The Conserved, Disease-Associated RNA Binding Protein dNab2 Interacts with the Fragile X Protein Ortholog in Drosophila Neurons

Cell Reports

Volumn 20, Issue 6, 2017, Pages 1372-1384

  Bienkowski, Rick S ^a   Banerjee, Ayan ^a   Rounds, J Christopher ^a   Rha, Jennifer ^a   Omotade, Omotola F ^a   Gross, Christina ^b   Morris, Kevin J ^a   Leung, Sara W ^a   Pak, ChangHui ^a   Jones, Stephanie K ^a   Santoro, Michael R ^a   Warren, Stephen T ^a   Zheng, James Q ^a   Bassell, Gary J ^a   Corbett, Anita H ^a   Moberg, Kenneth H ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

^b UNIVERSITY OF CINCINNATI   (United States)

Author keywords

CamKII; dNab2; Drosophila; fragile X mental retardation protein; futsch; memory; neurodevelopment; poly(A) tail; RNA binding protein; ZC3H14

Indexed keywords

CALCIUM CALMODULIN DEPENDENT PROTEIN KINASE II; DROSOPHILA PROTEIN; FMRP PROTEIN; FRAGILE X MENTAL RETARDATION PROTEIN; FUTSCH PROTEIN; MEMBRANE PROTEIN; MESSENGER RNA; NAB2 PROTEIN; POLYADENYLATED RNA; RNA BINDING PROTEIN; UNCLASSIFIED DRUG; ZINC FINGER PROTEIN; FMR1 PROTEIN, DROSOPHILA; NAB2 PROTEIN, DROSOPHILA;

ADULT; ANIMAL CELL; ANIMAL EXPERIMENT; ANIMAL TISSUE; ARTICLE; AXON; CONTROLLED STUDY; CYTOPLASM; DENDRITE; DROSOPHILA; FEMALE; GENE CONTROL; GENE INTERACTION; GENE LOSS; GENE REPRESSION; GENETIC LINKAGE; HIPPOCAMPAL NEURONAL CULTURE; LOCOMOTION; MALE; MOUSE; MURINE; MUSHROOM BODY; NERVE CELL DIFFERENTIATION; NONHUMAN; OLFACTORY MEMORY; PHENOTYPE; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN PROTEIN INTERACTION; REGULATOR GENE; RNA TRANSLATION; TRANSGENE; ANIMAL; CELL CULTURE; GENE EXPRESSION REGULATION; GENE REGULATORY NETWORK; GENETICS; MEMORY; METABOLISM; NERVE CELL; ODOR; PHYSIOLOGY; TUMOR CELL LINE;

ANIMALS; CALCIUM-CALMODULIN-DEPENDENT PROTEIN KINASE TYPE 2; CELL LINE, TUMOR; CELLS, CULTURED; DROSOPHILA; DROSOPHILA PROTEINS; FEMALE; FRAGILE X MENTAL RETARDATION PROTEIN; GENE EXPRESSION REGULATION, DEVELOPMENTAL; GENE REGULATORY NETWORKS; MALE; MEMORY; MICE; NEURONS; RNA, MESSENGER; RNA-BINDING PROTEINS; SMELL;

EID: 85026889740     PISSN: None     EISSN: 22111247     Source Type: Journal    
DOI: 10.1016/j.celrep.2017.07.038     Document Type: Article

References (77)

