Dominant mutations in the late 40S biogenesis factor Ltv1 affect cytoplasmic maturation of the small ribosomal subunit in Saccharomyces cerevisiae

Genetics

Volumn 185, Issue 1, 2010, Pages 199-209

  Fassio, Claire A ^a   Schofield, Brett J ^a   Seiser, Robert M ^b   Johnson, Arlen W ^c   Lycan, Deborah E ^a  

^a LEWIS AND CLARK COLLEGE   (United States)

^b ROOSEVELT UNIVERSITY   (United States)

^c UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

20S RRNA; GREEN FLUORESCENT PROTEIN; LTV1 PROTEIN; PROTEIN; RIBOSOME RNA; RPS2 PROTEIN; RPS3 PROTEIN; TRANSCRIPTION FACTOR; TSR1 PROTEIN; UNCLASSIFIED DRUG; FUNGAL RNA; LTV1 PROTEIN, S CEREVISIAE; MUTANT PROTEIN; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BIOGENESIS; CELL NUCLEUS; CONTROLLED STUDY; CYTOPLASM; FLUORESCENCE IN SITU HYBRIDIZATION; GENE DELETION; GENE MUTATION; GENE OVEREXPRESSION; NONHUMAN; NUCLEAR EXPORT SIGNAL; PRIORITY JOURNAL; PROTEIN LOCALIZATION; SACCHAROMYCES CEREVISIAE; SMALL RIBOSOMAL SUBUNIT; AMINO ACID SEQUENCE; CHEMISTRY; CYTOLOGY; DOMINANT GENE; GENETICS; METABOLISM; MOLECULAR GENETICS; MUTATION; PROTEIN TRANSPORT;

EUKARYOTA; SACCHAROMYCES CEREVISIAE;

AMINO ACID SEQUENCE; CELL NUCLEUS; CYTOPLASM; GENES, DOMINANT; MOLECULAR SEQUENCE DATA; MUTANT PROTEINS; MUTATION; PROTEIN TRANSPORT; RIBOSOME SUBUNITS, SMALL, EUKARYOTIC; RNA, FUNGAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 77956634055     PISSN: 00166731     EISSN: 00166731     Source Type: Journal    
DOI: 10.1534/genetics.110.115584     Document Type: Article

References (57)

