RNA futile cycling in model persisters derived from mazF accumulation

mBio

Volumn 6, Issue 6, 2015, Pages

  Mok, Wendy W K ^a   Park, Junyoung O ^a,b   Rabinowitz, Joshua D ^b   Brynildsen, Mark P ^a  

^a Princeton University   (United States)

^b PRINCETON UNIVERSITY   (United States)

Author keywords

[No Author keywords available]

Indexed keywords

ADENOSINE DIPHOSPHATE; ADENOSINE PHOSPHATE; ADENOSINE TRIPHOSPHATE; BACTERIAL PROTEIN; BACTERIAL TOXIN; BETA LACTAM ANTIBIOTIC; CYTIDINE DIPHOSPHATE; CYTIDINE PHOSPHATE; CYTIDINE TRIPHOSPHATE; GLUCOSE; GUANOSINE DIPHOSPHATE; GUANOSINE PHOSPHATE; GUANOSINE TRIPHOSPHATE; MAZE PROTEIN; MAZF TOXIN; OXYGEN; QUINOLINE DERIVED ANTIINFECTIVE AGENT; RIBONUCLEOTIDE; RIBONUCLEOTIDE MONOPHOSPHATE; UNCLASSIFIED DRUG; URIDINE DIPHOSPHATE; URIDINE PHOSPHATE; URIDINE TRIPHOSPHATE; ANTIINFECTIVE AGENT; BACTERIAL RNA; BETA LACTAM; DNA BINDING PROTEIN; ESCHERICHIA COLI PROTEIN; MAZE PROTEIN, E COLI; MAZF PROTEIN, E COLI; QUINOLONE DERIVATIVE; RIBONUCLEASE;

ANTIBIOTIC SENSITIVITY; ARTICLE; BACTERIAL GROWTH; BIOACCUMULATION; BIOLOGICAL MODEL; CONTROLLED STUDY; ESCHERICHIA COLI; GLUCOSE INTAKE; GROWTH INHIBITION; METABOLOMICS; NONHUMAN; NUCLEIC ACID STRUCTURE, METABOLISM AND FUNCTION; OXYGEN CONSUMPTION; PRIORITY JOURNAL; RNA CLEAVAGE; RNA DEGRADATION; RNA FUTILE CYCLE; RNA SYNTHESIS; TRANSCRIPTION TERMINATION; CITRIC ACID CYCLE; DRUG EFFECTS; DRUG TOLERANCE; ENZYMOLOGY; GENE EXPRESSION; GENETIC TRANSCRIPTION; GENETICS; METABOLISM; PROMOTER REGION; RNA STABILITY;

ANTI-BACTERIAL AGENTS; BETA-LACTAMS; DNA-BINDING PROTEINS; DRUG TOLERANCE; ENDORIBONUCLEASES; ESCHERICHIA COLI; ESCHERICHIA COLI PROTEINS; FLUOROQUINOLONES; GENE EXPRESSION; GLUCOSE; OXYGEN; PROMOTER REGIONS, GENETIC; RIBONUCLEOTIDES; RNA STABILITY; RNA, BACTERIAL; SUBSTRATE CYCLING; TRANSCRIPTION, GENETIC;

EID: 84952837530     PISSN: 21612129     EISSN: 21507511     Source Type: Journal    
DOI: 10.1128/mBio.01588-15     Document Type: Article

References (73)