1. Anderson, J.T., Wilson, S.M., Datar, K.V., Swanson, M.S., NAB2: a yeast nuclear polyadenylated RNA-binding protein essential for cell viability. Mol. Cell. Biol. 13 (1993), 2730–2741.
2. Antar, L.N., Li, C., Zhang, H., Carroll, R.C., Bassell, G.J., Local functions for FMRP in axon growth cone motility and activity-dependent regulation of filopodia and spine synapses. Mol. Cell. Neurosci. 32 (2006), 37–48.
3. Apponi, L.H., Leung, S.W., Williams, K.R., Valentini, S.R., Corbett, A.H., Pavlath, G.K., Loss of nuclear poly(A)-binding protein 1 causes defects in myogenesis and mRNA biogenesis. Hum. Mol. Genet. 19 (2010), 1058–1065.
4. Armstrong, J.D., de Belle, J.S., Wang, Z., Kaiser, K., Metamorphosis of the mushroom bodies; large-scale rearrangements of the neural substrates for associative learning and memory in Drosophila. Learn. Mem. 5 (1998), 102–114.
5. Ashraf, S.I., McLoon, A.L., Sclarsic, S.M., Kunes, S., Synaptic protein synthesis associated with memory is regulated by the RISC pathway in Drosophila. Cell 124 (2006), 191–205.
6. Barbee, S.A., Estes, P.S., Cziko, A.M., Hillebrand, J., Luedeman, R.A., Coller, J.M., Johnson, N., Howlett, I.C., Geng, C., Ueda, R., et al. Staufen- and FMRP-containing neuronal RNPs are structurally and functionally related to somatic P bodies. Neuron 52 (2006), 997–1009.
7. Bassell, G.J., Warren, S.T., Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Neuron 60 (2008), 201–214.
8. Bossie, M.A., DeHoratius, C., Barcelo, G., Silver, P., A mutant nuclear protein with similarity to RNA binding proteins interferes with nuclear import in yeast. Mol. Biol. Cell 3 (1992), 875–893.
9. Bozzetti, M.P., Specchia, V., Cattenoz, P.B., Laneve, P., Geusa, A., Sahin, H.B., Di Tommaso, S., Friscini, A., Massari, S., Diebold, C., Giangrande, A., The Drosophila fragile X mental retardation protein participates in the piRNA pathway. J. Cell Sci. 128 (2015), 2070–2084.
10. Castello, A., Fischer, B., Hentze, M.W., Preiss, T., RNA-binding proteins in Mendelian disease. Trends Genet. 29 (2013), 318–327.
11. Caudy, A.A., Myers, M., Hannon, G.J., Hammond, S.M., Fragile X-related protein and VIG associate with the RNA interference machinery. Genes Dev. 16 (2002), 2491–2496.
12. Chartier, A., Joly, W., Simonelig, M., Measurement of mRNA poly(A) tail lengths in Drosophila female germ cells and germ-line stem cells. Methods Mol. Biol. 1463 (2017), 93–102.
13. Chen, C.C., Wu, J.K., Lin, H.W., Pai, T.P., Fu, T.F., Wu, C.L., Tully, T., Chiang, A.S., Visualizing long-term memory formation in two neurons of the Drosophila brain. Science 335 (2012), 678–685.
14. Chintapalli, V.R., Al Bratty, M., Korzekwa, D., Watson, D.G., Dow, J.A., Mapping an atlas of tissue-specific Drosophila melanogaster metabolomes by high resolution mass spectrometry. PLoS ONE, 8, 2013, e78066.
15. Coyne, A.N., Yamada, S.B., Siddegowda, B.B., Estes, P.S., Zaepfel, B.L., Johannesmeyer, J.S., Lockwood, D.B., Pham, L.T., Hart, M.P., Cassel, J.A., et al. Fragile X protein mitigates TDP-43 toxicity by remodeling RNA granules and restoring translation. Hum. Mol. Genet. 24 (2015), 6886–6898.
