Isolation of an FMRP-associated messenger ribonucleoprotein particle and identification of nucleolin and the fragile X-related proteins as components of the complex

Molecular and Cellular Biology

Volumn 19, Issue 12, 1999, Pages 7925-7932

  Ceman, Stephanie ^a   Brown, Victoria ^a   Warren, Stephen T ^a  

^a EMORY UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

NUCLEOLIN; RIBONUCLEOPROTEIN;

ANIMAL CELL; ARTICLE; CELL CULTURE; CHROMOSOME FRAGILE SITE; GENE LOSS; IMMUNOPRECIPITATION; MASS SPECTROMETRY; MULTIGENE FAMILY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ANALYSIS; PROTEIN ISOLATION;

EID: 0033499661     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.19.12.7925     Document Type: Article

References (46)

1. Ashlej, C. T., J. S. Sutcliffe, C. B. Kunst, H. A. Leiner, E. E. Eichler, D. L. Nelson, and S. T. Warren. 1993. Human and murine FMR-1: alternative splicing and translational initiation downstream of the CGG repeat. Nat. Genet. 4:244-251.
2. Ashley, C. T., and S. T. Warren. 1995. Trinucleotide repeat expansion and human disease. Annu. Rev. Genet. 29:703-728.
3. Ashley, C. T., K. D. Wilkinson, D. Reines, and S. T. Warren. 1993. FMR1 protein: conserved RNP family domains and selective RNA binding. Science. 262:563-566.
4. Borer, R. A., C. F. Lehner, H. M. Eppenberger, and E. A. Nigg. 1989, Major nucleolar proteins shuttle between nucleus and cytoplasm. Cell 56:379-390.
5. Bouche, G., F. Amalric, M. Caizergues-Ferrer, and J. P. Zalta. 1979. Effects of heat shock on gene expression and subcellular protein distribution in Chinese hamster ovary cells. Nucleic Acids. Res. 7:1739-1747.
6. Bouvet, P., J. J. Diaz, K. Kindbeiter, J. J. Madjar, and F. Amalric. 1998. Nucleolin interacts with several ribosomal proteins through its RGG domain. J. Biol. Chem. 273:19025-19029.
7. Brown, V., K. Small, L. Lakkis, Y. Feng, C. Gunter, K. D. Wilkinson, and S. T. Warren. 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.
8. Bugler, B., M. Caizergues-Ferrer, G. Bouche, H. Bourbon, and F. Amalric. 1982. Detection and localization of a class of proteins immunologically related to a 100-kDa nucleolar protein. Eur. J. Biochem. 128:475-480.
9. Coffee, B., F. Zhang, S. T. Warren, and D. Reines. 1999. Acetylated histones are associated with FMR1 in normal but not fragile X-syndrome cells. Nat. Genet, 22:98-101.
10. Consortium, D.-B. F. X. 1994. FMR1 knockout mice: a model to study fragile X mental retardation. Cell 78:23-33.
11. Dreyfuss, G., M. J. Matunis, S. Pinol-Roma, and C. G. Burd. 1993. hnRNP proteins and the biogenesis of mRNA. Annu. Rev. Biochem. 62:289-321.
12. Eberhart, D. E., H. E. Malter, Y. Feng, and S. T. Warren. 1996. The fragile X mental retardation protein is a ribonucleoprotein containing both nuclear localization and nuclear export signals. Hum. Mol. Genet. 5:1083-1091.
13. Eberhart, D. E., and S. T. Warren. 1996. The molecular basis of fragile X syndrome. Cold Spring Harbor Symp. Quant. Biol. 61:679-687.
14. Feng, Y., D. Absher, D. E. Eberhart, V. Brown, H. Malter, and S. T. Warren. 1997. FMRP associates with polyribosomes as an mRNP, and the 1304N mutation of severe fragile X syndrome abolishes this association. Mol. Cell 1:109-118.
