Mutations in 16S rRNA that suppress cold-sensitive initiation factor 1 affect ribosomal subunit association

FEBS Journal

Volumn 278, Issue 18, 2011, Pages 3508-3517

  Belotserkovsky, Jaroslav M ^a   Dabbs, Eric R ^b   Isaksson, Leif A ^a  

^a STOCKHOLM UNIVERSITY   (Sweden)

^b UNIVERSITY OF THE WITWATERSRAND   (South Africa)

Author keywords

16S rRNA mutant; Escherichia coli; IF1; rRNA maturation; translation

Indexed keywords

INITIATION FACTOR 1; RNA 16S;

ARTICLE; BACTERIAL GENE; BACTERIAL GROWTH; CONTROLLED STUDY; ESCHERICHIA COLI; GENE MUTATION; IN VITRO STUDY; IN VIVO STUDY; INFA GENE; NONHUMAN; PRIORITY JOURNAL; RIBOSOME SUBUNIT; RNA STRUCTURE;

AMINO ACID SUBSTITUTION; COLD TEMPERATURE; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; METHYLTRANSFERASES; MODELS, MOLECULAR; MOLECULAR CHAPERONES; MUTAGENESIS, INSERTIONAL; MUTAGENESIS, SITE-DIRECTED; MUTANT PROTEINS; MUTATION; NUCLEIC ACID CONFORMATION; PROKARYOTIC INITIATION FACTOR-1; PROTEIN MULTIMERIZATION; RECOMBINANT PROTEINS; RIBOSOME SUBUNITS; RNA, BACTERIAL; RNA, RIBOSOMAL, 16S; SEQUENCE DELETION; SUPPRESSION, GENETIC;

ESCHERICHIA COLI;

EID: 80052472108     PISSN: 1742464X     EISSN: 17424658     Source Type: Journal    
DOI: 10.1111/j.1742-4658.2011.08272.x     Document Type: Article

References (39)

