The fragile X-related proteins FXR1P and FXR2P contain a functional nucleolar-targeting signal equivalent to the HIV-1 regulatory proteins

Human Molecular Genetics

Volumn 9, Issue 10, 2000, Pages 1487-1493

  Tamanini, Filippo ^a   Kirkpatrick, Laura L ^b   Schonkeren, Joris ^a   Van Unen, Leontine ^a   Bontekoe, Carola ^a   Bakker, Cathy ^a   Nelson, David L ^b   Galjaard, Hans ^a   Oostra, Ben A ^a   Hoogeveen, André T ^a  

^a ERASMUS UNIVERSITY ROTTERDAM   (Netherlands)

^b BAYLOR COLLEGE OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

LEPTOMYCIN B; NUCLEAR PROTEIN; REGULATOR PROTEIN; RNA BINDING PROTEIN; SIGNAL PEPTIDE; SYNTHETIC PEPTIDE; VIRUS PROTEIN;

ALTERNATIVE RNA SPLICING; AMINO ACID SEQUENCE; ANIMAL CELL; ARTICLE; CARBOXY TERMINAL SEQUENCE; CELL NUCLEUS; CELLULAR DISTRIBUTION; CONTROLLED STUDY; DNA TRANSFECTION; FIBROBLAST CULTURE; FRAGILE X SYNDROME; HUMAN IMMUNODEFICIENCY VIRUS 1; NONHUMAN; NUCLEOLUS; PRIORITY JOURNAL; PROTEIN LOCALIZATION;

ANIMALIA; HUMAN IMMUNODEFICIENCY VIRUS; HUMAN IMMUNODEFICIENCY VIRUS 1;

EID: 18744434657     PISSN: 09646906     EISSN: None     Source Type: Journal    
DOI: 10.1093/hmg/9.10.1487     Document Type: Article

References (55)

