A hierarchical model for assembly of eukaryotic 60S ribosomal subunit domains

Genes and Development

Volumn 28, Issue 2, 2014, Pages 198-210

  Gamalinda, Michael ^a   Ohmayer, Uli ^b   Jakovljevic, Jelena ^a   Kumcuoglu, Beril ^a   Woolford, Joshua ^a,c   Mbom, Bertrade ^a,d   Lin, Lawrence ^a,e   Woolford Jr , John L ^a  

^a CARNEGIE MELLON UNIVERSITY   (United States)

^b UNIVERSITY OF REGENSBURG   (Germany)

^c TULANE UNIVERSITY   (United States)

^d STANFORD UNIVERSITY   (United States)

^e UNIVERSITY OF CALIFORNIA   (United States)

Author keywords

Large ribosomal subunit; Preribosomes; Ribosomal proteins; Ribosome assembly

Indexed keywords

FUNGAL RNA; RIBOSOME PROTEIN; RIBOSOME RNA; RNA 5S; RNA 60 S; UNCLASSIFIED DRUG;

ANIMAL CELL; ARTICLE; BIOGENESIS; FUNGAL GENETICS; LARGE RIBOSOMAL SUBUNIT; MASS SPECTROMETRY; NONHUMAN; POLYACRYLAMIDE GEL ELECTROPHORESIS; PRIORITY JOURNAL; PROTEIN DEPLETION; PROTEIN FUNCTION; PROTEIN LOCALIZATION; PROTEIN QUATERNARY STRUCTURE; PROTEOMICS; STEADY STATE; YEAST;

LARGE RIBOSOMAL SUBUNIT; PRERIBOSOMES; RIBOSOMAL PROTEINS; RIBOSOME ASSEMBLY;

MODELS, MOLECULAR; PROTEIN STRUCTURE, QUATERNARY; PROTEIN STRUCTURE, TERTIARY; RIBOSOME SUBUNITS, LARGE, EUKARYOTIC; SACCHAROMYCES CEREVISIAE;

EID: 84892725662     PISSN: 08909369     EISSN: 15495477     Source Type: Journal    
DOI: 10.1101/gad.228825.113     Document Type: Article

References (62)

