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Volume 167, Issue 2

Ribosome hibernation: a new molecular framework for targeting nonreplicating persisters of mycobacteria Free

Abstract

Treatment of tuberculosis requires a multi-drug regimen administered for at least 6 months. The long-term chemotherapy is attributed in part to a minor subpopulation of nonreplicating cells that exhibit phenotypic tolerance to antibiotics. The origins of these cells in infected hosts remain unclear. Here we discuss some recent evidence supporting the hypothesis that hibernation of ribosomes in induced by zinc starvation, could be one of the primary mechanisms driving the development of nonreplicating persisters in hosts. We further analyse inconsistencies in previously reported studies to clarify the molecular principles underlying mycobacterial ribosome hibernation.

  • Received:
  • Accepted:
  • Published Online:
Keyword(s): cryo-EM structure analysis , drug tolerance , Mycobacterium tuberculosis , nonreplicating persisters , ribosome hibernation and zinc starvation
Funding
This study was supported by the:
  • National Institute of General Medical Sciences (Award GM061576)
    • Principle Award Recipient: RajendraK Agrawal
  • National Institute of Allergy and Infectious Diseases (Award AI144474)
    • Principle Award Recipient: AnilK Ojha
  • National Institute of Allergy and Infectious Diseases (Award AI132422)
    • Principle Award Recipient: AnilK Ojha
© 2021 The Authors
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2021-02-08
2024-04-20
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References

  1. Ignatius EH, Dooley KE. New drugs for the treatment of tuberculosis. Clin Chest Med 2019; 40:811–827 [View Article]
     [Google Scholar]
  2. Furin J, Cox H, Pai M. Tuberculosis. The Lancet 2019; 393:1642–1656 [View Article]
     [Google Scholar]
  3. WHO Rapid Communication: key changes to the treatment of multidrug- and rifampicin-resistant tuberculosis (MDR/RR-TB). http://wwwwhoint/tb/publications/2018/WHO_RapidCommunicationMDRTBpdf ; 2018
  4. Adepoju P. Tuberculosis and HIV responses threatened by COVID-19. The Lancet HIV 2020; 7:e319–e320 [View Article]
     [Google Scholar]
  5. Amimo F, Lambert B, Magit A. What does the COVID-19 pandemic mean for HIV, tuberculosis, and malaria control?. Trop Med Health 2020; 48:32 [View Article]
     [Google Scholar]
  6. Gold B, Nathan C. Targeting phenotypically tolerant Mycobacterium tuberculosis . Microbiol Spectr 2017; 5: [View Article]
     [Google Scholar]
  7. McCune RM, Feldmann FM, Lambert HP, McDermott W. Microbial persistence. I. The capacity of tubercle bacilli to survive sterilization in mouse tissues. J Exp Med 1966; 123:445–468
     [Google Scholar]
  8. Wallis RS, Patil S, Cheon S-H, Edmonds K, Phillips M et al. Drug tolerance in Mycobacterium tuberculosis . Antimicrob Agents Chemother 1999; 43:2600–2606 [View Article]
     [Google Scholar]
  9. Jindani A, Aber VR, Edwards EA, Mitchison DA. The early bactericidal activity of drugs in patients with pulmonary tuberculosis. Am Rev Respir Dis 1980; 121:939–949
     [Google Scholar]
  10. Manabe YC, Bishai WR. Latent Mycobacterium tuberculosis–persistence, patience and winning by waiting. Nat Med 2000; 6:1327–1329 [View Article]
     [Google Scholar]
  11. Gomez JE, McKinney JD. M. tuberculosis persistence, latency, and drug tolerance. Tuberculosis 2004; 84:29–44 [View Article]
