A new regulatory function of the region proximal to the RGG box in the fragile X mental retardation protein

Journal of Cell Science

Volumn 124, Issue 18, 2011, Pages 3060-3065

  Blackwell, Ernest ^a   Ceman, Stephanie ^a  

^a UNIVERSITY OF ILLINOIS AT URBANA CHAMPAIGN   (United States)

Author keywords

FMRP; Granules; Polyribosome; RGG box; RNA binding protein

Indexed keywords

FRAGILE X MENTAL RETARDATION PROTEIN; ISOPROTEIN; Y BOX BINDING PROTEIN 1;

ANIMAL CELL; ANIMAL TISSUE; ANTIBODY AFFINITY; ARTICLE; CONTROLLED STUDY; EXON; MALE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; POLYSOME; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN FUNCTION;

ALTERNATIVE SPLICING; ANIMALS; BRAIN; CELL LINE; COGNITION; CYTOPLASMIC GRANULES; EXONS; FRAGILE X MENTAL RETARDATION PROTEIN; FRAGILE X SYNDROME; HUMANS; MICE; MICE, INBRED CBA; PROTEIN BINDING; PROTEIN CONFORMATION; PROTEIN ISOFORMS; REGULATORY SEQUENCES, NUCLEIC ACID; RNA, MESSENGER; Y-BOX-BINDING PROTEIN 1;

EID: 80054026347     PISSN: 00219533     EISSN: 14779137     Source Type: Journal    
DOI: 10.1242/jcs.086751     Document Type: Article

References (39)