1. Lewis K. 2010. Persister cells. Annu Rev Microbiol 64:357-372. http:// dx.doi.org/10.1146/annurev.micro.112408.134306.
2. Bigger J. 1944. Treatment of staphylococcal infections with penicillin by intermittent sterilisation. Lancet 244:497-500. http://dx.doi.org/10.1016/ S0140-6736(00)74210-3.
3. Maisonneuve E, Gerdes K. 2014. Molecular mechanisms underlying bacterial persisters. Cell 157:539-548. http://dx.doi.org/10.1016/ j.cell.2014.02.050.
4. Fauvart M, De Groote VN, Michiels J. 2011. Role of persister cells in chronic infections: clinical relevance and perspectives on anti-persister therapies. J Med Microbiol 60:699-709. http://dx.doi.org/10.1099/ jmm.0.030932-0.
5. Grant SS, Hung DT. 2013. Persistent bacterial infections, antibiotic tolerance, and the oxidative stress response. Virulence 4:273-283. http:// dx.doi.org/10.4161/viru.23987.
6. Cohen N, Lobritz M, Collins J. 2013. Microbial persistence and the road to drug resistance. Cell Host Microbe 13:632-642. http://dx.doi.org/ 10.1016/j.chom.2013.05.009.
7. Gefen O, Balaban NQ. 2009. The importance of being persistent: heterogeneity of bacterial populations under antibiotic stress. FEMS Microbiol Rev 33:704-717. http://dx.doi.org/10.1111/j.1574-6976.2008.00156.x.
8. Wakamoto Y, Dhar N, Chait R, Schneider K, Signorino-Gelo F, Leibler S, McKinney JD. 2013. Dynamic persistence of antibiotic-stressed mycobacteria. Science 339:91-95. http://dx.doi.org/10.1126/science.1229858.
9. Orman MA, Brynildsen MP. 2013. Establishment of a method to rapidly assay bacterial persister metabolism. Antimicrob Agents Chemother 57: 4398-4409. http://dx.doi.org/10.1128/AAC.00372-13.
10. Allison KR, Brynildsen MP, Collins JJ. 2011. Metabolite-enabled eradication of bacterial persisters by aminoglycosides. Nature 473:216-220. http://dx.doi.org/10.1038/nature10069.
11. Barraud N, Buson A, Jarolimek W, Rice SA. 2013. Mannitol enhances antibiotic sensitivity of persister bacteria in Pseudomonas aeruginosa biofilms. PLoS One 8: e84220. http://dx.doi. org/1 0. 1 3 7 1 / journal.pone.0084220.
12. Mok WWK, Orman MA, Brynildsen MP. 2015. Impacts of global transcriptional regulators on persister metabolism. Antimicrob Agents Chemother 59:2713-2719. http://dx.doi.org/10.1128/AAC.04908-14.
13. Prax M, Bertram R. 2014. Metabolic aspects of bacterial persisters. Front Cell Infect Microbiol 4:148. http://dx.doi.org/10.3389/fcimb.2014.00148.
14. Amato SM, Fazen CH, Henry TC, Mok WWK, Orman MA, Sandvik EL, Volzing KG, Brynildsen MP. 2014. The role of metabolism in bacterial persistence. Front Microbiol 5:70. http://dx.doi.org/10.3389/ fmicb.2014.00070.
15. Shan Y, Lazinski D, Rowe S, Camilli A, Lewis K. 2015. Genetic basis of persister tolerance to aminoglycosides in Escherichia coli. mBio 6:e00078-15. http://dx.doi.org/10.1128/mBio.00078-15.
16. Spoering AL, Vulic M, Lewis K. 2006. GlpD and PlsB participate in persister cell formation in Escherichia coli. J Bacteriol 188:5136-5144. http://dx.doi.org/10.1128/JB.00369-06.
17. Girgis HS, Harris K, Tavazoie S. 2012. Large mutational target size for rapid emergence of bacterial persistence. Proc Natl Acad Sci U S A 109: 12740-12745. http://dx.doi.org/10.1073/pnas.1205124109.
18. Ma C, Sim S, Shi W, Du L, Xing D, Zhang Y. 2010. Energy production genes sucB and ubiF are involved in persister survival and tolerance to multiple antibiotics and stresses in Escherichia coli. FEMS Microbiol Lett 303:33-40.
19. Amato S, Orman M, Brynildsen M. 2013. Metabolic control of persister formation in Escherichia coli. Mol Cell 50:475-487. http://dx.doi.org/ 10.1016/j.molcel.2013.04.002.
20. Amato SM, Brynildsen MP. 2014. Nutrient transitions are a source of persisters in Escherichia coli biofilms. PLoS One 9:e93110. http:// dx.doi.org/10.1371/journal.pone.0093110.