     [Google Scholar]
  12. Ehrt S, Schnappinger D, Rhee KY. Metabolic principles of persistence and pathogenicity in Mycobacterium tuberculosis . Nat Rev Microbiol 2018; 16:496–507 [View Article]
     [Google Scholar]
  13. Hobby GL, Lenert TF. The in vitro action of antituberculous agents against multiplying and non-multiplying microbial cells. Am Rev Tuberc 1957; 76:1031–1048
     [Google Scholar]
  14. Sever JL, Youmans GP. The relation of oxygen tension to virulence of tubercle bacilli and to acquired resistance in tuberculosis. J Infect Dis 1957; 101:193–202 [View Article]
     [Google Scholar]
  15. Sever JL, Youmans GP. Enumeration of viable tubercle bacilli from the organs of nonimmunized and immunized mice. Am Rev Tuberc 1957; 76:616–635
     [Google Scholar]
  16. Via LE, Lin PL, Ray SM, Carrillo J, Allen SS et al. Tuberculous granulomas are hypoxic in guinea pigs, rabbits, and nonhuman primates. Infect Immun 2008; 76:2333–2340 [View Article]
     [Google Scholar]
  17. Wayne LG, Hayes LG. An in vitro model for sequential study of shiftdown of Mycobacterium tuberculosis through two stages of nonreplicating persistence. Infect Immun 1996; 64:2062–2069 [View Article]
     [Google Scholar]
  18. Sherman DR, Voskuil M, Schnappinger D, Liao R, Harrell MI et al. Regulation of the Mycobacterium tuberculosis hypoxic response gene encoding -crystallin. Proc Natl Acad Sci U S A 2001; 98:7534–7539 [View Article]
     [Google Scholar]
  19. Park H-D, Guinn KM, Harrell MI, Liao R, Voskuil MI et al. Rv3133c/dosR is a transcription factor that mediates the hypoxic response of Mycobacterium tuberculosis . Mol Microbiol 2003; 48:833–843 [View Article]
     [Google Scholar]
  20. Mayuri G, Das TK, Tyagi JS. Molecular analysis of the dormancy response in Mycobacterium smegmatis: expression analysis of genes encoding the DevR–DevS two-component system, Rv3134c and chaperone α-crystallin homologues. FEMS Microbiol Lett 2002; 211:231–237 [View Article]
     [Google Scholar]
  21. Galagan JE, Minch K, Peterson M, Lyubetskaya A, Azizi E et al. The Mycobacterium tuberculosis regulatory network and hypoxia. Nature 2013; 499:178–183 [View Article]
     [Google Scholar]
  22. Lim A, Eleuterio M, Hutter B, Murugasu-Oei B, Dick T. Oxygen depletion-induced dormancy in Mycobacterium bovis BCG. J Bacteriol 1999; 181:2252–2256 [View Article]
     [Google Scholar]
  23. Wayne LG, Sramek HA. Metronidazole is bactericidal to dormant cells of Mycobacterium tuberculosis . Antimicrob Agents Chemother 1994; 38:2054–2058 [View Article]
     [Google Scholar]
  24. Hoff DR, Caraway ML, Brooks EJ, Driver ER, Ryan GJ et al. Metronidazole lacks antibacterial activity in guinea pigs infected with Mycobacterium tuberculosis . Antimicrob Agents Chemother 2008; 52:4137–4140 [View Article]
     [Google Scholar]
  25. Carroll MW, Jeon D, Mountz JM, Lee JD, Jeong YJ et al. Efficacy and safety of metronidazole for pulmonary multidrug-resistant tuberculosis. Antimicrob Agents Chemother 2013; 57:3903–3909 [View Article]
     [Google Scholar]
  26. Brooks JV, Furney SK, Orme IM. Metronidazole therapy in mice infected with tuberculosis. Antimicrob Agents Chemother 1999; 43:1285–1288 [View Article]
     [Google Scholar]
  27. Klinkenberg LG, Sutherland LA, Bishai WR, Karakousis PC. Metronidazole lacks activity against Mycobacterium tuberculosis in an in vivo hypoxic granuloma model of latency. J Infect Dis 2008; 198:275–283 [View Article]