1. Verkerk, A.J., Pieretti, M., Sutcliffe, J.S., Fu, Y.H., Kuhl, D.P., Pizzuti, A., Reiner, O., Richards, S., Victoria, M.F., Zhang, F.P. et al. (1991) Identification of a gene (FMR-1) containing a CGG repeat coincident with a breakpoint cluster region exhibiting length variation in fragile X syndrome. Cell, 65, 905-914.
2. Pieretti, M., Zhang, F.P., Fu, Y.H., Warren, S.T., Oostra, B.A., Caskey, C.T. and Nelson, D.L. (1991) Absence of expression of the FMR-1 gene in fragile X syndrome. Cell, 66, 817-822.
3. Oberlé, I., Rousseau, F., Heitz, D., Kretz, C., Devys, D., Hanauer, A., Boue, J., Bertheas, M.F. and Mandel, J.L. (1991) Instability of a 550-base pair DNA segment and abnormal methylation in fragile X syndrome. Science, 252, 1097-1102.
4. Hoogeveen, A.T. and Oostra, B.A. (1997) The fragile X syndrome. J. Inherit. Metab. Dis., 20, 139-151.
5. Kambach, C. and Mattaj, I.W. (1992) Intracellular distribution of the U1A protein depends on active transport and nuclear binding to U1 snRNA. J. Cell Biol., 118, 11-21.
6. Siomi, H., Siomi, M.C., Nussbaum, R.L. and Dreyfuss, G. (1993) The protein product of the fragile X gene, FMR1, has characteristics of an RNA-binding protein. Cell, 74, 291-298.
7. Siomi, H., Choi, M., Siomi, M.C., Nussbaum, R.L. and Dreyfuss, G. (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.
8. Ashley Jr, C., Wilkinson, K.D., Reines, D. and Warren, S.T. (1993) FMR1 protein: conserved RNP family domains and selective RNA binding. Science, 262, 563-568.
9. Verheij, C., De Graaff, E., Bakker, C.E., Willemsen, R., Willems, P.J., Meijer, N., Galjaard, H., Reuser, A.J.J., Oostra, B.A. and Hoogeveen, A.T. (1995) Characterization of FMR1 proteins isolated from different tissues. Hum. Mol. Genet., 4, 895-901.
10. Willemsen, R., Bontekoe, C., Tamanini, F., Galjaard, H., Hoogeveen, A.T. and Oostra, B.A. (1996) Association of FMRP with ribosomal precursor particles in the nucleolus. Biochem. Biophys. Res. Commun., 225, 27-33.
11. Khandjian, E., Corbin, F., Woerly, S. and Rousseau, F. (1996) The fragile X mental retardation protein is associated with ribosomes. Nature Genet., 12, 91-93.
12. Tamanini, F., Meijer, N., Verheij, C., Willems, P.J., Galjaard, H., Oostra, B.A. and Hoogeveen, A.T. (1996) FMRP is associated to the ribosomes via RNA. Hum. Mol. Genet., 5, 809-813.
13. + mRNA in actively translating polyribosomes. Hum. Mol. Genet., 6, 1465-1472.
14. Eberhart, D.E., Malter, H.E., Feng, Y. and Warren, S.T. (1996) The fragile X mental retardation protein is a ribosonucleoprotein containing both nuclear localization and nuclear export signals. Hum. Mol. Genet., 5, 1083-1091.
15. Fridell, R.A., Benson, R.E., Hua, J., Bogerd, H.P. and Cullen, B.R. (1996) A nuclear role for the fragile X mental retardation protein. EMBO J., 15, 5408-5414.
16. Bardoni, B., Sittler, A., Shen, Y. and Mandel, J.L. (1997) Analysis of domains affecting intracellular localization of the FMRP protein. Neurobiol. Dis., 4, 329-336.
17. Siomi, M.C., Siomi, H., Sauer, W.H., Srinivasan, S., Nussbaum, R.L. and Dreyfuss, G. (1995) FXR1, an autosomal homolog of the fragile X mental retardation gene. EMBO J., 14, 2401-2408.
18. Zhang, Y., Oconnor, J.P., Siomi, M.C., Srinivasan. S., Dutra, A., Nussbaum, R.L. and Dreyfuss, G. (1995) The fragile X mental retardation syndrome protein interacts with novel homologs FXR1 and FXR2. EMBO J., 14, 5358-5366.
19. Coy, J.F., Sedlacek, Z., Bachner, D., Hameister, H., Joos, S., Lichter, P., Delius, H. and Poustka, A. (1995) Highly conserved 3′UTR and expression pattern of FXR1 points to a divergent gene regulation of FXR1 and FMR1. Hum. Mol. Genet., 4, 2209-2218.
20. Siomi, M.C., Zhang, Y., Siomi, H. and Dreyfuss, G. (1996) Specific sequences in the fragile X syndrome protein FMR1 and the FXR proteins mediate their binding to 60S ribosomal subunits and the interactions among them. Mol. Cell. Biol., 16, 3825-3832.