16. Cziko, A.M., McCann, C.T., Howlett, I.C., Barbee, S.A., Duncan, R.P., Luedemann, R., Zarnescu, D., Zinsmaier, K.E., Parker, R.R., Ramaswami, M., Genetic modifiers of dFMR1 encode RNA granule components in Drosophila. Genetics 182 (2009), 1051–1060.
17. Darnell, J.C., Klann, E., The translation of translational control by FMRP: therapeutic targets for FXS. Nat. Neurosci. 16 (2013), 1530–1536.
18. Darnell, J.C., Van Driesche, S.J., Zhang, C., Hung, K.Y., Mele, A., Fraser, C.E., Stone, E.F., Chen, C., Fak, J.J., Chi, S.W., et al. FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell 146 (2011), 247–261.
19. Donlin-Asp, P.G., Rossoll, W., Bassell, G.J., Spatially and temporally regulating translation via mRNA-binding proteins in cellular and neuronal function. FEBS Lett. 591 (2017), 1508–1525.
20. Dunn, K.W., Kamocka, M.M., McDonald, J.H., A practical guide to evaluating colocalization in biological microscopy. Am. J. Physiol. Cell Physiol. 300 (2011), C723–C742.
21. Edens, B.M., Ajroud-Driss, S., Ma, L., Ma, Y.C., Molecular mechanisms and animal models of spinal muscular atrophy. Biochim. Biophys. Acta 1852 (2015), 685–692.
22. Eichhorn, S.W., Subtelny, A.O., Kronja, I., Kwasnieski, J.C., Orr-Weaver, T.L., Bartel, D.P., mRNA poly(A)-tail changes specified by deadenylation broadly reshape translation in Drosophila oocytes and early embryos. eLife, 5, 2016, e16955.
23. Feng, Y., Gutekunst, C.A., Eberhart, D.E., Yi, H., Warren, S.T., Hersch, S.M., Fragile X mental retardation protein: nucleocytoplasmic shuttling and association with somatodendritic ribosomes. J. Neurosci. 17 (1997), 1539–1547.
24. Franklin, T.J., Godfrey, A., Polyribosomes in rat-liver preparations. Biochem. J. 98 (1966), 513–521.
25. Green, D.M., Marfatia, K.A., Crafton, E.B., Zhang, X., Cheng, X., Corbett, A.H., Nab2p is required for poly(A) RNA export in Saccharomyces cerevisiae and is regulated by arginine methylation via Hmt1p. J. Biol. Chem. 277 (2002), 7752–7760.
26. Griffith, L.C., Verselis, L.M., Aitken, K.M., Kyriacou, C.P., Danho, W., Greenspan, R.J., Inhibition of calcium/calmodulin-dependent protein kinase in Drosophila disrupts behavioral plasticity. Neuron 10 (1993), 501–509.
27. Gross, C., Berry-Kravis, E.M., Bassell, G.J., Therapeutic strategies in fragile X syndrome: dysregulated mGluR signaling and beyond. Neuropsychopharmacology 37 (2012), 178–195.
28. Guillemin, I., Becker, M., Ociepka, K., Friauf, E., Nothwang, H.G., A subcellular prefractionation protocol for minute amounts of mammalian cell cultures and tissue. Proteomics 5 (2005), 35–45.
29. Heisenberg, M., Mushroom body memoir: from maps to models. Nat. Rev. Neurosci. 4 (2003), 266–275.
30. Hu, J., Gao, S., Mutant of RNA binding protein Zc3h14 causes cell growth delay/arrest through inducing multinucleation and DNA damage. JSM Biochem. Mol. Biol., 2, 2014, 1006.
31. Hummel, T., Krukkert, K., Roos, J., Davis, G., Klämbt, C., Drosophila Futsch/22C10 is a MAP1B-like protein required for dendritic and axonal development. Neuron 26 (2000), 357–370.
32. Ishizuka, A., Siomi, M.C., Siomi, H., A Drosophila fragile X protein interacts with components of RNAi and ribosomal proteins. Genes Dev. 16 (2002), 2497–2508.
