Genetic analysis of the ribosome biogenesis factor Ltv1 of Saccharomyces cerevisiae

Genetics

Volumn 198, Issue 3, 2014, Pages 1071-1085

  Merwin, Jason R ^a   Bogar, Lucien B ^a   Poggi, Sarah B ^a   Fitch, Rebecca M ^a   Johnson, Arlen W ^b   Lycan, Deborah E ^a  

^a LEWIS AND CLARK COLLEGE   (United States)

^b UNIVERSITY OF TEXAS AT AUSTIN   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

EXPORTIN 1; FUNGAL PROTEIN; LTV1 PROTEIN; RIBOSOME PROTEIN; UNCLASSIFIED DRUG; CELL RECEPTOR; EXPORTIN 1 PROTEIN; GREEN FLUORESCENT PROTEIN; HYBRID PROTEIN; KARYOPHERIN; LTV1 PROTEIN, S CEREVISIAE; NUCLEAR EXPORT SIGNAL; PROTEIN BINDING; RIBOSOMAL PROTEIN S3; SACCHAROMYCES CEREVISIAE PROTEIN;

ARTICLE; BIOGENESIS; CARBOXY TERMINAL SEQUENCE; DELETION MUTANT; FUNGAL STRAIN; GENE OVEREXPRESSION; GENETIC ANALYSIS; IN SITU HYBRIDIZATION; NONHUMAN; NUCLEAR EXPORT SIGNAL; PLASMID; PROTEIN INTERACTION; RIBOSOME; SACCHAROMYCES CEREVISIAE; SUCROSE DENSITY GRADIENT CENTRIFUGATION; ACTIVE TRANSPORT; AMINO ACID SEQUENCE; BINDING SITE; CELL NUCLEUS; CHEMISTRY; CONSENSUS SEQUENCE; DOMINANT GENE; GENETIC COMPLEMENTATION; GENETICS; GROWTH, DEVELOPMENT AND AGING; IMMUNOPRECIPITATION; METABOLISM; MOLECULAR GENETICS; MUTATION; PHENOTYPE; STRUCTURE ACTIVITY RELATION;

ACTIVE TRANSPORT, CELL NUCLEUS; AMINO ACID SEQUENCE; BINDING SITES; CELL NUCLEUS; CONSENSUS SEQUENCE; GENES, DOMINANT; GENETIC COMPLEMENTATION TEST; GREEN FLUORESCENT PROTEINS; IMMUNOPRECIPITATION; KARYOPHERINS; MOLECULAR SEQUENCE DATA; MUTATION; NUCLEAR EXPORT SIGNALS; PHENOTYPE; PROTEIN BINDING; RECEPTORS, CYTOPLASMIC AND NUCLEAR; RECOMBINANT FUSION PROTEINS; RIBOSOMAL PROTEINS; RIBOSOMES; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS; STRUCTURE-ACTIVITY RELATIONSHIP;

EID: 84908615402     PISSN: 00166731     EISSN: 19432631     Source Type: Journal    
DOI: 10.1534/genetics.114.168294     Document Type: Article

References (59)

