Genetic modifiers of dFMR1 encode RNA granule components in Drosophila

Genetics

Volumn 182, Issue 4, 2009, Pages 1051-1060

  Cziko, Anne Marie J ^b,c   McCann, Cathal T ^a   Howlett, Iris C ^b,d   Barbee, Scott A ^b,e   Duncan, Rebecca P ^b,f   Luedemann, Rene ^b   Zarnescu, Daniela ^b   Zinsmaier, Konrad E ^b,c   Parker, Roy R ^b,c   Ramaswami, Mani ^a,b  

^a TRINITY COLLEGE DUBLIN   (Ireland)

^b University of Arizona   (United States)

^c UNIVERSITY OF ARIZONA   (United States)

^d UNIVERSITY OF CALIFORNIA   (United States)

^e UNIVERSITY OF DENVER   (United States)

^f LEWIS AND CLARK COLLEGE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN; MICRORNA; RIBONUCLEOPROTEIN; RNA;

ARTICLE; CONTROLLED STUDY; DENDRITE; DNA MODIFICATION; DROSOPHILA; FEMALE; GENE MUTATION; GENETIC ANALYSIS; IN VIVO STUDY; MOLECULAR MECHANICS; NERVE CELL CULTURE; NEURITE; NONHUMAN; PHENOTYPE; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROCESSING; RNA TRANSLATION; SIGNAL TRANSDUCTION; TRANSLATION REGULATION;

ALLELES; ANIMALS; BIOLOGICAL TRANSPORT; CELLS, CULTURED; DROSOPHILA; DROSOPHILA PROTEINS; EYE; FRAGILE X MENTAL RETARDATION PROTEIN; MICRORNAS; MUTATION; NEURONS; RIBONUCLEOPROTEINS; RNA, MESSENGER;

EID: 70350176190     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.109.103234     Document Type: Article

References (74)

