Mammalian DEAD box protein Ddx51 acts in 3′ end maturation of 28S rRNA by promoting the release of U8 snoRNA

Molecular and Cellular Biology

Volumn 30, Issue 12, 2010, Pages 2947-2956

  Srivastava, Leena ^a,c   Lapik, Yevgeniya R ^b,d   Wang, Minshi ^a   Pestov, Dimitri G ^a  

^a UNIVERSITY OF MEDICINE AND DENTISTRY OF NEW JERSEY   (United States)

^b UNIVERSITY OF ILLINOIS   (United States)

^c UNIVERSITY OF GEORGIA   (United States)

^d Harold Washington College   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DEAD BOX PROTEIN; DEAD BOX PROTEIN DDX51; GUANINE NUCLEOTIDE BINDING PROTEIN; INTERNAL TRANSCRIBED SPACER; PROTEIN SUBUNIT; RIBOSOME RNA; RNA 28S; SMALL NUCLEOLAR RNA; U 8 SMALL NUCLEOLAR RNA; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; CONTROLLED STUDY; DOWNSTREAM PROCESSING; EUKARYOTE; MOUSE; NONHUMAN; NUCLEOTIDE SEQUENCE; PRIORITY JOURNAL; PROMOTER REGION; PROTEIN ANALYSIS; PROTEIN PROTEIN INTERACTION; PROTEIN RNA BINDING; PROTEIN SECRETION; RNA PROCESSING; RNA SYNTHESIS; YEAST;

ANIMALS; BASE PAIRING; CELL LINE; CENTRIFUGATION, DENSITY GRADIENT; DEAD-BOX RNA HELICASES; GENE KNOCKDOWN TECHNIQUES; GENES, DOMINANT; GTP PHOSPHOHYDROLASES; MICE; MUTANT PROTEINS; MUTATION; NUCLEAR PROTEINS; PHENOTYPE; PROTEIN BINDING; RIBOSOMES; RNA 3' END PROCESSING; RNA PRECURSORS; RNA, RIBOSOMAL, 28S; RNA, SMALL NUCLEOLAR; TWO-HYBRID SYSTEM TECHNIQUES;

EUKARYOTA; MAMMALIA; METAZOA;

EID: 77953449290     PISSN: 02707306     EISSN: None     Source Type: Journal    
DOI: 10.1128/MCB.00226-10     Document Type: Article

References (61)

