Abstract
Ribosome is primarily regarded as the committing organelle for the translation process. Besides the expansion of its function from a translational machine for protein synthesis to a regulatory platform for protein quality control, the activity regulation and recycling of ribosome have been deepened significantly. Recent advances have confirmed a novel mechanism in the regulation of ribosome activity when a cell encounters adverse conditions. Due to the binding of certain protein factors onto a ribosome, the structural and functional change of the ribosome inside the cell will take place, thereby leading to the formation of inactive ribosomes (70S monomer or 100S dimer), or ribosome hibernation. By ribosome hibernation, the overall protein synthesis rate of a cell could be slowed down. The resistance to adverse conditions or chemicals of the host cell will be enhanced. In this paper, we discussed the phenomenon, molecular mechanism, and physiological effect of ribosome hibernation when cells are under stresses. And then, we discussed the resuscitation of a hibernating ribosome and the role of ribosome hibernation in the treatment of antimicrobial infection.
Keywords: Ribosome hibernation, stress response, ribosome dimer, resuscitation of hibernating ribosome, bacterial pathogenicity, translation process.
Graphical Abstract
[1]
Capel, M.S.; Engelman, D.M.; Freeborn, B.R.; Kjeldgaard, M.; Langer, J.A.; Ramakrishnan, V.; Schindler, D.G.; Schneider, D.K.; Schoenborn, B.P.; Sillers, I.Y. A complete mapping of the proteins in the small ribosomal subunit of Escherichia coli. Science, 1987, 238(4832), 1403-1406.[http://dx.doi.org/10.1126/science.3317832] [PMID: 3317832]
[2]
Ban, N.; Nissen, P.; Hansen, J.; Moore, P.B.; Steitz, T.A. The complete atomic structure of the large ribosomal subunit at 2.4 A resolution. Science, 2000, 289(5481), 905-920.[http://dx.doi.org/10.1126/science.289.5481.905] [PMID: 10937989]
[3]
Bashan, A.; Agmon, I.; Zarivach, R.; Schluenzen, F.; Harms, J.; Berisio, R.; Bartels, H.; Franceschi, F.; Auerbach, T.; Hansen, H.A.; Kossoy, E.; Kessler, M.; Yonath, A. Structural basis of the ribosomal machinery for peptide bond formation, translocation, and nascent chain progression. Mol. Cell, 2003, 11(1), 91-102.[http://dx.doi.org/10.1016/S1097-2765(03)00009-1] [PMID: 12535524]
[4]
Genuth, N.R.; Barna, M. The discovery of ribosome heterogeneity and its implications for gene regulation and organismal life. Mol. Cell, 2018, 71(3), 364-374.[http://dx.doi.org/10.1016/j.molcel.2018.07.018] [PMID: 30075139]
[5]
Wada, A. Growth phase coupled modulation of Escherichia coli ribosomes. Genes Cells, 1998, 3(4), 203-208.[http://dx.doi.org/10.1046/j.1365-2443.1998.00187.x] [PMID: 9663655]
[6]
Wada, A.; Mikkola, R.; Kurland, C.G.; Ishihama, A. Growth phase-coupled changes of the ribosome profile in natural isolates and laboratory strains of Escherichia coli. J. Bacteriol., 2000, 182(10), 2893-2899.[http://dx.doi.org/10.1128/JB.182.10.2893-2899.2000] [PMID: 10781560]
[7]
de la Cruz, J.; Gómez-Herreros, F.; Rodríguez-Galán, O.; Begley, V.; de la Cruz Muñoz-Centeno, M.; Chávez, S. Feedback regulation of ribosome assembly. Curr. Genet., 2018, 64(2), 393-404.[http://dx.doi.org/10.1007/s00294-017-0764-x] [PMID: 29022131]
[8]
