The 100S ribosome: Ribosomal hibernation induced by stress

Wiley Interdisciplinary Reviews: RNA

Volumn 5, Issue 5, 2014, Pages 723-732

  Yoshida, Hideji ^a   Wada, Akira ^b  

^a OSAKA MEDICAL COLLEGE   (Japan)

^b Yoshida Biological Laboratory   (Japan)

Author keywords

[No Author keywords available]

Indexed keywords

CYCLIC AMP CAMP RECEPTOR PROTEIN; DIMER; PROTEIN; RECEPTOR PROTEIN; RIBOSOME MODULATION FACTOR; RIBOSOME PROTEIN; UNCLASSIFIED DRUG; CYCLIC AMP; CYCLIC AMP BINDING PROTEIN; ESCHERICHIA COLI PROTEIN; HPF PROTEIN, E COLI; RIBOSOME MODULATION FACTOR, E COLI; RIBOSOME RNA;

100S RIBOSOME; ARTICLE; BACTERIAL SURVIVAL; BINDING SITE; BORDETELLA PARAPERTUSSIS; CELL VIABILITY; CONFORMATIONAL TRANSITION; CRYOELECTRON MICROSCOPY; CRYSTAL STRUCTURE; DIMERIZATION; ELECTRON MICROSCOPY; ELECTRON TOMOGRAPHY; ESCHERICHIA COLI; GAMMAPROTEOBACTERIA; GENE EXPRESSION; HIBERNATION; IN VITRO STUDY; LACTOCOCCUS LACTIS; NITROSOMONAS EUROPAEA; NONHUMAN; OSMOTIC STRESS; PASTEURELLA MULTOCIDA; PRIORITY JOURNAL; PROTEIN EXPRESSION; PROTEIN SECONDARY STRUCTURE; PROTEIN SYNTHESIS; QUORUM SENSING; RIBOSOME; RIBOSOME SUBUNIT; STAINING; STRESS; TRANSCRIPTION INITIATION; TRANSLATION INITIATION; XYLELLA FASTIDIOSA; BIOSYNTHESIS; GENE EXPRESSION REGULATION; GENETICS; METABOLISM; PHYSIOLOGICAL STRESS; PROTEIN MULTIMERIZATION;

ESCHERICHIA COLI; GAMMAPROTEOBACTERIA;

CYCLIC AMP; CYCLIC AMP RECEPTOR PROTEIN; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; GENE EXPRESSION REGULATION; PROTEIN BIOSYNTHESIS; PROTEIN MULTIMERIZATION; RIBOSOMAL PROTEINS; RIBOSOMES; RNA, RIBOSOMAL; STRESS, PHYSIOLOGICAL;

EID: 84906253520     PISSN: 17577004     EISSN: 17577012     Source Type: Journal    
DOI: 10.1002/wrna.1242     Document Type: Article

References (55)