     [Google Scholar]
  28. Balaban NQ, Merrin J, Chait R, Kowalik L, Leibler S. Bacterial persistence as a phenotypic switch. Science 2004; 305:1622–1625 [View Article]
     [Google Scholar]
  29. Mandal S, Njikan S, Kumar A, Early JV, Parish T. The relevance of persisters in tuberculosis drug discovery. Microbiology 2019; 165:492–499 [View Article]
     [Google Scholar]
  30. Vilchèze C, Jacobs WR. The isoniazid paradigm of killing, resistance, and persistence in Mycobacterium tuberculosis. J Mol Biol 2019; 431:3450–3461 [View Article]
     [Google Scholar]
  31. Keren I, Minami S, Rubin E, Lewis K. Characterization and transcriptome analysis of Mycobacterium tuberculosis persisters. MBio 2011; 2:e00100–00111 [View Article]
     [Google Scholar]
  32. Bryk R, Gold B, Venugopal A, Singh J, Samy R et al. Selective killing of nonreplicating mycobacteria. Cell Host Microbe 2008; 3:137–145 [View Article]
     [Google Scholar]
  33. Aldridge BB, Fernandez-Suarez M, Heller D, Ambravaneswaran V, Irimia D et al. Asymmetry and aging of mycobacterial cells lead to variable growth and antibiotic susceptibility. Science 2012; 335:100–104 [View Article]
     [Google Scholar]
  34. Javid B, Sorrentino F, Toosky M, Zheng W, Pinkham JT et al. Mycobacterial mistranslation is necessary and sufficient for rifampicin phenotypic resistance. Proc Natl Acad Sci U S A 2014; 111:1132–1137 [View Article]
     [Google Scholar]
  35. Wakamoto Y, Dhar N, Chait R, Schneider K, Signorino-Gelo F et al. Dynamic persistence of antibiotic-stressed mycobacteria. Science 2013; 339:91–95 [View Article]
     [Google Scholar]
  36. Jain P, Weinrick BC, Kalivoda EJ, Yang H, Munsamy V et al. Dual-Reporter mycobacteriophages (Φ2 DRMs) reveal preexisting Mycobacterium tuberculosis persistent cells in human sputum. MBio 2016; 7: [View Article]
     [Google Scholar]
  37. Safi H, Gopal P, Lingaraju S, Ma S, Levine C et al. Phase variation in Mycobacterium tuberculosis glpK produces transiently heritable drug tolerance. Proc Natl Acad Sci U S A 2019; 116:19665–19674 [View Article]
     [Google Scholar]
  38. Bellerose MM, Baek S-H, Huang C-C, Moss CE, Koh E-I et al. Common variants in the glycerol kinase gene reduce tuberculosis drug efficacy. mBio 2019; 10: [View Article]
     [Google Scholar]
  39. Quigley J, Peoples A, Sarybaeva A, Hughes D, Ghiglieri M et al. Novel antimicrobials from uncultured bacteria acting against Mycobacterium tuberculosis . mBio 2020; 11: [View Article]
     [Google Scholar]
  40. Keren I, Mulcahy LR, Lewis K. Persister eradication: lessons from the world of natural products. Methods Enzymol 2012; 517:387–406
     [Google Scholar]
  41. Mak PA, Rao SPS, Ping Tan M, Lin X, Chyba J et al. A high-throughput screen to identify inhibitors of ATP homeostasis in non-replicating Mycobacterium tuberculosis . ACS Chem Biol 2012; 7:1190–1197 [View Article]
     [Google Scholar]
  42. Ma S, Morrison R, Hobbs SJ, Soni V, Farrow-Johnson J et al. Transcriptional regulator-induced phenotype screen reveals drug potentiators in Mycobacterium tuberculosis . Nat Microbiol. 2020
     [Google Scholar]
  43. Li Y, Sharma MR, Koripella RK, Yang Y, Kaushal PS et al. Zinc depletion induces ribosome hibernation in mycobacteria. Proc Natl Acad Sci U S A 2018; 115:8191–8196 [View Article]
     [Google Scholar]
  44. Li Y, Corro J, Palmer C, Ojha AK. Progression from remodelling to hibernation of ribosomes in zinc starved mycobacteria. PNAS 2020In press
