Ribosome hibernation factor promotes Staphylococcal survival and differentially represses translation

Nucleic Acids Research

Volumn 44, Issue 10, 2016, Pages 4881-4893

  Basu, Arnab ^a   Yap, Mee Ngan F ^a  

^a SAINT LOUIS UNIVERSITY SCHOOL OF MEDICINE   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

HIBERNATION PROMOTING FACTOR; MESSENGER RNA; UNCLASSIFIED DRUG; BACTERIAL PROTEIN; RIBOSOME PROTEIN; START CODON;

ADAPTATION; AMINO TERMINAL SEQUENCE; ARTICLE; BACTERIAL STRAIN; BACTERIAL SURVIVAL; BACTERIAL VIABILITY; CARBOXY TERMINAL SEQUENCE; CONTROLLED STUDY; DIMERIZATION; NONHUMAN; PRIORITY JOURNAL; PROTEIN BINDING; PROTEIN FUNCTION; PROTEIN SYNTHESIS; RIBOSOME; STAPHYLOCOCCUS AUREUS; STRESS; TRANSLATION INITIATION; GENETICS; METABOLISM; MICROBIAL VIABILITY; MUTAGENESIS; MUTATION; PHYSIOLOGY; START CODON;

BACTERIAL PROTEINS; CODON, INITIATOR; DIMERIZATION; MICROBIAL VIABILITY; MUTAGENESIS; MUTATION; PROTEIN BIOSYNTHESIS; RIBOSOMAL PROTEINS; RIBOSOMES; STAPHYLOCOCCUS AUREUS;

EID: 84973520073     PISSN: 03051048     EISSN: 13624962     Source Type: Journal    
DOI: 10.1093/nar/gkw180     Document Type: Article

References (55)