15. Feng, Y., C.-A. Gutekunst, D. E. Eberhart, H. Yi, S. T. Warren, and S. M. Hersch. 1997. Fragile X mental retardation protein: nucleocytoplasmic shuttling and association with somatodendritic ribosomes. J. Neurosci. 17:1539-1547.
16. Ghisolfi, L., A. Kharrat, G. Joseph, F. Amalric, and M. Erard. 1992. Concerted activities of the RNA recognition and the glycine-rich C-terminal domains of nucleolin are required for efficient complex formation with preribosornal RNA. Eur. J. Biochem. 209:541-548.
17. Hamilton, B. J., E. Nagy, J. S. Malters, B. A. Arrick, and W. F. C. Rigby. 1993. Association of heterogeneous nuclear ribonucleoprotein A1 and C proteins with reiterated AUUUA sequences. J. Biol. Chem. 268:8881-8887.
18. Hornstra, I. K., D. L. Nelson, S. T. Warren, and T. P. Yang. 1993. High resolution methylation analysis of the FMR1 gene trinucleotide repeat region in fragile X syndrome. Hum. Mol. Genet. 2:1659-1665.
19. Kondo, K., L. R. Kowalski, and M. Inouye. 1992. Cold shock induction of yeast NSR1 protein and its role in pre-rRNA processing. J. Biol. Chem. 267:16259-16265.
20. Lapeyre, B., F. Amalric, S. H. Ghaffari, S. V. Rao, T. S. Dumbar, and M. O. Olson. 1986. Protein and cDNA sequence of a glycine-rich, dimethylarginine-containing region located near the carboxyl-terminal end of nucleolin (C23 and 100 kDa). J. Biol. Chem. 261:9167-9173.
21. Lee, W. C., Z. X. Xue, and T. Melese. 1991. The NSR1 gene encodes a protein that specifically binds nuclear localization sequences and has two RNA recognition motifs. J. Cell Biol. 112:1-12.
22. Lee, W. C., D. Zabetakis, and T. Melese. 1992. NSR1 is required for prerRNA processing and for the proper maintenance of steady-state levels of ribosomal subunits. Mol. Cell. Biol. 12:3865-3871.
23. Li, Z., K. Wilkinson, S. T. Warren, and Y. Feng. Selective translation inhibition in vitro by the fragile X mental retardation protein. Submitted for publication.
24. Limprasert, P., N. Zhong, C. Dobkin, and W. T. Brown. 1997. Polymorphism of FXR1 showing lack of association with autism. Am. J. Med. Genet. 74:453-454.
25. Long, E. O., S. Rosen-Bronson, D. R. Karp, M. Malnati, R. P. Sekaly, and D. Jaraqueraada. 1991. Efficient cDNA expression vectors for stable and transient expression of HLA-DR in transfected fibroblast and lymphoid cells. Hum. Immunol. 31:229-235.
26. Martin, M., L. F. Garcia-Fernandez, S. M. Diaz de la Espina, J. Noaillac-Depeyre, N. Gas, and F. Javier Medina. 1992. Identification and localization of a nucleolin homologue in onion nucleoli. Exp. Cell Res. 199:74-84.
27. Miranda, G. A., I. Chokler, and R. J. Aguilera. 1995. The murine nucleolin protein is an inducible DNA and ATP binding protein which is readily detected in nuclear extracts of lipopolysaccharide-treated splenocytes. Exp. Cell Res. 217:294-308.
28. Oberle, I., R. Heilig, J. P. Moisan, and C. Kloepfer. 1986. Fragile-X mental retardation syndrome with two flanking polymorphic DNA markers. Proc. Natl. Acad. Sci. USA 83:1016-1020.
29. Orrick, L. R., M. O. Olson, and H. Busch. 1973. Comparison of nucleolar proteins of normal liver and Novikoff hepatoma ascites cells by two-dimensional polyacrylamide gel electrophoresis. Proc. Natl. Acad. Sci. USA 70: 1316-1320.
