An unusual fibrillarin gene and protein: Structure and functional implications

Molecular Biology of the Cell

Volumn 8, Issue 6, 1997, Pages 1051-1061

  David, Emina ^a   McNeil, J Bryan ^a,b   Basile, Vincenzo ^a   Pearlman, Ronald E ^a  

^a YORK UNIVERSITY   (Canada)

^b AMGEN INC   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

FIBRILLARIN; RIBOSOME DNA; RIBOSOME RNA; RNA PRECURSOR;

AMINO ACID SEQUENCE; ARTICLE; IMMUNOCYTOCHEMISTRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN DETERMINATION; RNA PROCESSING; STRUCTURE ACTIVITY RELATION; TETRAHYMENA THERMOPHILA;

EUKARYOTA; MYXOZOA; PROTOZOA; SACCHAROMYCES CEREVISIAE; TETRAHYMENA; TETRAHYMENA THERMOPHILA;

EID: 0030910228     PISSN: 10591524     EISSN: None     Source Type: Journal    
DOI: 10.1091/mbc.8.6.1051     Document Type: Article

References (66)

1. Aris, J.P., and Bloebel, G. (1991). cDNA cloning and sequencing of human fibrillarin, a conserved nucleolar protein recognized by autoimmune antisera. Proc. Natl. Acad. Sci. USA 88, 931-935.
2. Balakin, A.G., Smith, L., and Fournier, M.J. (1996). The RNA world of the nucleolus: two major families of small RNAs defined by different box elements with related function. Cell 86, 823-834.
3. Baserga, S.J., Yang, X.W., and Steitz, J.A. (1991). An intact box C sequence in the U3 snRNA is required for binding of fibrillarin, the protein common to the major family of nucleolar snRNPs. EMBO J. 10, 2645-2651.
4. Broach, J.R., Li, Y.Y., Wu, L.C.C., and Jayarum, M. (1983). Vectors for inducible high-level expression in yeast. In: Experimental Manipulation of Gene Expression, ed. M. Inouye, Academic Press: New York, 100-101.
5. Cappai, R., Osborn, A.H., and Handman, E. (1994). Cloning and sequence of a Leishmania major homologue to the fibrillarin gene. Mol. Biochem. Parasitol. 64, 353-355.
6. Cassidy-Hanley, D., Bowen, J., Lee, J., Cole, E.S., VerPlank, L.A., Gaertig, J., Gorovsky, M.A., and Bruns, P.J. (1997). Germline and somatic transformation of mating Tetrahymena thermophila by particle bombardment. Genetics 146, 135-147.
7. Chen, D.-C., Yang, B.-C., and Kuo, T.-T. (1992). One step transformation of yeast in stationary phase. Curr. Genet. 21, 83-84.
8. Dente, L., Cesarini, G., and Cortese, R. (1983). pEMBL: a new family of single stranded plasmids. Nucleic Acids Res. 11, 1645-1655.
9. Dobson, M.J., Pearlman, R.E., Karaiskakis, A., Spyropolous, B., and Moens, P.B. (1994). Synaptonemal complex proteins: occurrence, epitope mapping and chromosome disjunction. J. Cell Sci. 107, 2749-2760.
10. Don, R.H., Cox, P.T., Wainwright, B.J., Baker, K., and Mattick, J.S. (1991). 'Touchdown' PCR to circumvent spurious priming during gene amplification. Nucleic Acids Res. 19, 4008.
11. Engberg, J. (1985). The ribosomal RNA genes of Tetrahymena: structure and function. Eur. J. Cell Biol. 36, 133-151.
12. Gaertig, J., Gu, L., Hai, B., and Gorovsky, M.A. (1994). High frequency vector-mediated transformation and gene replacement in Tetrahymena. Nucleic Acids Res. 22, 5391-5398.
13. Ghisolfi, L., Gerard, J., Amalric, F., and Erard, M. (1992). The glycine-rich domain of nucleolin has an unusual supersecondary structure responsible for its RNA-helix-destabilizing properties. J. Biol. Chem. 267, 2955-2959.
