Functional link between ribosome formation and biogenesis of iron-sulfur proteins

EMBO Journal

Volumn 24, Issue 3, 2005, Pages 580-588

  Yarunin, Alexander ^a   Panse, Vikram Govind ^a   Petfalski, Elisabeth ^b   Dez, Christophe ^b   Tollervey, David ^b   Hurt, Eduard C ^a  

^a UNIVERSITY OF HEIDELBERG   (Germany)

^b UNIVERSITY OF EDINBURGH   (United Kingdom)

Author keywords

eIF3; Iron sulfur cluster; Nar1; Ribosome export; Rli1

Indexed keywords

IRON SULFUR PROTEIN; RLI1 PROTEIN; RNA PRECURSOR; UNCLASSIFIED DRUG;

ARTICLE; BIOGENESIS; CFD1 GENE; CONTROLLED STUDY; FUNGAL GENE; GENETIC SCREENING; NAR1 GENE; NBP35 GENE; NONHUMAN; PRIORITY JOURNAL; PROTEIN FUNCTION; PROTEIN SYNTHESIS; PROTEIN TRANSPORT; RIBOSOME; RIBOSOME SUBUNIT; RNA PROCESSING; YEAST;

ADENOSINE TRIPHOSPHATASES; ATP-BINDING CASSETTE TRANSPORTERS; BASE SEQUENCE; BIOLOGICAL TRANSPORT, ACTIVE; DNA, FUNGAL; EUKARYOTIC INITIATION FACTOR-3; GENES, FUNGAL; GTP-BINDING PROTEINS; IRON-SULFUR PROTEINS; MUTATION; RIBOSOMES; RNA PRECURSORS; RNA, FUNGAL; RNA, RIBOSOMAL; SACCHAROMYCES CEREVISIAE; SACCHAROMYCES CEREVISIAE PROTEINS;

EID: 14744301484     PISSN: 02614189     EISSN: None     Source Type: Journal    
DOI: 10.1038/sj.emboj.7600540     Document Type: Article

References (58)

