Conserved Bacterial RNase YbeY Plays Key Roles in 70S Ribosome Quality Control and 16S rRNA Maturation

Molecular Cell

Volumn 49, Issue 3, 2013, Pages 427-438

  Jacob, Asha Ivy ^a   Köhrer, Caroline ^a   Davies, Bryan William ^b   RajBhandary, Uttam Lal ^a   Walker, Graham Charles ^a  

^a MASSACHUSETTS INSTITUTE OF TECHNOLOGY   (United States)

^b HARVARD MEDICAL SCHOOL   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

DOUBLE STRANDED RNA; KASUGAMYCIN; RIBONUCLEASE; RIBOSOME PROTEIN; RNA 16S; RNA 70S; SINGLE STRANDED RNA; UNCLASSIFIED DRUG; YBEY PROTEIN;

ARTICLE; BACTERIAL GENE; BACTERIAL GENOME; NONHUMAN; QUALITY CONTROL; RIBOSOME; RIBOSOME SUBUNIT; RNA CLEAVAGE; RNA DEGRADATION;

ARGININE; BASE SEQUENCE; CONSERVED SEQUENCE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; EXORIBONUCLEASES; HISTIDINE; HOT TEMPERATURE; METALLOPROTEINS; METALS; MODELS, BIOLOGICAL; MOLECULAR SEQUENCE DATA; MUTATION; PROTEIN BIOSYNTHESIS; RIBOSOME SUBUNITS, SMALL, BACTERIAL; RIBOSOMES; RNA PROCESSING, POST-TRANSCRIPTIONAL; RNA, RIBOSOMAL, 16S; STRESS, PHYSIOLOGICAL; SUBSTRATE SPECIFICITY;

BACTERIA (MICROORGANISMS);

EID: 84873465400     PISSN: 10972765     EISSN: 10974164     Source Type: Journal    
DOI: 10.1016/j.molcel.2012.11.025     Document Type: Article

References (59)