Slavov, N.; Semrau, S.; Airoldi, E.; Budnik, B.; van Oudenaarden, A. Differential stoichiometry among core ribosomal proteins. Cell Rep., 2015, 13(5), 865-873.[http://dx.doi.org/10.1016/j.celrep.2015.09.056] [PMID: 26565899]
[9]
Kondrashov, N.; Pusic, A.; Stumpf, C.R.; Shimizu, K.; Hsieh, A.C.; Ishijima, J.; Shiroishi, T.; Barna, M. Ribosome-mediated specificity in Hox mRNA translation and vertebrate tissue patterning. Cell, 2011, 145(3), 383-397.[http://dx.doi.org/10.1016/j.cell.2011.03.028] [PMID: 21529712]
[10]
Degenhardt, R.F.; Bonham-Smith, P.C. Arabidopsis ribosomal proteins RPL23aA and RPL23aB are differentially targeted to the nucleolus and are disparately required for normal development. Plant Physiol., 2008, 147(1), 128-142.[http://dx.doi.org/10.1104/pp.107.111799] [PMID: 18322146]
[11]
Kim, K.Y.; Park, S.W.; Chung, Y.S.; Chung, C.H.; Kim, J.I.; Lee, J.H. Molecular cloning of low-temperature-inducible ribosomal proteins from soybean. J. Exp. Bot., 2004, 55(399), 1153-1155.[http://dx.doi.org/10.1093/jxb/erh125] [PMID: 15020631]
[12]
Ferretti, M.B.; Karbstein, K. Does functional specialization of ribosomes really exist? RNA, 2019, 25(5), 521-538.[http://dx.doi.org/10.1261/rna.069823.118] [PMID: 30733326]
[13]
Culviner, P.H.; Laub, M.T. Global analysis of the E. coli toxin MazF reveals widespread cleavage of mRNA and the inhibition of RNA maturation and ribosome biogenesis. Mol. Cell, 2018, 70(5), 868-880.
[14]
Mets, T.; Lippus, M.; Schryer, D.; Liiv, A.; Kasari, V.; Paier, A.; Maiväli, Ü.; Remme, J.; Tenson, T.; Kaldalu, N. Toxins MazF and MqsR cleave Escherichia coli rRNA precursors at multiple sites. RNA Biol., 2017, 14(1), 124-135.[http://dx.doi.org/10.1080/15476286.2016.1259784] [PMID: 27858580]
[15]
Wade, J.T.; Laub, M.T. Concerns about “Stress-induced MazF-mediated proteins in Escherichia coli”. MBio, 2019, 10(3), e00825-e19.[http://dx.doi.org/10.1128/mBio.00825-19] [PMID: 31164463]
[16]
Dow, A.; Prisic, S. Alternative ribosomal proteins are required for growth and morphogenesis of Mycobacterium smegmatis under zinc limiting conditions. PLoS One, 2018, 13(4) e0196300.[http://dx.doi.org/10.1371/journal.pone.0196300] [PMID: 29684089]
[17]
Simsek, D.; Barna, M. An emerging role for the ribosome as a nexus for post-translational modifications. Curr. Opin. Cell Biol., 2017, 45, 92-101.[http://dx.doi.org/10.1016/j.ceb.2017.02.010] [PMID: 28445788]
[18]
Nesterchuk, M.V.; Sergiev, P.V.; Dontsova, O.A. Posttranslational modifications of ribosomal proteins in Escherichia coli. Acta Naturae, 2011, 3(2), 22-33.[http://dx.doi.org/10.32607/20758251-2011-3-2-22-33] [PMID: 22649682]
[19]
Xue, S.; Barna, M. Specialized ribosomes: A new frontier in gene regulation and organismal biology. Nat. Rev. Mol. Cell Biol., 2012, 13(6), 355-369.[http://dx.doi.org/10.1038/nrm3359] [PMID: 22617470]
[20]
Yoshida, H.; Wada, A. The 100S ribosome: Ribosomal hibernation induced by stress. Wiley Interdiscip. Rev. RNA, 2014, 5(5), 723-732.[http://dx.doi.org/10.1002/wrna.1242] [PMID: 24944100]
[21]
Matzov, D.; Aibara, S.; Basu, A.; Zimmerman, E.; Bashan, A.; Yap, M.F.; Amunts, A.; Yonath, A.E. The cryo-EM structure of hibernating 100S ribosome dimer from pathogenic Staphylococcus aureus. Nat. Commun., 2017, 8(1), 723.[http://dx.doi.org/10.1038/s41467-017-00753-8] [PMID: 28959035]
[22]
Basu, A.; Yap, M.N. Disassembly of the Staphylococcus aureus hibernating 100S ribosome by an evolutionarily conserved GTPase. Proc. Natl. Acad. Sci. USA, 2017, 114(39), E8165-E8173.[http://dx.doi.org/10.1073/pnas.1709588114] [PMID: 28894000]