1. Allmang, C., and D. Tollervey. 1998. The role of the 3′ external transcribed spacer in yeast pre-rRNA processing. J. Mol. Biol. 278:67-78.
2. Atzorn, V., P. Fragapane, and T. Kiss. 2004. U17/snR30 is a ubiquitous snoRNA with two conserved sequence motifs essential for 18S rRNA production. Mol. Cell. Biol. 24:1769-1778.
3. Bachellerie, J. P., J. Cavaillé, and A. Hüttenhofer. 2002. The expanding snoRNA world. Biochimie 84:775-790.
4. Beltrame, M., and D. Tollervey. 1992. Identification and functional analysis of two U3 binding sites on yeast pre-ribosomal RNA. EMBO J. 11:1531-1542.
5. Bernstein, K. A., S. Granneman, A. V. Lee, S. Manickam, and S. J. Baserga. 2006. Comprehensive mutational analysis of yeast DEXD/H box RNA helicases involved in large ribosomal subunit biogenesis. Mol. Cell. Biol. 26: 1195-1208.
6. Bleichert, F., and S. J. Baserga. 2007. The long unwinding road of RNA helicases. Mol. Cell 27:339-352.
7. Bohnsack, M. T., M. Kos, and D. Tollervey. 2008. Quantitative analysis of snoRNA association with pre-ribosomes and release of snR30 by Rok1 helicase. EMBO Rep. 9:1230-1236.
8. Borovjagin, A. V., and S. A. Gerbi. 2005. An evolutionary intra-molecular shift in the preferred U3 snoRNA binding site on pre-ribosomal RNA. Nucleic Acids Res. 33:4995-5005.
9. Cordin, O., J. Banroques, N. K. Tanner, and P. Linder. 2006. The DEAD-box protein family of RNA helicases. Gene 367:17-37.
10. de la Cruz, J., D. Kressler, and P. Linder. 1999. Unwinding RNA in Saccharomyces cerevisiae: DEAD-box proteins and related families. Trends Biochem. Sci. 24:192-198.
11. Dragon, F., J. E. G. Gallagher, P. A. Compagnone-Post, B. M. Mitchell, K. A. Porwancher, K. A. Wehner, S. Wormsley, R. E. Settlage, J. Shabanowitz, Y. Osheim, A. L. Beyer, D. F. Hunt, and S. J. Baserga. 2002. A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature 417:967-970.
12. Eichler, D. C., and N. Craig. 1994. Processing of eukaryotic ribosomal RNA. Prog. Nucleic Acid Res. Mol. Biol. 49:197-239.
13. Esguerra, J., J. Warringer, and A. Blomberg. 2008. Functional importance of individual rRNA 2′-O-ribose methylations revealed by high-resolution phenotyping. RNA 14:649-656.
14. Fromont-Racine, M., B. Senger, C. Saveanu, and F. Fasiolo. 2003. Ribosome assembly in eukaryotes. Gene 313:17-42.
15. Fuentes, J., K. Datta, S. Sullivan, A. Walker, and J. Maddock. 2007. In vivo functional characterization of the Saccharomyces cerevisiae 60S biogenesis GTPase Nog1. Mol. Genet. Genomics 278:105-123.
16. Gerbi, S. A., A. V. Borovjagin, M. Ezrokhi, and T. S. Lange. 2001. Ribosome biogenesis: role of small nucleolar RNA in maturation of eukaryotic rRNA. Cold Spring Harb. Symp. Quant. Biol. 66:575-590.
17. Ghosh, T., B. Peterson, N. Tomasevic, and B. A. Peculis. 2004. Xenopus U8 snoRNA binding protein is a conserved nuclear decapping enzyme. Mol. Cell 13:817-828.
18. Golemis, E. A., and R. Brent. 1997. Searching for interacting proteins with the two-hybrid system III, p. 43-72. In P. L. Bartel and S. Fields (ed.), The yeast two-hybrid system. Oxford University Press, New York, NY.
19. Grandi, P., V. Rybin, J. Bassler, E. Petfalski, D. Strauss, M. Marzioch, T. Schäfer, B. Kuster, H. Tschochner, D. Tollervey, A. C. Gavin, and E. Hurt. 2002. 90S pre-ribosomes include the 35S pre-rRNA, the U3 snoRNP, and 40S subunit processing factors but predominantly lack 60S synthesis factors. Mol. Cell 10:105-115.
20. Granneman, S., K. A. Bernstein, F. Bleichert, and S. J. Baserga. 2006. Comprehensive mutational analysis of yeast DEXD/H box RNA helicases required for small ribosomal subunit synthesis. Mol. Cell. Biol. 26:1183-1194.