1. AAKALU, G., W. B. SMITH, N. NGUYEN, C. JIANG and E. M. SCHUMAN, 2001 Dynamic visualization of local protein synthesis in hippocampal neurons. Neuron 30: 489-502.
2. ASHRAF, S. I., A. L. MCLOON, S. M. SCLARSIC and S. KUNES, 2006 Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell 124: 191-205.
3. BARBEE, S. A., P. S. ESTES, A. M. CZIKO, J. HILLEBRAND, R. A. LUEDEMAN et al., 2006 Staufen- and FMRP-containing neuronal RNPs are structurally and functionally related to somatic P bodies. Neuron 52: 997-1009.
4. BARBEE, S. A., A. L. LUBLIN and T. C. EVANS, 2002 A novel function for the Sm proteins in germ granule localization during C. elegans embryogenesis. Curr. Biol. 12: 1502-1506.
5. BARKOFF, A. F., K. S. DICKSON, N. K. GRAY and M. WICKENS, 2000 Translational control of cyclin B1 mRNA during meiotic maturation: coordinated repression and cytoplasmic polyadenylation. Dev. Biol. 220: 97-109.
6. BASSELL, G. J., and S. T. WARREN, 2008 Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Neuron 60: 201-214.
7. BECKHAM, C., A. HILLIKER, A.M. CZIKO, A. NOUEIRY, M. RAMASWAMI et al., 2008 The DEAD-box RNA helicase Ded1p affects and accumulates in Saccharomyces cerevisiae P-bodies. Mol. Biol. Cell 19: 984-993.
8. BOLDUC, F. V., K. BELL, H. COX, K. S. BROADIE and T. TULLY, 2008 Excess protein synthesis in Drosophila fragile X mutants impairs long-term memory. Nat. Neurosci. 11: 1143-1145.
9. BRAMHAM, C. R., and D. G. WELLS, 2007 Dendritic mRNA: transport, translation and function. Nat. Rev. Neurosci. 8: 776-789.
10. BRENNECKE, J., D. R. HIPFNER, A. STARK, R. B. RUSSELL and S. M. COHEN, 2003 bantam encodes a developmentally regulated microRNA that controls cell proliferation and regulates the proapoptotic gene hid in Drosophila. Cell 113: 25-36.
11. BUSZCZAK, M., and A. C. SPRADLING, 2006 The Drosophila P68 RNA helicase regulates transcriptional deactivation by promoting RNA release from chromatin. Genes Dev. 20: 977-989.
12. CAMATS, M., S. GUIL, M. KOKOLO and M. BACH-ELIAS, 2008 P68 RNA helicase (DDX5) alters activity of cis- and trans-acting factors of the alternative splicing of H-Ras. PLoS ONE 3: e2926.
13. CASADIO, A., K. C. MARTIN, M. GIUSTETTO, H. ZHU, M. CHEN et al., 1999 A transient, neuron-wide form of CREB-mediated long-term facilitation can be stabilized at specific synapses by local protein synthesis. Cell 99: 221-237.
14. CAUDY, A. A., M. MYERS, G. J. HANNON and S. M. HAMMOND, 2002 Fragile X-related protein and VIG associate with the RNA interference machinery. Genes Dev. 16: 2491-2496.
15. CEMAN, S., W. T. O'DONNELL, M. REED, S. PATTON, J. POHL et al., 2003 Phosphorylation influences the translation state of FMRP-associated polyribosomes. Hum. Mol. Genet. 12: 3295-3305.
16. CHU, C. Y., and T. M. RANA, 2006 Translation repression in human cells by microRNA-induced gene silencing requires RCK/p54. PLoS Biol. 4: e210.
17. COLLER, J., and R. PARKER, 2005 General translational repression by activators of mRNA decapping. Cell 122: 875-886.
18. COUGOT, N., S. N. BHATTACHARYYA, L. TAPIA-ARANCIBIA, R. BORDONNE, W. FILIPOWICZ et al., 2008 Dendrites of mammalian neurons contain specialized P-body-like structures that respond to neuronal activation. J. Neurosci. 28: 13793-13804.
19. DICTENBERG, J. B., S. A. SWANGER, L. N. ANTAR, R. H. SINGER and G. J. BASSELL, 2008 A direct role for FMRP in activity-dependent dendritic mRNA transport links filopodial-spine morphogenesis to fragile X syndrome. Dev. Cell 14: 926-939.