1. Allmang C, Kufel J, Chanfreau G, Mitchell P, Petfalski E, Tollervey D (1999) Functions of the exosome in rRNA, snoRNA and snRNA synthesis. EMBO J 18: 5399-5410
2. Baßler J, Grandi P, Gadal O, Leßmann T, Tollervey D, Lechner J, Hurt EC (2001) Identification of a 60S pre-ribosomal particle that is closely linked to nuclear export. Mol Cell 8: 517-529
3. Barton RM, Worman HJ (1999) Prenylated prelamin A interacts with Narf, a novel nuclear protein. J Biol Chem 274: 30008-30018
4. Beinert H, Kiley PJ (1999) Fe-S proteins in sensing and regulatory functions. Curr Opin Chem Biol 3: 152-157
5. Beltrame M, Tollervey D (1992) Identification and functional analysis of two U3 binding sites on yeast pre-ribosomal RNA. EMBO J 11: 1531-1542
6. Berthelot K, Muldoon M, Rajkowitsch L, Hughes J, McCarthy JE (2004) Dynamics and processivity of 40S ribosome scanning on mRNA in yeast. Mol Microbiol 51: 987-1001
7. Bisbal C, Martinand C, Silhol M, Lebleu B, Salehzada T (1995) Cloning and characterization of a RNAse L inhibitor. A new component of the interferon-regulated 2-5A pathway. J Biol Chem 270: 13308-13317
8. Browning KS, Gallie DR, Hershey JW, Hinnebusch AG, Maitra U, Merrick WC, Norbury C (2001) Unified nomenclature for the subunits of eukaryotic initiation factor 3. Trends Biochem Sci 26: 284
9. de la Cruz J, lost I, Kressler D, Under P (1997) The p20 and Ded1 proteins have antagonistic roles in eIF4E-dependent translation in Saccharomyces cerevisiae. Proc Natl Acad Sci USA 94: 5201-5206
10. Decottignies A, Goffeau A (1997) Complete inventory of the yeast ABC proteins. Nat Genet 15: 137-145
11. Dez C, Froment C, Noaillac-Depeyre J, Monsarrat B, Caizergues-Ferrer M, Henry Y (2004) Npa1p, a component of very early pre-60S ribosomal particles, associates with a subset of small nucleolar RNPs required for peptidyl transferase center modification. Mol Cell Biol 24: 6324-6337
12. Dong J, Lai R, Nielsen K, Fekete CA, Qiu H, Hinnebusch AG (2004) The essential ATP-binding cassette protein RLI1 functions in translation by promoting preinitiation complex assembly. J Biol Chem 279: 42157-42168
13. Faber AW, van Dijk M, Raue A, Vos JC (2002) Ngl2p is a Ccr4p-like RNA nuclease essential for the final step in 3′-end processing of 5.8S rRNA in Saccharomyces cerevisiae. RNA 8: 1095-1101
14. Fairman ME, Maroney PA, Wang W, Bowers HA, Gollnick P, Nilsen TW, Jankowsky E (2004) Protein displacement by DExH/D 'RNA helicases' without duplex unwinding. Science 304: 730-734
15. Fornerod M, Ohno M, Yoshida M, Mattaj IW (1997) CRM1 is an export receptor for leucine-rich nuclear export signals. Cell 90: 1051-1060
16. Fukuda M, Asano S, Nakamura T, Adachi M, Yoshida M, Yanagida M, Nishida E (1997) CRM1 is responsible for intracellular transport mediated by the nuclear export signal. Nature 390: 308-311
17. Gadal O, Strauß D, Braspenning J, Hoepfner D, Petfalski E, Philippsen P, Tollervey D, Hurt EC (2001a) A nuclear AAA-type ATPase (Rix7p) is required for biogenesis and nuclear export of 60S ribosomal subunits. EMBO J 20: 3695-3704
18. Gadal O, Strauß D, Kessl J, Trumpower B, Tollervey D, Hurt E (2001b) Nuclear export of 60S ribosomal subunits depends on Xpo1p and requires a NES-containing factor Nmd3p that associates with the large subunit protein Rpl10p. Mol Cell Biol 21: 3405-3415
19. Gadal O, Strauss D, Petfalski E, Gleizes PE, Gas N, Tollervey D, Hurt E (2002) Rlp7p is associated with 60S preribosomes, restricted to the granular component of the nucleolus, and required for pre-rRNA processing. J Cell Biol 157: 941-951