1. Antar, L. N., Afroz, R., Dictenberg, J. B., Carroll, R. C. and Bassell, G. J (2004). Metabotropic glutamate receptor activation regulates fragile x mental retardation protein and FMR1 mRNA localization differentially in dendrites and at synapses. J. Neurosci. 24, 2648-2655.
2. Aschrafi, A., Cunningham, B. A., Edelman, G. M. and Vanderklish, P. W. (2005). The fragile X mental retardation protein and group I metabotropic glutamate receptors regulate levels of mRNA granules in brain. Proc. Natl. Acad. Sci. USA 102, 2180-2185.
3. Ashley, C. T., Sutcliffe, J. S., Kunst, C. B., Leiner, H. A., Eichler, E. E., Nelson, D. L. and Warren, S. T. (1993). Human and murine FMR-1: alternative splicing and translational initiation downstream of the CGG-repeat. Nat. Genet. 4, 244-251.
4. Bardoni, B., Schenck, A. and Mandel, J.-L. (2001). The Fragile X mental retardation protein. Brain Res. Bull. 56, 375.
5. Bassell, G. J. and Warren, S. T. (2008). Fragile X syndrome: loss of local mRNA regulation alters synaptic development and function. Neuron 60, 201-214.
6. Beaulieu, M. A. (2002). A distinct FMRP polysomal population at an advanced stage of mammalian erythropoiesis. Biochem. Biophys. Res. Commun. 275, 608-610.
7. Blackwell, E., Zhang, X. and Ceman, S. (2010). Arginines of the RGG box regulate FMRP association with polyribosomes and mRNA. Hum. Mol. Genet. 19, 1530-1539.
8. 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.
9. Carpenter, A. E., Jones, T. R., Lamprecht, M. R., Clarke, C., Kang, I. H., Friman, O., Guertin, D. A., Chang, J. H., Lindquist, R. A., Moffat, J. et al. (2006). CellProfiler: image analysis software for identifying and quantifying cell phenotypes. Genome Biol. 7, R100.
10. Ceman S, Brown V and Warren, S. T. (1999). Isolation of an FMRP-associated messenger ribonucleoprotein particle and identification of nucleolin and the fragile Xrelated proteins as components of the complex. Mol. Cell. Biol. 19, 7925-7932.
11. Ceman, S., Nelson, R. and Warren, S. T. (2000). Identification of mouse YB1/p50 as a component of the FMRP-associated mRNP particle. Biochem. Biophys. Res. Commun. 279, 904-908.
12. Ceman, S., O'Donnell, W. T., Reed, M., Patton, S., Pohl, J. and Warren, S. T. (2003). Phosphorylation influences the translation state of FMRP-associated polyribosomes. Hum. Mol. Genet. 12, 3295-3305.
13. Coffee, R. L., Tessier, C. R., Woodruff, E. A. and Broadie, K. (2010). Fragile X mental retardation protein has a unique, evolutionarily conserved neuronal function not shared with FXR1P or FXR2P. Dis. Model. Mech. 3, 471-485.
14. Darnell, J. C., Jensen, K. B., Jin, P., Brown, V., Warren, S. T. and Darnell, R. B. (2001). Fragile X mental retardation protein targets G quartet mRNAs important for neuronal function. Cell 107, 489-499.
15. Darnell, J. C., Fraser, C. E., Mostovetsky, O. and Darnell, R. B. (2009). Discrimination of common and unique RNA-binding activities among Fragile-X mental retardation protein paralogs. Hum. Mol. Genet. 18, 3164-3177.
16. Davidovic, L., Bechara, E., Gravel, M., Jaglin, X. H., Tremblay, S., Sik, A., Bardoni, B. and Khandjian, E. W. (2006). The nuclear microspherule protein 58 is a novel RNA-binding protein that interacts with fragile X mental retardation protein in polyribosomal mRNPs from neurons. Hum. Mol. Genet. 15, 1525-1538.
17. Denman, R. B. and Sung, Y. J. (2002). Species-specific and isoform-specific RNA binding of human and mouse fragile X mental retardation proteins. Biochem. Biophys. Res. Commun. 292, 1063-1069.
18. Dolzhanskaya, N., Merz, G. and Denman, R. B. (2006). Alternative splicing modulates protein arginine methyltransferase-dependent methylation of fragile X syndrome mental retardation protein. Biochemistry 45, 10385-10393.
19. Dolzhanskaya, N., Bolton, D. C. and Denman, R. B. (2008). Chemical and structural probing of the N-Terminal residues encoded by FMR1 exon 15 and their effect on downstream arginine methylation,Ć. Biochemistry 47, 8491.
20. Eichler, E. E., Richards, S., Gibbs, R. A. and Nelson, D. L. (1993). Fine structure of the human FMR1 gene. Hum. Mol. Genet. 2, 1147-1153.
21. Evdokimova, V. M., Wei, C. L., Sitikov, A. S., Simonenko, P. N., Lazarev, O. A., Vasilenko, K. S., Ustinov, V. A., Hershey, J. W. and Ovchinnikov, L. P. (1995). The major protein of messenger ribonucleoprotein particles in somatic cells is a member of the Y-box binding transcription factor family. J. Biol. Chem. 270, 3186-3192.
22. Funakoshi, T., Kobayashi, S., Ohashi, S., Sato, T. A. and Anzai, K. (2003). Isolation and characterization of brain Y-box protein: developmentally regulated expression, polyribosomal association and dendritic localization. Brain Res. Mol. Brain Res. 118, 1-9.
23. Gary, J. D. and Clarke, S. (1998). RNA and protein interactions modulated by protein arginine methylation. Prog. Nucleic Acid Res. Mol. Biol. 61, 65-130.
24. Kanai, Y., Dohmae, N. and Hirokawa, N. (2004). Kinesin transports RNA isolation and characterization of an RNA-transporting granule. Neuron 43, 513-525.
25. Khandjian, E. W., Bardoni, B., Corbin, F., Sittler, A., Giroux, S., Heitz, D., Tremblay, S., Pinset, C., Montarras, D., Rousseau, F. et al. (1998). Novel isoforms of the fragile X related protein FXR1P are expressed during myogenesis. Hum. Mol. Genet. 7, 2121-2128.
26. Kim, M., Bellini, M. and Ceman, S. (2009). Fragile X mental retardation protein FMRP binds mRNAs in the nucleus. Mol. Cell. Biol. 29, 214-228.
27. Levenga, J., Buijsen, R. A. M., Rifé, M., Moine, H., Nelson, D. L., Oostra, B. A., Willemsen, R. and de Vrij, F. M. S. (2009). Ultrastructural analysis of the functional domains in FMRP using primary hippocampal mouse neurons. Neurobiol. Dis. 35, 241.
28. Ling, S. C., Fahrner, P. S., Greenough, W. T. and Gelfand, V. I. (2004). Transport of Drosophila fragile X mental retardation protein-containing ribonucleoprotein granules by kinesin-1 and cytoplasmic dynein. Proc. Natl. Acad. Sci. USA 101, 17428-17433.
29. Mazroui, R., Huot, M. E., Tremblay, S., Filion, C., Labelle, Y. and Khandjian, E.W. (2002). Trapping of messenger RNA by Fragile X Mental Retardation protein into cytoplasmic granules induces translation repression. Hum. Mol. Genet. 11, 3007-3017.
30. Mazroui, R., Huot, M. E., Tremblay, S., Boilard, N., Labelle, Y. and Khandjian, E. W. (2003). Fragile X Mental Retardation protein determinants required for its association with polyribosomal mRNPs. Hum. Mol. Genet. 12, 3087-3096.
31. Menon, R. P., Gibson, T. J. and Pastore, A. (2004). The C terminus of fragile X mental retardation protein interacts with the multi-domain Ran-binding protein in the microtubule-organising centre. J. Mol. Biol. 343, 43-53.
32. Minich, B., Maidebura, I. P. and Ovchinnikov, L. P. (1993). Purification and characterization of the major 50-kDa repressor protein from cytoplasmic mRNP of rabbit reticulocytes. Eur. J. Biochem. 212, 633-638.
33. Reis, S., Willemsen, R., van Unen, L., Hoogeveen, A. and Oostra, B. (2004). Prospects of TAT-mediated protein therapy for Fragile X syndrome. J. Mol. Histol. 35, 389.
34. Schaeffer, C., Bardoni, B., Mandel, J. L., Ehresmann, B., Ehresmann, C. and Moine, H. (2001). The fragile X mental retardation protein binds specifically to its mRNA via a purine quartet motif. EMBO J. 20, 4803-4813.
35. Siomi, M., Higashijima, K., Ishizuka, A. and Siomi, H. (2002). Casein kinase II phosphorylates the Fragile X Mental Retardation protein and modulates its biological properties. Mol. Cell. Biol. 22, 8438-8447.
36. Skabkin, M. A., Kiselyova, O. I., Chernov, K. G., Sorokin, A. V., Dubrovin, E. V., Yaminsky, I. V., Vasiliev, V. D. and Ovchinnikov, L. P. (2004). Structural organization of mRNA complexes with major core mRNP protein YB-1. Nucleic Acids Res. 32, 5621-5635.
37. Stetler, A., Winograd, C., Sayegh, J., Cheever, A., Patton, E., Zhang, X., Clarke, S. and Ceman, S. (2006). Identification and characterization of the methyl arginines in the fragile X mental retardation protein Fmrp. Hum. Mol. Genet. 15, 87-96.
38. Winograd, C., Clayton, D. and Ceman, S. (2008). Expression of fragile X mental retardation protein within the vocal control system of developing and adult male zebra finches. Neuroscience 157, 132-142.
39. Xie, W., Dolzhanskaya, N., LaFauci, G., Dobkin, C. and Denman, R. B. (2009). Tissue and developmental regulation of fragile X mental retardation 1 exon 12 and 15 isoforms. Neurobiol. Dis. 35, 52-62.