33. Jin, P., Zarnescu, D.C., Ceman, S., Nakamoto, M., Mowrey, J., Jongens, T.A., Nelson, D.L., Moses, K., Warren, S.T., Biochemical and genetic interaction between the fragile X mental retardation protein and the microRNA pathway. Nat. Neurosci. 7 (2004), 113–117.
34. Kaech, S., Banker, G., Culturing hippocampal neurons. Nat. Protoc. 1 (2006), 2406–2415.
35. Keleman, K., Krüttner, S., Alenius, M., Dickson, B.J., Function of the Drosophila CPEB protein Orb2 in long-term courtship memory. Nat. Neurosci. 10 (2007), 1587–1593.
36. Kelly, S.M., Leung, S.W., Apponi, L.H., Bramley, A.M., Tran, E.J., Chekanova, J.A., Wente, S.R., Corbett, A.H., Recognition of polyadenosine RNA by the zinc finger domain of nuclear poly(A) RNA-binding protein 2 (Nab2) is required for correct mRNA 3′-end formation. J. Biol. Chem. 285 (2010), 26022–26032.
37. 3His tandem zinc-finger polyadenosine RNA binding proteins. RNA Biol. 9 (2012), 555–562.
38. Kelly, S.M., Leung, S.W., Pak, C., Banerjee, A., Moberg, K.H., Corbett, A.H., A conserved role for the zinc finger polyadenosine RNA binding protein, ZC3H14, in control of poly(A) tail length. RNA 20 (2014), 681–688.
39. Kelly, S.M., Bienkowski, R., Banerjee, A., Melicharek, D.J., Brewer, Z.A., Marenda, D.R., Corbett, A.H., Moberg, K.H., The Drosophila ortholog of the Zc3h14 RNA binding protein acts within neurons to pattern axon projection in the developing brain. Dev. Neurobiol. 76 (2016), 93–106.
40. Kim, M., Bellini, M., Ceman, S., Fragile X mental retardation protein FMRP binds mRNAs in the nucleus. Mol. Cell. Biol. 29 (2009), 214–228.
41. Krashes, M.J., Waddell, S., Drosophila aversive olfactory conditioning. Cold Spring Harb. Protoc., 2011, 2011 pdb.prot5608.
42. Kunz, T., Kraft, K.F., Technau, G.M., Urbach, R., Origin of Drosophila mushroom body neuroblasts and generation of divergent embryonic lineages. Development 139 (2012), 2510–2522.
43. Lee, T., Luo, L., Mosaic analysis with a repressible cell marker for studies of gene function in neuronal morphogenesis. Neuron 22 (1999), 451–461.
44. Leung, S.W., Apponi, L.H., Cornejo, O.E., Kitchen, C.M., Valentini, S.R., Pavlath, G.K., Dunham, C.M., Corbett, A.H., Splice variants of the human ZC3H14 gene generate multiple isoforms of a zinc finger polyadenosine RNA binding protein. Gene 439 (2009), 71–78.
45. Li, Y., Wang, X., Zhang, X., Goodrich, D.W., Human hHpr1/p84/Thoc1 regulates transcriptional elongation and physically links RNA polymerase II and RNA processing factors. Mol. Cell. Biol. 25 (2005), 4023–4033.
46. Lu, R., Wang, H., Liang, Z., Ku, L., O'donnell, W.T., Li, W., Warren, S.T., Feng, Y., The fragile X protein controls microtubule-associated protein 1B translation and microtubule stability in brain neuron development. Proc. Natl. Acad. Sci. USA 101 (2004), 15201–15206.
47. Malik, B.R., Hodge, J.J., CASK and CaMKII function in Drosophila memory. Front. Neurosci., 8, 2014, 178.
48. Malik, B.R., Gillespie, J.M., Hodge, J.J., CASK and CaMKII function in the mushroom body α′/β′ neurons during Drosophila memory formation. Front. Neural Circuits, 7, 2013, 52.