30. Pieretti, M., F. Zhang, Y. H. Fu, S. T. Warren, B. A. Oostra, C. T. Caskey, and D. L. Nelson. 1991. Absence of expression of the FMR-1 gene in fragile X syndrome. Cell 66:817-822.
31. Price, D. K., F. Zhang, C. T. Ashley, and S. T. Warren. 1996. The chicken FMR1 gene is highly conserved with a CCT 5′ untranslated repeat and encodes an RNA-binding protein. Genomics 31:3-12.
32. Sant, A., J., N. S. Braunstein, and R. N. Germain. 1987. Predominant role of amino-terminal sequences in dictating efficiency of class II major histocompatibility complex alpha beta dimer expression. Proc. Natl. Acad. Sci. USA 84:8065-8069.
33. Schmidt-Zachmann, M. S., and E. A. Nigg. 1993. Protein localization to the nucleolus: a search for targeting domains in nucleolin. J. Cell Sci. 105:799-806.
34. 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.
35. Siomi, H., M. C. Siomi, R. L. Nussbaum, and G. Dreyfuss. 1993. The protein product of the fragile X gene, FMR1, has characteristics of an RNA binding protein. Cell 74:291-298.
36. Siomi, M., H. Siomi, W. H. Sauer, S. Srinivasan, R. L. Nussbaum, and G. Dreyfuss. 1995. FXR1, an autosomal homolog of the fragile X mental retardation gene. EMBO J. 14:2401-2408.
37. Siomi, M. C., Y. Zhang, H. Siomi, and G. Dreyfuss. 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.
38. Sittler, A., D. Devys, C. Weber, and J.-L. Mandel. 1996. Alternative splicing of exon 14 determines nuclear or cytoplasmic localisation of fmr1 protein isoforms. Hum. Mol. Genet. 5:95-102.
39. Sutcliffe, J. S., D. L. Nelson, F. Zhang, M. Pieretti, C. T. Caskey, D. Saxe, and S. T. Warren. 1992. DNA methylation represses FMR-1 transcription in fragile X syndrome. Hum. Mol. Genet. 1:397-400.
40. Tamanini, F., N. Meijer, C. Verheij, P. J. Willems, H. Galjaard, B. A. Oostra, and A. T. Hoogeveen. 1996. FMRP is associated to the ribosomes via RNA. Hum. Mol. Genet. 5:809-813.
41. Warren, S. T., and S. L. Sherman. The fragile X syndrome. In C. R, Scriver, A. L. Beaudet, W. S. Sly, and D. Valle (ed.), The metabolic and molecular basis of inherited disease, 8th ed., in press. McGraw-Hill Book Co., New York, N.Y.
42. Willemsen, R., C. F. T. Bontekoe, H. Galjaard, A. Hoogeveen, and B. Oostra. 1996. Association of FMRP with ribosomal precursor particles in the nucleolus. Biochem. Biophys. Res. Commun. 225:27-33.
43. Xue, Z., X. Shan, B. Lapeyre, and T. Melese. 1993. The amino terminus of mammalian nucleolin specifically recognizes SV40 T-antigen type nuclear localization sequences. Eur. J. Cell Biol. 62:13-21.
44. Yurkova, M. S., and M. T. Murray. 1997. A translation regulatory particle containing the Xenopus oocyte Y box protein mRNP3+4. J. Biol. Chem. 272:10870-10876.
45. Zaidi, S. H., and J. S. Malter. 1995. Nucleolin and heterogeneous nuclear ribonucleoprotein C proteins specifically interact with the 3′-untranslated region of amyloid protein precursor mRNA. J. Biol. Chem. 270:17292-17298.
46. Zhang, Y., J. P. O'Connor, M. C. Siomi, S. Srinivasan, A. Dutra, R. L. Nussbaum, and G. Dreyfuss. 1995. The fragile X mental retardation syndrome protein interacts with novel homologs FXR1 and FXR2. EMBO J. 14:5358-5366.