21. Gurney, T. J. 1985. Characterization of mouse 45S ribosomal RNA subspecies suggests that the first processing cleavage occurs 600 +/- 100 nucleotides from the 5′ end and the second 500 +/- 100 nucleotides from the 3′ end of a 13.9 kb precursor. Nucleic Acids Res. 13:4905-4919.
22. Henras, A. K., J. Soudet, M. Gérus, S. Lebaron, M. Caizergues-Ferrer, A. Mougin, and Y. Henry. 2008. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell. Mol. Life Sci. 65:2334-2359.
23. Hinsby, A. M., L. Kiemer, E. O. Karlberg, K. Lage, A. Fausbøll, A. S. Juncker, J. S. Andersen, M. Mann, and S. Brunak. 2006. A wiring of the human nucleolus. Mol. Cell 22:285-295.
24. Hughes, J. M., and M. J. Ares. 1991. Depletion of U3 small nucleolar RNA inhibits cleavage in the 5′ external transcribed spacer of yeast pre-ribosomal RNA and impairs formation of 18S ribosomal RNA. EMBO J. 10:4231-4239.
25. Jankowsky, E., C. H. Gross, S. Shuman, and A. M. Pyle. 2001. Active disruption of an RNA-protein interaction by a DExH/D RNA helicase. Science 291:121-125.
26. Jensen, B. C., Q. Wang, C. T. Kifer, and M. Parsons. 2003. The NOG1 GTP-binding protein is required for biogenesis of the 60 S ribosomal subunit. J. Biol. Chem. 278:32204-32211.
27. Kallstrom, G., J. Hedges, and A. Johnson. 2003. The putative GTPases Nog1p and Lsg1p are required for 60S ribosomal subunit biogenesis and are localized to the nucleus and cytoplasm, respectively. Mol. Cell. Biol. 23: 4344-4355.
28. Kass, S., K. Tyc, J. A. Steitz, and B. Sollner-Webb. 1990. The U3 small nucleolar ribonucleoprotein functions in the first step of preribosomal RNA processing. Cell 60:897-908. (Pubitemid 120034857)
29. Kass, S., N. Craig, and B. Sollner-Webb. 1987. Primary processing of mammalian rRNA involves two adjacent cleavages and is not species specific. Mol. Cell. Biol. 7:2891-2898.
30. King, T. H., B. Liu, R. R. McCully, and M. J. Fournier. 2003. Ribosome structure and activity are altered in cells lacking snoRNPs that form pseudouridines in the peptidyl transferase center. Mol. Cell 11:425-435.
31. Kiss, T. 2002. Small nucleolar RNAs: an abundant group of noncoding RNAs with diverse cellular functions. Cell 109:145-148.
32. Kos, M., and D. Tollervey. 2005. The Putative RNA helicase Dbp4p is required for release of the U14 snoRNA from preribosomes in Saccharomyces cerevisiae. Mol. Cell 20:53-64.
33. Kressler, D., E. Hurt, and J. Baßler. 30 October 2009, posting date. Driving ribosome assembly. Biochim. Biophys. Acta doi:10.1016/j.bbamcr. 2009.10.009.
34. Lafontaine, D. L., and D. Tollervey. 2001. The function and synthesis of ribosomes. Nat. Rev. Mol. Cell Biol. 2:514-520.
35. Lapik, Y. R., C. J. Fernandes, L. F. Lau, and D. G. Pestov. 2004. Physical and functional interaction between Pes1 and Bop1 in mammalian ribosome biogenesis. Mol. Cell 15:17-29.
36. Lapik, Y. R., J. M. Misra, L. F. Lau, and D. G. Pestov. 2007. Restricting conformational flexibility of the switch II region creates a dominant-inhibitory phenotype in Obg GTPase Nog1. Mol. Cell. Biol. 27:7735-7744.
37. Li, H. D., J. Zagorski, and M. J. Fournier. 1990. Depletion of U14 small nuclear RNA (snR128) disrupts production of 18S rRNA in Saccharomyces cerevisiae. Mol. Cell. Biol. 10:1145-1152.
38. Liang, X., and M. J. Fournier. 2006. The helicase Has1p is required for snoRNA release from pre-rRNA. Mol. Cell. Biol. 26:7437-7450.
39. Liang, X., Q. Liu, and M. J. Fournier. 2007. rRNA modifications in an intersubunit bridge of the ribosome strongly affect both ribosome biogenesis and activity. Mol. Cell 28:965-977.