[23]
Prossliner, T.; Skovbo Winther, K.; Sørensen, M.A.; Gerdes, K. Ribosome hibernation. Annu. Rev. Genet., 2018, 52, 321-348.[http://dx.doi.org/10.1146/annurev-genet-120215-035130] [PMID: 30476446]
[24]
Akanuma, G.; Kazo, Y.; Tagami, K.; Hiraoka, H.; Yano, K.; Suzuki, S.; Hanai, R.; Nanamiya, H.; Kato-Yamada, Y.; Kawamura, F. Ribosome dimerization is essential for the efficient regrowth of Bacillus subtilis. Microbiology, 2016, 162(3), 448-458.[http://dx.doi.org/10.1099/mic.0.000234] [PMID: 26743942]
[25]
Jermy, A. Bacterial physiology. Stressed bacteria aren’t lost without a leader. Nat. Rev. Microbiol., 2011, 9(12), 834-835.[http://dx.doi.org/10.1038/nrmicro2704] [PMID: 22064559]
[26]
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(1), 147-157.[http://dx.doi.org/10.1016/j.cell.2011.07.047] [PMID: 21944167]
[27]
Buskirk, A.R. Toxins that trash translation. Mol. Cell, 2018, 70(5), 759-760.[http://dx.doi.org/10.1016/j.molcel.2018.05.027] [PMID: 29883601]
[28]
Nigam, A.; Ziv, T.; Oron-Gottesman, A.; Engelberg-Kulka, H. Stress-induced MazF-mediated proteins in Escherichia coli. MBio, 2019, 10(2), e00340-e19.[http://dx.doi.org/10.1128/mBio.00340-19] [PMID: 30914510]
[29]
Nigam, A.; Ziv, T.; Oron-Gottesman, A.; Engelberg-Kulka, H. Reply to Wade and Laub, ‘Concerns about “Stress-induced MazF-mediated proteins in”’. MBio, 2019, 10(3), e01063-e19.[http://dx.doi.org/10.1128/mBio.01063-19]
[30]
Luidalepp, H.; Berger, S.; Joss, O.; Tenson, T.; Polacek, N. Ribosome shut-down by 16S rRNA fragmentation in stationary-phase Escherichia coli. J. Mol. Biol., 2016, 428(10 Pt B), 2237-2247.[http://dx.doi.org/10.1016/j.jmb.2016.01.033] [PMID: 27067112]
[31]
Oron-Gottesman, A.; Sauert, M.; Moll, I.; Engelberg-Kulka, H. A stress-induced bias in the reading of the genetic code in Escherichia coli. MBio, 2016, 7(6), e01855-e16.[http://dx.doi.org/10.1128/mBio.01855-16] [PMID: 27935840]
[32]
Nikolic, N.; Didara, Z.; Moll, I. MazF activation promotes translational heterogeneity of the grcA mRNA in Escherichia coli populations. Nucleic Acids Res., 2017, 46(6), 2918-2931.[http://dx.doi.org/10.7717/peerj.3830]
[33]
Nikolic, N.; Bergmiller, T.; Vandervelde, A.; Albanese, T.G.; Gelens, L.; Moll, I. Autoregulation of mazEF expression underlies growth heterogeneity in bacterial populations. Nucleic Acids Res., 2018, 46(6), 2918-2931.[http://dx.doi.org/10.1093/nar/gky079] [PMID: 29432616]
[34]
Mets, T.; Kasvandik, S.; Saarma, M.; Maiväli, Ü.; Tenson, T.; Kaldalu, N. Fragmentation of Escherichia coli mRNA by MazF and MqsR. Biochimie, 2019, 156, 79-91.[http://dx.doi.org/10.1016/j.biochi.2018.10.004] [PMID: 30315853]
[35]
Walsh, I.M.; Bowman, M.A.; Soto Santarriaga, I.F.; Rodriguez, A.; Clark, P.L. Synonymous codon substitutions perturb cotranslational protein folding in vivo and impair cell fitness. Proc. Natl. Acad. Sci. USA, 2020, 117(7), 3528-3534.[http://dx.doi.org/10.1073/pnas.1907126117] [PMID: 32015130]
[36]
Agafonov, D.E.; Kolb, V.A.; Spirin, A.S. Ribosome-associated protein that inhibits translation at the aminoacyl-tRNA binding stage. EMBO Rep., 2001, 2(5), 399-402.[http://dx.doi.org/10.1093/embo-reports/kve091] [PMID: 11375931]
[37]
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. USA, 1990, 87(7), 2657-2661.[http://dx.doi.org/10.1073/pnas.87.7.2657] [PMID: 2181444]
[38]
