Quantitative Proteomic Analysis of Ribosome Assembly and Turnover In Vivo

Journal of Molecular Biology

Volumn 403, Issue 3, 2010, Pages 331-345

  Sykes, Michael T ^a   Shajani, Zahra ^a   Sperling, Edit ^a   Beck, Andrea H ^a   Williamson, James R ^a  

^a SCRIPPS RESEARCH INSTITUTE   (United States)

Author keywords

Assembly intermediates; Proteomics; Quantitative mass spectrometry; Ribosome assembly; RNA protein interactions

Indexed keywords

NEOMYCIN; NITROGEN 15; RIBOSOME PROTEIN; ESCHERICHIA COLI PROTEIN; PROTEIN SYNTHESIS INHIBITOR; PROTEOME; RIBOSOME RNA;

ARTICLE; ESCHERICHIA COLI; MACROMOLECULE; MASS SPECTROMETRY; MOLECULAR DYNAMICS; MUTATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN METABOLISM; PROTEOMICS; QUANTITATIVE ANALYSIS; RIBOSOME; RIBOSOME SUBUNIT; STOICHIOMETRY; WILD TYPE; CHEMISTRY; DRUG EFFECTS; ELECTROSPRAY MASS SPECTROMETRY; GENETICS; LARGE RIBOSOMAL SUBUNIT; METABOLISM; SMALL RIBOSOMAL SUBUNIT;

ESCHERICHIA COLI;

ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; NEOMYCIN; PROTEIN SYNTHESIS INHIBITORS; PROTEOME; RIBOSOMAL PROTEINS; RIBOSOME SUBUNITS, LARGE, BACTERIAL; RIBOSOME SUBUNITS, SMALL, BACTERIAL; RIBOSOMES; RNA, RIBOSOMAL; SPECTROMETRY, MASS, ELECTROSPRAY IONIZATION;

EID: 77957754593     PISSN: 00222836     EISSN: None     Source Type: Journal    
DOI: 10.1016/j.jmb.2010.08.005     Document Type: Article

References (46)