1. Akerley B.J., Rubin E.J., Novick V.L., Amaya K., Judson N., Mekalanos J.J. A genome-scale analysis for identification of genes required for growth or survival of Haemophilus influenzae. Proc. Natl. Acad. Sci. USA 2002, 99:966-971.
2. Arraiano C.M., Andrade J.M., Domingues S., Guinote I.B., Malecki M., Matos R.G., Moreira R.N., Pobre V., Reis F.P., Saramago M., et al. The critical role of RNA processing and degradation in the control of gene expression. FEMS Microbiol. Rev. 2010, 34:883-923.
3. Awano N., Rajagopal V., Arbing M., Patel S., Hunt J., Inouye M., Phadtare S. Escherichia coli RNase R has dual activities, helicase and RNase. J. Bacteriol. 2010, 192:1344-1352.
4. Basturea G.N., Zundel M.A., Deutscher M.P. Degradation of ribosomal RNA during starvation: comparison to quality control during steady-state growth and a role for RNase PH. RNA 2011, 17:338-345.
5. Bollenbach T.J., Lange H., Gutierrez R., Erhardt M., Stern D.B., Gagliardi D. RNR1, a 3'-5' exoribonuclease belonging to the RNR superfamily, catalyzes 3' maturation of chloroplast ribosomal RNAs in Arabidopsis thaliana. Nucleic Acids Res. 2005, 33:2751-2763.
6. Brown T., Mackey K., Du T. Analysis of RNA by northern and slot blot hybridization. Curr. Protoc. Mol. Biol. 2004, Chapter 4. Unit 4.9.
7. Cameron V., Uhlenbeck O.C. 3'-Phosphatase activity in T4 polynucleotide kinase. Biochemistry 1977, 16:5120-5126.
8. Campbell T.L., Brown E.D. Genetic interaction screens with ordered overexpression and deletion clone sets implicate the Escherichia coli GTPase YjeQ in late ribosome biogenesis. J. Bacteriol. 2008, 190:2537-2545.
9. Casadaban M.J., Cohen S.N. Lactose genes fused to exogenous promoters in one step using a Mu-lac bacteriophage: in vivo probe for transcriptional control sequences. Proc. Natl. Acad. Sci. USA 1979, 76:4530-4533.
10. Chen C., Deutscher M.P. RNase R is a highly unstable protein regulated by growth phase and stress. RNA 2010, 16:667-672.
11. Cheng Z.F., Deutscher M.P. Purification and characterization of the Escherichia coli exoribonuclease RNase R. Comparison with RNase II. J. Biol. Chem. 2002, 277:21624-21629.
12. Cole S.E., LaRiviere F.J., Merrikh C.N., Moore M.J. A convergence of rRNA and mRNA quality control pathways revealed by mechanistic analysis of nonfunctional rRNA decay. Mol. Cell 2009, 34:440-450.
13. Condon C., Putzer H. The phylogenetic distribution of bacterial ribonucleases. Nucleic Acids Res. 2002, 30:5339-5346.
14. Davies B.W., Walker G.C. A highly conserved protein of unknown function is required by Sinorhizobium meliloti for symbiosis and environmental stress protection. J. Bacteriol. 2008, 190:1118-1123.
15. Davies B.W., Köhrer C., Jacob A.I., Simmons L.A., Zhu J., Aleman L.M., Rajbhandary U.L., Walker G.C. Role of Escherichia coli YbeY, a highly conserved protein, in rRNA processing. Mol. Microbiol. 2010, 78:506-518.
16. Deutscher M.P. Degradation of stable RNA in bacteria. J. Biol. Chem. 2003, 278:45041-45044.
17. Deutscher M.P. Maturation and degradation of ribosomal RNA in bacteria. Prog. Mol. Biol. Transl. Sci. 2009, 85:369-391.
18. Etchegaray J.P., Inouye M. Translational enhancement by an element downstream of the initiation codon in Escherichia coli. J. Biol. Chem. 1999, 274:10079-10085.
19. Gallagher S., Winston S.E., Fuller S.A., Hurrell J.G. Immunoblotting and immunodetection. Curr. Protoc. Mol. Biol. 2008, Chapter 10. Unit 10.18.
20. Ghosh S., Deutscher M.P. Oligoribonuclease is an essential component of the mRNA decay pathway. Proc. Natl. Acad. Sci. USA 1999, 96:4372-4377.
21. Gil R., Silva F.J., Peretó J., Moya A. Determination of the core of a minimal bacterial gene set. Microbiol. Mol. Biol. Rev. 2004, 68:518-537.
22. 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.
23. Inoue K., Chen J., Tan Q., Inouye M. Era and RbfA have overlapping function in ribosome biogenesis in Escherichia coli. J. Mol. Microbiol. Biotechnol. 2006, 11:41-52.
24. 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.
25. Kazakov A.E., Vassieva O., Gelfand M.S., Osterman A., Overbeek R. Bioinformatics classification and functional analysis of PhoH homologs. In Silico Biol. (Gedrukt) 2003, 3:3-15.
26. Kobayashi K., Ehrlich S.D., Albertini A., Amati G., Andersen K.K., Arnaud M., Asai K., Ashikaga S., Aymerich S., Bessieres P., et al. Essential Bacillus subtilis genes. Proc. Natl. Acad. Sci. USA 2003, 100:4678-4683.
27. LaRiviere F.J., Cole S.E., Ferullo D.J., Moore M.J. A late-acting quality control process for mature eukaryotic rRNAs. Mol. Cell 2006, 24:619-626.
28. Li Z., Deutscher M.P. The tRNA processing enzyme RNase T is essential for maturation of 5S RNA. Proc. Natl. Acad. Sci. USA 1995, 92:6883-6886.
29. Li Z., Pandit S., Deutscher M.P. Maturation of 23S ribosomal RNA requires the exoribonuclease RNase T. RNA 1999, 5:139-146.
30. Li Z., Pandit S., Deutscher M.P. RNase G (CafA protein) and RNase E are both required for the 5' maturation of 16S ribosomal RNA. EMBO J. 1999, 18:2878-2885.
31. Liang W., Deutscher M.P. A novel mechanism for ribonuclease regulation: transfer-messenger RNA (tmRNA) and its associated protein SmpB regulate the stability of RNase R. J. Biol. Chem. 2010, 285:29054-29058.