     [Google Scholar]
  45. Young R, Bremer H. Polypeptide-chain-elongation rate in Escherichia coli B/r as a function of growth rate. Biochem J 1976; 160:185–194 [View Article]
     [Google Scholar]
  46. Wilson DN, Nierhaus KH. The weird and wonderful world of bacterial ribosome regulation. Crit Rev Biochem Mol Biol 2007; 42:187–219 [View Article]
     [Google Scholar]
  47. Potrykus K, Cashel M. (p)ppGpp: still magical?. Annu Rev Microbiol 2008; 62:35–51 [View Article]
     [Google Scholar]
  48. Chatterji D, Ojha AK. Revisiting the stringent response, ppGpp and starvation signaling. Curr Opin Microbiol 2001; 4:160–165 [View Article][PubMed]
     [Google Scholar]
  49. Gourse RL, Chen AY, Gopalkrishnan S, Sanchez-Vazquez P, Myers A et al. Transcriptional responses to ppGpp and DksA. Annu Rev Microbiol 2018; 72:163–184 [View Article]
     [Google Scholar]
  50. Jacobson A, Gillespie D. Metabolic events occurring during recovery from prolonged glucose starvation in Escherichia coli . J Bacteriol 1968; 95:1030–1039 [View Article]
     [Google Scholar]
  51. Zundel MA, Basturea GN, Deutscher MP. Initiation of ribosome degradation during starvation in Escherichia coli . RNA 2009; 15:977–983 [View Article]
     [Google Scholar]
  52. Prossliner T, Skovbo Winther K, Sørensen MA, Gerdes K. Ribosome hibernation. Annu Rev Genet 2018; 52:321–348 [View Article]
     [Google Scholar]
  53. Tissieres A, Watson JD. Ribonucleoprotein particles from Escherichia coli . Nature 1958; 182:778–780 [View Article]
     [Google Scholar]
  54. McCarthy BJ. Variations in bacterial ribosomes. Biochim Biophys Acta 1960; 39:563–564 [View Article]
     [Google Scholar]
  55. 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 [View Article]
     [Google Scholar]
  56. Agafonov DE, Kolb VA, Nazimov IV, Spirin AS. A protein residing at the subunit interface of the bacterial ribosome. Proc Natl Acad Sci U S A 1999; 96:12345–12349 [View Article]
     [Google Scholar]
  57. Ueta M, Yoshida H, Wada C, Baba T, Mori H et al. 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 [View Article]
     [Google Scholar]
  58. Polikanov YS, Blaha GM, Steitz TA. How hibernation factors RMF, HPF, and Yfia turn off protein synthesis. Science 2012; 336:915–918 [View Article]
     [Google Scholar]
  59. De Bari H, Berry EA. Structure of Vibrio cholerae ribosome hibernation promoting factor. Acta Crystallogr Sect F Struct Biol Cryst Commun 2013; 69:228–236 [View Article]
     [Google Scholar]
  60. Ueta M, Wada C, Wada A. Formation of 100S ribosomes in Staphylococcus aureus by the hibernation promoting factor homolog Sa HPF. Genes Cells 2010; 15:43–58 [View Article]
     [Google Scholar]
  61. Tagami K, Nanamiya H, Kazo Y, Maehashi M, Suzuki S et al. Expression of a small (p)ppGpp synthetase, YwaC, in the (p)ppGpp mutant of Bacillus subtilis triggers YvyD‐dependent dimerization of ribosome. Microbiologyopen 2012; 1:115–134 [View Article]
     [Google Scholar]
  62. Puri P, Eckhardt TH, Franken LE, Fusetti F, Stuart MCA et al. Lactococcus lactis YfiA is necessary and sufficient for ribosome dimerization. Mol Microbiol 2014; 91:394–407 [View Article]
     [Google Scholar]
  63. Kline BC, McKay SL, Tang WW, Portnoy DA. The Listeria monocytogenes hibernation-promoting factor is required for the formation of 100S ribosomes, optimal fitness, and pathogenesis. J Bacteriol 2015; 197:581–591 [View Article]