49. Mastushita-Sakai, T., White-Grindley, E., Samuelson, J., Seidel, C., Si, K., Drosophila Orb2 targets genes involved in neuronal growth, synapse formation, and protein turnover. Proc. Natl. Acad. Sci. USA 107 (2010), 11987–11992.
50. Michel, C.I., Kraft, R., Restifo, L.L., Defective neuronal development in the mushroom bodies of Drosophila fragile X mental retardation 1 mutants. J. Neurosci. 24 (2004), 5798–5809.
51. Moore, M.J., From birth to death: the complex lives of eukaryotic mRNAs. Science 309 (2005), 1514–1518.
52. Morales, J., Hiesinger, P.R., Schroeder, A.J., Kume, K., Verstreken, P., Jackson, F.R., Nelson, D.L., Hassan, B.A., Drosophila fragile X protein, DFXR, regulates neuronal morphology and function in the brain. Neuron 34 (2002), 961–972.
53. Muddashetty, R.S., Kelić, S., Gross, C., Xu, M., Bassell, G.J., 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 (2007), 5338–5348.
54. Muddashetty, R.S., Nalavadi, V.C., Gross, C., Yao, X., Xing, L., Laur, O., Warren, S.T., Bassell, G.J., Reversible inhibition of PSD-95 mRNA translation by miR-125a, FMRP phosphorylation, and mGluR signaling. Mol. Cell 42 (2011), 673–688.
55. Napoli, I., Mercaldo, V., Boyl, P.P., Eleuteri, B., Zalfa, F., De Rubeis, S., Di Marino, D., Mohr, E., Massimi, M., Falconi, M., et al. The fragile X syndrome protein represses activity-dependent translation through CYFIP1, a new 4E-BP. Cell 134 (2008), 1042–1054.
56. Pak, C., Garshasbi, M., Kahrizi, K., Gross, C., Apponi, L.H., Noto, J.J., Kelly, S.M., Leung, S.W., Tzschach, A., Behjati, F., et al. Mutation of the conserved polyadenosine RNA binding protein, ZC3H14/dNab2, impairs neural function in Drosophila and humans. Proc. Natl. Acad. Sci. USA 108 (2011), 12390–12395.
57. Preiss, T., Hentze, M.W., From factors to mechanisms: translation and translational control in eukaryotes. Curr. Opin. Genet. Dev. 9 (1999), 515–521.
58. Rha, J., Jones, S.K., Fidler, J., Banerjee, A., Leung, S.W., Morris, K.J., Wong, J.C., Inglis, G.A.S., Shapiro, L., Deng, Q., et al. The RNA-binding protein, ZC3H14, is required for proper poly(A) tail length control, expression of synaptic proteins, and brain function in mice. Hum. Mol. Genet., 2017, 10.1093/hmg/ddx248 Published online June 29, 2017.
59. Richter, J.D., Bassell, G.J., Klann, E., Dysregulation and restoration of translational homeostasis in fragile X syndrome. Nat. Rev. Neurosci. 16 (2015), 595–605.
60. Roos, J., Hummel, T., Ng, N., Klämbt, C., Davis, G.W., Drosophila Futsch regulates synaptic microtubule organization and is necessary for synaptic growth. Neuron 26 (2000), 371–382.
61. Roux, P.P., Shahbazian, D., Vu, H., Holz, M.K., Cohen, M.S., Taunton, J., Sonenberg, N., Blenis, J., RAS/ERK signaling promotes site-specific ribosomal protein S6 phosphorylation via RSK and stimulates cap-dependent translation. J. Biol. Chem. 282 (2007), 14056–14064.
62. Santoro, M.R., Bray, S.M., Warren, S.T., Molecular mechanisms of fragile X syndrome: a twenty-year perspective. Annu. Rev. Pathol. 7 (2012), 219–245.
63. Santos, A.R., Kanellopoulos, A.K., Bagni, C., Learning and behavioral deficits associated with the absence of the fragile X mental retardation protein: what a fly and mouse model can teach us. Learn. Mem. 21 (2014), 543–555.