21. Bernier SP, Lebeaux D, DeFrancesco AS, Valomon A, Soubigou G, Coppée J, Ghigo J, Beloin C. 2013. Starvation, together with the SOS response, mediates high biofilm-specific tolerance to the fluoroquinolone ofloxacin. PLoS Genet 9:e1003144. http://dx.doi.org/10.1371/ journal.pgen.1003144.
22. Lebeaux D, Chauhan A, Létoffé S, Fischer F, de Reuse H, Beloin C, Ghigo J-. 2014. pH-mediated potentiation of aminoglycosides kills bacterial persisters and eradicates in vivo biofilms. J Infect Dis 210:1357-1366. http://dx.doi.org/10.1093/infdis/jiu286.
23. Kim J-S, Heo P, Yang T-J, Lee K-S, Cho D-H, Kim BT, Suh J-H, Lim H-J, Shin D, Kim S-K, Kweon D-H. 2011. Selective killing of bacterial persisters by a single chemical compound without affecting normal antibiotic-sensitive cells. Antimicrob Agents Chemother 55:5380-5383. http://dx.doi.org/10.1128/AAC.00708-11.
24. Luidalepp H, Jõers A, Kaldalu N, Tenson T. 2011. Age of inoculum strongly influences persister frequency and can mask effects of mutations implicated in altered persistence. J Bacteriol 193:3598-3605. http:// dx.doi.org/10.1128/JB.00085-11.
25. Roostalu J, Jõers A, Luidalepp H, Kaldalu N, Tenson T. 2008. Cell division in Escherichia coli cultures monitored at single cell resolution. BMC Microbiol 8:68. http://dx.doi.org/10.1186/1471-2180-8-68.
26. Ayrapetyan M, Williams TC, Baxter R, Oliver JD. 2015. Viable but nonculturable and persister cells coexist stochastically and are induced by human serum. Infect Immun 83:4194-4203. http://dx.doi.org/10.1128/ IAI.00404-15.
27. Keren I, Shah D, Spoering A, Kaldalu N, Lewis K. 2004. Specialized persister cells and the mechanism of multidrug tolerance in Escherichia coli. J Bacteriol 186:8172-8180. http://dx.doi.org/10.1128/JB.186.24.8172-8180.2004.
28. Cañas-Duarte SJ, Restrepo S, Pedraza JM. 2014. Novel protocol for persister cells isolation. PLoS One 9:e88660.
29. Shah D, Zhang Z, Khodursky A, Kaldalu N, Kurg K, Lewis K. 2006. Persisters: a distinct physiological state of E. coli. BMC Microbiol 6:53. http://dx.doi.org/10.1186/1471-2180-6-53.
30. Bokinsky G, Baidoo EEK, Akella S, Burd H, Weaver D, Alonso-Gutierrez J, García-Martín H, Lee TS, Keasling JD. 2013. HipA-triggered growth arrest and β-lactam tolerance in Escherichia coli are mediated by RelA-dependent ppGpp synthesis. J Bacteriol 195:3173-3182. http:// dx.doi.org/10.1128/JB.02210-12.
31. Vázquez-Laslop N, Lee H, Neyfakh AA. 2006. Increased persistence in Escherichia coli caused by controlled expression of toxins or other unrelated proteins. J Bacteriol 188:3494-3497. http://dx.doi.org/10.1128/ JB.188.10.3494-3497.2006.
32. Verstraeten N, Knapen W, Kint C, Liebens V, Van den Bergh B, Dewachter L, Michiels J, Fu Q, David C, Fierro A, Marchal K, Beirlant J, Versées W, Hofkens J, Jansen M, Fauvart M, Michiels J. 2015. Obg and membrane depolarization are part of a microbial bet-hedging strategy that leads to antibiotic tolerance. Mol Cell 59:9-21. http://dx.doi.org/ 10.1016/j.molcel.2015.05.011.
33. Kwan BW, Valenta JA, Benedik MJ, Wood TK. 2013. Arrested protein synthesis increases persister-like cell formation. Antimicrob Agents Chemother 57:1468-1473. http://dx.doi.org/10.1128/AAC.02135-12.
34. Gerdes K, Maisonneuve E. 2012. Bacterial persistence and toxinantitoxin loci. Annu Rev Microbiol 66:103-123. http://dx.doi.org/ 10.1146/annurev-micro-092611-150159.
35. Yamaguchi Y, Park J, Inouye M. 2011. Toxin-antitoxin systems in bacteria and archaea. Annu Rev Genet 45:61-79. http://dx.doi.org/10.1146/ annurev-genet-110410-132412.
36. Goeders N, Van Melderen L. 2014. Toxin-antitoxin systems as multilevel interaction systems. Toxins (Basel) 6:304-324. http://dx.doi.org/10.3390/ toxins6010304.
37. Van Melderen L. 2010. Toxin-antitoxin systems: why so many, what for? Curr Opin Microbiol 13:781-785. http://dx.doi.org/10.1016/ j.mib.2010.10.006.
