Neurosci 6:3682-3691.
13. Caudy AA, Myers M, Hannon GJ, Hammond SM (2002) Fragile X-related protein and VIG associate with the RNA interference machinery. Genes Dev 16:2491-2496.
14. Comery TA, Harris JB, Willems PJ, Oostra BA, Irwin SA, Weiler IJ, Greenough WT (1997) Abnormal dendritic spines in fragile X knockout mice: maturation and pruning deficits. Proc Natl Acad Sci USA 94:5401-5404.
15. Crittenden JR, Skoulakis EMC, Han K-A, Kalderon D, Davis RL (1998) Tripartite mushroom body architecture revealed by antigenic markers. Learn Mem 5:38-51.
16. Cubitt AB, Heimar R, Adams SR, Boyd AE, Gross LA, Tsien RY (1995) Understanding, improving and using green fluorescent proteins. Trends Biochem Sci 20:448-455.
17. Darnell JC, Jensen KB, Jin P, Brown V, Warren ST, Darnell RB (2001) Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell 107:489-499.
18. deBelle JS, Heisenberg M (1996) Expression of Drosophila mushroom body mutations in alternative genetic backgrounds: a case study of the mushroom body miniature gene (mbm). Proc Natl Acad Sci USA 93:9875-9880.
19. Devys D, Lutz Y, Rouyer N, Bellocq JP, Mandel JL (1993) The FMR-1 protein is cytoplasmic, most abundant in neurons and appears normal in carriers of a fragile X premutation. Nat Genet 4:335-340.
20. Dobkin C, Rabe A, Dumas R, El Idrissi A, HaubenstockH, Brown WT (2000) Fmr1 knockout mouse has a distinctive strain-specific learning impairment. Neuroscience 100:423-429.
21. Dockendorff TC, Su HS, McBride SM, Yang Z, Choi CH, Siwicki KK, Sehgal A, Jongens TA (2002) Drosophila lacking dfmr1 activity show defects in circadian output and fail to maintain courtship interest. Neuron 34:973-984.
22. Driscoll M, Gerstbrein B (2003) Dying for a cause: invertebrate genetics takes on human neurodegeneration. Nat Rev Genet 4:181-194.
23. Dura J-M, Préat T, Tully T (1993) Identification of linotte, a new gene affecting learning and memory in Drosophila melanogaster. J Neurogenet 9:1-14.
24. Dutch-Belgian Fragile X Consortium (1994) Fmr1 knockout mice: a model to study fragile X mental retardation. Cell 78:23-33.
25. Elgin SR, Miller DW (1978) Mass rearing of flies and mass production and harvesting of eggs. In: The genetics and biology of Drosophila (Wright TRF, ed), pp 112-121. New York: Academic.
26. Feng Y, Gutekunst CA, Eberhart DE, Yi H, Warren ST, Hersch SM (1997) Fragile X mental retardation protein: nucleocytoplasmic shuttling and association with somatodendritic ribosomes. J Neurosci 17:1539-1547.
27. Galvez R, Gopal AR, Greenough WT (2003) Somatosensory cortical barrel dendritic abnormalities in a mouse model of the fragile X mental retardation syndrome. Brain Res 971:83-89.
28. Gould EL, Loesch DZ, Martin M, Hagerman RJ, Armstrong SM, Huggins RM (2000) Melatonin profiles and sleep characteristics in boys with fragile X syndrome: a preliminary study. Am J Med Genet 95:307-315.
29. Greenough WT, Klintsova AY, Irwin SA, Galvez R, Bates KE, Weiler IJ (2001) Synaptic regulation of protein synthesis and the fragile X protein. Proc Natl Acad Sci USA 98:7101-7106.
30. Greenspan RJ (1997) Fly pushing: the theory and practice of Drosophila genetics. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory.
31. Guthrie S (2001) Axon guidance: Robos make the rules. Curr Biol 11:R300-R303.
32. Hagerman RJ (2002) The physical and behavioral phenotype. In: Fragile X syndrome: diagnosis, treatment, and research, Ed 3 (Hagermann PJ, ed), pp 3-109. Baltimore: Johns Hopkins UP.