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(6), 1951-1958.[http://dx.doi.org/10.1128/JB.187.6.1951-1958.2005] [PMID: 15743942]
[39]
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(2), 410-417.[http://dx.doi.org/10.1006/bbrc.1995.2302] [PMID: 7677746]
[40]
Tissieres, A.; Watson, J.D. Ribonucleoprotein particles from Escherichia coli. Nature, 1958, 182(4638), 778-780.[http://dx.doi.org/10.1038/182778b0] [PMID: 13590104]
[41]
Izutsu, K.; Wada, A.; Wada, C. Expression of ribosome modulation factor (RMF) in Escherichia coli requires ppGpp. Genes Cells, 2001, 6(8), 665-676.[http://dx.doi.org/10.1046/j.1365-2443.2001.00457.x] [PMID: 11532026]
[42]
Moen, B.; Janbu, A.O.; Langsrud, S.; Langsrud, O.; Hobman, J.L.; 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(6), 714-728.[http://dx.doi.org/10.1139/W09-016] [PMID: 19767843]
[43]
el-Sharoud, W.M.; Niven, G.W. The activity of ribosome modulation factor during growth of Escherichia coli under acidic conditions. Arch. Microbiol., 2005, 184(1), 18-24.[http://dx.doi.org/10.1007/s00203-005-0025-0] [PMID: 16088400]
[44]
Garay-Arroyo, A.; Colmenero-Flores, J.M.; Garciarrubio, A.; Covarrubias, A.A. Highly hydrophilic proteins in prokaryotes and eukaryotes are common during conditions of water deficit. J. Biol. Chem., 2000, 275(8), 5668-5674.[http://dx.doi.org/10.1074/jbc.275.8.5668] [PMID: 10681550]
[45]
Raivio, T.L.; Leblanc, S.K.; Price, N.L. The Escherichia coli Cpx envelope stress response regulates genes of diverse function that impact antibiotic resistance and membrane integrity. J. Bacteriol., 2013, 195(12), 2755-2767.[http://dx.doi.org/10.1128/JB.00105-13] [PMID: 23564175]
[46]
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(2), 625-630.[http://dx.doi.org/10.1002/j.1460-2075.1993.tb05695.x] [PMID: 8440252]
[47]
Krokowski, D.; Gaccioli, F.; Majumder, M.; Mullins, M.R.; Yuan, C.L.; Papadopoulou, B.; Merrick, W.C.; Komar, A.A.; Taylor, D.; Hatzoglou, M. Characterization of hibernating ribosomes in mammalian cells. Cell Cycle, 2011, 10(16), 2691-2702.[http://dx.doi.org/10.4161/cc.10.16.16844] [PMID: 21768774]
[48]
Gohara, D.W.; Yap, M.F. Survival of the drowsiest: The hibernating 100S ribosome in bacterial stress management. Curr. Genet., 2018, 64(4), 753-760.[http://dx.doi.org/10.1007/s00294-017-0796-2] [PMID: 29243175]
[49]
McKay, S.L.; Portnoy, D.A. Ribosome hibernation facilitates tolerance of stationary-phase bacteria to aminoglycosides. Antimicrob. Agents Chemother., 2015, 59(11), 6992-6999.[http://dx.doi.org/10.1128/AAC.01532-15] [PMID: 26324267]
[50]
Ortiz, J.O.; Brandt, F.; Matias, V.R.; Sennels, L.; Rappsilber, J.; Scheres, S.H.; Eibauer, M.; Hartl, F.U.; Baumeister, W. Structure of hibernating ribosomes studied by cryoelectron tomography in vitro and in situ. J. Cell Biol., 2010, 190(4), 613-621.[http://dx.doi.org/10.1083/jcb.201005007] [PMID: 20733057]
[51]
Shcherbakova, K.; Nakayama, H.; Shimamoto, N. Role of 100S ribosomes in bacterial decay period. Genes Cells, 2015, 20(10), 789-801.[http://dx.doi.org/10.1111/gtc.12273] [PMID: 26290418]
[52]
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(12), 1103-1112.[http://dx.doi.org/10.1111/j.1365-2443.2005.00903.x] [PMID: 16324148]
[53]
Duss, O.; Stepanyuk, G.A.; Puglisi, J.D.; Williamson, J.R. Transient protein-RNA interactions guide nascent ribosomal RNA folding. Cell, 2019, 179(6), 1357-1369.e1316.