14. Girard, J.P., Feliu, M., Caizergues-Ferrer, M., and Lapeyre, B. (1993). Schizosaccharomyces pombe is sensitive to cold shock. Nucleic Acids Res. 21, 1881-1887.
15. Girard, J.R., Lehtonen, H., Caizergues-Ferrer, M., Amalric, F., Tollervey, D., and Lapeyre, B. (1992). GAR1 is an essential small nucleolar RNP protein required for pre-rRNA processing in yeast. EMBO J. 11, 673-682.
16. Golding, G.B., Tsao, N., and Pearlman, R.E. (1994). Evidence for intron capture: an unusual path for the evolution of proteins. Proc. Natl. Acad. Sci. USA 91, 7506-7509.
17. Gorovsky, M.A., Yao, M.-C., Keevert, J.B., and Pleger G.L. (1975). Isolation of micro-and macronuclei of Tetrahymena pyriformis. Methods Cell Biol. 9, 311-327.
18. Heinonen, T.Y.K., and Pearlman, R.E. (1994). A germ line-specific sequence element in an intron in Tetrahymena thermophila. J. Biol. Chem. 269, 17428-17433.
19. Henriquez, R., Bloebel, G., and Aris, J.P. (1990). Isolation and sequencing of NOP1. J. Biol. Chem. 265, 2209-2215.
20. Higashinakagawa, T., Narushima-Iio, M., Saiga, H., Kondo, S., and Mita, T. (1992). Properties of extrachromosomal nucleoli from Tetrahymena pyriformis. Chromosoma 101, 413-419.
21. Higgins, D., and Sharp, P.M. (1989). Fast and sensitive multiple sequence alignments on a microcomputer. Comput. Appl. Biosci. 5, 151-153.
22. Hozak, P. (1995). Catching RNA polymerase I in flagranti: ribosomal genes are transcribed in the dense fibrillar component of the nucleolus. Exp. Cell Res. 216, 285-289.
23. Hughes, J.M.X., and Ares, M., Jr. (1991). Depletion of U3 small nucleolar RNA inhibits cleavage in the 5́ external transcribed spacer of yeast pre-ribosomal RNA and impairs formation of 18S ribosomal RNA. EMBO J. 10, 4231-4239.
24. Hugle, B., Hazan, R., Scheer, U., and Francke, W.W. (1985a). Localization of ribosomal protein S1 in the granular component of the interphase nucleolus and its distribution during mitosis. J. Cell Biol. 100, 873-886.
25. r. 40,000 protein specific to precursor particles of the large ribosomal subunit. Cell 41, 615-627.
26. Jansen, R.P., Hurt, E.C., Kern, H., Lehtonen, H., Carmo-Fonseca, M., Lapeyre, B., and Tollervey, D. (1991). Evolutionary conservation of the human nucleolar protein fibrillarin and its functional expression in yeast. J. Cell Biol. 113, 715-729.
27. Jong, A.Y.S., Clark, M.W., Gilbert, M., Oehm, A., and Campbell, J.L. (1987). Saccharomyces cerevisiae SSB1 protein and its relationship to nucleolar RNA-binding proteins. Mol. Cell. Biol. 7, 2947-2955.
28. Kass, S., Tyc, K., Steitz, J.A., and Sollner-Webb, B. (1990). The U3 small nucleolar ribonucleoprotein functions in the first step of pre-ribosomal RNA processing. Cell 60, 897-908.
29. Laemmli, U.K. (1970). Cleavage of structural proteins during the assembly of the head of bacteriophage T4. Nature 227, 680-685.
30. Lapeyre, B. (1992). GAR1 is an essential small nucleolar RNP protein required for pre-rRNA processing in yeast. EMBO J. 11, 673-682.