1. Laursen BS, Sorensen HP, Mortensen KK, &, Sperling-Petersen HU, (2005) Initiation of protein synthesis in bacteria. Microbiol Mol Biol Rev 69, 101-123.
2. Hershey JW, Yanov J, Johnston K, &, Fakunding JL, (1977) Purification and characterization of protein synthesis initiation factors IF1, IF2, and IF3 from Escherichia coli. Arch Biochem Biophys 182, 626-638.
3. Cummings HS, &, Hershey JW, (1994) Translation initiation factor IF1 is essential for cell viability in Escherichia coli. J Bacteriol 176, 198-205.
4. Grunberg-Manago M, Dessen P, Pantaloni D, Godefroy-Colburn T, Wolfe AD, &, Dondon J, (1975) Light-scattering studies showing the effect of initiation factors on the reversible dissociation of Escherichia coli ribosomes. J Mol Biol 94, 461-478.
5. Moreno JM, Drskjotersen L, Kristensen JE, Mortensen KK, &, Sperling-Petersen HU, (1999) Characterization of the domains of E. coli initiation factor IF2 responsible for recognition of the ribosome. FEBS Lett 455, 130-134.
6. Moazed D, Samaha RR, Gualerzi C, &, Noller HF, (1995) Specific protection of 16 S rRNA by translational initiation factors. J Mol Biol 248, 207-210.
7. Phadtare S, Kazakov T, Bubunenko M, Court DL, Pestova T, &, Severinov K, (2007) Transcription antitermination by translation initiation factor IF1. J Bacteriol 189, 4087-4093.
8. Croitoru V, Semrad K, Prenninger S, Rajkowitsch L, Vejen M, Laursen BS, Sperling-Petersen HU, &, Isaksson LA, (2006) RNA chaperone activity of translation initiation factor IF1. Biochimie 88, 1875-1882.
9. Milon P, Konevega AL, Gualerzi CO, &, Rodnina MV, (2008) Kinetic checkpoint at a late step in translation initiation. Mol Cell 30, 712-720.
10. Surkov S, Nilsson H, Rasmussen LC, Sperling-Petersen HU, &, Isaksson LA, (2010) Translation initiation region dependency of translation initiation in Escherichia coli by IF1 and kasugamycin. FEBS J 277, 2428-2439.
11. Carter AP, Clemons WM Jr, Brodersen DE, Morgan-Warren RJ, Hartsch T, Wimberly BT, &, Ramakrishnan V, (2001) Crystal structure of an initiation factor bound to the 30S ribosomal subunit. Science 291, 498-501.
12. Dahlquist KD, &, Puglisi JD, (2000) Interaction of translation initiation factor IF1 with the E. coli ribosomal A site. J Mol Biol 299, 1-15.
13. Cate JH, Yusupov MM, Yusupova GZ, Earnest TN, &, Noller HF, (1999) X-ray crystal structures of 70S ribosome functional complexes. Science 285, 2095-2104.
14. Croitoru V, Bucheli-Witschel M, Hagg P, Abdulkarim F, &, Isaksson LA, (2004) Generation and characterization of functional mutants in the translation initiation factor IF1 of Escherichia coli. Eur J Biochem 271, 534-544.
15. Belotserkovsky JM, Isak GI, &, Isaksson LA, (2011) Suppression of a cold-sensitive mutant initiation factor 1 by alterations in the 23S rRNA maturation region. FEBS J 278, 1745-1756.
16. Powers T, &, Noller HF, (1995) Hydroxyl radical footprinting of ribosomal proteins on 16S rRNA. RNA 1, 194-209.
17. Powers T, &, Noller HF, (1991) A functional pseudoknot in 16S ribosomal RNA. EMBO J 10, 2203-2214.
18. Bjorkman J, Samuelsson P, Andersson DI, &, Hughes D, (1999) Novel ribosomal mutations affecting translational accuracy, antibiotic resistance and virulence of Salmonella typhimurium. Mol Microbiol 31, 53-58.
19. Leclerc D, Melancon P, &, Brakier-Gingras L, (1991) Mutations in the 915 region of Escherichia coli 16S ribosomal RNA reduce the binding of streptomycin to the ribosome. Nucleic Acids Res 19, 3973-3977.
20. Tscherne JS, Nurse K, Popienick P, &, Ofengand J, (1999) Purification, cloning, and characterization of the 16 S RNA m2G1207 methyltransferase from Escherichia coli. J Biol Chem 274, 924-929.
21. 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.
22. Brodersen DE, Clemons WM Jr, Carter AP, Wimberly BT, &, Ramakrishnan V, (2002) Crystal structure of the 30 S ribosomal subunit from Thermus thermophilus: structure of the proteins and their interactions with 16 S RNA. J Mol Biol 316, 725-768.
23. Connell SR, Trieber CA, Stelzl U, Einfeldt E, Taylor DE, &, Nierhaus KH, (2002) The tetracycline resistance protein Tet(o) perturbs the conformation of the ribosomal decoding centre. Mol Microbiol 45, 1463-1472.
24. Prescott C, Krabben L, &, Nierhaus K, (1991) Ribosomes containing the C1054-deletion mutation in E. coli 16S rRNA act as suppressors at all three nonsense codons. Nucleic Acids Res 19, 5281-5283.
25. Ogle JM, Brodersen DE, Clemons WM Jr, Tarry MJ, Carter AP, &, Ramakrishnan V, (2001) Recognition of cognate transfer RNA by the 30S ribosomal subunit. Science 292, 897-902.
26. Brodersen DE, Clemons WM Jr, Carter AP, Morgan-Warren RJ, Wimberly BT, &, Ramakrishnan V, (2000) The structural basis for the action of the antibiotics tetracycline, pactamycin, and hygromycin B on the 30S ribosomal subunit. Cell 103, 1143-1154.
27. Dontsova O, Dokudovskaya S, Kopylov A, Bogdanov A, Rinke-Appel J, Junke N, &, Brimacombe R, (1992) Three widely separated positions in the 16S RNA lie in or close to the ribosomal decoding region; a site-directed cross-linking study with mRNA analogues. EMBO J 11, 3105-3116.
28. Yusupov MM, Yusupova GZ, Baucom A, Lieberman K, Earnest TN, Cate JH, &, Noller HF, (2001) Crystal structure of the ribosome at 5.5 A resolution. Science 292, 883-896.
29. Sun Q, Vila-Sanjurjo A, &, O'Connor M, (2010) Mutations in the intersubunit bridge regions of 16S rRNA affect decoding and subunit-subunit interactions on the 70S ribosome. Nucleic Acids Res 39, 3321-3330.
30. Liiv A, &, O'Connor M, (2006) Mutations in the intersubunit bridge regions of 23 S rRNA. J Biol Chem 281, 29850-29862.
31. Hirabayashi N, Sato NS, &, Suzuki T, (2006) Conserved loop sequence of helix 69 in Escherichia coli 23 S rRNA is involved in A-site tRNA binding and translational fidelity. J Biol Chem 281, 17203-17211.
32. Holmes KL, &, Culver GM, (2004) Mapping structural differences between 30S ribosomal subunit assembly intermediates. Nat Struct Mol Biol 11, 179-186.
33. Holmes KL, &, Culver GM, (2005) Analysis of conformational changes in 16 S rRNA during the course of 30 S subunit assembly. J Mol Biol 354, 340-357.
34. Ghosh S, &, Joseph S, (2005) Nonbridging phosphate oxygens in 16S rRNA important for 30S subunit assembly and association with the 50S ribosomal subunit. RNA 11, 657-667.
35. Serganov A, Benard L, Portier C, Ennifar E, Garber M, Ehresmann B, &, Ehresmann C, (2001) Role of conserved nucleotides in building the 16 S rRNA binding site for ribosomal protein S15. J Mol Biol 305, 785-803.
36. Brosius J, Ullrich A, Raker MA, Gray A, Dull TJ, Gutell RR, &, Noller HF, (1981) Construction and fine mapping of recombinant plasmids containing the rrnB ribosomal RNA operon of E. coli. Plasmid 6, 112-118.
37. Woodcock DM, Crowther PJ, Doherty J, Jefferson S, DeCruz E, Noyer-Weidner M, Smith SS, Michael MZ, &, Graham MW, (1989) Quantitative evaluation of Escherichia coli host strains for tolerance to cytosine methylation in plasmid and phage recombinants. Nucleic Acids Res 17, 3469-3478.
38. Baba T, Ara T, Hasegawa M, Takai Y, Okumura Y, Baba M, Datsenko KA, Tomita M, Wanner BL, &, Mori H, (2006) Construction of Escherichia coli K-12 in-frame, single-gene knockout mutants: the Keio collection. Mol Syst Biol 2, 2006.0008.
39. Cannone JJ, Subramanian S, Schnare MN, Collett JR, D'Souza LM, Du Y, Feng B, Lin N, Madabusi LV, Muller KM, et al. (2002) The comparative RNA web (CRW) site: an online database of comparative sequence and structure information for ribosomal, intron, and other RNAs. BMC Bioinformatics 3, 2.