33. Heisenberg M (2003) Mushroom body memoir: from maps to models. Nat Rev Neurosci 4:266-275.
34. Heisenberg M, Heusipp M, Wanke C (1995) Structural plasticity in the Drosophila brain. J Neurosci 15:1951-1960.
35. Hinton VJ, Brown WT, Wisniewski K, Rudelli RD (1991) Analysis of neocortex in three males with the fragile X syndrome. Am J Med Genet 41:289-294.
36. Hitier R, Chaminade M, Préat T (2001) The Drosophila castor gene is involved in postembryonic brain development. Mech Dev 103:3-11.
37. Huber KM, Gallagher SM, Warren ST, Bear MF (2002) Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc Natl Acad Sci USA 99:7746-7750.
38. Inlow JK, Restifo LL (2004) Molecular and comparative genetics of mental retardation. Genetics 166:835-881.
39. Inoue S, Shimoda M, Nishinokubi I, Siomi MC, Okamura M, Nakamura A, Kobayashi S, Ishida N, Siomi H (2002) A role for the Drosophila fragile X-related gene in circadian output. Curr Biol 12:1331-1335.
40. Irwin SA, Swain RA, Christmon CA, Chakravarti A, Weiler IJ, Greenough WT (2000) Evidence for altered Fragile-X mental retardation protein expression in response to behavioral stimulation. Neurobiol Learn Mem 73:87-93.
41. Irwin SA, Patel B, Idupulapati M, Harris JB, Crisostomo RA, Larsen BP, Kooy F, Willems PJ, Cras P, Kozlowski PB, Swain RA, Weiler IJ, Greenough WT (2001) Abnormal dendritic spine characteristics in the temporal and visual cortices of patients with fragile-X syndrome: a quantitative examination. Am J Med Genet 98:161-167.
42. Irwin SA, Idupulapati M, Gilbert ME, Harris JB, Chakravarti AB, Rogers EJ, Crisostomo RA, Larsen BP, Mehta A, Alcantara CJ, Patel B, Swain RA, Weiler IJ, Oostra BA, Greenough WT (2002) Dendritic spine and dendritic field characteristics of layer V pyramidal neurons in the visual cortex of fragile-X knockout mice. Am J Med Genet 111:140-146.
43. Ishizuka A, Siomi MC, Siomi H (2002) A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev 16:2497-2508.
44. Ito K, Sass H, Urban J, Hofbauer A, Schneuwly S (1997) GAL4-responsive UAS-tau as a tool for studying the anatomy and development of the Drosophila central nervous system. Cell Tissue Res 290:1-10.
45. Ivanco TL, Greenough WT (2002) Altered mossy fiber distributions in adult Fmr1 (FVB) knockout mice. Hippocampus 12:47-54.
46. Jin P, Warren ST (2000) Understanding the molecular basis of fragile X syndrome. Hum Mol Genet 9:901-908.
47. Jin P, Warren ST (2003) New insights into fragile X syndrome: from molecules to neurobehaviors. Trends Biochem Sci 28:152-158.
48. Jin P, Zarnescu DC, Ceman S, Nakamoto M, Mowrey J, Jongens TA, Nelson DL, Moses K, Warren ST (2004) Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nat Neurosci 7:113-117.
49. Kates WR, Folley BS, Lanham DC, Capone GT, Kaufmann WE (2002) Cerebral growth in Fragile X syndrome: review and comparison with Down syndrome. Microsc Res Tech 57:159-167.
50. Kaytor MD, Orr HT (2001) RNA targets of the fragile X protein. Cell 107:555-557.
51. Kazantsev A, Walker HA, Slepko N, Bear JE, Preisinger E, Steffan JS, Zhu YZ, Gertler FB, Housman DE, Marsh JL, Thompson LM (2002) A bivalent Huntingtin binding peptide suppresses polyglutamine aggregation and pathogenesis in Drosophila. Nat Genet 30:367-376.
52. Kirkpatrick LL, Mcllwain KA, Nelson DL (2001) Comparative genomic sequence analysis of the FXR gene family: FMR1, FXR1, and FXR2. Genomics 78:169-177.
53. Kooy RF (2003) Of mice and the fragile X syndrome. Trends Genet 19:148-154.
54. Kraft R, Levine RB, Restifo LL (1998) The steroid hormone 20-hydroxyecdysone enhances neurite growth of Drosophila mushroom body neurons isolated during metamorphosis. J Neurosci 18:8886-8899.