21. Feng, Y., Gutekunst, C.A., Eberhart, D.E., Yi, H., Warren, S.T. and Hersch, S.M. (1997) Fragile X mental retardation protein: nucleocytoplasmic shuttling and association with somatodendritic ribosomes. J. Neurosci., 17, 1539-1547.
22. Ceman, S., Brown, V. and Warren, S.T. (1999) Isolation of an FMRP-associated messenger ribonucleoprotein particle and identification of nucleolin and the fragile X-related proteins as components of the complex. Mol. Cell. Biol., 19, 7925-7932.
23. Tamanini, F., Van Unen, L., Bakker, C., Sacchi, N., Galjaard, H., Oostra, B.A. and Hoogeveen, A.T. (1999) Oligomerization properties of fragile-X mental-retardation protein (FMRP) and the fragile-X-related proteins FXR1P and FXR2P. Biochem. J., 343, 517-523.
24. Tamanini, F., Willemsen, R., van Unen, L., Bontekoe, C., Galjaard, H., Oostra, B.A. and Hoogeveen, A.T. (1997) Differential expression of FMR1, FXR1 and FXR2 proteins in human brain and testis. Hum. Mol. Genet., 6, 1315-1322.
25. Khandjian, E.W., Bardoni, B., Corbin, F., Sittler, A., Giroux, S., Heitz, D., Tremblay, S., Pinset, C., Montarras, D., Rousseau, F. and Mandel, J. (1998) Novel isoforms of the fragile X related protein FXR1P are expressed during myogenesis. Hum. Mol. Genet., 7, 2121-2128.
26. Kirkpatrick, L.L., McIlwain, K.A. and Nelson, D.L. (1999) Alternative splicing in the murine and human FXR1 genes. Genomics, 59, 193-202.
27. Tamanini, F., Bontekoe, C., Bakker, C.E., van Unen, L., Anar, B., Willemsen, R., Yoshida, M., Galjaard, H., Oostra, B.A. and Hoogeveen, A.T. (1999) Different targets for the fragile X-related proteins revealed by their distinct nuclear localizations. Hum. Mol. Genet., 8, 863-869.
28. Kubota, S., Siomi, H., Satoh, T., Endo, S., Maki, M. and Hatanaka, M. (1989) Functional similarity of HIV-1 rev and HTLV-1 rex proteins: identification of a new nucleolar-targeting signal in rev protein. Biochem. Biophys. Res. Commun., 162, 963-970.
29. Siomi, H., Shida, H., Nam, S.H., Nosaka, T., Maki, M. and Hatanaka, M. (1988) Sequence requirements for nucleolar localization of human T cell leukemia virus type I pX protein, which regulates viral RNA processing. Cell, 55, 197-209.
30. Agulhon, C., Blanchet, P., Kobetz, A., Marchant, D., Faucon, N., Sarda, P., Moraine, C., Sittler, A., Biancalana, V., Malafosse, A. and Abitbol, M. (1999) Expression of FMR1, FXR1, and FXR2 genes in human prenatal tissues. J. Neuropathol. Exp. Neurol., 58, 867-880.
31. Bardoni, B., Schenck, A. and Mandel, J.L. (1999) A novel RNA-binding nuclear protein that interacts with the fragile X mental retardation (FMR1) protein. Hum. Mol. Genet., 8, 2557-2566.
32. Schmidt-Zachmann, M.S. and Nigg, E.A. (1993) Protein localization to the nucleolus: a search for targeting domains in nucleolin. J Cell Sci., 105, 799-806.
33. Verkerk, A.J., De Graaff, E., De Boulle, K., Eichler, E.E., Konecki, D.S., Reyniers, E., Manca, A., Poustka, A., Willems, P.J., Nelson, D.L. and Oostra, B.A. (1993) Alternative splicing in the fragile X gene FMR1. Hum. Mol. Genet., 2, 399-404.
34. Sittler, A., Devys, D., Weber, C. and Mandel, J.-L. (1996) Alternative splicing of exon 14 determines nuclear or cytoplasmic localisation of FMR1 protein isoforms. Hum. Mol. Genet., 5, 95-102.
35. Endo, S., Kubota, S., Siomi, H., Adachi, A., Oroszlan, S., Maki, M. and Hatanaka, M. (1989) A region of basic amino-acid cluster in HIV-1 Tat protein is essential for trans-acting activity and nucleolar localization. Virus Genes, 3, 99-110.
36. Kubota, S., Copeland, T.D. and Pomerantz, R.J. (1999) Nuclear and nucleolar targeting of human ribosomal protein S25: common features shared with HIV-1 regulatory proteins. Oncogene. 18, 1503-1514.
