Human FMRP contains an integral tandem Agenet (Tudor) and KH motif in the amino terminal domain

Human Molecular Genetics

Volumn 24, Issue 6, 2015, Pages 1733-1740

  Myrick, Leila K ^a   Hashimoto, Hideharu ^a   Cheng, Xiaodong ^a   Warren, Stephen T ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN; FMR1 PROTEIN, HUMAN;

ACTION POTENTIAL DURATION; AMINO TERMINAL SEQUENCE; ARTICLE; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; CRYSTAL STRUCTURE; CRYSTALLOGRAPHY; DNA DAMAGE; GENE MUTATION; HUMAN; INTEGRAL TANDEM AGENET; KH MOTIF; MASS SPECTROMETRY; MATRIX ASSISTED LASER DESORPTION IONIZATION TIME OF FLIGHT MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN DEGRADATION; PROTEIN DOMAIN; PROTEIN EXPRESSION; PROTEIN FUNCTION; PROTEIN MOTIF; PROTEIN PROTEIN INTERACTION; PROTEIN SECONDARY STRUCTURE; RNA BINDING; SIGNAL TRANSDUCTION; CHEMISTRY; GENETICS; METABOLISM; MISSENSE MUTATION; PROTEIN TERTIARY STRUCTURE;

AMINO ACID MOTIFS; FRAGILE X MENTAL RETARDATION PROTEIN; HUMANS; MUTATION, MISSENSE; PROTEIN STRUCTURE, TERTIARY;

EID: 84925387280     PISSN: 09646906     EISSN: 14602083     Source Type: Journal    
DOI: 10.1093/hmg/ddu586     Document Type: Article

References (42)

