Fragile X mental retardation 1 and filamin A interact genetically in drosophila long-term memory

Frontiers in Neural Circuits

Volumn 3, Issue JAN, 2010, Pages

  Bolduc, François V ^a   Bell, Kimberly ^a   Rosenfelt, Cory ^a   Cox, Hilary ^a   Tully, Tim ^a  

^a Howard Hughes Medical Institute Cold Spring Harbor Laboratory Cold Spring Harbor   (United States)

Author keywords

Dendritic spine; Fi lamin A; Fragile X; Memory; Mental retardation

Indexed keywords

EID: 77955896670     PISSN: 16625110     EISSN: None     Source Type: Journal    
DOI: 10.3389/neuro.04.022.2009     Document Type: Article

References (73)

1. Aicardi, J., (1998). The etiology of developmental delay. Semin. Pediatr. Neurol. 5, 15-20.
2. Amir, R. E., Van den Veyver, I. B., Wan, M., Tran, C. Q., Francke, U., and Zoghbi, H. Y. (1999). Rett syndrome is caused by mutations in X-linked MECP2, encoding methyl-CpG-binding protein 2. Nat. Genet. 23, 185-188.
3. Battaglia, G., Granata, T., Farina, L., D'Incerti, L., Franceschetti, S., and Avanzini, G. (1997). Periventricular nodular heterotopia: epileptogenic fi ndings. Epilepsia 38, 1173-1182.
4. Bellenchi, G. C., Gurniak, C. B., Perlas, E., Middei, S., Ammassari-Teule, M., and Witke, W. (2007). N-cofi lin is associated with neuronal migration disorders and cell cycle control in the cerebral cortex. Genes Dev. 21, 2347-2357.
5. Berry-Kravis, E., and Huttenlocher, P. R. (1992). Cyclic AMP metabolism in fragile X syndrome. Ann. Neurol. 31, 22-26.
6. Berry-Kravis, E., and Sklena, P. (1993). Demonstration of abnormal cyclic AMP production in platelets from patients with fragile X syndrome. Am. J. Med. Genet. 45, 81-87.
7. Billuart, P., and Chelly, J. (2003). From fragile X mental retardation protein to Rac1 GTPase: new insights from Fly CYFIP. Neuron 38, 843-845.
8. Bolduc, F. V., Bell, K., Cox, H., Broadie, K. S., and Tully, T. (2008). Excess protein synthesis in Drosophila fragile X mutants impairs long-term memory. Nat. Neurosci. 11, 1143-1145.
9. Bolduc, F. V., and Tully, T. (2009). Fruit flies and intellectual disability. Fly (Austin) 3, 91-104.
10. Boynton, S., and Tully, T. (1992). Latheo, a new gene involved in associative learning and memory in Drosophila melanogaster, identifi ed from P element mutagenesis. Genetics 131, 655-672.
11. Cianchetti, C., Sannio-Fancello, G., Fratta, A. L., Manconi, F., Orano, A., Pischedda, M. P., Pruna, D., Spinicci, G., Archidiacono, N., and Filippi, G. (1991). Neuropsychological, psychiatric, and physical manifestations in 149 members from 18 fragile X families. Am. J. Med. Genet. 40, 234-243.
12. Collins, A. L., Levenson, J. M., Vilaythong, A. P., Richman, R., Armstrong, D. L., Noebels, J. L., David Sweatt, J., and Zoghbi, H. Y. (2004). Mild overexpression of MeCP2 causes a progressive neurological disorder in mice. Hum. Mol. Genet. 13, 2679-2689.
13. Comery, T. A., Harris, J. B., Willems, P. J., Oostra, B. A., Irwin, S. A., Weiler, I. J., and Greenough, W. T. (1997). Abnormal dendritic spines in fragile X knockout mice: maturation and pruning defi cits. Proc. Natl. Acad. Sci. U.S.A. 94, 5401-5404.