37. Malim, M.H., Hauber, J., Le, S.Y., Maizel, J.V. and Cullen, B.R. (1989) The HIV-1 rev trans-activator acts through a structured target sequence to activate nuclear export of unspliced viral mRNA. Nature, 338, 254-257.
38. Meyer, B.E. and Malim, M.H. (1994) The HIV-1 Rev trans-activator shuttles between the nucleus and the cytoplasm. Genes Dev., 8, 1538-1547.
39. Malim, M.H. and Cullen, B.R. (1991) HIV-1 structural gene expression requires the binding of multiple Rev monomers to the viral RRE: implications for HIV-1 latency. Cell, 65, 241-248.
40. Neville, M., Stutz, F., Lee, L., Davis, L.I. and Rosbash, M. (1997) The importin-beta family member Crm1p bridges the interaction between Rev and the nuclear pore complex during nuclear export. Curr. Biol., 7, 767-775.
41. Fornerod, M., Ohno, M., Yoshida, M. and Mattaj, I.W. (1997) CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90, 1051-1060.
42. Bogerd, H.P., Echarri, A., Ross, T.M. and Cullen, B.R. (1998) Inhibition of human immunodeficiency virus Rev and human T-cell leukemia virus Rex function, but not Mason-Pfizer monkey virus constitutive transport element activity, by a mutant human nucleoporin targeted to Crml. J. Virol., 12, 8627-8635.
43. Tan, R. and Frankel, A.D. (1998) A novel glutamine-RNA interaction identified by screening libraries in mammalian cells. Proc. Natl Acad. Sci. USA, 95, 4247-4252.
44. Tang, C.K. and Draper, D.E. (1990) Evidence for allosteric coupling between the ribosome and repressor binding sites of a translationally regulated mRNA. Biochemistry, 29, 4434-4439.
45. Li, Z., Paulovich, A.G. and Woolford Jr, J.L. (1995) Feedback inhibition of the yeast ribosomal protein gene CRY2 is mediated by the nucleotide sequence and secondary structure of CRY2 pre-mRNA. Mol. Cell. Biol., 15, 6454-6464.
46. Eng, F.J. and Warner, J.R. (1991) Structural basis for the regulation of splicing of a yeast messenger RNA. Cell, 65, 797-804.
47. Brown, V., Small, K., Lakkis, L., Feng, Y., Gunter, C., Wilkinson, K.D. and Warren, S.T. (1998) Purified recombinant Fmrp exhibits selective RNA binding as an intrinsic property of the fragile X mental retardation protein. J. Biol. Chem., 273, 15521-15527.
48. Tuteja, R. and Tuteja, N. (1998) Nucleolin: a multifunctional major nucleolar phosphoprotein. Crit. Rev. Biochem. Mol. Biol., 33, 407-436.
49. Bolivar, J., Guelman, S., Iglesias, C., Ortiz, M. and Valdivia, M.M. (1998) The fragile-X-related gene FXRI is a human autoantigen processed during apoptosis. J. Biol. Chem., 273, 17122-17127.
50. Okawa-Takatsuji, M., Aotsuka, S., Uwatoko, S., Sumiya, M. and Yokohari, R. (1992) The B cell repertoire in patients with systemic autoimmune diseases: analysis of Epstein-Barr virus (EBV)-inducible circulating precursors that produce autoantibodies against nuclear ribonucleoprotein (nRNP). Clin. Exp. Immunol., 90, 415-421.
51. Schwarze, S.R., Ho, A., Vocero-Akbani, A. and Dowdy, S.F. (1999) In vivo protein transduction: delivery of a biologically active protein into the mouse. Science, 285, 1569-1572.
52. Aarts, M.M., Rix, A., Guo, J., Bringhurst, R. and Henderson, J.E. (1999) The nucleolar targeting signal (NTS) of parathyroid hormone related protein mediates endocytosis and nucleolar translocation. J. Bone Miner. Res., 14, 1493-1503.
53. Verheij, C., Bakker, C.E., de Graaff, E., Keulemans, J., Willemsen, R., Verkerk, A.J., Galjaard, H., Reuser, A.J., Hoogeveen, A.T. and Oostra, B.A. (1993) Characterization and localization of the FMR-1 gene product associated with fragile X syndrome. Nature, 363, 722-724.
54. Laemmli, U.K. (1970) Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature, 227, 680-685.
55. Devys, D., Lutz, Y., Rouyer, N., Bellocq, J.P. and Mandel, J.L. (1993) The FMR-1 protein is cytoplasmic, most abundant in neurons and appears normal in carriers of a fragile X premutation. Nature Genet., 4, 335-340.