1. Bassell, G.J. andWarren, S.T. (2008) Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Neuron, 60, 201-214.
2. Santoro, M.R., Bray, S.M. and Warren, S.T. (2012) Molecular mechanisms of fragile X syndrome: a twenty-year perspective. Annu. Rev. Pathol., 7, 219-245.
3. Ashley, C.T. Jr, Wilkinson, K.D., Reines, D. and Warren, S.T. (1993) FMR1 protein: conserved RNP family domains and selective RNA binding. Science, 262, 563-566.
4. Brown, V., Jin, P., Ceman, S., Darnell, J.C., O'Donnell, W.T., Tenenbaum, S.A., Jin, X., Feng, Y., Wilkinson, K.D., Keene, J. D. et al. (2001) Microarray identification of FMRP-associated brain mRNAs and altered mRNA translational profiles in fragile X syndrome. Cell, 107, 477-487.
5. 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. (2011) FMRP stalls ribosomal translocation on mRNAs linked to synaptic function and autism. Cell, 146, 247-261.
6. Huber, K.M., Gallagher, S.M., Warren, S.T. and Bear, M.F. (2002) Altered synaptic plasticity in a mouse model of fragile X mental retardation. Proc. Natl. Acad. Sci. USA, 99, 7746-7750.
7. Osterweil, E.K., Krueger, D.D., Reinhold, K. and Bear, M.F. (2010) Hypersensitivity to mGluR5 and ERK1/2 leads to excessive protein synthesis in the hippocampus of a mouse model of fragile X syndrome. J. Neurosci., 30, 15616-15627.
8. Volk, L.J., Pfeiffer, B.E., Gibson, J.R. and Huber, K.M. (2007) Multiple Gq-coupled receptors converge on a common protein synthesis-dependent long-term depression that is affected in fragile X syndrome mental retardation. J. Neurosci., 27, 11624-11634.
9. Wang, H., Wu, L.J., Kim, S.S., Lee, F.J., Gong, B., Toyoda, H., Ren, M., Shang, Y.Z., Xu, H., Liu, F. et al. (2008) FMRP acts as a key messenger for dopamine modulation in the forebrain. Neuron, 59, 634-647.
10. 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.
11. Myrick, L.K., Nakamoto-Kinoshita, M., Lindor, N.M., Kirmani, S., Cheng, X. and Warren, S.T. (2014) Fragile X syndrome due to a missense mutation. Eur. J. Hum. Genet., 22, 1185-1189.
12. Bardoni, B., Schenck, A. and Mandel, J.L. (1999) A novel RNAbinding nuclear protein that interacts with the fragile X mental retardation (FMR1) protein. Hum. Mol. Genet., 8, 2557-2566.
13. Schenck, A., Bardoni, B., Moro, A., Bagni, C. and Mandel, J.L. (2001) 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, 8844-8849.
14. Bardoni, B., Castets, M., Huot, M.E., Schenck, A., Adinolfi, S., Corbin, F., Pastore, A., Khandjian, E.W. and Mandel, J.L. (2003) 82-FIP, a novel FMRP (fragile X mental retardation protein) interacting protein, shows a cell cycle-dependent intracellular localization. Hum. Mol. Genet., 12, 1689-1698.
15. Deng, P.Y., Rotman, Z., Blundon, J.A., Cho, Y., Cui, J., Cavalli, V., Zakharenko, S.S. and Klyachko, V.A. (2013) FMRP regulates neurotransmitter release and synaptic information transmission by modulating action potential duration via BK channels. Neuron, 77, 696-711.
16. Eberhart, D.E., Malter, H.E., Feng, Y. and Warren, S.T. (1996) The fragile X mental retardation protein is a ribonucleoprotein containing both nuclear localization and nuclear export signals. Hum. Mol. Genet., 5, 1083-1091.
17. Alpatov, R., Lesch, B.J., Nakamoto-Kinoshita, M., Blanco, A., Chen, S., Stutzer, A., Armache, K.J., Simon, M.D., Xu, C., Ali, M. et al. (2014) A chromatin-dependent role of the fragile X mental retardation protein FMRP in the DNA damage response. Cell, 157, 869-881.
18. Myrick, L.K., Deng, P.Y., Hashimoto, H., Oh, Y., Cho, Y., Poidevin, M.J., Suhl, J.A., Visootsak, J., Cavalli, V., Jin, P. et al. (2014) An independent role for presynaptic FMRP revealed by an FMR1 missense mutation associated with intellectual disability and seizures. PNAS, (in press).
19. Adinolfi, S., Ramos, A., Martin, S.R., Dal Piaz, F., Pucci, P., Bardoni, B., Mandel, J.L. and Pastore, A. (2003) The N-terminus of the fragile X mental retardation protein contains a novel domain involved in dimerization and RNA binding. Biochemistry, 42, 10437-10444.
20. Adinolfi, S., Bagni, C., Musco, G., Gibson, T., Mazzarella, L. and Pastore, A. (1999) Dissecting FMR1, the protein responsible for fragile X syndrome, in its structural and functional domains. RNA, 5, 1248-1258.
21. Yan, X. and Denman, R.B. (2011) Conformational-dependent and independent RNA binding to the fragile X mental retardation protein. J Nucleic Acids, 2011, 246127.