40. Matsuura, S., T. Morimoto, Y. Tashiro, T. Higashinakagawa, and M. Muramatsu. 1974. Ultrastructural and biochemical studies on the precursor ribosomal particles isolated from rat liver nucleoli. J. Cell Biol. 63:629-640.
41. Michot, B., N. Joseph, S. Mazan, and J. P. Bachellerie. 1999. Evolutionarily conserved structural features in the ITS2 of mammalian pre-rRNAs and potential interactions with the snoRNA U8 detected by comparative analysis of new mouse sequences. Nucleic Acids Res. 27:2271-2282.
42. Morrissey, J. P., and D. Tollervey. 1993. Yeast snR30 is a small nucleolar RNA required for 18S rRNA synthesis. Mol. Cell. Biol. 13:2469-2477.
43. Peculis, B. A. 1997. The sequence of the 5′ end of the U8 small nucleolar RNA is critical for 5.8S and 28S rRNA maturation. Mol. Cell. Biol. 17:3702-3713.
44. Peculis, B. A., and J. A. Steitz. 1993. Disruption of U8 nucleolar snRNA inhibits 5.8S and 28S rRNA processing in the Xenopus oocyte. Cell 73:1233-1245.
45. Peculis, B. A., and J. A. Steitz. 1994. Sequence and structural elements critical for U8 snRNP function in Xenopus oocytes are evolutionarily conserved. Genes Dev. 8:2241-2255.
46. Pestov, D. G., and L. F. Lau. 1994. Genetic selection of growth-inhibitory sequences in mammalian cells. Proc. Natl. Acad. Sci. U. S. A. 91:12549-12553.
47. Pestov, D. G., Y. R. Lapik, and L. F. Lau. 2008. Assays for ribosomal RNA processing and ribosome assembly. Curr. Protoc. Cell Biol., chapter 22, unit 22.11.
48. Saveanu, C., A. Namane, P. Gleizes, A. Lebreton, J. Rousselle, J. Noaillac-Depeyre, N. Gas, A. Jacquier, and M. Fromont-Racine. 2003. Sequential protein association with nascent 60S ribosomal particles. Mol. Cell. Biol. 23:4449-4460.
49. Shcherbik, N., M. Wang, Y. R. Lapik, L. Srivastava, and D. G. Pestov. 2010. Polyadenylation and degradation of incomplete RNA polymerase I transcripts in mammalian cells. EMBO Rep. 11:106-111.
50. Strezoska, Z., D. G. Pestov, and L. F. Lau. 2000. Bop1 is a mouse WD40 repeat nucleolar protein involved in 28S and 5. 8S RRNA processing and 60S ribosome biogenesis. Mol. Cell. Biol. 20:5516-5528.
51. Strezoska, Z., D. G. Pestov, and L. F. Lau. 2002. Functional inactivation of the mouse nucleolar protein Bop1 inhibits multiple steps in pre-rRNA processing and blocks cell cycle progression. J. Biol. Chem. 277:29617-29625.
52. Strunk, B. S., and K. Karbstein. 2009. Powering through ribosome assembly. RNA 15:2083-2104.
53. Tanner, N. K., and P. Linder. 2001. DExD/H box RNA helicases: from generic motors to specific dissociation functions. Mol. Cell 8:251-262.
54. Tanner, N. K., O. Cordin, J. Banroques, M. Doère, and P. Linder. 2003. The Q. motif: a newly identified motif in DEAD box helicases may regulate ATP binding and hydrolysis. Mol. Cell 11:127-138.
55. Thiry, M., and D. L. J. Lafontaine. 2005. Birth of a nucleolus: the evolution of nucleolar compartments. Trends Cell Biol. 15:194-199.
56. Tollervey, D. 1987. A yeast small nuclear RNA is required for normal processing of pre-ribosomal RNA. EMBO J. 6:4169-4175.
57. Tomasevic, N., and B. A. Peculis. 2002. Xenopus LSm proteins bind U8 snoRNA via an internal evolutionarily conserved octamer sequence. Mol. Cell. Biol. 22:4101-4112.
58. Tyc, K., and J. A. Steitz. 1989. U3, U8 and U13 comprise a new class of mammalian snRNPs localized in the cell nucleolus. EMBO J. 8:3113-3119.
59. Tycowski, K. T., M. D. Shu, and J. A. Steitz. 1994. Requirement for intron-encoded U22 small nucleolar RNA in 18S ribosomal RNA maturation. Science 266:1558-1561.
60. Venema, J., and D. Tollervey. 1999. Ribosome synthesis in Saccharomyces cerevisiae. Annu. Rev. Genet. 33:261-311.
61. Warner, J. R., and R. Soeiro. 1967. Nascent ribosomes from HeLa cells. Proc. Natl. Acad. Sci. U. S. A. 58:1984-1990.