1. AMBERG, D. C., A. L. GOLDSTEIN and C. N. COLE, 1992 Isolation and characterization of RAT1: an essential gene of Saccharomyces cerevisiae required for the efficient nucleocytoplasmic trafficking of mRNA. Genes Dev. 6: 1173-1189.
2. BELK, J. P., F. HE and A. JACOBSON, 1999 Overexpression of truncated Nmd3p inhibits protein synthesis in yeast. RNA 5: 1055-1070.
3. BRAND, R. C., J. KLOOTWIJK, T. J. VAN STEENBERGEN, A. J. DE KOK and R. J. PLANTA, 1977 Secondary methylation of yeast ribosomal precursor RNA. Eur. J. Biochem. 75: 311-318.
4. CHEN, W., J. BUCARIA, D. A. BAND, A. SUTTON and R. STERNGLANZ, 2003 Enp1, a yeast protein associated with U3 and U14 snoRNAs, is required for pre-rRNA processing and 40S subunit synthesis. Nucleic Acids Res. 31: 690-699.
5. DRAGON, F., J. E. GALLAGHER, P. A. COMPAGNONE-POST, B. M. MITCHELL, K. A. PORWANCHER et al., 2002 A large nucleolar U3 ribonucleoprotein required for 18S ribosomal RNA biogenesis. Nature 417: 967-970.
6. FATICA, A., M. OEFFINGER, M. DLAKIC and D. TOLLERVEY, 2003 Nob1p is required for cleavage of the 3′ end of 18S rRNA. Mol. Cell. Biol. 23: 1798-1807.
7. FATICA, A., D. TOLLERVEY and M. DLAKIC, 2004 PIN domain of Nob1p is required for D-site cleavage in 20S pre-rRNA. RNA 10: 1698-1701.
8. FORNEROD, M., and M. OHNO, 2002 Exportin-mediated nuclear export of proteins and ribonucleoproteins. Results Probl. Cell Differ. 35: 67-91.
9. FROMONT-RACINE, M., B. SENGER, C. SAVEANU and F. FASIOLO, 2003 Ribosome assembly in eukaryotes. Gene 313: 17-42.
10. GADAL, O., D. STRAUSS, J. KESSL, B. TRUMPOWER, D. TOLLERVEY et al., 2001 Nuclear export of 60s ribosomal subunits depends on Xpo1p and requires a nuclear export sequence-containing factor, Nmd3p, that associates with the large subunit protein Rpl10p. Mol. Cell. Biol. 21: 3405-3415.
11. GEERLINGS, T. H., A. W. FABER, M. D. BISTER, J. C. VOS and H. A. RAUE, 2003 Rio2p, an evolutionarily conserved, low abundant protein kinase essential for processing of 20 S Pre-rRNA in Saccharomyces cerevisiae. J. Biol. Chem. 278: 22537-22545.
12. GELPERIN, D., L. HORTON, J. BECKMAN, J. HENSOLD and S. K. LEMMON, 2001 Bms1p, a novel GTP-binding protein, and the related Tsr1p are required for distinct steps of 40S ribosome biogenesis in yeast. RNA 7: 1268-1283.
13. GIETZ, D., A. ST JEAN, R. A. WOODS and R. H. SCHIESTL, 1992 Improved method for high efficiency transformation of intact yeast cells. Nucleic Acids Res. 20: 1425.
14. GLEIZES, P. E., J. NOAILLAC-DEPEYRE, I. LEGER-SILVESTRE, F. TEULIERES, J. Y. DAUXOIS et al., 2001 Ultrastructural localization of rRNA shows defective nuclear export of preribosomes in mutants of the Nup82p complex. J. Cell Biol. 155: 923-936.
15. GRANDI, P., V. RYBIN, J. BASSLER, E. PETFALSKI, D. STRAUSS et al., 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.
16. GRANNEMAN, S., and S. J. BASERGA, 2004 Ribosome biogenesis: of knobs and RNA processing. Exp. Cell Res. 296: 43-50.
17. GRANNEMAN, S., M. R. NANDINENI and S. J. BASERGA, 2005 The putative NTPase Fap7 mediates cytoplasmic 20S pre-rRNA processing through a direct interaction with Rps14. Mol. Cell. Biol. 25: 10352-10364.
18. HEDGES, J., M. WEST and A. W. JOHNSON, 2005 Release of the export adapter, Nmd3p, from the 60S ribosomal subunit requires Rpl10p and the cytoplasmic GTPase Lsg1p. EMBO J. 24: 567-579.