32. Liang W., Deutscher M.P. Post-translational modification of RNase R is regulated by stress-dependent reduction in the acetylating enzyme Pka (YfiQ). RNA 2012, 18:37-41.
33. Liang X.H., Liu Q., Fournier M.J. Loss of rRNA modifications in the decoding center of the ribosome impairs translation and strongly delays pre-rRNA processing. RNA 2009, 15:1716-1728.
34. Mangiarotti G., Turco E., Ponzetto A., Altruda F. Precursor 16S RNA in active 30S ribosomes. Nature 1974, 247:147-148.
35. Muth G.W., Ortoleva-Donnelly L., Strobel S.A. A single adenosine with a neutral pKa in the ribosomal peptidyl transferase center. Science 2000, 289:947-950.
36. Oganesyan V., Busso D., Brandsen J., Chen S., Jancarik J., Kim R., Kim S.H. Structure of the hypothetical protein AQ_1354 from Aquifex aeolicus. Acta Crystallogr. D Biol. Crystallogr. 2003, 59:1219-1223.
37. Pagliarini D.J., Calvo S.E., Chang B., Sheth S.A., Vafai S.B., Ong S.E., Walford G.A., Sugiana C., Boneh A., Chen W.K., et al. A mitochondrial protein compendium elucidates complex I disease biology. Cell 2008, 134:112-123.
38. Pandey S.P., Minesinger B.K., Kumar J., Walker G.C. A highly conserved protein of unknown function in Sinorhizobium meliloti affects sRNA regulation similar to Hfq. Nucleic Acids Res. 2011, 39:4691-4708.
39. Penhoat C.H., Li Z., Atreya H.S., Kim S., Yee A., Xiao R., Murray D., Arrowsmith C.H., Szyperski T. NMR solution structure of Thermotoga maritima protein TM1509 reveals a Zn-metalloprotease-like tertiary structure. J. Struct. Funct. Genomics 2005, 6:51-62.
40. Powers T., Noller H.F. Dominant lethal mutations in a conserved loop in 16S rRNA. Proc. Natl. Acad. Sci. USA 1990, 87:1042-1046.
41. Powers T., Noller H.F. Allele-specific structure probing of plasmid-derived 16S ribosomal RNA from Escherichia coli. Gene 1993, 123:75-80.
42. Purusharth R.I., Madhuri B., Ray M.K. Exoribonuclease R in Pseudomonas syringae is essential for growth at low temperature and plays a novel role in the 3' end processing of 16 and 5 S ribosomal RNA. J. Biol. Chem. 2007, 282:16267-16277.
43. Rasouly A., Schonbrun M., Shenhar Y., Ron E.Z. YbeY, a heat shock protein involved in translation in Escherichia coli. J. Bacteriol. 2009, 191:2649-2655.
44. Rasouly A., Davidovich C., Ron E.Z. The heat shock protein YbeY is required for optimal activity of the 30S ribosomal subunit. J. Bacteriol. 2010, 192:4592-4596.
45. Roy-Chaudhuri B., Kirthi N., Culver G.M. Appropriate maturation and folding of 16S rRNA during 30S subunit biogenesis are critical for translational fidelity. Proc. Natl. Acad. Sci. USA 2010, 107:4567-4572.
46. Sambrook J., Russell D.W. Molecular Cloning. A Laboratory Manual 2001, Cold Spring Harbor Laboratory, Cold Spring Harbor, NY.
47. Sato A., Kobayashi G., Hayashi H., Yoshida H., Wada A., Maeda M., Hiraga S., Takeyasu K., Wada C. The GTP binding protein Obg homolog ObgE is involved in ribosome maturation. Genes Cells 2005, 10:393-408.
48. Shine J., Dalgarno L. Determinant of cistron specificity in bacterial ribosomes. Nature 1975, 254:34-38.
49. Siibak T., Peil L., Dönhöfer A., Tats A., Remm M., Wilson D.N., Tenson T., Remme J. Antibiotic-induced ribosomal assembly defects result from changes in the synthesis of ribosomal proteins. Mol. Microbiol. 2011, 80:54-67.
50. Sonnhammer E.L., Eddy S.R., Durbin R. Pfam: a comprehensive database of protein domain families based on seed alignments. Proteins 1997, 28:405-420.
51. Thompson J., Kim D.F., O'Connor M., Lieberman K.R., Bayfield M.A., Gregory S.T., Green R., Noller H.F., Dahlberg A.E. Analysis of mutations at residues A2451 and G2447 of 23S rRNA in the peptidyltransferase active site of the 50S ribosomal subunit. Proc. Natl. Acad. Sci. USA 2001, 98:9002-9007.
52. 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.
53. Verstraeten N., Fauvart M., Versées W., Michiels J. The universally conserved prokaryotic GTPases. Microbiol. Mol. Biol. Rev. 2011, 75:507-542.
54. Vesper O., Amitai S., Belitsky M., Byrgazov K., Kaberdina A.C., Engelberg-Kulka H., Moll I. Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli. Cell 2011, 147:147-157.
55. Wachi M., Umitsuki G., Shimizu M., Takada A., Nagai K. Escherichia coli cafA gene encodes a novel RNase, designated as RNase G, involved in processing of the 5' end of 16S rRNA. Biochem. Biophys. Res. Commun. 1999, 259:483-488.
56. Walter M., Kilian J., Kudla J. PNPase activity determines the efficiency of mRNA 3'-end processing, the degradation of tRNA and the extent of polyadenylation in chloroplasts. EMBO J. 2002, 21:6905-6914.
57. Wireman J.W., Sypherd P.S. In vitro assembly of 30S ribosomal particles from precursor 16S RNA of Escherichia coli. Nature 1974, 247:552-554.
58. Xu Z., O'Farrell H.C., Rife J.P., Culver G.M. A conserved rRNA methyltransferase regulates ribosome biogenesis. Nat. Struct. Mol. Biol. 2008, 15:534-536.
59. Zhan C., Fedorov E.V., Shi W., Ramagopal U.A., Thirumuruhan R., Manjasetty B.A., Almo S.C., Fiser A., Chance M.R., Fedorov A.A. The ybeY protein from Escherichia coli is a metalloprotein. Acta Crystallogr. Sect. F Struct. Biol. Cryst. Commun. 2005, 61:959-963.