38. Germain E, Roghanian M, Gerdes K, Maisonneuve E. 2015. Stochastic induction of persister cells by HipA through (p)ppGpp-mediated activation of mRNA endonucleases. Proc Natl Acad Sci U S A 112:5171-5176. http://dx.doi.org/10.1073/pnas.1423536112.
39. Aizenman E, Engelberg-Kulka H, Glaser G. 1996. An Escherichia coli chromosomal "addiction module" regulated by guanosine [corrected] 3=,5=-bispyrophosphate: a model for programmed bacterial cell death. Proc Natl Acad Sci U S A 93:6059-6063. http://dx.doi.org/10.1073/ pnas.93.12.6059.
40. Zhang Y, Zhang J, Hoeflich KP, Ikura M, Qing G, Inouye M. 2003. MazF cleaves cellular mRNAs specifically at ACA to block protein synthesis in Escherichia coli. Mol Cell 12:913-923. http://dx.doi.org/10.1016/ S1097-2765(03)00402-7.
41. Amitai S, Kolodkin-Gal I, Hananya-Meltabashi M, Sacher A, Engelberg-KulkaH. 2009. Escherichia coli MazF leads to the simultaneous selective synthesis of both "death proteins" and "survival proteins". PLoS Genet 5:e1000390. http://dx.doi.org/10.1371/journal.pgen.1000390.
42. Amitai S, Yassin Y, Engelberg-Kulka H. 2004. MazF-mediated cell death in Escherichia coli: a point of no return. J Bacteriol 186:8295-8300. http:// dx.doi.org/10.1128/JB.186.24.8295-8300.2004.
43. Pedersen K, Christensen SK, Gerdes K. 2002. Rapid induction and reversal of a bacteriostatic condition by controlled expression of toxins and antitoxins. Mol Microbiol 45:501-510. http://dx.doi.org/10.1046/j.1365-2958.2002.03027.x.
44. Tripathi A, Dewan PC, Siddique SA, Varadarajan R. 2014. MazFinduced growth inhibition and persister generation in Escherichia coli. J Biol Chem 289:4191-4205. http://dx.doi.org/10.1074/jbc.M113.510511.
45. Lutz R, Bujard H. 1997. Independent and tight regulation of transcriptional units in Escherichia coli via the LacR/O, the TetR/O and AraC/I1-I2 regulatory elements. Nucleic Acids Res 25:1203-1210. http://dx.doi.org/ 10.1093/nar/25.6.1203.
46. Robinson JL, Miller RV, Brynildsen MP. 2014. Model-driven identification of dosing regimens that maximize the antimicrobial activity of nitric oxide. Metab Eng Commun 1:12-18.
47. Adolfsen KJ, Brynildsen MP. 2015. Futile cycling increases sensitivity toward oxidative stress in Escherichia coli. Metab Eng 29:26-35. http:// dx.doi.org/10.1016/j.ymben.2015.02.006.
48. Izallalen M, Mahadevan R, Burgard A, Postier B, Didonato R, Sun J, Schilling CH, Lovley DR. 2008. Geobacter sulfurreducens strain engineered for increased rates of respiration. Metab Eng 10:267-275. http:// dx.doi.org/10.1016/j.ymben.2008.06.005.
49. Bennett BD, Yuan J, Kimball EH, Rabinowitz JD. 2008. Absolute quantitation of intracellular metabolite concentrations by an isotope ratiobased approach. Nat Protoc 3:1299-1311. http://dx.doi.org/10.1038/ nprot.2008.107.
50. Bennett BD, Kimball EH, Gao M, Osterhout R, Van Dien SJ, Rabinowitz JD. 2009. Absolute metabolite concentrations and implied enzyme active site occupancy in Escherichia coli. Nat Chem Biol 5:593-599. http:// dx.doi.org/10.1038/nchembio.186.
51. Chapman AG, Fall L, Atkinson DE. 1971. Adenylate energy charge in Escherichia coli during growth and starvation. J Bacteriol 108:1072-1086.
52. Vesper O, Amitai S, Belitsky M, Byrgazov K, Kaberdina A, Engelberg-Kulka H, Moll I. 2011. Selective translation of leaderless mRNAs by specialized ribosomes generated by MazF in Escherichia coli. Cell 147: 147-157. http://dx.doi.org/10.1016/j.cell.2011.07.047.
53. Orman MA, Brynildsen MP. 2013. Dormancy is not necessary or sufficient for bacterial persistence. Antimicrob Agents Chemother 57: 3230-3239. http://dx.doi.org/10.1128/AAC.00243-13.
54. Suzuki M, Zhang J, Liu M, Woychik NA, InouyeM. 2005. Single protein production in living cells facilitated by an mRNA interferase. Mol Cell 18:253-261. http://dx.doi.org/10.1016/j.molcel.2005.03.011.