[54]
Agafonov, D.E.; Kolb, V.A.; Nazimov, I.V.; Spirin, A.S. A protein residing at the subunit interface of the bacterial ribosome. Proc. Natl. Acad. Sci. USA, 1999, 96(22), 12345-12349.[http://dx.doi.org/10.1073/pnas.96.22.12345] [PMID: 10535924]
[55]
Basu, A.; Yap, M-N. Ribosome hibernation factor promotes Staphylococcal survival and differentially represses translation. Nucleic Acids Res., 2016, 44(10), 4881-4893.[http://dx.doi.org/10.1093/nar/gkw180] [PMID: 27001516]
[56]
Beckert, B.; Abdelshahid, M.; Schäfer, H.; Steinchen, W.; Arenz, S.; Berninghausen, O.; Beckmann, R.; Bange, G.; Turgay, K.; Wilson, D.N. Structure of the Bacillus subtilis hibernating 100S ribosome reveals the basis for 70S dimerization. EMBO J., 2017, 36(14), 2061-2072.[http://dx.doi.org/10.15252/embj.201696189] [PMID: 28468753]
[57]
Puri, P.; Eckhardt, T.H.; Franken, L.E.; Fusetti, F.; Stuart, M.C.; Boekema, E.J.; Kuipers, O.P.; Kok, J.; Poolman, B. Lactococcus lactis YfiA is necessary and sufficient for ribosome dimerization. Mol. Microbiol., 2014, 91(2), 394-407.[http://dx.doi.org/10.1111/mmi.12468] [PMID: 24279750]
[58]
Polikanov, Y.S.; Blaha, G.M.; Steitz, T.A. How hibernation factors RMF, HPF, and YfiA turn off protein synthesis. Science, 2012, 336(6083), 915-918.[http://dx.doi.org/10.1126/science.1218538] [PMID: 22605777]
[59]
Vila-Sanjurjo, A.; Schuwirth, B.S.; Hau, C.W.; Cate, J.H. Structural basis for the control of translation initiation during stress. Nat. Struct. Mol. Biol., 2004, 11(11), 1054-1059.[http://dx.doi.org/10.1038/nsmb850] [PMID: 15502846]
[60]
Beckert, B.; Turk, M.; Czech, A.; Berninghausen, O.; Beckmann, R.; Ignatova, Z.; Plitzko, J.M.; Wilson, D.N. Structure of a hibernating 100S ribosome reveals an inactive conformation of the ribosomal protein S1. Nat. Microbiol., 2018, 3(10), 1115-1121.[http://dx.doi.org/10.1038/s41564-018-0237-0] [PMID: 30177741]
[61]
Khusainov, I.; Vicens, Q.; Ayupov, R.; Usachev, K.; Myasnikov, A.; Simonetti, A.; Validov, S.; Kieffer, B.; Yusupova, G.; Yusupov, M.; Hashem, Y. Structures and dynamics of hibernating ribosomes from Staphylococcus aureus mediated by intermolecular interactions of HPF. EMBO J., 2017, 36(14), 2073-2087.[http://dx.doi.org/10.15252/embj.201696105] [PMID: 28645916]
[62]
Flygaard, R.K.; Boegholm, N.; Yusupov, M.; Jenner, L.B. Cryo-EM structure of the hibernating Thermus thermophilus 100S ribosome reveals a protein-mediated dimerization mechanism. Nat. Commun., 2018, 9(1), 4179.[http://dx.doi.org/10.1038/s41467-018-06724-x] [PMID: 30301898]
[63]
Mishra, S.; Ahmed, T.; Tyagi, A.; Shi, J.; Bhushan, S. Structures of Mycobacterium smegmatis 70S ribosomes in complex with HPF, tmRNA, and P-tRNA. Sci. Rep., 2018, 8(1), 13587.[http://dx.doi.org/10.1038/s41598-018-31850-3] [PMID: 30206241]
[64]
Franken, L.E.; Oostergetel, G.T.; Pijning, T.; Puri, P.; Arkhipova, V.; Boekema, E.J.; Poolman, B.; Guskov, A. A general mechanism of ribosome dimerization revealed by single-particle cryo-electron microscopy. Nat. Commun., 2017, 8(1), 722.[http://dx.doi.org/10.1038/s41467-017-00718-x] [PMID: 28959045]