14. Cornish, K. M., Munir, F., and Cross, G. (1999). Spatial cognition in males with Fragile-X syndrome: evidence for a neuropsychological phenotype. Cortex 35, 263-271.
15. De Boulle, K., Verkerk, A. J., Reyniers, E., Vits, L., Hendrickx, J., Van Roy, B., Van den Bos, F., de Graaff, E., Oostra, B. A., and Willems, P. J. (1993). A point mutation in the FMR-1 gene associated with fragile X mental retardation. Nat. Genet. 3, 31-35.
16. Didelot, G., Molinari, F., Tchenio, P., Comas, D., Milhiet, E., Munnich, A., Colleaux, L., and Preat, T. (2006). Tequila, a neurotrypsin ortholog, regulates long-term memory formation in Drosophila. Science 313, 851-853.
17. Dillon, C., and Goda, Y. (2005). The actin cytoskeleton: integrating form and function at the synapse. Annu. Rev. Neurosci. 28, 25-55.
18. Dubnau, J., Chiang, A. S., Grady, L., Barditch, J., Gossweiler, S., McNeil, J., Smith, P., Buldoc, F., Scott, R., Certa, U., Broger, C., and Tully, T. (2003). The staufen/pumilio pathway is involved in Drosophila long-term memory. Curr. Biol. 13, 286-296.
19. Dura, J. M., Preat, T., and Tully, T. (1993). Identifi cation of linotte, a new gene affecting learning and memory in Drosophila melanogaster. J. Neurogenet. 9, 1-14.
20. Engert, F., and Bonhoeffer, T. (1999). Dendritic spine changes associated with hippocampal long-term synaptic plasticity. Nature 399, 66-70.
21. Esue, O., Tseng, Y., and Wirtz D. (2009) Alpha-actinin and fi lamin cooperatively enhance the stiffness of actin filament networks. PLoS One 4: e4411.2009.
22. Fink, J. M., Dobyns, W. B., Guerrini, R., and Hirsch, B. A. (1997). Identifi cation of a duplication of Xq28 associated with bilateral periventricular nodular heterotopia. Am. J. Hum. Genet. 61, 379-387.
23. Flanagan, L. A., Chou, J., Falet, H., Neujahr, R., Hartwig, J. H., and Stossel, T. P. (2001). Filamin A, the Arp2/3 complex, and the morphology and function of cortical actin fi laments in human melanoma cells. J. Cell Biol. 155, 511-517.
24. Fmr1 knockout mice: a model to study fragile X mental retardation. The Dutch-Belgian Fragile X Consortium. Cell 78, 23-33. (1994).
25. Fox, J. W., Lamperti, E. D., Eksioglu, Y. Z., Hong, S. E., Feng, Y., Graham, D. A., Scheffer, I. E., Dobyns, W. B., Hirsch, B. A., Radtke, R. A., Berkovic, S. F., Huttenlocher, P. R., and Walsh, C. A. (1998). Mutations in fi lamin 1 prevent migration of cerebral cortical neurons in human periventricular heterotopia. Neuron 21, 1315-1325.
26. Guy, J., Hendrich, B., Holmes, M., Martin, J. E., and Bird, A. (2001). A mouse Mecp2-null mutation causes neurological symptoms that mimic Rett syndrome. Nat. Genet. 27, 322-326.
27. Hagberg, B., Hagberg, G., Lewerth, A., and Lindberg, U. (1981). Mild mental retardation in Swedish school children. II. Etiologic and pathogenetic aspects. Acta Paediatr. Scand. 70, 445-452.
28. Hartwig, J. H., and Stossel, T. P. (1975). Isolation and properties of actin, myosin, and a new actinbinding protein in rabbit alveolar macrophages. J. Biol. Chem. 250, 5696-5705.