19. HENRAS, A. K., J. SOUDET, M. GERUS, S. LEBARON, M. CAIZERGUES-FERRER et al., 2008 The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell. Mol. Life Sci. 65: 2334-2359.
20. HO, J. H., G. KALLSTROM and A. W. JOHNSON, 2000 Nmd3p is a Crm1p-dependent adapter protein for nuclear export of the large ribosomal subunit. J. Cell Biol. 151: 1057-1066.
21. HURT, E., S. HANNUS, B. SCHMELZL, D. LAU, D. TOLLERVEY et al., 1999 A novel in vivo assay reveals inhibition of ribosomal nuclear export in ran-cycle and nucleoporin mutants. J. Cell Biol. 144: 389-401.
22. ITO, T., T. CHIBA, R. OZAWA, M. YOSHIDA, M. HATTORI et al., 2001 A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc. Natl. Acad. Sci. USA 98: 4569-4574.
23. JOHNSON, A., 2009 Nuclear Export of Ribosomes, pp. 69-84 in Nuclear Transport, edited by R. H. KEHLENBACH. Landes Bioscience, Austin, TX.
24. JOHNSON, A. W., E. LUND and J. DAHLBERG, 2002 Nuclear export of ribosomal subunits. Trends Biochem. Sci. 27: 580-585.
25. 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.
26. KRESSLER, D., E. HURT and J. BABETALER, 2009 Driving ribosome assembly. Biochim. Biophys. Acta
27. LA COUR, T., L. KIEMER, A. MOLGAARD, R. GUPTA, K. SKRIVER et al., 2004 Analysis and prediction of leucine-rich nuclear export signals. Protein Eng. Des. Sel. 17: 527-536.
28. LAFONTAINE, D., J. VANDENHAUTE and D. TOLLERVEY, 1995 The 18S rRNA dimethylase Dim1p is required for pre-ribosomal RNA processing in yeast. Genes Dev. 9: 2470-2481.
29. LAFONTAINE, D. L., T. PREISS and D. TOLLERVEY, 1998 Yeast 18S rRNA dimethylase Dim1p: A quality control mechanism in ribosome synthesis? Mol. Cell. Biol. 18: 2360-2370.
30. LEBARON, S., C. PAPIN, R. CAPEYROU, Y. L. CHEN, C. FROMENT et al., 2009 The ATPase and helicase activities of Prp43p are stimulated by the G-patch protein Pfa1p during yeast ribosome biogenesis. EMBO J. 28: 3808-3819.
31. LEGER-SILVESTRE, I., P. MILKEREIT, S. FERREIRA-CERCA, C. SAVEANU, J. C. ROUSSELLE et al., 2004 The ribosomal protein Rps15p is required for nuclear exit of the 40S subunit precursors in yeast. EMBO J. 23: 2336-2347.
32. LI, Z., I. LEE, E. MORADI, N. J. HUNG, A. W. JOHNSON et al., 2009 Rational extension of the ribosome biogenesis pathway using network-guided genetics. PLoS Biol. 7: e1000213.
33. LOAR, J. W., R. M. SEISER, A. E. SUNDBERG, H. J. SAGERSON, N. ILIAS et al., 2004 Genetic and biochemical interactions among Yar1, Ltv1 and Rps3 define novel links between environmental stress and ribosome biogenesis in Saccharomyces cerevisiae. Genetics 168: 1877-1889.
34. MILKEREIT, P., D. STRAUSS, J. BASSLER, O. GADAL, H. KUHN et al., 2003 A Noc complex specifically involved in the formation and nuclear export of ribosomal 40 S subunits. J. Biol. Chem. 278: 4072-4081.
35. MOY, T. I., and P. A. SILVER, 1999 Nuclear export of the small ribosomal subunit requires the ran-GTPase cycle and certain nucleoporins. Genes Dev. 13: 2118-2133.
36. MOY, T. I., and P. A. SILVER, 2002 Requirements for the nuclear export of the small ribosomal subunit. J. Cell Sci. 115: 2985-2995.
37. NEUBER, A., J. FRANKE, A. WITTSTRUCK, G. SCHLENSTEDT, T. SOMMER et al., 2008 Nuclear export receptor Xpo1/Crm1 is physically and functionally linked to the spindle pole body in budding yeast. Mol. Cell. Biol. 28: 5348-5358.
38. PENG, W. T., M. D. ROBINSON, S. MNAIMNEH, N. J. KROGAN, G. CAGNEY et al., 2003 A panoramic view of yeast noncoding RNA processing. Cell 113: 919-933.