22. Zalfa, F., Adinolfi, S., Napoli, I., Kuhn-Holsken, E., Urlaub, H., Achsel, T., Pastore, A. and Bagni, C. (2005) Fragile X mental retardation protein (FMRP) binds specifically to the brain cytoplasmic RNAs BC1/BC200 via a novel RNA-binding motif. J. Biol. Chem., 280, 33403-33410.
23. Zalfa, F., Giorgi, M., Primerano, B., Moro, A., Di Penta, A., Reis, S., Oostra, B. and 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.
24. Wang, H., Iacoangeli, A., Lin, D., Williams, K., Denman, R.B., Hellen, C.U. and Tiedge, H. (2005) Dendritic BC1 RNA in translational control mechanisms. J. Cell Biol., 171, 811-821.
25. Iacoangeli, A., Rozhdestvensky, T.S., Dolzhanskaya, N., Tournier, B., Schutt, J., Brosius, J., Denman, R.B., Khandjian, E.W., Kindler, S. and Tiedge, H. (2008) On BC1 RNA and the fragile X mental retardation protein. Proc. Natl. Acad. Sci. USA, 105, 734-739.
26. Gabus, C., Mazroui, R., Tremblay, S., Khandjian, E.W. andDarlix, J.L. (2004) The fragile X mental retardation protein has nucleic acid chaperone properties. Nucleic Acids Res., 32, 2129-2137.
27. Johnson, E.M., Kinoshita, Y., Weinreb, D.B., Wortman, M.J., Simon, R., Khalili, K., Winckler, B. and Gordon, J. (2006) Role of Pur alpha in targeting mRNA to sites of translation in hippocampal neuronal dendrites. J. Neurosci. Res., 83, 929-943.
28. Lacoux, C., Di Marino, D., Boyl, P.P., Zalfa, F., Yan, B., Ciotti, M. T., Falconi, M., Urlaub, H., Achsel, T., Mougin, A. et al. (2012) BC1-FMRP interaction is modulated by 2'-O-methylation: RNA-binding activity of the tudor domain and translational regulation at synapses. Nucleic Acids Res., 40, 4086-4096.
29. Reeve, S.P., Lin, X., Sahin, B.H., Jiang, F., Yao, A., Liu, Z., Zhi, H., Broadie, K., Li, W., Giangrande, A. et al. (2008) Mutational analysis establishes a critical role for the N terminus of fragile X mental retardation protein FMRP. J. Neurosci., 28, 3221-3226.
30. Holm, L. and Rosenstrom, P. (2010) Dali server: conservation mapping in 3D. Nucleic Acids Res., 38, W545-549.
31. Arita, K., Isogai, S., Oda, T., Unoki, M., Sugita, K., Sekiyama, N., Kuwata, K., Hamamoto, R., Tochio, H., Sato, M. et al. (2012) Recognition of modification status on a histone H3 tail by linked histone reader modules of the epigenetic regulator UHRF1. Proc. Natl. Acad. Sci. USA, 109, 12950-12955.
32. Law, J.A., Du, J., Hale, C.J., Feng, S., Krajewski, K., Palanca, A. M., Strahl, B.D., Patel, D.J. and Jacobsen, S.E. (2013) Polymerase IV occupancy at RNA-directed DNA methylation sites requires SHH1. Nature, 498, 385-389.
33. Ramos, A., Hollingworth, D., Adinolfi, S., Castets, M., Kelly, G., Frenkiel, T.A., Bardoni, B. and Pastore, A. (2006) The structure of the N-terminal domain of the fragile X mental retardation protein: a platform for protein-protein interaction. Structure, 14, 21-31.
34. Adams-Cioaba, M.A., Guo, Y., Bian, C., Amaya, M.F., Lam, R., Wasney, G.A., Vedadi, M., Xu, C. and Min, J. (2010) Structural studies of the tandem Tudor domains of fragile X mental retardation related proteins FXR1 and FXR2. PLoS One, 5, e13559.
35. Valverde, R., Edwards, L. and Regan, L. (2008) Structure and function of KH domains. FEBS J, 275, 2712-2726.
36. Valverde, R., Pozdnyakova, I., Kajander, T., Venkatraman, J. and Regan, L. (2007) Fragile X mental retardation syndrome: structure of the KH1-KH2 domains of fragile X mental retardation protein. Structure, 15, 1090-1098.
37. Collins, S.C., Bray, S.M., Suhl, J.A., Cutler, D.J., Coffee, B., Zwick, M.E. and Warren, S.T. (2010) Identification of novel FMR1 variants by massively parallel sequencing in developmentally delayed males. Am. J. Med. Genet. A, 152A, 2512-2520.
38. Maurer-Stroh, S., Dickens, N.J., Hughes-Davies, L., Kouzarides, T., Eisenhaber, F. and Ponting, C.P. (2003) The Tudor domain 'Royal Family': Tudor, plant Agenet, Chromo, PWWP and MBT domains. Trends Biochem. Sci., 28, 69-74.
39. Otwinowski, Z., Borek, D., Majewski, W. and Minor, W. (2003) Multiparametric scaling of diffraction intensities. Acta Crystallogr. A, 59, 228-234.
40. Karplus, P.A. and Diederichs, K. (2012) Linking crystallographic model and data quality. Science, 336, 1030-1033.
41. Emsley, P., Lohkamp, B., Scott, W.G. and Cowtan, K. (2010) Features and development of Coot. Acta Crystallogr. D Biol. Crystallogr., 66, 486-501.
42. Adams, P.D., Afonine, P.V., Bunkoczi, G., Chen, V.B., Davis, I. W., Echols, N., Headd, J.J., Hung, L.W., Kapral, G.J., Grosse-Kunstleve, R.W. et al. (2010) PHENIX: a comprehensive Python-based system for macromolecular structure solution. Acta Crystallogr. D Biol. Crystallogr., 66, 213-221.