Functional domains of the 50S subunit mature late in the assembly process

Nucleic Acids Research

Volumn 42, Issue 5, 2014, Pages 3419-3435

  Jomaa, Ahmad ^a   Jain, Nikhil ^b   Davis, Joseph H ^c   Williamson, James R ^c   Britton, Robert A ^b   Ortega, Joaquin ^a  

^a MCMASTER UNIVERSITY   (Canada)

^b Michigan State University ^*  (United States)

^c Institute for Chemical Biology   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

GUANOSINE TRIPHOSPHATASE; HAPTOCORRIN; PROTEIN RBGA; RIBOSOME PROTEIN; RIBOSOME PROTEIN L16; RIBOSOME PROTEIN L27; RIBOSOME PROTEIN L28; RIBOSOME PROTEIN L33A; RIBOSOME PROTEIN L35; RIBOSOME PROTEIN L36; TRANSFER RNA; UNCLASSIFIED DRUG;

45S RIBOSOME SUBUNIT; 50S RIBOSOME SUBUNIT; ARTICLE; BACILLUS SUBTILIS; BIOGENESIS; CELL FUNCTION; CELL MATURATION; CELL STRUCTURE; CHEMICAL ANALYSIS; CHEMICAL LABELING; CONTROLLED STUDY; CRYOELECTRON MICROSCOPY; ENZYME ACTIVITY; ENZYME ANALYSIS; ENZYME RELEASE; LARGE RIBOSOMAL SUBUNIT; MASS SPECTROMETRY; NONHUMAN; PRIORITY JOURNAL; PROTEIN ASSEMBLY; PROTEIN BINDING; PROTEIN DEPLETION; QUANTITATIVE ANALYSIS; RIBOSOME SUBUNIT; RNA BINDING; STOICHIOMETRY;

BACILLUS SUBTILIS; GTP PHOSPHOHYDROLASES; MODELS, MOLECULAR; RIBOSOMAL PROTEINS; RIBOSOME SUBUNITS, LARGE, BACTERIAL; RNA, TRANSFER;

EID: 84899018786     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkt1295     Document Type: Article

References (54)