1. Buttgereit, F., and Brand, M.D. (1995). A hierarchy of ATP-consuming processes in mammalian cells. Biochem. J., 312, 163-167
2. Russell, J.B., and Cook, G.M. (1995). Energetics of bacterial growth: balance of anabolic, and catabolic reactions. Microbiol. Rev., 59, 48-62
3. Szaflarski, W., and Nierhaus, K.H. (2007). Question 7: optimized energy consumption for protein synthesis. Orig. Life Evol. Biosph., 37, 423-428
4. Polikanov, Y.S., Blaha, G.M., and Steitz, T.A. (2012). How hibernation factors RMF, HPF, and YfiA turn off protein synthesis. Science, 336, 915-918
5. Vila-Sanjurjo, A., Schuwirth, B.S., Hau, C.W., and Cate, J.H. (2004). Structural basis for the control of translation initiation during stress. Nat. Struct. Mol. Biol., 11, 1054-1059
6. Agafonov, D.E., Kolb, V.A., and Spirin, A.S. (2001). Ribosome-associated protein that inhibits translation at the aminoacyl-tRNA binding stage. EMBO Rep., 2, 399-402
7. Sharma, M.R., Donhofer, A., Barat, C., Marquez, V., Datta, P.P., Fucini, P., Wilson, D.N., and Agrawal, R.K. (2010). 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., 285, 4006-4014
8. Kato, T., Yoshida, H., Miyata, T., Maki, Y., Wada, A., and Namba, K. (2010). Structure of the 100S ribosome in the hibernation stage revealed by electron cryomicroscopy. Structure, 18, 719-724
9. Ortiz, J.O., Brandt, F., Matias, V.R., Sennels, L., Rappsilber, J., Scheres, S.H., Eibauer, M., Hartl, F.U., and Baumeister, W. (2010). Structure of hibernating ribosomes studied by cryoelectron tomography in vitro, and in situ. J. Cell Biol., 190, 613-621
10. Puri, P., Eckhardt, T.H., Franken, L.E., Fusetti, F., Stuart, M.C., Boekema, E.J., Kuipers, O.P., Kok, J., and Poolman, B. (2014). Lactococcus lactis YfiA is necessary, and sufficient for ribosome dimerization. Mol. Microbiol., 91, 394-407
11. Maki, Y., Yoshida, H., and Wada, A. (2000). Two proteins, YfiA, and YhbH, associated with resting ribosomes in stationary phase Escherichia coli. Genes Cells, 5, 965-974
12. Wada, A., Igarashi, K., Yoshimura, S., Aimoto, S., and Ishihama, A. (1995). Ribosome modulation factor: stationary growth phase-specific inhibitor of ribosome functions from Escherichia coli. Biochem. Biophys. Res. Commun., 214, 410-417
13. Yamagishi, M., Matsushima, H., Wada, A., Sakagami, M., Fujita, N., and Ishihama, A. (1993). Regulation of the Escherichia coli rmf gene encoding the ribosome modulation factor: growth phase-and growth rate-dependent control. EMBO J., 12, 625-630
14. Yoshida, H., Ueta, M., Maki, Y., Sakai, A., and Wada, A. (2009). Activities of Escherichia coli ribosomes in IF3, and RMF change to prepare 100S ribosome formation on entering the stationary growth phase. Genes Cells, 14, 271-280
15. Aiso, T., Yoshida, H., Wada, A., and Ohki, R. (2005). Modulation of mRNA stability participates in stationary-phase-specific expression of ribosome modulation factor. J. Bacteriol., 187, 1951-1958
16. Wada, A., Yamazaki, Y., Fujita, N., and Ishihama, A. (1990). 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., 87, 2657-2661
17. El-Sharoud, W.M., and Niven, G.W. (2007). The influence of ribosome modulation factor on the survival of stationary-phase Escherichia coli during acid stress. Microbiology, 153, 247-253
18. Niven, G.W. (2004). Ribosome modulation factor protects Escherichia coli during heat stress, but this may not be dependent on ribosome dimerisation. Arch. Microbiol., 182, 60-66
19. Ueta, M., Yoshida, H., Wada, C., Baba, T., Mori, H., and Wada, A. (2005). Ribosome binding proteins YhbH, and YfiA have opposite functions during 100S formation in the stationary phase of Escherichia coli. Genes Cells, 10, 1103-1112
20. Ueta, M., Ohniwa, R.L., Yoshida, H., Maki, Y., Wada, C., and Wada, A. (2008). Role of HPF (hibernation promoting factor) in translational activity in Escherichia coli. J. Biochem., 143, 425-433
21. Yoshida, H., and Wada, A. (2014). The 100S ribosome: ribosomal hibernation induced by stress. Wiley Interdiscip. Rev. RNA, 5, 723-732
22. Ueta, M., Wada, C., Daifuku, T., Sako, Y., Bessho, Y., Kitamura, A., Ohniwa, R.L., Morikawa, K., Yoshida, H., Kato, T., et al. (2013). Conservation of two distinct types of 100S ribosome in bacteria. Genes Cells, 18, 554-574
23. Ueta, M., Wada, C. andWada, A. (2010). Formation of 100S ribosomes in Staphylococcus aureus by the hibernation promoting factor homolog SaHPF. Genes Cells, 15, 43-58
24. Kline, B.C., McKay, S.L., Tang, W.W., and Portnoy, D.A. (2015). The Listeria monocytogenes hibernation-promoting factor is required for the formation of 100S ribosomes, optimal fitness, and pathogenesis. J. Bacteriol., 197, 581-591
25. Tagami, K., Nanamiya, H., Kazo, Y., Maehashi, M., Suzuki, S., Namba, E., Hoshiya, M., Hanai, R., Tozawa, Y., Morimoto, T., et al. (2012). Expression of a small (p)ppGpp synthetase, YwaC, in the (p)ppGpp(0) mutant of Bacillus subtilis triggers YvyD-dependent dimerization of ribosome. MicrobiologyOpen, 1, 115-134
26. Davis, A.R., Gohara, D.W., and Yap, M.N.F. (2014). Sequence selectivity of macrolide-induced translational attenuation. Proc. Natl. Acad. Sci. U.S.A., 111, 15379-15384
27. McKay, S.L., and Portnoy, D.A. (2015). Ribosome hibernation facilitates tolerance of stationary-phase bacteria to aminoglycosides. Antimicrob. Agents Chemother., 59, 6992-6999