1. Alberti, S., A. D. Gitler, and S. Lindquist, 2007 A suite of Gateway cloning vectors for high-throughput genetic analysis in Saccharomyces cerevisiae. Yeast 24: 913–919.
2. 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.
3. Bassler, J., P. Grandi, O. Gadal, T. Lessmann, E. Petfalski et al., 2001 Identification of a 60S preribosomal particle that is closely linked to nuclear export. Mol. Cell 8: 517–529.
4. Bradatsch, B., J. Katahira, E. Kowalinski, G. Bange, W. Yao et al., 2007 Arx1 functions as an unorthodox nuclear export receptor for the 60S preribosomal subunit. Mol. Cell 27: 767–779.
5. Campbell, M. G., and K. Karbstein, 2011 Protein-protein interactions within late pre-40S ribosomes. PLoS ONE 6: e16194.
6. Chen, S. S., and J. R. Williamson, 2013 Characterization of the ribosome biogenesis landscape in E. coli using quantitative mass spectrometry. J. Mol. Biol. 425: 767–779.
7. Dong, X., A. Biswas, K. E. Suel, L. K. Jackson, R. Martinez et al., 2009 Structural basis for leucine-rich nuclear export signal recognition by CRM1. Nature 458: 1136–1141.
8. Fassio, C. A., B. J. Schofield, R. M. Seiser, A. W. Johnson, and D. E. Lycan, 2010 Dominant mutations in the late 40S biogenesis factor Ltv1 affect cytoplasmic maturation of the small ribosomal subunit in Saccharomyces cerevisiae. Genetics 185: 199–209.
9. Faza, M. B., Y. Chang, L. Occhipinti, S. Kemmler, and V. G. Panse, 2012 Role of Mex67-Mtr2 in the nuclear export of 40S preribosomes. PLoS Genet. 8: e1002915.
10. Ferreira-Cerca, S., G. Poll, H. Kuhn, A. Neueder, S. Jakob et al., 2007 Analysis of the in vivo assembly pathway of eukaryotic 40S ribosomal proteins. Mol. Cell 28: 446–457.
11. Fornerod, M., and M. Ohno, 2002 Exportin-mediated nuclear export of proteins and ribonucleoproteins. Results Probl. Cell Differ. 35: 67–91.
12. Fornerod, M., M. Ohno, M. Yoshida, and I. W. Mattaj, 1997 CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90: 1051–1060.
13. 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.
14. 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.
15. Guttler, T., T. Madl, P. Neumann, D. Deichsel, L. Corsini et al., 2010 NES consensus redefined by structures of PKI-type and Rev-type nuclear export signals bound to CRM1. Nat. Struct. Mol. Biol. 17: 1367–1376.
16. Hedges, J., Y. I. Chen, M. West, C. Bussiere, and A. W. Johnson, 2006 Mapping the functional domains of yeast NMD3, the nuclear export adapter for the 60 S ribosomal subunit. J. Biol. Chem. 281: 36579–36587.
17. Hegde, V., M. Wang, and W. A. Deutsch, 2004 Human ribosomal protein S3 interacts with DNA base excision repair proteins hAPE/Ref-1 and hOGG1. Biochemistry 43: 14211–14217.
18. Ho, J. H., and A. W. Johnson, 1999 NMD3 encodes an essential cytoplasmic protein required for stable 60S ribosomal subunits in Saccharomyces cerevisiae. Mol. Cell. Biol. 19: 2389–2399.
19. 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.
20. Holzer, S., N. Ban, and S. Klinge, 2013 Crystal structure of the yeast ribosomal protein rpS3 in complex with its chaperone Yar1. J. Mol. Biol. 425: 4154–4160.
21. Hung, N. J., K. Y. Lo, S. S. Patel, K. Helmke, and A. W. Johnson, 2008 Arx1 is a nuclear export receptor for the 60S ribosomal subunit in yeast. Mol. Biol. Cell 19: 735–744.
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. James, P., J. Halladay, and E. A. Craig, 1996 Genomic libraries and a host strain designed for highly efficient two-hybrid selection in yeast. Genetics 144: 1425–1436.
24. Johnson, A., 2009 Nuclear export of ribosomes, pp. 69–84 in Nuclear Transport, edited by R. H. Kehlenbach. Landes Bioscience, Austin, TX.
25. Jung, S. O., J. Y. Lee, and J. Kim, 2001 Yeas3t ribosomal protein S3 has an endonuclease activity on AP DNA. Mol. Cells 12: 84–90.
26. Karbstein, K., 2011 Inside the 40S ribosome assembly machinery. Curr. Opin. Chem. Biol. 15: 657–663.
27. Koch, B., V. Mitterer, J. Niederhauser, T. Stanborough, G. Murat et al., 2012 Yar1 protects the ribosomal protein Rps3 from aggregation. J. Biol. Chem. 287: 21806–21815.
