The effect of ribosome assembly cofactors on in vitro 30S subunit reconstitution

Journal of Molecular Biology

Volumn 398, Issue 1, 2010, Pages 1-7

  Bunner, Anne E ^a   Nord, Stefan ^b   Wikström, P Mikael ^b   Williamson, James R ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

^b UMEÅ UNIVERSITY   (Sweden)

Author keywords

Era; Kinetics; Ribosome assembly; RimM; RimP YhbC

Indexed keywords

BINDING PROTEIN; ESCHERICHIA COLI RAS LIKE PROTEIN; RIBOSOME MATURATION FACTOR M PROTEIN; RIBOSOME MATURATION FACTOR P PROTEIN; RIBOSOME PROTEIN; RIBOSOME RNA; UNCLASSIFIED DRUG;

ARTICLE; BINDING KINETICS; BINDING SITE; BIOGENESIS; ENZYME ACTIVITY; IN VITRO STUDY; MASS SPECTROMETRY; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN DOMAIN; RIBOSOME SUBUNIT; RNA PROCESSING;

EID: 77950866260     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.02.036     Document Type: Article

References (45)

1. Bremer H., Dennis P.P. Modulation of chemical composition and other parameters of the cell by growth rate. Escherichia coli and Salmonella: Cellular and Molecular Biology 1996, 1553-1569. American Society for Microbiology, Washington, DC. 2nd edit. F.C. Neidhardt (Ed.).
2. Dez C., Tollervey D. Ribosome synthesis meets the cell cycle. Curr. Opin. Microbiol. 2004, 7:631-637.
3. Henras A.K., Soudet J., Gerus M., Lebaron S., Caizergues-Ferrer M., Mougin A., Henry Y. The post-transcriptional steps of eukaryotic ribosome biogenesis. Cell. Mol. Life Sci. 2008, 65:2334-2359.
4. Wilson D.N., Nierhaus K.H. The weird and wonderful world of bacterial ribosome regulation. Crit. Rev. Biochem. Mol. Biol. 2007, 42:187-219.
5. Traub P., Nomura M. Structure and function of E. coli ribosomes, V. Reconstitution of functionally active 30S ribosomal particles from RNA and proteins. Proc. Natl Acad. Sci. USA 1968, 59:777-784.
6. Nierhaus K.H., Dohme F. Total reconstitution of functionally active 50S ribosomal subunits from Escherichia coli. Proc. Natl Acad. Sci. USA 1974, 71:4713-4717.
7. Held W., Ballou B., Mizushima S., Nomura M. Assembly mapping of 30S ribosomal proteins from Escherichia coli: further studies. J. Biol. Chem. 1974, 249:3103-3111.
8. Grondek J., Culver G. Assembly of the 30S ribosomal subunit: positioning ribosomal protein S13 in the S7 assembly branch. RNA 2004, 10:1861-1866.
9. Bunner A.E., Trauger S.A., Siuzdak G., Williamson J.R. Quantitative ESI-TOF analysis of macromolecular assembly kinetics. Anal. Chem. 2008, 80:9379-9386.
10. Sperling E., Bunner A.E., Sykes M.T., Williamson J.R. Quantitative analysis of isotope distributions in proteomic mass spectrometry using least-squares Fourier transform convolution. Anal. Chem. 2008, 80:4906-4917.
11. Schuwirth B., Borovinskaya M., Hau C., Zhang W., Vila-Sanjurjo A., Holton J., Cate J. Structures of the bacterial ribosome at 3.5 Å resolution. Science 2005, 310:827-834.
12. Recht M., Williamson J. RNA tertiary structure and cooperative assembly of a large ribonucleoprotein complex. J. Mol. Biol. 2004, 344:395-407.
13. Samaha R., O'Brien B., O'Brien T., Noller H. Independent in vitro assembly of a ribonucleoprotein particle containing the 3' domain of 16S rRNA. Proc. Natl Acad. Sci. USA 1994, 91:7884-7888.
14. Weitzmann C., Cunningham P., Nurse K., Ofengand J. Chemical evidence for domain assembly of the Escherichia coli 30S ribosome. FASEB J. 1993, 7:177-180.
15. Powers T., Daubresse G., Noller H. Dynamics of in vitro assembly of 16S rRNA into 30S ribosomal subunits. J. Mol. Biol. 1993, 232:362-374.
16. Talkington M., Siuzdak G., Williamson J. An assembly landscape for the 30S ribosomal subunit. Nature 2005, 438:628-632.
17. Stern S., Powers T., Changchien L.M., Noller H.F. RNA-protein interactions in 30S ribosomal subunits: folding and function of 16S rRNA. Science 1989, 244:783-790.
18. Champney W.S. Kinetics of ribosome synthesis during a nutritional shift-up in Escherischia coli K-12. Mol. Gen. Genet. 1977, 152:259-266.
19. Kaczanowkska M., Rydén-Aulin M. Ribosome biogenesis and the translation process in Escherichia coli. Microbiol. Mol. Biol. Rev. 2007, 71:477-494.
20. de Narvaez C.C., Schaup H.W. In vivo transcriptionally coupled assembly of Escherichia coli ribosomal subunits. J. Mol. Biol. 1979, 134:1-22.
21. Connolly K., Culver G. Deconstructing ribosome construction. Trends Biochem. Sci. 2009, 34:256-263.