39. PERTSCHY, B., C. SCHNEIDER, M. GNADIG, T. SCHAFER, D. TOLLERVEY et al., 2009 RNA helicase Prp43 and its co-factor Pfa1 promote 20 to 18 S rRNA processing catalyzed by the endonuclease Nob1. J. Biol. Chem. 284: 35079-35091.
40. SCHAFER, T., D. STRAUSS, E. PETFALSKI, D. TOLLERVEY and E. HURT, 2003 The path from nucleolar 90S to cytoplasmic 40S preribosomes. EMBO J. 22: 1370-1380.
41. SCHAFER, T., B. MACO, E. PETFALSKI, D. TOLLERVEY, B. BOTTCHER et al., 2006 Hrr25-dependent phosphorylation state regulates organization of the pre-40S subunit. Nature 441: 651-655.
42. SEISER, R. M., A. E. SUNDBERG, B. J. WOLLAM, P. ZOBEL-THROPP, K. BALDWIN et al., 2006 Ltv1 is required for efficient nuclear export of the ribosomal small subunit in Saccharomyces cerevisiae. Genetics 174: 679-691. (Pubitemid 44656459)
43. SENGER, B., D. L. LAFONTAINE, J. S. GRAINDORGE, O. GADAL, A. CAMASSES et al., 2001 The nucle(ol)ar Tif6p and Efl1p are required for a late cytoplasmic step of ribosome synthesis. Mol. Cell 8: 1363-1373.
44. STAGE-ZIMMERMANN, T., U. SCHMIDT and P. A. SILVER, 2000 Factors affecting nuclear export of the 60S ribosomal subunit in vivo. Mol. Biol. Cell 11: 3777-3789.
45. STEVENS, A., C. L. HSU, K. R. ISHAM and F. W. LARIMER, 1991 Fragments of the internal transcribed spacer 1 of pre-rRNA accumulate in Saccharomyces cerevisiae lacking 5′-3′ exoribonuclease 1. J. Bacteriol. 173: 7024-7028.
46. STRUNK, B. S., and K. KARBSTEIN, 2009 Powering through ribosome assembly. RNA 15: 2083-2104.
47. THOMAS, F., and U. KUTAY, 2003 Biogenesis and nuclear export of ribosomal subunits in higher eukaryotes depend on the CRM1 export pathway. J. Cell Sci. 116: 2409-2419.
48. TROTTA, C. R., E. LUND, L. KAHAN, A. W. JOHNSON and J. E. DAHLBERG, 2003 Coordinated nuclear export of 60S ribosomal subunits and NMD3 in vertebrates. EMBO J. 22: 2841-2851.
49. TSCHOCHNER, H., and E. HURT, 2003 Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol. 13: 255-263.
50. UDEM, S. A., and J. R. WARNER, 1973 The cytoplasmic maturation of a ribosomal precursor ribonucleic acid in yeast. J. Biol. Chem. 248: 1412-1416.
51. VANROBAYS, E., P. E. GLEIZES, C. BOUSQUET-ANTONELLI, J. NOAILLAC-DEPEYRE, M. CAIZERGUES-FERRER et al., 2001 Processing of 20S pre-rRNA to 18S ribosomal RNA in yeast requires Rrp10p, an essential non-ribosomal cytoplasmic protein. EMBO J. 20: 4204-4213.
52. VANROBAYS, E., J. P. GELUGNE, P. E. GLEIZES and M. CAIZERGUES-FERRER, 2003 Late cytoplasmic maturation of the small ribosomal subunit requires RIO proteins in Saccharomyces cerevisiae. Mol. Cell. Biol. 23: 2083-2095.
53. VANROBAYS, E., A. LEPLUS, Y. N. OSHEIM, A. L. BEYER, L. WACHEUL et al., 2008 TOR regulates the subcellular distribution of DIM2, a KH domain protein required for cotranscriptional ribosome assembly and pre-40S ribosome export. RNA 14: 2061-2073.
54. VENEMA, J., and D. TOLLERVEY, 1999 Ribosome synthesis in Saccharomyces cerevisiae. Annu. Rev. Genet. 33: 261-311.
55. WEN, W., J. L. MEINKOTH, R. Y. TSIEN and S. S. TAYLOR, 1995 Identification of a signal for rapid export of proteins from the nucleus. Cell 82: 463-473.
56. ZEMP, I., and U. KUTAY, 2007 Nuclear export and cytoplasmic maturation of ribosomal subunits. FEBS Lett. 581: 2783-2793.
57. ZEMP, I., T. WILD, M. F. O'DONOHUE, F. WANDREY, B. WIDMANN et al., 2009 Distinct cytoplasmic maturation steps of 40S ribosomal subunit precursors require hRio2. J. Cell Biol. 185: 1167-1180.