31. Lapeyre, B., Bourbon, H., and Amalric, F. (1987). Nucleolin, the major nucleolar protein of growing eukaryotic cells: an unusual protein structure revealed by the nucleotide sequence. Proc. Nat. Acad. Sci. USA 84, 1472-1476.
32. Lapeyre, B., Mariottini, P., Matheiu, C., Ferrer, P., Amaldi, F., Amalric, F., and Caizergues-Ferre, M. (1990). Molecular cloning of Xenopus fibrillarin, a conserved U3 small nuclear ribonucleoprotein recognized by antisera from humans with autoimmune disease. Mol. Cell. Biol. 10, 430-434.
33. Lee, W.C., Xue, Z., and Melese, T. (1991). The NSR1 gene encodes a protein that specifically binds nuclear localization sequences and has two RNA recognition motifs. J. Cell Biol. 113, 1-12.
34. G-dimethylarginine. J. Biol. Chem. 260, 14304-14310.
35. Maxwell, E.S., and Fournier, M.J. (1995). The nucleolar small RNAs. Annu. Rev. Biochem. 35, 897-934.
36. Najbauer, J., Johnson, B.A., Young, A.L., and Aswad, D.W. (1993). Peptides with sequences similar to glycine, arginine-rich motifs in proteins interacting with RNA are efficiently recognized by methyltransferase(s) modifying arginine in numerous proteins. J. Biol. Chem. 268, 10501-10509.
37. Nilsson, J.R., and Leick, V. (1970). Nucleolar organization and ribosome formation in Tetrahymena pyriformis GL. Exp. Cell Res. 60, 361-372.
38. Ochs, R.L., Lischwe, M.A., Shen, E., Carrol, R.E., and Busch, H. (1985a). Nucleologenesis: composition and fate of prenucleolar bodies. Chromosoma 92, 330-336.
39. Ochs, R.L., Lischwe, M.A., Spohn, W.H., and Busch, H. (1985b). Fibrillarin: a new protein of the nucleolus identified by autoimmune sera. Biol. Cell. 54, 123-134.
40. Orum, H., Neilsen, H., and Engberg, J. (1993). Sequence and proposed secondary structure of the Tetrahymena thermophila U3-snRNA. Nucleic Acids Res. 21, 2511.
41. Parker, K.A., and Steitz, J.A. (1987). Structural analyses of the human U3 ribonucleoprotein particle reveal a conserved sequence available for base pairing with pre-rRNA. Mol. Cell. Biol. 7, 2899-2913.
42. Potter, S., Durovic, P., and Dennis, P. (1995). Ribosomal RNA precursor processing by a eukaryotic U3 small nucleolar RNA-like molecule in an archaeon. Science 268, 1056-1060.
43. Prescott, D. (1994). The DNA of ciliated protozoa. Microbiol. Rev. 58, 233-267.
44. Raska, I., Dundr, M., Koberna, K., Melcak, I., Risueno, M.-C., and Torok, I. (1995). Does the synthesis of ribosomal RNA take place within nucleolar fibrillar centers or dense fibrillar components? A critical appraisal. J. Struct. Biol. 114, 1-22.
45. Russell, I.D., and Tollervey, D. (1992). NOP3 is an essential yeast protein which is required for pre-rRNA processing. J. Cell Biol. 119, 737-747.
46. Saitou, N., and Nei, M. (1987). The neighbour joining method: a new method for constructing phylogenetic trees. Mol. Biol. Evol. 4, 406-425.
47. Sambrook, J., Fritsch, E.F., and Maniatis, T. (1989). Molecular Cloning: A Laboratory Manual, 2nd ed., Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
48. Sanger, F., Nicklen, S., and Coulson, A.R. (1977). DNA sequencing with chain terminating inhibitors. Proc. Natl. Acad. Sci. USA 74, 5466-5467.
49. Scheer, U., and Rose, K.M. (1984). Localization of RNA polymerase I in interphase cells and mitotic chromosomes by light and electron microscopic immunocytochemistry. Proc. Natl. Acad. Sci. USA 81, 1431-1435.