     [Google Scholar]
  64. Ueta M, Wada C, Daifuku T, Sako Y, Bessho Y et al. Conservation of two distinct types of 100S ribosome in bacteria. Genes Cells 2013; 18:554–574 [View Article]
     [Google Scholar]
  65. Krokowski D, Gaccioli F, Majumder M, Mullins MR, Yuan CL et al. Characterization of hibernating ribosomes in mammalian cells. Cell Cycle 2011; 10:2691–2702 [View Article]
     [Google Scholar]
  66. Sharma MR, Wilson DN, Datta PP, Barat C, Schluenzen F et al. Cryo-EM study of the spinach chloroplast ribosome reveals the structural and functional roles of plastid-specific ribosomal proteins. Proc Natl Acad Sci U S A 2007; 104:19315–19320 [View Article]
     [Google Scholar]
  67. Beckert B, Abdelshahid M, Schäfer H, Steinchen W, Arenz S et al. Structure of the Bacillus subtilis hibernating 100S ribosome reveals the basis for 70S dimerization. Embo J 2017; 36:2061–2072 [View Article]
     [Google Scholar]
  68. Flygaard RK, Boegholm N, Yusupov M, Jenner LB. Cryo-EM structure of the hibernating Thermus thermophilus 100S ribosome reveals a protein-mediated dimerization mechanism. Nat Commun 2018; 9:4179 [View Article]
     [Google Scholar]
  69. Franken LE, Oostergetel GT, Pijning T, Puri P, Arkhipova V et al. A general mechanism of ribosome dimerization revealed by single-particle cryo-electron microscopy. Nat Commun 2017; 8:722 [View Article]
     [Google Scholar]
  70. Khusainov I, Vicens Q, Ayupov R, Usachev K, Myasnikov A et al. Structures and dynamics of hibernating ribosomes from Staphylococcus aureus mediated by intermolecular interactions of HPF. Embo J 2017; 36:2073–2087 [View Article]
     [Google Scholar]
  71. Matzov D, Aibara S, Basu A, Zimmerman E, Bashan A et al. The cryo-EM structure of hibernating 100S ribosome dimer from pathogenic Staphylococcus aureus. Nat Commun 2017; 8:723 [View Article]
     [Google Scholar]
  72. Kato T, Yoshida H, Miyata T, Maki Y, Wada A et al. Structure of the 100S ribosome in the hibernation stage revealed by electron cryomicroscopy. Structure 2010; 18:719–724 [View Article]
     [Google Scholar]
  73. Ortiz JO, Brandt F, Matias VRF, Sennels L, Rappsilber J et al. Structure of hibernating ribosomes studied by cryoelectron tomography in vitro and in situ. J Cell Biol 2010; 190:613–621 [View Article]
     [Google Scholar]
  74. Trösch R, Willmund F. The conserved theme of ribosome hibernation: from bacteria to chloroplasts of plants. Biol Chem 2019; 400:879–893 [View Article]
     [Google Scholar]
  75. Izutsu K, Wada A, Wada C. Expression of ribosome modulation factor (RMF) in Escherichia coli requires ppGpp. Genes Cells 2001; 6:665–676 [View Article]
     [Google Scholar]
  76. Hood RD, Higgins SA, Flamholz A, Nichols RJ, Savage DF. The stringent response regulates adaptation to darkness in the cyanobacterium Synechococcus elongatus . Proc Natl Acad Sci U S A 2016; 113:E4867–E4876 [View Article]
     [Google Scholar]
  77. Basu A, Yap M-NF. Disassembly of the Staphylococcus aureus hibernating 100S ribosome by an evolutionarily conserved GTPase. Proc Natl Acad Sci U S A 2017; 114:E8165–E8173 [View Article]
     [Google Scholar]
  78. Salmon K, Hung SP, Mekjian K, Baldi P, Hatfield GW et al. Global gene expression profiling in Escherichia coli K12. The effects of oxygen availability and FNR. J Biol Chem 2003; 278:29837–29855
     [Google Scholar]
  79. Stolper DA, Revsbech NP, Canfield DE. Aerobic growth at nanomolar oxygen concentrations. Proc Natl Acad Sci U S A 2010; 107:18755–18760 [View Article]