29. Hayashi, M. L., Rao, B. S., Seo, J. S., Choi, H. S., Dolan, B. M., Choi, S. Y., Chattarji, S., and Tonegawa, S. (2007). Inhibition of p21-activated kinase rescues symptoms of fragile X syndrome in mice. Proc. Natl. Acad. Sci. U.S.A. 104, 11489-11494.
30. Hinton, V. J., Brown, W. T., Wisniewski, K., and Rudelli, R. D. (1991). Analysis of neocortex in three males with the fragile X syndrome. Am. J. Med. Genet. 41, 289-294.
31. Hinton, V. J., Halperin, J. M., Dobkin, C. S., Ding, X. H., Brown, W. T., and Miezejeski, C. M. (1995). Cognitive and molecular aspects of fragile X. J. Clin. Exp. Neuropsychol. 17, 518-528.
32. Hornstra, I. K., Nelson, D. L., Warren, S. T., and Yang, T. P. (1993). High resolution methylation analysis of the FMR1 gene trinucleotide repeat region in fragile X syndrome. Hum. Mol. Genet. 2, 1659-1665.
33. Hu, H., Qin, Y., Bochorishvili, G., Zhu, Y., van Aelst, L., and Zhu, J. J. (2008). Ras signaling mechanisms underlying impaired GluR1-dependent plasticity associated with fragile X syndrome. J. Neurosci. 28, 7847-7862.
34. Inlow, J. K., and Restifo, L. L. (2004). Molecular and comparative genetics of mental retardation. Genetics 166, 835-881.
35. Inoue, S., Shimoda, M., Nishinokubi, I., Siomi, M. C., Okamura, M., Nakamura, A., Kobayashi, S., Ishida, N., and Siomi, H. (2002). A role for the Drosophila fragile X-related gene in circadian output. Curr. Biol. 12, 1331-1335.
36. Irwin, S. A., Idupulapati, M., Gilbert, M. E., Harris, J. B., Chakravarti, A. B., Rogers, E. J., Crisostomo, R. A., Larsen, B. P., Mehta, A., Alcantara, C. J., Patel, B., Swain, R. A., Weiler, I. J., Oostra, B. A., and Greenough, W. T. (2002). Dendritic spine and dendritic fi eld characteristics of layer V pyramidal neurons in the visual cortex of fragile-X knockout mice. Am. J. Med. Genet. 111, 140-146.
37. Johannessen, C. M., Reczek, E. E., James, M. F., Brems, H., Legius, E., and Cichowski, K. (2005). The NF1 tumor suppressor critically regulates TSC2 and mTOR. Proc. Natl. Acad. Sci. U.S.A. 102, 8573-8578.
38. Kelleher, R. J. III, and Bear, M. F. (2008). The autistic neuron: troubled translation? Cell 135, 401-406.
39. Khandjian, E. W., Huot, M. E., Tremblay, S., Davidovic, L., Mazroui, R., and Bardoni, B. (2004). Biochemical evidence for the association of fragile X mental retardation protein with brain polyribosomal ribonucleoparticles. Proc. Natl. Acad. Sci. U.S.A. 101, 13357-13362.
40. Kooy, R. F., D'Hooge, R., Reyniers, E., Bakker, C. E., Nagels, G., De Boulle, K., Storm, K., Clincke, G., De Deyn, P. P., Oostra, B. A., and Willems, P. J. (1996). Transgenic mouse model for the fragile X syndrome. Am. J. Med. Genet. 64, 241-245.
41. Krashes, M. J., Keene, A. C., Leung, B., Armstrong, J. D., and Waddell, S. (2007). Sequential use of mushroom body neuron subsets during drosophila odor memory processing. Neuron 53, 103-115.
42. Li, Z., Zhang, Y., Ku, L., Wilkinson, K. D., Warren, S. T., and Feng, Y. (2001). The fragile X mental retardation protein inhibits translation via interacting with mRNA. Nucleic Acids Res. 29, 2276-2283.
43. Lu, Y., Lu, Y. S., Shuai, Y., Feng, C., Tully, T., Xie, Z., Zhong, Y., and Zhou, H. M. (2007). The AKAP Yu is required for olfactory long-term memory formation in Drosophila. Proc. Natl. Acad. Sci. U.S.A. 104, 13792-13797.