55. Davies J, Davis BD. 1968. Misreading of ribonucleic acid code words induced by aminoglycoside antibiotics. The effect of drug concentration. J Biol Chem 243:3312-3316.
56. Moazed D, Noller HF. 1987. Interaction of antibiotics with functional sites in 16S ribosomal RNA. Nature 327:389-394. http://dx.doi.org/ 10.1038/327389a0.
57. Gromadski KB, Rodnina MV. 2004. Streptomycin interferes with conformational coupling between codon recognition and GTPase activation on the ribosome. Nat Struct Mol Biol 11:316-322. http://dx.doi.org/ 10.1038/nsmb742.
58. Shapiro HM. 2000. Membrane potential estimation by flow cytometry. Methods 21:271-279. http://dx.doi.org/10.1006/meth.2000.1007.
59. Taber HW, Mueller JP, Miller PF, Arrow AS. 1987. Bacterial uptake of aminoglycoside antibiotics. Microbiol Res 51:439-457.
60. Ramos S, Schuldiner S, Kaback HR. 1976. The electrochemical gradient of protons and its relationship to active transport in Escherichia coli membrane vesicles. Proc Natl Acad Sci U S A 73:1892-1896. http://dx.doi.org/ 10.1073/pnas.73.6.1892.
61. Erental A, Sharon I, Engelberg-Kulka H. 2012. Two programmed cell death systems in Escherichia coli: an apoptotic-like death is inhibited by the mazEF-mediated death pathway. PLoS Biol 10:e1001281. http:// dx.doi.org/10.1371/journal.pbio.1001281.
62. Rotem E, Loinger A, Ronin I, Levin-Reisman I, Gabay C, Shoresh N, Biham O, Balaban NQ. 2010. Regulation of phenotypic variability by a threshold-based mechanism underlies bacterial persistence. Proc Natl Acad Sci U S A 107:12541-12546. http://dx.doi.org/10.1073/ pnas.1004333107.
63. Allison KR, Brynildsen MP, Collins JJ. 2011. Heterogeneous bacterial persisters and engineering approaches to eliminate them. Curr Opin Microbiol 14:593-598. http://dx.doi.org/10.1016/j.mib.2011.09.002.
64. Orman MA, Brynildsen MP. 2015. Inhibition of stationary phase respiration impairs persister formation in E. coli. Nat Commun 6:7983.
65. Kasari V, Mets T, Tenson T, Kaldalu N. 2013. Transcriptional crossactivation between toxin-antitoxin systems of Escherichia coli. BMC Microbiol 13:45. http://dx.doi.org/10.1186/1471-2180-13-45.
66. Gutnick D, Calvo JM, Klopotowski T, Ames BN. 1969. Compounds which serve as the sole source of carbon or nitrogen for Salmonella typhimurium LT-2. J Bacteriol 100:215-219.
67. Andrews JM. 2001. Determination of minimum inhibitory concentrations. J Antimicrob Chemother 48(Suppl 1):5-16. http://dx.doi.org/ 10.1093/jac/48.suppl_1.5.
68. Robinson JL, Brynildsen MP. 2013. A kinetic platform to determine the fate of nitric oxide in Escherichia coli. PLoS Comput Biol 9:e1003049. http://dx.doi.org/10.1371/journal.pcbi.1003049.
69. Lu W, Clasquin MF, Melamud E, Amador-Noguez D, Caudy AA, Rabinowitz JD. 2010. Metabolomic analysis via reversed-phase ionpairing liquid chromatography coupled to a stand alone Orbitrap mass spectrometer. Anal Chem 82:3212-3221. http://dx.doi.org/10.1021/ ac902837x.
70. Melamud E, Vastag L, Rabinowitz JD. 2010. Metabolomic analysis and visualization engine for LC-MS data. Anal Chem 82:9818-9826. http:// dx.doi.org/10.1021/ac1021166.
71. Guzman LM, Belin D, Carson MJ, Beckwith J. 1995. Tight regulation, modulation, and high-level expression by vectors containing the arabinose PBAD promoter. J Bacteriol 177:4121-4130.
72. Datsenko KA, Wanner BL. 2000. One-step inactivation of chromosomal genes in Escherichia coli K-12 using PCR products. Proc Natl Acad Sci U S A 97:6640-6645. http://dx.doi.org/10.1073/pnas.120163297.
73. Zaslaver A, Bren A, Ronen M, Itzkovitz S, Kikoin I, Shavit S, Liebermeister W, Surette MG, Alon U. 2006. A comprehensive library of fluorescent transcriptional reporters for Escherichia coli. Nat Methods 3:623-628.