     [Google Scholar]
  80. Wada A. Growth phase coupled modulation of Escherichia coli ribosomes. Genes to Cells 1998; 3:203–208 [View Article]
     [Google Scholar]
  81. Zhang Y, Mandava CS, Cao W, Li X, Zhang D et al. Hflx is a ribosome-splitting factor rescuing stalled ribosomes under stress conditions. Nat Struct Mol Biol 2015; 22:906–913 [View Article]
     [Google Scholar]
  82. Rudra P, Hurst-Hess KR, Cotten KL, Partida-Miranda A, Ghosh P. Mycobacterial HflX is a ribosome splitting factor that mediates antibiotic resistance. Proc Natl Acad Sci U S A 2020; 117:629–634 [View Article]
     [Google Scholar]
  83. Akiyama T, Williamson KS, Schaefer R, Pratt S, Chang CB et al. Resuscitation of Pseudomonas aeruginosa from dormancy requires hibernation promoting factor (PA4463) for ribosome preservation. Proc Natl Acad Sci U S A 2017; 114:3204–3209 [View Article]
     [Google Scholar]
  84. Sabharwal D, Song T, Papenfort K, Wai SN. The VrrA sRNA controls a stationary phase survival factor Vrp of Vibrio cholerae . RNA Biol 2015; 12:186–196 [View Article]
     [Google Scholar]
  85. Akanuma G, Kazo Y, Tagami K, Hiraoka H, Yano K et al. Ribosome dimerization is essential for the efficient regrowth of Bacillus subtilis . Microbiology 2016; 162:448–458 [View Article]
     [Google Scholar]
  86. Basu A, Yap M-NF. Ribosome hibernation factor promotes Staphylococcal survival and differentially represses translation. Nucleic Acids Res 2016; 44:4881–4893 [View Article]
     [Google Scholar]
  87. McKay SL, Portnoy DA. Ribosome hibernation facilitates tolerance of stationary-phase bacteria to aminoglycosides. Antimicrob Agents Chemother 2015; 59:6992–6999 [View Article]
     [Google Scholar]
  88. Kanehisa M et al. From genomics to chemical genomics: new developments in KEGG. Nucleic Acids Res 2006; 34:D354–D357 [View Article]
     [Google Scholar]
  89. Trauner A, Lougheed KEA, Bennett MH, Hingley-Wilson SM, Williams HD. The dormancy regulator DosR controls ribosome stability in hypoxic mycobacteria. J Biol Chem 2012; 287:24053–24063 [View Article]
     [Google Scholar]
  90. Carter AP, Clemons WM, Brodersen DE, Morgan-Warren RJ, Wimberly BT et al. Functional insights from the structure of the 30S ribosomal subunit and its interactions with antibiotics. Nature 2000; 407:340–348 [View Article]
     [Google Scholar]
  91. Francois B et al. Crystal structures of complexes between aminoglycosides and decoding a site oligonucleotides: role of the number of rings and positive charges in the specific binding leading to miscoding. Nucleic Acids Res 2005; 33:5677–5690 [View Article]
     [Google Scholar]
  92. Prisic S, Hwang H, Dow A, Barnaby O, Pan TS et al. Zinc regulates a switch between primary and alternative S18 ribosomal proteins in Mycobacterium tuberculosis . Mol Microbiol 2015; 97:263–280 [View Article][PubMed]
     [Google Scholar]
  93. Maciąg A, Dainese E, Rodriguez GM, Milano A, Provvedi R et al. Global analysis of the Mycobacterium tuberculosis Zur (FurB) regulon. J Bacteriol 2007; 189:730–740 [View Article]
     [Google Scholar]
  94. Owen GA, Pascoe B, Kallifidas D, Paget MSB. Zinc-responsive regulation of alternative ribosomal protein genes in Streptomyces coelicolor involves Zur and σR. J Bacteriol 2007; 189:4078–4086 [View Article]
     [Google Scholar]