1. Adilakshmi T, Bellur DL, Woodson SA. 2008. Concurrent nucleation of 16S folding and induced fit in 30S ribosome assembly. Nature 455: 1268-1272.
2. Allmang C, Tollervey D. 1998. The role of the 39 external transcribed spacer in yeast pre-rRNA processing. J Mol Biol 278: 67-78.
3. Babiano R, de la Cruz J. 2010. Ribosomal protein L35 is required for 27SB pre-rRNA processing in Saccharomyces cerevisiae. Nucleic Acids Res 38: 5177-5192.
4. Babiano R, Gamalinda M, Woolford JL Jr, de la Cruz J. 2012. Saccharomyces cerevisiae ribosomal protein L26 is not essential for ribosome assembly and function. Mol Cell Biol 32: 3228-3241.
5. Ban N, Nissen P, Hansen J, Moore PB, Steitz TA. 2000. The complete atomic structure of the large ribosomal subunit at 2.4 A° resolution. Science 289: 905-920.
6. Behrouzi R, Roh JH, Kilburn D, Briber RM, Woodson SA. 2012. Cooperative tertiary interaction network guides RNA folding. Cell 149: 348-357.
7. Ben-Shem A, Garreau de Loubresse N, Melnikov S, Jenner L, Yusupova G, Yusupov M. 2011. The structure of the eukaryotic ribosome at 3.0 A° resolution. Science 334: 1524-1529.
8. Bokinsky G, Rueda D, Misra VK, Rhodes MM, Gordus A, Babcock HP, Walter NG, Zhuang X. 2003. Single-molecule transition-state analysis of RNA folding. Proc Natl Acad Sci 100: 9302-9307.
9. Bradatsch B, Leidig C, Granneman S, Gnadig M, Tollervey D, Bottcher B, Beckmann R, Hurt E. 2012. Structure of the pre-60S ribosomal subunit with nuclear export factor Arx1 bound at the exit tunnel. Nat Struct Mol Biol 19: 1234-1241.
10. Buchmueller KL, Weeks KM. 2003. Near native structure in an RNA collapsed state. Biochemistry 42: 13869-13878.
11. Bussiere C, Hashem Y, Arora S, Frank J, Johnson AW. 2012. Integrity of the P-site is probed during maturation of the 60S ribosomal subunit. J Cell Biol 197: 747-759.
12. Chen SS, Williamson JR. 2013. Characterization of the ribosome biogenesis landscape in E. coli using quantitative mass spectrometry. J Mol Biol 425: 767-779.
13. Clatterbuck Soper SF, Dator RP, Limbach PA, Woodson SA. 2013. In vivo X-ray footprinting of pre-30S ribosomes reveals chaperone-dependent remodeling of late assembly intermediates. Mol Cell 52: 506-516.
14. Ellis SR, Gleizes PE. 2011. Diamond Blackfan anemia: Ribosomal proteins going rogue. Semin Hematol 48: 89-96.
15. Eppens NA, Rensen S, Granneman S, Raue HA, Venema J. 1999. The roles of Rrp5p in the synthesis of yeast 18S and 5.8S rRNA can be functionally and physically separated. RNA 5: 779-793.
16. Fernandez-Pevida A, Rodriguez-Galan O, Diaz-Quintana A, Kressler D, de la Cruz J. 2012. Yeast ribosomal protein L40 assembles late into precursor 60 S ribosomes and is required for their cytoplasmic maturation. J Biol Chem 287: 38390-38407.
17. Ferreira-Cerca S, Poll G, Gleizes PE, Tschochner H, Milkereit P. 2005. Roles of eukaryotic ribosomal proteins in maturation and transport of pre-18S rRNA and ribosome function. Mol Cell 20: 263-275.
18. Ferreira-Cerca S, Poll G, Kuhn H, Neueder A, Jakob S, Tschochner H, Milkereit P. 2007. Analysis of the in vivo assembly pathway of eukaryotic 40S ribosomal proteins. Mol Cell 28: 446-457.
19. Francisco-Velilla R, Remacha M, Ballesta JP. 2013. Carboxy terminal modifications of the P0 protein reveal alternative mechanisms of nuclear ribosomal stalk assembly. Nucleic Acids Res 41: 8628-8636.
20. Freed EF, Bleichert F, Dutca LM, Baserga SJ. 2010. When ribosomes go bad: Diseases of ribosome biogenesis. Mol Biosyst 6: 481-493.
21. Gamalinda M, Jakovljevic J, Babiano R, Talkish J, de la Cruz J, Woolford JL Jr. 2013. Yeast polypeptide exit tunnel ribosomal proteins L17, L35 and L37 are necessary to recruit lateassembling factors required for 27SB pre-rRNA processing. Nucleic Acids Res 41: 1965-1983.