28. Kos, M., and D. Tollervey, 2010 Yeast pre-rRNA processing and modification occur cotranscriptionally. Mol. Cell 37: 809–820.
29. Kressler, D., E. Hurt, and J. Bassler, 2010 Driving ribosome assembly. Biochim. Biophys. Acta 1803: 673–683.
30. 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.
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. 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.
33. McIntosh, K. B., A. Bhattacharya, I. M. Willis, and J. R. Warner, 2011 Eukaryotic cells producing ribosomes deficient in Rpl1 are hypersensitive to defects in the ubiquitin-proteasome system. PLoS ONE 6: e23579.
34. Milkereit, P., O. Gadal, A. Podtelejnikov, S. Trumtel, N. Gas et al., 2001 Maturation and intranuclear transport of pre-ribosomes requires Noc proteins. Cell 105: 499–509.
35. Monecke, T., T. Guttler, P. Neumann, A. Dickmanns, D. Gorlich et al., 2009 Crystal structure of the nuclear export receptor CRM1 in complex with Snurportin1 and RanGTP. Science 324: 1087–1091.
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. Osheim, Y. N., S. L. French, K. M. Keck, E. A. Champion, K. Spasov et al., 2004 Pre-18S ribosomal RNA is structurally compacted into the SSU processome prior to being cleaved from nascent transcripts in Saccharomyces cerevisiae. Mol. Cell 16: 943–954.
38. Panse, V. G., and A. W. Johnson, 2010 Maturation of eukaryotic ribosomes: acquisition of functionality. Trends Biochem. Sci. 35: 260–266.
39. Passmore, L. A., T. M. Schmeing, D. Maag, D. J. Applefield, M. G. Acker et al., 2007 The eukaryotic translation initiation factors eIF1 and eIF1A induce an open conformation of the 40S ribosome. Mol. Cell 26: 41–50.
40. Phipps, K. R., J. Charette, and S. J. Baserga, 2011 The small subunit processome in ribosome biogenesis: progress and prospects. Wiley Interdiscip Rev RNA 2: 1–21.
41. Rabhi, I., N. Guedel, I. Chouk, K. Zerria, M. R. Barbouche et al., 2004 A novel simple and rapid PCR-based site-directed mutagenesis method. Mol. Biotechnol. 26: 27–34.
42. 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.
43. 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.
44. 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.
45. Stade, K., C. S. Ford, C. Guthrie, and K. Weis, 1997 Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 90: 1041–1050.
46. Stellberger, T., R. Hauser, A. Baiker, V. R. Pothineni, J. Haas et al., 2010 Improving the yeast two-hybrid system with permutated fusions proteins: the Varicella Zoster Virus interactome. Proteome Sci. 8: 8.
47. Strunk, B. S., and K. Karbstein, 2009 Powering through ribosome assembly. RNA 15: 2083–2104.
48. Strunk, B. S., C. R. Loucks, M. Su, H. Vashisth, S. Cheng et al., 2011 Ribosome assembly factors prevent premature translation initiation by 40S assembly intermediates. Science 333: 1449–1453.
49. 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.
50. 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.
51. Tschochner, H., and E. Hurt, 2003 Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol. 13: 255–263.
52. 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.
53. Warner, J. R., and K. B. McIntosh, 2009 How common are extraribosomal functions of ribosomal proteins? Mol. Cell 34: 3–11.
54. 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.
55. Yadavilli, S., V. Hegde, and W. A. Deutsch, 2007 Translocation of human ribosomal protein S3 to sites of DNA damage is dependent on ERK-mediated phosphorylation following genotoxic stress. DNA Repair (Amst.) 6: 1453–1462.
56. Yao, W., M. Lutzmann, and E. Hurt, 2008 A versatile interaction platform on the Mex67-Mtr2 receptor creates an overlap between mRNA and ribosome export. EMBO J. 27: 6–16.
57. Zemp, I., and U. Kutay, 2007 Nuclear export and cytoplasmic maturation of ribosomal subunits. FEBS Lett. 581: 2783–2793.
58. 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.
59. Zhao, W. T., C. F. Zhou, X. B. Li, Y. F. Zhang, L. Fan et al., 2013 The von Hippel-Lindau protein pVHL inhibits ribosome biogenesis and protein synthesis. J. Biol. Chem. 288: 16588–16597.