1. Roszak DB, Colwell RR. Survival strategies of bacteria in the natural environment. Microbiol Rev 1987, 51:365-379.
2. Kolter R, Siegele DA, Tormo A. The stationary phase of the bacterial life cycle. Annu Rev Microbiol 1993, 47:855-874.
3. Huisman GW, Siegele DA, Zambrabo MM, Kolter R. Morphological and physiological changes during stationary phase. In: Neidhardt FC, ed. Escherichia coli and Salmonella: Cellular and Molecular Biology. ASM Press: Washington, DC 1996, 2: 1672-1682.
4. Loewen PC, Hengge-Aronis R. The role of the sigma factor sigma S (KatF) in bacterial global regulation. Annu Rev Microbiol 1994, 48:53-80.
5. Ishihama A. Modulation of the nucleoid, the transcription apparatus, and the translation machinery in bacteria for stationary phase survival. Genes Cells 1999, 4:135-143.
6. Ishihama A. Functional modulation of Escherichia coli RNA polymerase. Annu Rev Microbiol 2000, 54:499-518.
7. Tanaka K, Takayanagi Y, Fujita N, Ishihama A, Takahashi H. Heterogeneity of the principal sigma factor in Escherichia coli: the rpoS gene product, sigma 38, is a second principal sigma factor of RNA polymerase in stationary-phase Escherichia coli. Proc Natl Acad Sci U S A 1993, 90:3511-3515.
8. Shajani Z, Sykes MT, Williamson JR. Assembly of bacterial ribosomes. Annu Rev Biochem 2011, 80:501-526.
9. Kaczanowska M, Ryden-Aulin M. Ribosome biogenesis and the translation process in Escherichia coli. Microbiol Mol Biol Rev 2007, 71:477-494.
10. Korostelev A, Ermolenko DN, Noller HF. Structural dynamics of the ribosome. Curr Opin Chem Biol 2008, 12:674-683.
11. Nierhaus KH. Ribosome assembly. In: Nierhaus KH, Wilson DN, eds. Protein Synthesis and Ribosome Structure 2004, Weinheim: Wiley-VCH Verlag GmbH & Co. KGaA; 85-105.
12. Cashel M, Gentry DR, Hernandez VJ, Vinella D. The stringent response. In: Neidhardt FC, ed. Escherichia coli and Salmonella: Cellular and Molecular Biology. 1996, 1. ASM Press: Washington, DC 1458-1496.
13. Lazzarini R, Dahlberg A. The control of ribonucleic acid synthesis during amino acid deprivation in Escherichia coli. J Biol Chem 1971, 246:420-429.
14. Izutsu K, Wada A, Wada C. Expression of ribosome modulation factor (RMF) in Escherichia coli requires ppGpp. Genes Cells 2001, 6:665-676.
15. Wada A, Yamazaki Y, Fujita N, Ishihama A. Structure and probable genetic location of a "ribosome modulation factor" associated with 100S ribosomes in stationary-phase Escherichia coli cells. Proc Natl Acad Sci U S A 1990, 87:2657-2661.
16. Kato T, Yoshida H, Miyata T, Maki Y, Wada A, Namba K. Structure of the 100S ribosome in the hibernation stage revealed by electron cryomicroscopy. Structure 2010, 18:719-724.
17. Yoshida H, Yamamoto H, Uchiumi T, Wada A. RMF inactivates ribosomes by covering the peptidyl transferase centre and entrance of peptide exit tunnel. Genes Cells 2004, 9:271-278.
18. Polikanov YS, Blaha GM, Steitz TA. How hibernation factors RMF, HPF, and YfiA turn off protein synthesis. Science 2012, 336:915-918.
19. Wada A, Igarashi K, Yoshimura S, Aimoto S, Ishihama A. Ribosome modulation factor: stationary growth phase-specific inhibitor of ribosome functions from Escherichia coli. Biochem Biophys Res Commun 1995, 214:410-417.
20. Yamagishi M, Matsushima H, Wada A, Sakagami M, Fujita N, Ishihama A. Regulation of the Escherichia coli rmf gene encoding the ribosome modulation factor: growth phase- and growth rate-dependent control. EMBO J 1993, 12:625-630.
21. Aiso T, Yoshida H, Wada A, Ohki R. Modulation of mRNA stability participates in stationary-phase-specific expression of ribosome modulation factor. J Bacteriol 2005, 187:1951-1958.
22. Yoshida H, Maki Y, Kato H, Fujisawa H, Izutsu K, Wada C, Wada A. The ribosome modulation factor (RMF) binding site on the 100S ribosome of Escherichia coli. J Biochem 2002, 132:983-989.
23. Ueta M, Wada C, Wada A. Formation of 100S ribosomes in Staphylococcus aureus by the hibernation promoting factor homolog SaHPF. Genes Cells 2010, 15:43-58.
24. Tagami K, Nanamiya H, Kazo Y, Maehashi M, Suzuki S, Namba E, Hoshiya M, Hanai R, Tozawa Y, Morimoto T, et al. Expression of a small (p)ppGpp synthetase, YwaC, in the (p)ppGpp(0) mutant of Bacillus subtilis triggers YvyD-dependent dimerization of ribosome. Microbiologyopen 2012, 1:115-134.
25. Ueta M, Wada C, Daifuku T, Sako Y, Bessho Y, Kitamura A, Ohniwa RL, Morikawa K, Yoshida H, Kato T, et al. Conservation of two distinct types of 100S ribosome in bacteria. Genes Cells 2013, 18:554-574.
26. Puri P, Eckhardt TH, Franken LE, Fusetti F, Stuart MC, Boekema EJ, Kuipers OP, Kok J, Poolman B. Lactococcus lactis YfiA is necessary and sufficient for ribosome dimerization. Mol Microbiol 2014, 91:394-407.
27. Ueta M, Ohniwa RL, Yoshida H, Maki Y, Wada C, Wada A. Role of HPF (hibernation promoting factor) in translational activity in Escherichia coli. J Biochem 2008, 143:425-433.
28. McCarthy BJ. Variations in bacterial ribosomes. Biochim Biophys Acta 1960, 39:563-564.