  95. Gabriel SE, Helmann JD. Contributions of Zur-controlled ribosomal proteins to growth under zinc starvation conditions. J Bacteriol 2009; 191:6116–6122 [View Article]
     [Google Scholar]
  96. Makarova KS, Ponomarev VA, Koonin EV. Two C or not two C: recurrent disruption of Zn-ribbons, gene duplication, lineage-specific gene loss, and horizontal gene transfer in evolution of bacterial ribosomal proteins. Genome Biol 2001; 2:
     [Google Scholar]
  97. Yutin N, Puigbò P, Koonin EV, Wolf YI. Phylogenomics of prokaryotic ribosomal proteins. PLoS One 2012; 7:e36972 [View Article]
     [Google Scholar]
  98. Nanamiya H, Akanuma G, Natori Y, Murayama R, Kosono S et al. Zinc is a key factor in controlling alternation of two types of L31 protein in the Bacillus subtilis ribosome. Mol Microbiol 2004; 52:273–283 [View Article]
     [Google Scholar]
  99. Dow A, Prisic S. Alternative ribosomal proteins are required for growth and morphogenesis of Mycobacterium smegmatis under zinc limiting conditions. PLoS One 2018; 13:e0196300 [View Article]
     [Google Scholar]
  100. Chen Y-X, Xu Z-yu, Ge X, Hong J-Y, Sanyal S, ZY X, ZJ L et al. Selective translation by alternative bacterial ribosomes. Proc Natl Acad Sci U S A 2020; 117:19487–19496 [View Article]
     [Google Scholar]
  101. Tobiasson V, Dow A, Prisic S, Amunts A. Zinc depletion does not necessarily induce ribosome hibernation in mycobacteria. Proc Natl Acad Sci U S A 2019; 116:2395–2397 [View Article]
     [Google Scholar]
  102. 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; 8:13587 [View Article][PubMed]
     [Google Scholar]
  103. Schmitz KR, Carney DW, Sello JK, Sauer RT. Crystal structure of Mycobacterium tuberculosis ClpP1P2 suggests a model for peptidase activation by AAA+ partner binding and substrate delivery. Proc Natl Acad Sci U S A 2014; 111:E4587–E4595 [View Article][PubMed]
     [Google Scholar]
  104. Sauer RT, Baker TA. Aaa+ proteases: ATP-fueled machines of protein destruction. Annu Rev Biochem 2011; 80:587–612 [View Article][PubMed]
     [Google Scholar]
  105. Olivares AO, Baker TA, Sauer RT. Mechanistic insights into bacterial AAA+ proteases and protein-remodelling machines. Nat Rev Microbiol 2016; 14:33–44 [View Article][PubMed]
     [Google Scholar]
  106. Lo JH, Baker TA, Sauer RT. Characterization of the N-terminal repeat domain of Escherichia coli ClpA-A class I Clp/HSP100 ATPase. Protein Sci 2001; 10:551–559 [View Article][PubMed]
     [Google Scholar]
  107. Varshavsky A. N-degron and C-degron pathways of protein degradation. Proc Natl Acad Sci U S A 2019; 116:358–366 [View Article][PubMed]
     [Google Scholar]
  108. Dougan DA, Truscott KN, Zeth K. The bacterial N-end rule pathway: expect the unexpected. Mol Microbiol 2010; 76:545–558 [View Article][PubMed]
     [Google Scholar]
  109. Ninnis RL, Spall SK, Talbo GH, Truscott KN, Dougan DA. Modification of PATase by L/F-transferase generates a ClpS-dependent N-end rule substrate in Escherichia coli . Embo J 2009; 28:1732–1744 [View Article][PubMed]
     [Google Scholar]
  110. Gao X, Yeom J, Groisman EA. The expanded specificity and physiological role of a widespread N-degron recognin. Proc Natl Acad Sci U S A 2019; 116:18629–18637 [View Article][PubMed]
     [Google Scholar]
  111. Raju RM, Unnikrishnan M, Rubin DHF, Krishnamoorthy V, Kandror O et al. Mycobacterium tuberculosis ClpP1 and ClpP2 function together in protein degradation and are required for viability in vitro and during infection. PLoS Pathog 2012; 8:e1002511 [View Article][PubMed]