28. Fey, P.D., Endres, J.L., Yajjala, V.K., Widhelm, T.J., Boissy, R.J., Bose, J.L., and Bayles, K.W. (2013). A genetic resource for rapid, and comprehensive phenotype screening of nonessential Staphylococcus aureus genes. mBio, 4, doi: 10.1128/mBio.00537-12
29. Lee, C.Y., Buranen, S.L., and Ye, Z.H. (1991). Construction of single-copy integration vectors for Staphylococcus aureus. Gene, 103, 101-105
30. Pattee, P.A., and Neveln, D.S. (1975). Transformation analysis of three linkage groups in Staphylococcus aureus. J. Bacteriol., 124, 201-211
31. Spedding, G. (1990). Isolation, and analysis of ribosomes from prokaryotes, eukaryotes, and organelles. In: Spedding, G (ed). Ribosomes, and protein synthesis: a practical approach. Oxford University Press, NY, pp. 1-29
32. Becker, A.H., Oh, E., Weissman, J.S., Kramer, G., and Bukau, B. (2013). Selective ribosome profiling as a tool for studying the interaction of chaperones, and targeting factors with nascent polypeptide chains, and ribosomes. Nat. Protoc., 8, 2212-2239
33. Homann, O.R., and Johnson, A.D. (2010). MochiView: versatile software for genome browsing, and DNA motif analysis. BMC Biol., 8, 49
34. Ingolia, N.T., Ghaemmaghami, S., Newman, J.R., and Weissman, J.S. (2009). Genome-wide analysis in vivo of translation with nucleotide resolution using ribosome profiling. Science, 324, 218-223
35. LaCava, J., Molloy, K.R., Taylor, M.S., Domanski, M., Chait, B.T., and Rout, M.P. (2015). Affinity proteomics to study endogenous protein complexes: pointers, pitfalls, preferences, and perspectives. Biotechniques, 58, 103-119
36. Oh, E., Becker, A.H., Sandikci, A., Huber, D., Chaba, R., Gloge, F., Nichols, R.J., Typas, A., Gross, C.A., Kramer, G., et al. (2011). Selective ribosome profiling reveals the cotranslational chaperone action of trigger factor in vivo. Cell, 147, 1295-1308
37. Zundel, M.A., Basturea, G.N., and Deutscher, M.P. (2009). Initiation of ribosome degradation during starvation in Escherichia coli. RNA, 15, 977-983
38. Gerashchenko, M.V., and Gladyshev, V.N. (2014). Translation inhibitors cause abnormalities in ribosome profiling experiments. Nucleic Acids Res., 42, e134
39. Wilson, D.N. (2014). Ribosome-targeting antibiotics, and mechanisms of bacterial resistance. Nat. Rev. Microbiol., 12, 35-48
40. McCarthy, B.J. (1960). Variations in bacterial ribosomes. Biochim. Biophys. Acta, 39, 563-564
41. Tissieres, A., and Watson, J.D. (1958). Ribonucleoprotein particles from Escherichia coli. Nature, 182, 778-780
42. Ben-Shem, A., Garreau De Loubresse, N., Melnikov, S., Jenner, L., Yusupova, G., and Yusupov, M. (2011). The structure of the eukaryotic ribosome at 3.0 A resolution. Science, 334, 1524-1529
43. Van Dyke, N., Baby, J., and Van Dyke, M.W. (2006). Stm1p, a ribosome-associated protein, is important for protein synthesis in Saccharomyces cerevisiae under nutritional stress conditions. J. Mol. Biol., 358, 1023-1031
44. Bonnin, R.A., and Bouloc, P. (2015). RNA degradation in Staphylococcus aureus: diversity of ribonucleases, and their impact. Int. J. Genomics, 2015, 395753
45. Jones, S.E., Leong, V., Ortega, J., and Elliot, M.A. (2014). Development, antibiotic production, and ribosome assembly in Streptomyces venezuelae are impacted by RNase J, and RNase III deletion. J. Bacteriol., 196, 4253-4267
46. Shcherbakova, K., Nakayama, H., and Shimamoto, N. (2015). Role of 100S ribosomes in bacterial decay period. Genes Cells, 20, 789-801
47. Wada, A., Mikkola, R., Kurland, C.G., and Ishihama, A. (2000). Growth phase-coupled changes of the ribosome profile in natural isolates, and laboratory strains of Escherichia coli. J. Bacteriol., 182, 2893-2899
48. Brandt, F., Etchells, S.A., Ortiz, J.O., Elcock, A.H., Hartl, F.U., and Baumeister, W. (2009). The native 3D organization of bacterial polysomes. Cell, 136, 261-271
49. Han, Y., Gao, X., Liu, B., Wan, J., Zhang, X., and Qian, S.B. (2014). Ribosome profiling reveals sequence-independent post-initiation pausing as a signature of translation. Cell Res., 24, 842-851
50. Kudla, G., Murray, A.W., Tollervey, D., and Plotkin, J.B. (2009). Coding-sequence determinants of gene expression in Escherichia coli. Science, 324, 255-258
51. Tuller, T., Carmi, A., Vestsigian, K., Navon, S., Dorfan, Y., Zaborske, J., Pan, T., Dahan, O., Furman, I., and Pilpel, Y. (2010). An evolutionarily conserved mechanism for controlling the efficiency of protein translation. Cell, 141, 344-354
52. Cho, J., Rogers, J., Kearns, M., Leslie, M., Hartson, S.D., and Wilson, K.S. (2015). Escherichia coli persister cells suppress translation by selectively disassembling, and degrading their ribosomes. Mol. Microbiol., 95, 352-364
53. Ehrenberg, M., Bremer, H., and Dennis, P.P. (2013). Medium-dependent control of the bacterial growth rate. Biochimie, 95, 643-658
54. Scott, M., Gunderson, C.W., Mateescu, E.M., Zhang, Z., and Hwa, T. (2010). Interdependence of cell growth, and gene expression: origins, and consequences. Science, 330, 1099-1102
55. Proctor, R.A., Kriegeskorte, A., Kahl, B.C., Becker, K., Loffler, B., and Peters, G. (2014). Staphylococcus aureus Small Colony Variants (SCVs): a road map for the metabolic pathways involved in persistent infections. Front Cell Infect Microbiol, 4, 99