44. Maes, B., Fryns, J. P., Van Walleghem, M., and Van den Berghe, H. (1994). Cognitive functioning and information processing of adult mentally retarded men with fragile-X syndrome. Am. J. Med. Genet. 50, 190-200.
45. Matus, A., (2000). Actin-based plasticity in dendritic spines. Science 290, 754-758.
46. McBride, S. M., Choi, C. H., Wang, Y., Liebelt, D., Braunstein, E., Ferreiro, D., Sehgal, A., Siwicki, K. K., Dockendorff, T. C., Nguyen, H. T., McDonald, T. V., and Jongens, T. A. (2005). Pharmacological rescue of synaptic plasticity, courtship behavior, and mushroom body defects in a Drosophila model of fragile X syndrome. Neuron 45, 753-764.
47. Michel, C. I., Kraft, R., and Restifo, L. L. (2004). Defective neuronal development in the mushroom bodies of Drosophila fragile X mental retardation 1 mutants. J. Neurosci. 24, 5798-5809.
48. Moro, F., Pisano, T., Bernardina, B. D., Polli, R., Murgia, A., Zoccante, L., Darra, F., Battaglia, A., Pramparo, T., Zuffardi, O., and Guerrini, R. (2006). Periventricular heterotopia in fragile X syndrome. Neurology 67, 713-715.
49. Muddashetty, R. S., Kelic, S., Gross, C., Xu, M., and Bassell, G. J. (2007). Dysregulated metabotropic glutamate receptor-dependent translation of AMPA receptor and postsynaptic density-95 mRNAs at synapses in a mouse model of fragile X syndrome. J. Neurosci. 27, 5338-5348.
50. Pascual, A., and Preat, T. (2001). Localization of long-term memory within the Drosophila mushroom body. Science 294, 1115-1117.
51. Qian, M., Pan, G., Sun, L., Feng, C., Xie, Z., Tully, T., and Zhong, Y. (2007). Receptor-like tyrosine phosphatase PTP10D is required for long-term memory in Drosophila. J. Neurosci. 27, 4396-4402.
52. Quinn, W. G., Harris, W. A., and Benzer, S. (1974). Conditioned behavior in Drosophila melanogaster. Proc. Natl. Acad. Sci. U.S.A. 71, 708-712.
53. Raymond, F. L., and Tarpey, P. (2006). The genetics of mental retardation. Hum. Mol. Genet. 15 Spec No 2,R110-R116.
54. Reeve, S. P., Bassetto, L., Genova, G. K., Kleyner, Y., Leyssen, M., Jackson, F. R., and Hassan, B. A. (2005). The Drosophila fragile X mental retardation protein controls actin dynamics by directly regulating profi lin in the brain. Curr. Biol. 15, 1156-1163.
55. Restifo, L. L., (2005). Mental retardation genes in drosophila: New approaches to understanding and treating developmental brain disorders. Ment. Retard Dev. Disabil. Res. Rev. 11, 286-294.
56. Rudelli, R. D., Brown, W. T., Wisniewski, K., Jenkins, E. C., Laure-Kamionowska, M., Connell, F., and Wisniewski, H. M. (1985). Adult fragile X syndrome. Clinico-neuropathologic findings. Acta Neuropathol. (Berl.) 67, 289-295.
57. Schenck, A., Bardoni, B., Langmann, C., Harden, N., Mandel, J. L., and 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.
58. Shea, S. E., (2006). Mental retardation in children ages 6 to 16. Semin. Pediatr. Neurol. 13, 262-270.
59. Skinner, M., Hooper, S., Hatton, D. D., Roberts, J., Mirrett, P., Schaaf, J., Sullivan, K., Wheeler, A., Bailey, D. B., and Jr. (2005). Mapping nonverbal IQ in young boys with fragile X syndrome. Am. J. Med. Genet. A 132, 25-32.