     [Google Scholar]
  112. Akopian T, Kandror O, Raju RM, Unnikrishnan M, Rubin EJ et al. The active ClpP protease from M. tuberculosis is a complex composed of a heptameric ClpP1 and a ClpP2 ring. Embo J 2012; 31:1529–1541 [View Article][PubMed]
     [Google Scholar]
  113. Ollinger J, O'Malley T, Kesicki EA, Odingo J, Parish T. Validation of the essential ClpP protease in Mycobacterium tuberculosis as a novel drug target. J Bacteriol 2012; 194:663–668 [View Article][PubMed]
     [Google Scholar]
  114. Ziemski M, Leodolter J, Taylor G, Kerschenmeyer A, Weber-Ban E. Genome-wide interaction screen for Mycobacterium tuberculosis ClpCP protease reveals toxin-antitoxin systems as a major substrate class. Febs J 2021; 288:111–126 [View Article][PubMed]
     [Google Scholar]
  115. Li Y, Sharma MR, Koripella RK, Wade JT, Gray TA et al. Reply to Tobiasson et al.: zinc depletion is a specific signal for induction of ribosome hibernation in mycobacteria. Proc Natl Acad Sci U S A 2019; 116:2398–2399 [View Article][PubMed]
     [Google Scholar]
  116. Li Y, Koripella RK, Sharma MR, Lee RE, Agrawal RK et al. Replacement of S14 protein in ribosomes of zinc-starved mycobacteria reduces spectinamide sensitivity. Antimicrob Agents Chemother in press 2020 23 Dec 2020 [View Article][PubMed]
     [Google Scholar]
  117. Pyle CJ, Azad AK, Papp AC, Sadee W, Knoell DL et al. Elemental ingredients in the macrophage cocktail: role of ZIP8 in host response to Mycobacterium tuberculosis. Int J Mol Sci 2017; 18:2375 09 Nov 2017 [View Article][PubMed]
     [Google Scholar]
  118. Wagner D, Maser J, Lai B, Cai Z, Barry CE et al. Elemental analysis of Mycobacterium avium, Mycobacterium tuberculosis, and Mycobacterium smegmatis-containing phagosomes indicates pathogen-induced microenvironments within the host cell's endosomal system. J Immunol 2005; 174:1491–1500 [View Article][PubMed]
     [Google Scholar]
  119. Botella H, Peyron P, Levillain F, Poincloux R, Poquet Y et al. Mycobacterial p(1)-type ATPases mediate resistance to zinc poisoning in human macrophages. Cell Host Microbe 2011; 10:248–259 [View Article][PubMed]
     [Google Scholar]
  120. Corbin BD, Seeley EH, Raab A, Feldmann J, Miller MR et al. Metal chelation and inhibition of bacterial growth in tissue abscesses. Science 2008; 319:962–965 [View Article][PubMed]
     [Google Scholar]
  121. Lonergan ZR, Skaar EP. Nutrient zinc at the host-pathogen interface. Trends Biochem Sci 2019; 44:1041–1056 [View Article][PubMed]
     [Google Scholar]
  122. Lyadova IV. Neutrophils in tuberculosis: heterogeneity shapes the way?. Mediators Inflamm 2017; 2017:1–11 [View Article][PubMed]
     [Google Scholar]
  123. Niazi MKK, Dhulekar N, Schmidt D, Major S, Cooper R et al. Lung necrosis and neutrophils reflect common pathways of susceptibility to Mycobacterium tuberculosis in genetically diverse, immune-competent mice. Dis Model Mech 2015; 8:1141–1153 [View Article][PubMed]
     [Google Scholar]
http://instance.metastore.ingenta.com/content/journal/micro/10.1099/mic.0.001035
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Ribosome hibernation: a new molecular framework for targeting nonreplicating persisters of mycobacteria
Microbiology 167, 001035 (2021); https://doi.org/10.1099/mic.0.001035
/content/journal/micro/10.1099/mic.0.001035
/content/journal/micro/10.1099/mic.0.001035
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