22. Gartmann M, Blau M, Armache JP, Mielke T, Topf M, Beckmann R. 2010. Mechanism of eIF6-mediated inhibition of ribosomal subunit joining. J Biol Chem 285: 14848-14851.
23. Granneman S, Petfalski E, Swiatkowska A, Tollervey D. 2010. Cracking pre-40S ribosomal subunit structure by systematic analyses of RNA-protein cross-linking. EMBO J 29: 2026-2036.
24. Granneman S, Petfalski E, Tollervey D. 2011. A cluster of ribosome synthesis factors regulate pre-rRNA folding and 5.8S rRNA maturation by the Rat1 exonuclease. EMBO J 30: 4006-4019.
25. Greber BJ, Boehringer D, Montellese C, Ban N. 2012. Cryo-EM structures of Arx1 and maturation factors Rei1 and Jjj1 bound to the 60S ribosomal subunit. Nat Struct Mol Biol 19: 1228-1233.
26. Grummt I. 1999. Regulation of mammalian ribosomal gene transcription by RNA polymerase I. Prog Nucleic Acid Res Mol Biol 62: 109-154.
27. Held WA, Ballou B, Mizushima S, Nomura M. 1974. Assembly mapping of 30 S ribosomal proteins from Escherichia coli. Further studies. J Biol Chem 249: 3103-3111.
28. Hitchen J, Ivakine E, Melekhovets YF, Lalev A, Nazar RN. 1997. Structural features in the 39 external transcribed spacer affecting intragenic processing of yeast rRNA. J Mol Biol 274: 481-490.
29. Hofer A, Bussiere C, Johnson AW. 2007. Mutational analysis of the ribosomal protein Rpl10 from yeast. J Biol Chem 282: 32630-32639.
30. Holbrook SR. 2008. Structural principles from large RNAs. Annu Rev Biophys 37: 445-464.
31. Jakovljevic J, Ohmayer U, Gamalinda M, Talkish J, Alexander L, Linnemann J, Milkereit P, Woolford JL Jr. 2012. Ribosomal proteins L7 and L8 function in concert with six A3 assembly factors to propagate assembly of domains I and II of 25S rRNA in yeast 60S ribosomal subunits. RNA 18: 1805-1822.
32. Karbstein K. 2011. Inside the 40S ribosome assembly machinery. Curr Opin Chem Biol 15: 657-663.
33. Karbstein K. 2013. Quality control mechanisms during ribosome maturation. Trends Cell Biol 23: 242-250.
34. Kos M, Tollervey D. 2010. Yeast pre-rRNA processing and modification occur cotranscriptionally. Mol Cell 37: 809-820.
35. Kressler D, Hurt E, Bergler H, Bassler J. 2012. The power of AAA-ATPases on the road of pre-60S ribosome maturation-molecular machines that strip pre-ribosomal particles. Biochim Biophys Acta 1823: 92-100.
36. Kruiswijk T, Planta RJ, Krop JM. 1978. The course of the assembly of ribosomal subunits in yeast. Biochim Biophys Acta 517: 378-389.
37. Lebaron S, Segerstolpe A, French SL, Dudnakova T, de Lima Alves F, Granneman S, Rappsilber J, Beyer AL, Wieslander L, Tollervey D. 2013. Rrp5 binding at multiple sites coordinates pre-rRNA processing and assembly. Mol Cell 52: 707-719.
38. Li N, Chen Y, Guo Q, Zhang Y, Yuan Y, Ma C, Deng H, Lei J, Gao N. 2013. Cryo-EM structures of the late-stage assembly intermediates of the bacterial 50S ribosomal subunit. Nucleic Acids Res 41: 7073-7083.
39. Longtine MS, McKenzie A III, Demarini DJ, Shah NG, Wach A, Brachat A, Philippsen P, Pringle JR. 1998. Additional modules for versatile and economical PCR-based gene deletion and modification in Saccharomyces cerevisiae. Yeast 14: 953-961.
40. Matsuo Y, Granneman S, Thoms M, Manikas RG, Tollervey D, Hurt E. 2013. Coupled GTPase and remodelling ATPase activities form a checkpoint for ribosome export. Nature doi: 10.1038/nature12731.
41. Maxwell ES, Fournier MJ. 1995. The small nucleolar RNAs. Annu Rev Biochem 64: 897-934.
42. McCann KL, Baserga SJ. 2013. Genetics. Mysterious ribosomopathies. Science 341: 849-850.
43. Mulder AM, Yoshioka C, Beck AH, Bunner AE, Milligan RA, Potter CS, Carragher B, Williamson JR. 2010. Visualizing ribosome biogenesis: Parallel assembly pathways for the 30S subunit. Science 330: 673-677.