1. Bremer, H. and Dennis, P.D. (1996) Modulation of chemical composition and other parameters of the cell by growth rate. In: Neidhardt, F.C. (ed.), Escherichia coli and Salmonella. ASM Press, Washington D.C, pp. 1553-1569.
2. Traub, P. and Nomura, M. (1968) Structure and function of Escherichia coli ribosomes. I. Partial fractionation of the functionally active ribosomal proteins and reconstitution of artificial subribosomal particles. J. Mol. Biol., 34, 575-593.
3. Traub, P. and Nomura, M. (1968) Structure and function of E. coli ribosomes. V. Reconstitution of functionally active 30S ribosomal particles from RNA and proteins. Proc. Natl Acad. Sci. U.S.A., 59, 777-784.
4. Traub, P. and Nomura, M. (1969) Studies on the assembly of ribosomes in vitro. Cold Spring Harb. Symp. Quant. Biol., 34, 63-67.
5. Rohl, R. and Nierhaus, K.H. (1982) Assembly map of the large subunit (50S) of Escherichia coli ribosomes. Proc. Natl Acad. Sci. U.S.A., 79, 729-733.
6. Herold, M. and Nierhaus, K.H. (1987) Incorporation of six additional proteins to complete the assembly map of the 50 S subunit from Escherichia coli ribosomes. J. Biol. Chem., 262, 8826-8833.
7. Talkington, M.W., Siuzdak, G. and Williamson, J.R. (2005) An assembly landscape for the 30S ribosomal subunit. Nature, 438, 628-632. (Pubitemid 41740567
8. Adilakshmi, T., Bellur, D.L. and Woodson, S.A. (2008) Concurrent nucleation of 16S folding and induced fit in 30S ribosome assembly. Nature, 455, 1268-1272.
9. Sykes, M.T. and Williamson, J.R. (2009) A complex assembly landscape for the 30S ribosomal subunit. Annu. Rev. Biophys., 38, 197-215.
10. Britton, R.A. (2009) Role of GTPases in bacterial ribosome assembly. Annu. Rev. Microbiol., 63, 155-176.
11. Uicker, W.C., Schaefer, L. and Britton, R.A. (2006) The essential GTPase RbgA (YlqF) is required for 50S ribosome assembly in Bacillus subtilis. Mol. Microbiol., 59, 528-540.
12. Schaefer, L., Uicker, W.C., Wicker-Planquart, C., Foucher, A.E., Jault, J.M. and Britton, R.A. (2006) Multiple GTPases participate in the assembly of the large ribosomal subunit in Bacillus subtilis. J. Bacteriol., 188, 8252-8258. (Pubitemid 44845697
13. Hwang, J. and Inouye, M. (2006) The tandem GTPase, Der, is essential for the biogenesis of 50S ribosomal subunits in Escherichia coli. Mol. Microbiol., 61, 1660-1672.
14. Jiang, M., Datta, K., Walker, A., Strahler, J., Bagamasbad, P., Andrews, P.C. and Maddock, J.R. (2006) The Escherichia coli GTPase CgtAE is involved in late steps of large ribosome assembly. J. Bacteriol., 188, 6757-6770. (Pubitemid 44497887
15. Matsuo, Y., Morimoto, T., Kuwano, M., Loh, P.C., Oshima, T. and Ogasawara, N. (2006) The GTP-binding protein YlqF participates in the late step of 50 S ribosomal subunit assembly in Bacillus subtilis. J. Biol. Chem., 281, 8110-8117.
16. Li, N., Chen, Y., Guo, Q., Zhang, Y., Yuan, Y., Ma, C., Deng, H., Lei, J. and Gao, N. (2013) Cryo-EM structures of the late-stage assembly intermediates of the bacterial 50S ribosomal subunit. Nucleic Acids Res., 41, 7073-7083.
17. Morimoto, T., Loh, P.C., Hirai, T., Asai, K., Kobayashi, K., Moriya, S. and Ogasawara, N. (2002) Six GTP-binding proteins of the Era/Obg family are essential for cell growth in Bacillus subtilis. Microbiology, 148, 3539-3552. (Pubitemid 35414464
18. Jomaa, A., Stewart, G., Martin-Benito, J., Zielke, R., Campbell, T.L., Maddock, J.R., Brown, E.D. and Ortega, J. (2011) Understanding ribosome assembly: The structure of in vivo assembled immature 30S subunits revealed by cryo-electron microscopy. RNA, 17, 697-709.