[65]
Usachev, K.S.; Fatkhullin, B.F.; Klochkova, E.A.; Miftakhov, A.K.; Golubev, A.A.; Bikmullin, A.G.; Nurullina, L.I.; Garaeva, N.S.; Islamov, D.R.; Gabdulkhakov, A.G.; Lekontseva, N.V.; Tishchenko, S.V.; Balobanov, V.A.; Khusainov, I.S.; Yusupov, M.M.; Validov, S.Z. Dimerization of long hibernation promoting factor from Staphylococcus aureus: Structural analysis and biochemical characterization. J. Struct. Biol., 2020, 209(1), 107408-107408.[http://dx.doi.org/10.1016/j.jsb.2019.107408] [PMID: 31669310]
[66]
Usachev, K.S.; Validov, S.Z.; Khusainov, I.S.; Varfolomeev, A.A.; Klochkov, V.V.; Aganov, A.V.; Yusupov, M.M. Solution structure of the N-terminal domain of the Staphylococcus aureus hibernation promoting factor. J. Biomol. NMR, 2019, 73(5), 223-227.[http://dx.doi.org/10.1007/s10858-019-00254-4] [PMID: 31165320]
[67]
Kline, B.C.; McKay, S.L.; Tang, W.W.; Portnoy, D.A. The Listeria monocytogenes hibernation-promoting factor is required for the formation of 100S ribosomes, optimal fitness, and pathogenesis. J. Bacteriol., 2015, 197(3), 581-591.[http://dx.doi.org/10.1128/JB.02223-14] [PMID: 25422304]
[68]
Ganini, D.; Leinisch, F.; Kumar, A.; Jiang, J.; Tokar, E.J.; Malone, C.C.; Petrovich, R.M.; Mason, R.P. Fluorescent proteins such as eGFP lead to catalytic oxidative stress in cells. Redox Biol., 2017, 12, 462-468.[http://dx.doi.org/10.1016/j.redox.2017.03.002] [PMID: 28334681]
[69]
Kalyanaraman, B.; Zielonka, J. Green fluorescent proteins induce oxidative stress in cells: A worrisome new wrinkle in the application of the GFP reporter system to biological systems? Redox Biol., 2017, 12, 755-757.[http://dx.doi.org/10.1016/j.redox.2017.03.019] [PMID: 28415040]
[70]
El-Hajj, Z.W.; Newman, E.B. An Escherichia coli mutant that makes exceptionally long cells. J. Bacteriol., 2015, 197(8), 1507-1514.[http://dx.doi.org/10.1128/JB.00046-15] [PMID: 25691528]
[71]
Davis, A.R.; Gohara, D.W.; Yap, M.N. Sequence selectivity of macrolide-induced translational attenuation. Proc. Natl. Acad. Sci. USA, 2014, 111(43), 15379-15384.[http://dx.doi.org/10.1073/pnas.1410356111] [PMID: 25313041]
[72]
Ueta, M.; Wada, C.; Daifuku, T.; Sako, Y.; Bessho, Y.; Kitamura, A.; Ohniwa, R.L.; Morikawa, K.; Yoshida, H.; Kato, T.; Miyata, T.; Namba, K.; Wada, A. Conservation of two distinct types of 100S ribosome in bacteria. Genes Cells, 2013, 18(7), 554-574.[http://dx.doi.org/10.1111/gtc.12057] [PMID: 23663662]
[73]
Williamson, K.S.; Richards, L.A.; Perez-Osorio, A.C.; Pitts, B.; McInnerney, K.; Stewart, P.S.; Franklin, M.J. Heterogeneity in Pseudomonas aeruginosa biofilms includes expression of ribosome hibernation factors in the antibiotic-tolerant subpopulation and hypoxia-induced stress response in the metabolically active population. J. Bacteriol., 2012, 194(8), 2062-2073.[http://dx.doi.org/10.1128/JB.00022-12] [PMID: 22343293]
[74]
Feaga, H.A.; Kopylov, M.; Kim, J.K.; Jovanovic, M.; Dworkin, J. Ribosome dimerization protects the small subunit. 2020 JB.00009-00020.