22. Ofengand J., Rudd K.E. Bacterial, archeal, and organellar rRNA pseudouridines and methylated nucleosides and their enzymes. The Ribosome: Structure, Function, Antibiotics, and Cellular Interactions 2000, 175-189. ASM Press, Washington, DC. R.A. Garret, S.R. Douthwaite, A. Liljas, A.T. Matheson, P.B. Moore, H.F. Noller (Eds.).
23. Maki J.A., Schnobrich D.J., Culver G.M. The DnaK chaperone system facilitates 30S ribosomal subunit assembly. Mol. Cell 2002, 10:129-138.
24. Maki J.A., Southworth D.R., Culver G.M. Demonstration of the role of the DnaK chaperone system in assembly of 30S ribosomal subunits using a purified in vitro system. RNA 2003, 9:1418-1421.
25. Alix J.H., Nierhaus K.H. DnaK-facilitated ribosome assembly in Escherichia coli revisited. RNA 2003, 9:787-793.
26. Brown E.D. Conserved P-loop GTPases of unknown function in bacteria: an emerging and vital ensemble in bacterial physiology. Biochem. Cell Biol. 2005, 83:738-746.
27. Sayed A., Matsuyama S., Inouye M. Era, an essential Escherichia coli small G-protein, binds to the 30S ribosomal subunit. Biochem. Biophys. Res. Commun. 1999, 264:51-54.
28. Inoue K., Alsina J., Chen J., Inouye M. Suppression of defective ribosome assembly in a rbfA deletion mutant by overexpression of Era, an essential GTPase in Escherichia coli. Mol. Microbiol. 2003, 48:1005-1016.
29. Chen X., Court D.L., Ji X. Crystal structure of ERA: a GTPase-dependent cell cycle regulator containing an RNA binding motif. Proc. Natl Acad. Sci. USA 1999, 96:8396-8401.
30. Sharma M.R., Barat C., Wilson D.N., Booth T.M., Kawazoe M., Hori-Takemoto C., et al. Interaction of Era with the 30S ribosomal subunit implications for 30S subunit assembly. Mol. Cell 2005, 18:319-329.
31. Tu C., Zhou X., Tropea J.E., Austin B.P., Waugh D.S., Court D.L., Ji X. Structure of ERA in complex with the 3' end of 16S rRNA: implications for ribosome biogenesis. Proc. Natl Acad. Sci. USA 2009, 106:14843-14848.
32. Connolly K., Rife J.P., Culver G. Mechanistic insight into the ribosome biogenesis functions of the ancient protein KsgA. Mol. Microbiol. 2008, 70:1062-1075.
33. Lu Q., Inouye M. The gene for 16S rRNA methyltransferase (ksgA) functions as a multicopy suppressor for a cold-sensitive mutant of era, an essential RAS-like GTP-binding protein in Escherichia coli. J. Bacteriol. 1998, 180:5243-5246.
34. Britton R.A., Powell B.S., Dasgupta S., Sun Q., Margolin W., Lupski J.R., Court D.L. Cell cycle arrest in Era GTPase mutants: a potential growth rate-regulated checkpoint in Escherichia coli. Mol. Microbiol. 1998, 27:739-750.
35. Inoue K., Basu S., Inouye M. Dissection of 16S rRNA methyltransferase (KsgA) function in Escherichia coli. J. Bacteriol. 2007, 189:8510-8518.
36. Bylund G.O., Persson B.C., Lundberg L.A., Wikstrom P.M. A novel ribosome-associated protein is important for efficient translation in Escherichia coli. J. Bacteriol. 1997, 179:4567-4574.
37. Bylund G.O., Wipemo L.C., Lundberg L.A., Wikström P.M. RimM and RbfA are essential for efficient processing of 16S rRNA in Escherichia coli. J. Bacteriol. 1998, 180:73-82.
38. Lövgren J.M., Bylund G.O., Srivastava M.K., Lundberg L.A., Persson O.P., Wingsle G., Wikström P.M. The PRC-barrel domain of the ribosome maturation protein RimM mediates binding to ribosomal protein S19 in the 30S ribosomal subunits. RNA 2004, 10:1798-1812.
39. Suzuki S., Tatsuguchi A., Matsumoto E., Kawazoe M., Kaminishi T., Shirouzu M., et al. Structural characterization of the ribosome maturation protein, RimM. J. Bacteriol. 2007, 189:6397-6406.
40. Nord S., Bylund G.O., Lövgren J.M., Wikström P.M. The RimP protein is important for maturation of the 30S ribosomal subunit. J. Mol. Biol. 2009, 386:742-753.
41. Yu L., Gunasekera A.H., Mack J., Olejniczak E.T., Chovan L.E., Ruan X., et al. Solution structure and function of a conserved protein SP14.3 encoded by an essential Streptococcus pneumoniae gene. J. Mol. Biol. 2001, 311:593-604.
42. Butland G., Peregrin-Alvarez J.M., Li J., Yang W., Yang X., Canadien V., et al. Interaction network containing conserved and essential protein complexes in Escherichia coli. Nature 2005, 433:531-537.
43. Studier F.W., Moffatt B.A. Use of bacteriophage T7 RNA polymerase to direct selective high-level expression of cloned genes. J. Mol. Biol. 1986, 189:113-130.
44. Bertani G. Studies on lysogenesis. I. The mode of phage liberation by lysogenic Escherichia coli. J. Bacteriol. 1951, 62:293-300.
45. Pichon J., Marvaldi J., Marchis-Mouren G. The in vivo order of protein addition in the course of Escherichia coli 30S and 50S subunit biogenesis. J. Mol. Biol. 1975, 96:125-137.