29. Wada A. Growth phase coupled modulation of Escherichia coli ribosomes. Genes Cells 1998, 3:203-208.
30. Shimada T, Yoshida H, Ishihama A. Involvement of cyclic AMP receptor protein in regulation of the rmf gene encoding the ribosome modulation factor in Escherichia coli. J Bacteriol 2013, 195:2212-2219.
31. Terui Y, Tabei Y, Akiyama M, Higashi K, Tomitori H, Yamamoto K, Ishihama A, Igarashi K, Kashiwagi K. Ribosome modulation factor, an important protein for cell viability encoded by the polyamine modulon. J Biol Chem 2010, 285:28698-28707.
32. Niven GW. Ribosome modulation factor protects Escherichia coli during heat stress, but this may not be dependent on ribosome dimerization. Arch Microbiol 2004, 182:60-66.
33. el-Sharoud WM, Niven GW. The activity of ribosome modulation factor during growth of Escherichia coli under acidic conditions. Arch Microbiol 2005, 184:18-24.
34. Garay-Arroyo A, Colmenero-Flores JM, Garciarrubio A, Covarrubias AA. Highly hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit. J Biol Chem 2000, 275:5668-5674.
35. Moen B, Janbu AO, Langsrud S, Langsrud O, Hobman JL, Constantinidou C, Kohler A, Rudi K. Global responses of Escherichia coli to adverse conditions determined by microarrays and FT-IR spectroscopy. Can J Microbiol 2009, 55:714-728.
36. Belasco JG. mRNA Degradation in Prokaryotic Cells: An Overview. New York, NY: Academic Press; 1993, 3-12.
37. Chen LH, Emory SA, Bricker AL, Bouvet P, Belasco JG. Structure and function of a bacterial mRNA stabilizer: analysis of the 5' untranslated region of ompA mRNA. J Bacteriol 1991, 173:4578-4586.
38. Maki Y, Yoshida H, Wada A. Two proteins, YfiA and YhbH, associated with resting ribosomes in stationary phase Escherichia coli. Genes Cells 2000, 5:965-974.
39. Ueta M, Yoshida H, Wada C, Baba T, Mori H, Wada A. Ribosome binding proteins YhbH and YfiA have opposite functions during 100S formation in the stationary phase of Escherichia coli. Genes Cells 2005, 10:1103-1112.
40. DeLisa MP, Wu CF, Wang L, Valdes JJ, Bentley WE. DNA microarray-based identification of genes controlled by autoinducer 2-stimulated quorum sensing in Escherichia coli. J Bacteriol 2001, 183:5239-5247.
41. Yoshida H, Ueta M, Maki Y, Sakai A, Wada A. Activities of Escherichia coli ribosomes in IF3 and RMF change to prepare 100S ribosome formation on entering the stationary growth phase. Genes Cells 2009, 14:271-280.
42. Pietro FD, Brandi A, Dzeladini N, Fabbretti A, Carzaniga T, Piersimoni L, Pon CL, Giuliodori AM. Role of the ribosome-associated protein PY in the cold-shock response of Escherichia coli. Microbiologyopen 2013, 2:293-307.
43. Agafonov DE, Kolb VA, Spirin AS. Ribosome-associated protein that inhibits translation at the aminoacyl-tRNA binding stage. EMBO Rep 2001, 2:399-402.
44. Hauser R, Pech M, Kijek J, Yamamoto H, Titz B, Naeve F, Tovchigrechko A, Yamamoto K, Szaflarski W, Takeuchi N, et al. RsfA (YbeB) proteins are conserved ribosomal silencing factors. PLoS Genet 2012, 8:e1002815.
45. Schuwirth BS, Borovinskaya MA, Hau CW, Zhang W, Vila-Sanurjo A, Holton JM, Cate JH. Structures of the bacterial ribosome at 3.5 Å resolution. Science 2005, 310:827-834.
46. Takyar S, Hickerson RP, Noller HF. mRNA helicase activity of the ribosome. Cell 2005, 120:49-58.
47. Ortiz JO, Brandt F, Matias VR, Sennels L, Rappsilber J, Scheres SH, Eibauer M, Hartl FU, Baumeister W. Structure of hibernating ribosomes studied by cryoelectron tomography in vitro and in situ. J Cell Biol 2010, 190:613-621.
48. Sharma MR, Donhofer A, Barat C, Marquez V, Datta PP, Fucini P, Wilson DN, Agrawal RK. PSRP1 is not a ribosomal protein, but a ribosome-binding factor that is recycled by the ribosome-recycling factor (RRF) and elongation factor G (EF-G). J Biol Chem 2010, 285:4006-4014.
49. Hinnebusch AG. The eIF-2 alpha kinases: regulators of protein synthesis in starvation and stress. Semin Cell Biol 1994, 5:417-426.
50. Krokowski D, Gaccioli F, Majumder M, Mullins MR, Yuan CL, Papadopoulou B, Merrick WC, Komar AA, Taylor D, Hatzoglou M. Characterization of hibernating ribosomes in mammalian cells. Cell Cycle 2011, 10:2691-2702.
51. Kanjee U, Ogata K, Houry WA. Direct binding targets of the stringent response alarmone (p)ppGpp. Mol Microbiol 2012, 85:1029-1043.
52. Dennis P, Nomura M. Stringent control of ribosomal protein gene expression in Escherichia coli. Proc Natl Acad Sci U S A 1974, 71:3819-3823.
53. Gentry DR, Cashel M. Cellular localization of the Escherichia coli SpoT protein. J Bacteriol 1995, 177:3890-3893.
54. Shimada T, Fujita N, Yamamoto K, Ishihama A. Novel roles of cAMP receptor protein (CRP) in regulation of transport and metabolism of carbon sources. PLoS One 2011, 6:e20081.
55. Hirokawa G, Nijman RM, Raj VS, Kaji H, Igarashi K, Kaji A. The role of ribosome recycling factor in dissociation of 70S ribosomes into subunits. RNA 2005, 11:1317-1328.