20. Galani K, Nissan TA, Petfalski E, Tollervey D, Hurt E (2005) Real, a dynein related nuclear AAA-ATPase, is involved in late rRNA processing and nuclear export of 60S subunits. J Biol Chem 279: 55411-55418
21. Gleizes PE, Noaillac-Depeyre J, Leger-Silvestre I, Teulieres F, Dauxois JY, Pommel D, Azum-Gelade MC, Gas N (2001) Ultrastructural localization of rRNA shows defective nuclear export of preribosomes in mutants of the Nup82p complex. J Cell Biol 155: 923-936
22. Ho JHN, Johnson AW (1999) NMD3 encodes an essential cytoplasmic protein required for stable 60S ribosomal subunits in Saccharomyces cerevisiae. Mol Cell Biol 19: 2389-2399
23. Ho JHN, Kallstrom G, Johnson AW (2000) Nmd3p is a Crm1p dependent adapter protein for nuclear export of the large ribosomal subunit. J Cell Biol 151: 1057-1066
24. Hughes TR, Marton MJ, Jones AR, Roberts CJ, Stoughton R, Armour CD, Bennett HA, Coffey E, Dai H, He YD, Kidd MJ, King AM, Meyer MR, Slade D, Lum PY, Stepaniants SB, Shoemaker DD, Gachotte D, Chakraburtty K, Simon J, Bard M, Friend SH (2000) Functional discovery via a compendium of expression profiles. Cell 102: 109-126
25. Hurt E, Hannus S, Schmelzl B, Lau D, Tollervey D, Simos G (1999) A novel in vivo assay reveals inhibition of ribosomal nuclear export in ran-cycle and nucleoporin mutants. J Cell Biol 144: 389-401
26. Ito T, Chiba T, Ozawa R, Yoshida M, Hattori M, Sakaki Y (2001) A comprehensive two-hybrid analysis to explore the yeast protein interactome. Proc Natl Acad Sci USA 98: 4569-4574
27. Kispal G, Sipos K, Lange H, Fekete Z, Bedekovics T, Janáky T, Bassler J, Aguilar Netz DJ, Balk J, Rotte C, Lill R (2005) Biogenesis of cytosolic ribosomes requires the essential iron-sulfur protein Rli1p and mitochondria. EMBO J 2005, 20 January [E-pub ahead of print]
28. Kressler D, Linder P, De La Cruz J (1999) Protein trans-acting factors involved in ribosome biogenesis in Saccharomyces cerevisiae. Mol Cell Biol 19: 7897-7912
29. Letovsky S, Kasif S (2003) Predicting protein function from protein/protein interaction data: a probabilistic approach. Bioinformatics 19 (Suppl 1): i197-i204
30. Lill R, Kispal G (2000) Maturation of cellular Fe-S proteins: an essential function of mitochondria. Trends Biochem Sci 25: 352-356
31. Maniatis T, Fritsch ET, Sambrook J (1982) Molecular Cloning: A Laboratory Manual. Cold Spring Harbor, NY: Cold Spring Harbor Laboratory Press
32. Milkereit P, Gadal O, Podtelejnikov A, Trumtel S, Gas N, Petfalski E, Tollervey D, Mann M, Hurt E, Tschochner H (2001) Maturation and intranuclear transport of pre-ribosomes requires Noc-proteins. Cell 105: 499-509
33. Milkereit P, Strauss D, Bassler J, Gadal O, Kuhn H, Schutz S, Gas N, Lechner J, Hurt E, Tschochner H (2003) A Noc complex specifically involved in the formation and nuclear export of ribosomal 4OS subunits. J Biol Chem 278: 4072-4081
34. Morel Y, Barouki R (1999) Repression of gene expression by oxidative stress. Biochem J 342: 481-496
35. Moy TI, Silver PA (2002) Requirements for the nuclear export of the small ribosomal subunit. J Cell Sci 115: 2985-2995
36. Neumann S, Petfalski E, Brügger B, Großhans H, Wieland F, Tollervey D, Hurt E (2003) Formation and nuclear export of tRNA, rRNA and mRNA is regulated by the ubiquitin ligase Rsp5p. EMBO Rep 4: 1156-1162
37. Oeffinger M, Dlakic M, Tollervey D (2004) A pre-ribosome-associated HEAT-repeat protein is required for export of both ribosomal subunits. Genes Dev 18: 196-209
38. Peters JW, Lanzilotta WN, Lemon BJ, Seefeldt LC (1998) X-ray crystal structure of the Fe-only hydrogenase (CpI) from Clostridium pasteurianum to 1.8 angstrom resolution. Science 282: 1853-1858