64. Schenck, A., Bardoni, B., Moro, A., Bagni, C., Mandel, J.L., A highly conserved protein family interacting with the fragile X mental retardation protein (FMRP) and displaying selective interactions with FMRP-related proteins FXR1P and FXR2P. Proc. Natl. Acad. Sci. USA 98 (2001), 8844–8849.
65. Schenck, A., Bardoni, B., Langmann, C., Harden, N., Mandel, J.L., Giangrande, A., CYFIP/Sra-1 controls neuronal connectivity in Drosophila and links the Rac1 GTPase pathway to the fragile X protein. Neuron 38 (2003), 887–898.
66. Siller, S.S., Broadie, K., Neural circuit architecture defects in a Drosophila model of fragile X syndrome are alleviated by minocycline treatment and genetic removal of matrix metalloproteinase. Dis. Model. Mech. 4 (2011), 673–685.
67. Stackpole, E.E., Akins, M.R., Fallon, J.R., N-myristoylation regulates the axonal distribution of the fragile X-related protein FXR2P. Mol. Cell. Neurosci. 62 (2014), 42–50.
68. Stefani, G., Fraser, C.E., Darnell, J.C., Darnell, R.B., Fragile X mental retardation protein is associated with translating polyribosomes in neuronal cells. J. Neurosci. 24 (2004), 7272–7276.
69. Subtelny, A.O., Eichhorn, S.W., Chen, G.R., Sive, H., Bartel, D.P., Poly(A)-tail profiling reveals an embryonic switch in translational control. Nature 508 (2014), 66–71.
70. Sudhakaran, I.P., Hillebrand, J., Dervan, A., Das, S., Holohan, E.E., Hülsmeier, J., Sarov, M., Parker, R., VijayRaghavan, K., Ramaswami, M., FMRP and Ataxin-2 function together in long-term olfactory habituation and neuronal translational control. Proc. Natl. Acad. Sci. USA 111 (2014), E99–E108.
71. Tully, T., Quinn, W.G., Classical conditioning and retention in normal and mutant Drosophila melanogaster. J. Comp. Physiol. A Neuroethol. Sens. Neural Behav. Physiol. 157 (1985), 263–277.
72. Udagawa, T., Swanger, S.A., Takeuchi, K., Kim, J.H., Nalavadi, V., Shin, J., Lorenz, L.J., Zukin, R.S., Bassell, G.J., Richter, J.D., Bidirectional control of mRNA translation and synaptic plasticity by the cytoplasmic polyadenylation complex. Mol. Cell 47 (2012), 253–266.
73. Udagawa, T., Farny, N.G., Jakovcevski, M., Kaphzan, H., Alarcon, J.M., Anilkumar, S., Ivshina, M., Hurt, J.A., Nagaoka, K., Nalavadi, V.C., et al. Genetic and acute CPEB1 depletion ameliorate fragile X pathophysiology. Nat. Med. 19 (2013), 1473–1477.
74. Wan, L., Dockendorff, T.C., Jongens, T.A., Dreyfuss, G., Characterization of dFMR1, a Drosophila melanogaster homolog of the fragile X mental retardation protein. Mol. Cell. Biol. 20 (2000), 8536–8547.
75. Yang, Z., Edenberg, H.J., Davis, R.L., Isolation of mRNA from specific tissues of Drosophila by mRNA tagging. Nucleic Acids Res., 33, 2005, e148.
76. Zalfa, F., Giorgi, M., Primerano, B., Moro, A., Di Penta, A., Reis, S., Oostra, B., Bagni, C., The fragile X syndrome protein FMRP associates with BC1 RNA and regulates the translation of specific mRNAs at synapses. Cell 112 (2003), 317–327.
77. Zhang, Y.Q., Bailey, A.M., Matthies, H.J., Renden, R.B., Smith, M.A., Speese, S.D., Rubin, G.M., Broadie, K., Drosophila fragile X-related gene regulates the MAP1B homolog Futsch to control synaptic structure and function. Cell 107 (2001), 591–603.