50. Schimmang, T., Tollervey, T., Kern, H., Frank, R., and Hurt, E.C. (1989). A yeast nucleolar protein related to mammalian fibrillarin is associated with small nucleolar RNA and is essential for viability. EMBO J. 13, 4015-4024.
51. Schmidt-Zachmann, M., Hugle-Dorr, B., and Francke, W.W. (1987). A constitutive nucleolar protein identified as a member of the nucleoplasmin family. EMBO J. 6, 1881-1890.
52. Shen, X., Yu, L., Weir, J.W., and Gorovsky, M.A. (1995). Linker histones are not essential and affect chromatin condensation in vivo. Cell 82, 47-56.
53. Sherman, F., Fink, G.R., and Hicks, J.B. (1986). Methods in Yeast Genetics: A Laboratory Course Manual, Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press.
54. Spector, D.L., Ochs, R.L., and Busch, H. (1984). Silver staining immunofluorescence and immunoelectron microscopic localization of nucleolar phosphoproteins B23 and C23. Chromosoma 90, 139-148.
55. Stargell, L.A., and Gorovsky, M.A. (1994). TATA-binding protein and nuclear differentiation in Tetrahymena thermophila. Mol. Cell. Biol. 14, 723-734.
56. Takemasa, T., Takagi, T., Kobayashi, T., Konishi, K., and Watanabe, Y. (1990). The third calmodulin family protein in Tetrahymena. Cloning of the cDNA for Tetrahymena calcium-binding protein of 23 kDa (TCBP-23). J. Biol. Chem. 265, 2514-2517.
57. Tollervey, D., Lehtonen, H., Carmo-Fonseca, M., and Hurt, E.C. (1991). The small nucleolar RNP protein NOP1 (fibrillarin) is required for pre-rRNA processing in yeast. EMBO J. 10, 573-583.
58. Tourancheau, A.B., Tsao, N., Klobutcher, L.A., Pearlman, R.E., and Adoutte, A. (1995). Genetic code deviations in the ciliates: evidence for multiple and independent events. EMBO J. 14, 3262-3267.
59. Turley, S.J., Tan, E.M., and Pollard, K.M. (1993). Molecular cloning and sequence analysis of U3 snoRNA-associated mouse fibrillarin. Biochim. Biophys. Acta 1216, 119-122.
60. Tyc, K., and Steitz, J.A. (1989). U3, U8 and U13 comprise a new class of mammalian snRNPs localized in the cell nucleolus. EMBO J. 8, 3113-3119.
61. Vernet, T., Dignard, D., and Thomas, D.Y. (1987). A family of yeast expression vectors containing the phage f1 intergenic region. Gene 52, 225-233.
62. Vohra, G.B., Golding, G.B., Tsao, N., and Pearlman, R.E. (1992). A phylogenetic analysis based on the gene encoding phosphoglycerate kinase. J. Mol. Evol. 34, 383-395.
63. Wenkert, D., and Allis, C.D. (1984). Timing of the appearance of macronuclear-specific histone variant hv1 and gene expression in developing new macronuclei of Tetrahymena thermophila. J. Cell Biol. 98, 2107-2117.
64. Yang, C.H., Lambie, E.J., Hardin, J., Craft, J., and Snyder, M. (1989). Higher order structure is present in the yeast nucleus: autoantibody probes demonstrate that the nucleolus lies opposite the spindle pole body. Chromosoma 98, 123-128.
65. Yao, M.-C. (1996). Programmed DNA deletions in Tetrahymena: mechanisms and implications. Trends Genet. 12, 26-30.
66. Yao, M.-C., and Gall, J.G. (1977). A single integrated gene for ribosomal RNA in a eukaryote. Cell 12, 121-132.