19. Chen, S.S. and Williamson, J.R. (2013) Characterization of the ribosome biogenesis landscape in E. coli using quantitative mass spectrometry. J. Mol. Biol., 425, 767-779.
20. Bunner, A.E., Trauger, S.A., Siuzdak, G. and Williamson, J.R. (2008) Quantitative ESI-TOF analysis of macromolecular assembly kinetics. Anal. Chem., 80, 9379-9386.
21. Sperling, E., Bunner, A.E., Sykes, M.T. and Williamson, J.R. (2008) Quantitative analysis of isotope distributions in proteomic mass spectrometry using least-squares Fourier transform convolution. Anal. Chem., 80, 4906-4917.
22. Chen, S.S., Sperling, E., Silverman, J.M., Davis, J.H. and Williamson, J.R. (2012) Measuring the dynamics of E. coli ribosome biogenesis using pulse-labeling and quantitative mass spectrometry. Mol. Biosyst., 8, 3325-3334.
23. Ludtke, S.J., Baldwin, P.R. and Chiu, W. (1999) EMAN: Semiautomated software for high-resolution single-particle reconstructions. J. Struct. Biol., 128, 82-97.
24. Mindell, J.A. and Grigorieff, N. (2003) Accurate determination of local defocus and specimen tilt in electron microscopy. J. Struct. Biol., 142, 334-347.
25. Scheres, S.H., Nunez-Ramirez, R., Sorzano, C.O., Carazo, J.M. and Marabini, R. (2008) Image processing for electron microscopy single-particle analysis using XMIPP. Nat. Protoc., 3, 977-990.
26. Schuwirth, B.S., Borovinskaya, M.A., Hau, C.W., Zhang, W., Vila-Sanjurjo, A., Holton, J.M. and Cate, J.H. (2005) Structures of the bacterial ribosome at 3.5 A resolution. Science, 310, 827-834. (Pubitemid 41567336
27. Rosenthal, P.B. and Henderson, R. (2003) Optimal determination of particle orientation, absolute hand, and contrast loss in single-particle electron cryomicroscopy. J. Mol. Biol., 333, 721-745.
28. Fernandez, J.J., Luque, D., Caston, J.R. and Carrascosa, J.L. (2008) Sharpening high resolution information in single particle electron cryomicroscopy. J. Struct. Biol., 164, 170-175.
29. Scheres, S.H., Marabini, R., Lanzavecchia, S., Cantele, F., Rutten, T., Fuller, S.D., Carazo, J.M., Burnett, R.M. and San Martin, C. (2005) Classification of single-projection reconstructions for cryo-electron microscopy data of icosahedral viruses. J. Struct. Biol., 151, 79-91.
30. Scheres, S.H., Valle, M., Nunez, R., Sorzano, C.O., Marabini, R., Herman, G.T. and Carazo, J.M. (2005) Maximum-likelihood multi-reference refinement for electron microscopy images. J. Mol. Biol., 348, 139-149.
31. Scheres, S.H., Gao, H., Valle, M., Herman, G.T., Eggermont, P.P., Frank, J. and Carazo, J.M. (2007) Disentangling conformational states of macromolecules in 3D-EM through likelihood optimization. Nat. Methods, 4, 27-29.
32. Leong, V., Kent, M., Jomaa, A. and Ortega, J. (2013) Escherichia coli rimM and yjeQ null strains accumulate immature 30S subunits of similar structure and protein complement. RNA, 19, 789-802.
33. Scheres, S.H., Valle, M. and Carazo, J.M. (2005) Fast maximumlikelihood refinement of electron microscopy images. Bioinformatics, 21(Suppl. 2), ii243-ii244.
34. Pettersen, E.F., Goddard, T.D., Huang, C.C., Couch, G.S., Greenblatt, D.M., Meng, E.C. and Ferrin, T.E. (2004) UCSF Chimera-A visualization system for exploratory research and analysis. J. Comput. Chem., 25, 1605-1612.
35. Achila, D., Gulati, M., Jain, N. and Britton, R.A. (2012) Biochemical characterization of ribosome assembly GTPase RbgA in Bacillus subtilis. J. Biol. Chem., 287, 8417-8423.
36. Schmeing, T.M., Voorhees, R.M., Kelley, A.C. and Ramakrishnan, V. (2011) How mutations in tRNA distant from the anticodon affect the fidelity of decoding. Nat. Struct. Mol. Biol., 18, 432-436.