44. Nowotny V, Nierhaus KH. 1982. Initiator proteins for the assembly of the 50S subunit from Escherichia coli ribosomes. Proc Natl Acad Sci 79: 7238-7242.
45. O'Donohue MF, Choesmel V, Faubladier M, Fichant G, Gleizes PE. 2010. Functional dichotomy of ribosomal proteins during the synthesis of mammalian 40S ribosomal subunits. J Cell Biol 190: 853-866.
46. Ohmayer U, Gamalinda M, Sauert M, Ossowski J, Poll G, Linnemann J, Hierlmeier T, Perez-Fernandez J, Kumcuoglu B, Leger-Silvestre I, et al. 2013. Studies on the assembly characteristics of large subunit ribosomal proteins in S. cerevisiae. PLoS ONE 8: e68412.
47. Poll G, Braun T, Jakovljevic J, Neueder A, Jakob S, Woolford JL Jr, Tschochner H, Milkereit P. 2009. rRNA maturation in yeast cells depleted of large ribosomal subunit proteins. PLoS ONE 4: e8249.
48. Pyle AM, Fedorova O, Waldsich C. 2007. Folding of group II introns: A model system for large, multidomain RNAs? Trends Biochem Sci 32: 138-145.
49. Robledo S, Idol RA, Crimmins DL, Ladenson JH, Mason PJ, Bessler M. 2008. The role of human ribosomal proteins in the maturation of rRNA and ribosome production. RNA 14: 1918-1929.
50. Rohl R, Nierhaus KH. 1982. Assembly map of the large subunit (50S) of Escherichia coli ribosomes. Proc Natl Acad Sci 79: 729-733.
51. Sahasranaman A, Dembowski J, Strahler J, Andrews P, Maddock J, Woolford JL Jr. 2011. Assembly of Saccharomyces cerevisiae 60S ribosomal subunits: Role of factors required for 27S pre-rRNA processing. EMBO J 30: 4020-4032.
52. Saveanu C, Namane A, Gleizes PE, Lebreton A, Rousselle JC, Noaillac-Depeyre J, Gas N, Jacquier A, Fromont-Racine M. 2003. Sequential protein association with nascent 60S ribosomal particles. Mol Cell Biol 23: 4449-4460.
53. Schillewaert S, Wacheul L, Lhomme F, Lafontaine DL. 2012. The evolutionarily conserved protein Las1 is required for pre-rRNA processing at both ends of ITS2. Mol Cell Biol 32: 430-444.
54. Schuwirth BS, Borovinskaya MA, Hau CW, Zhang W, Vila-Sanjurjo A, Holton JM, Cate JH. 2005. Structures of the bacterial ribosome at 3.5 A° resolution. Science 310: 827-834.
55. Sengupta J, Bussiere C, Pallesen J, West M, Johnson AW, Frank J. 2010. Characterization of the nuclear export adaptor protein Nmd3 in association with the 60S ribosomal subunit. J Cell Biol 189: 1079-1086.
56. Shajani Z, Sykes MT, Williamson JR. 2011. Assembly of bacterial ribosomes. Annu Rev Biochem 80: 501-526.
57. Strunk BS, Loucks CR, Su M, Vashisth H, Cheng S, Schilling J, Brooks CL III, Karbstein K, Skiniotis G. 2011. Ribosome assembly factors prevent premature translation initiation by 40S assembly intermediates. Science 333: 1449-1453.
58. Strunk BS, Novak MN, Young CL, Karbstein K. 2012. A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits. Cell 150: 111-121.
59. Talkish J, Zhang J, Jakovljevic J, Horsey EW, Woolford JL Jr. 2012. Hierarchical recruitment into nascent ribosomes of assembly factors required for 27SB pre-rRNA processing in Saccharomyces cerevisiae. Nucleic Acids Res 40: 8646-8661.
60. Ulbrich C, Diepholz M, Bassler J, Kressler D, Pertschy B, Galani K, Bottcher B, Hurt E. 2009. Mechanochemical removal of ribosome biogenesis factors from nascent 60S ribosomal subunits. Cell 138: 911-922.
61. Woodson SA. 2011. RNA folding pathways and the self-assembly of ribosomes. Acc Chem Res 44: 1312-1319.
62. Zhang J, Harnpicharnchai P, Jakovljevic J, Tang L, Guo Y, Oeffinger M, Rout MP, Hiley SL, Hughes T, Woolford JL Jr. 2007. Assembly factors Rpf2 and Rrs1 recruit 5S rRNA and ribosomal proteins rpL5 and rpL11 into nascent ribosomes. Genes & Dev 21: 2580-2592.