1. Schuwirth B.S., Borovinskaya M.A., Hau C.W., Zhang W., Vila-Sanjurjo A., Holton J.M., Cate J.H.D. Structures of the bacterial ribosome at 3.5 Å resolution. Science 2005, 310:827-834.
2. Selmer M., Dunham C.M., Murphy F.V., Weixlbaumer A., Petry S., Kelley A.C., et al. Structure of the 70S ribosome complexed with mRNA and tRNA. Science 2006, 313:1935-1942.
3. Korostelev A., Trakhanov S., Laurberg M., Noller H.F. Crystal structure of a 70S ribosome-tRNA complex reveals functional interactions and rearrangements. Cell 2006, 126:1065-1077.
4. Mizushima S., Nomura M. Assembly mapping of 30S ribosomal proteins from E. coli. Nature 1970, 226:1214-1218.
5. Nomura M. Assembly of bacterial ribosomes. Science 1973, 179:864-873.
6. Herold M., Nierhaus K.H. Incorporation of six additional proteins to complete the assembly map of the 50 S subunit from Escherichia coli ribosomes. J. Biol. Chem. 1987, 262:8826-8833.
7. Wilson D.N., Nierhaus K.H. The weird and wonderful world of bacterial ribosome regulation. Crit. Rev. Biochem. Mol. Biol. 2007, 42:187-219.
8. de Narvaez C.C., Schaup H.W. In vivo transcriptionally coupled assembly of Escherichia coli ribosomal subunits. J. Mol. Biol. 1979, 134:1-22.
9. Lewicki B.T., Margus T., Remme J., Nierhaus K.H. Coupling of rRNA transcription and ribosomal assembly in vivo. Formation of active ribosomal subunits in Escherichia coli requires transcription of rRNA genes by host RNA polymerase which cannot be replaced by bacteriophage T7 RNA polymerase. J. Mol. Biol. 1993, 231:581-593.
10. Talkington M.W.T., Siuzdak G., Williamson J.R. An assembly landscape for the 30S ribosomal subunit. Nature 2005, 438:628-632.
11. 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.
12. Adilakshmi T., Bellur D.L., Woodson S.A. Concurrent nucleation of 16S folding and induced fit in 30S ribosome assembly. Nature 2008, 455:1268-1272.
13. Traub P., Nomura M. Structure and function of Escherichia coli ribosomes. VI. Mechanism of assembly of 30 s ribosomes studied in vitro. J. Mol. Biol. 1969, 40:391-413.
14. Held W.A., Nomura M. Rate determining step in the reconstitution of Escherichia coli 30S ribosomal subunits. Biochemistry 1973, 12:3273-3281.
15. Holmes K.L., Culver G.M. Analysis of conformational changes in 16 S rRNA during the course of 30 S subunit assembly. J. Mol. Biol. 2005, 354:340-357.
16. Holmes K.L., Culver G.M. Mapping structural differences between 30S ribosomal subunit assembly intermediates. Nat. Struct. Mol. Biol. 2004, 11:179-186.
17. Sykes M.T., Williamson J.R. A complex assembly landscape for the 30S ribosomal subunit. Annu. Rev. Biophys. 2009, 38:197-215.
18. Charollais J., Pflieger D., Vinh J., Dreyfus M., Iost I. The DEAD-box RNA helicase SrmB is involved in the assembly of 50S ribosomal subunits in Escherichia coli. Mol. Microbiol. 2003, 48:1253-1265.
19. Charollais J., Dreyfus M., Iost I. CsdA, a cold-shock RNA helicase from Escherichia coli, is involved in the biogenesis of 50S ribosomal subunit. Nucleic Acids Res. 2004, 32:2751-2759.
20. Al Refaii A., Alix J.H. Ribosome biogenesis is temperature-dependent and delayed in Escherichia coli lacking the chaperones DnaK or DnaJ. Mol. Microbiol. 2009, 71:748-762.
21. Jiang M., Datta K., Walker A., Strahler J., Bagamasbad P., Andrews P.C., Maddock J.R. The Escherichia coli GTPase CgtAE is involved in late steps of large ribosome assembly. J. Bacteriol. 2006, 188:6757-6770.
22. Sharpe Elles L.M., Sykes M.T., Williamson J.R., Uhlenbeck O.C. A dominant negative mutant of the E. coli RNA helicase DbpA blocks assembly of the 50S ribosomal subunit. Nucleic Acids Res. 2009, 37:6503-6514.
23. Mehta R., Champney W.S. 30S ribosomal subunit assembly is a target for inhibition by aminoglycosides in Escherichia coli. Antimicrob. Agents Chemother. 2002, 46:1546-1549.
24. Mehta R., Champney W.S. Neomycin and paromomycin inhibit 30S ribosomal subunit assembly in Staphylococcus aureus. Curr. Microbiol. 2003, 47:237-243.
25. Foster C., Champney W.S. Characterization of a 30S ribosomal subunit assembly intermediate found in Escherichia coli cells growing with neomycin or paromomycin. Arch. Microbiol. 2008, 189:441-449.
26. Champney W.S., Burdine R. Macrolide antibiotics inhibit 50S ribosomal subunit assembly in Bacillus subtilis and Staphylococcus aureus. Antimicrob. Agents Chemother. 1995, 39:2141-2144.
27. Chittum H.S., Champney W.S. Erythromycin inhibits the assembly of the large ribosomal subunit in growing Escherichia coli cells. Curr. Microbiol. 1995, 30:273-279.
28. Snijders A.P.L., de Vos M.G.J., Wright P.C. Novel approach for peptide quantitation and sequencing based on 15N and 13C metabolic labeling. J. Proteome Res. 2005, 4:578-585.
29. Nelson C.J., Huttlin E.L., Hegeman A.D., Harms A.C., Sussman M.R. Implications of 15N-metabolic labeling for automated peptide identification in Arabidopsis thaliana. Proteomics 2007, 7:1279-1292.
30. 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.
31. Lindahl L. Intermediates and time kinetics of the in vivo assembly of Escherichia coli ribosomes. J. Mol. Biol. 1975, 92:15-37.
32. Marvaldi J., Pichon J., Delaage M., Marchis-Mouren G. Individual ribosomal protein pool size and turnover rate in Escherichia coli. J. Mol. Biol. 1974, 84:83-96.
33. Iost I., Charollais J., Vinh J., Pflieger D. Characterization of E. coli ribosomal particles: combined analysis of whole proteins by mass spectrometry and of proteolytic digests by liquid chromatography-tandem mass spectrometry. Methods Mol. Biol. 2008, 432:321-341.
34. Kaberdina A.C., Szaflarski W., Nierhaus K.H., Moll I. An unexpected type of ribosomes induced by kasugamycin: a look into ancestral times of protein synthesis?. Mol. Cell 2009, 33:227-236.
35. Kaplan R., Apirion D. The fate of ribosomes in Escherichia coli cells starved for a carbon source. J. Biol. Chem. 1975, 250:1854-1863.
36. Maruyama H.B., Okamura S. Ribosome degradation and the degradation products in starved Escherichia coli. V. Ribonucleoprotein particles from glucose-starved cells. J. Bacteriol. 1972, 110:442-446.
37. Borovinskaya M.A., Pai R.D., Zhang W., Schuwirth B.S., Holton J.M., Hirokawa G., et al. Structural basis for aminoglycoside inhibition of bacterial ribosome recycling. Nat. Struct. Mol. Biol. 2007, 14:727-732.
38. Siibak T., Peil L., Xiong L., Mankin A., Remme J., Tenson T. Erythromycin- and chloramphenicol-induced ribosomal assembly defects are secondary effects of protein synthesis inhibition. Antimicrob. Agents Chemother. 2009, 53:563-571.
39. Nowotny V., Nierhaus K.H. Initiator proteins for the assembly of the 50S subunit from Escherichia coli ribosomes. Proc. Natl Acad. Sci. USA 1982, 79:7238-7242.
40. Nowotny V., Nierhaus K.H. Assembly of the 30S subunit from Escherichia coli ribosomes occurs via two assembly domains which are initiated by S4 and S7. Biochemistry 1988, 27:7051-7055.
41. Zengel J.M., Lindahl L. Diverse mechanisms for regulating ribosomal protein synthesis in Escherichia coli. Prog. Nucleic Acid Res. Mol. Biol. 1994, 47:331-370.
42. Sykes M.T., Sperling E., Chen S.S., Williamson J.R. Quantitation of the ribosomal protein autoregulatory network using mass spectrometry. Anal. Chem. 2010, 82:5038-5045.
43. Ong S.E., Mann M. Mass spectrometry-based proteomics turns quantitative. Nat. Chem. Biol. 2005, 1:252-262.
44. Bunner A.E., Beck A.H., Williamson J.R. Kinetic cooperativity in Escherichia coli 30S ribosomal subunit reconstitution reveals additional complexity in the assembly landscape. Proc. Natl Acad. Sci. USA 2010, 107:5417-5422.
45. Bunner A.E., Nord S., Wikström P.M., Williamson J.R. The effect of ribosome assembly cofactors on in vitro 30S subunit reconstitution. J. Mol. Biol. 2010, 398:1-7.
46. Staehelin T., Maglott D. Preparation of Escherichia coli ribosomal subunits active in polypeptide synthesis. Methods Enzymol. 1971, 20:449-456.