20. DIDIOT, M. C., M. SUBRAMANIAN, E. FLATTER, J. L. MANDEL and H. MOINE, 2009 Cells lacking the fragile X mental retardation protein (FMRP) have normal RISC activity but exhibit altered stress granule assembly. Mol. Biol. Cell 20: 428-437.
21. DOCKENDORFF, T. C., H. S. SU, S. M. MCBRIDE, Z. YANG, C. H. CHOI et al., 2002 Drosophila lacking dfmr1 activity show defects in circadian output and fail to maintain courtship interest. Neuron 34: 973-984.
22. ESTES, P. S., M. O'SHEA, S. CLASEN and D. C. ZARNESCU, 2008 Fragile X protein controls the efficacy of mRNA transport in Drosophila neurons. Mol. Cell. Neurosci. 39: 170-179.
23. EULALIO, A., J. REHWINKEL, M. STRICKER, E. HUNTZINGER, S. F. YANG et al., 2007 Target-specific requirements for enhancers of decapping in miRNA-mediated gene silencing. Genes Dev. 21: 2558-2570.
24. FENG, Y., D. ABSHER, D. E. EBERHART, V. BROWN, H. E. MALTER et al., 1997 FMRP associates with polyribosomes as an mRNP, and the I304N mutation of severe fragile X syndrome abolishes this association. Mol. Cell 1: 109-118.
25. GAO, F. B., 2008 Post-transcriptional control of neuronal development by microRNA networks. Trends Neurosci. 31: 20-26.
26. GIORGI, C., G. W. YEO, M. E. STONE, D. B. KATZ, C. BURGE et al., 2007 The EJC factor eIF4AIII modulates synaptic strength and neuronal protein expression. Cell 130: 179-191. (Pubitemid 47031322)
27. GONSALVEZ, G. B., T. K. RAJENDRA, L. TIAN and A. G. MATERA, 2006 The Sm-protein methyltransferase, dart5, is essential for germ-cell specification and maintenance. Curr. Biol. 16: 1077-1089.
28. GRUEBER, W. B., L. Y. JAN and Y. N. JAN, 2002 Tiling of the Drosophila epidermis by multidendritic sensory neurons. Development 129: 2867-2878.
29. HUBER, K. M., S. M. GALLAGHER, S. T. WARREN and M. F. BEAR, 2002 Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc. Natl. Acad. Sci. USA 99: 7746-7750.
30. ISHIZUKA, A., M. C. SIOMI and H. SIOMI, 2002 A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev. 16: 2497-2508.
31. JALAL, C., H. UHLMANN-SCHIFFLER and H. STAHL, 2007 Redundant role of DEAD box proteins p68 (Ddx5) and p72/p82 (Ddx17) in ribosome biogenesis and cell proliferation. Nucleic Acids Res. 35: 3590-3601.
32. JIN, P., R. S. ALISCH and S. T. WARREN, 2004a RNA and microRNAs in fragile X mental retardation. Nat. Cell Biol. 6: 1048-1053.
33. JIN, P., D. C. ZARNESCU, S. CEMAN, M. NAKAMOTO, J. MOWREY et al., 2004b Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nat. Neurosci. 7: 113-117.
34. JOHN, B., A. J. ENRIGHT, A. ARAVIN, T. TUSCHL, C. SANDER et al., 2004 Human MicroRNA targets. PLoS Biol. 2: e363.
35. KAHLINA, K., I. GOREN, J. PFEILSCHIFTER and S. FRANK, 2004 p68 DEAD box RNA helicase expression in keratinocytes. Regulation, nucleolar localization, and functional connection to proliferation and vascular endothelial growth factor gene expression. J. Biol. Chem. 279: 44872-44882.
36. KANAI, Y., N. DOHMAE and N. HIROKAWA, 2004 Kinesin transports RNA: isolation and characterization of an RNA-transporting granule. Neuron 43: 513-525.
37. KELEMAN, K., S. KRUTTNER, M. ALENIUS and B. J. DICKSON, 2007 Function of the Drosophila CPEB protein Orb2 in longterm courtship memory. Nat. Neurosci. 10: 1587-1593.
38. KIEBLER, M. A., and G. J. BASSELL, 2006 Neuronal RNA granules: movers and makers. Neuron 51: 685-690.