55. Laggerbauer B, Ostareck D, Keidel EM, Ostareck-Lederer A, Fischer U (2001) Evidence that fragile X mental retardation protein is a negative regulator of translation. Hum Mol Genet 10:329-338.
56. Lasko P (2002) Diabetic flies? Using Drosophila melanogaster to understand the causes of monogenic and genetically complex diseases. Clin Genet 62:358-367.
57. Lee A, Li W, Xu K, Bogert BA, Su K, Gao FB (2003) Control of dendritic development by the Drosophila fragile X-related gene involves the small GTPase Rac1. Development 130:5543-5552.
58. Lee T, Luo L (1999) Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22:451-461.
59. Lee T, Lee A, Luo L (1999) Development of the Drosophila mushroom bodies: sequential generation of three distinct types of neurons from a neuroblast. Development 126:4065-4076.
60. Li Z, Zhang Y, Ku L, Wilkinson KD,Warren ST, Feng Y (2001) The fragile X mental retardation protein inhibits translation via interacting with mRNA. Nucleic Acids Res 29:2276-2283.
61. Liu Z, Steward R, Luo L (2000) Drosophila Lis1 is required for neuroblast proliferation, dendritic elaboration and axonal transport. Nat Cell Biol 2:776-783.
62. Mayford M, Kandel ER (1999) Genetic approaches to memory storage. Trends Genet 15:463-470.
63. Mazroui R, Huot ME, Tremblay S, Filion C, Labelle Y, Khandjian EW (2002) Trapping of messenger RNA by Fragile X Mental Retardation Protein into cytoplasmic granules induces translation repression. Hum Mol Genet 11:3007-3017.
64. McGuire SE, Le PT, Davis RL (2001) The role of Drosophila mushroom body signaling in olfactory memory. Science 293:1330-1333.
65. Mineur YS, Sluyter F, de Wit S, Oostra BA, Crusio WE (2002) Behavioral and neuroanatomical characterization of the Fmr1 knockout mouse. Hippocampus 12:39-46.
66. Morales J, Hiesinger PR, Schroeder AJ, Kume K, Verstreken P, Jackson FR, Nelson DL, Hassan BA (2002) Drosophila fragile X protein, DFXR, regulates neuronal morphology and function in the brain. Neuron 34:961-972.
67. Moreau-Fauvarque C, Taillebourg E, Boissoneau E, Mesnard J, Dura J-M (1998) The receptor tyrosine kinase gene linotte is required for neuronal pathway selection in the Drosophila mushroom bodies. Mech Dev 78:47-61.
68. Moreau-Fauvarque C, Taillebourg E, Préat T, Dura J-M (2002) Mutation of linotte causes behavioral defects independent of pigeon in Drosophila. Neuro Report 13:2309-2312.
69. Nimchinsky EA, Oberlander AM, Svoboda K (2001) Abnormal development of dendritic spines in FMR1 knock-out mice. J Neurosci 21:5139-5146.
70. O'Donnell WT, Warren ST (2002) A decade of molecular studies of fragile X syndrome. Annu Rev Neurosci 25:315-338.
71. Oostra BA, Willemsen R (2003) A fragile balance: FMR1 expression levels. Hum Mol Genet 12:R249-R257.
72. Paradee W, Melikian HE, Rasmussen DL, Kenneson A, Conn PJ, Warren ST (1999) Fragile X mouse: strain effects of knockout phenotype and evidence suggesting deficient amygdala function. Neuroscience 94:185-192.
73. Pascual A, Préat T (2001) Localization of long-term memory within the Drosophila mushroom body. Science 294:1115-1117.
74. Rein K, Zockler M, Mader M, Grubel C, Heisenberg M (2002) The Drosophila standard brain. Curr Biol 12:227-231.
75. Restifo LL, Merrill VKL (1994) Two Drosophila regulatory genes, Deformed and the Broad-Complex, share common functions in development of adult CNS, head, and salivary glands. Dev Biol 162:465-485.
76. Restifo LL, White K (1991) Mutations in asteroid hormone-regulated gene disrupt the metamorphosis of the central nervous system in Drosophila. Dev Biol 148:174-194.
77. Robertson HM, Preston CR, Phillis RW, Johnson-Schlitz DM, Benz WK, Engels WR (1988) A stable genomic source ofP element transposase in Drosophila melanogaster. Genetics 118:461-470.