37. Dunkle, J.A., Xiong, L., Mankin, A.S. and Cate, J.H. (2010) Structures of the Escherichia coli ribosome with antibiotics bound near the peptidyl transferase center explain spectra of drug action. Proc. Natl Acad. Sci. U.S.A., 107, 17152-17157.
38. Nomura, M. and Erdmann, V.A. (1970) Reconstitution of 50S ribosomal subunits from dissociated molecular components. Nature, 228, 744-748.
39. Fahnestock, S., Held, W. and Nomura, M. (1973) The assembly of bacterial ribosomes. In: Markham, R., Bancroft, J.B., Davies, D.R., Hopwood, D.E. and Horne, R.W. (eds), Generation of Sub-cellular Structures. North-Holland, Amsterdam, pp. 179-217.
40. Deroo, S., Hyung, S.J., Marcoux, J., Gordiyenko, Y., Koripella, R.K., Sanyal, S. and Robinson, C.V. (2012) Mechanism and rates of exchange of L7/L12 between ribosomes and the effects of binding EF-G. ACS Chem. Biol., 7, 1120-1127.
41. Schmalisch, M., Langbein, I. and Stulke, J. (2002) The general stress protein Ctc of Bacillus subtilis is a ribosomal protein. J. Mol. Microbiol. Biotechnol., 4, 495-501.
42. Korepanov, A.P., Korobeinikova, A.V., Shestakov, S.A., Garber, M.B. and Gongadze, G.M. (2012) Protein L5 is crucial for in vivo assembly of the bacterial 50S ribosomal subunit central protuberance. Nucleic Acids Res., 40, 9153-9159.
43. Wilson, D.N. and Nierhaus, K.H. (2006) The E-site story: The importance of maintaining two tRNAs on the ribosome during protein synthesis. Cell Mol. Life Sci., 63, 2725-2737.
44. Yusupov, M.M., Yusupova, G.Z., Baucom, A., Lieberman, K., Earnest, T.N., Cate, J.H. and Noller, H.F. (2001) Crystal structure of the ribosome at 5.5 A resolution. Science, 292, 883-896. (Pubitemid 32422479
45. Teraoka, H. and Nierhaus, K.H. (1978) Protein L16 induces a conformational change when incorporated into a L16-deficient core derived from Escherichia coli ribosomes. FEBS Lett., 88, 223-226. (Pubitemid 8320525
46. Guo, Q., Goto, S., Chen, Y., Feng, B., Xu, Y., Muto, A., Himeno, H., Deng, H., Lei, J. and Gao, N. (2013) Dissecting the in vivo assembly of the 30S ribosomal subunit reveals the role of RimM and general features of the assembly process. Nucleic Acids Res., 41, 2609-2620.
47. Strunk, B.S., Loucks, C.R., Su, M., Vashisth, H., Cheng, S., Schilling, J., Brooks, C.L. 3rd, Karbstein, K. and Skiniotis, G. (2011) Ribosome assembly factors prevent premature translation initiation by 40S assembly intermediates. Science, 333, 1449-1453.
48. Strunk, B.S., Novak, M.N., Young, C.L. and Karbstein, K. (2012) A translation-like cycle is a quality control checkpoint for maturing 40S ribosome subunits. Cell, 150, 111-121.
49. Karbstein, K. (2013) Quality control mechanisms during ribosome maturation. Trends Cell Biol., 23, 242-250.
50. Kazemie, M. (1975) The importance of Escherichia coli ribosomal proteins L1, L11 and L16 for the association of ribosomal subunits and the formation of the 70-S initiation complex. Eur. J. Biochem., 58, 501-510.
51. West, M., Hedges, J.B., Chen, A. and Johnson, A.W. (2005) Defining the order in which Nmd3p and Rpl10p load onto nascent 60S ribosomal subunits. Mol. Cell. Biol., 25, 3802-3813.
52. Maguire, B.A., Beniaminov, A.D., Ramu, H., Mankin, A.S. and Zimmermann, R.A. (2005) A protein component at the heart of an RNA machine: The importance of protein l27 for the function of the bacterial ribosome. Mol. Cell, 20, 427-435.
53. Maguire, B.A. and Wild, D.G. (1997) The roles of proteins L28 and L33 in the assembly and function of Escherichia coli ribosomes in vivo. Mol. Microbiol., 23, 237-245.
54. Maeder, C. and Draper, D.E. (2005) A small protein unique to bacteria organizes rRNA tertiary structure over an extensive region of the 50 S ribosomal subunit. J. Mol. Biol., 354, 436-446.