60. Sokol, N. S., and Cooley, L. (2003). Drosophila filamin is required for follicle cell motility during oogenesis. Dev. Biol. 260, 260-272.
61. Stefani, G., Fraser, C. E., Darnell, J. C., and Darnell, R. B. (2004). Fragile X mental retardation protein is associated with translating polyribosomes in neuronal cells. J. Neurosci. 24, 7272-7276.
62. Stossel, T. P., Condeelis, J., Cooley, L., Hartwig, J. H., Noegel, A., Schleicher, M., and Shapiro, S. S. (2001). Filamins as integrators of cell mechanics and signalling. Nat. Rev. Mol. Cell Biol. 2, 138-145.
63. Tang, Y., Marwaha, S., Rutkowski, J. L., Tennekoon, G. I., Phillips, P. C., and Field, J. (1998). A role for Pak protein kinases in Schwann cell transformation. Proc. Natl. Acad. Sci. U.S.A. 95, 5139-5144.
64. Trottier, Y., Imbert, G., Poustka, A., Fryns, J. P., and Mandel, J. L. (1994). Male with typical fragile X phenotype is deleted for part of the FMR1 gene and for about 100 kb of upstream region. Am. J. Med. Genet. 51, 454-457.
65. Tully, T., Preat, T., Boynton, S. C., and Del Vecchio, M. (1994). Genetic dissection of consolidated memory in Drosophila. Cell 79, 35-47.
66. Tully, T., and Quinn, W. G. (1985). Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol. [A] 157, 263-277.
67. Vanderklish, P. W., and Edelman, G. M. (2002). Dendritic spines elongate after stimulation of group 1 metabotropic glutamate receptors in cultured hippocampal neurons. Proc. Natl. Acad. Sci. U.S.A. 99, 1639-1644.
68. Weiler, I. J., Spangler, C. C., Klintsova, A. Y., Grossman, A. W., Kim, S. H., Bertaina-Anglade, V., Khaliq, H., de Vries, F. E., Lambers, F. A., Hatia, F., Base, C. K., and Greenough, W. T. (2004). Fragile X mental retardation protein is necessary for neurotransmitter- activated protein translation at synapses. Proc. Natl. Acad. Sci. U.S.A. 101, 17504-17509.
69. Wisniewski, K. E., Segan, S. M., Miezejeski, C. M., Sersen, E. A., and Rudelli, R. D. (1991). The Fra(X) syndrome: neurological, electrophysiological, and neuropathological abnormalities. Am. J. Med. Genet. 38, 476-480.
70. Wohrle, D., Kotzot, D., Hirst, M. C., Manca, A., Korn, B., Schmidt, A., Barbi, G., Rott, H. D., Poustka, A., Davies, K. E. and Steinbach, P. (1992). A microdeletion of less than 250 kb, including the proximal part of the FMR-I gene and the fragile-X site, in a male with the clinical phenotype of fragile-X syndrome. Am. J. Hum. Genet. 51, 299-306.
71. Xia, S., Miyashita, T., Fu, T. F., Lin, W. Y., Wu, C. L., Pyzocha, L., Lin, I. R., Saitoe, M., Tully, T., and Chiang, A. S. (2005). NMDA receptors mediate olfactory learning and memory in Drosophila. Curr. Biol. 15, 603-615.
72. Yin, J. C., Wallach, J. S., Del Vecchio, M., Wilder, E. L., Zhou, H., Quinn, W. G., and Tully, T. (1994). Induction of a dominant negative CREB transgene specifi cally blocks long-term memory in Drosophila. Cell 79, 49-58.
73. Yu, D., Akalal, D. B., and Davis, R. L. (2006). Drosophila alpha/beta mushroom body neurons form a branch-specifi c, long-term cellular memory trace after spaced olfactory conditioning. Neuron 52, 845-855.