39. Puig O, Caspary F, Rigaut G, Rutz B, Bouveret E, Bragado-Nilsson E, Wilm M, Seraphin B (2001) The tandem affinity purification (TAP) method: a general procedure of protein complex purification. Methods 24: 218-229
40. Roy A, Solodovnikova N, Nicholson T, Antholine W, Walden WE (2003) A novel eukaryotic factor for cytosolic Fe-S cluster assembly. EMBO J 22: 4826-4835
41. Samarsky DA, Fournier MJ (1999) A comprehensive database for the small nucleolar RNAs from Saccharomyces cerevisiae. Nucleic Acids Res 27: 161-164
42. Santos-Rosa H, Moreno H, Simos G, Segref A, Fahrenkrog B, Pante N, Hurt E (1998) Nuclear mRNA export requires complex formation between Mex67p and Mtr2p at the nuclear pores. Mol Cell Biol 18: 6826-6838
43. Schäfer T, Strauß D, Petfalski E, Tollervey D, Hurt EC (2003) The path from nucleolar 90S to cytoplasmic 40S pre-ribosomes. EMBO J 22: 1370-1380
44. Senger B, Lafontaine D, Graindorge J-S, Gadal O, Camasses A, Sanni A, Garnier J-M, Bteitenbach M, Hurt E, Fasiolo F (2001) The nucle(ol)ar Tif6p and Efl1p are required for a late cytoplasmic step of ribosome synthesis. Mol Cell 8: 1363-1373
45. Siniossoglou S, Wimmer C, Rieger M, Doye V, Tekotte H, Weise C, Emig S, Segref A, Hurt EC (1996) A novel complex of nucleoporins, which includes Sec13p and a Sec13p homolog, is essential for normal nuclear pores. Cell 84: 265-275
46. Stade K, Ford CS, Guthrie C, Weis K (1997) Exportin 1 (Crm1p) is an essential nuclear export factor. Cell 90: 1041-1050
47. Stage-Zimmermann T, Schmidt U, Silver PA (2000) Factors affecting nuclear export of the 60S ribosomal subunit in vivo. Mol Biol Cell 11: 3777-3789
48. Suzuki N, Noguchi E, Nakashima N, Oki M, Ohba T, Tartakoff A, Ohishi M, Nishimoto T (2001) The Saccharomyces cerevisiae small GTPase, Gsp1p/Ran, is involved in 3′ processing of 7S to 5.8S rRNA and in degradation of the excised 5′-A0 fragment of 35S pre-rRNA, both of which are carried out by the exosome. Genetics 158: 613-625
49. Thomas F, Kutay U (2003) Biogenesis and nuclear export of ribosomal subunits in higher eukaryotes depend on the CRM1 export pathway. J Cell Sci 116: 2409-2419
50. Tollervey D, Lehtonen H, Jansen RP, Kern H, Hurt EC (1993) Temperature-sensitive mutations demonstrate roles for yeast fibrillarin in pre-rRNA processing, pre-rRNA methylation, and ribosome assembly. Cell 72: 443-457
51. Trotta CR, Lund E, Kahan L, Johnson AW, Dahlberg JE (2003) Coordinated nuclear export of 60S ribosomal subunits and NMD3 in vertebrates. EMBO J 22: 2841-2851
52. Tschochner H, Hurt E (2003) Pre-ribosomes on the road from the nucleolus to the cytoplasm. Trends Cell Biol 13: 255-263
53. Valasek L, Hasek J, Nielsen KH, Hinnebusch AG (2001) Dual function of eIF3j/Hcr1p in processing 20S pre-rRNA and translation initiation. J Biol Chem 276: 43351-43360
54. Valasek L, Mathew A, Shin BS, Nielsen KH, Szamecz B, Hinnebusch AG (2003) The yeast eIF3 subunits TIF32/3, NIP1/c, and eIF5 make critical connections with the 40S ribosome in vivo. Genes Dev 17: 786-799
55. Venema J, Tollervey D (1999) Ribosome synthesis in Saccharomyces cerevisiae. Anna Rev Genet 33: 261-311
56. Vitale G, Fabre E, Hurt EC (1996) NBP35 encodes an essential and evolutionary conserved protein in Saccharomyces cerevisiae with homology to a superfamily of bacterial ATPases. Gene 178: 97-106
57. Warner JR (1999) The economics of ribosome biosynthesis in yeast. Trends Biochem Sci 24: 437-440
58. Wimmer C, Doye V, Grandi P, Nehrbass U, Hurt E (1992) A new subclass of nucleoporins that functionally interacts with nuclear pore protein NSP1. EMBO J 11: 5051-5061