[75]
Song, S.; Wood, T.K. ppGpp ribosome dimerization model for bacterial persister formation and resuscitation. Biochem. Biophys. Res. Commun., 2020, 523(2), 281-286.[http://dx.doi.org/10.1016/j.bbrc.2020.01.102] [PMID: 32007277]
[76]
Ueta, M.; Wada, C.; Bessho, Y.; Maeda, M.; Wada, A. Ribosomal protein L31 in Escherichia coli contributes to ribosome subunit association and translation, whereas short L31 cleaved by protease 7 reduces both activities. Genes Cells, 2017, 22(5), 452-471.[http://dx.doi.org/10.1111/gtc.12488] [PMID: 28397381]
[77]
Zhang, Y.; Mandava, C.S.; Cao, W.; Li, X.; Zhang, D.; Li, N.; Zhang, Y.; Zhang, X.; Qin, Y.; Mi, K.; Lei, J.; Sanyal, S.; Gao, N. HflX is a ribosome-splitting factor rescuing stalled ribosomes under stress conditions. Nat. Struct. Mol. Biol., 2015, 22(11), 906-913.[http://dx.doi.org/10.1038/nsmb.3103] [PMID: 26458047]
[78]
Gaca, A.O.; Colomer-Winter, C.; Lemos, J.A. Many means to a common end: the intricacies of (p)ppGpp metabolism and its control of bacterial homeostasis. J. Bacteriol., 2015, 197(7), 1146-1156.[http://dx.doi.org/10.1128/JB.02577-14] [PMID: 25605304]
[79]
Yamasaki, R.; Song, S.; Benedik, M.J.; Wood, T.K. Persister cells resuscitate using
membrane sensors that activate chemotaxis, lower cAMP levels, and revive ribosomes.
iScience, 2020, 23(1), 100792.
[80]
Fisher, R.A.; Gollan, B.; Helaine, S. Persistent bacterial infections and persister cells. Nat. Rev. Microbiol., 2017, 15(8), 453-464.[http://dx.doi.org/10.1038/nrmicro.2017.42] [PMID: 28529326]
[81]
Song, S.; Wood, T.K. Persister cells resuscitate via ribosome modification by 23S rRNA pseudouridine synthase RluD. Environ. Microbiol., 2020, 22(3), 850-857.[http://dx.doi.org/10.1111/1462-2920.14828] [PMID: 31608580]
[82]
Akiyama, T.; Williamson, K.S.; Schaefer, R.; Pratt, S.; Chang, C.B.; Franklin, M.J. Resuscitation of Pseudomonas aeruginosa from dormancy requires hibernation promoting factor (PA4463) for ribosome preservation. Proc. Natl. Acad. Sci. USA, 2017, 114(12), 3204-3209.[http://dx.doi.org/10.1073/pnas.1700695114] [PMID: 28270601]
[83]
Li, Y.; Sharma, M.R.; Koripella, R.K.; Yang, Y.; Kaushal, P.S.; Lin, Q.; Wade, J.T.; Gray, T.A.; Derbyshire, K.M.; Agrawal, R.K.; Ojha, A.K. Zinc depletion induces ribosome hibernation in mycobacteria. Proc. Natl. Acad. Sci. USA, 2018, 115(32), 8191-8196.[http://dx.doi.org/10.1073/pnas.1804555115] [PMID: 30038002]
[84]
Tobiasson, V.; Dow, A.; Prisic, S.; Amunts, A. Zinc depletion does not necessarily induce ribosome hibernation in mycobacteria. Proc. Natl. Acad. Sci. USA, 2019, 116(7), 2395-2397.[http://dx.doi.org/10.1073/pnas.1817490116] [PMID: 30683730]
[85]
Li, Y.; Sharma, M.R.; Koripella, R.K.; Wade, J.T.; Gray, T.A.; Derbyshire, K.M.; Agrawal, R.K.; Ojha, A.K. Reply to Tobiasson et al.: Zinc depletion is a specific signal for induction of ribosome hibernation in mycobacteria. Proc. Natl. Acad. Sci. USA, 2019, 116(7), 2398-2399.[http://dx.doi.org/10.1073/pnas.1821103116] [PMID: 30683729]
Related Journals
Current Protein & Peptide Science
Related Books
Frontiers in Protein and Peptide Sciences
Article Metrics
35