39. KRICHEVSKY, A. M., and K. S. KOSIK, 2001 Neuronal RNA granules: a link between RNA localization and stimulation-dependent translation. Neuron 32: 683-696.
40. KWAK, J. E., E. DRIER, S. A. BARBEE, M. RAMASWAMI, J. C. YIN et al., 2008 GLD2 poly(A) polymerase is required for long-term memory. Proc. Natl. Acad. Sci. USA 105: 14644-14649.
41. LAGGERBAUER, B., D. OSTARECK, E.M. KEIDEL, A. OSTARECK-LEDERER and U. FISCHER, 2001 Evidence that fragile X mental retardation protein is a negative regulator of translation. Hum. Mol. Genet. 10: 329-338.
42. LECUYER, E., H. YOSHIDA, N. PARTHASARATHY, C. ALM, T. BABAK et al., 2007 Global analysis of mRNA localization reveals a prominent role in organizing cellular architecture and function. Cell 131: 174-187.
43. LEE, A., W. LI, K. XU, B. A. BOGERT, K. SU et al., 2003 Control of dendritic development by the Drosophila fragile X-related gene involves the small GTPase Rac1. Development 130: 5543-5552.
44. LI, Y., L. LIN and P. JIN, 2008 The microRNA pathway and fragile X mental retardation protein. Biochim. Biophys. Acta 1779: 702-705.
45. MARTIN, K. C., 2004 Local protein synthesis during axon guidance and synaptic plasticity. Curr. Opin. Neurobiol. 14: 305-310.
46. MARTIN, K. C., and A. EPHRUSSI, 2009 mRNA localization: gene expression in the spatial dimension. Cell 136: 719-730.
47. MAZROUI, R., M. E. HUOT, S. TREMBLAY, C. FILION, Y. LABELLE et al., 2002 Trapping of messenger RNA by Fragile X Mental Retardation protein into cytoplasmic granules induces translation repression. Hum. Mol. Genet. 11: 3007-3017.
48. MILLER, L. C., V. BLANDFORD, R. MCADAM, M. R. SANCHEZ-CARBENTE, F. BADEAUX et al., 2009 Combinations of DEAD box proteins distinguish distinct types of RNA: protein complexes in neurons. Mol. Cell. Neurosci. 40: 485-495.
49. MOHR, E., N. PRAKASH, K. VIELUF, C. FUHRMANN, F. BUCK et al., 2001 Vasopressin mRNA localization in nerve cells: characterization of cis-acting elements and trans-acting factors. Proc. Natl. Acad. Sci. USA 98: 7072-7079.
50. MUDDASHETTY, R., T. KHANAM, A. KONDRASHOV, M. BUNDMAN, A. IACOANGELI et al., 2002 Poly(A)-binding protein is associated with neuronal BC1 and BC200 ribonucleoprotein particles. J. Mol. Biol. 321: 433-445.
51. NAKAMURA, A., K. SATO and K. HANYU-NAKAMURA, 2004 Drosophila cup is an eIF4E binding protein that associates with Bruno and regulates oskar mRNA translation in oogenesis. Dev. Cell 6: 69-78.
52. NARAYANAN, U., V. NALAVADI, M. NAKAMOTO, D. C. PALLAS, S. CEMAN et al., 2007 FMRP phosphorylation reveals an immediate-early signaling pathway triggered by group I mGluR and mediated by PP2A. J. Neurosci. 27: 14349-14357.
53. NARAYANAN, U., V. NALAVADI, M. NAKAMOTO, G. THOMAS, S. CEMAN et al., 2008 S6K1 phosphorylates and regulates fragile X mental retardation protein (FMRP) with the neuronal protein synthesis-dependent mammalian target of rapamycin (mTOR) signaling cascade. J. Biol. Chem. 283: 18478-18482.
54. NARRO, M. L., F. YANG, R. KRAFT, C. WENK, A. EFRAT et al., 2007 NeuronMetrics: software for semi-automated processing of cultured neuron images. Brain Res. 1138: 57-75.
55. O'DONNELL, W. T., and S. T. WARREN, 2002 A decade of molecular studies of fragile X syndrome. Annu. Rev. Neurosci. 25: 315-338.
56. PARK, J. W., K. PARISKY, A. M. CELOTTO, R. A. REENAN and B. R. GRAVELEY, 2004 Identification of alternative splicing regulators by RNA interference in Drosophila. Proc. Natl. Acad. Sci. USA 101: 15974-15979.