78. Roman G, Davis RL (2001) Molecular biology and anatomy of Drosophila olfactory associative learning. BioEssays 23:571-581.
79. Rudelli RD, Brown WT, Wisniewski K, Jenkins EC, Laure-Kamionowska M, Connell F, Wisniewski HM (1985) Adult fragile X syndrome: cliniconeuropathologic findings. Acta Neuropathol (Berl) 67:289-295.
80. Schaeffer C, Bardoni B, Mandel JL, Ehresmann B, Ehresmann C, Moine H (2001) The fragile X mental retardation protein binds specifically to its mRNA via a purine quartet motif. EMBO J 20:4803-4813.
81. Schenck A, Bardoni B, Langmann C, Harden N, Mandel J-L, Giangrande A (2003) CYFIP/Sra-1 controls neuronal connectivity in Drosophila and links the Rac1 GTPase pathway to the fragile X protein. Neuron 38:887-898.
82. Sherman S (2002) Epidemiology. In: Fragile X syndrome: diagnosis, treatment, and research, Ed 3 (Hagermann PJ, ed), pp 136-168. Baltimore: Johns Hopkins UP.
83. Simon A, Boquet I, Synguélakis M, Préat T (1998) The Drosophila putative kinase Linotte (Derailed) prevents central brain axons from converging on a newly described interhemispheric ring. Mech Dev 76:45-55.
84. Siomi MC, Higashijima K, Ishizuka A, Siomi H (2002) Casein kinase II phosphorylates the fragile X mental retardation protein and modulates its biological properties. Mol Cell Biol 22:8438-8447.
85. Strausfeld NJ, Hansen L, Li Y, Gomez RS, Ito K (1998) Evolution, discovery, and interpretations of arthropod mushroom bodies. Learn Mem 5:11-37.
86. Strausfeld NJ, Sinakevitch I, Vilinsky I (2003) The mushroom bodies of Drosophila melanogaster: an immunocytological and Golgi study of Kenyon cell organization in the calyces and lobes. Microsc Res Tech 62:151-169.
87. Technau GM (1984) Fiber number in the mushroom bodies of adult Drosophila melanogaster depends on age, sex and experience. J Neurogenet 1:113-126.
88. Technau G, Heisenberg M (1982) Neural reorganization during metamorphosis of the corpora pedunculata in Drosophila melanogaster. Nature 295:405-407.
89. Todd PK, Mack KJ (2000) Sensory stimulation increases cortical expression of the fragile X mental retardation protein in vivo. Brain Res Mol Brain Res 80:17-25.
90. Wan L, Dockendorff TC, Jongens TA, Dreyfuss G (2000) Characterization of dFMR1, a Drosophila melanogaster homolog of the fragile X mental retardation protein. Mol Cell Biol 20:8536-8547.
91. Warrick JM, Chan HY, Gray-Board GL, Chai Y, Paulson HL, Bonini NM (1999) Suppression of polyglutamine-mediated neurodegeneration in Drosophila by the molecular chaperone HSP70. Nat Genet 23:425-428.
92. Weiler IJ, Irwin SA, Klintsova AY, Spencer CM, Brazelton AD, Miyashiro K, Comery TA, Patel B, Eberwine J, Greenough WT (1997) Fragile X mental retardation protein is translated near synapses in response to neurotransmitter activation. Proc Natl Acad Sci USA 94:5395-5400.
93. Withers GS, Banker G (1998) Characterizing and studying neuronal cultures. In: Culturing nerve cells (Banker G, Goslin K, eds), pp 113-151. Cambridge, MA: MIT.
94. Zalfa F, Giorgi M, Primerano B, Moro A, Di Penta A, Reis S, Oostra B, Bagni C (2003) The fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses. Cell 112:317-327.
95. Zars T (2000) Behavioral functions of the insect mushroom bodies. Curr Opin Neurobiol 10:790-795.
96. Zars T, Fisher M, Schulz R, Heisenberg M (2000) Localization of a short-term memory in Drosophila. Science 288:672-675.
97. Zhang YQ, Bailey AM, Matthies HJ, Renden RB, Smith MA, Speese SD, Rubin GM, Broadie K (2001) Drosophila fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function. Cell 107:591-603.