57. PIERETTI, M., F. P. ZHANG, Y. H. FU, S. T. WARREN, B. A. OOSTRA et al., 1991 Absence of expression of the FMR-1 gene in fragile X syndrome. Cell 66: 817-822.
58. PREUSS, F., J. Y. FAN, M. KALIVE, S. BAO, E. SCHUENEMANN et al., 2004 Drosophila doubletime mutations which either shorten or lengthen the period of circadian rhythms decrease the protein kinase activity of casein kinase I. Mol. Cell. Biol. 24: 886-898.
59. RAAB-GRAHAM, K. F., P. C. HADDICK, Y. N. JAN and L. Y. JAN, 2006 Activity- and mTOR-dependent suppression of Kv1.1 channel mRNA translation in dendrites. Science 314: 144-148.
60. RICHTER, J. D., and E. KLANN, 2009 Making synaptic plasticity and memory last: mechanisms of translational regulation. Genes Dev. 23: 1-11.
61. ROOK, M. S., M. LU and K. S. KOSIK, 2000 CaMKIIalpha 3′ untranslated region-directed mRNA translocation in living neurons: visualization by GFP linkage. J. Neurosci. 20: 6385-6393.
62. SCHRATT, G. M., F. TUEBING, E. A. NIGH, C. G. KANE, M. E. SABATINI et al., 2006 A brain-specific microRNA regulates dendritic spine development. Nature 439: 283-289.
63. SI, K., S. LINDQUIST and E. R. KANDEL, 2003 A neuronal isoform of the aplysia CPEB has prion-like properties. Cell 115: 879-891.
64. SIGRIST, S. J., P. R. THIEL, D. F. REIFF, P. E. LACHANCE, P. LASKO et al., 2000 Postsynaptic translation affects the efficacy and morphology of neuromuscular junctions. Nature 405: 1062-1065.
65. SIOMI, H., M. CHOI, M. C. SIOMI, R. L. NUSSBAUM and G. DREYFUSS, 1994 Essential role for KH domains in RNA binding: impaired RNA binding by a mutation in the KH domain of FMR1 that causes fragile X syndrome. Cell 77: 33-39.
66. SIOMI, H., A. ISHIZUKA and M. C. SIOMI, 2004 RNA interference: A new mechanism by which FMRP acts in the normal brain? What can Drosophila teach us? Ment. Retard. Dev. Disabil. Res. Rev. 10: 68-74.
67. SIOMI, M. C., K. HIGASHIJIMA, A. ISHIZUKA and H. SIOMI, 2002 Casein kinase II phosphorylates the fragile X mental retardation protein and modulates its biological properties. Mol. Cell. Biol. 22: 8438-8447.
68. SUTTON, M. A., and E. M. SCHUMAN, 2006 Dendritic protein synthesis, synaptic plasticity, and memory. Cell 127: 49-58. (Pubitemid 44466643)
69. WAN, L., T. C. DOCKENDORFF, T. A. JONGENS and G. DREYFUSS, 2000 Characterization of dFMR1, a Drosophila melanogaster homolog of the fragile X mental retardation protein. Mol. Cell. Biol. 20: 8536-8547.
70. WEST, N., A. M. ROY-ENGEL, H. IMATAKA, N. SONENBERG and P. DEININGER, 2002 Shared protein components of SINE RNPs. J. Mol. Biol. 321: 423-432.
71. WU, L., D. WELLS, J. TAY, D. MENDIS, M. A. ABBOTT et al., 1998 CPEB-mediated cytoplasmic polyadenylation and the regulation of experience-dependent translation of alpha-CaMKII mRNA at synapses. Neuron 21: 1129-1139.
72. YE, B., C. PETRITSCH, I. E. CLARK, E. R. GAVIS, L. Y. JAN et al., 2004 Nanos and Pumilio are essential for dendrite morphogenesis in Drosophila peripheral neurons. Curr. Biol. 14: 314-321.
73. ZARNESCU, D. C., P. JIN, J. BETSCHINGER, M. NAKAMOTO, Y. WANG et al., 2005 Fragile X protein functions with lgl and the par complex in flies and mice. Dev. Cell 8: 43-52.
74. ZHANG, Y. Q., A. M. BAILEY, H. J. MATTHIES, R. B. RENDEN, M. A. SMITH et al., 2001 Drosophila fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function. Cell 107: 591-603.